Sperm function during incubation with oestrus oviductal fluid differs in bulls with different fertility
A. Kumaresan A B , A. Johannisson A and A.-S. Bergqvist A C
+ Author Affiliations
- Author Affiliations
A Division of Reproduction, Department of Clinical Sciences, Faculty of Veterinary Medicine and Animal Science, Swedish University of Agricultural Sciences, PO Box 7054, SE-750 07 Uppsala, Sweden.
B Present address: Theriogenology Laboratory, Animal Reproduction, Gynaecology and Obstetrics, National Dairy Research Institute, Karnal, 132001 Haryana, India.
C Corresponding author. Email: ann-sofi.bergqvist@slu.se
Reproduction, Fertility and Development 29(6) 1096-1106 https://doi.org/10.1071/RD15474
Submitted: 14 November 2015 Accepted: 1 March 2016 Published: 26 April 2016
Abstract
Spermatozoa undergo several modifications in the oviduct before acquiring fertilising capacity. Although spermatozoa are exposed to similar conditions in the oviduct, the speed of the response varies with the male and the state of the spermatozoa. We hypothesised that spermatozoa from bulls with different fertility may differ in their ability to respond to oviductal fluid (ODF). Frozen–thawed spermatozoa from four bulls were incubated with oestrus oviductal fluid (OODF) for 6 h. Sperm kinematics, tyrosine phosphorylation, phosphorylation patterns, capacitation and acrosome reaction were analysed at hourly intervals. The amplitude of lateral head displacement (ALH) and straightness coefficient (STR) were higher (P < 0.05) in bulls with higher fertility compared with those with lower fertility, at 1–4 h of incubation. At 4 h of incubation and onwards, spermatozoa from bulls with higher fertility showed a lower degree (P < 0.05) of tyrosine phosphorylation and higher degree of capacitation and acrosome reaction. At least five tyrosine-phosphorylated sperm proteins were detected in all bulls. However, the expression of two phosphorylated sperm proteins (183 and 109 kDa) was upregulated in bulls with lower fertility. It may be concluded that cryopreserved spermatozoa from high- and low- fertile bulls differ in their ability to respond to OODF. This may help in developing tools for assessing fertility of bulls, once validated in more animals.
Additional keywords: acrosome reaction, bovine, capacitation, tyrosine phosphorylation.
References
Austin, C. R. (1951). Observation of the penetration of sperm into the mammalian egg. Aust. J. Sci. Res. B 4, 581–596.| 1:STN:280:DyaG38%2FisFGqsw%3D%3D&md5=d4ef88420694a768c1706a9dfac89749CAS | 14895481PubMed |
Bailey, J. L., Bilodeau, J. F., and Cormier, N. (2000). Semen cryopreservation in domestic animals: a damaging and capacitating phenomenon. J. Androl. 21, 1–7.
| 1:STN:280:DC%2BD3c7jtl2ktg%3D%3D&md5=5c0560e354465ee5bf9ebf491488228dCAS | 10670514PubMed |
Bergqvist, A.-S., Yokoo, M., Heldin, P., Frendin, J., Sato, E., and Rodríguez-Martínez, H. (2005). Hyaluronan and its binding proteins in the epithelium and intraluminal fluid of the bovine oviduct. Zygote 13, 207–218.
| Hyaluronan and its binding proteins in the epithelium and intraluminal fluid of the bovine oviduct.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVags73M&md5=9cac4291c840f5fcd78b44727757fbddCAS | 16261765PubMed |
Bergqvist, A.-S., Ballester, J., Johannisson, A., Hernandez, M., Lundeheim, N., and Rodríguez-Martínez, H. (2006). In vitro capacitation of bull spermatozoa by oviductal fluid and its components. Zygote 14, 259–273.
| In vitro capacitation of bull spermatozoa by oviductal fluid and its components.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xms1elsLo%3D&md5=a85f8c148370a9fc141fc1b13a2c6f08CAS | 16822337PubMed |
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 | 1:CAS:528:DC%2BC3cXlvVWgu7w%3D&md5=96449c9192210f2ad83ac0b1d7b234e1CAS | 20233626PubMed |
Chang, M. C. (1951). Fertilising capacity of sperm deposited into the fallopian tubes. Nature 168, 697–698.
| Fertilising capacity of sperm deposited into the fallopian tubes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG38%2Fht1Cgtw%3D%3D&md5=cd77c782682de63f56dc1783996a04caCAS | 14882325PubMed |
Farrell, P. B., Presicce, G. A., Brockett, C. C., and Foote, R. H. (1998). Quantification of bull sperm characteristics measured by CASA and the relationship to fertility. Theriogenology 49, 871–879.
| Quantification of bull sperm characteristics measured by CASA and the relationship to fertility.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7ps1Kntg%3D%3D&md5=9fdfb08a07f167df7d57d3b454ceaeadCAS | 10732095PubMed |
Fraser, L. R., Abeydeera, L. R., and Niwa, K. (1995). Ca2+-regulating mechanisms that modulate bull sperm capacitation and acrosomal exocytosis as determined by chlortetracycline analysis. Mol. Reprod. Dev. 40, 233–241.
| Ca2+-regulating mechanisms that modulate bull sperm capacitation and acrosomal exocytosis as determined by chlortetracycline analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXktFajs7c%3D&md5=a011ff7d86aa11dfb5f78c2c43ec07a0CAS | 7766417PubMed |
Freeman, S. L., and England, G. C. W. (2013). Storage and release of spermatozoa from the preuterine tube reservoir. PLoS ONE 8, e57006.
| Storage and release of spermatozoa from the preuterine tube reservoir.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjslyksro%3D&md5=1690b8740f8bb9703a1e14df87341ae4CAS | 23451135PubMed |
Gillan, L., Kroetsch, T., Maxwell, W. M. C., 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 |
Grippo, A. A., Way, A. L., and Killian, G. J. (1995). Effect of bovine ampullary and isthmic oviductal fluid on motility, acrosome reaction and fertility of bull spermatozoa. J. Reprod. Fertil. 105, 57–64.
| Effect of bovine ampullary and isthmic oviductal fluid on motility, acrosome reaction and fertility of bull spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXptVKmt7w%3D&md5=e46c48544cb388f7573cc7f5a485aafdCAS | 7490715PubMed |
Gualtieri, R., Boni, R., Tosti, E., Zagami, M., and Talevi, R. (2005). Intracellular calcium and protein tyrosine phosphorylation during the release of bovine sperm adhering to the fallopian tube epithelium in vitro. Reproduction 129, 51–60.
| Intracellular calcium and protein tyrosine phosphorylation during the release of bovine sperm adhering to the fallopian tube epithelium in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1eltbo%3D&md5=08fcf0308189a8457b3a2ddd621ad4ccCAS | 15615898PubMed |
Hallap, T., Nagy, S., Jaakma, U., Johannisson, A., and Rodriguez-Martinez, H. (2005). Mitochondrial activity of frozen–thawed spermatozoa assessed by MitoTracker Deep Red 633. Theriogenology 63, 2311–2322.
| Mitochondrial activity of frozen–thawed spermatozoa assessed by MitoTracker Deep Red 633.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtFyrtbc%3D&md5=3368c0c107a0e036f5d4c18241bdcec5CAS | 15826692PubMed |
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 | 1:CAS:528:DC%2BC3cXhtleqsLrN&md5=b9b46ad696190e78090222e98e731277CAS | 20845370PubMed |
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 | 1:CAS:528:DC%2BC3cXhsVCktrnL&md5=43d44c3f53d799c219aa6a7c1d0024f1CAS | 20886635PubMed |
Holt, C., Holt, W. V., Moore, H. D. M., Reed, H. C. B., and Curnock, R. M. (1997). Objectively measured boar sperm motility parameters correlate with the outcomes of on-farm inseminations: results of two fertility trials. J. Androl. 18, 312–323.
| 1:STN:280:DyaK2szks1Kntg%3D%3D&md5=62647f934d5fdef5398619f81e170c77CAS | 9203061PubMed |
Januskauskas, A., Johannisson, A., Soderquist, L., and Rodriguez-Martinez, H. (2000). Assessment of sperm characteristics post-thaw and response to calcium ionophore in relation to fertility in Swedish dairy AI bulls. Theriogenology 53, 859–875.
| Assessment of sperm characteristics post-thaw and response to calcium ionophore in relation to fertility in Swedish dairy AI bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitlGmuro%3D&md5=df8f8be5fc0394779ebbc9025c3e7be8CAS | 10730975PubMed |
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 | 1:STN:280:DC%2BD3szgsFaqtQ%3D%3D&md5=1a4c52cbbdc96273dce072d36ff499d2CAS | 12832022PubMed |
Kadirvel, G., Kathiravan, P., and Kumar, S. (2011). Protein tyrosine phosphorylation and zona-binding ability of in vitro-capacitated and cryopreserved buffalo spermatozoa. Theriogenology 75, 1630–1639.
| Protein tyrosine phosphorylation and zona-binding ability of in vitro-capacitated and cryopreserved buffalo spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotFWgt7w%3D&md5=0a4750b06031853f1ec1826b09184dbfCAS | 21458055PubMed |
Kavanaugh, J. F., Grippo, A. A., and Killian, G. J. (1992). Cannulation of the bovine ampullary and isthmic oviduct. J. Invest. Surg. 5, 11–17.
| Cannulation of the bovine ampullary and isthmic oviduct.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK383kslKquw%3D%3D&md5=bf79f5b0099ffe75c778ddcafcba876aCAS | 1576101PubMed |
Killian, G. J. (2004). Evidence for the role of oviduct secretions in sperm function, fertilisation and embryo development. Anim. Reprod. Sci. 82–83, 141–153.
| Evidence for the role of oviduct secretions in sperm function, fertilisation and embryo development.Crossref | GoogleScholarGoogle Scholar | 15271449PubMed |
Kumaresan, A., Ansari, M. R., and Garg, A. (2005). Modulation of post-thaw sperm functions with oviductal proteins in buffaloes. Anim. Reprod. Sci. 90, 73–84.
| Modulation of post-thaw sperm functions with oviductal proteins in buffaloes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFKmt7rK&md5=d6ffb7ba3a282f8d6e667e51dbd8be81CAS | 15950408PubMed |
Kumaresan, A., Ansari, M. R., Garg, A., and Kataria, M. (2006a). Effect of oviductal proteins on sperm functions and lipid peroxidation levels during cryopreservation in buffaloes. Anim. Reprod. Sci. 93, 246–257.
| Effect of oviductal proteins on sperm functions and lipid peroxidation levels during cryopreservation in buffaloes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkvVyisb4%3D&md5=d786bfadd84902c17b18958b966c8047CAS | 16198514PubMed |
Kumaresan, A., Ansari, M. R., and Garg, A. (2006b). Effect of non-luteal and luteal oviductal proteins on buffalo spermatozoa function during cryopreservation. Buffalo Journal 22, 45–53.
Kumaresan, A., Siqueira, A. P., Hossain, M. S., and Bergqvist, A.-S. (2011). Cryopreservation-induced alterations in protein tyrosine phosphorylation of spermatozoa from different portions of the boar ejaculate. Cryobiology 63, 137–144.
| Cryopreservation-induced alterations in protein tyrosine phosphorylation of spermatozoa from different portions of the boar ejaculate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFCqsLbO&md5=46e9d7e0cbc607a3736375e59d9cb9ddCAS | 21893053PubMed |
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 | 1:CAS:528:DC%2BC38XhtVSltb7L&md5=01864a6767459e6abe6529118de45b87CAS | 22674908PubMed |
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 | 1:CAS:528:DC%2BC38XmtVKiu7o%3D&md5=60c223d886bc532ae23955067215490fCAS | 22541541PubMed |
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 | 1:CAS:528:DC%2BC2cXhsV2ltrfJ&md5=daa2cb90a25968a65f00aee81e3a4b95CAS | 25175760PubMed |
Larson, J. L., and Miller, D. J. (2000). Can relative spermatozoal galactosyltransferase activity be predictive of dairy bull fertility? J. Dairy Sci. 83, 2473–2479.
| Can relative spermatozoal galactosyltransferase activity be predictive of dairy bull fertility?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosVCgsLs%3D&md5=4683eb7c9a029365dfa22a7171973b78CAS | 11104266PubMed |
McNutt, T. L., and Killian, G. J. (1991). Influence of bovine follicular and oviduct fluids on sperm capacitation in vitro. J. Androl. 12, 244–252.
| 1:STN:280:DyaK38%2FhtFWnsw%3D%3D&md5=272ad164e6918205a3d742faceada420CAS | 1917690PubMed |
Mortimer, S. T., and Mortimer, D. (1990). Kinematics of human spermatozoa incubated under capacitating conditions. J. Androl. 11, 195–203.
| 1:STN:280:DyaK3czks1Kguw%3D%3D&md5=307b8ccdcca74e62cf4a6be56be959dbCAS | 2384341PubMed |
Muhammad Aslam, M. K., Kumaresan, A., Sharma, V. K., Tajmul, M., Chhillar, S., Chakravarty, A. K., Manimaran, A., Mohanty, T. K., Srinivasan, A., and Yadav, S. (2014). Identification of putative fertility markers in seminal plasma of crossbred bulls through differential proteomics. Theriogenology 82, 1254–1262.e1.
| Identification of putative fertility markers in seminal plasma of crossbred bulls through differential proteomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFGltLfK&md5=0cb2894fd76a301ea7ceeb1c63d95b63CAS |
Nagy, S., Johannisson, A., Wahlsten, T., Ijäs, R., Andersson, M., and Rodriguez-Martinez, H. (2013). Sperm chromatin structure and sperm morphology: their association with fertility in AI dairy Ayrshire sires. Theriogenology 79, 1153–1161.
| Sperm chromatin structure and sperm morphology: their association with fertility in AI dairy Ayrshire sires.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3svovVyquw%3D%3D&md5=3d932a3cac486c1b8e56082880299541CAS | 23523176PubMed |
Naz, R. K., and Rajesh, P. B. (2004). Role of tyrosine phosphorylation in sperm capacitation–acrosome reaction. Reprod. Biol. Endocrinol. 2, 75.
| Role of tyrosine phosphorylation in sperm capacitation–acrosome reaction.Crossref | GoogleScholarGoogle Scholar | 15535886PubMed |
Petrunkina, A. M., and Harrison, R. A. P. (2011). Cytometric solutions in veterinary andrology: developments, advantages and limitations. Cytometry 79A, 338–348.
| Cytometric solutions in veterinary andrology: developments, advantages and limitations.Crossref | GoogleScholarGoogle Scholar |
Petrunkina, A. M., Simon, K., Günzel-Apel, A. R., and Topfer-Petersen, E. (2004). Kinetics of protein tyrosine phosphorylation in sperm selected by binding to homologous and heterologous oviductal explants: how specific is the regulation by the oviduct? Theriogenology 61, 1617–1634.
| Kinetics of protein tyrosine phosphorylation in sperm selected by binding to homologous and heterologous oviductal explants: how specific is the regulation by the oviduct?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhslWnu74%3D&md5=df6bb7d400e1a1c8ee78ed584945ec19CAS | 15019459PubMed |
Rodríguez-Martínez, H. (2003). Laboratory semen assessment and prediction of fertility: still utopia? Reprod. Domest. Anim. 38, 312–318.
| Laboratory semen assessment and prediction of fertility: still utopia?Crossref | GoogleScholarGoogle Scholar | 12887570PubMed |
Rodriguez-Martinez, H. (2007). Role of oviduct in sperm capacitation. Theriogenology 68, S138–S146.
| Role of oviduct in sperm capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotlaitLY%3D&md5=14fd835a33a6736fea7ac5a1dd098df6CAS | 17452049PubMed |
Rodríguez-Martínez, H. (2013). Semen evaluation techniques and their relationship with fertility. Anim. Reprod. 10, 148–159.
Rodriguez-Martinez, H., Tienthai, P., Suzuki, K., Funahashi, K., Ekwall, H., and Johannisson, A. (2001). Oviduct involvement in sperm capacitation and oocyte development. Reproduction 58, 129–145.
| 1:STN:280:DC%2BD383kt1SntQ%3D%3D&md5=e568272d6adf6ce2155b82438eea01bdCAS | 11980185PubMed |
Saacke, R. G., Dalton, J. C., Nadir, S., Nebel, R. L., and Bame, J. H. (2000). Relationship of seminal traits and insemination time to fertilisation rate and embryo quality. Anim. Reprod. Sci. 60–61, 663–677.
| Relationship of seminal traits and insemination time to fertilisation rate and embryo quality.Crossref | GoogleScholarGoogle Scholar | 10844233PubMed |
Shojaei, H., Kroetsch, T., Wilde, R., Blondin, P., Kastelic, J. P., and Thundathil, J. C. (2012). Moribund sperm in frozen–thawed semen, and sperm motion end points post-thaw and post-swim-up, are related to fertility in Holstein AI bulls. Theriogenology 77, 940–951.
| Moribund sperm in frozen–thawed semen, and sperm motion end points post-thaw and post-swim-up, are related to fertility in Holstein AI bulls.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC383mtFyqug%3D%3D&md5=e77cd2f3eb9b0747768dff7bc716530eCAS | 22137769PubMed |
Sidhu, K. S., Mate, K. E., Gunasekera, T., Veal, D., Hetherington, L., Baker, M. A., Aitken, R. J., and Rodger, J. C. (2004). A flow cytometric assay for global estimation of tyrosine phosphorylation associated with capacitation of spermatozoa from two marsupial species, the tammar wallaby (Marcropus eugenii) and the brushtail possum (Trichosurus vulpecula). Reproduction 127, 95–103.
| A flow cytometric assay for global estimation of tyrosine phosphorylation associated with capacitation of spermatozoa from two marsupial species, the tammar wallaby (Marcropus eugenii) and the brushtail possum (Trichosurus vulpecula).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvVOiurc%3D&md5=4f38703d0d3431164186a7f275acb4eaCAS | 15056774PubMed |
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 | 1:STN:280:DC%2BD3c%2FovFOgsw%3D%3D&md5=2580ceb08f7609f8f72f2017aa0535d4CAS | 10624605PubMed |
Urner, F., and Sakkas, D. (2003). Protein phosphorylation in mammalian spermatozoa. Reproduction 125, 17–26.
| Protein phosphorylation in mammalian spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhvFGls78%3D&md5=0acec5e91682e19c192b141cf0151b14CAS | 12622692PubMed |
Visconti, P. E., Bailey, J. L., Moore, G. D., Pan, D., Olds-Clarke, P., and Kopf, G. S. (1995). Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development 121, 1129–1137.
| 1:CAS:528:DyaK2MXltVamur8%3D&md5=e380ae62dc6412f0d981e7bfd0a88e74CAS | 7743926PubMed |
Visconti, P. E., Galantino-Homer, H., Ning, X., Moore, G. D., Valenzuela, J. P., Jorgez, C. J., Alvarez, J. G., and Kopf, G. S. (1999). Cholesterol efflux-mediated signal transduction in mammalian sperm. Beta-cyclodextrins initiate transmembrane signalling leading to an increase in protein tyrosine phosphorylation and capacitation. J. Biol. Chem. 274, 3235–3242.
| Cholesterol efflux-mediated signal transduction in mammalian sperm. Beta-cyclodextrins initiate transmembrane signalling leading to an increase in protein tyrosine phosphorylation and capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXpsVCisQ%3D%3D&md5=88fc7889489daad6350bbe63ebfccf98CAS | 9915865PubMed |
Wang, W. H., Abeydeera, L. R., Fraser, L. R., and Niwa, K. (1995). Functional analysis using chlortetracycline fluorescence and in vitro fertilisation of frozen–thawed ejaculated boar spermatozoa incubated in a protein-free chemically defined medium. J. Reprod. Fertil. 104, 305–313.
| Functional analysis using chlortetracycline fluorescence and in vitro fertilisation of frozen–thawed ejaculated boar spermatozoa incubated in a protein-free chemically defined medium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXntlCjs7g%3D&md5=c28ba75d62f460e9cc69a0878fd56543CAS | 7473423PubMed |
Watson, P. F. (2000). The causes of reduced fertility with cryopreserved semen. Anim. Reprod. Sci. 60–61, 481–492.
| The causes of reduced fertility with cryopreserved semen.Crossref | GoogleScholarGoogle Scholar | 10844218PubMed |
Whitfield, C. H., and Parkinson, T. J. (1992). Relationship between fertility of bovine semen and in vitro induction of acrosome reactions by heparin. Theriogenology 38, 11–20.
| Relationship between fertility of bovine semen and in vitro induction of acrosome reactions by heparin.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvFyktQ%3D%3D&md5=9d01debaed864aa2837b091b936d1adcCAS | 16727114PubMed |
