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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Sperm functional attributes and oviduct explant binding capacity differs between bulls with different fertility ratings in the water buffalo (Bubalus bubalis)

Kaustubh Kishor Saraf A * , Raushan Kumar Singh A * , Arumugam Kumaresan A D , Samiksha Nayak A , Shivani Chhillar A , Sreela Lathika A , Tirtha Kumar Datta B and Tushar Kumar Mohanty C
+ Author Affiliations
- Author Affiliations

A Theriogenology Lab, Animal Reproduction, Gynaecology & Obstetrics, ICAR-National Dairy Research Institute, Karnal-132001, Haryana, India.

B Animal Biotechnology Centre, National Dairy Research Institute, Karnal-132001, Haryana, India.

C Artificial Breeding Research Centre, National Dairy Research Institute, Karnal-132001, Haryana, India.

D Corresponding author. Emails: ogkumaresan@gmail.com; a.kumaresan@icar.gov.in

Reproduction, Fertility and Development 31(2) 395-403 https://doi.org/10.1071/RD17452
Submitted: 26 October 2017  Accepted: 19 July 2018   Published: 23 August 2018

Abstract

We report here the differences in sperm functional attributes and sperm–oviduct binding index in bulls with different field fertility ratings. Cryopreserved spermatozoa from Murrah buffalo bulls (n = 9) with different fertility ratings were evaluated for membrane integrity, capacitation status, acrosome intactness and protein tyrosine phosphorylation status. Frozen­–thawed spermatozoa were incubated with oviduct explants for 1 h under 5% CO2, 38.5°C with 95% relative humidity and the number of spermatozoa bound to the unit area of oviduct explants (binding index; BI) was assessed using 5,5′,6,6′-tetrachloro-1,1′,3,3′-tetraethylbenzimidazolyl-carbocyanine iodide (JC-1) fluorescent staining. The proportion of membrane-intact and acrosome-intact spermatozoa was significantly (P < 0.05) higher and the proportion of capacitated spermatozoa was significantly (P < 0.05) lower in high-fertile bulls compared with medium- and low-fertile bulls. The relationship between BI and bull fertility was significant and positive (r = 0.69; P = 0.04). BI was negatively and significantly (r = −0.83; P = 0.01) related to membrane-compromised spermatozoa. It was concluded that the sperm–oviduct explant binding index was positively related to (1) the proportion of membrane-intact spermatozoa in a given semen sample and (2) in vivo fertility of the buffalo bull, indicating the possibility of developing a fertility prediction tool using a sperm–oviduct explant binding model, once validated on a greater number of bulls.

Additional keywords: bull fertility, sperm function, sperm–oviduct binding index.


References

Andrabi, S. M. H. (2009). Factors affecting the quality of cryopreserved buffalo (Bubalus bubalis) bull spermatozoa. Reprod. Domest. Anim. 44, 552–569.
Factors affecting the quality of cryopreserved buffalo (Bubalus bubalis) bull spermatozoa.Crossref | GoogleScholarGoogle Scholar |

Ardon, F., Helms, D., Sahin, E., Bollwein, H., To¨pfer-Petersen, E., and Waberski, D. (2008). Chromatin-unstable boar spermatozoa have little chance of reaching oocytes in vivo. Reproduction 135, 461–470.
Chromatin-unstable boar spermatozoa have little chance of reaching oocytes in vivo.Crossref | GoogleScholarGoogle Scholar |

Birck, A., Christensen, P., Labouriau, R., Pedersen, J., and Borchersen, S. (2010). In vitro induction of the acrosome reaction in bull sperm and the relationship to field fertility using low-dose inseminations. Theriogenology 73, 1180–1191.
In vitro induction of the acrosome reaction in bull sperm and the relationship to field fertility using low-dose inseminations.Crossref | GoogleScholarGoogle Scholar |

DeMott, R. P., Lefebvre, R., and Suarez, S. S. (1995). Carbohydrates mediate the adherence of hamster sperm to oviductal epithelium. Biol. Reprod. 52, 1395–1403.
Carbohydrates mediate the adherence of hamster sperm to oviductal epithelium.Crossref | GoogleScholarGoogle Scholar |

De Pauw, I. M., Van Soom, A., Laevens, H., Verberckmoes, S., and de Kruif, A. (2002). Sperm binding to epithelial oviduct explants in bulls with different non return rates investigated with a new in vitro model. Biol. Reprod. 67, 1073–1079.
Sperm binding to epithelial oviduct explants in bulls with different non return rates investigated with a new in vitro model.Crossref | GoogleScholarGoogle Scholar |

Ellington, J. E., Evenson, D. P., Wright, R. W., Jones, A. E., Schneider, C. S., Hiss, G. A., and Brisbois, R. S. (1999). Higher-quality human sperm in a sample selectively attach to oviduct (fallopian tube) epithelial cells in vitro. Fertil. Steril. 71, 924–929.
Higher-quality human sperm in a sample selectively attach to oviduct (fallopian tube) epithelial cells in vitro.Crossref | GoogleScholarGoogle Scholar |

Fazeli, A., Duncan, A. E., Watson, P. F., and Holt, W. V. (1999). Sperm-oviduct interaction: induction of capacitation and preferential binding of uncapacitated spermatozoa to oviductal epithelial cells in porcine species. Biol. Reprod. 60, 879–886.
Sperm-oviduct interaction: induction of capacitation and preferential binding of uncapacitated spermatozoa to oviductal epithelial cells in porcine species.Crossref | GoogleScholarGoogle Scholar |

Green, C. E., and Watson, P. F. (2001). Comparison of the capacitation-like state of cooled boar spermatozoa with true capacitation. Reproduction 122, 889–898.
Comparison of the capacitation-like state of cooled boar spermatozoa with true capacitation.Crossref | GoogleScholarGoogle Scholar |

Gualtieri, R., and Talevi, R. (2000). In vitro-cultured bovine oviductal cells bind acrosome-intact sperm and retain this ability upon sperm release. Biol. Reprod. 62, 1754–1762.
In vitro-cultured bovine oviductal cells bind acrosome-intact sperm and retain this ability upon sperm release.Crossref | GoogleScholarGoogle Scholar |

Gualtieri, R., and Talevi, R. (2003). Selection of highly fertilization-competent bovine spermatozoa through adhesion to the Fallopian tube epithelium in vitro. Reproduction 125, 251–258.
Selection of highly fertilization-competent bovine spermatozoa through adhesion to the Fallopian tube epithelium in vitro.Crossref | GoogleScholarGoogle Scholar |

Hallap, T., Nagy, S., Jaakma, Ü., Johannisson, A., and Rodriguez-Martinez, H. (2006). Usefulness of a triple fluorochrome combination Merocyanine 540/Yo-Pro 1/Hoechst 33342 in assessing membrane stability of viable frozen-thawed spermatozoa from Estonian Holstein AI bulls. Theriogenology 65, 1122–1136.
Usefulness of a triple fluorochrome combination Merocyanine 540/Yo-Pro 1/Hoechst 33342 in assessing membrane stability of viable frozen-thawed spermatozoa from Estonian Holstein AI bulls.Crossref | GoogleScholarGoogle Scholar |

Harayama, H., Nishijima, K., Murase, T., Sakase, M., and Fukushima, M. (2010). Relationship of protein tyrosine phosphorylation state with tolerance to frozen storage and the potential to undergo cyclic AMP-dependent hyperactivation in the spermatozoa of Japanese Black bulls. Mol. Reprod. Dev. 77, 910–921.
Relationship of protein tyrosine phosphorylation state with tolerance to frozen storage and the potential to undergo cyclic AMP-dependent hyperactivation in the spermatozoa of Japanese Black bulls.Crossref | GoogleScholarGoogle Scholar |

Holt, W. V., and Fazeli, A. (2010). The oviduct as a complex mediator of mammalian sperm function and selection. Mol. Reprod. Dev. 77, 934–943.
The oviduct as a complex mediator of mammalian sperm function and selection.Crossref | GoogleScholarGoogle Scholar |

Hunter, R. H. F., and Wilmut, I. (1984). Sperm transport in the cow: peri-ovulatory redistribution of viable cells within the oviduct. Reprod. Nutr. Dev. 24, 597–608.
Sperm transport in the cow: peri-ovulatory redistribution of viable cells within the oviduct.Crossref | GoogleScholarGoogle Scholar |

Hunter, R. H. F., Nichol, R., and Crabtree, S. M. (1980). Transport of spermatozoa in the ewe: timing of the establishment of a functional population in the oviduct. Reprod. Nutr. Dev. 20, 1869–1875.
Transport of spermatozoa in the ewe: timing of the establishment of a functional population in the oviduct.Crossref | GoogleScholarGoogle Scholar |

Hunter, R. H. F., Fléchon, B., and Fléchon, J. E. (1987). Pre-and peri-ovulatory distribution of viable spermatozoa in the pig oviduct: a scanning electron microscope study. Tissue Cell 19, 423–436.
Pre-and peri-ovulatory distribution of viable spermatozoa in the pig oviduct: a scanning electron microscope study.Crossref | GoogleScholarGoogle Scholar |

Januskauskas, A., Johannisson, A., and Rodriguez-Martinez, H. (2003). Subtle membrane changes in cryopreserved bull semen in relation with sperm viability, chromatin structure, and field fertility. Theriogenology 60, 743–758.
Subtle membrane changes in cryopreserved bull semen in relation with sperm viability, chromatin structure, and field fertility.Crossref | GoogleScholarGoogle Scholar |

Kalab, P., Peknicová, J., Geussova, G., and Moos, J. (1998). Regulation of protein tyrosine phosphorylation in boar sperm through a cAMP-dependent pathway. Mol. Reprod. Dev. 51, 304–314.
Regulation of protein tyrosine phosphorylation in boar sperm through a cAMP-dependent pathway.Crossref | GoogleScholarGoogle Scholar |

Kaul, G., Sharma, G. S., Singh, B., and Gandhi, K. K. (2001). Capacitation and acrosome reaction in buffalo bull spermatozoa assessed by chlortetracycline and Pisum sativum agglutinin fluorescence assay. Theriogenology 55, 1457–1468.
Capacitation and acrosome reaction in buffalo bull spermatozoa assessed by chlortetracycline and Pisum sativum agglutinin fluorescence assay.Crossref | GoogleScholarGoogle Scholar |

Kumar, D., Kumar, P., Singh, P., Yadav, S. P., Sarkar, S. K., Bharadwaj, A., and Yadav, P. S. (2014). Characteristics of frozen thawed semen in predicting the fertility of buffalo bulls. Indian J. Anim. Sci. 84, 389–392.

Kumar, V., Kumaresan, A., DS, P. K., Lathika, S., Nayak, S., et al. (2017). Anandamide exerts a suppressive effect on sperm binding to oviduct explants through CB1 receptors in the water buffalo (Bubalus bubalis). Anim. Reprod. Sci. 185, 188–194.
Anandamide exerts a suppressive effect on sperm binding to oviduct explants through CB1 receptors in the water buffalo (Bubalus bubalis).Crossref | GoogleScholarGoogle Scholar |

Kumaresan, A., Johannisson, A., Humblot, P., and Bergqvist, A. S. (2012a). Oviductal fluid modulates the dynamics of tyrosine phosphorylation in cryopreserved boar spermatozoa during capacitation. Mol. Reprod. Dev. 79, 525–540.
Oviductal fluid modulates the dynamics of tyrosine phosphorylation in cryopreserved boar spermatozoa during capacitation.Crossref | GoogleScholarGoogle Scholar |

Kumaresan, A., Siqueira, A. P., Hossain, M. S., Johannisson, A., Eriksson, I., Wallgren, M., and Bergqvist, A. S. (2012b). Quantification of kinetic changes in protein tyrosine phosphorylation and cytosolic Ca2+ concentration in boar spermatozoa during cryopreservation. Reprod. Fertil. Dev. 24, 531–542.
Quantification of kinetic changes in protein tyrosine phosphorylation and cytosolic Ca2+ concentration in boar spermatozoa during cryopreservation.Crossref | GoogleScholarGoogle Scholar |

Kumaresan, A., González, R., Johannisson, A., and Berqvist, A. S. (2014). Dynamic quantification of intracellular calcium and protein tyrosine phosphorylation in cryopreserved boar spermatozoa during short-time incubation with oviductal fluid. Theriogenology 82, 1145–1153.
Dynamic quantification of intracellular calcium and protein tyrosine phosphorylation in cryopreserved boar spermatozoa during short-time incubation with oviductal fluid.Crossref | GoogleScholarGoogle Scholar |

Kumaresan, A., Johannisson, A., and Bergqvist, A. S. (2017a). Sperm function during incubation with oestrus oviductal fluid differs in bulls with different fertility. Reprod. Fertil. Dev. 29, 1096–1106.
Sperm function during incubation with oestrus oviductal fluid differs in bulls with different fertility.Crossref | GoogleScholarGoogle Scholar |

Kumaresan, A., Johannisson, A., Al-Essawe, E. M., and Morrell, J. M. (2017b). Sperm viability, reactive oxygen species, and DNA fragmentation index combined can discriminate between above-and below-average fertility bulls. J. Dairy Sci. 100, 5824–5836.
Sperm viability, reactive oxygen species, and DNA fragmentation index combined can discriminate between above-and below-average fertility bulls.Crossref | GoogleScholarGoogle Scholar |

Leemans, B., Gadella, B. M., Sostaric, E., Nelis, H., Stout, T. A., Hoogewijs, M., and Van Soom, A. (2014). Oviduct binding and elevated environmental pH induce protein tyrosine phosphorylation in stallion spermatozoa. Biol. Reprod. 91, 13–21.
Oviduct binding and elevated environmental pH induce protein tyrosine phosphorylation in stallion spermatozoa.Crossref | GoogleScholarGoogle Scholar |

Lefebvre, R., and Suarez, S. S. (1996). Effect of capacitation on bull sperm binding to homologous oviductal epithelium. Biol. Reprod. 54, 575–582.
Effect of capacitation on bull sperm binding to homologous oviductal epithelium.Crossref | GoogleScholarGoogle Scholar |

Lefebvre, R., Chenoweth, P. J., Drost, M., LeClear, C. T., MacCubbin, M., Dutton, J. T., and Suarez, S. S. (1995). Characterization of the oviductal sperm reservoir in cattle. Biol. Reprod. 53, 1066–1074.
Characterization of the oviductal sperm reservoir in cattle.Crossref | GoogleScholarGoogle Scholar |

Mastroianni, L. (1999). The fallopian tube and reproductive health. J. Pediatr. Adolesc. Gynecol. 12, 121–126.
The fallopian tube and reproductive health.Crossref | GoogleScholarGoogle Scholar |

Pena, F. J., Saravia, F., Johannisson, A., Wallgren, M., and Rodriguez-Martinez, H. (2007). Detection of early changes in sperm membrane integrity pre-freezing can estimate post-thaw quality of boar spermatozoa. Anim. Reprod. Sci. 97, 74–83.
Detection of early changes in sperm membrane integrity pre-freezing can estimate post-thaw quality of boar spermatozoa.Crossref | GoogleScholarGoogle Scholar |

Petrunkina, A. M., and Harrison, R. A. P. (2011). Cytometric solutions in veterinary andrology: developments, advantages, and limitations. Cytometry A 79A, 338–348.
Cytometric solutions in veterinary andrology: developments, advantages, and limitations.Crossref | GoogleScholarGoogle Scholar |

Petrunkina, A. M., Gehlhaar, R., Drommer, W., Waberski, D., and Topfer-Petersen, E. (2001). Selective sperm binding to pig oviductal epithelium in vitro. Reproduction 121, 889–896.
Selective sperm binding to pig oviductal epithelium in vitro.Crossref | GoogleScholarGoogle Scholar |

Rodriguez-Martinez, H., Saravia, F., Wallgren, M., Tienthai, P., Johannisson, A., Vazquez, J. M., and Calvete, J. J. (2005). Boar spermatozoa in the oviduct. Theriogenology 63, 514–535.
Boar spermatozoa in the oviduct.Crossref | GoogleScholarGoogle Scholar |

Saraf, K. K., Kumaresan, A., Chhillar, S., Nayak, S., Lathika, S., Datta, T. K., and Mohanty, T. K. (2017a). Spermatozoa with high mitochondrial membrane potential and low tyrosine phosphorylation preferentially bind to oviduct explants in the water buffalo (Bubalus bubalis). Anim. Reprod. Sci. 180, 30–36.
Spermatozoa with high mitochondrial membrane potential and low tyrosine phosphorylation preferentially bind to oviduct explants in the water buffalo (Bubalus bubalis).Crossref | GoogleScholarGoogle Scholar |

Saraf, K. K., Kumaresan, A., Nayak, S., Chhillar, S., Sreela, L., Kumar, S., Tripathi, U. K., Datta, T. K., and Mohanty, T. K. (2017b). Development of an in vitro oviduct epithelial explants model for studying sperm-oviduct binding in the buffalo. Reprod. Domest. Anim. 52, 687–691.
Development of an in vitro oviduct epithelial explants model for studying sperm-oviduct binding in the buffalo.Crossref | GoogleScholarGoogle Scholar |

Singh, R. K., Kumaresan, A., Chhillar, S., Rajak, S. K., Tripathi, U. K., Nayak, S., and Malhotra, R. (2016). Identification of suitable combinations of in vitro sperm-function test for the prediction of fertility in buffalo bull. Theriogenology 86, 2263–2271.e1.
Identification of suitable combinations of in vitro sperm-function test for the prediction of fertility in buffalo bull.Crossref | GoogleScholarGoogle Scholar |

Thomas, P. G., Ball, B. A., Miller, P. G., Brinsko, S. P., and Southwood, L. (1994). A subpopulation of morphologically normal, motile spermatozoa attach to equine oviductal epithelial cell monolayers. Biol. Reprod. 51, 303–309.
A subpopulation of morphologically normal, motile spermatozoa attach to equine oviductal epithelial cell monolayers.Crossref | GoogleScholarGoogle Scholar |

Thundathil, J., Gil, J., Januskauskas, A., Larsson, B., Soderquist, L., Mapletoft, R., and Rodriguez-Martinez, H. (1999). Relationship between the proportion of capacitated spermatozoa present in frozen-thawed bull semen and fertility with artificial insemination. Int. J. Androl. 22, 366–373.
Relationship between the proportion of capacitated spermatozoa present in frozen-thawed bull semen and fertility with artificial insemination.Crossref | GoogleScholarGoogle Scholar |

Troedsson, M. H., Liu, I. K., and Crabo, B. G. (1998). Sperm transport and survival in the mare: a review. Theriogenology 50, 807–818.

Visconti, P. E., Moore, G. D., Bailey, J. L., Leclerc, P., Connors, S. A., Pan, D., and Kopf, G. S. (1995). Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. Development 121, 1139–1150.

Waberski, D., Magnus, F., Ardon, F., Petrunkina, A. M., Weitze, K. F., and Töpfer-Petersen, E. (2006). Binding of boar spermatozoa to oviductal epithelium in vitro in relation to sperm morphology and storage time. Reproduction 131, 311–318.
Binding of boar spermatozoa to oviductal epithelium in vitro in relation to sperm morphology and storage time.Crossref | GoogleScholarGoogle Scholar |

Yeste, M., Lloyd, R. E., Badia, E., Briz, M., Bonet, S., and Holt, W. V. (2009). Direct contact between boar spermatozoa and porcine oviductal epithelial cell (OEC) cultures is needed for optimal sperm survival in vitro. Anim. Reprod. Sci. 113, 263–278.
Direct contact between boar spermatozoa and porcine oviductal epithelial cell (OEC) cultures is needed for optimal sperm survival in vitro.Crossref | GoogleScholarGoogle Scholar |

Yeste, M., Castillo-Martín, M., Bonet, S., and Briz, M. D. (2012). Direct binding of boar ejaculate and epididymal spermatozoa to porcine epididymal epithelial cells is also needed to maintain sperm survival in in vitro co-culture. Anim. Reprod. Sci. 131, 181–193.
Direct binding of boar ejaculate and epididymal spermatozoa to porcine epididymal epithelial cells is also needed to maintain sperm survival in in vitro co-culture.Crossref | GoogleScholarGoogle Scholar |

Yeste, M., Holt, W. V., Bonet, S., Rodríguez‐Gil, J. E., and Lloyd, R. E. (2014). Viable and morphologically normal boar spermatozoa alter the expression of heat-shock protein genes in oviductal epithelial cells during co-culture in vitro. Mol. Reprod. Dev. 81, 805–819.
Viable and morphologically normal boar spermatozoa alter the expression of heat-shock protein genes in oviductal epithelial cells during co-culture in vitro.Crossref | GoogleScholarGoogle Scholar |