Testicular stem cells for fertility preservation: Preclinical studies on male germ cell transplantation and testicular grafting

Pediatric Blood and Cancer

Volumn 53, Issue 2, 2009, Pages 274-280

  Schlatt, Stefan ^a,b   Ehmcke, Jens ^a,b   Jahnukainen, Kirsi ^a,c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Cancer therapy; Fertility preservation; Spermatogonial stem cells

Indexed keywords

ALKYLATING AGENT; CISPLATIN; GONADORELIN AGONIST; GONADORELIN ANTAGONIST;

CELL FUNCTION; CELL PROTECTION; CELL TRANSPLANTATION; CONFERENCE PAPER; GERM CELL; GERM CELL TRANSPLANTATION; HUMAN; MALE FERTILITY; NONHUMAN; PRESERVATION; PRIMATE; PRIORITY JOURNAL; RODENT; SPERMATOGONIUM; STEM CELL; TESTICULAR GRAFTING; TESTIS CELL; TRANSPLANTATION; ANIMAL; CRYOPRESERVATION; MALE; MALE INFERTILITY; METHODOLOGY; PHYSIOLOGY; REVIEW; STEM CELL TRANSPLANTATION; TESTIS;

ANIMALS; CRYOPRESERVATION; HUMANS; INFERTILITY, MALE; MALE; SPERMATOGONIA; STEM CELL TRANSPLANTATION; STEM CELLS; TESTIS;

EID: 67649968214     PISSN: 15455009     EISSN: 15455017     Source Type: Journal    
DOI: 10.1002/pbc.22002     Document Type: Conference Paper

References (57)

1. Robey PG. Stem cells near the century mark. J Clin Invest 2000;105:1489-1491.
2. Holtzer H. Stem cells and tissue homeostasis. New York: Cambridge University Press; 1978. pp. 1-28.
3. Watt FM, Hogan BL. Out of Eden: Stem cells and their niches. Science 2000;287:1427-1430. (Pubitemid 30127126)
4. Li L, Xie T. Stem cell niche: Structure and function. Annu Rev Cell Dev Biol 2005;21:605-631. (Pubitemid 41740648)
5. Ehmcke J, Hübner K, Schöler HR, et al. Spermatogonia: Origin, physiology and prospects for conservation and manipulation of the male germ line. Reprod Fertil Dev 2006;18:7-12. (Pubitemid 41831070)
6. Ehmcke J, Wistuba J, Schlatt S. Spermatogonial stem cells: Questions, models and perspectives. Hum Reprod Update 2006;12:275-282.
7. Meachem S, von Schönfeldt V, Schlatt S. Spermatogonia: Stem cells with a great perspective. Reproduction 2001;121:825-834. (Pubitemid 32547311)
8. De Rooij FG, Russel LD. All you wanted to know about spermatogonia but were afraid to ask. J Androl 2000;21:776-798. (Pubitemid 30808061)
9. Kanatsu-Shinohara M, Toyokuni S, Morimoto T, et al. Functional assessment of self-renewal activity of male germline stem cells following cytotoxic damage and serial transplantation. Biol Reprod 2003;68:1801-1807. (Pubitemid 36519788)
10. Ogawa T, Ohmura M, Yumura Y, et al. Expansion of murine spermatogonial stem cells through serial transplantation. Biol Reprod 2003;68:316-322. (Pubitemid 36076351)
11. Huckins C, Oakberg EF. Morphological and quantitative analysis of spermatogonia in mouse testes using whole mounted seminiferous tubules. I. The normal testes. Anat Rec 1978;192:519-528.
12. Lok D, Weenk D, de Rooij DG. Morphology, proliferation and differentiation of undifferentiated spermatogonia in the Chinese hamster and the ram. Anat Rec 1982;203:83-99.
13. De Rooij DG, Lok D, Weenk D. Feedback regulation of the proliferation of the undifferentiated spermatogonia in the Chinese hamster by the differentiating spermatogonia. Cell Tissue Kinet 1985;18:71-81. (Pubitemid 15198986)
14. Ogawa T, Ohmura M, Ohbo K. The niche for spermatogonial stem cells in the mammalian testis. Int J Hematol 2005;82:381-388. (Pubitemid 46638685)
15. Chuma S, Kanatsu-Shinohara M, Inoue K, et al. Spermatogenesis from epiblast and primordial germ cells following transplantation into postnatal mouse testis. Development 2005;132:117-122. (Pubitemid 40207971)
16. Nayernia K, Drabent B, Meinhardt A, et al. Triple knockouts reveal gene interactions affecting fertility of male mice. Mol Reprod Dev 2005;70:406-416. (Pubitemid 40315974)
17. Chiarini-Garcia H, Raymer AM, Russell LD. Non-random distribution of spermatogonia in rats: Evidence of niches in the seminiferous tubules. Reproduction 2003;126:669-680. (Pubitemid 37540628)
18. Yoshida S, Sukeno M, Nabeshima Y. A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 2007;317:1722-1726. (Pubitemid 47461832)
19. Dobrinski I. Transplantation of germ cells and testis tissue for the study and preservation of fertility. Soc Reprod Fertil Suppl 2007;65:447-458.
20. Clermont Y. Spermatogenesis in man. A study of the spermatogonial population. Fertil Steril 1966;17:705-721.
21. Clermont Y, Leblond CP. Differentiation and renewal of spermatogonia in the monkey, Macaca rhesus. Am J Anat 1959;104:237-273.
22. Clermont Y. Two classes of spermatogonial stem cells in the monkey (Cercopithecus aethiops). Am J Anat 1969;126:57-71.
23. Simorangkir DR, Marshall GR, Ehmcke J, et al. Prepubertal expansion of dark and pale type A spermatogonia in the rhesus monkey (Macaca mulatta) results from proliferation during infantile and juvenile development in a relatively gonadotropin independent manner. Biol Reprod 2005;73:1109-1115. (Pubitemid 41698600)
24. van Alphen MMA, van den Kant HJG, de Rooij DG. Repopulation of the seminiferous epithelium of the rhesus monkey after X-irradiation. Radiat Res 1988;113:487-500. (Pubitemid 18079177)
25. van Alphen MMA, van den Kant HJG, Davids JAG, et al. Dose-response studies on the spermatogonial stem cells of the Rhesus monkey (Macaca mulatta) after X-irradiation. Radiat Res 1989; 199:443-451.
26. Ehmcke J, Luetjens CM, Schlatt S. Clonal organization of proliferating spermatogonial stem cells in adult males of two species of non-human primates, Macaca mulatta and Callithrix jacchus. Biol Reprod 2005;72:293-300.
27. Ehmcke J, Simorangkir DR, Schlatt S. Identification of the starting point for spermatogenesis and characterization of the testicular stem cell in adult male rhesus monkeys. Hum Reprod 2005;20:1185-1193. (Pubitemid 40790240)
28. Ehmcke J, Schlatt S. A revised model for spermatogonial expansion in man: Lessons from non-human primates. Reproduction 2006;132:673-680. (Pubitemid 44782517)
29. van Alphen MMA, van de Kant HJG, de Rooij DG. Depletion of the spermatogonia from the seminiferous epithelium of the rhesus monkey after X irradiation. Radiat Res 1988;113:473-486. (Pubitemid 18079176)
30. Jahnukainen K, Ehmcke J, Schlatt S. Testicular xenografts: A novel approach to study cytotoxic damage in juvenile primate testis. Cancer Res 2006;66:3813-3818.
31. Jahnukainen K, Ehmcke J, Nurmio M, et al. Irradiation causes acute and long-term spermatogonial depletion in cultured and xenotransplanted testicular tissue from juvenile nonhuman primates. Endocrinology 2007;148:5541-5548. (Pubitemid 350012619)
32. Hahn EW, Feingold SM, Simpson L, et al. Recovery from aspermia induced by low-dose radiation in seminoma patients. Cancer 1982;50:337-340. (Pubitemid 12089397)
33. Anserini P, Chiodi S, Spinelli S, et al. Semen analysis following allogeneic bone marrow transplantation. Additional data for evidence-based counseling. Bone Marrow Transplant 2002;30:447-451.
34. de Rooij DG, van de Kant HJ, Dol R, et al. Long-term effects of irradiation before adulthood on reproductive function in the male rhesus monkey. Biol Reprod 2002;66:486-494. (Pubitemid 34101848)
35. Meseguer M, Garrido N, Remohi J, et al. Testicular sperm extraction (TESE) and ICSI in patients with permanent azoospermia after chemotherapy. Hum Reprod 2003;18:1281-1285. (Pubitemid 36740577)
36. Relander T, Cavallin-Stahl E, Garwicz S, et al. Gonadal and sexual function in men treated for childhood cancer. Med Pediatr Oncol 2000;35:52-63. (Pubitemid 30447825)
37. Brydoy M, Fossa SD, Klepp O, et al. Paternity following treatment for testicular cancer. J Natl Cancer Inst 2005;97:1580-1588. (Pubitemid 41662712)
38. Viviani S, Santoro A, Ragni G, et al. Gonadal toxicity after combination chemotherapy for Hodgkin's disease. Comparative results of MOPP vs ABVD. Eur J Cancer Clin Oncol 1985;21:601-605. (Pubitemid 15116991)
39. Wallace WH, Anderson RA, Irvine DS. Fertility preservation for young patients with cancer: Who is at risk and what can be offered? Lancet Oncol 2005;6:209-218.
40. Kamischke A, Jurgens H, Hertle L, et al. Cryopreservation of sperm from adolescents and adults with malignancies. J Androl 2004;25:586-592. (Pubitemid 38880193)
41. Baukloh V. German Society for Human Reproductive Biology retrospective multicentre study on mechanical and enzymatic preparation of fresh and cryopreserved testicular biopsies. Hum Reprod 2002;17:1788-1794.
42. Shetty G, Meistrich ML. Hormonal approaches to preservation and restoration of male fertility after cancer treatment. J Natl Cancer Inst Monogr 2005;34:36-39.
43. Jahnukainen K, Ehmcke J, Söder O, et al. Clinical potential and putative risks of fertility preservation in children utilizing gonadal tissue or germline stem cells. Pediatr Res 2006;59:40R-47R. (Pubitemid 43740034)
44. Orwig KE, Schlatt S. Cryopreservation and transplantation of spermatogonia and testicular tissue for preservation of male fertility. J Natl Cancer Inst Monogr 2005;34:51-56.
45. Brinster RL, Avarbock MR. Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci USA 1994;91:11303-11307.
46. Brinster RL, Zimmermann JW. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci USA 1994;91:11298-11302.
47. Schlatt S, Rosiepen G, Weinbauer GF, et al. Germ cell transfer into rat, bovine, monkey and human testes. Hum Reprod 1999;14:144-150. (Pubitemid 29046329)
48. Schlatt S, Foppiani L, Rolf C, et al. Germ cell transplantation into X-irradiated monkey testes. Hum Reprod 2002;17:55-62. (Pubitemid 34130261)
49. Radford JA, Shalet SM, Lieberman BA. Fertility after treatment for cancer. BMJ 1999;319:935-936.
50. Radford J. Restoration of fertility after treatment for cancer. Horm Res 2003;59:21-23.
51. Paris MC, Schlatt S. Ovarian and testicular tissue xenografting: Its potential for germline preservation of companion animals, nondomestic and endangered species. Reprod Fertil Dev 2007;19:771-782. (Pubitemid 47206971)
52. Jahnukainen K, Ehmcke J, Hergenrother SD, et al. Effect of cold storage and cryopreservation of immature non-human primate testicular tissue on spermatogonial stem cell potential in xenografts. Hum Reprod 2007;22:1060-1067.
53. Schlatt S, Honaramooz A, Ehmcke J, et al. Limited survival of adult human testicular tissue as ectopic xenograft. Hum Reprod 2006;21:384-389. (Pubitemid 43159912)
54. Geens M, De Block G, Goossens E, et al. Spermatogonial survival after grafting human testicular tissue to immunodeficient mice. Hum Reprod 2006;21:390-396. (Pubitemid 43159913)
55. Brook PF, Radford JA, Shalet SM, et al. Isolation of germ cells from human testicular tissue for low temperature storage and autotransplantation. Fertil Steril 2001;75:269-274.
56. Keros V, Rosenlund B, Hultenby K, et al. Optimizing cryopreservation of human testicular tissue: Comparison of protocols with glycerol, propanediol and dimethylsulphoxide as cryoprotectants. Hum Reprod 2005;20:1676-1687. (Pubitemid 40852266)
57. Kvist K, Thorup J, Byskov AG, et al. Cryopreservation of intact testicular tissue from boys with cryptorchidism. Hum Reprod 2006;21:484-491. (Pubitemid 43159927)