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Reproductive Biology and Endocrinology
Published in: Reproductive Biology and Endocrinology 1/2012

Open Access 01-12-2012 | Research

MT3 melatonin binding site, MT1 and MT2 melatonin receptors are present in oocyte, but only MT1 is present in bovine blastocyst produced in vitro

Authors: Rafael V Sampaio, Dhúllia Stefanne B Conceição, Moysés S Miranda, Lucia de Fatima S Sampaio, Otávio Mitio Ohashi

Published in: Reproductive Biology and Endocrinology | Issue 1/2012

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Abstract

Background

Melatonin inclusion into in vitro oocyte maturation (IVM) protocols has been suggested because it possesses a powerful free radical scavenger capability that improves the quality of the oocyte used in in vitro embryo production (IVP). The aim of our study was to investigate the presence of melatonin membrane receptors (MT1and MT2) and MT3, which is the melatonin binding site of NQO2 enzyme, in both oocytes and hatched blastocysts to consider an additional subcellular mechanism responsible for the effects of melatonin on IVP.

Methods

The presence of the high affinity melatonin receptors was investigated through an autoradiographic binding assay, using the non-permeable ligand [125I]-iodomelatonin (17 pM) in embryos. The kind of melatonin site was investigated in oocytes and embryos by immunocytochemistry. In vitro fertilized bovine embryos produced from in vitro maturated oocytes supplemented with melatonin (0.0001 to 1000 nM) were analysed to determine their cleavage and blastocyst formation rates.

Results

The [125I]-iodomelatonin (17 pM) binding in blastocysts was blocked by pre-incubation with melatonin (30000 nM), showing the presence of the high affinity melatonin receptors. MT1, MT2 and NQO2 immunoreactivity was observed in oocytes. MT1 immunoreactivity was observed in hatched blastocysts, however MT2 and NQO2 were not observed in this embryonic stage. Melatonin (pM) triggered significant difference in both cleavage and blastocysts formation rates.

Conclusions

The high affinity MT1 melatonin receptor must be taking part in IVM events; furthermore it is the first melatonin receptor to appear during bovine embryo development in vitro.
Appendix
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Literature
1.
Irmak MK, Topal T, Oter S: Melatonin seems to be a mediator that transfers the environmental stimuli to oocytes for inheritance of adaptive changes through epigenetic inheritance system. Med Hypotheses. 2005, 64: 1138-1143. 10.1016/j.mehy.2004.12.014.CrossRefPubMed
2.
Torres-Farfan C, Rocco V, Monsó C, Valenzuela FJ, Campino C, Germain A, Torrealba F, Valenzuela GJ, Seron-Ferre M: Maternal melatonin effects on clock gene expression in a nonhuman primate fetus. Endocrinology. 2006, 147: 4618-4626. 10.1210/en.2006-0628.CrossRefPubMed
3.
Dubocovich ML: Melatonin receptors: role on sleep and circadian rhythm regulation. Sleep Med. 2007, 3: 34-42.CrossRef
4.
Seron-Ferre M, Valenzuela GJ, Torres-Farfan C: Circadian clocks during embryonic and fetal development. Birth Defects Res C Embryo Today. 2007, 81: 204-214. 10.1002/bdrc.20101.CrossRefPubMed
5.
Lardone PJ, Carrillo-Vico A, Molinero P, Rubio A, Guerrero JM: A novel interplay between membrane and nuclear melatonin receptors in human lymphocytes: significance in IL-2 production. Cell Mol Life Sci. 2009, 66: 516-525. 10.1007/s00018-008-8601-5.CrossRefPubMed
6.
Romero MP, García-Pergañeda A, Guerrero JM, Osuna C: Membrane-bound calmodulin in Xenopus laevis oocytes as a novel binding site for melatonin. FASEB J. 1998, 12: 1401-08.PubMed
7.
Sampaio LFS: Un unexpected effect of 5-MCA-NAT in chick retina development. Int J Dev Neurosci. 2009, 27: 511-515. 10.1016/j.ijdevneu.2009.07.001.CrossRef
8.
Banerjee J, Maitra D, Diamond MP, Abu-Soud HM: Melatonin prevents hypochlorous acid-induced alterations in microtubule and chromosomal structure in metaphase-II mouse oocytes. J Pineal Res. 2012, 53: 122-128. 10.1111/j.1600-079X.2012.00977.x.CrossRefPubMed
9.
Fischer TW, Slominski A, Zmijewski MA, Reiter RJ, Paus R: Melatonin as a major skin protectant: from free radical scavenging to DNA damage repair. Exp Dermatol. 2008, 17: 713-730. 10.1111/j.1600-0625.2008.00767.x.CrossRefPubMed
10.
Galano A, Tan D-X, Reiter RJ: Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res. 2011, 51: 1-16. 10.1111/j.1600-079X.2011.00916.x.CrossRefPubMed
11.
Srinivasan V, Spence WD, Pandi-Perumal SR, Zakharia R, Bhatnagar KP, Brzezinski A: Melatonin and human reproduction: shedding light on the darkness hormone. Gynecol Endocrinol. 2009, 25: 779-785. 10.3109/09513590903159649.CrossRefPubMed
12.
Scherbarth F, Steinlechner S: Endocrine mechanisms of seasonal adaptation in small mammals: from early results to present understanding. J Comp Physiol B. 2010, 180: 935-952. 10.1007/s00360-010-0498-2.CrossRefPubMed
13.
Taketani T, Tamura H, Takasaki A, Lee L, Kizuka F, Tamura I, Taniguchi K, Maekawa R, Assada H, Shimamura K, Reiter RJ, Sugino N: Protective role of melatonin in progesterone production by human luteal cells. J Pineal Res. 2011, 51: 207-213. 10.1111/j.1600-079X.2011.00878.x.CrossRefPubMed
14.
Shi JM, Tian XZ, Zhou GB, Wang L, Gao C, Zhu SE, Zeng SM, Tian JH, Liu GS: Melatonin exists in porcine follicular fluid and improves in vitro maturation and parthenogenetic development of porcine oocytes. J Pineal Res. 2009, 47: 318-323. 10.1111/j.1600-079X.2009.00717.x.CrossRefPubMed
15.
Tamura H, Takasaki A, Taketani T, Tanabe M, Kizuka F, Lee L, Tamura I, Maekawa R, Aasada H, Yamagata Y, Sugino N: The role of melatonin as an antioxidant in the follicle. J Ovarian Res. 2012, 26: 5-5.CrossRef
16.
Yasuo S, Yoshimura T, Ebihara S, Korf HW: Melatonin transmits photoperiodic signals through the MT1 melatonin receptor. J Neurosci. 2009, 29: 2885-2889. 10.1523/JNEUROSCI.0145-09.2009.CrossRefPubMed
17.
Malpaux B, Migaud M, Tricoire H, Chemineau P: Biology of mammalian photoperiodism and the critical role of the pineal gland and melatonin. J Biol Rhythms. 2001, 16: 336-47. 10.1177/074873001129002051.CrossRefPubMed
18.
Prendergast BJ: MT1 melatonin receptors mediate somatic, behavioral, and reproductive neuroendocrine responses to photoperiod and melatonin in Siberian hamsters (Phodopus sungorus). Endocrinology. 2010, 151: 714-721. 10.1210/en.2009-0710.PubMedCentralCrossRefPubMed
19.
Trecherel E, Batailler M, Chesneau D, Delagrange P, Malpaux B, Chemineau P, Migaud M: Functional characterization of polymorphic variants for ovine MT1 melatonin receptors: possible implication for seasonal reproduction in sheep. Anim Reprod Sci. 2010, 122: 328-34. 10.1016/j.anireprosci.2010.10.007.CrossRefPubMed
20.
Carcangiu V, Mura MC, Vacca GM, Dettori ML, Pazzola M, Daga C, Luridiana S: Characterization of the melatonin receptor gene MT1 in mouflon (Ovis Gmelini Musimon) and its relationship with reproductive activity. Mol Reprod Dev. 2010, 77: 196-PubMed
21.
Carcangiu V, Luridiana S, Vacca GM, Daga C, Mura MC: A polymorphism at the melatonin receptor 1A (MTNR1A) gene in Sarda ewes affects fertility after AI in the spring. Reprod Fertil Dev. 2011, 23: 376-380. 10.1071/RD10014.CrossRefPubMed
22.
McElhinny AS, Davis FC, Warner CM: The effect of melatonin on cleavage rate of C57BL/6 and CBA/Ca preimplantation embryos cultured in vitro. J Pineal Res. 1996, 21: 44-48. 10.1111/j.1600-079X.1996.tb00269.x.CrossRefPubMed
23.
Ishizuka B, Kuribayashi Y, Murai K, Amemiya A, Itoh MT: The effect of melatonin on in vitro fertilization and embryo development in mice. J Pineal Res. 2000, 28: 48-51. 10.1034/j.1600-079x.2000.280107.x.CrossRefPubMed
24.
Rodriguez-Osorio N, Kim IJ, Wang H, Kaya A, Memili E: Melatonin increases cleavage rate of porcine preimplantation embryos in vitro. J Pineal Res. 2007, 43: 283-288. 10.1111/j.1600-079X.2007.00475.x.CrossRefPubMed
25.
Manjunatha BM, Devaraj M, Gupta PS, Ravindra JP, Nandi S: Effect of taurine and melatonin in the culture medium on buffalo in vitro embryo development. Reprod Domest Anim. 2009, 44: 12-16. 10.1111/j.1439-0531.2007.00982.x.CrossRefPubMed
26.
Casao A, Mendoza N, Pérez-Pé R, Grasa P, Abecia JA, Forcada F, Cebrián-Pérez JA, Muino-Blanco T: Melatonin prevents capacitation and apoptotic-like changes of ram spermatozoa and increases fertility rate. J Pineal Res. 2010, 48: 39-46. 10.1111/j.1600-079X.2009.00722.x.CrossRefPubMed
27.
Bevers MM, Dieleman SJ, Van Den Hurk R, Izadyar F: Regulation and modulation of oocyte maturation in the bovine. Theriogenology. 1997, 47: 13-22. 10.1016/S0093-691X(96)00335-4.CrossRef
28.
Sirard MA: Resumption of meiosis: mechanism involved in meiotic progression and its relation with developmental competence. Theriogenology. 2001, 55: 1241-54. 10.1016/S0093-691X(01)00480-0.CrossRefPubMed
29.
Lonergan P, Fair T: In vitro-produced bovine embryos – Dealing with the warts. Theriogenology. 2008, 69: 17-22. 10.1016/j.theriogenology.2007.09.007.CrossRefPubMed
30.
Papis K, Poleszczuk O, Wenta-Muchalska E, Modlinski JA: Melatonin effect on bovine embryo development in vitro in relation to oxygen concentration. J Pineal Res. 2007, 43: 321-26. 10.1111/j.1600-079X.2007.00479.x.CrossRefPubMed
31.
Takada L, Martins Junior A, Mingoti GZ, Balieiro JCC, Cipolla-Neto J, Coelho LA: Effect of melatonin on DNA damage of bovine cumulus cells during in vitro maturation (IVM) and on in vitro embryo development. Res Vet Sci. 2012, 92: 124-127. 10.1016/j.rvsc.2010.11.004.CrossRefPubMed
32.
Tamura H, Nakamura Y, Korkmaz A, Manchester LC, Tan DX, Sugino N, Reiter RJ: Melatonin and the ovary: physiological and pathophysiological implications. Fertil Steril. 2009, 92: 328-343. 10.1016/j.fertnstert.2008.05.016.CrossRefPubMed
33.
Miranda M, Dos S, Bressan FF, Zecchin KG, Vercesi AE, Mesquita LG, Merighe GK, King WA, Ohashi OM, Pimentel JR, Perecin F, Meirelles FV: Serum starved apoptotic fibroblasts reduce blastocyst production but enable development to term after SCNT in cattle. Cloning Stem Cells. 2009, 11: 565-573. 10.1089/clo.2009.0028.CrossRef
34.
Lonergan P, Rizos D, Gutierrez-Adan A, Fair T, Boland MP: Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns. Reprod Dom Anim. 2003, 38: 259-67. 10.1046/j.1439-0531.2003.00437.x.CrossRef
35.
Holm P, Booth PJ, Schmidt MH, Greve T, Callesen H: High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins. Theriogenology. 1999, 52: 683-700. 10.1016/S0093-691X(99)00162-4.CrossRefPubMed
36.
Mondou E, Dufort I, Gohin M, Fournier E, Sirard MA: Analysis of microRNAs and their precursors in bovine early embryonic development. Mol Hum Reprod. 2012, 18: 425-34. 10.1093/molehr/gas015.CrossRefPubMed
37.
Reybier K, Perio P, Ferry G, Bouajila J, Delagrange P, Boutin JA, Nepveu F: Insights into the redox cycle of human quinone reductase 2. Free Radic Res. 2011, 45: 1184-1195. 10.3109/10715762.2011.605788.CrossRefPubMed
38.
Aversa S, Pellegrino S, Barberi I, Reiter RJ, Gitto E: Potential utility of melatonin as an antioxidant during pregnancy and in the perinatal period. J Matern Fetal Neonatal Med. 2011, 25: 207-221.CrossRefPubMed
39.
Espino J, Ortiz A, Bejarano I, Lozano GM, Monllor F, García JF, Rodríguez AB, Pariente JA: Melatonin protects human spermatozoa from apoptosis via melatonin receptor- and extracellular signal-regulated kinase-mediated pathways. Fertil Steril. 2011, 95: 2290-2296. 10.1016/j.fertnstert.2011.03.063.CrossRefPubMed
40.
El-Raey M, Geshi M, Somfai T, Kaneda M, Hirako M, Abdel-Ghaffar AE, Sosa GA, El-Roos ME, Nagai T: Evidence of melatonin synthesis in the cumulus oocyte complexes and its role in enhancing oocyte maturation in vitro in cattle. Mol Reprod Dev. 2011, 78: 250-262. 10.1002/mrd.21295.CrossRefPubMed
41.
Sampaio LFS: Melatonin inhibitory effect on cAMP accumulation in the chick retina development. Int J Dev Neurosci. 2008, 26: 277-282. 10.1016/j.ijdevneu.2008.02.001.CrossRef
42.
Dubocovich ML, Delagrange P, Krause DN, Sugden D, Cardinali DP, Olcese J: International Union of Basic and Clinical Pharmacology. LXXV. Nomenclature, classification, and pharmacology of G protein-coupled melatonin receptors. Pharmacol Rev. 2010, 62: 343-380. 10.1124/pr.110.002832.PubMedCentralCrossRefPubMed
43.
Bilodeau-Goeseels S: Cows are not mice: the role of cyclic AMP, phosphodiesterases, and adenosine monophosphate-activated protein kinase in the maintenance of meiotic arrest in bovine oocytes. Mol Reprod Dev. 2011, 78: 734-743. 10.1002/mrd.21337.CrossRefPubMed
Metadata
Title
MT3 melatonin binding site, MT1 and MT2 melatonin receptors are present in oocyte, but only MT1 is present in bovine blastocyst produced in vitro
Authors
Rafael V Sampaio
Dhúllia Stefanne B Conceição
Moysés S Miranda
Lucia de Fatima S Sampaio
Otávio Mitio Ohashi
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2012
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-10-103

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