Serum- and feeder-free culture of mouse germline stem cells

Biology of Reproduction

Volumn 84, Issue 1, 2011, Pages 97-105

  Kanatsu Shinohara, Mito ^a   Inoue, Kimiko ^b   Ogonuki, Narumi ^b   Morimoto, Hiroko ^a   Ogura, Atsuo ^b   Shinohara, Takashi ^a  

^a KYOTO UNIVERSITY   (Japan)

^b INST OF PHYS AND CHEMICAL RESEARCH   (Japan)

Author keywords

Culture; Developmental biology; Gametogenesis; Self renewal; Sertoli cells; Serum; Spermatogenesis; Testis; Transplantation

Indexed keywords

FETUIN;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; GLIA CELL; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEMINIFEROUS TUBULE; SPERMATOGENESIS; SPERMATOGONIUM; STEM CELL;

ALPHA-FETOPROTEINS; ANIMALS; CELL ADHESION; CELL CULTURE TECHNIQUES; CELL PROLIFERATION; CULTURE MEDIA; LIPIDS; MALE; MICE; SPERMATOGONIA; STEM CELLS;

MUS;

EID: 78651515404     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.110.086462     Document Type: Article

References (38)

1. de Rooij DG, Russell LD. All you wanted to know about spermatogonia but were afraid to ask. J Androl 2000; 21:776-798.
2. Brinster RL, Zimmermann JW. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci U S A 1994; 91:11298-11302.
3. Meistrich ML, van Beek MEAB. Spermatogonial stem cells. In: Desjardins CC, Ewing LL (eds.), Cell and Molecular Biology of the Testis. New York: Oxford University Press; 1993:266-295.
4. Tegelenbosch RAJ, de Rooij DG. A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101 F1 hybrid mouse. Mutat Res 1993; 290:193-200.
5. Meng X, Lindahl M, Hyvönen ME, Parvinen M, de Rooij DG, Hess MW, Raatikainen-Ahokas A, Sainio K, Rauvala H, Lakso M, Pichel JG, Westphal H, et al. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 2000; 287:1489-1493.
6. 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.
7. 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, et al. Genetic and epigenetic properties of mouse male germline stem cells during long-term culture. Development 2005; 132:4155-4163. (Pubitemid 41488864)
8. Liu X, Wu H, Loring J, Hormuzdi S, Disteche CM, Bornstein P, Jaenisch R. Trisomy eight in ES cells is a common potential problem in gene targeting and interferes with germline transmission. Dev Dyn 1997; 209: 85-91.
9. Longo L, Bygrave A, Grosveld FG, Pandolfi PP. The chromosome makeup of mouse embryonic stem cells is predictive of somatic and germ cell chimerism. Transgenic Res 1997; 6:321-328.
10. Kanatsu-Shinohara M, Ikawa M, Takehashi M, Ogonuki N, Miki H, Inoue K, Kazuki Y, Lee J, Toyokuni S, Oshimura M, Ogura A, Shinohara T. Production of knockout mice by random and targeted mutagenesis in spermatogonial stem cells. Proc Natl Acad Sci U S A 2006; 103:8018-8023.
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, et al. Generation of pluripotent stem cells from neonatal mouse testis. Cell 2004; 119:1001-1012.
12. Kanatsu-Shinohara M, Miki H, Inoue K, Ogonuki N, Toyokuni S, Ogura A, Shinohara T. Long-term culture of mouse male germline stem cells under serum- or feeder-free conditions. Biol Reprod 2005; 72:985-991. (Pubitemid 40404276)
13. Kanatsu-Shinohara M, Inoue K, Lee J, Miki H, Ogonuki N, Toyokuni S, Ogura A, Shinohara T. Anchorage-independent growth of mouse male germline stem cells in vitro. Biol Reprod 2006; 74:522-529.
14. Ying Q-L, Nichols J, Chambers I, Smith A. BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with Stat3. Cell 2003; 115:281-292.
15. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992; 255:1707-1710.
16. Kubota H, Avarbock MR, Brinster RL. Growth factors essential for selfrenewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci U S A 2004; 101:16489-16494. (Pubitemid 39557740)
17. Kubota H, Brinster RL. Culture of rodent spermatogonial stem cells, male germline stem cells of the postnatal animal. Methods Cell Biol 2008; 86: 59-84.
18. 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.
19. 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.
20. Shinohara T, Avarbock MR, Brinster RL. β1- And α6-integrin are surface markers on mouse spermatogonial stem cells. Proc Natl Acad Sci U S A 1999; 96:5504-5509.
21. Kanatsu-Shinohara M, Takehashi M, Takashima S, Lee J, Morimoto H, Chuma S, Raducanu A, Nakatsuji N, Fässler R, Shinohara T. Homing of mouse spermatogonial stem cells to germline niche depends on β1- integrin. Cell Stem Cell 2008; 3:533-542.
22. Kanatsu-Shinohara M, Ogonuki N, Inoue K, Ogura A, Toyokuni S, Honjo T, Shinohara T. Allogeneic offspring produced by male germline stem cell transplantation into infertile mouse testis. Biol Reprod 2003; 68:167-173.
23. Nagano M, Avarbock MR, Brinster RL. Pattern and kinetics of mouse donor spermatogonial stem cell colonization in recipient testes. Biol Reprod 1999; 60:1429-1436.
24. Ogonuki N, Mochida K, Miki H, Inoue K, Fray M, Iwaki T, Moriwaki K, Obata Y, Morozumi K, Yanagimachi K, Ogura A. Spermatozoa and spermatids retrieved from frozen reproductive organs or frozen whole bodies of male mice can produce normal offspring. Proc Natl Acad Sci U S A 2006; 103:13098-13103.
25. Kimura Y, Yanagimachi R. Mouse oocytes injected with testicular spermatozoa or round spermatids can develop into normal offspring. Development 1995; 121:2397-2405.
26. Schroeder AC, Schultz RM, Kopf GS, Taylor FR, Becker RB, Eppig JJ. Fetuin inhibits zona pellucida hardening and conversion of ZP2 to ZP2f during spontaneous mouse oocyte maturation in vitro in the absence of serum. Biol Reprod 1990; 43:891-897.
27. Pyne S, Lee SC, Long J, Pyne NJ. Role of sphingosine kinases and lipid phosphate phosphatases in regulating spatial sphingosine 1-phosphate signaling in heath and disease. Cell Signal 2009; 21:14-21.
28. Lee J, Kanatsu-Shinohara M, Morimoto H, Kazuki Y, Takashima S, Oshimura M, Toyokuni S, Shinohara T. Genetic reconstruction of mouse spermatogonial stem cell self-renewal in vitro by Ras-cyclin D2 activation. Cell Stem Cell 2009; 5:76-86.
29. Palermo G, Joris H, Devroey P, Van Steirteghem AC. Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet 1992; 340:17-18.
30. Brown WM, Saunders NR, Mollgard K, Dziegielewska KM. Fetuin-an old friend revisited. Bioessays 1992; 14:749-755.
31. Pebay A, Wong RCB, Pitson SM, Wolvetang EJ, Peh GS-L, Filipczyk A, Koh KLL, Tellis I, Nguyen LTV, Pera MF. Essential roles of sphingosine- 1-phosphate and platelet-derived growth factor in the maintenance of human embryonic stem cells. Stem Cells 2005; 23:1541-1548.
32. Garcia-Gonzalo FR, Izpisú Belmonte JC. Albumin-associated lipids regulate human embryonic stem cell self-renewal. PLoS One 2008; 1: E1384.
33. Wu Z, Luby-Phelps K, Bugde A, Molyneux LA, Denard B, Li WH, Süel GM, Garbers DL. Capacity for stochastic self-renewal and differentiation in mammalian spermatogonial stem cells. J Cell Biol 2009; 187:513-524.
34. 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.
35. Hamra FK, Chapman KM, Nguyen DM, Williams-Stephens AA, Hammer RE, Garbers DL. Self-renewal, expansion, and transfection of rat spermatogonial stem cells in culture. Proc Natl Acad Sci U S A 2005; 102: 17430-17435.
36. Ryu BY, Kubota H, Avarbock MR, Brinster RL. Conservation of spermatogonial stem cell self-renewal signaling between mouse and rat. Proc Natl Acad Sci U S A 2005; 102:14302-14307.
37. Aponte PM, Soda T, Teerds KJ, Mizrak SC, van de Kant HJ, de Rooij DG. Propagation of bovine spermatogonial stem cells in vitro. Reproduction 2008; 136:543-557.
38. Sadri-Ardekani H, Mizrak SC, van Daalen SK, Korver CM, Roepers-Gajadien HL, Koruji M, Hovingh S, de Reijke TM, de la Rosette JJ, van der Veen F, de Rooij DG, Repping S, et al. Propagation of human spermatogonial stem cells in vitro. JAMA 2009; 302:2127-2134.