Hormone suppression with GnRH antagonist promotes spermatogenic recovery from transplanted spermatogonial stem cells in irradiated cynomolgus monkeys

Andrology

Volumn 1, Issue 6, 2013, Pages 886-898

  Shetty, G ^a   Uthamanthil, R K ^a,b   Zhou, W ^a   Shao, S H ^a   Weng, C C ^a   Tailor, R C ^a   Hermann, B P ^c,d   Orwig, K E ^c   Meistrich, M L ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

Author keywords

Gonadotropin releasing hormone antagonist; Infertility; Radiation; Spermatogenesis; Transplantation

Indexed keywords

GONADORELIN ANTAGONIST; GREEN FLUORESCENT PROTEIN; VIRUS DNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOLOGOUS STEM CELL TRANSPLANTATION; CELL DIFFERENTIATION; CRYOPRESERVATION; GERM CELL; HORMONAL REGULATION; IRRADIATION; LENTIVIRINAE; MACACA FASCICULARIS; MALE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RADIATION DOSE; RADIATION RESPONSE; SPERMATOGENESIS; SPERMATOZOON; TESTIS; TESTIS SIZE; TESTIS WEIGHT; TREATMENT DURATION; XENOTRANSPLANTATION;

GONADOTROPIN-RELEASING HORMONE-ANTAGONIST; INFERTILITY; RADIATION; SPERMATOGENESIS; TRANSPLANTATION;

ANIMALS; GERM CELLS; GONADOTROPIN-RELEASING HORMONE; HORMONE ANTAGONISTS; MACACA FASCICULARIS; MALE; MICE; OLIGOPEPTIDES; SPERM COUNT; SPERMATOGENESIS; SPERMATOGONIA; TESTIS; TRANSPLANTATION, HETEROLOGOUS;

EID: 84886441660     PISSN: 20472919     EISSN: 20472927     Source Type: Journal    
DOI: 10.1111/j.2047-2927.2013.00126.x     Document Type: Article

References (41)

1. Anserini P, Chiodi S, Spinelli S, Costa M, Conte N, Copello F et al. (2002) Semen analysis following allogeneic bone marrow transplantation. Additional data for evidence-based counselling. Bone Marrow Transplant 30, 447-451.
2. Boekelheide K, Schoenfeld H, Hall SJ, Weng CCY, Shetty G, Leith J et al. (2005) Gonadotropin-releasing hormone antagonist (cetrorelix) therapy fails to protect non-human primates (Macaca arctoides) from radiation-induced spermatogenic failure. J Androl 26, 222-234.
3. Brinster RL. (2007) Male germline stem cells: from mice to men. Science 316, 404-405.
4. Dobrinski I, Ogawa T, Avarbock MR & Brinster RL. (2001) Effect of the GnRH-agonist leuprolide on colonization of recipient testes by donor spermatogonial stem cells after transplantation in mice. Tissue Cell 33, 200-207.
5. Hermann BP, Sukhwani M, Lin CC, Sheng Y, Tomko J, Rodriguez M et al. (2007) Characterization, cryopreservation, and ablation of spermatogonial stem cells in adult rhesus macaques. Stem Cells 25, 2330-2338.
6. Hermann BP, Sukhwani M, Simorangkir DR, Chu T, Plant TM & Orwig KE. (2009) Molecular dissection of the male germ cell lineage identifies putative spermatogonial stem cells in rhesus macaques. Hum Reprod 24, 1704-1716.
7. Hermann BP, Sukhwani M, Winkler F, Pascarella JN, Peters KA, Sheng Y et al. (2012) Spermatogonial stem cell transplantation into rhesus testes regenerates spermatogenesis producing functional sperm. Cell Stem Cell 11, 715-726.
8. Honaramooz A & Yang Y. (2011) Recent advances in application of male germ cell transplantation in farm animals. Vet Med Int 2011, Article ID: 657860.
9. Jacob A, Barker H, Goodman A & Holmes J. (1998) Recovery of spermatogenesis following bone marrow transplantation. Bone Marrow Transplant 22, 277-279.
10. Jahnukainen K, Ehmcke J, Quader MA, Saiful Huq M, Epperly MW, Hergenrother S et al. (2011) Testicular recovery after irradiation differs in prepubertal and pubertal non-human primates, and can be enhanced by autologous germ cell transplantation. Hum Reprod 26, 1945-1954.
11. Kamischke A, Kuhlmann M, Weinbauer GF, Luetjens M, Yeung C-H, Kronholz HL et al. (2003) Gonadal protection from radiation by GnRH antagonist or recombinant human FSH: a controlled trial in a male nonhuman primate (Macaca fascicularis). J Endocrinol 179, 183-194.
12. Kanatsu-Shinohara M, Takehashi M, Takashima S, Lee J, Morimoto H, Chuma S et al. (2008) Homing of mouse spermatogonial stem cells to germline niche depends on beta1-integrin. Cell Stem Cell 3, 533-542.
13. Lois C, Hong EJ, Pease S, Brown EJ & Baltimore D. (2002) Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295, 868-872.
14. Marshall GR, Ramaswamy S & Plant TM. (2005) Gonadotropin-independent proliferation of the pale type A spermatogonia in the adult rhesus monkey (Macaca mulatta). Biol Reprod 73, 222-229.
15. Masala A, Faedda R, Alagna S, Satta A, Chiarelli G, Rovasio PP et al. (1997) Use of testosterone to prevent cyclophosphamide-induced azoospermia. Ann Intern Med 126, 292-295.
16. Meistrich ML & Kangasniemi M. (1997) Hormone treatment after irradiation stimulates recovery of rat spermatogenesis from surviving spermatogonia. J Androl 18, 80-87.
17. Meistrich ML, Wilson G & Huhtaniemi I. (1999) Hormonal treatment after cytotoxic therapy stimulates recovery of spermatogenesis. Cancer Res 59, 3557-3560.
18. 1 rats. J Androl 22, 809-817.
19. Meistrich ML, Vassilopoulou-Sellin R & Lipshultz LI. (2005) Gonadal dysfunction. In: Cancer: Principles and Practice of Oncology (eds VT DeVita, S Hellman & SA Rosenberg ), pp. 2560-2574. Lippincott Williams & Wilkins, Philadelphia, PA.
20. Meng J, Holdcraft RW, Shima JE, Griswold MD & Braun RE. (2005) Androgens regulate the permeability of the blood-testis barrier. Proc Natl Acad Sci USA 102, 16696-16700.
21. Ogawa T, Dobrinski I, Avarbock MR & Brinster RL. (1998) Leuprolide, a gonadotropin-releasing hormone agonist, enhances colonization after spermatogonial transplantation into mouse testes. Tissue Cell 30, 583-588.
22. Ogawa T, Dobrinski I & Brinster RL. (1999) Recipient preparation is critical for spermatogonial transplantation in the rat. Tissue Cell 31, 461-472.
23. Ohmura M, Ogawa T, Ono M, Dezawa M, Hosaka M, Kubota Y et al. (2003) Increment of murine spermatogonial cell number by gonadotropin-releasing hormone analogue is independent of stem cell factor c-kit signal. Biol Reprod 68, 2304-2313.
24. Orwig KE & Schlatt S. (2005) Cryopreservation and transplantation of spermatogonia and testicular tissue for preservation of male fertility. J Natl Cancer Inst Monogr 34, 51-56.
25. Ramaswamy S, Marshall GR, Pohl CR, Friedman RL & Plant TM. (2003) Inhibitory and stimulatory regulation of testicular inhibin B secretion by luteinizing hormone and follicle-stimulating hormone, respectively, in the rhesus monkey (Macaca mulatta). Endocrinology 144, 1175-1185.
26. Rodriguez-Sosa JR & Dobrinski I. (2009) Recent developments in testis tissue xenografting. Reproduction 138, 187-194.
27. Ryu BY, Orwig KE, Oatley JM, Lin CC, Chang LJ, Avarbock MR et al. (2007) Efficient generation of transgenic rats through the male germline using lentiviral transduction and transplantation of spermatogonial stem cells. J Androl 28, 353-360.
28. Sato T, Katagiri K, Gohbara A, Inoue K, Ogonuki N, Ogura A et al. (2011) In vitro production of functional sperm in cultured neonatal mouse testes. Nature 471, 504-507.
29. Schlatt S, Foppiani L, Rolf C, Weinbauer GF & Nieschlag E. (2002) Germ cell transplantation into X-irradiated monkey testes. Hum Reprod 17, 55-62.
30. Shetty G & Meistrich ML. (2005) Hormonal approaches to preservation and restoration of male fertility after cancer treatment. J Natl Cancer Inst Monogr 34, 36-39.
31. Shetty G, Wilson G, Huhtaniemi I, Shuttlesworth GA, Reissmann T & Meistrich ML. (2000) Gonadotropin-releasing hormone analogs stimulate and testosterone inhibits the recovery of spermatogenesis in irradiated rats. Endocrinology 141, 1735-1745.
32. Shetty G, Weng CC, Meachem SJ, Bolden-Tiller OU, Zhang Z, Pakarinen P et al. (2006) Both testosterone and FSH independently inhibit spermatogonial differentiation in irradiated rats. Endocrinology 147, 472-482.
33. Shetty G, Porter KL, Zhou W, Shao SH, Weng CC & Meistrich ML. (2011) Androgen suppression-induced stimulation of spermatogonial differentiation in juvenile spermatogonial depletion mice acts by elevating the testicular temperature. Endocrinology 152, 3504-3514.
34. Thomson AB, Critchley HO, Kelnar CJ & Wallace WH. (2002) Late reproductive sequelae following treatment of childhood cancer and options for fertility preservation. Best Pract Res Clin Endocrinol Metab 16, 311-334.
35. Udagawa K, Ogawa T, Watanabe T, Yumura Y, Takeda M & Hosaka M. (2001) GnRH analog, leuprorelin acetate, promotes regeneration of rat spermatogenesis after severe chemical damage. Int J Urol 8, 615-622.
36. Velez de la Calle JF & Jegou B. (1990) Protection by steroid contraceptives against procarbazine-induced sterility and genotoxicity in male rats. Cancer Res 50, 1308-1315.
37. Wang G, Shao SH, Weng CC, Wei C & Meistrich ML. (2010) Hormonal suppression restores fertility in irradiated mice from both endogenous and donor-derived stem spermatogonia. Toxicol Sci 117, 225-237.
38. Zhang Z, Renfree MB & Short RV. (2003) Successful intra- and interspecific male germ cell transplantation in the rat. Biol Reprod 68, 961-967.
39. Zhang Z, Shao S & Meistrich ML. (2006) Irradiated mouse testes efficiently support spermatogenesis derived from donor germ cells of mice and rats. J Androl 27, 365-375.
40. Zhang Z, Shao S & Meistrich ML. (2007) The radiation-induced block in spermatogonial differentiation is due to damage to the somatic environment, not the germ cells. J Cell Physiol 211, 149-158.
41. Zheng N, Monckton DG, Wilson G, Hagemeister F, Chakraborty R, Connor TH et al. (2000) Frequency of minisatellite repeat number changes at the MS205 locus in human sperm before and after cancer chemotherapy. Environ Mol Mutagen 36, 134-145.