哺乳动物子宫腔胞外囊泡的组分及功能研究进展
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摘要
胞外囊泡(Extracellular vesicles,EVs)是细胞间通讯的一种媒介,包含两个大亚类—微泡和外泌体。胞外囊泡能选择性地包裹着脂质、蛋白质、mRNAs、miRNAs以及DNA等物质,可以远距离的运输到靶细胞,通过调控靶细胞的转录、翻译等来影响细胞的功能。哺乳动物子宫腔液中含有丰富的胞外囊泡,它们对精子获能,胚胎与母体子宫间的相互识别以及胚胎附植都具有重要作用。本文主要对子宫腔液中胞外囊泡的组分及其在胚胎附植过程中的作用进行综述。
Extracellular vesicles(EVs) are a mediator of intercellular communication and contain two major subclasses—microvesicles and exosomes. Extracellular vesicles can selectively encapsulate lipids, proteins, mRNAs, miRNAs, and DNA. They can be transported to target cells from a long distance, and affect the function of cells by regulating the transcription and translation of target cells. Mammalian uterine fluid is rich in extracellular vesicles, which play an important role in sperm capacitation, mutual recognition between embryos and maternal uterus, and embryo attachment. This article reviews the components of extracellular vesicles in uterine fluid and their role in embryonic attachment.
Extracellular vesicles(EVs) are a mediator of intercellular communication and contain two major subclasses—microvesicles and exosomes. Extracellular vesicles can selectively encapsulate lipids, proteins, mRNAs, miRNAs, and DNA. They can be transported to target cells from a long distance, and affect the function of cells by regulating the transcription and translation of target cells. Mammalian uterine fluid is rich in extracellular vesicles, which play an important role in sperm capacitation, mutual recognition between embryos and maternal uterus, and embryo attachment. This article reviews the components of extracellular vesicles in uterine fluid and their role in embryonic attachment.
引文
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[17]Piccin A,Murphy W G,Smith O P.Circulating microparticles:pathophysiology and clinical implications[J].Blood Reviews,2007,21(3):157-171.
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[22]Sato-Kuwabara Y,Melo S A,Soares F A,et al.The fusion of two worlds:non-coding RNAs and extracellular vesicles--diagnostic and therapeutic implications(Review)[J].Int J Oncol,2015,46(1):17-27.
[23]Greening D W,Gopal S K,Xu R,et al.Exosomes and their roles in immune regulation and cancer[J].Seminars in Cell&Developmental Biology,2015,40:72-81.
[24]王琎,陈建英.细胞外囊泡研究新进展[J].中国组织工程研究,2017,21(4):621-626.
[25]Andreu Z,Y??Ez-M?M A.Tetraspanins in Extracellular Vesicle Formation and Function[J].Frontiers in Immunology.2014,5.
[26]Henne W M,Buchkovich N J,Emr S D.The ESCRT Pathway[J].Developmental Cell,2011,21(1):77-91.
[27]Baietti M F,Zhang Z,Mortier E,et al.Syndecan-syntenin-ALIX regulates the biogenesis of exosomes[J].Nature Cell Biology,2012,14(7):677-685.
[28]Ostrowski M,Carmo N B,Krumeich S,et al.Rab27a and Rab27b control different steps of the exosome secretion pathway[J].Nature Cell Biology,2010,12(1):19-30.
[29]Yu X,Harris S L,Levine A J.The Regulation of Exosome Secretion:a Novel Function of the p53 Protein[J].Cancer Research,2006,66(9):4795-4801.
[30]Chaput N,Ta?eb J,Schartz N,et al.The potential of exosomes in immunotherapy of cancer[J].Blood Cells,Molecules,and Diseases,2005,35(2):111-115.
[31]Xu R,Greening D W,Rai A,et al.Highly-purified exosomes and shed microvesicles isolated from the human colon cancer cell line LIM1863 by sequential centrifugal ultrafiltration are biochemically and functionally distinct[J].Methods,2015,87:11-25.
[32]Kowal J,Arras G,Colombo M,et al.Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes[J].Proceedings of the National Academy of Sciences,2016,113(8):E968-E977.
[33]Salicioni A M,Platt M D,Wertheimer E V,et al.Signalling pathways involved in sperm capacitation[J].Society of Reproduction and Fertility supplement,2007,65:245.
[34]Visconti P E,Krapf D,de la Vega-Beltrán JL,et al.Ion channels,phosphorylation and mammalian sperm capacitation[J].Asian Journal of Andrology,2011,13(3):395-405.
[35]Visconti P E.Understanding the molecular basis of sperm capacitation through kinase design[J].Proc Natl Acad Sci U S A.,2009,106(3):667-668.
[36]Thie M,Fuchs P,Denker H W.Epithelial cell polarity and embryo implantation in mammals[J].The International journal of developmental biology,1996,40(1):389.
[37]Paiva P,Hannan N J,Hincks C,et al.Human chorionic gonadotrophin regulates FGF2 and other cytokines produced by human endometrial epithelial cells,providing a mechanism for enhancing endometrial receptivity[J].Human Reproduction,2011,26(5):1153-1162.
[38]Thouas G A,Dominguez F,Green M P,et al.Soluble Ligands and Their Receptors in Human Embryo Development and Implantation[J].Endocrine Reviews,2015,36(1):92-130.
[39]Burns G W,Brooks K E,Spencer T E.Extracellular Vesicles Originate from the Conceptus and Uterus During Early Pregnancy in Sheep1[J].Biology of Reproduction,2016,94(3).
[40]Griffiths G S,Galileo D S,Reese K,et al.Investigating the role of murine epididymosomes and uterosomes in GPI-linked protein transfer to sperm using SPAM1 as a model[J].Molecular Reproduction and Development,2008,75(11):1627-1636.
[41]Braundmeier A G,Dayger C A,Mehrotra P,et al.EMMPRIN Is Secreted by Human Uterine Epithelial Cells in Microvesicles and Stimulates Metalloproteinase Production by Human Uterine Fibroblast Cells[J].Reproductive Sciences,2012,19(12):1292-1301.
[42]Racicot K,Schmitt A,Ott T.The myxovirusresistance protein,MX1,is a component of exosomes secreted by uterine epithelial cells[J].Am J Reprod Immunol,2012,67(6):498-505.
[43]Aplin J D.Embryo implantation:the molecular mechanism remains elusive[J].Reproductive biomedicine online,2007,14 Spec No 1:49-55.
[44]Greening D W,Nguyen H P T,Elgass K,et al.Human Endometrial Exosomes Contain HormoneSpecific Cargo Modulating Trophoblast Adhesive Capacity:Insights into Endometrial-Embryo Interactions1[J].Biology of Reproduction,2016,94(2).
[45]Salomon C,Yee S,Scholz-Romero K,et al.Extravillous trophoblast cells-derived exosomes promote vascular smooth muscle cell migration[J].Frontiers in Pharmacology,2014,5.
[46]Desrochers L M,Bordeleau F,Reinhart-King CA,et al.Microvesicles provide a mechanism for intercellular communication by embryonic stem cells during embryo implantation[J].Nat Commun,2016,7:11958.
[47]Mccallie B,Schoolcraft W B,Katz-Jaffe M G.Aberration of blastocyst microRNA expression is associated with human infertility[J].Fertility and Sterility,2010,93(7):2374-2382.
[48]Altm?e S,Martinez-Conejero J A,Esteban FJ,et al.MicroRNAs miR-30b,miR-30d,and miR-494 Regulate Human Endometrial Receptivity[J].Reproductive Sciences,2012,20(3):308-317.
[49]Vilella F,Moreno-Moya J M,Balaguer N,et al.Hsa-miR-30d,secreted by the human endometrium,is taken up by the pre-implantation embryo and might modify its transcriptome[J].Development,2015,142(18):3210-3221.
[50]Ruiz-González I,Xu J,Wang X,et al.Exosomes,endogenous retroviruses and toll-like receptors:pregnancy recognition in ewes[J].REPRODUCTION,2015,149(3):281-291.
[51]Liang X,Zhang L,Wang S,et al.Exosomes secreted by mesenchymal stem cells promote endothelial cell angiogenesis by transferring miR-125a[J].Journal of Cell Science,2016,129(11):2182-2189.
[52]Hu S,Ren G,Liu J,et al.MicroRNA Expression and Regulation in Mouse Uterus during Embryo Implantation[J].Journal of Biological Chemistry,2008,283(34):23473-23484.
[53]Kusama K,Nakamura K,Bai R,et al.Intrauterine exosomes are required for bovine conceptus implantation[J].Biochemical and Biophysical Research Communications,2018,495(1):1370-1375.
[2]Xu R,Greening D W,Zhu H,et al.Extracellular vesicle isolation and characterization:toward clinical application[J].Journal of Clinical Investigation,2016,126(4):1152-1162.
[3]Raposo G,Stoorvogel W.Extracellular vesicles:Exosomes,microvesicles,and friends[J].The Journal of Cell Biology,2013,200(4):373-383.
[4]Aliotta J M,Pereira M,Johnson K W,et al.Microvesicle entry into marrow cells mediates tissue-specific changes in mRNA by direct delivery of mRNA and induction of transcription[J].Experimental Hematology,2010,38(3):233-245.
[5]Johnstone R M,Adam M,Hammond J R,et al.Vesicle formation during reticulocyte maturation.Association of plasma membrane activities with released vesicles(exosomes)[J].The Journal of biological chemistry,1987,262(19):9412-9420.
[6]Ng Y H,Rome S,Jalabert A,et al.Endometrial exosomes/microvesicles in the uterine microenvironment:a new paradigm for embryo-endometrial cross talk at implantation[J].PLoSOne,2013,8(3):e58502.
[7]Raj D A A,Fiume I,Capasso G,et al.A multiplex quantitative proteomics strategy for protein biomarker studies in urinary exosomes[J].Kidney International,2012,81(12):1263-1272.
[8]Foster B P,Balassa T,Benen T D,et al.Extracellular vesicles in blood,milk and body fluids of the female and male urogenital tract and with special regard to reproduction[J].Critical reviews in clinical laboratory sciences,2016,53(6):379-395.
[9]Asea A,Jean-Pierre C,Kaur P,et al.Heat shock protein-containing exosomes in mid-trimester amniotic fluids[J].Journal of Reproductive Immunology,2008,79(1):12-17.
[10]Poliakov A,Spilman M,Dokland T,et al.Structural heterogeneity and protein composition of exosome-like vesicles(prostasomes)in human semen[J].The Prostate,2009,69(2):159-167.
[11]Larssen P,Wik L,Czarnewski P,et al.Tracing Cellular Origin of Human Exosomes Using Multiplex Proximity Extension Assays[J].Molecular&Cellular Proteomics,2017,16(8):1547.
[12]Burnett L A,Nowak R A.Exosomes mediate embryo and maternal interactions at implantation and during pregnancy[J].Frontiers in bioscience(Scholar edition),2016,8:79.
[13]Luo S,Ishibashi O,Ishikawa G,et al.Human Villous Trophoblasts Express and Secrete Placenta-Specific MicroRNAs into Maternal Circulation via Exosomes1[J].Biology of Reproduction,2009,81(4):717-729.
[14]Rufino-Ramos D,Albuquerque P R,Carmona V,et al.Extracellular vesicles:Novel promising delivery systems for therapy of brain diseases[J].Journal of Controlled Release,2017,262:247-258.
[15]Bianco F,Perrotta C,Novellino L,et al.Acid sphingomyelinase activity triggers microparticle release from glial cells[J].EMBOJ.,2009,28(8):1043-1054.
[16]Di Vizio D,Kim J,Hager M H,et al.Oncosome Formation in Prostate Cancer:Association with a Region of Frequent Chromosomal Deletion in Metastatic Disease[J].Cancer Research,2009,69(13):5601-5609.
[17]Piccin A,Murphy W G,Smith O P.Circulating microparticles:pathophysiology and clinical implications[J].Blood Reviews,2007,21(3):157-171.
[18]Camussi G,Deregibus M C,Bruno S,et al.Exosomes/microvesicles as a mechanism of cell-to-cell communication[J].Kidney International,2010,78(9):838-848.
[19]Akers J C,Gonda D,Kim R,et al.Biogenesis of extracellular vesicles(EV):exosomes,microvesicles,retrovirus-like vesicles,and apoptotic bodies[J].Journal of Neuro-Oncology,2013,113(1):1-11.
[20]Maas S L N,Breakefield X O,Weaver A M.Extracellular Vesicles:Unique Intercellular Delivery Vehicles[J].Trends in Cell Biology,2017,27(3):172-188.
[21]Théry C,Ostrowski M,Segura E.Membrane vesicles as conveyors of immune responses[J].Nature Reviews Immunology,2009,9(8):581-593.
[22]Sato-Kuwabara Y,Melo S A,Soares F A,et al.The fusion of two worlds:non-coding RNAs and extracellular vesicles--diagnostic and therapeutic implications(Review)[J].Int J Oncol,2015,46(1):17-27.
[23]Greening D W,Gopal S K,Xu R,et al.Exosomes and their roles in immune regulation and cancer[J].Seminars in Cell&Developmental Biology,2015,40:72-81.
[24]王琎,陈建英.细胞外囊泡研究新进展[J].中国组织工程研究,2017,21(4):621-626.
[25]Andreu Z,Y??Ez-M?M A.Tetraspanins in Extracellular Vesicle Formation and Function[J].Frontiers in Immunology.2014,5.
[26]Henne W M,Buchkovich N J,Emr S D.The ESCRT Pathway[J].Developmental Cell,2011,21(1):77-91.
[27]Baietti M F,Zhang Z,Mortier E,et al.Syndecan-syntenin-ALIX regulates the biogenesis of exosomes[J].Nature Cell Biology,2012,14(7):677-685.
[28]Ostrowski M,Carmo N B,Krumeich S,et al.Rab27a and Rab27b control different steps of the exosome secretion pathway[J].Nature Cell Biology,2010,12(1):19-30.
[29]Yu X,Harris S L,Levine A J.The Regulation of Exosome Secretion:a Novel Function of the p53 Protein[J].Cancer Research,2006,66(9):4795-4801.
[30]Chaput N,Ta?eb J,Schartz N,et al.The potential of exosomes in immunotherapy of cancer[J].Blood Cells,Molecules,and Diseases,2005,35(2):111-115.
[31]Xu R,Greening D W,Rai A,et al.Highly-purified exosomes and shed microvesicles isolated from the human colon cancer cell line LIM1863 by sequential centrifugal ultrafiltration are biochemically and functionally distinct[J].Methods,2015,87:11-25.
[32]Kowal J,Arras G,Colombo M,et al.Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes[J].Proceedings of the National Academy of Sciences,2016,113(8):E968-E977.
[33]Salicioni A M,Platt M D,Wertheimer E V,et al.Signalling pathways involved in sperm capacitation[J].Society of Reproduction and Fertility supplement,2007,65:245.
[34]Visconti P E,Krapf D,de la Vega-Beltrán JL,et al.Ion channels,phosphorylation and mammalian sperm capacitation[J].Asian Journal of Andrology,2011,13(3):395-405.
[35]Visconti P E.Understanding the molecular basis of sperm capacitation through kinase design[J].Proc Natl Acad Sci U S A.,2009,106(3):667-668.
[36]Thie M,Fuchs P,Denker H W.Epithelial cell polarity and embryo implantation in mammals[J].The International journal of developmental biology,1996,40(1):389.
[37]Paiva P,Hannan N J,Hincks C,et al.Human chorionic gonadotrophin regulates FGF2 and other cytokines produced by human endometrial epithelial cells,providing a mechanism for enhancing endometrial receptivity[J].Human Reproduction,2011,26(5):1153-1162.
[38]Thouas G A,Dominguez F,Green M P,et al.Soluble Ligands and Their Receptors in Human Embryo Development and Implantation[J].Endocrine Reviews,2015,36(1):92-130.
[39]Burns G W,Brooks K E,Spencer T E.Extracellular Vesicles Originate from the Conceptus and Uterus During Early Pregnancy in Sheep1[J].Biology of Reproduction,2016,94(3).
[40]Griffiths G S,Galileo D S,Reese K,et al.Investigating the role of murine epididymosomes and uterosomes in GPI-linked protein transfer to sperm using SPAM1 as a model[J].Molecular Reproduction and Development,2008,75(11):1627-1636.
[41]Braundmeier A G,Dayger C A,Mehrotra P,et al.EMMPRIN Is Secreted by Human Uterine Epithelial Cells in Microvesicles and Stimulates Metalloproteinase Production by Human Uterine Fibroblast Cells[J].Reproductive Sciences,2012,19(12):1292-1301.
[42]Racicot K,Schmitt A,Ott T.The myxovirusresistance protein,MX1,is a component of exosomes secreted by uterine epithelial cells[J].Am J Reprod Immunol,2012,67(6):498-505.
[43]Aplin J D.Embryo implantation:the molecular mechanism remains elusive[J].Reproductive biomedicine online,2007,14 Spec No 1:49-55.
[44]Greening D W,Nguyen H P T,Elgass K,et al.Human Endometrial Exosomes Contain HormoneSpecific Cargo Modulating Trophoblast Adhesive Capacity:Insights into Endometrial-Embryo Interactions1[J].Biology of Reproduction,2016,94(2).
[45]Salomon C,Yee S,Scholz-Romero K,et al.Extravillous trophoblast cells-derived exosomes promote vascular smooth muscle cell migration[J].Frontiers in Pharmacology,2014,5.
[46]Desrochers L M,Bordeleau F,Reinhart-King CA,et al.Microvesicles provide a mechanism for intercellular communication by embryonic stem cells during embryo implantation[J].Nat Commun,2016,7:11958.
[47]Mccallie B,Schoolcraft W B,Katz-Jaffe M G.Aberration of blastocyst microRNA expression is associated with human infertility[J].Fertility and Sterility,2010,93(7):2374-2382.
[48]Altm?e S,Martinez-Conejero J A,Esteban FJ,et al.MicroRNAs miR-30b,miR-30d,and miR-494 Regulate Human Endometrial Receptivity[J].Reproductive Sciences,2012,20(3):308-317.
[49]Vilella F,Moreno-Moya J M,Balaguer N,et al.Hsa-miR-30d,secreted by the human endometrium,is taken up by the pre-implantation embryo and might modify its transcriptome[J].Development,2015,142(18):3210-3221.
[50]Ruiz-González I,Xu J,Wang X,et al.Exosomes,endogenous retroviruses and toll-like receptors:pregnancy recognition in ewes[J].REPRODUCTION,2015,149(3):281-291.
[51]Liang X,Zhang L,Wang S,et al.Exosomes secreted by mesenchymal stem cells promote endothelial cell angiogenesis by transferring miR-125a[J].Journal of Cell Science,2016,129(11):2182-2189.
[52]Hu S,Ren G,Liu J,et al.MicroRNA Expression and Regulation in Mouse Uterus during Embryo Implantation[J].Journal of Biological Chemistry,2008,283(34):23473-23484.
[53]Kusama K,Nakamura K,Bai R,et al.Intrauterine exosomes are required for bovine conceptus implantation[J].Biochemical and Biophysical Research Communications,2018,495(1):1370-1375.