Insight into the evolution of nidovirus endoribonuclease based on the finding that nsp15 from porcine Deltacoronavirus functions as a dimer
Identifieur interne : 000537 ( Pmc/Checkpoint ); précédent : 000536; suivant : 000538Insight into the evolution of nidovirus endoribonuclease based on the finding that nsp15 from porcine Deltacoronavirus functions as a dimer
Auteurs : Anjun Zheng ; Yuejun Shi [République populaire de Chine] ; Zhou Shen ; Gang Wang ; Jiale Shi ; Qiqi Xiong [République populaire de Chine] ; Liurong Fang ; Shaobo Xiao ; Zhen F. Fu ; Guiqing PengSource :
- The Journal of Biological Chemistry [ 0021-9258 ] ; 2018.
Abstract
Nidovirus endoribonucleases (NendoUs) include nonstructural protein 15 (nsp15) from coronaviruses and nsp11 from arteriviruses, both of which have been reported to participate in the viral replication process and in the evasion of the host immune system. Results from a previous study of coronaviruses SARS-CoV, HCoV-229E, and MHV nsp15 indicate that it mainly forms a functional hexamer, whereas nsp11 from the arterivirus PRRSV is a dimer. Here, we found that porcine
Url:
DOI: 10.1074/jbc.RA118.003756
PubMed: 29887523
PubMed Central: 6078464
Affiliations:
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PMC:6078464Le document en format XML
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<author><name sortKey="Zheng, Anjun" sort="Zheng, Anjun" uniqKey="Zheng A" first="Anjun" last="Zheng">Anjun Zheng</name>
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<author><name sortKey="Shi, Jiale" sort="Shi, Jiale" uniqKey="Shi J" first="Jiale" last="Shi">Jiale Shi</name>
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<author><name sortKey="Fu, Zhen F" sort="Fu, Zhen F" uniqKey="Fu Z" first="Zhen F." last="Fu">Zhen F. Fu</name>
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<author><name sortKey="Peng, Guiqing" sort="Peng, Guiqing" uniqKey="Peng G" first="Guiqing" last="Peng">Guiqing Peng</name>
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<series><title level="j">The Journal of Biological Chemistry</title>
<idno type="ISSN">0021-9258</idno>
<idno type="eISSN">1083-351X</idno>
<imprint><date when="2018">2018</date>
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<front><div type="abstract" xml:lang="en"><p>Nidovirus endoribonucleases (NendoUs) include nonstructural protein 15 (nsp15) from coronaviruses and nsp11 from arteriviruses, both of which have been reported to participate in the viral replication process and in the evasion of the host immune system. Results from a previous study of coronaviruses SARS-CoV, HCoV-229E, and MHV nsp15 indicate that it mainly forms a functional hexamer, whereas nsp11 from the arterivirus PRRSV is a dimer. Here, we found that porcine <italic>Deltacoronavirus</italic>
(PDCoV) nsp15 primarily exists as dimers and monomers <italic>in vitro</italic>
. Biological experiments reveal that a PDCoV nsp15 mutant lacking the first 27 amino acids of the N-terminal domain (Asn-1–Asn-27) forms more monomers and displays decreased enzymatic activity, indicating that this region is important for its dimerization. Moreover, multiple sequence alignments and three-dimensional structural analysis indicated that the C-terminal region (His-251–Val-261) of PDCoV nsp15 is 10 amino acids shorter and forms a shorter loop than that formed by the equivalent sequence (Gln-259–Phe-279) of SARS-CoV nsp15. This result may explain why PDCoV nsp15 failed to form hexamers. We speculate that NendoUs may have originated from XendoU endoribonucleases (XendoUs) forming monomers in eukaryotic cells, that NendoU from arterivirus gained the ability to form dimers, and that the coronavirus variants then evolved the capacity to assemble into hexamers. We further propose that PDCoV nsp15 may be an intermediate in this evolutionary process. Our findings provide a theoretical basis for improving our understanding of NendoU evolution and offer useful clues for designing drugs and vaccines against nidoviruses.</p>
</div>
</front>
</TEI>
<pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Biol Chem</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Biol. Chem</journal-id>
<journal-id journal-id-type="hwp">jbc</journal-id>
<journal-id journal-id-type="pmc">jbc</journal-id>
<journal-id journal-id-type="publisher-id">JBC</journal-id>
<journal-title-group><journal-title>The Journal of Biological Chemistry</journal-title>
</journal-title-group>
<issn pub-type="ppub">0021-9258</issn>
<issn pub-type="epub">1083-351X</issn>
<publisher><publisher-name>American Society for Biochemistry and Molecular Biology</publisher-name>
<publisher-loc>11200 Rockville Pike, Suite 302, Rockville, MD 20852-3110, U.S.A.</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">29887523</article-id>
<article-id pub-id-type="pmc">6078464</article-id>
<article-id pub-id-type="publisher-id">RA118.003756</article-id>
<article-id pub-id-type="doi">10.1074/jbc.RA118.003756</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Microbiology</subject>
</subj-group>
</article-categories>
<title-group><article-title>Insight into the evolution of nidovirus endoribonuclease based on the finding that nsp15 from porcine <italic>Deltacoronavirus</italic>
functions as a dimer</article-title>
<alt-title alt-title-type="short">Evolution of nidovirus endoribonuclease</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Zheng</surname>
<given-names>Anjun</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>§</sup>
</xref>
<xref ref-type="author-notes" rid="FN1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Shi</surname>
<given-names>Yuejun</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>§</sup>
</xref>
<xref ref-type="aff" rid="aff3"><sup>¶</sup>
</xref>
<xref ref-type="author-notes" rid="FN1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Shen</surname>
<given-names>Zhou</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>§</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wang</surname>
<given-names>Gang</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>§</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Shi</surname>
<given-names>Jiale</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>§</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Xiong</surname>
<given-names>Qiqi</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>¶</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fang</surname>
<given-names>Liurong</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>§</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Xiao</surname>
<given-names>Shaobo</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>§</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fu</surname>
<given-names>Zhen F.</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>‖</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Peng</surname>
<given-names>Guiqing</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>§</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>2</sup>
</xref>
</contrib>
<aff id="aff1">From the<label>‡</label>
State Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine,</aff>
<aff id="aff2"><label>§</label>
Key Laboratory of Preventive Veterinary Medicine in Hubei Province, The Cooperative Innovation Center for Sustainable Pig Production, and</aff>
<aff id="aff3"><label>¶</label>
College of Life Science and Technology, Huazhong Agricultural University, Wuhan 430070, China and</aff>
<aff id="aff4">the<label>‖</label>
Department of Pathology, College of Veterinary Medicine, University of Georgia, Athens, Georgia 30602</aff>
</contrib-group>
<author-notes><corresp id="cor1"><label>2</label>
To whom correspondence should be addressed:
<addr-line>State Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, 1 Shi-zi-shan St., Wuhan 430070, China.</addr-line>
Tel.:
<phone>86-18071438015</phone>
; Fax:
<fax>86-27-87280480</fax>
; E-mail: <email>penggq@mail.hzau.edu.cn</email>
.</corresp>
<fn fn-type="equal" id="FN1"><label>1</label>
<p>Both authors contributed equally to this work.</p>
</fn>
<fn fn-type="edited-by"><p>Edited by Charles E. Samuel</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>3</day>
<month>8</month>
<year>2018</year>
</pub-date>
<pub-date pub-type="epub"><day>10</day>
<month>6</month>
<year>2018</year>
</pub-date>
<volume>293</volume>
<issue>31</issue>
<fpage>12054</fpage>
<lpage>12067</lpage>
<history><date date-type="received"><day>28</day>
<month>4</month>
<year>2018</year>
</date>
<date date-type="rev-recd"><day>31</day>
<month>5</month>
<year>2018</year>
</date>
</history>
<permissions><copyright-statement>© 2018 Zheng et al.</copyright-statement>
<copyright-year>2018</copyright-year>
<copyright-holder>Zheng et al.</copyright-holder>
<license><license-p>Published under exclusive license by The American Society for Biochemistry and Molecular Biology, Inc.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:href="zbc03118012054.pdf"></self-uri>
<abstract><p>Nidovirus endoribonucleases (NendoUs) include nonstructural protein 15 (nsp15) from coronaviruses and nsp11 from arteriviruses, both of which have been reported to participate in the viral replication process and in the evasion of the host immune system. Results from a previous study of coronaviruses SARS-CoV, HCoV-229E, and MHV nsp15 indicate that it mainly forms a functional hexamer, whereas nsp11 from the arterivirus PRRSV is a dimer. Here, we found that porcine <italic>Deltacoronavirus</italic>
(PDCoV) nsp15 primarily exists as dimers and monomers <italic>in vitro</italic>
. Biological experiments reveal that a PDCoV nsp15 mutant lacking the first 27 amino acids of the N-terminal domain (Asn-1–Asn-27) forms more monomers and displays decreased enzymatic activity, indicating that this region is important for its dimerization. Moreover, multiple sequence alignments and three-dimensional structural analysis indicated that the C-terminal region (His-251–Val-261) of PDCoV nsp15 is 10 amino acids shorter and forms a shorter loop than that formed by the equivalent sequence (Gln-259–Phe-279) of SARS-CoV nsp15. This result may explain why PDCoV nsp15 failed to form hexamers. We speculate that NendoUs may have originated from XendoU endoribonucleases (XendoUs) forming monomers in eukaryotic cells, that NendoU from arterivirus gained the ability to form dimers, and that the coronavirus variants then evolved the capacity to assemble into hexamers. We further propose that PDCoV nsp15 may be an intermediate in this evolutionary process. Our findings provide a theoretical basis for improving our understanding of NendoU evolution and offer useful clues for designing drugs and vaccines against nidoviruses.</p>
</abstract>
<kwd-group><kwd>viral protein</kwd>
<kwd>endoribonuclease</kwd>
<kwd>protein purification</kwd>
<kwd>oligomerization</kwd>
<kwd>protein evolution</kwd>
<kwd>endoribonuclease</kwd>
<kwd>evolution</kwd>
<kwd>nidovirus</kwd>
<kwd>oligomerization</kwd>
<kwd>PDCoV nsp15</kwd>
</kwd-group>
<funding-group><award-group id="award1"><funding-source><institution-wrap><institution>National Natural Science Foundation of China (NSFC)
</institution>
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<award-group id="award2"><funding-source><institution-wrap><institution>China Postdoctoral Science Foundation
</institution>
<institution-id institution-id-type="open-funder-registry">10.13039/501100002858</institution-id>
</institution-wrap>
</funding-source>
<award-id>No.2017M612484</award-id>
</award-group>
<award-group id="award3"><funding-source><institution-wrap><institution>Natural Science Foundation of Hubei Province (Hubei Provincial Natural Science Foundation)
</institution>
<institution-id institution-id-type="open-funder-registry">10.13039/501100003819</institution-id>
</institution-wrap>
</funding-source>
<award-id>2016CFA069</award-id>
</award-group>
<award-group id="award4"><funding-source>National Key R&D Plan OF China
</funding-source>
<award-id>No. 2018YFD0500100</award-id>
</award-group>
</funding-group>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>République populaire de Chine</li>
</country>
<region><li>Hubei</li>
</region>
<settlement><li>Wuhan</li>
</settlement>
</list>
<tree><noCountry><name sortKey="Fang, Liurong" sort="Fang, Liurong" uniqKey="Fang L" first="Liurong" last="Fang">Liurong Fang</name>
<name sortKey="Fu, Zhen F" sort="Fu, Zhen F" uniqKey="Fu Z" first="Zhen F." last="Fu">Zhen F. Fu</name>
<name sortKey="Peng, Guiqing" sort="Peng, Guiqing" uniqKey="Peng G" first="Guiqing" last="Peng">Guiqing Peng</name>
<name sortKey="Shen, Zhou" sort="Shen, Zhou" uniqKey="Shen Z" first="Zhou" last="Shen">Zhou Shen</name>
<name sortKey="Shi, Jiale" sort="Shi, Jiale" uniqKey="Shi J" first="Jiale" last="Shi">Jiale Shi</name>
<name sortKey="Wang, Gang" sort="Wang, Gang" uniqKey="Wang G" first="Gang" last="Wang">Gang Wang</name>
<name sortKey="Xiao, Shaobo" sort="Xiao, Shaobo" uniqKey="Xiao S" first="Shaobo" last="Xiao">Shaobo Xiao</name>
<name sortKey="Zheng, Anjun" sort="Zheng, Anjun" uniqKey="Zheng A" first="Anjun" last="Zheng">Anjun Zheng</name>
</noCountry>
<country name="République populaire de Chine"><region name="Hubei"><name sortKey="Shi, Yuejun" sort="Shi, Yuejun" uniqKey="Shi Y" first="Yuejun" last="Shi">Yuejun Shi</name>
</region>
<name sortKey="Xiong, Qiqi" sort="Xiong, Qiqi" uniqKey="Xiong Q" first="Qiqi" last="Xiong">Qiqi Xiong</name>
</country>
</tree>
</affiliations>
</record>
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