Melatonin protects uterus and oviduct exposed to nicotine in mice

Seyed Saadat, Seyedeh Nazanin; Mohammadghasemi, Fahimeh; Khajeh Jahromi, Sina; Homafar, Mohammad Amin; Haghiri, Mostafa

doi:10.2478/intox-2014-0007

Abstract

Smoking is associated with higher infertility risk. The aim of this study was to evaluate protective effects of melatonin on the uterus and oviduct in mice exposed to nicotine. Adult female mice (n=32) were divided into four groups. Group A: control animals received normal saline, Group B: injected with nicotine 40 μg/kg, Group C: injected with melatonin 10 μg, Group D: injected with nicotine 40 μg/kg and melatonin 10 μg. All animals were treated over 15 days intraperitoneally. On the 16^th day, animals in the estrus phase were dissected and their uterus and oviducts were removed. Immunohistochemistry was recruited for studying apoptosis and for detection of estrogen receptor (ER) alpha in luminal epithelium of the uterus and oviduct. Enzyme-linked immunosorbent assay was used for serum estradiol level determination. Nicotine in group B decreased estradiol level and ERalpha numbers both in the uterus and oviduct (p<0.05). Co-administration of melatonin-nicotine in Group D ameliorated the histology of the uterus and oviduct, increased ERalpha numbers and reduced apoptosis in the uterus and oviduct compared with the nicotine Group B (p<0.05). This study indicates that nicotine impairs the histology of the uterus and oviduct and co-administration of melatonin-nicotine ameliorates these findings, partly through alteration in ERalpha numbers and reduction of apoptosis

References

Abd-Allah AR, El-Sayed el SM, Abdel-Wahab MH, Hamada FM. (2003). Effect of melatonin on estrogen and progesterone receptors in relation to uterine contraction in rats. Pharmacol Res 47: 349-354.
Search in Google Scholar
Adriaens I, Jacquet P, Cortvrindt R, Janssen K, Smitz J. (2006). Melatonin has dose-dependent effects on folliculogenesis, oocyte maturation capacity and steroidogenesis. Toxicology 228: 333-343.
Search in Google Scholar
Barbieri RL, Sluss PM, Powers RD, McShane PM, Vitonis A, Ginsburg E, Cramer DC. (2005). Association of body mass index, age, and cigarette smoking with serum testosterone levels in cycling women undergoing in vitro fertilization. Fertil Steril 83: 302-308.
Search in Google Scholar
Bodis J, Hanf V, Torok A, Tinneberg HR, Borsay P, Szabo I. (1997). Influence of nicotine on progesterone and estradiol production of cultured human granulosa cells. Early Pregnancy 3: 34-37.
Search in Google Scholar
Byers M, Kuiper GG, Gustafsson JA, Park-Sarge OK. (1997). Estrogen receptorbeta mRNA expression in rat ovary: down-regulation by gonadotropins. Mol Endocrinol 11: 172-182.
Search in Google Scholar
Chuffa LG, Seiva FR, Favaro WJ, Amorim JP, Teixeira GR, Mendes LO, Fioruci- Fontanelli BA, Pinheiro PF, Martinez M, Martinez FE. (2013). Melatonin and ethanol intake exert opposite effects on circulating estradiol and progesterone and differentially regulate sex steroid receptors in the ovaries, oviducts, and uteri of adult rats. Reprod Toxicol 39: 40-49.
Search in Google Scholar
Danforth DN, Jr., Tamarkin L, Do R, Lippman ME. (1983). Melatonin-induced increase in cytoplasmic estrogen receptor activity in hamster uteri. Endocrinology 113: 81-85.
Search in Google Scholar
Dechanet C, Anahory T, Mathieu Daude JC, Quantin X, Reyftmann L, Hamamah S, Hedon B, Dechaud H. (2011). Effects of cigarette smoking on reproduction. Hum Reprod Update 17: 76-95.
Search in Google Scholar
Emmen JM, Couse JF, Elmore SA, Yates MM, Kissling GE, Korach KS. (2005). In vitro growth and ovulation of follicles from ovaries of estrogen receptor (ER){alpha} and ER{beta} null mice indicate a role for ER{beta} in follicular maturation. Endocrinology 146: 2817-2826.
Search in Google Scholar
Garcia-Navarro A, Gonzalez-Puga C, Escames G, Lopez LC, Lopez A, Lopez- Cantarero M, Camacho E, Espinosa A, Gallo MA, Acuna-Castroviejo D. (2007). Cellular mechanisms involved in the melatonin inhibition of HT-29 human colon cancer cell proliferation in culture. J Pineal Res 43: 195-205.
Search in Google Scholar
Ghasemi F, Faghani M, Khajehjahromi S, Bahadori M, Nasiri E, Hemadi M. ( 2010). Effect of Melatonin on proliferative activity and apoptosis in spermatogenic cells in mouse under chemotherapy. Journal of Reproduction & contraception 21: 79-94.10.1016/S1001-7844(10)60016-8
Search in Google Scholar
Gocze PM, Szabo I, Freeman DA. (1999). Influence of nicotine, cotinine, anabasine and cigarette smoke extract on human granulosa cell progesterone and estradiol synthesis. Gynecol Endocrinol 13: 266-272.
Search in Google Scholar
Guneli E, Tugyan K, Ozturk H, Gumustekin M, Cilaker S, Uysal N. (2008). Effect of melatonin on testicular damage in streptozotocin-induced diabetes rats. Eur Surg Res 40: 354-360.
Search in Google Scholar
Heldring N, Pike A, Andersson S. (2007). Estrogen receptors: how do they signal and what are their targets. Physiol Rev 87: 905-931.
Search in Google Scholar
Kummer S, Jeruschke S, Wegerich LV, Peters A, Lehmann P, Seibt A, Mueller F, Koleganova N, Halbenz E, Schmitt CP, Bettendorf M, Mayatepek E, Gross- Weissmann ML, Oh J. (2011). Estrogen receptor alpha expression in podocytes mediates protection against apoptosis in-vitro and in-vivo. PLoS One 6: e27457.
Search in Google Scholar
Meresman G. (2011). Relevance of apoptosis in the female reproductive system. Invest Clin 52: 274-290.
Search in Google Scholar
Michnovicz JJ, Hershcopf RJ, Naganuma H, Bradlow HL, Fishman J. (1986). Increased 2-hydroxylation of estradiol as a possible mechanism for the antiestrogenic effect of cigarette smoking. N Engl J Med 315: 1305-1309.
Search in Google Scholar
Mohammadghasemi F, Jahromi SK, Hajizadeh H, Homafar MA, Saadat N. (2012). The protective effects of exogenous melatonin on nicotine-induced changes in mouse ovarian follicles. J Reprod Infertil 13: 143-150.
Search in Google Scholar
Petrik JJ, Gerstein HC, Cesta CE, Kellenberger LD, Alfaidy N, Holloway AC. (2009). Effects of rosiglitazone on ovarian function and fertility in animals with reduced fertility following fetal and neonatal exposure to nicotine. Endocrine 36: 281-290.
Search in Google Scholar
Sanders SR, Cuneo SP, Turzillo AM. (2002). Effects of nicotine and cotinine on bovine theca interna and granulosa cells. Reprod Toxicol 16: 795-800.
Search in Google Scholar
Shao R, Feng Y, Zou S, Weijdegard B, Wu G, Brannstrom M, Billig H. (2012). The role of estrogen in the pathophysiology of tubal ectopic pregnancy. Am J Transl Res 4: 269-278.
Search in Google Scholar
Take G, Erdogan D, Helvacioglu F, Goktas G, Ozbey G, Uluoglu C, Yucel B, Guney Y, Hicsonmez A, Ozkan S. (2009). Effect of melatonin and time of administration on irradiation-induced damage to rat testes. Braz J Med Biol Res 42: 621-628.
Search in Google Scholar
Tamura H, Nakamura Y, Korkmaz A, Manchester LC, Tan DX, Sugino N, Reiter RJ. (2009). Melatonin and the ovary: physiological and pathophysiological implications. Fertil Steril 92: 328-343.
Search in Google Scholar
Tanavde VS, Maitra A. (2003). In vitro modulation of steroidogenesis and gene expression by melatonin: a study with porcine antral follicles. Endocr Res 29: 399-410.
Search in Google Scholar
Tuttle AM, Stampfli M, Foster WG. (2009). Cigarette smoke causes follicle loss in mice ovaries at concentrations representative of human exposure. Hum Reprod 24: 1452-1459.
Search in Google Scholar
Wang H, Eriksson H, Sahlin L. (2000). Estrogen receptors alpha and beta in the female reproductive tract of the rat during the estrous cycle. Biol Reprod 63: 1331-1340.
Search in Google Scholar
Wang H, Masironi B, Eriksson H, Sahlin L. (1999). A comparative study of estrogen receptors alpha and beta in the rat uterus. Biol Reprod 61: 955-964.
Search in Google Scholar
Woo MM, Tai CJ, Kang SK, Nathwani PS, Pang SF, Leung PC. (2001). Direct action of melatonin in human granulosa-luteal cells. J Clin Endocrinol Metab 86: 4789-4797.
Search in Google Scholar
Yoo YM, Jeung EB. (2009). Melatonin-induced estrogen receptor alpha-mediated calbindin-D9k expression plays a role in H2O2-mediated cell death in rat pituitary GH3 cells. J Pineal Res 47: 301-307.
Search in Google Scholar

Melatonin protects uterus and oviduct exposed to nicotine in mice

Abstract

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