The Identity and Fate Decision Control of Spermatogonial Stem Cells. Where Is the Point of No Return?

Current Topics in Developmental Biology

Volumn 102, Issue , 2013, Pages 61-95

  Nagano, Makoto C ^a   Yeh, Jonathan R ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Cell fate decision; Commitment; Heterogeneity; Regeneration; Stem cell marker

Indexed keywords

EID: 84871747595     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-416024-8.00003-9     Document Type: Chapter

References (125)

1. Adolfsson J., Borge O.J., Bryder D., Theilgaard-Mönch K., Astrand-Grundström I., Sitnicka E., et al. Upregulation of Flt3 expression within the bone marrow Lin(-)Sca1(+)c-kit(+) stem cell compartment is accompanied by loss of self-renewal capacity. Immunity 2001, 15:659-669.
2. Aguirre A., Rubio M.E., Gallo V. Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature 2010, 467:323-327.
3. Ballow D., Meistrich M.L., Matzuk M., Rajkovic A. Sohlh1 is essential for spermatogonial differentiation. Developmental Biology 2006, 294:161-167.
4. Barrios F., Filipponi D., Campolo F., Gori M., Bramucci F., Pellegrini M., et al. SOHLH1 and SOHLH2 control Kit expression during postnatal male germ cell development. Journal of Cell Science 2012, 125:1455-1464.
5. Boyer L.A., Lee T.I., Cole M.F., Johnstone S.E., Levine S.S., Zucker J.P., et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005, 122:947-956.
6. Braydich-Stolle L., Kostereva N., Dym M., Hofmann M.C. Role of Src family kinases and N-Myc in spermatogonial stem cell proliferation. Developmental Biology 2007, 304:34-45.
7. Brinster R.L., Avarbock M.R. Germline transmission of donor haplotype following spermatogonial transplantation. Proceedings of the National Academy of Sciences of the United States of America 1994, 91:11303-11307.
8. Brinster R.L., Zimmermann J.W. Spermatogenesis following male germ-cell transplantation. Proceedings of the National Academy of Sciences of the United States of America 1994, 91:11298-11302.
9. Buaas F.W., Kirsh A.L., Sharma M., McLean D.J., Morris J.L., Griswold M.D., et al. Plzf is required in adult male germ cells for stem cell self-renewal. Nature Genetics 2004, 36:647-652.
10. Bucci L.R., Meistrich M.L. Effects of busulfan on murine spermatogenesis: Cytotoxicity, sterility, sperm abnormalities, and dominant lethal mutations. Mutation Research 1987, 176:259-268.
11. Christensen J.L., Weissman I.L. Flk-2 is a marker in hematopoietic stem cell differentiation: A simple method to isolate long-term stem cells. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:14541-14546.
12. Clouthier D.E., Avarbock M.R., Maika S.D., Hammer R.E., Brinster R.L. Rat spermatogenesis in mouse testis. Nature 1996, 381:418-421.
13. Costoya J.A., Hobbs R.M., Barna M., Cattoretti G., Manova K., Sukhwani M., et al. Essential role of Plzf in maintenance of spermatogonial stem cells. Nature Genetics 2004, 36:653-659.
14. Dann C.T., Alvarado A.L., Molyneux L.A., Denard B.S., Garbers D.L., Porteus M.H. Spermatogonial stem cell self-renewal requires OCT4, a factor downregulated during retinoic acid-induced differentiation. Stem Cells 2008, 26:2928-2937.
15. David G., Alland L., Hong S.H., Wong C.W., DePinho R.A., Dejean A. Histone deacetylase associated with mSin3A mediates repression by the acute promyelocytic leukemia-associated PLZF protein. Oncogene 1998, 16:2549-2556.
16. de Rooij D.G., Okabe M., Nishimune Y. Arrest of spermatogonial differentiation in jsd/jsd, Sl17H/Sl17H, and cryptorchid mice. Biology of Reproduction 1999, 61:842-847.
17. de Rooij D.G., Russell L.D. All you wanted to know about spermatogonia but were afraid to ask. Journal of Andrology 2001, 21:776-798.
18. de Rooij D.G., van Dissel-Emiliani F.M., van Pelt A.M. Regulation of spermatogonial proliferation. Annals of the New York Academy of Sciences 1989, 564:140-153.
19. Dobrinski I., Ogawa T., Avarbock M.R., Brinster R.L. Computer assisted image analysis to assess colonization of recipient seminiferous tubules by spermatogonial stem cells from transgenic donor mice. Molecular Reproduction and Development 1999, 53:142-148.
20. Doulatov S., Notta F., Rice K.L., Howell L., Zelent A., Licht J.D., et al. PLZF is a regulator of homeostatic and cytokine-induced myeloid development. Genes & Development 2009, 23:2076-2087.
21. Ebata K.T., Yeh J.R., Zhang X., Nagano M.C. Soluble growth factors stimulate spermatogonial stem cell divisions that maintain a stem cell pool and produce progenitors in vitro. Experimental Cell Research 2011, 317:1319-1329.
22. Ebata K.T., Zhang X., Nagano M.C. Expression patterns of cell-surface molecules on male germ line stem cells during postnatal mouse development. Molecular Reproduction and Development 2005, 72:171-181.
23. Ebata K.T., Zhang X., Nagano M.C. Male germ line stem cells have an altered potential to proliferate and differentiate during postnatal development in mice. Biology of Reproduction 2007, 76:841-847.
24. Fernando P., Brunette S., Megeney L.A. Neural stem cell differentiation is dependent upon endogenous caspase 3 activity. The FASEB Journal 2005, 19:1671-1673.
25. Filipponi D., Hobbs R.M., Ottolenghi S., Rossi P., Jannini E.A., Pandolfi P.P., et al. Repression of kit expression by Plzf in germ cells. Molecular and Cellular Biology 2007, 27:6770-6781.
26. França L.R., Ogawa T., Avarbock M.R., Brinster R.L., Russell L.D. Germ cell genotype controls cell cycle during spermatogenesis in the rat. Biology of Reproduction 1998, 59:1371-1377.
27. Fujita J., Crane A.M., Souza M.K., Dejosez M., Kyba M., Flavell R.A., et al. Caspase activity mediates the differentiation of embryonic stem cells. Cell Stem Cell 2008, 2:595-601.
28. Fuller M.T., Spradling A.C. Male and female Drosophila germline stem cells: Two versions of immortality. Science 2007, 316:402-404.
29. Giuili G., Tomljenovic A., Labrecque N., Oulad-Abdelghani M., Rassoulzadegan M., Cuzin F. Murine spermatogonial stem cells: Targeted transgene expression and purification in an active state. EMBO Reports 2002, 3:753-759.
30. Grasso M., Fuso A., Dovere L., de Rooij D.G., Stefanini M., Boitani C., et al. Distribution of GFRA1-expressing spermatogonia in adult mouse testis. Reproduction 2012, 143:325-332.
31. Greenbaum M.P., Iwamori T., Buchold G.M., Matzuk M.M. Germ cell intercellular bridges. Cold Spring Harbor Perspectives in Biology 2011, 3:a005850.
32. Hamra F.K., Chapman K.M., Nguyen D., Garbers D.L. Identification of neuregulin as a factor required for formation of aligned spermatogonia. The Journal of Biological Chemistry 2007, 282:721-730.
33. Hamra F.K., Schultz N., Chapman K.M., Grellhesl D.M., Cronkhite J.T., Hammer R.E., et al. Defining the spermatogonial stem cell. Developmental Biology 2004, 269:393-410.
34. Han I.S., Sylvester S.R., Kim K.H., Schelling M.E., Venkateswaran S., Blanckaert V.D., et al. Basic fibroblast growth factor is a testicular germ cell product which may regulate Sertoli cell function. Molecular Endocrinology 1993, 7:889-897.
35. Hao J., Yamamoto M., Richardson T.E., Chapman K.M., Denard B.S., Hammer R.E., et al. Sohlh2 knockout mice are male-sterile because of degeneration of differentiating type A spermatogonia. Stem Cells 2008, 26:1587-1597.
36. Hayashi K., de Sousa Chuva, Lopes S.M., Kaneda M., Tang F., Hajkova P., et al. MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis. PloS One 2008, 3:e1738.
37. Henrique D. On equivalence groups and the Notch/LN-12 communication system. Stem cell biology 2001, 37-60. Cold Spring Harbor Laboratory Press, New York. D.R. Marshak, R.L. Gardner, D. Gottlieb (Eds.).
38. Hobbs R.M., Fagoonee S., Papa A., Webster K., Altruda F., Nishinakamura R., et al. Functional antagonism between Sall4 and Plzf defines germline progenitors. Cell Stem Cell 2012, 10:284-298.
39. Hobbs R.M., Seandel M., Falciatori I., Rafii S., Pandolfi P.P. Plzf regulates germline progenitor self-renewal by opposing mTORC1. Cell 2010, 142:468-479.
40. Huckins C. The spermatogonial stem cell population in adult rats. I. Their morphology, proliferation and maturation. The Anatomical Record 1971, 169:533-557.
41. Ishii K., Kanatsu-Shinohara M., Toyokuni S., Shinohara T. FGF2 mediates mouse spermatogonial stem cell self-renewal via upregulation of Etv5 and Bcl6b through MAP2K1 activation. Development 2012, 139:1734-1743.
42. Janzen V., Fleming H.E., Riedt T., Karlsson G., Riese M.J., Lo Celso C., et al. Hematopoietic stem cell responsiveness to exogenous signals is limited by caspase-3. Cell Stem Cell 2008, 2:584-594.
43. Kanatsu-Shinohara M., Inoue K., Miki H., Ogonuki N., Takehashi M., Morimoto T., et al. Clonal origin of germ cell colonies after spermatogonial transplantation in mice. Biology of Reproduction 2006, 75:68-74.
44. Kanatsu-Shinohara M., Miki H., Inoue K., Ogonuki N., Toyokuni S., Ogura A., et al. Long-term culture of mouse male germline stem cells under serum-or feeder-free conditions. Biology of Reproduction 2005, 72:985-991.
45. Kanatsu-Shinohara M., Ogonuki N., Inoue K., Miki H., Ogura A., Toyokuni S., et al. Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biology of Reproduction 2003, 69:612-616.
46. Kanatsu-Shinohara M., Takashima S., Ishii K., Shinohara T. Dynamic changes in EPCAM expression during spermatogonial stem cell differentiation in the mouse testis. PLoS One 2011, 6:e23663.
47. Kanatsu-Shinohara M., Toyokuni S., Shinohara T. CD9 is a surface marker on mouse and rat male germline stem cells. Biology of Reproduction 2004, 70:70-75.
48. Kanellopoulou C., Muljo S.A., Kung A.L., Ganesan S., Drapkin R., Jenuwein T., et al. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes & Development 2005, 19:489-501.
49. Kaucher A.V., Oatley M.J., Oatley J.M. NEUROG3 is a critical downstream effector for STAT3-regulated differentiation of mammalian stem and progenitor spermatogonia. Biology of Reproduction 2012, 86:164-174.
50. Kiel M.J., Yilmaz O.H., Iwashita T., Yilmaz O.H., Terhorst C., Morrison S.J. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 2005, 121:1109-1121.
51. Klein A.M., Nakagawa T., Ichikawa R., Yoshida S., Simons B.D. Mouse germ line stem cells undergo rapid and stochastic turnover. Cell Stem Cell 2010, 7:214-224.
52. Kubota H., Avarbock M.R., Brinster R.L. Spermatogonial stem cells share some, but not all, phenotypic and functional characteristics with other stem cells. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:6487-6492.
53. Kubota H., Avarbock M.R., Brinster R.L. Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:16489-16494.
54. Kunath T., Saba-El-Leil M.K., Almousailleakh M., Wray J., Meloche S., Smith A. FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development 2007, 134:2895-2902.
55. Labbaye C., Quaranta M.T., Pagliuca A., Militi S., Licht J.D., Testa U., et al. PLZF induces megakaryocytic development, activatesTpo receptor expression and interacts with GATA1 protein. Oncogene 2002, 21:6669-6679.
56. Leblond C.P., Clermont Y. Spermiogenesis of rat, mouse, hamster and guinea pig as revealed by the periodic acid-fuchsin sulfurous acid technique. The American Journal of Anatomy 1952, 90:167-215.
57. Lee J., Kanatsu-Shinohara M., Inoue K., Ogonuki N., Miki H., Toyokuni S., et al. Akt mediates self-renewal division of mouse spermatogonial stem cells. Development 2007, 134:1853-1859.
58. Lee J., Kanatsu-Shinohara M., Morimoto H., Kazuki Y., Takashima S., Oshimura M., et al. Genetic reconstruction of mouse spermatogonial stem cell self-renewal in vitro by Ras-cyclin D2 activation. Cell Stem Cell 2009, 5:76-86.
59. Lee J., Shinohara T. Epigenetic modifications and self-renewal regulation of mouse germline stem cells. Cell Research 2011, 21:1164-1171.
60. Melton C., Judson R.L., Blelloch R. Opposing microRNA familiesregulate self-renewal in mouse embryonic stem cells. Nature 2010, 463:621-626.
61. Meng X., Lindahl M., Hyvönen M.E., Parvinen M., de Rooij D.G., Hess M.W., et al. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 2000, 287:1489-1493.
62. Mondal B.C., Mukherjee T., Mandal L., Evans C.J., Sinenko S.A., Martinez-Agosto J.A., et al. Interaction between differentiating cell- and niche-derived signals in hematopoietic progenitor maintenance. Cell 2011, 147:1589-1600.
63. Mullaney B.P., Skinner M.K. Basic fibroblast growth factor (bFGF) gene expression and protein production during pubertal development of the seminiferous tubule: Follicule-stimulating hormone-induced Sertoli cell bFGF expression. Endocrinology 1992, 131:2928-2934.
64. Murchison E.P., Partridge J.F., Tam O.H., Cheloufi S., Hannon G.J. Characterization of Dicer-deficient murine embryonic stem cells. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:12135-12140.
65. Nagano M.C. Homing efficiency and proliferation kinetics of male germ line stem cells following transplantation in mice. Biology of Reproduction 2003, 69:701-707.
66. Nagano M., Avarbock M.R., Brinster R.L. Pattern and kinetics of mouse donor spermatogonial stem cell colonization in recipient testes. Biology of Reproduction 1999, 60:1429-1436.
67. Nakagawa T., Nabeshima Y., Yoshida S. Functional identification of the actual and potential stem cell compartments in mouse spermatogenesis. Developmental Cell 2007, 12:195-206.
68. Nakagawa T., Sharma M., Nabeshima Y., Braun R.E., Yoshida S. Functional hierarchy and reversibility within the murine spermatogenic stem cell compartment. Science 2010, 328:62-67.
69. Niu Z., Goodyear S.M., Rao S., Wu X., Tobias J.W., Avarbock M.R., et al. MicroRNA-21 regulates the self-renewal of mouse spermatogonial stem cells. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:12740-12745.
70. Niwa H., Miyazaki J., Smith A.G. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nature Genetics 2000, 24:372-376.
71. Oakberg E.F. Spermatogonial stem-cell renewal in the mouse. The Anatomical Record 1971, 169:515-531.
72. Oatley J.M., Avarbock M.R., Brinster R.L. 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. The Journal of Biological Chemistry 2007, 282:25842-25851.
73. Oatley J.M., Avarbock M.R., Telaranta A.I., Fearon D.T., Brinster R.L. Identifying genes important for spermatogonial stem cell self-renewal and survival. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:9524-9529.
74. Oatley J.M., Brinster R.L. Regulation of spermatogonial stem cell self-renewal in mammals. Annual Review of Cell and Developmental Biology 2008, 24:263-286.
75. Oatley J.M., Brinster R.L. The germline stem cell niche unit in mammalian testes. Physiological Reviews 2012, 92:577-595.
76. Oatley J.M., Kaucher A.V., Avarbock M.R., Brinster R.L. Regulation of mouse spermatogonial stem cell differentiation by STAT3 signaling. Biology of Reproduction 2010, 83:427-433.
77. Oatley M.J., Kaucher A.V., Racicot K.E., Oatley J.M. 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. Biology of Reproduction 2011, 85:347-456.
78. Oatley J.M., Oatley M.J., Avarbock M.R., Tobias J.W., Brinster R.L. Colony stimulating factor 1 is an extrinsic stimulator of mouse spermatogonial stem cell self-renewal. Development 2009, 136:1191-1199.
79. Ohta H., Yomogida K., Yamada S., Okabe M., Nishimune Y. Real-time observation of transplanted 'green germ cells': Proliferation and differentiation of stem cells. Development, Growth & Differentiation 2000, 42:105-112.
80. O'Shaughnessy P.J., Hu L., Baker P.J. Effect of germ cell depletion on levels of specific mRNA transcripts in mouse Sertoli cells and Leydig cells. Reproduction 2008, 135:839-850.
81. Phillips B.T., Gassei K., Orwig K.E. Spermatogonial stem cell regulation and spermatogenesis. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 2010, 365:1663-1678.
82. Rappolee D.A., Basilico C., Patel Y., Werb Z. Expression and function of FGF-4 in peri-implantation development in mouse embryos. Development 1994, 120:2259-2269.
83. Reynolds B.A., Rietze R.L. Neural stem cells and neurospheres-Re-evaluating the relationship. Nature Methods 2005, 2:333-336.
84. Ryu B.Y., Orwig K.E., Oatley J.M., Avarbock M.R., Brinster R.L. Effects of aging and niche microenvironment on spermatogonial stem cell self-renewal. Stem Cells 2006, 24:1505-1511.
85. Sabatini D.M. mTOR and cancer: Insights into a complex relationship. Nature Reviews. Cancer 2006, 6:729-734.
86. Sada A., Hasegawa K., Pin P.H., Saga Y. NANOS2 acts downstream of glial cell line-derived neurotrophic factor signaling to suppress differentiation of spermatogonial stem cells. Stem Cells 2012, 30:280-291.
87. Sada A., Suzuki A., Suzuki H., Saga Y. The RNA-binding protein NANOS2 is required to maintain murine spermatogonial stem cells. Science 2009, 325:1394-1398.
88. Sato T., van Es J.H., Snippert H.J., Stange D.E., Vries R.G., Es J.H., et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 2011, 469:415-418.
89. Savitt J., Singh D., Zhang C., Chen L.C., Folmer J., Shokat K.M., et al. The in vivo response of stem and other undifferentiated spermatogonia to the reversible inhibition of glial cell line-derived neurotrophic factor signaling in the adult. Stem Cells 2012, 30:732-740.
90. Schlesser H.N., Simon L., Hofmann M.C., Murphy K.M., Murphy T., Hess R.A., et al. Effects of ETV5 (ets variant gene 5) on testis and body growth, time course of spermatogonial stem cell loss, and fertility in mice. Biology of Reproduction 2008, 78:483-489.
91. Shinohara T., Avarbock M.R., Brinster R.L. beta1- and alpha6-integrin are surface markers on mouse spermatogonial stem cells. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:5504-5509.
92. Shinohara T., Orwig K.E., Avarbock M.R., Brinster R.L. Spermatogonial stem cell enrichment by multiparameter selection of mouse testis cells. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:8346-8351.
93. Silva J., Smith A. Capturing pluripotency. Cell 2008, 132:532-536.
94. Simchen G. Commitment to meiosis: What determines the mode of division in budding yeast?. BioEssays 2009, 31:169-177.
95. Simchen G., Pinon R., Salts Y. Sporulation in Saccharomyces cerevisiae: Premeiotic DNA synthesis, readiness and commitment. Experimental Cell Research 1972, 75:207-218.
96. Simon L., Ekman G.C., Garcia T., Carnes K., Zhang Z., Murphy T., et al. ETV5 regulates sertoli cell chemokines involved in mouse stem/progenitor spermatogonia maintenance. Stem Cells 2010, 28:1882-1892.
97. Sommer R.J. As good as they get: Cells in nematode vulva development and evolution. Current Opinion in Cell Biology 2001, 13:715-720.
98. Subramanyam D., Blelloch R. From microRNAs to targets: Pathway discovery in cell fate transitions. Current Opinion in Genetics & Development 2011, 21:498-503.
99. Suh N., Blelloch R. Small RNAs in early mammalian development: From gametes to gastrulation. Development 2011, 138:1653-1661.
100. Suzuki H., Ahn H.W., Chu T., Bowden W., Gassei K., Orwig K., et al. SOHLH1 and SOHLH2 coordinate spermatogonial differentiation. Developmental Biology 2012, 361:301-312.
101. Suzuki A., Igarashi K., Aisaki K., Kanno J., Saga Y. NANOS2 interacts with the CCR4-NOT deadenylation complex and leads to suppression of specific RNAs. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:3594-3599.
102. Suzuki H., Sada A., Yoshida S., Saga Y. The heterogeneity of spermatogonia is revealed by their topology and expression of marker proteins including the germ cell-specific proteins Nanos2 and Nanos3. Developmental Biology 2009, 336:222-231.
103. Tegelenbosch R.A., de Rooij D.G. A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101 F1 hybrid mouse. Mutation Research 1993, 290:193-200.
104. Tokuda M., Kadokawa Y., Kurahashi H., Marunouchi T. CDH1 is a specific marker for undifferentiated spermatogonia in mouse testes. Biology of Reproduction 2007, 76:130-141.
105. Tong M.H., Mitchell D., Evanoff R., Griswold M.D. Expression of Mirlet7 family microRNAs in response to retinoic acid-induced spermatogonial differentiation in mice. Biology of Reproduction 2011, 85:189-197.
106. Toyoda S., Miyazaki T., Miyazaki S., Yoshimura T., Yamamoto M., Tashiro F., et al. Sohlh2 affects differentiation of KIT positive oocytes and spermatogonia. Developmental Biology 2009, 325:238-248.
107. Tsuda M., Sasaoka Y., Kiso M., Abe K., Haraguchi S., Kobayashi S., et al. Conserved role of nanos proteins in germ cell development. Science 2009, 301:1239-1241.
108. van den Aardweg G.J., de Ruiter-Bootsma A.L., Kramer M.F., Davids J.A. Growth and differentiation of spermatogenetic colonies in the mouse testis after irradiation with fission neutrons. Radiation Research 1983, 94:447-463.
109. van Pelt A.M., de Rooij D.G. Synchronization of the seminiferous epithelium after vitamin A replacement in vitamin A-deficient mice. Biology of Reproduction 1990, 43:363-367.
110. van Pelt A.M., de Rooij D.G. Retinoic acid is able to reinitiate spermatogenesis in vitamin A-deficient rats and high replicate doses support the full development of spermatogenic cells. Endocrinology 1991, 128:697-704.
111. Wang Y., Medvid R., Melton C., Jaenisch R., Blelloch R. DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nature Genetics 2007, 39:380-385.
112. Weissman I.L. Translating stem and progenitor cell biology to the clinic: Barriers and opportunities. Science 2000, 287:1442-1446.
113. Wu X., Oatley J.M., Oatley M.J., Kaucher A.V., Avarbock M.R., Brinster R.L. The POU domain transcription factor POU3F1 is an important intrinsic regulator of GDNF-induced survival and self-renewal of mouse spermatogonial stem cells. Biology of Reproduction 2010, 82:1103-1111.
114. Yeh J.R., Zhang X., Nagano M.C. Establishment of a short-term in vitro assay for mouse spermatogonial stem cells. Biology of Reproduction 2007, 77:897-904.
115. Yeh J.R., Zhang X., Nagano M.C. Wnt5a is a cell-extrinsic factor that supports self-renewal of mouse spermatogonial stem cells. Journal of Cell Science 2011, 124:2357-2366.
116. Yeh J.R., Zhang X., Nagano M.C. Indirect Effects of Wnt3a/β-Catenin Signalling Support Mouse Spermatogonial Stem Cells In Vitro. PLoS One 2012, 7:e40002.
117. Ying Q.L., Wray J., Nichols J., Batlle-Morera L., Doble B., Woodgett J., et al. The ground state of embryonic stem cell self-renewal. Nature 2008, 453:519-523.
118. Yoshida S. Stem cells in mammalian spermatogenesis. Development, Growth & Differentiation 2010, 52:311-317.
119. Yoshida S., Sukeno M., Nabeshima Y. A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 2007, 317:1722-1726.
120. Zhang X., Ebata K.T., Nagano M.C. Genetic analysis of the clonal origin of regenerating mouse spermatogenesis following transplantation. Biology of Reproduction 2003, 69:1872-1878.
121. Zhang X., Ebata K.T., Robaire B., Nagano M.C. Aging of male germ line stem cells in mice. Biology of Reproduction 2006, 74:119-124.
122. Zhou Q., Li Y., Nie R., Friel P., Mitchell D., Evanoff R.M., et al. Expression of stimulated by retinoic acid gene 8 (Stra8) and maturation of murine gonocytes and spermatogonia induced by retinoic acid in vitro. Biology of Reproduction 2008, 78:537-545.
123. Zhou Q., Nie R., Li Y., Friel P., Mitchell D., Hess R.A., et al. 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. Biology of Reproduction 2008, 79:35-42.
124. Zhou S., Schuetz J.D., Bunting K.D., Colapietro A.M., Sampath J., Morris J.J., et al. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nature Medicine 2001, 7:1028-1034.
125. Zohni K., Zhang X., Tan S.L., Chan P., Nagano M.C. The efficiency of male fertility restoration is dependent on the recovery kinetics of spermatogonial stem cells after cytotoxic treatment with busulfan in mice. Human Reproduction 2012, 27:44-53.