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RESEARCH ARTICLE

Oocyte quality determines bovine embryo development after fertilisation with hydrogen peroxide-stressed spermatozoa

Mohammad Bozlur Rahman A D , Leen Vandaele A , Tom Rijsselaere A , Mahdi Zhandi B , Dominiek Maes A , Mohammed Shamsuddin C and Ann Van Soom A
+ Author Affiliations
- Author Affiliations

A Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium.

B Department of Animal Science, University of Tehran, Karaj, Iran.

C Department of Surgery and Obstetrics, Bangladesh Agricultural University, Mymensingh, Bangladesh.

D Corresponding author. Email: mohammadbozlur.rahman@ugent.be

Reproduction, Fertility and Development 24(4) 608-618 https://doi.org/10.1071/RD11237
Submitted: 18 September 2011  Accepted: 12 October 2011   Published: 25 November 2011

Abstract

Exposure of gametes to specific stressors at sublethal levels can enhance the gametes’ subsequent performance in processes such as cryopreservation. In the present study, bull spermatozoa were subjected to H2O2 for 4 h at 100-, 200- and 500-μM levels; computer-assisted sperm analysis (CASA) and terminal deoxynucleotidyl transferase-mediated dUTP nick-end labelling (TUNEL) assay were used for evaluation of subsequent sperm motility and DNA integrity, respectively. Exposure of spermatozoa to H2O2 did not affect sperm motility but DNA integrity was negatively affected by 500 μM H2O2 compared with mock-exposed spermatozoa, whereas both motility and DNA integrity were affected compared with untreated spermatozoa. Nevertheless, insemination of oocytes with spermatozoa exposed to 200 μM H2O2 increased fertilisation, cleavage and blastocyst rates (P < 0.05). Furthermore, the higher blastocyst yield after fertilisation of oocytes with spermatozoa exposed to 200 μM H2O2 was related to oocyte diameter, with large–medium oocytes yielding higher blastocyst rates, while small-diameter oocytes consistently failed to develop into blastocysts. In conclusion, the results indicate that exposure of spermatozoa to 200 μM H2O2 before sperm–oocyte interaction may enhance in vitro embryo production in cattle. However, this increased embryo production is largely dependent on the intrinsic quality of the oocytes.

Additional keywords: DNA damage, oxidative stress, total cell number.


References

Aitken, R. J., and Clarkson, J. S. (1987). Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J. Reprod. Fertil. 81, 459–469.
Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXltlyjsw%3D%3D&md5=29b9a6ba3cc6ba15caac4ccdb2afb2f0CAS | 2828610PubMed |

Aitken, R. J., and De Iuliis, G. N. (2007). Origins and consequences of DNA damage in male germ cells. Reprod. Biomed. Online 14, 72–733.

Aitken, R. J., and Fisher, H. (1994). Reactive oxygen species generation and human spermatozoa – the balance of benefit and risk. Bioessays 16, 259–267.
Reactive oxygen species generation and human spermatozoa – the balance of benefit and risk.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXksl2jtrs%3D&md5=138b41c15afff9409dc224ceb838d9c1CAS |

Aitken, R. J., and West, K. M. (1990). Analysis of the relationship between reactive oxygen species production and leukocyte infiltration in fractions of human semen separated on Percoll gradients. Int. J. Androl. 13, 433–451.
Analysis of the relationship between reactive oxygen species production and leukocyte infiltration in fractions of human semen separated on Percoll gradients.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M3lsl2qug%3D%3D&md5=92d845b9623a63795e0f9028ca7cc6d3CAS | 1965724PubMed |

Aitken, R. J., Paterson, M., Fisher, H., Buckingham, D. W., and Vanduin, M. (1995). Redox regulation of tyrosine phosphorylation in human spermatozoa and its role in the control of human sperm function. J. Cell Sci. 108, 2017–2025.
| 1:CAS:528:DyaK2MXls1Olt7Y%3D&md5=a697c8919441e5088a297004a0d84ed3CAS | 7544800PubMed |

Aitken, R. J., Gordon, E., Harkiss, D., Twigg, J. P., Milne, P., Jennings, Z., and Irvine, D. S. (1998). Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. Biol. Reprod. 59, 1037–1046.
Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmvFyqu74%3D&md5=4da4a7579bbafd4e35069dcc3d440824CAS | 9780307PubMed |

Aitken, R. J., De Iuliis, G. N., and McLachlan, R. I. (2009). Biological and clinical significance of DNA damage in the male germ line. Int. J. Androl. 32, 46–56.
Biological and clinical significance of DNA damage in the male germ line.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivVWgsLo%3D&md5=1a4bfeee01e604e31b2686624693ab9cCAS | 19076252PubMed |

Alvarez, J. G., Touchstone, J. C., Blasco, L., and Storey, B. T. (1987). Spontaneous lipid peroxidation and production of hydrogen peroxide and superoxide in human spermatozoa – superoxide dismutase as major enzyme protectant against oxygen toxicity. J. Androl. 8, 338–348.
| 1:CAS:528:DyaL2sXmtFGhtb4%3D&md5=ae2920c31a2c7517a8474ee27e65860aCAS | 2822642PubMed |

Balhorn, R., Corzett, M., and Mazrimas, J. A. (1992). Formation of intraprotamine disulfides in vitro. Arch. Biochem. Biophys. 296, 384–393.
Formation of intraprotamine disulfides in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XkvVGmsrg%3D&md5=aa64ba1acba64cfa4f8c7652f4a077f0CAS | 1632631PubMed |

Barnes, F. L., and First, N. L. (1991). Embryonic transcription in in vitro-cultured bovine embryos. Mol. Reprod. Dev. 29, 117–123.
Embryonic transcription in in vitro-cultured bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXltFWhurs%3D&md5=29d900083815c828e0709f2722fd919cCAS | 1878221PubMed |

Bilodeau, J. F., Blanchette, S., Gagnon, C., and Sirard, M. A. (2001). Thiols prevent H2O2-mediated loss of sperm motility in cryopreserved bull semen. Theriogenology 56, 275–286.
| 1:CAS:528:DC%2BD3MXlvVyntb4%3D&md5=494b51bb397fe8a8a472f99f4a276036CAS | 11480619PubMed |

Brevini, T. A. L., Lonergan, P., Cillo, F., Francisci, C., Favetta, L. A., Fair, T., and Gandolfi, F. (2002). Evolution of mRNA polyadenylation between oocyte maturation and first embryonic cleavage in cattle and its relation with developmental competence. Mol. Reprod. Dev. 63, 510–517.
Evolution of mRNA polyadenylation between oocyte maturation and first embryonic cleavage in cattle and its relation with developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotlCgt74%3D&md5=a452366c8972fbc6b0fe351a94fabe5dCAS |

Brouwers, J. F. H. M., and Gadella, B. M. (2003). In situ detection and localization of lipid peroxidation in individual bovine sperm cells. Free Radic. Biol. Med. 35, 1382–1391.
In situ detection and localization of lipid peroxidation in individual bovine sperm cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpt1equrg%3D&md5=72790cc41ef1de8f8349852e4eb5480aCAS |

Brouwers, J. F. H. M., Gadella, B. M., van Golde, L. M. G., and Tielens, A. G. M. (1998). Quantitative analysis of phosphatidylcholine molecular species using HPLC and light-scattering detection. J. Lipid Res. 39, 344–353.
| 1:CAS:528:DyaK1cXht1aitLg%3D&md5=fe6aaf4388078c4c32a705a0d675736fCAS |

Caixeta, E. S., Ripamonte, P., Franco, M. M., Junior, J. B., and Dode, M. A. (2009). Effect of follicle size on mRNA expression in cumulus cells and oocytes of Bos indicus: an approach to identify marker genes for developmental competence. Reprod. Fertil. Dev. 21, 655–664.
Effect of follicle size on mRNA expression in cumulus cells and oocytes of Bos indicus: an approach to identify marker genes for developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmsVCrtbc%3D&md5=4843eb6acd9d2e22b9537683242ab0b3CAS | 19486602PubMed |

Chatterjee, S., and Gagnon, C. (2001). Production of reactive oxygen species by spermatozoa undergoing cooling, freezing and thawing. Mol. Reprod. Dev. 59, 451–458.
Production of reactive oxygen species by spermatozoa undergoing cooling, freezing and thawing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXltVWmsb4%3D&md5=e0f1ca170302d7aeb1995f4cc326d88eCAS | 11468782PubMed |

Christmann, M., Tomicic, M. T., Roos, W. P., and Kaina, B. (2003). Mechanisms of human DNA repair: an update. Toxicology 193, 3–34.
| 1:CAS:528:DC%2BD3sXos1KhsLo%3D&md5=6fcce6a6264bf40f0708ef41af7ff851CAS | 14599765PubMed |

de Lamirande, E., and Gagnon, C. (1993). A positive role for the superoxide anion in triggering hyperactivation and capacitation of human spermatozoa. Int. J. Androl. 16, 21–25.
A positive role for the superoxide anion in triggering hyperactivation and capacitation of human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXks1yrs7g%3D&md5=494c97c92bd649960ffb3deef12752a4CAS | 8385650PubMed |

de Lamirande, E., and Gagnon, C. (1995). Impact of reactive oxygen species on spermatozoa – a balancing act between beneficial and detrimental effects. Hum. Reprod. 10, 15–21.
| 8592032PubMed |

Donnison, M., and Pfeffer, P. L. (2004). Isolation of genes associated with developmentally competent bovine oocytes and quantitation of their levels during development. Biol. Reprod. 71, 1813–1821.
Isolation of genes associated with developmentally competent bovine oocytes and quantitation of their levels during development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWgsr%2FL&md5=33790237928b3de3427b513302a936d5CAS | 15286031PubMed |

Du, Y., Pribenszky, C., Molnar, M., Zhang, X., Yang, H., Kuwayama, M., Pedersen, A. M., Villemoes, K., Bolund, L., and Vajta, G. (2008). High hydrostatic pressure: a new way to improve in vitro developmental competence of porcine matured oocytes after vitrification. Reproduction 135, 13–17.
High hydrostatic pressure: a new way to improve in vitro developmental competence of porcine matured oocytes after vitrification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhs1CksL8%3D&md5=40791d16b93fdb5869c2b24e049634e6CAS | 18159079PubMed |

du Plessis, S. S., McAllister, D. A., Luu, A., Savia, J., Agarwal, A., and Lampiao, F. (2010). Effects of H2O2 exposure on human sperm motility parameters, reactive oxygen species levels and nitric oxide levels. Andrologia 42, 206–210.
Effects of H2O2 exposure on human sperm motility parameters, reactive oxygen species levels and nitric oxide levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXosF2ls78%3D&md5=baf97e3339ee8eb1afc7a97917f99cc5CAS | 20500750PubMed |

Duru, N. K., Morshedi, M., and Oehninger, S. (2000). Effects of hydrogen peroxide on DNA and plasma membrane integrity of human spermatozoa. Fertil. Steril. 74, 1200–1207.
Effects of hydrogen peroxide on DNA and plasma membrane integrity of human spermatozoa.Crossref | GoogleScholarGoogle Scholar |

Fair, T. (2003). Follicular oocyte growth and acquisition of developmental competence. Anim. Reprod. Sci. 78, 203–216.
Follicular oocyte growth and acquisition of developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksF2gtrw%3D&md5=98cb999fb96fb0b9171bd2680434923bCAS | 12818645PubMed |

Fatehi, A. N., Bevers, M. M., Schoevers, E., Roelen, B. A. J., Colenbrander, B., and Gadella, B. M. (2006). DNA damage in bovine sperm does not block fertilization and early embryonic development but induces apoptosis after the first cleavages. J. Androl. 27, 176–188.
DNA damage in bovine sperm does not block fertilization and early embryonic development but induces apoptosis after the first cleavages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xit12jtb0%3D&md5=d7a77e86ad84f497be01f8f86650051cCAS | 16304212PubMed |

Grunewald, S., Paasch, U., Glander, H. J., and Anderegg, U. (2005). Mature human spermatozoa do not transcribe novel RNA. Andrologia 37, 69–71.
Mature human spermatozoa do not transcribe novel RNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpslGitLo%3D&md5=44caf9eff172fc2842c057e9722a1a65CAS | 16026427PubMed |

Hendricks, K. E. M., and Hansen, P. J. (2009). Can programmed cell death be induced in post-ejaculatory bull and stallion spermatozoa? Theriogenology 71, 1138–1146.
Can programmed cell death be induced in post-ejaculatory bull and stallion spermatozoa?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsV2qs78%3D&md5=8f8db1abb1625e71591b80da13ce43f3CAS |

Hendricks, K. E. M., and Hansen, P. J. (2010). Consequences for the bovine embryo of being derived from a spermatozoon subjected to oxidative stress. Aust. Vet. J. 88, 307–310.
Consequences for the bovine embryo of being derived from a spermatozoon subjected to oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnns1WntA%3D%3D&md5=96587db5aecbd25dc81ea3f206df9786CAS |

Henkel, R., Ichikawa, T., Sanchez, R., Miska, W., Ohmori, H., and Schill, W. B. (1997). Differentiation of ejaculates showing reactive oxygen species production by spermatozoa or leukocytes. Andrologia 29, 295–301.
Differentiation of ejaculates showing reactive oxygen species production by spermatozoa or leukocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c%2FptVaquw%3D%3D&md5=2cb3c8fde0aa68cb50f0a039fc62e25cCAS | 9430434PubMed |

Hoflack, G., Opsomer, G., Rijsselaere, T., Van Soom, A., Maes, D., de Kruif, A., and Duchateau, L. (2007). Comparison of computer-assisted sperm motility analysis parameters in semen from Belgian Blue and Holstein–Friesian bulls. Reprod. Domest. Anim. 42, 153–161.
Comparison of computer-assisted sperm motility analysis parameters in semen from Belgian Blue and Holstein–Friesian bulls.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2s7kvF2rug%3D%3D&md5=fe91b8f37f7faf45a88044db7fed1aa9CAS | 17348972PubMed |

Holland, M. K., Alvarez, J. G., and Storey, B. T. (1982). Production of superoxide and activity of superoxide-dismutase in rabbit epididymal spermatozoa. Biol. Reprod. 27, 1109–1118.
Production of superoxide and activity of superoxide-dismutase in rabbit epididymal spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXjtF2qug%3D%3D&md5=3d439eb39dd9218c684802a4ca6f236aCAS | 6297628PubMed |

Huang, S. Y., Pribenszky, C., Kuo, Y. H., Teng, S. H., Chen, Y. H., Chung, M. T., and Chiu, Y. F. (2009). Hydrostatic pressure pre-treatment affects the protein profile of boar sperm before and after freezing–thawing. Anim. Reprod. Sci. 112, 136–149.
Hydrostatic pressure pre-treatment affects the protein profile of boar sperm before and after freezing–thawing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivVWktLY%3D&md5=2a49c99e47c4c0f934903021e7bfd878CAS | 18538515PubMed |

Jimenez-Macedo, A. R., Paramio, M. T., Anguita, B., Morato, R., Romaguera, R., Mogas, T., and Izquierdo, D. (2007). Effect of ICSI and embryo biopsy on embryo development and apoptosis according to oocyte diameter in prepubertal goats. Theriogenology 67, 1399–1408.
Effect of ICSI and embryo biopsy on embryo development and apoptosis according to oocyte diameter in prepubertal goats.Crossref | GoogleScholarGoogle Scholar | 17400287PubMed |

Krisher, R. L. (2004). The effect of oocyte quality on development. J. Anim. Sci. 82, E14–E23.
| 15471793PubMed |

Leyens, G., Verhaeghe, B., Landtmeters, M., Marchandise, J., Knoops, B., and Donnay, I. (2004). Peroxiredoxin 6 is upregulated in bovine oocytes and cumulus cells during in vitro maturation: role of intercellular communication. Biol. Reprod. 71, 1646–1651.
Peroxiredoxin 6 is upregulated in bovine oocytes and cumulus cells during in vitro maturation: role of intercellular communication.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpt1yitr8%3D&md5=425d9cd5e3861ed32ce09e4a62f615ddCAS | 15240427PubMed |

Li, Z. X., Yang, J., and Huang, H. F. (2006). Oxidative stress induces H2AX phosphorylation in human spermatozoa. FEBS Lett. 580, 6161–6168.
Oxidative stress induces H2AX phosphorylation in human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFOhsrzM&md5=0715dff9a6f52a3f7fcbee9dec5f9103CAS |

Lin, L., Kragh, P. M., Purup, S., Kuwayama, M., Du, Y. T., Zhang, X. Q., Yang, H. M., Bolund, L., Callesen, H., and Vajta, G. (2009). Osmotic stress induced by sodium chloride, sucrose or trehalose improves cryotolerance and developmental competence of porcine oocytes. Reprod. Fertil. Dev. 21, 338–344.
Osmotic stress induced by sodium chloride, sucrose or trehalose improves cryotolerance and developmental competence of porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVensb8%3D&md5=9a0b9c08dbc368544469eef9ce6d2794CAS | 19210925PubMed |

Lopes, S., Jurisicova, A., Sun, J. G., and Casper, R. F. (1998). Reactive oxygen species: potential cause for DNA fragmentation in human spermatozoa. Hum. Reprod. 13, 896–900.
Reactive oxygen species: potential cause for DNA fragmentation in human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjs12gtbo%3D&md5=156b622124f84cbcb7c7753db4bba221CAS | 9619544PubMed |

Manandhar, G., MirandaVizuete,, A., Pedrajas, J. R., Krause, W. J., Zimmerman, S., Sutovsky, M., and Sutovsky, P. (2009). Peroxiredoxin 2 and peroxidase enzymatic activity of mammalian spermatozoa. Biol. Reprod. 80, 1168–1177.
Peroxiredoxin 2 and peroxidase enzymatic activity of mammalian spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlGms7c%3D&md5=8ce2c08eb32120c1d35bafbd9d91bee7CAS | 19208552PubMed |

Matsuda, Y., and Tobari, I. (1989). Repair capacity of fertilized mouse eggs for X-ray damage induced in sperm and mature oocytes. Mutat. Res 210, 35–47.
| 1:CAS:528:DyaL1MXptFemtQ%3D%3D&md5=b36d233be494780644930a422a131413CAS | 2909869PubMed |

Meirelles, F. V., Caetano, A. R., Watanabe, Y. F., Ripamonte, P., Carambula, S. F., Merighe, G. K., and Garcia, S. M. (2004). Genome activation and developmental block in bovine embryos. Anim. Reprod. Sci. 82–83, 13–20.
Genome activation and developmental block in bovine embryos.Crossref | GoogleScholarGoogle Scholar | 15271440PubMed |

Memili, E., and First, N. L. (2000). Zygotic and embryonic gene expression in cow: a review of timing and mechanisms of early gene expression as compared with other species. Zygote 8, 87–96.
Zygotic and embryonic gene expression in cow: a review of timing and mechanisms of early gene expression as compared with other species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjvVemtLo%3D&md5=485e4839513c595a5016a2a4f6247550CAS | 10840878PubMed |

Mitchell, L. A., De Iuliis, G. N., and Aitken, R. J. (2011). The TUNEL assay consistently underestimates DNA damage in human spermatozoa and is influenced by DNA compaction and cell vitality: development of an improved methodology. Int. J. Androl. 34, 2–13.
The TUNEL assay consistently underestimates DNA damage in human spermatozoa and is influenced by DNA compaction and cell vitality: development of an improved methodology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXitlehur4%3D&md5=183c492c8c09eb1e4db54b7aad8a67a1CAS | 20158539PubMed |

O’Flaherty, C., and de Souza, A. R. (2011). Hydrogen peroxide modifies human sperm peroxiredoxins in a dose-dependent manner. Biol. Reprod. 84, 238–247.
Hydrogen peroxide modifies human sperm peroxiredoxins in a dose-dependent manner.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVelsbk%3D&md5=0d31659e8244e29234f708cf83201c31CAS | 20864641PubMed |

Oehninger, S., Blackmore, P., Mahony, M., and Hodgen, G. (1995). Effects of hydrogen peroxide on human spermatozoa. J. Assist. Reprod. Genet. 12, 41–47.
Effects of hydrogen peroxide on human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK28%2FnvVWrug%3D%3D&md5=5f12bac2a52ce9b9fca834c02636700dCAS | 7580009PubMed |

Pribenszky, C., and Vajta, G. (2010). Cells under pressure: how sublethal hydrostatic pressure stress treatment increases gametes’ and embryos’ performance? Reprod. Fertil. Dev. 23, 48–55.

Pribenszky, C., Molnar, M., Horvath, A., Harnos, A., and Szenci, O. (2006). Hydrostatic pressure induced increase in post-thaw motility of frozen boar spermatozoa. Reprod. Fertil. Dev. 18, 162–163.
Hydrostatic pressure induced increase in post-thaw motility of frozen boar spermatozoa.Crossref | GoogleScholarGoogle Scholar |

Pribenszky, C., Molnar, M., Horvath, A., Kutvolgyi, G., Harnos, A., Szenci, O., Dengg, J., and Lederer, J. (2007). Improved post-thaw motility, viability and fertility are achieved by hydrostatic pressure-treated bull semen. Reprod. Fertil. Dev. 19, 181–182.
Improved post-thaw motility, viability and fertility are achieved by hydrostatic pressure-treated bull semen.Crossref | GoogleScholarGoogle Scholar |

Pribenszky, C., Du, Y., Molnar, A., Harnos, A., and Vajta, G. (2008). Increased stress tolerance of matured pig oocytes after high hydrostatic pressure treatment. Anim. Reprod. Sci. 106, 200–207.
Increased stress tolerance of matured pig oocytes after high hydrostatic pressure treatment.Crossref | GoogleScholarGoogle Scholar | 18329829PubMed |

Pribenszky, C., Vajta, G., Molnar, M., Du, Y., Lin, L., Bolund, L., and Yovich, J. (2010). Stress for stress tolerance? A fundamentally new approach in mammalian embryology. Biol. Reprod. 83, 690–697.
Stress for stress tolerance? A fundamentally new approach in mammalian embryology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlGlsrfL&md5=39b1b328b40c31a18cdbe5133f697bc1CAS | 20554920PubMed |

Raha, S., and Robinson, B. H. (2001). Mitochondria, oxygen free radicals and apoptosis. Am. J. Med. Genet. 106, 62–70.
Mitochondria, oxygen free radicals and apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MrjtVylug%3D%3D&md5=f83948922bf5bcc4de4b7e985745b5c5CAS | 11579426PubMed |

Rhee, S. G. (2006). Cell signalling. H2O2, a necessary evil for cell signalling. Science 312, 1882–1883.
Cell signalling. H2O2, a necessary evil for cell signalling.Crossref | GoogleScholarGoogle Scholar | 16809515PubMed |

Sancar, A., Lindsey-Boltz, L. A., Unsal-Kacmaz, K., and Linn, S. (2004). Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73, 39–85.
Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmslagsrk%3D&md5=d8125018cc1220b6d1642f494d221d72CAS | 15189136PubMed |

Sawyer, D. E., Mercer, B. G., Wiklendt, A. M., and Aitken, R. J. (2003). Quantitative analysis of gene-specific DNA damage in human spermatozoa. Mutat. Res. 529, 21–34.
Quantitative analysis of gene-specific DNA damage in human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXms12jtr4%3D&md5=961e4f122d2c99c997933bc8361af137CAS | 12943917PubMed |

Schiller, J., Muller, K., Suss, R., Arnhold, J., Gey, C., Herrmann, A., Lessig, J., Arnold, K., and Muller, P. (2003). Analysis of the lipid composition of bull spermatozoa by MALDI-TOF mass spectrometry – a cautionary note. Chem. Phys. Lipids 126, 85–94.
| 1:CAS:528:DC%2BD3sXot1OltLk%3D&md5=e9b46cce36dd5c38353809d29c6d3f8aCAS | 14580713PubMed |

Silva, P. F., Gadella, B. M., Colenbrander, B., and Roelen, B. A. (2007). Exposure of bovine sperm to pro-oxidants impairs the developmental competence of the embryo after the first cleavage. Theriogenology 67, 609–619.
Exposure of bovine sperm to pro-oxidants impairs the developmental competence of the embryo after the first cleavage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitlyqug%3D%3D&md5=537059c903481dc471acb5252451f7d3CAS | 17056104PubMed |

Simon, L., and Lewis, S. E. M. (2011). Sperm DNA damage or progressive motility: which one is the better predictor of fertilization in vitro? Syst. Biol. Reprod. Med , .
Sperm DNA damage or progressive motility: which one is the better predictor of fertilization in vitro?Crossref | GoogleScholarGoogle Scholar | 21299480PubMed |

Slupphaug, G., Kavli, B., and Krokan, H. E. (2003). The interacting pathways for prevention and repair of oxidative DNA damage. Mutat. Res. 531, 231–251.
The interacting pathways for prevention and repair of oxidative DNA damage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpt1ertLw%3D&md5=ae46f64005188e1363c420ca553df3caCAS | 14637258PubMed |

Storey, B. T. (1997). Biochemistry of the induction and prevention of lipoperoxidative damage in human spermatozoa. Mol. Hum. Reprod. 3, 203–213.
Biochemistry of the induction and prevention of lipoperoxidative damage in human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjt1arsrs%3D&md5=21d9aa13f4acd09c330d4ee3da231408CAS | 9237246PubMed |

Telford, N. A., Watson, A. J., and Schultz, G. A. (1990). Transition from maternal to embryonic control in early mammalian development – a comparison of several species. Mol. Reprod. Dev. 26, 90–100.
Transition from maternal to embryonic control in early mammalian development – a comparison of several species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c3mslOhtQ%3D%3D&md5=9fba85bb0339b45b5570cc49f8f79f96CAS | 2189447PubMed |

Thys, M., Vandaele, L., Morrell, J. M., Mestach, J., Van Soom, A., Hoogewijs, M., and Rodriguez-Martinez, H. (2009). In vitro-fertilizing capacity of frozen–thawed bull spermatozoa selected by single-layer (glycidoxypropyltrimethoxysilane) silane-coated silica colloidal centrifugation. Reprod. Domest. Anim. 44, 390–394.
In vitro-fertilizing capacity of frozen–thawed bull spermatozoa selected by single-layer (glycidoxypropyltrimethoxysilane) silane-coated silica colloidal centrifugation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MrisFWhtA%3D%3D&md5=5c22e204af1410185faac8ac630fcd27CAS | 18992094PubMed |

Van Soom, A., Vandaele, L., Goossens, K., de Kruif, A., and Peelman, L. (2007). Gamete origin in relation to early embryo development. Theriogenology 68, S131–S137.
Gamete origin in relation to early embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotlaitLk%3D&md5=93ca77b83ae7bab0f8cba45ac7289cacCAS | 17467789PubMed |

Vandaele, L., Mateusen, B., Maes, D., de Kruif, A., and Van Soom, A. (2006). Is apoptosis in bovine in vitro-produced embryos related to early developmental kinetics and in vivo bull fertility? Theriogenology 65, 1691–1703.
Is apoptosis in bovine in vitro-produced embryos related to early developmental kinetics and in vivo bull fertility?Crossref | GoogleScholarGoogle Scholar | 16280159PubMed |

Vandaele, L., Mateusen, B., Maes, D. G. D., de Kruif, A., and Van Soom, A. (2007). Temporal detection of caspase-3 and -7 in bovine in vitro-produced embryos of different developmental capacity. Reproduction 133, 709–718.
Temporal detection of caspase-3 and -7 in bovine in vitro-produced embryos of different developmental capacity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFeku70%3D&md5=b76f9da3ace40cd03401e8107c2c7eb5CAS | 17504915PubMed |

Vandaele, L., Thys, M., Bijttebier, J., Van Langendonckt, A., Donnay, I., Maes, D., Meyer, E., and Van Soom, A. (2010). Short-term exposure to hydrogen peroxide during oocyte maturation improves bovine embryo development. Reproduction 139, 505–511.
Short-term exposure to hydrogen peroxide during oocyte maturation improves bovine embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtV2lsb8%3D&md5=97eb0414b47c697e32dee6ecf0194742CAS | 19939885PubMed |

Vilfan, I. D., Conwell, C. C., and Hud, N. V. (2004). Formation of native-like mammalian sperm cell chromatin with folded bull protamine. J. Biol. Chem. 279, 20 088–20 095.
Formation of native-like mammalian sperm cell chromatin with folded bull protamine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjs1Whsbc%3D&md5=8d6becddb6f7c33bd7c6d36d9eff8f50CAS |

Vishwanath, R. (2003). Artificial insemination: the state of the art. Theriogenology 59, 571–584.
| 1:STN:280:DC%2BD38jjslKrsw%3D%3D&md5=b32806771983a4f7975b79108c5694b0CAS | 12499005PubMed |

Wathes, D. C., Abayasekara, D. R. E., and Aitken, R. J. (2007). Polyunsaturated fatty acids in male and female reproduction. Biol. Reprod. 77, 190–201.
Polyunsaturated fatty acids in male and female reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1OnsL0%3D&md5=f9f27869c67f75e6ac523b7c248cc21dCAS | 17442851PubMed |

Watson, P. F. (2000). The causes of reduced fertility with cryopreserved semen. Anim. Reprod. Sci. 60, 481–492.
The causes of reduced fertility with cryopreserved semen.Crossref | GoogleScholarGoogle Scholar | 10844218PubMed |