Sire Effect and Sperm Apoptosis on Bovine Embryonic Cleavage and Subsequent In Vitro Embryo Development

Chaveiro, Antonio; Santos, Pedro; Carvalhais, Isabel; Agrícola, Ricardo; Faheem, Marwa; Habibi, Afrooz; Moreira da Silva, Fernando

doi:https://doi.org/10.3814/2010/324529

SRX Veterinary Science

On this page

Abstract References Copyright Related Articles

Research Article | Open Access

Volume 2010 | Article ID 324529 | https://doi.org/10.3814/2010/324529

Sire Effect and Sperm Apoptosis on Bovine Embryonic Cleavage and Subsequent In Vitro Embryo Development

Antonio Chaveiro,^1,2Pedro Santos,¹Isabel Carvalhais,^1,2Ricardo Agrícola,^1,2Marwa Faheem,^1,2Afrooz Habibi,¹and Fernando Moreira da Silva^1,2

Received24 Sept 2009

Accepted02 Nov 2009

Published13 Dec 2009

Abstract

The present study was conducted to evaluate sire effect on the kinetics of in vitro cleavage and further embryonic development after in vitro fertilization (IVF) using bulls of an Azorean rare breed called “Ramo Grande” (RG), and examine whether a relationship exists between bull's sperm apoptosis and sire in vitro fertility. Results showed that cleavage and blastocyst rates were statistically different between bulls (P<.05), being possible to notice different ability to produce embryos with good development competence (P<.05), as assessed by the proportion of fertilized oocytes that reached blastocyst stage. The proportion of blastocysts that continued the development to hatched blastocysts stage ranged from 9.1 to 87.5% (P<.05). Differences in sperm apoptosis increased during the swim-up procedure, which was statistically different (P<.05) between bulls, being negatively correlated with the ability of those bulls to fertilize oocytes and resulting embryos to develop to hatched blastocysts (R=−0.96, P≤.01). In conclusion, this study clearly demonstrated great differences between bulls, concerning apoptosis levels, which were negatively related to bull's ability to produce good quality embryos after IVF.

References

P. Comizzoli, B. Marquant-Le Guienne, Y. Heyman, and J. P. Renard, “Onset of the first S-phase is determined by a paternal effect during the G1-phase in bovine zygotes,” Biology of Reproduction, vol. 62, no. 6, pp. 1677–1684, 2000.
View at: Google Scholar
F. Ward, D. Rizos, M. P. Boland, and P. Lonergan, “Effect of reducing sperm concentration during IVF on the ability to distinguish between bulls of high and low field fertility: work in progress,” Theriogenology, vol. 59, no. 7, pp. 1575–1584, 2003.
View at: Publisher Site | Google Scholar
F. Ward, D. Rizos, D. Corridan, K. Quinn, M. Boland, and P. Lonergan, “Paternal influence on the time of first embryonic cleavage post insemination and the implications for subsequent bovine embryo development in vitro and fertility in vivo,” Molecular Reproduction and Development, vol. 60, no. 1, pp. 47–55, 2001.
View at: Publisher Site | Google Scholar
A. Chaveiro, Bull sperm cryopreservation, fundamental and applied aspects, Dissertation, Veterinary Faculty, Utrecht University, Utrecht, The Netherlands, 2005.
T. Said, A. Agarwal, S. Grunewald et al., “Selection of nonapoptotic spermatozoa as a new tool for enhancing assisted reproduction outcomes: an in vitro model,” Biology of Reproduction, vol. 74, no. 3, pp. 530–537, 2006.
View at: Publisher Site | Google Scholar
E. Seli, D. K. Gardner, W. B. Schoolcraft, O. Moffatt, and D. Sakkas, “Extent of nuclear DNA damage in ejaculated spermatozoa impacts on blastocyst development after in vitro fertilization,” Fertility and Sterility, vol. 82, no. 2, pp. 378–383, 2004.
View at: Publisher Site | Google Scholar
G. D. Ball, M. L. Leibfried, R. W. Lenz, R. L. Ax, B. D. Bavister, and N. L. First, “Factors affecting successful in vitro fertilization of bovine follicular oocytes,” Biology of Reproduction, vol. 28, no. 3, pp. 717–725, 1983.
View at: Google Scholar
J. J. Parrish, J. L. Susko-Parrish, M. L. Leibfried-Rutledge, E. S. Critser, W. H. Eyestone, and N. L. First, “Bovine in vitro fertilization with frozen-thawed semen,” Theriogenology, vol. 25, no. 4, pp. 591–600, 1986.
View at: Google Scholar
J. J. Parrish, J. Susko-Parrish, M. A. Winer, and N. L. First, “Capacitation of bovine sperm by heparin,” Biology of Reproduction, vol. 38, no. 5, pp. 1171–1180, 1988.
View at: Google Scholar
B. Marquant-Le Guienne, P. Humblot, M. Thibier, and C. Thibault, “Evaluation of bull semen fertility by homologous in vitro fertilization tests,” Reproduction Nutrition Development, vol. 30, no. 2, pp. 259–266, 1990.
View at: Google Scholar
T. G. Kroetsch and R. Stubbings, “Sire and insemination dose does effect in vitro fertilization of bovine oocytes,” Theriogenology, vol. 37, p. 240, 1992.
View at: Google Scholar
B. Marquant-Le Guienne, P. Humblot, N. Guillon, O. Gerard, and M. Thibier, “In vitro fertilization as a tool to evaluate fertility in the bovine,” in Proceedings of the 12th International Congress on Animal Reproduction, pp. 662–664, The Hague, The Netherlands, August 1992.
View at: Google Scholar
L. Vandaele, B. Mateusen, D. Maes, A. de Kruif, and A. Van Soom, “Is apoptosis in bovine in vitro produced embryos related to early developmental kinetics and in vivo bull fertility?,” Theriogenology, vol. 65, no. 9, pp. 1691–1703, 2006.
View at: Publisher Site | Google Scholar
M. Anzar, L. He, M. M. Buhr, T. G. Kroetsch, and K. P. Pauls, “Sperm apoptosis in fresh and cryopreserved bull semen detected by flow cytometry and its relationship with fertility,” Biology of Reproduction, vol. 66, no. 2, pp. 354–360, 2002.
View at: Google Scholar
A. Chaveiro, P. Santos, and F. M. da Silva, “Assessment of sperm apoptosis in cryopreserved bull semen after swim-up treatment: a flow cytometric study,” Reproduction in Domestic Animals, vol. 42, no. 1, pp. 17–21, 2007.
View at: Publisher Site | Google Scholar
B. R. Zhang, B. Larsson, N. Lundeheim, and H. Rodriguez-Martinez, “Relationship between embryo development in vitro and 56-day nonreturn rates of cows inseminated with frozen-thawed semen from dairy bulls,” Theriogenology, vol. 48, no. 2, pp. 221–231, 1997.
View at: Publisher Site | Google Scholar
F. Ward, P. Lonergan, D. Rizos, D. Corridan, and M. Boland, “Bull effects on kinetics of fertilization in vitro and the implications for subsequent embryo development,” Theriogenology, vol. 55, p. 375, 2001.
View at: Google Scholar
A. H. Walters, R. G. Saacke, R. E. Pearson, and F. C. Gwazdauskas, “The incidence of apoptosis after IVF with morphologically abnormal bovine spermatozoa,” Theriogenology, vol. 64, no. 6, pp. 1404–1421, 2005.
View at: Publisher Site | Google Scholar
D. Rizos, F. Ward, P. Duffy, M. P. Boland, and P. Lonergan, “Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality,” Molecular Reproduction and Development, vol. 61, no. 2, pp. 234–248, 2002.
View at: Publisher Site | Google Scholar
D. Sakkas, “The use of blastocyst culture to avoid inheritance of an abnormal paternal genome after ICSI,” Human Reproduction, vol. 14, no. 1, pp. 4–5, 1999.
View at: Publisher Site | Google Scholar
T. A. L. Brevini Gandolfi and F. Gandolfi, “The maternal legacy to the embryo: cytoplasmic components and their effects on early development,” Theriogenology, vol. 55, no. 6, pp. 1255–1276, 2001.
View at: Publisher Site | Google Scholar
A. N. Fatehi, M. M. Bevers, E. Schoevers, B. A. J. Roelen, B. Colenbrander, and B. M. Gadella, “DNA damage in bovine sperm does not block fertilization and early embryonic development but induces apoptosis after the first cleavages,” Journal of Andrology, vol. 27, no. 2, pp. 176–188, 2006.
View at: Publisher Site | Google Scholar
S.-L. Weng, S. L. Taylor, M. Morshedi et al., “Caspase activity and apoptotic markers in ejaculated human sperm,” Molecular Human Reproduction, vol. 8, no. 11, pp. 984–991, 2002.
View at: Google Scholar
G. Barroso, S. Taylor, M. Morshedi, F. Manzur, F. Gavino, and S. Oehninger, “Mitochondrial membrane potential integrity and plasma membrane translocation of phosphatidylserine as early apoptotic markers: a comparison of two different sperm subpopulations,” Fertility and Sterility, vol. 85, no. 1, pp. 149–154, 2006.
View at: Publisher Site | Google Scholar
G. Martin, O. Sabido, P. Durand, and R. Levy, “Phosphatidylserine externalization in human sperm induced by calcium ionophore A23187: relationship with apoptosis, membrane scrambling and the acrosome reaction,” Human Reproduction, vol. 20, no. 12, pp. 3459–3468, 2005.
View at: Publisher Site | Google Scholar
S. Grunewald, T. Baumann, U. Paasch, and H.-J. Glander, “Capacitation and acrosome reaction in nonapoptotic human spermatozoa,” in Annals of the New York Academy of Sciences, vol. 1090, pp. 138–146, 2006.
View at: Publisher Site | Google Scholar
U. Paasch, S. Grunewald, G. Fitzl, and H. J. Glander, “Deterioration of plasma membrane is associated with activated caspases in human spermatozoa,” Journal of Andrology, vol. 24, no. 2, pp. 246–252, 2003.
View at: Google Scholar
U. Paasch, S. Grunewald, A. Agarwal, and H.-J. Glandera, “Activation pattern of caspases in human spermatozoa,” Fertility and Sterility, vol. 81, pp. 802–809, 2004.
View at: Publisher Site | Google Scholar
G. Martin, N. Cagnon, O. Sabido et al., “Kinetics of occurrence of some features of apoptosis during the cryopreservation process of bovine spermatozoa,” Human Reproduction, vol. 22, no. 2, pp. 380–388, 2007.
View at: Publisher Site | Google Scholar
S. Oehninger, M. Morshedi, S.-L. Weng, S. Taylor, H. Duran, and S. Beebe, “Presence and significance of somatic cell apoptosis markers in human ejaculated spermatozoa,” Reproductive BioMedicine Online, vol. 7, no. 4, pp. 469–476, 2003.
View at: Google Scholar
X. Wang, R. K. Sharma, S. C. Sikka, A. J. Thomas, Jr., T. Falcone, and A. Agarwal, “Oxidative stress is associated with increased apoptosis leading to spermatozoa DNA damage in patients with male factor infertility,” Fertility and Sterility, vol. 80, no. 3, pp. 531–535, 2003.
View at: Publisher Site | Google Scholar
U. Paasch, R. K. Sharma, A. K. Gupta et al., “Cryopreservation and thawing is associated with varying extent of activation of apoptotic machinery in subsets of ejaculated human spermatozoa,” in Biology of Reproduction, vol. 71, no. 6, pp. 1828–1837, 2004.
View at: Publisher Site | Google Scholar
S. L. Taylor, S. L. Weng, P. Fox et al., “Somatic cell apoptosis markers and pathways in human ejaculated sperm: potential utility as indicators of sperm quality,” Molecular Human Reproduction, vol. 10, no. 11, pp. 825–834, 2004.
View at: Publisher Site | Google Scholar
G. Martin, O. Sabido, P. Durand, and R. Levy, “Cryopreservation induces an apoptosis-like mechanism in bull sperm,” Biology of Reproduction, vol. 71, no. 1, pp. 28–37, 2004.
View at: Publisher Site | Google Scholar
A. Januskauskas, A. Johannisson, and H. Rodriguez-Martinez, “Subtle membrane changes in cryopreserved bull semen in relation with sperm viability, chromatin structure, and field fertility,” Theriogenology, vol. 60, no. 4, pp. 743–758, 2003.
View at: Publisher Site | Google Scholar
D. A. Spandidos, E. Koumantakis, S. Sifakis, and G. Sourvinos, “Microsatellite mutations in spontaneously aborted embryos,” Fertility and Sterility, vol. 70, no. 5, pp. 892–895, 1998.
View at: Publisher Site | Google Scholar
D. Nudell, M. Castillo, P. J. Turek, and R. R. Pera, “Increased frequency of mutations in DNA from infertile men with meiotic arrest,” Human Reproduction, vol. 15, no. 6, pp. 1289–1294, 2000.
View at: Google Scholar
D. Sakkas, G. Manicardi, D. Bizzaro, and P. G. Bianchi, “Possible consequences of performing intracytoplasmic sperm injection (ICSI) with sperm possessing nuclear DNA damage,” Human Fertility, vol. 3, no. 1, pp. 26–30, 2000.
View at: Google Scholar
B. Baccetti, G. Collodel, and P. Piomboni, “Apoptosis in human ejaculated sperm cells (notulae seminologicae 9),” Journal of Submicroscopic Cytology and Pathology, vol. 28, no. 4, pp. 587–596, 1996.
View at: Google Scholar
S. Lopes, J. G. Sun, A. Jurisicova, J. Meriano, and R. F. Casper, “Sperm deoxyribonucleic acid fragmentation is increased in poor-quality semen samples and correlates with failed fertilization in intracytoplasmic sperm injection,” Fertility and Sterility, vol. 69, no. 3, pp. 528–532, 1998.
View at: Google Scholar
A. Agarwal and T. M. Said, “Role of sperm chromatin abnormalities and DNA damage in male infertility,” Human Reproduction Update, vol. 9, no. 4, pp. 331–345, 2003.
View at: Publisher Site | Google Scholar
N. K. Duru, M. Morshedi, A. Schuffner, and S. Oehninger, “Cryopreservation-thawing of fractionated human spermatozoa and plasma membrane translocation of phosphatidylserine,” Fertility and Sterility, vol. 75, no. 2, pp. 263–268, 2001.
View at: Publisher Site | Google Scholar
N. K. Duru, M. S. Morshedi, A. Schuffner, and S. Oehninger, “Cryopreservation-thawing of fractionated human spermatozoa is associated with membrane phosphatidylserine externalization and not DNA fragmentation,” Journal of Andrology, vol. 22, no. 4, pp. 646–651, 2001.
View at: Google Scholar
M. Muratori, M. Maggi, S. Spinelli, E. Filimberti, G. Forti, and E. Baldi, “Spontaneous DNA fragmentation in swim-up selected human spermatozoa during long term incubation,” Journal of Andrology, vol. 24, no. 2, pp. 253–262, 2003.
View at: Google Scholar
L. N. Eid, S. F. Lorton, and J. J. Parrish, “Paternal influence on S-phase in the first cell cycle of the bovine embryo,” Biology of Reproduction, vol. 51, no. 6, pp. 1232–1237, 1994.
View at: Publisher Site | Google Scholar

Copyright

Copyright © 2010 Antonio Chaveiro et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation

Download other formats

Order printed copies

Views

240

Downloads

0

Citations