Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Germ cell transplantation for the propagation of companion animals, non-domestic and endangered species

I. Dobrinski A C and A. J. Travis B
+ Author Affiliations
- Author Affiliations

A Center for Animal Transgenesis and Germ Cell Research, School of Veterinary Medicine, University of Pennsylvania, 382 West Street Rd., Kennett Square, PA 19348, USA.

B Baker Institute for Animal Health, Cornell University College of Veterinary Medicine, Ithaca, NY 14853, USA.

C Corresponding author. Email: dobrinsk@vet.upenn.edu

Reproduction, Fertility and Development 19(6) 732-739 https://doi.org/10.1071/RD07036
Submitted: 26 February 2007  Accepted: 21 March 2007   Published: 2 August 2007

Abstract

The transplantation of spermatogonial stem cells between males results in a recipient animal producing spermatozoa carrying a donor’s haplotype. First pioneered in rodents, this technique has now been used in several animal species. Importantly, germ cell transplantation was successful between unrelated, immuno-competent large animals, whereas efficient donor-derived spermatogenesis in rodents requires syngeneic or immuno-compromised recipients. Transplantation requires four steps: recipient preparation, donor cell isolation, transplantation and identifying donor-derived spermatozoa. There are two main applications for this technology. First, genetic manipulation of isolated germ line stem cells and subsequent transplantation will result in production of transgenic spermatozoa. Transgenesis through the male germ line has tremendous potential in species in which embryonic stem cells are not available and somatic cell nuclear transfer and reprogramming pose several problems. Second, spermatogonial stem cell transplantation within or between species offers a means of preserving the reproductive potential of genetically valuable individuals. This might have significance in the captive propagation of non-domestic animals of high conservation value. Transplantation of germ cells is a uniquely valuable approach for the study, preservation and manipulation of male fertility in mammalian species.

Additional keywords: non-rodent animals, testis.


Acknowledgements

Work from the authors’ laboratories presented here was supported by 5R01RR017359–04 (NCRR/NIH), 2R42-HD044780–02 (NIH/NICHD) and USDA/CSREES/NRICGP (2003–35203–13486) to ID and the Morris Animal Foundation, the Cornell Feline Health Center and the Baker Institute (A.J.T.).


References

Avarbock, M. R. , Brinster, C. J., , and Brinster, R. L. (1996). Reconstitution of spermatogenesis from frozen spermatogonial stem cells.  Nat. Med. 2, 693–696.
Crossref | GoogleScholarGoogle Scholar | PubMed | Meistrich M. L., and van Beek M. E. A. B. (1993). Spermatogonial stem cells. In ‘Cell and Molecular Biology of Testis’. (Eds C. Desjardins and L. L. Ewing.) pp. 266–295. (Oxford University Press: Oxford.)

Mikkola, M. , Sironen, A. , Kopp, C. , Taponen, J. , Sukura, A. , Vilkki, J. , Katila, T. , and Andersson, M. (2006). Transplantation of normal boar testicular cells resulted in complete focal spermatogenesis in a boar affected by the immotile short-tail sperm defect. Reprod. Dom. Anim. 41, 124–128.
Crossref | GoogleScholarGoogle Scholar | Russell L. D., Ettlin R. A.,SinhaHikim A. P., and Clegg E. D. (1990). Mammalian spermatogenesis. In ‘Histological and Histopathological Evaluation of the Testis’. (Eds L. D. Russell, R. A. Ettlin, A. P. SinhaHikim and E. D. Clegg.) pp. 1–40. (Cache River Press: Clearwater, FL.)

Ryu, B.-Y. , Kubota, H. , Avarbock, M. R. , and Brinster, R. L. (2005). Conservation of spermatogonial stem cell self-renewal signaling between mouse and rat. Proc. Natl. Acad. Sci. USA 102, 14302–14307.
Crossref | GoogleScholarGoogle Scholar |

Schlatt, S. , Foppiani, L. , Rolf, C. , Weinbauer, G. F. , and Nieschlag, E. (2002). Germ cell transplantation into X-irradiated monkey testes. Hum. Reprod. 17, 55–62.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Schnieke, A. E. , Kind, A. J. , Ritchie, W. A. , Mycock, K. , Scott, A. R. , Ritchie, M. , Wilmut, I. , Colman, A. , and Campbell, K. H. (1997). Human factor IX transgenic sheep produced by transfer of nuclei from transfected fetal fibroblasts. Science 278((5346)), 2130–2133.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Shinohara, T. , Avarbock, M. R. , and Brinster, R. L. (1999). β1- and α6-integrin are surface markers on mouse spermatogonial stem cells. Proc. Natl. Acad. Sci. USA 96, 5504–5509.
Crossref | GoogleScholarGoogle Scholar |

Shinohara, T. , Orwig, K. E. , Avarbock, M. R. , and Brinster, R. L. (2000a). Spermatogonial stem cell enrichment by multiparameter selection of mouse testis cells. Proc. Natl. Acad. Sci. USA 97, 8346–8351.
Crossref | GoogleScholarGoogle Scholar |

Shinohara, T. , Avarbock, M. R. , and Brinster, R. L. (2000b). Functional analysis of spermatogonial stem cells in Steel and cryptorchid infertile mouse models. Dev. Biol. 220, 401–411.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Shinohara, T. , Orwig, K. E. , Avarbock, M. R. , and Brinster, R. L. (2001). Remodeling of the postnatal mouse testis is accompanied by dramatic changes in stem cell number and niche accessibility. Proc. Natl. Acad. Sci. USA 98, 6186–6191.
Crossref | GoogleScholarGoogle Scholar |

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.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Shinohara, T. , Kato, M. , Takehashi, M. , Lee, J. , Chuma, S. , Nakatsuji, N. , Kanatsu-Shinohara, M. , and Hirabayashi, M. (2006). Rats produced by inrespecies spermatogonial transplantation in mice and in vitro microinsemination. Proc. Natl. Acad. Sci. USA 103, 13624–13628.
Crossref | GoogleScholarGoogle Scholar |

Takeuchi, Y. , Yoshizaki, G. , and Takeuchi, T. (2003). Generation of live fry from intraperitoneally transplanted primordial germ cells in rainbow trout. Biol. Reprod. 69, 1142–1149.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Tegelenbosch, R. A. J. , and de Rooij, D. G. (1993). A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101 F1 hybrid mouse. Mut. Res. 290, 193–200.


Ventela, S. , Ohta, H. , Parvinen, M. , and Nishimune, Y. (2002). Development of stages of the cycle in mouse seminiferous epithelium after transplantation of green fluorescent protein-labeled spermatogonial stem cells. Biol. Reprod. 66, 1422–1429.
Crossref | GoogleScholarGoogle Scholar | PubMed |

von Schonfeldt, V. , Krishnamurthy, H. , Foppiani, L. , and Schlatt, S. (1999). Magnetic cell sorting is a fast and effective method of enriching viable spermatogonia from Djungarian hamster, mouse, and marmoset monkey testes. Biol. Reprod. 61, 582–589.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wistuba, J. , Schlatt, S. , Cantauw, C. , von Schonfeldt, V. , Nieschlag, E. , and Behr, R. (2002). Transplantation of wild-type spermatogonia leads to complete spermatogenesis in testes of cyclic 3′,5′-adenosine monophosphate response element modulator-deficient mice. Biol. Reprod. 67, 1052–1057.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Yomogida, K. , Yagura, Y. , Tadokoro, Y. , and Nishimune, Y. (2003). Dramatic expansion of germinal stem cells by ectopically expressed human glial cell line-derived neurotrophic factor in mouse Sertoli cells. Biol. Reprod. 69, 1303–1307.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Yoshizaki, G. , Tago, Y. , Takeuchi, Y. , Sawatari, E. , Kobayashi, T. , and Takeuchi, T. (2005). Green fluorescent protein labeling of primordial germ cells using a nontransgenic method and its application for germ cell transplantation in salmonidae. Biol. Reprod. 73, 88–93.
Crossref | GoogleScholarGoogle Scholar | PubMed |

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.
Crossref | GoogleScholarGoogle Scholar | PubMed |