Leptin and leptin receptor are detectable in equine spermatozoa but are not involved in in vitro fertilisation
Anna Lange-Consiglio A , Bruna Corradetti B , Claudia Perrini A , Davide Bizzaro B and Fausto Cremonesi A C D
+ Author Affiliations
- Author Affiliations
A Large Animal Hospital, Reproduction Unit, Università degli Studi di Milano, Via dell’Università 6, 26900 Lodi, Italy.
B Department of Life and Environmental Sciences, Università Politecnica delle Marche, Via Brecce Bianche, 60131 Ancona, Italy.
C Department of Veterinary Science for Animal Health, Production and Food Safety, Università degli Studi di Milano, Via Celoria, 20133 Milano, Italy.
D Corresponding author. Email: fausto.cremonesi@unimi.it
Reproduction, Fertility and Development 28(5) 574-585 https://doi.org/10.1071/RD14130
Submitted: 12 April 2014 Accepted: 15 August 2014 Published: 13 October 2014
Abstract
In human and swine, leptin (OB) has been identified in seminal plasma and leptin receptors (OB-R) on the cell surface of spermatozoa, indicating that spermatozoa are a target for OB. This hormone has also been detected in follicular fluid (FF) in women and mares, although its role requires further study. The aims of this study were to investigate the immunolocalisation and the expression of OB and OB-R in equine spermatozoa and to evaluate the involvement of OB in equine in vitro fertilisation (IVF). Since progesterone (P) and OB are both found in FF, the individual and combined effects of these two hormones were studied in equine IVF and compared with the results obtained from the use of FF for in vitro sperm preparation. For the first time, we were able to identify OB and OB-R mRNA and their corresponding proteins in equine spermatozoa. When spermatozoa were treated with OB, there was a decrease in the three motility parameters VSL, STR and LIN, commonly associated with hyperactivation, whilst the acrosome reaction rate increased (P < 0.05). The fertilisation rate was 51% with FF, 46.15% with P, 43.64% with P+OB and 0% with OB alone. The percentage of eight-cell stage embryos was 18.7% with FF, 17.1% with P and 16.7% with OB+P. OB alone did not permit oocyte fertilisation, indicating that, in the horse, OB is involved in capacitation and hyperactivation but not in sperm penetration.
Additional keywords: follicular fluid, horse, hyperactivation, immunocytochemistry, progesterone.
References
Abavisani, A., Baghbanzadeh, A., Shayan, P., and Dehghani, H. (2011). Leptin mRNA in bovine spermatozoa. Res. Vet. Sci. 90, 439–442.| Leptin mRNA in bovine spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsVCiurk%3D&md5=c53a6dff9f24646bd53c88388ba2029eCAS | 20728190PubMed |
Anckaert, E., Mees, M., Schiettecatte, J., and Smitz, J. (2002). Clinical validation of a fully automated 17beta-oestradiol and progesterone assay (VIDAS) for use in monitoring assisted reproduction treatment. Clin. Chem. Lab. Med. 40, 824–831.
| Clinical validation of a fully automated 17beta-oestradiol and progesterone assay (VIDAS) for use in monitoring assisted reproduction treatment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XosFynsrw%3D&md5=dca40e24646a2999902a27ce91c51aa2CAS | 12392313PubMed |
Aquila, S., Gentile, M., Middea, E., Catalano, S., and Andò, S. (2005a). Autocrine regulation of insulin secretion in human ejaculated spermatozoa. Endocrinology 146, 552–557.
| Autocrine regulation of insulin secretion in human ejaculated spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXotlWjtQ%3D%3D&md5=b425519fb402d3f2f59f1a44acfd415cCAS | 15550513PubMed |
Aquila, S., Gentile, M., Middea, E., Catalano, S., Morelli, C., Pezzi, V., and Andò, S. (2005b). Leptin secretion by human ejaculated spermatozoa. J. Clin. Endocrinol. Metab. 90, 4753–4761.
| Leptin secretion by human ejaculated spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXnvVWksro%3D&md5=54a6a31b05c361ce51cd97102c9fdf52CAS | 15944217PubMed |
Aquila, S., Rago, V., Guido, C., Casaburi, I., Zupo, S., and Carpino, A. (2008). Leptin and leptin receptor in pig spermatozoa: evidence of their involvement in sperm capacitation and survival. Reproduction 136, 23–32.
| Leptin and leptin receptor in pig spermatozoa: evidence of their involvement in sperm capacitation and survival.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovVSgu7s%3D&md5=f58ce7d9649e643d7ceaa05ab307230cCAS | 18367502PubMed |
Baldi, E., Luconi, M., Bonaccorsi, L., and Forti, G. (1998). Non-genomic effects of progesterone on spermatozoa: mechanisms of signal transduction and clinical implications. Front. Biosci. 3, D1051–D1059.
| 1:CAS:528:DyaK1cXntlKgsr4%3D&md5=8eb4d86d1175719a61ef296e3769288cCAS | 9792892PubMed |
Baumber, J., and Meyers, S. A. (2006). Hyperactivated motility in rhesus macaque (Macaca mulatta) spermatozoa. J. Androl. 27, 459–468.
| Hyperactivated motility in rhesus macaque (Macaca mulatta) spermatozoa.Crossref | GoogleScholarGoogle Scholar | 16339455PubMed |
Bezard, J. (1992). In vitro fertilization in the mare. In ‘Proceedings of the International Scientific Conference on Biotechnics in Horse Reproduction, Cracow, Poland. p. 12. (Agricultural University of Cracow: Cracow.) [Abstract]
Blackmore, P. F., Beebe, S. J., Danforth, D. R., and Alexander, N. (1990). Progesterone and 17 alpha-hydroxyprogesterone. Novel stimulators of calcium influx in human sperm. J. Biol. Chem. 265, 1376–1380.
| 1:CAS:528:DyaK3cXpt1SitA%3D%3D&md5=61ee046ba1b0f1d79660b33e59e118b2CAS | 2104840PubMed |
Brewis, I. A., Morton, I. E., Moore, H. D., and England, G. C. (2001). Solubilized zona pellucida proteins and progesterone induce calcium influx and the acrosome reaction in capacitated dog spermatozoa. Mol. Reprod. Dev. 60, 491–497.
| Solubilized zona pellucida proteins and progesterone induce calcium influx and the acrosome reaction in capacitated dog spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXosl2qt7w%3D&md5=d2cb453b4aedadbe0963173e30799802CAS | 11746960PubMed |
Chehab, F. F., Lim, M. E., and Lu, R. (1996). Correction of the sterility defect in homozygous obese female mice by treatment with human recombinant leptin. Nat. Genet. 12, 318–320.
| Correction of the sterility defect in homozygous obese female mice by treatment with human recombinant leptin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhvVSgtb0%3D&md5=f3674f52ae07dad9c034d1837cc21ab4CAS | 8589726PubMed |
Cheng, F. P., Fazeli, A. R., Voorhout, W. F., Marks, A., Bevers, M. M., and Colenbrander, B. (1996). Use of peanut agglutinin to assess the acrosomal status and the zona pellucida-induced acrosome reaction in stallion spermatozoa. J. Androl. 17, 674–682.
| 1:STN:280:DyaK2s7mvVyjtw%3D%3D&md5=bbdfbebe4f7287f3da5ce29c144647f0CAS | 9016398PubMed |
Cheng, F. P., Fazeli, A. R., Voorhout, W. F., Tremoleda, J. L., Bevers, M. M., and Colenbrander, B. (1998). Progesterone in mare follicular fluid induces the acrosome reaction in stallion spermatozoa and enhances in vitro binding to the zona pellucida. Int. J. Androl. 21, 57–66.
| Progesterone in mare follicular fluid induces the acrosome reaction in stallion spermatozoa and enhances in vitro binding to the zona pellucida.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXksVOksLw%3D&md5=c065a030045681199d5628a7074d6841CAS | 9675614PubMed |
Das, P. J., Paria, N., Gustafson-Seabury, A., Vishnoi, M., Chaki, S. P., Love, C. C., Varner, D. D., Chowdhary, B. P., and Raudsepp, T. (2010). Total RNA isolation from stallion sperm and testis biopsies. Theriogenology 74, 1099–1106.
| Total RNA isolation from stallion sperm and testis biopsies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFWqtLbN&md5=8968aed856f0d3edb074e8f619c29fa1CAS | 20615536PubMed |
De Ambrogi, M., Spinaci, M., Galeati, G., and Tamanini, C. (2007). Leptin receptor in boar spermatozoa. Int. J. Androl. 30, 458–461.
| 1:CAS:528:DC%2BD2sXht1Oqu7vI&md5=b944fb14fa6a6acfbfc1fae11257bb57CAS | 17355241PubMed |
De Placido, G., Alviggi, C., Clarizia, R., Mollo, A., Alviggi, E., Strina, I., Fiore, E., Wilding, M., Pagano, T., and Matarese, G. (2006). Intra-follicular leptin concentration as a predictive factor for in vitro oocyte fertilisation in assisted reproductive techniques. J. Endocrinol. Invest. 29, 719–726.
| Intra-follicular leptin concentration as a predictive factor for in vitro oocyte fertilisation in assisted reproductive techniques.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlajsbnF&md5=e6768ea9cd168e6a1c22b3c70f6d6d85CAS | 17033261PubMed |
Dell’Aquila, M. E., Albrizio, M., Maritato, F., Minoia, P., and Hinrichs, K. (2003). Meiotic competence of equine oocytes and pronucleus formation after intracytoplasmic sperm injection (ICSI) as related to granulosa cell apoptosis. Biol. Reprod. 68, 2065–2072.
| Meiotic competence of equine oocytes and pronucleus formation after intracytoplasmic sperm injection (ICSI) as related to granulosa cell apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXks1GgsL8%3D&md5=42b1cb393427cbc61c4b1c5894553aafCAS | 12606481PubMed |
Ellington, J. E., Ball, B. A., and Yang, X. (1993). Binding of stallion spermatozoa to the equine zona pellucida after co-culture with oviductal epithelial cells. J. Reprod. Fertil. 98, 203–208.
| Binding of stallion spermatozoa to the equine zona pellucida after co-culture with oviductal epithelial cells.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3szkslWluw%3D%3D&md5=910b9444de13273c793fed0fd05f4062CAS | 7688425PubMed |
Emiliozzi, C., Cordonier, H., Guérin, J. F., Ciapa, B., Benchaïb, M., and Fénichel, P. (1996). Effects of progesterone on human spermatozoa prepared for in vitro fertilisation. Int. J. Androl. 19, 39–47.
| Effects of progesterone on human spermatozoa prepared for in vitro fertilisation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XisFOqs78%3D&md5=e49d8c168cefbfb51ae548de6523d1f7CAS | 8698537PubMed |
Flesch, F. M., Colenbrander, B., van Golde, L. M., and Gadella, B. M. (1999). Capacitation induces tyrosine phosphorylation of proteins in the boar sperm plasma membrane. Biochem. Biophys. Res. Commun. 262, 787–792.
| Capacitation induces tyrosine phosphorylation of proteins in the boar sperm plasma membrane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlsFyhu70%3D&md5=a564e9fd1be1141581fc8bb2acf7a8e8CAS | 10471403PubMed |
Foresta, C., Rossato, M., Mioni, R., and Zorzi, M. (1992). Progesterone induces capacitation in human spermatozoa. Andrologia 24, 33–35.
| Progesterone induces capacitation in human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xkt1Slu7c%3D&md5=b414dcc28da37f8daa81070347b49817CAS | 1519774PubMed |
Galantino-Homer, H. L., Visconti, P. E., and Kopf, G. S. (1997). Regulation of protein tyrosine phosphorylation during bovine sperm capacitation by a cyclic adenosine 3′,5′-monophosphate-dependent pathway. Biol. Reprod. 56, 707–719.
| Regulation of protein tyrosine phosphorylation during bovine sperm capacitation by a cyclic adenosine 3′,5′-monophosphate-dependent pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXht1GhtLg%3D&md5=4c4a25672372913e197c5a84a9b22e84CAS | 9047017PubMed |
González-Fernández, L., Macıas-Garcıa, B., Loux, S. C., Varner, D. D., and Hinrichs, K. (2013). Focal adhesion kinases and calcium/calmodulin-dependent protein kinases regulate protein tyrosine phosphorylation in stallion sperm. Biol. Reprod. 88, 138.
| Focal adhesion kinases and calcium/calmodulin-dependent protein kinases regulate protein tyrosine phosphorylation in stallion sperm.Crossref | GoogleScholarGoogle Scholar | 23595906PubMed |
Graham, J. K. (1996). Methods for induction of capacitation and the acrosome reaction of stallion spermatozoa. Vet. Clin. North Am. Equine Pract. 12, 111–117.
| 1:STN:280:DyaK283psVyktg%3D%3D&md5=75c5dfbe9f697d4d74c7dbb8ee6d785fCAS | 8726453PubMed |
Gregoraszczuk, E. L., Ptak, A., Wojtowicz, A. K., Gorska, T., and Nowak, K. W. (2004). Oestrus cycle-dependent action of leptin on basal and GH or IGF-I stimulated steroid secretion by whole porcine follicles. Endocr. Regul. 38, 15–21.
| 1:CAS:528:DC%2BD2cXhtVOhtbzM&md5=b071209844adeef886dd062469d2908cCAS | 15147234PubMed |
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=c170ebbf693815c45439f09dc4ee143bCAS | 16026427PubMed |
Ho, H. C., and Suarez, S. S. (2001). An inositol 1,4,5-trisphosphate receptor-gated intracellular Ca2+ store is involved in regulating sperm hyperactivated motility. Biol. Reprod. 65, 1606–1615.
| An inositol 1,4,5-trisphosphate receptor-gated intracellular Ca2+ store is involved in regulating sperm hyperactivated motility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvVersb0%3D&md5=f1af26ab08dcc4076f92209070d112f1CAS | 11673282PubMed |
Holmquist, L. (1982). Surface modification of Beckman Ultra-Clear centrifuge tubes for density gradient centrifugation of lipoproteins. J. Lipid Res. 23, 1249–1250.
| 1:STN:280:DyaL3s%2FosVCnsA%3D%3D&md5=c111a6800254136aa4555d3ed76c9228CAS | 7175383PubMed |
Jope, T., Lammert, A., Kratzsch, J., Paasch, U., and Glander, H. J. (2003). Leptin and leptin receptor in human seminal plasma and in human spermatozoa. Int. J. Androl. 26, 335–341.
| Leptin and leptin receptor in human seminal plasma and in human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXis12jtQ%3D%3D&md5=947f65486ab2eb5c7c4b67d45c9918cbCAS | 14636218PubMed |
Kaláb, P., Pĕknicová, J., Geussová, 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 | 9771651PubMed |
Kirkman-Brown, J. C., Punt, E. L., Barratt, C. L., and Publicover, S. J. (2002). Zona pellucida and progesterone-induced Ca21 signalling and acrosome reaction in human spermatozoa. J. Androl. 23, 306–315.
| 1:CAS:528:DC%2BD38XjvVKmt7g%3D&md5=fd19ab16a777a1727b156bb630936815CAS | 12002428PubMed |
Lackey, B. R., Gray, S. L., and Henricks, D. M. (2002). Measurement of leptin and insulin-like growth factor-I in seminal plasma from different species. Physiol. Res. 51, 309–311.
| 1:CAS:528:DC%2BD38XnsFGlsLY%3D&md5=390eea3bc0f5801b4d2c809125883099CAS | 12234124PubMed |
Lampiao, F., and du Plessis, S. S. (2008). Insulin and leptin enhance human sperm motility, acrosome reaction and nitric oxide production. Asian J. Androl. 10, 799–807.
| Insulin and leptin enhance human sperm motility, acrosome reaction and nitric oxide production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWhtrbM&md5=74db2bf691091d85f86e2944800dd526CAS | 18645684PubMed |
Lange Consiglio, A., Dell’Aquila, M. E., Fiandanese, N., Ambruosi, B., Cho, Y. S., Bosi, G., Arrighi, S., Lacalandra, G. M., and Cremonesi, F. (2009). Effects of leptin on in vitro maturation, fertilisation and embryonic cleavage after ICSI and early developmental expression of leptin (Ob) and leptin receptor (ObR) proteins in the horse. Reprod. Biol. Endocrinol. 7, 113.
| Effects of leptin on in vitro maturation, fertilisation and embryonic cleavage after ICSI and early developmental expression of leptin (Ob) and leptin receptor (ObR) proteins in the horse.Crossref | GoogleScholarGoogle Scholar | 19835605PubMed |
Lange-Consiglio, A., Arrighi, S., Fiandanese, N., Pocar, P., Aralla, M., Bosi, G., Borromeo, V., Berrini, A., Meucci, A., Dell’aquila, M. E., and Cremonesi, F. (2013). Follicular fluid leptin concentrations and expression of leptin and leptin receptor in the equine ovary and in vitro-matured oocyte with reference to pubertal development and breeds. Reprod. Fertil. Dev. 25, 837–846.
| Follicular fluid leptin concentrations and expression of leptin and leptin receptor in the equine ovary and in vitro-matured oocyte with reference to pubertal development and breeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXptVOqtLg%3D&md5=dfdec8d786ff3256a80911ca3855370fCAS | 22951190PubMed |
Leclerc, P., de Lamirande, E., and Gagnon, C. (1996). Cyclic adenosine 3′,5′monophosphate-dependent regulation of protein tyrosine phosphorylation in relation to human sperm capacitation and motility. Biol. Reprod. 55, 684–692.
| Cyclic adenosine 3′,5′monophosphate-dependent regulation of protein tyrosine phosphorylation in relation to human sperm capacitation and motility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XltlKgur4%3D&md5=1cf568ae70ea7a1399f06ba238c5eed0CAS | 8862788PubMed |
Li, H. W., Chiu, P. C., Cheung, M. P., Yeung, W. S., and O, W. S. (2009). Effect of leptin on motility, capacitation and acrosome reaction of human spermatozoa. Int. J. Androl. 32, 687–694.
| Effect of leptin on motility, capacitation and acrosome reaction of human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFOqt7jN&md5=82fe0f2628f854a1d758c618c3957875CAS | 19076257PubMed |
Llanos, M. N., and Anabalón, M. C. (1996). Studies related to progesterone-induced hamster sperm acrosome reaction. Mol. Reprod. Dev. 45, 313–319.
| Studies related to progesterone-induced hamster sperm acrosome reaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmslWlurY%3D&md5=57b4784b1239cbc9e77bcfd895eb20afCAS | 8916042PubMed |
Luconi, M., Bonaccorsi, L., Krausz, C., Gervasi, G., Forti, G., and Baldi, E. (1995). Stimulation of protein tyrosine phosphorylation by platelet-activating factor and progesterone in human spermatozoa. Mol. Cell. Endocrinol. 108, 35–42.
| Stimulation of protein tyrosine phosphorylation by platelet-activating factor and progesterone in human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjvVelsLY%3D&md5=63e601d4986031e5ac43a95724da8085CAS | 7758838PubMed |
Marquez, B., and Suarez, S. S. (2004). Different signalling pathways in bovine sperm regulate capacitation and hyperactivation. Biol. Reprod. 70, 1626–1633.
| Different signalling pathways in bovine sperm regulate capacitation and hyperactivation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktlOmtr4%3D&md5=5ef4ffa7e15d73eec1226dcae5bca5faCAS | 14766720PubMed |
Marquez, B., and Suarez, S. S. (2007). Bovine sperm hyperactivation is promoted by alkaline-stimulated Ca2+ influx. Biol. Reprod. 76, 660–665.
| Bovine sperm hyperactivation is promoted by alkaline-stimulated Ca2+ influx.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsFCmsr8%3D&md5=403e7afaf6ceb264da19350608cb4553CAS | 17182893PubMed |
Marquez, B., Ignotz, G., and Suarez, S. S. (2007). Contributions of extracellular and intracellular Ca2+ to regulation of sperm motility: release of intracellular stores can hyperactivate CatSper1 and CatSper2 null sperm. Dev. Biol. 303, 214–221.
| Contributions of extracellular and intracellular Ca2+ to regulation of sperm motility: release of intracellular stores can hyperactivate CatSper1 and CatSper2 null sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhvVGgsbw%3D&md5=971c7a68ac7abfb52e4f922950800dfcCAS | 17174296PubMed |
McPartlin, L. A., Suarez, S. S., Czaya, C. A., Hinrichs, K., and Bedford-Guaus, S. J. (2009). Hyperactivation of stallion sperm is required for successful in vitro fertilisation of equine oocytes. Biol. Reprod. 81, 199–206.
| Hyperactivation of stallion sperm is required for successful in vitro fertilisation of equine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnslaqs7w%3D&md5=97c3408edb0c074f47fc18a40ce5d80eCAS | 19208544PubMed |
Meizel, S. (1997). Amino acid neurotransmitter receptor/chloride channels of mammalian sperm and the acrosome reaction. Biol. Reprod. 56, 569–574.
| Amino acid neurotransmitter receptor/chloride channels of mammalian sperm and the acrosome reaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXht1Cltrs%3D&md5=420240d82405fb2e920b7c66abc6dc10CAS | 9046998PubMed |
Meizel, S., and Turner, K. O. (1991). Progesterone acts at the plasma membrane of human sperm. Mol. Cell. Endocrinol. 77, R1–R5.
| Progesterone acts at the plasma membrane of human sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXksVahs7k%3D&md5=a6cc1b94c44e4cabfcf34ed0740f5082CAS | 1815993PubMed |
Melendrez, C. S., Meizel, S., and Berger, T. (1994). Comparison of the ability of progesterone and heat-solubilised porcine zona pellucida to initiate the porcine sperm acrosome reaction in vitro. Mol. Reprod. Dev. 39, 433–438.
| Comparison of the ability of progesterone and heat-solubilised porcine zona pellucida to initiate the porcine sperm acrosome reaction in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXisFWjt78%3D&md5=eca98e25f6830cc214e22ad351bc0a5cCAS | 7893492PubMed |
Meyers, S. A., Overstreet, J. W., Liu, I. K., and Drobnis, E. Z. (1995). Capacitation in vitro of stallion spermatozoa: comparison of progesterone-induced acrosome reactions in fertile and subfertile males. J. Androl. 16, 47–54.
| 1:CAS:528:DyaK2MXkvF2ltb8%3D&md5=f1465606772197c127d688250c76e5afCAS | 7768752PubMed |
Meyers, S. A., Liu, I. K., Overstreet, J. W., Vadas, S., and Drobnis, E. Z. (1996). Zona pellucida binding and zona-induced acrosome reactions in horse spermatozoa: comparisons between fertile and subfertile stallions. Theriogenology 46, 1277–1288.
| Zona pellucida binding and zona-induced acrosome reactions in horse spermatozoa: comparisons between fertile and subfertile stallions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVOntw%3D%3D&md5=5e71e678067f42a941619c77a33f2671CAS | 16727991PubMed |
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=8ec60dc57f482bfdaead162cc9c915d1CAS | 2384341PubMed |
Murase, T., and Roldan, E. R. (1996). Progesterone and the zona pellucida activate different transducing pathways in the sequence of events leading to diacylglycerol generation during mouse sperm acrosomal exocytosis. Biochem. J. 320, 1017–1023.
| 1:CAS:528:DyaK2sXislamsA%3D%3D&md5=858dac811bd759efd2f9fe2b935b5816CAS | 9003394PubMed |
Palmer, E., Bézard, J., Magistrini, M., and Duchamp, G. (1991). In vitro fertilisation in the horse. A retrospective study. J. Reprod. Fertil. Suppl. 44, 375–384.
| 1:STN:280:DyaK387nslantg%3D%3D&md5=3958b9bd12612c281c19030ed7d475f9CAS | 1795281PubMed |
Roldan, E. R., Murase, T., and Shi, Q. X. (1994). Exocytosis in spermatozoa in response to progesterone and zona pellucida. Science 266, 1578–1581.
| Exocytosis in spermatozoa in response to progesterone and zona pellucida.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXisVGlsrY%3D&md5=ade3e83421d94fc613bf6a3187ccfc0eCAS | 7985030PubMed |
Somanath, P. R., Suraj, K., and Gandhi, K. K. (2000). Caprine sperm acrosome reaction: promotion by progesterone and homologous zona pellucida. Small Rumin. Res. 37, 279–286.
| Caprine sperm acrosome reaction: promotion by progesterone and homologous zona pellucida.Crossref | GoogleScholarGoogle Scholar | 10867326PubMed |
Suarez, S. S., Dai, X. B., DeMott, R. P., Redfern, K., and Mirando, M. A. (1992). Movement characteristics of boar sperm obtained from the oviduct or hyperactivated in vitro. J. Androl. 13, 75–80.
| 1:STN:280:DyaK383gt1Skug%3D%3D&md5=cdcc33de83b7435a0e075b2041735584CAS | 1551808PubMed |
Tardif, S., Dubé, C., and Bailey, J. L. (2003). Porcine sperm capacitation and tyrosine kinase activity are dependent on bicarbonate and calcium but protein tyrosine phosphorylation is only associated with calcium. Biol. Reprod. 68, 207–213.
| Porcine sperm capacitation and tyrosine kinase activity are dependent on bicarbonate and calcium but protein tyrosine phosphorylation is only associated with calcium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtFSl&md5=db9d6df4bf01462b26728400a0384892CAS | 12493715PubMed |
Tesarik, J., Moos, J., and Mendoza, C. (1993). Stimulation of protein tyrosine phosphorylation by a progesterone receptor on the cell surface of human sperm. Endocrinology 133, 328–335.
| 1:CAS:528:DyaK3sXlsFagsLk%3D&md5=d2443f3b7479e00d4837ec0c457ab54dCAS | 7686481PubMed |
Thérien, I., and Manjunath, P. (2003). Effect of progesterone on bovine sperm capacitation and acrosome reaction. Biol. Reprod. 69, 1408–1415.
| Effect of progesterone on bovine sperm capacitation and acrosome reaction.Crossref | GoogleScholarGoogle Scholar | 12826580PubMed |
Thomas, T. (2004). The complex effects of leptin on bone metabolism through multiple pathways. Curr. Opin. Pharmacol. 4, 295–300.
| The complex effects of leptin on bone metabolism through multiple pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktVKqsrc%3D&md5=99cd2f91a78d903ed9b3d0fdd70b2d71CAS | 15140423PubMed |
Travis, A. J., Tutuncu, L., Jorgez, C. J., Ord, T. S., Jones, B. H., Kopf, G. S., and Williams, C. J. (2004). Requirements for glucose beyond sperm capacitation during in vitro fertilisation in the mouse. Biol. Reprod. 71, 139–145.
| Requirements for glucose beyond sperm capacitation during in vitro fertilisation in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltFKktbk%3D&md5=2c37da6efa7d4e1dbc460a827888f19fCAS | 14985248PubMed |
Uhler, M. L., Leung, A., Chan, S. Y., and Wang, C. (1992). Direct effects of progesterone and antiprogesterone on human sperm hyperactivated motility and acrosome reaction. Fertil. Steril. 58, 1191–1198.
| 1:STN:280:DyaK3s%2FptlWqtg%3D%3D&md5=8a41a1dc0f0dd70d56a1b8a1d64b125cCAS | 1459270PubMed |
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=3a5e557f6d8bdd8835209e76a978c08cCAS | 7743926PubMed |
Zhang, Y., Proenca, R., Maffei, M., Barone, M., Leopold, L., and Friedman, J. M. (1994). Positional cloning of the mouse obese gene and its human homologue. Nature 372, 425–432.
| Positional cloning of the mouse obese gene and its human homologue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXisVGqsbs%3D&md5=6eb0692a692c62e8d30630babcf18d83CAS | 7984236PubMed |
