miR-23a and miR-27a promote human granulosa cell apoptosis by targeting SMAD51

Biology of Reproduction

Volumn 93, Issue 4, 2015, Pages

  Nie, Mingyue ^a,b   Yu, Song ^a,b   Peng, Sha ^b   Fang, Ying ^b   Wang, Hongmei ^a,b   Yang, Xiaokui ^a  

^a CAPITAL MEDICAL UNIVERSITY   (China)

^b INSTITUTE OF ZOOLOGY   (China)

Author keywords

Apoptosis; Granulosa cells; miR 23a; miR 27a; Ovary; SMAD5

Indexed keywords

CASPASE 3; CASPASE 8; FAS ANTIGEN; FAS LIGAND; MICRORNA; MICRORNA 23A; MICRORNA 27A; SMAD5 PROTEIN; UNCLASSIFIED DRUG; CASP3 PROTEIN, HUMAN; CASP8 PROTEIN, HUMAN; MIRN23 MICRORNA, HUMAN; MIRN27 MICRORNA, HUMAN; SMAD5 PROTEIN, HUMAN;

ADULT; APOPTOSIS; ARTICLE; CONTROLLED STUDY; EMBRYO TRANSFER; FEMALE; FERTILIZATION IN VITRO; GRANULOSA CELL; HUMAN; HUMAN CELL; LUCIFERASE ASSAY; PRIORITY JOURNAL; PROTEIN TARGETING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; GENETIC TRANSFECTION; GENETICS; MALE; PHYSIOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ADULT; APOPTOSIS; CASPASE 3; CASPASE 8; FAS LIGAND PROTEIN; FEMALE; FERTILIZATION IN VITRO; GRANULOSA CELLS; HUMANS; MALE; MICRORNAS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SMAD5 PROTEIN; TRANSFECTION;

EID: 84947230968     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.115.130690     Document Type: Article

References (43)

1. Adhikari D, Liu K. Molecular mechanisms underlying the activation of mammalian primordial follicles. Endocr Rev 2009; 30:438-464.
2. Inoue N, Matsuda F, Goto Y, Manabe N. Role of cell-death ligandreceptor system of granulosa cells in selective follicular atresia in porcine ovary. J Reprod Dev 2011; 57:169-175.
3. Johnson AL. Granulosa cell apoptosis: conservation of cell signaling in an avian ovarian model system. Biol Signals Recept 2000; 9:96-101.
4. Sontakke SD, Mohammed BT, McNeilly AS, Donadeu FX. Characterization of microRNAs differentially expressed during bovine follicle development. Reproduction 2014; 148:271-283.
5. Donadeu FX, Schauer SN, Sontakke SD. Involvement of miRNAs in ovarian follicular and luteal development. J Endocrinol 2012; 215: 323-334.
6. Toloubeydokhti T, Bukulmez O, Chegini N. Potential regulatory functions of microRNAs in the ovary. Semin Reprod Med 2008; 26:469-478.
7. Yoon JH, Abdelmohsen K, Gorospe M. Functional interactions among microRNAs and long noncoding RNAs. Semin Cell Dev Biol 2014; 34: 9-14.
8. Bentwich I, Avniel A, Karov Y, Aharonov R, Gilad S, Barad O, Barzilai A, Einat P, Einav U, Meiri E, Sharon E, Spector Y, et al. Identification of hundreds of conserved and nonconserved human microRNAs. Nat Genet 2005; 37:766-770.
9. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009; 19:92-105.
10. Hossain MM, Ghanem N, Hoelker M, Rings F, Phatsara C, Tholen E, Schellander K, Tesfaye D. Identification and characterization of miRNAs expressed in the bovine ovary. BMC Genomics 2009; 10:443.
11. Lei L, Jin S, Gonzalez G, Behringer RR, WoodruffTK. The regulatory role of Dicer in folliculogenesis in mice. Mol Cell Endocrinol 2010; 315: 63-73.
12. Liu J, Yao W, Yao Y, Du X, Zhou J, Ma B, Liu H, Li Q, Pan Z. MiR-92a inhibits porcine ovarian granulosa cell apoptosis by targeting Smad7 gene. FEBS Lett 2014; 588:4497-4503.
13. Liu J, Du X, Zhou J, Pan Z, Liu H, Li Q. MicroRNA-26b functions as a proapoptotic factor in porcine follicular granulosa cells by targeting Smaand Mad-related protein 4. Biol Reprod 2014; 91:146.
14. Chhabra R, Dubey R, Saini N. Gene expression profiling indicate role of ER stress in miR-23a;27a;24-2 cluster induced apoptosis in HEK293T cells. RNA Biol 2011; 8:648-664.
15. Yang X, Zhou Y, Peng S, Wu L, Lin HY, Wang S, Wang H. Differentially expressed plasma microRNAs in premature ovarian failure patients and the potential regulatory function of mir-23a in granulosa cell apoptosis. Reproduction 2012; 144:235-244.
16. Kim YJ, Ku SY, Kim YY, Liu HC, Chi SW, Kim SH, Choi YM, Kim JG, Moon SY. MicroRNAs transfected into granulosa cells may regulate oocyte meiotic competence during in vitro maturation of mouse follicles. Hum Reprod 2013; 28:3050-3061.
17. Xu L, Xiang J, Shen J, Zou X, Zhai S, Yin Y, Li P, Wang X, Sun Q. Oncogenic MicroRNA-27a is a target for genistein in ovarian cancer cells. Anticancer Agents Med Chem 2013; 13:1126-1132.
18. Shi FT, Cheung AP, Klausen C, Huang HF, Leung PC. Growth differentiation factor 9 reverses activin A suppression of steroidogenic acute regulatory protein expression and progesterone production in human granulosa-lutein cells. J Clin Endocrinol Metab 2010; 95:E172-E180.
19. Xu B, Zhang YW, Tong XH, Liu YS. Characterization of microRNA profile in human cumulus granulosa cells: Identification of microRNAs that regulate Notch signaling and are associated with PCOS. Mol Cell Endocrinol 2015; 404:26-36.
20. Karita M, Yamashita Y, Hayashi A, Yoshida Y, Hayashi M, Yamamoto H, Tanabe A, Terai Y, Ohmichi M. Does advanced-stage endometriosis affect the gene expression of estrogen and progesterone receptors in granulosa cells? Fertil Steril 2011; 95:889-894.
21. Yang X, Fraser M, Moll UM, Basak A, Tsang BK. Akt-mediated cisplatin resistance in ovarian cancer: modulation of p53 action on caspasedependent mitochondrial death pathway. Cancer Res 2006; 66:3126-3136.
22. Yang X, Fraser M, Abedini MR, Bai T, Tsang BK. Regulation of apoptosis-inducing factor-mediated, cisplatin-induced apoptosis by Akt. Br J Cancer 2008; 98:803-808.
23. Quirk SM, Cowan RG, Joshi SG, Henrikson KP. Fas antigen-mediated apoptosis in human granulosa/luteal cells. Biol Reprod 1995; 52:279-287.
24. Matsuda-Minehata F, Inoue N, Goto Y, Manabe N. The regulation of ovarian granulosa cell death by pro-and anti-apoptotic molecules. J Reprod Dev 2006; 52:695-705.
25. Hughes MA, Harper N, Butterworth M, Cain K, Cohen GM, MacFarlane M. Reconstitution of the death-inducing signaling complex reveals a substrate switch that determines CD95-mediated death or survival. Mol Cell 2009; 35:265-279.
26. Christenson LK. MicroRNA control of ovarian function. Anim Reprod 2010; 7:129-133.
27. Jiang L, Huang J, Li L, Chen Y, Chen X, Zhao X, Yang D. MicroRNA-93 promotes ovarian granulosa cells proliferation through targeting CDKN1A in polycystic ovarian syndrome. J Clin Endocrinol Metab 2015; 100: E729-E738.
28. Wang T, Li F, Tang S. MiR-30a upregulates BCL2A1, IER3 and cyclin D2 expression by targeting FOXL2. Oncol Lett 2015; 9:967-971.
29. Liu N, Sun YY, Zhang XW, Chen S, Wang Y, Zhang ZX, Song SW, Qiu GB, Fu WN. Oncogenic miR-23a in pancreatic ductal adenocarcinogenesis via inhibiting APAF1. Dig Dis Sci 2015; 60:2000-2008.
30. Sabirzhanov B, Zhao Z, Stoica BA, Loane DJ, Wu J, Borroto C, Dorsey SG, Faden AI. Downregulation of miR-23a and miR-27a following experimental traumatic brain injury induces neuronal cell death through activation of proapoptotic Bcl-2 proteins. J Neurosci 2014; 34: 10055-10071.
31. Liu G, Cao P, Chen H, Yuan W, Wang J, Tang X. MiR-27a regulates apoptosis in nucleus pulposus cells by targeting PI3K. PLoS One 2013; 8: e75251.
32. Musto A, Navarra A, Vocca A, Gargiulo A, Minopoli G, Romano S, Romano MF, Russo T, Parisi S. miR-23a, miR-24 and miR-27a protect differentiating ESCs from BMP4-induced apoptosis. Cell Death Differ 2015; 22:1047-1057.
33. Jahid S, Sun J, Edwards RA, Dizon D, Panarelli NC, Milsom JW, Sikandar SS, Gumus ZH. Lipkin SM. miR-23a promotes the transition from indolent to invasive colorectal cancer. Cancer Discov 2012; 2: 540-553.
34. Cao M, Li Y, Lu H, Meng Q, Wang L, Cai L, Dong X. MiR-23a-mediated migration/invasion is rescued by its target, IRS-1, in non-small cell lung cancer cells. J Cancer Res Clin Oncol 2014; 140:1661-1670.
35. Shang J, Yang F, Wang Y, Wang Y, Xue G, Mei Q, Wang F, Sun S. MicroRNA-23a antisense enhances 5-fluorouracil chemosensitivity through APAF-1/caspase-9 apoptotic pathway in colorectal cancer cells. J Cell Biochem 2014; 115:772-784.
36. Li Z, Hu S, Wang J, Cai J, Xiao L, Yu L, Wang Z. MiR-27a modulates MDR1/P-glycoprotein expression by targeting HIPK2 in human ovarian cancer cells. Gynecol Oncol 2010; 119:125-130.
37. Yang RJ, Li JY, Zhao ZH, Gao X, Gao HJ, Xu SZ. Fas expression and mediated activation of an apoptosis programme in bovine follicular granulosa cells in vitro. Reprod Domest Anim 2012; 47:537-543.
38. Lopez-Rios J. Sensing BMP pathway activity by immune detection of phosphorylated R-Smad proteins in mouse embryonic kidney. Methods Mol Biol 2012; 886:267-273.
39. Shimizu T, Kayamori T, Murayama C, Miyamoto A. Bone morphogenetic protein (BMP)-4 and BMP-7 suppress granulosa cell apoptosis via different pathways: BMP-4 via PI3K/PDK-1/Akt and BMP-7 via PI3K/PDK-1/PKC. Biochem Biophys Res Commun 2012; 417:869-873.
40. Tripurani SK, Cook RW, Eldin KW, Pangas SA. BMP-specific SMADs function as novel repressors of PDGFA and modulate its expression in ovarian granulosa cells and tumors. Oncogene 2013; 32:3877-3885.
41. Hayano S, Komatsu Y, Pan H, Mishina Y. Augmented BMP signaling in the neural crest inhibits nasal cartilage morphogenesis by inducing p53-mediated apoptosis. Development 2015; 142:1357-1367.
42. Pangas SA, Li X, Umans L, Zwijsen A, Huylebroeck D, Gutierrez C, Wang D, Martin JF, Jamin SP, Behringer RR, Robertson EJ, Matzuk MM. Conditional deletion of Smad1 and Smad5 in somatic cells of male and female gonads leads to metastatic tumor development in mice. Mol Cell Biol 2008; 28:248-257.
43. Van Themsche C, Chaudhry P, Leblanc V, Parent S, Asselin E. XIAP gene expression and function is regulated by autocrine and paracrine TGFbeta signaling. Mol Cancer 2010; 9:216.