褪黑素对牦牛黄体细胞生长及功能影响的研究

doi:10.11843/j.issn.0366-6964.2022.02.013

Abstract

Abstract: This experiment was intended to research the effect of melatonin(MT)on the growth, antioxidant activity and function in yak luteal cells. The 2nd-passage luteal cells from healthy yak were used as research object in this experiment, and the effect of different concentrations (0 (Control), 25, 125, 250, and 500 pg·mL^-1) of melatonin on the growth and function in yak luteal cells were compared. Cell proliferation and viability were evaluated by CCK-8 assay. qRT-PCR was conducted to analyse the mRNA expression levels of several genes, including proliferation-related gene PCNA, apoptosis-related genes BCL-2, BAX, FAS, antioxidant-related genes SOD1, SOD2, GPX1 and CAT, as well as progesterone synthesis-related genes HSD3β, STAR and CYP11A1. The levels of ROS and progesterone were determined by ELISA. The results showed that the supplementation of different concentrations of MT could promote luteal cells proliferation and accelerate them into the plateau phase. MT could promote the mRNA expression of cell-proliferated gene PCNA and anti-apoptosis-related gene BCL-2, and repress the expression of apoptosis-related genes BAX, FAS. MT could reduce the ROS level and promote progesterone secretion significantly in luteal cells, moreover, the above effects were most obvious when the MT concentration was 250 pg·mL^-1. At this concentration, the mRNA expression levels of antioxidant-related genes SOD2, GPX1, CAT, and progesterone synthesis-related genes STAR and CYP11A1 significantly up-regulated. Compared with MT treatment alone, the co-treatment with MT and MT receptor inhibitor Luzindole could significantly increase the ROS level and decrease the expression level of SOD2, GPX1 and CAT. The level of progesterone and the expression of STAR and CYP11A1 decreased significantly. In conclusion, MT promotes yak luteal cells proliferation by up-regulating the mRNA expression level of PCNA and BCL-2, and repressing the expression level of BAX and FAS. MT may regulate the ROS level and progesterone level through its receptor. This study provides theoretical basis for the application of MT in the treatment of reproductive diseases caused by corpus luteum abnormality and the improvement in the reproductive performance of yak.

Key words: melatonin, yak, luteal cells, antioxidant activity, progesterone

CLC Number:

S823.85.3

CHENG Huaqin, YUAN Yujie, LUO Wen, GAO Shaoshuai, YE Linxia, LI Jian, YIN Shi. Research on the Effect of Melatonin on the Growth and Function of Yak Luteal Cells[J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(2): 459-469.

References 47

[1]	XIONG X R,LAN D L,LI J,et al.Supplementation of cilostazol during in vitro maturation enhances the meiosis and developmental competence of yak oocytes by influencing cAMP content and mRNA expression[J].Anim Reprod Sci,2017,186:21-30.
[2]	CHAUBE S K,PRASAD P V,THAKUR S C,et al.Hydrogen peroxide modulates meiotic cell cycle and induces morphological features characteristic of apoptosis in rat oocytes cultured in vitro[J].Apoptosis,2005,10(4):863-874.
[3]	TIWARI M,CHAUBE S K.Moderate increase of reactive oxygen species triggers meiotic resumption in rat follicular oocytes[J].J Obstet Gynaecol Res,2016,42(5):536-546.
[4]	FUJII J,IUCHI Y,OKADA F.Fundamental roles of reactive oxygen species and protective mechanisms in the female reproductive system[J].Reprod Biol Endocrinol,2005,3(1):43.
[5]	MAO X B,GU C S,CHEN D W,et al.Oxidative stress-induced diseases and tea polyphenols[J].Oncotarget,2017,8(46):81649-81661.
[6]	DEVINE P J,PERREAULT S D,LUDERER U.Roles of reactive oxygen species and antioxidants in ovarian toxicity[J].Biol Reprod,2012,86(2):27.
[7]	TALUKDER S,INGENHOFF L,KERRISK K L,et al.Plasma oxidative stress biomarkers and progesterone profiles in a dairy cow diagnosed with an ovarian follicular cyst[J].Vet Q,2014,34(2):113-117.
[8]	AL-GUBORY K H,GARREL C,FAURE P,et al.Roles of antioxidant enzymes in corpus luteum rescue from reactive oxygen species-induced oxidative stress[J].Reprod Biomed Online,2012,25(6):551-560.
[9]	闫昭明,郭秋平,仲银召,等.茶多酚的生物学特性及其在畜牧生产中的应用[J].动物营养学报,2019,31(4):1525-1532.YAN Z M,GUO Q P,ZHONG Y Z,et al.Tea polyphenols functions and their application in animal production[J].Chinese Journal of Animal Nutrition,2019,31(4):1525-1532.(in Chinese)
[10]	TAMURA H,KAWAMOTO M,SATO S,et al.Long-term melatonin treatment delays ovarian aging[J].J Pineal Res,2017,62(2):e12381.
[11]	CARLONI S,FAVRAIS G,SALIBA E,et al.Melatonin modulates neonatal brain inflammation through endoplasmic reticulum stress,autophagy,and miR-34a/silent information regulator 1 pathway[J].J Pineal Res,2016,61(3):370-380.
[12]	CHEN Z,LEI L J,WEN D,et al.Melatonin attenuates palmitic acid-induced mouse granulosa cells apoptosis via endoplasmic reticulum stress[J].J Ovarian Res,2019,12(1):43.
[13]	LI R Y,LUO X,LI L B,et al.The protective effects of melatonin against oxidative stress and inflammation induced by acute cadmium exposure in mice testis[J].Biol Trace Elem Res,2016,170(1):152-164.
[14]	YANG F X,LI L,CHEN K L,et al.Melatonin alleviates β-zearalenol and HT-2 toxin-induced apoptosis and oxidative stress in bovine ovarian granulosa cells[J].Environ Toxicol Pharmacol,2019,68:52-60.
[15]	HIBAOUI Y,ROULET E,RUEGG U T.Melatonin prevents oxidative stress-mediated mitochondrial permeability transition and death in skeletal muscle cells[J].J Pineal Res,2009,47(3):238-252.
[16]	HE R J,CUI M,LIN H,et al.Melatonin resists oxidative stress-induced apoptosis in nucleus pulposus cells[J].Life Sci,2018,199:122-130.
[17]	LV Y H,ZHANG P F,GUO J Y,et al.Melatonin protects mouse spermatogonial stem cells against hexavalent chromium-induced apoptosis and epigenetic histone modification[J].Toxicol Appl Pharmacol,2018,340:30-38.
[18]	ZHANG L,ZHANG Z Z,WANG J,et al.Melatonin regulates the activities of ovary and delays the fertility decline in female animals via MT1/AMPK pathway[J].J Pineal Res,2019,66(3):e12550.
[19]	CHEN L,ZHANG J J,ZHANG X,et al.Melatonin protects against defects induced by malathion during porcine oocyte maturation[J].J Cell Physiol,2020,235(3):2836-2846.
[20]	DAIR E L,SIMOES R S,SIMÕES M J,et al.Effects of melatonin on the endometrial morphology and embryo implantation in rats[J].Fertil Steril,2008,89(5):1299-1305.
[21]	BARBERINO R S,MENEZES V G,RIBEIRO A E A S,et al.Melatonin protects against cisplatin-induced ovarian damage in mice via the MT1 receptor and antioxidant activity[J].Biol Reprod,2017,96(6):1244-1255.
[22]	TAMURA H,TAKASAKI A,MIWA I,et al.Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate[J].J Pineal Res,2008,44(3):280-287.
[23]	RAHMAN S A,BIBBO C,OLCESE J,et al.Relationship between endogenous melatonin concentrations and uterine contractions in late third trimester of human pregnancy[J].J Pineal Res,2019,66(4):e12566.
[24]	张文华.催产素对牛黄体细胞中突触素表达的影响[D].杨凌:西北农林科技大学,2012.ZHANG W H.Effect of oxytocin on the expression of SYP in bovine luteal cells[D].Yangling:Northwest A & F University,2012.(in Chinese)
[25]	MIYAMOTO A,SHIRASUNA K,SHIMIZU T,et al.Regulation of corpus luteum development and maintenance:specific roles of angiogenesis and action of prostaglandin F2α[J].Soc Reprod Fertil Suppl,2010,67:289-304.
[26]	BHURKE A S,BAGCHI I C,BAGCHI M K.Progesterone-regulated endometrial factors controlling implantation[J].Am J Reprod Immunol,2016,75(3):237-245.
[27]	FRUNGIERI M B,CALANDRA R S,ROSSI S P.Local actions of melatonin in somatic cells of the testis[J].Int J Mol Sci,2017,18(6):1170.
[28]	FENG T Y,LI Q,REN F,et al.Melatonin protects goat spermatogonial stem cells against oxidative damage during cryopreservation by improving antioxidant capacity and inhibiting mitochondrial apoptosis pathway[J].Oxid Med Cell Longev,2020,2020:5954635.
[29]	GUO Y,SUN J Y,LI T,et al.Melatonin ameliorates restraint stress-induced oxidative stress and apoptosis in testicular cells via NF-κB/iNOS and Nrf2/HO-1 signaling pathway[J].Sci Rep,2017,7(1):9599.
[30]	BAHRAMI N,GOUDARZI M,HOSSEINZADEH A,et al.Evaluating the protective effects of melatonin on di(2-ethylhexyl) phthalate-induced testicular injury in adult mice[J].Biomed Pharmacother,2018,108:515-523.
[31]	MOHAMMADGHASEMI F,JAHROMI S K.Melatonin ameliorates testicular damages induced by nicotine in mice[J].Iran J Basic Med Sci,2018,21(6):639-644.
[32]	ROMEU L R G,DA MOTTA E L A,MAGANHIN C C,et al.Effects of melatonin on histomorphology and on the expression of steroid receptors,VEGF,and PCNA in ovaries of pinealectomized female rats[J].Fertil Steril,2011,95(4):1379-1384.
[33]	LUO X,JIA S J,MA Q L,et al.Suppressive effects of subchronic aluminum overload on the splenic immune function may be related to oxidative stress in mice[J].Biol Trace Elem Res,2014,157(3):249-255.
[34]	WANG X,SHARMA R K,SIKKA S C,et al.Oxidative stress is associated with increased apoptosis leading to spermatozoa DNA damage in patients with male factor infertility[J].Fertil Steril,2003,80(3):531-535.
[35]	宋超.褪黑素在延缓昆明小鼠卵巢衰老中的作用研究[D].杨凌:西北农林科技大学,2019.SONG C.Effect of melatonin on delaying the ovarian aging in Kunming mice[D].Yangling:Northwest A & F University,2019.(in Chinese)
[36]	MUKHERJEE A,HALDAR C,VISHWAS D K.Melatonin prevents dexamethasone-induced testicular oxidative stress and germ cell apoptosis in golden hamster,Mesocricetus auratus[J].Andrologia,2015,47(8):920-931.
[37]	TANABE M,TAMURA H,TAKETANI T,et al.Melatonin protects the integrity of granulosa cells by reducing oxidative stress in nuclei,mitochondria,and plasma membranes in mice[J].J Reprod Dev,2015,61(1):35-41.
[38]	HARDELAND R.Melatonin:Signaling mechanisms of a pleiotropic agent[J].Biofactors,2009,35(2):183-192.
[39]	WANG J M,JIANG C,ZHANG K,et al.Melatonin receptor activation provides cerebral protection after traumatic brain injury by mitigating oxidative stress and inflammation via the Nrf2 signaling pathway[J].Free Radic Biol Med,2019,131:345-355.
[40]	JUSZCZAK M,ROSZCZYK M,KOWALCZYK E,et al.The influence of melatonin receptors antagonists,luzindole and 4-phenyl-2-propionamidotetralin (4-P-PDOT),on melatonin-dependent vasopressin and adrenocorticotropic hormone (ACTH) release from the rat hypothalamo-hypophysial system.In vitro and in vivo studies[J].J Physiol Pharmacol,2014,65(6):777-784.
[41]	NODA Y,OTA K,SHIRASAWA T,et al.Copper/zinc superoxide dismutase insufficiency impairs progesterone secretion and fertility in female mice[J].Biol Reprod,2012,86(1):1-8.
[42]	CARLSON J C,WU X M,SAWADA M.Oxygen radicals and the control of ovarian corpus luteum function[J].Free Radic Biol Med,1993,14(1):79-84.
[43]	李曼曼,于昊,薛洋,等.生殖激素对山羊颗粒细胞孕酮合成的影响[J].中国兽医学报,2020,40(8):1652-1659.LI M M,YU H,XUE Y,et al.Effects of reproductive hormones on progesterone synthesis in granulosa cells of goats[J].Chinese Journal of Veterinary Science,2020,40(8):1652-1659.(in Chinese)
[44]	QU X L,YAN L Y,GUO R H,et al.ROS-induced GATA4 and GATA6 downregulation inhibits StAR expression in LPS-treated porcine granulosa-lutein cells[J].Oxid Med Cell Longev,2019,2019:5432792.
[45]	王振宇.褪黑素对妊娠期猪黄体细胞孕酮分泌的调节作用及机制研究[D].杨凌:西北农林科技大学,2017.WANG Z Y.The regulation and mechanism of melatonin on progesterone secretion in porcine corpus luteum cells[D].Yangling:Northwest A & F University,2017.(in Chinese)
[46]	FANG L L,LI Y R,WANG S J,et al.Melatonin induces progesterone production in human granulosa-lutein cells through upregulation of StAR expression[J].Aging (Albany NY),2019,11(20):9013-9024.
[47]	ZHANG W L,WANG Z Y,ZHANG L,et al.Melatonin stimulates the secretion of progesterone along with the expression of cholesterol side-chain cleavage enzyme (P450 scc) and steroidogenic acute regulatory protein (StAR) in corpus luteum of pregnant sows[J].Theriogenology,2018,108:297-305.

Research on the Effect of Melatonin on the Growth and Function of Yak Luteal Cells

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