In vitro propagation of spermatogonial stem cells from KM mice

Frontiers in Bioscience

Volumn 11, Issue SUPPL. 2, 2006, Pages 2614-2622

  Shi, Yu Qiang ^a   Wang, Qing Zhong ^a,b   Liao, Shang Ying ^a   Zhang, Yan ^a   Liu, Yi Xun ^a   Han, Chun Sheng ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b SHANDONG NORMAL UNIVERSITY   (China)

Author keywords

Glial Cell Line Derived Neurotrophic Factor; Long term culture; Proliferation; Serum Free Culture; Spermatogonial Stem Cell

Indexed keywords

EID: 33744470575     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/1995     Document Type: Article

References (59)

1. ML Meistrich & MEAB van Beek: Spermatogonial stem cells. In: Cell and Molecular Biology of the Testis. Eds: Desjardins C & Ewing LL, Oxford University Press, NY (1993)
2. McLaren, A.: Germ and somatic cell lineages in the developing gonad. Mol Cell Endocrinol, 163, 3-9 (2000)
3. LD Russell, RA Ettlin, AP Hikim & ED Clegg: Mammalian spermatogenesis. In: Histological and histopathological evaluation of the testis. Cache River Press, Clearwater, FL (1990)
4. Chiarini-Garcia, H., A. M. Raymer & L. D. Russell: Non-random distribution of spermatogonia in rats: evidence of niches in the seminiferous tubules. Reproduction, 126, 669-80 (2003)
5. Ohta, H., K. Yomogida, K. Dohmae & Y. Nishimune: Regulation of proliferation and differentiation in spermatogonial stem cells: the role of c-kit and its ligand SCF. Development, 127, 2125-31 (2000)
6. Brinster, R. L. & M. R. Avarbock: Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci U S A, 91, 11303-7 (1994)
7. van Pelt, A. M., H. L. Roepers-Gajadien, I. S. Gademan, L. B. Creemers, D. G. de Rooij & F. M. van Dissel-Emiliani: Establishment of cell lines with rat spermatogonial stem cell characteristics. Endocrinology, 143, 1845-50 (2002)
8. Feng, L. X., Y. Chen, L. Dettin, R. A. Pera, J. C. Herr, E. Goldberg & M. Dym: Generation and in vitro differentiation of a spermatogonial cell line. Science, 297, 392-5 (2002)
9. Nagano, M., M. R. Avarbock, E. B. Leonida, C. J. Brinster & R. L. Brinster: Culture of mouse spermatogonial stem cells. Tissue Cell, 30, 389-97 (1998)
10. Nagano, M., B.-Y. Ryu, C. J. Brinster, M. R. Avarbock & R. L. Brinster: Maintenance of Mouse Male Germ Line Stem Cells In Vitro. Biol Reprod, 68, 2207-2214 (2003)
11. Kubota, H., M. R. Avarbock & R. L. Brinster: Culture conditions and single growth factors affect fate determination of mouse spermatogonial stem cells. Biol Reprod, 71, 722-31 (2004)
12. Kubota, H., M. R. Avarbock & R. L. Brinster: Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci U S A, 101, 16489-94 (2004)
13. Kanatsu-Shinohara, M., N. Ogonuki, K. Inoue, H. Miki, A. Ogura, S. Toyokuni & T. Shinohara: Long-Term Proliferation in Culture and Germline Transmission of Mouse Male Germline Stem Cells. Biol Reprod, 69, 612-616 (2003)
14. Kanatsu-Shinohara, M., H. Miki, K. Inoue, N. Ogonuki, S. Toyokuni, A. Ogura & T. Shinohara: Long-term culture of mouse male germline stem cells under serum-or feeder-free conditions. Biol Reprod, 72, 985-91 (2005)
15. Ogawa, T., M. Ohmura, Y. Tamura, K. Kita, K. Ohbo, T. Suda & Y. Kubota: Derivation and morphological characterization of mouse spermatogonial stem cell lines. Arch Histol Cytol, 67, 297-306 (2004)
16. Ogawa, T., J. M. Arechaga, M. R. Avarbock & R. L. Brinster: Transplantation of testis germinal cells into mouse seminiferous tubules. Int J Dev Biol, 41, 111-22 (1997)
17. Kubota, H., M. R. Avarbock & R. L. Brinster: Spermatogonial stem cells share some, but not all, phenotypic and functional characteristics with other stem cells. Proc Natl Acad Sci U S A, 100, 6487-92 (2003)
18. Anderson, R., K. Schaible, J. Heasman & C. Wylie: Expression of the homophilic adhesion molecule, Ep-CAM, in the mammalian germ line. J Reprod Fertil, 116, 379-84 (1999)
19. Kanatsu-Shinohara, M., S. Toyokuni & T. Shinohara: CD9 Is a Surface Marker on Mouse and Rat Male Germline Stem Cells. Biol Reprod, 70, 70-75 (2004)
20. Kanatsu-Shinohara, M., K. Inoue, J. Lee, M. Yoshimoto, N. Ogonuki, H. Miki, S. Baba, T. Kato, Y. Kazuki, S. Toyokuni, M. Toyoshima, O. Niwa, M. Oshimura, T. Heike, T. Nakahata, F. Ishino, A. Ogura & T. Shinohara: Generation of pluripotent stem cells from neonatal mouse testis. Cell, 119, 1001-12 (2004)
21. Schrans-Stassen, B. H., H. J. van de Kant, D. G. de Rooij & A. M. van Pelt: Differential expression of c-kit in mouse undifferentiated and differentiating type A spermatogonia. Endocrinology, 140, 5894-900 (1999)
22. Meng, X., M. Lindahl, M. E. Hyvonen, M. Parvinen, D. G. de Rooij, M. W. Hess, A. Raatikainen-Ahokas, K. Sainio, H. Rauvala, M. Lakso, J. G. Pichel, H. Westphal, M. Saarma & H. Sariola: Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science, 287, 1489-93 (2000)
23. Yomogida, K., Y. Yagura, Y. Tadokoro & Y. Nishimune: Dramatic expansion of germinal stem cells by ectopically expressed human glial cell line-derived neurotrophic factor in mouse Sertoli cells. Biol Reprod, 69, 1303-7 (2003)
24. Fujiwara, Y., T. Komiya, H. Kawabata, M. Sato, H. Fujimoto, M. Furusawa & T. Noce: Isolation of a DEAD-family protein gene that encodes a murine homolog of Drosophila vasa and its specific expression in germ cell lineage. Proc Natl Acad Sci U S A, 91, 12258-62 (1994)
25. Niederberger, C., A. I. Agulnik, Y. Cho, D. Lamb & C. E. Bishop: In situ hybridization shows that Dazla expression in mouse testis is restricted to premeiotic stages IV-VI of spermatogenesis. Mamm Genome, 8, 277-8 (1997)
26. Moore, F. L., J. Jaruzelska, M. S. Fox, J. Urano, M. T. Firpo, P. J. Turek, D. M. Dorfman & R. A. Pera: Human Pumilio-2 is expressed in embryonic stem cells and germ cells and interacts with DAZ (Deleted in AZoospermia) and DAZ-like proteins. Proc Natl Acad Sci U S A, 100, 538-43 (2003)
27. Kuramochi-Miyagawa, S., T. Kimura, K. Yomogida, A. Kuroiwa, Y. Tadokoro, Y. Fujita, M. Sato, Y. Matsuda & T. Nakano: Two mouse piwi-related genes: miwi and mili. Mech Dev, 108, 121-33 (2001)
28. Yoshida, S., A. Takakura, K. Ohbo, K. Abe, J. Wakabayashi, M. Yamamoto, T. Suda & Y. Nabeshima: Neurogenin3 delineates the earliest stages of spermatogenesis in the mouse testis. Dev Biol, 269, 447-58 (2004)
29. Buaas, F. W., A. L. Kirsh, M. Sharma, D. J. McLean, J. L. Morris, M. D. Griswold, D. G. de Rooij & R. E. Braun: Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet, 36, 647-52 (2004)
30. Nichols, J., B. Zevnik, K. Anastassiadis, H. Niwa, D. Klewe-Nebenius, I. Chambers, H. Scholer & A. Smith: Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell, 95, 379-91 (1998)
31. Kehler, J., E. Tolkunova, B. Koschorz, M. Pesce, L. Gentile, M. Boiani, H. Lomeli, A. Nagy, K. J. McLaughlin, H. R. Scholer & A. Tomilin: Oct4 is required for primordial germ cell survival. EMBO Rep, 5, 1078-83 (2004)
32. Avilion, A. A., S. K. Nicolis, L. H. Pevny, L. Perez, N. Vivian & R. Lovell-Badge: Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev, 17, 126-40 (2003)
33. Chambers, I., D. Colby, M. Robertson, J. Nichols, S. Lee, S. Tweedie & A. Smith: Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell, 113, 643-55 (2003)
34. Mitsui, K., Y. Tokuzawa, H. Itoh, K. Segawa, M. Murakami, K. Takahashi, M. Maruyama, M. Maeda & S. Yamanaka: The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell, 113, 631-42 (2003)
35. Yamaguchi, S., H. Kimura, M. Tada, N. Nakatsuji & T. Tada: Nanog expression in mouse germ cell development. Gene Expr Patterns, 5, 639-46 (2005)
36. Botquin, V., H. Hess, G. Fuhrmann, C. Anastassiadis, M. K. Gross, G. Vriend & H. R. Scholer: New POU dimer configuration mediates antagonistic control of an osteopontin preimplantation enhancer by Oct-4 and Sox-2. Genes Dev, 12, 2073-90 (1998)
37. Nishimoto, M., A. Fukushima, A. Okuda & M. Muramatsu: The gene for the embryonic stem cell coactivator UTF1 carries a regulatory element which selectively interacts with a complex composed of Oct-3/4 and Sox-2. Mol Cell Biol, 19, 5453-65 (1999)
38. Yuan, H., N. Corbi, C. Basilico & L. Dailey: Developmental-specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct-3. Genes Dev, 9, 2635-45 (1995)
39. Okumura-Nakanishi, S., M. Saito, H. Niwa & F. Ishikawa: Oct-3/4 and Sox2 regulate Oct-3/4 gene in embryonic stem cells. J Biol Chem, 280, 5307-17 (2005)
40. Kuroda, T., M. Tada, H. Kubota, H. Kimura, S. Y. Hatano, H. Suemori, N. Nakatsuji & T. Tada: Octamer and Sox elements are required for transcriptional cis regulation of Nanog gene expression. Mol Cell Biol, 25, 2475-85 (2005)
41. Boyer, L. A., T. I. Lee, M. F. Cole, S. E. Johnstone, S. S. Levine, J. P. Zucker, M. G. Guenther, R. M. Kumar, H. L. Murray, R. G. Jenner, D. K. Gifford, D. A. Melton, R. Jaenisch & R. A. Young: Core transcriptional regulatory circuitry in human embryonic stem cells. Cell, 122, 947-56 (2005)
42. Smith, A. G., J. K. Heath, D. D. Donaldson, G. G. Wong, J. Moreau, M. Stahl & D. Rogers: Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature, 336, 688-90 (1988)
43. Williams, R. L., D. J. Hilton, S. Pease, T. A. Willson, C. L. Stewart, D. P. Gearing, E. F. Wagner, D. Metcalf, N. A. Nicola & N. M. Gough: Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature, 336, 684-7 (1988)
44. Farini, D., M. L. Scaldaferri, S. Iona, G. La Sala & M. De Felici: Growth factors sustain primordial germ cell survival, proliferation and entering into meiosis in the absence of somatic cells. Dev Biol, 285, 49-56 (2005)
45. Donovan, P. J.: Growth factor regulation of mouse primordial germ cell development. Curr Top Dev Biol, 29, 189-225 (1994)
46. Smith, A. G.: Embryo-derived stem cells: of mice and men. Annu Rev Cell Dev Biol, 17, 435-62 (2001)
47. Berger, C. N. & K. S. Sturm: Self renewal of embryonic stem cells in the absence of feeder cells and exogenous leukaemia inhibitory factor. Growth Factors, 14, 145-59 (1997)
48. Dani, C., I. Chambers, S. Johnstone, M. Robertson, B. Ebrahimi, M. Saito, T. Taga, M. Li, T. Burdon, J. Nichols & A. Smith: Paracrine induction of stem cell renewal by LIF-deficient cells: a new ES cell regulatory pathway. Dev Biol, 203, 149-62 (1998)
49. Reubinoff, B. E., M. F. Pera, C. Y. Fong, A. Trounson & A. Bongso: Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat Biotechnol, 18, 399-404 (2000)
50. Stewart, C. L., P. Kaspar, L. J. Brunet, H. Bhatt, I. Gadi, F. Kontgen & S. J. Abbondanzo: Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature, 359, 76-9 (1992)
51. Ryu, B. Y., H. Kubota, M. R. Avarbock & R. L. Brinster: Conservation of spermatogonial stem cell self-renewal signaling between mouse and rat. Proc Natl Acad Sci U S A, 102, 14302-7 (2005)
52. Tadokoro, Y., K. Yomogida, H. Ohta, A. Tohda & Y. Nishimune: Homeostatic regulation of germinal stem cell proliferation by the GDNF/FSH pathway. Mech Dev, 113, 29-39 (2002)
53. Sariola, H. & M. Saarma: Novel functions and signalling pathways for GDNF. J Cell Sci, 116, 3855-62 (2003)
54. Paratcha, G., F. Ledda & C. F. Ibanez: The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands. Cell, 113, 867-79 (2003)
55. Scholer, H. R., R. Balling, A. K. Hatzopoulos, N. Suzuki & P. Gruss: Octamer binding proteins confer transcriptional activity in early mouse embryogenesis. Embo J, 8, 2551-7 (1989)
56. Scholer, H. R., A. K. Hatzopoulos, R. Balling, N. Suzuki & P. Gruss: A family of octamer-specific proteins present during mouse embryogenesis: evidence for germline-specific expression of an Oct factor. Embo J, 8, 2543-50 (1989)
57. Rosner, M. H., M. A. Vigano, K. Ozato, P. M. Timmons, F. Poirier, P. W. Rigby & L. M. Staudt: A POU-domain transcription factor in early stem cells and germ cells of the mammalian embryo. Nature, 345, 686-92 (1990)
58. Okamoto, K., H. Okazawa, A. Okuda, M. Sakai, M. Muramatsu & H. Hamada: A novel octamer binding transcription factor is differentially expressed in mouse embryonic cells. Cell, 60, 461-72 (1990)
59. Koshimizu, U., T. Taga, M. Watanabe, M. Saito, Y. Shirayoshi, T. Kishimolo & N. Nakatsuji: Functional requirement of gp130-mediated signaling for growth and survival of mouse primordial germ cells in vitro and derivation of embryonic germ (EG) cells. Development, 122, 1235-42 (1996)