Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Donor sperm production in heterologous recipients by testis germ cell transplantation in the dromedary camel

Muren Herrid https://orcid.org/0000-0002-3975-5481 A E , Peter Nagy B , Jutka Juhasz B , Jane M. Morrell C , M. Billah A , Kamal Khazanehdari D and Julian A. Skidmore A
+ Author Affiliations
- Author Affiliations

A Camel Reproduction Centre, PO Box 79914, Dubai, United Arab Emirates.

B Emirates Industry for Camel Milk and Products, Dubai, United Arab Emirates.

C Division of Reproduction, Clinical Sciences, Swedish University of Agricultural Sciences, Uppsala, Sweden.

D Molecular Biology and Genetics Laboratory, PO Box 597, Dubai, United Arab Emirates.

E Corresponding author. Email: mherrid@gmail.com

Reproduction, Fertility and Development 31(3) 538-546 https://doi.org/10.1071/RD18191
Submitted: 28 May 2018  Accepted: 12 September 2018   Published: 12 October 2018

Abstract

The object of this study was to investigate if testis germ cell transplantation (TGCT) into a heterologous recipient would result in donor-origin spermatogenesis in the dromedary camel. First, we investigated a workable protocol for TGCT in camels, including donor cell isolation, enrichment by density gradient centrifugation (Percoll and Bovicoll), rete testis injection and microsatellite detection of donor and recipient genotypes. Second, the effects of three doses of Dolichos biflorus agglutinin (DBA), a glycoprotein that specifically binds to gonocytes or Type A spermatogonia, on testis germ cell depletion were investigated by direct injection into the rete testis of a male camel. Seven recipients were prepared with DBA treatment, two males were castrated at 4 weeks for depletion assessment and the remaining five received donor cells 4–6 weeks after treatment. On average, ~17 million cells were isolated per gram of testis tissue, with 19.5 ± 1.9% DBA-positive (DBA+) cells. Percoll centrifugation yielded a 1.5-fold increase in DBA+ cells while Bovicoll centrifugation produced a 2.5-fold increase from the input cells of 18.6 ± 2.1% DBA+ cells. Semen was collected from the recipients 13–20 weeks after transfer and the presence of donor DNA in the samples was determined using microsatellite markers. In two of the five recipients, all semen samples were shown to be positive for donor-derived cells. These results demonstrate for the first time that: (1) heterologous testicular germ cell transplantation in camels is feasible and the recipients are able to produce spermatozoa of donor origin and (2) DBA can be used effectively to deplete endogenous stem cells.

Additional keywords : chemical depletion, gamete biology, spermatogenesis, stem cells.


References

Anglin, E., Davey, R., Herrid, M., Hope, S., Kurkuri, M., and Pasic, P. (2010). Cell microarrays for the screening of factors that allow the enrichment of bovine testicular cells. Cytometry A 77, 881–889.
Cell microarrays for the screening of factors that allow the enrichment of bovine testicular cells.Crossref | GoogleScholarGoogle Scholar |

Avery, B., and Greve, T. (1995). Impact of Percoll on bovine spermatozoa used for in vitro insemination. Theriogenology 44, 871–878.
Impact of Percoll on bovine spermatozoa used for in vitro insemination.Crossref | GoogleScholarGoogle Scholar |

Borjigin, U., Davey, R., Hutton, K., and Herrid, M. (2010). Expression of promyelocytic leukaemia zinc-finger in ovine testis and its application in evaluating the enrichment efficiency of differential plating. Reprod. Fertil. Dev. 22, 733–742.
Expression of promyelocytic leukaemia zinc-finger in ovine testis and its application in evaluating the enrichment efficiency of differential plating.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, 11303–11307.
Germline transmission of donor haplotype following spermatogonial transplantation.Crossref | GoogleScholarGoogle Scholar |

Brinster, C. J., Ry, B. Y., Avarbock, M. R., Karagenc, L., Brinster, R. L., and Orwig, K. E. (2003). Restoration of fertility by germ cell transplantation requires effective recipient preparation. Biol. Reprod. 69, 412–420.
Restoration of fertility by germ cell transplantation requires effective recipient preparation.Crossref | GoogleScholarGoogle Scholar |

Chuma, S., Kanatsu-Shinohara, M., Inoue, K., Ogonuki, N., Miki, H., Toyokuni, S., Hosokawa, M., Nakatsuji, N., Ogura, A., and Shinohara, T. (2005). Spermatogenesis from epiblast and primordial germ cells following transplantation into postnatal mouse testis. Development 132, 117–122.
Spermatogenesis from epiblast and primordial germ cells following transplantation into postnatal mouse testis.Crossref | GoogleScholarGoogle Scholar |

Furimsky, A., Vuong, N., Xu, H., Kumarathasan, P., Xu, M., Weerachatyanukul, W., Bou Khali, M., Kates, M., and Tanphaichitr, N. (2005). Percoll gradient-centrifuged capacitated mouse sperm have increased fertilizing ability and higher contents of sulfogalactosylglycerolipid and docosahexaenoic acid-containing phosphatidylcholine compared to washed capacitated mouse sperm. Biol. Reprod. 72, 574–583.
Percoll gradient-centrifuged capacitated mouse sperm have increased fertilizing ability and higher contents of sulfogalactosylglycerolipid and docosahexaenoic acid-containing phosphatidylcholine compared to washed capacitated mouse sperm.Crossref | GoogleScholarGoogle Scholar |

Gabor, F., Bogner, E., Weissenboeck, A., and Wirth, M. (2004). The lectin–cell interaction and its implications to intestinal lectin-mediated drug delivery. Adv. Drug Deliv. Rev. 56, 459–480.
The lectin–cell interaction and its implications to intestinal lectin-mediated drug delivery.Crossref | GoogleScholarGoogle Scholar |

Goel, S., Sugimoto, M., Minami, N., Yamada, M., Kume, S., and Imai, H. (2007). Identification, isolation, and in vitro culture of porcine gonocytes. Biol. Reprod. 77, 127–137.
Identification, isolation, and in vitro culture of porcine gonocytes.Crossref | GoogleScholarGoogle Scholar |

Herrid, M., and McFarlane, J. R. (2013). Application of testis germ cell transplantation in breeding systems of food producing species: a review. Anim. Biotechnol. 24, 293–306.
Application of testis germ cell transplantation in breeding systems of food producing species: a review.Crossref | GoogleScholarGoogle Scholar |

Herrid, M., Vignarajan, S., Davey, R., Dobrinski, I., and Hill, J. R. (2006). Successful transplantation of bovine testicular cells to heterologous recipients. Reproduction 132, 617–624.
Successful transplantation of bovine testicular cells to heterologous recipients.Crossref | GoogleScholarGoogle Scholar |

Herrid, M., Davey, R. J., and Hill, J. R. (2007). Characterization of germ cells from pre-pubertal bull calves in preparation for germ cell transplantation. Cell Tissue Res. 330, 321–329.
Characterization of germ cells from pre-pubertal bull calves in preparation for germ cell transplantation.Crossref | GoogleScholarGoogle Scholar |

Herrid, M., Olejnik, J., Jackson, M., Suchowerska, N., Stockwell, S., Davey, R., Hutton, K., Hope, S., and Hill, J. R. (2009a). Irradiation enhances the efficiency of testicular germ cell transplantation in sheep. Biol. Reprod. 81, 898–905.
Irradiation enhances the efficiency of testicular germ cell transplantation in sheep.Crossref | GoogleScholarGoogle Scholar |

Herrid, M., Davey, R. J., Hutton, K., Colditz, I. G., and Hill, J. R. (2009b). A comparison of methods for preparing enriched populations of bovine spermatogonia. Reprod. Fertil. Dev. 21, 393–399.
A comparison of methods for preparing enriched populations of bovine spermatogonia.Crossref | GoogleScholarGoogle Scholar |

Herrid, M., Vajta, G., and Skidmore, J. A. (2017). Current status and future direction of cryopreservation of camelid embryos. Theriogenology 89, 20–25.
Current status and future direction of cryopreservation of camelid embryos.Crossref | GoogleScholarGoogle Scholar |

Hill, J. R., and Dobrinski, I. (2006). Male germ cell transplantation in livestock. Reprod. Fertil. Dev. 18, 13–18.
Male germ cell transplantation in livestock.Crossref | GoogleScholarGoogle Scholar |

Honaramooz, A., Megee, S. O., and Dobrinski, I. (2002). Germ cell transplantation in pigs. Biol. Reprod. 66, 21–28.
Germ cell transplantation in pigs.Crossref | GoogleScholarGoogle Scholar |

Honaramooz, A., Behboodi, E., Blash, S., Megee, S. O., and Dobrinski, I. (2003a). Germ cell transplantation in goats. Mol. Reprod. Dev. 64, 422–428.
Germ cell transplantation in goats.Crossref | GoogleScholarGoogle Scholar |

Honaramooz, A., Behboodi, E., Megee, S. O., Overton, S. A., Galantino-Homer, H., Echelard, Y., and Dobrinski, I. (2003b). Fertility and germline transmission of donor haplotype following germ cell transplantation in immunocompetent goats. Biol. Reprod. 69, 1260–1264.
Fertility and germline transmission of donor haplotype following germ cell transplantation in immunocompetent goats.Crossref | GoogleScholarGoogle Scholar |

Honaramooz, A., Behboodi, E., Hausler, C. L., Blash, S., Ayres, S., Azuma, C., Echelard, Y., and Dobrinski, I. (2005). Depletion of endogenous germ cells in male pigs and goats in preparation for germ cell transplantation. J. Androl. 26, 698–705.
Depletion of endogenous germ cells in male pigs and goats in preparation for germ cell transplantation.Crossref | GoogleScholarGoogle Scholar |

Izadyar, R. F., Spierenberg, G. T., Creemers, L. B., den Ouden, K., and de Rooij, D. G. (2002). Isolation and purification of type A spermatogonia from the bovine testis. Reproduction 124, 85–94.
Isolation and purification of type A spermatogonia from the bovine testis.Crossref | GoogleScholarGoogle Scholar |

Kanatsu-Shinohara, M., Ogonuki, N., Matoba, S., Morimoto, H., Ogura, A., and Shinohara, T. (2014). Improved serum- and feeder-free culture of mouse germline stem cells. Biol. Reprod. 91, 88.

Kim, M., Rao, M. V., Tweardy, D. J., Prakash, M., Galili, U., and Gorelik, E. (1993). Lectin-induced apoptosis of tumour cells. Glycobiology 3, 447–453.
Lectin-induced apoptosis of tumour cells.Crossref | GoogleScholarGoogle Scholar |

Lin, Z., Bao, J., Kong, Q., Bai, Y., Luo, F., Songyang, Z., Wu, Y., and Huang, J. (2017). Effective production of recipient male pigs for spermatogonial stem cell transplantation by intratesticular injection with busulfan. Theriogenology 89, 365–373.e2.
Effective production of recipient male pigs for spermatogonial stem cell transplantation by intratesticular injection with busulfan.Crossref | GoogleScholarGoogle Scholar |

Loréa, P., Goldschmidt, D., Darro, F., Salmon, I., Bovin, N., Gabius, H. J., Kiss, R., and Danguy, A. (1997). In vitro characterization of lectin-induced alterations on the proliferative activity of three human melanoma cell lines. Melanoma Res. 7, 353–363.
In vitro characterization of lectin-induced alterations on the proliferative activity of three human melanoma cell lines.Crossref | GoogleScholarGoogle Scholar |

Morrell, J. M., and Mayer, I. (2017). Reproduction biotechnologies in germplasm banking of livestock species: a review. Zygote 25, 545–557.

Nagy, P., Skidmore, J. A., and Juhasz, J. (2013). Use of assisted reproduction for the improvement of milk production in dairy camels (Camelus dromedarius). Anim. Reprod. Sci. 136, 205–210.
Use of assisted reproduction for the improvement of milk production in dairy camels (Camelus dromedarius).Crossref | GoogleScholarGoogle Scholar |

Ogawa, T., Dobrinski, I., and Brinster, R. L. (1999). Recipient preparation is critical for spermatogonial transplantation in the rat. Tissue Cell 31, 461–472.
Recipient preparation is critical for spermatogonial transplantation in the rat.Crossref | GoogleScholarGoogle Scholar |

Onofre, J., Baert, Y., Faes, K., and Goossens, E. (2016). Cryopreservation of testicular tissue or testicular cell suspensions: a pivotal step in fertility preservation. Hum. Reprod. Update 22, 744–761.
Cryopreservation of testicular tissue or testicular cell suspensions: a pivotal step in fertility preservation.Crossref | GoogleScholarGoogle Scholar |

Petrossian, K., Banner, L. R., and Oppenheimer, S. B. (2007). Lectin binding and effects in culture on human cancer and non-cancer cell lines: examination of issues of interest in drug design strategies. Acta Histochem. 109, 491–500.
Lectin binding and effects in culture on human cancer and non-cancer cell lines: examination of issues of interest in drug design strategies.Crossref | GoogleScholarGoogle Scholar |

Piller, S. C., Ewart, G. D., Jans, D. A., Gage, P. W., and Cox, G. B. (1999). The amino-terminal region of Vpr from human immunodeficiency virus type 1 forms ion channels and kills neurons. J. Virol. 73, 4230–4238.

Redden, E., Davey, R., Borjigin, U., Hutton, K., Hinch, G., Hope, S., Hill, J., and Herrid, M. (2009). Large quantity cryopreservation of bovine testicular cells and its effect on enrichment of type A spermatogonia. Cryobiology 58, 190–195.
Large quantity cryopreservation of bovine testicular cells and its effect on enrichment of type A spermatogonia.Crossref | GoogleScholarGoogle Scholar |

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.
Remodeling of the postnatal mouse testis is accompanied by dramatic changes in stem cell number and niche accessibility.Crossref | GoogleScholarGoogle Scholar |

Skidmore, J. A., Morton, K. M., and Billah, M. (2013). Artificial insemination in dromedary camels. Anim. Reprod. Sci. 136, 178–186.
Artificial insemination in dromedary camels.Crossref | GoogleScholarGoogle Scholar |

Stockwell, S., Herrid, M., Davey, R., Brownlee, A., Hutton, K., and Hill, J. R. (2009). Microsatellite detection of donor-derived sperm DNA following germ cell transplantation in cattle. Reprod. Fertil. Dev. 21, 462–468.
Microsatellite detection of donor-derived sperm DNA following germ cell transplantation in cattle.Crossref | GoogleScholarGoogle Scholar |

Verini-Supplizi, A., Stradaioli, G., Fagioli, O., and Parillo, F. (2000). Localization of the lectin reactive sites in adult and prepubertal horse testes. Res. Vet. Sci. 69, 113–118.
Localization of the lectin reactive sites in adult and prepubertal horse testes.Crossref | GoogleScholarGoogle Scholar |

Wrobel, K. H. (2000). Prespermatogenesis and spermatogoniogenesis in the bovine testis. Anat. Embryol. (Berl.) 202, 209–222.
Prespermatogenesis and spermatogoniogenesis in the bovine testis.Crossref | GoogleScholarGoogle Scholar |

Yang, Y., Yarahmadi, M., and Honaramooz, A. (2010). Development of novel strategies for the isolation of piglet testis cells with a high proportion of gonocytes. Reprod. Fertil. Dev. 22, 1057–1065.
Development of novel strategies for the isolation of piglet testis cells with a high proportion of gonocytes.Crossref | GoogleScholarGoogle Scholar |