MicroRNA-378 regulates oocyte maturation via the suppression of aromatase in porcine cumulus cells

American Journal of Physiology - Endocrinology and Metabolism

Volumn 308, Issue 6, 2015, Pages E525-E534

  Pan, Bo ^a   Toms, Derek ^a   Shen, Wei ^b   Li, Julang ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b QINGDAO AGRICULTURAL UNIVERSITY   (China)

Author keywords

Cumulus; microRNA 378; Oocyte

Indexed keywords

ADAMTS1 PROTEIN; AROMATASE; BONE MORPHOGENETIC PROTEIN 15; GROWTH DIFFERENTIATION FACTOR 9; MICRORNA; MICRORNA 378; UNCLASSIFIED DRUG; ESTRADIOL;

ANIMAL CELL; ARTICLE; BLASTOCYST; CONTROLLED STUDY; CULTURE MEDIUM; CUMULUS CELL; FEMALE; FERTILIZATION IN VITRO; GENE EXPRESSION; GENE TRANSFER; GERMINAL VESICLE; NONHUMAN; OOCYTE MATURATION; OVARY FOLLICLE; PIG; PRACTICE GUIDELINE; PRIORITY JOURNAL; VIRAL GENE DELIVERY SYSTEM; ZONA PELLUCIDA; ANIMAL; CELL CULTURE; DOWN REGULATION; GENE EXPRESSION REGULATION; GENETICS; IN VITRO OOCYTE MATURATION; METABOLISM; OOCYTE; OOCYTE DEVELOPMENT; PARACRINE SIGNALING; PHYSIOLOGY;

ANIMALS; AROMATASE; CELLS, CULTURED; CUMULUS CELLS; DOWN-REGULATION; ESTRADIOL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; IN VITRO OOCYTE MATURATION TECHNIQUES; MICRORNAS; OOCYTES; OOGENESIS; PARACRINE COMMUNICATION; SWINE;

EID: 84937418182     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00480.2014     Document Type: Article

References (62)

1. Abd El Naby WS, Hagos TH, Hossain MM, Salilew-Wondim D, Gad AY, Rings F, Cinar MU, Tholen E, Looft C, Schellander K, Hoelker M, Tesfaye D. Expression analysis of regulatory microRNAs in bovine cumulus oocyte complex and preimplantation embryos. Zygote 21: 31-51, 2013.
2. Ackert CL, Gittens JE, O'Brien MJ, Eppig JJ, Kidder GM. Intercellular communication via connexin43 gap junctions is required for ovarian folliculogenesis in the mouse. Dev Biol 233: 258-270, 2001.
3. Baley J, Li J. MicroRNAs and ovarian function. J Ovarian Res 5: 8, 2012.
4. Barbato C, Ruberti F, Pieri M, Vilardo E, Costanzo M, Ciotti MT, Zona C, Cogoni C. MicroRNA-92 modulates K(+) Cl(-) co-transporter KCC2 expression in cerebellar granule neurons. J Neurochem 113: 591-600, 2010.
5. Brown HM, Dunning KR, Robker RL, Boerboom D, Pritchard M, Lane M, Russell DL. ADAMTS1 cleavage of versican mediates essential structural remodeling of the ovarian follicle and cumulus-oocyte matrix during ovulation in mice. Biol Reprod 83: 549-557, 2010.
6. Brown RM, Davis MG, Hayashi K, MacLean JA. Regulated expression of Rhox8 in the mouse ovary: evidence for the role of progesterone and RHOX5 in granulosa cells. Biol Reprod 88: 126, 2013.
7. Buccione R, Schroeder AC, Eppig JJ. Interactions between somatic cells and germ cells throughout mammalian oogenesis. Biol Reprod 43: 543-547, 1990.
8. Carletti MZ, Fiedler SD, Christenson LK. MicroRNA 21 blocks apoptosis in mouse periovulatory granulosa cells. Biol Reprod 83: 286-295, 2010.
9. Chen J, Torcia S, Xie F, Lin CJ, Cakmak H, Franciosi F, Horner K, Onodera C, Song JS, Cedars MI, Ramalho-Santos M, Conti M. Somatic cells regulate maternal mRNA translation and developmental competence of mouse oocytes. Nat Cell Biol 15: 1415-1423, 2013.
10. Chen L, Russell PT, Larsen WJ. Functional significance of cumulus expansion in the mouse: roles for the preovulatory synthesis of hyaluronic acid within the cumulus mass. Mol Reprod Dev 34: 87-93, 1993.
11. da Silveira JC, Veeramachaneni DN, Winger QA, Carnevale EM, Bouma GJ. Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: a possible new form of cell communication within the ovarian follicle. Biol Reprod 86: 71, 2012.
12. Eichner LJ, Perry MC, Dufour CR, Bertos N, Park M, St-Pierre J, Giguère V. miR-378(*) mediates metabolic shift in breast cancer cells via the PGC-1β/ERRγ transcriptional pathway. Cell Metab 12: 352-361, 2010.
13. Elvin JA, Yan C, Wang P, Nishimori K, Matzuk MM. Molecular characterization of the follicle defects in the growth differentiation factor 9-deficient ovary. Mol Endocrinol 13: 1018-1034, 1999.
14. Eppig JJ. Intercommunication between mammalian oocytes and companion somatic cells. Bioessays 13: 569-574, 1991.
15. Eppig JJ, Wigglesworth K, Chesnel F. Secretion of cumulus expansion enabling factor by mouse oocytes: relationship to oocyte growth and competence to resume meiosis. Dev Biol 158: 400-409, 1993.
16. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806-811, 1998.
17. Fulop C, Szanto S, Mukhopadhyay D, Bardos T, Kamath RV, Rugg MS, Day AJ, Salustri A, Hascall VC, Glant TT, Mikecz K. Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6 deficient mice. Development 130: 2253-2261, 2003.
18. Gallo RV. Pulsatile LH release during the ovulatory LH surge on proestrus in the rat. Biol Reprod 24: 100-104, 1981.
19. Gittens JE, Barr KJ, Vanderhyden BC, Kidder GM. Interplay between paracrine signaling and gap junctional communication in ovarian follicles. J Cell Sci 118: 113-122, 2005.
20. Gui LM, Joyce IM. RNA interference evidence that growth differentiation factor-9 mediates oocyte regulation of cumulus expansion in mice. Biol Reprod 72: 195-199, 2005.
21. Helwak A, Kudla G, Dudnakova T, Tollervey D. Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell 153: 654-665, 2013.
22. Hess KA, Chen L, Larsen WJ. Inter-alpha-inhibitor binding to hyaluronan in the cumulus extracellular matrix is required for optimal ovulation and development of mouse oocytes. Biol Reprod 61: 436-443, 1999.
23. Hirao Y, Nagai T, Kubo M, Miyano T, Miyake M, Kato S. In vitro growth and maturation of pig oocytes. J Reprod Fertil 100: 333-339, 1994.
24. Hwang HW, Mendell JT. MicroRNAs in cell proliferation, cell death, and tumorigenesis. Br J Cancer 96 Suppl: R40-R44, 2007.
25. Jamnongjit M, Gill A, Hammes SR. Epidermal growth factor receptor signaling is required for normal ovarian steroidogenesis and oocyte maturation. Proc Natl Acad Sci USA 102: 16257-16262, 2005.
26. Juengel JL, Hudson NL, Heath DA, Smith P, Reader KL, Lawrence SB, O'Connell AR, Laitinen MP, Cranfield M, Groome NP, Ritvos O, McNatty KP. Growth differentiation factor 9 and bone morphogenetic protein 15 are essential for ovarian follicular development in sheep. Biol Reprod 67: 1777-1789, 2002.
27. Kidder GM, Vanderhyden BC. Bidirectional communication between oocytes and follicle cells: ensuring oocyte developmental competence. Can J Physiol Pharmacol 88: 399-413, 2010.
28. Kim J, Bagchi IC, Bagchi MK. Control of ovulation in mice by progesterone receptor-regulated gene networks. Mol Hum Reprod 15: 821-828, 2009.
29. Knight PG, Glister C. TGF-beta superfamily members and ovarian follicle development. Reproduction 132: 191-206, 2006.
30. Linher K, Wu D, Li J. Glial cell line-derived neurotrophic factor: an intraovarian factor that enhances oocyte developmental competence in vitro. Endocrinology 148: 4292-4301, 2007.
31. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(+Delta Delta C(T)) Method. Methods 25: 402-408, 2001.
32. Ma T, Jiang H, Gao Y, Zhao Y, Dai L, Xiong Q, Xu Y, Zhao Z, Zhang J. Microarray analysis of differentially expressed microRNAs in nonregressed and regressed bovine corpus luteum tissue; microRNA-378 may suppress luteal cell apoptosis by targeting the interferon gamma receptor 1 gene. J Appl Genet 52: 481-486, 2011.
33. MacLean JA 2nd, Rao MK, Doyle KM, Richards JS, Wilkinson MF. Regulation of the Rhox5 homeobox gene in primary granulosa cells: preovulatory expression and dependence on SP1/SP3 and GABP. Biol Reprod 73: 1126-1134, 2005.
34. Matsumoto H, Ma W, Smalley W, Trzaskos J, Breyer RM, Dey SK. Diversification of cyclooxygenase-2-derived prostaglandins in ovulation and implantation. Biol Reprod 64: 1557-1565, 2001.
35. Miles JR, McDaneld TG, Wiedmann RT, Cushman RA, Echternkamp SE, Vallet JL, Smith TP. MicroRNA expression profile in bovine cumulus-oocyte complexes: possible role of let-7 and miR-106a in the development of bovine oocytes. Anim Reprod Sci 130: 16-26, 2012.
36. Nagyova E, Scsukova S, Kalous J, Mlynarcikova A. Effects of RU486 and indomethacin on meiotic maturation, formation of extracellular matrix, and progesterone production by porcine oocyte-cumulus complexes. Domest Anim Endocrinol 48: 7-14, 2014.
37. Ochsner SA, Russell DL, Day AJ, Breyer RM, Richards JS. Decreased expression of tumor necrosis factor-alpha-stimulated gene 6 in cumulus cells of the cyclooxygenase-2 and EP2 null mice. Endocrinology 144: 1008-1019, 2003.
38. Rankin T, Familari M, Lee E, Ginsberg A, Dwyer N, Blanchette-Mackie J, Drago J, Westphal H, Dean J. Mice homozygous for an insertional mutation in the Zp3 gene lack a zona pellucida and are infertile. Development 122: 2903-2910, 1996.
39. Robker RL, Russell DL, Espey LL, Lydon JP, O'Malley BW, Richards JS. Progesterone-regulated genes in the ovulation process: ADAMTS-1 and cathepsin L proteases. Proc Natl Acad Sci USA 97: 4689-4694, 2000.
40. Salustri A, Yanagishita M, Underhill CB, Laurent TC, Hascall VC. Localization and synthesis of hyaluronic acid in the cumulus cells and mural granulosa cells of the preovulatory follicle. Dev Biol 151: 541-551, 1992.
41. Schauer SN, Sontakke SD, Watson ED, Esteves CL, Donadeu FX. Involvement of miRNAs in equine follicle development. Reproduction 146: 273-282, 2013.
42. Sen A, Prizant H, Light A, Biswas A, Hayes E, Lee HJ, Barad D, Gleicher N, Hammes SR. Androgens regulate ovarian follicular development by increasing follicle stimulating hormone receptor and microRNA-125b expression. Proc Natl Acad Sci USA 111: 3008-3013, 2014.
43. Shimada M, Nishibori M, Yamashita Y, Ito J, Mori T, Richards JS. Down-regulated expression of A disintegrin and metalloproteinase with thrombospondin-like repeats-1 by progesterone receptor antagonist is associated with impaired expansion of porcine cumulus-oocyte complexes. Endocrinology 145: 4603-4614, 2004.
44. Shimada M, Yamashita Y, Ito J, Okazaki T, Kawahata K, Nishibori M. Expression of two progesterone receptor isoforms in cumulus cells and their roles during meiotic resumption of porcine oocytes. J Mol Endocrinol 33: 209-225, 2004.
45. Simon AM, Goodenough DA, Li E, Paul DL. Female infertility in mice lacking connexin 37. Nature 385: 525-529, 1997.
46. Sirotkin AV, Ovcharenko D, Grossmann R, Laukova M, Mlyncek M. Identification of microRNAs controlling human ovarian cell steroidogenesis via a genome-scale screen. J Cell Physiol 219: 415-420, 2009.
47. Sohel MM, Hoelker M, Noferesti SS, Salilew-Wondim D, Tholen E, Looft C, Rings F, Uddin MJ, Spencer TE, Schellander K, Tesfaye D. Exosomal and Non-Exosomal Transport of Extra-Cellular microRNAs in Follicular Fluid: Implications for Bovine Oocyte Developmental Competence. PLoS One 8: e78505, 2013.
48. Su YQ, Wu X, O'Brien MJ, Pendola FL, Denegre JN, Matzuk MM, Eppig JJ. Synergistic roles of BMP15 and GDF9 in the development and function of the oocyte-cumulus cell complex in mice: genetic evidence for an oocyte-granulosa cell regulatory loop. Dev Biol 276: 64-73, 2004.
49. Sugiura K, Su YQ, Eppig JJ. Targeted suppression of Has2 mRNA in mouse cumulus cell-oocyte complexes by adenovirus-mediated shorthairpin RNA expression. Mol Reprod Dev 76: 537-547, 2009.
50. Sugiura K, Su YQ, Li Q, Wigglesworth K, Matzuk MM, Eppig JJ. Estrogen promotes the development of mouse cumulus cells in coordination with oocyte-derived GDF9 and BMP15. Mol Endocrinol 24: 2303-2314, 2010.
51. Suh N, Baehner L, Moltzahn F, Melton C, Shenoy A, Chen J, Blelloch R. MicroRNA function is globally suppressed in mouse oocytes and early embryos. Curr Biol 20: 271-277, 2010.
52. Testart J, Lassalle B, Frydman R, Belaisch JC. A study of factors affecting the success of human fertilization in vitro. II. Influence of semen quality and oocyte maturity on fertilization and cleavage. Biol Reprod 28: 425-431, 1983.
53. Toms D, Tsoi S, Dobrinsky J, Dyck MK, Li J. The effects of glial cell line-derived neurotrophic factor on the in vitro matured porcine oocyte transcriptome. Mol Reprod Dev 81: 217-229, 2014.
54. Toms D, Xu S, Pan B, Wu D, Li J. Progesterone receptor expression in granulosa cells is suppressed by microRNA-378-3p. Mol Cell Endocrinol 399: 95-102, 2015.
55. Troppmann B, Kossack N, Nordhoff V, Schüring AN, Gromoll J. MicroRNA miR-513a-3p acts as a co-regulator of luteinizing hormone/ chorionic gonadotropin receptor gene expression in human granulosa cells. Mol Cell Endocrinol 390: 65-72, 2014.
56. Varani S, Elvin JA, Yan C, DeMayo J, DeMayo FJ, Horton HF, Byrne MC, Matzuk MM. Knockout of pentraxin 3, a downstream target of growth differentiation factor-9, causes female subfertility. Mol Endocrinol 16: 1154-1167, 2002.
57. Williams AH, Liu N, van Rooij E, Olson EN. MicroRNA control of muscle development and disease. Curr Opin Cell Biol 21: 461-469, 2009.
58. Xu S, Linher-Melville K, Yang BB, Wu D, Li J. Micro-RNA378 (miR-378) regulates ovarian estradiol production by targeting aromatase. Endocrinology 152: 3941-3951, 2011.
59. Yan G, Zhang L, Fang T, Zhang Q, Wu S, Jiang Y, Sun H, Hu Y. MicroRNA-145 suppresses mouse granulosa cell proliferation by targeting activin receptor IB. FEBS Lett 586: 3263-3270, 2012.
60. Yao G, Yin M, Lian J, Tian H, Liu L, Li X, Sun F. MicroRNA-224 is involved in transforming growth factor-beta-mediated mouse granulosa cell proliferation and granulosa cell function by targeting Smad4. Mol Endocrinol 24: 540-551, 2010.
61. Yin M, Wang X, Yao G, Lü M, Liang M, Sun Y, Sun F. Transactivation of micrornA-320 by microRNA-383 regulates granulosa cell functions by targeting E2F1 and SF-1 proteins. J Biol Chem 289: 18239-18257, 2014.
62. Yoshida H, Takakura N, Kataoka H, Kunisada T, Okamura H, Nishikawa SI. Stepwise requirement of c-kit tyrosine kinase in mouse ovarian follicle development. Dev Biol 184: 122-137, 1997.