Mitochondrial Phosphoenolpyruvate Carboxykinase Regulates Osteogenic Differentiation by Modulating AMPK/ULK1‐Dependent Autophagy
Identifieur interne : 000574 ( Pmc/Checkpoint ); précédent : 000573; suivant : 000575Mitochondrial Phosphoenolpyruvate Carboxykinase Regulates Osteogenic Differentiation by Modulating AMPK/ULK1‐Dependent Autophagy
Auteurs : Zheng Li ; Xuenan Liu ; Yuan Zhu ; Yangge Du ; Xuejiao Liu ; Longwei Lv ; Xiao Zhang ; Yunsong Liu ; Ping Zhang ; Yongsheng ZhouSource :
- Stem Cells (Dayton, Ohio) [ 1066-5099 ] ; 2019.
Abstract
Mitochondrial phosphoenolpyruvate carboxykinase (PCK2) is a rate‐limiting enzyme that plays critical roles in multiple physiological processes. The decompensation of PCK2 leads to various energy metabolic disorders. However, little is known regarding the effects of PCK2 on osteogenesis by human mesenchymal stem cells (hMSCs). Here, we report a novel function of PCK2 as a positive regulator of MSCs osteogenic differentiation. In addition to its well‐known role in anabolism, we demonstrate that PCK2 regulates autophagy. PCK2 deficiency significantly suppressed autophagy, leading to the impairment of osteogenic capacity of MSCs. On the other hand, autophagy was promoted by PCK2 overexpression; this was accompanied by increased osteogenic differentiation of MSCs. Moreover, PCK2 regulated osteogenic differentiation of MSCs via AMP‐activated protein kinase (AMPK)/unc‐51 like autophagy activating kinase 1(ULK1)‐dependent autophagy. Collectively, our present study unveiled a novel role for PCK2 in integrating autophagy and bone formation, providing a potential target for stem cell‐based bone tissue engineering that may lead to improved therapies for metabolic bone diseases.
Url:
DOI: 10.1002/stem.3091
PubMed: 31574189
PubMed Central: 6916635
Affiliations:
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Yangge" sort="Du, Yangge" uniqKey="Du Y" first="Yangge" last="Du">Yangge Du</name><affiliation><nlm:aff id="stem3091-aff-0001"></nlm:aff></affiliation><affiliation><nlm:aff id="stem3091-aff-0002"></nlm:aff></affiliation></author><author><name sortKey="Liu, Xuejiao" sort="Liu, Xuejiao" uniqKey="Liu X" first="Xuejiao" last="Liu">Xuejiao Liu</name><affiliation><nlm:aff id="stem3091-aff-0001"></nlm:aff></affiliation><affiliation><nlm:aff id="stem3091-aff-0002"></nlm:aff></affiliation></author><author><name sortKey="Lv, Longwei" sort="Lv, Longwei" uniqKey="Lv L" first="Longwei" last="Lv">Longwei Lv</name><affiliation><nlm:aff id="stem3091-aff-0001"></nlm:aff></affiliation><affiliation><nlm:aff id="stem3091-aff-0002"></nlm:aff></affiliation></author><author><name sortKey="Zhang, Xiao" sort="Zhang, Xiao" uniqKey="Zhang X" first="Xiao" last="Zhang">Xiao Zhang</name><affiliation><nlm:aff id="stem3091-aff-0001"></nlm:aff></affiliation><affiliation><nlm:aff id="stem3091-aff-0002"></nlm:aff></affiliation></author><author><name sortKey="Liu, Yunsong" sort="Liu, Yunsong" uniqKey="Liu Y" first="Yunsong" last="Liu">Yunsong Liu</name><affiliation><nlm:aff id="stem3091-aff-0001"></nlm:aff></affiliation><affiliation><nlm:aff id="stem3091-aff-0002"></nlm:aff></affiliation></author><author><name sortKey="Zhang, Ping" sort="Zhang, Ping" uniqKey="Zhang P" first="Ping" last="Zhang">Ping Zhang</name><affiliation><nlm:aff id="stem3091-aff-0001"></nlm:aff></affiliation><affiliation><nlm:aff id="stem3091-aff-0002"></nlm:aff></affiliation></author><author><name sortKey="Zhou, Yongsheng" sort="Zhou, Yongsheng" uniqKey="Zhou Y" first="Yongsheng" last="Zhou">Yongsheng Zhou</name><affiliation><nlm:aff id="stem3091-aff-0001"></nlm:aff></affiliation><affiliation><nlm:aff id="stem3091-aff-0002"></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31574189</idno><idno type="pmc">6916635</idno><idno 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id="stem3091-aff-0001"></nlm:aff></affiliation><affiliation><nlm:aff id="stem3091-aff-0002"></nlm:aff></affiliation></author><author><name sortKey="Liu, Xuenan" sort="Liu, Xuenan" uniqKey="Liu X" first="Xuenan" last="Liu">Xuenan Liu</name><affiliation><nlm:aff id="stem3091-aff-0001"></nlm:aff></affiliation><affiliation><nlm:aff id="stem3091-aff-0002"></nlm:aff></affiliation></author><author><name sortKey="Zhu, Yuan" sort="Zhu, Yuan" uniqKey="Zhu Y" first="Yuan" last="Zhu">Yuan Zhu</name><affiliation><nlm:aff id="stem3091-aff-0001"></nlm:aff></affiliation><affiliation><nlm:aff id="stem3091-aff-0002"></nlm:aff></affiliation></author><author><name sortKey="Du, Yangge" sort="Du, Yangge" uniqKey="Du Y" first="Yangge" last="Du">Yangge Du</name><affiliation><nlm:aff id="stem3091-aff-0001"></nlm:aff></affiliation><affiliation><nlm:aff id="stem3091-aff-0002"></nlm:aff></affiliation></author><author><name sortKey="Liu, Xuejiao" sort="Liu, Xuejiao" uniqKey="Liu X" first="Xuejiao" last="Liu">Xuejiao Liu</name><affiliation><nlm:aff id="stem3091-aff-0001"></nlm:aff></affiliation><affiliation><nlm:aff id="stem3091-aff-0002"></nlm:aff></affiliation></author><author><name sortKey="Lv, Longwei" sort="Lv, Longwei" uniqKey="Lv L" first="Longwei" last="Lv">Longwei Lv</name><affiliation><nlm:aff id="stem3091-aff-0001"></nlm:aff></affiliation><affiliation><nlm:aff id="stem3091-aff-0002"></nlm:aff></affiliation></author><author><name sortKey="Zhang, Xiao" sort="Zhang, Xiao" uniqKey="Zhang X" first="Xiao" last="Zhang">Xiao Zhang</name><affiliation><nlm:aff id="stem3091-aff-0001"></nlm:aff></affiliation><affiliation><nlm:aff id="stem3091-aff-0002"></nlm:aff></affiliation></author><author><name sortKey="Liu, Yunsong" sort="Liu, Yunsong" uniqKey="Liu Y" first="Yunsong" last="Liu">Yunsong Liu</name><affiliation><nlm:aff id="stem3091-aff-0001"></nlm:aff></affiliation><affiliation><nlm:aff id="stem3091-aff-0002"></nlm:aff></affiliation></author><author><name sortKey="Zhang, Ping" sort="Zhang, Ping" uniqKey="Zhang P" first="Ping" last="Zhang">Ping Zhang</name><affiliation><nlm:aff id="stem3091-aff-0001"></nlm:aff></affiliation><affiliation><nlm:aff id="stem3091-aff-0002"></nlm:aff></affiliation></author><author><name sortKey="Zhou, Yongsheng" sort="Zhou, Yongsheng" uniqKey="Zhou Y" first="Yongsheng" last="Zhou">Yongsheng Zhou</name><affiliation><nlm:aff id="stem3091-aff-0001"></nlm:aff></affiliation><affiliation><nlm:aff id="stem3091-aff-0002"></nlm:aff></affiliation></author></analytic><series><title level="j">Stem Cells (Dayton, Ohio)</title><idno type="ISSN">1066-5099</idno><idno type="eISSN">1549-4918</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Abstract</title><p>Mitochondrial phosphoenolpyruvate carboxykinase (PCK2) is a rate‐limiting enzyme that plays critical roles in multiple physiological processes. The decompensation of PCK2 leads to various energy metabolic disorders. However, little is known regarding the effects of PCK2 on osteogenesis by human mesenchymal stem cells (hMSCs). Here, we report a novel function of PCK2 as a positive regulator of MSCs osteogenic differentiation. In addition to its well‐known role in anabolism, we demonstrate that PCK2 regulates autophagy. PCK2 deficiency significantly suppressed autophagy, leading to the impairment of osteogenic capacity of MSCs. On the other hand, autophagy was promoted by PCK2 overexpression; this was accompanied by increased osteogenic differentiation of MSCs. Moreover, PCK2 regulated osteogenic differentiation of MSCs via AMP‐activated protein kinase (AMPK)/unc‐51 like autophagy activating kinase 1(ULK1)‐dependent autophagy. Collectively, our present study unveiled a novel role for PCK2 in integrating autophagy and bone formation, providing a potential target for stem cell‐based bone tissue engineering that may lead to improved therapies for metabolic bone diseases. <sc>stem cells</sc><italic>2019;37:1542–1555</italic></p></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></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">Stem Cells</journal-id><journal-id journal-id-type="iso-abbrev">Stem Cells</journal-id><journal-id journal-id-type="doi">10.1002/(ISSN)1549-4918</journal-id><journal-id journal-id-type="publisher-id">STEM</journal-id><journal-title-group><journal-title>Stem Cells (Dayton, Ohio)</journal-title></journal-title-group><issn pub-type="ppub">1066-5099</issn><issn pub-type="epub">1549-4918</issn><publisher><publisher-name>John Wiley & Sons, Inc.</publisher-name><publisher-loc>Hoboken, USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31574189</article-id><article-id pub-id-type="pmc">6916635</article-id><article-id pub-id-type="doi">10.1002/stem.3091</article-id><article-id pub-id-type="publisher-id">STEM3091</article-id><article-categories><subj-group subj-group-type="overline"><subject>Stem Cell Technology: Epigenetics, Genomics, Proteomics, and Metabonomics</subject></subj-group><subj-group subj-group-type="heading"><subject>Stem Cell Technology: Epigenetics, Genomics, Proteomics, and Metabonomics</subject></subj-group></article-categories><title-group><article-title>Mitochondrial Phosphoenolpyruvate Carboxykinase Regulates Osteogenic Differentiation by Modulating AMPK/ULK1‐Dependent Autophagy</article-title><alt-title alt-title-type="right-running-head">PCK2 Promotes Osteogenesis by MSCs via Autophagy</alt-title><alt-title alt-title-type="left-running-head">Li, Liu, Zhu et al.</alt-title></title-group><contrib-group><contrib id="stem3091-cr-0001" contrib-type="author"><name><surname>Li</surname><given-names>Zheng</given-names></name><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0003-0215-4401</contrib-id><xref ref-type="aff" rid="stem3091-aff-0001"><sup>1</sup></xref><xref ref-type="aff" rid="stem3091-aff-0002"><sup>2</sup></xref></contrib><contrib id="stem3091-cr-0002" contrib-type="author"><name><surname>Liu</surname><given-names>Xuenan</given-names></name><xref ref-type="aff" rid="stem3091-aff-0001"><sup>1</sup></xref><xref ref-type="aff" rid="stem3091-aff-0002"><sup>2</sup></xref></contrib><contrib id="stem3091-cr-0003" contrib-type="author"><name><surname>Zhu</surname><given-names>Yuan</given-names></name><xref ref-type="aff" rid="stem3091-aff-0001"><sup>1</sup></xref><xref ref-type="aff" rid="stem3091-aff-0002"><sup>2</sup></xref></contrib><contrib id="stem3091-cr-0004" contrib-type="author"><name><surname>Du</surname><given-names>Yangge</given-names></name><xref ref-type="aff" rid="stem3091-aff-0001"><sup>1</sup></xref><xref ref-type="aff" rid="stem3091-aff-0002"><sup>2</sup></xref></contrib><contrib id="stem3091-cr-0005" contrib-type="author"><name><surname>Liu</surname><given-names>Xuejiao</given-names></name><xref ref-type="aff" rid="stem3091-aff-0001"><sup>1</sup></xref><xref ref-type="aff" rid="stem3091-aff-0002"><sup>2</sup></xref></contrib><contrib id="stem3091-cr-0006" contrib-type="author"><name><surname>Lv</surname><given-names>Longwei</given-names></name><xref ref-type="aff" rid="stem3091-aff-0001"><sup>1</sup></xref><xref ref-type="aff" rid="stem3091-aff-0002"><sup>2</sup></xref></contrib><contrib id="stem3091-cr-0007" contrib-type="author"><name><surname>Zhang</surname><given-names>Xiao</given-names></name><xref ref-type="aff" rid="stem3091-aff-0001"><sup>1</sup></xref><xref ref-type="aff" rid="stem3091-aff-0002"><sup>2</sup></xref></contrib><contrib id="stem3091-cr-0008" contrib-type="author"><name><surname>Liu</surname><given-names>Yunsong</given-names></name><xref ref-type="aff" rid="stem3091-aff-0001"><sup>1</sup></xref><xref ref-type="aff" rid="stem3091-aff-0002"><sup>2</sup></xref></contrib><contrib id="stem3091-cr-0009" contrib-type="author" corresp="yes"><name><surname>Zhang</surname><given-names>Ping</given-names></name><xref ref-type="aff" rid="stem3091-aff-0001"><sup>1</sup></xref><xref ref-type="aff" rid="stem3091-aff-0002"><sup>2</sup></xref><address><email>zhangping332@bjmu.edu.cn</email></address></contrib><contrib id="stem3091-cr-0010" contrib-type="author" corresp="yes"><name><surname>Zhou</surname><given-names>Yongsheng</given-names></name><xref ref-type="aff" rid="stem3091-aff-0001"><sup>1</sup></xref><xref ref-type="aff" rid="stem3091-aff-0002"><sup>2</sup></xref><address><email>kqzhouysh@hsc.pku.edu.cn</email></address></contrib></contrib-group><aff id="stem3091-aff-0001"><label><sup>1</sup></label><named-content content-type="organisation-division">Department of Prosthodontics</named-content><institution>School and Hospital of Stomatology, Peking University</institution><city>Beijing</city><country country="CN">People's Republic of China</country></aff><aff id="stem3091-aff-0002"><label><sup>2</sup></label><named-content content-type="organisation-division">National Engineering Lab for Digital and Material Technology of Stomatology, National Clinical Research Center for Oral Diseases</named-content><institution>Peking University School and Hospital of Stomatology, Peking University</institution><city>Beijing</city><country country="CN">People's Republic of China</country></aff><author-notes><corresp id="correspondenceTo"><label>*</label>Correspondence: Ping Zhang, Ph.D., Department of Prosthodontics, Peking University School and Hospital of Stomatology, 22 Zhongguancun South Avenue, Haidian District, Beijing 100081, People's Republic of China. Telephone: 86‐10‐82195370; e‐mail: <email>zhangping332@bjmu.edu.cn</email>; or Yongsheng Zhou, D.D.S., Ph.D., Vice Dean of the School, Chair and Professor of Department of Prosthodontics, Peking University School and Hospital of Stomatology, 22 Zhongguancun South Avenue, Haidian District, Beijing 100081, People's Republic of China. Telephone: 86‐10‐82195370; e‐mail: <email>kqzhouysh@hsc.pku.edu.cn</email></corresp></author-notes><pub-date pub-type="epub"><day>14</day><month>10</month><year>2019</year></pub-date><pub-date pub-type="ppub"><month>12</month><year>2019</year></pub-date><volume>37</volume><issue>12</issue><issue-id pub-id-type="doi">10.1002/stem.v37.12</issue-id><fpage>1542</fpage><lpage>1555</lpage><history><date date-type="received"><day>05</day><month>3</month><year>2019</year></date><date date-type="accepted"><day>01</day><month>9</month><year>2019</year></date></history><permissions><pmc-comment> © 2019 AlphaMed Press </pmc-comment>
<copyright-statement content-type="article-copyright">©2019 The Authors. <sc>stem cells</sc> published by Wiley Periodicals, Inc. on behalf of AlphaMed Press 2019</copyright-statement><license license-type="creativeCommonsBy-nc"><license-p>This is an open access article under the terms of the <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> License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="file:STEM-37-1542.pdf"></self-uri><abstract><title>Abstract</title><p>Mitochondrial phosphoenolpyruvate carboxykinase (PCK2) is a rate‐limiting enzyme that plays critical roles in multiple physiological processes. The decompensation of PCK2 leads to various energy metabolic disorders. However, little is known regarding the effects of PCK2 on osteogenesis by human mesenchymal stem cells (hMSCs). Here, we report a novel function of PCK2 as a positive regulator of MSCs osteogenic differentiation. In addition to its well‐known role in anabolism, we demonstrate that PCK2 regulates autophagy. PCK2 deficiency significantly suppressed autophagy, leading to the impairment of osteogenic capacity of MSCs. On the other hand, autophagy was promoted by PCK2 overexpression; this was accompanied by increased osteogenic differentiation of MSCs. Moreover, PCK2 regulated osteogenic differentiation of MSCs via AMP‐activated protein kinase (AMPK)/unc‐51 like autophagy activating kinase 1(ULK1)‐dependent autophagy. Collectively, our present study unveiled a novel role for PCK2 in integrating autophagy and bone formation, providing a potential target for stem cell‐based bone tissue engineering that may lead to improved therapies for metabolic bone diseases. <sc>stem cells</sc><italic>2019;37:1542–1555</italic></p></abstract><abstract abstract-type="graphical"><p>The essential role of mitochondrial phosphoenolpyruvate carboxykinase (PCK2) in regulating gluconeogenesis and TCA cycle flux makes it indispensable for mesenchymal stem cells osteogenic differentiation, which is a nutrient‐consuming process. PCK2 regulates osteogenic differentiation of mesenchymal stem cells through modulating autophagy. The phosphorylation of AMP‐activated protein kinase (AMPK) and phosphorylation unc‐51 like autophagy activating kinase 1 (ULK1) are regulated by PCK2 during osteogenic differentiation, suggesting that AMPK/ULK1‐mediated autophagy is involved in the PCK2 regulated osteogenic capacity of mesenchymal stem cells.<boxed-text position="anchor" content-type="graphic" id="stem3091-blkfxd-0001" orientation="portrait"><graphic xlink:href="STEM-37-1542-g007.jpg" position="anchor" id="nlm-graphic-1" orientation="portrait"></graphic></boxed-text></p></abstract><kwd-group kwd-group-type="author-generated"><kwd id="stem3091-kwd-0001">Autophagy</kwd><kwd id="stem3091-kwd-0002">Mesenchymal stem cells</kwd><kwd id="stem3091-kwd-0004">Osteogenic differentiation</kwd><kwd id="stem3091-kwd-0003">Mitochondrial phosphoenolpyruvate carboxykinase</kwd></kwd-group><funding-group><award-group id="funding-0001"><funding-source><institution-wrap><institution>National Natural Science Foundation of China </institution><institution-id institution-id-type="open-funder-registry">10.13039/501100001809</institution-id></institution-wrap></funding-source><award-id>81870742</award-id></award-group><award-group id="funding-0002"><funding-source><institution-wrap><institution>Beijing Nova Program </institution><institution-id institution-id-type="open-funder-registry">10.13039/501100005090</institution-id></institution-wrap></funding-source><award-id>Z181100006218037</award-id></award-group><award-group id="funding-0003"><funding-source>Capital Culturing Project for Leading Talents in Scientific and Technological Innovation in Beijing</funding-source><award-id>Z171100001117169</award-id></award-group></funding-group><counts><fig-count count="6"></fig-count><table-count count="1"></table-count><page-count count="14"></page-count><word-count count="10501"></word-count></counts><custom-meta-group><custom-meta><meta-name>source-schema-version-number</meta-name><meta-value>2.0</meta-value></custom-meta><custom-meta><meta-name>cover-date</meta-name><meta-value>December 2019</meta-value></custom-meta><custom-meta><meta-name>details-of-publishers-convertor</meta-name><meta-value>Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.3 mode:remove_FC converted:17.12.2019</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc><affiliations><list></list><tree><noCountry><name sortKey="Du, Yangge" sort="Du, Yangge" uniqKey="Du Y" first="Yangge" last="Du">Yangge Du</name><name sortKey="Li, Zheng" sort="Li, Zheng" uniqKey="Li Z" first="Zheng" last="Li">Zheng Li</name><name sortKey="Liu, Xuejiao" sort="Liu, Xuejiao" uniqKey="Liu X" first="Xuejiao" last="Liu">Xuejiao Liu</name><name sortKey="Liu, Xuenan" sort="Liu, Xuenan" uniqKey="Liu X" first="Xuenan" last="Liu">Xuenan Liu</name><name sortKey="Liu, Yunsong" sort="Liu, Yunsong" uniqKey="Liu Y" first="Yunsong" last="Liu">Yunsong Liu</name><name sortKey="Lv, Longwei" sort="Lv, Longwei" uniqKey="Lv L" first="Longwei" last="Lv">Longwei Lv</name><name sortKey="Zhang, Ping" sort="Zhang, Ping" uniqKey="Zhang P" first="Ping" last="Zhang">Ping Zhang</name><name sortKey="Zhang, Xiao" sort="Zhang, Xiao" uniqKey="Zhang X" first="Xiao" last="Zhang">Xiao Zhang</name><name sortKey="Zhou, Yongsheng" sort="Zhou, Yongsheng" uniqKey="Zhou Y" first="Yongsheng" last="Zhou">Yongsheng Zhou</name><name sortKey="Zhu, Yuan" sort="Zhu, Yuan" uniqKey="Zhu Y" first="Yuan" last="Zhu">Yuan Zhu</name></noCountry></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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