APC/CCDH1 synchronizes ribose-5-phosphate levels and DNA synthesis to cell cycle progression
Identifieur interne : 000A49 ( Pmc/Checkpoint ); précédent : 000A48; suivant : 000A50APC/CCDH1 synchronizes ribose-5-phosphate levels and DNA synthesis to cell cycle progression
Auteurs : Yang Li [République populaire de Chine] ; Cui-Fang Yao [République populaire de Chine] ; Fu-Jiang Xu [République populaire de Chine] ; Yuan-Yuan Qu [République populaire de Chine] ; Jia-Tao Li [République populaire de Chine] ; Yan Lin [République populaire de Chine] ; Zhong-Lian Cao [République populaire de Chine] ; Peng-Cheng Lin [République populaire de Chine] ; Wei Xu [République populaire de Chine] ; Shi-Min Zhao [République populaire de Chine] ; Jian-Yuan Zhao [République populaire de Chine]Source :
- Nature Communications [ 2041-1723 ] ; 2019.
Abstract
Accumulation of nucleotide building blocks prior to and during S phase facilitates DNA duplication. Herein, we find that the anaphase-promoting complex/cyclosome (APC/C) synchronizes ribose-5-phosphate levels and DNA synthesis during the cell cycle. In late G1 and S phases, transketolase-like 1 (TKTL1) is overexpressed and forms stable TKTL1-transketolase heterodimers that accumulate ribose-5-phosphate. This accumulation occurs by asymmetric production of ribose-5-phosphate from the non-oxidative pentose phosphate pathway and prevention of ribose-5-phosphate removal by depleting transketolase homodimers. In the G2 and M phases after DNA synthesis, expression of the APC/C adaptor CDH1 allows APC/CCDH1 to degrade D-box-containing TKTL1, abrogating ribose-5-phosphate accumulation by TKTL1. TKTL1-overexpressing cancer cells exhibit elevated ribose-5-phosphate levels. The low CDH1 or high TKTL1-induced accumulation of ribose-5-phosphate facilitates nucleotide and DNA synthesis as well as cell cycle progression in a ribose-5-phosphate-saturable manner. Here we reveal that the cell cycle control machinery regulates DNA synthesis by mediating ribose-5-phosphate sufficiency.
Url:
DOI: 10.1038/s41467-019-10375-x
PubMed: 31175280
PubMed Central: 6555833
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synchronizes ribose-5-phosphate levels and DNA synthesis to cell cycle progression</title>
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<institution>School of Pharmacy,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 200438 P.R. China</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country>
<wicri:regionArea>Shanghai</wicri:regionArea>
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</author>
<author><name sortKey="Lin, Peng Cheng" sort="Lin, Peng Cheng" uniqKey="Lin P" first="Peng-Cheng" last="Lin">Peng-Cheng Lin</name>
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<institution>Qinghai University for Nationalities,</institution>
</institution-wrap>
Xining, 810007 P. R. China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Xining</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Xu, Wei" sort="Xu, Wei" uniqKey="Xu W" first="Wei" last="Xu">Wei Xu</name>
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<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 200438 P.R. China</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country>
<wicri:regionArea>Shanghai</wicri:regionArea>
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<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 200438 P.R. China</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country>
<wicri:regionArea>Shanghai</wicri:regionArea>
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<institution>Collaborative Innovation Center for Biotherapy, West China Hospital,</institution>
<institution>Sichuan University,</institution>
</institution-wrap>
Chengdu, 610041 P.R. China</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country>
<wicri:regionArea>Chengdu</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Zhao, Shi Min" sort="Zhao, Shi Min" uniqKey="Zhao S" first="Shi-Min" last="Zhao">Shi-Min Zhao</name>
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<institution-id institution-id-type="GRID">grid.8547.e</institution-id>
<institution>Obstetrics & Gynecology Hospital of Fudan University, State Key Laboratory of Genetic Engineering, School of Life Sciences and Institutes of Biomedical Sciences,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 200438 P.R. China</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country>
<wicri:regionArea>Shanghai</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id>
<institution-id institution-id-type="GRID">grid.8547.e</institution-id>
<institution>Key Laboratory of Reproduction Regulation of NPFPC and Collaborative Innovation Center for Genetics and Development, Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 200438 P.R. China</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country>
<wicri:regionArea>Shanghai</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="Aff6"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0807 1581</institution-id>
<institution-id institution-id-type="GRID">grid.13291.38</institution-id>
<institution>Collaborative Innovation Center for Biotherapy, West China Hospital,</institution>
<institution>Sichuan University,</institution>
</institution-wrap>
Chengdu, 610041 P.R. China</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country>
<wicri:regionArea>Chengdu</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Zhao, Jian Yuan" sort="Zhao, Jian Yuan" uniqKey="Zhao J" first="Jian-Yuan" last="Zhao">Jian-Yuan Zhao</name>
<affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id>
<institution-id institution-id-type="GRID">grid.8547.e</institution-id>
<institution>Obstetrics & Gynecology Hospital of Fudan University, State Key Laboratory of Genetic Engineering, School of Life Sciences and Institutes of Biomedical Sciences,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 200438 P.R. China</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country>
<wicri:regionArea>Shanghai</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id>
<institution-id institution-id-type="GRID">grid.8547.e</institution-id>
<institution>Key Laboratory of Reproduction Regulation of NPFPC and Collaborative Innovation Center for Genetics and Development, Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 200438 P.R. China</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country>
<wicri:regionArea>Shanghai</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="Aff6"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0807 1581</institution-id>
<institution-id institution-id-type="GRID">grid.13291.38</institution-id>
<institution>Collaborative Innovation Center for Biotherapy, West China Hospital,</institution>
<institution>Sichuan University,</institution>
</institution-wrap>
Chengdu, 610041 P.R. China</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country>
<wicri:regionArea>Chengdu</wicri:regionArea>
</affiliation>
</author>
</analytic>
<series><title level="j">Nature Communications</title>
<idno type="eISSN">2041-1723</idno>
<imprint><date when="2019">2019</date>
</imprint>
</series>
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<front><div type="abstract" xml:lang="en"><p id="Par1">Accumulation of nucleotide building blocks prior to and during S phase facilitates DNA duplication. Herein, we find that the anaphase-promoting complex/cyclosome (APC/C) synchronizes ribose-5-phosphate levels and DNA synthesis during the cell cycle. In late G<sub>1</sub>
and S phases, transketolase-like 1 (TKTL1) is overexpressed and forms stable TKTL1-transketolase heterodimers that accumulate ribose-5-phosphate. This accumulation occurs by asymmetric production of ribose-5-phosphate from the non-oxidative pentose phosphate pathway and prevention of ribose-5-phosphate removal by depleting transketolase homodimers. In the G<sub>2</sub>
and M phases after DNA synthesis, expression of the APC/C adaptor CDH1 allows APC/C<sup>CDH1</sup>
to degrade D-box-containing TKTL1, abrogating ribose-5-phosphate accumulation by TKTL1. TKTL1-overexpressing cancer cells exhibit elevated ribose-5-phosphate levels. The low CDH1 or high TKTL1-induced accumulation of ribose-5-phosphate facilitates nucleotide and DNA synthesis as well as cell cycle progression in a ribose-5-phosphate-saturable manner. Here we reveal that the cell cycle control machinery regulates DNA synthesis by mediating ribose-5-phosphate sufficiency.</p>
</div>
</front>
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<author><name sortKey="Coy, Jf" uniqKey="Coy J">JF Coy</name>
</author>
<author><name sortKey="Lochelt, M" uniqKey="Lochelt M">M Lochelt</name>
</author>
</analytic>
</biblStruct>
</listBibl>
</div1>
</back>
</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Nat Commun</journal-id>
<journal-id journal-id-type="iso-abbrev">Nat Commun</journal-id>
<journal-title-group><journal-title>Nature Communications</journal-title>
</journal-title-group>
<issn pub-type="epub">2041-1723</issn>
<publisher><publisher-name>Nature Publishing Group UK</publisher-name>
<publisher-loc>London</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31175280</article-id>
<article-id pub-id-type="pmc">6555833</article-id>
<article-id pub-id-type="publisher-id">10375</article-id>
<article-id pub-id-type="doi">10.1038/s41467-019-10375-x</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>APC/C<sup>CDH1</sup>
synchronizes ribose-5-phosphate levels and DNA synthesis to cell cycle progression</article-title>
</title-group>
<contrib-group><contrib contrib-type="author" equal-contrib="yes"><name><surname>Li</surname>
<given-names>Yang</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="yes"><name><surname>Yao</surname>
<given-names>Cui-Fang</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-7900-5319</contrib-id>
<name><surname>Xu</surname>
<given-names>Fu-Jiang</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Qu</surname>
<given-names>Yuan-Yuan</given-names>
</name>
<xref ref-type="aff" rid="Aff3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Li</surname>
<given-names>Jia-Tao</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lin</surname>
<given-names>Yan</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Cao</surname>
<given-names>Zhong-Lian</given-names>
</name>
<xref ref-type="aff" rid="Aff4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lin</surname>
<given-names>Peng-Cheng</given-names>
</name>
<xref ref-type="aff" rid="Aff5">5</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Xu</surname>
<given-names>Wei</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
<xref ref-type="aff" rid="Aff6">6</xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Zhao</surname>
<given-names>Shi-Min</given-names>
</name>
<address><email>zhaosm@fudan.edu.cn</email>
</address>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
<xref ref-type="aff" rid="Aff6">6</xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Zhao</surname>
<given-names>Jian-Yuan</given-names>
</name>
<address><email>zhaojy@fudan.edu.cn</email>
</address>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
<xref ref-type="aff" rid="Aff6">6</xref>
</contrib>
<aff id="Aff1"><label>1</label>
<institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id>
<institution-id institution-id-type="GRID">grid.8547.e</institution-id>
<institution>Obstetrics & Gynecology Hospital of Fudan University, State Key Laboratory of Genetic Engineering, School of Life Sciences and Institutes of Biomedical Sciences,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 200438 P.R. China</aff>
<aff id="Aff2"><label>2</label>
<institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id>
<institution-id institution-id-type="GRID">grid.8547.e</institution-id>
<institution>Key Laboratory of Reproduction Regulation of NPFPC and Collaborative Innovation Center for Genetics and Development, Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 200438 P.R. China</aff>
<aff id="Aff3"><label>3</label>
<institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id>
<institution-id institution-id-type="GRID">grid.8547.e</institution-id>
<institution>Fudan University Shanghai Cancer Center,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 200438 P.R. China</aff>
<aff id="Aff4"><label>4</label>
<institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id>
<institution-id institution-id-type="GRID">grid.8547.e</institution-id>
<institution>School of Pharmacy,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 200438 P.R. China</aff>
<aff id="Aff5"><label>5</label>
<institution-wrap><institution-id institution-id-type="GRID">grid.443642.3</institution-id>
<institution>Key Laboratory for Tibet Plateau Phytochemistry of Qinghai Province, College of Pharmacy,</institution>
<institution>Qinghai University for Nationalities,</institution>
</institution-wrap>
Xining, 810007 P. R. China</aff>
<aff id="Aff6"><label>6</label>
<institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0807 1581</institution-id>
<institution-id institution-id-type="GRID">grid.13291.38</institution-id>
<institution>Collaborative Innovation Center for Biotherapy, West China Hospital,</institution>
<institution>Sichuan University,</institution>
</institution-wrap>
Chengdu, 610041 P.R. China</aff>
</contrib-group>
<pub-date pub-type="epub"><day>7</day>
<month>6</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>7</day>
<month>6</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="collection"><year>2019</year>
</pub-date>
<volume>10</volume>
<elocation-id>2502</elocation-id>
<history><date date-type="received"><day>21</day>
<month>4</month>
<year>2018</year>
</date>
<date date-type="accepted"><day>3</day>
<month>5</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>© The Author(s) 2019</copyright-statement>
<license license-type="OpenAccess"><license-p><bold>Open Access</bold>
This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit <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 id="Abs1"><p id="Par1">Accumulation of nucleotide building blocks prior to and during S phase facilitates DNA duplication. Herein, we find that the anaphase-promoting complex/cyclosome (APC/C) synchronizes ribose-5-phosphate levels and DNA synthesis during the cell cycle. In late G<sub>1</sub>
and S phases, transketolase-like 1 (TKTL1) is overexpressed and forms stable TKTL1-transketolase heterodimers that accumulate ribose-5-phosphate. This accumulation occurs by asymmetric production of ribose-5-phosphate from the non-oxidative pentose phosphate pathway and prevention of ribose-5-phosphate removal by depleting transketolase homodimers. In the G<sub>2</sub>
and M phases after DNA synthesis, expression of the APC/C adaptor CDH1 allows APC/C<sup>CDH1</sup>
to degrade D-box-containing TKTL1, abrogating ribose-5-phosphate accumulation by TKTL1. TKTL1-overexpressing cancer cells exhibit elevated ribose-5-phosphate levels. The low CDH1 or high TKTL1-induced accumulation of ribose-5-phosphate facilitates nucleotide and DNA synthesis as well as cell cycle progression in a ribose-5-phosphate-saturable manner. Here we reveal that the cell cycle control machinery regulates DNA synthesis by mediating ribose-5-phosphate sufficiency.</p>
</abstract>
<abstract id="Abs2" abstract-type="web-summary"><p id="Par2">Ribose-5-phosphate (R5P) is required for DNA synthesis, but how this is regulated during cell cycle progression is unclear. Here the authors report that the cell cycle regulator APC/C-CDH1 synchronizes cell cycle progression with R5P-derived DNA synthesis by controlling TKTL1 stability</p>
</abstract>
<kwd-group kwd-group-type="npg-subject"><title>Subject terms</title>
<kwd>Biochemistry</kwd>
<kwd>Cancer</kwd>
<kwd>Cell biology</kwd>
<kwd>Cell-cycle exit</kwd>
<kwd>Checkpoints</kwd>
</kwd-group>
<funding-group><award-group><funding-source><institution-wrap><institution-id institution-id-type="FundRef">https://doi.org/10.13039/501100001809</institution-id>
<institution>National Natural Science Foundation of China (National Science Foundation of China)</institution>
</institution-wrap>
</funding-source>
<award-id>31330023</award-id>
<principal-award-recipient><name><surname>Zhao</surname>
<given-names>Shi-Min</given-names>
</name>
</principal-award-recipient>
</award-group>
</funding-group>
<custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name>
<meta-value>© The Author(s) 2019</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>République populaire de Chine</li>
</country>
</list>
<tree><country name="République populaire de Chine"><noRegion><name sortKey="Li, Yang" sort="Li, Yang" uniqKey="Li Y" first="Yang" last="Li">Yang Li</name>
</noRegion>
<name sortKey="Cao, Zhong Lian" sort="Cao, Zhong Lian" uniqKey="Cao Z" first="Zhong-Lian" last="Cao">Zhong-Lian Cao</name>
<name sortKey="Li, Jia Tao" sort="Li, Jia Tao" uniqKey="Li J" first="Jia-Tao" last="Li">Jia-Tao Li</name>
<name sortKey="Li, Yang" sort="Li, Yang" uniqKey="Li Y" first="Yang" last="Li">Yang Li</name>
<name sortKey="Lin, Peng Cheng" sort="Lin, Peng Cheng" uniqKey="Lin P" first="Peng-Cheng" last="Lin">Peng-Cheng Lin</name>
<name sortKey="Lin, Yan" sort="Lin, Yan" uniqKey="Lin Y" first="Yan" last="Lin">Yan Lin</name>
<name sortKey="Lin, Yan" sort="Lin, Yan" uniqKey="Lin Y" first="Yan" last="Lin">Yan Lin</name>
<name sortKey="Qu, Yuan Yuan" sort="Qu, Yuan Yuan" uniqKey="Qu Y" first="Yuan-Yuan" last="Qu">Yuan-Yuan Qu</name>
<name sortKey="Xu, Fu Jiang" sort="Xu, Fu Jiang" uniqKey="Xu F" first="Fu-Jiang" last="Xu">Fu-Jiang Xu</name>
<name sortKey="Xu, Fu Jiang" sort="Xu, Fu Jiang" uniqKey="Xu F" first="Fu-Jiang" last="Xu">Fu-Jiang Xu</name>
<name sortKey="Xu, Wei" sort="Xu, Wei" uniqKey="Xu W" first="Wei" last="Xu">Wei Xu</name>
<name sortKey="Xu, Wei" sort="Xu, Wei" uniqKey="Xu W" first="Wei" last="Xu">Wei Xu</name>
<name sortKey="Xu, Wei" sort="Xu, Wei" uniqKey="Xu W" first="Wei" last="Xu">Wei Xu</name>
<name sortKey="Yao, Cui Fang" sort="Yao, Cui Fang" uniqKey="Yao C" first="Cui-Fang" last="Yao">Cui-Fang Yao</name>
<name sortKey="Zhao, Jian Yuan" sort="Zhao, Jian Yuan" uniqKey="Zhao J" first="Jian-Yuan" last="Zhao">Jian-Yuan Zhao</name>
<name sortKey="Zhao, Jian Yuan" sort="Zhao, Jian Yuan" uniqKey="Zhao J" first="Jian-Yuan" last="Zhao">Jian-Yuan Zhao</name>
<name sortKey="Zhao, Jian Yuan" sort="Zhao, Jian Yuan" uniqKey="Zhao J" first="Jian-Yuan" last="Zhao">Jian-Yuan Zhao</name>
<name sortKey="Zhao, Shi Min" sort="Zhao, Shi Min" uniqKey="Zhao S" first="Shi-Min" last="Zhao">Shi-Min Zhao</name>
<name sortKey="Zhao, Shi Min" sort="Zhao, Shi Min" uniqKey="Zhao S" first="Shi-Min" last="Zhao">Shi-Min Zhao</name>
<name sortKey="Zhao, Shi Min" sort="Zhao, Shi Min" uniqKey="Zhao S" first="Shi-Min" last="Zhao">Shi-Min Zhao</name>
</country>
</tree>
</affiliations>
</record>
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