Exclusion of small terminase mediated DNA threading models for genome packaging in bacteriophage T4
Identifieur interne : 000103 ( Pmc/Curation ); précédent : 000102; suivant : 000104Exclusion of small terminase mediated DNA threading models for genome packaging in bacteriophage T4
Auteurs : Song Gao [États-Unis, République populaire de Chine] ; Liang Zhang [États-Unis] ; Venigalla B. Rao [États-Unis]Source :
- Nucleic Acids Research [ 0305-1048 ] ; 2016.
Abstract
Tailed bacteriophages and herpes viruses use powerful molecular machines to package their genomes. The packaging machine consists of three components: portal, motor (large terminase; TerL) and regulator (small terminase; TerS). Portal, a dodecamer, and motor, a pentamer, form two concentric rings at the special five-fold vertex of the icosahedral capsid. Powered by ATPase, the motor ratchets DNA into the capsid through the portal channel. TerS is essential for packaging, particularly for genome recognition, but its mechanism is unknown and controversial. Structures of gear-shaped TerS rings inspired models that invoke DNA threading through the central channel. Here, we report that mutations of basic residues that line phage T4 TerS (gp16) channel do not disrupt DNA binding. Even deletion of the entire channel helix retained DNA binding and produced progeny phage
Url:
DOI: 10.1093/nar/gkw184
PubMed: 26984529
PubMed Central: 4872099
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Exclusion of small terminase mediated DNA threading models for genome packaging in bacteriophage T4</title><author><name sortKey="Gao, Song" sort="Gao, Song" uniqKey="Gao S" first="Song" last="Gao">Song Gao</name><affiliation wicri:level="1"><nlm:aff id="AFF1">Department of Biology, The Catholic University of America, 620 Michigan Avenue Northeast, Washington, DC 20064, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biology, The Catholic University of America, 620 Michigan Avenue Northeast, Washington, DC 20064</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="AFF2">Jiangsu Key Laboratory of Marine Pharmaceutical Compound Screening, Huaihai Institute of Technology, Lianyungang 222005, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Jiangsu Key Laboratory of Marine Pharmaceutical Compound Screening, Huaihai Institute of Technology, Lianyungang 222005</wicri:regionArea></affiliation></author><author><name sortKey="Zhang, Liang" sort="Zhang, Liang" uniqKey="Zhang L" first="Liang" last="Zhang">Liang Zhang</name><affiliation wicri:level="1"><nlm:aff id="AFF1">Department of Biology, The Catholic University of America, 620 Michigan Avenue Northeast, Washington, DC 20064, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biology, The Catholic University of America, 620 Michigan Avenue Northeast, Washington, DC 20064</wicri:regionArea></affiliation></author><author><name sortKey="Rao, Venigalla B" sort="Rao, Venigalla B" uniqKey="Rao V" first="Venigalla B." last="Rao">Venigalla B. Rao</name><affiliation wicri:level="1"><nlm:aff id="AFF1">Department of Biology, The Catholic University of America, 620 Michigan Avenue Northeast, Washington, DC 20064, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biology, The Catholic University of America, 620 Michigan Avenue Northeast, Washington, DC 20064</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26984529</idno><idno type="pmc">4872099</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4872099</idno><idno type="RBID">PMC:4872099</idno><idno type="doi">10.1093/nar/gkw184</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000103</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000103</idno><idno type="wicri:Area/Pmc/Curation">000103</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000103</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Exclusion of small terminase mediated DNA threading models for genome packaging in bacteriophage T4</title><author><name sortKey="Gao, Song" sort="Gao, Song" uniqKey="Gao S" first="Song" last="Gao">Song Gao</name><affiliation wicri:level="1"><nlm:aff id="AFF1">Department of Biology, The Catholic University of America, 620 Michigan Avenue Northeast, Washington, DC 20064, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biology, The Catholic University of America, 620 Michigan Avenue Northeast, Washington, DC 20064</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="AFF2">Jiangsu Key Laboratory of Marine Pharmaceutical Compound Screening, Huaihai Institute of Technology, Lianyungang 222005, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Jiangsu Key Laboratory of Marine Pharmaceutical Compound Screening, Huaihai Institute of Technology, Lianyungang 222005</wicri:regionArea></affiliation></author><author><name sortKey="Zhang, Liang" sort="Zhang, Liang" uniqKey="Zhang L" first="Liang" last="Zhang">Liang Zhang</name><affiliation wicri:level="1"><nlm:aff id="AFF1">Department of Biology, The Catholic University of America, 620 Michigan Avenue Northeast, Washington, DC 20064, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biology, The Catholic University of America, 620 Michigan Avenue Northeast, Washington, DC 20064</wicri:regionArea></affiliation></author><author><name sortKey="Rao, Venigalla B" sort="Rao, Venigalla B" uniqKey="Rao V" first="Venigalla B." last="Rao">Venigalla B. Rao</name><affiliation wicri:level="1"><nlm:aff id="AFF1">Department of Biology, The Catholic University of America, 620 Michigan Avenue Northeast, Washington, DC 20064, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biology, The Catholic University of America, 620 Michigan Avenue Northeast, Washington, DC 20064</wicri:regionArea></affiliation></author></analytic><series><title level="j">Nucleic Acids Research</title><idno type="ISSN">0305-1048</idno><idno type="eISSN">1362-4962</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Tailed bacteriophages and herpes viruses use powerful molecular machines to package their genomes. The packaging machine consists of three components: portal, motor (large terminase; TerL) and regulator (small terminase; TerS). Portal, a dodecamer, and motor, a pentamer, form two concentric rings at the special five-fold vertex of the icosahedral capsid. Powered by ATPase, the motor ratchets DNA into the capsid through the portal channel. TerS is essential for packaging, particularly for genome recognition, but its mechanism is unknown and controversial. Structures of gear-shaped TerS rings inspired models that invoke DNA threading through the central channel. Here, we report that mutations of basic residues that line phage T4 TerS (gp16) channel do not disrupt DNA binding. Even deletion of the entire channel helix retained DNA binding and produced progeny phage <italic>in vivo</italic>. On the other hand, large oligomers of TerS (11-mers/12-mers), but not small oligomers (trimers to hexamers), bind DNA. These results suggest that TerS oligomerization creates a large outer surface, which, but not the interior of the channel, is critical for function, probably to wrap viral genome around the ring during packaging initiation. Hence, models involving TerS-mediated DNA threading may be excluded as an essential mechanism for viral genome packaging.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Hendrix, R W" uniqKey="Hendrix R">R.W. Hendrix</name></author><author><name sortKey="Smith, M C" uniqKey="Smith M">M.C. Smith</name></author><author><name sortKey="Burns, R N" uniqKey="Burns R">R.N. Burns</name></author><author><name sortKey="Ford, M E" uniqKey="Ford M">M.E. Ford</name></author><author><name sortKey="Hatfull, G F" uniqKey="Hatfull G">G.F. Hatfull</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Rao, V B" uniqKey="Rao V">V.B. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Nucleic Acids Res</journal-id><journal-id journal-id-type="iso-abbrev">Nucleic Acids Res</journal-id><journal-id journal-id-type="hwp">nar</journal-id><journal-id journal-id-type="publisher-id">nar</journal-id><journal-title-group><journal-title>Nucleic Acids Research</journal-title></journal-title-group><issn pub-type="ppub">0305-1048</issn><issn pub-type="epub">1362-4962</issn><publisher><publisher-name>Oxford University Press</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26984529</article-id><article-id pub-id-type="pmc">4872099</article-id><article-id pub-id-type="doi">10.1093/nar/gkw184</article-id><article-categories><subj-group subj-group-type="heading"><subject>Structural Biology</subject></subj-group></article-categories><title-group><article-title>Exclusion of small terminase mediated DNA threading models for genome packaging in bacteriophage T4</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Gao</surname><given-names>Song</given-names></name><xref ref-type="aff" rid="AFF1"><sup>1</sup></xref><xref ref-type="aff" rid="AFF2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Zhang</surname><given-names>Liang</given-names></name><xref ref-type="aff" rid="AFF1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Rao</surname><given-names>Venigalla B.</given-names></name><xref ref-type="aff" rid="AFF1"><sup>1</sup></xref><xref ref-type="corresp" rid="COR1">*</xref></contrib><aff id="AFF1"><label>1</label>Department of Biology, The Catholic University of America, 620 Michigan Avenue Northeast, Washington, DC 20064, USA</aff><aff id="AFF2"><label>2</label>Jiangsu Key Laboratory of Marine Pharmaceutical Compound Screening, Huaihai Institute of Technology, Lianyungang 222005, China</aff></contrib-group><author-notes><corresp id="COR1"><label>*</label>To whom correspondence should be addressed. Tel: +1 202 319 5271; Fax: +1 202 319 5721; Email: <email>rao@cua.edu</email></corresp></author-notes><pub-date pub-type="ppub"><day>19</day><month>5</month><year>2016</year></pub-date><pub-date pub-type="epub"><day>16</day><month>3</month><year>2016</year></pub-date><pub-date pub-type="pmc-release"><day>16</day><month>3</month><year>2016</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
<volume>44</volume><issue>9</issue><fpage>4425</fpage><lpage>4439</lpage><history><date date-type="accepted"><day>04</day><month>3</month><year>2016</year></date><date date-type="rev-recd"><day>03</day><month>3</month><year>2016</year></date><date date-type="received"><day>09</day><month>2</month><year>2016</year></date></history><permissions><copyright-statement>© The Author(s) 2016. Published by Oxford University Press on behalf of Nucleic Acids Research.</copyright-statement><copyright-year>2016</copyright-year><license license-type="creative-commons" xlink:href="http://creativecommons.org/licenses/by-nc/4.0/"><license-p>This is an Open Access article distributed under the terms of the Creative Commons Attribution License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc/4.0/">http://creativecommons.org/licenses/by-nc/4.0/</ext-link>), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact <email>journals.permissions@oup.com</email></license-p></license></permissions><self-uri xlink:title="pdf" xlink:href="gkw184.pdf"></self-uri><abstract><p>Tailed bacteriophages and herpes viruses use powerful molecular machines to package their genomes. The packaging machine consists of three components: portal, motor (large terminase; TerL) and regulator (small terminase; TerS). Portal, a dodecamer, and motor, a pentamer, form two concentric rings at the special five-fold vertex of the icosahedral capsid. Powered by ATPase, the motor ratchets DNA into the capsid through the portal channel. TerS is essential for packaging, particularly for genome recognition, but its mechanism is unknown and controversial. Structures of gear-shaped TerS rings inspired models that invoke DNA threading through the central channel. Here, we report that mutations of basic residues that line phage T4 TerS (gp16) channel do not disrupt DNA binding. Even deletion of the entire channel helix retained DNA binding and produced progeny phage <italic>in vivo</italic>. On the other hand, large oligomers of TerS (11-mers/12-mers), but not small oligomers (trimers to hexamers), bind DNA. These results suggest that TerS oligomerization creates a large outer surface, which, but not the interior of the channel, is critical for function, probably to wrap viral genome around the ring during packaging initiation. Hence, models involving TerS-mediated DNA threading may be excluded as an essential mechanism for viral genome packaging.</p></abstract><counts><page-count count="15"></page-count></counts><custom-meta-group><custom-meta><meta-name>cover-date</meta-name><meta-value>19 May 2016</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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