Myc/Mycn-mediated glycolysis enhances mouse spermatogonial stem cell self-renewal
Myc plays critical roles in the self-renewal division of various stem cell types. In spermatogonial stem cells (SSCs), Myc controls SSC fate decisions because Myc overexpression induces enhanced self-renewal division, while depletion of Max, a Myc-binding partner, leads to meiotic induction. However...
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| Veröffentlicht in: | Genes & development 2016-12, Vol.30 (23), p.2637-2648 |
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| creator | Kanatsu-Shinohara, Mito Tanaka, Takashi Ogonuki, Narumi Ogura, Atsuo Morimoto, Hiroko Cheng, Pei Feng Eisenman, Robert N Trumpp, Andreas Shinohara, Takashi |
| description | Myc plays critical roles in the self-renewal division of various stem cell types. In spermatogonial stem cells (SSCs), Myc controls SSC fate decisions because Myc overexpression induces enhanced self-renewal division, while depletion of Max, a Myc-binding partner, leads to meiotic induction. However, the mechanism by which Myc acts on SSC fate is unclear. Here we demonstrate a critical link between Myc/Mycn gene activity and glycolysis in SSC self-renewal. In SSCs, Myc/Mycn are regulated by Foxo1, whose deficiency impairs SSC self-renewal. Myc/Mycn-deficient SSCs not only undergo limited self-renewal division but also display diminished glycolytic activity. While inhibition of glycolysis decreased SSC activity, chemical stimulation of glycolysis or transfection of active Akt1 or Pdpk1 (phosphoinositide-dependent protein kinase 1 ) augmented self-renewal division, and long-term SSC cultures were derived from a nonpermissive strain that showed limited self-renewal division. These results suggested that Myc-mediated glycolysis is an important factor that increases the frequency of SSC self-renewal division. |
| doi_str_mv | 10.1101/gad.287045.116 |
| format | Article |
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In spermatogonial stem cells (SSCs), Myc controls SSC fate decisions because Myc overexpression induces enhanced self-renewal division, while depletion of Max, a Myc-binding partner, leads to meiotic induction. However, the mechanism by which Myc acts on SSC fate is unclear. Here we demonstrate a critical link between Myc/Mycn gene activity and glycolysis in SSC self-renewal. In SSCs, Myc/Mycn are regulated by Foxo1, whose deficiency impairs SSC self-renewal. Myc/Mycn-deficient SSCs not only undergo limited self-renewal division but also display diminished glycolytic activity. While inhibition of glycolysis decreased SSC activity, chemical stimulation of glycolysis or transfection of active Akt1 or Pdpk1 (phosphoinositide-dependent protein kinase 1 ) augmented self-renewal division, and long-term SSC cultures were derived from a nonpermissive strain that showed limited self-renewal division. These results suggested that Myc-mediated glycolysis is an important factor that increases the frequency of SSC self-renewal division.</description><identifier>ISSN: 0890-9369</identifier><identifier>EISSN: 1549-5477</identifier><identifier>DOI: 10.1101/gad.287045.116</identifier><identifier>PMID: 28007786</identifier><language>eng</language><publisher>United States: Cold Spring Harbor Laboratory Press</publisher><subject>3-Phosphoinositide-Dependent Protein Kinases - metabolism ; Animals ; Cell Division - genetics ; Cell Proliferation - genetics ; Cell Self Renewal - genetics ; Gene Expression Regulation, Developmental - genetics ; Gene Knockout Techniques ; Glycolysis - genetics ; Male ; Mice ; Mice, Inbred C57BL ; N-Myc Proto-Oncogene Protein - genetics ; N-Myc Proto-Oncogene Protein - metabolism ; Proto-Oncogene Proteins c-myc - genetics ; Proto-Oncogene Proteins c-myc - metabolism ; Research Paper ; RNA Splicing Factors - metabolism ; Spermatogonia - cytology ; Stem Cells - enzymology ; Stem Cells - metabolism</subject><ispartof>Genes & development, 2016-12, Vol.30 (23), p.2637-2648</ispartof><rights>2016 Kanatsu-Shinohara et al.; Published by Cold Spring Harbor Laboratory Press.</rights><rights>2016</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c533t-f3780bc6255baa51dd503873452b5c57fce89dfb87da2bf48a0e3c8a2102824b3</citedby><cites>FETCH-LOGICAL-c533t-f3780bc6255baa51dd503873452b5c57fce89dfb87da2bf48a0e3c8a2102824b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5204355/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5204355/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,886,27926,27927,53793,53795</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28007786$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kanatsu-Shinohara, Mito</creatorcontrib><creatorcontrib>Tanaka, Takashi</creatorcontrib><creatorcontrib>Ogonuki, Narumi</creatorcontrib><creatorcontrib>Ogura, Atsuo</creatorcontrib><creatorcontrib>Morimoto, Hiroko</creatorcontrib><creatorcontrib>Cheng, Pei Feng</creatorcontrib><creatorcontrib>Eisenman, Robert N</creatorcontrib><creatorcontrib>Trumpp, Andreas</creatorcontrib><creatorcontrib>Shinohara, Takashi</creatorcontrib><title>Myc/Mycn-mediated glycolysis enhances mouse spermatogonial stem cell self-renewal</title><title>Genes & development</title><addtitle>Genes Dev</addtitle><description>Myc plays critical roles in the self-renewal division of various stem cell types. In spermatogonial stem cells (SSCs), Myc controls SSC fate decisions because Myc overexpression induces enhanced self-renewal division, while depletion of Max, a Myc-binding partner, leads to meiotic induction. However, the mechanism by which Myc acts on SSC fate is unclear. Here we demonstrate a critical link between Myc/Mycn gene activity and glycolysis in SSC self-renewal. In SSCs, Myc/Mycn are regulated by Foxo1, whose deficiency impairs SSC self-renewal. Myc/Mycn-deficient SSCs not only undergo limited self-renewal division but also display diminished glycolytic activity. While inhibition of glycolysis decreased SSC activity, chemical stimulation of glycolysis or transfection of active Akt1 or Pdpk1 (phosphoinositide-dependent protein kinase 1 ) augmented self-renewal division, and long-term SSC cultures were derived from a nonpermissive strain that showed limited self-renewal division. These results suggested that Myc-mediated glycolysis is an important factor that increases the frequency of SSC self-renewal division.</description><subject>3-Phosphoinositide-Dependent Protein Kinases - metabolism</subject><subject>Animals</subject><subject>Cell Division - genetics</subject><subject>Cell Proliferation - genetics</subject><subject>Cell Self Renewal - genetics</subject><subject>Gene Expression Regulation, Developmental - genetics</subject><subject>Gene Knockout Techniques</subject><subject>Glycolysis - genetics</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>N-Myc Proto-Oncogene Protein - genetics</subject><subject>N-Myc Proto-Oncogene Protein - metabolism</subject><subject>Proto-Oncogene Proteins c-myc - genetics</subject><subject>Proto-Oncogene Proteins c-myc - metabolism</subject><subject>Research Paper</subject><subject>RNA Splicing Factors - metabolism</subject><subject>Spermatogonia - cytology</subject><subject>Stem Cells - enzymology</subject><subject>Stem Cells - metabolism</subject><issn>0890-9369</issn><issn>1549-5477</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNUctKA0EQHETR-Lh6lD162aTnPXsRJPiCiAh6HmZne5OVfcSdjZK_d0Ki6M1D0910dVFFEXJOYUwp0MncFWNmNAgZd7VHRlSKLJVC630yApNBmnGVHZHjEN4AQIFSh-SIGQCtjRqR58e1n8Rq0waLyg1YJPN67bt6HaqQYLtwrceQNN0qYBKW2Ddu6OZdW7k6CQM2icc6TliXaY8tfrr6lByUrg54tusn5PX25mV6n86e7h6m17PUS86HtOTaQO4VkzJ3TtKikMCN5kKyXHqpS48mK8rc6MKxvBTGAXJvHKPADBM5PyFXW97lKo_aPbZD72q77KvG9Wvbucr-vbTVws67DysZCC5lJLjcEfTd-wrDYJsqbOy4FqNdS43MhGZCsf9AmTY00xvoeAv1fRdCj-WPIgp2E5mNkdltZHFX8eHit48f-HdG_AuuiJPP</recordid><startdate>20161201</startdate><enddate>20161201</enddate><creator>Kanatsu-Shinohara, Mito</creator><creator>Tanaka, Takashi</creator><creator>Ogonuki, Narumi</creator><creator>Ogura, Atsuo</creator><creator>Morimoto, Hiroko</creator><creator>Cheng, Pei Feng</creator><creator>Eisenman, Robert N</creator><creator>Trumpp, Andreas</creator><creator>Shinohara, Takashi</creator><general>Cold Spring Harbor Laboratory Press</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>5PM</scope></search><sort><creationdate>20161201</creationdate><title>Myc/Mycn-mediated glycolysis enhances mouse spermatogonial stem cell self-renewal</title><author>Kanatsu-Shinohara, Mito ; Tanaka, Takashi ; Ogonuki, Narumi ; Ogura, Atsuo ; Morimoto, Hiroko ; Cheng, Pei Feng ; Eisenman, Robert N ; Trumpp, Andreas ; Shinohara, Takashi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c533t-f3780bc6255baa51dd503873452b5c57fce89dfb87da2bf48a0e3c8a2102824b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>3-Phosphoinositide-Dependent Protein Kinases - metabolism</topic><topic>Animals</topic><topic>Cell Division - genetics</topic><topic>Cell Proliferation - genetics</topic><topic>Cell Self Renewal - genetics</topic><topic>Gene Expression Regulation, Developmental - genetics</topic><topic>Gene Knockout Techniques</topic><topic>Glycolysis - genetics</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>N-Myc Proto-Oncogene Protein - genetics</topic><topic>N-Myc Proto-Oncogene Protein - metabolism</topic><topic>Proto-Oncogene Proteins c-myc - genetics</topic><topic>Proto-Oncogene Proteins c-myc - metabolism</topic><topic>Research Paper</topic><topic>RNA Splicing Factors - metabolism</topic><topic>Spermatogonia - cytology</topic><topic>Stem Cells - enzymology</topic><topic>Stem Cells - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kanatsu-Shinohara, Mito</creatorcontrib><creatorcontrib>Tanaka, Takashi</creatorcontrib><creatorcontrib>Ogonuki, Narumi</creatorcontrib><creatorcontrib>Ogura, Atsuo</creatorcontrib><creatorcontrib>Morimoto, Hiroko</creatorcontrib><creatorcontrib>Cheng, Pei Feng</creatorcontrib><creatorcontrib>Eisenman, Robert N</creatorcontrib><creatorcontrib>Trumpp, Andreas</creatorcontrib><creatorcontrib>Shinohara, Takashi</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genes & development</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kanatsu-Shinohara, Mito</au><au>Tanaka, Takashi</au><au>Ogonuki, Narumi</au><au>Ogura, Atsuo</au><au>Morimoto, Hiroko</au><au>Cheng, Pei Feng</au><au>Eisenman, Robert N</au><au>Trumpp, Andreas</au><au>Shinohara, Takashi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Myc/Mycn-mediated glycolysis enhances mouse spermatogonial stem cell self-renewal</atitle><jtitle>Genes & development</jtitle><addtitle>Genes Dev</addtitle><date>2016-12-01</date><risdate>2016</risdate><volume>30</volume><issue>23</issue><spage>2637</spage><epage>2648</epage><pages>2637-2648</pages><issn>0890-9369</issn><eissn>1549-5477</eissn><abstract>Myc plays critical roles in the self-renewal division of various stem cell types. In spermatogonial stem cells (SSCs), Myc controls SSC fate decisions because Myc overexpression induces enhanced self-renewal division, while depletion of Max, a Myc-binding partner, leads to meiotic induction. However, the mechanism by which Myc acts on SSC fate is unclear. Here we demonstrate a critical link between Myc/Mycn gene activity and glycolysis in SSC self-renewal. In SSCs, Myc/Mycn are regulated by Foxo1, whose deficiency impairs SSC self-renewal. Myc/Mycn-deficient SSCs not only undergo limited self-renewal division but also display diminished glycolytic activity. While inhibition of glycolysis decreased SSC activity, chemical stimulation of glycolysis or transfection of active Akt1 or Pdpk1 (phosphoinositide-dependent protein kinase 1 ) augmented self-renewal division, and long-term SSC cultures were derived from a nonpermissive strain that showed limited self-renewal division. 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| subjects | 3-Phosphoinositide-Dependent Protein Kinases - metabolism Animals Cell Division - genetics Cell Proliferation - genetics Cell Self Renewal - genetics Gene Expression Regulation, Developmental - genetics Gene Knockout Techniques Glycolysis - genetics Male Mice Mice, Inbred C57BL N-Myc Proto-Oncogene Protein - genetics N-Myc Proto-Oncogene Protein - metabolism Proto-Oncogene Proteins c-myc - genetics Proto-Oncogene Proteins c-myc - metabolism Research Paper RNA Splicing Factors - metabolism Spermatogonia - cytology Stem Cells - enzymology Stem Cells - metabolism |
| title | Myc/Mycn-mediated glycolysis enhances mouse spermatogonial stem cell self-renewal |
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