Identification and immunolocalisation of melatonin MT1 and MT2 receptors in Rasa Aragonesa ram spermatozoa

Reproduction, Fertility and Development

Volumn 24, Issue 7, 2012, Pages 953-961

  Casao, Adriana ^a   Gallego, Margarita ^b   Abecia, Joś Alfonso ^a   Forcada, Fernando ^a   Ṕrez Ṕ, Rosaura ^a   Muio Blanco, Teresa ^a   Cebrin Ṕrez, Joś Lvaro ^a  

^a UNIVERSITY OF ZARAGOZA   (Spain)

^b UNIVERSIDAD DE ZARAGOZA   (Spain)

Author keywords

immunocytochemistry; immunofluorescence; western blot.

Indexed keywords

MELATONIN 1 RECEPTOR; MELATONIN 2 RECEPTOR; RECEPTOR SUBTYPE;

ACROSOME; ARTICLE; IMMUNOLOCALIZATION; NONHUMAN; RASA ARAGONESA; SEASONAL VARIATION; SEMINAL PLASMA; SHEEP; SPERM; SPERMATOZOON; SPERMATOZOON TAIL;

ANIMALS; BLOTTING, WESTERN; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOHISTOCHEMISTRY; MALE; MOLECULAR WEIGHT; PROTEIN MULTIMERIZATION; RECEPTOR, MELATONIN, MT1; RECEPTOR, MELATONIN, MT2; SHEEP; SPERM COUNT; SPERM MOTILITY; SPERMATOZOA;

OVIS ARIES; RASA ARAGONESA;

EID: 84865847090     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD11242     Document Type: Article

References (47)

1. 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. doi:10.1074/JBC. M
2. Ayoub, M. A., Levoye, A., Delagrange, P., and Jockers, R. (2004). Preferential formation of MT1/MT2 melatonin receptor heterodimers with distinct ligand interaction properties compared with MT2 homodimers. Mol. Pharmacol. 66, 312-321. doi:10.1124/MOL.104.0
3. Balao da Silva, C. M., Macías-García, B., Miró-Morán, A., González- Fernández, L., Morillo-Rodriguez, A., Ortega-Ferrusola, C., Gallardo- Bolanos, J. M., Stilwell, G., Tapia, J. A., and Pena, F. J. (2011). Melatonin reduces lipid peroxidation and apoptotic-like changes in stallion spermatozoa. J. Pineal Res. 51, 172-179. doi:10.1111/J.1600- 079X.2011.00873.X
4. Breitbart, H., Lax, J., Rotem, R., and Naor, Z. (1992). Role of protein-kinase- Cin the acrosome reaction of mammalian spermatozoa. Biochem. J. 281, 473-476.
5. 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. doi:10.1186/1477-7827-8-5
6. 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. doi:10.1111/J.1600- 079X.2009.00722.X
7. Casao, A., Vega, S., Palacín, I., Pérez-Pe, R., Lavina, A., Quintín, F. J., Sevilla, E., Abecia, J. A., Cebrián-Pérez, J. A., Forcada, F., and Muino- 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. doi:10.1111/J.1439-0531.2008.01215.X
8. 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 M receptors stimulate c-Jun N-terminal kinase via pertussis toxin-sensitive and -insensitive G proteins. Cell Signal. 14, 249-257. doi:10.1016/S0898-6568(01)00240-6
9. Chemineau, P., Malpaux, B., Delgadillo, J. A., Guerin, Y., Ravault, J. P., Thimonier, J., and Pelletier, J. (1992). Control of sheep and goat reproduction: use of light and melatonin. Anim. Reprod. Sci. 30, 157-184. doi:10.1016/0378-4320(92)90010-B
10. Cogé, F., Guenin, S. P., Fery, I., Migaud, M., Devavry, S., Slugocki, C., Legros, C., Ouvry, C., Cohen, W., Renault, N., Nosjean, O., Malpaux, B., Delagrange, P., and Boutin, J. A. (2009). The end of a myth: cloning and characterization of the ovine melatoninMT2 receptor. Br. J. Pharmacol. 158, 1248-1262. doi:10.1111/J.1476-5381.2009.00453.X
11. Cola's, C., Grasa, P., Casao, A., Gallego, M., Abecia, J. A., Forcada, F., Cebria'n-Pe'rez, J. A., and Muino-Blanco, T. (2009). Changes in calmodulin immunocytochemical localization associated with capacitation and acrosomal exocytosis of ram spermatozoa. Theriogenology 71, 789-800. doi:10.1016/J. THERIOGENOLOGY.2008.10.0
12. Coyan, K., Kaya, A., Karaca, F., Ataman, M. B., and Yildiz, C. (1998). The effect of melatonin on sperm quality and testicular size of normospermic and pathospermic rams in the anoestrous season. Wien Tierarztl. Monatsschr. 85, 383-388. [In German with English Abstract]
13. de Lamirande, E., and O'Flaherty, C. (2008). Sperm activation: role of reactive oxygen species and kinases. Biochim. Biosphys. Acta 1784, 106-115. doi:10.1016/J.BBAPAP.2007.08.0
14. Dubocovich, M. L., and Markowska, M. (2005). Functional MT1 and M melatonin receptors in mammals. Endocrine 27, 101-110. doi:10.1385/ENDO:27:2:1
15. Dubocovich,M.L.,Rivera-Bermudez,M.A.,Gerdin,M. J., andMasana,M.I. (2003). Molecular pharmacology, regulation and function of mammalian melatonin receptors. Front. Biosci. 8, d1093-d1108. doi:10.2741/1
16. Dubocovich, M., Delagrange, P., and Olcese, J. (2009). 'Melatonin Receptors.' Available at: http://www.iuphar-db.org/DATABASE/FamilyMenuForward? familyId=39 [Verified 31 November 2011].
17. European Community Commission (1986). Scientific procedure and breeding of animals for use in scientific procedures establishments. In 'Directive 86/609/EEC.' (Ed. European Community Commission.) pp. 1-28. (European Community Commission: Brussel.)
18. Espino, J., Ortiz, Á ., Bejarano, I., Lozano, G. M., Monllor, F., Garci'a, J. F., Rodri'guez, 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. doi:10.1016/J.FERTNSTERT.2011.03.0
19. Frungieri, M. B., Mayerhofer, A., Zitta, K., Pignataro, O. P., Calandra, R. S., and Gonzalez-Calvar, S. I. (2005). Direct effect of melatonin on Syrian hamster testes: melatonin subtype 1a receptors, inhibition of androgen production, and interaction with the local corticotropin-releasing hormone system. Endocrinology 146, 1541-1552. doi:10.1210/EN. 2004-0
20. Fujinoki, M. (2008). Melatonin-enhanced hyperactivation of hamster sperm. Reproduction 136, 533-541. doi:10.1530/REP-08-0
21. García-López, N., Ollero, M., Muino-Blanco, T., and Cebrián-Pérez, J. A. (1996).Adextran swim-up procedure for separation of highly motile and viable ram spermatozoa from seminal plasma. Theriogenology 46, 141-151. doi:10.1016/0093-691X(96)00149-5
22. Gilman, A. G. (1995). G-Proteins and regulation of adenylyl-cyclase. Biosci. Rep. 15, 65-97. doi:10.1007/B
23. 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, C110-C118.
24. Ishii, H., Tanaka, N., Kobayashi, M., Kato, M., and Sakuma, Y. (2009). Gene structures, biochemical characterization and distribution of rat melatonin receptors. J. Physiol. Sci. 59, 37-47. doi:10.1007/S12576-008-0003-9
25. 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. doi:10.1007/S11248-008- 9191-6
26. Izzo, G., Francesco, A., Ferrara, D., Campitiello, M. R., Serino, I., Minucci, S., and d'Istria, M. (2010). Expression of melatonin (MT1, MT2) and melatonin-related receptors in the adult rat testes and during development. Zygote 18, 257-264. doi:10.1017/S
27. 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. doi:10.1038/BJP. 2008.1
28. Kaya, A., Baspinar, N., Yildiz, C., Kurtoglu, F., Ataman, M. B., and Haliloglu, S. (2000). Influence of melatonin implantation on sperm quality, biochemical composition of the seminal plasma and plasma testosterone levels in rams. Rev. Med. Vet. 151, 1143-1146.
29. 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. doi:10.1046/J.1439-0272.2000.00336.X
30. Levoye, A., Dam, J., Ayoub, M. A., Guilllaume, J. L., Couturier, C., Delagrange, P., and Jockers, R. (2006). The orphan GPR50 receptor specifically inhibits MT1 melatonin receptor function through heterodimerization. EMBO J. 25, 3012-3023. doi:10.1038/SJ.EMBOJ. 7
31. Lincoln, G. A. (1996). Melatonin regulation of gonadotropin and prolactin secretion in the ram: the dual site hypothesis. Acta Neurobiol. Exp. 56, 846. [Abstract]
32. Mandiki, S. N. M., Derycke, G., Bister, J. L., and Paquay, R. (1998). Influence of season and age on sexual maturation parameters of Texel, Suffolk and Ile-de-France rams: 1. Testicular size, semen quality and reproductive capacity. Small Rumin. Res. 28, 67-79. doi:10.1016/S0921-4488(97)00073-4
33. 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. doi:10.1677/JME.0.0
34. Morgan, P. J., Barrett, P., Howell, H. E., and Helliwell, R. (1994). Melatonin receptors: localization, molecular pharmacology and physiological significance. Neurochem. Int. 24, 101-146. doi:10.1016/0197-0)90100-7
35. 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. doi:10.1111/J.1365-2605. 1996.TB00477.X
36. Ortiz, A., Espino, J., Bejarano, I., Lozano, G. M., Monllor, F., Garci'a, J. F., Pariente, J. A., and Rodri'guez, A. B. (2011). High endogenous melatonin concentrations enhance sperm quality and short-term in vitro exposure to melatonin improves aspects of sperm motility. J. Pineal Res. 50, 132-139.
37. Pin, J. P., Neubig, R., Bouvier, M., Devi, L., Filizola, M., Javitch, J. A., Lohse, M. J., Milligan, G., Palczewski, K., Parmentier, M., and Spedding, M. (2007). International Union of Basic and Clinical Pharmacology. LXVII. Recommendations for the recognition and nomenclature of G protein-coupled receptor heteromultimers. Pharmacol. Rev. 59, 5-13. doi:10.1124/PR.59.1.5
38. Radogna, F., Paternoster, L., Albertini, M. C., Cerella, C., Accorsi, A., Bucchini, A., Spadoni, G., Diamantini, G., Tarzia, G., De Nicola, M., D'Alessio, M., and Ghibelli, L. (2007). Melatonin antagonizes apoptosis via receptor interaction in U937 monocytic cells. J. Pineal Res. 43, 154-162. doi:10.1111/J.1600-079X.2007.00455.X
39. Reppert, S. M., Weaver, D. R., and Ebisawa, T. (1994). Cloning and characterization of a mammalian melatonin receptor that mediates reproductive and circadian responses. Neuron 13, 1177-1185. doi:10.1016/0896-6273(94)90055-8
40. Rosa, H. J. D., and Bryant, M. J. (2003). Seasonality of reproduction in sheep. Small Rumin. Res. 48, 155-171. doi:10.1016/S0921-4488(03) 00038-5
41. Solakidi, S., Psarra, A. M., Nikolaropoulos, S., and Sekeris, C. E. (2005). Estrogen receptors alpha and beta (ERalpha and ERbeta) and androgen receptor (AR) in human sperm: localization of ERbeta and AR in mitochondria of the midpiece. Hum. Reprod. 20, 3481-3487. doi:10.1093/HUMREP/D
42. van Vuuren, R. J., Pitout, M. J., van Aswegen, C. H., and Theron, J. J. (1992). Putative melatonin receptor in human spermatozoa. Clin. Biochem. 25, 125-127. doi:10.1016/0009-9120(92)80056-M
43. Webster, J. R., Suttie, J. M., Veenvliet, B. A., Manley, T. R., and Littlejohn, R. P. (1991). Effect of melatonin implants on secretion of luteinizing hormone in intact and castrated rams. J. Reprod. Fertil. 92, 21-31. doi:10.1530/JRF.0.0
44. Williams, L. M., Hannah, L. T., Hastings,M. H., and Maywood, E. S. (1995). Melatonin receptors in the rat brain and pituitary. J. Pineal Res. 19, 173-177. doi:10.1111/J.1600-079X.1995.TB00186.X
45. Witt-Enderby, P. A., Masana, M. I., and Dubocovich, M. L. (1998). Physiological exposure to melatonin supersensitizes the cyclic adenosine 30,50-monophosphate-dependent signal transduction cascade in Chinese hamster ovary cells expressing the human mt1 melatonin receptor. Endocrinology 139, 3064-3071. doi:10.1210/EN.139.7.3
46. 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. Cytoskel. 46, 28-42. doi:10.1002/(SICI)1097- 0169(200005)46:1,28::AIDCM4.3.0. CO;2-5
47. Witt-Enderby, P. A., Bennett, J., Jarzynka, M. J., Firestine, S., and Melan, M. A. (2003). Melatonin receptors and their regulation: biochemical and structural mechanisms. Life Sci. 72, 2183-2198. doi:10.1016/S0024-3205(03)00098- 5