Melatonin mitigates PGF-induced apoptosis during luteal regression in heat-exposed rats
Hadi Tavakolikazerooni; Hao Yu; Saif Ullah; Wael Ennab; Dagan Mao
Abstract
Keywords
References
Abate M, Festa A, Falco M, Lombardi A, Luce A, Grimaldi A, Zappavigna S, Sperlongano P, Irace C, Caraglia M, Misso G. Mitochondria as playmakers of apoptosis, autophagy and senescence. Semin Cell Dev Biol. 2020:98:139-53.
Abbott SM, Malkani RG, Zee PC. Circadian disruption and human health: a bidirectional relationship. Eur J Neurosci. 2020;51(1):567-83.
Agarwal A, Aponte-Mellado A, Premkumar BJ, Shaman A, Gupta S. The effects of oxidative stress on female reproduction: a review. Reprod Biol Endocrinol. 2012;10:49.
Alchalabi AS, Rahim H, Aklilu E, Al-Sultan II, Aziz AR, Malek MF, Ronald SH, Khan MA. Histopathological changes associated with oxidative stress induced by electromagnetic waves in rats’ ovarian and uterine tissues. Asian Pac J Reprod. 2016;5(4):301-10.
Al-Shahat A, Hulail MA, Soliman NM, Khamis T, Fericean LM, Arisha AH, Moawad RS. Melatonin mitigates cisplatin-induced ovarian dysfunction via altering steroidogenesis, inflammation, apoptosis, oxidative stress, and PTEN/PI3K/Akt/mTOR/AMPK signaling pathway in female rats. Pharmaceutics. 2022;14(12):2769.
Andrabi SA, Sayeed I, Siemen D, Wolf G, Horn TF. Direct inhibition of the mitochondrial permeability transition pore: a possible mechanism responsible for anti‐apoptotic effects of melatonin. FASEB J. 2004;18(7):869-71.
Asadi M, Taghizadeh S, Kaviani E, Vakili O, Taheri‐Anganeh M, Tahamtan M, Savardashtaki A. Caspase‐3: structure, function, and biotechnological aspects. Biotechnol Appl Biochem. 2022;69(4):1633-45.
Bai WJ, Jin PJ, Kuang MQ, Wei QW, Shi FX, Davis JS, Mao DG. Temporal regulation of extracellular signal-regulated kinase 1/2 phosphorylation, heat shock protein 70 and activating transcription factor 3 during prostaglandin F-induced luteal regression in pseudopregnant rats following heat stress. Reprod Fertil Dev. 2017;29(6):1184-93.
Bei M, Wang Q, Yu W, Han L, Yu J. Effects of heat stress on ovarian development and the expression of HSP genes in mice. J Therm Biol. 2020;89:102532.
Belhadj Slimen I, Najar T, Ghram A, Dabbebi H, Ben Mrad M, Abdrabbah M. Reactive oxygen species, heat stress and oxidative-induced mitochondrial damage. A review. Int J Hyperthermia. 2014;30(7):513-23.
Boice A, Bouchier-Hayes L. Targeting apoptotic caspases in cancer. Biochim Biophys Acta Mol Cell Res. 2020;1867(6):118688.
Boni R. Heat stress, a serious threat to reproductive function in animals and humans. Mol Reprod Dev. 2019;86(10):1307-23.
Chakravarthi VP, Ratri A, Masumi S, Borosha S, Ghosh S, Christenson LK, Roby KF, Wolfe MW, Rumi MAK. Granulosa cell genes that regulate ovarian follicle development beyond the antral stage: the role of estrogen receptor β. Mol Cell Endocrinol. 2021;528:111212.
Chen Y-J, Feng Q, Liu Y-X. Expression of the steroidogenic acute regulatory protein and luteinizing hormone receptor and their regulation by tumor necrosis factor α in rat corpora lutea. Biol Reprod. 1999;60(2):419-27.
Christen F, Desrosiers V, Dupont-Cyr BA, Vandenberg GW, Le François NR, Tardif J-C, Dufresne F, Lamarre SG, Blier PU. Thermal tolerance and thermal sensitivity of heart mitochondria: mitochondrial integrity and ROS production. Free Radic Biol Med. 2018;116:11-8.
Cipolla-Neto J, Amaral FGD. Melatonin as a hormone: new physiological and clinical insights. Endocr Rev. 2018;39(6):990-1028.
Collier RJ, Renquist BJ, Xiao Y. 100-Year Review: stress physiology including heat stress. J Dairy Sci. 2017;100(12):10367-80.
Cruz MHC, Leal CLV, Cruz JF, Tan DX, Reiter RJ. Essential actions of melatonin in protecting the ovary from oxidative damage. Theriogenology. 2014;82(7):925-32.
Emami NK, Jung U, Voy B, Dridi S. Radical response: effects of heat stress-induced oxidative stress on lipid metabolism in the avian liver. Antioxidants. 2020;10(1):35.
Esch T, Stefano GB. The neurobiology of stress management. Neuroendocrinol Lett. 2010;31(1):19-39. PMid:20150886.
Guo N, Meng C, Bai W, Wei Q, Shi F, Davis JS, Mao D. Prostaglandin F2α induces expression of activating transcription factor 3 (ATF3) and activates MAPK signaling in the rat corpus luteum. Acta Histochem. 2015;117(2):211-8.
Haduch A, Bromek E, Wójcikowski J, Gołembiowska K, Daniel WA. Melatonin supports CYP2D-mediated serotonin synthesis in the brain. Drug Metab Dispos. 2016;44(3):445-52.
Hassan MU, Ghareeb RY, Nawaz M, Mahmood A, Shah AN, Abdel-Megeed A, Abdelsalam NR, Hashem M, Alamri S, Thabit MA, Qari SH. Melatonin: a vital protectant for crops against heat stress: mechanisms and prospects. Agronomy (Basel). 2022;12(5):1116.
He B, Yin C, Gong Y, Liu J, Guo H, Zhao R. Melatonin‐induced increase of lipid droplets accumulation and in vitro maturation in porcine oocytes is mediated by mitochondrial quiescence. J Cell Physiol. 2018;233(1):302-12.
Hernandez F, Peluffo MC, Bas D, Stouffer RL, Tesone M. Local effects of the sphingosine 1‐phosphate on prostaglandin F2alpha‐induced luteolysis in the pregnant rat. Mol Reprod Dev. 2009;76(12):1153-64.
Hojo T, Skarzynski DJ, Okuda K. Apoptosis, autophagic cell death, and necroptosis: different types of programmed cell death in bovine corpus luteum regression. J Reprod Dev. 2022;68(6):355-60.
Jagota A, Kalyani D. Effect of melatonin on age induced changes in daily serotonin rhythms in suprachiasmatic nucleus of male Wistar rat. Biogerontology. 2010;11(3):299-308.
Jara-Gutiérrez Á, Baladrón V. The role of prostaglandins in different types of cancer. Cells. 2021;10(6):1487.
Jiang Y-F, Hsu M-C, Cheng C-H, Tsui K-H, Chiu C-H. Ultrastructural changes of goat corpus luteum during the estrous cycle. Anim Reprod Sci. 2016;170:38-50.
Khan A, Dou J, Wang Y, Jiang X, Khan MZ, Luo H, Usman T, Zhu H. Evaluation of heat stress effects on cellular and transcriptional adaptation of bovine granulosa cells. J Anim Sci Biotechnol. 2020a;11:25.
Khan A, Khan MZ, Umer S, Khan IM, Xu H, Zhu H, Wang Y. Cellular and molecular adaptation of bovine granulosa cells and oocytes under heat stress. Animals (Basel). 2020b;10(1):110.
Kumariya S, Ubba V, Jha RK, Gayen JR. Autophagy in ovary and polycystic ovary syndrome: role, dispute and future perspective. Autophagy. 2021;17(10):2706-33.
Li H, Pei X, Yu H, Wang W, Mao D. Autophagic and apoptotic proteins in goat corpus luteum and the effect of Adiponectin/AdipoRon on luteal cell autophagy and apoptosis. Theriogenology. 2024;214:245-56.
Li L, Wu J, Luo M, Sun Y, Wang G. The effect of heat stress on gene expression, synthesis of steroids, and apoptosis in bovine granulosa cells. Cell Stress Chaperones. 2016;21(3):467-75.
Liu X, Shi Y, Hou X, Wan C, He S, Chong X, Liu M, Li H, Liu F. Microarray analysis of intestinal immune-related gene expression in heat-stressed rats. Int J Hyperthermia. 2014;30(5):324-7.
Lockshin RA, Zakeri Z. Programmed cell death and apoptosis: origins of the theory. Nat Rev Mol Cell Biol. 2001;2(7):545-50.
Manchester LC, Coto‐Montes A, Boga JA, Andersen LPH, Zhou Z, Galano A, Vriend J, Tan DX, Reiter RJ. Melatonin: an ancient molecule that makes oxygen metabolically tolerable. J Pineal Res. 2015;59(4):403-19.
Mohseni M, Mihandoost E, Shirazi A, Sepehrizadeh Z, Bazzaz JT, Ghazi-khansari M. Melatonin may play a role in modulation of bax and bcl-2 expression levels to protect rat peripheral blood lymphocytes from gamma irradiation-induced apoptosis. Mutat Res. 2012;738-739:19-27.
Mojaverrostami S, Asghari N, Khamisabadi M, Khoei HH. The role of melatonin in polycystic ovary syndrome: a review. Int J Reprod Biomed. 2019;17(12):865-82.
Nanas I, Chouzouris T-M, Dovolou E, Dadouli K, Stamperna K, Kateri I, Barbagianni M, Amiridis GS. Early embryo losses, progesterone and pregnancy associated glycoproteins levels during summer heat stress in dairy cows. J Therm Biol. 2021;98:102951.
Onaolapo AY, Aina OA, Onaolapo OJ. Melatonin attenuates behavioural deficits and reduces brain oxidative stress in a rodent model of schizophrenia. Biomed Pharmacother. 2017;92:373-83.
Pan B, Sengoku K, Takuma N, Goishi K, Horikawa M, Tamate K, Ishikawa M. Differential expression of heparin-binding epidermal growth factor-like growth factor in the rat ovary. Mol Cell Endocrinol. 2004;214(1-2):1-8.
Qi L, Guo N, Wei Q, Jin P, Wang W, Mao D. The involvement of NR4A1 and NR4A2 in the regulation of the luteal function in rats. Acta Histochem. 2018;120(8):713-9.
Reiter RJ, Mayo JC, Tan DX, Sainz RM, Alatorre‐Jimenez M, Qin L. Melatonin as an antioxidant: under promises but over delivers. J Pineal Res. 2016;61(3):253-78.
Rostami A, Moosavi SA, Moghadam HD, Bolookat ER. Micronuclei assessment of the radioprotective effects of melatonin and vitamin C in human lymphocytes. Cell J. 2016;18(1):46-51.
Sainz RM, Mayo JC, Rodriguez C, Tan DX, Lopez-Burillo S, Reiter RJ. Melatonin and cell death: differential actions on apoptosis in normal and cancer cells. Cell Mol Life Sci. 2003;60(7):1407-26.
Shah KB, Tripathy S, Suganthi H, Rudraiah M. Profiling of luteal transcriptome during prostaglandin F2-alpha treatment in buffalo cows: analysis of signaling pathways associated with luteolysis. PLoS One. 2014;9(8):e104127.
Soravia C, Ashton BJ, Thornton A, Ridley AR. The impacts of heat stress on animal cognition: implications for adaptation to a changing climate. Wiley Interdiscip Rev Clim Change. 2021;12(4):e713.
Sugino N, Suzuki T, Kashida S, Karube A, Takiguchi S, Kato H. Expression of Bcl-2 and Bax in the human corpus luteum during the menstrual cycle and in early pregnancy: regulation by human chorionic gonadotropin. J Clin Endocrinol Metab. 2000;85(11):4379-86. PMid:11095483.
Sun T-C, Li H-Y, Li X-Y, Yu K, Deng S-L, Tian L. Protective effects of melatonin on male fertility preservation and reproductive system. Cryobiology. 2020;95:1-8.
Tang Z, Chen J, Zhang Z, Bi J, Xu R, Lin Q, Wang Z. HIF‐1α activation promotes luteolysis by enhancing ROS levels in the corpus luteum of pseudopregnant rats. Oxid Med Cell Longev. 2021;2021(1):1764929.
Ullah S, Zhang M, Yu H, Mustafa S, Shafiq M, Wei Q, Wang W, Jan M, Mao D. Heat exposure affected the reproductive performance of pregnant mice: enhancement of autophagy and alteration of subcellular structure in the corpus luteum. Reprod Biol. 2019;19(3):261-9.
Wang H-L, Xing G-D, Qian Y, Sun X-F, Zhong J-F, Chen K-L. Dihydromyricetin attenuates heat stress-induced apoptosis in dairy cow mammary epithelial cells through suppressing mitochondrial dysfunction. Ecotoxicol Environ Saf. 2021;214:112078.
Warren CF, Wong-Brown MW, Bowden NA. BCL-2 family isoforms in apoptosis and cancer. Cell Death Dis. 2019;10(3):177.
Wolfenson D, Sonego H, Bloch A, Shaham-Albalancy A, Kaim M, Folman Y, Meidan R. Seasonal differences in progesterone production by luteinized bovine thecal and granulosa cells. Domest Anim Endocrinol. 2002;22(2):81-90.
Xu L, Li D, Li H, Zhang O, Huang Y, Shao H, Wang Y, Cai S, Zhu Y, Jin S, Ding C. Suppression of obesity by melatonin through increasing energy expenditure and accelerating lipolysis in mice fed a high-fat diet. Nutr Diabetes. 2022;12(1):42.
Yu H, Zhao J, Pei X, Xia Y, Li H, Wang W, Mao D. Dual role of NR4A1 in porcine ovarian granulosa cell differentiation and granulosa-lutein cell regression in vitro. Theriogenology. 2023;198:292-304.
Yu J, Liu F, Yin P, Wu D, Jin Y, Liu X. Integrating miRNA and mRNA expression profiles in response to heat stress-induced injury in rat small intestine. Funct Integr Genomics. 2011;11(2):203-13.
Zhao F, Whiting S, Lambourne S, Aitken RJ, Sun Y. Melatonin alleviates heat stress-induced oxidative stress and apoptosis in human spermatozoa. Free Radic Biol Med. 2021;164:410-6.
Zheng B, Meng J, Zhu Y, Ding M, Zhang Y, Zhou J. Melatonin enhances SIRT1 to ameliorate mitochondrial membrane damage by activating PDK1/Akt in granulosa cells of PCOS. J Ovarian Res. 2021;14(1):152.
Submitted date:
11/02/2024
Accepted date:
04/22/2025
Facebook
Google+
Twitter
LinkedIn
Mendeley
StumbleUpon
CiteULike
Reddit
Email