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

Relationship between sperm apoptosis and bull fertility: in vivo and in vitro studies

Lauren Erickson A B , Tom Kroetsch C and Muhammad Anzar A B D
+ Author Affiliations
- Author Affiliations

A Cryobiology Lab, Canadian Animal Genetic Resource Program, Agriculture and Agri-Food Canada, Saskatoon Research Center, 52 Campus Drive, Saskatoon, Saskatchewan S7N 5B4, Canada.

B Department of Veterinary Biomedical Sciences, Western College of Veterinary Medicine, University of Saskatchewan, 52 Campus Drive, Saskatoon, Saskatchewan S7N 5B4, Canada.

C Semex Alliance, 130 Stone Road West, Guelph, ON N1G 3Z2, Canada.

D Corresponding authors. Emails: anzarm@agr.gc.ca; muhammad.anzar@usask.ca

Reproduction, Fertility and Development 28(9) 1369-1375 https://doi.org/10.1071/RD14417
Submitted: 30 October 2014  Accepted: 16 January 2015   Published: 13 March 2015

Abstract

The objectives of this study were to confirm the relationship of apoptosis-associated membrane and nuclear changes in bull spermatozoa with field fertility, to predict the fertility of beef bulls used for natural breeding and to study the role of DNA-nicked spermatozoa in early embryonic development. In Experiment 1, the relationship between fertility and different sperm populations identified by the Annexin V/propidium iodide (PI) and terminal deoxynucleotidyl transferase mediated dUTP nick end labeling (TUNEL) assays was determined. Bull fertility was related to live (P < 0.05) and necrotic (P < 0.01) and DNA-nicked (P < 0.001) spermatozoa. In Experiment 2, the percentage of DNA-nicked spermatozoa was determined in 15 beef bulls used for natural breeding and their fertility potential was determined using a regression model developed in Experiment 1.The predicted fertility deviation of beef bulls ranged from –7.3 to 2.4. In Experiment 3, the effect of DNA-nicked spermatozoa on in vitro cleavage and blastocyst rates was evaluated, using 30 000 or 300 000 spermatozoa per droplet. Cleavage rate was adversely affected (P < 0.05) by DNA-nicked spermatozoa, regardless of sperm concentration. Blastocyst rate was lower (P < 0.05) in high DNA-nicked spermatozoa at the lower sperm concentration. In conclusion, the incidence of DNA-nicked spermatozoa is a useful marker to predict a bull’s fertility potential. DNA-nicked spermatozoa showed adverse effects on early embryonic development.

Additional keywords: beef, blastocyst, cleavage, dairy, DNA nicks, membrane asymmetry.


References

Aitken, R. J., and Baker, M. A. (2013). Causes and consequences of apoptosis in spermatozoa; contributions to infertility and impacts on development. Int. J. Dev. Biol. 57, 265–272.
Causes and consequences of apoptosis in spermatozoa; contributions to infertility and impacts on development.Crossref | GoogleScholarGoogle Scholar | 23784837PubMed |

Aitken, R. J., Findlay, J. K., Hutt, K. J., and Kerr, J. B. (2011). Apoptosis in the germ line. Reproduction 141, 139–150.
Apoptosis in the germ line.Crossref | GoogleScholarGoogle Scholar | 21148286PubMed |

Anzar, M., He, L. W., Buhr, M. M., Kroetsch, T. G., and Pauls, K. P. (2002). Sperm apoptosis in fresh and cryopreserved bull semen detected by flow cytometry and its relationship with fertility. Biol. Reprod. 66, 354–360.
Sperm apoptosis in fresh and cryopreserved bull semen detected by flow cytometry and its relationship with fertility.Crossref | GoogleScholarGoogle Scholar | 11804948PubMed |

Anzar, M., Kroetsch, T., and Boswall, L. (2011). Cryopreservation of bull semen shipped overnight and its effect on post-thaw sperm motility, plasma membrane integrity, mitochondrial membrane potential and normal acrosomes. Anim. Reprod. Sci. 126, 23–31.
Cryopreservation of bull semen shipped overnight and its effect on post-thaw sperm motility, plasma membrane integrity, mitochondrial membrane potential and normal acrosomes.Crossref | GoogleScholarGoogle Scholar | 21621352PubMed |

Arends, M. J., and Wyllie, A. H. (1991). Apoptosis: mechanisms and roles in pathology. Int. Rev. Exp. Pathol. 32, 223–254.
Apoptosis: mechanisms and roles in pathology.Crossref | GoogleScholarGoogle Scholar | 1677933PubMed |

Brackett, B. G., and Oliphant, G. (1975). Capacitation of rabbit spermatozoa in vitro. Biol. Reprod. 12, 260–274.
Capacitation of rabbit spermatozoa in vitro.Crossref | GoogleScholarGoogle Scholar | 1122333PubMed |

Dogan, S., Mason, M. C., Govindaraju, A., Belser, L., Kaya, A., Stokes, J., Rowe, D., and Memili, E. (2013). Interrelationships between apoptosis and fertility in bull spermatozoa. J. Reprod. Dev. 59, 18–26.
| 22986927PubMed |

Gillan, L., Kroetsch, T., Maxwell, W. M., and Evans, G. (2008). Assessment of in vitro sperm characteristics in relation to fertility in dairy bulls. Anim. Reprod. Sci. 103, 201–214.
Assessment of in vitro sperm characteristics in relation to fertility in dairy bulls.Crossref | GoogleScholarGoogle Scholar | 17208395PubMed |

Gorczyca, W., Traganos, F., Jesionowska, H., and Darzynkiewicz, Z. (1993). Presence of DNA strand breaks and increased sensitivity of DNA in situ to denaturation in abnormal human sperm cells: analogy to apoptosis of somatic cells. Exp. Cell Res. 207, 202–205.
Presence of DNA strand breaks and increased sensitivity of DNA in situ to denaturation in abnormal human sperm cells: analogy to apoptosis of somatic cells.Crossref | GoogleScholarGoogle Scholar | 8391465PubMed |

Gravance, C. G., Vishwanath, R., Pitt, C., Garner, D. L., and Casey, P. J. (1998). Effects of cryopreservation on bull sperm head morphometry. J. Androl. 19, 704–709.
| 9876021PubMed |

Martin, S. J., Reutelingsperger, C. P., McGahon, A. J., Rader, J. A., van Schie, R. C., LaFace, D. M., and Green, D. R. (1995). Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182, 1545–1556.
Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl.Crossref | GoogleScholarGoogle Scholar | 7595224PubMed |

Martin, G., Sabido, O., Durand, P., and Levy, R. (2004). Cryopreservation induces an apoptosis-like mechanism in bull spermatozoa. Biol. Reprod. 71, 28–37.
Cryopreservation induces an apoptosis-like mechanism in bull spermatozoa.Crossref | GoogleScholarGoogle Scholar | 14973261PubMed |

Martin, G., Cagnon, N., Sabido, O., Sion, B., Grizard, G., Durand, P., and Levy, R. (2007). Kinetics of occurrence of some features of apoptosis during the cryopreservation process of bovine spermatozoa. Hum. Reprod. 22, 380–388.
Kinetics of occurrence of some features of apoptosis during the cryopreservation process of bovine spermatozoa.Crossref | GoogleScholarGoogle Scholar | 17092986PubMed |

Mocé, E., and Graham, J. K. (2008). In vitro evaluation of sperm quality. Anim. Reprod. Sci. 105, 104–118.
In vitro evaluation of sperm quality.Crossref | GoogleScholarGoogle Scholar | 18178345PubMed |

Rodríguez-Martínez, H. (2006). Can we increase the estimated value of semen assessment? Reprod. Domest. Anim. 41, 2–10.
Can we increase the estimated value of semen assessment?Crossref | GoogleScholarGoogle Scholar | 16984464PubMed |

Saacke, R. G. (2008). Sperm morphology: its relevance to compensable and uncompensable traits in semen. Theriogenology 70, 473–478.
Sperm morphology: its relevance to compensable and uncompensable traits in semen.Crossref | GoogleScholarGoogle Scholar | 18495234PubMed |

Simon, L., Lutton, D., McManus, J., and Lewis, S. E. (2011). Sperm DNA damage measured by the alkaline Comet assay as an independent predictor of male infertility and in vitro fertilisation success. Fertil. Steril. 95, 652–657.
Sperm DNA damage measured by the alkaline Comet assay as an independent predictor of male infertility and in vitro fertilisation success.Crossref | GoogleScholarGoogle Scholar | 20864101PubMed |

Van Doormaal, B. (1993). Linear model evaluations of non-return rates for dairy and beef bulls in Canadian AI. Can. J. Anim. Sci. 73, 795–804.
Linear model evaluations of non-return rates for dairy and beef bulls in Canadian AI.Crossref | GoogleScholarGoogle Scholar |

Vaux, D. L., and Korsmeyer, S. J. (1999). Cell death in development. Cell 96, 245–254.
Cell death in development.Crossref | GoogleScholarGoogle Scholar | 9988219PubMed |

Vermes, I., Haanen, C., Steffens-Nakken, H., and Reutelingsperger, C. (1995). A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein-labelled Annexin V. J. Immunol. Methods 184, 39–51.
A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein-labelled Annexin V.Crossref | GoogleScholarGoogle Scholar | 7622868PubMed |

Walters, A. H., Saacke, R. G., Pearson, R. E., and Gwazdauskas, F. C. (2005). The incidence of apoptosis after IVF with morphologically abnormal bovine spermatozoa. Theriogenology 64, 1404–1421.
The incidence of apoptosis after IVF with morphologically abnormal bovine spermatozoa.Crossref | GoogleScholarGoogle Scholar | 15893815PubMed |

Waterhouse, K. E., Haugan, T., Kommisrud, E., Tverdal, A., Flatberg, G., Farstad, W., Evenson, D. P., and De Angelis, P. M. (2006). Sperm DNA damage is related to field fertility of semen from young Norwegian Red bulls. Reprod. Fertil. Dev. 18, 781–788.
Sperm DNA damage is related to field fertility of semen from young Norwegian Red bulls.Crossref | GoogleScholarGoogle Scholar | 17032587PubMed |

Wyllie, A. H., Kerr, J. F., and Currie, A. R. (1980). Cell death: the significance of apoptosis. Int. Rev. Cytol. 68, 251–306.
Cell death: the significance of apoptosis.Crossref | GoogleScholarGoogle Scholar | 7014501PubMed |

Yin, Y., Stahl, B. C., DeWolf, W. C., and Morgentaler, A. (1998). p53-mediated germ cell quality control in spermatogenesis. Dev. Biol. 204, 165–171.
p53-mediated germ cell quality control in spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 9851850PubMed |