A bioenergetic shift is required for spermatogonial differentiation
A bioenergetic balance between glycolysis and mitochondrial respiration is particularly important for stem cell fate specification. It however remains to be determined whether undifferentiated spermatogonia switch their preference for bioenergy production during differentiation. In this study, we fo...
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| Veröffentlicht in: | Cell discovery 2020-08, Vol.6 (1), p.56-56, Article 56 |
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| creator | Chen, Wei Zhang, Zhaoran Chang, Chingwen Yang, Zhichang Wang, Pengxiang Fu, Haihui Wei, Xiao Chen, Eric Tan, Suxu Huang, Wen Sun, Liangliang Ni, Ting Yang, Yi Wang, Yuan |
| description | A bioenergetic balance between glycolysis and mitochondrial respiration is particularly important for stem cell fate specification. It however remains to be determined whether undifferentiated spermatogonia switch their preference for bioenergy production during differentiation. In this study, we found that ATP generation in spermatogonia was gradually increased upon retinoic acid (RA)-induced differentiation. To accommodate this elevated energy demand, RA signaling concomitantly switched ATP production in spermatogonia from glycolysis to mitochondrial respiration, accompanied by increased levels of reactive oxygen species. Disrupting mitochondrial respiration significantly blocked spermatogonial differentiation. Inhibition of glucose conversion to glucose-6-phosphate or pentose phosphate pathway also repressed the formation of c-Kit
+
differentiating germ cells, suggesting that metabolites produced from glycolysis are required for spermatogonial differentiation. We further demonstrated that the expression levels of several metabolic regulators and enzymes were significantly altered upon RA-induced differentiation, with both RNA-seq and quantitative proteomic analyses. Taken together, our data unveil a critically regulated bioenergetic balance between glycolysis and mitochondrial respiration that is required for spermatogonial proliferation and differentiation. |
| doi_str_mv | 10.1038/s41421-020-0183-x |
| format | Article |
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+
differentiating germ cells, suggesting that metabolites produced from glycolysis are required for spermatogonial differentiation. We further demonstrated that the expression levels of several metabolic regulators and enzymes were significantly altered upon RA-induced differentiation, with both RNA-seq and quantitative proteomic analyses. Taken together, our data unveil a critically regulated bioenergetic balance between glycolysis and mitochondrial respiration that is required for spermatogonial proliferation and differentiation.</description><identifier>ISSN: 2056-5968</identifier><identifier>EISSN: 2056-5968</identifier><identifier>DOI: 10.1038/s41421-020-0183-x</identifier><identifier>PMID: 32864161</identifier><language>eng</language><publisher>Singapore: Springer Singapore</publisher><subject>631/136/532 ; 631/80 ; Bioenergetics ; Biomedical and Life Sciences ; c-Kit protein ; Cell Biology ; Cell Culture ; Cell Cycle Analysis ; Cell differentiation ; Cell fate ; Cell Physiology ; Electron transport ; Germ cells ; Glycolysis ; Life Sciences ; Metabolites ; Mitochondria ; Pentose phosphate pathway ; Reactive oxygen species ; Respiration ; Retinoic acid ; Ribonucleic acid ; RNA ; Spermatogonia ; Stem Cells</subject><ispartof>Cell discovery, 2020-08, Vol.6 (1), p.56-56, Article 56</ispartof><rights>The Author(s) 2020</rights><rights>The Author(s) 2020. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c447t-2b552e8513246d560cf75351116ac54043b953057ffcf4c9ee94de8bb536b43a3</citedby><cites>FETCH-LOGICAL-c447t-2b552e8513246d560cf75351116ac54043b953057ffcf4c9ee94de8bb536b43a3</cites><orcidid>0000-0001-7896-1184 ; 0000-0002-0939-1269</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7431567/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7431567/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,27923,27924,41119,42188,51575,53790,53792</link.rule.ids></links><search><creatorcontrib>Chen, Wei</creatorcontrib><creatorcontrib>Zhang, Zhaoran</creatorcontrib><creatorcontrib>Chang, Chingwen</creatorcontrib><creatorcontrib>Yang, Zhichang</creatorcontrib><creatorcontrib>Wang, Pengxiang</creatorcontrib><creatorcontrib>Fu, Haihui</creatorcontrib><creatorcontrib>Wei, Xiao</creatorcontrib><creatorcontrib>Chen, Eric</creatorcontrib><creatorcontrib>Tan, Suxu</creatorcontrib><creatorcontrib>Huang, Wen</creatorcontrib><creatorcontrib>Sun, Liangliang</creatorcontrib><creatorcontrib>Ni, Ting</creatorcontrib><creatorcontrib>Yang, Yi</creatorcontrib><creatorcontrib>Wang, Yuan</creatorcontrib><title>A bioenergetic shift is required for spermatogonial differentiation</title><title>Cell discovery</title><addtitle>Cell Discov</addtitle><description>A bioenergetic balance between glycolysis and mitochondrial respiration is particularly important for stem cell fate specification. It however remains to be determined whether undifferentiated spermatogonia switch their preference for bioenergy production during differentiation. In this study, we found that ATP generation in spermatogonia was gradually increased upon retinoic acid (RA)-induced differentiation. To accommodate this elevated energy demand, RA signaling concomitantly switched ATP production in spermatogonia from glycolysis to mitochondrial respiration, accompanied by increased levels of reactive oxygen species. Disrupting mitochondrial respiration significantly blocked spermatogonial differentiation. Inhibition of glucose conversion to glucose-6-phosphate or pentose phosphate pathway also repressed the formation of c-Kit
+
differentiating germ cells, suggesting that metabolites produced from glycolysis are required for spermatogonial differentiation. We further demonstrated that the expression levels of several metabolic regulators and enzymes were significantly altered upon RA-induced differentiation, with both RNA-seq and quantitative proteomic analyses. Taken together, our data unveil a critically regulated bioenergetic balance between glycolysis and mitochondrial respiration that is required for spermatogonial proliferation and differentiation.</description><subject>631/136/532</subject><subject>631/80</subject><subject>Bioenergetics</subject><subject>Biomedical and Life Sciences</subject><subject>c-Kit protein</subject><subject>Cell Biology</subject><subject>Cell Culture</subject><subject>Cell Cycle Analysis</subject><subject>Cell differentiation</subject><subject>Cell fate</subject><subject>Cell Physiology</subject><subject>Electron transport</subject><subject>Germ cells</subject><subject>Glycolysis</subject><subject>Life Sciences</subject><subject>Metabolites</subject><subject>Mitochondria</subject><subject>Pentose phosphate pathway</subject><subject>Reactive oxygen species</subject><subject>Respiration</subject><subject>Retinoic acid</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Spermatogonia</subject><subject>Stem Cells</subject><issn>2056-5968</issn><issn>2056-5968</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp1kUtLxDAUhYMoKuoPcFdw46aam1fTjSCDLxDc6Dqk6c0Y6TRj0or-ezvM4Atc3Qv3O4dzOYQcAz0DyvV5FiAYlJTRkoLm5fsW2WdUqlLWSm__2PfIUc4vlFKQTGstd8keZ1oJULBPZpdFEyL2mOY4BFfk5-CHIuQi4esYEraFj6nIS0wLO8R57IPtijZ4jwn7IdghxP6Q7HjbZTzazAPydH31OLst7x9u7maX96UTohpK1kjJUEvgTKhWKup8JbkEAGWdFFTwppacysp754WrEWvRom4ayVUjuOUH5GLtuxybBbZuCpBsZ5YpLGz6MNEG8_vSh2czj2-mEhykqiaD041Biq8j5sEsQnbYdbbHOGbDBNd1zRRTE3ryB32JY-qn91aUUFBpqCcK1pRLMeeE_isMULNqyaxbMlNLZtWSeZ80bK3JE9vPMX07_y_6BLknk70</recordid><startdate>20200818</startdate><enddate>20200818</enddate><creator>Chen, Wei</creator><creator>Zhang, Zhaoran</creator><creator>Chang, Chingwen</creator><creator>Yang, Zhichang</creator><creator>Wang, Pengxiang</creator><creator>Fu, Haihui</creator><creator>Wei, Xiao</creator><creator>Chen, Eric</creator><creator>Tan, Suxu</creator><creator>Huang, Wen</creator><creator>Sun, Liangliang</creator><creator>Ni, Ting</creator><creator>Yang, Yi</creator><creator>Wang, Yuan</creator><general>Springer Singapore</general><general>Springer Nature B.V</general><scope>C6C</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-7896-1184</orcidid><orcidid>https://orcid.org/0000-0002-0939-1269</orcidid></search><sort><creationdate>20200818</creationdate><title>A bioenergetic shift is required for spermatogonial differentiation</title><author>Chen, Wei ; Zhang, Zhaoran ; Chang, Chingwen ; Yang, Zhichang ; Wang, Pengxiang ; Fu, Haihui ; Wei, Xiao ; Chen, Eric ; Tan, Suxu ; Huang, Wen ; Sun, Liangliang ; Ni, Ting ; Yang, Yi ; Wang, Yuan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c447t-2b552e8513246d560cf75351116ac54043b953057ffcf4c9ee94de8bb536b43a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>631/136/532</topic><topic>631/80</topic><topic>Bioenergetics</topic><topic>Biomedical and Life Sciences</topic><topic>c-Kit protein</topic><topic>Cell Biology</topic><topic>Cell Culture</topic><topic>Cell Cycle Analysis</topic><topic>Cell differentiation</topic><topic>Cell fate</topic><topic>Cell Physiology</topic><topic>Electron transport</topic><topic>Germ cells</topic><topic>Glycolysis</topic><topic>Life Sciences</topic><topic>Metabolites</topic><topic>Mitochondria</topic><topic>Pentose phosphate pathway</topic><topic>Reactive oxygen species</topic><topic>Respiration</topic><topic>Retinoic acid</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>Spermatogonia</topic><topic>Stem Cells</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chen, Wei</creatorcontrib><creatorcontrib>Zhang, Zhaoran</creatorcontrib><creatorcontrib>Chang, Chingwen</creatorcontrib><creatorcontrib>Yang, Zhichang</creatorcontrib><creatorcontrib>Wang, Pengxiang</creatorcontrib><creatorcontrib>Fu, Haihui</creatorcontrib><creatorcontrib>Wei, Xiao</creatorcontrib><creatorcontrib>Chen, Eric</creatorcontrib><creatorcontrib>Tan, Suxu</creatorcontrib><creatorcontrib>Huang, Wen</creatorcontrib><creatorcontrib>Sun, Liangliang</creatorcontrib><creatorcontrib>Ni, Ting</creatorcontrib><creatorcontrib>Yang, Yi</creatorcontrib><creatorcontrib>Wang, Yuan</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>ProQuest Health and Medical</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>ProQuest Biological Science Journals</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Cell discovery</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chen, Wei</au><au>Zhang, Zhaoran</au><au>Chang, Chingwen</au><au>Yang, Zhichang</au><au>Wang, Pengxiang</au><au>Fu, Haihui</au><au>Wei, Xiao</au><au>Chen, Eric</au><au>Tan, Suxu</au><au>Huang, Wen</au><au>Sun, Liangliang</au><au>Ni, Ting</au><au>Yang, Yi</au><au>Wang, Yuan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A bioenergetic shift is required for spermatogonial differentiation</atitle><jtitle>Cell discovery</jtitle><stitle>Cell Discov</stitle><date>2020-08-18</date><risdate>2020</risdate><volume>6</volume><issue>1</issue><spage>56</spage><epage>56</epage><pages>56-56</pages><artnum>56</artnum><issn>2056-5968</issn><eissn>2056-5968</eissn><abstract>A bioenergetic balance between glycolysis and mitochondrial respiration is particularly important for stem cell fate specification. It however remains to be determined whether undifferentiated spermatogonia switch their preference for bioenergy production during differentiation. In this study, we found that ATP generation in spermatogonia was gradually increased upon retinoic acid (RA)-induced differentiation. To accommodate this elevated energy demand, RA signaling concomitantly switched ATP production in spermatogonia from glycolysis to mitochondrial respiration, accompanied by increased levels of reactive oxygen species. Disrupting mitochondrial respiration significantly blocked spermatogonial differentiation. Inhibition of glucose conversion to glucose-6-phosphate or pentose phosphate pathway also repressed the formation of c-Kit
+
differentiating germ cells, suggesting that metabolites produced from glycolysis are required for spermatogonial differentiation. We further demonstrated that the expression levels of several metabolic regulators and enzymes were significantly altered upon RA-induced differentiation, with both RNA-seq and quantitative proteomic analyses. Taken together, our data unveil a critically regulated bioenergetic balance between glycolysis and mitochondrial respiration that is required for spermatogonial proliferation and differentiation.</abstract><cop>Singapore</cop><pub>Springer Singapore</pub><pmid>32864161</pmid><doi>10.1038/s41421-020-0183-x</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0001-7896-1184</orcidid><orcidid>https://orcid.org/0000-0002-0939-1269</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | 631/136/532 631/80 Bioenergetics Biomedical and Life Sciences c-Kit protein Cell Biology Cell Culture Cell Cycle Analysis Cell differentiation Cell fate Cell Physiology Electron transport Germ cells Glycolysis Life Sciences Metabolites Mitochondria Pentose phosphate pathway Reactive oxygen species Respiration Retinoic acid Ribonucleic acid RNA Spermatogonia Stem Cells |
| title | A bioenergetic shift is required for spermatogonial differentiation |
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