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. Howev...

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Published inGenes & development Vol. 30; no. 23; pp. 2637 - 2648
Main Authors Kanatsu-Shinohara, Mito, Tanaka, Takashi, Ogonuki, Narumi, Ogura, Atsuo, Morimoto, Hiroko, Cheng, Pei Feng, Eisenman, Robert N., Trumpp, Andreas, Shinohara, Takashi
Format Journal Article
LanguageEnglish
Published United States Cold Spring Harbor Laboratory Press 01.12.2016
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
spermatogenesis
spermatogonial stem cells
self-renewal
Myc
glycolysis
Online AccessGet full text
ISSN0890-9369
1549-5477
DOI10.1101/gad.287045.116

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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. These results suggested that Myc -mediated glycolysis is an important factor that increases the frequency of SSC self-renewal division.
AbstractList 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.
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.
Here, Kanatsu-Shinohara et al. investigated the mechanisms underlying Myc regulation of spermatogonial stem cell (SSC) fate. Their findings suggest that Myc-mediated glycolysis is an important factor that increases the frequency of SSC self-renewal division. 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.
Author Cheng, Pei Feng
Ogonuki, Narumi
Ogura, Atsuo
Trumpp, Andreas
Morimoto, Hiroko
Shinohara, Takashi
Kanatsu-Shinohara, Mito
Eisenman, Robert N.
Tanaka, Takashi
AuthorAffiliation 2 Precursory Research for Embryonic Science and Technology (PRESTO), Japan Science and Technology Agency, Kyoto 606-8501, Japan
4 Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, Washington 98109, USA
5 Division of Stem Cells and Cancer, Deutsches Krebsforshungszentrum (DKFZ), 69120 Heidelberg, Germany
1 Department of Molecular Genetics, Graduate School of Medicine, Kyoto University, Kyoto 606-8501, Japan
3 Bioresource Center, RIKEN, Tsukuba 305-0074, Japan
AuthorAffiliation_xml – name: 2 Precursory Research for Embryonic Science and Technology (PRESTO), Japan Science and Technology Agency, Kyoto 606-8501, Japan
– name: 5 Division of Stem Cells and Cancer, Deutsches Krebsforshungszentrum (DKFZ), 69120 Heidelberg, Germany
– name: 1 Department of Molecular Genetics, Graduate School of Medicine, Kyoto University, Kyoto 606-8501, Japan
– name: 4 Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, Washington 98109, USA
– name: 3 Bioresource Center, RIKEN, Tsukuba 305-0074, Japan
Author_xml – sequence: 1
  givenname: Mito
  surname: Kanatsu-Shinohara
  fullname: Kanatsu-Shinohara, Mito
– sequence: 2
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  fullname: Tanaka, Takashi
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/28007786$$D View this record in MEDLINE/PubMed
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Issue 23
Keywords spermatogenesis
spermatogonial stem cells
self-renewal
Myc
glycolysis
Language English
License 2016 Kanatsu-Shinohara et al.; Published by Cold Spring Harbor Laboratory Press.
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SSID ssj0006066
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Snippet 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 plays critical roles in the self-renewal division of various stem cell types. In spermatogonial stem cells (SSCs), Myc controls SSC fate decisions because...
Here, Kanatsu-Shinohara et al. investigated the mechanisms underlying Myc regulation of spermatogonial stem cell (SSC) fate. Their findings suggest that...
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StartPage 2637
SubjectTerms 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
URI https://www.ncbi.nlm.nih.gov/pubmed/28007786
https://www.proquest.com/docview/1852781972
https://www.proquest.com/docview/1859472462
https://pubmed.ncbi.nlm.nih.gov/PMC5204355
Volume 30
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