miRNA调控哺乳动物卵泡发育和卵母细胞成熟的研究进展

doi:10.11843/j.issn.0366-6964.2019.11.001

摘要/Abstract

摘要： 雌性哺乳动物的卵泡发育和卵母细胞成熟受繁殖关键基因的时空调控，miRNA作为一类小的非编码RNA，调节大部分此类基因的表达。近十几年来，研究者通过高通量测序、敲除miRNA生成过程中的关键基因以及过表达或抑制miRNA表达等方法找到了大量与哺乳动物卵泡发育和卵母细胞生长相关的miRNAs。通过研究这些miRNAs及其靶基因的互作关系，最终确定其在哺乳动物卵泡发育和卵母细胞成熟中的作用。本文综述了雌性哺乳动物主要生殖细胞及细胞外miRNAs在卵泡发育和卵母细胞成熟过程中的表达及潜在作用，以期为深入探究雌性哺乳动物繁殖调控机制提供参考。

Abstract: The regulation of female mammalian follicular development and oocyte maturation involves the spatiotemporal regulation of those genes that play key roles in reproduction. miRNAs, as a class of small non-coding RNAs, regulate the expression of most of these genes. Over the last decade, a large number of miRNAs involved in mammalian follicular development and oocyte growth were found through high-throughput sequencing, knockout of key genes involved in miRNA generation, and functional inhibition or overexpression of miRNAs. The function of these miRNAs in mammalian follicular development and oocyte maturation were ultimately determined by studying the interaction with their target genes. The present review focuses on the expression and potential function of major miRNAs during follicular development and oocyte maturation in reproductive cells or extracellular. These results can provide a reference for further exploring the regulation mechanism of mammalian reproduction.

中图分类号:

S814.1

贺小云, 刘秋月, 储明星. miRNA调控哺乳动物卵泡发育和卵母细胞成熟的研究进展[J]. 畜牧兽医学报, 2019, 50(11): 2175-2185.

HE Xiaoyun, LIU Qiuyue, CHU Mingxing. Advances in miRNA Regulating Mammalian Follicular Development and Oocyte Maturation[J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2019, 50(11): 2175-2185.

参考文献 111

[1]	BARANYAI T,HERCZEG K,ONÓDI Z,et al.Isolation of exosomes from blood plasma:qualitative and quantitative comparison of ultracentrifugation and size exclusion chromatography methods[J].PLoS One,2015,10(12):e0145686.
[2]	BETTEGOWDA A,SMITH G W.Mechanisms of maternal mRNA regulation:implications for mammalian early embryonic development[J].Front Biosci,2007,12:3713-3726.
[3]	GREGORY R I,YAN K P,AMUTHAN G,et al.The microprocessor complex mediates the genesis of microRNAs[J].Nature,2004, 432(7014):235-240.
[4]	HUTVÁGNER G,ZAMORE P D.A microRNA in a multiple-turnover RNAi enzyme complex[J].Science, 2002,297(5589):2056-2060.
[5]	YI R,QIN Y,MACARA I G,et al.Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs[J].Genes Dev,2003,17(24):3011-3016.
[6]	TESFAYE D,GEBREMEDHN S,SALILEW-WONDIM D,et al.microRNAs:tiny molecules with a significant role in mammalian follicular and oocyte development[J].Reproduction,2018,155(3):R121-R135.
[7]	BERNSTEIN E,KIM S Y,CARMELL M A,et al.Dicer is essential for mouse development[J].Nat Genet,2003,35(3):215-217.
[8]	HONG X M,LUENSE L J,MCGINNIS L K,et al.Dicer1 is essential for female fertility and normal development of the female reproductive system[J].Endocrinology,2008,149(12):6207-6212.
[9]	NAGARAJA A K,ANDREU-VIEYRA C,FRANCO H L,et al.Deletion of dicer in somatic cells of the female reproductive tract causes sterility[J].Mol Endocrinol,2008,22(10):2336-2352.
[10]	LUENSE L J,CARLETTI M Z,CHRISTENSON L K.Role of Dicer in female fertility[J].Trends Endocrinol Metab,2009, 20(6):265-272.
[11]	LEI L,JIN S Y,GONZALEZ G,et al.The regulatory role of Dicer in folliculogenesis in mice[J].Mol Cell Endocrinol,2010, 315(1-2):63-73.
[12]	SÁNCHEZ F,SMITZ J.Molecular control of oogenesis[J].Biochim Biophys Acta,2012,1822(12):1896-1912.
[13]	IMBAR T,EISENBERG I.Regulatory role of microRNAs in ovarian function[J].Fertil Steril,2014,101(6):1524-1530.
[14]	LIANG Y,RIDZON D,WONG L,et al.Characterization of microRNA expression profiles in normal human tissues[J].BMC Genomics,2007,8:166.
[15]	AHN H W,MORIN R D,ZHAO H,et al.microRNA transcriptome in the newborn mouse ovaries determined by massive parallel sequencing[J].Mol Hum Reprod,2010,16(7):463-471.
[16]	HOSSAIN M,GHANEM N,HOELKER M,et al.Identification and characterization of miRNAs expressed in the bovine ovary[J]. BMC Genomics,2009,10:443.
[17]	LING Y H,REN C H,GUO X F,et al.Identification and characterization of microRNAs in the ovaries of multiple and uniparous goats (Capra hircus) during follicular phase[J].BMC Genomics,2014,15:339.
[18]	DI R,HE J N,SONG S H,et al.Characterization and comparative profiling of ovarian microRNAs during ovine anestrus and the breeding season[J].BMC Genomics,2014,15:899.
[19]	LI M Z,LIU Y K,WANG T,et al.Repertoire of porcine microRNAs in adult ovary and testis by deep sequencing[J].Int J Biol Sci,2011,7(7):1045-1055.
[20]	徐源,孙铁成,张爱玲,等.卵巢miRNA研究进展[J].畜牧兽医学报,2014,45(4):509-516.
	XU Y,SUN T C,ZHANG A L,et al.Progress on the research of ovarian miRNA[J].Acta Veterinaria et Zootechnica Sinica,2014, 45(4):509-516.(in Chinese)
[21]	PAN B,LI J L.microRNA-21 up-regulates metalloprotease by down-regulating TIMP3 during cumulus cell-oocyte complex in vitro maturation[J].Mol Cell Endocrinol,2018,477:29-38.
[22]	XU L,SUN H X,ZHANG M,et al.microRNA-145 protects follicular granulosa cells against oxidative stress-induced apoptosis by targeting Krüppel-like factor 4[J].Mol Cell Endocrinol,2017,452:138-147.
[23]	SOHEL M H,AKYUZ B,KONCA Y,et al.Oxidative stress modulates the expression of apoptosis-associated microRNAs in bovine granulosa cells in vitro[J].Cell Tissue Res,2019,376(2):295-308.
[24]	ELIAS K M,FENDLER W,STAWISKI K,et al.Diagnostic potential for a serum miRNA neural network for detection of ovarian cancer[J].eLife,2017,6:e28932
[25]	GOV E,KORI M,ARGA K Y.Multiomics analysis of tumor microenvironment reveals Gata2 and miRNA-124-3p as potential novel biomarkers in ovarian Cancer[J].OMICS,2017,21(10):603-615.
[26]	XU B,HUA J,ZHANG Y W,et al.Proliferating cell nuclear antigen (PCNA) regulates primordial follicle assembly by promoting apoptosis of oocytes in fetal and neonatal mouse ovaries[J].PLoS One,2011,6(1):e16046.
[27]	ZHANG H,JIANG X H,ZHANG Y W,et al.microRNA 376a regulates follicle assembly by targeting Pcna in fetal and neonatal mouse ovaries[J].Reproduction,2014,148(1):43-54.
[28]	YANG S H,WANG S,LUO A Y,et al.Expression patterns and regulatory functions of microRNAs during the initiation of primordial follicle development in the neonatal mouse ovary[J].Biol Reprod,2013,89(5):126.
[29]	ZHANG X D,ZHANG Y H,LING Y H,et al.Characterization and differential expression of microRNAs in the ovaries of pregnant and non-pregnant goats (Capra hircus)[J].BMC Genomics,2013,14:157.
[30]	SALEM M,O'BRIEN J A,BERNAUDO S,et al.miR-590-3p promotes ovarian cancer growth and metastasis via a novel FOXA2-versican pathway[J].Cancer Res,2018,78(15):4175-4190.
[31]	SONTAKKE S D,MOHAMMED B T,MCNEILLY A S,et al.Characterization of microRNAs differentially expressed during bovine follicle development[J].Reproduction,2014,148(3):271-283.
[32]	SALILEW-WONDIM D,AHMAD I,GEBREMEDHN S,et al.The expression pattern of microRNAs in granulosa cells of subordinate and dominant follicles during the early luteal phase of the bovine estrous cycle[J].PLoS One,2014,9(9):e106795.
[33]	HATZIRODOS N,IRVING-RODGERS H F,HUMMITZSCH K,et al.Transcriptome profiling of granulosa cells of bovine ovarian follicles during growth from small to large antral sizes[J].BMC Genomics,2014,15:24.
[34]	GEBREMEDHN S,SALILEW-WONDIM D,HOELKER M,et al.microRNA-183-96-182 cluster regulates bovine granulosa cell proliferation and cell cycle transition by coordinately targeting FOXO1[J].Biol Reprod,2016,94(6):127.
[35]	PIERCE M L,WESTON M D,FRITZSCH B,et al.microRNA-183 family conservation and ciliated neurosensory organ expression[J]. Evol Dev,2008,10(1):106-113.
[36]	CHEN M L,LIN K,LIN S K.NLRP3 inflammasome signaling as an early molecular response is negatively controlled by miR-186 in CFA-induced prosopalgia mice[J].Braz J Med Biol Res,2018,51(9):e7602.
[37]	AN X P,SONG Y X,HOU J X,et al.Identification and profiling of microRNAs in the ovaries of polytocous and monotocous goats during estrus[J].Theriogenology,2016,85(4):769-780.
[38]	HUANG L,YIN Z J,FENG Y F,et al.Identification and differential expression of microRNAs in the ovaries of pigs (Sus scrofa) with high and low litter sizes[J].Anim Genet,2016,47(5):543-551.
[39]	ZI X D,LU J Y,MA L.Identification and comparative analysis of the ovarian microRNAs of prolific and non-prolific goats during the follicular phase using high-throughput sequencing[J].Sci Rep,2017,7:1921.
[40]	LI Q Q,DU X,PAN Z X,et al.The transcription factor SMAD4 and miR-10b contribute to E2 release and cell apoptosis in ovarian granulosa cells by targeting CYP19A1[J].Mol Cell Endocrinol,2018,476:84-95.
[41]	TAO J,CONG H B,WANG H Y,et al.miR-30a-5p inhibits osteosarcoma cell proliferation and migration by targeting FOXD1[J]. Biochem Biophys Res Commun,2018,503(2):1092-1097.
[42]	HATZIRODOS N,HUMMITZSCH K,IRVING-RODGERS H F,et al.Transcriptome profiling of granulosa cells from bovine ovarian follicles during atresia[J].BMC Genomics,2014,15:40.
[43]	LI P F,MENG J Z,LIU W Z,et al.Transcriptome analysis of bovine ovarian follicles at predeviation and onset of deviation stages of a follicular wave[J].Int J Genomics,2016,2016:3472748.
[44]	WU S G,SUN H X,ZHANG Q,et al.microRNA-132 promotes estradiol synthesis in ovarian granulosa cells via translational repression of Nurr1[J].Reprod Biol Endocrinol,2015,13:94.
[45]	NIE M Y,YU S,PENG S,et al.miR-23a and miR-27a promote human granulosa cell apoptosis by targeting SMAD5[J].Biol Reprod,2015,93(4):98.
[46]	ZHANG L,ZHANG X X,ZHANG X J,et al.miRNA-143 mediates the proliferative signaling pathway of FSH and regulates estradiol production[J].J Endocrinol,2017,234(1):1-14.
[47]	WANG L L,LI C,LI R,et al.microRNA-764-3p regulates 17β-estradiol synthesis of mouse ovarian granulosa cells by targeting steroidogenic factor-1[J].In Vitro Cell Dev Biol Anim,2016,52(3):365-373.
[48]	ZHOU J W,LEI B,LI H N,et al.microRNA-144 is regulated by CP2 and decreases COX-2 expression and PGE2 production in mouse ovarian granulosa cells[J].Cell Death Dis,2017,8(2):e2597.
[49]	YU C L,LI M L,WANG Y,et al.miR-375 mediates CRH signaling pathway in inhibiting E2 synthesis in porcine ovary[J]. Reproduction,2017,153(1):63-73.
[50]	TOMS D,XU S Y,PAN B,et al.Progesterone receptor expression in granulosa cells is suppressed by microRNA-378-3p[J].Mol Cell Endocrinol,2015,399:95-102.
[51]	SIROTKIN A V,KISOVÁ 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.
[52]	DAI A Y,SUN H X,FANG T,et al.microRNA-133b stimulates ovarian estradiol synthesis by targeting Foxl2[J].FEBS Lett,2013,587(15):2474-2482.
[53]	HU Z G,SHEN W J,KRAEMER F B,et al.micro-RNAs 125a and 455 repress lipoprotein-supported steroidogenesis by targeting scavenger receptor class B type I in steroidogenic cells[J].Mol Cell Biol,2012,32(24):5035-5045.
[54]	LIU J Y,LI X Y,YAO Y,et al.miR-1275 controls granulosa cell apoptosis and estradiol synthesis by impairing LRH-1/CYP19A1 axis[J].Biochim Biophys Acta,2018,1861(3):246-257.
[55]	ZHANG J F,JI X W,ZHOU D D,et al.miR-143 is critical for the formation of primordial follicles in mice[J].Front Biosci,2013,18:588-597.
[56]	LI X D,JIN Y H,MU Z K,et al.microRNA-146a-5p enhances cisplatin-induced apoptosis in ovarian cancer cells by targeting multiple anti-apoptotic genes[J].Int J Oncol,2017,51(1):327-335.
[57]	LIU J Y,TU F,YAO W,et al.Conserved miR-26b enhances ovarian granulosa cell apoptosis through HAS2-HA-CD44-Caspase-3 pathway by targeting HAS2[J].Sci Rep,2016,6:21197.
[58]	WRIGHT E C,HALE B J,YANG C X,et al.microRNA-21 and PDCD4 expression during in vitro oocyte maturation in pigs[J].Reprod Biol Endocrinol,2016,14:21.
[59]	LIANG H H,PAN Z W,ZHAO X G,et al.lncRNA PFL contributes to cardiac fibrosis by acting as a competing endogenous RNA of let-7d[J].Theranostics,2018,8(4):1180-1194.
[60]	CHEN H,LIU C,JIANG H,et al.Regulatory role of miRNA-375 in expression of BMP15/GDF9 receptors and its effect on proliferation and apoptosis of bovine cumulus cells[J].Cell Physiol Biochem,2017,41(2):439-450.
[61]	CHEN X,XIE M X,LIU D,et al.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[J].Mol Med Rep, 2015,12(4):5155-5162.
[62]	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]. Genet Mol Res,2014,13(2):2504-2512.
[63]	TU J J,YANG Y Z,HOI-HUNG A C,et al.Conserved miR-10 family represses proliferation and induces apoptosis in ovarian granulosa cells[J].Sci Rep,2017,7:41304.
[64]	GENG Y,SUI C,XUN Y,et al.miRNA-99a can regulate proliferation and apoptosis of human granulosa cells via targeting IGF-1R in polycystic ovary syndrome[J].J Assist Reprod Genet,2019,36(2):211-221.
[65]	YAO Y L,NIU J Q,SIZHU S L,et al.microRNA-125b regulates apoptosis by targeting bone morphogenetic protein receptor 1B in yak granulosa cells[J].DNA Cell Biol,2018,37(11):878-887.
[66]	ANDREAS E,HOELKER M,NEUHOFF C,et al.microRNA 17-92 cluster regulates proliferation and differentiation of bovine granulosa cells by targeting PTEN and BMPR2 genes[J].Cell Tissue Res,2016,366(1):219-230.
[67]	PENG J Y,AN X P,FANG F,et al.microRNA-10b suppresses goat granulosa cell proliferation by targeting brain-derived neurotropic factor[J].Domest Anim Endocrinol,2015,54:60-67.
[68]	ZHANG Q,SUN H X,JIANG Y,et al.microRNA-181a suppresses mouse granulosa cell proliferation by targeting activin receptor IIA[J].PLoS One,2013,8(3):e59667.
[69]	CAI G Q,MA X D,CHEN B L,et al.microRNA-145 negatively regulates cell proliferation through targeting IRS1 in isolated ovarian granulosa cells from patients with polycystic ovary syndrome[J].Reprod Sci,2017,24(6):902-910.
[70]	YAO G D,YIN M M,LIAN J,et al.microRNA-224 is involved in transforming growth factor-β-mediated mouse granulosa cell proliferation and granulosa cell function by targeting Smad4[J].Mol Endocrinol,2010,24(3):540-551.
[71]	WANG Y,LEE A T C,MA J Z I,et al.Profiling microRNA expression in hepatocellular carcinoma reveals microRNA-224 up-regulation and apoptosis inhibitor-5 as a microRNA-224-specific target[J].J Biol Chem,2008,283(19):13205-13215.
[72]	YUAN X L,DENG X,ZHOU X F,et al.miR-126-3p promotes the cell proliferation and inhibits the cell apoptosis by targeting TSC1 in the porcine granulosa cells[J].In vitro Cell Dev Biol Anim,2018,54(10):715-724.
[73]	PANDE H O,TESFAYE D,HOELKER M,et al.microRNA-424/503 cluster members regulate bovine granulosa cell proliferation and cell cycle progression by targeting SMAD7 gene through activin signalling pathway[J].J Ovarian Res,2019,11:34.
[74]	LI X F,WANG H D,SHENG Y,et al.microRNA-224 delays oocyte maturation through targeting Ptx3 in cumulus cells[J].Mech Dev,2017,143:20-25.
[75]	PAN B,TOMS D,SHEN W,et al.microRNA-378 regulates oocyte maturation via the suppression of aromatase in porcine cumulus cells[J]. Am J Physiol Endocrinol Metab,2015,308(6):E525-E534.
[76]	XU S Y,LINHER-MELVILLE K,YANG B B,et al.microRNA-378(miR-378) regulates ovarian estradiol production by targeting aromatase[J].Endocrinology,2011,152(10):3941-3951.
[77]	SINHA P B,TESFAYE D,RINGS F,et al.micro-RNA-130b is involved in bovine granulosa and cumulus cells function,oocyte maturation and blastocyst formation[J].J Ovarian Res,2017,10(1):37.
[78]	TRIPURANI S K,WEE G,LEE K B,et al.micro-RNA-212 post-transcriptionally regulates oocyte-specific basic-helix-loop-helix transcription factor,factor in the germline alpha (FIGLA),during bovine early embryogenesis[J].PLoS One,2013,8(9):e76114.
[79]	FENG R Z,SANG Q,ZHU Y,et al.miRNA-320 in the human follicular fluid is associated with embryo quality in vivo and affects mouse embryonic development in vitro[J].Sci Rep,2015,5:8689.
[80]	PANG R T K,LIU W M,LEUNG C O N,et al.miR-135A regulates preimplantation embryo development through down-regulation of E3 ubiquitin ligase seven in absentia homolog 1A (SIAH1A) expression[J].PLoS One,2011,6(11):e27878.
[81]	TRIPURANI S K,LEE K B,WEE G,et al.micro-RNA-196a regulates bovine newborn ovary homeobox gene (NOBOX) expression during early embryogenesis[J].BMC Dev Biol,2011,11:25.
[82]	MILES J R,MCDANELD T G,WIEDMANN R T,et al.microRNA expression profile in bovine cumulus-oocyte complexes:possible role of let-7 and miR-106a in the development of bovine oocytes[J].Anim Reprod Sci,2012,130(1-2):16-26.
[83]	CAO R,WU W J,ZHOU X L,et al.Expression and preliminary functional profiling of the let-7 family during porcine ovary follicle atresia[J].Mol Cells,2015,38(4):304-311.
[84]	CUI L,FANG L,MAO X D,et al.GDNF-induced down-regulation of miR-145-5p enhances human oocyte maturation and cumulus cell viability[J]. J Clin Endocrinol Metab,2018,103(7):2510-2521.
[85]	SOHEL M H,HOELKER M,NOFERESTI S S,et al.Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid:implications for bovine oocyte developmental competence[J].PLoS One,2013,8(11):e78505.
[86]	NAVAKANITWORAKUL R,HUNG W T,GUNEWARDENA S,et al.Characterization and small RNA content of extracellular vesicles in follicular fluid of developing bovine antral follicles[J].Sci Rep,2016,6:25486.
[87]	DA SILVEIRA J C,CARNEVALE E M,WINGER Q A,et al.Regulation of ACVR1 and ID2 by cell-secreted exosomes during follicle maturation in the mare[J].Reprod Biol Endocrinol,2014,12:44.
[88]	SCALICI E,TRAVER S,MULLET T,et al.Circulating microRNAs in follicular fluid,powerful tools to explore in vitro fertilization process[J].Sci Rep,2016,6:24976.
[89]	SØRENSEN A E,WISSING M L,ENGLUND A L M,et al.microRNA species in follicular fluid associating with polycystic ovary syndrome and related intermediary phenotypes[J].J Clin Endocrinol Metab,2016,101(4):1579-1589.
[90]	WILCZYNSKA A,GIT A,ARGASINSKA J,et al.CPEB and miR-15/16 co-regulate translation of cyclin E1 mRNA during Xenopus oocyte maturation[J].PLoS One,2016,11(2):e0146792.
[91]	LIU J Y,YAO W,YAO Y,et al.miR-92a inhibits porcine ovarian granulosa cell apoptosis by targeting Smad7 gene[J].FEBS Lett,2014,588(23):4497-4503.
[92]	XIONG F,HU L Q,ZHANG Y,et al.miR-22 inhibits mouse ovarian granulosa cell apoptosis by targeting SIRT1[J].Biol Open, 2016, 5(3):367-371.
[93]	SIROTKIN A V,OVCHARENKO D,GROSSMANN R,et al.Identification of microRNAs controlling human ovarian cell steroidogenesis via a genome-scale screen[J].J Cell Physiol,2010,219(2):415-420.
[94]	YIN M M,WANG X R,YAO G D,et al.Transactivation of microRNA-320 by microRNA-383 regulates granulosa cell functions by targeting E2F1 and SF-1 proteins[J].J Biol Chem,2014,289(26):18239-18257.
[95]	DONADEU F X,SONTAKKE S D,IOANNIDIS J.microRNA indicators of follicular steroidogenesis[J].Reprod Fertil Dev,2016, 29(5):906-912.
[96]	NOFERESTI S S,SOHEL M H,HOELKER M,et al.Controlled ovarian hyperstimulation induced changes in the expression of circulatory miRNA in bovine follicular fluid and blood plasma[J].J Ovarian Res,2015,8:81.
[97]	LI L,ZHENG P,DEAN J.Maternal control of early mouse development[J].Development,2010,137(6):859-870.
[98]	BUDNA J,RYBSKA M,CIESIÓLKA S,et al.Expression of genes associated with BMP signaling pathway in porcine oocytes before and after IVM-a microarray approach[J].Reprod Biol Endocrinol,2017,15:43.
[99]	FAIR T,CARTER F,PARK S,et al.Global gene expression analysis during bovine oocyte in vitro maturation[J].Theriogenology, 2007,68 Suppl 1:S91-S97.
[100]	XIONG X R,LAN D L,LI J,et al.Identification of candidate miRNAs and expression profile of yak oocytes before and after in vitro maturation by high-throughput sequencing[J].Reprod Domest Anim,2016,51(6):886-894.
[101]	FREIMER J W,KRISHNAKUMAR R,COOK M S,et al.Expression of alternative Ago2 isoform associated with loss of microRNA-driven translational repression in mouse oocytes[J].Curr Biol,2018,28(2):296-302.
	e3.
[102]	FU Y H,LI J X,TANG Q Z,et al.Integrated analysis of methylome,transcriptome and miRNAome of three pig breeds[J]. Epigenomics, 2018,10(5):597-612.
[103]	XIAO G H,XIA C L,YANG J,et al.miR-133b regulates the expression of the actin protein TAGLN2 during oocyte growth and maturation:a potential target for infertility therapy[J].PLoS One,2014,9(6):e100751.
[104]	BATTAGLIA R,VENTO M E,RAGUSA M,et al.microRNAs are stored in human MII oocyte and their expression profile changes in reproductive aging[J].Biol Reprod,2016,95(6):131.
[105]	MAIA J,CAJA S,STRANO MORAES M C,et al.Exosome-based cell-cell communication in the tumor microenvironment[J]. Front Cell Dev Biol,2018,6:18.
[106]	MELO S A,LUECKE L B,KAHLERT C,et al.Glypican-1 identifies cancer exosomes and detects early pancreatic cancer[J]. Nature, 2015,523(7559):177-182.
[107]	BURNS G W,BROOKS K E,SPENCER T E.Extracellular vesicles originate from the conceptus and uterus during early pregnancy in sheep[J].Biol Reprod,2016,94(3):56.
[108]	DA SILVEIRA J C,ANDRADE G M,DEL COLLADO M,et al.Supplementation with small-extracellular vesicles from ovarian follicular fluid during in vitro production modulates bovine embryo development[J].PLoS One,2017,12(6):e0179451.
[109]	KEERTHIKUMAR S,CHISANGA D,ARIYARATNE D,et al.ExoCarta:a web-based compendium of exosomal cargo[J].J Mol Biol,2016,428(4):688-692.
[110]	HAILAY T,HOELKER M,GEBREMEDHN S,et al.115 Exosome-mediated microRNA expression profile in follicular fluid of metabolically divergent postpartum cows[J].Reprod Fertil Dev,2019,31(1):183-184.
[111]	MATSUNO Y,ONUMA A,FUJIOKA Y A,et al.Effects of exosome-like vesicles on cumulus expansion in pigs in vitro[J].J Reprod Dev,2017,63(1):51-58.