Melatonin reduces LH, 17 beta-estradiol and induces differential regulation of sex steroid receptors in reproductive tissues during rat ovulation

Reproductive Biology and Endocrinology

Volumn 9, Issue , 2011, Pages

  A Chuffa, Luiz Gustavo ^a,b   Seiva, Fábio R F ^b   Fávaro, Wagner J ^b   Teixeira, Giovana R ^b   Amorim, João P A ^a,b   Mendes, Leonardo O ^a,b   Fioruci, Beatriz A ^a,b   Pinheiro, Patrícia Fernanda F ^b   Fernandes, Ana Angélica H ^b   Franci, Janete A A ^d   Delella, Flávia K ^a   Martinez, Marcelo ^c   Martinez, Francisco E ^b  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO CARLOS   (Brazil)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

6 SULFATOXIMELATONIN; ANDROGEN RECEPTOR; ESTRADIOL; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; HORMONE RECEPTOR; LUTEINIZING HORMONE; MELATONIN; MELATONIN RECEPTOR; PROGESTERONE RECEPTOR; PROGESTERONE RECEPTOR A; PROGESTERONE RECEPTOR B; SEX STEROID RECEPTOR; UNCLASSIFIED DRUG; MELATONIN 1 RECEPTOR; STEROID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENDOCRINE DISEASE; ESTRUS; FEMALE; HORMONE BLOOD LEVEL; NONHUMAN; OVARY; OVIDUCT; OVULATION; PROTEIN EXPRESSION; RAT; UPREGULATION; UTERUS; ANIMAL; BLOOD; DRUG EFFECT; METABOLISM; REPRODUCTION; UTERINE TUBE; WISTAR RAT;

ANIMALIA; RATTUS; RATTUS NORVEGICUS;

ANIMALS; ESTRADIOL; FALLOPIAN TUBES; FEMALE; LUTEINIZING HORMONE; MELATONIN; OVARY; OVULATION; RATS; RATS, WISTAR; RECEPTOR, MELATONIN, MT1; RECEPTORS, STEROID; REPRODUCTION; UTERUS;

EID: 79960889533     PISSN: None     EISSN: 14777827     Source Type: Journal    
DOI: 10.1186/1477-7827-9-108     Document Type: Article

References (54)

1. Masana MI, Dubocovich ML. Melatonin receptor signaling: finding the path through the dark. Sci STKE 2001, 107:pe39.
2. 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, 16:336-347. 10.1177/074873001129002051, 11506379.
3. Glass JD, Knotts LK. A brain site for the antigonadal action of melatonin in the white-footed mouse (Peromyscus leucopus): involvement of the immunoreactive GnRH neuronal system. Neuroendocrinology 1987, 46:48-55. 10.1159/000124795, 3302747.
4. Ronnberg L, Kauppila A, Leppaluoto J, Martikainen H, Vakkuri O. Circadian and seasonal variation in human preovulatory follicular fluid melatonin concentration. J Clin Endocrinol Metab 1990, 71:492-496.
5. 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, 18804205.
6. Dardes RC, Baracat EC, Simões MJ. Modulation of estrous cycle and LH, FSH and melatonin levels by pinealectomy and sham-pinealectomy in female rats. Prog Neuropsychopharmacol Biol Psychiatry 2000, 24:441-453. 10.1016/S0278-5846(99)00110-4, 10836491.
7. Soares JM, Simões MJ, Oshima CT, Mora OA, De Lima GR, Baracat EC. Pinealectomy changes rat ovarian interstitial cell morphology and decreases progesterone receptor expression. Gynecol Endocrinol 2003, 17:115-123.
8. Okatani Y, Morioka N, Hayashi K. Changes in nocturnal pineal melatonin synthesis during the premenopausal period: relation to estrogen levels in female rats. J Pineal Res 1999, 27:65-72. 10.1111/j.1600-079X.1999.tb00598.x, 10496141.
9. Chuffa LG, Amorim JP, Teixeira GR, Mendes LO, Fioruci BA, Pinheiro PF, Seiva FR, Novelli EL, Mello Júnior W, Martinez M, Martinez FE. Long-term melatonin treatment reduces ovarian mass and enhances tissue antioxidant defenses during ovulation in the rat. Braz J Med Biol Res 2011, 44:217-223. 10.1590/S0100-879X2011007500018, 21344135.
10. Kachi T, Tanaka D, Watanabe S, Suzuki R, Tonosaki Y, Fujieda H. Physiological pineal effects on female reproductive function of laboratory rats: prenatal development of pups, litter size and estrous cycle in middle age. Chronobiol Int 2006, 23:289-300. 10.1080/07420520600588713, 16687302.
11. Diaz E, Pazo D, Esquifino AI, Diaz B. Effects of ageing and exogenous melatonin on pituitary responsiveness to GnRH in rats. J Reprod Fertil 2000, 119:151-156.
12. Díaz E, Fernández C, Castrillón PO, Esquifino AI, Marín B, Díaz López B. Effect of exogenous melatonin on neuroendocrine-reproductive function of middle-aged female rats. J Reprod Fertil 1999, 117:331-337. 10.1530/jrf.0.1170331, 10690201.
13. Abd-Allah AR, El-Sayed EM, Abdel-Wahab MH, Hamada FM. Effect of melatonin on estrogen and progesterone receptors in relation to uterine contraction in rats. Pharmacol Res 2003, 47:349-354. 10.1016/S1043-6618(03)00014-8, 12644393.
14. Rato AG, Pedrero JG, Martinez MA, Del Rio B, Lazo PS, Ramos S. Melatonin blocks the activation of estrogen receptor for DNA binding. FASEB J 1999, 13:857-868.
15. Romeu LRG, Motta ELA, Maganhin CC, Oshima CTF, Fonseca MC, Barrueco KF, Simões RS, Pellegrino R, Baracat EC, Soares-Junior JM. Effects of melatonin on histomorphology and on the expression of steroid receptors, VEGF, and PCNA in ovaries of pinealectomized female rats. Fertil Steril 2011, 95:1379-1384. 10.1016/j.fertnstert.2010.04.042, 20605140.
16. Horne AW, King AE, Shaw E, McDonald SE, Williams AR, Saunders PT, Critchley HO. Attenuated sex steroid receptor expression in fallopian tube of women with ectopic pregnancy. J Clin Endocrinol Metab 2009, 94:5146-5154. 10.1210/jc.2009-1476, 2989877, 19864448.
17. Mulac-Jericevic B, Lydon JP, DeMayo FJ, Conneely OM. Defective mammary gland morphogenesis in mice lacking the progesterone receptor B isoform. Proc Natl Acad Sci 2003, 100:9744-9749. 10.1073/pnas.1732707100, 187836, 12897242.
18. Kuiper GGJM, Enmark E, Pelto Huikko M, Nilsson S, Gustafsson JA. Cloning of a novel estrogen receptor expressed in rat prostate and ovary. Proc Natl Acad Sci 1996, 93:5925-5930. 10.1073/pnas.93.12.5925, 39164, 8650195.
19. Okada A, Sato T, Ohta Y, Iguchi T. Sex steroid hormone receptors in the developing female reproductive tract of laboratory rodents. J Toxicol Sci 2005, 30:75-89. 10.2131/jts.30.75, 15928456.
20. Bardin A, Hoffmann P, Boulle N, Katsaros D, Vignon F, Pujol P, Lazennec G. Involvement of estrogen receptor beta in ovarian carcinogenesis. Cancer Res 2004, 64:5861-5869. 10.1158/0008-5472.CAN-04-0552, 15313930.
21. Kraus WL, Montano MM, Katzenellenbogen BS. Identification of multiple, widely spaced estrogen-responsive regions in the rat progesterone receptor gene. Mol Endocrinol 1994, 8:952-969. 10.1210/me.8.8.952, 7997237.
22. Schneider W, Ramachandran C, Satyaswaroop PG, Shyamala G. Murine progesterone receptor exists predominantly as the 83-kDa A form. J Steroid Biochem Mol Biol 1991, 38:285-291. 10.1016/0960-0760(91)90099-Q, 2009220.
23. Syvala H, Vienonen A, Ylikomi T, Blauer M, Zhuang Y, Tuohimaa P. Expression of the chicken progesterone receptor forms A and B is differentially regulated by estrogen in vivo. Biochem Biophys Res Commun 1997, 231:573-576. 10.1006/bbrc.1997.6149, 9070848.
24. Benitez-King G. Melatonin as a cytoskeletal modulator: implications for cell physiology and disease. J Pineal Res 2006, 40:1-9. 10.1111/j.1600-079X.2005.00282.x, 16313492.
25. Olsen NJ, Kovacs WJ. Gonadal steroids and immunity. Endocr Rev 1996, 17:369-384.
26. Molis TM, Spriggs LL, Hill SM. Modulation of estrogen receptor mRNA expression by melatonin in MCF-7 human breast cancer cells. Mol Endocrinol 1994, 8:1681-1690. 10.1210/me.8.12.1681, 7708056.
27. Revel FG, Ansel L, Klosen P, Saboureau M, Pevet P, Mikkelsen JD, Simonneaux V. Kisspeptin: a key link to seasonal breeding. Rev Endocr Metab Disord 2007, 8:57-65. 10.1007/s11154-007-9031-7, 17380397.
28. Malpaux B, Thiéry JC, Chemineau P. Melatonin and the seasonal control of reproduction. Reprod Nutr Dev 1999, 39:355-366. 10.1051/rnd:19990308, 10420438.
29. Revel FG, Saboureau M, Masson-Pevet M, Pevet P, Mikkelsen JD, Simonneaux V. Kisspeptin mediates the photoperiodic control of reproduction in hamsters. Curr Biol 2006, 16:1730-1735. 10.1016/j.cub.2006.07.025, 16950111.
30. Chiba A, Akema T, Toyoda J. Effects of pinealectomy and melatonin on the timing of the proestrous luteinizing hormone surge in the rat. Neuroendocrinology 1994, 59:163-168. 10.1159/000126654, 8127406.
31. Reiter RJ, Johnson LY, Vanghan MK, Richardson BA, Petterborg LJ. Variation in pineal melatonin content during the estrous cycle of the rat. Proc Soc Exp Biol Med 1982, 169:416-419.
32. Brzezinski A, Seibel MM, Lynch HJ, Deng MH, Wurtman RJ. Melatonin in human preovulatory follicular fluid. J Clin Endocrinol Metab 1987, 64:865-867. 10.1210/jcem-64-4-865, 3818907.
33. Macchi MM, Bruce JN. Human pineal physiology and functional significance of melatonin. Front Neuroendocrinol 2004, 25:177-195. 10.1016/j.yfrne.2004.08.001, 15589268.
34. Tamura H, Nakamura Y, Takiguchi S, Kashida S, Yamagata Y, Sugino N, Kato H. Melatonin directly suppresses steroid production by preovulatory follicles in the cyclic hamster. J Pineal Res 1998, 25:135-141. 10.1111/j.1600-079X.1998.tb00551.x, 9745981.
35. Martínez-Campa CM, González A, Mediavilla MD, Alonso-González C, Sánchez-Barceló EJ, Cos S. Melatonin enhances the inhibitory effect of aminoglutethimide on aromatase activity in MCF-7 human breast cancer cells. Breast Cancer Res Treat 2005, 94:249-254. 10.1007/s10549-005-9006-x, 16244789.
36. Graham C, Cook MR, Kavet R, Sastre A, Smith DK. Prediction of nocturnal plasma melatonin from morning urinary measures. J Pineal Res 1998, 24:230-238. 10.1111/j.1600-079X.1998.tb00538.x, 9572533.
37. Wurtman RJ, Axelrod J, Chu EW. Melatonin, a pineal substance: effect on the rat ovary. Science 1963, 141:277-278. 10.1126/science.141.3577.277, 14002083.
38. Chuffa LG, Amorim JP, Teixeira GR, Mendes LO, Fioruci BA, Pinheiro PF, Seiva FR, Novelli EL, de Mello Júnior W, Martinez M, Almeida-Francia CC, Martinez FE. Long-term exogenous melatonin treatment modulates overall feed efficiency and protects ovarian tissue against injuries caused by ethanol-induced oxidative stress in adult UChB rats. Alcohol Clin Exp Res 2011, 35:1498-1508.
39. Adriaens I, Jacquet P, Cortvrindt R, Janssen K, Smitz J. Melatonin has dose-dependent effects on folliculogenesis, oocyte maturation capacity and steroidogenesis. Toxicology 2006, 228:333-343. 10.1016/j.tox.2006.09.018, 17084011.
40. Brzezinski A, Fibich T, Cohen M, Schenker JG, Laufer N. Effects of melatonin on progesterone production by human granulosa lutein cells in culture. Fertil Steril 1992, 58:526-529.
41. Aronika SM, Kraus WL, Katzenellenbogen BS. Estrogen action via the cAMP signaling pathway: stimulation of adenylate cyclase and cAMP-regulated gene transcription. Proc Natl Acad Sci 1994, 91:8517-8521. 10.1073/pnas.91.18.8517, 44637, 8078914.
42. Godson C, Reppert SM. The mel1a melatonin receptor is coupled to parallel signal transduction pathways. Endocrinology 1997, 138:397-404. 10.1210/en.138.1.397, 8977429.
43. Chalbos D, Galtier F. Differential effect of forms A and B of human progesterone receptor on estradiol-dependent transcription. J Biol Chem 1994, 269:23007-23012.
44. Vegeto E, Shahbaz MM, Wen DX, Goldman ME, O'Malley BW, McDonnell DP. Human progesterone receptor A form is a celland promoter-specific repressor of human progesterone receptor B function. Mol Endocrinol 1993, 7:1244-1255. 10.1210/me.7.10.1244, 8264658.
45. Okatani Y, Watanabe K, Morioka N, Hayashi K, Sagara Y. Nocturnal change in pineal melatonin synthesis during puberty: relation to estrogen and progesterone levels in female rats. J Pineal Res 1997, 22:33-41. 10.1111/j.1600-079X.1997.tb00300.x, 9062868.
46. Moujir F, Bordon R, Santana C, Abreu P, Hernandez G, Alonso R. Ovarian steroids block the isoproterenol-induced elevation of pineal melatonin production in the female rat. Neurosci Lett 1990, 119:12-14. 10.1016/0304-3940(90)90743-S, 1982958.
47. Giangrande PH, Pollio G, McDonnell DP. Mapping and characterization of the functional domains responsible for the differential activity of the A and B isoforms of the human progesterone receptor. J Biol Chem 1997, 272:32889-32900. 10.1074/jbc.272.52.32889, 9407067.
48. Mulac-Jericevic B, Conneely OM. Reproductive tissue selective actions of progesterone receptors. Reproduction 2004, 128:139-146. 10.1530/rep.1.00189, 15280552.
49. Cos S, González A, Martínez-Campa C, Mediavilla MD, Alonso-González C, Sánchez-Barceló EJ. Estrogen-signaling pathway: a link between breast cancer and melatonin oncostatic actions. Cancer Detect Prev 2006, 30:118-128. 10.1016/j.cdp.2006.03.002, 16647824.
50. Li W, Boomsma RA, Verhage HG. Immunocytochemical analysis of estrogen and progestin receptors in uteri of steroid-treated and pregnant cats. Biol Reprod 1992, 47:1073-1081. 10.1095/biolreprod47.6.1073, 1493171.
51. Zhao H, Pang SF, Poon AMS. Variations of mt1 melatonin receptor density in the rat uterus during decidualization, the estrous cycle and in response to exogenous steroid treatment. J Pineal Res 2002, 33:140-145. 10.1034/j.1600-079X.2002.02898.x, 12220327.
52. Tibbetts TA, Mendoza-Meneses M, O'Malley BW, Conneely OM. Mutual and intercompartmental regulation of estrogen receptor and progesterone receptor expression in the mouse uterus. Biol Reprod 1998, 59:1143-1152. 10.1095/biolreprod59.5.1143, 9780321.
53. Kuiper GJM, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson JA. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors α and β. Endocrinology 1997, 138:863-870. 10.1210/en.138.3.863, 9048584.
54. Clemens JW, Jarzynka MJ, Witt-Enderby PA. Down-regulation of mt1 melatonin receptors in rat ovary following estrogen exposure. Life Sci 2001, 69:27-35. 10.1016/S0024-3205(01)01097-9, 11411803.