New evidence of melatonin receptor contribution to ram sperm functionality
Marta Gonzalez-Arto A , Carolina Luna A , Rosaura Pérez-Pé A , Teresa Muiño-Blanco A , José A. Cebrián-Pérez A and Adriana Casao A B
+ Author Affiliations
- Author Affiliations
A Grupo Biología y Fisiología de la Reproducción, Instituto de Investigación de Ciencias Ambientales de Aragón (IUCA), Departamento de Bioquímica y Biología Molecular y Celular, Facultad de Veterinaria, Universidad de Zaragoza, C/Miguel Servet, 177, 50013, Zaragoza, Spain.
B Corresponding author. Email: adriana@unizar.es
Reproduction, Fertility and Development 28(7) 924-935 https://doi.org/10.1071/RD14302
Submitted: 19 August 2014 Accepted: 30 October 2014 Published: 17 December 2014
Abstract
The present study analysed the involvement of melatonin, acting via its receptors (MT1 and MT2), in ram sperm functionality. Indirect immunofluorescence assays revealed no changes in the distribution or intensity of MT1 receptors, whereas different subpopulations were established for MT2 receptors in control, in vitro capacitated and acrosome-reacted ram spermatozoa. Chlortetracycline staining revealed the following correlations between the pattern of staining for MT2 receptors in: (1) non-capacitated (NC) sperm rate and the proportion of spermatozoa with equal immunostaining intensity in the acrosome and post-acrosome (r = 0.59, P < 0.001); (2) in capacitated (C) sperm rate and the proportion of spermatozoa with stronger reactivity in the acrosome (r = 0.60, P < 0.001); and (3) in acrosome-reacted (AR) sperm rate and the proportion of spermatozoa with more intense staining on the post-acrosome (r = 0.67, P < 0.001). Incubation of swim-up-selected samples with either 1 μM melatonin or MT1 and MT2 receptor agonists (2-phenylmelatonin 1 µM and 8-Methoxy-2-propionamidotetralin (8M-PDOT) 1 µM and 10 nM) at 39°C and 5% CO2 for 3 h resulted in a higher proportion of the NC pattern compared with the control group (P < 0.05), whereas treatment with MT1 and MT2 receptor antagonists (luzindole 1 µM and 4-phenyl-2-propionamidotetralin (4P-PDOT) 1 µM and 10 nM) decreased the proportion of spermatozoa exhibiting the NC pattern (P < 0.001) concomitant with an increase in those exhibiting the C pattern (P < 0.01). In conclusion, melatonin exerts a modulating effect on ram sperm functionality, primarily via activation of the MT2 receptor.
Additional keywords: agonist, antagonist, chlortetracycline, MT1 receptor, MT2 receptor.
References
Almog, T., Lazar, S., Reiss, N., Etkovitz, N., Milch, E., Rahamim, N., Dobkin-Bekman, M., Rotem, R., Kalina, M., Ramon, J., Raziel, A., Brietbart, H., Seger, R., and Naor, Z. (2008). Identification of extracellular signal-regulated kinase 1/2 and p38 MAPK as regulators of human sperm motility and acrosome reaction and as predictors of poor spermatozoan quality. J. Biol. Chem. 283, 14 479–14 489.| Identification of extracellular signal-regulated kinase 1/2 and p38 MAPK as regulators of human sperm motility and acrosome reaction and as predictors of poor spermatozoan quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlvFyjsL4%3D&md5=a570df225ae62d279a3bc72f84260342CAS |
Beaumont, V., Hepworth, M. B., Luty, J. S., Kelly, E., and Henderson, G. (1998). Somatostatin receptor desensitization in NG108–15 cells: a consequence of receptor sequestration. J. Biol. Chem. 273, 33 174–33 183.
| Somatostatin receptor desensitization in NG108–15 cells: a consequence of receptor sequestration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkvQ%3D%3D&md5=6bad9de003b7bcbbdf4a654e1f6cadfdCAS |
Bendahmane, M., Lynch, C., and Tulsiani, D. R. P. (2001). Calmodulin signals capacitation and triggers the agonist-induced acrosome reaction in mouse spermatozoa. Arch. Biochem. Biophys. 390, 1–8.
| Calmodulin signals capacitation and triggers the agonist-induced acrosome reaction in mouse spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjs1Gkurk%3D&md5=390a29c8c09e263f184503b811739d90CAS | 11368508PubMed |
Benítez-King, G., Huerto-Delgadillo, L., and Anton-Tay, F. (1993). Binding of 3H-melatonin to calmodulin. Life Sci. 53, 201–207.
| Binding of 3H-melatonin to calmodulin.Crossref | GoogleScholarGoogle Scholar | 8321083PubMed |
Breitbart, H. (2003). Signaling pathways in sperm capacitation and acrosome reaction. Cell. Mol. Biol. 49, 321–327.
| 1:CAS:528:DC%2BD3sXls1Krsbk%3D&md5=cffdc1f4df07c8dce671504edf1ab7a5CAS | 12887084PubMed |
Breitbart, H., Lax, J., Rotem, R., and Naor, Z. (1992). Role of protein-kinase-C in the acrosome reaction of mammalian spermatozoa. Biochem. J. 281, 473–476.
| 1:CAS:528:DyaK38XjvVOiug%3D%3D&md5=87b618acb396b1bebf5dce16c0b1625dCAS | 1736894PubMed |
Breitbart, H., Rotman, T., Rubinstein, S., and Etkovitz, N. (2010). Role and regulation of PI3K in sperm capacitation and the acrosome reaction. Mol. Cell. Endocrinol. 314, 234–238.
| Role and regulation of PI3K in sperm capacitation and the acrosome reaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFynurbI&md5=0c206cab99c35d4bc401f298ec3204fdCAS | 19560510PubMed |
Casao, A., Cebrian, I., Asumpcao, M., Perez-Pe, R., Abecia, J., Forcada, F., Cebrian-Perez, J., and Muino-Blanco, T. (2010a). Seasonal variations of melatonin in ram seminal plasma are correlated to those of testosterone and antioxidant enzymes. Reprod. Biol. Endocrinol. 8, 59.
| Seasonal variations of melatonin in ram seminal plasma are correlated to those of testosterone and antioxidant enzymes.Crossref | GoogleScholarGoogle Scholar | 20540737PubMed |
Casao, A., Mendoza, N., Pérez-Pé, R., Grasa, A., Abecia, J. A., Forcada, F., Cebrián-Pérez, J. A., and Muino-Blanco, T. (2010b). Melatonin prevents capacitation and apoptotic-like changes of ram spermatozoa and increases fertility rate. J. Pineal Res. 48, 39–46.
| Melatonin prevents capacitation and apoptotic-like changes of ram spermatozoa and increases fertility rate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1WhtLzL&md5=3969e0d4917bd9798415706a1bf5d1d9CAS | 19919602PubMed |
Casao, A., Vega, S., Palacín, I., Pérez-Pe, R., Laviña, A., Quintín, F. J., Sevilla, E., Abecia, J. A., Cebrián-Pérez, J. A., Forcada, F., and Muiño-Blanco, T. (2010c). Effects of melatonin implants during non-breeding season on sperm motility and reproductive parameters in Rasa aragonesa rams. Reprod. Domest. Anim. 45, 425–432.
| Effects of melatonin implants during non-breeding season on sperm motility and reproductive parameters in Rasa aragonesa rams.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnvFGrtLc%3D&md5=2bf9d57c082a1fd56f33aa33593f38a7CAS | 18954380PubMed |
Casao, A., Gallego, M., Abecia, J. A., Forcada, F., Pérez-Pé, R., Muiño-Blanco, T., and Cebrián-Pérez, J. Á. (2012). Identification and immunolocalisation of melatonin MT1 and MT2 receptors in Rasa aragonesa ram spermatozoa. Reprod. Fertil. Dev. 24, 953–961.
| Identification and immunolocalisation of melatonin MT1 and MT2 receptors in Rasa aragonesa ram spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Grs7vJ&md5=1de053e62111af3491557d741afddfd4CAS | 22935156PubMed |
Chan, A. S. L., Lai, F. P. L., Lo, R. K. H., Voyno-Yasenetskaya, T. A., Stanbridge, E. J., and Wong, Y. H. (2002). Melatonin MT1 and MT2 receptors stimulate c-Jun N-terminal kinase via pertussis toxin-sensitive and -insensitive G proteins. Cell. Signal. 14, 249–257.
| Melatonin MT1 and MT2 receptors stimulate c-Jun N-terminal kinase via pertussis toxin-sensitive and -insensitive G proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xms1GqsQ%3D%3D&md5=15df591e8faae0c06b1bd8f62dabd68cCAS |
Colas, C., James, P., Howes, L., Jones, R., Cebrian-Perez, J. A., and Muiño-Blanco, T. (2008). Cyclic-AMP initiates protein tyrosine phosphorylation independent of cholesterol efflux during ram sperm capacitation. Reprod. Fertil. Dev. 20, 649–658.
| Cyclic-AMP initiates protein tyrosine phosphorylation independent of cholesterol efflux during ram sperm capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotlCnu70%3D&md5=7520ad1eef7e1333e301e75e119a038bCAS | 18671912PubMed |
da Silva, C. M. B., Macías-García, B., Miró-Morán, A., González-Fernández, L., Morillo-Rodriguez, A., Ortega-Ferrusola, C., Gallardo-Bolaños, J. M., Stilwell, G., Tapia, J. A., and Peña, F. J. (2011). Melatonin reduces lipid peroxidation and apoptotic-like changes in stallion spermatozoa. J. Pineal Res. 51, 172–179.
| Melatonin reduces lipid peroxidation and apoptotic-like changes in stallion spermatozoa.Crossref | GoogleScholarGoogle Scholar |
de Lamirande, E., and O’Flaherty, C. (2008). Sperm activation: role of reactive oxygen species and kinases. Biochim. Biophys. Acta 1784, 106–115.
| Sperm activation: role of reactive oxygen species and kinases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXptlersQ%3D%3D&md5=d412567a4acc642353bd4f233bd96d8aCAS | 17920343PubMed |
Di Francesco, S., Mariotti, E., Tsantarliotou, M., Sattar, A., Venditto, I., Rubessa, M., Zicarelli, L., and Gasparrini, B. (2010). Melatonin promotes in vitro sperm capacitation in buffalo (Bubalus bubalis). Reprod. Fertil. Dev. 22, 311–312.
| Melatonin promotes in vitro sperm capacitation in buffalo (Bubalus bubalis).Crossref | GoogleScholarGoogle Scholar |
Dragileva, E., Rubinstein, S., and Breitbart, H. (1999). Intracellular Ca2+–Mg2+-ATPase regulates calcium influx and acrosomal exocytosis in bull and ram spermatozoa. Biol. Reprod. 61, 1226–1234.
| Intracellular Ca2+–Mg2+-ATPase regulates calcium influx and acrosomal exocytosis in bull and ram spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvFertrs%3D&md5=1ca71579ee163ca6491494ecdf44dbf5CAS | 10529268PubMed |
Dubocovich, M. L., and Markowska, M. (2005). Functional MT1 and MT2 melatonin receptors in mammals. Endocrine 27, 101–110.
| Functional MT1 and MT2 melatonin receptors in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFansLjE&md5=d377d73d2a4456e15826eb3686033f87CAS | 16217123PubMed |
Espino, J., Ortiz, Á., Bejarano, I., Lozano, G. M., Monllor, F., García, J. F., Rodríguez, A. B., and Pariente, J. A. (2011). Melatonin protects human spermatozoa from apoptosis via melatonin receptor- and extracellular signal-regulated kinase-mediated pathways. Fertil. Steril. 95, 2290–2296.
| Melatonin protects human spermatozoa from apoptosis via melatonin receptor- and extracellular signal-regulated kinase-mediated pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsFWns7g%3D&md5=5a7c7001299cd074e992e2b080a03b9bCAS | 21497337PubMed |
Fujinoki, M. (2008). Melatonin-enhanced hyperactivation of hamster sperm. Reproduction 136, 533–541.
| Melatonin-enhanced hyperactivation of hamster sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVCjtrnK&md5=af6d6c59e651f7e69851e35568d17b7fCAS | 18715981PubMed |
Gadella, B. M., Tsai, P. S., Boerke, A., and Brewis, I. A. (2008). Sperm head membrane reorganisation during capacitation. Int. J. Dev. Biol. 52, 473–480.
| Sperm head membrane reorganisation during capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht12qs7bF&md5=4b1d6a2ce26bf48b3a8f2128e3191270CAS | 18649260PubMed |
García-López, N., Ollero, M., Muino-Blanco, T., and Cebrian-Perez, J. A. (1996). A dextran swim-up procedure for separation of highly motile and viable ram spermatozoa from seminal plasma. Theriogenology 46, 141–151.
| A dextran swim-up procedure for separation of highly motile and viable ram spermatozoa from seminal plasma.Crossref | GoogleScholarGoogle Scholar |
Gerdin, M. J., Masana, M. I., Ren, D., Miller, R. J., and Dubocovich, M. L. (2003). Short-term exposure to melatonin differentially affects the functional sensitivity and trafficking of the hMT1 and hMT2 melatonin receptors. J. Pharmacol. Exp. Ther. 304, 931–939.
| Short-term exposure to melatonin differentially affects the functional sensitivity and trafficking of the hMT1 and hMT2 melatonin receptors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXit1ejurk%3D&md5=a5c94312c2037c7f5129597a388e6b73CAS | 12604667PubMed |
Gerdin, M. J., Masana, M. I., and Dubocovich, M. L. (2004). Melatonin-mediated regulation of human MT1 melatonin receptors expressed in mammalian cells. Biochem. Pharmacol. 67, 2023–2030.
| Melatonin-mediated regulation of human MT1 melatonin receptors expressed in mammalian cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjvVCisrw%3D&md5=707c8c32f43acd2eb75105cbbc395565CAS | 15135299PubMed |
Gillan, L., Evans, G., and Maxwell, W. M. (1997). Capacitation status and fertility of fresh and frozen–thawed ram spermatozoa. Reprod. Fertil. Dev. 9, 481–487.
| Capacitation status and fertility of fresh and frozen–thawed ram spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c%2FnvVOrtw%3D%3D&md5=dfd534eab1ead42cd521211ba0f11cbbCAS | 9418976PubMed |
Gómez, M. C., Catt, J. W., Gillan, L., Evans, G., and Maxwell, W. M. C. (1997). Effect of culture, incubation and acrosome reaction of fresh and frozen–thawed ram spermatozoa for in vitro fertilization and intracytoplasmic sperm injection. Reprod. Fertil. Dev. 9, 665–673.
| Effect of culture, incubation and acrosome reaction of fresh and frozen–thawed ram spermatozoa for in vitro fertilization and intracytoplasmic sperm injection.Crossref | GoogleScholarGoogle Scholar | 9623485PubMed |
Grasa, P., Martí, J. I., Muiño-Blanco, T., and Cebrián-Pérez, J. A. (2003). Different functional states of ram spermatozoa analysed by partition in an aqueous two-phase system. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 795, 83–91.
| Different functional states of ram spermatozoa analysed by partition in an aqueous two-phase system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmvVKns74%3D&md5=9bd7df18c816d7ac2c7291f5576dc9ccCAS | 12957172PubMed |
Grasa, P., Cebrian-Perez, J. A., and Muino-Blanco, T. (2006). Signal transduction mechanisms involved in in vitro ram sperm capacitation. Reproduction 132, 721–732.
| Signal transduction mechanisms involved in in vitro ram sperm capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlWktbrJ&md5=67a079a6e31c724cc488b812f1b4a01dCAS | 17071773PubMed |
Hardeland, R. (2009). Melatonin: signaling mechanisms of a pleiotropic agent. Biofactors 35, 183–192.
| Melatonin: signaling mechanisms of a pleiotropic agent.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsVSls78%3D&md5=c76fa8212f30a8639b221dd616e2ca5fCAS | 19449447PubMed |
Hickey, K. D., and Buhr, M. M. (2011). Lipid bilayer composition affects transmembrane protein orientation and function. J. Lipids 2011, 208457.
| Lipid bilayer composition affects transmembrane protein orientation and function.Crossref | GoogleScholarGoogle Scholar | 21490797PubMed |
Hunt, A. E., Al-Ghoul, W. M., Gillette, M. U., and Dubocovich, M. L. (2001). Activation of MT2 melatonin receptors in rat suprachiasmatic nucleus phase advances the circadian clock. Am. J. Physiol. Cell Physiol. 280, 110–118.
Iwanaga, A., Wang, G., Gantulga, D., Sato, T., Baljinnyam, T., Shimizu, K., Takumi, K., Hayashi, M., Akashi, T., Fuse, H., Sugihara, K., Asano, M., and Yoshioka, K. (2008). Ablation of the scaffold protein JLP causes reduced fertility in male mice. Transgenic Res. 17, 1045–1058.
| Ablation of the scaffold protein JLP causes reduced fertility in male mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1yrsr%2FK&md5=77f9b5e86ab17dfba52c8375dea97f35CAS | 18574703PubMed |
Jang, H. Y., Kim, Y. H., Kim, B. W., Park, I. C., Cheong, H. T., Kim, J. T., Park, C. K., Kong, H. S., Lee, H. K., and Yang, B. K. (2010). Ameliorative effects of melatonin against hydrogen peroxide-induced oxidative stress on boar sperm characteristics and subsequent in vitro embryo development. Reprod. Domest. Anim. 45, 943–950.
| Ameliorative effects of melatonin against hydrogen peroxide-induced oxidative stress on boar sperm characteristics and subsequent in vitro embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1WrsLvK&md5=417619477561784f847f1f147e03617fCAS | 19473309PubMed |
Jockers, R., Maurice, P., Boutin, J. A., and Delagrange, P. (2008). Melatonin receptors, heterodimerization, signal transduction and binding sites: what’s new? Br. J. Pharmacol. 154, 1182–1195.
| Melatonin receptors, heterodimerization, signal transduction and binding sites: what’s new?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXosVCjtLk%3D&md5=274927764f349239b0081349fdfff242CAS | 18493248PubMed |
Karagiannidis, A., Varsakeli, S., Alexopoulos, C., and Amarantidis, I. (2000). Seasonal variation in semen characteristics of Chios and Friesian rams in Greece. Small Rumin. Res. 37, 125–130.
| Seasonal variation in semen characteristics of Chios and Friesian rams in Greece.Crossref | GoogleScholarGoogle Scholar | 10818312PubMed |
Kokolis, N., Theodosiadou, E., Tsantarliotou, M., Rekkas, C., Goulas, P., and Smokovitis, A. (2000). The effect of melatonin implants on blood testosterone and acrosin activity in spermatozoa of the ram. Andrologia 32, 107–114.
| The effect of melatonin implants on blood testosterone and acrosin activity in spermatozoa of the ram.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisVClt7Y%3D&md5=ee2f1b11c76050cd38efda692ec0f877CAS | 10755193PubMed |
Langford, G. A., Ainsworth, L., Marcus, G. J., and Shrestha, J. N. (1987). Photoperiod entrainment of testosterone, luteinizing hormone, follicle-stimulating hormone, and prolactin cycles in rams in relation to testis size and semen quality. Biol. Reprod. 37, 489–499.
| Photoperiod entrainment of testosterone, luteinizing hormone, follicle-stimulating hormone, and prolactin cycles in rams in relation to testis size and semen quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXls12itrs%3D&md5=38c8a48d6c9449297531139b00d72756CAS | 3118978PubMed |
Lincoln, G. A., Almeida, O. F., and Arendt, J. (1981). Role of melatonin and circadian rhythms in seasonal reproduction in rams. J. Reprod. Fertil. Suppl. 30, 23–31.
| 1:CAS:528:DyaL38XpvVCkug%3D%3D&md5=8f0440343c3c577e8174f19dd7fb4807CAS | 6962843PubMed |
Lincoln, G. A., Lincoln, C. E., and McNeilly, A. S. (1990). Seasonal cycles in the blood plasma concentration of FSH, inhibin and testosterone, and testicular size in rams of wild, feral and domesticated breeds of sheep. J. Reprod. Fertil. 88, 623–633.
| Seasonal cycles in the blood plasma concentration of FSH, inhibin and testosterone, and testicular size in rams of wild, feral and domesticated breeds of sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhslaltbw%3D&md5=4731952e121d331a2c8afe6799e60fb7CAS | 2109070PubMed |
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 | 1:CAS:528:DC%2BC3MXjsVKru7o%3D&md5=0903acede00f597cbc0a81cc4724583bCAS | 21412339PubMed |
Martín-Hidalgo, D., Barón, F. J., Bragado, M. J., Carmona, P., Robina, A., García-Marín, L. J., and Gil, M. C. (2011). The effect of melatonin on the quality of extended boar semen after long-term storage at 17°C. Theriogenology 75, 1550–1560.
| The effect of melatonin on the quality of extended boar semen after long-term storage at 17°C.Crossref | GoogleScholarGoogle Scholar | 21320723PubMed |
Misztal, T., Romanowicz, K., and Barcikowski, B. (2002). Melatonin: a modulator of the GnRH/LH axis in sheep. Reprod. Biol. 2, 267–275.
| 14666149PubMed |
Morgan, P. J., Lawson, W., Davidson, G., and Howell, H. E. (1989). Melatonin inhibits cyclic-AMP production in cultured ovine par tuberalis cells. J. Mol. Endocrinol. 3, R5–R8.
| Melatonin inhibits cyclic-AMP production in cultured ovine par tuberalis cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXlvVyjsr4%3D&md5=2b82d0dffd93ad66afc28e6bd609ce41CAS |
Nixon, B., and Aitken, R. J. (2009). The biological significance of detergent-resistant membranes in spermatozoa. J. Reprod. Immunol. 83, 8–13.
| The biological significance of detergent-resistant membranes in spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVyntrvF&md5=50e4d95e3deff7002350398755703123CAS | 19857901PubMed |
Nonno, R., Lucini, V., Pannacci, M., Mazzucchelli, C., Angeloni, D., Fraschini, F., and Stankov, B. M. (1998). Pharmacological characterization of the human melatonin Mel1a receptor following stable transfection into NIH3T3 cells. Br. J. Pharmacol. 124, 485–492.
| Pharmacological characterization of the human melatonin Mel1a receptor following stable transfection into NIH3T3 cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjslSisrs%3D&md5=b024f91eb663ea5c27797f9b8b015de9CAS | 9647472PubMed |
Ollero, M., Pascual, M. L., Muiñio-Blanco, T., Cebrián-Pérez, J. A., and López-Pérez, M. J. (1994). Revealing surface changes associated with maturation of ram spermatozoa by centrifugal counter-current distribution in an aqueous two-phase system. J. Chromatogr. A 668, 173–178.
| Revealing surface changes associated with maturation of ram spermatozoa by centrifugal counter-current distribution in an aqueous two-phase system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXksFegtbg%3D&md5=447de10d41dd8d69efa7405dcdd32a25CAS | 7516244PubMed |
Ollero, M., Muino-Blanco, T., Lopez-Perez, M. J., and Cebrian-Perez, J. A. (1996). Viability of ram spermatozoa in relation to the abstinence period and successive ejaculations. Int. J. Androl. 19, 287–292.
| Viability of ram spermatozoa in relation to the abstinence period and successive ejaculations.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s7jvVOltQ%3D%3D&md5=69f3aae54c43a9226bf562710e70bdafCAS | 8985777PubMed |
Ollero, M., Cebrian-Perez, J. A., and Muiño-Blanco, T. (1997). Improvement of cryopreserved ram sperm heterogeneity and viability by addition of seminal plasma. J. Androl. 18, 732–739.
| 1:STN:280:DyaK1c%2Fpt1Cntg%3D%3D&md5=24d3525325e65290ab16796768a84462CAS | 9432147PubMed |
Palacín, I., Abecia, J. A., Forcada, F., Casao, A., Cebrian-Perez, J. A., Muino-Blanco, T., Palacios, C., and Pontes, J. M. (2008). Effect of exogenous melatonin treatment on out of season ram fertility. Ital. J. Anim. Sci. 7, 199–206.
Parrish, J. J., Susko-Parrish, J., Winer, M. A., and First, N. L. (1988). Capacitation of bovine sperm by heparin. Biol. Reprod. 38, 1171–1180.
| Capacitation of bovine sperm by heparin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXkslWit7g%3D&md5=42dfa83157c4564e056cb28bdbb515f8CAS | 3408784PubMed |
Pascual, M. L., Muiño-Blanco, T., Cebrián-Pérez, J. A., and López-Pérez, M. J. (1993). Sperm cell heterogeneity revealed by centrifugal counter-current distribution in an aqueous two-phase system. J. Chromatogr. 617, 51–57.
| Sperm cell heterogeneity revealed by centrifugal counter-current distribution in an aqueous two-phase system.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3szovVOqsQ%3D%3D&md5=3016f9485a5be5a7b5bfda9841644c6fCAS | 8376537PubMed |
Pozo, D., Reiter, R. J., Calvo, J. R., and Guerrero, J. M. (1997). Inhibition of cerebellar nitric oxide synthase and cyclic GMP production by melatonin via complex formation with calmodulin. J. Cell. Biochem. 65, 430–442.
| Inhibition of cerebellar nitric oxide synthase and cyclic GMP production by melatonin via complex formation with calmodulin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXivFKiurk%3D&md5=5ccd7fc07372e6e2d4111d25da8da8fcCAS | 9138098PubMed |
Rosa, H. J. D., and Bryant, M. J. (2003). Seasonality of reproduction in sheep. Small Rumin. Res. 48, 155–171.
| Seasonality of reproduction in sheep.Crossref | GoogleScholarGoogle Scholar |
Roy, D., Angelini, N. L., Fujieda, H., Brown, G. M., and Belsham, D. D. (2001). Cyclical regulation of GnRH gene expression in GT1-7 GnRH-secreting neurons by melatonin. Endocrinology 142, 4711–4720.
| 1:CAS:528:DC%2BD3MXnslGqtb4%3D&md5=674847f5bef6f6d000058c0b7bb8b1f2CAS | 11606436PubMed |
Si, Y., and Olds-Clarke, P. (2000). Evidence for the involvement of calmodulin in mouse sperm capacitation. Biol. Reprod. 62, 1231–1239.
| Evidence for the involvement of calmodulin in mouse sperm capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisl2ht7k%3D&md5=a62dc60d8218cd7df61ebf9bf80fdb9fCAS | 10775171PubMed |
Sjöblom, M., Säfsten, B., and Flemström, G. (2003). Melatonin-induced calcium signaling in clusters of human and rat duodenal enterocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 284, G1034–G1044.
| 12584110PubMed |
Smokovitis, A., Kokolis, N., Taitzoglou, I., and Rekkas, C. (1992). Plasminogen-activator: the indentification of an additional proteinase at the outer acrosomal membrane of human and boar spermatozoa. Int. J. Fertil. 37, 308–314.
| 1:STN:280:DyaK3s%2FltlWktQ%3D%3D&md5=ba68b167c2194e00f1f8c31d2d36050aCAS | 1358844PubMed |
Trecherel, E., Batailler, M., Chesneau, D., Delagrange, P., Malpaux, B., Chemineau, P., and Migaud, M. (2010). Functional characterization of polymorphic variants for ovine MT1 melatonin receptors: Possible implication for seasonal reproduction in sheep. Anim. Reprod. Sci. 122, 328–334.
| Functional characterization of polymorphic variants for ovine MT1 melatonin receptors: Possible implication for seasonal reproduction in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFahs7vL&md5=637375d7c039662434616941ecb47d54CAS | 21075566PubMed |
Tsantarliotou, M. P., Kokolis, N. A., and Smokovitis, A. (2008). Melatonin administration increased plasminogen activator activity in ram spermatozoa. Theriogenology 69, 458–465.
| Melatonin administration increased plasminogen activator activity in ram spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVSmsrk%3D&md5=15bd078e5cbc94a0bfc111fbec22e713CAS | 18045674PubMed |
Tulsiani, D. R., Zeng, H. T., and Abou-Haila, A. (2007). Biology of sperm capacitation: evidence for multiple signalling pathways. Soc. Reprod. Fertil. Suppl. 63, 257–272.
| 1:CAS:528:DC%2BD1cXpvVyktLw%3D&md5=b0c4e5e3241f0bb079ec176f77c738b6CAS | 17566278PubMed |
Visconti, P. E., and Kopf, G. S. (1998). Regulation of protein phosphorylation during sperm capacitation. Biol. Reprod. 59, 1–6.
| Regulation of protein phosphorylation during sperm capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktFaksLw%3D&md5=8bfc30e10008bda7ad7684be5a187e9bCAS | 9674985PubMed |
Ward, C. R., and Storey, B. T. (1984). Determination of the time course of capacitation in mouse spermatozoa using a chlortetracycline fluorescence assay. Dev. Biol. 104, 287–296.
| Determination of the time course of capacitation in mouse spermatozoa using a chlortetracycline fluorescence assay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXkvVKksLc%3D&md5=eae83208a17fe583105e884bd4140fbcCAS | 6745485PubMed |
Witt-Enderby, P. A., Masana, M. I., and Dubocovich, M. L. (1998). Physiological exposure to melatonin supersensitizes the cyclic adenosine 3′,5′-monophosphate-dependent signal transduction cascade in Chinese hamster ovary cells expressing the human mt1 melatonin receptor. Endocrinology 139, 3064–3071.
| 1:CAS:528:DyaK1cXktV2ht7w%3D&md5=2bd5d29d650c849ac392872aa68a2711CAS | 9645677PubMed |
Witt-Enderby, P. A., MacKenzie, R. S., McKeon, R. M., Carroll, E. A., Bordt, S. L., and Melan, M. A. (2000). Melatonin induction of filamentous structures in non-neuronal cells that is dependent on expression of the human mt1 melatonin receptor. Cell Motil. Cytoskeleton 46, 28–42.
| Melatonin induction of filamentous structures in non-neuronal cells that is dependent on expression of the human mt1 melatonin receptor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXksFSgsb8%3D&md5=734e877321074c63e92558b82d9ba73eCAS | 10842331PubMed |
