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Published in: Journal of Assisted Reproduction and Genetics 2/2019

01-02-2019 | Review

Extracellular vesicle mediated embryo-endometrial cross talk during implantation and in pregnancy

Authors: Noble K. Kurian, Deepak Modi

Published in: Journal of Assisted Reproduction and Genetics | Issue 2/2019

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Abstract

Extracellular vesicles are lipoproteinaceous membrane-enclosed nanometer-sized structures produced by cells and are thought to mediate cellular communications. Loaded with a specific set of miRNA and protein depending on their tissue of origin, these extracellular vesicles modulate diverse set of biological processes in their target tissues. In recent years, data has gathered on the roles of extracellular vesicles in embryo implantation and pregnancy. Embryo, oviduct, endometrial epithelium and stroma/decidua derived vesicles interact with trophoblast cells and promote their growth and differentiation to aid in embryo implantation. The placental vesicles are detected in maternal circulation that aids in feto-maternal immune tolerance, their levels vary in women with pregnancy-related complications like preeclampsia. Beyond the host, the microbes in the genital tract are also reported to produce extracellular vesicles which are thought to be responsible for inflammation and preterm births. This review focuses on the extracellular vesicular trafficking involved in success of pregnancy.
Literature
1.
go back to reference Modi DN, Godbole G, Suman P, Gupta SK. Endometrial biology during trophoblast invasion. Front Biosci (Schol Ed). 2012;4:1151–71. Modi DN, Godbole G, Suman P, Gupta SK. Endometrial biology during trophoblast invasion. Front Biosci (Schol Ed). 2012;4:1151–71.
2.
go back to reference Modi DN, Bhartiya P. Physiology of embryo-endometrial cross talk. Biomed Res J. 2015;2(1):83–104.CrossRef Modi DN, Bhartiya P. Physiology of embryo-endometrial cross talk. Biomed Res J. 2015;2(1):83–104.CrossRef
3.
go back to reference Ashary N, Tiwari A, Modi D. Embryo implantation: war in times of love. Endocrinology. 2018;159(2):1188–98.PubMedCrossRef Ashary N, Tiwari A, Modi D. Embryo implantation: war in times of love. Endocrinology. 2018;159(2):1188–98.PubMedCrossRef
4.
go back to reference Bhusane K, Bhutada S, Chaudhari U, Savardekar L, Katkam R, Sachdeva G. Secrets of endometrial receptivity: some are hidden in uterine secretome. Am J Reprod Immunol. 2016;75(3):226–36.PubMedCrossRef Bhusane K, Bhutada S, Chaudhari U, Savardekar L, Katkam R, Sachdeva G. Secrets of endometrial receptivity: some are hidden in uterine secretome. Am J Reprod Immunol. 2016;75(3):226–36.PubMedCrossRef
5.
go back to reference Evans J, Salamonsen LA, Winship A, Menkhorst E, Nie G, Gargett CE, et al. Fertile ground: human endometrial programming and lessons in health and disease. Nat Rev Endocrinol. 2016;12(11):654–67.PubMedCrossRef Evans J, Salamonsen LA, Winship A, Menkhorst E, Nie G, Gargett CE, et al. Fertile ground: human endometrial programming and lessons in health and disease. Nat Rev Endocrinol. 2016;12(11):654–67.PubMedCrossRef
6.
go back to reference Shah J, Gangadharan A, Shah V. Effect of intrauterine instillation of granulocyte colony-stimulating factor on endometrial thickness and clinical pregnancy rate in women undergoing in vitro fertilization cycles: an observational cohort study. Int J Infertil Fetal Med. 2014;5(3):100–6.CrossRef Shah J, Gangadharan A, Shah V. Effect of intrauterine instillation of granulocyte colony-stimulating factor on endometrial thickness and clinical pregnancy rate in women undergoing in vitro fertilization cycles: an observational cohort study. Int J Infertil Fetal Med. 2014;5(3):100–6.CrossRef
8.
go back to reference Godbole G, Suman P, Malik A, Galvankar M, Joshi N, Fazleabas A, et al. Decrease in expression of HOXA10 in the decidua after embryo implantation promotes trophoblast invasion. Endocrinology. 2017;158(8):2618–33.PubMedPubMedCentralCrossRef Godbole G, Suman P, Malik A, Galvankar M, Joshi N, Fazleabas A, et al. Decrease in expression of HOXA10 in the decidua after embryo implantation promotes trophoblast invasion. Endocrinology. 2017;158(8):2618–33.PubMedPubMedCentralCrossRef
9.
go back to reference Sharma S, Godbole G, Modi D. Decidual control of trophoblast invasion. Am J Reprod Immunol. 2016;75(3):341–50.PubMedCrossRef Sharma S, Godbole G, Modi D. Decidual control of trophoblast invasion. Am J Reprod Immunol. 2016;75(3):341–50.PubMedCrossRef
10.
go back to reference James-Allan LB, Whitley GS, Leslie K, Wallace AE, Cartwright JE. Decidual cell regulation of trophoblast is altered in pregnancies at risk of pre-eclampsia. J Mol Endocrinol. 2018;60(3):239–46.PubMedPubMedCentralCrossRef James-Allan LB, Whitley GS, Leslie K, Wallace AE, Cartwright JE. Decidual cell regulation of trophoblast is altered in pregnancies at risk of pre-eclampsia. J Mol Endocrinol. 2018;60(3):239–46.PubMedPubMedCentralCrossRef
11.
go back to reference Garrido-Gomez T, Dominguez F, Quiñonero A, Diaz-Gimeno P, Kapidzic M, Gormley M, et al. Defective decidualization during and after severe preeclampsia reveals a possible maternal contribution to the etiology. Proc Natl Acad Sci U S A. 2017;114(40):E8468–77.PubMedPubMedCentralCrossRef Garrido-Gomez T, Dominguez F, Quiñonero A, Diaz-Gimeno P, Kapidzic M, Gormley M, et al. Defective decidualization during and after severe preeclampsia reveals a possible maternal contribution to the etiology. Proc Natl Acad Sci U S A. 2017;114(40):E8468–77.PubMedPubMedCentralCrossRef
12.
go back to reference MikoŁaj P, Balaj ZL, Breakefield XO, Lai CP. Extracellular vesicles: composition, biological relevance, and methods of study. Bioscience. 2015;65(8):783–97.CrossRef MikoŁaj P, Balaj ZL, Breakefield XO, Lai CP. Extracellular vesicles: composition, biological relevance, and methods of study. Bioscience. 2015;65(8):783–97.CrossRef
13.
go back to reference Laulagnier K, Motta C, Hamdi S, Sébastien ROY, Fauvelle F, Pageaux JF, et al. Mast cell-and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem J. 2004;380(1):161–71.PubMedPubMedCentralCrossRef Laulagnier K, Motta C, Hamdi S, Sébastien ROY, Fauvelle F, Pageaux JF, et al. Mast cell-and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem J. 2004;380(1):161–71.PubMedPubMedCentralCrossRef
14.
go back to reference Llorente A, Skotland T, Sylvänne T, Kauhanen D, Róg T, Orłowski A, et al. Molecular lipidomics of exosomes released by PC-3 prostate cancer cells. Biochim Biophys Acta. 2013;1831:1302–9.PubMedCrossRef Llorente A, Skotland T, Sylvänne T, Kauhanen D, Róg T, Orłowski A, et al. Molecular lipidomics of exosomes released by PC-3 prostate cancer cells. Biochim Biophys Acta. 2013;1831:1302–9.PubMedCrossRef
15.
go back to reference Mellisho EA, Velásquez AE, Nuñez MJ, Cabezas JG, Cueto JA, Fader C, et al. Identification and characteristics of extracellular vesicles from bovine blastocysts produced in vitro. PLoS One. 2017;12(5):e0178306.PubMedPubMedCentralCrossRef Mellisho EA, Velásquez AE, Nuñez MJ, Cabezas JG, Cueto JA, Fader C, et al. Identification and characteristics of extracellular vesicles from bovine blastocysts produced in vitro. PLoS One. 2017;12(5):e0178306.PubMedPubMedCentralCrossRef
16.
go back to reference Giacomini E, Vago R, Sanchez AM, Podini P, Zarovni N, Murdica V, et al. Secretome of in vitro cultured human embryos contains extracellular vesicles that are uptaken by the maternal side. Sci Rep. 2017;7(1):5210.PubMedPubMedCentralCrossRef Giacomini E, Vago R, Sanchez AM, Podini P, Zarovni N, Murdica V, et al. Secretome of in vitro cultured human embryos contains extracellular vesicles that are uptaken by the maternal side. Sci Rep. 2017;7(1):5210.PubMedPubMedCentralCrossRef
17.
go back to reference Qu P, Qing S, Liu R, Qin H, Wang W, Qiao F, et al. Effects of embryo-derived exosomes on the development of bovine cloned embryos. PLoS One. 2017;12(3):e0174535.PubMedPubMedCentralCrossRef Qu P, Qing S, Liu R, Qin H, Wang W, Qiao F, et al. Effects of embryo-derived exosomes on the development of bovine cloned embryos. PLoS One. 2017;12(3):e0174535.PubMedPubMedCentralCrossRef
18.
go back to reference Desrochers LM, Bordeleau F, Reinhart-King CA, Cerione RA, Antonyak MA. Microvesicles provide a mechanism for intercellular communication by embryonic stem cells during embryo implantation. Nat Commun. 2016;7:11958.PubMedPubMedCentralCrossRef Desrochers LM, Bordeleau F, Reinhart-King CA, Cerione RA, Antonyak MA. Microvesicles provide a mechanism for intercellular communication by embryonic stem cells during embryo implantation. Nat Commun. 2016;7:11958.PubMedPubMedCentralCrossRef
19.
go back to reference Burns GW, Brooks KE, Spencer TE. Extracellular vesicles originate from the conceptus and uterus during early pregnancy in sheep. Biol Reprod. 2016;94:56.PubMedCrossRef Burns GW, Brooks KE, Spencer TE. Extracellular vesicles originate from the conceptus and uterus during early pregnancy in sheep. Biol Reprod. 2016;94:56.PubMedCrossRef
20.
go back to reference Capalbo A, Ubaldi FM, Cimadomo D, Noli L, Khalaf Y, Farcomeni A, et al. MicroRNAs in spent blastocyst culture medium are derived from trophectoderm cells and can be explored for human embryo reproductive competence assessment. Fertil Steril. 2016;105:225–35.PubMedCrossRef Capalbo A, Ubaldi FM, Cimadomo D, Noli L, Khalaf Y, Farcomeni A, et al. MicroRNAs in spent blastocyst culture medium are derived from trophectoderm cells and can be explored for human embryo reproductive competence assessment. Fertil Steril. 2016;105:225–35.PubMedCrossRef
21.
go back to reference Cuman C, Van Sinderen M, Gantier MP, Rainczuk K, Sorby K, Rombauts L, et al. Human blastocyst secreted microRNA regulate endometrial epithelial cell adhesion. EBioMedicine. 2015;2:1528–35.PubMedPubMedCentralCrossRef Cuman C, Van Sinderen M, Gantier MP, Rainczuk K, Sorby K, Rombauts L, et al. Human blastocyst secreted microRNA regulate endometrial epithelial cell adhesion. EBioMedicine. 2015;2:1528–35.PubMedPubMedCentralCrossRef
23.
go back to reference Noli L, Capalbo A, Dajani Y, Cimadomo D, Bvumbe J, Rienzi L, et al. Human embryos created by embryo splitting secrete significantly lower levels of miRNA-30c. Stem Cells Dev. 2016;25:1853–62.PubMedPubMedCentralCrossRef Noli L, Capalbo A, Dajani Y, Cimadomo D, Bvumbe J, Rienzi L, et al. Human embryos created by embryo splitting secrete significantly lower levels of miRNA-30c. Stem Cells Dev. 2016;25:1853–62.PubMedPubMedCentralCrossRef
24.
go back to reference Rosenbluth EM, Shelton DN, Wells LM, Sparks AE, Van Voorhis BJ. Human embryos secrete microRNAs into culture media–a potential biomarker for implantation. Fertil Steril. 2014;101:1493–500.PubMedCrossRef Rosenbluth EM, Shelton DN, Wells LM, Sparks AE, Van Voorhis BJ. Human embryos secrete microRNAs into culture media–a potential biomarker for implantation. Fertil Steril. 2014;101:1493–500.PubMedCrossRef
25.
go back to reference Pérez-Cerezales S, Ramos-Ibeas P, Acuña OS, Avilés M, Coy P, Rizos D, et al. The oviduct: from sperm selection to the epigenetic landscape of the embryo. Biol Reprod. 2017;98(3):262–76.CrossRef Pérez-Cerezales S, Ramos-Ibeas P, Acuña OS, Avilés M, Coy P, Rizos D, et al. The oviduct: from sperm selection to the epigenetic landscape of the embryo. Biol Reprod. 2017;98(3):262–76.CrossRef
26.
go back to reference Al-Dossary AA, Strehler EE, Martin-DeLeon PA. Expression and secretion of plasma membrane Ca2+-ATPase 4a (PMCA4a) during murine estrus: association with oviductal exosomes and uptake in sperm. PLoS One. 2013;8(11):e80181.PubMedPubMedCentralCrossRef Al-Dossary AA, Strehler EE, Martin-DeLeon PA. Expression and secretion of plasma membrane Ca2+-ATPase 4a (PMCA4a) during murine estrus: association with oviductal exosomes and uptake in sperm. PLoS One. 2013;8(11):e80181.PubMedPubMedCentralCrossRef
27.
go back to reference Almiñana C, Corbin E, Tsikis G, Alcântara-Neto AS, Labas V, Reynaud K, et al. Oviduct extracellular vesicles protein content and their role during oviduct–embryo cross-talk. Reproduction. 2017;154(3):253–68.CrossRef Almiñana C, Corbin E, Tsikis G, Alcântara-Neto AS, Labas V, Reynaud K, et al. Oviduct extracellular vesicles protein content and their role during oviduct–embryo cross-talk. Reproduction. 2017;154(3):253–68.CrossRef
28.
go back to reference Lopera-Vásquez R, Hamdi M, Fernandez-Fuertes B, Maillo V, Beltrán-Breña P, Calle A, et al. Extracellular vesicles from BOEC in in vitro embryo development and quality. PLoS One. 2016;11(2):e0148083.PubMedPubMedCentralCrossRef Lopera-Vásquez R, Hamdi M, Fernandez-Fuertes B, Maillo V, Beltrán-Breña P, Calle A, et al. Extracellular vesicles from BOEC in in vitro embryo development and quality. PLoS One. 2016;11(2):e0148083.PubMedPubMedCentralCrossRef
29.
go back to reference Godbole G, Suman P, Gupta SK, Modi D. Decidualized endometrial stromal cell derived factors promote trophoblast invasion. Fertil Steril. 2011;95(4):1278–83.PubMedCrossRef Godbole G, Suman P, Gupta SK, Modi D. Decidualized endometrial stromal cell derived factors promote trophoblast invasion. Fertil Steril. 2011;95(4):1278–83.PubMedCrossRef
30.
go back to reference Zhu XM, Han T, Sargent IL, Wang YL, Yao YQ. Conditioned medium from human decidual stromal cells has a concentration-dependent effect on trophoblast cell invasion. Placenta. 2009;30(1):74–8.PubMedCrossRef Zhu XM, Han T, Sargent IL, Wang YL, Yao YQ. Conditioned medium from human decidual stromal cells has a concentration-dependent effect on trophoblast cell invasion. Placenta. 2009;30(1):74–8.PubMedCrossRef
31.
go back to reference Greening DW, Nguyen HP, Elgass K, Simpson RJ, Salamonsen LA. Human endometrial exosomes contain hormone-specific cargo modulating trophoblast adhesive capacity: insights into endometrial-embryo interactions. Biol Reprod. 2016;94:38.PubMedCrossRef Greening DW, Nguyen HP, Elgass K, Simpson RJ, Salamonsen LA. Human endometrial exosomes contain hormone-specific cargo modulating trophoblast adhesive capacity: insights into endometrial-embryo interactions. Biol Reprod. 2016;94:38.PubMedCrossRef
32.
go back to reference Ng YH, Rome S, Jalabert A, Forterre A, Singh H, Hincks CL, et al. Endometrial exosomes/microvesicles in the uterine microenvironment: a new paradigm for embryo-endometrial cross talk at implantation. PLoS One. 2013;8:e58502.PubMedPubMedCentralCrossRef Ng YH, Rome S, Jalabert A, Forterre A, Singh H, Hincks CL, et al. Endometrial exosomes/microvesicles in the uterine microenvironment: a new paradigm for embryo-endometrial cross talk at implantation. PLoS One. 2013;8:e58502.PubMedPubMedCentralCrossRef
33.
go back to reference Kusama K, Nakamura K, Bai R, Nagaoka K, Sakurai T, Imakawa K. Intrauterine exosomes are required for bovine conceptus implantation. Biochem Biophys Res Commun. 2018;495(1):1370–5.PubMedCrossRef Kusama K, Nakamura K, Bai R, Nagaoka K, Sakurai T, Imakawa K. Intrauterine exosomes are required for bovine conceptus implantation. Biochem Biophys Res Commun. 2018;495(1):1370–5.PubMedCrossRef
34.
go back to reference Nguyen MA, Karunakaran D, Geoffrion M, Cheng HS, Tandoc K, Matic LP, et al. Extracellular vesicles secreted by atherogenic macrophages transfer microRNA to inhibit cell migration. Arterioscler Thromb Vasc Biol. 2018;38(1):49–63.PubMedCrossRef Nguyen MA, Karunakaran D, Geoffrion M, Cheng HS, Tandoc K, Matic LP, et al. Extracellular vesicles secreted by atherogenic macrophages transfer microRNA to inhibit cell migration. Arterioscler Thromb Vasc Biol. 2018;38(1):49–63.PubMedCrossRef
35.
go back to reference Patil VS, Sachdeva G, Modi DN, Katkam RR, Manjramkar DD, Hinduja I, et al. Rab coupling protein (RCP): a novel target of progesterone action in primate endometrium. J Clin Mol Endocrinol. 2005;35(2):357–72.CrossRef Patil VS, Sachdeva G, Modi DN, Katkam RR, Manjramkar DD, Hinduja I, et al. Rab coupling protein (RCP): a novel target of progesterone action in primate endometrium. J Clin Mol Endocrinol. 2005;35(2):357–72.CrossRef
36.
go back to reference Rosas C, Gabler F, Vantman D, Romero C, Vega M. Levels of Rabs and WAVE family proteins associated with translocation of GLUT4 to the cell surface in endometria from hyperinsulinemic PCOS women. Hum Reprod. 2010;25(11):2870–7.PubMedCrossRef Rosas C, Gabler F, Vantman D, Romero C, Vega M. Levels of Rabs and WAVE family proteins associated with translocation of GLUT4 to the cell surface in endometria from hyperinsulinemic PCOS women. Hum Reprod. 2010;25(11):2870–7.PubMedCrossRef
37.
go back to reference Koh YQ, Peiris HN, Vaswani K, Reed S, Rice GE, Salomon C, et al. Characterization of exosomal release in bovine endometrial intercaruncular stromal cells. Reprod Biol Endocrinol. 2016;14(1):78.PubMedPubMedCentralCrossRef Koh YQ, Peiris HN, Vaswani K, Reed S, Rice GE, Salomon C, et al. Characterization of exosomal release in bovine endometrial intercaruncular stromal cells. Reprod Biol Endocrinol. 2016;14(1):78.PubMedPubMedCentralCrossRef
38.
go back to reference Harp D, Driss A, Mehrabi S, Chowdhury I, Xu W, Liu D, et al. Exosomes derived from endometriotic stromal cells have enhanced angiogenic effects in vitro. Cell Tissue Res. 2016;365(1):187–96.PubMedPubMedCentralCrossRef Harp D, Driss A, Mehrabi S, Chowdhury I, Xu W, Liu D, et al. Exosomes derived from endometriotic stromal cells have enhanced angiogenic effects in vitro. Cell Tissue Res. 2016;365(1):187–96.PubMedPubMedCentralCrossRef
39.
go back to reference Maida Y, Takakura M, Nishiuchi T, Yoshimoto T, Kyo S. Exosomal transfer of functional small RNAs mediates cancer-stroma communication in human endometrium. Cancer Med. 2016;5(2):304–14.PubMedCrossRef Maida Y, Takakura M, Nishiuchi T, Yoshimoto T, Kyo S. Exosomal transfer of functional small RNAs mediates cancer-stroma communication in human endometrium. Cancer Med. 2016;5(2):304–14.PubMedCrossRef
40.
go back to reference Zhang J, Li S, Li L, Li M, Guo C, Yao J, et al. Exosome and exosomal microRNA: trafficking, sorting, and function. Genomics Proteomics Bioinformatics. 2015;13(1):17–24.PubMedPubMedCentralCrossRef Zhang J, Li S, Li L, Li M, Guo C, Yao J, et al. Exosome and exosomal microRNA: trafficking, sorting, and function. Genomics Proteomics Bioinformatics. 2015;13(1):17–24.PubMedPubMedCentralCrossRef
41.
go back to reference Burton GJ, Jones CJ. Syncytial knots, sprouts, apoptosis, and trophoblast deportation from the human placenta. Taiwan J Obstet Gynecol. 2009;48(1):28–37.PubMedCrossRef Burton GJ, Jones CJ. Syncytial knots, sprouts, apoptosis, and trophoblast deportation from the human placenta. Taiwan J Obstet Gynecol. 2009;48(1):28–37.PubMedCrossRef
42.
go back to reference Salomon C, Yee SW, Mitchell MD, Rice GE. The possible role of extravillous trophoblast-derived exosomes on the uterine spiral arterial remodeling under both normal and pathological conditions. Biomed Res Int. 2014;2014:1–10.CrossRef Salomon C, Yee SW, Mitchell MD, Rice GE. The possible role of extravillous trophoblast-derived exosomes on the uterine spiral arterial remodeling under both normal and pathological conditions. Biomed Res Int. 2014;2014:1–10.CrossRef
43.
go back to reference Adam S, Elfeky O, Kinhal V, Dutta S, Lai A, Jayabalan N, et al. Fetal-maternal communication via extracellular vesicles–implications for complications of pregnancies. Placenta. 2017;54:83–8.PubMedCrossRef Adam S, Elfeky O, Kinhal V, Dutta S, Lai A, Jayabalan N, et al. Fetal-maternal communication via extracellular vesicles–implications for complications of pregnancies. Placenta. 2017;54:83–8.PubMedCrossRef
44.
go back to reference Tannetta D, Collett G, Vatish M, Redman C, Sargent I. Syncytiotrophoblast extracellular vesicles–circulating biopsies reflecting placental health. Placenta. 2017a;52:134–8.PubMedPubMedCentralCrossRef Tannetta D, Collett G, Vatish M, Redman C, Sargent I. Syncytiotrophoblast extracellular vesicles–circulating biopsies reflecting placental health. Placenta. 2017a;52:134–8.PubMedPubMedCentralCrossRef
45.
go back to reference Tannetta D, Masliukaite I, Vatish M, Redman C, Sargent I. Update of syncytiotrophoblast derived extracellular vesicles in normal pregnancy and preeclampsia. J Reprod Immunol. 2017b;119:98–106.PubMedCrossRef Tannetta D, Masliukaite I, Vatish M, Redman C, Sargent I. Update of syncytiotrophoblast derived extracellular vesicles in normal pregnancy and preeclampsia. J Reprod Immunol. 2017b;119:98–106.PubMedCrossRef
46.
47.
go back to reference Truong G, Guanzon D, Kinhal V, Elfeky O, Lai A, Longo S, et al. Oxygen tension regulates the miRNA profile and bioactivity of exosomes released from extravillous trophoblast cells–liquid biopsies for monitoring complications of pregnancy. PLoS One. 2017;12(3):e0174514.PubMedPubMedCentralCrossRef Truong G, Guanzon D, Kinhal V, Elfeky O, Lai A, Longo S, et al. Oxygen tension regulates the miRNA profile and bioactivity of exosomes released from extravillous trophoblast cells–liquid biopsies for monitoring complications of pregnancy. PLoS One. 2017;12(3):e0174514.PubMedPubMedCentralCrossRef
48.
go back to reference Salomon C, Guanzon D, Scholz-Romero K, Longo S, Correa P, Illanes SE, et al. Placental exosomes as early biomarker of preeclampsia: potential role of exosomal microRNAs across gestation. J Clin Endocrinol Metab. 2017;102(9):3182–94.PubMedCrossRef Salomon C, Guanzon D, Scholz-Romero K, Longo S, Correa P, Illanes SE, et al. Placental exosomes as early biomarker of preeclampsia: potential role of exosomal microRNAs across gestation. J Clin Endocrinol Metab. 2017;102(9):3182–94.PubMedCrossRef
49.
go back to reference Jayabalan N, Nair S, Nuzhat Z, Rice GE, Zuñiga FA, Sobrevia L, et al. Cross talk between adipose tissue and placenta in obese and gestational diabetes mellitus pregnancies via exosomes. Front Endocrinol. 2017;8:239.CrossRef Jayabalan N, Nair S, Nuzhat Z, Rice GE, Zuñiga FA, Sobrevia L, et al. Cross talk between adipose tissue and placenta in obese and gestational diabetes mellitus pregnancies via exosomes. Front Endocrinol. 2017;8:239.CrossRef
50.
go back to reference Sáez T, Salsoso R, Leiva A, Toledo F, de Vos P, Faas M, et al. Human umbilical vein endothelium-derived exosomes play a role in foetoplacental endothelial dysfunction in gestational diabetes mellitus. Biochim Biophys Acta Mol Basis Dis. 2018;1864(2):499–508.PubMedCrossRef Sáez T, Salsoso R, Leiva A, Toledo F, de Vos P, Faas M, et al. Human umbilical vein endothelium-derived exosomes play a role in foetoplacental endothelial dysfunction in gestational diabetes mellitus. Biochim Biophys Acta Mol Basis Dis. 2018;1864(2):499–508.PubMedCrossRef
51.
go back to reference Sáez T, de Vos P, Sobrevia L, Faas MM. Is there a role for exosomes in foetoplacental endothelial dysfunction in gestational diabetes mellitus? Placenta. 2018;61:48–54.PubMedCrossRef Sáez T, de Vos P, Sobrevia L, Faas MM. Is there a role for exosomes in foetoplacental endothelial dysfunction in gestational diabetes mellitus? Placenta. 2018;61:48–54.PubMedCrossRef
52.
go back to reference Ying W, Riopel M, Bandyopadhyay G, Dong Y, Birmingham A, Seo JB, et al. Adipose tissue macrophage-derived exosomal miRNAs can modulate in vivo and in vitro insulin sensitivity. Cell. 2017;171(2):372–84.PubMedCrossRef Ying W, Riopel M, Bandyopadhyay G, Dong Y, Birmingham A, Seo JB, et al. Adipose tissue macrophage-derived exosomal miRNAs can modulate in vivo and in vitro insulin sensitivity. Cell. 2017;171(2):372–84.PubMedCrossRef
53.
go back to reference Zhang Y, Yu M, Tian W. Physiological and pathological impact of exosomes of adipose tissue. Cell Proliferat. 2016;49(1):3–13.CrossRef Zhang Y, Yu M, Tian W. Physiological and pathological impact of exosomes of adipose tissue. Cell Proliferat. 2016;49(1):3–13.CrossRef
54.
go back to reference Pelzer ES, Willner D, Buttini M, Hafner LM, Theodoropoulos C, Huygens F. The fallopian tube microbiome: implications for reproductive health. Oncotarget. 2018;9(30):21541.PubMedPubMedCentralCrossRef Pelzer ES, Willner D, Buttini M, Hafner LM, Theodoropoulos C, Huygens F. The fallopian tube microbiome: implications for reproductive health. Oncotarget. 2018;9(30):21541.PubMedPubMedCentralCrossRef
55.
go back to reference Champer M, Wong AM, Champer J, Brito IL, Messer PW, Hou JY, et al. The role of the vaginal microbiome in gynecological cancer: a review. BJOG. 2017. Champer M, Wong AM, Champer J, Brito IL, Messer PW, Hou JY, et al. The role of the vaginal microbiome in gynecological cancer: a review. BJOG. 2017.
56.
go back to reference Younes JA, Lievens E, Hummelen R, van der Westen R, Reid G, Petrova MI. Women and their microbes: the unexpected friendship. Trends Microbiol. 2017. Younes JA, Lievens E, Hummelen R, van der Westen R, Reid G, Petrova MI. Women and their microbes: the unexpected friendship. Trends Microbiol. 2017.
57.
go back to reference Vinturache AE, Gyamfi-Bannerman C, Hwang J, Mysorekar IU, Jacobsson B. Maternal microbiome–a pathway to preterm birth. Semin Fetal Neonatal Med. 2016;21(2):94–9.PubMedCrossRef Vinturache AE, Gyamfi-Bannerman C, Hwang J, Mysorekar IU, Jacobsson B. Maternal microbiome–a pathway to preterm birth. Semin Fetal Neonatal Med. 2016;21(2):94–9.PubMedCrossRef
58.
go back to reference Ofir-Birin Y, Heidenreich M, Regev-Rudzki N. Pathogen-derived extracellular vesicles coordinate social behaviour and host manipulation. Semin Cell Dev Biol. 2017;67:83–90.PubMedCrossRef Ofir-Birin Y, Heidenreich M, Regev-Rudzki N. Pathogen-derived extracellular vesicles coordinate social behaviour and host manipulation. Semin Cell Dev Biol. 2017;67:83–90.PubMedCrossRef
59.
go back to reference Nudel K, Massari P, Genco CA. Neisseria gonorrhoeae modulates cell death in human endocervical epithelial cells through export of exosome-associated cIAP2. Infect Immun. 2015;83(9):3410–7.PubMedPubMedCentralCrossRef Nudel K, Massari P, Genco CA. Neisseria gonorrhoeae modulates cell death in human endocervical epithelial cells through export of exosome-associated cIAP2. Infect Immun. 2015;83(9):3410–7.PubMedPubMedCentralCrossRef
60.
go back to reference Bianchi-Jassir F, Seale AC, Kohli-Lynch M, Lawn JE, Baker CJ, Bartlett L, et al. Preterm birth associated with group B Streptococcus maternal colonization worldwide: systematic review and meta-analyses. Clin Infect Dis. 2017;65(suppl_2):S133–42.PubMedPubMedCentralCrossRef Bianchi-Jassir F, Seale AC, Kohli-Lynch M, Lawn JE, Baker CJ, Bartlett L, et al. Preterm birth associated with group B Streptococcus maternal colonization worldwide: systematic review and meta-analyses. Clin Infect Dis. 2017;65(suppl_2):S133–42.PubMedPubMedCentralCrossRef
61.
go back to reference Surve MV, Anil A, Kamath KG, Bhutda S, Sthanam LK, Pradhan A, Srivastava R, Basu B, Dutta S, Sen S, Modi D, Banerjee A . Membrane vesicles of group B streptococcus disrupt feto-maternal barrier leading to preterm birth. PLoS Pathog 2016; 12(9): e1005816. Surve MV, Anil A, Kamath KG, Bhutda S, Sthanam LK, Pradhan A, Srivastava R, Basu B, Dutta S, Sen S, Modi D, Banerjee A . Membrane vesicles of group B streptococcus disrupt feto-maternal barrier leading to preterm birth. PLoS Pathog 2016; 12(9): e1005816.
62.
go back to reference Vyas N, Walvekar A, Tate D, Lakshmanan V, Bansal D, Cicero AL, et al. Vertebrate hedgehog is secreted on two types of extracellular vesicles with different signaling properties. Sci Rep. 2014;4:7357.PubMedPubMedCentralCrossRef Vyas N, Walvekar A, Tate D, Lakshmanan V, Bansal D, Cicero AL, et al. Vertebrate hedgehog is secreted on two types of extracellular vesicles with different signaling properties. Sci Rep. 2014;4:7357.PubMedPubMedCentralCrossRef
Metadata
Title
Extracellular vesicle mediated embryo-endometrial cross talk during implantation and in pregnancy
Authors
Noble K. Kurian
Deepak Modi
Publication date
01-02-2019
Publisher
Springer US
Published in
Journal of Assisted Reproduction and Genetics / Issue 2/2019
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-018-1343-x

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