Conceptus implantation and placentation: molecules related to epithelial–mesenchymal transition, lymphocyte homing, endogenous retroviruses, and exosomes

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• 作者：Kazuhiko Imakawa ; Rulan Bai ; Hiroshi Fujiwara…
• 关键词：EMT ; ERV ; Exosome ; Gene expression ; Implantation
• 刊名：Reproductive Medicine and Biology
• 出版年：2016
• 出版时间：January 2016
• 年：2016
• 卷：15
• 期：1
• 页码：1-11
• 全文大小：1,389 KB
• 参考文献：1.Amoroso EC. The evolution of viviparity. J R Soc Med. 1968;61:1188–200.
  2.Bazer FW, Spencer TE, Johnson GA, Burghardt RC, Wu G. Comparative aspects of implantation. Reproduction. 2009;138:195–209.PubMed CrossRef
  3.Hearn JP, Webley GE, Gidley-Baird AA. Chorionic gonadotrophin and embryo-maternal recognition during the peri-implantation period in primates. J Reprod Fertil. 1991;92:497–509.PubMed CrossRef
  4.Soares MJ, Faria TN, Roby KF, Deb S. Pregnancy and the prolactin family of hormones: coordination of anterior pituitary, uterine, and placental expression. Endocr Rev. 1991;12:402–23.PubMed CrossRef
  5.Short RV. Implantation and the maternal recognition of pregnancy. In: Wolstenhome GEW, O’Connor M, editors. “Foetal Anatomy”, Ciba Foundation Symposium. London: J&A Churchill; 1969. p. 2–26.
  6.Quagliarello J, Goldsmith L, Steinetz B, Lustig DS, Weiss G. Induction of relaxin secretion in nonpregnant women by human chorionic gonadotropin. J Clin Endocrinol Metab. 1980;51:74–7.PubMed CrossRef
  7.Godkin JD, Bazer FW, Moffatt J, Sessions F, Roberts RM. Purification and properties of a major, low molecular weight protein released by the trophoblast of sheep blastocysts at day 13–21. J Reprod Fertil. 1982;65:141–50.PubMed CrossRef
  8.Imakawa K, Anthony RV, Kazami M, Marotti KR, Polites HG, Roberts RM. Interferon-like sequence of ovine trophoblast protein secreted by embryonic trophectoderm. Nature. 1987;330:377–9.PubMed CrossRef
  9.Stewert HJ, McCann SHE, Barker PJ, Lee KE, Lamming GE, Flint APF. Interferon sequence homology and receptor binding activity of ovine trophoblast antiluteolytic protein. J Endocrinol. 1987;115:R13–5.CrossRef
  10.Charpigny G, Reinard P, Huet JC, Guillomot M, Charlier M, Pernollet JC, Martal J. High homology between a trophoblastic protein (trophoblastin) isolated from ovine embryo and α-interferon. FEBS Lett. 1988;228:12–6.PubMed CrossRef
  11.Roberts RM, Cross JC, Leaman DW. Interferons as hormones of pregnancy. Endocr Rev. 1992;13:432–52.PubMed
  12.Imakawa K, Hansen TR, Malathy PV, Anthony RV, Polites HG, Marotti KR, Roberts RM. Molecular cloning and characterization of complementary deoxyribonucleic acids corresponding to bovine trophoblast-1: a comparison with ovine trophoblast protein-1 and bovine interferon-alpha II. Mol Endocrinol. 1989;3:127–39.PubMed CrossRef
  13.Pestka S, Langer JA, Zoon KC, Samuel CE. Interferons and their actions. Annual Rev Biochem. 1987;56:727–77.CrossRef
  14.Niwano Y, Hansen TR, Kazemi M, Malathy PV, Johnson HD, Roberts RM, Imakawa K. Suppression of T-lymphocyte blastogenesis by ovine trophoblast protein-1 and human interferon-alpha may be independent of interleukin-2 production. Am J Reprod Immunol. 1989;20:21–6.PubMed CrossRef
  15.Roberts RM, Imakawa K, Niwano Y, Kazemi M, Malathy PV, Hansen TR, Glass AA, Kronenberg LH. Interferon production by the preimplantation sheep embryo. J Interferon Res. 1989;9:175–87.PubMed CrossRef
  16.Pontzer CH, Bazer FW, Johnson HM. Antiproliferative activity of a pregnancy recognition hormone, ovine trophoblast protein-1. Cancer Res. 1991;51:5304–7.PubMed
  17.Pontzer CH, Yamamoto JK, Bazer FW, Ott TL, Johnson HM. Potent anti-feline immunodeficiency virus and anti-human immunodeficiency virus effect of IFN-τ. J Immunol. 1997;158:4351–7.PubMed
  18.Pestka S, Krause CD, Walter MR. Interferons, interferon-like cytokines, and their receptors. Immunol Rev. 2004;202:8–32.PubMed CrossRef
  19.Rosenfeld CS, Han CS, Alexenko AP, Spencer TE, Roberts RM. Expression of interferon receptor subunits, IFNAR1 and IFNAR2, in the ovine uterus. Biol Reprod. 2002;67:847–53.PubMed CrossRef
  20.Imakawa K, Tamura K, Lee R-S, Ji Y, Kogo H, Sakai S, Christenson RK. Temporal expression of type I interferon receptor in the peri-implantation ovine extra-embryonic membranes: demonstration that human IFN-alpha can bind to this receptor. Endocr J. 2002;49:195–205.PubMed CrossRef
  21.Ott TL, Yin J, Wiley AA, Kim HT, Gerami-Naini B, Spencer TE, Bartol FF, Burghardt RC, Bazer FW. Effects of the estrous cycle and early pregnancy on uterine expression of Mx protein in sheep (Ovis aries). Biol Reprod. 1998;59:784–94.PubMed CrossRef
  22.Johnson GA, Spencer TE, Hansen TR, Austin KJ, Burghardt RC, Bazer FW. Expression of the interferon tau inducible ubiquitin cross-reactive protein in the ovine uterus. Biol Reprod. 1999;61:312–8.PubMed CrossRef
  23.Hicks BA, Etter SJ, Carnahan KG, Joyce MM, Assiri AA, Carling S, Kodali K, Johnson GA, Hansen TR, Mirando MA, Woods GL, Vanderwall DK, Ott TL. Expression of the uterine Mx protein in cyclic and pregnant cows, gilts, and mares. J Anim Sci. 2003;81:1552–62.PubMed
  24.Shirasuna K, Nitta A, Sineenard J, Shimizu T, Bollwein H, Miyamoto A. Vascular and immune regulation of corpus luteum development, maintenance, and regression in the cow. Domest Anim Endocrinol. 2012;43:198–211.PubMed CrossRef
  25.Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. How cells respond to interferons. Ann Rev Biochem. 1998;67:227–64.PubMed CrossRef
  26.Kim S, Choi Y, Bazer FW, Spencer TE. Identification of genes in the ovine endometrium regulated by interferon tau independent of signal transducer and activator of transcription 1. Endocrinology. 2003;144:5203–14.PubMed CrossRef
  27.Chen Y, Antoniou E, Liu Z, Hearne LB, Roberts RM. A microarray analysis for genes regulated by interferon-τ in ovine luminal epithelial cells. Reproduction. 2007;134:123–35.PubMed CrossRef
  28.Spencer TE, Sandra O, Wolf E. Genes involved in conceptus-endometrial interactions in ruminants: insights from reductionism and thoughts on holistic approaches. Reproduction. 2008;135:165–79.PubMed CrossRef
  29.Gray CA, Adelson DL, Bazer FW, Burghardt RC, Meeusen EN, Spencer TE. Discovery and characterization of an epithelial-specific galectin in the endometrium that forms crystals in the trophectoderm. Proc Natl Acad Sci USA. 2004;101:7982–7.PubMedCentral PubMed CrossRef
  30.Mohamed OA, Jonaert M, Labelle-Dumais C, Kuroda K, Clarke HJ, Dufort D. Uterine Wnt/β-catenin signaling is required for implantation. Proc Natl Acad Sci USA. 2005;102:8579–84.PubMedCentral PubMed CrossRef
  31.Nagaoka K, Sakai A, Nojima H, Suda Y, Yokomizo Y, Imakawa K, Sakai S, Christenson RK. Expression of a chemokine, IFN-gamma-inducible protein 10 kDa, is stimulated by IFN-τ in the ovine endometrium. Biol Reprod. 2003;68:1413–21.PubMed CrossRef
  32.Imakawa K, Imai M, Sakai A, Suzuki M, Nagaoka K, Sakai S, Lee S-R, Chang K-T, Echterrnkamp SE, Christenson RK. Regulation of conceptus adhesion by endometrial CXC chemokines during the implantation period in sheep. Mol Reprod Dev. 2006;73:850–58.PubMed CrossRef
  33.Nagaoka K, Nojima H, Watanabe F, Christenson RK, Sakai S, Imakawa K. Regulation of blastocyst migration, apposition and initial adhesion by a chemokine, IFN-γ-inducible protein 10 kDa (IP-10), during early gestation. J Biol Chem. 2003;278:29048–56.PubMed CrossRef
  34.Imakawa K, Nagaoka K, Nojima H, Hara Y, Christenson RK. Changes in immune cell distribution and IL-10 production are regulated through endometrial IP-10 expression in the goat uterus. Am J Reprod Immunol. 2005;53:54–64.PubMed CrossRef
  35.Aplin JD, Hey NA, Graham RA. Human endometrial MUC1 carries keratan sulfate: characteristic glycoforms in the luminal epithelium at receptivity. Glycobiology. 1998;8:269–76.PubMed CrossRef
  36.Armant DR. Blastocysts don’t go it alone. Extrinsic signals fine-tune the intrinsic developmental program of trophoblast cells. Dev Biol. 2005;280:260–80.PubMedCentral PubMed CrossRef
  37.Akiyama SK. Integrins in cell adhesion and signaling. Hum Cell. 1996;9:181–6.PubMed
  38.MacIntyre DM, Lim HC, Ryan K, Kimmins S, Small JA, MacLaren LA. Implantation-associated changes in bovine uterine expression of integrins and extracellular matrix. Biol Reprod. 2002;66:1430–6.PubMed CrossRef
  39.Pfarrer C, Hirsch P, Guillomot M, Leiser R. Interaction of integrin receptors with extracellular matrix is involved in trophoblast giant cell migration in bovine placentomes. Placenta. 2003;24:588–97.PubMed CrossRef
  40.Pfarrer CD. Characterization of the bovine placenta by cytoskeleton, integrin receptors, and extracellular matrix. Methods Mol Med. 2006;121:323–35.PubMed
  41.Yamakoshi S, Bai R, Chaen T, Ideta A, Aoyagi Y, Sakurai T, Konno T, Imakawa K. Expression of mesenchymal-related genes by the bovine trophectoderm following conceptus attachment to the endometrial epithelium. Reproduction. 2012;143:377–87.PubMed CrossRef
  42.Osborn L, Hession C, Tizard R, Vassallo C, Luhowskyj S, Chi-Rosso G, Lobb R. Direct expression cloning of vascular cell adhesion molecule 1, a cytokine-induced endothelial protein that binds to lymphocytes. Cell. 1989;59:1203–11.PubMed CrossRef
  43.May MJ, Entwistle G, Humphries MJ, Ager A. VCAM-1-1 is a CS1 peptide-inhibitable adhesion molecule expressed by lymph node high endothelium. J Cell Sci. 1993;106:109–19.PubMed
  44.Ding YB, Chen GY, Xia JG, Zang XW, Yang HY, Yang L. Association of VCAM-1 overexpression with oncogenesis, tumor angiogenesis and metastasis of gastric carcinoma. World J Gastroenterol. 2003;9:1409–14.PubMedCentral PubMed CrossRef
  45.Gurtner GC, Davis V, Li H, McCoy MJ, Sharpe A, Cybulsky MI. Targeted disruption of the murine VCAM-1 gene: essential role of VCAM-1 in chorioallantoic fusion and placentation. Genes Dev. 1995;9:1–14.PubMed CrossRef
  46.Konac E, Alp E, Onen HI, Korucuoglu U, Biri AA, Menevse S. Endometrial mRNA expression of matrix metalloproteinases, their tissue inhibitors and cell adhesion molecules in unexplained infertility and implantation failure patients. Reprod Biomed Online. 2009;19:391–7.PubMed CrossRef
  47.Rahman AN, Snibson KJ, Lee CS, Meeusen EN. Effects of implantation and early pregnancy on the expression of cytokines and vascular surface molecules in the sheep endometrium. J Reprod Immunol. 2004;64:45–58.PubMed CrossRef
  48.Henninger DD, Panés J, Eppihimer M, Russell J, Gerritsen M, Anderson DC, Granger DN. Cytokine-induced VCAM-1 and ICAM-1 expression in different organs of the mouse. J Immunol. 1997;158:1825–32.PubMed
  49.Denucci CC, Mitchell JS, Shimizu Y. Integrin function in T-cell homing to lymphoid and non-lymphoid sites: getting there and staying there. Crit Rev Immunol. 2009;29:87–109.PubMedCentral PubMed CrossRef
  50.Stephens LE, Sutherland AE, Klimanskaya IV, Andrieux A, Meneses J, Pedersen RA, Damsky CH. Deletion of β 1 integrins in mice results in inner cell mass failure and peri-implantation lethality. Genes Develop. 1995;9:1883–95.PubMed CrossRef
  51.Yang JT, Rayburn H, Hynes RO. Cell adhesion events mediated by α4 integrins are essential in placental and cardiac development. Development. 1995;121:549–60.PubMed
  52.Bai R, Bai H, Kuse M, Ideta A, Aoyagi Y, Fujiwara H, Okuda K, Imakawa K, Sakurai T. Involvement of VCAM1 in the bovine conceptus adhesion to the uterine endometrium. Reproduction. 2014;148:119–27.PubMed CrossRef
  53.Sakurai T, Bai H, Bai R, Arai M, Iwazawa M, Zhang J, Konno T, Godkin JD, Okuda K, Imakawa K. Coculture system that mimics in vivo attachment processes in bovine trophoblast cells. Biol Reprod. 2012;87:1–11.CrossRef
  54.Biggers JD, Bell JE, Benos DL. Mammalian blastocyst: transport functions in a developing epithelium. Am J Physiol. 1988;255:C419–32.PubMed
  55.Kang HM, Kim K, Kwon HB, Cho WK. Regulation of laminin gene expression in the expansion of mouse blastocysts. Mol Reprod Dev. 1990;27:191–9.PubMed CrossRef
  56.Fleming TP, Sheth B, Fesenko I. Cell adhesion in the preimplantation mammalian embryo and its role in trophectodermal differentiation and blastocyst morphogenesis. Front Biosci. 2000;6:1000–7.CrossRef
  57.Denker HW. Implantation: a cell biological paradox. J Exp Zool. 1993;266:541–58.PubMed CrossRef
  58.Wathes DC, Wooding FB. An electron microscopic study of implantation in the cow. Am J Anat. 1980;159:285–306.PubMed CrossRef
  59.Peinado H, Olmeda D, Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype. Nat Rev Cancer. 2007;7:415–28.PubMed CrossRef
  60.Wang X, Zheng M, Liu G, Xia W, McKeown-Longo PJ, Hung MC, Zhao I. Küppel-like factor 8 induces epithelial to mesenchymal transition and epithelial cell invasion. Cancer Res. 2007;67:7184–93.PubMed CrossRef
  61.Yang J, Weinberg RA. Epithelial–mesenchymal transition: at the crossroads of development and tumor metastasis. Develop Cell. 2008;14:818–29.CrossRef
  62.Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelium-mesenchymal transitions in development and disease. Cell. 2009;139:871–90.PubMed CrossRef
  63.Mess A, Carter AM. Evolutionary transformations of fetal membrane characters in Eutheria with special reference to Afrotheria. J Exp Zool B Mol Dev Evol. 2006;306:140–63.PubMed CrossRef
  64.Mess A. Evolutionary transformations of chorioallantoic placental characters in Rodentia with special reference to hystricognath species. J Exp Zool A Comp Exp Biol. 2003;299:78–98.PubMed CrossRef
  65.Welsh AO, Enders AC. Trophoblast-decidual cell interactions and establishment of maternal blood circulation in the parietal yolk sac placenta of the rat. Anat Rec. 1987;217:203–19.PubMed CrossRef
  66.Enders AC, Blankenship TN, Conley AJ, Jones CJ. Structure of the midterm placenta of the spotted hyena, Crocuta crocuta, with emphasis on the diverse hemophagous regions. Cells Tissues Organs. 2006;183:141–55.PubMed CrossRef
  67.Enders AC, Carter AM. What can comparative studies of placental structure tell us?—a review. Placenta. 2004;25 Suppl A:S3–9.
  68.de Parseval N, Lazar V, Casella JF, Benit L, Heidmann T. Survey of human genes of retroviral origin: identification and transcriptome of the genes with coding capacity for complete envelope proteins. J Virol. 2003;77:10414–22.PubMedCentral PubMed CrossRef
  69.Blaise S, de Parseval N, Heidmann T. Functional characterization of two newly identified Human Endogenous Retrovirus coding envelope genes. Retrovirology. 2005;2:19.PubMedCentral PubMed CrossRef
  70.Mi S, Lee X, Li X, Veldman GM, Finnerty H, Racie L, LaVallie E, Tang XY, Edouard P, Howes S, Keith JC, McCoy JM. Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature. 2000;403:785–9.PubMed CrossRef
  71.Blaise S, de Parseval N, Benit L, Heidmann T. Genomewide screening for fusogenic human endogenous retrovirus envelops identifies syncytins 2, a gene conserved on primate evolution. Proc Natl Acad Sci USA. 2003;100:13013–8.PubMedCentral PubMed CrossRef
  72.Be L, Kanellopoulos C, Sapin V, Dupressoir A, Marceau G, Heidmann T. Placenta-specific murine envelope genes of retroviral origin conserved in Muridae. Science. 2005;102:725–30.
  73.Arnaud F, Caporale M, Varela M, Biek R, Chessa B, Alberti A, Golder M, Mura M, Zhang YP, Yu L, Pereira F, Demartini JC, Leymaster K, Spencer TE, Palmarini M. A paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses. PLoS Pathog. 2007;11:e170.CrossRef
  74.Heidmann O, Vernochet C, Dupressoir A, Heidmannn T. Identification of an endogenous retroviral envelope gene with fusogenic activity and placenta-specific expression in the rabbit: a new “syncytins” in a third order of mammals. Retrovirology. 2009;6:107.PubMedCentral PubMed CrossRef
  75.Cornelis G, Heidmann O, Bernard-Stoecklin S, Reynaud K, Véron G, Mulot B, Dupressoir A, Heidmann T. Ancestral capture of syncytin-Car1, a fusogenic endogenous retroviral envelope gene involved in placentation and conserved in Carnivora. Proc Natl Acad Sci USA. 2012;109:E432–41.PubMedCentral PubMed CrossRef
  76.Koshi K, Suzuki Y, Nakaya Y, Imai K, Hosoe M, Takahashi T, Kizaki K, Miyazawa T, Hashizume K. Bovine trophoblastic cell differentiation and binucleation involves enhanced endogenous retrovirus element expression. Reprod Biol Endocrinol. 2012;10:41.PubMedCentral PubMed CrossRef
  77.Cornelis G, Heidmann O, Degrelle SA, Vernochet C, Lavialle C, Letzelter C, Bernard-Stoecklin S, Hassanin A, Mulot B, Guillomot M, Hue I, Heidmann T, Dupressoir A. Captured retroviral envelope syncytin gene associated with the unique placental structure of higher ruminants. Proc Natl Acad Sci USA. 2013;110:E828–37.PubMedCentral PubMed CrossRef
  78.Cornelis G, Vernochet C, Carradec Q, Souquere S, Mulot B, Catzeflis F, Nilsson MA, Menzies BR, Renfree MB, Pierron G, Zeller U, Heidmann O, Dupressoir A, Heidmann T. Retroviral envelope gene captures and syncytin exaptation for placentation in marsupials. Proc Natl Acad Sci USA. 2015;112:E487–96.PubMedCentral PubMed CrossRef
  79.Boeke JD, Stoye JP. Retrotransposons, Endogenous Retroviruses, and the Evolution of Retroelements. In: Coffin JM, Hughes SH, Varmus HE, editors. Retroviruses. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 1997.
  80.Best S, Le Tissier PR, Stoye JP. Endogenous retroviruses and the evolution of resistance to retroviral infection. Trends Microbiol. 1997;5:313–8.PubMed CrossRef
  81.Harris JR. Placental endogenous retrovirus (ERV): structural, functional, and evolutionary significance. BioEssays. 1998;20:307–16.PubMed CrossRef
  82.Rawn SM, Cross JC. The evolution, regulation, and function of placenta-specific genes. Annu Rev Cell Dev Biol. 2008;24:159–81.PubMed CrossRef
  83.Macfarlan TS, Gifford WD, Driscoll S, Lettieri K, Rowe HM, Bonanomi D, Firth, Singer O, Trono D, Pfaff SL. Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature. 2012;487:57–63.PubMedCentral PubMed
  84.Huppertz B, Kaufmann P, Kingdom J. Trophoblast turnover in health and diseases. Fetal Matern Med Rev. 2002;13:103–18.CrossRef
  85.Dupressoir A, Marceau G, Vernochet C, Bénit L, Kanellopoulos C, Sapin V, Heidmann T. Syncytin-A and syncytin-B, two fusogenic placenta-specific murine envelope genes of retroviral origin conserved in Muridae. Proc Natl Acad Sci USA. 2005;102:725–30.PubMedCentral PubMed CrossRef
  86.Schubert SW, Lamoureux N, Kilian K, Klein-Hitpass L, Hashemolhosseini S. Identification of integrin-alpha4, Rb1, and syncytin a as murine placental target genes of the transcription factor GCMa/Gcm1. J Biol Chem. 2008;283:5460–5.PubMed CrossRef
  87.Schreiber J, Riethmacher-Sonnenberg E, Riethmacher D, Tuerk EE, Enderich J, Bösl MR, Wegner M. Placental failure in mice lacking the mammalian homolog of glial cells missing, GCMa. Mol Cell Biol. 2000;20:2466–74.PubMedCentral PubMed CrossRef
  88.Mangeney M, Renard M, Schlecht-Louf G, Bouallaga I, Heidmann O, Letzelter C, Richaud A, Ducos B, Heidmann T. Placental syncytins: genetic disjunction between the fusogenic and immunosuppressive activity of retroviral envelope proteins. Proc Natl Acad Sci USA. 2007;104:20534–9.PubMedCentral PubMed CrossRef
  89.Wooding FB, Beckers JF. Trinucleate cells and the ultrastructural localization of bovine placental lactogen. Cell Tissue Res. 1987;247:667–73.PubMed CrossRef
  90.Dunlap KA, Palmarini M, Varela M, Burghardt RC, Hayashi K, Farmer JL, Spencer TE. Endogenous retroviruses regulate periimplantation placental growth and differentiation. Proc Natl Acad Sci USA. 2006;103:14390–5.PubMedCentral PubMed CrossRef
  91.Baba K, Nakaya Y, Shojima T, Muroi Y, Kizaki K, Hashizume K, Imakawa K, Miyazawa T. Identification of novel endogenous betaretroviruses which are transcribed in the bovine placenta. J Virol. 2011;85:1237–45.PubMedCentral PubMed CrossRef
  92.Nakaya Y, Koshi K, Nakagawa S, Hashizume K, Miyazawa T. Fematrin-1 is involved in fetomaternal cell-to-cell fusion in Bovinae placenta and has contributed to diversity of ruminant placentation. J Virol. 2013;87:10563–72.PubMedCentral PubMed CrossRef
  93.Wooding FB. Current topic: the synepitheliochorial placenta of ruminants: binucleate cell fusions and hormone production. Placenta. 1992;13:101–13.PubMed CrossRef
  94.Carter AM. Evolution of placental structure and function in ruminants. In: Juengel JE, Miyamoto A, Price C, Reynolds LP, Smith MF, Webb R, editors. Reproduction in domestic ruminants VIII. England: Context Products Ltd. 2014. p. 387–99.
  95.Nakagawa S, Bai H, Sakurai T, Nakaya Y, Konno T, Miyazawa T, Gojobori T, Imakawa K. Dynamic evolution of endogenous retrovirus-derived genes expressed in bovine conceptuses during the period of placentation. Genome Biol Evol. 2013;5:296–306.PubMedCentral PubMed CrossRef
  96.Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A, Ratajczak MZ. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia. 2006;20:1487–95.PubMed CrossRef
  97.Rechavi O, Goldstein I, Kloog Y. Intercellular exchange of proteins: the immune cell habit of sharing. FEBS Lett. 2009;583:1792–9.PubMed CrossRef
  98.Mincheva-Nilsson L, Baranov V. Placenta-derived exosomes and syncytiotrophoblast microparticles and their role in human reproduction: immune modulation for pregnancy success. Am J Reprod Immunol. 2014;72:440–57.PubMed CrossRef
  99.Witwer KW, Buzás EI, Bemis LT, Bora A, Lässer C, Lötvall J, Nolte-’t Hoen EN, Piper MG, Sivaraman S, Skog J, Théry C, Wauben MH, Hochberg F. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles. 2013;2:20360.
  100.Mincheva-Nilsson L, Baranov V. The role of placental exosomes in reproduction. Am J Reprod Immunol. 2010;63:520–33.PubMed CrossRef
  101.Vlassov AV, Magdaleno S, Setterquist R, Conrad R. Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim Biophys Acta. 2012;820:940–8.CrossRef
  102.Gong R, Peng X, Kang S, Feng H, Huang J, Zhang W, Lin D, Tien P, Xiao G. Structural characterization of the fusion core in syncytin, envelope protein of human endogenous retrovirus family W. Biochem Biophys Res Commun. 2005;331:1193–200.PubMed CrossRef
  103.Record M. Intercellular communication by exosomes in placenta: a possible role in cell fusion? Placenta. 2014;35:297–302.PubMed CrossRef
  104.Laulagnier K, Grand D, Dujardin A, Hamdi S, Vincent-Schneider H, Lankar D, Salles JP, Bonnerot C, Perret B, Record M. PLD2 is enriched on exosomes and its activity is correlated to the release of exosomes. FEBS Lett. 2004;572:11–4.PubMed CrossRef
  105.Record M, Subra C, Silvente-Poirot S, Poirot M. Exosomes as intercellular signalosomes and pharmacological effectors. Biochem Pharmacol. 2011;81:1171–82.PubMed CrossRef
  106.Huppertz B, Borges M. Placenta trophoblast fusion. Methods Mol Biol. 2008;475:135–47.PubMed CrossRef
  107.Record M. Exosomal lipids in cell–cell communication. In: Zhang H-G, editor. Emerging concepts of tumor exosome-mediated cell–cell communication. USA: Springer; 2012. p. 47–68.
  
• 作者单位：Kazuhiko Imakawa (1)
  Rulan Bai (1)
  Hiroshi Fujiwara (2)
  Kazuya Kusama (1)
  
  1. Laboratory of Theriogenology and Animal Breeding, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo, 113-8657, Japan
  2. Department of Obstetrics and Gynecology, Graduate School of Medicine Science, Kanazawa University, Kanazawa, 920-1192, Japan
  
• 刊物主题：Reproductive Medicine; Gynecology; Urology/Andrology;
• 出版者：Springer Japan
• ISSN：1447-0578

文摘

Processes of conceptus implantation and placentation, unique to mammalian reproduction, have been extensively studied. It was once thought that processes of these events varied greatly, notably between invasive and noninvasive modes of implantation and/or placentation. Regardless of the mode of implantation, however, physiological and biochemical processes in conceptus implantation to the maternal endometrium including the kinds of gene expression and their products are now considered not to differ so much. Recent progress has identified that in addition to the hormones, cytokines, proteases and cell adhesion molecules classically characterized, epithelial–mesenchymal transition, molecules related to lymphocyte homing, the expression of endogenous retroviruses and possibly exosomes are all required for the progression of conceptus implantation to placentation. In this review, therefore, new findings related to these events are integrated into the context of conceptus implantation to the maternal endometrium. Keywords EMT ERV Exosome Gene expression Implantation