Tools to study pathogen-host interactions in bats
Identifieur interne : 001918 ( Pmc/Corpus ); précédent : 001917; suivant : 001919Tools to study pathogen-host interactions in bats
Auteurs : Arinjay Banerjee ; Vikram Misra ; Tony Schountz ; Michelle L. BakerSource :
- Virus Research [ 0168-1702 ] ; 2018.
Abstract
Bats are important reservoir hosts for emerging zoonotic viruses. Viruses detected in bats are difficult to isolate using traditional cell lines. Bat cell lines provide critical tools to dissect host pathogen interactions. Little is known about immune cell populations and their responses in bats. Sharing reagents and cell lines will accelerate research and virus discovery.
Url:
DOI: 10.1016/j.virusres.2018.02.013
PubMed: 29454637
PubMed Central: 7114677
Links to Exploration step
PMC:7114677Le document en format XML
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<author><name sortKey="Banerjee, Arinjay" sort="Banerjee, Arinjay" uniqKey="Banerjee A" first="Arinjay" last="Banerjee">Arinjay Banerjee</name>
<affiliation><nlm:aff id="aff0005">Department of Veterinary Microbiology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Canada</nlm:aff>
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<author><name sortKey="Misra, Vikram" sort="Misra, Vikram" uniqKey="Misra V" first="Vikram" last="Misra">Vikram Misra</name>
<affiliation><nlm:aff id="aff0005">Department of Veterinary Microbiology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Canada</nlm:aff>
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<author><name sortKey="Schountz, Tony" sort="Schountz, Tony" uniqKey="Schountz T" first="Tony" last="Schountz">Tony Schountz</name>
<affiliation><nlm:aff id="aff0010">Department of Microbiology, Immunology and Pathology, Arthropod-borne and Infectious Diseases laboratory, Colorado State University, Fort Collins, USA</nlm:aff>
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<author><name sortKey="Baker, Michelle L" sort="Baker, Michelle L" uniqKey="Baker M" first="Michelle L." last="Baker">Michelle L. Baker</name>
<affiliation><nlm:aff id="aff0015">CSIRO, Health and Biosecurity Business Unit, Australian Animal Health Laboratory, Geelong, Australia</nlm:aff>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Tools to study pathogen-host interactions in bats</title>
<author><name sortKey="Banerjee, Arinjay" sort="Banerjee, Arinjay" uniqKey="Banerjee A" first="Arinjay" last="Banerjee">Arinjay Banerjee</name>
<affiliation><nlm:aff id="aff0005">Department of Veterinary Microbiology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Canada</nlm:aff>
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<author><name sortKey="Misra, Vikram" sort="Misra, Vikram" uniqKey="Misra V" first="Vikram" last="Misra">Vikram Misra</name>
<affiliation><nlm:aff id="aff0005">Department of Veterinary Microbiology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Canada</nlm:aff>
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<author><name sortKey="Schountz, Tony" sort="Schountz, Tony" uniqKey="Schountz T" first="Tony" last="Schountz">Tony Schountz</name>
<affiliation><nlm:aff id="aff0010">Department of Microbiology, Immunology and Pathology, Arthropod-borne and Infectious Diseases laboratory, Colorado State University, Fort Collins, USA</nlm:aff>
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<author><name sortKey="Baker, Michelle L" sort="Baker, Michelle L" uniqKey="Baker M" first="Michelle L." last="Baker">Michelle L. Baker</name>
<affiliation><nlm:aff id="aff0015">CSIRO, Health and Biosecurity Business Unit, Australian Animal Health Laboratory, Geelong, Australia</nlm:aff>
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<series><title level="j">Virus Research</title>
<idno type="ISSN">0168-1702</idno>
<idno type="eISSN">1872-7492</idno>
<imprint><date when="2018">2018</date>
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<front><div type="abstract" xml:lang="en"><title>Highlights</title>
<p><list list-type="simple" id="lis0005"><list-item id="lsti0005"><label>•</label>
<p id="par0005">Bats are important reservoir hosts for emerging zoonotic viruses.</p>
</list-item>
<list-item id="lsti0010"><label>•</label>
<p id="par0010">Viruses detected in bats are difficult to isolate using traditional cell lines.</p>
</list-item>
<list-item id="lsti0015"><label>•</label>
<p id="par0015">Bat cell lines provide critical tools to dissect host pathogen interactions.</p>
</list-item>
<list-item id="lsti0020"><label>•</label>
<p id="par0020">Little is known about immune cell populations and their responses in bats.</p>
</list-item>
<list-item id="lsti0025"><label>•</label>
<p id="par0025">Sharing reagents and cell lines will accelerate research and virus discovery.</p>
</list-item>
</list>
</p>
</div>
</front>
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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">Virus Res</journal-id>
<journal-id journal-id-type="iso-abbrev">Virus Res</journal-id>
<journal-title-group><journal-title>Virus Research</journal-title>
</journal-title-group>
<issn pub-type="ppub">0168-1702</issn>
<issn pub-type="epub">1872-7492</issn>
<publisher><publisher-name>Elsevier B.V.</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">29454637</article-id>
<article-id pub-id-type="pmc">7114677</article-id>
<article-id pub-id-type="publisher-id">S0168-1702(17)30820-1</article-id>
<article-id pub-id-type="doi">10.1016/j.virusres.2018.02.013</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Tools to study pathogen-host interactions in bats</article-title>
</title-group>
<contrib-group><contrib contrib-type="author" id="aut0005"><name><surname>Banerjee</surname>
<given-names>Arinjay</given-names>
</name>
<xref rid="aff0005" ref-type="aff">a</xref>
</contrib>
<contrib contrib-type="author" id="aut0010"><name><surname>Misra</surname>
<given-names>Vikram</given-names>
</name>
<xref rid="aff0005" ref-type="aff">a</xref>
</contrib>
<contrib contrib-type="author" id="aut0015"><name><surname>Schountz</surname>
<given-names>Tony</given-names>
</name>
<xref rid="aff0010" ref-type="aff">b</xref>
</contrib>
<contrib contrib-type="author" id="aut0020"><name><surname>Baker</surname>
<given-names>Michelle L.</given-names>
</name>
<email>michelle.baker@csiro.au</email>
<xref rid="aff0015" ref-type="aff">c</xref>
<xref rid="cor0005" ref-type="corresp">⁎</xref>
</contrib>
</contrib-group>
<aff id="aff0005"><label>a</label>
Department of Veterinary Microbiology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Canada</aff>
<aff id="aff0010"><label>b</label>
Department of Microbiology, Immunology and Pathology, Arthropod-borne and Infectious Diseases laboratory, Colorado State University, Fort Collins, USA</aff>
<aff id="aff0015"><label>c</label>
CSIRO, Health and Biosecurity Business Unit, Australian Animal Health Laboratory, Geelong, Australia</aff>
<author-notes><corresp id="cor0005"><label>⁎</label>
Corresponding author. <email>michelle.baker@csiro.au</email>
</corresp>
</author-notes>
<pub-date pub-type="pmc-release"><day>15</day>
<month>2</month>
<year>2018</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="ppub"><day>15</day>
<month>3</month>
<year>2018</year>
</pub-date>
<pub-date pub-type="epub"><day>15</day>
<month>2</month>
<year>2018</year>
</pub-date>
<volume>248</volume>
<fpage>5</fpage>
<lpage>12</lpage>
<history><date date-type="received"><day>29</day>
<month>10</month>
<year>2017</year>
</date>
<date date-type="rev-recd"><day>1</day>
<month>2</month>
<year>2018</year>
</date>
<date date-type="accepted"><day>12</day>
<month>2</month>
<year>2018</year>
</date>
</history>
<permissions><copyright-statement>© 2018 Elsevier B.V. All rights reserved.</copyright-statement>
<copyright-year>2018</copyright-year>
<copyright-holder>Elsevier B.V.</copyright-holder>
<license><license-p>Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.</license-p>
</license>
</permissions>
<abstract abstract-type="author-highlights" id="abs0005"><title>Highlights</title>
<p><list list-type="simple" id="lis0005"><list-item id="lsti0005"><label>•</label>
<p id="par0005">Bats are important reservoir hosts for emerging zoonotic viruses.</p>
</list-item>
<list-item id="lsti0010"><label>•</label>
<p id="par0010">Viruses detected in bats are difficult to isolate using traditional cell lines.</p>
</list-item>
<list-item id="lsti0015"><label>•</label>
<p id="par0015">Bat cell lines provide critical tools to dissect host pathogen interactions.</p>
</list-item>
<list-item id="lsti0020"><label>•</label>
<p id="par0020">Little is known about immune cell populations and their responses in bats.</p>
</list-item>
<list-item id="lsti0025"><label>•</label>
<p id="par0025">Sharing reagents and cell lines will accelerate research and virus discovery.</p>
</list-item>
</list>
</p>
</abstract>
<abstract id="abs0010"><p>Bats are natural reservoirs for a variety of emerging viruses that cause significant disease in humans and domestic animals yet rarely cause clinical disease in bats. The co-evolutionary history of bats with viruses has been hypothesized to have shaped the bat-virus relationship, allowing both to exist in equilibrium. Progress in understanding bat-virus interactions and the isolation of bat-borne viruses has been accelerated in recent years by the development of susceptible bat cell lines. Viral sequences similar to severe acute respiratory syndrome corona virus (SARS-CoV) have been detected in bats, and filoviruses such as Marburg virus have been isolated from bats, providing definitive evidence for the role of bats as the natural host reservoir. Although viruses can be readily detected in bats using molecular approaches, virus isolation is far more challenging. One of the limitations in using traditional culture systems from non-reservoir species is that cell types and culture conditions may not be compatible for isolation of bat-borne viruses. There is, therefore, a need to develop additional bat cell lines that correspond to different cell types, including less represented cell types such as immune cells, and culture them under more physiologically relevant conditions to study virus host interactions and for virus isolation. In this review, we highlight the current progress in understanding bat-virus interactions in bat cell line systems and some of the challenges and limitations associated with cell lines. Future directions to address some of these challenges to better understand host-pathogen interactions in these intriguing mammals are also discussed, not only in relation to viruses but also other pathogens carried by bats including bacteria and fungi.</p>
</abstract>
<kwd-group id="kwd0005"><title>Keywords</title>
<kwd>Bats</kwd>
<kwd>Chiroptera</kwd>
<kwd>Viral reservoirs</kwd>
<kwd>Virus isolation</kwd>
<kwd>Cell lines</kwd>
<kwd>Host-pathogen interaction</kwd>
</kwd-group>
</article-meta>
</front>
<body><sec id="sec0005"><label>1</label>
<title>Introduction</title>
<p id="par0030">Bats are an ancient and diverse group of mammals, comprising almost a quarter of all mammalian diversity and inhabiting all continents, other than Antarctica. Phylogenetic analyses based on molecular data classified bats into the suborders Yinpterochiroptera and Yangochiroptera (<xref rid="bib0410" ref-type="bibr">Teeling et al., 2016</xref>
; <xref rid="bib0405" ref-type="bibr">Teeling et al., 2005</xref>
). The Yinpterochiroptera suborder includes the non echolocating Pteropodidae family and the echolocating Rhinolophoidea family. The Yangochiroptera consist of the remaining echolocating microbat families. The two suborders diverged over 50 million years ago (<xref rid="bib0200" ref-type="bibr">Lei and Dong, 2016</xref>
; <xref rid="bib0305" ref-type="bibr">O'Leary et al., 2013</xref>
; <xref rid="bib0385" ref-type="bibr">Simmons et al., 2008</xref>
). Members of both suborders serve as reservoir or suspected reservoir hosts for a number of zoonotic viruses that are highly pathogenic in humans (<xref rid="bib0060" ref-type="bibr">Calisher et al., 2006</xref>
; <xref rid="bib0270" ref-type="bibr">Moratelli and Calisher, 2015</xref>
), yet cause no clinical disease in bats that are naturally or experimentally infected. The long co-evolutionary history of bats and their viruses has been speculated to have shaped the unique host-pathogen relationship (<xref rid="bib0365" ref-type="bibr">Schountz et al., 2017</xref>
).</p>
<p id="par0035">Although bats have been linked with a number of viruses, identifying wildlife reservoirs can be a challenging process, requiring extensive ecological sampling. Evidence that a pathogen is permanently maintained in a population, often in the absence of disease, is required to confidently identify its reservoir (<xref rid="bib0060" ref-type="bibr">Calisher et al., 2006</xref>
; <xref rid="bib0140" ref-type="bibr">Haydon et al., 2002</xref>
). Detection of fragments of viral genomes, combined with serological evidence for viral exposure in multiple individuals of a species are generally the first lines of evidence to associate a host with a pathogen (<xref rid="bib0120" ref-type="bibr">Halpin et al., 2011</xref>
; <xref rid="bib0215" ref-type="bibr">Li et al., 2005</xref>
; <xref rid="bib0395" ref-type="bibr">Swanepoel et al., 2007</xref>
; <xref rid="bib0445" ref-type="bibr">Young et al., 1996</xref>
). Additional evidence in the form of virus isolation and the ability to link a reservoir to a spillover event is necessary to confirm the association. Examples of bat viruses that are confirmed or speculated to have ‘jumped’ from bats into humans and agricultural animals include coronaviruses (severe acute respiratory syndrome coronavirus [SARS-CoV], porcine epidemic diarrhea [PEDV] virus), filoviruses (ebolaviruses and Marburg virus), and henipaviruses (Nipah and Hendra viruses) [reviewed by (<xref rid="bib0270" ref-type="bibr">Moratelli and Calisher, 2015</xref>
)]. Consistent with the definition of a wildlife reservoir, infection of bats by some of these viruses results in viremia and viral shedding in the absence of clinical disease (<xref rid="bib0120" ref-type="bibr">Halpin et al., 2011</xref>
; <xref rid="bib0375" ref-type="bibr">Schuh et al., 2017</xref>
). The spillover of some of these viruses to other susceptible hosts, including humans, can result in severe disease and mortality due to the lack of therapeutics and vaccines.</p>
<p id="par0040">The emergence of zoonotic diseases is increasing globally and mammals, including bats, are major sources of emerging and re-emerging pathogens (<xref rid="bib0335" ref-type="bibr">Plowright et al., 2015</xref>
). The drivers of disease emergence include anthropogenic changes to the environment (<italic>e.g.</italic>
, agricultural intensification), climate change and the encroachment of human populations into wildlife habitats (<xref rid="bib0400" ref-type="bibr">Tait et al., 2014</xref>
). The biological characterization of a newly identified virus often begins with its isolation in cultured cells. Although detection of virus-specific antibodies by serology and the use of molecular methods, such as viral sequencing, are often readily achievable, virus isolation from bats has been far more challenging. For example, bats are implicated as the reservoirs of ebolaviruses based on the detection of viral genome, serological evidence and their confirmed role as a reservoir for the closely related Marburg virus. However, ebolaviruses have yet to be isolated from bats to definitively link them to spillover events (<xref rid="bib0210" ref-type="bibr">Leroy et al., 2005</xref>
). Identifying wildlife reservoirs and the viruses they host will require the development of better laboratory tools for virus isolation to study replication kinetics and virus-host interactions. In this perspective, we discuss the importance of reservoir species specific cell lines as tools to study emerging wildlife pathogens with a focus on bats.</p>
</sec>
<sec id="sec0010"><label>2</label>
<title>Current status of cell lines derived from bats</title>
<p id="par0045">Virus isolation is generally attempted in established immortalized cell lines, such as the type I interferon deficient BHK-21 (baby Syrian hamster kidney cells) (<xref rid="bib0330" ref-type="bibr">Otsuki et al., 1979</xref>
) or Vero E6 cell lines (African green monkey kidney cells) (<xref rid="bib0110" ref-type="bibr">Govorkova et al., 1996</xref>
). Different primary cells from bats have been studied and some immortalized cell lines have also been generated (<xref rid="tbl0005" ref-type="table">Table 1</xref>
). Established cell lines from non-reservoir host species are convenient tools for virus isolation but do not always support propagation or isolation of viruses from wildlife. For example, a bat herpesvirus isolated from cell lines established from the Schreiber’s long-fingered bat, <italic>Miniopterus schreibersii</italic>
, failed to replicate in cells from a variety of other species, including cells from the black flying fox, <italic>Pteropus alecto</italic>
(<xref rid="bib0450" ref-type="bibr">Zhang et al., 2012</xref>
). The henipavirus Cedar virus was isolated from primary cells of its putative natural reservoir, <italic>P. alecto</italic>
whereas other cell lines showed no visible cytopathic effect (<xref rid="bib0245" ref-type="bibr">Marsh et al., 2012</xref>
). Similarly, the paramyxovirus Menangle virus was isolated using the same <italic>P. alecto</italic>
kidney cell line (<xref rid="bib0040" ref-type="bibr">Barr et al., 2012</xref>
).<table-wrap position="float" id="tbl0005"><label>Table 1</label>
<caption><p>Some cell types established from bats and range of viruses that have been used in studies with these cells.</p>
</caption>
<alt-text id="at0290">Table 1</alt-text>
<table frame="hsides" rules="groups"><thead><tr><th align="left">Bat primary cells or cell lines</th>
<th align="left">Origin</th>
<th align="left">Virus/pseudovirus used in the study</th>
<th align="left">Reference</th>
</tr>
</thead>
<tbody><tr><td align="left"><italic>Artibeus jamaicensis</italic>
primary cells</td>
<td align="left">Embryonic, primary kidney cells</td>
<td align="left">Dengue virus, MERS-CoV</td>
<td align="left"><xref rid="bib0275" ref-type="bibr">Moreira-Soto et al. (2017)</xref>
; <xref rid="bib0285" ref-type="bibr">Munster et al. (2016)</xref>
</td>
</tr>
<tr><td align="left"><italic>Carollia perspicillata.</italic>
</td>
<td align="left">Trachea</td>
<td align="left">Vesicular stomatitis virus (VSV) and Rift-Valley fever virus</td>
<td align="left"><xref rid="bib0100" ref-type="bibr">Eckerle et al. (2014)</xref>
</td>
</tr>
<tr><td align="left"><italic>Carollia perspicillata</italic>
– CpKd</td>
<td align="left">Kidney</td>
<td align="left">Bat-associated influenza viruses</td>
<td align="left"><xref rid="bib0160" ref-type="bibr">Hoffmann et al. (2016)</xref>
</td>
</tr>
<tr><td align="left"><italic>Eidolon helvum</italic>
</td>
<td align="left">Trachea</td>
<td align="left">VSV and Rift-Valley fever virus</td>
<td align="left"><xref rid="bib0100" ref-type="bibr">Eckerle et al. (2014)</xref>
</td>
</tr>
<tr><td align="left"><italic>Eidolon helvum</italic>
– EidNi/41</td>
<td align="left">Kidney</td>
<td align="left">Bat-associated influenza viruses, Ebolavirus, MERS-CoV, Influenza A virus, O'nyong–nyong virus</td>
<td align="left"><xref rid="bib0160" ref-type="bibr">Hoffmann et al. (2016)</xref>
, <xref rid="bib0300" ref-type="bibr">Ng et al. (2015)</xref>
; <xref rid="bib0055" ref-type="bibr">Cai et al. (2014)</xref>
; <xref rid="bib0340" ref-type="bibr">Poole et al. (2014)</xref>
; <xref rid="bib0045" ref-type="bibr">Biesold et al. (2011)</xref>
</td>
</tr>
<tr><td align="left"><italic>Epomops buettikoferi</italic>
– EpoNi/22.1</td>
<td align="left">Kidney</td>
<td align="left">Bat-associated influenza viruses, Influenza A virus</td>
<td align="left"><xref rid="bib0160" ref-type="bibr">Hoffmann et al. (2016)</xref>
; <xref rid="bib0340" ref-type="bibr">Poole et al. (2014)</xref>
</td>
</tr>
<tr><td align="left"><italic>Eptesicus fuscus –</italic>
Efk3</td>
<td align="left">kidney</td>
<td align="left">VSV, porcine epidemic diarrhea virus, herpes simplex virus and MERS-CoV</td>
<td align="left"><xref rid="bib0025" ref-type="bibr">Banerjee et al. (2016)</xref>
</td>
</tr>
<tr><td align="left"><italic>Hypsignathus monstrosus –</italic>
hypLu/45.1</td>
<td align="left">Lung</td>
<td align="left">MERS-CoV, Influenza A virus</td>
<td align="left"><xref rid="bib0055" ref-type="bibr">Cai et al. (2014)</xref>
; <xref rid="bib0340" ref-type="bibr">Poole et al. (2014)</xref>
</td>
</tr>
<tr><td align="left"><italic>Hypsignathus monstrosus</italic>
– hypNi/1.1</td>
<td align="left">Kidney</td>
<td align="left">Bat-associated influenza viruses, MERS-CoV, Influenza A virus, African Henipavirus</td>
<td align="left"><xref rid="bib0160" ref-type="bibr">Hoffmann et al. (2016)</xref>
; <xref rid="bib0055" ref-type="bibr">Cai et al. (2014)</xref>
; <xref rid="bib0340" ref-type="bibr">Poole et al. (2014)</xref>
;. <xref rid="bib0190" ref-type="bibr">Kruger et al., (2013)</xref>
</td>
</tr>
<tr><td align="left"><italic>Miniopterus schreibersii</italic>
primary cells</td>
<td align="left">Lymph node (MsLn), Kidney (MsKi)</td>
<td align="left">Miniopterus schreibersii herpesvirus (MsHV)</td>
<td align="left"><xref rid="bib0450" ref-type="bibr">Zhang et al. (2012)</xref>
</td>
</tr>
<tr><td align="left"><italic>Myotis daubentonii –</italic>
MyDauLu/47.1</td>
<td align="left">Lung</td>
<td align="left">Influenza A virus</td>
<td align="left"><xref rid="bib0340" ref-type="bibr">Poole et al. (2014)</xref>
</td>
</tr>
<tr><td align="left"><italic>Myotis davidii</italic>
– MdKi</td>
<td align="left">Kidney</td>
<td align="left">Sendai virus</td>
<td align="left"><xref rid="bib0230" ref-type="bibr">Liang et al. (2015)</xref>
</td>
</tr>
<tr><td align="left"><italic>Myotis myotis</italic>
</td>
<td align="left">brain (MmBr), tonsil (MmTo), peritoneal cavity (MmPca), nasal epithelium (MmNep) and nervus olfactorius (MmNol)</td>
<td align="left">Rabies virus, European bat lyssavirus (EBLV – 1 and 2)</td>
<td align="left"><xref rid="bib0150" ref-type="bibr">He et al. (2014)</xref>
</td>
</tr>
<tr><td align="left"><italic>Myotis velifer incautus</italic>
(MVI-it) – CRL-6012</td>
<td align="left">intercapsular tumor</td>
<td align="left">Novel bat gammaherpesvirus</td>
<td align="left"><xref rid="bib0380" ref-type="bibr">Shabman et al. (2016)</xref>
; <xref rid="bib0165" ref-type="bibr">Host and Damania (2016)</xref>
</td>
</tr>
<tr><td align="left"><italic>Pipistrellus ceylonicus</italic>
</td>
<td align="left">Embryonic</td>
<td align="left">Chandipura virus (CHPV), novel adenovirus (BtAdv-RLM)</td>
<td align="left"><xref rid="bib0280" ref-type="bibr">Mourya et al. (2013)</xref>
</td>
</tr>
<tr><td align="left"><italic>Pipistrellus subflavus</italic>
– ESU-BSL</td>
<td align="left">Lung</td>
<td align="left">MERS-CoV</td>
<td align="left"><xref rid="bib0055" ref-type="bibr">Cai et al. (2014)</xref>
</td>
</tr>
<tr><td align="left"><italic>Pteropus alecto</italic>
</td>
<td align="left">Aorta, bone marrow, brain, foetus, foetal membranes, heart, kidney, liver, lymph nodes, lung, muscle, pharynx, placenta, salivary gland, small intestine, skin, spleen, testes, thymus, uterus</td>
<td align="left">Hendra virus, Pulau virus, Sendai virus, Nipah virus, Hendra virus</td>
<td align="left"><xref rid="bib0465" ref-type="bibr">Zhou et al. (2013)</xref>
; <xref rid="bib0075" ref-type="bibr">Crameri et al. (2009)</xref>
; <xref rid="bib0415" ref-type="bibr">Virtue et al. (2011)</xref>
</td>
</tr>
<tr><td align="left"><italic>Pteropus alecto</italic>
</td>
<td align="left">Kidney</td>
<td align="left">Influenza A virus, Sendai virus, Pteropine orthoreovirus NB, Nipah virus, Hendra virus</td>
<td align="left"><xref rid="bib0090" ref-type="bibr">Dlugolenski et al. (2013)</xref>
; <xref rid="bib0465" ref-type="bibr">Zhou et al. (2013)</xref>
; <xref rid="bib0415" ref-type="bibr">Virtue et al. (2011)</xref>
</td>
</tr>
<tr><td align="left"><italic>Pteropus alecto</italic>
</td>
<td align="left">Embryonic</td>
<td align="left">Nipah virus, Hendra virus</td>
<td align="left"><xref rid="bib0415" ref-type="bibr">Virtue et al. (2011)</xref>
</td>
</tr>
<tr><td align="left"><italic>Rhinolophus affinis</italic>
</td>
<td align="left">embryonic</td>
<td align="left">VSV</td>
<td align="left"><xref rid="bib0220" ref-type="bibr">Li et al., (2015)</xref>
</td>
</tr>
<tr><td align="left"><italic>Rhinolophus sinicus</italic>
</td>
<td align="left">splenocytes</td>
<td align="left">VSV</td>
<td align="left"><xref rid="bib0220" ref-type="bibr">Li et al., (2015)</xref>
</td>
</tr>
<tr><td align="left"><italic>Rousettus aegyptiacus –</italic>
RO6E, RO5T</td>
<td align="left">Kidney</td>
<td align="left">MERS-CoV, Influenza A virus, Ebola virus, Marburg virus</td>
<td align="left"><xref rid="bib0055" ref-type="bibr">Cai et al. (2014)</xref>
; <xref rid="bib0340" ref-type="bibr">Poole et al. (2014)</xref>
;. <xref rid="bib0185" ref-type="bibr">Krahling et al. (2010)</xref>
</td>
</tr>
<tr><td align="left"><italic>Rousettus aegyptiacus</italic>
– RoNi/7.1</td>
<td align="left">Kidney</td>
<td align="left">Bat-associated influenza viruses, MERS-CoV, Influenza A virus</td>
<td align="left"><xref rid="bib0160" ref-type="bibr">Hoffmann et al. (2016)</xref>
; <xref rid="bib0055" ref-type="bibr">Cai et al. (2014)</xref>
; <xref rid="bib0340" ref-type="bibr">Poole et al. (2014)</xref>
</td>
</tr>
<tr><td align="left"><italic>Tadaria brasiliensis</italic>
– Tb1Lu</td>
<td align="left">Lung</td>
<td align="left">Bovine leukemia virus, Influenza A virus, mammalian reovirus serotype 3 Dearing</td>
<td align="left"><xref rid="bib0115" ref-type="bibr">Graves and Ferrer (1976)</xref>
; <xref rid="bib0340" ref-type="bibr">Poole et al. (2014)</xref>
;. <xref rid="bib0355" ref-type="bibr">Sandekian et al. (2013)</xref>
</td>
</tr>
<tr><td align="left"><italic>Rousettus aegyptiacus</italic>
immortalized cells</td>
<td align="left">Foetus</td>
<td align="left">Vaccinia Ankara</td>
<td align="left"><xref rid="bib0170" ref-type="bibr">Jordan et al. (2009)</xref>
</td>
</tr>
</tbody>
</table>
</table-wrap>
</p>
<p id="par0050">Cell lines have defined characteristics based on their tissue of origin and method of immortalization. For a cell to be suitable for virus propagation, it must bear an appropriate receptor to bind with an incoming virus and it must be permissive. Because viruses differ in their cellular tropisms, working with a few cell lines with epithelial or fibroblastic characteristics limits our ability to isolate or study viruses that may have a tropism towards cell types that are more difficult to immortalize. Current cell lines may lack receptors required by viruses to replicate when cells are infected at low multiplicity of infections. For example, bat cells from various species were resistant to infection with vesicular stomatitis virus (VSV) pseudotypes bearing the SARS-CoV spike protein until the cells were transfected to express the human SARS-CoV receptor, angiotensin-converting enzyme 2 (ACE2) (<xref rid="bib0155" ref-type="bibr">Hoffmann et al., 2013</xref>
). Although the lack of appropriate receptors on cell lines makes it difficult to isolate some viruses, this lack of susceptibility to infection can also help us understand the early events in virus infection. For instance, differences in the susceptibility of cells from a variety of bats to filoviruses also led to the identification of unique amino acid substitutions in the filovirus receptor, Neimann-Pick type C1 (NPC1), providing insight into the host range of ebolaviruses (<xref rid="bib0300" ref-type="bibr">Ng et al., 2015</xref>
). Similarly, Widagdo et al. have shown that dipeptidyl peptidase 4 (DPP4, CD26), a cellular receptor for MERS-CoV, is expressed in specific cell types in different tissues which also varies between bat species (<xref rid="bib0430" ref-type="bibr">Widagdo et al., 2017</xref>
). These studies demonstrate the need to develop cell lines from different organs and bat species and clone them for a variety of cell types as viral receptors may not be equally distributed.</p>
</sec>
<sec id="sec0015"><label>3</label>
<title>Considerations for development of cell lines</title>
<p id="par0055">Chiroptera consists of over 1200 bat species and different species may have co-evolved with different viruses. Viruses detected in one species, may not infect cells established from a different bat species. Thus, the choice of bat species for generating cell lines capable of supporting a particular virus should be supported by evidence that the species is susceptible to that virus. For example, SARS-CoV-like coronaviruses have been detected in <italic>Rhinolophus sinicus</italic>
(<xref rid="bib0195" ref-type="bibr">Lau et al., 2005</xref>
), and this species is the logical candidate for generating cell lines that can support replication and isolation of these viruses.</p>
<p id="par0060">Because propagation of viruses in cell lines can select for members of the virus population that replicate most efficiently in the chosen cell type, the choice of cell line should be taken into consideration. Propagation of viruses in cell lines other than those of the natural host may lead to accumulation of adaptive mutations or attenuate the virus (<xref rid="bib0070" ref-type="bibr">Combe and Sanjuan, 2014</xref>
), which in turn has implications for assessing host-pathogen interactions either <italic>in vivo</italic>
or <italic>in vitro</italic>
. For example, although wild type Marburg virus causes no disease in mice, it can be adapted to mice by serial passage to cause lethal disease (<xref rid="bib0350" ref-type="bibr">Qiu et al., 2014</xref>
). Deep sequencing of Marburg virus after adaptation to mice and following propagation in Vero E6 cells has revealed the sequential mutations associated with each passage as the virus adapts to a new host either <italic>in vivo</italic>
or <italic>in vitro</italic>
(<xref rid="bib0425" ref-type="bibr">Wei et al., 2017</xref>
). This is also thought to have occurred with Tacaribe virus, which was isolated from artibeus bats and passaged 20 times in newborn mice, resulting in point mutations and deletions (<xref rid="bib0240" ref-type="bibr">Malmlov et al., 2017</xref>
; <xref rid="bib0360" ref-type="bibr">Sayler et al., 2014</xref>
).</p>
<p id="par0065">Bats experience a range of body temperatures during different physiological activities (from 4 to 8 °C during hibernation to 41 °C during flight) (<xref rid="bib0310" ref-type="bibr">O'Shea et al., 2014</xref>
). Thus, viruses isolated from bats should be studied at different relevant physiological temperatures. Propagation of viruses at temperatures other than the nominal of the reservoir species may also lead to the generation of attenuation mutants; a strategy that has been used for vaccine development for decades. There is evidence that arthropod viruses found in mosquitoes and ticks accumulate mutations when grown at different temperatures (<xref rid="bib0205" ref-type="bibr">Lemm et al., 1990</xref>
). Thus, propagation of viruses in susceptible cell lines [reviewed by (<xref rid="bib0130" ref-type="bibr">Hare et al., 2016</xref>
)] and at optimized temperatures may minimize mutations and produce viruses similar to wild type virus found in wildlife reservoirs or arthropod vectors [reviewed by (<xref rid="bib0345" ref-type="bibr">Prescott et al., 2017</xref>
)].</p>
<p id="par0070">Controlling for temperature to match temperatures experienced by bats during hibernation is a challenge because <italic>in vitro</italic>
cell culture systems are not viable at low temperatures. Although Miller et al. were able to grow bat cells at temperatures ranging from 37 to 41 °C (<xref rid="bib0260" ref-type="bibr">Miller et al., 2016</xref>
), our attempts to cultivate big brown bat cells (Efk3) at lower temperatures of 26–30 °C were not successful (Banerjee and Misra, unpublished). There is evidence that experimental infection of different reptiles and amphibians with chikungunya virus produce varying amounts of viremia depending on the host’s body temperature (<xref rid="bib0135" ref-type="bibr">Hartwig et al., 2015</xref>
). There is a need to develop a system to test the replication potential of bat-borne viruses at lower temperatures such as those experienced by bats during torpor and hibernation, rather than only propagating them in cells cultured at 37 °C.</p>
<p id="par0075">The virus stock that is used to experimentally infect bats is usually generated by propagation in cells of non-bat origin, such as Vero E6 cells. It is unknown whether propagation of a virus in a monkey cell line alters the genotype of the virus. We have previously infected bats with a virus isolated from bat urine and subsequently propagated in bat cells (Baker et al., unpublished). A problem with propagating this virus in bat cells was achieving high virus titre to perform experimental infection studies in bats, perhaps because bat cells appear to have constitutive type I IFN activation (<xref rid="bib0475" ref-type="bibr">Zhou et al., 2016b</xref>
). It may be necessary to develop interferon-deficient bat cell lines to propagate bat viruses. Recently, Zhang et al. knocked out an antiviral cell signaling receptor, interferon alpha receptor 2 (IFNAR2) in bat cells using CRISPR/Cas9 technology (<xref rid="bib0455" ref-type="bibr">Zhang et al., 2017</xref>
). Similarly, this technology can be used to generate interferon-deficient bat cells in culture.</p>
<p id="par0080">There are several challenges to establishing primary cells from wildlife species. These challenges range from obtaining healthy tissues to determining the ideal cell types. Primary cells maintain genetic integrity and are therefore most appropriate for the study of natural infection of cells. However, primary cells have finite numbers of cell division before undergoing senescence, thus, it can become problematic for long-term studies. Immortalized cells frequently accumulate chromosomal aberrations over time; therefore, caution must be exercised when maintaining cell stocks. Nonetheless, they are convenient and often receptive to genetic manipulations, including transfection of plasmids and targeted changes (<italic>e.g.</italic>
, CRISPR), and often the only cells available that are capable of supporting replication. Thus, the ability to conduct experiments in primary or immortalized cells has advantages and disadvantages.</p>
<p id="par0085">Primary cells can also harbor latent viruses that can become reactivated during <italic>in vitro</italic>
cultivation when the cells are outside the host and isolated from other components of the immune system that would otherwise control virus replication. Most mammals, including bats harbor persistent viruses [reviewed by (<xref rid="bib0060" ref-type="bibr">Calisher et al., 2006</xref>
)], and viruses have been isolated or identified by next generation sequencing (NGS) from bat cell lines (<xref rid="bib0380" ref-type="bibr">Shabman et al., 2016</xref>
). Cell lines from any species of bat should therefore only be handled under controlled biosafety conditions and thoroughly tested before being used for experimental studies. This is also a limitation when working with wild-caught bats.</p>
</sec>
<sec id="sec0020"><label>4</label>
<title>Using cell lines to assess the immune response in bats to viral infections</title>
<p id="par0090">Research in the field of bat immunology steadily increased after bats were implicated as ancestral reservoirs of the coronavirus that caused the SARS outbreak in 2003 (<xref rid="bib0020" ref-type="bibr">Baker et al., 2013</xref>
; <xref rid="bib0195" ref-type="bibr">Lau et al., 2005</xref>
; <xref rid="bib0215" ref-type="bibr">Li et al., 2005</xref>
). Over 200 viruses have been identified in bats and additional new viruses are discovered on a regular basis (<xref rid="bib0270" ref-type="bibr">Moratelli and Calisher, 2015</xref>
; <xref rid="bib0370" ref-type="bibr">Schountz, 2014</xref>
). Few viruses have been documented to cause disease in bats in addition to rabies and related lyssaviruses (<xref rid="bib0080" ref-type="bibr">Davis et al., 2012</xref>
; <xref rid="bib0085" ref-type="bibr">Davis et al., 2013</xref>
; <xref rid="bib0255" ref-type="bibr">McColl et al., 2002</xref>
). Experimental inoculation of Jamaican fruit bats with high doses of Tacaribe virus caused significant morbidity and mortality similar to natural infection of artibeus bats (<xref rid="bib0095" ref-type="bibr">Downs et al., 1963</xref>
). However, the inoculated bats did not transmit the virus. Based on their observations, Cogswell-Hawkinson et al. speculate that Jamaican fruit bats may not be a reservoir host for Tacaribe virus (<xref rid="bib0065" ref-type="bibr">Cogswell-Hawkinson et al., 2012</xref>
). Lloviu virus, a filovirus was isolated from dead bats in Spain (<xref rid="bib0290" ref-type="bibr">Negredo et al., 2011</xref>
). These examples appear to be exceptions to the usual resistance to viral disease displayed by most bats. Bats have been hypothesized to have evolved unique aspects of their immune systems, such as a strict control of the inflammatory process (<xref rid="bib0030" ref-type="bibr">Banerjee et al., 2017</xref>
) and constitutive expression of antiviral interferons (<xref rid="bib0475" ref-type="bibr">Zhou et al., 2016b</xref>
) to better survive infections with these viruses. Testing this hypothesis has been possible, in part through the establishment of well characterized cell lines (<xref rid="bib0365" ref-type="bibr">Schountz et al., 2017</xref>
).</p>
<p id="par0095">Cell lines from several bat species including members of both the Yinpterochiroptera (<italic>Pteropus alecto, Eidolon helvum</italic>
and <italic>Rousettus aegyptiacus)</italic>
and Yangochiroptera (<italic>Eptesicus fuscus,</italic>
and <italic>Myotis myotis)</italic>
suborders, have been established (<xref rid="bib0025" ref-type="bibr">Banerjee et al., 2016</xref>
; <xref rid="bib0045" ref-type="bibr">Biesold et al., 2011</xref>
; <xref rid="bib0075" ref-type="bibr">Crameri et al., 2009</xref>
; <xref rid="bib0150" ref-type="bibr">He et al., 2014</xref>
; <xref rid="bib0175" ref-type="bibr">Jordan et al., 2012</xref>
) (<xref rid="tbl0005" ref-type="table">Table 1</xref>
). These cell lines have been used to cultivate viruses that are speculated or confirmed to have spilled over from bats. These cell lines have also allowed researchers to study the innate immune responses to viruses. Cytokines produced in response to activation of selected innate immune response pathways in bat cells have led to a better understanding of how bats might respond to viral infections in the wild. Bat cells can respond to viruses or viral antigens through the production of antiviral interferons and interferon stimulated genes (<xref rid="bib0045" ref-type="bibr">Biesold et al., 2011</xref>
; <xref rid="bib0325" ref-type="bibr">Omatsu et al., 2008</xref>
; <xref rid="bib0460" ref-type="bibr">Zhou et al., 2011</xref>
; <xref rid="bib0465" ref-type="bibr">Zhou et al., 2013</xref>
). The use of bat cell lines has also led to the discovery of viral proteins that counteract the innate immune response in these cells (<xref rid="bib0415" ref-type="bibr">Virtue et al., 2011</xref>
). Less work has been performed on the adaptive immune responses of bats using cell lines, in part due to the lack of research on bat T and B cells. However, a recent report used <italic>P. alecto</italic>
cell lines to examine the repertoire of self and Hendra virus epitopes presented by MHC class I molecules (<xref rid="bib0435" ref-type="bibr">Wynne et al., 2016</xref>
). More research is needed to establish <italic>in vitro</italic>
and <italic>ex vivo</italic>
cultures of immune cells from representative bat species.</p>
</sec>
<sec id="sec0025"><label>5</label>
<title>Developing bat specific reagents</title>
<p id="par0100">Establishing cell lines from different species of bats provides the opportunity to perform comparative studies between bat species and with other mammals. Several cell lines have been developed from bats, including some that support the replication of viruses from different families (<xref rid="tbl0005" ref-type="table">Table 1</xref>
). However, to better characterize bat immune responses, we need to develop cell lines or a system where we can continuously establish immune cells <italic>in vitro</italic>
. Current wildlife cell lines are composed primarily of epithelial or fibroblast cell types, which limit the responses generated following infection. These cells may lack many of the receptors and cytokine responses of specialized immune cells. Isolating and developing representative immune cell lines will allow the study of both adaptive and innate immune responses of bats. This also involves developing species and cell-type specific reagents that will allow characterization and culture of immune cells <italic>in vitro</italic>
. Recently, immune cells from black flying foxes have been functionally and phenotypically characterized (<xref rid="bib0250" ref-type="bibr">Martinez Gomez et al., 2016</xref>
), along with the establishment of bone-marrow derived dendritic cells and macrophages using black flying fox reagents developed in the laboratory (<xref rid="bib0470" ref-type="bibr">Zhou et al., 2016a</xref>
). Systems such as these will further allow exploration of the adaptive immune response in potential reservoir bat species. More efforts are required to generate similar cell types in other bat species. Sharing of resources will play a key role in expanding our understanding of the unique immune response in bats.</p>
<p id="par0105">Although primary cells are good tools to attempt virus isolation, they have a limited life-span. There are several technologies that can be used to immortalize these primary cells. Immortalized cell lines replicate indefinitely in culture and provide researchers with valuable tools to study viruses and cell-virus interactions. Some of these bat cell lines have been established using existing technology such as simian virus 40 large T-antigen and human hTERT expression systems (<xref rid="bib0005" ref-type="bibr">Ali and DeCaprio, 2001</xref>
; <xref rid="bib0145" ref-type="bibr">He et al., 2009</xref>
; <xref rid="bib0440" ref-type="bibr">Xie et al., 2015</xref>
), whereas others have been generated by using novel technologies such as a bat polyomavirus large T-antigen to immortalize cells (<xref rid="bib0025" ref-type="bibr">Banerjee et al., 2016</xref>
) and other bat specific reagents to generate dendritic cells and macrophages (<xref rid="bib0470" ref-type="bibr">Zhou et al., 2016a</xref>
). Polyomavirus large T-antigen binds to and attenuates the tumor suppressor protein p53 and proteins of the retinoblastoma tumor suppressor family (pRb, p130 and p107) promoting cell cycle progression. Gamma-herpesviruses have also been used to immortalize cells of the immune system, such as B lymphocytes (<xref rid="bib0225" ref-type="bibr">Liang et al., 2011</xref>
). These novel technologies or combination of cell immortalization techniques can be modified for the generation of cell lines from representative cell and tissue types from less studied species of bats and other neglected wildlife reservoirs.</p>
<p id="par0110">Studying the host-pathogen relationship in wildlife species is often challenging, with <italic>in vivo</italic>
experiments difficult and costly to perform. Developing cell lines will allow preliminary research, which can later be validated <italic>in vivo</italic>
in bats. These cell lines can be used to study or isolate viruses that spillover from animal reservoirs to humans, and pathogens that cause disease in wildlife. The advantages of developing cell lines do not end at studying the immune responses and isolating viruses. These cell lines can be used to propagate isolated viruses to high titre for the development of diagnostic kits and potential vaccines. Studying pathogen-host interactions may also allow us to identify biomarkers associated with viral infection that could be used to predict and prevent spillover to other susceptible hosts. For example, biochemical or hormonal changes linked to increases in viral replication in wild bat populations may be used to predict periods of increased risk of spillover to other susceptible species.</p>
</sec>
<sec id="sec0030"><label>6</label>
<title>Using cell lines to study host responses to pathogens that cause disease in bats</title>
<p id="par0115">In addition to viruses, bats may also be reservoirs, or even dead-end hosts, for other pathogens such as bacteria (<xref rid="bib0035" ref-type="bibr">Banskar et al., 2016</xref>
), fungi or parasites. Bats do not seem to be refractory to disease when it comes to extracellular pathogens such as fungi (<xref rid="bib0480" ref-type="bibr">Zukal et al., 2014</xref>
). The white-nose syndrome (WNS) fungus, <italic>Pseudogymnoascus destructans</italic>
, causes significant wing damage at the sites of infection in little brown bats (<italic>Myotis lucifugus</italic>
) (<xref rid="bib0420" ref-type="bibr">Warnecke et al., 2012</xref>
; <xref rid="bib0480" ref-type="bibr">Zukal et al., 2014</xref>
). Big brown bats (<italic>Eptesicus fuscus</italic>
) seem to be relatively resistant to the fungus (<xref rid="bib0105" ref-type="bibr">Frank et al., 2014</xref>
). Identifying, isolating and characterizing the interaction of extracellular and intracellular pathogens with their host can be better facilitated by the availability of bat species specific cell lines.</p>
<p id="par0120">Research to understand bacterial and fungal infections in bats is growing and has led to the identification of potential pathogenic bacterial species in bats (<xref rid="bib0015" ref-type="bibr">Avena et al., 2016</xref>
; <xref rid="bib0035" ref-type="bibr">Banskar et al., 2016</xref>
). Cell lines, as previously shown (<xref rid="bib0295" ref-type="bibr">Nepelska et al., 2017</xref>
), can be effective tools to dissect the role of these organisms in the overall health of bats. Transcriptomic data from bat cells infected with various pathogens, including bacteria and viruses, will shed light on global pathways that are activated or suppressed in response to these pathogens. These data can be used to develop hypotheses on the overall impact these pathogens might have on bats at an organism level. Recently, a novel <italic>Streptomyces</italic>
species with anti-fungal activity was identified in bats (<xref rid="bib0125" ref-type="bibr">Hamm et al., 2017</xref>
). WNS has caused the death of millions of little brown bats in North America (<xref rid="bib0010" ref-type="bibr">Alves et al., 2014</xref>
; <xref rid="bib0180" ref-type="bibr">Knudsen et al., 2013</xref>
; <xref rid="bib0480" ref-type="bibr">Zukal et al., 2014</xref>
) and this new compound amongst others (<xref rid="bib0050" ref-type="bibr">Boire et al., 2016</xref>
) might help to curb the spread of WNS. Potential toxic effects of this drug can be tested in uninfected bat cell lines before testing them in live bats or other relevant animal models.</p>
</sec>
<sec id="sec0035"><label>7</label>
<title>Developing <italic>in vivo</italic>
bat models</title>
<p id="par0125">In addition to cell lines, there is a need for laboratory bred bats with known and tested infection status for <italic>ex vivo</italic>
and <italic>in vivo</italic>
experiments. Establishing a wild-caught bat colony is challenging but achievable with sufficient resources to house and maintain the bats. Although studies using wild-caught outbred bats potentially provide the best representation of what occurs naturally during virus infection, it can be difficult to obtain reproducible data using wild caught animals due to their high genetic diversity. The current infection status and history of viral infections in wild caught bats is also difficult to determine which in turn may affect the outcome and interpretation of experimental infections. There is therefore a need to establish inbred laboratory colonies of bats of known infection status. As much of the knowledge that has been obtained regarding the host responses of bats has been gained from studies using bat cell lines, experimental infections of captive bats provide an opportunity to test whether observations made <italic>in vitro</italic>
also apply <italic>in vivo</italic>
. Studies in captive animals are also necessary to confirm the role of bats as ‘reservoirs’ by carrying out long-term experiments to detect virus shedding and the lack of associated pathology in bats with known infection status (i.e. laboratory bred bats). This was recently attempted with Egyptian rousette bats that were infected with Marburg virus. The bats shed virus between 5 and 19 days post infection (<xref rid="bib0375" ref-type="bibr">Schuh et al., 2017</xref>
), but longer term studies might be necessary to further establish bats as reservoirs. Thus there is a need to develop more reliable animal models with known infection status.</p>
</sec>
<sec id="sec0040"><label>8</label>
<title>Conclusion</title>
<p id="par0130">Although several different cell lines have been established from different species of bats (<xref rid="tbl0005" ref-type="table">Table 1</xref>
), we are still faced with the challenge of isolating several viruses that have been detected in bats. We have detected little brown bat coronavirus sequences (<xref rid="bib0265" ref-type="bibr">Misra et al., 2009</xref>
; <xref rid="bib0390" ref-type="bibr">Subudhi et al., 2017</xref>
) and others have detected ebolavirus sequences [reviewed by (<xref rid="bib0315" ref-type="bibr">Olival and Hayman, 2014</xref>
)] in bats by polymerase chain reaction (PCR), next generation sequencing (NGS) and serology. As discussed, virus isolation is more challenging than nucleic acid detection but with the availability of additional cell lines from various organs and species and technologies such as CRISPR to develop cell lines deficient in components of the immune system, attempts to isolate and propagate viruses <italic>in vitro</italic>
should be more successful.</p>
<p id="par0135">Chiroptera consists of over 1200 species and much remains unknown about their relationship with their microorganisms. Bats are genetically diverse and results from studies done in one bat species may not represent other species of bats. Thus, there is a need to study other species of bats to gain deeper insights into bat-microbe co-evolution, bat immune system and ecological interactions of bats. Bats host more zoonotic viruses per mammalian species (<xref rid="bib0235" ref-type="bibr">Luis et al., 2013</xref>
; <xref rid="bib0320" ref-type="bibr">Olival et al., 2017</xref>
), even more than rodents, the largest group of mammals. Collaboration between laboratories will be required to develop cell lines from different bat tissues, bat specific reagents and to establish laboratory bat colonies to explore the length and breadth of microbe-host interactions in these ecologically important mammals (<xref rid="fig0005" ref-type="fig">Fig. 1</xref>
).<fig id="fig0005"><label>Fig. 1</label>
<caption><p>There is a need to develop more model cell lines and animal models to decipher the immune responses of bats to viruses. Viruses display tropism towards different cell types and there is a need to generate cell lines representative of the multitude of cell types found in bats to increase the chances of isolating the viruses that they carry. Alternatively, genetically modified cell lines can be generated that do not express antiviral interferons from these cell types for virus isolation. These cells may be used to propagate bat-borne viruses to high titres for <italic>ex vivo, in vitro</italic>
and <italic>in vivo</italic>
experiments. Generating cell lines from a variety of different tissues and bats will allow researchers to explore virus susceptibility and virus-host interactions in these intriguing mammals. Generation of outbred (wild-caught) and inbred (laboratory bred) bat colonies with known infection status will enable systemic immune response studies with relevant viruses isolated from bats. The ability to resist infections with some of these viruses may be an effect of several evolutionary adaptations, which can be better dissected by studying the systemic responses in bats.</p>
</caption>
<alt-text id="at0285">Fig. 1</alt-text>
<graphic xlink:href="gr1_lrg"></graphic>
</fig>
</p>
</sec>
<sec id="sec0045"><title>Conflicts of interest</title>
<p id="par0140">None.</p>
</sec>
</body>
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<ack id="ack0005"><title>Acknowledgements</title>
<p>AB is funded through a <funding-source id="gs0005">Saskatchewan Innovation</funding-source>
and <funding-source id="gs0010">Opportunity scholarship</funding-source>
and the <funding-source id="gs0015">Department of Veterinary Microbiology at the University of Saskatchewan, Canada</funding-source>
. VM is funded through a Discovery Grant awarded by the <funding-source id="gs0020">Natural Sciences and Engineering Research Council of Canada</funding-source>
(NSERC).</p>
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</pmc>
</record>
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