Signaling molecules and pathways regulating the fate of spermatogonial stem cells

Microscopy Research and Technique

Volumn 72, Issue 8, 2009, Pages 586-595

  He, Zuping ^a   Kokkinaki, Maria ^a   Dym, Martin ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Differentiation; Renewal; Signaling pathways; Spermatogonial stem cells

Indexed keywords

CELL SIGNALING; CYTOLOGY; DISEASES; GENE THERAPY; MAMMALS; MOLECULES; SIGNALING;

CELL-BE; CELL/B.E; CELL/BE; DIFFERENTIATION; RENEWAL; SELF RENEWAL; SIGNALING MOLECULES; SIGNALLING PATHWAYS; SPERMATOGONIAL STEM CELL; STEM-CELL;

STEM CELLS;

ALPHA6 INTEGRIN; BETA1 INTEGRIN; BIOLOGICAL MARKER; BONE MORPHOGENETIC PROTEIN; CD133 ANTIGEN; CD9 ANTIGEN; ENZYME; EPIDERMAL GROWTH FACTOR; ETS RELATED MOLECULE; FIBROBLAST GROWTH FACTOR 2; G PROTEIN COUPLED RECEPTOR 125; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; JANUS KINASE; NEUROGENIN3; OCTAMER TRANSCRIPTION FACTOR 4; PHOSPHATIDYLINOSITOL 3 KINASE; PROMYELOCYTE LEUKEMIA ZINC FINGER FACTOR; PROTEIN BCL 6; PROTEIN GFRA1; PROTEIN KINASE B; PROTEIN PCNA; PROTEIN RET; PROTEIN STRA8; PROTEIN TYROSINE KINASE; RECEPTOR; STEM CELL FACTOR; THY 1 ANTIGEN; TISSUE NONSPECIFIC ALKALINE PHOSPHATASE; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

CELL DIFFERENTIATION; CELL FATE; CELL RENEWAL; HUMAN; MOLECULAR MECHANICS; MORPHOLOGICAL TRAIT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SPERMATOGENESIS; SPERMATOGONIUM; STEM CELL; TESTIS CANCER; XENOTRANSPLANTATION;

MAMMALIA;

EID: 67650819027     PISSN: 1059910X     EISSN: 10970029     Source Type: Journal    
DOI: 10.1002/jemt.20698     Document Type: Review

References (108)

1. Baron BW, Nucifora G, McCabe N, Espinosa R, 3rd, Le Beau MM, McKeithan TW. 1993. Identification of the gene associated with the recurring chromosomal translocations t(3;14)(q27;q32) and t(3;22)(q27;q11) in B-cell lymphomas. Proc Natl Acad Sci USA 90:5262-5266.
2. Bellvé AR, Cavicchia JC, Millette CF, O'Brien DA, Bhatnagar YM, Dym M. 1977. Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J Cell Biol 74:68-85. (Pubitemid 8141486)
3. Besser D. 2004. Expression of nodal, lefty-a, and lefty-B in undifferentiated human embryonic stem cells requires activation of Smad2/3. J Biol Chem 279:45076-45084. (Pubitemid 39430922)
4. Beumer TL, Roepers-Gajadien HL, Gademan IS, Kal HB, de Rooij DG. 2000. Involvement of the D-type cyclins in germ cell proliferation and differentiation in the mouse. Biol Reprod 63:1893-1898. (Pubitemid 30954202)
5. Blume-Jensen P, Jiang G, Hyman R, Lee KF, O'Gorman S, Hunter T. 2000. Kit/stem cell factor receptor-induced activation of phosphatidylinositol 30-kinase is essential for male fertility. Nat Genet 24:157-162. (Pubitemid 30094716)
6. Brawley C, Matunis E. 2004. Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo. Science 304:1331-1334. (Pubitemid 38697431)
7. Braydich-Stolle L, Nolan C, Dym M, Hofmann MC. 2005. Role of glial cell line-derived neurotrophic factor in germ-line stem cell fate. Ann N YAcad Sci 1061:94-99. (Pubitemid 43211589)
8. Braydich-Stolle L, Kostereva N, Dym M, Hofmann MC. 2007. Role of Src family kinases and N-Myc in spermatogonial stem cell proliferation. Dev Biol 304:34-45. (Pubitemid 46399669)
9. Brinster RL. 2007. Male germline stem cells: From mice to men. Science 316:404-405. (Pubitemid 46651480)
10. Brinster RL, Avarbock MR. 1994. Germ line transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci USA 91:11303-11307.
11. Brinster RL, Zimmerman JW. 1994. Spermatogenesis following male germ cell transplantation. Proc Natl Acad Sci USA 91:11298-11302. (Pubitemid 24356331)
12. Buaas FW, Kirsh AL, Sharma M, McLean DJ, Morris JL, Griswold MD, de Rooij DG, Braun RE. 2004. Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet 36:647-652. (Pubitemid 38715995)
13. Buageaw A, Sukhwani M, Ben-Yehudah A, Ehmcke J, Rawe VY, Pholpramool C, Orwig KE, Schlatt S. 2005. GDNF family receptor alpha1 phenotype of spermatogonial stem cells in immature mouse testes. Biol Reprod 73:1011-1016. (Pubitemid 41507506)
14. Chen D, McKearin D. 2005. Gene circuitry controlling a stem cell niche. Curr Biol 15:179-184.
15. Chen C, Ouyang W, Grigura V, Zhou Q, Carnes K, Lim H, Zhao GQ, Arber S, Kurpios N, Murphy TL, Cheng AM, Hassell JA, Chandrashekar V, Hofmann MC, Hess RA, Murphy KM. 2005. ERM is required for transcriptional control of the spermatogonial stem cell niche. Nature 436:1030-1034. (Pubitemid 41191687)
16. Clermont Y. 1963. The cycle of the seminiferous epithelium in man. Am J Anat 112:35-51.
17. Clermont Y. 1966a. Renewal of spermatogonia in man. Am J Anat 118:509-524.
18. Clermont Y. 1966b. Spermatogenesis in man. A study of the spermatogonial population. Fertil Steril 17:705-721.
19. Clermont Y. 1972. Kinetics of spermatogenesis in mammals: Seminiferous epithelium cycle and spermatogonial renewal. Physiol Rev 52:198-236.
20. Clouthier DE, Avarbock MR, Maika SD, Hammer RE, Brinster RL. 1996. Rat spermatogenesis in mouse testis. Nature 381:418-421.
21. Conrad S, Renninger M, Hennenlotter J, Wiesner T, Just L, Bonin M, Aicher W, Buhring HJ, Mattheus U, Mack A, Wagner HJ, Minger S, Matzkies M, Reppel M, Hescheler J, Sievert KD, Stenzl A, Skutella T. 2008. Generation of pluripotent stem cells from adult human testis. Nature 456:344-349.
22. Costoya JA, Hobbs RM, Barna M, Cattoretti G, Manova K, Sukhwani M, Orwig KE, Wolgemuth DJ, Pandolfi PP. 2004. Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 36:653-659.
23. Cotton L, Gibbs GM, Sanchez-Partida LG, Morrison JR, de Kretser DM, O'Bryan MK. 2006. FGFR-1 [corrected] signaling is involved in spermiogenesis and sperm capacitation. J Cell Sci 119:75-84. (Pubitemid 43169300)
24. de Rooij DG. 1998. Stem cells in the testis. Int J Exp Pathol 79:67-80.
25. de Rooij DG, Grootegoed JA. 1998. Spermatogonial stem cells. Curr Opin Cell Biol 10:694-701.
26. de Rooij DG, Mizrak SC. 2008. Deriving multipotent stem cells from mouse spermatogonial stem cells: A new tool for developmental and clinical research. Development 135:2207-2213.
27. de Rooij DG, Russell LD. 2000. All you wanted to know about spermatogonia but were afraid to ask. J Androl 21:776-798. (Pubitemid 30808061)
28. Dettin L, Ravindranath N, Hofmann MC, Dym M. 2003. Morphological characterization of the spermatogonial subtypes in the neonatal mouse testis. Biol Reprod 69:1565-1571. (Pubitemid 37362839)
29. Dirami G, Ravindranath N, Achi MV, Dym M. 2001. Expression of Notch pathway components in spermatogonia and Sertoli cells of neonatal mice. J Androl 22:944-952. (Pubitemid 33020315)
30. Dolci S, Pellegrini M, Di Agostino S, Geremia R, Rossi P. 2001. Signaling through extracellular signal-regulated kinase is required for spermatogonial proliferative response to stem cell factor. J Biol Chem 276:40225-40233. (Pubitemid 37391442)
31. Dym M. 1994. Spermatogonial stem cells of the testis. Proc Natl Acad Sci USA 91:11287-11289.
32. Dym M, Clermont Y. 1970. Role of spermatogonia in the repair of the seminiferous epithelium following X-irradiation of the rat testis. Am J Anat 128:265-282.
33. Dym M, He Z, Jiang J, Pant D, Kokkinaki M. 2009. Spermatogonial stem cells: Unlimited potential. Reproduction, Fertility and Development 21:15-21.
34. Dym M, Jia MC, Dirami G, Price JM, Rabin SJ, Mocchetti I, Ravindranath N. 1995. Expression of c-kit receptor and its autophosphorylation in immature rat type A spermatogonia. Biol Reprod 52:8-19.
35. Ehmcke J, Schlatt S. 2006. A revised model for spermatogonial expansion in man: Lessons from non-human primates. Reproduction 132:673-680. (Pubitemid 44782517)
36. Falender AE, Shimada M, Lo YK, Richards JS. 2005. TAF4b, a TBP associated factor, is required for oocyte development and function. Dev Biol 288:405-419. (Pubitemid 41790752)
37. Feng LX, Ravindranath N, Dym M. 2000. Stem cell factor/c-kit upregulates cyclin D3 and promotes cell cycle progression via the phosphoinositide 3-kinase/p70 S6 kinase pathway in spermatogonia. J Biol Chem 275:25572-25576. (Pubitemid 30687061)
38. Feng LX, Chen Y, Dettin L, Pera RA, Herr JC, Goldberg E, Dym M. 2002. Generation and in vitro differentiation of a spermatogonial cell line. Science 297:392-395. (Pubitemid 34790767)
39. Filipponi D, Hobbs RM, Ottolenghi S, Rossi P, Jannini EA, Pandolfi PP, Dolci S. 2007. Repression of kit expression by Plzf in germ cells. Mol Cell Biol 27:6770-6781. (Pubitemid 47483628)
40. Giuili G, Tomljenovic A, Labrecque N, Oulad-Abdelghani M, Rassoulzadegan M, Cuzin F. 2002. Murine spermatogonial stem cells: Targeted transgene expression and purification in an active state. EMBO Rep 3:753-759. (Pubitemid 34966014)
41. Guan K, Nayernia K, Maier LS, Wagner S, Dressel R, Lee JH, Nolte J, Wolf F, Li M, Engel W, Hasenfuss G. 2006. Pluripotency of spermatogonial stem cells from adult mouse testis. Nature 440:1199-1203.
42. He Z, Jiang J, Hofmann MC, Dym M. 2007. Gfra1 silencing in mouse spermatogonial stem cells results in their differentiation via the inactivation of RET tyrosine kinase. Biol Reprod 77:723-733. (Pubitemid 47494388)
43. He Z, Jiang J, Kokkinaki M, Golestaneh N, Hofmann MC, Dym M. 2008a. Gdnf upregulates c-Fos transcription via the Ras/Erk1/2 pathway to promote mouse spermatogonial stem cell proliferation. Stem Cells 26:266-278.
44. He Z, Jiang J, Kokkinaki M, Hofmann MC, Dym M. 2008b. Nodal stimulates the proliferation and survival of mouse spermatogonial stem cells through the activation of Smad2/3 and Oct-4 transcription via an autocrine pathway. Proceedings of 41st Society for the Study of Reproduction Annual Meeting. Biol Reprod p 184.
45. Hermann BP, Sukhwani M, Lin CC, Sheng Y, Tomko J, Rodriguez M, Shuttleworth JJ, McFarland D, Hobbs RM, Pandolfi PP, Schatten GP, Orwig KE. 2007. Characterization, cryopreservation, and ablation of spermatogonial stem cells in adult rhesus macaques. Stem Cells 25:2330-2338. (Pubitemid 47480492)
46. Hofmann MC, Braydich-Stolle L, Dym M. 2005. Isolation of male germ-line stem cells; influence of GDNF. Dev Biol 279:114-124. (Pubitemid 40222173)
47. Honaramooz A, Megee SO, Dobrinski I. 2002a. Germ cell transplantation in pigs. Biol Reprod 66:21-28.
48. Honaramooz A, Snedaker A, Boiani M, Scholer H, Dobrinski I, Schlatt S. 2002b. Sperm from neonatal mammalian testes grafted in mice. Nature 418:778-781. (Pubitemid 34894100)
49. Hu J, Chen YX, Wang D, Qi X, Li TG, Hao J, Mishina Y, Garbers DL, Zhao GQ. 2004. Developmental expression and function of Bmp4 in spermatogenesis and in maintaining epididymal integrity. Dev Biol 276:158-171. (Pubitemid 39456433)
50. Huyghe E, Matsuda T, Thonneau P. 2003. Increasing incidence of testicular cancer worldwide: A review. J Urol 170:5-11. (Pubitemid 36734401)
51. Itman C, Loveland KL. 2008. SMAD expression in the testis: An insight into BMP regulation of spermatogenesis. Dev Dyn 237:97-111.
52. James D, Levine AJ, Besser D, Hemmati-Brivanlou A. 2005. TGFbeta/activin/nodal signaling is necessary for the maintenance of pluripotency in human embryonic stem cells. Development 132:1273-1282. (Pubitemid 40528787)
53. Kanatsu-Shinohara M, Ogonuki N, Inoue K, Miki H, Ogura A, Toyokuni S, Shinohara T. 2003. Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol Reprod 69:612-616. (Pubitemid 36885967)
54. 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. 2004a. Generation of pluripotent stem cells from neonatal mouse testis. Cell 119:1001-1012. (Pubitemid 40037613)
55. Kanatsu-Shinohara M, Toyokuni S, Shinohara T. 2004b. CD9 is a surface marker on mouse and rat male germline stem cells. Biol Reprod 70:70-75. (Pubitemid 38063552)
56. Kanatsu-Shinohara M, Lee J, Inoue K, Ogonuki N, Miki H, Toyokuni S, Ikawa M, Nakamura T, Ogura A, Shinohara T. 2008. Pluripotency of a single spermatogonial stem cell in mice. Biol Reprod 78:681-687.
57. Kawase E, Wong MD, Ding BC, Xie T. 2004. Gbb/Bmp signaling is essential for maintaining germline stem cells and for repressing bam transcription in the Drosophila testis. Development 131:1365-1375. (Pubitemid 38443890)
58. Kiger AA, Jones DL, Schulz C, Rogers MB, Fuller MT. 2001. Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science 294:2542-2545. (Pubitemid 34027293)
59. Kissel H, Timokhina I, Hardy MP, Rothschild G, Tajima Y, Soares V, Angeles M, Whitlow SR, Manova K, Besmer P. 2000. Point mutation in kit receptor tyrosine kinase reveals essential roles for kit signaling in spermatogenesis and oogenesis without affecting other kit responses. EMBO J 19:1312-1326. (Pubitemid 30151027)
60. Klippel A, Escobedo MA, Wachowicz MS, Apell G, Brown TW, Giedlin MA, Kavanaugh WM, Williams LT. 1998. Activation of phosphatidylinositol 3-kinase is sufficient for cell cycle entry and promotes cellular changes characteristic of oncogenic transformation. Mol Cell Biol 18:5699-5711. (Pubitemid 28450521)
61. Kokkinaki M, Lee TL, He Z, Jiang J, Golestaneh N, Hofmann MC, Chan WY, Dym M. 2008. The molecular signature of spermatogonial stem cells in the 6-day-old mouse testis. Biol Reprod (in press). 23 December 2008 [Epub ahead of print]. Available online at http://www.biolreprod.org/cgi/content/abstract/ biolreprod.108.073809.
62. Kossack N, Meneses J, Shefi S, Nguyen HN, Chavez S, Nicholas C, Gromoll J, Turek PJ, Reijo-Pera RA. Isolation and characterization of pluripotent human spermatogonial stem cell-derived cells. Stem Cells (in press). 16 October 2008 [Epub ahead of print].
63. Kubota H, Avarbock MR, Brinster RL. 2003. Spermatogonial stem cells share some, but not all, phenotypic and functional characteristics with other stem cells. Proc Natl Acad Sci USA 100:6487-6492. (Pubitemid 36666608)
64. Kubota H, Avarbock MR, Brinster RL. 2004a. Culture conditions and single growth factors affect fate determination of mouse spermatogonial stem cells. Biol Reprod 71:722-731. (Pubitemid 39108631)
65. Kubota H, Avarbock MR, Brinster RL. 2004b. Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci USA 101:16489-16494. (Pubitemid 39557740)
66. Lee J, Kanatsu-Shinohara M, Inoue K, Ogonuki N, Miki H, Toyokuni S, Kimura T, Nakano T, Ogura A, Shinohara T. 2007. Akt mediates self-renewal division of mouse spermatogonial stem cells. Development 134:1853-1859. (Pubitemid 46939231)
67. Matzuk MM. 2004. Germ-line immortality. Proc Natl Acad Sci USA 101:16395-16396.
68. McIntyre A, Gilbert D, Goddard N, Looijenga L, Shipley J. 2008. Genes, chromosomes and the development of testicular germ cell tumors of adolescents and adults. Genes Chromosomes Cancer 47:547-557. (Pubitemid 351748341)
69. Meistrich ML. 1986. Relationship between spermatogonial stem cell survival and testis function after cytotoxic therapy. Br J Cancer Suppl 7:89-101.
70. Meng X, Lindahl M, Hyvonen ME, Parvinen M, de Rooij DG, Hess MW, Raatikainen-Ahokas A, Sainio K, Rauvala H, Lakso M, Pichel JG, Westphal H, Saarma M, Sariola H. 2000. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 287:1489-1493. (Pubitemid 30127143)
71. Meng X, de Rooij DG, Westerdahl K, Saarma M, Sariola H. 2001. Promotion of seminomatous tumors by targeted overexpression of glial cell line-derived neurotrophic factor in mouse testis. Cancer Res 61:3267-3271. (Pubitemid 32695010)
72. Nagano M, McCarrey JR, Brinster RL. 2001. Primate spermatogonial stem cells colonize mouse testes. Biol Reprod 64:1409-1416. (Pubitemid 32373060)
73. Nagano M, Patrizio P, Brinster RL. 2002. Long-term survival of human spermatogonial stem cells in mouse testes. Fertil Steril 78:1225-1233. (Pubitemid 35463119)
74. Nakagawa T, Nabeshima Y, Yoshida S. 2007. Functional identification of the actual and potential stem cell compartments in mouse spermatogenesis. Dev Cell 12:195-206.
75. Naughton CK, Jain S, Strickland AM, Gupta A, Milbrandt J. 2006. Glial cell-line derived neurotrophic factor-mediated RET signaling regulates spermatogonial stem cell fate. Biol Reprod 74:314-321. (Pubitemid 43122282)
76. Oatley JM, Brinster RL. 2006. Spermatogonial stem cells. Methods Enzymol 419:259-282.
77. Oatley JM, Avarbock MR, Telaranta AI, Fearon DT, Brinster RL. 2006. Identifying genes important for spermatogonial stem cell self-renewal and survival. Proc Natl Acad Sci USA 103:9524-9529. (Pubitemid 43955858)
78. Oatley JM, Avarbock MR, Brinster RL. 2007. 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 282:25842-25851.
79. Ogawa T, Dobrinski I, Avarbock MR, Brinster RL. 2000. Transplantation of male germ line stem cells restores fertility in infertile mice. Nat Med 6:29-34. (Pubitemid 30048522)
80. Ohbo K, Yoshida S, Ohmura M, Ohneda O, Ogawa T, Tsuchiya H, Kuwana T, Kehler J, Abe K, Scholer HR, Suda T. 2003. Identification and characterization of stem cells in prepubertal spermatogenesis in mice small star, filled. Dev Biol 258:209-225. (Pubitemid 36627667)
81. Ohmura M, Yoshida S, Ide Y, Nagamatsu G, Suda T, Ohbo K. 2004. Spatial analysis of germ stem cell development in Oct-4/EGFP transgenic mice. Arch Histol Cytol 67:285-296. (Pubitemid 40215902)
82. Ohta H, Yomogida K, Dohmae K, Nishimune Y. 2000. Regulation of proliferation and differentiation in spermatogonial stem cells: The role of c-kit and its ligand SCF. Development 127:2125-2131. (Pubitemid 30386676)
83. Payne C, Braun RE. 2006. Glial cell line-derived neurotrophic factor maintains a POZ-itive influence on stem cells. Proc Natl Acad Sci USA 103:9751-9752. (Pubitemid 43993569)
84. Pellegrini M, Grimaldi P, Rossi P, Geremia R, Dolci S. 2003. Developmental expression of BMP4/ALK3/SMAD5 signaling pathway in the mouse testis: A potential role of BMP4 in spermatogonia differentiation. J Cell Sci 116:3363-3372. (Pubitemid 37038984)
85. Perez-Sala D, Rebollo A. 1999. Novel aspects of Ras proteins biology: Regulation and implications. Cell Death Differ 6:722-728. (Pubitemid 29425382)
86. Ramalho-Santos M, Willenbring H. 2007. On the origin of the term "stem cell". Cell Stem Cell 1:35-38.
87. Regaud C. 1901a. Études sur la structure des tubes séminifères et sur la spermatogénèse chez les mammifères. Part 1. Arch Anat Microsc Morphol Exp 4:101-156.
88. Regaud C. 1901b. Études sur la structure des tubes séminifères et sur la spermatogénèse chez les mammifères. Part 2. Arch Anat Microsc Morphol Exp 4:231-380.
89. Rossi P, Dolci S, Albanesi C, Grimaldi P, Ricca R, Geremia R. 1993. Follicle-stimulating hormone induction of steel factor (SLF) mRNA in mouse Sertoli cells and stimulation of DNA synthesis in spermatogonia by soluble SLF. Dev Biol 155:68-74. (Pubitemid 23112046)
90. Schlatt S, Weinbauer GF. 1994. Immunohistochemical localization of proliferating cell nuclear antigen as a tool to study cell proliferation in rodent and primate testes. Int J Androl 17:214-222. (Pubitemid 24283260)
91. Schrans-Stassen BH, van de Kant HJ, de Rooij DG, van Pelt AM. 1999. Differential expression of c-kit in mouse undifferentiated and differentiating type A spermatogonia. Endocrinology 140:5894-5900.
92. Seandel M, James D, Shmelkov SV, Falciatori I, Kim J, Chavala S, Scherr DS, Zhang F, Torres R, Gale NW, Yancopoulos GD, Murphy A, Valenzuela DM, Hobbs RM, Pandolfi PP, Rafii S. 2007. Generation of functional multipotent adult stem cells from GPR1251 germline progenitors. Nature 449:346-350. (Pubitemid 47443477)
93. Shinohara T, Avarbock MR, Brinster RL. 1999. Beta1- and alpha6-integrin are surface markers on mouse spermatogonial stem cells. Proc Natl Acad Sci USA 96:5504-5509.
94. Stoop H, Honecker F, van de Geijn GJ, Gillis AJ, Cools MC, de Boer M, Bokemeyer C, Wolffenbuttel KP, Drop SL, de Krijger RR, Dennis N, Summersgill B, McIntyre A, Shipley J, Oosterhuis JW, Looijenga LH. 2008. Stem cell factor as a novel diagnostic marker for early malignant germ cells. J Pathol 216:43-54.
95. Suzuki K, Yanagida K, Yanagimachi R. 1998. Comparison of the media for isolation and storage of round spermatid nuclei before intracytoplasmic injection. J Assist Reprod Genet 15:154-157. (Pubitemid 28155260)
96. Szakmary A, Cox DN, Wang Z, Lin H. 2005. Regulatory relationship among piwi, pumilio, and bag-of-marbles in Drosophila germline stem cell self-renewal and differentiation. Curr Biol 15:171-178.
97. Tajima Y, Sawada K, Morimoto T, Nishimune Y. 1994. Switching of mouse spermatogonial proliferation from the c-kit receptor-independent type to the receptor-dependent type during differentiation. J Reprod Fertil 102:117-122. (Pubitemid 24344588)
98. Tokuda M, Kadokawa Y, Kurahashi H, Marunouchi T. 2007. CDH1 is a specific marker for undifferentiated spermatogonia in mouse testes. Biol Reprod 76:130-141. (Pubitemid 46013456)
99. Trupp M, Scott R, Whittemore SR, Ibanez CF. 1999. Ret-dependent and -independent mechanisms of glial cell line-derived neurotrophic factor signaling in neuronal cells. J Biol Chem 274:20885-20894. (Pubitemid 129519586)
100. Tulina N, Matunis E. 2001. Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science 294:2546-2549. (Pubitemid 34027294)
101. Walschaerts M, Huyghe E, Muller A, Bachaud JM, Bujan L, Thonneau P. 2008. Doubling of testicular cancer incidence rate over the last 20 years in southern France. Cancer Causes Control 19:155-161.
102. Weissman IL. 2000. Stem cells: Units of development, units of regeneration, and units in evolution. Cell 100:157-168. (Pubitemid 30046304)
103. Wittinghofer A. 1998. Signal transduction via Ras. Biol Chem 379:933-937.
104. Yamamoto T, Taya S, Kaibuchi K. 1999. Ras-induced transformation and signaling pathway. J Biochem (Tokyo) 126:799-803.
105. Yoon S, Seger R. 2006. The extracellular signal-regulated kinase: Multiple substrates regulate diverse cellular functions. Growth Factors 24:21-44. (Pubitemid 43108774)
106. Yoshida S, Takakura A, Ohbo K, Abe K, Wakabayashi J, Yamamoto M, Suda T, Nabeshima Y. 2004. Neurogenin3 delineates the earliest stages of spermatogenesis in the mouse testis. Dev Biol 269:447-458. (Pubitemid 38521110)
107. Yoshida S, Sukeno M, Nabeshima Y. 2007. A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 317:1722-1726. (Pubitemid 47461832)
108. Yoshinaga K, Nishikawa S, Ogawa M, Hayashi S, Kunisada T, Fujimoto T, Nishikawa S. 1991. Role of c-kit in mouse spermatogenesis: Identification of spermatogonia as a specific site of c-kit expression and function. Development 113:689-699.