Pluripotent cell derivation from male germline cells by suppression of Dmrt1 and Trp53

Journal of Reproduction and Development

Volumn 61, Issue 5, 2015, Pages 473-484

  Tanaka, Takashi ^a   Kanatsu Shinohara, Mito ^a,b   Hirose, Michiko ^c   Ogura, Atsuo ^c   Shinohara, Takashi ^a  

^a KYOTO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c INST OF PHYS AND CHEMICAL RESEARCH   (Japan)

Author keywords

Dmrt1; Pluripotency; Primordial germ cells; Spermatogonia; Trp53

Indexed keywords

DMRT1 PROTEIN; PROTEIN P53; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR;

ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CLONE; CELL CULTURE; COMPARATIVE STUDY; CYTOLOGY; FEASIBILITY STUDY; GENE SILENCING; GENETICS; INDUCED PLURIPOTENT STEM CELL; INSTITUTE FOR CANCER RESEARCH MOUSE; MALE; MAMMALIAN EMBRYO; METABOLISM; MOUSE; RNA INTERFERENCE; SPERMATOGENESIS; SPERMATOGONIUM;

ANIMALS; CELLS, CULTURED; CLONE CELLS; EMBRYO, MAMMALIAN; FEASIBILITY STUDIES; GENE KNOCKDOWN TECHNIQUES; INDUCED PLURIPOTENT STEM CELLS; MALE; MICE; MICE, INBRED ICR; RNA INTERFERENCE; RNA, SMALL INTERFERING; SPERMATOGENESIS; SPERMATOGONIA; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84944632874     PISSN: 09168818     EISSN: 13484400     Source Type: Journal    
DOI: 10.1262/jrd.2015-059     Document Type: Article

References (47)

1. Sabour D, Schöler HR. Reprogramming and the mammalian germline: the Weismann barrier revisited. Curr Opin Cell Biol 2012; 24: 716-723. [Medline] [CrossRef]
2. Illmensee K, Stevens LC. Teratomas and chimeras. Sci Am 1979; 240: 120-132. [Medline] [CrossRef]
3. Matsui Y, Zsebo K, Hogan BL. Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell 1992; 70: 841-847. [Medline] [CrossRef]
4. Resnick JL, Bixler LS, Cheng L, Donovan PJ. Long-term proliferation of mouse primordial germ cells in culture. Nature 1992; 359: 550-551. [Medline] [CrossRef]
5. Labosky PA, Barlow DP, Hogan BL. Mouse embryonic germ (EG) cell lines: transmission through the germline and differences in the methylation imprint of insulin-like growth factor 2 receptor (Igf2r) gene compared with embryonic stem (ES) cell lines. Development 1994; 120: 3197-3204. [Medline]
6. Stewart CL, Gadi I, Bhatt H. Stem cells from primordial germ cells can reenter the germ line. Dev Biol 1994; 161: 626-628. [Medline] [CrossRef]
7. Kanatsu-Shinohara M, Ogonuki N, Inoue K, Miki H, Ogura A, Toyokuni S, Shinohara T. Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol Reprod 2003; 69: 612-616. [Medline] [CrossRef]
8. Meistrich ML, van Beek MEAB. Spermatogonial stem cells. In: Desjardins C, Ewing LL (eds.), Cell and Molecular Biology of the Testis. New York: Oxford University Press; 1993: 266-295.
9. de Rooij DG, Russell LD. All you wanted to know about spermatogonia but were afraid to ask. J Androl 2000; 21: 776-798. [Medline]
10. Kanatsu-Shinohara M, Shinohara T. Spermatogonial stem cell self-renewal and development. Annu Rev Cell Dev Biol 2013; 29: 163-187. [Medline] [CrossRef]
11. Kanatsu-Shinohara M, Inoue K, Lee J, Yoshimoto M, Ogonuki N, Miki H, Baba S, Kato T, Kazuki Y, Toyokuni S, Toyoshima M, Niwa O, Oshimura M, Heike T, Nakahata T, Ishino F, Ogura A, Shinohara T. Generation of pluripotent stem cells from neonatal mouse testis. Cell 2004; 119: 1001-1012. [Medline] [CrossRef]
12. Takashima S, Hirose M, Ogonuki N, Ebisuya M, Inoue K, Kanatsu-Shinohara M, Tanaka T, Nishida E, Ogura A, Shinohara T. Regulation of pluripotency in male germline stem cells by Dmrt1. Genes Dev 2013; 27: 1949-1958. [Medline] [CrossRef]
13. Harvey M, McArthur MJ, Montgomery CA Jr, Bradley A, Donehower LA. Genetic background alters the spectrum of tumors that develop in p53-deficient mice. FASEB J 1993; 7: 938-943. [Medline]
14. Looijenga LH, Hersmus R, Gillis AJ, Pfundt R, Stoop HJ, van Gurp RJ, Veltman J, Beverloo HB, van Drunen E, van Kessel AG, Pera RR, Schneider DT, Summersgill B, Shipley J, McIntyre A, van der Spek P, Schoenmakers E, Oosterhuis JW. Genomic and expression profiling of human spermatocytic seminomas: primary spermatocyte as tumorigenic precursor and DMRT1 as candidate chromosome 9 gene. Cancer Res 2006; 66: 290-302. [Medline] [CrossRef]
15. Matson CK, Murphy MW, Sarver AL, Griswold MD, Bardwell VJ, Zarkower D. DMRT1 prevents female reprogramming in the postnatal mammalian testis. Nature 2011; 476: 101-104. [Medline] [CrossRef]
16. Chuma S, Kanatsu-Shinohara M, Inoue K, Ogonuki N, Miki H, Toyokuni S, Hosokawa M, Nakatsuji N, Ogura A, Shinohara T. Spermatogenesis from epiblast and primordial germ cells following transplantation into postnatal mouse testis. Development 2005; 132: 117-122. [Medline] [CrossRef]
17. Ogawa T, Aréchaga JM, Avarbock MR, Brinster RL. Transplantation of testis germinal cells into mouse seminiferous tubules. Int J Dev Biol 1997; 41: 111-122. [Medline]
18. Kanatsu-Shinohara M, Muneto T, Lee J, Takenaka M, Chuma S, Nakatsuji N, Horiuchi T, Shinohara T. Long-term culture of male germline stem cells from hamster testes. Biol Reprod 2008; 78: 611-617. [Medline] [CrossRef]
19. Lee J, Kanatsu-Shinohara M, Ogonuki N, Miki H, Inoue K, Morimoto T, Morimoto H, Ogura A, Shinohara T. Heritable imprinting defect caused by epigenetic abnormalities in mouse spermatogonial stem cells. Biol Reprod 2009; 80: 518-527. [Medline] [CrossRef]
20. Kawase Y, Iwata T, Watanabe M, Kamada N, Ueda O, Suzuki H. Application of the piezo-micromanipulator for injection of embryonic stem cells into mouse blastocysts. Contemp Top Lab Anim Sci 2001; 40: 31-34. [Medline]
21. Kanatsu-Shinohara M, Toyokuni S, Shinohara T. CD9 is a surface marker on mouse and rat male germline stem cells. Biol Reprod 2004; 70: 70-75. [Medline] [CrossRef]
22. Morimoto H, Lee J, Tanaka T, Ishii K, Toyokuni S, Kanatsu-Shinohara M, Shinohara T. In vitro transformation of mouse testis cells by oncogene transfection. Biol Reprod 2012; 86: 148: 1-11. [Medline] [CrossRef]
23. Kimura T, Tomooka M, Yamano N, Murayama K, Matoba S, Umehara H, Kanai Y, Nakano T. AKT signaling promotes derivation of embryonic germ cells from primordial germ cells. Development 2008; 135: 869-879. [Medline] [CrossRef]
24. Leitch HG, Blair K, Mansfield W, Ayetey H, Humphreys P, Nichols J, Surani MA, Smith A. Embryonic germ cells from mice and rats exhibit properties consistent with a generic pluripotent ground state. Development 2010; 137: 2279-2287. [Medline] [CrossRef]
25. Leitch HG, Nichols J, Humphreys P, Mulas C, Martello G, Lee C, Jones K, Surani MA, Smith A. Rebuilding pluripotency from primordial germ cells. Stem Cell Reports 2013; 1: 66-78. [Medline] [CrossRef]
26. Nagamatsu G, Kosaka T, Saito S, Honda H, Takubo K, Kinoshita T, Akiyama H, Sudo T, Horimoto K, Oya M, Suda T. Induction of pluripotent stem cells from primordial germ cells by single reprogramming factors. Stem Cells 2013; 31: 479-487. [Medline] [CrossRef]
27. Matsui Y, Takehara A, Tokitake Y, Ikeda M, Obara Y, Morita-Fujimura Y, Kimura T, Nakano T. The majority of early primordial germ cells acquire pluripotency by AKT activation. Development 2014; 141: 4457-4467. [Medline] [CrossRef]
28. Kanatsu-Shinohara M, Lee J, Inoue K, Ogonuki N, Miki H, Toyokuni S, Ikawa M, Nakamura T, Ogura A, Shinohara T. Pluripotency of a single spermatogonial stem cell in mice. Biol Reprod 2008; 78: 681-687. [Medline] [CrossRef]
29. Hirasawa R, Matoba S, Inoue K, Ogura A. Somatic donor cell type correlates with embryonic, but not extra-embryonic, gene expression in postimplantation cloned embryos. PLoS ONE 2013; 8: e76422. [Medline] [CrossRef]
30. Okae H, Matoba S, Nagashima T, Mizutani E, Inoue K, Ogonuki N, Chiba H, Funayama R, Tanaka S, Yaegashi N, Nakayama K, Sasaki H, Ogura A, Arima T. RNA sequencing-based identification of aberrant imprinting in cloned mice. Hum Mol Genet 2014; 23: 992-1001. [Medline] [CrossRef]
31. Spiller CM, Bowles J, Koopman P. Nodal/Cripto signaling in fetal male germ cell development: implications for testicular germ cell tumors. Int J Dev Biol 2013; 57: 211-219. [Medline] [CrossRef]
32. Looijenga LH, Verkerk AJ, Dekker MC, van Gurp RJ, Gillis AJ, Oosterhuis JW. Genomic imprinting in testicular germ cell tumours. APMIS 1998; 106: 187-195, discussion:196-197. [Medline] [CrossRef]
33. Kanatsu-Shinohara M, Ogonuki N, Iwano T, Lee J, Kazuki Y, Inoue K, Miki H, Takehashi M, Toyokuni S, Shinkai Y, Oshimura M, Ishino F, Ogura A, Shinohara T. Genetic and epigenetic properties of mouse male germline stem cells during long-term culture. Development 2005; 132: 4155-4163. [Medline] [CrossRef]
34. Heaney JD, Anderson EL, Michelson MV, Zechel JL, Conrad PA, Page DC, Nadeau JH. Germ cell pluripotency, premature differentiation and susceptibility to testicular teratomas in mice. Development 2012; 139: 1577-1586. [Medline] [CrossRef]
35. Krentz AD, Murphy MW, Kim S, Cook MS, Capel B, Zhu R, Matin A, Sarver AL, Parker KL, Griswold MD, Looijenga LH, Bardwell VJ, Zarkower D. The DM domain protein DMRT1 is a dose-sensitive regulator of fetal germ cell proliferation and pluripotency. Proc Natl Acad Sci USA 2009; 106: 22323-22328. [Medline] [CrossRef]
36. Zhu R, Bhattacharya C, Matin A. The role of dead-end in germ-cell tumor development. Ann N Y Acad Sci 2007; 1120: 181-186. [Medline] [CrossRef]
37. Cook MS, Coveney D, Batchvarov I, Nadeau JH, Capel B. BAX-mediated cell death affects early germ cell loss and incidence of testicular teratomas in Dnd1(Ter/Ter) mice. Dev Biol 2009; 328: 377-383. [Medline] [CrossRef]
38. Kimura T, Suzuki A, Fujita Y, Yomogida K, Lomeli H, Asada N, Ikeuchi M, Nagy A, Mak TW, Nakano T. Conditional loss of PTEN leads to testicular teratoma and enhances embryonic germ cell production. Development 2003; 130: 1691-1700. [Medline] [Cross-Ref]
39. Lee J, Kanatsu-Shinohara M, Inoue K, Ogonuki N, Miki H, Toyokuni S, Kimura T, Nakano T, Ogura A, Shinohara T. Akt mediates self-renewal division of mouse spermatogonial stem cells. Development 2007; 134: 1853-1859. [Medline] [CrossRef]
40. Oatley JM, Avarbock MR, Brinster RL. Glial cell line-derived neurotrophic factor regulation of genes essential for self-renewal of mouse spermatogonial stem cells is dependent on Src family kinase signaling. J Biol Chem 2007; 282: 25842-25851. [Medline] [CrossRef]
41. Goertz MJ, Wu Z, Gallardo TD, Hamra FK, Castrillon DH. Foxo1 is required in mouse spermatogonial stem cells for their maintenance and the initiation of spermatogenesis. J Clin Invest 2011; 121: 3456-3466. [Medline] [CrossRef]
42. Huang Y, Mao X, Boyce T, Zhu GZ. Dispensable role of PTEN in mouse spermatogenesis. Cell Biol Int 2011; 35: 905-908. [Medline] [CrossRef]
43. Imamura M, Miura K, Iwabuchi K, Ichisaka T, Nakagawa M, Lee J, Kanatsu-Shinohara M, Shinohara T, Yamanaka S. Transcriptional repression and DNA hypermethylation of a small set of ES cell marker genes in male germline stem cells. BMC Dev Biol 2006; 6: 34. [Medline] [CrossRef]
44. Western PS, van den Bergen JA, Miles DC, Sinclair AH. Male fetal germ cell differentiation involves complex repression of the regulatory network controlling pluripotency. FASEB J 2010; 24: 3026-3035. [Medline] [CrossRef]
45. Morimoto H, Kanatsu-Shinohara M, Takashima S, Chuma S, Nakatsuji N, Takehashi M, Shinohara T. Phenotypic plasticity of mouse spermatogonial stem cells. PLoS ONE 2009; 4: e7909. [Medline] [CrossRef]
46. Takashima S, Kanatsu-Shinohara M, Tanaka T, Morimoto H, Inoue K, Ogonuki N, Jijiwa M, Takahashi M, Ogura A, Shinohara T. Functional differences between GDNFdependent and FGF2-dependent mouse spermatogonial stem cell self-renewal. Stem Cell Reports 2015; 4: 489-502. [Medline] [CrossRef]
47. Tada T, Tada M, Hilton K, Barton SC, Sado T, Takagi N, Surani MA. Epigenotype switching of imprintable loci in embryonic germ cells. Dev Genes Evol 1998; 207: 551-561. [Medline] [CrossRef]