Distinct Subcellular Compartments of Dendritic Cells Used for Cross-Presentation
Identifieur interne : 000B94 ( Ncbi/Merge ); précédent : 000B93; suivant : 000B95Distinct Subcellular Compartments of Dendritic Cells Used for Cross-Presentation
Auteurs : Jun Imai ; Mayu Otani ; Takahiro SakaiSource :
- International Journal of Molecular Sciences [ 1422-0067 ] ; 2019.
Abstract
Dendritic cells (DCs) present exogenous protein-derived peptides on major histocompatibility complex class I molecules to prime naïve CD8+ T cells. This DC specific ability, called cross-presentation (CP), is important for the activation of cell-mediated immunity and the induction of self-tolerance. Recent research revealed that endoplasmic reticulum-associated degradation (ERAD), which was first identified as a part of the unfolded protein response—a quality control system in the ER—plays a pivotal role in the processing of exogenous proteins in CP. Moreover, DCs express a variety of immuno-modulatory molecules and cytokines to regulate T cell activation in response to the environment. Although both CP and immuno-modulation are indispensable, contrasting ER conditions are required for their correct activity. Since ERAD substrates are unfolded proteins, their accumulation may result in ER stress, impaired cell homeostasis, and eventually apoptosis. In contrast, activation of the unfolded protein response should be inhibited for DCs to express immuno-modulatory molecules and cytokines. Here, we review recent advances on antigen CP, focusing on intracellular transport routes for exogenous antigens and distinctive subcellular compartments involved in ERAD.
Url:
DOI: 10.3390/ijms20225606
PubMed: 31717517
PubMed Central: 6888166
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<author><name sortKey="Sakai, Takahiro" sort="Sakai, Takahiro" uniqKey="Sakai T" first="Takahiro" last="Sakai">Takahiro Sakai</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Distinct Subcellular Compartments of Dendritic Cells Used for Cross-Presentation</title>
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<front><div type="abstract" xml:lang="en"><p>Dendritic cells (DCs) present exogenous protein-derived peptides on major histocompatibility complex class I molecules to prime naïve CD8<sup>+</sup>
T cells. This DC specific ability, called cross-presentation (CP), is important for the activation of cell-mediated immunity and the induction of self-tolerance. Recent research revealed that endoplasmic reticulum-associated degradation (ERAD), which was first identified as a part of the unfolded protein response—a quality control system in the ER—plays a pivotal role in the processing of exogenous proteins in CP. Moreover, DCs express a variety of immuno-modulatory molecules and cytokines to regulate T cell activation in response to the environment. Although both CP and immuno-modulation are indispensable, contrasting ER conditions are required for their correct activity. Since ERAD substrates are unfolded proteins, their accumulation may result in ER stress, impaired cell homeostasis, and eventually apoptosis. In contrast, activation of the unfolded protein response should be inhibited for DCs to express immuno-modulatory molecules and cytokines. Here, we review recent advances on antigen CP, focusing on intracellular transport routes for exogenous antigens and distinctive subcellular compartments involved in ERAD.</p>
</div>
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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">Int J Mol Sci</journal-id>
<journal-id journal-id-type="iso-abbrev">Int J Mol Sci</journal-id>
<journal-id journal-id-type="publisher-id">ijms</journal-id>
<journal-title-group><journal-title>International Journal of Molecular Sciences</journal-title>
</journal-title-group>
<issn pub-type="epub">1422-0067</issn>
<publisher><publisher-name>MDPI</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31717517</article-id>
<article-id pub-id-type="pmc">6888166</article-id>
<article-id pub-id-type="doi">10.3390/ijms20225606</article-id>
<article-id pub-id-type="publisher-id">ijms-20-05606</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Review</subject>
</subj-group>
</article-categories>
<title-group><article-title>Distinct Subcellular Compartments of Dendritic Cells Used for Cross-Presentation</article-title>
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<contrib-group><contrib contrib-type="author"><name><surname>Imai</surname>
<given-names>Jun</given-names>
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<xref rid="c1-ijms-20-05606" ref-type="corresp">*</xref>
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<contrib contrib-type="author"><name><surname>Otani</surname>
<given-names>Mayu</given-names>
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<contrib contrib-type="author"><name><surname>Sakai</surname>
<given-names>Takahiro</given-names>
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<aff id="af1-ijms-20-05606">Laboratory of Physiological Chemistry, Faculty of Pharmacy, Takasaki University of Health and Welfare, Takasaki, Gunma 370-0033, Japan;<email>nrd15766@gmail.com</email>
(M.O.);<email>sakai@takasaki-u.ac.jp</email>
(T.S.)</aff>
<author-notes><corresp id="c1-ijms-20-05606"><label>*</label>
Correspondence: <email>jimai@takasaki-u.ac.jp</email>
; Tel.: +81-27-352-1180</corresp>
</author-notes>
<pub-date pub-type="epub"><day>09</day>
<month>11</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="collection"><month>11</month>
<year>2019</year>
</pub-date>
<volume>20</volume>
<issue>22</issue>
<elocation-id>5606</elocation-id>
<history><date date-type="received"><day>26</day>
<month>8</month>
<year>2019</year>
</date>
<date date-type="accepted"><day>06</day>
<month>11</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>© 2019 by the authors.</copyright-statement>
<copyright-year>2019</copyright-year>
<license license-type="open-access"><license-p>Licensee MDPI, Basel, Switzerland. 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>Dendritic cells (DCs) present exogenous protein-derived peptides on major histocompatibility complex class I molecules to prime naïve CD8<sup>+</sup>
T cells. This DC specific ability, called cross-presentation (CP), is important for the activation of cell-mediated immunity and the induction of self-tolerance. Recent research revealed that endoplasmic reticulum-associated degradation (ERAD), which was first identified as a part of the unfolded protein response—a quality control system in the ER—plays a pivotal role in the processing of exogenous proteins in CP. Moreover, DCs express a variety of immuno-modulatory molecules and cytokines to regulate T cell activation in response to the environment. Although both CP and immuno-modulation are indispensable, contrasting ER conditions are required for their correct activity. Since ERAD substrates are unfolded proteins, their accumulation may result in ER stress, impaired cell homeostasis, and eventually apoptosis. In contrast, activation of the unfolded protein response should be inhibited for DCs to express immuno-modulatory molecules and cytokines. Here, we review recent advances on antigen CP, focusing on intracellular transport routes for exogenous antigens and distinctive subcellular compartments involved in ERAD.</p>
</abstract>
<kwd-group><kwd>dendritic cells</kwd>
<kwd>cross-presentation</kwd>
<kwd>major histocompatibility class I</kwd>
<kwd>endoplasmic reticulum-associated degradation</kwd>
<kwd>unfolded protein response</kwd>
<kwd>inflammation</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="ijms-20-05606-f001" orientation="portrait" position="float"><label>Figure 1</label>
<caption><p>Signal transduction of the unfolded protein response (UPR). Under normal conditions, all three endoplasmic reticulum (ER) stress sensors (i.e., protein kinase double-stranded RNA-dependent (PKR)-like ER Kinase (PERK), activating transcription factor 6 (ATF6), and inositol-requiring enzyme 1 (IRE1)) are associated with binding immunoglobulin protein (BiP). When unfolded proteins accumulate in the ER, BiP dissociates from PERK, ATF6, and IRE1 to bind with the unfolded proteins. As a result, the three molecular sensors are activated: (<bold>a</bold>
) PERK forms a homo-dimer complex and phosphorylates eIF2α, which attenuates translation. This inhibits the incorporation of newly synthesized proteins into the ER. In parallel, the selective translation of the transcription factor ATF4 is carried out. (<bold>b</bold>
) ATF6, which has dissociated from BiP, is transported into the Golgi apparatus and processed by the Golgi-resident endoproteases S1P and S2P. The resultant ATF6 cytosolic fragment acts as a transcription factor and activates the transcription of ER-resident molecular chaperones, which accelerate the folding of accumulated unfolded proteins. (<bold>c</bold>
) Activated IRE1 homo-dimerizes and self-phosphorylates. This conformational change determines the nonconventional splicing of X-box binding protein 1 (XBP1) mRNA. The resultant XBP1 spliced isoform (XBP1s) acts as a transcription factor and induces the transcription of three groups of molecules. (i) ER-resident molecular chaperones. (ii) ERAD-related molecules, to remove unfolded proteins from ER. (iii) Lipid synthesis related molecules. IRE1 also shows regulated IRE1-dependent decay (RIDD) activity to decrease the translation of ER-resident proteins, after completing nonconventional splicing of the XBP1 mRNA. (<bold>d</bold>
) If ER stress is too severe to be suppressed by the above-mentioned pathways, ATF4 acts as a transcription factor and induces the transcription of CCAAT/enhancer binding protein homologous transcription factor (CHOP) and GADD33. The ATF4/CHOP heterodimer induces apoptosis to eliminate stressed cells. GADD33 negatively regulates the PERK pathway, by dephosphorylating eI2Fα, to delay the activation of ATF4/CHOP. The dashed line indicates the nuclear membrane.</p>
</caption>
<graphic xlink:href="ijms-20-05606-g001"></graphic>
</fig>
<fig id="ijms-20-05606-f002" orientation="portrait" position="float"><label>Figure 2</label>
<caption><p>The molecular mechanisms of endoplasmic reticulum-associated degradation (ERAD) and cross-presentation (CP). The processing of exogenous proteins in CP involves a part of the molecular machinery of ERAD; however, significant differences exist. ERAD is carried out in the ER, while ERAD-dependent antigen processing during CP takes place in the non-classical endosomes, together with ER-resident molecules. The recognition of unfolded proteins by ER-resident molecules is similar in both processes, except for the EDEMs. Both the HRD1 and the Sec61 complexes are utilized in ERAD, but the HRD1 complex is not essential for CP. Additionally, several kinds of ERAD-related molecules, such as E3s, cofactors of VCP (i.e., NPL4 and UFD1), co-chaperones of Hsp70 (i.e., Bag6), deglycosidase, and deubiquitinase, play an important role in ERAD but are not investigated in CP. Solid arrows indicate mechanisms supported by experimental evidence. Dashed arrows indicate hypothetical mechanisms that still lack experimental evidence.</p>
</caption>
<graphic xlink:href="ijms-20-05606-g002"></graphic>
</fig>
<fig id="ijms-20-05606-f003" orientation="portrait" position="float"><label>Figure 3</label>
<caption><p>The crosstalk between CP, UPR, and inflammation. Pathogen-related stimuli, such as pattern recognition receptor (PRR) ligation, cytokines, and cell-extrinsic UPR can induce ER stress in Dendritic cells (DCs). Accumulation of unfolded proteins for CP also contributes to trigger/sustain ER stress in DCs. Although ER stress activates the UPR to restore ER homeostasis, the UPR itself accelerates the transcription of several inflammatory cytokines both directly, via UPR-related transcription factors, and indirectly, through the activation of different signaling cascades (e.g., NF-κB, PRRs). When the UPR of DCs is over-activated, the immunoregulatory functions of DCs are dismissed and this may result in chronic inflammation and ultimately cancer. However, when the UPR is over-repressed, CP efficiency is impaired. Thus, the non-canonical UPR of DCs has to cope with opposite requirements in order to maintain both ER homeostasis and adequate CP/immune-modulatory functions. The precise molecular mechanisms to evade UPR over-activation are, however, not known, except for the established suppressive function of GADD33. Black arrows indicate activation, T-arrows indicate suppression, blue arrows indicate pathways involved in the non-canonical UPR. The asterisks of IRE1 and XBPs indicate the risk factor for inflammatory disease among the UPR-related molecules.</p>
</caption>
<graphic xlink:href="ijms-20-05606-g003"></graphic>
</fig>
</floats-group>
</pmc>
<affiliations><list></list>
<tree><noCountry><name sortKey="Imai, Jun" sort="Imai, Jun" uniqKey="Imai J" first="Jun" last="Imai">Jun Imai</name>
<name sortKey="Otani, Mayu" sort="Otani, Mayu" uniqKey="Otani M" first="Mayu" last="Otani">Mayu Otani</name>
<name sortKey="Sakai, Takahiro" sort="Sakai, Takahiro" uniqKey="Sakai T" first="Takahiro" last="Sakai">Takahiro Sakai</name>
</noCountry>
</tree>
</affiliations>
</record>
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