ERM蛋白在哺乳动物卵母细胞成熟和受精中的研究进展

doi:10.11843/j.issn.0366-6964.2023.11.005

Abstract

Abstract: Fertilization is the basic characteristic of sexual reproduction and forming the foundation of individual development. The maturation of oocytes is a prerequisite for successful fertilization and embryonic development. Oocytes are carefully regulated by a series of molecular mechanisms during maturation and fertilization. The ezrin-radixin-moesin (ERM) proteins act as a bridge between the oocyte membrane and the cytoskeleton, which directly or indirectly mediate many of the signaling pathways found in recent years that regulated mammalian oocyte maturation and fertilization. Therefore, ERM proteins have likewise become the focus of research on such biological events. This paper reviewed the research progress of the ERM protein family in the process of oocyte maturation and fertilization by regulating the formation of microvilli, polar-body extrusion, the exchange of information between oocytes and granulose cells, and sperm-egg fusion. These will provide a theoretical reference for ensuring the success rate of in vitro maturation and in vitro fertilization of mammalian oocytes and improving the reproductive efficiency of female mammals.

Key words: ERM proteins, membrane-cytoskeleton linkage, meiosis, fertilization

CLC Number:

S814

SHAO Jing, ZHANG Ying, TANG Yu, XU Baozeng. Research Progress of ERM Proteins in Mammalian Oocyte Maturation and Fertilization[J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(11): 4477-4487.

References 87

[1]	LI L,ZHENG P,DEAN J.Maternal control of early mouse development[J].Development,2010,137(6):859-870.
[2]	REYES J M,ROSS P J.Cytoplasmic polyadenylation in mammalian oocyte maturation[J].Wiley Interdiscip Rev RNA,2016, 7(1): 71-89.
[3]	LANKES W T,FURTHMAYR H.Moesin:A member of the protein 4.1-talin-ezrin family of proteins[J].Proc Natl Acad Sci U S A,1991, 88(19): 8297-8301.
[4]	SVITKINA T M.Actin cell cortex:Structure and molecular organization[J].Trends Cell Biol,2020,30(7):556-565.
[5]	SENJU Y,TSAI F C.A biophysical perspective of the regulatory mechanisms of ezrin/radixin/moesin proteins[J].Biophys Rev, 2022, 14(1):199-208.
[6]	BENNABI I,TERRET M E,VERLHAC M H.Meiotic spindle assembly and chromosome segregation in oocytes[J].J Cell Biol, 2016, 215(5):611-619.
[7]	GATTI M,BELLI B,DE RUBEIS M,et al.Ultrastructural evaluation of mouse oocytes exposed in vitro to different concentrations of the fungicide mancozeb[J].Biology (Basel),2023,12(5):698.
[8]	VISWANATHA R,BRETSCHER A,GARBETT D.Dynamics of ezrin and EBP50 in regulating microvilli on the apical aspect of epithelial cells[J].Biochem Soc Trans,2014,42(1):189-194.
[9]	PHANG J M,HARROP S J,DUFF A P,et al.Structural characterization suggests models for monomeric and dimeric forms of full-length ezrin[J].Biochem J,2016,473(18):2763-2782.
[10]	SHABARDINA V,KASHIMA Y,SUZUKI Y,et al.Emergence and evolution of ERM proteins and merlin in metazoans[J]. Genome Biol Evol,2020,12(1):3710-3724.
[11]	CLUCAS J,VALDERRAMA F.ERM proteins in cancer progression[J].J Cell Sci,2014,127(Pt 2):267-275.
[12]	VOGL A W,GUTTMAN J A.An introduction to actin and actin-rich structures[J].Anat Rec (Hoboken),2018,301(12):1986-1990.
[13]	DEHAPIOT B,HALET G.Ran GTPase promotes oocyte polarization by regulating ERM (ezrin/radixin/moesin) inactivation[J]. Cell Cycle,2013,12(11):1672-1678.
[14]	ROBERTSON T F,CHENGAPPA P,ATRIA D G,et al.Lymphocyte egress signal sphingosine-1-phosphate promotes ERM-guided,bleb-based migration[J].J Cell Biol,2021,220(6):e202007182.
[15]	LUBART Q,VITET H,DALONNEAU F,et al.Role of phosphorylation in moesin interactions with PIP2-containing biomimetic membranes[J].Biophys J,2018,114(1):98-112.
[16]	BRETSCHER A,EDWARDS K,FEHON R G.ERM proteins and merlin:integrators at the cell cortex[J].Nat Rev Mol Cell Biol,2002,3(8):586-599.
[17]	ALI M,KHRAMUSHIN A,YADAV V K,et al.Elucidation of short linear motif-based interactions of the FERM domains of ezrin,radixin,moesin,and merlin[J].Biochemistry,2023,62(11):1594-1607.
[18]	TAKAI Y,KITANO K,TERAWAKI S I,et al.Structural basis of the cytoplasmic tail of adhesion molecule CD43 and its binding to ERM proteins[J].J Mol Biol,2008,381(3):634-644.
[19]	PANICKER S R,YAGO T,SHAO B J,et al.Neutrophils lacking ERM proteins polarize and crawl directionally but have decreased adhesion strength[J].Blood Adv,2020,4(15):3559-3571.
[20]	SCHÖN M,MEY I,STEINEM C.Influence of cross-linkers on ezrin-bound minimal actin cortices[J].Prog Biophys Mol Biol,2019,144:91-101.
[21]	ROBERTS R E,DEWITT S,HALLETT M B.Membrane tension and the role of ezrin during phagocytosis[J].Adv Exp Med Biol,2020,1246:83-102.
[22]	RAHIMI N,HO R X Y,CHANDLER K B,et al.The cell adhesion molecule TMIGD1 binds to moesin and regulates tubulin acetylation and cell migration[J].J Biomed Sci,2021,28(1):61.
[23]	YANG G,HIRUMA S,KITAMURA A,et al.Molecular basis of functional exchangeability between ezrin and other actin-membrane associated proteins during cytokinesis[J].Exp Cell Res,2021,403(2):112600.
[24]	MURIEL O,TOMAS A,SCOTT C C,et al.Moesin and cortactin control actin-dependent multivesicular endosome biogenesis[J]. Mol Biol Cell, 2016,27(21):3305-3316.
[25]	STEFANI C,GONZALEZ-RODRIGUEZ D,SENJU Y,et al.Ezrin enhances line tension along transcellular tunnel edges via NMIIa driven actomyosin cable formation[J].Nat Commun,2017,8:15839.
[26]	GAETA I M,MEENDERINK L M,POSTEMA M M,et al.Direct visualization of epithelial microvilli biogenesis[J].Curr Biol,2021,31(12):2561-2575. e6.
[27]	ABEYSUNDARA N,SIMMONDS A J,HUGHES S C.Moesin is involved in polarity maintenance and cortical remodeling during asymmetric cell division[J].Mol Biol Cell,2018,29(4):419-434.
[28]	MAO L N,LOU H Y,LOU Y Y,et al.Behaviour of cytoplasmic organelles and cytoskeleton during oocyte maturation[J].Reprod Biomed Online,2014,28(3):284-299.
[29]	HSUEH A J W,KAWAMURA K,CHENG Y,et al.Intraovarian control of early folliculogenesis[J].Endocr Rev,2015,36(1):1-24.
[30]	WANG N,LUO L L,XU J J,et al.Obesity accelerates ovarian follicle development and follicle loss in rats[J].Metabolism, 2014,63(1):94-103.
[31]	ZHANG H,RISAL S,GORRE N,et al.Somatic cells initiate primordial follicle activation and govern the development of dormant oocytes in mice[J].Curr Biol,2014,24(21):2501-2508.
[32]	YAN H,ZHANG J W,WEN J,et al.CDC42 controls the activation of primordial follicles by regulating PI3K signaling in mouse oocytes[J].BMC Biol,2018,16(1):73.
[33]	TEILMANN S C.Differential expression and localisation of connexin-37 and connexin-43 in follicles of different stages in the 4-week-old mouse ovary[J].Mol Cell Endocrinol,2005,234(1-2):27-35.
[34]	DUKIC A R,GERBAUD P,GUIBOURDENCHE J,et al.Ezrin-anchored PKA phosphorylates serine 369 and 373 on connexin 43 to enhance gap junction assembly,communication,and cell fusion[J].Biochem J,2018,475(2):455-476.
[35]	PIDOUX G,GERBAUD P,DOMPIERRE J,et al.A PKA-ezrin-CX43 signaling complex controls gap junction communication and thereby trophoblast cell fusion[J].J Cell Sci,2014,127(Pt 19):4172-4185.
[36]	WINTERHAGER E,KIDDER G M.Gap junction connexins in female reproductive organs:implications for women’s reproductive health[J].Hum Reprod Update,2015,21(3):340-352.
[37]	LI R,ALBERTINI D F.The road to maturation:Somatic cell interaction and self-organization of the mammalian oocyte[J].Nat Rev Mol Cell Biol,2013,14(3):141-152.
[38]	ZHANG Y,WANG Y,FENG X A,et al.Oocyte-derived microvilli control female fertility by optimizing ovarian follicle selection in mice[J].Nat Commun,2021,12(1):2523.
[39]	BRETSCHER A,WEBER K.Purification of microvilli and an analysis of the protein components of the microfilament core bundle[J].Exp Cell Res,1978,116(2):397-407.
[40]	EL-HAYEK S,YANG Q,ABBASSI L,et al.Mammalian oocytes locally remodel follicular architecture to provide the foundation for germline-soma communication[J].Curr Biol,2018,28(7):1124-1131. e3.
[41]	王周吉.猪卵泡形成中后期卵母细胞发育和闭锁变化的超微结构研究[J].东北农学院学报,1987,18(3):279-287.WANG Z J.Ultrastructural studies on the developmental and atretic changes of oocytes in middle and late follicles of sows[J].Journal of Northeast Agricultural University,1987,18(3):279-287.(in Chinese)
[42]	SANTIQUET N W,DEVELLE Y,LAROCHE A,et al.Regulation of gap-junctional communication between cumulus cells during in vitro maturation in swine,a gap-FRAP study[J].Biol Reprod,2012,87(2):46.
[43]	YONEMURA S,TSUKITA S,TSUKITA S.Direct involvement of ezrin/radixin/moesin (ERM)-binding membrane proteins in the organization of microvilli in collaboration with activated ERM proteins[J].J Cell Biol,1999,145(7):1497-1509.
[44]	BRUNET S,VERLHAC M H.Positioning to get out of meiosis:The asymmetry of division[J].Hum Reprod Update,2011, 17(1):68-75.
[45]	CHAIGNE A,VERLHAC M H,TERRET M E.Spindle positioning in mammalian oocytes[J].Exp Cell Res,2012,318(12): 1442-1447.
[46]	YI K X,RUBINSTEIN B,LI R.Symmetry breaking and polarity establishment during mouse oocyte maturation[J].Philos Trans R Soc B Biol Sci,2013,368(1629):20130002.
[47]	SUN S C,GAO W W,XU Y N,et al.Degradation of actin nucleators affects cortical polarity of aged mouse oocytes[J].Fertil Steril,2012,97(4):984-990.
[48]	DENG M Q,KISHIKAWA H,YANAGIMACHI R,et al.Chromatin-mediated cortical granule redistribution is responsible for the formation of the cortical granule-free domain in mouse eggs[J].Dev Biol,2003,257(1):166-176.
[49]	NAMGOONG S,KIM N H.Roles of actin binding proteins in mammalian oocyte maturation and beyond[J].Cell Cycle,2016, 15(14):1830-1843.
[50]	YI K X,UNRUH J R,DENG M Q,et al.Dynamic maintenance of asymmetric meiotic spindle position through Arp2/3-complex-driven cytoplasmic streaming in mouse oocytes[J].Nat Cell Biol,2011,13(10):1252-1258.
[51]	LARSON S M,LEE H J,HUNG P H,et al.Cortical mechanics and meiosis II completion in mammalian oocytes are mediated by myosin-II and Ezrin-Radixin-Moesin (ERM) proteins[J].Mol Biol Cell,2010,21(18):3182-3192.
[52]	PRIMAKOFF P,MYLES D G.Penetration,adhesion,and fusion in mammalian sperm-egg interaction[J].Science,2002, 296(5576): 2183-2185.
[53]	WILSON N F,SNELL W J.Microvilli and cell-cell fusion during fertilization[J].Trends Cell Biol,1998,8(3):93-96.
[54]	TALANSKY B E,MALTER H E,COHEN J.A preferential site for sperm-egg fusion in mammals[J].Mol Reprod Dev,1991,28(2): 183-188.
[55]	GARCÍA-ORTIZ A,SERRADOR J M.ERM proteins at the crossroad of leukocyte polarization,migration and intercellular adhesion[J].Int J Mol Sci,2020,21(4):1502.
[56]	LI Y H,HOU Y,MA W,et al.Localization of CD9 in pig oocytes and its effects on sperm-egg interaction[J].Reproduction, 2004,127(2):151-157.
[57]	JÉGOU A,ZIYYAT A,BARRAUD-LANGE V,et al.CD9 tetraspanin generates fusion competent sites on the egg membrane for mammalian fertilization[J].Proc Natl Acad Sci U S A,2011,108(27):10946-10951.
[58]	ZHOU G B,LIU G S,MENG Q G,et al.Tetraspanin CD9 in bovine oocytes and its role in fertilization[J].J Reprod Dev,2009, 55(3): 305-308.
[59]	MIYADO K,YOSHIDA K,YAMAGATA K,et al.The fusing ability of sperm is bestowed by CD9-containing vesicles released from eggs in mice[J].Proc Natl Acad Sci U S A,2008,105(35):12921-12926.
[60]	INOUE N,SAITO T,WADA I.Unveiling a novel function of CD9 in surface compartmentalization of oocytes[J].Development, 2020,147(15):dev189985.
[61]	BENAMMAR A,ZIYYAT A,LEFōVRE B,et al.Tetraspanins and mouse oocyte microvilli related to fertilizing ability[J].Reprod Sci,2017,24(7):1062-1069.
[62]	KAJI K,ODA S,SHIKANO T,et al.The gamete fusion process is defective in eggs of CD9-deficient mice[J].Nat Genet,2000, 24(3):279-282.
[63]	ZHU G Z,MILLER B J,BOUCHEIX C,et al.Residues SFQ (173-175) in the large extracellular loop of CD9 are required for gamete fusion[J].Development,2002,129(8):1995-2002.
[64]	LE NAOUR F,RUBINSTEIN E,JASMIN C,et al.Severely reduced female fertility in CD9-deficient mice[J].Science,2000, 287(5451):319-321.
[65]	SALA-VALDÉS M,URSA Á,CHARRIN S,et al.EWI-2 and EWI-F link the tetraspanin web to the actin cytoskeleton through their direct association with ezrin-radixin-moesin proteins[J].J Biol Chem,2006,281(28):19665-19675.
[66]	KINOSHITA T,FUJITA M.Thematic review series:glycosylphosphatidylinositol (GPI) anchors:biochemistry and cell biology biosynthesis of GPI-anchored proteins:Special emphasis on GPI lipid remodeling[J].J Lipid Res,2016,57(1):6-24.
[67]	COONROD S A,NAABY-HANSEN S,SHETTY J,et al.Treatment of mouse oocytes with PI-PLC releases 70-kDa (pI 5) and 35- to 45-kDa (pI 5.5) protein clusters from the egg surface and inhibits sperm-oolemma binding and fusion[J].Dev Biol,1999, 207(2):334-349.
[68]	BIANCHI E,DOE B,GOULDING D,et al.Juno is the egg Izumo receptor and is essential for mammalian fertilization[J].Nature, 2014,508(7497):483-487.
[69]	胡文萍,汤继顺,张壮彪,等.Izumo1和Juno在哺乳动物受精过程中的研究进展[J].畜牧兽医学报,2019,50(9):1737-1745.HU W P,TANG J S,ZHANG Z B,et al.Progress of Izumo1 and Juno in mammalian fertilization[J].Acta Veterinaria et Zootechnica Sinica,2019,50(9):1737-1745.(in Chinese)
[70]	LOPEZ S,RODRIGUEZ-GALLARDO S,SABIDO-BOZO S,et al.Endoplasmic reticulum export of GPI-anchored proteins[J].Int J Mol Sci,2019,20(14):3506.
[71]	BÄR S,ROMMELAERE J,NVESCH J P F.Vesicular transport of progeny parvovirus particles through ER and Golgi regulates maturation and cytolysis[J].PLoS Pathog,2013,9(9):e1003605.
[72]	MAHÉ C,ZLOTKOWSKA A M,REYNAUD K,et al.Sperm migration,selection,survival,and fertilizing ability in the mammalian oviduct[J].Biol Reprod,2021,105(2):317-331.
[73]	GURAYA S S.Recent progress in the structure,origin,composition,and function of cortical granules in animal egg[J].Int Rev Cytol,1982,78:257-360.
[74]	孙青原,秦鹏春.牛卵母细胞发育的超微结构研究[J].山东农业大学学报,1989(4):9-16.SUN Q Y,QIN P C.Study on ultrastructure of bovine oocyte development[J].Journal of Shandong Agricultural University,1989(4): 9-16.(in Chinese)
[75]	SUN Q Y,LAI L X,BONK A,et al.Cytoplasmic changes in relation to nuclear maturation and early embryo developmental potential of porcine oocytes:effects of gonadotropins,cumulus cells,follicular size,and protein synthesis inhibition[J].Mol Reprod Dev,2001,59(2):192-198.
[76]	WANG W H,HOSOE M,SHIOYA Y.Induction of cortical granule exocytosis of pig oocytes by spermatozoa during meiotic maturation[J].J Reprod Fertil,1997,109(2):247-255.
[77]	YU X B,ZHANG X C,ZHAO P,et al.Fertilized egg cells secrete endopeptidases to avoid polytubey[J].Nature,2021, 592(7854):433-437.
[78]	TSUBAMOTO H,HASEGAWA A,NAKATA Y,et al.Expression of recombinant human zona pellucida protein 2 and its binding capacity to spermatozoa[J].Biol Reprod,1999,61(6):1649-1654.
[79]	TSAADON A,ELIYAHU E,SHTRAIZENT N,et al.When a sperm meets an egg:block to polyspermy[J].Mol Cell Endocrinol, 2006, 252(1-2):107-114.
[80]	ROJAS J,HINOSTROZA F,VERGARA S,et al.Knockin’ on egg’s door:maternal control of egg activation that influences cortical granule exocytosis in animal species[J].Front Cell Dev Biol,2021,9:704867.
[81]	SACHDEV M,MANDAL A,MULDERS S,et al.Oocyte specific oolemmal SAS1B involved in sperm binding through intra-acrosomal SLLP1 during fertilization[J].Dev Biol,2012,363(1):40-51.
[82]	HERRERO M B,MANDAL A,DIGILIO L C,et al.Mouse SLLP1,a sperm lysozyme-like protein involved in sperm-egg binding and fertilization[J].Dev Biol,2005,284(1):126-142.
[83]	KÖRSCHGEN H,KUSKE M,KARMILIN K,et al.Intracellular activation of ovastacin mediates pre-fertilization hardening of the zona pellucida[J].Mol Hum Reprod,2017,23(9):607-616.
[84]	GARCÍA-MARTÍNEZ S,GADEA J,COY P,et al.Addition of exogenous proteins detected in oviductal secretions to in vitro culture medium does not improve the efficiency of in vitro fertilization in pigs[J].Theriogenology,2020,157:490-497.
[85]	PIEHL L L,FISCHMAN M L,HELLMAN U,et al.Boar seminal plasma exosomes:effect on sperm function and protein identification by sequencing[J].Theriogenology,2013,79(7):1071-1082.
[86]	陈晓勇,敦伟涛,孙洪新,等.哺乳动物卵子皮质反应机制的研究进展[J].黑龙江畜牧兽医,2010(8):27-30.CHEN X Y,DUN W T,SUN H X,et al.Research progress of mechanism of the cortical reaction in mammalian eggs[J].Heilongjiang Animal Science and Veterinary Medicine,2010(8):27-30.(in Chinese)
[87]	ZHUAN Q R,LI J,ZHOU G Z,et al.Procyanidin b2 protects aged oocytes against meiotic defects through cortical tension modulation[J].Front Vet Sci,2022,9:795050.

Research Progress of ERM Proteins in Mammalian Oocyte Maturation and Fertilization

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