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

Effect of seminal plasma from high- and low-fertility bulls on cauda epididymal sperm function

S. A. Holden A , B. Fernandez-Fuertes B , E. M. Murphy A , P. Lonergan B and S. Fair A C
+ Author Affiliations
- Author Affiliations

A Laboratory of Animal Reproduction, Department of Biological Sciences, School of Natural Sciences, Faculty of Science and Engineering, University of Limerick, Castletroy, Limerick, V94 T9PX, Ireland.

B School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Dublin, D04 N2E5, Ireland.

C Corresponding author. Email: sean.fair@ul.ie

Reproduction, Fertility and Development - https://doi.org/10.1071/RD17136
Submitted: 6 February 2017  Accepted: 9 May 2017   Published online: 2 June 2017

Abstract

The aim of this study was to characterise the effect of seminal plasma (SP) from bulls of high or low fertility on sperm function. First, the effect of SP on the motility of fresh cauda epididymal spermatozoa (CES) and frozen–thawed ejaculated spermatozoa was assessed (Experiment 1a). Seminal plasma was then collected from bulls of known high and low fertility. Pooled CES were incubated in the SP from each bull, diluted and assessed for motility and viability on Days 1, 2, 3 and 5 after packaging as fresh semen (Experiment 1b). Also assessed were motility, kinematics, viability and mitochondrial membrane potential after thawing (Experiment 1c) as well as hypotonic resistance (Experiment 2) and fertilisation potential using in vitro fertilisation (Experiment 3). Seminal plasma increased the motility of CES (P < 0.05); however, there was no effect of SP on the motility and viability of fresh CES or on CES post-thaw motility, viability and mitochondrial membrane potential (P > 0.05). The hypotonic resistance of CES was reduced by SP (P < 0.05), irrespective of whether the SP was from high- or low-fertility bulls. Seminal plasma from high- or low-fertility bulls had no effect on cleavage or blastocyst rates (P > 0.05). In conclusion, SP affects the physiological function of CES but there is no difference between SP from high- or low-fertility bulls.

Additional keywords: bovine, fresh, frozen-thawed, hypotonic resistance.


References

Al Naib, A., Hanrahan, J. P., Lonergan, P., and Fair, S. (2011a). In vitro assessment of sperm from bulls of high and low field fertility. Theriogenology 76, 161–167.
In vitro assessment of sperm from bulls of high and low field fertility.CrossRef | 1:STN:280:DC%2BC3Mrntlyjsg%3D%3D&md5=456f835761b781f4660a28f637775a93CAS |

Al Naib, A., Ward, F., Kelly, A. K., Wade, M., Marti, J. I., and Lonergan, P. (2011b). Effect of duration of storage at ambient temperature on fertilizing ability and mucus penetration ability of fresh bovine sperm. Theriogenology 76, 1070–1075.
Effect of duration of storage at ambient temperature on fertilizing ability and mucus penetration ability of fresh bovine sperm.CrossRef | 1:STN:280:DC%2BC3MfgvFanug%3D%3D&md5=99c68afcab566e67fdd7f3a036f393f2CAS |

Aurich, J. E., Schönherr, U., Hoppe, H., and Aurich, C. (1997). Effects of antioxidants on motility and membrane integrity of chilled–stored stallion semen. Theriogenology 48, 185–192.
Effects of antioxidants on motility and membrane integrity of chilled–stored stallion semen.CrossRef | 1:STN:280:DC%2BD28zgtVyluw%3D%3D&md5=4df0b03ae15e625ec71d9916dfd0bcd7CAS |

Baas, J. W., Molan, P., and Shannon, P. (1983). Factors in seminal plasma of bulls that affect the viability and motility of spermatozoa. J. Reprod. Fertil. 68, 275–280.
Factors in seminal plasma of bulls that affect the viability and motility of spermatozoa.CrossRef | 1:CAS:528:DyaL3sXksFWisLo%3D&md5=8ead7de249abba35bba98bcb6532ca2bCAS |

Barrios, B., Pérez-Pé, R., Gallego, M., Tato, A., Osada, J., Muiño-Blanco, T., and Cebrián-Pérez, J. A. (2000). Seminal plasma proteins revert the cold-shock damage on ram sperm membrane 1. Biol. Reprod. 63, 1531–1537.
Seminal plasma proteins revert the cold-shock damage on ram sperm membrane 1.CrossRef | 1:CAS:528:DC%2BD3cXnslCrtrs%3D&md5=7e211f1b4b49d6671cf0cb1de7847e2aCAS |

Bedford, J. M. (2015). The functions – or not – of seminal plasma? Biol. Reprod. 92, 18.
The functions – or not – of seminal plasma?CrossRef |

Berry, D. P., Evans, R. D., and Mc Parland, S. (2011). Evaluation of bull fertility in dairy and beef cattle using cow field data. Theriogenology 75, 172–181.
Evaluation of bull fertility in dairy and beef cattle using cow field data.CrossRef | 1:STN:280:DC%2BC3M%2FitVWiuw%3D%3D&md5=cc163a4a52516daee0a563d2de55ace7CAS |

Bertol, M. A., Weiss, R. R., Kozicki, L. E., Abreu, A. C., Pereira, J. F., and da Silva, J. J. (2016). In vitro and in vivo fertilization potential of cryopreserved spermatozoa from bull epididymides stored for up to 30 hours at ambient temperature (18°C–20°C). Theriogenology 86, 1014–1021.
In vitro and in vivo fertilization potential of cryopreserved spermatozoa from bull epididymides stored for up to 30 hours at ambient temperature (18°C–20°C).CrossRef |

Breininger, E., Cetica, P., and Beconi, M. (2010). Capacitation inducers act through diverse intracellular mechanisms in cryopreserved bovine sperm. Theriogenology 74, 1036–1049.
Capacitation inducers act through diverse intracellular mechanisms in cryopreserved bovine sperm.CrossRef | 1:CAS:528:DC%2BC3cXhtFWqtLnE&md5=5666802ead73028cb6b1e63090a1b82cCAS |

Bromfield, J. J. (2016). A role for seminal plasma in modulating pregnancy outcomes in domestic species. Reproduction 152, R223–R232.
A role for seminal plasma in modulating pregnancy outcomes in domestic species.CrossRef |

Bromfield, J. J., Schjenken, J. E., Chin, P. Y., Care, A. S., Jasper, M. J., and Robertson, S. A. (2014). Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring. Proc. Natl. Acad. Sci. USA 111, 2200–2205.
Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring.CrossRef | 1:CAS:528:DC%2BC2cXisFOqtLc%3D&md5=8edd01884c98f5f67710f9a74e3b3ff8CAS |

Chaveiro, A., Cerqueira, C., Silva, J., Franco, J., and Moreira da Silva, F. (2015). Evaluation of frozen thawed cauda epididymal sperms and in vitro fertilizing potential of bovine sperm collected from the cauda epididymal. Iran J. Vet. Res. 16, 188–193.
| 1:STN:280:DC%2BC28bpt1Whtg%3D%3D&md5=9bc9f124874ce82a5b252e8ba0f2bdb1CAS |

de Graaf, S. P., Evans, G., Gillan, L., Guerra, M. M. P., Maxwell, W. M. C., and O’Brien, J. K. (2007). The influence of antioxidant, cholesterol and seminal plasma on the in vitro quality of sorted and non-sorted ram spermatozoa. Theriogenology 67, 217–227.
The influence of antioxidant, cholesterol and seminal plasma on the in vitro quality of sorted and non-sorted ram spermatozoa.CrossRef | 1:CAS:528:DC%2BD28Xhtlars73P&md5=bdf7f0588b86df831d229847893d14eaCAS |

de Graaf, S. P., Leahy, T., Marti, J., Evans, G., and Maxwell, W. M. (2008). Application of seminal plasma in sex-sorting and sperm cryopreservation. Theriogenology 70, 1360–1363.
Application of seminal plasma in sex-sorting and sperm cryopreservation.CrossRef | 1:CAS:528:DC%2BD1cXhtlKqsL%2FO&md5=604a82080f4d0bca9af873ea5ebe82c5CAS |

DeJarnette, J., and Amann, R. (2010). Understanding estimates of AI sire fertility: from A to Z. In ‘23rd Technical Conference on Artificial Insemination & Reproduction, Milwaukee, WI’. Available at http://www.selectsires.com/programs/docs/UnderstandingAISireFertility.pdf?version=20170404 [accessed 12 May 2017]

Druart, X., Gatti, J. L., Huet, S., Dacheux, J. L., and Humblot, P. (2009). Hypotonic resistance of boar spermatozoa: sperm subpopulations and relationship with epididymal maturation and fertility. Reproduction 137, 205–213.
Hypotonic resistance of boar spermatozoa: sperm subpopulations and relationship with epididymal maturation and fertility.CrossRef | 1:CAS:528:DC%2BD1MXovV2ks7k%3D&md5=f549b4a50725cf4a1bf297d9a3c2e3f7CAS |

Faulkner, L. C., Hopwood, M. L., and Wiltbank, J. N. (1968). Seminal vesiculectomy in bulls. II. Seminal characteristics and breeding trials. J. Reprod. Fertil. 16, 179–182.
Seminal vesiculectomy in bulls. II. Seminal characteristics and breeding trials.CrossRef | 1:STN:280:DyaF1czhvVyrtg%3D%3D&md5=c318498d9285b18c32ca8ece7b2fb020CAS |

Fernandez-Fuertes, B., Narciandi, F., O’Farrelly, C., Kelly, A. K., Fair, S., Meade, K. G., and Lonergan, P. (2016). Cauda epididymis-specific beta-defensin 126 promotes sperm motility but not fertilizing ability in cattle. Biol. Reprod. 95, 122.
Cauda epididymis-specific beta-defensin 126 promotes sperm motility but not fertilizing ability in cattle.CrossRef |

Garner, D. L., Thomas, C. A., Gravance, C. G., Marshall, C. E., DeJarnette, J. M., and Allen, C. H. (2001). Seminal plasma addition attenuates the dilution effect in bovine sperm. Theriogenology 56, 31–40.
Seminal plasma addition attenuates the dilution effect in bovine sperm.CrossRef | 1:STN:280:DC%2BD3MvhvFSjtw%3D%3D&md5=53d05fe4ee431ad43199eb69ba4449e9CAS |

Graham, J. K. (1994). Effect of seminal plasma on the motility of epididymal and ejaculated spermatozoa of the ram and bull during the cryopreservation process. Theriogenology 41, 1151–1162.
Effect of seminal plasma on the motility of epididymal and ejaculated spermatozoa of the ram and bull during the cryopreservation process.CrossRef | 1:STN:280:DC%2BD28zgtVahtw%3D%3D&md5=a0ca48e4aef486be44d393e37d3e22c5CAS |

Henault, M. A., and Killian, G. J. (1996). Effect of homologous and heterologous seminal plasma on the fertilizing ability of ejaculated bull spermatozoa assessed by penetration of zona-free bovine oocytes. J. Reprod. Fertil. 108, 199–204.
Effect of homologous and heterologous seminal plasma on the fertilizing ability of ejaculated bull spermatozoa assessed by penetration of zona-free bovine oocytes.CrossRef | 1:CAS:528:DyaK2sXntVSnsw%3D%3D&md5=a084c8a8293474b95125bf5dd41abe25CAS |

Henault, M. A., Killian, G. J., Kavanaugh, J. F., and Griel, L. C. (1995). Effect of accessory sex gland fluid from bulls of differing fertilities on the ability of cauda epididymal sperm to penetrate zona-free bovine oocytes. Biol. Reprod. 52, 390–397.
Effect of accessory sex gland fluid from bulls of differing fertilities on the ability of cauda epididymal sperm to penetrate zona-free bovine oocytes.CrossRef | 1:CAS:528:DyaK2MXjt12ksrg%3D&md5=eb1543cb0840cfe0232087021b35ef3bCAS |

Hewitt, D. A., Leahy, R., Sheldon, I. M., and England, G. C. W. (2001). Cryopreservation of epididymal dog sperm. Anim. Reprod. Sci. 67, 101–111.
Cryopreservation of epididymal dog sperm.CrossRef | 1:STN:280:DC%2BD3MzksFSjtA%3D%3D&md5=6e05cfff41e3d257e4c7d4a454a7ae90CAS |

Holden, S. A., Murphy, C., Moreno, J. F., Butler, S., Cromie, A., Lonergan, P., and Fair, S. (2016). In vitro characterisation of fresh and frozen sex-sorted bull sperm. Reprod. Fertil. Dev. , .
In vitro characterisation of fresh and frozen sex-sorted bull sperm.CrossRef |

Holden, S. A., Fernandez-Fuertes, B., Murphy, C., Whelan, H., O’Gorman, A., Brennan, L., Butler, S. T., Lonergan, P., and Fair, S. (2017). Relationship between in vitro sperm functional assessments, seminal plasma composition, and field fertility after AI with either non-sorted or sex-sorted bull semen. Theriogenology 87, 221–228.
Relationship between in vitro sperm functional assessments, seminal plasma composition, and field fertility after AI with either non-sorted or sex-sorted bull semen.CrossRef | 1:STN:280:DC%2BC2svksVSruw%3D%3D&md5=8ea8cec351a482132ca20d067a9ded11CAS |

Juyena, N. S., and Stelletta, C. (2012). Seminal plasma: an essential attribute to spermatozoa. J. Androl. 33, 536–551.
Seminal plasma: an essential attribute to spermatozoa.CrossRef |

Kątska, L., Ryńska, B., and Smora̧ag, Z. (1996). Effect of seminal plasma on the in vitro fertilizability of bull spermatozoa. Anim. Reprod. Sci. 44, 23–31.
Effect of seminal plasma on the in vitro fertilizability of bull spermatozoa.CrossRef |

Khan, M. I. R., and Ijaz, A. (2008). Effects of osmotic pressure on motility, plasma membrane integrity and viability in fresh and frozen–thawed buffalo spermatozoa. Animal 2, 548–553.
Effects of osmotic pressure on motility, plasma membrane integrity and viability in fresh and frozen–thawed buffalo spermatozoa.CrossRef | 1:STN:280:DC%2BC38vptVymtQ%3D%3D&md5=155527851251fb684c54e612d28412dfCAS |

Kikuchi, K., Nagai, T., Kashiwazaki, N., Ikeda, H., Noguchi, J., Shimada, A., Soloy, E., and Kaneko, H. (1998). Cryopreservation and ensuing in vitro fertilization ability of boar spermatozoa from epididymides stored at 4°C. Theriogenology 50, 615–623.
Cryopreservation and ensuing in vitro fertilization ability of boar spermatozoa from epididymides stored at 4°C.CrossRef | 1:STN:280:DC%2BD3c7ps1Ojsw%3D%3D&md5=4ae5e55ac2260b8748017dc61c4f17fbCAS |

Koppers, A. J., De Iuliis, G. N., Finnie, J. M., McLaughlin, E. A., and Aitken, R. J. (2008). Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa. J. Clin. Endocrinol. Metab. 93, 3199–3207.
Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa.CrossRef | 1:CAS:528:DC%2BD1cXpvVOlsLw%3D&md5=faba9e79a4df48bdb03d6e57e7d1a839CAS |

Langlais, J., and Roberts, K. D. (1985). A molecular membrane model of sperm capacitation and the acrosome reaction of mammalian spermatozoa. Gamete Res. 12, 183–224.
A molecular membrane model of sperm capacitation and the acrosome reaction of mammalian spermatozoa.CrossRef | 1:CAS:528:DyaL2MXlvFentbY%3D&md5=31f7f53bd693ab0ff5113c9bb0e80aafCAS |

Leahy, T., and Gadella, B. M. (2015). New insights into the regulation of cholesterol efflux from the sperm membrane. Asian J. Androl. 17, 561–567.
New insights into the regulation of cholesterol efflux from the sperm membrane.CrossRef | 1:CAS:528:DC%2BC2MXhvValt73M&md5=87d2f6dca1b44c7f5062e329805be153CAS |

Li, H., Hung, P. H., and Suarez, S. S. (2015). Ejaculated mouse sperm enter cumulus–oocyte complexes more efficiently in vitro than epididymal sperm. PLoS One 10, e0127753.
Ejaculated mouse sperm enter cumulus–oocyte complexes more efficiently in vitro than epididymal sperm.CrossRef |

Lima, F. S., Risco, C. A., Thatcher, M. J., Benzaquen, M. E., Archbald, L. F., Santos, J. E., and Thatcher, W. W. (2009). Comparison of reproductive performance in lactating dairy cows bred by natural service or timed artificial insemination. J. Dairy Sci. 92, 5456–5466.
Comparison of reproductive performance in lactating dairy cows bred by natural service or timed artificial insemination.CrossRef | 1:CAS:528:DC%2BD1MXhtlKnsrbL&md5=3ead27745cd55d9222ff57fb92df1f2bCAS |

Liu, Y., Wang, D. K., and Chen, L. M. (2012). The physiology of bicarbonate transporters in mammalian reproduction. Biol. Reprod. 86, 99.
The physiology of bicarbonate transporters in mammalian reproduction.CrossRef |

Manjunath, P., Bergeron, A., Lefebvre, J., and Fan, J. (2007). Seminal plasma proteins: functions and interaction with protective agents during semen preservation. Soc. Reprod. Fertil. Suppl. 65, 217–228.
| 1:CAS:528:DC%2BD1cXpvVyrt70%3D&md5=13f595b595ce281e1265142e10c9eb31CAS |

Martins, C. F., Driessen, K., Costa, P. M., Carvalho-Neto, J. O., de Sousa, R. V., Rumpf, R., and Dode, M. N. (2009). Recovery, cryopreservation and fertilization potential of bovine spermatozoa obtained from epididymides stored at 5 degrees C by different periods of time. Anim. Reprod. Sci. 116, 50–57.
Recovery, cryopreservation and fertilization potential of bovine spermatozoa obtained from epididymides stored at 5 degrees C by different periods of time.CrossRef | 1:CAS:528:DC%2BD1MXhtVKkt7jP&md5=440030c4bf2bbcac5291283474e1bb51CAS |

Martinus, R., Molan, P., and Shannon, P. (1991). Deleterious effect of seminal plasma in the cryo-preservation of bovine spermatozoa. N. Z. J. Agric. Res. 34, 281–285.
Deleterious effect of seminal plasma in the cryo-preservation of bovine spermatozoa.CrossRef |

Maxwell, W. M., de Graaf, S. P., Ghaoui, R.-H., and Evans, G. (2007). Seminal plasma effects on sperm handling and female fertility. Soc. Reprod. Fertil. Suppl. 64, 13–38.
| 1:CAS:528:DC%2BD1cXpvVyku7c%3D&md5=c591daa5ffb823cb3a9d18f43e10b185CAS |

McCarthy, M. J., Baumber, J., Kass, P. H., and Meyers, S. A. (2010). Osmotic stress induces oxidative cell damage to rhesus macaque spermatozoa. Biol. Reprod. 82, 644–651.
Osmotic stress induces oxidative cell damage to rhesus macaque spermatozoa.CrossRef | 1:CAS:528:DC%2BC3cXisVersrw%3D&md5=2f81cd988e76287f44a068444e02394eCAS |

Moraes, E. A., Graham, J. K., Torres, C. A. A., Meyers, M., and Spizziri, B. (2010). Delivering cholesterol or cholestanol to bull sperm membranes improves cryosurvival. Anim. Reprod. Sci. 118, 148–154.
Delivering cholesterol or cholestanol to bull sperm membranes improves cryosurvival.CrossRef | 1:CAS:528:DC%2BC3cXhtVGltbs%3D&md5=aed99c87a12bd442b44b06a97819d2e0CAS |

Murphy, C., Holden, S. A., Murphy, E. M., Cromie, A. R., Lonergan, P., and Fair, S. (2016). The impact of storage temperature and sperm number on the fertility of liquid-stored bull semen. Reprod. Fertil. Dev. 28, 1349–1359.
The impact of storage temperature and sperm number on the fertility of liquid-stored bull semen.CrossRef | 1:CAS:528:DC%2BC28Xht1Gjt77O&md5=8ffa5f2e1095cd2de16d3d2050d46280CAS |

Odhiambo, J. F., Poole, D. H., Hughes, L., Dejarnette, J. M., Inskeep, E. K., and Dailey, R. A. (2009). Pregnancy outcome in dairy and beef cattle after artificial insemination and treatment with seminal plasma or transforming growth factor beta-1. Theriogenology 72, 566–571.
Pregnancy outcome in dairy and beef cattle after artificial insemination and treatment with seminal plasma or transforming growth factor beta-1.CrossRef | 1:CAS:528:DC%2BD1MXptl2ns70%3D&md5=36690b83865fb8ad418117042fee11d5CAS |

O’Meara, C. M., Donovan, A., Hanrahan, J. P., Duffy, P., Fair, S., Evans, A. C. O., and Lonergan, P. (2007). Resuspending ram spermatozoa in seminal plasma after cryopreservation does not improve pregnancy rate in cervically inseminated ewes. Theriogenology 67, 1262–1268.
Resuspending ram spermatozoa in seminal plasma after cryopreservation does not improve pregnancy rate in cervically inseminated ewes.CrossRef | 1:CAS:528:DC%2BD2sXjs1Ojs7Y%3D&md5=598d1d36e87b69e42d84e716f5008aebCAS |

Pang, S. F., Chow, P. H., and Wong, T. M. (1979). The role of the seminal vesicles, coagulating glands and prostate glands on the fertility and fecundity of mice. J. Reprod. Fertil. 56, 129–132.
The role of the seminal vesicles, coagulating glands and prostate glands on the fertility and fecundity of mice.CrossRef | 1:STN:280:DyaE1M3ktFOmsw%3D%3D&md5=c14a942b53f4a9943ee5fc94fe324d9eCAS |

Papa, F. O., Melo, C. M., Fioratti, E. G., Dell’Aqua, J. A., Zahn, F. S., and Alvarenga, M. A. (2008). Freezing of stallion epididymal sperm. Anim. Reprod. Sci. 107, 293–301.
Freezing of stallion epididymal sperm.CrossRef | 1:CAS:528:DC%2BD1cXoslWktLw%3D&md5=52e1468639f904c10fac542bf75dbae9CAS |

Peitz, B., and Olds-Clarke, P. (1986). Effects of seminal vesicle removal on fertility and uterine sperm motility in the house mouse. Biol. Reprod. 35, 608–617.
Effects of seminal vesicle removal on fertility and uterine sperm motility in the house mouse.CrossRef | 1:STN:280:DyaL2s%2Fns1ynsg%3D%3D&md5=02d4c338b50d67d05e60eaefec370b90CAS |

Pfeiffer, K. E., Binversie, J. A., Rhinehart, J. D., and Larson, J. E. (2012). Exposure of beef females to the biostimulatory effects of bulls with or without deposition of seminal plasma prior to AI. Anim. Reprod. Sci. 133, 27–34.
Exposure of beef females to the biostimulatory effects of bulls with or without deposition of seminal plasma prior to AI.CrossRef | 1:STN:280:DC%2BC38jnsVCmtw%3D%3D&md5=7d8ea0d686d2a95090b3e335ec5ac647CAS |

Queen, K., Dhabuwala, C. B., and Pierrepoint, C. G. (1981). The effect of the removal of the various accessory sex glands on the fertility of male rats. J. Reprod. Fertil. 62, 423–426.
The effect of the removal of the various accessory sex glands on the fertility of male rats.CrossRef | 1:STN:280:DyaL3M3kt1antA%3D%3D&md5=23ee9dcb163d7261ce7506d734c52a6dCAS |

Robertson, S. A. (2005). Seminal plasma and male factor signalling in the female reproductive tract. Cell Tissue Res. 322, 43–52.
Seminal plasma and male factor signalling in the female reproductive tract.CrossRef |

Robertson, S. A., and Sharkey, D. J. (2016). Seminal fluid and fertility in women. Fertil. Steril. 106, 511–519.
Seminal fluid and fertility in women.CrossRef |

Shannon, P. (1965a). Contribution of seminal plasma, sperm numbers, and gas phase to dilution effects of bovine spermatozoa. J. Dairy Sci. 48, 1357–1361.
Contribution of seminal plasma, sperm numbers, and gas phase to dilution effects of bovine spermatozoa.CrossRef | 1:STN:280:DyaF28%2FpvVWlsw%3D%3D&md5=7c1ddbb7fc2aa618cdaa2c3c5d40d639CAS |

Shannon, P. (1965b). Presence of a heat-labile toxic protein in bovine seminal plasma. J. Dairy Sci. 48, 1362–1365.
Presence of a heat-labile toxic protein in bovine seminal plasma.CrossRef | 1:CAS:528:DyaF2MXltVWlu74%3D&md5=b41aceeb4b7fc72800319d152e537a8cCAS |

Vadnais, M. L., Galantino-Homer, H. L., and Althouse, G. C. (2007). Current concepts of molecular events during bovine and porcine spermatozoa capacitation. Arch. Androl. 53, 109–123.
Current concepts of molecular events during bovine and porcine spermatozoa capacitation.CrossRef | 1:CAS:528:DC%2BD2sXnsVyrurw%3D&md5=762d00001f6f153a6a6cb52a69683060CAS |

Wales, R. G., Wallace, J. C., and White, I. G. (1966). Composition of bull epididymal and testicular fluid. J. Reprod. Fertil. 12, 139–144.
Composition of bull epididymal and testicular fluid.CrossRef | 1:CAS:528:DyaF28XkvVCntb0%3D&md5=20b5853d7609046cc40bc5bd8ba97812CAS |

Ward, F., Rizos, D., Corridan, D., Quinn, K., Boland, M., and Lonergan, P. (2001). 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. Mol. Reprod. Dev. 60, 47–55.
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.CrossRef | 1:CAS:528:DC%2BD3MXlvFWisrY%3D&md5=f044814f7e56b497f36530445dcd3c46CAS |

Way, A. L., Griel, L. C., and Killian, G. J. (2000). Effects of accessory sex gland fluid on viability, capacitation, and the acrosome reaction of cauda epididymal bull spermatozoa. J. Androl. 21, 213–219.
| 1:STN:280:DC%2BD3c7nslaqtQ%3D%3D&md5=a0a1068d09ea040c17e1185f893e3a1aCAS |



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