Replicon RNA Viral Vectors as Vaccines
Identifieur interne : 000B25 ( Pmc/Corpus ); précédent : 000B24; suivant : 000B26Replicon RNA Viral Vectors as Vaccines
Auteurs : Kenneth LundstromSource :
- Vaccines [ 2076-393X ] ; 2016.
Abstract
Single-stranded RNA viruses of both positive and negative polarity have been used as vectors for vaccine development. In this context, alphaviruses, flaviviruses, measles virus and rhabdoviruses have been engineered for expression of surface protein genes and antigens. Administration of replicon RNA vectors has resulted in strong immune responses and generation of neutralizing antibodies in various animal models. Immunization of mice, chicken, pigs and primates with virus-like particles, naked RNA or layered DNA/RNA plasmids has provided protection against challenges with lethal doses of infectious agents and administered tumor cells. Both prophylactic and therapeutic efficacy has been achieved in cancer immunotherapy. Moreover, recombinant particles and replicon RNAs have been encapsulated by liposomes to improve delivery and targeting. Replicon RNA vectors have also been subjected to clinical trials. Overall, immunization with self-replicating RNA viruses provides high transient expression levels of antigens resulting in generation of neutralizing antibody responses and protection against lethal challenges under safe conditions.
Url:
DOI: 10.3390/vaccines4040039
PubMed: 27827980
PubMed Central: 5192359
Links to Exploration step
PMC:5192359Le document en format XML
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<front><div type="abstract" xml:lang="en"><p>Single-stranded RNA viruses of both positive and negative polarity have been used as vectors for vaccine development. In this context, alphaviruses, flaviviruses, measles virus and rhabdoviruses have been engineered for expression of surface protein genes and antigens. Administration of replicon RNA vectors has resulted in strong immune responses and generation of neutralizing antibodies in various animal models. Immunization of mice, chicken, pigs and primates with virus-like particles, naked RNA or layered DNA/RNA plasmids has provided protection against challenges with lethal doses of infectious agents and administered tumor cells. Both prophylactic and therapeutic efficacy has been achieved in cancer immunotherapy. Moreover, recombinant particles and replicon RNAs have been encapsulated by liposomes to improve delivery and targeting. Replicon RNA vectors have also been subjected to clinical trials. Overall, immunization with self-replicating RNA viruses provides high transient expression levels of antigens resulting in generation of neutralizing antibody responses and protection against lethal challenges under safe conditions.</p>
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<pmc article-type="review-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Vaccines (Basel)</journal-id>
<journal-id journal-id-type="iso-abbrev">Vaccines (Basel)</journal-id>
<journal-id journal-id-type="publisher-id">vaccines</journal-id>
<journal-title-group><journal-title>Vaccines</journal-title>
</journal-title-group>
<issn pub-type="epub">2076-393X</issn>
<publisher><publisher-name>MDPI</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">27827980</article-id>
<article-id pub-id-type="pmc">5192359</article-id>
<article-id pub-id-type="doi">10.3390/vaccines4040039</article-id>
<article-id pub-id-type="publisher-id">vaccines-04-00039</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Review</subject>
</subj-group>
</article-categories>
<title-group><article-title>Replicon RNA Viral Vectors as Vaccines</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Lundstrom</surname>
<given-names>Kenneth</given-names>
</name>
</contrib>
</contrib-group>
<contrib-group><contrib contrib-type="editor"><name><surname>Borges</surname>
<given-names>Olga</given-names>
</name>
<role>Academic Editor</role>
</contrib>
</contrib-group>
<aff id="af1-vaccines-04-00039">PanTherapeutics, CH 1095 Lutry, Switzerland;<email>lundstromkenneth@gmail.com</email>
; Tel.: +41-79-776-6351</aff>
<pub-date pub-type="epub"><day>07</day>
<month>11</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection"><month>12</month>
<year>2016</year>
</pub-date>
<volume>4</volume>
<issue>4</issue>
<elocation-id>39</elocation-id>
<history><date date-type="received"><day>13</day>
<month>7</month>
<year>2016</year>
</date>
<date date-type="accepted"><day>28</day>
<month>10</month>
<year>2016</year>
</date>
</history>
<permissions><copyright-statement>© 2016 by the author; licensee MDPI, Basel, Switzerland.</copyright-statement>
<copyright-year>2016</copyright-year>
<license><license-p><pmc-comment>CREATIVE COMMONS</pmc-comment>
This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC-BY) license (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
).</license-p>
</license>
</permissions>
<abstract><p>Single-stranded RNA viruses of both positive and negative polarity have been used as vectors for vaccine development. In this context, alphaviruses, flaviviruses, measles virus and rhabdoviruses have been engineered for expression of surface protein genes and antigens. Administration of replicon RNA vectors has resulted in strong immune responses and generation of neutralizing antibodies in various animal models. Immunization of mice, chicken, pigs and primates with virus-like particles, naked RNA or layered DNA/RNA plasmids has provided protection against challenges with lethal doses of infectious agents and administered tumor cells. Both prophylactic and therapeutic efficacy has been achieved in cancer immunotherapy. Moreover, recombinant particles and replicon RNAs have been encapsulated by liposomes to improve delivery and targeting. Replicon RNA vectors have also been subjected to clinical trials. Overall, immunization with self-replicating RNA viruses provides high transient expression levels of antigens resulting in generation of neutralizing antibody responses and protection against lethal challenges under safe conditions.</p>
</abstract>
<kwd-group><kwd>alphaviruses</kwd>
<kwd>flaviviruses</kwd>
<kwd>measles viruses</kwd>
<kwd>rhabdoviruses</kwd>
<kwd>antibodies</kwd>
<kwd>infectious diseases</kwd>
<kwd>tumors</kwd>
<kwd>disease protection</kwd>
</kwd-group>
</article-meta>
</front>
<body><sec id="sec1-vaccines-04-00039"><title>1. Introduction</title>
<p>Vaccine development against infectious diseases has classically been based on live attenuated or inactivated infectious agents [<xref rid="B1-vaccines-04-00039" ref-type="bibr">1</xref>
]. Recently, the approach of vaccination with recombinantly expressed antigens and immunogens from viral and non-viral delivery systems has been introduced to the repertoire [<xref rid="B2-vaccines-04-00039" ref-type="bibr">2</xref>
,<xref rid="B3-vaccines-04-00039" ref-type="bibr">3</xref>
]. In this context, immunization with surface proteins and antigens has elicited strong humoral and cellular immune responses and vaccinated animals showed protection against challenges with lethal doses of infectious agents or tumor cells [<xref rid="B4-vaccines-04-00039" ref-type="bibr">4</xref>
].</p>
<p>The types of non-viral vectors applied include liposomes [<xref rid="B5-vaccines-04-00039" ref-type="bibr">5</xref>
], immunostimulatory complexes (ISCOMs) composed of adjuvant Quil A and peptides [<xref rid="B6-vaccines-04-00039" ref-type="bibr">6</xref>
], and multiple antigen peptides (MAPs) also known as dendrimers [<xref rid="B7-vaccines-04-00039" ref-type="bibr">7</xref>
]. A number of viral vectors based on adenoviruses, alphaviruses, avipoxiviruses, enteroviruses, flaviviruses, measles viruses (MV), rhabdoviruses, and vaccinia viruses have been engineered for vaccine development [<xref rid="B3-vaccines-04-00039" ref-type="bibr">3</xref>
,<xref rid="B8-vaccines-04-00039" ref-type="bibr">8</xref>
]. In this context, self-replicating RNA virus vectors have proven highly efficient for immunization studies in various animal models [<xref rid="B9-vaccines-04-00039" ref-type="bibr">9</xref>
]. Among RNA viruses, rabies virus (RABV) and vesicular stomatitis virus (VSV) belonging to the rhabdovirus family carry a single-stranded RNA (ssRNA) genome of a negative polarity [<xref rid="B10-vaccines-04-00039" ref-type="bibr">10</xref>
]. Likewise, MV possess a negative-sense ssRNA genome [<xref rid="B11-vaccines-04-00039" ref-type="bibr">11</xref>
]. In contrast, flaviviruses and alphaviruses are of positive polarity. West Nile virus [<xref rid="B12-vaccines-04-00039" ref-type="bibr">12</xref>
] and Kunjin virus [<xref rid="B13-vaccines-04-00039" ref-type="bibr">13</xref>
] are the most common flaviviruses applied for immunization studies. Similarly, expression vectors have been engineered for alphaviruses such as Semliki Forest virus (SFV) [<xref rid="B14-vaccines-04-00039" ref-type="bibr">14</xref>
], Sindbis virus (SIN) [<xref rid="B15-vaccines-04-00039" ref-type="bibr">15</xref>
] and Venezuelan equine encephalitis virus (VEE) [<xref rid="B16-vaccines-04-00039" ref-type="bibr">16</xref>
].</p>
<p>In this review, various self-replicating RNA virus vectors are described and their applications as recombinant virus particles, RNA replicons and layered DNA plasmids are compared. Moreover, examples are given of utilization of self-replicating RNA virus systems for immunization studies in various animal models to elicit humoral and cellular immune responses and to generate neutralizing antibodies, as well as protection against challenges with pathogens and tumor cells. Finally, a summary of clinical trials already conducted or in progress that apply self-replicating RNA viruses is presented. However, due to the large number of publications available, it is only possible to present key findings and examples of vaccine development for self-replicating viral vectors.</p>
</sec>
<sec id="sec2-vaccines-04-00039"><title>2. Self-Replicating RNA Expression Systems</title>
<p>Expression systems have been engineered for RNA viruses as described below. All ssRNA viruses share the feature of high level of RNA replication in the cytoplasm, which provides the basis for extreme transient expression of heterologous genes. However, the different polarities of the ssRNA genomes of self-replicating RNA viruses have required the design of vectors with specific features. Moreover, the viral vectors can be utilized in different forms as indicated for the individual types of viruses below.</p>
<sec id="sec2dot1-vaccines-04-00039"><title>2.1. Alphaviruses</title>
<p>Alphavirus-based expression systems have been developed in different formats for SFV [<xref rid="B14-vaccines-04-00039" ref-type="bibr">14</xref>
], SIN [<xref rid="B15-vaccines-04-00039" ref-type="bibr">15</xref>
] and VEE [<xref rid="B16-vaccines-04-00039" ref-type="bibr">16</xref>
], here illustrated for SFV (<xref ref-type="fig" rid="vaccines-04-00039-f001">Figure 1</xref>
). In all cases, the basic component is represented by the alphavirus non-structural genes (nsP1-4), responsible for rapid and high quantity cytoplasmic RNA replication [<xref rid="B17-vaccines-04-00039" ref-type="bibr">17</xref>
]. The replication-deficient system carries the gene of interest (GoI) downstream of the nsP1-4 genes in the alphavirus expression vector to be driven by the 26S subgenomic promoter. RNA replicon vectors can be generated by in vitro transcription for direct RNA immunization. In case of production of recombinant particles, in vitro transcribed RNA from an alphavirus helper vector is co-transfected or co-electroporated into baby hamster kidney (BHK) cells. The replication-proficient system utilizes a full-length vector, where the GoI can be introduced either downstream of the nsP1-4 genes or the structural genes. In vitro transcribed RNA can be applied for immunization, but due to the presence of full-length alphavirus genomic RNA, replication-proficient particles are generated. The DNA layered system applies plasmids carrying alternatively the nonstructural genes or the full-length genome and the GoI for direct immunization with DNA. All vector system approaches described above have proven efficient in immunization studies as presented below [<xref rid="B4-vaccines-04-00039" ref-type="bibr">4</xref>
].</p>
</sec>
<sec id="sec2dot2-vaccines-04-00039"><title>2.2. Flaviviruses</title>
<p>Among flaviviruses, Kunjin virus [<xref rid="B18-vaccines-04-00039" ref-type="bibr">18</xref>
], West Nile virus [<xref rid="B19-vaccines-04-00039" ref-type="bibr">19</xref>
,<xref rid="B20-vaccines-04-00039" ref-type="bibr">20</xref>
], yellow fever virus [<xref rid="B21-vaccines-04-00039" ref-type="bibr">21</xref>
,<xref rid="B22-vaccines-04-00039" ref-type="bibr">22</xref>
], dengue virus [<xref rid="B23-vaccines-04-00039" ref-type="bibr">23</xref>
,<xref rid="B24-vaccines-04-00039" ref-type="bibr">24</xref>
] and tick-borne encephalitis virus [<xref rid="B25-vaccines-04-00039" ref-type="bibr">25</xref>
,<xref rid="B26-vaccines-04-00039" ref-type="bibr">26</xref>
] have been engineered for the development of vectors for DNA, RNA and recombinant particle delivery. In Kunjin virus vectors, the GoI is inserted between the first 20 codons of the core protein (C20) and the last 22 codons of the envelope gene (E22) in frame with the rest of the viral polyprotein (<xref ref-type="fig" rid="vaccines-04-00039-f002">Figure 2</xref>
) [<xref rid="B27-vaccines-04-00039" ref-type="bibr">27</xref>
]. The GoI is expressed initially as a fusion with the Kunjin virus polyprotein, which is then processed into individual proteins. Introduction of flanking FMDV-2A protease sequences allows the cleavage of Kunjin virus sequences from the expressed recombinant protein [<xref rid="B28-vaccines-04-00039" ref-type="bibr">28</xref>
]. To facilitate vector production, a system has been engineered for transfection of Kunjin virus replicon RNA into the tetKUNCprMEC packaging cell line.</p>
</sec>
<sec id="sec2dot3-vaccines-04-00039"><title>2.3. Measles Viruses</title>
<p>Expression systems have been engineered, whereby replicating MV is rescued from cloned DNA expression constructs [<xref rid="B29-vaccines-04-00039" ref-type="bibr">29</xref>
] (<xref ref-type="fig" rid="vaccines-04-00039-f003">Figure 3</xref>
). Reverse genetics has allowed the rescue of recombinant measles virus in an HEK293 helper cell line, where foreign genes were introduced between the phosphoprotein (P) and the matrix protein (M) or between the hemagglutinin (H) and the large protein (L), respectively, in the measles virus genome [<xref rid="B30-vaccines-04-00039" ref-type="bibr">30</xref>
]. Transfection of the helper cell line with recombinant MV constructs and a plasmid expressing the MV polymerase L gene is followed by transfer of syncytia to Vero cell cultures after 3 days, and recombinant MV particles are harvested when reaching 80%–90% cytopathic effects.</p>
</sec>
<sec id="sec2dot4-vaccines-04-00039"><title>2.4. Rhabdoviruses</title>
<p>Both RABV [<xref rid="B10-vaccines-04-00039" ref-type="bibr">10</xref>
,<xref rid="B31-vaccines-04-00039" ref-type="bibr">31</xref>
] and VSV [<xref rid="B32-vaccines-04-00039" ref-type="bibr">32</xref>
,<xref rid="B33-vaccines-04-00039" ref-type="bibr">33</xref>
] have been subjected to expression vector engineering (<xref ref-type="fig" rid="vaccines-04-00039-f004">Figure 4</xref>
). Similar to MV, reverse genetics has been applied for efficient recovery of VSV based on recombinant vaccinia virus, where the VSV N, P and L genes were inserted downstream of a T7 promoter and an internal ribosome entry site (IRES) [<xref rid="B33-vaccines-04-00039" ref-type="bibr">33</xref>
]. The role of vaccinia virus has been to provide T7 RNA polymerase. However, vaccinia virus causes strong cytopathic effects in transfected cells, the vaccinia virus DNA polymerase contributes to homologous recombination between full-length genome and helper plasmids, and vaccinia virus may also contaminate recombinant virus stocks. For this reason, a BHK cell line stably expressing the T7 RNA polymerase was engineered as a vaccinia virus-free system for RABV [<xref rid="B31-vaccines-04-00039" ref-type="bibr">31</xref>
]. In addition to rhabdovirus vectors, chimeric virus-like particles (VLPs) have been generated by expressing the VSV glycoprotein (VSV-G) in trans with the SFV replicon by introduction of a mutated SFV 26S promoter for packaging of infectious SFV pseudoparticles [<xref rid="B34-vaccines-04-00039" ref-type="bibr">34</xref>
]. This system provides high biosafety standards as VSV-G shares no homology with the SFV genome.</p>
</sec>
</sec>
<sec id="sec3-vaccines-04-00039"><title>3. Self-Replicating RNA Virus-Based Vaccines</title>
<p>Self-replicating RNA virus vectors have been frequently used for vaccine development against infectious diseases and various types of cancers [<xref rid="B9-vaccines-04-00039" ref-type="bibr">9</xref>
]. Both vectors based on ssRNA viruses of positive (Kunjin virus, SFV, SIN, VEE) and negative (MV, RABV, VSV) polarity have been utilized for the expression of viral surface proteins and tumor antigens followed by immunization studies in animal models. Moreover, for vaccination, different approaches including recombinant particles, RNA replicons and layered DNA plasmids have been applied.</p>
<sec id="sec3dot1-vaccines-04-00039"><title>3.1. Vaccines against Infectious Diseases</title>
<p>The targets for vaccine development for infectious diseases comprise mainly surface antigens of pathogenic viruses (<xref ref-type="table" rid="vaccines-04-00039-t001">Table 1</xref>
) and other infectious agents (<xref ref-type="table" rid="vaccines-04-00039-t002">Table 2</xref>
). Obvious targets for vaccine development have been antigens of influenza virus and HIV. In this context, recombinant SFV particles expressing influenza nucleoprotein (NP) have demonstrated strong immune responses [<xref rid="B35-vaccines-04-00039" ref-type="bibr">35</xref>
]. Similarly, VEE-based expression of hemagglutinin (HA) elicited strong immune responses and even provided protection against challenges with H5N1 virus in chicken [<xref rid="B36-vaccines-04-00039" ref-type="bibr">36</xref>
]. Likewise, expression of the swine influenza virus HA H3N2 gene from VEE vectors protected swine from influenza virus challenges [<xref rid="B37-vaccines-04-00039" ref-type="bibr">37</xref>
]. In another study, the swine influenza HA gene was expressed from replication-deficient alphavirus particles showing no spread of vaccine or reversion to virulence in the intended host (pig) or non-host (mouse) species [<xref rid="B38-vaccines-04-00039" ref-type="bibr">38</xref>
]. Specific humoral and interferon-γ (IFN-γ) responses were observed in pigs, which were also protected against influenza virus challenges. Recombinant MV vectors carrying the HA gene have also been applied for vaccination studies [<xref rid="B39-vaccines-04-00039" ref-type="bibr">39</xref>
]. Also VSV vectors have been utilized for vaccine development against influenza virus [<xref rid="B40-vaccines-04-00039" ref-type="bibr">40</xref>
]. Instead of using full-length HA, expression of the stalk domain of HA generated chimeric HA (cHA) antigens. Both intramuscular and intranasal immunization of mice resulted in HA stalk-specific, cross-reactive antibodies. Prime-boost vaccination provided protection against lethal challenges with both homologous and heterologous influenza strains, which was significantly superior with intranasal administration.</p>
<p>For obvious reasons HIV has been a popular target for vaccine development. For instance, administration of Kunjin replicons expressing the HIV-1 gag antigen to BALB/c mice elicited gag-specific antibodies and protective gag-specific CD8+ T cell responses [<xref rid="B41-vaccines-04-00039" ref-type="bibr">41</xref>
]. Interestingly, a single immunization with Kunjin virus particles induced 4.5-fold higher CD8+ T-cell responses and protection agains HIV challenges was obtained after two injections. Furthermore, RNA optimized Kunjin virus constructs for SIV Gag-Pol demonstrated improved effector memory and central memory responses as well as protection in primates [<xref rid="B45-vaccines-04-00039" ref-type="bibr">45</xref>
]. Alphavirus vectors have also been employed for HIV vaccine development. Immunization with SFV particles expressing the Env [<xref rid="B42-vaccines-04-00039" ref-type="bibr">42</xref>
] and gp41 [<xref rid="B43-vaccines-04-00039" ref-type="bibr">43</xref>
] genes elicited humoral and cytotoxic T-lymphocyte (CTL) responses in mice. Interestingly, priming with a low dose (0.2 µg) DNA-based SFV replicon expressing the HIV Env and a Gag-Pol-Nef fusion prior to a heterologous boost with poxvirus (MVA) and/or HIV gp140 protein formulated in glycopyranosyl lipid A resulted in significantly enhanced immune responses [<xref rid="B44-vaccines-04-00039" ref-type="bibr">44</xref>
]. Moreover, when macaques were immunized with a VSV vector carrying the SIV Env (smE660) gene neutralizing antibodies were obtained [<xref rid="B46-vaccines-04-00039" ref-type="bibr">46</xref>
]. However, when challenged with SIVsmE660, all animals were infected. In contrast, vaccination with a combination of gag and Env resulted in immunity [<xref rid="B47-vaccines-04-00039" ref-type="bibr">47</xref>
]. RABV vectors have also been employed for the expression of SIV Env and gag in macaques [<xref rid="B48-vaccines-04-00039" ref-type="bibr">48</xref>
]. Although immune responses were detected for RABV glycoprotein G, no cellular responses were obtained against SIV antigens. However, replacing the RABV G with VSV G resulted in SIV-specific immune responses and immunized macaques were protected against SIV challenges.</p>
<p>A number of immunization studies have targeted such lethal viruses as Ebola and Lassa viruses. For instance, dose-dependent protection against Ebola virus was achieved in guinea pigs when immunized with Kunjin virus particles expressing the Ebola virus wild-type glycoprotein GP or a mutant GP (D637L) [<xref rid="B49-vaccines-04-00039" ref-type="bibr">49</xref>
]. Similarly, African green monkeys were subcutaneously immunized with Kunjin particles carrying the Ebola GP D673L mutant [<xref rid="B50-vaccines-04-00039" ref-type="bibr">50</xref>
]. Protection of three out of four primates was obtained against challenges with Zaire Ebola virus. Application of VSV vectors expressing the Ebola GP gene has also provided protection of macaques after challenges with the West African EBOV-Makuna strain [<xref rid="B51-vaccines-04-00039" ref-type="bibr">51</xref>
]. Likewise, protection against three different Ebola strains was achieved by expression of Ebola GP from VSV vectors [<xref rid="B52-vaccines-04-00039" ref-type="bibr">52</xref>
]. Alphavirus vectors have also been utilized for vaccine development against Ebola virus. In this context, RNA replicons derived from an attenuated VEE strain were applied for the expression of Ebola GP and nucleoprotein (NP) [<xref rid="B53-vaccines-04-00039" ref-type="bibr">53</xref>
]. Immunization studies showed that VEE-GP alone or in combination with VEE-NP provided protection of both BALB/c mice and guinea pigs. In contrast, VEE-NP alone did not confer protection in guinea pigs, but did in mice. In another study, C57BL/6 mice were immunized with VEE particles expressing Ebola NP, which protected animals from Ebola virus challenges [<xref rid="B54-vaccines-04-00039" ref-type="bibr">54</xref>
].</p>
<p>VSV vectors have been subjected to immunization studies for expression of the Lassa virus glycoprotein (strain Josiah, Sierra Leone), which generated protection in guinea pigs after a single prophylactic injection [<xref rid="B55-vaccines-04-00039" ref-type="bibr">55</xref>
]. It was also shown that macaques were protected against challenges with the genetically distinct Liberian Lassa virus isolate. Importantly, previous VSV-based Lassa virus vaccination did not have an impact on immunization with VSV-Ebola GP particles [<xref rid="B77-vaccines-04-00039" ref-type="bibr">77</xref>
]. Furthermore, alphaviruses have been used for vaccine development against Lassa virus [<xref rid="B56-vaccines-04-00039" ref-type="bibr">56</xref>
]. Guinea pigs immunized with VEE particles expressing Lassa virus glycoprotein or nucleoprotein showed protection against lethal challenges with Lassa virus. Furthermore, a dual expression approach for Ebola and Lassa virus glycoproteins was engineered, which led to protection against both Ebola and Lassa virus challenges.</p>
<p>A number of other viral antigens have been subjected to vaccine development. Currently, relevant targets comprise dengue virus, severe acute respiratory syndrome coronavirus (SARS-CoV) and Middle East respiratory syndrome corona virus (MERS-CoV). For instance, mice immunized with VEE particles expressing the SARS-CoV glycoprotein provided protection against lethal SARS-CoV challenges [<xref rid="B57-vaccines-04-00039" ref-type="bibr">57</xref>
]. Furthermore, mice were immunized with MV vectors expressing the MERS-CoV glycoprotein, which resulted in induction of T-cell and antibody responses and protection against lethal doses of MERS-CoV [<xref rid="B58-vaccines-04-00039" ref-type="bibr">58</xref>
]. Respiratory syncytial virus (RSV) has also been targeted with recombinant MV vectors by expression of the RSV fusion protein (RSV-F) [<xref rid="B39-vaccines-04-00039" ref-type="bibr">39</xref>
]. Immunization of cotton rats induced neutralizing antibodies against RSV and protected against RSV infection in the lungs. In another application, lipid nanoparticle (LNP) formulations were engineered for VEE RNA replicons, which demonstrated protection against RSV challenges in vaccinated mice [<xref rid="B59-vaccines-04-00039" ref-type="bibr">59</xref>
]. Furthermore, immunization of African green monkeys with VEE particles expressing human RSV-F and metapneumovirus F (hMPV-F) proteins generated RSV-F and MPV-F-specific antibodies resulting in protection against RSV and MPV challenges [<xref rid="B60-vaccines-04-00039" ref-type="bibr">60</xref>
]. In the context of dengue virus vaccines, a hybrid MV vector expressing the hepatitis B surface antigen (HBsAg) and the dengue virus 2 envelope protein (DV2) elicited neutralizing antibodies against MV, HBsAg and DV2 [<xref rid="B61-vaccines-04-00039" ref-type="bibr">61</xref>
]. In another study, MV-DV2 vaccination of mice generated IFN-γ and DV2 antibody responses and protection against four DV serotypes [<xref rid="B62-vaccines-04-00039" ref-type="bibr">62</xref>
]. Alphavirus vectors have also been evaluated for dengue vaccine development. Expression of two configurations of dengue virus E antigen (prME and E85) provided protection in macaques [<xref rid="B63-vaccines-04-00039" ref-type="bibr">63</xref>
]. Moreover, a single immunization of BALB/c mice was sufficient to induce neutralizing antibodies and T-cell responses [<xref rid="B64-vaccines-04-00039" ref-type="bibr">64</xref>
]. The neonatal immunization was durable, could be boosted later in life and provided protection against challenges with dengue virus. Additional viral targets evaluated for vaccine development are listed in <xref ref-type="table" rid="vaccines-04-00039-t001">Table 1</xref>
.</p>
<p>Vaccine development has also been extended to other infectious diseases than caused by viral infections (<xref ref-type="table" rid="vaccines-04-00039-t002">Table 2</xref>
). In this context, mice vaccinated with SFV vectors expressing the <italic>Plasmodium falciparum</italic>
Pf332 antigen elicited immunological memory [<xref rid="B68-vaccines-04-00039" ref-type="bibr">68</xref>
]. Similarly, strong immunity and long-term protection against <italic>Mycobacterium tuberculosis</italic>
was obtained in mice immunized with SIN plasmid DNA vectors carrying the <italic>M. tuberculosis</italic>
85A antigen (Ag85A) [<xref rid="B69-vaccines-04-00039" ref-type="bibr">69</xref>
]. Furthermore, expression of the botulinum neurotoxin A from layered SFV DNA plasmids elicited antibody and lymphoproliferative responses in immunized BALB/c mice [<xref rid="B70-vaccines-04-00039" ref-type="bibr">70</xref>
]. Co-expression of granulocyte-macrophage colony-stimulating factor (GM-CSF) enhanced the immune response. Replication-deficient SFV particles carrying the <italic>Brucella abortus</italic>
translation initiation factor 3 (IF3) were subjected to immunization studies in BALB/c mice, which resulted in protection against challenges with the virulent <italic>B. abortus</italic>
strain 2308 [<xref rid="B71-vaccines-04-00039" ref-type="bibr">71</xref>
]. In another study, SIN vectors were utilized for the expression of the protective antigen (PA) for <italic>Bacillus antracis</italic>
in Swiss Webster mice leading to the generation of specific and neutralizing antibodies and partial protection against challenges with pathogenic bacteria [<xref rid="B72-vaccines-04-00039" ref-type="bibr">72</xref>
].</p>
<p>Recombinant SIN vectors were applied for the expression of a class I major histocompatibility complex-restricted 9-mer epitope of the <italic>Plasmodium yoelii</italic>
circumsporozoite protein (CS), which induced a strong epitope-specific CD8+ T-cell response and a high degree of protection against malaria infection in mice [<xref rid="B73-vaccines-04-00039" ref-type="bibr">73</xref>
]. Another approach to develop malaria vaccines involves the application of a live attenuated MV vaccine expressing recombinant antigens against malaria [<xref rid="B78-vaccines-04-00039" ref-type="bibr">78</xref>
]. A modified replication-competent VSV vector pseudotyped with the glycoprotein of the lymphocytic choriomeningitis virus (VSV-GP) expressing ovalbumin (OVA) induced humoral and cellular immune responses after a single administration in mice [<xref rid="B74-vaccines-04-00039" ref-type="bibr">74</xref>
]. Due to the generation of neutralizing antibodies against VSV, immunization boosters were only possible for VSV-GP-OVA. CTL responses of similar potency as obtained for state-of-the-art adenovirus administration were observed and complete protection against challenges with <italic>Listeria</italic>
monocytogenes was obtained in mice. In the context of prion disease, SFV DNA, RNA and recombinant particles were employed for the expression of prion protein (PRNP), which allowed generation of monoclonal antibodies against PRNP in immunized mice [<xref rid="B75-vaccines-04-00039" ref-type="bibr">75</xref>
]. Although not directly applied for vaccine development, the generated monoclonal antibodies will be useful for basic research and diagnostics for prions. Alphavirus vectors have also been applied for the development of vaccines against Staphylococcus enterotoxin B (SEB) [<xref rid="B76-vaccines-04-00039" ref-type="bibr">76</xref>
]. Subcutaneous administration of VEE particles expressing SEB resulted in protection against challenge of wild-type SEB in mice.</p>
</sec>
<sec id="sec3dot2-vaccines-04-00039"><title>3.2. Vaccines against Cancer</title>
<p>A number of immunization studies have been carried out with self-replicating RNA virus vectors in the area of oncology (<xref ref-type="table" rid="vaccines-04-00039-t003">Table 3</xref>
). For instance, attenuated oncolytic MV strains such as the Edmonston-B (MV-Edm) strain demonstrated anti-tumor activity [<xref rid="B79-vaccines-04-00039" ref-type="bibr">79</xref>
]. The MV-Edm strain does not cause any significant cytopathic effect in normal tissue, but can selectively infect and replicate in tumor cells based on evaluations in cell lines, primary cancer cells and xenograft and syngeneic models for B-cell Non-Hodgkin lymphoma [<xref rid="B80-vaccines-04-00039" ref-type="bibr">80</xref>
], ovarian cancer [<xref rid="B81-vaccines-04-00039" ref-type="bibr">81</xref>
], glioblastoma multiforme [<xref rid="B82-vaccines-04-00039" ref-type="bibr">82</xref>
], breast [<xref rid="B83-vaccines-04-00039" ref-type="bibr">83</xref>
] and prostate [<xref rid="B79-vaccines-04-00039" ref-type="bibr">79</xref>
] cancers. In this context, tumor regression was obtained in SCID mice with human lymphoma xenografts after intratumoral injection of MV-Edm [<xref rid="B80-vaccines-04-00039" ref-type="bibr">80</xref>
]. Moreover, co-administration of MV vectors expressing carcinoembryonic antigen (CEA) and thyroidal sodium iodide symporter (NIS) in mice with SKOV3ip.1 ovarian xenografts showed superior tumor regression in comparison to treatment with either MV-CEA or MV-NIS alone [<xref rid="B81-vaccines-04-00039" ref-type="bibr">81</xref>
]. To improve delivery and enhance efficacy, CD46 and signaling lymphocytic activation molecule (SLAM) ablating mutations in the hemagglutinin protein in combination with the display of a single-chain antibody against the epidermal growth factor receptor (EGFR) were incorporated into MV vectors for tumor targeting [<xref rid="B82-vaccines-04-00039" ref-type="bibr">82</xref>
]. Tumor regression and significantly extended survival were observed after intratumoral administration of MV. Evaluation of MV-CEA delivery in an MDA-MB-231 mammary tumor model revealed a significant delay in tumor growth and prolonged survival [<xref rid="B83-vaccines-04-00039" ref-type="bibr">83</xref>
]. Moreover, intratumoral administration of MV-CEA vectors showed tumor growth delay and improved survival in a subcutaneous PC-3 xenograft model [<xref rid="B79-vaccines-04-00039" ref-type="bibr">79</xref>
].</p>
<p>Rhabdoviruses have also been applied in cancer therapy [<xref rid="B84-vaccines-04-00039" ref-type="bibr">84</xref>
]. VSV vectors lack pre-existing immunity in humans and have demonstrated high susceptibility of cancer cells. Particularly, VSV vectors have been subjected to aggressive pancreatic ductal adenocarcinoma (PDAC) showing superiority to Sendai virus and RSV in 13 clinically relevant human pancreatic cell lines, although the response varied from one cell line to another [<xref rid="B85-vaccines-04-00039" ref-type="bibr">85</xref>
]. Moreover, evaluation in ten PDAC cell lines of three VSV vectors expressing the wild-type matrix protein or ∆M51 showed activation of VSV-mediated apoptosis [<xref rid="B86-vaccines-04-00039" ref-type="bibr">86</xref>
]. However, high constitutive expression of IFN-stimulated genes (ISGs) was discovered in three cell lines, which also contributed to resistance to apoptosis.</p>
<p>Kunjin virus replicons expressing the granulocyte colony-stimulating factor (GM-CSF) have been subjected to intratumoral administration, which resulted in cure in less than 50% of mice with established CT26 colon carcinoma and B16-OVA melanomas [<xref rid="B87-vaccines-04-00039" ref-type="bibr">87</xref>
]. Subcutaneous injection led to regression in CT26 lung metastasis. Moreover, Kunjin vectors were engineered to express a CTL epitope of HPV16 E7 protein, which induced E7-directed T-cell responses and provided protection against challenges with an E7-expressing epithelial tumor in mice [<xref rid="B88-vaccines-04-00039" ref-type="bibr">88</xref>
]. In this study, the Kunjin VLPs were more effective than RNA replicons or DNA vectors.</p>
<p>Alphavirus vectors have been applied in many studies on cancer vaccines [<xref rid="B4-vaccines-04-00039" ref-type="bibr">4</xref>
,<xref rid="B8-vaccines-04-00039" ref-type="bibr">8</xref>
]. In principle, tumor-associated antigens (TAAs), immunomodulating cytokines and combination therapies of TAAs and cytokines, TAAs and antibodies, cytokines and antibodies and even microRNAs (miRNAs) have been evaluated. In this context, intratumoral injection of SFV particles expressing enhanced green fluorescent protein (EGFP) showed apoptosis induction in mice implanted with human non-small cell lung carcinoma H353a cells in mice [<xref rid="B109-vaccines-04-00039" ref-type="bibr">109</xref>
]. Furthermore, intratumoral administration of SFV particles into BALB/c mice with implanted sarcoma K-BALB sarcoma and CT26 colon tumors resulted in significant tumor growth inhibition [<xref rid="B103-vaccines-04-00039" ref-type="bibr">103</xref>
]. Also, vaccination of mice with SFV RNA replicons expressing β-galactosidase showed protection against challenges with colon tumor cells [<xref rid="B100-vaccines-04-00039" ref-type="bibr">100</xref>
]. Only a single intratumoral injection of 1 μg of SFV-LacZ RNA resulted in 10–20 days of survival extension in mice with existing tumors. Similarly, SIN-LacZ vectors demonstrated therapeutic efficacy in a mouse CT26 colon carcinoma model [<xref rid="B101-vaccines-04-00039" ref-type="bibr">101</xref>
]. Despite not targeting specifically CT26 cells, SIN vectors showed susceptibility to mediastinal lymph nodes (MLNs), which induced effector and memory CD8+ T-cells displaying robust cytotoxicity. The well-characterized human carcinoembryonic antigen (CEA) elicited neutralizing antibodies after VEE VLP immunization [<xref rid="B120-vaccines-04-00039" ref-type="bibr">120</xref>
]. Moreover, melanoma antigens such as tyrosine-related proteins TRP-1 and TRP-2, gp100 and melanoma antigen tyrosinase (Tyr) have been expressed from VEE vectors [<xref rid="B94-vaccines-04-00039" ref-type="bibr">94</xref>
,<xref rid="B112-vaccines-04-00039" ref-type="bibr">112</xref>
]. For instance, immunization of mice with VEE-TRP-2 particles resulted in growth inhibition of B16 transplantable melanoma and strong therapeutic potency [<xref rid="B111-vaccines-04-00039" ref-type="bibr">111</xref>
]. Vaccination with VEE-TRP-2 VLPs was more efficient than the combination of VEE-gp100 and VEE-Tyr particles. Furthermore, VEE particles carrying the Tyr gene induced immune responses and tumor protection in mice after administration of VEE VLPs alone or an initial vaccination with plasmid DNA followed by boosting with VEE VLPs [<xref rid="B112-vaccines-04-00039" ref-type="bibr">112</xref>
].</p>
<p>Breast cancer has been targeted in several therapeutic and prophylactic vaccine studies. SIN plasmid DNA carrying the neu gene were subjected to immunization of mice resulting in inhibition of growth of challenged A2L2 tumor cells [<xref rid="B94-vaccines-04-00039" ref-type="bibr">94</xref>
]. Interestingly, vaccination two days after tumor challenge was inefficient. In contrast, immunization in a prime-boost protocol with SIN-neu DNA followed by adenovirus vectors carrying the neu gene prolonged the survival of mice. Due to their potency of stimulation of antigen-specific T-cells, dendritic cells (DCs) were transduced by VEE-neu particles, which resulted in high-level transgene expression, DC maturation and secretion of pro-inflammatory cytokines [<xref rid="B95-vaccines-04-00039" ref-type="bibr">95</xref>
]. Robust neu-specific CD8+ T-cell and anti-neu IgG responses were observed after a single immunization. Moreover, regression of large established tumors was obtained. Another TAA attractive for immunotherapy is the six-transmembrane epithelial antigen of the prostate (STEAP), which has demonstrated up-regulation in multiple cancer cell lines [<xref rid="B121-vaccines-04-00039" ref-type="bibr">121</xref>
]. Transgenic adenocarcinoma of mouse prostate (TRAMPC-2) tumor-bearing mice pre-immunized with VEE VLPs expressing STEAP demonstrated a strong immune response and a significantly prolonged overall survival [<xref rid="B116-vaccines-04-00039" ref-type="bibr">116</xref>
]. The therapeutic affect was assessed for mice with 31-day-old tumors, which resulted in a modest but significant delay in tumor growth. Furthermore, VEE VLPs have been applied for expression of the prostate stem cell antigen (PSCA) in TRAMP mice, where the initial immunization with a PSCA DNA plasmid was followed by VEE-PSCA VLP delivery [<xref rid="B117-vaccines-04-00039" ref-type="bibr">117</xref>
]. The outcome was a specific immune response and protection against tumor challenges in 90% of TRAMP mice. Also, the prostate-specific membrane antigen (PSMA) has been expressed from VEE vectors demonstrating strong humoral and cellular immune responses in subcutaneously immunized mice [<xref rid="B115-vaccines-04-00039" ref-type="bibr">115</xref>
]. VEE VLPs expressing the prostate-specific antigen (PSA) were used for immunization of mice followed by a challenge with TRAMP cells [<xref rid="B118-vaccines-04-00039" ref-type="bibr">118</xref>
]. The VEE VLPs were capable of infecting DCs in vitro and induced a robust PSA-specific response in vivo. Tumors in vaccinated animals showed low PSA expression levels and tumor growth was significantly delayed.</p>
<p>The P815A antigen is expressed in P815 mastocytoma tumors, which triggered an immunization study on the P1A gene coding for the PP815A antigen [<xref rid="B119-vaccines-04-00039" ref-type="bibr">119</xref>
]. SFV particles expressing the P1A gene elicited strong CTL responses and protected immunized mice from challenges with P815 tumors. Other interesting TAA vaccine targets have been the E6 and E7 proteins of the human papilloma virus (HPV). Immunization with SFV particles expressing HPV type 16 E6,7 showed strong HPV-specific CTL activity and eradicated HPV-transformed tumors [<xref rid="B97-vaccines-04-00039" ref-type="bibr">97</xref>
]. Similarly, immunization of mice with VEE particles carrying the HPV16 E7 gene prevented tumor development and eliminated established tumors in 67% of vaccinated animals [<xref rid="B99-vaccines-04-00039" ref-type="bibr">99</xref>
]. In another study, tattoo injection [<xref rid="B122-vaccines-04-00039" ref-type="bibr">122</xref>
] of SFV-HPV E6,7 particles resulted in antigen expression in both the skin and draining lymph nodes leading to ten-fold lower antigen levels in comparison to intramuscular administration [<xref rid="B98-vaccines-04-00039" ref-type="bibr">98</xref>
]. However, tattoo injection provided higher or equal levels of immune responses.</p>
<p>Cytokines have played an important role in immunotherapy and vaccine development [<xref rid="B8-vaccines-04-00039" ref-type="bibr">8</xref>
]. For instance, interleukin-12 (IL-12) has been expressed from both SFV and SIN vectors. In this context, SFV vectors expressing IL-12 induced tumor regression with long-term tumor-free survival in the MC38 colon carcinoma model [<xref rid="B102-vaccines-04-00039" ref-type="bibr">102</xref>
]. Repeated intratumoral administration increased the anti-tumor response. In another study, immunization with SFV-luciferase and SFV-IL-12 particles was evaluated in a woodchuck model in which hepatocellular carcinoma (HCC) is induced by the infection by woodchuck hepatitis virus (WHV) [<xref rid="B105-vaccines-04-00039" ref-type="bibr">105</xref>
]. High luciferase expression levels were observed in tumors and IL-12 secretion was measured in the serum after intratumoral injections. In tumor-bearing woodchucks, partial tumor remission was seen. Tumor volumes were reduced by 80%, but tumor growth was restored with time. The plasmid vector pTonL2(T)-mIL12, which provides liver-specific and inducible IL-12 expression, has been compared to SFV-IL-12 particle delivery in a L-PK/c-myc transgenic mouse model of HCC [<xref rid="B106-vaccines-04-00039" ref-type="bibr">106</xref>
]. Overexpression of the c-myc gene in the liver of the transgenic animals induces spontaneous hepatic tumors with characteristics similar to human HCCs. Intratumoral administration of SFV-IL-12 resulted in tumor growth arrest and 100% survival rates. Mice treated with plasmid DNA showed a slightly lower survival rate despite higher IL-12 and IFN-γ levels in serum. The strong anti-tumor response in SFV-IL-12-treated mice was most likely due to the apoptosis and type 1 IFN response induced by SFV particles. Recombinant SIN particles were demonstrated to target tumor cells in SCID mice, which encouraged intraperitoneal injection of SIN-IL-12 particles in mice with established ovarian tumors [<xref rid="B113-vaccines-04-00039" ref-type="bibr">113</xref>
]. The treatment resulted in systemic targeting and eradication of tumor cells without any adverse effects observed. Glioma-bearing mice were immunized with SFV-IL-12 particles, which induced apoptosis of glioma cells and facilitated the uptake of apoptotic cells by DCs and provided prolonged survival of vaccinated animals [<xref rid="B91-vaccines-04-00039" ref-type="bibr">91</xref>
]. Moreover, DCs isolated from bone marrow were transduced with SFV vectors expressing IL-12 for the treatment of brain tumor-bearing mice [<xref rid="B92-vaccines-04-00039" ref-type="bibr">92</xref>
]. The outcome was prolonged survival of immunized animals. In another study, SFV-IL-12 particles were tested in rat RG2 gliomas [<xref rid="B93-vaccines-04-00039" ref-type="bibr">93</xref>
]. Low dose (5 × 10<sup>7</sup>
VLPs) treatment resulted in a 70% reduction in tumor volume, whereas high-dose (5 × 10<sup>8</sup>
VLPs) showed an 87% reduction in tumor volume. Moreover, intratumoral administration of 10<sup>6</sup>
oncolytic SFV particles expressing EGFP generated significant tumor regression in melanoma-bearing SCID mice [<xref rid="B123-vaccines-04-00039" ref-type="bibr">123</xref>
]. Other cytokines such as Il-18 have also been evaluated for alphavirus-based expression in ovarian and colon cancer models [<xref rid="B104-vaccines-04-00039" ref-type="bibr">104</xref>
]. The enhanced SFV10E vector, which provides ten-fold higher levels of expression than the conventional SFV vector [<xref rid="B124-vaccines-04-00039" ref-type="bibr">124</xref>
], was applied for immunization of BALB/c mice [<xref rid="B114-vaccines-04-00039" ref-type="bibr">114</xref>
]. After in vitro verification of secretion of active IL-18, mice with subcutaneous K-BALB and CT26 tumors were injected with SFV-IL-18 particles, which led to tumor regression and disappearance of tumors in some treated animals. Moreover, GM-CSF, an immunostimulatory cytokine, has been expressed from SFV vectors [<xref rid="B114-vaccines-04-00039" ref-type="bibr">114</xref>
]. Intraperitoneal administration of SFV-GM-CSF particles was evaluated in an ovarian mouse tumor model, which resulted in activation of macrophages to tumor cytotoxicity. Although no prolongation in survival of tumor-bearing mice was achieved, tumor growth was inhibited for two weeks.</p>
<p>Among the growth factors targeted for vaccine development, the vascular endothelial growth factor receptor 2 (VEGFR-2) was introduced into the SFV vector [<xref rid="B96-vaccines-04-00039" ref-type="bibr">96</xref>
]. Immunization of mice with SFV-VEGFR-2 particles resulted in substantial inhibition of both tumor growth and spread of pulmonary metastases. Furthermore, vaccination led to tumor inhibition in mice with established CT26 colon tumors and metastatic 4T1 mammary tumors. In another approach, SFV particles carrying the endostatin gene were administered to mice bearing B16 brain tumors [<xref rid="B89-vaccines-04-00039" ref-type="bibr">89</xref>
]. The treatment resulted in a substantial reduction in intratumoral vascularization in tumor sections and a significant inhibition of tumor growth. Endostatin serum levels were three-fold higher 7 days after intravenous administration of SFV-endostatin in comparison to administration of the retrovirus-based GCsap-Endostatin promoting inhibition of angiogenesis in established tumors. In another approach, SIN vectors have been employed for the expression of a fusion protein of HPV16 E7 protein and calreticulin (CRT), an ER Ca2<sup>+</sup>
-binding transporter participating in antigen processing and presentation with major histocompatibility complex (MHC) class I [<xref rid="B108-vaccines-04-00039" ref-type="bibr">108</xref>
]. Immunization of mice bearing E7-expressing tumors with SIN-E7-CRT particles significantly increased E7-specific CD8+ T-cell precursors and a strong anti-tumor response. Furthermore, a significant reduction in lung tumor nodules was observed in immuno-compromised BALB/c mice.</p>
<p>Combination therapy has been evaluated for alphavirus-based gene delivery. For instance, SFV layered DNA vectors were engineered to express one to four domains of VEGFR-2 and IL-12 [<xref rid="B110-vaccines-04-00039" ref-type="bibr">110</xref>
]. Co-immunization with SFV replicon DNA expressing survivin and β-hCG antigens was verified in mice resulting in efficient humoral and cellular immune responses against survivin, β-hCG and VEGFR-2. Moreover, tumor growth was inhibited and the survival rate in a B16 melanoma mouse model was improved. Furthermore, immunization with SFV HPV E6/E7 was combined with sunitib and a single low-dose of irradiation, which enhanced the intratumoral ratio of anti-tumor effector cells to myeloid-derived suppressor cells [<xref rid="B107-vaccines-04-00039" ref-type="bibr">107</xref>
]. Triple treatment of tumor-bearing mice demonstrated enhanced anti-tumor efficacy and provided 100% tumor-free survival.</p>
<p>An interesting approach comprises the introduction of micro RNA-124 (miR-124) into an SFV4 vector [<xref rid="B90-vaccines-04-00039" ref-type="bibr">90</xref>
]. As IFN-1 tolerance has been associated with the SFV nsP3-nsP4 genes, conditionally replicating SFV4-miR-124 virus was able to replicate in neurons and allowed targeting of gliomas otherwise sensitive to IFN-1. Evaluation of CT-2A mouse astrocytoma cells and IFN-1 pretreated human glioblastoma cells showed increased oncolytic potency. Moreover, a single intraperitoneal injection of SFV4-miR-124 into mice with implanted CT-2A orthotopic gliomas showed significant inhibition of tumor growth and improved survival rates.</p>
</sec>
<sec id="sec3dot3-vaccines-04-00039"><title>3.3. Clinical Trials</title>
<p>Self-replicating RNA virus vectors have been subjected to several clinical studies, albeit at an inferior level in comparison to adenovirus, AAV and lentivirus vectors. For instance, healthy volunteers were subjected to low-dose (3 × 10<sup>5</sup>
pfu) immunization with the VSV-based Ebola vaccine (rVSV-ZEBOV) expressing the Zaire Ebola virus glycoprotein in a double-blinded study in comparison to a previous study with a high dose (5 × 10<sup>7</sup>
pfu) [<xref rid="B125-vaccines-04-00039" ref-type="bibr">125</xref>
]. No serious adverse events occurred and the overall safety was good. The low-dose immunization improved early tolerability, but generated inferior antibody responses and failed to prevent vaccine-induced arthritis, dermatitis or vasculitis. Furthermore, VSV particles expressing the HIV-1 gag gene were evaluated in a clinical trial on safety and immunogenicity [<xref rid="B126-vaccines-04-00039" ref-type="bibr">126</xref>
]. In the randomized double-blinded placebo-controlled dose-escalation study, healthy HIV-negative volunteers received 4.6 × 10<sup>3</sup>
to 3.4 × 10<sup>7</sup>
pfu of rVSV HIV-1 gag vaccine intramuscularly at months 0 and 2. All vaccinated individuals showed antibody responses against VSV, and gag-specific T-cell responses were detected in 63%. Overall, the safety profile was good.</p>
<p>Alphaviruses have been subjected to some gene therapy and vaccine studies. In one approach, replication-deficient SFV particles were encapsulated in liposomes to promote passive targeting of tumors [<xref rid="B127-vaccines-04-00039" ref-type="bibr">127</xref>
]. Initially, intraperitoneal administration of encapsulated SFV-LacZ particles showed enhanced accumulation of β-galactosidase in SCID mice implanted with LNCaP prostate tumors. Liposome-encapsulated SFV particles expressing the p40 and p35 subunits of IL-12 generated active secreted IL-12 in BHK-21 cells [<xref rid="B128-vaccines-04-00039" ref-type="bibr">128</xref>
]. Next, encapsulated SFV-IL-12 particles were administered intravenously in terminally ill melanoma and kidney carcinoma patients in a phase I clinical trial. The patients showed a five to ten-fold increase in IL-12 plasma levels. The maximum tolerated dose was determined to 3 × 10<sup>9</sup>
infectious particles and the safety profile was good. A phase I dose-escalation trial was conducted in prostate cancer patients with VEE particles expressing PSMA [<xref rid="B129-vaccines-04-00039" ref-type="bibr">129</xref>
]. Patients with castration-resistant metastatic prostate cancer (CRPC) received up to five doses of either 0.9 × 10<sup>7</sup>
IU or 0.36 × 10<sup>8</sup>
IU of VEE-PSMA particles at weeks 1, 4, 7, 10 and 18. The study showed no toxicity and good toleration of the vaccination. However, only weak PSMA-specific immune responses were detected and no clinical benefits obtained. In another clinical trial, VEE particles expressing the CEA tumor antigen were demonstrated to efficiently infect DCs [<xref rid="B120-vaccines-04-00039" ref-type="bibr">120</xref>
]. The VEE particles could be repeatedly administered and overcame high titers of neutralizing antibodies and elevated regulatory T cells (Tregs), which allowed induction of clinically relevant CEA-specific T cell and antibody responses. In another approach, VEE particles expressing the cytomegalovirus (CMV) gB and pp65/IE1 fusion protein were evaluated in a phase I randomized, double-blinded clinical trial [<xref rid="B67-vaccines-04-00039" ref-type="bibr">67</xref>
]. Intramuscular or subcutaneous immunization at weeks 0, 8 and 24 of CMV seronegative adult volunteers showed good tolerance with only mild to moderate local reactions and no clinically important changes. Neutralizing and multifunctional T-cell responses against CMV antigens were detected in all vaccinated individuals.</p>
</sec>
</sec>
<sec id="sec4-vaccines-04-00039"><title>4. Conclusions</title>
<p>Self-replicating RNA viruses represented by ssRNA viruses of both negative and positive polarity have been subjected to engineering of efficient gene delivery vectors, which can be applied in the form of recombinant particles, RNA replicons and layered DNA plasmid vectors. In this context, measles (MV), rhabdoviruses, flaviviruses and alphaviruses expressing surface antigens from viruses and other infectious agents have been subjected to immunization studies in animal models. Moreover, similar studies have been conducted with tumor antigens. It seems that MV-, rabies virus (RABV)-, vesicular stomatitis virus (VSV)-, Kunjin virus-, Semliki Forest virus (SFV)-, Sindbis virus (SIN)- and Venezuelan equine encephalitis virus (VEE)-based delivery efficiently elicits humoral and cellular immune responses in immunized animals. Furthermore, numerous cases have demonstrated protection against challenges with lethal viruses/infectious agents or with tumor cells. Most of the studies have been conducted with replication-deficient recombinant particles. However, promising results have also been obtained with layered DNA plasmid vectors. A limited number of studies have applied administration of RNA replicons, but the results have been quite encouraging. The obvious advantage to using nucleic acid-based delivery is the elimination of any risk of virus progeny production through recombination events. On the other hand, superior delivery and prolonged duration of expression can be achieved with recombinant viral particles, especially applying replication-proficient oncolytic viruses. For this reason, it is difficult to make any recommendations related to which delivery format to use, and the choice of target will play an important role in decision making.</p>
<p>Similarly, it is practically impossible to favor one viral vector system over another. Reverse genetics systems engineered for MV and rhabdoviruses and packaging cell lines for flaviviruses surely facilitate recombinant particle production and ease of use. Although packaging cell lines have also been generated for alphaviruses, the straightforward in vitro RNA transcription has provided the means for sufficient preparation of replicon RNA and particles for immunization studies. Obviously, plasmid DNA can be directly applied for vaccinations. In comparison to other viral vectors and also non-viral delivery systems, self-replicating RNA viruses can surely be considered competitive (<xref ref-type="fig" rid="vaccines-04-00039-f005">Figure 5</xref>
and <xref ref-type="table" rid="vaccines-04-00039-t004">Table 4</xref>
). An extensive comparison to other delivery systems is not within the scope of this review, so only a few examples are addressed. Clearly, adenovirus-based vaccine development and gene therapy has a longer history, which has generated a multitude [<xref rid="B130-vaccines-04-00039" ref-type="bibr">130</xref>
] of vector improvements and also resulted a number of clinical trials [<xref rid="B131-vaccines-04-00039" ref-type="bibr">131</xref>
,<xref rid="B132-vaccines-04-00039" ref-type="bibr">132</xref>
]. Similarly, herpes simplex virus (HSV) vectors have been frequently applied and HSV-GM-CSF have, for instance, been subjected to phase I−III human clinical trials in glioblastoma and melanoma patients [<xref rid="B133-vaccines-04-00039" ref-type="bibr">133</xref>
]. HSV vectors were recently approved by the FDA for use in standard patient care [<xref rid="B134-vaccines-04-00039" ref-type="bibr">134</xref>
]. Related to non-viral vectors, recently dendrimer-RNA nanoparticles have demonstrated protective immunity against lethal challenges with Ebola virus, influenza H1N1 virus and <italic>Toxoplasma gondii</italic>
after a single injection in BALB/c mice [<xref rid="B135-vaccines-04-00039" ref-type="bibr">135</xref>
].</p>
<p>Overall, self-replicating RNA viral vectors possess several attractive features. The presence of RNA replicons provides the efficient means for rapid generation of a large number of RNA copies for immediate protein translation in the cytoplasm of host cells. Moreover, the strong subgenomic promoter utilized by alphaviruses generates extreme levels of heterologous gene expression. The transient nature of expression is also an advantage for immunization studies. Furthermore, there is no risk of integration of viral genes in the host genome as the viral RNA is degraded within 3–5 days. In the case of immunization with layered alphavirus DNA vectors, approximately 100- to 1000-fold lower doses are required compared to immunizations with conventional plasmid DNA [<xref rid="B136-vaccines-04-00039" ref-type="bibr">136</xref>
].</p>
<p>Although strong immune responses have been obtained and protection against challenges with lethal pathogens and tumor cells have been achieved and even tumor regression observed in animals with established tumors, some further technology development is necessary. Much development has been invested in vector design including mutant vectors, enhancement signals, targeting DCs and fusion constructs. Furthermore, quite an effort has been paid to the evaluation of different target antigens and immunogens. Several studies, particularly clinical trials, have indicated that although target-specific immune responses have been obtained, further investment is required in finding the right dose for the achievement of optimal response. One area which recently has received much attention is combination therapy. Tumor-associated antigens (TAAs) have been combined with cytokines and antibodies, as well as drugs and radiation co-administered with cytokines. Additionally, optimization of adjuvant composition and stability issues in case of RNA delivery needs to be addressed. Further research in these areas will certainly provide progress and should make immunotherapy an important approach in both prophylactic and therapeutic applications.</p>
</sec>
</body>
<back><notes notes-type="COI-statement"><title>Conflicts of Interest</title>
<p>The author declares no conflict of interest.</p>
</notes>
<glossary><title>Abbreviations</title>
<p>The following abbreviations are used in this manuscript:
<array><tbody><tr><td align="left" valign="middle" rowspan="1" colspan="1">MDPI</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Multidisciplinary Digital Publishing Institute</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">DOAJ</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Directory of open access journals</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">CEA</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Carcinoembryonic antigen</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">CMV</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Cytomegalovirus</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">CRPC</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Castration-resistant metastatic prostate cancer</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">CRT</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Calreticulin</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">CTL</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Cytotoxic T-lymphocyte</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">DC</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Dendritic cell</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">EGFP</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Enhanced green fluorescent protein</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">EGFR</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Epidermal growth factor receptor</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">GFP</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Green fluorescent protein</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">GM-CSF</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Granylocyte macrophage colony-stimulating factor</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">GoI</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Gene of interest</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">HA</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Hemagglutinin</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">HBV</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Hepatitis B virus</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">HCC</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Hepatocellular carcinoma</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">HPV</td>
<td align="left" valign="middle" rowspan="1" colspan="1">zhuman papilloma virus</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">IF3</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Initiation factor 3</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">IFN</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Interferon</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">IL</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Interleukin</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">ISG</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Interferon-stimulated gene</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">MERS-CoV</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Middle East respiratory syndrome coronavirus</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">MHC</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Major histocompatibility complex</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">miRNA</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Micro RNA</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">MLN</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Mediastinal lymph nodes</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">MV</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Measles virus</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">NIS</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Sodium iodide symporter</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">NP</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Nucleoprotein</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">PDAC</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Pancreatic ductal adenocarcinoma</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">PSMA</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Prostate-specific membrane antigen</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">PSCA</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Prostate stem cell antigen</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">RABV</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Rabies virus;</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">RSV</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Respiratory syndrome virus</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">SARS-CoV</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Severe acute respiratory syndrome coronavirus</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">SFV</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Semliki Forest virus</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">SEB</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Staphylococcus enterotoxin B</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">SIN</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Sindbis virus</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">ssRNA</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Single-stranded RNA</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">STEAP</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Six-transmembrane epithelial antigen of the prostate</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">TAA</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Tumor-associated antigen</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">TRAMP</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Transgene adenocarcinoma of the mouse prostate</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">TRP</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Tyrosine-related protein</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">Tyr</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Tyrosinase</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">VEE</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Venezuelan equine encephalitis virus</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">VEGFR</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Vascular endothelial growth factor receptor</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">VLPs</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Virus-like particles</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">VSV</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Vesicular stomatitis virus</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1">WHV</td>
<td align="left" valign="middle" rowspan="1" colspan="1">Woodchuck hepatitis virus</td>
</tr>
</tbody>
</array>
</p>
</glossary>
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<floats-group><fig id="vaccines-04-00039-f001" position="float"><label>Figure 1</label>
<caption><p>SFV-Based Expression Systems. (<bold>A</bold>
) Replication-deficient system. In vitro transcribed RNA from expression and helper vectors are transfected into BHK-21 cells for generation of replication-deficient particles; (<bold>B</bold>
) Replication-proficient system. In vitro transcribed RNA from full-length vector is transfected into BHK-21 cells for generation of replication-proficient particles; (<bold>C</bold>
) DNA layered system. Plasmid DNA is transfected into host cells. 26S, SFV26S subgenomic promoter; CMV, cytomegalovirus promoter; pA, polyadenylation signal; SP6, SP6 phage RNA polymerase promoter.</p>
</caption>
<graphic xlink:href="vaccines-04-00039-g001"></graphic>
</fig>
<fig id="vaccines-04-00039-f002" position="float"><label>Figure 2</label>
<caption><p>Kunjin Virus-Based Expression Systems. Expression vector based on Kunjin virus RNA and DNA expression systems. 3′ UTR, 3′ untranslated region; 5′ UTR, 5′ untranslated region; C20, first 20 amino acids of KUN C protein; CMV, cytomegalovirus promoter; E22, 22 last amino acids of KUN E protein; F, FMDV (foot-and-mouse disease virus) 2A autoprotease; HDVr, hepatitis delta virus ribozyme; ns1-5, nonstructural proteins; pA, polyadenylation signal; SP6, SP6 phage RNA polymerase promoter; U, mouse ubiquitin sequence.</p>
</caption>
<graphic xlink:href="vaccines-04-00039-g002"></graphic>
</fig>
<fig id="vaccines-04-00039-f003" position="float"><label>Figure 3</label>
<caption><p>Measles Virus-Based Expression system. The measles virus structural proteins are flanked by T7 RNA polymerase promoter and the T7 RNA polymerase terminator. Foreign genes can be inserted between the P and M or H and L genes. H, MV hemagglutinin; L, MV L protein; M, MV matrix protein; N, MV nucleocapsid protein; T7, T7 RNA polymerase promoter; T7 term, T7 RNA polymerase terminator.</p>
</caption>
<graphic xlink:href="vaccines-04-00039-g003"></graphic>
</fig>
<fig id="vaccines-04-00039-f004" position="float"><label>Figure 4</label>
<caption><p>Rabies Virus-Based Expression Systems. The structural genes are from the HEP-Flury strain except the G protein from the CVS strain. Foreign genes can be inserted between the N and P or G and L genes, respectively. CMV, cytomegalovirus promoter; G, rabies G protein; L, rabies L protein; M, rabies matrix protein; N, rabies nucleocapsid protein.</p>
</caption>
<graphic xlink:href="vaccines-04-00039-g004"></graphic>
</fig>
<fig id="vaccines-04-00039-f005" position="float"><label>Figure 5</label>
<caption><p>Schematic Presentation of the Life-Cycle of Self-Replicating RNA Viruses and Their Advantages. Several cell receptors are recognized providing a broad range of susceptible host cells. RNA released in the cytoplasm is immediately subjected to RNA replication and translation. Extreme RNA replication is the basis for highly efficient transgene expression.</p>
</caption>
<graphic xlink:href="vaccines-04-00039-g005"></graphic>
</fig>
<table-wrap id="vaccines-04-00039-t001" position="float"><object-id pub-id-type="pii">vaccines-04-00039-t001_Table 1</object-id>
<label>Table 1</label>
<caption><p>Self-replicating RNA viral vector-based immunizations against viral diseases.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Virus</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Target</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Vector</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Immunization</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Response</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Reference</th>
</tr>
</thead>
<tbody><tr><td rowspan="6" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Influenza</td>
<td align="center" valign="middle" rowspan="1" colspan="1">NP</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" rowspan="1" colspan="1">systemic NP immune response</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B35-vaccines-04-00039" ref-type="bibr">35</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">HA</td>
<td align="center" valign="middle" rowspan="1" colspan="1">VEE VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">chicken</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against influenza virus</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B36-vaccines-04-00039" ref-type="bibr">36</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">HA</td>
<td align="center" valign="middle" rowspan="1" colspan="1">VEE VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">swine</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against influenza virus</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B37-vaccines-04-00039" ref-type="bibr">37</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">HA</td>
<td align="center" valign="middle" rowspan="1" colspan="1">VEE VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">swine</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against influenza virus</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B38-vaccines-04-00039" ref-type="bibr">38</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">HA</td>
<td align="center" valign="middle" rowspan="1" colspan="1">rMV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" rowspan="1" colspan="1">neutralizing Abs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B39-vaccines-04-00039" ref-type="bibr">39</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">cHA</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VSV</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">protection against influenza virus</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B40-vaccines-04-00039" ref-type="bibr">40</xref>
]</td>
</tr>
<tr><td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">HIV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Gag</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Kunjin VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against HIV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B41-vaccines-04-00039" ref-type="bibr">41</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Env</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" rowspan="1" colspan="1">neutralizing Abs, humoral response</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B42-vaccines-04-00039" ref-type="bibr">42</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">gp41</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV-VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" rowspan="1" colspan="1">generation of mAbs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B43-vaccines-04-00039" ref-type="bibr">43</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Env</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SFV DNA</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">T cell and IgG immune responses</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B44-vaccines-04-00039" ref-type="bibr">44</xref>
]</td>
</tr>
<tr><td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">SIV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Gag-Pol</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Kunjin VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">macaques</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against SIV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B45-vaccines-04-00039" ref-type="bibr">45</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Env</td>
<td align="center" valign="middle" rowspan="1" colspan="1">VSV VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">macaques</td>
<td align="center" valign="middle" rowspan="1" colspan="1">neutralizing Abs </td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B46-vaccines-04-00039" ref-type="bibr">46</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Gag-Env</td>
<td align="center" valign="middle" rowspan="1" colspan="1">VSV VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">macaques</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against SIV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B47-vaccines-04-00039" ref-type="bibr">47</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Gag-Env</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">RABV VLPs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">macaques</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">protection against SIV</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B48-vaccines-04-00039" ref-type="bibr">48</xref>
]</td>
</tr>
<tr><td rowspan="5" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Ebola</td>
<td align="center" valign="middle" rowspan="1" colspan="1">GP</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Kunjin VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">guinea pig</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against Ebola</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B49-vaccines-04-00039" ref-type="bibr">49</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">GP</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Kunjin VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">primate</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against Ebola</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B50-vaccines-04-00039" ref-type="bibr">50</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">GP</td>
<td align="center" valign="middle" rowspan="1" colspan="1">VSV VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">macaques</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against Ebola</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B51-vaccines-04-00039" ref-type="bibr">51</xref>
,<xref rid="B52-vaccines-04-00039" ref-type="bibr">52</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">GP, NP</td>
<td align="center" valign="middle" rowspan="1" colspan="1">VEE VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against Ebola</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B53-vaccines-04-00039" ref-type="bibr">53</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NP</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VEE VLPs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">protection against Ebola</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B54-vaccines-04-00039" ref-type="bibr">54</xref>
]</td>
</tr>
<tr><td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Lassa</td>
<td align="center" valign="middle" rowspan="1" colspan="1">G</td>
<td align="center" valign="middle" rowspan="1" colspan="1">VSV VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">guinea pig</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against Lassa</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B55-vaccines-04-00039" ref-type="bibr">55</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">G</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VEE VLPs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">guinea pig</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">protection against Lassa</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B56-vaccines-04-00039" ref-type="bibr">56</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SARS-CoV</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">G</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VEE VLPs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">protection against SARS-CoV</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B57-vaccines-04-00039" ref-type="bibr">57</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MERS-CoV</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">G</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MV</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">protection against SARS-CoV</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B58-vaccines-04-00039" ref-type="bibr">58</xref>
]</td>
</tr>
<tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">RSV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">F</td>
<td align="center" valign="middle" rowspan="1" colspan="1">MV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">rat</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against RSV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B39-vaccines-04-00039" ref-type="bibr">39</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">F</td>
<td align="center" valign="middle" rowspan="1" colspan="1">VEE LNPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against RSV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B59-vaccines-04-00039" ref-type="bibr">59</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">F</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VEE VLPs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">primate</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">protection against RSV </td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B60-vaccines-04-00039" ref-type="bibr">60</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MPV</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">F</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VEE VLPs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">primate</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">protection against MPV</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B60-vaccines-04-00039" ref-type="bibr">60</xref>
]</td>
</tr>
<tr><td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Dengue</td>
<td align="center" valign="middle" rowspan="1" colspan="1">DV2-HBsAg</td>
<td align="center" valign="middle" rowspan="1" colspan="1">MV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" rowspan="1" colspan="1">neutralizing Abs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B61-vaccines-04-00039" ref-type="bibr">61</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">DV2</td>
<td align="center" valign="middle" rowspan="1" colspan="1">MV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against dengue virus</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B62-vaccines-04-00039" ref-type="bibr">62</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">prME-E85</td>
<td align="center" valign="middle" rowspan="1" colspan="1">VEE VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">macaques</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against dengue virus</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B63-vaccines-04-00039" ref-type="bibr">63</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">prME-E85</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VEE VLPs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">protection against dengue virus</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B64-vaccines-04-00039" ref-type="bibr">64</xref>
]</td>
</tr>
<tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">HBV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">MHB</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV-VSV G</td>
<td align="center" valign="middle" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against HBV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B65-vaccines-04-00039" ref-type="bibr">65</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">DV2-HBsAg</td>
<td align="center" valign="middle" rowspan="1" colspan="1">MV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against HBV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B62-vaccines-04-00039" ref-type="bibr">62</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HBsAg</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MV</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">macaques</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">protection against HBV</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B66-vaccines-04-00039" ref-type="bibr">66</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CMV</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">gB-pp65/IE1</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VEE VLPs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">human</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">neutralizing Abs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B67-vaccines-04-00039" ref-type="bibr">67</xref>
]</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p>Abs, antibodies; cHA, chimeric hemagglutinin; CMV, cytomegalovirus; DV2, dengue virus 2; G, glycoprotein; HA, hemagglutinin; HBV, hepatitis B virus; HBsAg, HBV surface antigen; LNPs, lipid nanoparticles; mAbs, monoclonal antibodies; MERS-CoV, Middle East respiratory syndrome coronavirus; MV, measles virus; MPV, metapneumonia virus; NP, nucleoprotein; RABV, rabies virus; RSV, respiratory syncytial virus; SARS-CoV, severe acute respiratory syndrome coronavirus; SFV, Semliki Forest virus; VEE, Venezuelan equine encephalitis virus; VLPs, virus-like particles.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<table-wrap id="vaccines-04-00039-t002" position="float"><object-id pub-id-type="pii">vaccines-04-00039-t002_Table 2</object-id>
<label>Table 2</label>
<caption><p>Self-Replicating RNA Viral Vector-Based Immunizations against Infectious Diseases.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Agent</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Target</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Vector</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Immunization</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Response</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Reference</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>P. falciparum</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Ag Pf332</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV VLPs/RNA</td>
<td align="center" valign="middle" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" rowspan="1" colspan="1">immunological memory</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B68-vaccines-04-00039" ref-type="bibr">68</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>M. tuberculosis</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Ag 85A</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SIN DNA</td>
<td align="center" valign="middle" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against <italic>M.</italic>
<italic>tuberculosis</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B69-vaccines-04-00039" ref-type="bibr">69</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>C. botulinum</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">BoNTA-Hc</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV DNA</td>
<td align="center" valign="middle" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Ab and lymphoproliferative response</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B70-vaccines-04-00039" ref-type="bibr">70</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>B. abortus</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">IF3</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against <italic>Brucella</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B71-vaccines-04-00039" ref-type="bibr">71</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>B. antracis</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">PA</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SIN VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against <italic>B. antracis</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B72-vaccines-04-00039" ref-type="bibr">72</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Malaria</td>
<td align="center" valign="middle" rowspan="1" colspan="1">CS</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SIN VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against malaria</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B73-vaccines-04-00039" ref-type="bibr">73</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>L. monocytogenes</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">OVA</td>
<td align="center" valign="middle" rowspan="1" colspan="1">VSV-GP</td>
<td align="center" valign="middle" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protection against <italic>Listeria</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B74-vaccines-04-00039" ref-type="bibr">74</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Prion</td>
<td align="center" valign="middle" rowspan="1" colspan="1">PRNP</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" rowspan="1" colspan="1">monoclonal Abs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B75-vaccines-04-00039" ref-type="bibr">75</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Staphylococcus</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SEB</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VEE VLPs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">mouse</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">protection against enterotoxin</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B76-vaccines-04-00039" ref-type="bibr">76</xref>
]</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p>Abs, antibodies; CS, circumsporozoite protein; IF3, translation initiation factor 3; MV, measles virus; MPV, metapneumonia virus; OVA, ovalbumin; PRNP, prion protein; SEB, staphylococcus enterotoxin B; SFV, Semliki Forest virus; SIN, Sindbis virus; VEE, Venezuelan equine encephalitis virus; VLPs, virus-like particles; VSV-GP, vesicular stomatitis virus pseudotyped with lymphocytic choriomeningitis glycoprotein.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<table-wrap id="vaccines-04-00039-t003" position="float"><object-id pub-id-type="pii">vaccines-04-00039-t003_Table 3</object-id>
<label>Table 3</label>
<caption><p>Self-Replicating RNA Viral Vector-Based Immunizations against Cancers.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Cancer</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Target</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Vector</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Response</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Reference</th>
</tr>
</thead>
<tbody><tr><td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Brain</td>
<td align="center" valign="middle" rowspan="1" colspan="1">GFP, SLAM, EGFR</td>
<td align="center" valign="middle" rowspan="1" colspan="1">MV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">replication in/lysis of cancer cells</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B79-vaccines-04-00039" ref-type="bibr">79</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Endostatin</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">tumor inhibition</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B89-vaccines-04-00039" ref-type="bibr">89</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">miR-124</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV-miR-124</td>
<td align="center" valign="middle" rowspan="1" colspan="1">prolonged survival</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B90-vaccines-04-00039" ref-type="bibr">90</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">IL-12</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SFV-IL-12</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">prolonged survival</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B91-vaccines-04-00039" ref-type="bibr">91</xref>
,<xref rid="B92-vaccines-04-00039" ref-type="bibr">92</xref>
,<xref rid="B93-vaccines-04-00039" ref-type="bibr">93</xref>
]</td>
</tr>
<tr><td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Breast</td>
<td align="center" valign="middle" rowspan="1" colspan="1">CEA</td>
<td align="center" valign="middle" rowspan="1" colspan="1">MV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">tumor growth delay, better survival</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B83-vaccines-04-00039" ref-type="bibr">83</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Neu</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SIN DNA</td>
<td align="center" valign="middle" rowspan="1" colspan="1">immune responses, tumor protection</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B94-vaccines-04-00039" ref-type="bibr">94</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Neu</td>
<td align="center" valign="middle" rowspan="1" colspan="1">VEE VLPs + DCs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">tumor regression by transduced DCs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B95-vaccines-04-00039" ref-type="bibr">95</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VEGFR-2</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SFV VLPs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">tumor inhibition</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B96-vaccines-04-00039" ref-type="bibr">96</xref>
]</td>
</tr>
<tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Cervical</td>
<td align="center" valign="middle" rowspan="1" colspan="1">HPV E6, 7</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">tumor eradication</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B97-vaccines-04-00039" ref-type="bibr">97</xref>
,<xref rid="B98-vaccines-04-00039" ref-type="bibr">98</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">HPV E7</td>
<td align="center" valign="middle" rowspan="1" colspan="1">VEE VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">eradication of existing tumors</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B99-vaccines-04-00039" ref-type="bibr">99</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HPV E7 Epitope</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Kunjin VLPs/RNA/DNA</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">tumor protection in mice</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B88-vaccines-04-00039" ref-type="bibr">88</xref>
]</td>
</tr>
<tr><td rowspan="7" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Colon</td>
<td align="center" valign="middle" rowspan="1" colspan="1">GM-CSF</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Kunjin VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">regression of tumors and metastasis</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B87-vaccines-04-00039" ref-type="bibr">87</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">VEGFR-2</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">reduced tumor and metastasis growth</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B96-vaccines-04-00039" ref-type="bibr">96</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">LacZ</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV RNA</td>
<td align="center" valign="middle" rowspan="1" colspan="1">tumor protection in mice</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B100-vaccines-04-00039" ref-type="bibr">100</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Lac Z</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SIN VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">anti-tumor CD8+ T-cell immunity</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B101-vaccines-04-00039" ref-type="bibr">101</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">IL-12</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">tumor elimination</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B102-vaccines-04-00039" ref-type="bibr">102</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">SFV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">tumor growth inhibition</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B103-vaccines-04-00039" ref-type="bibr">103</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">IL-18</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SFV VLPs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">tumor regression in mice</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B104-vaccines-04-00039" ref-type="bibr">104</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Liver</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">IL-12</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SFV VLPs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">anti-tumor responses in woodchucks</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B105-vaccines-04-00039" ref-type="bibr">105</xref>
,<xref rid="B106-vaccines-04-00039" ref-type="bibr">106</xref>
]</td>
</tr>
<tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Lung</td>
<td align="center" valign="middle" rowspan="1" colspan="1">HPV E6/E7</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV + Sun + Rad</td>
<td align="center" valign="middle" rowspan="1" colspan="1">tumor-free survival</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B107-vaccines-04-00039" ref-type="bibr">107</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">HPV E7-CRT</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SIN VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">long-term anti-tumor effect</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B108-vaccines-04-00039" ref-type="bibr">108</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">EGFP</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SFV VLPs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">apoptosis, tumor regression in mice</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B109-vaccines-04-00039" ref-type="bibr">109</xref>
]</td>
</tr>
<tr><td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Melanoma</td>
<td align="center" valign="middle" rowspan="1" colspan="1">GM-CSF</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Kunjin VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">tumor regression</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B87-vaccines-04-00039" ref-type="bibr">87</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">VEGF-2-IL-12 + Sur + β-hCG</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">tumor inhibition</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B110-vaccines-04-00039" ref-type="bibr">110</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">TRP-2</td>
<td align="center" valign="middle" rowspan="1" colspan="1">VEE VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">humoral and cellular immunity</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B111-vaccines-04-00039" ref-type="bibr">111</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Tyr</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VEE VLPs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">T-cell responses, tumor protection in mice</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B112-vaccines-04-00039" ref-type="bibr">112</xref>
]</td>
</tr>
<tr><td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Ovarian</td>
<td align="center" valign="middle" rowspan="1" colspan="1">CEA, NIS</td>
<td align="center" valign="middle" rowspan="1" colspan="1">MV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">superior dual therapy</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B81-vaccines-04-00039" ref-type="bibr">81</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">IL-12</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SIN VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">tumor targeting, eradication</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B113-vaccines-04-00039" ref-type="bibr">113</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">IL-18</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">therapeutic anti-tumor response</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B91-vaccines-04-00039" ref-type="bibr">91</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">GM-CSF</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SFV VLPs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">tumor growth inhibition</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B114-vaccines-04-00039" ref-type="bibr">114</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Pancreatic</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Matrix protein</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VSV VLPs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">killing of tumor cells in vitro and in vivo</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B85-vaccines-04-00039" ref-type="bibr">85</xref>
]</td>
</tr>
<tr><td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Prostate</td>
<td align="center" valign="middle" rowspan="1" colspan="1">CEA</td>
<td align="center" valign="middle" rowspan="1" colspan="1">MV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">replication in/lysis of cancer cells</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B79-vaccines-04-00039" ref-type="bibr">79</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">PSMA</td>
<td align="center" valign="middle" rowspan="1" colspan="1">VEE VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">cellular and humoral immunity in mice</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B115-vaccines-04-00039" ref-type="bibr">115</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">STEAP</td>
<td align="center" valign="middle" rowspan="1" colspan="1">VEE VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">CD8+ T-cell response, tumor growth delay</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B116-vaccines-04-00039" ref-type="bibr">116</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PSCA</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">DNA + VEE VLPs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">long-term protective immune response</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B117-vaccines-04-00039" ref-type="bibr">117</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Sarcoma</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PSA</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VEE VLPs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PSA-cell clearance, tumor growth delay</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B118-vaccines-04-00039" ref-type="bibr">118</xref>
]</td>
</tr>
<tr><td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Skin</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV</td>
<td align="center" valign="middle" rowspan="1" colspan="1">SFV VLPs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">tumor growth inhibition</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B103-vaccines-04-00039" ref-type="bibr">103</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">P1A</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SFV VLPs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">strong CTL-response, tumor protection</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B119-vaccines-04-00039" ref-type="bibr">119</xref>
]</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p>CEA, carcinoembryonic antigen; CRT, calreticulin; CTL, cytotoxic T lymphocyte; EGFP, enhanced green fluorescent protein; EGFR, epidermal growth factor receptor; GFP, green fluorescent protein; GM-CSF, granulocyte macrophage colony-stimulating factor; HPV, human papilloma virus; MV, measles virus; NIS, sodium iodide symporter; PSMA, prostate-specific membrane antigen; PSCA, prostate stem cell antigen; RABV, rabies virus; SFV, Semliki Forest virus; SIN, Sindbis virus; SLAM, signaling lymphocytic activation molecule; STEAP, six-transmembrane epithelial antigen of the prostate; Sun, sunitab; Sur, survivin; TRP, tyrosine-related protein; Tyr, melanoma antigen tyrosinase; VEE, Venezuelan equine encephalitis virus; VEGFR, vascular endothelial growth factor receptor; VLPs, virus-like particles; VSV, vesicular stomatitis virus.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<table-wrap id="vaccines-04-00039-t004" position="float"><object-id pub-id-type="pii">vaccines-04-00039-t004_Table 4</object-id>
<label>Table 4</label>
<caption><p>Comparison of Self-replicating RNA Viral Vectors with other Viral Vectors.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Viral Vector</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Genome</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Capacity</th>
<th align="left" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Special Features</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Alphavirus</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ssRNA</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">6–8 kb</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">broad host range, high titer, cytoplasmic RNA, extreme transient expression, no chromosomal integration, choice of DNA, RNA replicon and particle delivery</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Flavivirus</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ssRNA</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">5 kb</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">broad host range, packaging system, choice of DNA, RNA replicon and particle delivery</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Measles virus</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ssRNA</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">5 kb</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">packaging cell line, measles virus strains for immunization, cytoplasmic RNA</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Rhabdovirus</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ssRNA</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">5 kb</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">reverse genetics systems, broad host range cytoplasmic RNA</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Adenovirus</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">dsDNA</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">>8 kb</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">broad host range, packaging cell line, nuclear translocation necessary, transient expression, potential integration</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">AAV</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ssDNA</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><4 kb</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">multiple AAV serotypes for avoiding immune responses, nuclear translocation necessary, chromosomal integration</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Herpes simplex virus</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">dsDNA</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">30–40 kb</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">large packaging capacity, nuclear translocation necessary, latent long-term transgene expression after integration</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Lentivirus</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">dsRNA</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">8 kb</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">transduction of dividing and non-dividing cells, nuclear translocation necessary, chromosomal integration</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Retrovirus</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">dsRNA</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">4 kb</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">transduction of only dividing cells, nuclear translocation necessary, chromosomal integration</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Vaccinia</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">dsDNA</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">25 kb</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">large packaging capacity, nuclear translocation necessary</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p>AAV, adeno-associated virus; dsDNA, double-stranded DNA; ssDNA, single-stranded DNA; ssRNA, single-stranded RNA.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</floats-group>
</pmc>
</record>
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