CoChat
Sign Up
Cited by 228Reproductive Biology and FertilityMicroRNA in disease regulationOvarian function and disorders

MicroRNAs in ovarian follicular atresia and granulosa cell apoptosis

Open access
Zhang, Jinbi, Xu, Yinxue, Liu, Honglin, Pan, Zengxiang·2019·Reproductive Biology and Endocrinology
DOI 10.1186/s12958-018-0450-yPMC PMC6329178
Open this paper in CoChat — free accountOpen PDF

Abstract

MicroRNAs (miRNAs) are short, noncoding RNAs that posttranscriptionally regulate gene expression. In the past decade, studies on miRNAs in ovaries have revealed the key roles of miRNAs in ovarian development and function. In this review, we first introduce the development of follicular atresia research and then summarize genome-wide studies on the ovarian miRNA profiles of different mammalian species. Differentially expressed miRNA profiles during atresia and other biological processes are herein compared. In addition, current knowledge on confirmed functional miRNAs during the follicular atresia process, which is mostly indicated by granulosa cell (GC) apoptosis, is presented. The main miRNA families and clusters, including the let-7 family, miR-23-27-24 cluster, miR-183-96-182 cluster and miR-17-92 cluster, and related pathways that are involved in follicular atresia are thoroughly summarized. A deep understanding of the roles of miRNA networks will not only help elucidate the mechanisms of GC apoptosis, follicular development, atresia and their disorders but also offer new diagnostic and treatment strategies for infertility and other ovarian dysfunctions.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1186/s12958-018-0450-y

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • In a genome-wide analysis of ovarian miRNA expression profiles in humans, mice, cows, pigs, goats, and other mammals, the miR-23 functional cluster is upregulated in human ovarian follicles, showing species specificity, which assumes a part in follicular atresia and promotes granulosa cell apoptosis.

    “In a genome-wide analysis of ovarian miRNA expression profiles in humans, mice, cows, pigs, goats, and other mammals, the miR-23 functional cluster is upregulated in human ovarian follicles, showing species specificity, which assumes a part in follicular atresia and promotes granulosa cell apoptosis [123].”

    From Recent advances of miR-23 in human diseases and growth development (2025) · cites this paper as [123]

    Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The citation lists haven’t been fetched yet

References 129 · Cited by 228

Research works printed but not linked: 129

  1. [1]Quirk SM Cowan RG Harman RM Hu CL Porter DA Ovarian follicular growth and atresia: the relationship between cell proliferation and survival J Anim Sci 2004 82 E-Suppl E40 E52 10.2527/2004.8213_supplE40x 15471814 · DOI
  2. [2]Baker TG A quantitative and cytological study of germ cells in human ovaries Proc R Soc Lond B Biol Sci 1963 158 417 433 10.1098/rspb.1963.0055 14070052 · DOI
  3. [3]Brachova P, Hung WT, Mcginnis LK, Christenson LK. MicroRNA regulation of endocrine functions in the ovary. In: Menon, Goldstrohm, editors. Post-transcriptional Mechanisms in Endocrine Regulation. Cham: Springer; 2016.
  4. [4]Faddy M Gosden R Gougeon A Richardson SJ Nelson J Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause Hum Reprod 1992 7 1342 1346 10.1093/oxfordjournals.humrep.a137570 1291557 · DOI
  5. [5]Manabe N Goto Y Matsudaminehata F Inoue N Maeda A Sakamaki K Miyano T Regulation mechanism of selective atresia in porcine follicles: regulation of granulosa cell apoptosis during atresia J Reprod Dev 2004 50 493 514 10.1262/jrd.50.493 15514456 · DOI
  6. [6]Moor R HAY MF Dott H Cran D Macroscopic identification and steroidogenic function of atretic follicles in sheep J Endocrinol 1978 77 309 318 10.1677/joe.0.0770309 660074 · DOI
  7. [7]Maeda A Goto Y Matsuda-Minehata F Cheng Y Inoue N Manabe N Changes in expression of interleukin-6 receptors in granulosa cells during follicular atresia in pig ovaries J Reprod Dev 2007 53 727 736 10.1262/jrd.19011 17380037 · DOI
  8. [8]Rodgers RJ Irving-Rodgers HF Morphological classification of bovine ovarian follicles Reproduction 2010 139 309 318 10.1530/REP-09-0177 19786400 · DOI
  9. [9]Nishimoto H Hamano S Hill GA Miyamoto A Tetsuka M Classification of bovine follicles based on the concentrations of steroids, glucose and lactate in follicular fluid and the status of accompanying follicles J Reprod Dev 2009 55 219 10.1262/jrd.20114 19194065 · DOI
  10. [10]Rosales-Torres AM Avalos-Rodriguez A Vergara-Onofre M Hernandez-Perez O Ballesteros LM Garcia-Macedo R Ortiz-Navarrete V Rosado A Multiparametric study of atresia in ewe antral follicles: histology, flow cytometry, internucleosomal DNA fragmentation, and lysosomal enzyme activities in granulosa cells and follicular fluid Mol Reprod Dev 2000 55 270 281 10.1002/(SICI)1098-2795(200003)55:3<270::AID-MRD5>3.0.CO;2-H 10657046 · DOI
  11. [11]Jinbi Z, Fei L, Zengxiang P, et al. Comparative study of methods to determine the follicular atresia extent in pigs. J Nanjing Agric Univ. 2013;1:115-9.
  12. [12]Marion GB Gier HT Choudary JB Micromorphology of the bovine ovarian follicular system J Anim Sci 1968 27 451 10.2527/jas1968.272451x 5646345 · DOI
  13. [13]Tilly JL Kowalski KI Johnson AL Hsueh AJ Involvement of apoptosis in ovarian follicular atresia and postovulatory regression Endocrinology 1991 129 2799 2801 10.1210/endo-129-5-2799 1718732 · DOI
  14. [14]Hughes FM Jr Gorospe WC Biochemical identification of apoptosis (programmed cell death) in granulosa cells: evidence for a potential mechanism underlying follicular atresia Endocrinology 1991 129 2415 2422 10.1210/endo-129-5-2415 1935775 · DOI
  15. [15]Jolly PD Tisdall DJ Heath DA Lun S McNatty KP Apoptosis in bovine granulosa cells in relation to steroid synthesis, cyclic adenosine 3′,5′-monophosphate response to follicle-stimulating hormone and luteinizing hormone, and follicular atresia Biol Reprod 1994 51 934 944 10.1095/biolreprod51.5.934 7849196 · DOI
  16. [16]Murdoch WJ Programmed cell death in preovulatory ovine follicles Biol Reprod 1995 53 8 12 10.1095/biolreprod53.1.8 7669860 · DOI
  17. [17]Sugimoto M Manabe N Kimura Y MYOUMOTO A IMAI Y OHNO H MIYAMOTO H Ultrastructural changes in granulosa cells in porcine antral follicles undergoing atresia indicate apoptotic cell death J Reprod Dev 1998 44 7 14 10.1262/jrd.44.7 · DOI
  18. [18]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 10.1262/jrd.18069 16926526 · DOI
  19. [19]Manabe N, Kimura Y, Uchio K, Tajima C, Matsushita H, Nakayama M, Sugimoto M, Miyamoto H. Regulatory mechanisms of granulosa cell apoptosis in ovarian follicle atresia. In: Ikura K, Nagao M, Masuda S, Sasaki R, editors. Animal cell technology: challenges for the 21st century. Dordrecht: Springer; 2002. p. 343–7.
  20. [20]Yu YS Sui HS Han ZB Li W Luo MJ Tan JH Apoptosis in granulosa cells during follicular atresia: relationship with steroids and insulin-like growth factors Cell Res 2004 14 341 346 10.1038/sj.cr.7290234 15353131 · DOI
  21. [21]Hussein MR Apoptosis in the ovary: molecular mechanisms Hum Reprod Update 2005 11 162 178 10.1093/humupd/dmi001 15705959 · DOI
  22. [22]Jääskeläinen M Kyrönlahti A Anttonen M Nishi Y Yanase T Secchiero P Zauli G Tapanainen J Heikinheimo M Vaskivuo T TRAIL pathway components and their putative role in granulosa cell apoptosis in the human ovary Differentiation 2009 77 369 376 10.1016/j.diff.2008.12.001 19281785 · DOI
  23. [23]Dressing GE Pang Y Dong J Thomas P Progestin signaling through mPRα in Atlantic croaker granulosa/theca cell cocultures and its involvement in progestin inhibition of apoptosis Endocrinology 2010 151 5916 5926 10.1210/en.2010-0165 20962051 PMC2999484 · DOI
  24. [24]Saller S, Kunz L, Dissen G, Stouffer R, Ojeda S, Berg D, Berg U, Mayerhofer A. Oxytocin receptors in the primate ovary: molecular identity and link to apoptosis in human granulosa cells. Hum Reprod. 2010. 10.1093/humrep/dep467. PMC2839908 20097922 · DOI
  25. [25]Lee Y Kim M Han J Yeom KH Lee S Baek SH Kim VN MicroRNA genes are transcribed by RNA polymerase II EMBO J 2004 23 4051 4060 10.1038/sj.emboj.7600385 15372072 PMC524334 · DOI
  26. [26]Tanzer A Stadler PF Molecular evolution of a microRNA cluster J Mol Biol 2004 339 327 335 10.1016/j.jmb.2004.03.065 15136036 · DOI
  27. [27]Chang T-C Pertea M Lee S Salzberg SL Mendell JT Genome-wide annotation of microRNA primary transcript structures reveals novel regulatory mechanisms Genome Res 2015 25 1401 1409 10.1101/gr.193607.115 26290535 PMC4561498 · DOI · Paper page
  28. [28]Kwon SC Nguyen TA Choi Y-G Jo MH Hohng S Kim VN Woo J-S Structure of human DROSHA Cell 2016 164 81 90 10.1016/j.cell.2015.12.019 26748718 · DOI
  29. [29]Meister G Landthaler M Patkaniowska A Dorsett Y Teng G Tuschl T Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs Mol Cell 2004 15 185 197 10.1016/j.molcel.2004.07.007 15260970 · DOI · Paper page
  30. [30]Wahid F Shehzad A Khan T Kim YY MicroRNAs: synthesis, mechanism, function, and recent clinical trials Biochim Biophys Acta 1803 2010 1231 1243 20619301
  31. [32]Donadeu FX Schauer SN Sontakke SD Involvement of miRNAs in ovarian follicular and luteal development J Endocrinol 2012 215 323 334 10.1530/JOE-12-0252 23038794 · DOI
  32. [33]Hossain MM Sohel MM Schellander K Tesfaye D Characterization and importance of microRNAs in mammalian gonadal functions Cell Tissue Res 2012 349 679 690 10.1007/s00441-012-1469-6 22842772 · DOI
  33. [34]Imbar T Eisenberg I Regulatory role of microRNAs in ovarian function Fertil Steril 2014 101 1524 1530 10.1016/j.fertnstert.2014.04.024 24882616 · DOI
  34. [35]Christenson LK MicroRNA control of ovarian function Anim Reprod 2010 7 129 133 21666774 PMC3111027
  35. [36]Maalouf SW Liu WS Pate JL MicroRNA in ovarian function Cell Tissue Res 2016 363 7 18 10.1007/s00441-015-2307-4 26558383 · DOI
  36. [37]Mcginnis LK Luense LJ Christenson LK MicroRNA in ovarian biology and disease Cold Spring Harb Perspect Med 2015 5 9 a022962 10.1101/cshperspect.a022962 25986593 PMC4561398 · DOI
  37. [38]Li Y Fang Y Liu Y Yang X MicroRNAs in ovarian function and disorders J Ovarian Res 2015 8 1 8 10.1186/s13048-015-0124-8 26232057 PMC4522283 · DOI
  38. [39]Hao W, Guo Y, Hao GM, Wang W. Research progress on miRNA-related mechanism of polycystic ovary syndrome. J Reprod Med. 2016;12:1126-9.
  39. [40]Wu N Gaur U Zhu Q Chen B Xu Z Zhao X Yang M Li D Expressed microRNA associated with high rate of egg production in chicken ovarian follicles Anim Genet 2017 48 205 216 10.1111/age.12516 27781291 · DOI
  40. [41]Jing Y Ke H Ren T Lou Y Zhao A High-throughput sequencing reveals differential expression of miRNAs in prehierarchal follicles of laying and brooding geese Physiol Genomics 2016 48 455 463 10.1152/physiolgenomics.00011.2016 27199452 PMC4967221 · DOI
  41. [42]Lin F Li R Pan ZX Zhou B Yu DB Wang XG Ma XS Han J Shen M Liu HL miR-26b promotes granulosa cell apoptosis by targeting ATM during follicular atresia in porcine ovary PLoS One 2012 7 e38640 10.1371/journal.pone.0038640 22737216 PMC3380909 · DOI
  42. [43]Sontakke SD Mohammed BT McNeilly AS Donadeu FX Characterization of microRNAs differentially expressed during bovine follicle development Reproduction 2014 148 271 283 10.1530/REP-14-0140 24920665 · DOI
  43. [44]Raphatphorn N Wei-Ting H Sumedha G Davis JS Wilaiwan C Christenson LK Characterization and small RNA content of extracellular vesicles in follicular fluid of developing bovine antral follicles Sci Rep 2016 6 25486 10.1038/srep25486 27158133 PMC4860563 · DOI
  44. [45]McBride D Carré W Sontakke SD Hogg CO Law A Donadeu FX Clinton M Identification of miRNAs associated with the follicular-luteal transition in the ruminant ovary Reproduction 2012 144 221 233 10.1530/REP-12-0025 22653318 · DOI
  45. [46]Yang S Wang S Luo A Ding T Lai Z Shen W Ma X Cao C Shi L Jiang J Expression patterns and regulatory functions of microRNAs during the initiation of primordial follicle development in the neonatal mouse ovary Biol Reprod 2013 89 126 23986572
  46. [47]Bahrami A, Miraieashtiani SR, Sadeghi M, Najafi A. miRNA-mRNA network involved in folliculogenesis interactome: systems biology approach. Reproduction. 2017;154. 10.1530/REP-17-0049. 28450315 · DOI
  47. [48]Gebremedhn S Salilew-Wondim D Ahmad I Sahadevan S Hossain MM Hoelker M Rings F Neuhoff C Tholen E Looft C MicroRNA expression profile in bovine granulosa cells of Preovulatory dominant and subordinate follicles during the late follicular phase of the estrous cycle PLoS One 2015 10 e0125912 10.1371/journal.pone.0125912 25993098 PMC4438052 · DOI
  48. [49]Fawzy IO Hamza MT Hosny KA Esmat G El Tayebi HM Abdelaziz AI miR-1275: a single microRNA that targets the three IGF2-mRNA-binding proteins hindering tumor growth in hepatocellular carcinoma FEBS Lett 2016 589 2257 2265 10.1016/j.febslet.2015.06.038 26160756 · DOI
  49. [50]Liu J Li X Yao Y Li Q Pan Z Li Q miR-1275 controls granulosa cell apoptosis and estradiol synthesis by impairing LRH-1/CYP19A1 axis Biochim Biophys Acta 2018 1861 246 10.1016/j.bbagrm.2018.01.009 29378329 · DOI
  50. [51]Hirata H Hinoda Y Ueno K Shahryari V Tabatabai ZL Dahiya R MicroRNA-1826 targets VEGFC, beta-catenin (CTNNB1) and MEK1 (MAP2K1) in human bladder cancer Carcinogenesis 2012 33 41 48 10.1093/carcin/bgr239 22049531 PMC3276333 · DOI
  51. [52]Hao Y Yang J Yin S Zhang H Fan Y Sun C Gu J Xi JJ The synergistic regulation of VEGF-mediated angiogenesis through miR-190 and target genes RNA 2014 20 1328 1336 10.1261/rna.044651.114 24962367 PMC4105756 · DOI
  52. [53]Chu HW Cheng CW Chou WC Hu LY Wang HW Hsiung CN Hsu HM Wu PE Hou MF Shen CY A novel estrogen receptor-microRNA 190a-PAR-1-pathway regulates breast cancer progression, a finding initially suggested by genome-wide analysis of loci associated with lymph-node metastasis Hum Mol Genet 2014 23 355 367 10.1093/hmg/ddt426 24009311 · DOI
  53. [54]Giannakakis A Sandaltzopoulos R Greshock J Liang S Huang J Hasegawa K Li C O'Brienjenkins A Katsaros D Weber BL miR-210 links hypoxia with cell cycle regulation and is deleted in human epithelial ovarian cancer Cancer Biol Ther 2008 7 255 264 10.4161/cbt.7.2.5297 18059191 PMC3233968 · DOI
  54. [55]Gee HE Camps C Buffa FM Patiar S Winter SC Betts G Homer J Corbridge R Cox G West CM hsa-mir-210 is a marker of tumor hypoxia and a prognostic factor in head and neck cancer Cancer 2010 116 2148 2158 20187102
  55. [56]Su JL Chen PS Johansson G Kuo ML Function and regulation of let-7 family microRNAs MicroRNA 2012 1 1 34 39 10.2174/2211536611201010034 25048088 · DOI
  56. [57]Roush S Slack FJ The let-7 family of microRNAs Trends Cell Biol 2008 18 505 516 10.1016/j.tcb.2008.07.007 18774294 · DOI
  57. [58]Zhou J Liu J Pan Z Du X Li X Ma B Yao W Li Q Liu H The let-7g microRNA promotes follicular granulosa cell apoptosis by targeting transforming growth factor-β type 1 receptor Mol Cell Endocrinol 2015 409 103 112 10.1016/j.mce.2015.03.012 25817543 · DOI
  58. [59]Cao R Wu WJ Zhou XL Xiao P Wang Y Liu HL Expression and preliminary functional profiling of the let-7 family during porcine ovary follicle atresia Mol Cells 2015 38 304 311 10.14348/molcells.2015.2122 25824548 PMC4400304 · DOI
  59. [60]Zhou Y, Zhu YZ, Zhang SH, Wang HM, Wang SY. MicroRNA expression profiles in premature ovarian failure patients and its potential regulate functions. Chin J Birth Health Hered. 2011;5:20-2.
  60. [61]Cao R Wu W Zhou X Liu K Li B Huang X Zhang Y Liu H Let-7g induces granulosa cell apoptosis by targeting MAP3K1 in the porcine ovary Int J Biochem Cell Biol 2015 68 148 157 10.1016/j.biocel.2015.08.011 26299328 · DOI
  61. [62]Heldin CH Landström M Moustakas A Mechanism of TGF-β signaling to growth arrest, apoptosis, and epithelial–mesenchymal transition Curr Opin Cell Biol 2009 21 166 10.1016/j.ceb.2009.01.021 19237272 · DOI
  62. [63]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 2010 24 540 551 10.1210/me.2009-0432 20118412 PMC5419098 · DOI
  63. [64]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 Sma-and mad-related protein 4 Biol Reprod 2014 91 146 25395673
  64. [65]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 10.1016/j.febslet.2014.10.021 25448599 · DOI
  65. [67]Yao W Pan Z Du X Zhang J Li Q miR-181b-induced SMAD7 downregulation controls granulosa cell apoptosis through TGF-Î2 signaling by interacting with the TGFBR1 promoter J Cell Physiol 2018 233 9 6807 6821 10.1002/jcp.26431 29319157 PMC13482426 · DOI
  66. [68]Nakao A Afrakhte M Morn A Nakayama T Christian JL Heuchel R Itoh S Kawabata M Heldin NE Heldin Amp CH Identification of SMAD7, a TGFβ-inducible antagonist of TGF-β signalling Nature 1997 389 631 635 10.1038/39369 9335507 · DOI
  67. [69]Schiffer M Bitzer M Roberts IS Kopp JB Ten DP Mundel P Böttinger EP Apoptosis in podocytes induced by TGF-beta and Smad7 J Clin Invest 2001 108 807 816 10.1172/JCI200112367 11560950 PMC200928 · DOI
  68. [70]Mendell JT miRiad roles for the miR-17-92 cluster in development and disease Cell 2008 133 217 222 10.1016/j.cell.2008.04.001 18423194 PMC2732113 · DOI
  69. [71]Dews M Fox JL Hultine S Sundaram P Wang W Liu YY Furth E Enders GH El-Deiry W Schelter JM The myc-miR-17~92 axis blunts TGF-beta signaling and production of multiple TGF{beta}-dependent antiangiogenic factors Cancer Res 2010 70 8233 8246 10.1158/0008-5472.CAN-10-2412 20940405 PMC3007123 · DOI
  70. [72]Mestdagh P Boström AK Impens F Fredlund E Van PG De AP Von SK Ghesquière B Schulte S Dews M The miR-17-92 microRNA cluster regulates multiple components of the TGF-β pathway in neuroblastoma Mol Cell 2010 40 762 773 10.1016/j.molcel.2010.11.038 21145484 PMC3032380 · DOI · Paper page
  71. [73]Talbert DR Wappel RL Moran DM Shell SA Bacus SS The role of Myc and the miR-17~92 cluster in histone deacetylase inhibitor induced apoptosis of solid tumors J Cancer Ther 2013 04 907 918 10.4236/jct.2013.44102 · DOI
  72. [74]Liang T Yu J Liu C Guo L An exploration of evolution, maturation, expression and function relationships in mir-23 ∼ 27 ∼ 24 cluster PLoS One 2014 9 e106223 10.1371/journal.pone.0106223 25157521 PMC4144971 · DOI
  73. [75]Wang F Zhu Y Guo L Dong L Liu H Yin H Zhang Z Li Y Liu C Ma Y A regulatory circuit comprising GATA1/2 switch and microRNA-27a/24 promotes erythropoiesis Nucleic Acids Res 2014 42 442 457 10.1093/nar/gkt848 24049083 PMC3874166 · DOI
  74. [76]Zhou Q Gallagher R Ufret-Vincenty R Li X Olson EN Wang S Regulation of angiogenesis and choroidal neovascularization by members of microRNA-23~27~24 clusters Proc Natl Acad Sci U S A 2011 108 8287 8292 10.1073/pnas.1105254108 21536891 PMC3100947 · DOI · Paper page
  75. [77]Li X Liu X Xu W Zhou P Gao P Jiang S Lobie PE Zhu T c-MYC-regulated miR-23a/24-2/27a cluster promotes mammary carcinoma cell invasion and hepatic metastasis by targeting Sprouty2 J Biol Chem 2013 288 18121 18133 10.1074/jbc.M113.478560 23649631 PMC3689956 · DOI
  76. [78]Nie M Yu S Peng S Fang Y Wang H Yang X miR-23a and miR-27a promote human granulosa cell apoptosis by targeting SMAD5 Biol Reprod 2015 93 98 10.1095/biolreprod.115.130690 26400397 · DOI
  77. [79]Li P Sheng C Huang L Zhang H Huang L Cheng Z Zhu Q MiR-183/−96/−182 cluster is up-regulated in most breast cancers and increases cell proliferation and migration Breast Cancer Res 2014 16 473 10.1186/s13058-014-0473-z 25394902 PMC4303194 · DOI
  78. [80]Mohammed BT Sontakke SD Ioannidis J Duncan WC Donadeu FX The adequate corpus luteum: miR-96 promotes luteal cell survival and progesterone production J Clin Endocrinol Metab 2017 102 2188 10.1210/jc.2017-00259 28368475 PMC5505194 · DOI
  79. [81]Shi F Lapolt PS Relationship between FoxO1 protein levels and follicular development, atresia, and luteinization in the rat ovary J Endocrinol 2003 179 195 203 10.1677/joe.0.1790195 14596671 · DOI
  80. [82]Herndon MK Law NC Donaubauer EM Kyriss B Hunzicker-Dunn M Forkhead box O member FOXO1 regulates the majority of follicle-stimulating hormone responsive genes in ovarian granulosa cells Mol Cell Endocrinol 2016 434 116 126 10.1016/j.mce.2016.06.020 27328024 PMC4983523 · DOI
  81. [83]Ma J Zhan Y Xu Z Li Y Luo A Ding F Cao X Chen H Liu Z ZEB1 induced miR-99b/let-7e/miR-125a cluster promotes invasion and metastasis in esophageal squamous cell carcinoma Cancer Lett 2017 398 37 45 10.1016/j.canlet.2017.04.006 28408353 · DOI
  82. [84]Khuu C Jevnaker AM Bryne M Osmundsen H An investigation into anti-proliferative effects of microRNAs encoded by the miR-106a-363 cluster on human carcinoma cells and keratinocytes using microarray profiling of miRNA transcriptomes Front Genet 2014 5 246 10.3389/fgene.2014.00246 25202322 PMC4142865 · DOI
  83. [85]Men Y Fan Y Shen Y Lu L Kallen AN The steroidogenic acute regulatory protein (StAR) is regulated by the H19/let-7 Axis Endocrinology 2017 158 402 409 27813675 PMC5413078
  84. [86]Geng XJ Zhao DM Mao GH Tan L MicroRNA-150 regulates steroidogenesis of mouse testicular Leydig cells by targeting STAR Reproduction 2017 154 129 10.1530/REP-17-0234 28611112 · DOI
  85. [87]Dai A Sun H Fang T Zhang Q Wu S Jiang Y Ding L Yan G Hu Y MicroRNA-133b stimulates ovarian estradiol synthesis by targeting Foxl2 FEBS Lett 2013 587 2474 2482 10.1016/j.febslet.2013.06.023 23810756 · DOI
  86. [88]Xu S Linhermelville K Yang BB Wu D Li J Micro-RNA378 (miR-378) regulates ovarian estradiol production by targeting aromatase Endocrinology 2011 152 3941 3951 10.1210/en.2011-1147 21846797 PMC3176644 · DOI
  87. [89]Wang L Cong L Rong L Deng Y Tan Y Chao T Qi H MicroRNA-764-3p regulates 17β-estradiol synthesis of mouse ovarian granulosa cells by targeting steroidogenic factor-1 In Vitro Cell Dev Biol Anim 2016 52 365 373 10.1007/s11626-015-9977-9 26676955 · DOI
  88. [90]Lü M Tian H Cao Y He X Chen L Song X Ping P Huang H Sun F Downregulation of miR-320a/383-sponge-like long non-coding RNA NLC1-C (narcolepsy candidate-region 1 genes) is associated with male infertility and promotes testicular embryonal carcinoma cell proliferation Cell Death Dis 2015 6 e1960 10.1038/cddis.2015.267 26539909 PMC4670917 · DOI
  89. [91]Sirotkin AV Kisová G Brenaut P Ovcharenko D Grossmann R Mlyncek M Involvement of microRNA Mir15a in control of human ovarian granulosa cell proliferation, apoptosis, steroidogenesis, and response to FSH Microrna 2014 3 29 10.2174/2211536603666140227232824 25069510 · DOI
  90. [92]Amsterdam A, Kerental I, Aharoni D, Dantes A, Land-Bracha A, Rimon, Sasson R, Hirsh L. Steroidogenesis and apoptosis in the mammalian ovary. Steroids. 2003;68(10):861-7. 14667978
  91. [93]Zhang J, Liu Y, Yao W, Li Q, Liu HL, Pan Z. Initiation of follicular atresia: gene networks during early atresia in pig ovaries. Reproduction. 2018. 10.1530/REP-18-0058. 29743261 · DOI
  92. [94]Ji DLY Kim V Muth DC Witwer KW Validated MicroRNA target databases: An evaluation Drug Dev Res 2015 76 389 396 10.1002/ddr.21278 26286669 PMC4777876 · DOI
  93. [95]Tripurani SK Xiao C Salem M Yao J Cloning and analysis of fetal ovary microRNAs in cattle Anim Reprod Sci 2010 120 16 22 10.1016/j.anireprosci.2010.03.001 20347535 · DOI
  94. [96]Torley KJ da Silveira JC Smith P Anthony RV Veeramachaneni DNR Winger QA Bouma GJ Expression of miRNAs in ovine fetal gonads: potential role in gonadal differentiation Reprod Biol Endocrinol 2011 9 2 10.1186/1477-7827-9-2 21223560 PMC3027096 · DOI
  95. [97]Ahn HW Morin RD Zhao H Harris RA Coarfa C Chen Z-J Milosavljevic A Marra MA Rajkovic A MicroRNA transcriptome in the newborn mouse ovaries determined by massive parallel sequencing Mol Hum Reprod 2010 16 463 471 10.1093/molehr/gaq017 20215419 PMC2882868 · DOI
  96. [98]Ro S Song R Park C Zheng H Sanders KM Yan W Cloning and expression profiling of small RNAs expressed in the mouse ovary RNA 2007 13 2366 2380 10.1261/rna.754207 17951331 PMC2080611 · DOI
  97. [99]Mishima T Takizawa T Luo S-S Ishibashi O Kawahigashi Y Mizuguchi Y Ishikawa T Mori M Kanda T Goto T Takizawa T MicroRNA (miRNA) cloning analysis reveals sex differences in miRNA expression profiles between adult mouse testis and ovary Reproduction 2008 136 811 822 10.1530/REP-08-0349 18772262 · DOI
  98. [100]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 10.1186/1471-2164-10-443 19765282 PMC2762473 · DOI
  99. [101]Huang J Ju Z Li Q Hou Q Wang C Li J Li R Wang L Sun T Hang S Solexa sequencing of novel and differentially expressed microRNAs in testicular and ovarian tissues in Holstein cattle Int J Biol Sci 2011 7 1016 1026 10.7150/ijbs.7.1016 21912509 PMC3164151 · DOI
  100. [102]Li M Liu Y Wang T Guan J Luo Z Chen H Wang X Chen L Ma J Mu Z Repertoire of porcine microRNAs in adult ovary and testis by deep sequencing Int J Biol Sci 2011 7 1045 1055 10.7150/ijbs.7.1045 21927574 PMC3174389 · DOI
  101. [103]Yang H Lin S Lei X Yuan C Tian Z Yu Y Zhao Z Chen J Identification and profiling of microRNAs from ovary of estrous Kazakh sheep induced by nutritional status in the anestrous season Anim Reprod Sci 2016 175 18 10.1016/j.anireprosci.2016.10.004 27773477 · DOI
  102. [104]Xu B Zhang YW Zheng SX Tong XH Liu YS Expression profile of MicroRNAs and their targeted pathways in human ovaries detected by next-generation small RNA sequencing DNA Cell Biol 2016 35 226 10.1089/dna.2015.3176 26828676 · DOI
  103. [105]Furlong HC Stämpfli MR Gannon AM Foster WG Identification of microRNAs as potential markers of ovarian toxicity J Appl Toxicol 2018 38 5 744 752 10.1002/jat.3583 29377183 PMC5901046 · DOI
  104. [106]Ling Y-H Ren C-H Guo X-F Xu L-N Huang Y-F Luo J-C Zhang Y-H Zhang X-R Zhang Z-J Identification and characterization of microRNAs in the ovaries of multiple and uniparous goats (Capra hircus) during follicular phase BMC Genomics 2014 15 339 10.1186/1471-2164-15-339 24886377 PMC4035069 · DOI
  105. [107]Miles JR McDaneld TG Wiedmann RT Cushman RA Echternkamp SE Vallet JL Smith TPL 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 2012 130 16 26 10.1016/j.anireprosci.2011.12.021 22269106 · DOI
  106. [108]Xu Y-W Wang B Ding C-H Li T Gu F Zhou C Differentially expressed micoRNAs in human oocytes J Assist Reprod Genet 2011 28 559 566 10.1007/s10815-011-9590-0 21647640 PMC3158253 · DOI
  107. [109]Xu B Zhang Y-W Tong X-H Liu Y-S 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 10.1016/j.mce.2015.01.030 25622783 · DOI
  108. [110]Xie S Batnasan E Zhang Q Li Y MicroRNA expression is altered in granulosa cells of ovarian Hyperresponders Reprod Sci 2016 23 1001 1010 10.1177/1933719115625849 26763554 · DOI
  109. [111]Hong L Peng S Li Y Fang Y Wang Q Klausen C Yin C Wang S Pck L Yang X MiR-106a increases granulosa cell viability and is down-regulated in women with diminished ovarian reserve J Clin Endocrinol Metab 2018 103 6 2157 2166 10.1210/jc.2017-02344 29590425 · DOI
  110. [112]Fiedler SD Carletti MZ Hong X Christenson LK Hormonal regulation of MicroRNA expression in periovulatory mouse mural granulosa cells Biol Reprod 2008 79 1030 1037 10.1095/biolreprod.108.069690 18716288 PMC2780477 · DOI
  111. [113]Sang Q Yao Z Wang H Feng R Wang H Zhao X Xing Q Jin L He L Wu L Wang L Identification of microRNAs in human follicular fluid: characterization of microRNAs that govern steroidogenesis in vitro and are associated with polycystic ovary syndrome in vivo J Clin Endocrinol Metab 2013 98 3068 3079 10.1210/jc.2013-1715 23666971 · DOI
  112. [114]Sørensen AE, Wissing ML, Englund AL, Dalgaard LT. MicroRNA species in follicular fluid associating with polycystic ovary syndrome and related intermediary phenotypes. J Clin Endocrinol Metab. 2016. 10.1210/jc.2015-3588. PMC4880172 26771704 · DOI
  113. [115]Santonocito M Vento M Guglielmino MR Battaglia R Wahlgren J Ragusa M Barbagallo D Borzì P Rizzari S Maugeri M Molecular characterization ofexosomes and their microRNA cargo in human follicular fluid: bioinformatic analysis reveals that exosomal microRNAs control pathways involved in follicular maturation Fertil Steril 2014 102 1751 1761.e1751 10.1016/j.fertnstert.2014.08.005 25241362 · DOI
  114. [116]Andrade GM, Meirelles FV, Perecin F, Silveira JD. Cellular and extracellular vesicular origins of miRNAs within the bovine ovarian follicle. Reprod Domest Anim. 2017. 10.1111/rda.13021. 28691325 · DOI
  115. [117]Jiang L Huang J Chen Y Yang Y Li R Li Y Chen X Yang D Identification of several circulating microRNAs from a genome-wide circulating microRNA expression profile as potential biomarkers for impaired glucose metabolism in polycystic ovarian syndrome Endocrine 2016 53 280 290 10.1007/s12020-016-0878-9 26860517 · DOI
  116. [118]Peng JY An XP Fang F Gao KX Xin HY Han P Bao LJ Ma HD Cao BY MicroRNA-10b suppresses goat granulosa cell proliferation by targeting brain-derived neurotropic factor Domest Anim Endocrinol 2016 54 60 10.1016/j.domaniend.2015.09.005 26513157 · DOI
  117. [119]Carletti MZ Fiedler SD Christenson LK MicroRNA 21 blocks apoptosis in mouse Periovulatory granulosa cells Biol Reprod 2010 83 286 295 10.1095/biolreprod.109.081448 20357270 PMC2907287 · DOI
  118. [120]Fang X Hu L Zhang Y Xiao X Xiao J miR-22 inhibits mouse ovarian granulosa cell apoptosis by targeting SIRT1 Biology Open 2016 5 367 371 10.1242/bio.016907 26912776 PMC4810753 · DOI
  119. [121]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 10.1530/REP-11-0371 22653319 · DOI
  120. [122]Liu J Tu F Yao W Li X Xie Z Liu H Li Q Pan Z Conserved miR-26b enhances ovarian granulosa cell apoptosis through HAS2-HA-CD44-Caspase-3 pathway by targeting HAS2 Sci Rep 2016 6 21197 10.1038/srep21197 26887530 PMC4758074 · DOI
  121. [123]Tu F Pan ZX Yao Y Liu HL Liu SR Xie Z Li QF miR-34a targets the inhibin beta B gene, promoting granulosa cell apoptosis in the porcine ovary Genet Mol Res 2014 13 2504 2512 10.4238/2014.January.14.6 24446339 · DOI
  122. [124]Yuan XU Zhang AL Xiao G Zhe Z Chen ZM Hao Z Jia-Qi LI p53 and NFκB regulate microRNA-34c expression in porcine ovarian granulosa cells J Integr Agric 2016 15 1816 1824 10.1016/S2095-3119(15)61178-9 · DOI
  123. [125]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 100 729 738 10.1210/jc.2014-3827 PMC4422895 25695884 · DOI
  124. [126]Wang C Li D Zhang S Xing Y Gao Y Wu J MicroRNA-125a-5p induces mouse granulosa cell apoptosis by targeting signal transducer and activator of transcription 3 Menopause 2016 23 100 10.1097/GME.0000000000000507 26154273 · DOI
  125. [127]Du X Li Q Pan Z Li Q Androgen receptor and miRNA-126* axis controls follicle-stimulating hormone receptor expression in porcine ovarian granulosa cells Reproduction 2016 152 161 10.1530/REP-15-0517 27222597 · DOI
  126. [128]Chen X Xie M Liu D Shi K Downregulation of microRNA-146a inhibits ovarian granulosa cell apoptosis by simultaneously targeting interleukin-1 receptor-associated kinase and tumor necrosis factor receptor-associated factor 6 Mol Med Rep 2015 12 5155 10.3892/mmr.2015.4036 26151128 · DOI
  127. [129]Yin M, Wang X, Yao G, Lu M, Liang M, Sun Y, Sun F. Transactivation of miR-320 by miR-383 regulates granulosa cell functions by targeting E2F1 and SF-1 proteins. J Biol Chem. 2014;289:18239-57. PMC4140302 24828505
  128. [130]Toms D Xu S Bo P Wu D Li J Progesterone receptor expression in granulosa cells is suppressed by microRNA-378-3p Mol Cell Endocrinol 2015 399 95 102 10.1016/j.mce.2014.07.022 25150622 · DOI
  129. [131]Yin M Lü M Yao G Tian H Lian J Liu L Liang M Wang Y Sun F Transactivation of microRNA-383 by steroidogenic factor-1 promotes estradiol release from mouse ovarian granulosa cells by targeting RBMS1 Mol Endocrinol 2012 26 1129 10.1210/me.2011-1341 22593182 PMC5417001 · DOI

Authors
Zhang, J., Xu, Y., Liu, H., & Pan, Z.
Affiliations
Nanjing Agricultural University (CN)
Corresponding author
Pan, Zengxiang
ORCID
Venue
Reproductive Biology and Endocrinology
Publisher
Springer Science and Business Media LLC
Published
2019-01-10
Volume
17
Issue
1
Pages
9-9
ISSN
1477-7827 (ISSN-L)
DOI
10.1186/s12958-018-0450-y
PMC
PMC6329178
OpenAlex
W2912444667
Cited by
228
References
129
Citations by year
2026: 14 · 2025: 32 · 2024: 41 · 2023: 40 · 2022: 39 · 2021: 26 · 2020: 25 · 2019: 11
FWCI
4.33
Type
journal article
Language
en
Open access
Licence
Locations
  • Reproductive Biology and Endocrinology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Natural Science Foundation of China (31672421, 20160721)
  • Natural Science Foundation of Jiangsu Province (BK20161453)
  • Fundamental Research Funds for the Central Universities (Y0201600160)
Topics
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
  • Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
Keywords
microRNA, follicular atresia, granulosa cell apoptosis, ovarian development, microRNA expression profiles, let-7 family, miR-183/96/182 cluster, miR-17-92 cluster, miRNA network, infertility, ovarian dysfunction
MeSH terms
Animals, Female, Follicular Atresia, Ovarian Follicle, Granulosa Cells, Humans, Infertility, Female, Apoptosis, Gene Expression Profiling, MicroRNAs

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review