Spermatogonial stem cells: Unlimited potential

Reproduction, Fertility and Development

Volumn 21, Issue 1, 2009, Pages 15-21

  Dym, M ^a   He, Z ^a   Jiang, J ^a   Pant, D ^a   Kokkinaki, M ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Differentiation; Embryonic stem cells; GFRA1; GPR125; Pluripotency; Renewal

Indexed keywords

CELL MARKER; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 125; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR FAMILY RECEPTOR ALPHA 1; UNCLASSIFIED DRUG;

ANIMAL CELL; CELL DIFFERENTIATION; CELL REGENERATION; CELL RENEWAL; CONFERENCE PAPER; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; FEMALE; FERTILIZATION IN VITRO; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MALE; MEDICAL ETHICS; MOUSE; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; SKIN CELL; SOMATIC CELL; SPERMATOGONIUM; STEM CELL; TESTIS BIOPSY;

ANIMALS; CELL DIFFERENTIATION; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR RECEPTORS; HUMANS; MALE; MICE; PLURIPOTENT STEM CELLS; RECEPTORS, G-PROTEIN-COUPLED; SPERMATOGONIA;

MUS;

EID: 57449086427     PISSN: 10313613     EISSN: None     Source Type: Journal    
DOI: 10.1071/RD08221     Document Type: Conference Paper

References (55)

1. Aoi, T., Yae, K., Nakagawa, M., Ichisaka, T., Okita, K., Takahashi, K., Chiba, T., and Yamanaka, S. (2008). Generation of pluripotent stem cells from adult mouse liver and stomach cells. Science 321, 699-702. doi:10.1126/SCIENCE.1154884
2. Brawley, C., and Matunis, E. (2004). Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo. Science 304, 1331-1334. doi:10.1126/SCIENCE.1097676
3. Brinster, R. L., and Avarbock, M. R. (1994). Germ line transmission of donor haplotype following spermatogonial transplantation. Proc. Natl Acad. Sci. USA 91, 11 303-11 307. doi:10.1073/PNAS.91.24.11303
4. Brinster, R. L., and Zimmerman, J. W. (1994). Spermatogenesis following male germ cell transplantation. Proc. Natl Acad. Sci. USA 91, 11 298-11 302. doi:10.1073/PNAS.91.24.11298
5. Buaas, F. W., Kirsh, A. L., Sharma, M., McLean, D. J., Morris, J. L., Griswold, M. D., de Rooij, D. G., and Braun, R. E. (2004). Plzf is required in adult male germ cells for stem cell self-renewal. Nat. Genet. 36, 647-652. doi:10.1038/NG1366
6. Buageaw, A., Sukhwani, M., Ben-Yehudah, A., Ehmcke, J., Rawe, V. Y., Pholpramool, C., Orwig, K. E., and Schlatt, S. (2005). GDNF family receptor alpha1 phenotype of spermatogonial stem cells in immature mouse testes. Biol. Reprod. 73, 1011-1016. doi:10.1095/BIOLREPROD.105.043810
7. Clermont, Y. (1963). The cycle of the seminiferous epithelium in man. Am. J. Anat. 112, 35-51. doi:10.1002/AJA.1001120103
8. Clermont, Y. (1966a). Renewal of spermatogonia in man. Am. J. Anat. 118, 509-524. doi:10.1002/AJA.1001180211
9. Clermont, Y. (1966b). Spermatogenesis in man. A study of the spermatogonial population. Fertil. Steril. 17, 705-721.
10. Clermont, Y. (1972). Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol. Rev. 52, 198-236.
11. Clermont, Y., and Bustos-Obregon, E. (1968). Re-examination of spermatogonial renewal in the rat by means of seminiferous tubules mounted 'in toto'. Am. J. Anat. 122, 237-247. doi:10.1002/AJA.1001220205
12. Conrad, S., Renninger, M., Hennenlotter, J., Wiesner, T., Just, L., et al. (2008). Generation of pluripotent stem cells from adult human testis. Nature, in press. doi:10.1038/NATURE07404
13. Costoya, J. A., Hobbs, R. M., Barna, M., Cattoretti, G., Manova, K., Sukhwani, M., Orwig, K. E., Wolgemuth, D. J., and Pandolfi, P. P. (2004). Essential role of Plzf in maintenance of spermatogonial stem cells. Nat. Genet. 36, 653-659. doi:10.1038/NG1367
14. Dann, C. T., Alvarado, A. L., Molyneux, L. A., Denard, B. S., Garbers, D. L., and Porteus, M. H. (2008). Spermatogonial stem cell self renewal requires OCT4, a factor down-regulated during retinoic acid induced differentiation. Stem Cells, in press.
15. de Rooij, D. G., and Grootegoed, J. A. (1998). Spermatogonial stem cells. Curr. Opin. Cell Biol. 10, 694-701. doi:10.1016/S0955-0674(98) 80109-9
16. de Rooij, D. G., and Russell, L. D. (2000). All you wanted to know about spermatogonia but were afraid to ask. J. Androl. 21, 776-798.
17. Dobrinski, I., Avarbock, M. R., and Brinster, R. L. (1999). Transplantation of germ cells from rabbits and dogs into mouse testes. Biol. Reprod. 61, 1331-1339. doi:10.1095/BIOLREPROD61.5.1331
18. Dobrinski, I., Avarbock, M. R., and Brinster, R. L. (2000). Germ cell transplantation from large domestic animals into mouse testes. Mol. Reprod. Dev. 57, 270-279. doi:10.1002/1098-2795(200011)57:3〈270:: AIDMRD9〉 3.0.CO;2-Z
19. Dym, M. (1994). Spermatogonial stem cells of the testis. Proc. Natl Acad. Sci. USA 91, 11 287-11 289. doi:10.1073/PNAS.91.24.11287
20. Dym, M., and 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. doi:10.1002/AJA.1001280302
21. Dym, M., and Fawcett, D. W. (1971). Further observations on the numbers of spermatogonia, spermatocytes, and spermatids connected by intercellular bridges in the mammalian testis. Biol. Reprod. 4, 195-215.
22. Ehmcke, J., and Schlatt, S. (2006). A revised model for spermatogonial expansion in man: lessons from non-human primates. Reproduction 132, 673-680. doi:10.1530/REP.1.01081
23. Golestaneh, N., Kokkinaki, M., Jiang, J., DeStefano, D., Fernandez-Bueno, C., Gallicano, Y., and Dym, M. (2007). Human sperm stem cells can 'de-differentiate' into pluripotency. In 'Proceedings of the American Society of Cell Biology, Annual Meeting'.
24. Greenbaum, M. P., Yan, W., Wu, M. H., Lin, Y. N., Agno, J. E., Sharma, M., Braun, R. E., Rajkovic, A., and Matzuk, M. M. (2006). TEX14 is essential for intercellular bridges and fertility in male mice. Proc. Natl Acad. Sci. USA 103, 4982-4987. doi:10.1073/PNAS.0505123103
25. Guan, K., Nayernia, K., Maier, L. S., Wagner, S., Dressel, R., et al. (2006). Pluripotency of spermatogonial stem cells from adult mouse testis. Nature 440, 1199-1203. doi:10.1038/NATURE04697
26. Hanna, J., Wernig, M., Markoulaki, S., Sun, C. W., Meissner, A., et al. (2007). Treatment of sickle cell anemia mouse model with iPS cells generated from autologous skin. Science 318, 1920-1923. doi:10.1126/ SCIENCE.1152092
27. He, Z., Jiang, J., Hofmann, M. C., and 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.
28. Hermann, B. P., Sukhwani, M., Lin, C. C., Sheng, Y., Tomko, J., et al. (2007). Characterization, cryopreservation, and ablation of spermatogonial stem cells in adult rhesus macaques. Stem Cells 25, 2330-2338. doi:10.1634/STEMCELLS.2007-0143
29. Hofmann, M. C., Braydich-Stolle, L., Dettin, L., Johnson, E., and Dym, M. (2005a). Immortalization of mouse germ line stem cells. Stem Cells 23, 200-210. doi:10.1634/STEMCELLS.2003-0036
30. Hofmann, M. C., Braydich-Stolle, L., and Dym, M. (2005b). Isolation of male germ-line stem cells; influence of GDNF. Dev. Biol. 279, 114-124. doi:10.1016/J.YDBIO.2004.12.006
31. Huckins, C. (1971). The spermatogonial stem cell population in adult rats. I. Their morphology, proliferation and maturation. Anat. Rec. 169, 533-557. doi:10.1002/AR.1091690306
32. Kanatsu-Shinohara, M., Inoue, K., Lee, J., Yoshimoto, M., Ogonuki, N., et al. (2004). Generation of pluripotent stem cells from neonatal mouse testis. Cell 119, 1001-1012. doi:10.1016/J.CELL.2004.11.011
33. Kim, K., Lerou, P., Yabuuchi, A., Lengerke, C., Ng, K., West, J., Kirby, A., Daly, M. J., and Daley, G. Q. (2007). Histocompatible embryonic stem cells by parthenogenesis. Science 315, 482-486. doi:10.1126/ SCIENCE.1133542
34. Kim, J. B., Zaehres, H., Wu, G., Gentile, L., Ko, K., et al. (2008). Pluripotent stem cells induced from adult neural stem cells by reprogramming with two factors. Nature 454, 646-650. doi:10.1038/NATURE07061
35. Kim, N. W., Piatyszek, M. A., Prowse, K. R., Harley, C. B., West, M. D., Ho, P. L., Coviello, G. M., Wright, W. E., Weinrich, S. L., and Shay, J. W. (1994). Specific association of human telomerase activity with immortal cells and cancer. Science 266, 2011-2015. doi:10.1126/ SCIENCE.7605428
36. Meissner, A., Wernig, M., and Jaenisch, R. (2007). Direct reprogramming of genetically unmodified fibroblasts into pluripotent stem cells. Nat. Biotechnol. 25, 1177-1181. doi:10.1038/NBT1335
37. Meng, X., Lindahl, M., Hyvonen, M. E., Parvinen, M., de Rooij, D. G., et al. (2000). Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 287, 1489-1493. doi:10.1126/SCIENCE.287. 5457.1489
38. Nagano, M., McCarrey, J. R., and Brinster, R. L. (2001). Primate spermatogonial stem cells colonize mouse testes. Biol. Reprod. 64, 1409-1416. doi:10.1095/BIOLREPROD64.5.1409
39. Nagano, M., Patrizio, P., and Brinster, R. L. (2002). Long-term survival of human spermatogonial stem cells in mouse testes. Fertil. Steril. 78, 1225-1233. doi:10.1016/S0015-0282(02)04345-5
40. Naughton, C. K., Jain, S., Strickland, A. M., Gupta, A., and Milbrandt, J. (2006). Glial cell-line derived neurotrophic factor-mediated RET signaling regulates spermatogonial stem cell fate. Biol. Reprod. 74, 314-321. doi:10.1095/BIOLREPROD.105.047365
41. Oakberg, E. F. (1971). Spermatogonial stem-cell renewal in the mouse. Anat. Rec. 169, 515-531. doi:10.1002/AR.1091690305
42. Ohbo, K., Yoshida, S., Ohmura, M., Ohneda, O., Ogawa, T., et al. (2003). Identification and characterization of stem cells in prepubertal spermatogenesis in mice small star, filled. Dev. Biol. 258, 209-225. doi:10.1016/S0012-1606(03)00111-8
43. Ohmura, M., Yoshida, S., Ide, Y., Nagamatsu, G., Suda, T., and Ohbo, K. (2004). Spatial analysis of germ stem cell development in Oct-4/EGFP transgenic mice. Arch. Histol. Cytol. 67, 285-296. doi:10.1679/AOHC.67.285
44. Okita, K., Ichisaka, T., and Yamanaka, S. (2007). Generation of germline-competent induced pluripotent stem cells. Nature 448, 313-317. doi:10.1038/NATURE05934
45. Orwig, K. E., Shinohara, T., Avarbock, M. R., and Brinster, R. L. (2002). Functional analysis of stem cells in the adult rat testis. Biol. Reprod. 66, 944-949.
46. Ramalho-Santos, M., and Willenbring, H. (2007). On the origin of the term 'stem cell'. Cell Stem Cell 1, 35-38. doi:10.1016/J.STEM.2007.05. 013
47. Regaud, C. (1901). Études sur la structure des tubes séminiféres et sur la spermatogénèse chez les mammifères. Archives d'Anatomie Microscopiques et de Morphologie Expérimentale 4, 101-156.
48. Sanchez-Pernaute, R., Lee, H., Patterson, M., Reske-Nielsen, C., Yoshizaki, T., Sonntag, K. C., Studer, L., and Isacson, O. (2008). Parthenogenetic dopamine neurons from primate embryonic stem cells restore function in experimental Parkinson's disease. Brain 131, 2127-2139. doi:10.1093/BRAIN/AWN144
49. Seandel, M., James, D., Shmelkov, S. V., Falciatori, I., Kim, J., et al. (2007). Generation of functional multipotent adult stem cells from GPR125+ germline progenitors. Nature 449, 346-350. doi:10.1038/NATURE06129
50. Stadtfeld, M., Nagaya, M., Utikal, J., Weir, G., and Hochedlinger, K. (2008). Induced pluripotent stem cells generated without viral integration. ScienceXpress, in press.
51. Takahashi, K., and Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676. doi:10.1016/J.CELL.2006.07.024
52. Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., and Yamanaka, S. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872. doi:10.1016/J.CELL.2007.11.019
53. Wernig, M., Meissner, A., Foreman, R., Brambrink, T., Ku, M., Hochedlinger, K., Bernstein, B. E., and Jaenisch, R. (2007). In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448, 318-324. doi:10.1038/NATURE05944
54. Yoshida, S., Nabeshima, Y., and Nakagawa, T. (2008). Stem cell heterogeneity: actual and potential stem cell compartments in mouse spermatogenesis. Ann. N. Y. Acad. Sci. 1120, 47-58. doi:10.1196/ANNALS.1411.003
55. Yoshinaga, K., Nishikawa, S., Ogawa, M., Hayashi, S., Kunisada, T., Fujimoto, T., and 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.