Transplantation of male germ line stem cells restores fertility in infertile mice

Nature Medicine

Volumn 6, Issue 1, 2000, Pages 29-34

  Ogawa, Takehiko ^a,b   Dobrinski, Ina ^a,c   Avarbock, Mary R ^a   Brinster, Ralph L ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b YOKOHAMA CITY UNIVERSITY   (Japan)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; AZOOSPERMIA; GERM LINE; MALE; MALE INFERTILITY; MOUSE; MUTANT; NONHUMAN; OLIGOSPERMIA; PRIORITY JOURNAL; PROGENY; SPERMATOGENESIS; STEM CELL TRANSPLANTATION;

ANIMALS; CELL TRANSPLANTATION; CROSSES, GENETIC; FEMALE; FERTILITY; HOMOZYGOTE; HUMANS; INFERTILITY, MALE; MALE; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; PROTO-ONCOGENE PROTEINS C-KIT; SEMINIFEROUS TUBULES; SPERMATOGENESIS; SPERMATOZOA; STEM CELL FACTOR;

ANIMALIA;

EID: 0033966174     PISSN: 10788956     EISSN: None     Source Type: Journal    
DOI: 10.1038/71496     Document Type: Article

References (45)

1. Greenberg, S.H., Lipshultz, L.I. & Wein, A.J. Experience with 425 subfertile male patients. J. Urol. 119, 507-510 (1978).
2. rd ed. (eds. Lipshulz, L.I. & Howard, S.S.) 173-193 (Mosby, St. Louis, 1997).
3. Russell, L.D., Ettlin, R.A., SinhaHikim, A.P. & Clegg, E.D. in Histological and Histopathological Evaluation of the Testis 1-40 (Cache River, Clearwater, Florida 1990).
4. Silvers, W.K. in The Coat Colors of Mice 206-223 (Springer Verlag, New York, 1979).
5. Brinster, R.L. & Zimmermann, J.W. Spermatogenesis following male germ-cell transplantation. Proc. Natl. Acad. Sci. USA 91, 11298-11302 (1994).
6. Brinster, R.L. & Avarbock, M.R. Germline transmission of donor haplotype following spermatogonial transplantation. Proc. Natl. Acad. Sci. USA 91, 11303-11307 (1994).
7. Ogawa, T., Aréchaga, J.M., Avarbock, M.R. & Brinster, R.L. Transplantation of testis germinal cells into mouse seminiferous tubules. Int. J. Dev. Biol. 41, 111-122 (1997).
8. Chabot, B., Stephenson, D.A., Chapman, V.M., Besmer, P. & Bernstein, A. The proto-oncogene c-kit encoding a transmembrane tyrosine kinase receptor maps to the mouse W locus. Nature 335, 88-89 (1988).
9. Geissler, E.N., Ryan, M.A., & Housman, D.E. The dominat white spotting (W) locus of the mouse encodes the c-kit proto-oncogene. Cell 55, 185-192 (1988).
10. Zsebo, K.M. et al. Stem cell factor is encoded at the Sl locus of the mouse and is the ligand for the c-kit tyrosine kinase receptor. Cell 63, 213-224(1990).
11. Huang, E. et al. The hematopoietic growth factor KL is encoded by the Sl locus and is the ligand of the c-kit receptor, the gene product of the W locus. Cell 63, 225-233, 1990.
12. Nocka, K. et al. Expression of c-kit gene products in known cellular targets of W mutations in normal and W mutant mice - evidence for impaired c-kit kinase in mutant mice. Genes Dev. 3, 816-826 (1989).
13. Ogawa, M. et al. Expression and function of c-kit in hemopoietic progenitor cells. J. Exp. Med. 174, 63-71 (1991).
14. Sorrentino, V., Giorgi, M., Geremia, R., Besmer, P. & Rossi, P. Expression of the c-kit proto-oncogene in the murine male germ cells. Oncogene 6, 149-151 (1991).
15. Matsui, Y., Zsebo, K.M. & Hogan, B.L.M. Embryonic expression of a haematopoietic growth factor encoded by the Sl locus and the ligand for c-kit. Nature 347, 667-669 (1990).
16. Russell, E.S. Hereditary anemias of the mouse: A review for geneticists. Adv. Genet. 20, 357-459 (1979).
17. Russell, E.S., Bernstein, S.E., Lawson, F.A. & Smith, L.J. Long-continued function of normal blood-forming tissue transplanted into genetically anemic hosts. J. Natl. Cancer Inst. 23, 557-566 (1959).
18. McCulloch, E.A., Siminovich, E.A., & Till, J.L. Spleen-colony formation in anemic mice of genotype W/W. Science 144, 844-846 (1964).
19. Bernstein, S.E. Tissue transplantation as an analytic and therapeutic tool in hereditary anemias. Am. J. Surg. 119, 448-451 (1970).
20. Mayer, T.C., & Green, M.C. An experimental analysis of the pigment defect caused by mutations at the W and Sl loci in mice. Dev. Biol. 18, 62-75 (1968).
21. Huszar, D., Sharpe, A. & Jaenisch, R. Migration and proliferation of cultured neural crest cells in W mutant neural crest chimeras. Development 112, 131-141 (1991).
22. Manova, K. et al. The expression pattern of the c-kit ligand in gonads of mice supports a role for the c-kit receptor in oocyte growth and in proliferation of spermatogonia. Dev. Biol. 157, 85-99 (1993).
23. Dolci, S. et al. Primordial germ cell survival in culture requires membrane bound mast cell growth factor. Nature 352, 809-811 (1991).
24. Yoshinaga, K. et al. Role of c-kit in mouse spermatogenesis: identification of spermatogonia as a specific site of c-kit expression and function. Development 113, 689-699 (1991).
25. Nakayama, H. et al. Effect of the steel locus on mouse spermatogenesis. Development 402, 117-126 (1988).
26. d mutation. Cell 64, 1025-1035 (1991).
27. Ogawa, T., Dobrinski, I., Avarbock, M.R. & Brinster, R.L. Leuprolide, a gonadotropin-releasing hormone agonist, enhances colonization after spermatogonial transplantation into mouse testes. Tissue Cell 30, 583-588 (1998).
28. Russell, L.D., Franca, L.R. & Brinster, R.L. Ultrastructural observations of spermatogenesis in mice resulting from transplantation of mouse spermatogonia. J. Androl. 17, 603-614 (1996).
29. Bellvé, A.R. Purification, culture, and fractionation of spermatogenic cells. Meth. Enzymol. 225, 84-113 (1993).
30. McCoshen, J.A. & McCallion, D.J. A study of the primordial germ cells during their migratory phase in Steel mutant mice. Experientia 31, 589-590 (1975).
31. 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. Mol. Reprod. Dev. 53, 142-148 (1999a).
32. 6-intergin are surface markers on mouse spermatogonial stem cells. Proc. Natl. Acad. Sci. USA 96, 5504-5509 (1999).
33. Fleischman, R.A., Saltman, D.L., Stastny, V. & Zneimer, S. Deletion of the c-kit protoconcogene in the human developmental defect piebald trait. Proc. Nat. Acad. Sci. USA 88, 10885-10889 (1991).
34. Silber, S.J. What forms of male infertility are there left to cure? Hum. Reprod. 10, 503-504 (1995).
35. Tesarik, J., Mendoza, C., & Testart, J. Viable embryos from injection of round spermatids into oocytes. N. Engl. J. Med. 333, 525 (1995).
36. Martin-du Pan, R.C. & Campana, A. Physiopathology of spermatogenic arrest. Fertil. Steril. 60, 937-946 (1993).
37. Clouthier, D.E., Avarbock, M.R., Maika, S.D., Hammer, R.E. & Brinster, R.L. Rat spermatogenesis in mouse testis. Nature 381, 418-421 (1996).
38. Jiang F.-X. & Short, R.V. Male germ cell transplantation in rats: Apparent synchronization of spermatogenesis between host and donor seminiferous epithelia. Int. J. Androl. 18, 326-330 (1995).
39. Ogawa, T., Dobrinski, I., Avarbock, M.R. & Brinster, R.L. Xenogeneic spermatogenesis following transplantation of hamster germ cells to mouse testes. Biol. Reprod. 60, 515-521 (1999).
40. Ogawa, T., Dobrinski, I., & Brinster, R.L. Recipient preparation is critical for spermatogonial transplantation in the rat. Tissue Cell 31, 461-530 (1999).
41. Dobrinski, I., Avarbock, M.R. & Brinster, R.L. Transplantation of germ cells from rabbits and dogs into mouse testes. Biol. Reprod. 61, 1331-1339 (1999).
42. Schlatt, S. et al. Germ cell transfer into rat, bovine, monkey and human testes. Hum. Reprod. 14, 144-150 (1999).
43. Nagano, M., Avarbock, M.R., Leonida, E.B., Brinster, C.J. & Brinster, R.L. Culture of mouse spermatogonial stem cells. Tissue Cell 30, 389-397 (1998).
44. Dirami, G., Ravindranath, N., Pursel, V. & Dym, M. Effects of stem cell factor and granulocyte macrophage-colony stimulating factor on survival of porcine type A spermatogonia cultured in KSOM. Biol. Reprod. 61, 225-230 (1999).
45. Avarbock, M.R., Brinster, C.J. & Brinster, R.L. Reconstitution of spermatogenesis from frozen spermatogonial stem cells. Nature Med. 2, 693-696 (1996).