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Ethanol promotes apoptosis in rat ovarian granulosa cells via the Bcl-2 family dependent intrinsic apoptotic pathway
Corresponding Author(s) : Jingyuan Xiong
Cellular and Molecular Biology,
Vol. 64 No. 1: Issue 1
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- Lim SS, Vos T, Flaxman AD, Danaei G, Shibuya K, Adair-Rohani H, et al. A comparative risk assessment of burden of disease and injury attributable to 67 risk factors and risk factor clusters in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012; 380: 2224-2260.
- Rehm J, Baliunas D, Borges GL, Graham K, Irving H, Kehoe T, et al. The relation between different dimensions of alcohol consumption and burden of disease: an overview. Addiction 2010; 105: 817-843.
- Clair C, Rigotti NA, Porneala B, Fox CS, D'Agostino RB, Pencina MJ, et al. Association of smoking cessation and weight change with cardiovascular disease among adults with and without diabetes. Jama 2013; 309: 1014-1021.
- Freedman ND, Leitzmann MF, Hollenbeck AR, Schatzkin A, Abnet CC. Cigarette smoking and subsequent risk of lung cancer in men and women: analysis of a prospective cohort study. Lancet Oncol 2008; 9: 649-656.
- Zhou S, Zhou R, Zhong T, Li R, Tan J, Zhou H. Association of smoking and alcohol drinking with dementia risk among elderly men in China. Curr Alzheimer Res 2014; 11: 899-907.
- Cicero TJ, Bell RD. Ethanol-induced reductions in testicular steroidogenesis: major differences between in vitro and in vitro approaches. Steroids 1982; 40: 561-568.
- Eid NA, Shibata MA, Ito Y, Kusakabe K, Hammad H, Otsuki Y. Involvement of Fas system and active caspases in apoptotic signalling in testicular germ cells of ethanol-treated rats. Int J Androl 2002; 25: 159-167.
- Villalta J, Ballescí JL, Nicolás JM, Martínez de Osaba MJ, Antúnez E, Pimentel C. Testicular function in asymptomatic chronic alcoholics: relation to ethanol intake. Alcohol Clin Exp Res 1997; 21: 128-133.
- Hadi HA, Hill JA, Castillo RA. Alcohol and reproductive function: a review. Obstet Gynecol Surv 1987; 42(2): 69-74.
- Pajarinen JT, Karhunen PJ. Spermatogenic arrest and ‘Sertoli cell-only' syndrome-common alcohol-induced disorders of the human testis. Int J Androl 1994; 17: 292-299.
- Ramlau-Hansen CH, Toft G, Jensen MS, Strandberg-Larsen K, Hansen ML, Olsen J. Maternal alcohol consumption during pregnancy and semen quality in the male offspring: two decades of follow-up. Hum Reprod 2010; 25: 2340-2345.
- Muralidharan P, Sarmah S, Zhou FC, Marrs JA. Fetal alcohol spectrum disorder (FASD) associated neural defects: complex mechanisms and potential therapeutic targets. Brain Sci 2013; 3: 964-991.
- Patra J, Bakker R, Irving H, Jaddoe VW, Malini S, Rehm J. Dose-response relationship between alcohol consumption before and during pregnancy and the risks of low birthweight, preterm birth and small for gestational age (SGA)-a systematic review and meta-analyses. BJOG 2011; 118: 1411-1421.
- Hakim RB, Gray RH, Zacur H. Alcohol and caffeine consumption and decreased fertility. Fertil Steril 1998; 70: 632-637.
- Jensen TK, Hjollund NH, Henriksen TB, Scheike T, Kolstad H, Giwercman A, et al. Does moderate alcohol consumption affect fertility? Follow up study among couples planning first pregnancy. BMJ 1998; 317: 505-510.
- Mello NK, Bree MP, Mendelson JH, Ellingboe J, King NW, Sehgal P. Alcohol self-administration disrupts reproductive function in female macaque monkeys. Science 1983; 221: 677-679.
- Gavaler JS, Van Thiel DH, Lester R. Ethanol: a gonadal toxin in the mature rat of both sexes. Alcohol Clin Exp Res 1980; 4: 271-276.
- Binelli M, Murphy BD. Coordinated regulation of follicle development by germ and somatic cells. Reprod Fertil Dev 2010; 22: 1-12.
- Matsuda F, Inoue N, Manabe N, Ohkura S. Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells. J Reprod Dev 2012; 58: 44-50.
- Manabe N, Goto Y, Matsuda-Minehata F, Inoue N, Maeda A, Sakamaki K, et al. Regulation mechanism of selective atresia in porcine follicles: regulation of granulosa cell apoptosis during atresia. J Reprod Dev 2004; 50: 493-514.
- Jin X, Xiao LJ, Zhang XS, Liu YX. Apoptosis in ovary. Front Biosci (Schol Ed) 2011; 3: 680-697.
- Ku BM, Lee YK, Jeong JY, Mun J, Han JY, Roh GS, et al. Ethanol-induced oxidative stress is mediated by p38 MAPK pathway in mouse hippocampal cells. Neurosci Lett 2007; 419: 64-67.
- Do H, Park HJ, Sohn EH, Kim BO, Um SH, Kwak JH, et al. Ethanol induces cell cycle arrest and triggers apoptosis via Sp1-dependent p75NTR expression in human neuroblastoma cells. Cell Biol Toxicol 2013; 29: 365-380.
- Guo W, Baluda MA, Park NH. Ethanol upregulates the expression of p21 WAF1/CIP1 and prolongs G1 transition via a p53-independent pathway in human epithelial cells. Oncogene 1997; 15: 1143-1149.
- Ku BM, Joo Y, Mun J, Roh GS, Kang SS, Cho GJ, et al. Heme oxygenase protects hippocampal neurons from ethanol-induced neurotoxicity. Neurosci Lett 2006; 405: 168-171.
- Yamamoto CM, Sinha Hikim AP, Huynh PN, Shapiro B, Lue Y, Salameh WA, et al. Redistribution of Bax is an early step in an apoptotic pathway leading to germ cell death in rats, triggered by mild testicular hyperthermia. Biol Reprod 2000; 63: 1683-1690.
- Tamura DY, Moore EE, Partrick DA, Johnson JL, Offner PJ, Harbeck RJ, et al. Clinically relevant concentrations of ethanol attenuate primed neutrophil bactericidal activity. J Trauma 1998; 44: 320-324.
- Kokoszka JE, Waymire KG, Levy SE, Sligh JE, Cai J, Jones DP, et al. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 2004; 427: 461-465.
- Cho CC, Su LH, Huang YC, Pan YJ, Sun CH. Regulation of a Myb transcription factor by cyclin-dependent kinase 2 in Giardia lamblia. J Biol Chem 2012; 287: 3733-3750.
- Lovekamp-Swan T, Davis BJ. Mechanisms of phthalate ester toxicity in the female reproductive system. Environ Health Perspect 2003; 111: 139-145.
- Hsueh AJ, Billig H, Tsafriri A. Ovarian follicle atresia: a hormonally controlled apoptotic process. Endocr Rev 1994; 15: 707-724.
- Hussein MR. Apoptosis in the ovary: molecular mechanisms. Hum Reprod Update 2005; 11: 162-177.
- Jiang JY, Cheung CK, Wang Y, Tsang BK. Regulation of cell death and cell survival gene expression during ovarian follicular development and atresia. Front Biosci 2003; 8: d222-237
- Hughes FM Jr, Gorospe WC. Biochemical identification of apoptosis (programmed cell death) in granulosa cells: evidence for a potential mechanism underlying follicular atresia. Endocrinology 1991; 129: 2415-2422.
- Drevnick PE, Sandheinrich MB, Oris JT. Increased ovarian follicular apoptosis in fathead minnows (Pimephales promelas) exposed to dietary methylmercury. Aquat Toxicol 2006; 79: 49-54.
- Kaipia A, Hsueh AJ. Regulation of ovarian follicle atresia. Annu Rev Physiol 1997. 59: 349-363.
- Boone DL, Tsang BK. Caspase-3 in the rat ovary: localization and possible role in follicular atresia and luteal regression. Biol Reprod 1998; 58: 1533-1539.
- Tang XL, Yang XY, Jung HJ, Kim SY, Jung SY, Choi DY, et al. Asiatic acid induces colon cancer cell growth inhibition and apoptosis through mitochondrial death cascade. Biol Pharm Bull 2009; 32: 1399-1405.
- Groc L, Bezin L, Jiang H, Jackson TS, Levine RA. Bax, Bcl-2, and cyclin expression and apoptosis in rat substantia nigra during development. Neurosci Lett 2001; 306: 198-202.
- Oltvai ZN, Milliman CL, Korsmeyer SJ. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 1993; 74: 609-619.
References
Lim SS, Vos T, Flaxman AD, Danaei G, Shibuya K, Adair-Rohani H, et al. A comparative risk assessment of burden of disease and injury attributable to 67 risk factors and risk factor clusters in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012; 380: 2224-2260.
Rehm J, Baliunas D, Borges GL, Graham K, Irving H, Kehoe T, et al. The relation between different dimensions of alcohol consumption and burden of disease: an overview. Addiction 2010; 105: 817-843.
Clair C, Rigotti NA, Porneala B, Fox CS, D'Agostino RB, Pencina MJ, et al. Association of smoking cessation and weight change with cardiovascular disease among adults with and without diabetes. Jama 2013; 309: 1014-1021.
Freedman ND, Leitzmann MF, Hollenbeck AR, Schatzkin A, Abnet CC. Cigarette smoking and subsequent risk of lung cancer in men and women: analysis of a prospective cohort study. Lancet Oncol 2008; 9: 649-656.
Zhou S, Zhou R, Zhong T, Li R, Tan J, Zhou H. Association of smoking and alcohol drinking with dementia risk among elderly men in China. Curr Alzheimer Res 2014; 11: 899-907.
Cicero TJ, Bell RD. Ethanol-induced reductions in testicular steroidogenesis: major differences between in vitro and in vitro approaches. Steroids 1982; 40: 561-568.
Eid NA, Shibata MA, Ito Y, Kusakabe K, Hammad H, Otsuki Y. Involvement of Fas system and active caspases in apoptotic signalling in testicular germ cells of ethanol-treated rats. Int J Androl 2002; 25: 159-167.
Villalta J, Ballescí JL, Nicolás JM, Martínez de Osaba MJ, Antúnez E, Pimentel C. Testicular function in asymptomatic chronic alcoholics: relation to ethanol intake. Alcohol Clin Exp Res 1997; 21: 128-133.
Hadi HA, Hill JA, Castillo RA. Alcohol and reproductive function: a review. Obstet Gynecol Surv 1987; 42(2): 69-74.
Pajarinen JT, Karhunen PJ. Spermatogenic arrest and ‘Sertoli cell-only' syndrome-common alcohol-induced disorders of the human testis. Int J Androl 1994; 17: 292-299.
Ramlau-Hansen CH, Toft G, Jensen MS, Strandberg-Larsen K, Hansen ML, Olsen J. Maternal alcohol consumption during pregnancy and semen quality in the male offspring: two decades of follow-up. Hum Reprod 2010; 25: 2340-2345.
Muralidharan P, Sarmah S, Zhou FC, Marrs JA. Fetal alcohol spectrum disorder (FASD) associated neural defects: complex mechanisms and potential therapeutic targets. Brain Sci 2013; 3: 964-991.
Patra J, Bakker R, Irving H, Jaddoe VW, Malini S, Rehm J. Dose-response relationship between alcohol consumption before and during pregnancy and the risks of low birthweight, preterm birth and small for gestational age (SGA)-a systematic review and meta-analyses. BJOG 2011; 118: 1411-1421.
Hakim RB, Gray RH, Zacur H. Alcohol and caffeine consumption and decreased fertility. Fertil Steril 1998; 70: 632-637.
Jensen TK, Hjollund NH, Henriksen TB, Scheike T, Kolstad H, Giwercman A, et al. Does moderate alcohol consumption affect fertility? Follow up study among couples planning first pregnancy. BMJ 1998; 317: 505-510.
Mello NK, Bree MP, Mendelson JH, Ellingboe J, King NW, Sehgal P. Alcohol self-administration disrupts reproductive function in female macaque monkeys. Science 1983; 221: 677-679.
Gavaler JS, Van Thiel DH, Lester R. Ethanol: a gonadal toxin in the mature rat of both sexes. Alcohol Clin Exp Res 1980; 4: 271-276.
Binelli M, Murphy BD. Coordinated regulation of follicle development by germ and somatic cells. Reprod Fertil Dev 2010; 22: 1-12.
Matsuda F, Inoue N, Manabe N, Ohkura S. Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells. J Reprod Dev 2012; 58: 44-50.
Manabe N, Goto Y, Matsuda-Minehata F, Inoue N, Maeda A, Sakamaki K, et al. Regulation mechanism of selective atresia in porcine follicles: regulation of granulosa cell apoptosis during atresia. J Reprod Dev 2004; 50: 493-514.
Jin X, Xiao LJ, Zhang XS, Liu YX. Apoptosis in ovary. Front Biosci (Schol Ed) 2011; 3: 680-697.
Ku BM, Lee YK, Jeong JY, Mun J, Han JY, Roh GS, et al. Ethanol-induced oxidative stress is mediated by p38 MAPK pathway in mouse hippocampal cells. Neurosci Lett 2007; 419: 64-67.
Do H, Park HJ, Sohn EH, Kim BO, Um SH, Kwak JH, et al. Ethanol induces cell cycle arrest and triggers apoptosis via Sp1-dependent p75NTR expression in human neuroblastoma cells. Cell Biol Toxicol 2013; 29: 365-380.
Guo W, Baluda MA, Park NH. Ethanol upregulates the expression of p21 WAF1/CIP1 and prolongs G1 transition via a p53-independent pathway in human epithelial cells. Oncogene 1997; 15: 1143-1149.
Ku BM, Joo Y, Mun J, Roh GS, Kang SS, Cho GJ, et al. Heme oxygenase protects hippocampal neurons from ethanol-induced neurotoxicity. Neurosci Lett 2006; 405: 168-171.
Yamamoto CM, Sinha Hikim AP, Huynh PN, Shapiro B, Lue Y, Salameh WA, et al. Redistribution of Bax is an early step in an apoptotic pathway leading to germ cell death in rats, triggered by mild testicular hyperthermia. Biol Reprod 2000; 63: 1683-1690.
Tamura DY, Moore EE, Partrick DA, Johnson JL, Offner PJ, Harbeck RJ, et al. Clinically relevant concentrations of ethanol attenuate primed neutrophil bactericidal activity. J Trauma 1998; 44: 320-324.
Kokoszka JE, Waymire KG, Levy SE, Sligh JE, Cai J, Jones DP, et al. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 2004; 427: 461-465.
Cho CC, Su LH, Huang YC, Pan YJ, Sun CH. Regulation of a Myb transcription factor by cyclin-dependent kinase 2 in Giardia lamblia. J Biol Chem 2012; 287: 3733-3750.
Lovekamp-Swan T, Davis BJ. Mechanisms of phthalate ester toxicity in the female reproductive system. Environ Health Perspect 2003; 111: 139-145.
Hsueh AJ, Billig H, Tsafriri A. Ovarian follicle atresia: a hormonally controlled apoptotic process. Endocr Rev 1994; 15: 707-724.
Hussein MR. Apoptosis in the ovary: molecular mechanisms. Hum Reprod Update 2005; 11: 162-177.
Jiang JY, Cheung CK, Wang Y, Tsang BK. Regulation of cell death and cell survival gene expression during ovarian follicular development and atresia. Front Biosci 2003; 8: d222-237
Hughes FM Jr, Gorospe WC. Biochemical identification of apoptosis (programmed cell death) in granulosa cells: evidence for a potential mechanism underlying follicular atresia. Endocrinology 1991; 129: 2415-2422.
Drevnick PE, Sandheinrich MB, Oris JT. Increased ovarian follicular apoptosis in fathead minnows (Pimephales promelas) exposed to dietary methylmercury. Aquat Toxicol 2006; 79: 49-54.
Kaipia A, Hsueh AJ. Regulation of ovarian follicle atresia. Annu Rev Physiol 1997. 59: 349-363.
Boone DL, Tsang BK. Caspase-3 in the rat ovary: localization and possible role in follicular atresia and luteal regression. Biol Reprod 1998; 58: 1533-1539.
Tang XL, Yang XY, Jung HJ, Kim SY, Jung SY, Choi DY, et al. Asiatic acid induces colon cancer cell growth inhibition and apoptosis through mitochondrial death cascade. Biol Pharm Bull 2009; 32: 1399-1405.
Groc L, Bezin L, Jiang H, Jackson TS, Levine RA. Bax, Bcl-2, and cyclin expression and apoptosis in rat substantia nigra during development. Neurosci Lett 2001; 306: 198-202.
Oltvai ZN, Milliman CL, Korsmeyer SJ. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 1993; 74: 609-619.