Quantitative analysis of male germline stem cell differentiation reveals a role for the p53-mTORC1 pathway in spermatogonial maintenance

References

• Ma XM, Blenis J. Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 2009; 10:307-18; PMID:19339977; http://dx.doi.org/10.1038/nrm2672
   PubMed Web of Science ®Google Scholar
• Yilmaz OH, Valdez R, Theisen BK, Guo W, Ferguson DO, Wu H, Morrison SJ. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature 2006; 441:475-82; PMID:16598206; http://dx.doi.org/10.1038/nature04703
   PubMed Web of Science ®Google Scholar
• Chen C, Liu Y, Liu R, Ikenoue T, Guan KL, Liu Y, Zheng P. TSC-mTOR maintains quiescence and function of hematopoietic stem cells by repressing mitochondrial biogenesis and reactive oxygen species. J Exp Med 2008; 205:2397-408; PMID:18809716; http://dx.doi.org/10.1084/jem.20081297
   PubMed Web of Science ®Google Scholar
• Magri L, Galli R. mTOR signaling in neural stem cells: from basic biology to disease. Cell Mol Life Sci 2013; 70:2887-98; PMID:23124271; http://dx.doi.org/10.1007/s00018-012-1196-x
   PubMed Web of Science ®Google Scholar
• Xiang X, Zhao J, Xu G, Li Y, Zhang W. mTOR and the differentiation of mesenchymal stem cells. Acta Biochim Biophys Sin (Shanghai) 2011; 43:501-10; PMID:21642276; http://dx.doi.org/10.1093/abbs/gmr041
   PubMed Web of Science ®Google Scholar
• Castilho RM, Squarize CH, Chodosh LA, Williams BO, Gutkind JS. mTOR mediates Wnt-induced epidermal stem cell exhaustion and aging. Cell Stem Cell 2009; 5:279-89; PMID:19733540; http://dx.doi.org/10.1016/j.stem.2009.06.017
   PubMed Web of Science ®Google Scholar
• Buaas FW, Kirsh AL, Sharma M, McLean DJ, Morris JL, Griswold MD, de Rooij DG, Braun RE. Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet 2004; 36:647-52; PMID:15156142; http://dx.doi.org/10.1038/ng1366
   PubMed Web of Science ®Google Scholar
• Costoya JA, Hobbs RM, Barna M, Cattoretti G, Manova K, Sukhwani M, Orwig KE, Wolgemuth DJ, Pandolfi PP. Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 2004; 36:653-9; PMID:15156143; http://dx.doi.org/10.1038/ng1367
   PubMed Web of Science ®Google Scholar
• Hobbs RM, Seandel M, Falciatori I, Rafii S, Pandolfi PP. Plzf regulates germline progenitor self-renewal by opposing mTORC1. Cell 2010; 142:468-79; PMID:20691905; http://dx.doi.org/10.1016/j.cell.2010.06.041
   PubMed Web of Science ®Google Scholar
• Hobbs RM, La HM, Makela JA, Kobayashi T, Noda T, Pandolfi PP. Distinct germline progenitor subsets defined through Tsc2-mTORC1 signaling. EMBO Rep 2015; 16:467-80; PMID:25700280; http://dx.doi.org/10.15252/embr.201439379
   PubMed Web of Science ®Google Scholar
• Lane DP. Cancer. p53, guardian of the genome. Nature 1992; 358:15-6; PMID:1614522; http://dx.doi.org/10.1038/358015a0
   PubMed Web of Science ®Google Scholar
• Bieging KT, Mello SS, Attardi LD. Unravelling mechanisms of p53-mediated tumour suppression. Nat Rev Cancer 2014; 14:359-70; PMID:24739573; http://dx.doi.org/10.1038/nrc3711
   PubMed Web of Science ®Google Scholar
• Solozobova V, Blattner C. p53 in stem cells. World J Biol Chem 2011; 2:202-14; PMID:21949570; http://dx.doi.org/10.4331/wjbc.v2.i9.202
   PubMedGoogle Scholar
• Hasty P, Sharp ZD, Curiel TJ, Campisi J. mTORC1 and p53: clash of the gods? Cell Cycle 2013; 12:20-5; PMID:23255104; http://dx.doi.org/10.4161/cc.22912
   PubMed Web of Science ®Google Scholar
• Korotchkina LG, Leontieva OV, Bukreeva EI, Demidenko ZN, Gudkov AV, Blagosklonny MV. The choice between p53-induced senescence and quiescence is determined in part by the mTOR pathway. Aging (Albany NY) 2010; 2:344-52; PMID:20606252
   PubMedGoogle Scholar
• Levine AJ, Harris CR, Puzio-Kuter AM. The interfaces between signal transduction pathways: IGF-1/mTor, p53 and the Parkinson Disease pathway. Oncotarget 2012; 3:1301-7; PMID:23211569
   PubMed Web of Science ®Google Scholar
• Leontieva OV, Novototskaya LR, Paszkiewicz GM, Komarova EA, Gudkov AV, Blagosklonny MV. Dysregulation of the mTOR pathway in p53-deficient mice. Cancer Biol Ther 2013; 14:1182-8; PMID:24184801; http://dx.doi.org/10.4161/cbt.26947
   PubMed Web of Science ®Google Scholar
• Oatley JM, Brinster RL. Regulation of spermatogonial stem cell self-renewal in mammals. Annu Rev Cell Dev Biol 2008; 24:263-86; PMID:18588486; http://dx.doi.org/10.1146/annurev.cellbio.24.110707.175355
   PubMed Web of Science ®Google Scholar
• de Rooij DG, Russell LD. All you wanted to know about spermatogonia but were afraid to ask. J Androl 2000; 21:776-98; PMID:11105904
   PubMed Web of Science ®Google Scholar
• Buageaw A, Sukhwani M, Ben-Yehudah A, Ehmcke J, Rawe VY, Pholpramool C, Orwig KE, Schlatt S. GDNF family receptor alpha1 phenotype of spermatogonial stem cells in immature mouse testes. Biol Reprod 2005; 73:1011-6; PMID:16014811; http://dx.doi.org/10.1095/biolreprod.105.043810
   PubMed Web of Science ®Google Scholar
• Meng X, Lindahl M, Hyvonen ME, Parvinen M, de Rooij DG, Hess MW, Raatikainen-Ahokas A, Sainio K, Rauvala H, Lakso M, et al. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 2000; 287:1489-93; PMID:10688798; http://dx.doi.org/10.1126/science.287.5457.1489
   PubMed Web of Science ®Google Scholar
• Ballow D, Meistrich ML, Matzuk M, Rajkovic A. Sohlh1 is essential for spermatogonial differentiation. Dev Biol 2006; 294:161-7; PMID:16564520; http://dx.doi.org/10.1016/j.ydbio.2006.02.027
   PubMed Web of Science ®Google Scholar
• Suzuki H, Ahn HW, Chu T, Bowden W, Gassei K, Orwig K, Rajkovic A. SOHLH1 and SOHLH2 coordinate spermatogonial differentiation. Dev Biol 2012; 361:301-12; PMID:22056784; http://dx.doi.org/10.1016/j.ydbio.2011.10.027
   PubMed Web of Science ®Google Scholar
• Anderson EL, Baltus AE, Roepers-Gajadien HL, Hassold TJ, de Rooij DG, van Pelt AM, Page DC. Stra8 and its inducer, retinoic acid, regulate meiotic initiation in both spermatogenesis and oogenesis in mice. Proc Natl Acad Sci U S A 2008; 105:14976-80; PMID:18799751; http://dx.doi.org/10.1073/pnas.0807297105
   PubMed Web of Science ®Google Scholar
• Baltus AE, Menke DB, Hu YC, Goodheart ML, Carpenter AE, de Rooij DG, Page DC. In germ cells of mouse embryonic ovaries, the decision to enter meiosis precedes premeiotic DNA replication. Nat Genet 2006; 38:1430-4; PMID:17115059; http://dx.doi.org/10.1038/ng1919
   PubMed Web of Science ®Google Scholar
• Zhou Q, Nie R, Li Y, Friel P, Mitchell D, Hess RA, Small C, Griswold MD. Expression of stimulated by retinoic acid gene 8 (Stra8) in spermatogenic cells induced by retinoic acid: an in vivo study in vitamin A-sufficient postnatal murine testes. Biol Reprod 2008; 79:35-42; PMID:18322276; http://dx.doi.org/10.1095/biolreprod.107.066795
   PubMed Web of Science ®Google Scholar
• Menke DB, Koubova J, Page DC. Sexual differentiation of germ cells in XX mouse gonads occurs in an anterior-to-posterior wave. Dev Biol 2003; 262:303-12; PMID:14550793; http://dx.doi.org/10.1016/S0012-1606(03)00391-9
   PubMed Web of Science ®Google Scholar
• Imudia AN, Wang N, Tanaka Y, White YA, Woods DC, Tilly JL. Comparative gene expression profiling of adult mouse ovary-derived oogonial stem cells supports a distinct cellular identity. Fertil Steril 2013; 100(5):1451-8.
   PubMed Web of Science ®Google Scholar
• Takubo K, Ohmura M, Azuma M, Nagamatsu G, Yamada W, Arai F, Hirao A, Suda T. Stem cell defects in ATM-deficient undifferentiated spermatogonia through DNA damage-induced cell-cycle arrest. Cell Stem Cell 2008; 2:170-82; PMID:18371438; http://dx.doi.org/10.1016/j.stem.2007.10.023
   PubMed Web of Science ®Google Scholar
• Valli H, Sukhwani M, Dovey SL, Peters KA, Donohue J, Castro CA, Chu T, Marshall GR, Orwig KE. Fluorescence- and magnetic-activated cell sorting strategies to isolate and enrich human spermatogonial stem cells. Fertil Steril 2014; 102:566-80 e7; PMID:24890267; http://dx.doi.org/10.1016/j.fertnstert.2014.04.036
   PubMed Web of Science ®Google Scholar
• Oatley MJ, Kaucher AV, Racicot KE, Oatley JM. Inhibitor of DNA binding 4 is expressed selectively by single spermatogonia in the male germline and regulates the self-renewal of spermatogonial stem cells in mice. Biol Reprod 2011; 85:347-56; PMID:21543770; http://dx.doi.org/10.1095/biolreprod.111.091330
   PubMed Web of Science ®Google Scholar
• Yoshida S, Sukeno M, Nakagawa T, Ohbo K, Nagamatsu G, Suda T, Nabeshima Y. The first round of mouse spermatogenesis is a distinctive program that lacks the self-renewing spermatogonia stage. Development 2006; 133:1495-505; PMID:16540512; http://dx.doi.org/10.1242/dev.02316
   PubMed Web of Science ®Google Scholar
• Sada A, Suzuki A, Suzuki H, Saga Y. The RNA-binding protein NANOS2 is required to maintain murine spermatogonial stem cells. Science 2009; 325:1394-8; PMID:19745153; http://dx.doi.org/10.1126/science.1172645
   PubMed Web of Science ®Google Scholar
• Dettin L, Ravindranath N, Hofmann MC, Dym M. Morphological characterization of the spermatogonial subtypes in the neonatal mouse testis. Biol Reprod 2003; 69:1565-71; PMID:12855601; http://dx.doi.org/10.1095/biolreprod.103.016394
   PubMed Web of Science ®Google Scholar
• Boateng KA, Bellani MA, Gregoretti IV, Pratto F, Camerini-Otero RD. Homologous pairing preceding SPO11-mediated double-strand breaks in mice. Dev Cell 2013; 24:196-205; PMID:23318132; http://dx.doi.org/10.1016/j.devcel.2012.12.002
   PubMed Web of Science ®Google Scholar
• Chuma S, Nakatsuji N. Autonomous transition into meiosis of mouse fetal germ cells in vitro and its inhibition by gp130-mediated signaling. Dev Biol 2001; 229:468-79; PMID:11203703; http://dx.doi.org/10.1006/dbio.2000.9989
   PubMed Web of Science ®Google Scholar
• Di Carlo AD, Travia G, De Felici M. The meiotic specific synaptonemal complex protein SCP3 is expressed by female and male primordial germ cells of the mouse embryo. Int J Dev Biol 2000; 44:241-4; PMID:10794082
   PubMed Web of Science ®Google Scholar
• Romanienko PJ, Camerini-Otero RD. The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell 2000; 6:975-87; PMID:11106738; http://dx.doi.org/10.1016/S1097-2765(00)00097-6
   PubMed Web of Science ®Google Scholar
• Beumer TL, Roepers-Gajadien HL, Gademan IS, van Buul PP, Gil-Gomez G, Rutgers DH, de Rooij DG. The role of the tumor suppressor p53 in spermatogenesis. Cell Death Differ 1998; 5:669-77; PMID:10200522; http://dx.doi.org/10.1038/sj.cdd.4400396
   PubMed Web of Science ®Google Scholar
• Lu WJ, Chapo J, Roig I, Abrams JM. Meiotic recombination provokes functional activation of the p53 regulatory network. Science 2010; 328:1278-81; PMID:20522776; http://dx.doi.org/10.1126/science.1185640
   PubMed Web of Science ®Google Scholar
• Fingar DC, Salama S, Tsou C, Harlow E, Blenis J. Mammalian cell size is controlled by mTOR and its downstream targets S6K1 and 4EBP1/eIF4E. Genes Dev 2002; 16:1472-87; PMID:12080086; http://dx.doi.org/10.1101/gad.995802
   PubMed Web of Science ®Google Scholar
• Ruvinsky I, Sharon N, Lerer T, Cohen H, Stolovich-Rain M, Nir T, Dor Y, Zisman P, Meyuhas O. Ribosomal protein S6 phosphorylation is a determinant of cell size and glucose homeostasis. Genes Dev 2005; 19:2199-211; PMID:16166381; http://dx.doi.org/10.1101/gad.351605
   PubMed Web of Science ®Google Scholar
• Rotter V, Schwartz D, Almon E, Goldfinger N, Kapon A, Meshorer A, Donehower LA, Levine AJ. Mice with reduced levels of p53 protein exhibit the testicular giant-cell degenerative syndrome. Proc Natl Acad Sci U S A 1993; 90:9075-9; PMID:8415656; http://dx.doi.org/10.1073/pnas.90.19.9075
   PubMed Web of Science ®Google Scholar
• de Keizer PL, Laberge RM, Campisi J. p53: Pro-aging or pro-longevity? Aging (Albany NY) 2010; 2:377-9; PMID:20657035
   PubMedGoogle Scholar
• Rodier F, Campisi J, Bhaumik D. Two faces of p53: aging and tumor suppression. Nucleic Acids Res 2007; 35:7475-84; PMID:17942417; http://dx.doi.org/10.1093/nar/gkm744
   PubMed Web of Science ®Google Scholar
• Ferder IC, Wang N. Hypermaintenance and hypofunction of aged spermatogonia: insight from age-related increase of Plzf expression. Oncotarget 2015; PMID:25986924.
   PubMed Web of Science ®Google Scholar
• Kofman AE, McGraw MR, Payne CJ. Rapamycin increases oxidative stress response gene expression in adult stem cells. Aging (Albany NY) 2012; 4:279-89; PMID:22529334
   PubMedGoogle Scholar
• Chan F, Oatley MJ, Kaucher AV, Yang QE, Bieberich CJ, Shashikant CS, Oatley JM. Functional and molecular features of the Id4+ germline stem cell population in mouse testes. Genes Dev 2014; 28:1351-62; PMID:24939937; http://dx.doi.org/10.1101/gad.240465.114
   PubMed Web of Science ®Google Scholar
• Kippin TE, Martens DJ, van der Kooy D. p21 loss compromises the relative quiescence of forebrain stem cell proliferation leading to exhaustion of their proliferation capacity. Genes Dev 2005; 19:756-67; PMID:15769947; http://dx.doi.org/10.1101/gad.1272305
   PubMed Web of Science ®Google Scholar
• Cheng T, Rodrigues N, Shen H, Yang Y, Dombkowski D, Sykes M, Scadden DT. Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science 2000; 287:1804-8; PMID:10710306; http://dx.doi.org/10.1126/science.287.5459.1804
   PubMed Web of Science ®Google Scholar
• Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA, Jr., Butel JS, Bradley A. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 1992; 356:215-21; PMID:1552940; http://dx.doi.org/10.1038/356215a0
   PubMed Web of Science ®Google Scholar