Generic placeholder image

Current Drug Metabolism

Editor-in-Chief

ISSN (Print): 1389-2002
ISSN (Online): 1875-5453

Review Article

Exosomes and Female Infertility

Author(s): Xiaoyan Sun, Xiaoling Ma, Xia Yang and Xuehong Zhang*

Volume 20, Issue 10, 2019

Page: [773 - 780] Pages: 8

DOI: 10.2174/1389200220666191015155910

Price: $65

Abstract

Background: Exosomes are small Extracellular Vesicles (EVs) (40-100 nm) secreted by living cells and mediate the transmission of information between cells. The number and contents of exosomes are associated with diseases such as inflammatory diseases, cancer, metabolic diseases and what we are focusing in this passage-female infertility.

Objective: This review focused on the role of exosomes in oocyte development, declined ovarian function, PCOS, uterine diseases, endometrial receptivity and fallopian tube dysfunction in the female.

Methods: We conducted an extensive search for research articles involving relationships between exosomes and female infertility on the bibliographic database.

Results: It has been reported that exosomes can act as a potential therapeutic device to carry cargoes to treat female infertility. However, the pathophysiological mechanisms of exosomes in female infertility have not been entirely elucidated. Further researches are needed to explore the etiology and provide evidence for potential clinical treatment.

Conclusions: This review systematically summarized the role exosomes play in female infertility and its potential as drug delivery.

Keywords: Exosomes, microRNAs, female infertility, oocyte, endometrial receptivity, drug delivery.

Graphical Abstract
[1]
Johnstone, R.M.; Adam, M.; Hammond, J.R.; Orr, L.; Turbide, C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J. Biol. Chem., 1987, 262(19), 9412-9420.
[PMID: 3597417]
[2]
Harding, C.; Heuser, J.; Stahl, P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J. Cell Biol., 1983, 97(2), 329-339.
[http://dx.doi.org/10.1083/jcb.97.2.329] [PMID: 6309857]
[3]
Raposo, G.; Nijman, H.W.; Stoorvogel, W.; Liejendekker, R.; Harding, C.V.; Melief, C.J.; Geuze, H.J. B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med., 1996, 183(3), 1161-1172.
[http://dx.doi.org/10.1084/jem.183.3.1161] [PMID: 8642258]
[4]
Bang, C.; Thum, T. Exosomes: New players in cell-cell communication. Int. J. Biochem. Cell Biol., 2012, 44(11), 2060-2064.
[http://dx.doi.org/10.1016/j.biocel.2012.08.007] [PMID: 22903023]
[5]
Milane, L.; Singh, A.; Mattheolabakis, G.; Suresh, M.; Amiji, M.M. Exosome mediated communication within the tumor microenvironment. J. Control. Release, 2015, 219, 278-294.
[http://dx.doi.org/10.1016/j.jconrel.2015.06.029] [PMID: 26143224]
[6]
Console, L.; Scalise, M.; Indiveri, C. Exosomes in inflammation and role as biomarkers. Clin. Chim. Acta, 2019, 488, 165-171.
[http://dx.doi.org/10.1016/j.cca.2018.11.009] [PMID: 30419221]
[7]
Kahlert, C.; Kalluri, R. Exosomes in tumor microenvironment influence cancer progression and metastasis. J. Mol. Med. (Berl.), 2013, 91(4), 431-437.
[http://dx.doi.org/10.1007/s00109-013-1020-6] [PMID: 23519402]
[8]
da Silveira, J.C.; Veeramachaneni, D.N.; Winger, Q.A.; Carnevale, E.M.; Bouma, G.J. Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: a possible new form of cell communication within the ovarian follicle. Biol. Reprod., 2012, 86(3), 71.
[http://dx.doi.org/10.1095/biolreprod.111.093252] [PMID: 22116803]
[9]
Ng, Y.H.; Rome, S.; Jalabert, A.; Forterre, A.; Singh, H.; Hincks, C.L.; Salamonsen, L.A. Endometrial exosomes/microvesicles in the uterine microenvironment: A new paradigm for embryo-endometrial cross talk at implantation. PLoS One, 2013, 8(3)e58502
[http://dx.doi.org/10.1371/journal.pone.0058502] [PMID: 23516492]
[10]
Fereshteh, Z.; Bathala, P.; Galileo, D.S.; Martin-DeLeon, P.A. Detection of extracellular vesicles in the mouse vaginal fluid: Their delivery of sperm proteins that stimulate capacitation and modulate fertility. J. Cell. Physiol., 2019, 234(8), 12745-12756.
[http://dx.doi.org/10.1002/jcp.27894] [PMID: 30536802]
[11]
Harding, C.; Heuser, J.; Stahl, P. Endocytosis and intracellular processing of transferrin and colloidal gold-transferrin in rat reticulocytes: Demonstration of a pathway for receptor shedding. Eur. J. Cell Biol., 1984, 35(2), 256-263.
[PMID: 6151502]
[12]
Pan, B.T.; Teng, K.; Wu, C.; Adam, M.; Johnstone, R.M. Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J. Cell Biol., 1985, 101(3), 942-948.
[http://dx.doi.org/10.1083/jcb.101.3.942] [PMID: 2993317]
[13]
Raposo, G.; Stoorvogel, W. Extracellular vesicles: Exosomes, microvesicles, and friends. J. Cell Biol., 2013, 200(4), 373-383.
[http://dx.doi.org/10.1083/jcb.201211138] [PMID: 23420871]
[14]
Lawson, C.; Vicencio, J.M.; Yellon, D.M.; Davidson, S.M. Microvesicles and exosomes: New players in metabolic and cardiovascular disease. J. Endocrinol., 2016, 228(2), R57-R71.
[http://dx.doi.org/10.1530/JOE-15-0201] [PMID: 26743452]
[15]
Van Niel, G.; D’Angelo, G.; Raposo, G. Shedding light on the cell biology of extracellular vesicles. Nat. Rev. Mol. Cell Biol., 2018, 19(4), 213-228.
[http://dx.doi.org/10.1038/nrm.2017.125] [PMID: 29339798]
[16]
Cordonnier, M.; Chanteloup, G.; Isambert, N.; Seigneuric, R.; Fumoleau, P.; Garrido, C.; Gobbo, J. Exosomes in cancer theranostic: Diamonds in the rough. Cell Adhes. Migr., 2017, 11(2), 151-163.
[http://dx.doi.org/10.1080/19336918.2016.1250999] [PMID: 28166442]
[17]
Cocucci, E.; Racchetti, G.; Meldolesi, J. Shedding microvesicles: Artefacts no more. Trends Cell Biol., 2009, 19(2), 43-51.
[http://dx.doi.org/10.1016/j.tcb.2008.11.003] [PMID: 19144520]
[18]
Shao, H.; Im, H.; Castro, C.M.; Breakefield, X.; Weissleder, R.; Lee, H. New technologies for analysis of extracellular vesicles. Chem. Rev., 2018, 118(4), 1917-1950.
[http://dx.doi.org/10.1021/acs.chemrev.7b00534] [PMID: 29384376]
[19]
Rekker, K.; Saare, M.; Roost, A.M.; Kubo, A.L.; Zarovni, N.; Chiesi, A.; Salumets, A.; Peters, M. Comparison of serum exosome isolation methods for microRNA profiling. Clin. Biochem., 2014, 47(1-2), 135-138.
[http://dx.doi.org/10.1016/j.clinbiochem.2013.10.020] [PMID: 24183884]
[20]
Lee, K.; Shao, H.; Weissleder, R.; Lee, H. Acoustic purification of extracellular microvesicles. ACS Nano, 2015, 9(3), 2321-2327.
[http://dx.doi.org/10.1021/nn506538f] [PMID: 25672598]
[21]
Zhao, Z.; Yang, Y.; Zeng, Y.; He, M. A microfluidic ExoSearch chip for multiplexed exosome detection towards blood-based ovarian cancer diagnosis. Lab Chip, 2016, 16(3), 489-496.
[http://dx.doi.org/10.1039/C5LC01117E] [PMID: 26645590]
[22]
Kholia, S.; Ranghino, A.; Garnieri, P.; Lopatina, T.; Deregibus, M.C.; Rispoli, P.; Brizzi, M.F.; Camussi, G. Extracellular vesicles as new players in angiogenesis. Vascul. Pharmacol., 2016, 86, 64-70.
[http://dx.doi.org/10.1016/j.vph.2016.03.005] [PMID: 27013016]
[23]
van Niel, G.; Charrin, S.; Simoes, S.; Romao, M.; Rochin, L.; Saftig, P.; Marks, M.S.; Rubinstein, E.; Raposo, G. The tetraspanin CD63 regulates ESCRT-independent and -dependent endosomal sorting during melanogenesis. Dev. Cell, 2011, 21(4), 708-721.
[http://dx.doi.org/10.1016/j.devcel.2011.08.019] [PMID: 21962903]
[24]
Sokolova, V.; Ludwig, A.K.; Hornung, S.; Rotan, O.; Horn, P.A.; Epple, M.; Giebel, B. Characterisation of exosomes derived from human cells by nanoparticle tracking analysis and scanning electron microscopy. Colloids Surf. B Biointerfaces, 2011, 87(1), 146-150.
[http://dx.doi.org/10.1016/j.colsurfb.2011.05.013] [PMID: 21640565]
[25]
Gardiner, C.; Ferreira, Y.J.; Dragovic, R.A.; Redman, C.W.; Sargent, I.L. Extracellular vesicle sizing and enumeration by nanoparticle tracking analysis. J. Extracell. Vesicles, 2013, 2, 2.
[http://dx.doi.org/10.3402/jev.v2i0.19671] [PMID: 24009893]
[26]
Aghajanova, L.; Hoffman, J.; Mok-Lin, E.; Herndon, C.N. Obstetrics and gynecology residency and fertility needs. Reprod. Sci., 2017, 24(3), 428-434.
[http://dx.doi.org/10.1177/1933719116657193] [PMID: 27368879]
[27]
Hanson, B.; Johnstone, E.; Dorais, J.; Silver, B.; Peterson, C.M.; Hotaling, J. Female infertility, infertility-associated diagnoses, and comorbidities: A review. J. Assist. Reprod. Genet., 2017, 34(2), 167-177.
[http://dx.doi.org/10.1007/s10815-016-0836-8] [PMID: 27817040]
[28]
Conforti, A.; Mascia, M.; Cioffi, G.; De Angelis, C.; Coppola, G.; De Rosa, P.; Pivonello, R.; Alviggi, C.; De Placido, G. Air pollution and female fertility: A systematic review of literature. Reprod. Biol. Endocrinol., 2018, 16(1), 117.
[http://dx.doi.org/10.1186/s12958-018-0433-z] [PMID: 30594197]
[29]
Di Pietro, C. Exosome-mediated communication in the ovarian follicle. J. Assist. Reprod. Genet., 2016, 33(3), 303-311.
[http://dx.doi.org/10.1007/s10815-016-0657-9] [PMID: 26814471]
[30]
Machtinger, R.; Laurent, L.C.; Baccarelli, A.A. Extracellular vesicles: Roles in gamete maturation, fertilization and embryo implantation. Hum. Reprod. Update, 2016, 22(2), 182-193.
[PMID: 26663221]
[31]
Revelli, A.; Delle Piane, L.; Casano, S.; Molinari, E.; Massobrio, M.; Rinaudo, P. Follicular fluid content and oocyte quality: From single biochemical markers to metabolomics. Reprod. Biol. Endocrinol., 2009, 7, 40.
[http://dx.doi.org/10.1186/1477-7827-7-40] [PMID: 19413899]
[32]
Martinez, R.M.; Liang, L.; Racowsky, C.; Dioni, L.; Mansur, A.; Adir, M.; Bollati, V.; Baccarelli, A.A.; Hauser, R.; Machtinger, R. Extracellular microRNAs profile in human follicular fluid and IVF outcomes. Sci. Rep., 2018, 8(1), 17036.
[http://dx.doi.org/10.1038/s41598-018-35379-3] [PMID: 30451969]
[33]
Sohel, M.M.; Hoelker, M.; Noferesti, S.S.; Salilew-Wondim, D.; Tholen, E.; Looft, C.; Rings, F.; Uddin, M.J.; Spencer, T.E.; Schellander, K.; Tesfaye, D. Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: Implications for bovine oocyte developmental competence. PLoS One, 2013, 8(11)e78505
[http://dx.doi.org/10.1371/journal.pone.0078505] [PMID: 24223816]
[34]
Santonocito, M.; Vento, M.; Guglielmino, M.R.; Battaglia, R.; Wahlgren, J.; Ragusa, M.; Barbagallo, D.; Borzi, P.; Rizzari, S.; Maugeri, M.; Scollo, P.; Tatone, C.; Valadi, H.; Purrello, M.; Di Pietro, C. Molecular characterization of exosomes and their microRNA cargo in human follicular fluid: Bioinformatic analysis reveals that exosomal microRNAs control pathways involved in follicular maturation. Fertil. Steril., 2014, 102(6), 1751-1761.
[http://dx.doi.org/10.1016/j.fertnstert.2014.08.005] [PMID: 25241362]
[35]
Da Silveira, J.C.; Winger, Q.A.; Bouma, G.J.; Carnevale, E.M. Effects of age on follicular fluid exosomal microRNAs and granulosa cell transforming growth factor-β signalling during follicle development in the mare. Reprod. Fertil. Dev., 2015, 27(6), 897-905.
[http://dx.doi.org/10.1071/RD14452] [PMID: 25945781]
[36]
Hung, W.T.; Hong, X.; Christenson, L.K.; McGinnis, L.K. Extracellular vesicles from bovine follicular fluid support cumulus expansion. Biol. Reprod., 2015, 93(5), 117.
[http://dx.doi.org/10.1095/biolreprod.115.132977] [PMID: 26423123]
[37]
Gross, J.C.; Chaudhary, V.; Bartscherer, K.; Boutros, M. Active Wnt proteins are secreted on exosomes. Nat. Cell Biol., 2012, 14(10), 1036-1045.
[http://dx.doi.org/10.1038/ncb2574] [PMID: 22983114]
[38]
Noferesti, S.S.; Sohel, M.M.; Hoelker, M.; Salilew-Wondim, D.; Tholen, E.; Looft, C.; Rings, F.; Neuhoff, C.; Schellander, K.; Tesfaye, D. Controlled ovarian hyperstimulation induced changes in the expression of circulatory miRNA in bovine follicular fluid and blood plasma. J. Ovarian Res., 2015, 8, 81.
[http://dx.doi.org/10.1186/s13048-015-0208-5] [PMID: 26645573]
[39]
Hung, W.T.; Navakanitworakul, R.; Khan, T.; Zhang, P.; Davis, J.S.; McGinnis, L.K.; Christenson, L.K. Stage-specific follicular extracellular vesicle uptake and regulation of bovine granulosa cell proliferation. Biol. Reprod., 2017, 97(4), 644-655.
[http://dx.doi.org/10.1093/biolre/iox106] [PMID: 29025042]
[40]
Diez-Fraile, A.; Lammens, T.; Tilleman, K.; Witkowski, W.; Verhasselt, B.; De Sutter, P.; Benoit, Y.; Espeel, M.; D’Herde, K. Age-associated differential microRNA levels in human follicular fluid reveal pathways potentially determining fertility and success of in vitro fertilization. Hum. Fertil. (Camb.), 2014, 17(2), 90-98.
[http://dx.doi.org/10.3109/14647273.2014.897006] [PMID: 24684237]
[41]
Machtinger, R.; Rodosthenous, R.S.; Adir, M.; Mansour, A.; Racowsky, C.; Baccarelli, A.A.; Hauser, R. Extracellular microRNAs in follicular fluid and their potential association with oocyte fertilization and embryo quality: An exploratory study. J. Assist. Reprod. Genet., 2017, 34(4), 525-533.
[http://dx.doi.org/10.1007/s10815-017-0876-8] [PMID: 28188594]
[42]
Iwai, M.; Hamatani, T.; Nakamura, A.; Kawano, N.; Kanai, S.; Kang, W.; Yoshii, N.; Odawara, Y.; Yamada, M.; Miyamoto, Y.; Saito, T.; Saito, H.; Miyado, M.; Umezawa, A.; Miyado, K.; Tanaka, M. Membrane protein CD9 is repositioned and released to enhance uterine function. Lab. Invest., 2019, 99(2), 200-209.
[http://dx.doi.org/10.1038/s41374-018-0145-1] [PMID: 30401958]
[43]
Kaji, K.; Oda, S.; Miyazaki, S.; Kudo, A. Infertility of CD9-deficient mouse eggs is reversed by mouse CD9, human CD9, or mouse CD81; polyadenylated mRNA injection developed for molecular analysis of sperm-egg fusion. Dev. Biol., 2002, 247(2), 327-334.
[http://dx.doi.org/10.1006/dbio.2002.0694] [PMID: 12086470]
[44]
Rotterdam ESHRE/ASRM-Sponsored PCOS Consensus Workshop Group. Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome. Fertil. Steril., 2004, 81(1), 19-25.
[http://dx.doi.org/10.1016/j.fertnstert.2003.10.004] [PMID: 14711538]
[45]
Teede, H.J.; Misso, M.L.; Costello, M.F.; Dokras, A.; Laven, J.; Moran, L.; Piltonen, T.; Norman, R.J. Recommendations from the international evidence-based guideline for the assessment and management of polycystic ovary syndrome. Hum. Reprod., 2018, 33(9), 1602-1618.
[http://dx.doi.org/10.1093/humrep/dey256] [PMID: 30052961]
[46]
Joham, A.E.; Boyle, J.A.; Ranasinha, S.; Zoungas, S.; Teede, H.J. Contraception use and pregnancy outcomes in women with polycystic ovary syndrome: data from the Australian longitudinal study on women’s health. Hum. Reprod., 2014, 29(4), 802-808.
[http://dx.doi.org/10.1093/humrep/deu020] [PMID: 24549213]
[47]
Sørensen, A.E.; Wissing, M.L.; Salö, S.; Englund, A.L.; Dalgaard, L.T. MicroRNAs related to Polycystic Ovary Syndrome (PCOS). Genes (Basel), 2014, 5(3), 684-708.
[http://dx.doi.org/10.3390/genes5030684] [PMID: 25158044]
[48]
Sorensen, A.E.; Udesen, P.B.; Wissing, M.L.; Englund, A.L.M.; Dalgaard, L.T. MicroRNAs related to androgen metabolism and polycystic ovary syndrome. Chem. Biol. Interact, 2016, 259(Pt A), 8-16.
[http://dx.doi.org/10.1016/j.cbi.2016.06.008] [PMID: 27270454]
[49]
Wang, L.P.; Peng, X.Y.; Lv, X.Q.; Liu, L.; Li, X.L.; He, X.; Lv, F.; Pan, Y.; Wang, L.; Liu, K.F.; Zhang, X.M. High throughput circRNAs sequencing profile of follicle fluid exosomes of polycystic ovary syndrome patients. J. Cell. Physiol., 2019. Epub ahead of print
[http://dx.doi.org/10.1002/jcp.28201] [PMID: 30779115]
[50]
Koiou, E.; Tziomalos, K.; Katsikis, I.; Kalaitzakis, E.; Kandaraki, E.A.; Tsourdi, E.A.; Delkos, D.; Papadakis, E.; Panidis, D. Circulating platelet-derived microparticles are elevated in women with polycystic ovary syndrome diagnosed with the 1990 criteria and correlate with serum testosterone levels. Eur. J. Endocrinol., 2011, 165(1), 63-68.
[http://dx.doi.org/10.1530/EJE-11-0144] [PMID: 21543377]
[51]
Koiou, E.; Tziomalos, K.; Katsikis, I.; Papadakis, E.; Kandaraki, E.A.; Panidis, D. Platelet-derived microparticles in overweight/obese women with the polycystic ovary syndrome. Gynecol. Endocrinol., 2013, 29(3), 250-253.
[http://dx.doi.org/10.3109/09513590.2012.743005] [PMID: 23216335]
[52]
Carvalho, L.M.L.; Ferreira, C.N.; Sóter, M.O.; Sales, M.F.; Rodrigues, K.F.; Martins, S.R.; Candido, A.L.; Reis, F.M.; Silva, I.F.O.; Campos, F.M.F.; Gomes, K.B. Microparticles: Inflammatory and haemostatic biomarkers in polycystic ovary syndrome. Mol. Cell. Endocrinol., 2017, 443, 155-162.
[http://dx.doi.org/10.1016/j.mce.2017.01.017] [PMID: 28088464]
[53]
Carvalho, L.M.L.; Ferreira, C.N.; Candido, A.L.; Reis, F.M.; Sóter, M.O.; Sales, M.F.; Silva, I.F.O.; Nunes, F.F.C.; Gomes, K.B. Metformin reduces total microparticles and microparticles-expressing tissue factor in women with polycystic ovary syndrome. Arch. Gynecol. Obstet., 2017, 296(4), 617-621.
[http://dx.doi.org/10.1007/s00404-017-4471-0] [PMID: 28795250]
[54]
Heffner, L.J. Advanced maternal age-how old is too old? N. Engl. J. Med., 2004, 351(19), 1927-1929.
[http://dx.doi.org/10.1056/NEJMp048087] [PMID: 15525717]
[55]
Knight, P.G.; Glister, C. TGF-beta superfamily members and ovarian follicle development. Reproduction, 2006, 132(2), 191-206.
[http://dx.doi.org/10.1530/rep.1.01074] [PMID: 16885529]
[56]
Panagiotou, N.; Neytchev, O.; Selman, C.; Shiels, P.G. Extracellular vesicles, ageing, and therapeutic interventions. Cells, 2018, 7(8)E110
[http://dx.doi.org/10.3390/cells7080110] [PMID: 30126173]
[57]
Sun, L.; Li, D.; Song, K.; Wei, J.; Yao, S.; Li, Z.; Su, X.; Ju, X.; Chao, L.; Deng, X.; Kong, B.; Li, L. Exosomes derived from human umbilical cord mesenchymal stem cells protect against cisplatin-induced ovarian granulosa cell stress and apoptosis in vitro. Sci. Rep., 2017, 7(1), 2552.
[http://dx.doi.org/10.1038/s41598-017-02786-x] [PMID: 28566720]
[58]
Huang, B.; Lu, J.; Ding, C.; Zou, Q.; Wang, W.; Li, H. Exosomes derived from human adipose mesenchymal stem cells improve ovary function of premature ovarian insufficiency by targeting SMAD. Stem Cell Res. Ther., 2018, 9(1), 216.
[http://dx.doi.org/10.1186/s13287-018-0953-7] [PMID: 30092819]
[59]
Webber, L.; Davies, M.; Anderson, R.; Bartlett, J.; Braat, D.; Cartwright, B.; Cifkova, R.; de Muinck Keizer-Schrama, S.; Hogervorst, E.; Janse, F.; Liao, L.; Vlaisavljevic, V.; Zillikens, C.; Vermeulen, N. ESHRE guideline: Management of women with premature ovarian insufficiency. Hum. Reprod., 2016, 31(5), 926-937.
[http://dx.doi.org/10.1093/humrep/dew027] [PMID: 27008889]
[60]
Jankowska, K. Premature ovarian failure. Przegl. Menopauz., 2017, 16(2), 51-56.
[http://dx.doi.org/10.5114/pm.2017.68592] [PMID: 28721130]
[61]
Yang, P.C. Induced Pluripotent Stem Cell (iPSC)-derived exosomes for precision medicine in heart failure. Circ. Res., 2018, 122(5), 661-663.
[http://dx.doi.org/10.1161/CIRCRESAHA.118.312657] [PMID: 29496797]
[62]
Chen, L.; Xiang, B.; Wang, X.; Xiang, C. Exosomes derived from human menstrual blood-derived stem cells alleviate fulminant hepatic failure. Stem Cell Res. Ther., 2017, 8(1), 9.
[http://dx.doi.org/10.1186/s13287-016-0453-6] [PMID: 28115012]
[63]
Meyer, K.; Yankner, B.A. Slowing down aging. Cell Metab., 2017, 26(4), 592-593.
[http://dx.doi.org/10.1016/j.cmet.2017.09.012] [PMID: 28978424]
[64]
Xiao, G.Y.; Cheng, C.C.; Chiang, Y.S.; Cheng, W.T.; Liu, I.H.; Wu, S.C. Exosomal miR-10a derived from amniotic fluid stem cells preserves ovarian follicles after chemotherapy. Sci. Rep., 2016, 6, 23120.
[http://dx.doi.org/10.1038/srep23120] [PMID: 26979400]
[65]
Makieva, S.; Giacomini, E.; Ottolina, J.; Sanchez, A.M.; Papaleo, E.; Viganò, P. Inside the endometrial cell signaling subway: Mind the gap(s). Int. J. Mol. Sci., 2018, 19(9)E2477
[http://dx.doi.org/10.3390/ijms19092477] [PMID: 30134622]
[66]
Greening, D.W.; Nguyen, H.P.; Elgass, K.; Simpson, R.J.; Salamonsen, L.A. Human endometrial exosomes contain hormone-specific cargo modulating trophoblast adhesive capacity: Insights into endometrial-embryo interactions. Biol. Reprod., 2016, 94(2), 38.
[http://dx.doi.org/10.1095/biolreprod.115.134890] [PMID: 26764347]
[67]
Blázquez, R.; Sánchez-Margallo, F.M.; Álvarez, V.; Matilla, E.; Hernández, N.; Marinaro, F.; Gómez-Serrano, M.; Jorge, I.; Casado, J.G.; Macías-García, B. Murine embryos exposed to human endometrial MSCs-derived extracellular vesicles exhibit higher VEGF/PDGF AA release, increased blastomere count and hatching rates. PLoS One, 2018, 13(4)e0196080
[http://dx.doi.org/10.1371/journal.pone.0196080] [PMID: 29684038]
[68]
Bidarimath, M.; Khalaj, K.; Kridli, R.T.; Kan, F.W.; Koti, M.; Tayade, C. Extracellular vesicle mediated intercellular communication at the porcine maternal-fetal interface: A new paradigm for conceptus-endometrial cross-talk. Sci. Rep., 2017, 7, 40476.
[http://dx.doi.org/10.1038/srep40476] [PMID: 28079186]
[69]
Zeng, S.; Bick, J.; Ulbrich, S.E.; Bauersachs, S. Cell type-specific analysis of transcriptome changes in the porcine endometrium on Day 12 of pregnancy. BMC Genomics, 2018, 19(1), 459.
[http://dx.doi.org/10.1186/s12864-018-4855-y] [PMID: 29898663]
[70]
Kawano, N.; Miyado, K.; Yoshii, N.; Kanai, S.; Saito, H.; Miyado, M.; Inagaki, N.; Odawara, Y.; Hamatani, T.; Umezawa, A. Absence of CD9 reduces endometrial VEGF secretion and impairs uterine repair after parturition. Sci. Rep., 2014, 4, 4701.
[http://dx.doi.org/10.1038/srep04701] [PMID: 24736431]
[71]
Tanbo, T.; Fedorcsak, P. Endometriosis-associated infertility: Aspects of pathophysiological mechanisms and treatment options. Acta Obstet. Gynecol. Scand., 2017, 96(6), 659-667.
[http://dx.doi.org/10.1111/aogs.13082] [PMID: 27998009]
[72]
Harp, D.; Driss, A.; Mehrabi, S.; Chowdhury, I.; Xu, W.; Liu, D.; Garcia-Barrio, M.; Taylor, R.N.; Gold, B.; Jefferson, S.; Sidell, N.; Thompson, W. Exosomes derived from endometriotic stromal cells have enhanced angiogenic effects in vitro. Cell Tissue Res., 2016, 365(1), 187-196.
[http://dx.doi.org/10.1007/s00441-016-2358-1] [PMID: 26841879]
[73]
Zhao, L.; Gu, C.; Ye, M.; Zhang, Z.; Li, L.; Fan, W.; Meng, Y. Integration analysis of microRNA and mRNA paired expression profiling identifies deregulated microRNA-transcription factor-gene regulatory networks in ovarian endometriosis. Reprod. Biol. Endocrinol., 2018, 16(1), 4.
[http://dx.doi.org/10.1186/s12958-017-0319-5] [PMID: 29357938]
[74]
Shi, X.Y.; Gu, L.; Chen, J.; Guo, X.R.; Shi, Y.L. Downregulation of miR-183 inhibits apoptosis and enhances the invasive potential of endometrial stromal cells in endometriosis. Int. J. Mol. Med., 2014, 33(1), 59-67.
[http://dx.doi.org/10.3892/ijmm.2013.1536] [PMID: 24173391]
[75]
Wu, D.; Lu, P.; Mi, X.; Miao, J. Exosomal miR-214 from endometrial stromal cells inhibits endometriosis fibrosis. Mol. Hum. Reprod., 2018, 24(7), 357-365.
[http://dx.doi.org/10.1093/molehr/gay019] [PMID: 29660008]
[76]
Sun, H.; Li, D.; Yuan, M.; Li, Q.; Li, N.; Wang, G. Eutopic stromal cells of endometriosis promote neuroangiogenesis via exosome pathway. Biol. Reprod., 2019, 100(3), 649-659.
[http://dx.doi.org/doi:10.1093/biolre/ioy212] [PMID: 30295741]
[77]
Nothnick, W.B. MicroRNAs and endometriosis: distinguishing drivers from passengers in disease pathogenesis. Semin. Reprod. Med., 2017, 35(2), 173-180.
[http://dx.doi.org/10.1055/s-0037-1599089] [PMID: 28212593]
[78]
Sun, H.; Li, D.; Yuan, M.; Li, Q.; Zhen, Q.; Li, N.; Wang, G. Macrophages alternatively activated by endometriosis-exosomes contribute to the development of lesions in mice. Mol. Hum. Reprod., 2018.
[PMID: 30428082]
[79]
Hrazdirová, L.; Kužel, D.; Žižka, Z. Asherman’s syndrome I-history, prevalence, histopathology, classification, ethiology, symtomatology and investigations. Ceska Gynekol., 2010, 75(6), 492-498.
[PMID: 27534003]
[80]
Di Spiezio Sardo, A.; Calagna, G.; Scognamiglio, M.; O’Donovan, P.; Campo, R.; De Wilde, R.L. Prevention of intrauterine post-surgical adhesions in hysteroscopy. A systematic review. Eur. J. Obstet. Gynecol. Reprod. Biol., 2016, 203, 182-192.
[http://dx.doi.org/10.1016/j.ejogrb.2016.05.050] [PMID: 27337414]
[81]
Roy, K.K.; Baruah, J.; Sharma, J.B.; Kumar, S.; Kachawa, G.; Singh, N. Reproductive outcome following hysteroscopic adhesiolysis in patients with infertility due to Asherman’s syndrome. Arch. Gynecol. Obstet., 2010, 281(2), 355-361.
[http://dx.doi.org/10.1007/s00404-009-1117-x] [PMID: 19455349]
[82]
Akhurst, R.J.; Hata, A. Targeting the TGFβ signalling pathway in disease. Nat. Rev. Drug Discov., 2012, 11(10), 790-811.
[http://dx.doi.org/10.1038/nrd3810] [PMID: 23000686]
[83]
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), 304-314.
[http://dx.doi.org/10.1002/cam4.545] [PMID: 26700550]
[84]
Nakamura, K.; Jinnin, M.; Harada, M.; Kudo, H.; Nakayama, W.; Inoue, K.; Ogata, A.; Kajihara, I.; Fukushima, S.; Ihn, H. Altered expression of CD63 and exosomes in scleroderma dermal fibroblasts. J. Dermatol. Sci., 2016, 84(1), 30-39.
[http://dx.doi.org/10.1016/j.jdermsci.2016.06.013] [PMID: 27443953]
[85]
Almughlliq, F.B.; Koh, Y.Q.; Peiris, H.N.; Vaswani, K.; McDougall, S.; Graham, E.M.; Burke, C.R.; Mitchell, M.D. Effect of exosomes from plasma of dairy cows with or without an infected uterus on prostaglandin production by endometrial cell lines. J. Dairy Sci., 2017, 100(11), 9143-9152.
[http://dx.doi.org/10.3168/jds.2017-13261] [PMID: 28865856]
[86]
Honoré, G.M.; Holden, A.E.; Schenken, R.S. Pathophysiology and management of proximal tubal blockage. Fertil. Steril., 1999, 71(5), 785-795.
[http://dx.doi.org/10.1016/S0015-0282(99)00014-X] [PMID: 10231034]
[87]
Pérez-Cerezales, S.; Ramos-Ibeas, P.; Acuña, O.S.; Avilés, M.; Coy, P.; Rizos, D.; Gutiérrez-Adán, A. The oviduct: From sperm selection to the epigenetic landscape of the embryo. Biol. Reprod., 2018, 98(3), 262-276.
[http://dx.doi.org/10.1093/biolre/iox173] [PMID: 29228115]
[88]
Bathala, P.; Fereshteh, Z.; Li, K.; Al-Dossary, A.A.; Galileo, D.S.; Martin-DeLeon, P.A. Oviductal extracellular vesicles (oviductosomes, OVS) are conserved in humans: Murine OVS play a pivotal role in sperm capacitation and fertility. Mol. Hum. Reprod., 2018, 24(3), 143-157.
[http://dx.doi.org/10.1093/molehr/gay003] [PMID: 29370405]
[89]
Al-Dossary, A.A.; Strehler, E.E.; Martin-Deleon, P.A. 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
[http://dx.doi.org/10.1371/journal.pone.0080181] [PMID: 24244642]
[90]
Almiñana, C.; Corbin, E.; Tsikis, G.; Alcântara-Neto, A.S.; Labas, V.; Reynaud, K.; Galio, L.; Uzbekov, R.; Garanina, A.S.; Druart, X.; Mermillod, P. Oviduct extracellular vesicles protein content and their role during oviduct-embryo cross-talk. Reproduction, 2017, 154(3), 153-168.
[http://dx.doi.org/10.1530/REP-17-0054] [PMID: 28630101]
[91]
Almiñana, C.; Tsikis, G.; Labas, V.; Uzbekov, R.; da Silveira, J.C.; Bauersachs, S.; Mermillod, P. Deciphering the oviductal extracellular vesicles content across the estrous cycle: implications for the gametes-oviduct interactions and the environment of the potential embryo. BMC Genomics, 2018, 19(1), 622.
[http://dx.doi.org/10.1186/s12864-018-4982-5] [PMID: 30134841]
[92]
Al-Dossary, A.A.; Martin-Deleon, P.A. Role of exosomes in the reproductive tract oviductosomes mediate interactions of oviductal secretion with gametes/early embryo. Front. Biosci., 2016, 21, 1278-1285.
[http://dx.doi.org/10.2741/4456] [PMID: 27100506]
[93]
Fereshteh, Z.; Schmidt, S.A.; Al-Dossary, A.A.; Accerbi, M.; Arighi, C.; Cowart, J.; Song, J.L.; Green, P.J.; Choi, K.; Yoo, S.; Martin-DeLeon, P.A. Murine Oviductosomes (OVS) microRNA profiling during the estrous cycle: Delivery of OVS-borne microRNAs to sperm where miR-34c-5p localizes at the centrosome. Sci. Rep., 2018, 8(1), 16094.
[http://dx.doi.org/10.1038/s41598-018-34409-4] [PMID: 30382141]
[94]
Bunggulawa, E.J.; Wang, W.; Yin, T.; Wang, N.; Durkan, C.; Wang, Y.; Wang, G. Recent advancements in the use of exosomes as drug delivery systems. J. Nanobiotechnology, 2018, 16(1), 81.
[http://dx.doi.org/10.1186/s12951-018-0403-9] [PMID: 30326899]
[95]
Aryani, A.; Denecke, B. Exosomes as a nanodelivery system: A Key to the future of neuromedicine? Mol. Neurobiol., 2016, 53(2), 818-834.
[http://dx.doi.org/10.1007/s12035-014-9054-5] [PMID: 25502465]
[96]
Ha, D.; Yang, N.; Nadithe, V. Exosomes as therapeutic drug carriers and delivery vehicles across biological membranes: Current perspectives and future challenges. Acta Pharm. Sin. B, 2016, 6(4), 287-296.
[http://dx.doi.org/10.1016/j.apsb.2016.02.001] [PMID: 27471669]
[97]
Kooijmans, S.A.; Vader, P.; van Dommelen, S.M.; van Solinge, W.W.; Schiffelers, R.M. Exosome mimetics: A novel class of drug delivery systems. Int. J. Nanomedicine, 2012, 7, 1525-1541.
[PMID: 22619510]
[98]
Xiao, B.; Zhu, Y.; Huang, J.; Wang, T.; Wang, F.; Sun, S. Exosomal transfer of bone marrow mesenchymal stem cell-derived miR-340 attenuates endometrial fibrosis. Biol. Open, 2019, 8(5), 1-9.
[http://dx.doi.org/10.1242/bio.039958] [PMID: 30890521]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy