Stepwise multipolyubiquitination of p53 by the E6AP-E6 ubiquitin ligase complex.
Identifieur interne : 002331 ( Ncbi/Merge ); précédent : 002330; suivant : 002332Stepwise multipolyubiquitination of p53 by the E6AP-E6 ubiquitin ligase complex.
Auteurs : Yuji Masuda [Japon] ; Yasushi Saeki [Japon] ; Naoko Arai [Japon] ; Hidehiko Kawai [Japon] ; Iwao Kukimoto [Japon] ; Keiji Tanaka [Japon] ; Chikahide Masutani [Japon]Source :
- The Journal of biological chemistry [ 1083-351X ] ; 2019.
Abstract
The human papillomavirus (HPV) oncoprotein E6 specifically binds to E6AP (E6-associated protein), a HECT (homologous to the E6AP C terminus)-type ubiquitin ligase, and directs its ligase activity toward the tumor suppressor p53. To examine the biochemical reaction in vitro, we established an efficient reconstitution system for the polyubiquitination of p53 by the E6AP-E6 complex. We demonstrate that E6AP-E6 formed a stable ternary complex with p53, which underwent extensive polyubiquitination when the isolated ternary complex was incubated with E1, E2, and ubiquitin. Mass spectrometry and biochemical analysis of the reaction products identified lysine residues as p53 ubiquitination sites. A p53 mutant with arginine substitutions of its 18 lysine residues was not ubiquitinated. Analysis of additional p53 mutants retaining only one or two intact ubiquitination sites revealed that chain elongation at each of these sites was limited to 5-6-mers. We also determined the size distribution of ubiquitin chains released by en bloc cleavage from polyubiquitinated p53 to be 2-6-mers. Taken together, these results strongly suggest that p53 is multipolyubiquitinated with short chains by E6AP-E6. In addition, analysis of growing chains provided strong evidence for step-by-step chain elongation. Thus, we hypothesize that p53 is polyubiquitinated in a stepwise manner through the back-and-forth movement of the C-lobe, and the permissive distance for the movement of the C-lobe restricts the length of the chains in the E6AP-E6-p53 ternary complex. Finally, we show that multipolyubiquitination at different sites provides a signal for proteasomal degradation.
DOI: 10.1074/jbc.RA119.008374
PubMed: 31492752
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wicri:rule="url">Japon</country><wicri:regionArea>Department of Genome Dynamics, Research Institute of Environmental Medicine, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601</wicri:regionArea><wicri:noRegion>Nagoya 464-8601</wicri:noRegion></affiliation></author><author><name sortKey="Saeki, Yasushi" sort="Saeki, Yasushi" uniqKey="Saeki Y" first="Yasushi" last="Saeki">Yasushi Saeki</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, 2-1-6 Kamikitazawa, Setagaya-ku, Tokyo 156-8506, Japan.</nlm:affiliation><country xml:lang="fr">Japon</country><wicri:regionArea>Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, 2-1-6 Kamikitazawa, Setagaya-ku, Tokyo 156-8506</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Arai, Naoko" sort="Arai, Naoko" uniqKey="Arai N" first="Naoko" last="Arai">Naoko Arai</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, 2-1-6 Kamikitazawa, Setagaya-ku, Tokyo 156-8506, Japan.</nlm:affiliation><country xml:lang="fr">Japon</country><wicri:regionArea>Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, 2-1-6 Kamikitazawa, Setagaya-ku, Tokyo 156-8506</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Kawai, Hidehiko" sort="Kawai, Hidehiko" uniqKey="Kawai H" first="Hidehiko" last="Kawai">Hidehiko Kawai</name><affiliation wicri:level="1"><nlm:affiliation>Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima 734-8553, Japan.</nlm:affiliation><country xml:lang="fr">Japon</country><wicri:regionArea>Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima 734-8553</wicri:regionArea><wicri:noRegion>Hiroshima 734-8553</wicri:noRegion></affiliation></author><author><name sortKey="Kukimoto, Iwao" sort="Kukimoto, Iwao" uniqKey="Kukimoto I" first="Iwao" last="Kukimoto">Iwao Kukimoto</name><affiliation wicri:level="1"><nlm:affiliation>Pathogen Genomics Center, National Institute of Infectious Diseases, 4-7-1 Gakuen, Musashi-murayama, Tokyo 208-0011, Japan.</nlm:affiliation><country xml:lang="fr">Japon</country><wicri:regionArea>Pathogen Genomics Center, National Institute of Infectious Diseases, 4-7-1 Gakuen, Musashi-murayama, Tokyo 208-0011</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Tanaka, Keiji" sort="Tanaka, Keiji" uniqKey="Tanaka K" first="Keiji" last="Tanaka">Keiji Tanaka</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, 2-1-6 Kamikitazawa, Setagaya-ku, Tokyo 156-8506, Japan.</nlm:affiliation><country xml:lang="fr">Japon</country><wicri:regionArea>Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, 2-1-6 Kamikitazawa, Setagaya-ku, Tokyo 156-8506</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Masutani, Chikahide" sort="Masutani, Chikahide" uniqKey="Masutani C" first="Chikahide" last="Masutani">Chikahide Masutani</name><affiliation wicri:level="1"><nlm:affiliation>Department of Genome Dynamics, Research Institute of Environmental Medicine, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan.</nlm:affiliation><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Genome Dynamics, Research Institute of Environmental Medicine, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601</wicri:regionArea><wicri:noRegion>Nagoya 464-8601</wicri:noRegion></affiliation></author></analytic><series><title level="j">The Journal of biological chemistry</title><idno type="eISSN">1083-351X</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The human papillomavirus (HPV) oncoprotein E6 specifically binds to E6AP (E6-associated protein), a HECT (homologous to the E6AP C terminus)-type ubiquitin ligase, and directs its ligase activity toward the tumor suppressor p53. To examine the biochemical reaction <i>in vitro</i>, we established an efficient reconstitution system for the polyubiquitination of p53 by the E6AP-E6 complex. We demonstrate that E6AP-E6 formed a stable ternary complex with p53, which underwent extensive polyubiquitination when the isolated ternary complex was incubated with E1, E2, and ubiquitin. Mass spectrometry and biochemical analysis of the reaction products identified lysine residues as p53 ubiquitination sites. A p53 mutant with arginine substitutions of its 18 lysine residues was not ubiquitinated. Analysis of additional p53 mutants retaining only one or two intact ubiquitination sites revealed that chain elongation at each of these sites was limited to 5-6-mers. We also determined the size distribution of ubiquitin chains released by <i>en bloc</i> cleavage from polyubiquitinated p53 to be 2-6-mers. Taken together, these results strongly suggest that p53 is multipolyubiquitinated with short chains by E6AP-E6. In addition, analysis of growing chains provided strong evidence for step-by-step chain elongation. Thus, we hypothesize that p53 is polyubiquitinated in a stepwise manner through the back-and-forth movement of the C-lobe, and the permissive distance for the movement of the C-lobe restricts the length of the chains in the E6AP-E6-p53 ternary complex. Finally, we show that multipolyubiquitination at different sites provides a signal for proteasomal degradation.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">31492752</PMID><DateRevised><Year>2019</Year><Month>10</Month><Day>23</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1083-351X</ISSN><JournalIssue CitedMedium="Internet"><Volume>294</Volume><Issue>41</Issue><PubDate><Year>2019</Year><Month>Oct</Month><Day>11</Day></PubDate></JournalIssue><Title>The Journal of biological chemistry</Title><ISOAbbreviation>J. Biol. Chem.</ISOAbbreviation></Journal><ArticleTitle>Stepwise multipolyubiquitination of p53 by the E6AP-E6 ubiquitin ligase complex.</ArticleTitle><Pagination><MedlinePgn>14860-14875</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1074/jbc.RA119.008374</ELocationID><Abstract><AbstractText>The human papillomavirus (HPV) oncoprotein E6 specifically binds to E6AP (E6-associated protein), a HECT (homologous to the E6AP C terminus)-type ubiquitin ligase, and directs its ligase activity toward the tumor suppressor p53. To examine the biochemical reaction <i>in vitro</i>, we established an efficient reconstitution system for the polyubiquitination of p53 by the E6AP-E6 complex. We demonstrate that E6AP-E6 formed a stable ternary complex with p53, which underwent extensive polyubiquitination when the isolated ternary complex was incubated with E1, E2, and ubiquitin. Mass spectrometry and biochemical analysis of the reaction products identified lysine residues as p53 ubiquitination sites. A p53 mutant with arginine substitutions of its 18 lysine residues was not ubiquitinated. Analysis of additional p53 mutants retaining only one or two intact ubiquitination sites revealed that chain elongation at each of these sites was limited to 5-6-mers. We also determined the size distribution of ubiquitin chains released by <i>en bloc</i> cleavage from polyubiquitinated p53 to be 2-6-mers. Taken together, these results strongly suggest that p53 is multipolyubiquitinated with short chains by E6AP-E6. In addition, analysis of growing chains provided strong evidence for step-by-step chain elongation. Thus, we hypothesize that p53 is polyubiquitinated in a stepwise manner through the back-and-forth movement of the C-lobe, and the permissive distance for the movement of the C-lobe restricts the length of the chains in the E6AP-E6-p53 ternary complex. Finally, we show that multipolyubiquitination at different sites provides a signal for proteasomal degradation.</AbstractText><CopyrightInformation>© 2019 Masuda et al.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Masuda</LastName><ForeName>Yuji</ForeName><Initials>Y</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-6229-1988</Identifier><AffiliationInfo><Affiliation>Department of Genome Dynamics, Research Institute of Environmental Medicine, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan masuda@riem.nagoya-u.ac.jp.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Nagoya University Graduate School of Medicine, 65 Tsurumai-cho, Showa-ku, Nagoya 466-8550, Japan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Saeki</LastName><ForeName>Yasushi</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, 2-1-6 Kamikitazawa, Setagaya-ku, Tokyo 156-8506, Japan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Arai</LastName><ForeName>Naoko</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, 2-1-6 Kamikitazawa, Setagaya-ku, Tokyo 156-8506, Japan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kawai</LastName><ForeName>Hidehiko</ForeName><Initials>H</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-2213-7166</Identifier><AffiliationInfo><Affiliation>Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima 734-8553, Japan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kukimoto</LastName><ForeName>Iwao</ForeName><Initials>I</Initials><AffiliationInfo><Affiliation>Pathogen Genomics Center, National Institute of Infectious Diseases, 4-7-1 Gakuen, Musashi-murayama, Tokyo 208-0011, Japan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tanaka</LastName><ForeName>Keiji</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, 2-1-6 Kamikitazawa, Setagaya-ku, Tokyo 156-8506, Japan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Masutani</LastName><ForeName>Chikahide</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Department of Genome Dynamics, Research Institute of Environmental Medicine, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Nagoya University Graduate School of Medicine, 65 Tsurumai-cho, Showa-ku, Nagoya 466-8550, Japan.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>09</Month><Day>06</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>J Biol Chem</MedlineTA><NlmUniqueID>2985121R</NlmUniqueID><ISSNLinking>0021-9258</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">E3 ubiquitin ligase</Keyword><Keyword MajorTopicYN="N">E6-associated protein</Keyword><Keyword MajorTopicYN="N">Lys48-linked ubiquitin chain</Keyword><Keyword MajorTopicYN="N">enzyme mechanism</Keyword><Keyword MajorTopicYN="N">human papillomavirus (HPV) oncoprotein E6</Keyword><Keyword MajorTopicYN="N">in vitro reconstitution</Keyword><Keyword MajorTopicYN="N">linkage specificity</Keyword><Keyword MajorTopicYN="N">mass spectrometry (MS)</Keyword><Keyword MajorTopicYN="N">p53</Keyword><Keyword MajorTopicYN="N">polyubiquitin 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