Extracellular vesicles and reproduction-promotion of successful pregnancy

Cellular and Molecular Immunology

Volumn 11, Issue 6, 2014, Pages 548-563

  Tannetta, Dionne ^a   Dragovic, Rebecca ^a   Alyahyaei, Zahraa ^a   Southcombe, Jennifer ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

exosomes; Extracellular vesicles; microvesicles; nanoparticle tracking analysis; pre eclampsia; pregnancy

Indexed keywords

ADAPTATION; AMNION FLUID; APOPTOSIS; CELL INTERACTION; CLINICAL PRACTICE; ENDOMETRIUM; ENDOSOME; EXOCYTOSIS; EXOSOME; EXTRACELLULAR VESICLE; GAMETE; HUMAN; IMMUNE SYSTEM; MEMBRANE VESICLE; NIDATION; OOCYTE; OVARY FOLLICLE FLUID; PARTICLE SIZE; PREECLAMPSIA; PREGNANCY; PREMATURE LABOR; REVIEW; SEMINAL PLASMA; SYNCYTIOTROPHOBLAST; SYSTEMIC CIRCULATION; TROPHOBLAST; ANIMAL; EXTRACELLULAR SPACE; FEMALE; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY OUTCOME; REPRODUCTION; SECRETORY VESICLE;

ANIMALS; EXTRACELLULAR SPACE; FEMALE; HUMANS; OBSTETRIC LABOR, PREMATURE; PRE-ECLAMPSIA; PREGNANCY; PREGNANCY OUTCOME; REPRODUCTION; SECRETORY VESICLES;

EID: 84908504659     PISSN: 16727681     EISSN: 20420226     Source Type: Journal    
DOI: 10.1038/cmi.2014.42     Document Type: Review

References (123)

1. Aalberts M, Stout TA, Stoorvogel W. Prostasomes: extracellular vesicles from the prostate. Reproduction 2014; 147: R1-R14
2. Fest S, Aldo PB, Abrahams VM, Visintin I, Alvero A, Chen R et al. Trophoblast-macrophage interactions: a regulatory network for the protection of pregnancy Am J Reprod Immunol 2007; 57: 55-66
3. Apps R, Murphy SP, Fernando R, Gardner L, Ahad T, Moffett A. Human leucocyte antigen (HLA) expression of primary trophoblast cells and placental cell lines, determined using single antigen beads to characterize allotype specificities of anti-HLA antibodies. Immunology 2009; 127: 26-39
4. Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009; 9: 581-593
5. Redman CW, Sargent IL. Microparticles and immunomodulation in pregnancy and pre-eclampsia. J Reprod Immunol 2007; 76: 61-7
6. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007; 9: 654-659
7. Chen X, Liang H, Zhang J, Zen K, Zhang CY. Horizontal transfer of microRNAs: molecular mechanisms and clinical applications. Protein Cell 2012; 3: 28-37
8. Mouillet JF, Chu T, Sadovsky Y. Expression patterns of placental microRNAs. Birth Defects Res A Clin Mol Teratol 2011; 91: 737-743
9. Liang Y, Ridzon D, Wong L, Chen C. Characterization of microRNA expression profiles in normal human tissues. BMC Genomics 2007; 8: 166.
10. Zhu XM, Han T, Sargent IL, Yin GW, Yao YQ. Differential expression profile of microRNAs in human placentas from preeclamptic pregnancies vs normal pregnancies. Am J Obstet Gynecol 2009; 200: 661 e1-e7
11. Miura K, Miura S, Yamasaki K, Higashijima A, Kinoshita A, Yoshiura K et al. Identification of pregnancy-associated microRNAs in maternal plasma. Clin Chem 2010; 56: 1767-1771
12. Morales Prieto DM, Markert UR. MicroRNAs in pregnancy. J Reprod Immunol 2011; 88: 106-111
13. Luo SS, Ishibashi O, Ishikawa G, Ishikawa T, Katayama A, Mishima T et al. Human villous trophoblasts express and secrete placentaspecific microRNAs into maternal circulation via exosomes. Biol Reprod 2009; 81: 717-729
14. Donker RB, Mouillet JF, Chu T, Hubel CA, Stolz DB, Morelli AE et al. The expression profile of C19MC microRNAs in primary human trophoblast cells and exosomes. Mol Hum Reprod 2012; 18: 417-424
15. Noguer-Dance M, Abu-Amero S, Al-Khtib M, Lefevre A, Coullin P, Moore GE et al. The primate-specific microRNA gene cluster (C19MC) is imprinted in the placenta. Hum Mol Genet 2010; 19: 3566-3582
16. Bullerdiek J, Flor I. Exosome-delivered microRNAs of "chromosome 19 microRNA cluster" as immunomodulators in pregnancy and tumorigenesis. Mol Cytogenet 2012; 5: 27.
17. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 2013; 200: 373-383
18. Redman CWG, Tannetta DS, Dragovic RA, Gardiner C, Southcombe JH, Collett GP et al. Review: Does size matter? Placental debris and the pathophysiology of pre- eclampsia. Placenta 2012; 33: S48-S54
19. Chamley LW, Holland OJ, Chen Q, Viall CA, Stone PR, Abumaree M. Review: where is the maternofetal interface? Placenta 2014; 35(Suppl): S74-S80
20. Cronqvist T, Salje K, Familari M, Guller S, Schneider H, Gardiner C et al. Syncytiotrophoblast vesicles show altered micro-RNA and haemoglobin content after ex-vivo perfusion of placentas with haemoglobin to mimic preeclampsia. PLoS ONE 2014; 9: e90020.
21. Chamley LW, Chen Q, Ding J, Stone PR, Abumaree M. Trophoblast deportation: just a waste disposal system or antigen sharing? J Reprod Immunol 2011; 88: 99-105
22. Abumaree MH, Chamley LW, Badri M, El-Muzaini MF. Trophoblast debris modulates the expression of immune proteins in macrophages: a key to maternal tolerance of the fetal allograft? J Reprod Immunol 2012; 94: 131-141
23. Hedlund M, Stenqvist AC, Nagaeva O, Kjellberg L, Wulff M, Baranov V et al. Human placenta expresses and secretes NKG2D ligands via exosomes that down-modulate the cognate receptor expression: evidence for immunosuppressive function. J Immunol 2009; 183: 340-351
24. van der Pol E, Coumans F, Varga Z, Krumrey M, Nieuwland R. Innovation in detection of microparticles and exosomes. J Thromb Haemost 2013; 11(Suppl 1): 36-45
25. van der Pol E, Hoekstra AG, Sturk A, Otto C, van Leeuwen TG, Nieuwland R. Optical and non-optical methods for detection and characterization of microparticles and exosomes. J Thromb Haemost 2010; 8: 2596-2607
26. Witwer KW, Buzas EI, Bemis LT, Bora A, Lasser C, Lotvall J et al. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles 2013; 2.
27. Ayers L, Kohler M, Harrison P, Sargent I, Dragovic R, SchaapMet al. Measurement of circulating cell-derived microparticles by flow cytometry: sources of variability within the assay. Thromb Res 2011; 127: 370-377
28. Lacroix R, Robert S, Poncelet P, Kasthuri RS, Key NS, Dignat-George F. Standardization of platelet-derived microparticle enumeration by flow cytometry with calibrated beads: results of the International Society on Thrombosis and Haemostasis SSC Collaborative Workshop. J Thromb Haemost 2010; 8: 2571-2574
29. Dragovic RA, Southcombe JH, Tannetta DS, Redman CW, Sargent IL. Multicolor flow cytometry and nanoparticle tracking analysis of extracellular vesicles in the plasma of normal pregnant and preeclamptic women. Biol Reprod 2013; 89: 151.
30. Perez-Pujol S, Marker PH, Key NS. Platelet microparticles are heterogeneous and highly dependent on the activation mechanism: studies using a new digital flow cytometer. Cytometry A 2007; 71: 38-45
31. Tannetta DS, Dragovic RA, Gardiner C, Redman CW, Sargent IL. Characterisation of syncytiotrophoblast vesicles in normal pregnancy and pre-eclampsia: expression of Flt-1 and endoglin. PLoS ONE 2013; 8: e56754.
32. Nolte-'t Hoen EN, van der Vlist EJ, Aalberts M, Mertens HC, Bosch BJ, Bartelink W et al. Quantitative and qualitative flow cytometric analysis of nanosized cell-derived membrane vesicles. Nanomedicine 2012; 8: 712-720
33. van der Vlist EJ, Nolte-'t Hoen EN, Stoorvogel W, Arkesteijn GJ, Wauben MH. Fluorescent labeling of nano-sized vesicles released by cells and subsequent quantitative and qualitative analysis by high-resolution flow cytometry. Nat Protoc 2012; 7: 1311-1326
34. Montoro-Garcia S, Shantsila E, Orenes-Pinero E, Lozano ML, Lip GY. An innovative flow cytometric approach for small-size platelet microparticles: influence of calcium. Thromb Haemost 2012; 108: 373-383
35. Lok CA, van der Post JA, Sargent IL, Hau CM, Sturk A, Boer K et al. Changes in microparticle numbers and cellular origin during pregnancy and preeclampsia. Hypertens Pregnancy 2008; 27: 344-360
36. Dragovic RA, Gardiner C, Brooks AS, Tannetta DS, Ferguson DJ, Hole P et al. Sizing and phenotyping of cellular vesicles using Nanoparticle Tracking Analysis. Nanomedicine 2011; 7: 780-788
37. Kaji K, Oda S, Shikano T, Ohnuki T, Uematsu Y, Sakagami J et al. The gamete fusion process is defective in eggs of Cd9-deficient mice. Nat Genet 2000; 24: 279-282
38. Miyado K, Yamada G, Yamada S, Hasuwa H, Nakamura Y, Ryu F et al. Requirement of CD9 on the egg plasma membrane for fertilization. Science 2000; 287: 321-324
39. Barraud-Lange V, Chalas Boissonnas C, Serres C, Auer J, Schmitt A, Lefevre B et al. Membrane transfer from oocyte to sperm occurs in two CD9-independent ways that do not supply the fertilising ability of Cd9-deleted oocytes. Reproduction 2012; 144: 53-66
40. Gupta S, Primakoff P, Myles DG. Can the presence of wild-type oocytes during insemination rescue the fusion defect of CD9 null oocytes? Mol Reprod Dev 2009; 76: 602.
41. Miyado K, Yoshida K, Yamagata K, Sakakibara K, Okabe M, Wang X et al. The fusing ability of sperm is bestowed by CD9-containing vesicles released from eggs in mice. Proc Natl Acad Sci USA 2008; 105: 12921-12926
42. Rubinstein E, Ziyyat A, Prenant M, Wrobel E, Wolf JP, Levy S et al. Reduced fertility of female mice lacking CD81. Dev Biol 2006; 290: 351-358
43. Tanigawa M, Miyamoto K, Kobayashi S, Sato M, Akutsu H, Okabe M et al. Possible involvement of CD81 in acrosome reaction of sperm in mice. Mol Reprod Dev 2008; 75: 150-155
44. Ohnami N, Nakamura A, Miyado M, Sato M, Kawano N, Yoshida K et al. CD81 and CD9 work independently as extracellular components upon fusion of sperm and oocyte. Biol Open 2012; 1: 640-647
45. 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.
46. da Silveira JC, Veeramachaneni DN, Winger QA, Carnevale EM, Bouma GJ. 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: 71.
47. Diez-Fraile A, Lammens T, Tilleman K, Witkowski W, Verhasselt B, de Sutter P et al. Age-associated differential microRNA levels in human follicular fluid reveal pathways potentially determining fertility and success of in vitro fertilization. Hum Fertil (Camb) 2014; in press.
48. Sang Q, Yao Z, Wang H, Feng R, Zhao X, Xing Q et al. Identification of microRNAs in human follicular fluid: characterization of microRNAs that govern steroidogenesis in vitro and are associated with polycystic ovary syndrome in vivo. J Clin Endocrinol Metab 2013; 98: 3068-3079
49. Sohel MM, Hoelker M, Noferesti SS, Salilew-Wondim D, Tholen E, Looft C et al. Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: implications for bovine oocyte developmental competence. PLoS ONE 2013; 8: e78505.
50. Al-Dossary AA, Strehler EE, Martin-Deleon PA. Expression and secretion of plasma membrane Ca21-ATPase 4a (PMCA4a) during murine estrus: association with oviductal exosomes and uptake in sperm. PLoS ONE 2013; 8: e80181.
51. Ng YH, Rome S, Jalabert A, Forterre A, Singh H, Hincks CL et al. Endometria l exosomes/microvesicles in the uterine microenvironment: a new paradigm for embryo-endometrial cross talk at implantation. PLoS ONE 2013; 8: e58502.
52. Braundmeier AG, Dayger CA, Mehrotra P, Belton RJ Jr, Nowak RA. EMMPRIN is secreted by human uterine epithelial cells in microvesicles and stimulates metalloproteinase production by human uterine fibroblast cells. Reprod Sci 2012; 19: 1292-301
53. Burnett LA, Light MM, Mehrotra P, Nowak RA. Stimulation of GPR30 increases release of EMMPRIN-containing microvesicles in human uterine epithelial cells. J Clin Endocrinol Metab 2012; 97: 4613-4622
54. Ronquist G. Prostasomes are mediators of intercellular communication: from basic research to clinical implications. J Intern Med 2012; 271: 400-413
55. Skibinski G, Kelly RW, Harkiss D, James K. Immunosuppression by human seminal plasma-extracellular organelles (prostasomes) modulate activity of phagocytic cells Am J Reprod Immunol 1992; 28: 97-103
56. Tarazona R, Delgado E, Guarnizo MC, Roncero RG, Morgado S, Sanchez-Correa B et al. Human prostasomes express CD48 and interfere with NK cell function. Immunobiology 2011; 216: 41-46
57. Kitamura M, Namiki M, Matsumiya K, Tanaka K, Matsumoto M, Hara T et al. Membrane cofactor protein (CD46) in seminal plasma is a prostasome-bound form with complement regulatory activity and measles virus neutralizing activity. Immunology 1995; 84: 626-632
58. Rooney IA, Atkinson JP, Krul ES, Schonfeld G, Polakoski K, Saffitz JE et al. Physiologic relevance of the membrane attack complex inhibitory protein CD59 in human seminal plasma: CD59 is present on extracellular organelles (prostasomes), binds cell membranes, and inhibits complement-mediated lysis. J Exp Med 1993; 177: 1409-1420
59. Saez F, Motta C, Boucher D, Grizard G. Antioxidant capacity of prostasomes in human semen. MolHumReprod 1998; 4: 667-672
60. Jones JL, Saraswati S, Block AS, Lichti CF, Mahadevan M, Diekman AB. Galectin-3 is associated with prostasomes in human semen. Glycoconj J 2010; 27: 227-236
61. Harris LK. IFPA Gabor than Award lecture: transformation of the spiral arteries in human pregnancy: key events in the remodelling timeline. Placenta 2011; 32: S154-S158
62. Red-Horse K, Zhou Y, Genbacev O, Prakobphol A, Foulk R, McMaster M et al. Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface J Clin Invest 2004; 114: 744-754
63. Knofler M, Pollheimer J. IFPA Award in Placentology Lecture: molecular regulation of human trophoblast invasion. Placenta 2012; 33: S55-S62
64. Burton GJ, Jauniaux E, Charnock-Jones DS. Human early placental development: potential roles of the endometrial glands. Placenta 2007; 28(Suppl A): S64-S69
65. Sargent IL, Borzychowski AM, Redman CW. NK cells and human pregnancy-an inflammatory view. Trends Immunol 2006; 27: 399-404
66. Kshirsagar SK, Alam SM, Jasti S, Hodes H, Nauser T, GilliamMet al. Immunomodulatory molecules are released from the first trimester and term placenta via exosomes. Placenta 2012; 33: 982-990
67. Orozco AF, Jorgez CJ, Ramos-Perez WD, Popek EJ, Yu X, Kozinetz CA et al. Placental release of distinct DNA-associated micro-particles into maternal circulation: reflective of gestation time and preeclampsia. Placenta 2009; 30: 891-897
68. Pap E, Pallinger E, Falus A, Kiss AA, Kittel A, Kovacs P et al. T lymphocytes are targets for platelet- and trophoblast-derived microvesicles during pregnancy. Placenta 2008; 29: 826-832
69. Sargent I, Dragovic RA, Tannetta D, Redman C, Extracellular vesicles in normal pregnancy and pre-eclampsia. In:Extracellular Vesicles in Health and Disease. Oxford: Pan Stanford Publishing, 2014; 357-390
70. Atay S, Gercel-Taylor C, Kesimer M, Taylor DD Morphologic and proteomic characterization of exosomes released by cultured extravillous trophoblast cells. Exp Cell Res 2011; 317: 1192-1202
71. Gonen-Gross T, Achdout H, Arnon TI, Gazit R, Stern N, Horejsi V et al. The CD85J/leukocyte inhibitory receptor-1 distinguishes between conformed and beta 2-microglobulin-free HLA-G molecules. J Immunol 2005; 175: 4866-4874
72. Bainbridge DR, Ellis SA, Sargent IL. HLA-G suppresses proliferation of CD41 T-lymphocytes. J Reprod Immunol 2000; 48: 17-26
73. Atay S, Gercel-Taylor C, Suttles J, Mor G, Taylor DD. Trophoblastderived exosomes mediate monocyte recruitment and differentiation. Am J Reprod Immunol 2011; 65: 65-77
74. Atay S, Gercel-Taylor C, Taylor DD. Human trophoblast-derived exosomal fibronectin induces pro-inflammatory IL-1beta production by macrophages. Am J Reprod Immunol 2011; 66: 259-269
75. Burton GJ, Sebire NJ, Myatt L, Tannetta D, Wang YL, Sadovsky Y et al. Optimising sample collection for placental research. Placenta 2014; 35: 9-22
76. Burton GJ, Jones CJ. Syncytial knots, sprouts, apoptosis, and trophoblast deportation from the human placenta. Taiwan J Obstet Gynecol 2009; 48: 28-37
77. Knight M, Redman CW, Linton EA, Sargent IL. Shedding of syncytiotrophoblast microvilli into the maternal circulation in preeclamptic pregnancies. Br J Obstet Gynaecol 1998; 105: 632-640
78. Germain SJ, Sacks GP, Sooranna SR, Sargent IL, Redman CW. Systemic inflammatory priming in normal pregnancy and preeclampsia: the role of circulating syncytiotrophoblast microparticles. J Immunol 2007; 178: 5949-5956
79. Reddy A, Zhong XY, Rusterholz C, Hahn S, Holzgreve W, RedmanCW et al. The effect of labour and placental separation on the shedding of syncytiotrophoblast microparticles, cell-free DNA and mRNA in normal pregnancy and pre-eclampsia. Placenta 2008; 29: 942-949
80. Sabapatha A, Gercel-Taylor C, Taylor DD. Specific isolation of placenta-derived exosomes from the circulation of pregnant women and their immunoregulatory consequences. Am J Reprod Immunol 2006; 56: 345-355
81. Johansen M, Redman CW, Wilkins T, Sargent IL. Trophoblast deportation in human pregnancy-its relevance for pre-eclampsia. Placenta 1999; 20: 531-539
82. Takahashi Y, Nishikawa M, Shinotsuka H, Matsui Y, Ohara S, Imai T et al. Visualization and in vivo tracking of the exosomes of murine melanoma B16-BL6 cells in mice after intravenous injection. J Biotechnol 2013; 165: 77-84
83. Southcombe J, Tannetta D, Redman C, Sargent I. The immunomodulatory role of syncytiotrophoblast microvesicles. PLoS ONE 2011; 6: e20245.
84. Holland OJ, Linscheid C, Hodes HC, Nauser TL, Gilliam M, Stone P et al. Minor histocompatibility antigens are expressed in syncytiotrophoblast and trophoblast debris: implications for maternal alloreactivity to the fetus. Am J Pathol 2012; 180: 256-266
85. Mincheva-Nilsson L, Nagaeva O, Chen T, Stendahl U, Antsiferova J, Mogren I et al. Placenta-derived soluble MHC class I chain-related molecules down-regulate NKG2D receptor on peripheral blood mononuclear cells during human pregnancy: a possible novel immune escape mechanism for fetal survival. J Immunol 2006; 176: 3585-3592
86. Thibault G, Degenne D, Girard AC, Guillaumin JM, Lacord M, Bardos P. The inhibitory effect of human syncytiotrophoblast plasma membrane vesicles on in vitro lymphocyte proliferation is associated with reduced interleukin 2 receptor expression. Cell Immunol 1991; 138: 165-174
87. Arkwright PD, Rademacher TW, Boutignon F, Dwek RA, Redman CW. Suppression of allogeneic reactivity in vitro by the syncytiotrophoblast membrane glycocalyx of the human term placenta is carbohydrate dependent. Glycobiology 1994; 4: 39-47
88. Gupta AK, Rusterholz C, Holzgreve W, Hahn S. Syncytiotrophoblast micro-particles do not induce apoptosis in peripheral T lymphocytes, but differ in their activity depending on the mode of preparation. J Reprod Immunol 2005; 68: 15-26
89. Taylor DD, Akyol S, Gercel-Taylor C. Pregnancy-associated exosomes and their modulation of T cell signaling. J Immunol 2006; 176: 1534-1542
90. Stenqvist AC, Nagaeva O, Baranov V, Mincheva-Nilsson L. Exosomes secreted by human placenta carry functional Fas ligand and TRAIL molecules and convey apoptosis in activated immune cells, suggesting exosome-mediated immune privilege of the fetus. J Immunol 2013; 191: 5515-5523
91. Abumaree MH, Stone PR, Chamley LW. The effects of apoptotic, deported human placental trophoblast on macrophages: possible consequences for pregnancy. J Reprod Immunol 2006; 72: 33-45
92. Sacks GP, Studena K, Sargent K, Redman CW. Normal pregnancy and preeclampsia both produce inflammatory changes in peripheral blood leukocytes akin to those of sepsis. Am J Obstet Gynecol 1998; 179: 80-86
93. Messerli M, May K, Hansson SR, Schneider H, Holzgreve W, Hahn S et al. Feto- maternal interactions in pregnancies: placental microparticles activate peripheral blood monocytes. Placenta 2010; 31: 106-112
94. Aly AS, Khandelwal M, Zhao J, Mehmet AH, Sammel MD, Parry S. Neutrophils are stimulated by syncytiotrophoblast microvillous membranes to generate superoxide radicals in women with preeclampsia. Am J Obstet Gynecol 2004; 190: 252-258
95. Gupta AK, Hasler P, Holzgreve W, Gebhardt S, Hahn S. Induction of neutrophil extracellular DNA lattices by placental microparticles and IL-8 and their presence in preeclampsia. Hum Immunol 2005; 66: 1146-1154
96. Redman CW, Tannetta DS, Dragovic RA, Gardiner C, Southcombe JH, Collett GP et al. Review: Does size matter? Placental debris and the pathophysiology of pre-eclampsia. Placenta 2012; 33(Suppl): S48-S54
97. Delorme-Axford E, Donker RB, Mouillet JF, Chu T, Bayer A, Ouyang Y et al. Human placental trophoblasts confer viral resistance to recipient cells. Proc Natl Acad Sci U S A 2013; 110: 12048-12053
98. Keller S, Rupp C, Stoeck A, Runz S, Fogel M, LugertS et al. CD24 is a marker of exosomes secreted into urine and amniotic fluid. Kidney Int 2007; 72: 1095-1102
99. Asea A, Jean-Pierre C, Kaur P, Rao P, Linhares IM, Skupski D et al. Heat shock protein-containing exosomes in mid-trimester amniotic fluids. J Reprod Immunol 2008; 79: 12-17
100. Bretz NP, Ridinger J, Rupp AK, Rimbach K, Keller S, Rupp C et al. Body fluid exosomes promote secretion of inflammatory cytokines in monocytic cells via Toll-like receptor signaling. J Biol Chem 2013; 288: 36691-36702
101. Francavilla F, Santucci R, Barbonetti A, Francavilla S. Naturallyoccurring antisperm antibodies in men: interference with fertility and clinical implications. An update. Front Biosci 2007; 12: 2890-2911
102. Allegrucci C, Ronquist G, Ove Nilsson B, Carlsson L, Lundqvist M, Minelli A et al. Circulating human antisperm antibodies recognize prostasomes. Am J Reprod Immunol 2001; 46: 211-219
103. Carlsson L, Ronquist G, Nilsson BO, Larsson A. Dominant prostasome immunogens for sperm-agglutinating autoantibodies of infertile men. J Androl 2004; 25: 699-705
104. Tavoosidana G, Ronquist G, Darmanis S, Yan J, Carlsson L, Wu D et al. Multiple recognition assay reveals prostasomes as promising plasma biomarkers for prostate cancer. Proc Natl Acad Sci USA 2011; 108: 8809-8814
105. Tannetta D, Sargent I. Placental disease and the maternal syndrome of preeclampsia: missing links? Curr Hypertens Rep 2013; 15: 590-599
106. Burton GJ, Jauniaux E. Placental oxidative stress: from miscarriage to preeclampsia. J Soc Gynecol Investig 2004; 11: 342-52
107. Redman CW, Sargent IL. Latest advances in understanding preeclampsia. Science 2005; 308: 1592-4
108. Goswami D, Tannetta DS, Magee LA, Fuchisawa A, Redman CW, Sargent IL et al. Excess syncytiotrophoblast microparticle shedding is a feature of early-onset pre-eclampsia, but not normotensive intrauterine growth restriction. Placenta 2006; 27: 56-61
109. Chen Y, Huang Y, Jiang R, Teng Y. Syncytiotrophoblast-derived microparticle shedding in early-onset and late-onset severe preeclampsia. Int J Gynaecol Obstet 2012; 119: 234-238
110. Marques F, Campos FM, Filho OA, Carvalho AT, Dusse LM, Gomes KB. Circulating microparticles in severe preeclampsia. Clin Chim Acta 2012; 414: 253-258
111. Redman CW. Preeclampsia: a multi-stress disorder. Rev Med Interne 2011; 32(Suppl 1): S41-S44
112. Holder BS, Tower CL, Jones CJ, Aplin JD, Abrahams VM. Heightened pro-inflammatory effect of preeclamptic placental microvesicles on peripheral blood immune cells in humans. Biol Reprod 2012; 86: 103.
113. Cester N, Staffolani R, Rabini RA, Magnanelli R, Salvolini E, Galassi R et al. Pregnancy induced hypertension: a role for peroxidation in microvillus plasma membranes. Mol Cell Biochem 1994; 131: 151-155
114. Macey MG, Bevan S, Alam S, Verghese L, Agrawal S, Beski S et al. Platelet activation and endogenous thrombin potential in preeclampsia. Thromb Res 2010; 125: e76-e81
115. Gardiner C, Tannetta DS, Simms CA, Harrison P, Redman CW, Sargent IL. Syncytiotrophoblast microvesicles released from preeclampsia placentae exhibit increased tissue factor activity. PLoS ONE 2011; 6: e26313.
116. Reverdiau P, Jarousseau AC, Thibault G, Khalfoun B, Watier H, Lebranchu Y et al. Tissue factor activity of syncytiotrophoblast plasma membranes and tumoral trophoblast cells in culture. Thromb Haemost 1995; 73: 49-54
117. Smarason AK, Sargent IL, Starkey PM, Redman CW. The effect of placental syncytiotrophoblast microvillous membranes from normal and pre-eclamptic women on the growth of endothelial cells in vitro. Br J Obstet Gynaecol 1993; 100: 943-949
118. Gupta AK, Rusterholz C, Huppertz B, Malek A, Schneider H, Holzgreve W et al. A comparative study of the effect of three different syncytiotrophoblast micro-particles preparations on endothelial cells. Placenta 2005; 26: 59-66
119. Hoegh AM, Tannetta D, Sargent I, Borup R, Nielsen FC, Redman C et al. Effect of syncytiotrophoblast microvillous membrane treatment on gene expression in human umbilical vein endothelial cells. Br J Obstet Gynaecol 2006; 113: 1270-1279
120. Cockell AP, Learmont JG, Smarason AK, Redman CW, Sargent IL, Poston L. Human placental syncytiotrophoblast microvillous membranes impair maternal vascular endothelial function. Br J Obstet Gynaecol 1997; 104: 235-240
121. von Dadelszen P, Hurst G, Redman CW. Supernatants from cocultured endothelial cells and syncytiotrophoblast microvillous membranes activate peripheral blood leukocytes in vitro. Hum Reprod 1999; 14: 919-924
122. Blumenstein M, McMaster MT, Black MA, Wu S, Prakash R, Cooney J et al. A proteomic approach identifies early pregnancy biomarkers for preeclampsia: novel linkages between a predisposition to preeclampsia and cardiovascular disease. Proteomics 2009; 9: 2929-2945
123. Rasanen J, Girsen A, Lu X, Lapidus JA, Standley M, Reddy A et al. Comprehensive maternal serum proteomic profiles of preclinical and clinical preeclampsia. J Proteome Res 2010; 9: 4274-4281