Xenografting restores spermatogenesis to cryptorchid testicular tissue but does not rescue the phenotype of idiopathic testicular degeneration in the horse (Equus caballus)

Reproduction, Fertility and Development

Volumn 22, Issue 4, 2010, Pages 673-683

  Turner, Regina M ^a   Rathi, Rahul ^a   Honaramooz, Ali ^a   Zeng, Wenxian ^a   Dobrinski, Ina ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Fertility; Stallion; Testicular pathology

Indexed keywords

GONADOTROPIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOTRANSPLANTATION; CELL DIFFERENTIATION; CELL SURVIVAL; CONTROLLED STUDY; CRYPTORCHISM; HORSE; IDIOPATHIC DISEASE; MALE; MEIOSIS; MOUSE; NONHUMAN; PHENOTYPE; SEMINIFEROUS TUBULE; SPERMATOGENESIS; SPERMATOGONIUM; TESTIS; TESTIS ATROPHY; XENOGRAFT;

AGE FACTORS; ANIMALS; CRYPTORCHIDISM; DISEASE MODELS, ANIMAL; HISTOCYTOCHEMISTRY; HORSE DISEASES; HORSES; MALE; MICE; MICE, NUDE; MICE, SCID; SPERMATOGENESIS; TESTIS; TRANSPLANTATION, HETEROLOGOUS;

EQUIDAE; EQUUS CABALLUS; MAMMALIA; MUS; SUS;

EID: 77950611602     PISSN: 10313613     EISSN: None     Source Type: Journal    
DOI: 10.1071/RD09014     Document Type: Article

References (41)

1. Allen, W. R., and Stewart, F. (1992). Equine chorionic gonadotropin. In 'Equine Reproduction'. (Eds A. O. McKinnon and J. L.Voss.) pp. 81-96. (Lea & Febiger: Philadelphia, PA.)
2. Arregui, L., Rathi, R., Modelski, M., Zeng,W., Gomendio, M., Roldan, E. R., and Dobrinski, I. (2008a). Pre-grafting suppression of spermatogenesis improves germcell proliferation and differentiation in adult mouse testis allografts. In 'Proceedings of the Annual Meeting of the Society for Reproduction and Fertility'. p. 39.
3. Arregui, L., Rathi, R., Zeng, W., Honaramooz, A., Gomendio, M., Roldan, E. R., and Dobrinski, I. (2008b). Xenografting of adult mammalian testis tissue. Anim. Reprod. Sci. 106, 65-76. doi:10.1016/ J.ANIREPROSCI.2007.03.026 (Pubitemid 351467020)
4. Blanchard, T., and Varner, D. (1993). Testicular degeneration. In 'Equine Reproduction'. (Eds A. O. McKinnon and J. L. Voss.) pp. 855-860. (Lea & Febiger: Philadelphia.)
5. Bousfield,G. R., Butnev,V.Y., Gotschall, R. R., Baker,V. L., and Moore,W.T. (1996). Structural features of mammalian gonadotropins. Mol. Cell. Endocrinol. 125, 3-19. doi:10.1016/S0303-7207(96)03945-7 (Pubitemid 27037780)
6. Chen, H., and Zirkin, B. R. (1999). Long-term suppression of Leydig cell steroidogenesis prevents Leydig cell aging. Proc. Natl Acad. Sci. USA 96, 14 877-14 881. doi:10.1073/PNAS.96.26.14877 (Pubitemid 30019733)
7. Friedman, R. M., Lopez, F. J., Tucker, J. A., King, L. R., and Negro-Vilar,A. (1994). Fertility after cryptorchidism: a comparative analysis of early orchidopexy with and without concomitant hormonal therapy in the young male rat. J. Urol. 151, 227-233.
8. Geens, M., De Block, G., Goossens, E., Frederickx,V.,Van Steirteghem, A., and Tournaye, H. (2006). Spermatogonial survival after grafting human testicular tissue to immunodeficient mice. Hum. Reprod. 21, 390-396. doi:10.1093/HUMREP/DEI412 (Pubitemid 43159913)
9. Hinrichs, K. (2005). Update on equine ICSI and cloning. Theriogenology 64, 535-541. doi:10.1016/J.THERIOGENOLOGY.2005.05.010 (Pubitemid 40984940)
10. Honaramooz, A., Snedaker, A., Boiani, M., Scholer, H., Dobrinski, I., and Schlatt, S. (2002). Sperm from neonatal mammalian testes grafted in mice. Nature 418, 778-781. doi:10.1038/NATURE00918
11. Honaramooz, A., Li, M. W., Penedo, M. C., Meyers, S., and Dobrinski, I. (2004). Accelerated maturation of primate testis by xenografting into mice. Biol. Reprod. 70, 1500-1503. doi:10.1095/BIOLREPROD.103. 025536
12. Honaramooz, A., Zeng,W., Rathi, R., Koster, J., Ryder, O., and Dobrinski, I. (2005). Testis tissue xenografting to preserve germ cells from a cloned banteng calf. Reprod. Fertil. Dev. 17, 247. doi:10.1071/ RDV17N2AB193
13. Jégou, B., Laws, A. O., and de Kretser, D. M. (1983). The effect of cryptorchidism and subsequent orchidopexy on testicular function in adult rats. J. Reprod. Fertil. 69, 137-145. doi:10.1530/JRF.0.0690137
14. Jégou,B., Peake, R.A., Irby,D. C., and de Kretser,D.M. (1984). Effects of the induction of experimental cryptorchidism and subsequent orchidopexy on testicular function in immature rats. Biol. Reprod. 30, 179-187. doi:10.1095/BIOLREPROD30.1.179 (Pubitemid 14153657)
15. Johnson, L. (1989). Evaluation of the human testis and its age-related dysfunction. Prog. Clin. Biol. Res. 302, 35-60.
16. Kim,Y., Selvaraj,V., Pukazhenthi,B., andTravis,A. J. (2007). Effect of donor age on success of spermatogenesis in feline testis xenografts. Reprod. Fertil. Dev. 19, 869-876. doi:10.1071/RD07056 (Pubitemid 47367606)
17. Kogan, B. A., Gupta, R., and Juenemann, K. P. (1987). Fertility in cryptorchidism: improved timing of fixation and treatment in an experimental model. J. Urol. 138, 1046-1047. (Pubitemid 17150821)
18. Kumi-Diaka, J., and Dennis, S. M. (1978).The Sertoli cell index as a measure of testicular degeneration in the bull. Vet. Rec. 103, 112-114.
19. Kumi-Diaka, J., Nagaratnam, V., and Rwuaan, J. S. (1981). Seasonal and age-related changes in semen quality and testicular morphology of bulls in a tropical environment. Vet. Rec. 108, 13-15.
20. Lugg, J. A., Penson, D. F., Sadeghi, F., Petrie, B., Freedman, A. L., Gonzalez-Cadavid, N. F., Hikim, A. S., and Rajfer, J. (1996). Prevention of seminiferous tubular atrophy in a naturally cryptorchid rat model by early surgical intervention. J. Androl. 17, 726-732.
21. Ma, P., Ge, Y., Wang, S., Ma, J., Xue, S., and Han, D. (2004). Spermatogenesis following syngeneic testicular transplantation in BALB/c mice. Reproduction 128, 163-170. doi:10.1530/REP.1.00165
22. Monet-Kuntz, C., Barenton, B., Locatelli, A., Fontaine, I., Perreau, C., and Hochereau-de Reviers, M. T. (1987). Effects of experimental cryptorchidism and subsequent orchidopexy on seminiferous tubule functions in the lamb. J. Androl. 8, 148-154.
23. Motton, D. D., and Roser, J. F. (1997). HCG binding to the testicular LH receptor is similar in fertile, subfertile, and infertile stallions. J. Androl. 18, 411-416.
24. Nishimune, Y., Aizawa, S., and Komatsu, T. (1978). Testicular germ cell differentiation in vivo. Fertil. Steril. 29, 95-102.
25. Oatley, J. M., de Avila, D. M., Reeves, J. J., and McLean, D. J. (2004). Spermatogenesis and germ cell transgene expression in xenografted bovine testicular tissue. Biol. Reprod. 71, 494-501. doi:10.1095/ BIOLREPROD.104.027953
26. Oatley, J. M., Reeves, J. J., and McLean, D. J. (2005). Establishment of spermatogenesis in neonatal bovine testicular tissue following ectopic xenografting varies with donor age. Biol. Reprod. 72, 358-364. doi:10.1095/BIOLREPROD.104.030783 (Pubitemid 40129711)
27. Ohta, H., and Wakayama, T. (2005). Generation of normal progeny by intracytoplasmic sperm injection following grafting of testicular tissue from cloned mice that died postnatally. Biol. Reprod. 73, 390-395. doi:10.1095/BIOLREPROD.105.041673 (Pubitemid 41170193)
28. Overbeek, P. A., Gorlov, I. P., Sutherland, R. W., Houston, J. B., Harrison,W. R., Boettger-Tong, H. L., Bishop, C. E., and Agoulnik, A. I. (2001). A transgenic insertion causing cryptorchidism in mice. Genesis 30, 26-35. doi:10.1002/GENE.1029 (Pubitemid 32521151)
29. Rathi, R., Honaramooz, A., Zeng, W., Turner, R., and Dobrinski, I. (2006). Germ cell development in equine testis tissue xenografted into mice. Reproduction 131, 1091-1098. doi:10.1530/REP.1.01101 (Pubitemid 43904982)
30. Rodriguez-Sosa, J. R., and Dobrinski, I. (2009). Recent developments in testis tissue xenografting. Reproduction 138, 187-194. doi:10.1530/ REP-09-0012
31. Roser, J. F. (1995). Endocrine regulation of reproductive function in fertile, subfertile and infertile stallions. Reprod. Domest. Anim. 30, 245-250. doi:10.1111/J.1439-0531.1995.TB00154.X
32. Roser, J. F. (1997). Endocrine basis for testicular function in the stallion. Theriogenology 48, 883-892. doi:10.1016/S0093-691X(97)00309-9 (Pubitemid 28135503)
33. Schlatt, S., Kim, S. S., and Gosden, R. (2002). Spermatogenesis and steroidogenesis in mouse, hamster and monkey testicular tissue after cryopreservation and heterotopic grafting to castrated hosts. Reproduction 124, 339-346. doi:10.1530/REP.0.1240339
34. Schlatt, S., Honaramooz, A., Boiani, M., Scholer, H. R., and Dobrinski, I. (2003). Progeny from sperm obtained after ectopic grafting of neonatal mouse testes. Biol. Reprod. 68, 2331-2335. doi:10.1095/ BIOLREPROD.102.014894
35. Schlatt, S., Honaramooz, A., Ehmcke, J., Goebell, P. J., Rubben, H., Dhir, R., Dobrinski, I., and Patrizio, P. (2006). Limited survival of adult human testicular tissue as ectopic xenograft. Hum. Reprod. 21, 384-389. doi:10.1093/HUMREP/DEI352 (Pubitemid 43159912)
36. Shinohara,T., Inoue, K., Ogonuki,N., Kanatsu-Shinohara, M., Miki, H., et al. (2002). Birth of offspring following transplantation of cryopreserved immature testicular pieces and in vitro microinsemination. Hum. Reprod. 17, 3039-3045. doi:10.1093/HUMREP/17.12.3039
37. Snedaker, A. K., Honaramooz, A., and Dobrinski, I. (2004). A game of cat and mouse: xenografting of testis tissue from domestic kittens results in complete cat spermatogenesis in a mouse host. J. Androl. 25, 926-930.
38. Stewart, B. L., and Roser, J. F. (1998). Effects of age, season, and fertility status on plasma and intratesticular immunoreactive (IR) inhibin concentrations in stallions. Domest. Anim. Endocrinol. 15, 129-139. doi:10.1016/S0739-7240(97)00083-0 (Pubitemid 29305042)
39. Turner, R. M., Rathia, R., Zeng, W., Honaramooz, A., and Dobrinski, I. (2006). Xenografting to study testis function in stallions. Anim. Reprod. Sci. 94, 161-164. doi:10.1016/J.ANIREPROSCI.2006.03.051
40. Voss, J. L. (1992). Human chorionic gonadotropin. In 'Equine Reproduction'. (EdsA.O. McKinnon and J. L.Voss.) pp. 325-328. (Lea&Febiger: Philadelphia, PA.)
41. Watson, E. D., Clarke, C. J., Else, R.W., and Dixon, P. M. (1994). Testicular degeneration in 3 stallions. Equine Vet. J. 26, 507-510.