Progesterone induces the release of bull spermatozoa from oviductal epithelial cells
J. Romero-Aguirregomezcorta
A , S. Cronin A , E. Donnellan A and S. Fair A B
+ 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, Limerick, V94 PH61, Ireland.
B Corresponding author. Email: sean.fair@ul.ie
Reproduction, Fertility and Development 31(9) 1463-1472 https://doi.org/10.1071/RD18316
Submitted: 11 August 2018 Accepted: 3 March 2019 Published: 29 April 2019
Abstract
The mechanism that causes the detachment of spermatozoa from the oviductal reservoir around the time of ovulation remains to be elucidated. Because the cumulus cells of the bovine oocyte are known to secrete progesterone (P4), and P4 has been shown to act upon cation channels of spermatozoa (CatSper) in human spermatozoa, it was hypothesised that P4 could induce hyperactivation due to an influx of extracellular calcium, and this would facilitate detachment of spermatozoa from oviductal epithelial cells. Therefore, this study aimed to investigate the role and mechanism of action of P4 in the release of spermatozoa from bovine oviduct epithelial cells (BOEC). Initial dose–response assessments on sperm hyperactivation determined the optimum concentration of P4 (10 nM), mibefradil (a non-specific Ca2+ channel antagonist; 5 µM), NNC 55-0396 dihydrochloride (NNC; a CatSper antagonist; 2 µM), mifepristone (a classical and membrane P4 receptor antagonist; 400 nM) and AG205 (a membrane P4 receptor antagonist; 10 μM). BOEC explants were incubated with frozen–thawed bovine spermatozoa for 30 min, following which loosely bound spermatozoa were removed. Two experiments were completed. In Experiment 1, BOECs were treated for 30 min with either no treatment, P4, NNC, mibefradil, P4 + mibefradil, P4 + NNC, P4 + mibefradil + NNC or P4 + EGTA. In Experiment 2, BOECs were treated for 30 min with either no treatment, P4, mifepristone, AG205, mifepristone + AG205, P4 + mifepristone, P4 + AG205 or P4 + mifepristone + AG205. The number of spermatozoa remaining bound per millimetre squared of BOEC explant was determined. Progesterone stimulated the release of bound spermatozoa from BOEC explants, whereas NNC, mibefradil and EGTA inhibited this release. The release of spermatozoa by P4 was inhibited in the presence of both mifepristone and AG205, whereas the combination of both had the greatest inhibitory action on P4 release of spermatozoa. These findings suggest the presence of a P4 membrane receptor on bovine spermatozoa and that P4-induced release of spermatozoa from BOECs is likely mediated by extracellular Ca2+.
Additional keywords: membrane progesterone receptor, oviduct, progesterone receptor membrane component 1 (PGRMC1), unbinding.
References
Alasmari, W., Costello, S., Correia, J., Oxenham, S. K., Morris, J., Fernandes, L., Ramalho-Santos, J., Kirkman-Brown, J., Michelangeli, F., Publicover, S., and Barratt, C. L. (2013). Ca2+ signals generated by CatSper and Ca2+ stores regulate different behaviors in human sperm. J. Biol. Chem. 288, 6248–6258.| Ca2+ signals generated by CatSper and Ca2+ stores regulate different behaviors in human sperm.Crossref | GoogleScholarGoogle Scholar | 23344959PubMed |
Baldi, E., Luconi, M., Muratori, M., Marchiani, S., Tamburrino, L., and Forti, G. (2009). Nongenomic activation of spermatozoa by steroid hormones: facts and fictions. Mol. Cell. Endocrinol. 308, 39–46.
| Nongenomic activation of spermatozoa by steroid hormones: facts and fictions.Crossref | GoogleScholarGoogle Scholar | 19549590PubMed |
Blackmore, P. F., Neulen, J., Lattanzio, F., and Beebe, S. J. (1991). Cell surface-binding sites for progesterone mediate calcium uptake in human sperm. J. Biol. Chem. 266, 18655–18659.
| 1833399PubMed |
Bosch, P., de Avila, J. M., Ellington, J. E., and Wright, R. W. (2001). Heparin and Ca2+-free medium can enhance release of bull sperm attached to oviductal epithelial cell monolayers. Theriogenology 56, 247–260.
| Heparin and Ca2+-free medium can enhance release of bull sperm attached to oviductal epithelial cell monolayers.Crossref | GoogleScholarGoogle Scholar | 11480617PubMed |
Breitbart, H. (2002). Intracellular calcium regulation in sperm capacitation and acrosomal reaction. Mol. Cell. Endocrinol. 187, 139–144.
| Intracellular calcium regulation in sperm capacitation and acrosomal reaction.Crossref | GoogleScholarGoogle Scholar | 11988321PubMed |
Bronson, R. A., Peresleni, T., and Golightly, M. (1999). Progesterone promotes the acrosome reaction in capacitated human spermatozoa as judged by flow cytometry and CD46 staining. Mol. Hum. Reprod. 5, 507–512.
| Progesterone promotes the acrosome reaction in capacitated human spermatozoa as judged by flow cytometry and CD46 staining.Crossref | GoogleScholarGoogle Scholar | 10340996PubMed |
Bui, P. H., Quesada, A., Handforth, A., and Hankinson, O. (2008). The mibefradil derivative NNC55-0396, a specific T-type calcium channel antagonist, exhibits less CYP3A4 inhibition than mibefradil. Drug Metab. Dispos. 36, 1291–1299.
| The mibefradil derivative NNC55-0396, a specific T-type calcium channel antagonist, exhibits less CYP3A4 inhibition than mibefradil.Crossref | GoogleScholarGoogle Scholar | 18411403PubMed |
Carlson, A. E., Quill, T. A., Westenbroek, R. E., Schuh, S. M., Hille, B., and Babcock, D. F. (2005). Identical phenotypes of CatSper1 and CatSper2 null sperm. J. Biol. Chem. 280, 32238–32244.
| Identical phenotypes of CatSper1 and CatSper2 null sperm.Crossref | GoogleScholarGoogle Scholar | 16036917PubMed |
Chabbert-Buffet, N., Meduri, G., Bouchard, P., and Spitz, I. M. (2005). Selective progesterone receptor modulators and progesterone antagonists: mechanisms of action and clinical applications. Hum. Reprod. Update 11, 293–307.
| Selective progesterone receptor modulators and progesterone antagonists: mechanisms of action and clinical applications.Crossref | GoogleScholarGoogle Scholar | 15790602PubMed |
Chang, H., and Suarez, S. S. (2012). Unexpected flagellar movement patterns and epithelial binding behavior of mouse sperm in the oviduct. Biol. Reprod. 86, 140.
| Unexpected flagellar movement patterns and epithelial binding behavior of mouse sperm in the oviduct.Crossref | GoogleScholarGoogle Scholar | 22337334PubMed |
Chian, R. C., Lapointe, S., and Sirard, M. A. (1995). Capacitation in vitro of bovine spermatozoa by oviduct epithelial cell monolayer conditioned medium. Mol. Reprod. Dev. 42, 318–324.
| Capacitation in vitro of bovine spermatozoa by oviduct epithelial cell monolayer conditioned medium.Crossref | GoogleScholarGoogle Scholar | 8579846PubMed |
Chien, C. H., Lai, J. N., Liao, C. F., Wang, O. Y., Lu, L. M., Huang, M. I., Lee, W. F., Shie, M. C., and Chien, E. J. (2009). Mifepristone acts as progesterone antagonist of non-genomic responses but inhibits phytohemagglutinin-induced proliferation in human T cells. Hum. Reprod. 24, 1968–1975.
| Mifepristone acts as progesterone antagonist of non-genomic responses but inhibits phytohemagglutinin-induced proliferation in human T cells.Crossref | GoogleScholarGoogle Scholar | 19401324PubMed |
Costello, S., Michelangeli, F., Nash, K., Lefievre, L., Morris, J., Machado-Oliveira, G., Barratt, C., Kirkman-Brown, J., and Publicover, S. (2009). Ca2+-stores in sperm: their identities and functions. Reproduction 138, 425–437.
| Ca2+-stores in sperm: their identities and functions.Crossref | GoogleScholarGoogle Scholar | 19542252PubMed |
Curtis, M. P., Kirkman-Brown, J. C., Connolly, T. J., and Gaffney, E. A. (2012). Modelling a tethered mammalian sperm cell undergoing hyperactivation. J. Theor. Biol. 309, 1–10.
| Modelling a tethered mammalian sperm cell undergoing hyperactivation.Crossref | GoogleScholarGoogle Scholar | 22727894PubMed |
Darszon, A., Lopez-Martinez, P., Acevedo, J. J., Hernandez-Cruz, A., and Trevino, C. L. (2006). T-type Ca2+ channels in sperm function. Cell Calcium 40, 241–252.
| T-type Ca2+ channels in sperm function.Crossref | GoogleScholarGoogle Scholar | 16797697PubMed |
Demott, R. P., and Suarez, S. S. (1992). Hyperactivated sperm progress in the mouse oviduct. Biol. Reprod. 46, 779–785.
| Hyperactivated sperm progress in the mouse oviduct.Crossref | GoogleScholarGoogle Scholar | 1591334PubMed |
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 | 10231058PubMed |
Falkenstein, E., Heck, M., Gerdes, D., Grube, D., Christ, M., Weigel, M., Buddhikot, M., Meizel, S., and Wehling, M. (1999). Specific progesterone binding to a membrane protein and related nongenomic effects on Ca2+-fluxes in sperm. Endocrinology 140, 5999–6002.
| Specific progesterone binding to a membrane protein and related nongenomic effects on Ca2+-fluxes in sperm.Crossref | GoogleScholarGoogle Scholar | 10579369PubMed |
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 | 10084961PubMed |
Gadella, B. M., and Boerke, A. (2016). An update on post-ejaculatory remodeling of the sperm surface before mammalian fertilization. Theriogenology 85, 113–124.
| An update on post-ejaculatory remodeling of the sperm surface before mammalian fertilization.Crossref | GoogleScholarGoogle Scholar | 26320574PubMed |
Gil, P. I., Guidobaldi, H. A., Teves, M. E., Unates, D. R., Sanchez, R., and Giojalas, L. C. (2008). Chemotactic response of frozen–thawed bovine spermatozoa towards follicular fluid. Anim. Reprod. Sci. 108, 236–246.
| Chemotactic response of frozen–thawed bovine spermatozoa towards follicular fluid.Crossref | GoogleScholarGoogle Scholar | 17889460PubMed |
Green, C. E., Bredl, J., Holt, W. V., Watson, P. F., and Fazeli, A. (2001). Carbohydrate mediation of boar sperm binding to oviductal epithelial cells in vitro. Reproduction 122, 305–315.
| Carbohydrate mediation of boar sperm binding to oviductal epithelial cells in vitro.Crossref | GoogleScholarGoogle Scholar | 11467982PubMed |
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 | 10819780PubMed |
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 | 15615898PubMed |
Guo, M., Zhang, C., Wang, Y., Feng, L., Wang, Z., Niu, W., Du, X., Tang, W., Li, Y., Wang, C., and Chen, Z. (2016). Progesterone receptor membrane component 1 mediates progesterone-induced suppression of oocyte meiotic prophase i and primordial folliculogenesis. Sci. Rep. 6, 36869.
| Progesterone receptor membrane component 1 mediates progesterone-induced suppression of oocyte meiotic prophase i and primordial folliculogenesis.Crossref | GoogleScholarGoogle Scholar | 27848973PubMed |
Gwathmey, T. M., Ignotz, G. G., and Suarez, S. S. (2003). PDC-109 (BSP-A1/A2) promotes bull sperm binding to oviductal epithelium in vitro and may be involved in forming the oviductal sperm reservoir. Biol. Reprod. 69, 809–815.
| PDC-109 (BSP-A1/A2) promotes bull sperm binding to oviductal epithelium in vitro and may be involved in forming the oviductal sperm reservoir.Crossref | GoogleScholarGoogle Scholar | 12748117PubMed |
Harper, C. V., Barratt, C. L., and Publicover, S. J. (2004). Stimulation of human spermatozoa with progesterone gradients to simulate approach to the oocyte. Induction of [Ca2+]i oscillations and cyclical transitions in flagellar beating. J. Biol. Chem. 279, 46315–46325.
| Stimulation of human spermatozoa with progesterone gradients to simulate approach to the oocyte. Induction of [Ca2+]i oscillations and cyclical transitions in flagellar beating.Crossref | GoogleScholarGoogle Scholar | 15322137PubMed |
Ho, H. C., Granish, K. A., and Suarez, S. S. (2002). Hyperactivated motility of bull sperm is triggered at the axoneme by Ca2+ and not cAMP. Dev. Biol. 250, 208–217.
| Hyperactivated motility of bull sperm is triggered at the axoneme by Ca2+ and not cAMP.Crossref | GoogleScholarGoogle Scholar | 12297107PubMed |
Ho, K., Wolff, C. A., and Suarez, S. S. (2009). CatSper-null mutant spermatozoa are unable to ascend beyond the oviductal reservoir. Reprod. Fertil. Dev. 21, 345–350.
| CatSper-null mutant spermatozoa are unable to ascend beyond the oviductal reservoir.Crossref | GoogleScholarGoogle Scholar | 19210926PubMed |
Ignotz, G. G., Cho, M. Y., and Suarez, S. S. (2007). Annexins are candidate oviductal receptors for bovine sperm surface proteins and thus may serve to hold bovine sperm in the oviductal reservoir. Biol. Reprod. 77, 906–913.
| Annexins are candidate oviductal receptors for bovine sperm surface proteins and thus may serve to hold bovine sperm in the oviductal reservoir.Crossref | GoogleScholarGoogle Scholar | 17715429PubMed |
Ishijima, S. (2011). Dynamics of flagellar force generated by a hyperactivated spermatozoon. Reproduction 142, 409–415.
| Dynamics of flagellar force generated by a hyperactivated spermatozoon.Crossref | GoogleScholarGoogle Scholar | 21670125PubMed |
Johnson, G. P., English, A. M., Cronin, S., Hoey, D. A., Meade, K. G., and Fair, S. (2017). Genomic identification, expression profiling, and functional characterization of CatSper channels in the bovine. Biol. Reprod. 97, 302–312.
| Genomic identification, expression profiling, and functional characterization of CatSper channels in the bovine.Crossref | GoogleScholarGoogle Scholar | 29044427PubMed |
Kirkman-Brown, J. C., Punt, E. L., Barratt, C. L., and Publicover, S. J. (2002). Zona pellucida and progesterone-induced Ca2+ signaling and acrosome reaction in human spermatozoa. J. Androl. 23, 306–315.
| 12002428PubMed |
Kirkman-Brown, J. C., Barratt, C. L., and Publicover, S. J. (2004). Slow calcium oscillations in human spermatozoa. Biochem. J. 378, 827–832.
| Slow calcium oscillations in human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 14606954PubMed |
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 | 8835378PubMed |
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 | 8527509PubMed |
Lefebvre, R., Lo, M. C., and Suarez, S. S. (1997). Bovine sperm binding to oviductal epithelium involves fucose recognition. Biol. Reprod. 56, 1198–1204.
| Bovine sperm binding to oviductal epithelium involves fucose recognition.Crossref | GoogleScholarGoogle Scholar | 9160719PubMed |
Li, M., Hansen, J. B., Huang, L., Keyser, B. M., and Taylor, J. T. (2005). Towards selective antagonists of T-type calcium channels: design, characterization and potential applications of NNC 55–0396. Cardiovasc. Drug Rev. 23, 173–196.
| Towards selective antagonists of T-type calcium channels: design, characterization and potential applications of NNC 55–0396.Crossref | GoogleScholarGoogle Scholar | 16007233PubMed |
Lishko, P. V., and Kirichok, Y. (2010). The role of Hv1 and CatSper channels in sperm activation. J. Physiol. 588, 4667–4672.
| The role of Hv1 and CatSper channels in sperm activation.Crossref | GoogleScholarGoogle Scholar | 20679352PubMed |
Lishko, P. V., Botchkina, I. L., and Kirichok, Y. (2011). Progesterone activates the principal Ca2+ channel of human sperm. Nature 471, 387–391.
| Progesterone activates the principal Ca2+ channel of human sperm.Crossref | GoogleScholarGoogle Scholar | 21412339PubMed |
Lösel, R. M., Falkenstein, E., Feuring, M., Schultz, A., Tillmann, H. C., Rossol-Haseroth, K., and Wehling, M. (2003). Nongenomic steroid action: controversies, questions, and answers. Physiol. Rev. 83, 965–1016.
| Nongenomic steroid action: controversies, questions, and answers.Crossref | GoogleScholarGoogle Scholar | 12843413PubMed |
Lösel, R., Breiter, S., Seyfert, M., Wehling, M., and Falkenstein, E. (2005). Classic and non-classic progesterone receptors are both expressed in human spermatozoa. Horm. Metab. Res. 37, 10–14.
| Classic and non-classic progesterone receptors are both expressed in human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 15702432PubMed |
Loux, S. C., Crawford, K. R., Ing, N. H., Gonzalez-Fernandez, L., Macias-Garcia, B., Love, C. C., Varner, D. D., Velez, I. C., Choi, Y. H., and Hinrichs, K. (2013). CatSper and the relationship of hyperactivated motility to intracellular calcium and pH kinetics in equine sperm. Biol. Reprod. 89, 123.
| CatSper and the relationship of hyperactivated motility to intracellular calcium and pH kinetics in equine sperm.Crossref | GoogleScholarGoogle Scholar | 24048572PubMed |
Luconi, M., Bonaccorsi, L., Maggi, M., Pecchioli, P., Krausz, C., Forti, G., and Baldi, E. (1998). Identification and characterization of functional nongenomic progesterone receptors on human sperm membrane. J. Clin. Endocrinol. Metab. 83, 877–885.
| 9506743PubMed |
Lyons, A., Narciandi, F., Donnellan, E., Romero-Aguirregomezcorta, J., Farrelly, C. O., Lonergan, P., Meade, K. G., and Fair, S. (2018). Recombinant β-defensin 126 promotes bull sperm binding to bovine oviductal epithelia. Reprod. Fertil. Dev. 30, 1472–1481.
| Recombinant β-defensin 126 promotes bull sperm binding to bovine oviductal epithelia.Crossref | GoogleScholarGoogle Scholar |
Machado, S. A. (2013). Regulation of boar sperm function by the oviduct – formation of a sperm reservoir, modulation of Ca2+ influx, and release from storage. Ph.D. Thesis, University of Illinois at Urbana–Champaign.
Maller, J. L., and Krebs, E. G. (1977). Progesterone-stimulated meiotic cell division in Xenopus oocytes. Induction by regulatory subunit and inhibition by catalytic subunit of adenosine 3′:5′-monophosphate-dependent protein kinase. J. Biol. Chem. 252, 1712–1718.
| 190238PubMed |
Marquez, B., and Suarez, S. S. (2004). Different signaling pathways in bovine sperm regulate capacitation and hyperactivation. Biol. Reprod. 70, 1626–1633.
| Different signaling pathways in bovine sperm regulate capacitation and hyperactivation.Crossref | GoogleScholarGoogle Scholar | 14766720PubMed |
Miller, D. J. (2018). Review: the epic journey of sperm through the female reproductive tract. Animal 12, s110–s120.
| Review: the epic journey of sperm through the female reproductive tract.Crossref | GoogleScholarGoogle Scholar | 29551099PubMed |
Mingoti, G. Z., Garcia, J. M., and Rosa-e-Silva, A. A. (2002). Steroidogenesis in cumulus cells of bovine cumulus–oocyte-complexes matured in vitro with BSA and different concentrations of steroids. Anim. Reprod. Sci. 69, 175–186.
| Steroidogenesis in cumulus cells of bovine cumulus–oocyte-complexes matured in vitro with BSA and different concentrations of steroids.Crossref | GoogleScholarGoogle Scholar | 11812628PubMed |
Mir, S. U., Ahmed, I. S., Arnold, S., and Craven, R. J. (2012). Elevated progesterone receptor membrane component 1/sigma-2 receptor levels in lung tumors and plasma from lung cancer patients. Int. J. Cancer 131, E1–E9.
| Elevated progesterone receptor membrane component 1/sigma-2 receptor levels in lung tumors and plasma from lung cancer patients.Crossref | GoogleScholarGoogle Scholar | 21918976PubMed |
Mullins, M. E., Horowitz, B. Z., Linden, D. H., Smith, G. W., Norton, R. L., and Stump, J. (1998). Life-threatening interaction of mibefradil and beta-blockers with dihydropyridine calcium channel blockers. JAMA 280, 157–158.
| Life-threatening interaction of mibefradil and beta-blockers with dihydropyridine calcium channel blockers.Crossref | GoogleScholarGoogle Scholar | 9669789PubMed |
Peluso, J. J., Liu, X., Saunders, M. M., Claffey, K. P., and Phoenix, K. (2008). Regulation of ovarian cancer cell viability and sensitivity to cisplatin by progesterone receptor membrane component-1. J. Clin. Endocrinol. Metab. 93, 1592–1599.
| Regulation of ovarian cancer cell viability and sensitivity to cisplatin by progesterone receptor membrane component-1.Crossref | GoogleScholarGoogle Scholar | 18319313PubMed |
Pollard, J. W., Plante, C., King, W. A., Hansen, P. J., Betteridge, K. J., and Suarez, S. S. (1991). Fertilizing capacity of bovine sperm may be maintained by binding of oviductal epithelial cells. Biol. Reprod. 44, 102–107.
| Fertilizing capacity of bovine sperm may be maintained by binding of oviductal epithelial cells.Crossref | GoogleScholarGoogle Scholar | 2015341PubMed |
Publicover, S., Harper, C. V., and Barratt, C. (2007). [Ca2+]i signalling in sperm – making the most of what you’ve got. Nat. Cell Biol. 9, 235–242.
| [Ca2+]i signalling in sperm – making the most of what you’ve got.Crossref | GoogleScholarGoogle Scholar | 17330112PubMed |
Qi, H., Moran, M. M., Navarro, B., Chong, J. A., Krapivinsky, G., Krapivinsky, L., Kirichok, Y., Ramsey, I. S., Quill, T. A., and Clapham, D. E. (2007). All four CatSper ion channel proteins are required for male fertility and sperm cell hyperactivated motility. Proc. Natl Acad. Sci. USA 104, 1219–1223.
| All four CatSper ion channel proteins are required for male fertility and sperm cell hyperactivated motility.Crossref | GoogleScholarGoogle Scholar | 17227845PubMed |
Ren, D., Navarro, B., Perez, G., Jackson, A. C., Hsu, S., Shi, Q., Tilly, J. L., and Clapham, D. E. (2001). A sperm ion channel required for sperm motility and male fertility. Nature 413, 603–609.
| A sperm ion channel required for sperm motility and male fertility.Crossref | GoogleScholarGoogle Scholar | 11595941PubMed |
Singh, A. P., and Rajender, S. (2015). CatSper channel, sperm function and male fertility. Reprod. Biomed. Online 30, 28–38.
| CatSper channel, sperm function and male fertility.Crossref | GoogleScholarGoogle Scholar | 25457194PubMed |
Strünker, T., Goodwin, N., Brenker, C., Kashikar, N. D., Weyand, I., Seifert, R., and Kaupp, U. B. (2011). The CatSper channel mediates progesterone-induced Ca2+ influx in human sperm. Nature 471, 382–386.
| The CatSper channel mediates progesterone-induced Ca2+ influx in human sperm.Crossref | GoogleScholarGoogle Scholar | 21412338PubMed |
Sumigama, S., Mansell, S., Miller, M., Lishko, P. V., Cherr, G. N., Meyers, S. A., and Tollner, T. (2015). Progesterone accelerates the completion of sperm capacitation and activates CatSper channel in spermatozoa from the rhesus macaque. Biol. Reprod. 93, 130.
| Progesterone accelerates the completion of sperm capacitation and activates CatSper channel in spermatozoa from the rhesus macaque.Crossref | GoogleScholarGoogle Scholar | 26490839PubMed |
Tamburrino, L., Marchiani, S., Minetti, F., Forti, G., Muratori, M., and Baldi, E. (2014). The CatSper calcium channel in human sperm: relation with motility and involvement in progesterone-induced acrosome reaction. Hum. Reprod. 29, 418–428.
| The CatSper calcium channel in human sperm: relation with motility and involvement in progesterone-induced acrosome reaction.Crossref | GoogleScholarGoogle Scholar | 24430778PubMed |
Teves, M. E., Guidobaldi, H. A., Unates, D. R., Sanchez, R., Miska, W., Publicover, S. J., Morales Garcia, A. A., and Giojalas, L. C. (2009). Molecular mechanism for human sperm chemotaxis mediated by progesterone. PLoS One 4, e8211.
| Molecular mechanism for human sperm chemotaxis mediated by progesterone.Crossref | GoogleScholarGoogle Scholar | 19997608PubMed |
Thomas, P. (2008). Characteristics of membrane progestin receptor alpha (mPRalpha) and progesterone membrane receptor component 1 (PGMRC1) and their roles in mediating rapid progestin actions. Front. Neuroendocrinol. 29, 292–312.
| Characteristics of membrane progestin receptor alpha (mPRalpha) and progesterone membrane receptor component 1 (PGMRC1) and their roles in mediating rapid progestin actions.Crossref | GoogleScholarGoogle Scholar | 18343488PubMed |
Thomas, P., Tubbs, C., and Garry, V. F. (2009). Progestin functions in vertebrate gametes mediated by membrane progestin receptors (mPRs): identification of mPRalpha on human sperm and its association with sperm motility. Steroids 74, 614–621.
| Progestin functions in vertebrate gametes mediated by membrane progestin receptors (mPRs): identification of mPRalpha on human sperm and its association with sperm motility.Crossref | GoogleScholarGoogle Scholar | 19071147PubMed |
Vicente-Carrillo, A., Alvarez-Rodriguez, M., and Rodriguez-Martinez, H. (2017). The CatSper channel modulates boar sperm motility during capacitation. Reprod. Biol. 17, 69–78.
| The CatSper channel modulates boar sperm motility during capacitation.Crossref | GoogleScholarGoogle Scholar | 28077244PubMed |
Villanueva-Díaz, C., Arias-Martinez, J., Bermejo-Martinez, L., and Vadillo-Ortega, F. (1995). Progesterone induces human sperm chemotaxis. Fertil. Steril. 64, 1183–1188.
| Progesterone induces human sperm chemotaxis.Crossref | GoogleScholarGoogle Scholar | 7589674PubMed |
Yanagimachi, R. (1970). The movement of golden hamster spermatozoa before and after capacitation. J. Reprod. Fertil. 23, 193–196.
| The movement of golden hamster spermatozoa before and after capacitation.Crossref | GoogleScholarGoogle Scholar | 5472441PubMed |
Yanagimachi, R., and Chang, M. C. (1963). Sperm ascent through the oviduct of the hamster and rabbit in relation to the time of ovulation. J. Reprod. Fertil. 6, 413–420.
| Sperm ascent through the oviduct of the hamster and rabbit in relation to the time of ovulation.Crossref | GoogleScholarGoogle Scholar | 14086867PubMed |
