Xenogeneic and endogenous spermatogenesis following transplantation of rat germ cells into testes of immunocompetent mice
Ning Qu A B , Munekazu Naito A , Jun Li A , Hayato Terayama A , Shuichi Hirai A and Masahiro Itoh A
+ Author Affiliations
- Author Affiliations
A Department of Anatomy, Tokyo Medical University, Tokyo 160-8402, Japan.
B Corresponding author. Email: quning@tokyo-med.ac.jp
Reproduction, Fertility and Development 24(2) 337-343 https://doi.org/10.1071/RD10349
Submitted: 28 December 2010 Accepted: 27 June 2011 Published: 26 October 2011
Abstract
Spermatogonial stem cells (SSCs) are the foundation of spermatogenesis, and are characterised by their ability to self-renew and to produce differentiated progeny that form spermatozoa. It has been demonstrated that rat spermatogenesis can occur in the seminiferous tubules of congenitally immunodeficient recipient mice after transplantation of rat SSCs. However, the testis is often viewed as an immune-privileged site in that autoimmunogenic antigens on germ cells do not normally elicit an immune response in situ. In the present study, we tried to transplant rat SSCs into immunocompetent mice after depletion of their own germ cells by means of busulfan. The results showed that some transplanted SSCs could undergo complete spermatogenesis in recipient mouse testes, the rat spermatozoa being detected in 7 of 28 recipient epididymides. A significant increase in mouse spermatozoa was also noted in all 28 epididymides of recipient mice regardless of whether rat spermatozoa were concurrently present or not. These results suggest that transplanted rat SSCs can be tolerated in the testes of immunocompetent mice and that the transplantation of rat SSCs stimulates endogenous spermatogenesis in the recipient mice.
Additional keywords: immune response, spermatogonial stem cells, testis.
References
Barker, C. F., and Billingham, R. E. (1978). Immunologically privileged sites. Adv. Immunol. 25, 1–54.| Immunologically privileged sites.Crossref | GoogleScholarGoogle Scholar |
Brinster, R. L., and Avarbock, M. R. (1994). Germline transmission of donor haplotype following spermatogonial transplantation. Proc. Natl. Acad. Sci. USA 91, 11 303–11 307.
| Germline transmission of donor haplotype following spermatogonial transplantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitlyku7g%3D&md5=4132671e16c467ff9b594e0648d12bc9CAS |
Brinster, R. L., and Zimmermann, J. (1994). Spermatogenesis following male germ cell transplantation. Proc. Natl. Acad. Sci. USA 91, 11 298–11 302.
| Spermatogenesis following male germ cell transplantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitlyku7s%3D&md5=3aa92860af20c3f78c79cfdcf8ba9303CAS |
Clouthier, D., Avarbock, M., Maika, S., Hammer, R. E., and Brinster, R. L. (1996). Rat spermatogenesis in mouse testis. Nature 381, 418–421.
| Rat spermatogenesis in mouse testis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjsVWgtrw%3D&md5=19d32e5a3987a1c43271b061a9b02b24CAS | 8632797PubMed |
Delfino, F. J., Boustead, J. N., Fix, C., and Walker, W. H. (2003). NF-kappaB and TNF-alpha stimulate androgen receptor expression in Sertoli cells. Mol. Cell. Endocrinol. 201, 1–12.
| NF-kappaB and TNF-alpha stimulate androgen receptor expression in Sertoli cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXivFeru7s%3D&md5=64036439b39ab34791da94fd9c76b321CAS | 12706288PubMed |
Dobrinski, I., Avarbock, M., and Brinster, R. L. (1999). Transplantation of germ cells from rabbits and dogs into mouse testes. Biol. Reprod. 61, 1331–1339.
| Transplantation of germ cells from rabbits and dogs into mouse testes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvFert7Y%3D&md5=c502cf58f51e7c165b2150d170a64feaCAS | 10529282PubMed |
Dobrinski, I., Avarbock, M., and Brinster, R. L. (2000). Germ cell transplantation from large domestic animals into mouse testes. Mol. Reprod. Dev. 57, 270–279.
| Germ cell transplantation from large domestic animals into mouse testes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnt1yls7k%3D&md5=d9b3fae46efa8df463819ba32c812740CAS | 11013435PubMed |
Guitton, N., Touzalin, A. M., Sharpe, R. M., Cheng, C. Y., Pinon-Lataillade, G., Merritte, H., Chenal, C., and Jegou, B. (2000). Regulatory influence of germ cells on Sertoli cell function in the pre-pubertal rat after acute irradiation of the testis. Int. J. Androl. 23, 332–339.
| Regulatory influence of germ cells on Sertoli cell function in the pre-pubertal rat after acute irradiation of the testis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FnslOgug%3D%3D&md5=a90c3cf5b3699b783737aaa15362b308CAS | 11114978PubMed |
Head, J. R., and Billingham, R. E. (1985). Immune privilege in the testis. II. Evaluation of potential local factors. Transplantation 40, 269–274.
| Immune privilege in the testis. II. Evaluation of potential local factors.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2MzgtFChuw%3D%3D&md5=b0715b9f293209b6877310bf4305bef8CAS | 3898493PubMed |
Itoh, M., Terayama, H., Naito, M., Ogawa, Y., and Tainosho, S. (2005). Tissue microcircumstances for leukocytic infiltration into the testis and epididymis in mice. J. Reprod. Immunol. 67, 57–67.
| Tissue microcircumstances for leukocytic infiltration into the testis and epididymis in mice.Crossref | GoogleScholarGoogle Scholar | 16111766PubMed |
Jonsson, C. K., Zetterstrom, R. H., Holst, M., Parvinen, M., and Soder, O. (1999). Constitutive expression of interleukin-1alpha messenger ribonucleic acid in rat Sertoli cells is dependent upon interaction with germ cells. Endocrinology 140, 3755–3761.
| Constitutive expression of interleukin-1alpha messenger ribonucleic acid in rat Sertoli cells is dependent upon interaction with germ cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkslKqs7g%3D&md5=1cc1c2216375ebd2ccf95cb0251beab3CAS | 10433236PubMed |
Maguire, S. M., Millar, M. R., Sharpe, R. M., and Saunders, P. T. (1993). Stage-dependent expression of mRNA for cyclic protein 2 during spermatogenesis is modulated by elongated spermatids. Mol. Cell. Endocrinol. 94, 79–88.
| Stage-dependent expression of mRNA for cyclic protein 2 during spermatogenesis is modulated by elongated spermatids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlslyhurc%3D&md5=ea96a797e13182002ac8c17c919b11adCAS | 8375577PubMed |
McKinnell, C., and Sharpe, R. M. (1997). Regulation of the secretion and synthesis of rat Sertoli cell SGP-1, SGP-2 and CP-2 by elongated spermatids. Int. J. Androl. 20, 171–179.
| 1:CAS:528:DyaK2sXnt1ynsbc%3D&md5=e20e7d2aa425a2ab994fa820cf724906CAS | 9354187PubMed |
Nagano, M., McCarrey, G., and Brinster, R. L. (2001). Primate spermatogonial stem cells colonize mouse testes. Biol. Reprod. 64, 1409–1416.
| Primate spermatogonial stem cells colonize mouse testes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtFKqsrg%3D&md5=b77a2b8d59770ed657766fa5bb2909a0CAS | 11319145PubMed |
Ogawa, T., Dobrinski, I., Avarbock, M. R., and Brinster, R. L. (1999). Xenogeneic spermatogenesis following transplantation of hamster germ cells to mouse testes. Biol. Reprod. 60, 515–521.
| Xenogeneic spermatogenesis following transplantation of hamster germ cells to mouse testes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXotlymsg%3D%3D&md5=7b44cc0d286ff5d542c3a5b442bcad4fCAS | 9916022PubMed |
Pollanen, P., and Maddocks, S. (1988). Macrophages, lymphocytes and MHC II antigen in the ram and rat testis. J. Reprod. Fertil. 82, 437–445.
| Macrophages, lymphocytes and MHC II antigen in the ram and rat testis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c3gtVSlug%3D%3D&md5=18edd03955c1eab588d1654e8b6ea7c6CAS | 3163001PubMed |
Russell, I., and Brinster, R. L. (1996). Ultrastructural observations of spermatogenesis following transplantation of rat testis cells into mouse seminiferous tubules. J. Androl. 17, 615–627.
| 1:STN:280:DyaK2s7mvVOqug%3D%3D&md5=1ce9d2106444b740fbe10c80e855b442CAS |
Shinohara, T., Orwig, K. E., Avarbock, M. R., and Brinster, R. L. (2002). Germ line stem cell competition in postnatal mouse testes. Biol. Reprod. 66, 1491–1497.
| Germ line stem cell competition in postnatal mouse testes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtFWns7c%3D&md5=34662bb5a1850346eb48ba67662ca650CAS | 11967215PubMed |
Shinohara, T., Orwig, K. E., Avarbock, M. R., and Brinster, R. L. (2003). Restoration of spermatogenesis in infertile mice by Sertoli cell transplantation. Biol. Reprod. 68, 1064–1071.
| Restoration of spermatogenesis in infertile mice by Sertoli cell transplantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsFGksLs%3D&md5=be6703a72ae40689a4208ab89f88798dCAS | 12604661PubMed |
Sofikitis, N., Kaponis, A., Mio, Y., Makredimas, D., Giannakis, D., Yamamoto, Y., Kanakas, N., Kawamura, H., Georgiou, J., Schrader, M., Lolis, E., Giannakopoulos, X., Loutradis, D., Tarlatzia, V., and Miyagawa, I. (2003). Germ cell transplantation: a review and progress report on ICSI from spermatozoa generated in xenogeneic testes. Hum. Reprod. Update 3, 291–307.
| Germ cell transplantation: a review and progress report on ICSI from spermatozoa generated in xenogeneic testes.Crossref | GoogleScholarGoogle Scholar |
Syed, V., Gomez, E., and Hecht, N. B. (1999). Messenger ribonucleic acids encoding a serotonin receptor and a novel gene are induced in Sertoli cells by a secreted factor(s) from male rat meiotic germ cells. Endocrinology 140, 5754–5760.
| Messenger ribonucleic acids encoding a serotonin receptor and a novel gene are induced in Sertoli cells by a secreted factor(s) from male rat meiotic germ cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns12htLs%3D&md5=1b956f62c0ff9f03c13882be27dc0d3eCAS | 10579341PubMed |
Tanaka, A., Nagayoshi, M., Awata, M., Mawatari, Y., Tanaka, I., and Sofikitis, N. (1997). Conclusions from the transplantation of human or hamster spermatogonia/primary spermatocytes to rat or mouse testis. Fertil. Steril. 68, S61.
| Conclusions from the transplantation of human or hamster spermatogonia/primary spermatocytes to rat or mouse testis.Crossref | GoogleScholarGoogle Scholar |
Tung, K. S. K. (1993). Regulation of testicular autoimmune disease. In ‘Cell and Molecular Biology of the Testis’. pp. 474–490. (Eds C. Desjardins and L.L. Ewing) (Oxford University Press: New York.)
Vidal, F., Lopez, P., Lopez-Fernandez, L. A., Ranc, F., Scimeca, J. C., Cuzin, F., and Rassoulzadegan, M. (2001). Gene trap analysis of germ cell signaling to Sertoli cells: NGF-TrkA mediated induction of Fra1 and Fos by post-meiotic germ cells. J. Cell Sci. 114, 435–443.
| 1:CAS:528:DC%2BD3MXht1Kgu74%3D&md5=1130fdef8d35d1ffd238caf63027ccadCAS | 11148144PubMed |
Wang, D. Z., Zhou, X. H., Yuan, Y. L., and Zheng, X. M. (2010). Optimal dose of busulfan for depleting testicular germ cells of recipient mice before spermatogonial transplantation. Asian J. Androl. 12, 263–270.
| Optimal dose of busulfan for depleting testicular germ cells of recipient mice before spermatogonial transplantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXisFehtbc%3D&md5=fe8dcf0ab72f5c6b44ff8354b02b4375CAS | 20010847PubMed |
Wyatt, C. R., Law, L., Magnuson, J. A., Griswold, M. D., and Magnuson, N. S. (1988). Suppression of lymphocyte proliferation by cultured Sertoli cells. J. Reprod. Immunol. 14, 27–40.
| Suppression of lymphocyte proliferation by cultured Sertoli cells.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M%2FmvVGrtQ%3D%3D&md5=45148e1457028c13c112c1e684992105CAS | 3199389PubMed |
Zhang, Z., Renfree, M. B., and Short, R. V. (2003). Successful intra- and interspecific male germ cell transplantation in the rat. Biol. Reprod. 68, 961–967.
| Successful intra- and interspecific male germ cell transplantation in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsFGks70%3D&md5=9dd54c24a416de99e0505eb9735b40b0CAS | 12604649PubMed |
