miRNA调节卵泡颗粒细胞凋亡及其机制的研究进展

doi:10.16431/j.cnki.1671-7236.2021.12.011

Abstract

Abstract: Microribonucleic acid (microRNA, miRNA) is a type of endogenous non-coding RNA, which have a wide range of gene expression regulation.They can regulate the expression of corresponding proteins by affecting target genes at the post-transcriptional level, and then regulate cell life activities.miRNA is expressed in mammalian follicular granulosa cells and regulate the apoptosis of granulosa cells.Granulosa cells, as the most numerous cell group in ovarian follicles, play a vital role in the process of follicular development.They not only provide nutrients for oocytes, but also regulate their development and maturity.Granulosa cell apoptosis is an important cause of follicle atresia, which affects the number and quality of follicles and thus affecting the reproductive performance of female animals.The apoptosis of granulosa cells is regulated by a variety of factors.This paper briefly describes the regulatory effect and mechanism of miRNA on ovarian granulosa cell apoptosis, including miRNA regulating granulosa cell apoptosis by regulating hormone secretion and the expression of apoptosis-related factors, the effect of miRNA on granular cell apoptosis related signal pathway, miRNA regulating ovarian-derived diseases caused by granular cell apoptosis, and summarizes the miRNA that regulate granular cell apoptosis and the potential role of miRNA in disease diagnosis and treatment, in order to provide guidance and reference for the pathogenesis and treatment of subsequent related ovarian diseases and improve the reproductive performance of female mammals.

Key words: granulosa cells; apoptosis; ovarian-derived diseases; miRNA

CLC Number:

S852.2

LI Xuan, TONG Junshuo, ZHANG Dachong, WANG Bingyun, CHEN Shengfeng, LIU Canying. Research Advances on miRNA in Regulating the Apoptosis of Follicular Granulosa Cells and Its Mechanism[J]. China Animal Husbandry and Veterinary Medicine, 2021, 48(12): 4429-4441.

References

[1] 刘鹏,李向臣,姚雅馨,等.卵巢颗粒细胞凋亡的调控因素[J].现代生物医学进展,2009,9(13):2562-2564. LIU P,LI X C,YAO Y X,et al.The regulating factors apoptosis of ovary granular cells[J].Progress in Modern Biomedicine,2009,9(13):2562-2564.(in Chinese)
[2] MANABE N,GOTO Y,MATSUDA-MINEHATA F,et al.Regulation mechanism of selective atresia in porcine follicles:Regulation of granulosa cell apoptosis during atresia[J].Journal of Reproduction and Development,2004,50(5):493-514.
[3] MATSUDA F,INOUE N,MANABE N,et al.Follicular growth and atresia in mammalian ovaries:Regulation by survival and death of granulosa cells[J].Journal of Reproduction and Development,2012,58(1):44-50.
[4] TU J,CHEUNG A H,CHAN C L,et al.The role of microRNAs in ovarian granulosa cells in health and disease[J].Frontiers in Endocrinology,2019,10:174.
[5] BARTEL D P.Metazoan microRNAs[J].Cell,2018,173(1):20-51.
[6] JOVANOVIC M,HENGARTNER M O.miRNAs and apoptosis:RNAs to die for[J].Oncogene,2006,25(46):6176-6187.
[7] KEDDE M,AGAMI R.Interplay between microRNAs and RNA-binding proteins determines developmental processes[J].Cell Cycle,2008,7(7):899-903.
[8] MITCHELL P S,PARKIN R K,KROH E M,et al.Circulating microRNAs as stable blood-based markers for cancer detection[J].Proceedings of the National Academy of Sciences of the United States of America,2008,105(30):10513-10518.
[9] WANG L,ROMERO M,RATAJCZAK P,et al.Increased apoptosis is linked to severe acute GVHD in patients with Fanconi anemia[J].Bone Marrow Transplant,2013,48(6):849-853.
[10] AMBROS V.The functions of animal microRNAs[J].Nature,2004,431(7006):350-355.
[11] BARTEL D P.microRNAs:Target recognition and regulatory functions[J].Cell,2009,136(2):215-233.
[12] SHIN C,NAM J W,FARH K K,et al.Expanding the microRNA targeting code:Functional sites with centered pairing[J].Molecular Cell,2010,38(6):789-802.
[13] BARTEL D P.microRNAs:Genomics,biogenesis,mechanism,and function[J].Cell,2004,116(2):281-297.
[14] FILIPOWICZ W,BHATTACHARYYA S N,SONENBERG N.Mechanisms of post-transcriptional regulation by microRNAs:Are the answers in sight?[J].Nature Reviews Genetics,2008,9(2):102-114.
[15] ZIELAK-STECIWKO A E,BROWNE J A,MCGETTIGAN P A,et al.Expression of microRNAs and their target genes and pathways associated with ovarian follicle development in cattle[J].Physiological Genomics,2014,46(19):735-745.
[16] CARLETTI M Z,FIEDLER S D,CHRISTENSON L K.microRNA 21 blocks apoptosis in mouse periovulatory granulosa cells[J].Biology of Reproduction,2010,83(2):286-295.
[17] GONG Z,YANG J,BAI S,et al.microRNAs regulate granulosa cells apoptosis and follicular development——A review[J].Asian-Australasian Journal of Animal Sciences,2020,33(11):1714-1724.
[18] WORKU T,REHMAN Z U,TALPUR H S,et al.microRNAs:New insight in modulating follicular atresia:A review[J].InternationalJournal of Molecular Sciences,2017,18(2):333.
[19] BARNETT K R,SCHILLING C,GREENFELD C R,et al.Ovarian follicle development and transgenic mouse models[J].Human Reproduction Update,2006,12(5):537-555.
[20] SALAS-HUETOS A,JAMES E R,ASTON K I,et al.The expression of miRNAs in human ovaries,oocytes,extracellular vesicles,and early embryos:A systematic review[J].Cells,2019,8(12):1564.
[21] ZHANG S,WANG L,WANG L,et al.miR-17-5p affects porcine granulosa cell growth and oestradiol synthesis by targeting E2F1 gene[J].Reproduction in Domestic Animals,2019,54(11):1459-1469.
[22] SHIOTA M,SUGAI N,TAMURA M,et al.Correlation of mitogen-activated protein kinase activities with cell survival and apoptosis in porcine granulosa cells[J].Zoological Science,2003,20(2):193-201.
[23] 蒋秀敏,刘雨生,许波.miR-483-5p通过靶基因ERK1调控人类颗粒细胞增殖凋亡平衡[J].安徽医科大学学报,2015,50(11):1639-1644. JIANG X M,LIU Y S,XU B.Characterization of miRNA-483-5p and targeted gene ERK1 in the regulation of proliferation-apoptosis balance of human granulosa cells[J].Acta Universitatis Medicinalis Anhui,2015,50(11):1639-1644.(in Chinese)
[24] MA M,ZHANG J,GAO X,et al.miR-361-5p mediates SMAD4 to promote porcine granulosa cell apoptosis through VEGFA[J].Biomolecules,2020,10(9):1281.
[25] DU X,LIU L,LI Q,et al.NORFA,long intergenic noncoding RNA,maintains sow fertility by inhibiting granulosa cell death[J].Communications Biology,2020,3(1):131.
[26] LIN F,LI R,PAN Z X,et al.miR-26b promotes granulosa cell apoptosis by targeting ATM during follicular atresia in porcine ovary[J].PLoS One,2012,7(6):e38640.
[27] TU F,PAN Z X,YAO Y,et al.miR-34a targets the inhibin beta B gene,promoting granulosa cell apoptosis in the porcine ovary[J].Genetics and Molecular Research,2014,13(2):2504-2512.
[28] SIROTKIN A V,KISOVA G,BRENAUT P,et al.Involvement of microRNA Mir15a in control of human ovarian granulosa cell proliferation,apoptosis,steroidogenesis,and response to FSH[J].MicroRNA,2014,3(1):29-36.
[29] 李花,赵新广,刘丹卓.卵巢早衰病理因素研究现状及展望[J].中医药导报,2012,18(8):4-6. LI H,ZHAO X G,LIU D Z.Reserch status and prospect on the pathological factor of premature ovarian failure[J].Guiding Journal of Traditional Chinese Medicine and Pharmacy,2012,18(8):4-6.(in Chinese)
[30] DAI A,SUN H,FANG T,et al.microRNA-133b stimulates ovarian estradiol synthesis by targeting Foxl2[J].Febs Letters,2013,587(15):2474-2482.
[31] DU X,ZHANG L,LI X,et al.TGF-beta signaling controls FSHR signaling-reduced ovarian granulosa cell apoptosis through the SMAD4/miR-143 axis[J].Cell Death and Disease,2016,7(11):e2476.
[32] ZHANG K,KAUFMAN R J.From endoplasmic-reticulum stress to the inflammatory response[J].Nature,2008,454(7203):455-462.
[33] DU X,WANG L,LI Q,et al.miR-130a/TGF-beta1 axis is involved in sow fertility by controlling granulosa cell apoptosis[J].Theriogenology,2020,157:407-417.
[34] LI Q,DU X,PAN Z,et al.The transcription factor SMAD4 and miR-10b contribute to E₂ release and cell apoptosis in ovarian granulosa cells by targeting CYP19A1[J].Molecular and Cellular Endocrinology,2018,476:84-95.
[35] LIU J,LI X,YAO Y,et al.miR-1275 controls granulosa cell apoptosis and estradiol synthesis by impairing LRH-1/CYP19A1 axis[J].Biochimica et Biophysica Acta-Gene Regulatory Mechanisms,2018,1861(3):246-257.
[36] WANG M,LIU M,SUN J,et al.microRNA-27a-3p affects estradiol and androgen imbalance by targeting Creb1 in the granulosa cells in mouse polycytic ovary syndrome model[J].Reproductive Biology,2017,17(4):295-304.
[37] JOLLY P D,TISDALL D J,DE’ATH G,et al.Granulosa cell apoptosis,aromatase activity,cyclic adenosine 3’,5’-monophosphate response to gonadotropins,and follicular fluid steroid levels during spontaneous and induced follicular atresia in ewes[J].Biology of Reproduction,1997,56(4):830-836.
[38] WANG Y,ASSELIN E,TSANG B K.Involvement of transforming growth factor alpha in the regulation of rat ovarian X-linked inhibitor of apoptosis protein expression and follicular growth by follicle-stimulating hormone[J].Biology of Reproduction,2002,66(6):1672-1680.
[39] MANI A M,FENWICK M A,CHENG Z,et al.IGF1 induces up-regulation of steroidogenic and apoptotic regulatory genes via activation of phosphatidylinositol-dependent kinase/AKT in bovine granulosa cells[J].Reproduction,2010,139(1):139-151.
[40] MACK E M,SMITH J E,KURZ S G,et al.cAMP-dependent regulation of ovulatory response genes is amplified by IGF1 due to synergistic effects on Akt phosphorylation and NF-kappaB transcription factors[J].Reproduction,2012,144(5):595-602.
[41] CAI G,MA X,CHEN B,et al.microRNA-145 negatively regulates cell proliferation through targeting IRS1 in isolated ovarian granulosa cells from patients with polycystic ovary syndrome[J].Reproductive Sciences,2017,24(6):902-910.
[42] XU R,WANG Z.Involvement of transcription factor FoxO1 in the pathogenesis of polycystic ovary syndrome[J].Frontiers in Physiology,2021,12:649295.
[43] XING Y Q,LI A,YANG Y,et al.The regulation of FOXO1 and its role in disease progression[J].Life Sciences,2018,193:124-131.
[44] SHEN M,LIU Z,LI B,et al.Involvement of FoxO1 in the effects of follicle-stimulating hormone on inhibition of apoptosis in mouse granulosa cells[J].Cell Death & Disease,2014,5:e1475.
[45] HERNDON M K,LAW N C,DONAUBAUER E M,et al.Forkhead box O member FOXO1 regulates the majority of follicle-stimulating hormone responsive genes in ovarian granulosa cells[J].Molecular and Cellular Endocrinology,2016,434:116-126.
[46] ZHANG M,ZHANG Q,HU Y,et al.miR-181a increases FoxO1 acetylation and promotes granulosa cell apoptosis via SIRT1 downregulation[J].Cell Death and Disease,2017,8(10):e3088.
[47] CAO R,WU W,ZHOU X,et al.Let-7g induces granulosa cell apoptosis by targeting MAP3K1 in the porcine ovary[J].International Journal of Biochemistry and Cell Biology,2015,68:148-157.
[48] QU Y,ZHANG J,WU S,et al.SIRT1 promotes proliferation and inhibits apoptosis of human malignant glioma cell lines[J].Neuroscience Letters,2012,525(2):168-172.
[49] SRISUTTEE R,KOH S S,MALILAS W,et al.SIRT1 sensitizes hepatocellular carcinoma cells expressing hepatitis B virus X protein to oxidative stress-induced apoptosis[J].Biochemical and Biophysical Research Communications,2012,429(1-2):45-50.
[50] XIONG F,HU L,ZHANG Y,et al.miR-22 inhibits mouse ovarian granulosa cell apoptosis by targeting SIRT1[J].Biology Open,2016,5(3):367-371.
[51] COHEN H Y,MILLER C,BITTERMAN K J,et al.Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase[J].Science,2004,305(5682):390-392.
[52] ZHAO F,ZHAO W,REN S,et al.Roles of SIRT1 in granulosa cell apoptosis during the process of follicular atresia in porcine ovary[J].Anim Reproduction Science,2014,151(1-2):34-41.
[53] LUO H,HAN Y,LIU J,et al.Identification of microRNAs in granulosa cells from patients with different levels of ovarian reserve function and the potential regulatory function of miR-23a in granulosa cell apoptosis[J].Gene,2019,686:250-260.
[54] JIAJIE T,YANZHOU Y,HOI-HUNG A C,et al.Conserved miR-10 family represses proliferation and induces apoptosis in ovarian granulosa cells[J].Scientific Reports,2017,7:41304.
[55] PENG J Y,AN X P,FANG F,et al.microRNA-10b suppresses goat granulosa cell proliferation by targeting brain-derived neurotropic factor[J].Domestic Animal Endocrinology,2016,54:60-67.
[56] HETZ C.The unfolded protein response:Controlling cell fate decisions under ER stress and beyond[J].Nature Reviews Molecular Cell Biology,2012,13(2):89-102.
[57] RON D,WALTER P.Signal integration in the endoplasmic reticulum unfolded protein response[J].Nature Reviews Molecular Cell Biology,2007,8(7):519-529.
[58] ROZPEDEK W,PYTEL D,MUCHA B,et al.The role of the PERK/eIF2alpha/ATF4/CHOP signaling pathway in tumor progression during endoplasmic reticulum stress[J].Current Molecular Medicine,2016,16(6):533-544.
[59] LI J,ZHUO J Y,ZHOU W,et al.Endoplasmic reticulum stress triggers delanzomib-induced apoptosis in HCC cells through the PERK/eIF2alpha/ATF4/CHOP pathway[J].American Journal of Translational Research,2020,12(6):2875-2889.
[60] GUO Y,GUO R,SU Y,et al.The PERK/eIF2alpha/ATF4/CHOP pathway plays a role in regulating monocrotaline-induced endoplasmic reticulum stress in rat liver[J].Research in Veterinary Science,2020,130:237-239.
[61] LIN P,YANG Y,LI X,et al.Endoplasmic reticulum stress is involved in granulosa cell apoptosis during follicular atresia in goat ovaries[J].Molecular Reproduction and Development,2012,79(6):423-432.
[62] LIU K,SHI Y,GUO X,et al.CHOP mediates ASPP2-induced autophagic apoptosis in hepatoma cells by releasing Beclin-1 from Bcl-2 and inducing nuclear translocation of Bcl-2[J].Cell Death & Disease,2014,5:e1323.
[63] REGAN S,KNIGHT P G,YOVICH J L,et al.Granulosa cell apoptosis in the ovarian follicle-A changing view[J].Front Endocrinol (Lausanne),2018,9:61.
[64] CHITNIS N S,PYTEL D,BOBROVNIKOVA-MARJON E,et al.miR-211 is a prosurvival microRNA that regulates chop expression in a PERK-dependent manner[J].Molecular Cell,2012,48(3):353-364.
[65] XIONG Y,CHEN H,LIN P,et al.ATF6 knockdown decreases apoptosis,arrests the S phase of the cell cycle,and increases steroid hormone production in mouse granulosa cells[J].American Journal of Physiology-Cell Physiology,2017,312(3):C341-C353.
[66] MIYAZAWA K,MIYAZONO K.Regulation of TGF-beta family signaling by inhibitory Smads[J].Cold Spring Harbor Perspectives in Biology,2017,9(3):a022095.
[67] ZHOU J,LIU J,PAN Z,et al.The let-7g microRNA promotes follicular granulosa cell apoptosis by targeting transforming growth factor-beta type 1 receptor[J].Molecular and Cellular Endocrinology,2015,409:103-112.
[68] YU M,LIU J.microRNA-30d-5p promotes ovarian granulosa cell apoptosis by targeting Smad2[J].Experimental and Therapeutic Medicine,2020,19(1):53-60.
[69] DU X,PAN Z,LI Q,et al.SMAD4 feedback regulates the canonical TGF-beta signaling pathway to control granulosa cell apoptosis[J].Cell Death and Disease,2018,9(2):151.
[70] YANG L,DU X,LIU L,et al.miR-1306 mediates the feedback regulation of the TGF-beta/SMAD signaling pathway in granulosa cells[J].Cells,2019,8(4):298.
[71] LI Q,DU X,LIU L,et al.miR-126* is a novel functional target of transcription factor SMAD4 in ovarian granulosa cells[J].Gene,2019,711:143953.
[72] LIU J,YAO W,YAO Y,et al.miR-92a inhibits porcine ovarian granulosa cell apoptosis by targeting Smad7 gene[J].Febs Letters,2014,588(23):4497-4503.
[73] ZHANG J Q,GAO B W,GUO H X,et al.miR-181a promotes porcine granulosa cell apoptosis by targeting TGFBR1 via the activin signaling pathway[J].Molecular and Cellular Endocrinology,2020,499:110603.
[74] HUANG X,LIU C,HAO C,et al.Identification of altered microRNAs and mRNAs in the cumulus cells of PCOS patients:miRNA-509-3p promotes oestradiol secretion by targeting MAP3K8[J].Reproduction,2016,151(6):643-655.
[75] 唐忠庆,吴坚,郑赓唐,等.多囊卵巢综合征与卵巢颗粒细胞凋亡基因蛋白Bcl-2、Bax、P53的相关性研究[J].世界最新医学信息文摘,2016,16(A5):98-99. TANG Z Q,WU J,ZHENG G T,et al.Study on the correlation between polycystic ovary syndrome and ovarian granulosa cell apoptosis gene proteins Bcl-2,Bax,P53[J].World Latest Medicine Information,2016,16(A5):98-99.(in Chinese)
[76] FU X,HE Y,WANG X,et al.microRNA-16 promotes ovarian granulosa cell proliferation and suppresses apoptosis through targeting PDCD4 in polycystic ovarian syndrome[J].Cellular Physiology and Biochemistry,2018,48(2):670-682.
[77] ZHAO Y,TAO M,WEI M,et al.Mesenchymal stem cells derived exosomal miR-323-3p promotes proliferation and inhibits apoptosis of cumulus cells in polycystic ovary syndrome (PCOS)[J].Artificial Cells,Nanomedicine and Biotechnology,2019,47(1):3804-3813.
[78] SUN X,SU S,ZHANG G,et al.miR-204 suppresses cell proliferation and promotes apoptosis in ovarian granulosa cells via targeting TPT1 in polycystic ovary syndrome[J].Biochemistry and Cell Biology,2019,97(5):554-562.
[79] LI D,XU D,XU Y,et al.microRNA-141-3p targets DAPK1 and inhibits apoptosis in rat ovarian granulosa cells[J].Cell Biochemistry and Function,2017,35(4):197-201.
[80] YAO L,LI M,HU J,et al.miRNA-335-5p negatively regulates granulosa cell proliferation via SGK3 in PCOS[J].Reproduction,2018,156(5):439-449.
[81] WANG C,LI D,ZHANG S,et al.microRNA-125a-5p induces mouse granulosa cell apoptosis by targeting signal transducer and activator of transcription 3[J].Menopause,2016,23(1):100-107.
[82] CHEN X,XIE M,LIU D,et al.Downregulation of microRNA146a inhibits ovarian granulosa cell apoptosis by simultaneously targeting interleukin1 receptorassociated kinase and tumor necrosis factor receptorassociated factor 6[J].Molecular Medicine Reports,2015,12(4):5155-5162.
[83] INOUE N,MATSUDA F,GOTO Y,et al.Role of cell-death ligand-receptor system of granulosa cells in selective follicular atresia in porcine ovary[J].Journal of Reproduction and Development,2011,57(2):169-175.
[84] NIE M,YU S,PENG S,et al.miR-23a and miR-27a promote human granulosa cell apoptosis by targeting SMAD5[J].Biology of Reproduction,2015,93(4):98.
[85] LIU T,LIN J,CHEN C,et al.microRNA-146b-5p overexpression attenuates premature ovarian failure in mice by inhibiting the Dab2ip/Ask1/p38-Mapk pathway and gammaH2A.X phosphorylation[J].Cell Proliferation,2021,54(1):e12954.
[86] DANG Y,WANG X,HAO Y,et al.microRNA-379-5p is associate with biochemical premature ovarian insufficiency through PARP1 and XRCC6[J].Cell Death and Disease,2018,9(2):106.
[87] SUN B,MA Y,WANG F,et al.miR-644-5p carried by bone mesenchymal stem cell-derived exosomes targets regulation of p53 to inhibit ovarian granulosa cell apoptosis[J].Stem Cell Research and Therapy,2019,10(1):360.
[88] AI A,XIONG Y,WU B,et al.Induction of miR-15a expression by tripterygium glycosides caused premature ovarian failure by suppressing the Hippo-YAP/TAZ signaling effector Lats1[J].Gene,2018,678:155-163.
[89] XU Z,STOKOE D,KANE L P,et al.The inducible expression of the tumor suppressor gene PTEN promotes apoptosis and decreases cell size by inhibiting the PI3K/Akt pathway in Jurkat T cells[J].Cell Growth and Differentiation,2002,13(7):285-296.
[90] YANG M,LIN L,SHA C,et al.Bone marrow mesenchymal stem cell-derived exosomal miR-144-5p improves rat ovarian function after chemotherapy-induced ovarian failure by targeting PTEN[J].Laboratory Investigation,2020,100(3):342-352.
[91] LI Y,XIANG Y,SONG Y,et al.Dysregulated miR-142,-33b and -423 in granulosa cells target TGFBR1 and SMAD7:A possible role in polycystic ovary syndrome[J].Molecular Human Reproduction,2019,25(10):638-646.
[92] YANG L,LI Y,WANG X,et al.microRNA320a inhibition decreases insulininduced KGN cell proliferation and apoptosis by targeting PCGF1[J].Molecular Medicine Reports,2017,16(4):5706-5712.
[93] LU J,XUE Y,WANG Y,et al.ciRS-126 inhibits proliferation of ovarian granulosa cells through targeting the miR-21-PDCD4-ROS axis in a polycystic ovarian syndrome model[J].Cell and Tissue Research,2020,381(1):189-201.
[94] ZHANG X,DANG Y,LIU R,et al.microRNA-127-5p impairs function of granulosa cells via HMGB2 gene in premature ovarian insufficiency[J].Journal of Cellular Physiology,2020,235(11):8826-8838.
[95] LEE R C,FEINBAUM R L,AMBROS V.The C.elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14[J].Cell,1993,75:843-854.
[96] XIE X,LU J,KULBOKAS E J,et al.Systematic discovery of regulatory motifs in human promoters and 3'UTRs by comparison of several mammals[J].Nature,2005,434(7031):338-345.
[97] CAO T,ZHEN X C.Dysregulation of miRNA and its potential therapeutic application in schizophrenia[J].CNS Neuroscience & Therapeutics,2018,24(7):586-597.
[98] LIANG J,WANG S,WANG Z.Role of microRNAs in embryo implantation[J].Reproductive Biology and Endocrinology,2017,15(1):90.
[99] LI Y,FANG Y,LIU Y,et al.microRNAs in ovarian function and disorders[J].Journal of Ovarian Research,2015,8:51.
[100] ZHANG J,XU Y,LIU H,et al.microRNAs in ovarian follicular atresia and granulosa cell apoptosis[J].Reproductive Biology and Endocrinology,2019,17(1):9.

Research Advances on miRNA in Regulating the Apoptosis of Follicular Granulosa Cells and Its Mechanism

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[15]	ZHU Xinying, GUO Shuai, ZHAN Xiaoyan, ZHONG Dengke, ZHENG Jiangping, HUA Zhimin, LI Tianshun. Effects of miR-188 on the Proliferation, Migration and Apoptosis of Mouse Breast Cancer Cells [J]. China Animal Husbandry and Veterinary Medicine, 2022, 49(3): 1153-1161.