High levels of circulating extracellular vesicles with altered expression and function during pregnancy

Immunobiology

Volumn 221, Issue 7, 2016, Pages 753-760

  Nardi, Fabiola da Silva ^a,b,c   Michelon, Tatiana Ferreira ^d   Neumann, Jorge ^d   Manvailer, Luis Felipe Santos ^b,c   Wagner, Bettina ^b   Horn, Peter A ^b   Bicalho, Maria da Graça ^a   Rebmann, Vera ^b  

^a FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

^b UNIVERSITY HOSPITAL ESSEN   (Germany)

^c MINISTRY OF EDUCATION OF BRAZIL   (Brazil)

^d Reproductive Immunology Centre   (Brazil)

Author keywords

Caspase 3 activity; Extracellular vesicles; IL 10; NK cells; Pregnancy; TGF 1

Indexed keywords

BIOLOGICAL MARKER; CASPASE 3; CD56 ANTIGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; NANOPARTICLE; TRANSFORMING GROWTH FACTOR BETA1;

ADULT; ANALYTIC METHOD; ARTICLE; CELL FUNCTION; CELL TRANSPORT; CONTROLLED STUDY; DENSITOMETRY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXOSOME; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOREGULATION; MATERNAL BLOOD; NANOPARTICLE TRACKING ANALYSIS; NATURAL KILLER CELL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PREGNANT WOMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; SECOND TRIMESTER PREGNANCY; ULTRACENTRIFUGATION; WESTERN BLOTTING; CELL CULTURE; CELL SEPARATION; GENE EXPRESSION REGULATION; IMMUNOLOGY; METABOLISM; MIDDLE AGED; PREGNANCY; YOUNG ADULT;

ADULT; CASPASE 3; CD56 ANTIGEN; CELL SEPARATION; CELLS, CULTURED; EXTRACELLULAR VESICLES; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-10; KILLER CELLS, NATURAL; MIDDLE AGED; PREGNANCY; TRANSFORMING GROWTH FACTOR BETA1; YOUNG ADULT;

EID: 84962487967     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2016.03.001     Document Type: Article

References (56)

1. Abrahams V.M., Straszewski-Chavez S.L., Guller S., Mor G. First trimester trophoblast cells secrete Fas ligand which induces immune cell apoptosis. Mol. Hum. Reprod. 2004, 10:55.
2. Admyre C., Johansson S.M., Paulie S., Gabrielsson S. Direct exosome stimulation of peripheral human T cells detected by ELISPOT. Eur. J. Immunol. 2006, 36:1772.
3. Alijotas-Reig J., Palacio-Garcia C., Llurba E., Vilardell-Tarres M. Cell-derived microparticles and vascular pregnancy complications: a systematic and comprehensive review. Fertil. Steril. 2013, 99:441.
4. Babst M. MVB vesicle formation: eSCRT-dependent, ESCRT-independent and everything in between. Curr. Opin. Cell Biol. 2011, 23:452.
5. Balaj L., Lessard R., Dai L., Cho Y.J., Pomeroy S.L., Breakefield X.O., Skog J. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat. Commun. 2011, 2:180.
6. Beer A.E., Kwak J.Y., Ruiz J.E. Immunophenotypic profiles of peripheral blood lymphocytes in women with recurrent pregnancy losses and in infertile women with multiple failed in vitro fertilization cycles. Am. J. Reprod. Immunol. 1996, 35:376.
7. Caby M.P., Lankar D., Vincendeau-Scherrer C., Raposo G., Bonnerot C. Exosomal-like vesicles are present in human blood plasma. Int. Immunol. 2005, 17:879.
8. Caradec J., Kharmate G., Hosseini-Beheshti E., Adomat H., Gleave M., Guns E. Reproducibility and efficiency of serum-derived exosome extraction methods. Clin. Biochem. 2014, 47:1286.
9. Chantakru S., Miller C., Roach L.E., Kuziel W.A., Maeda N., Wang W.C., Evans S.S., Croy B.A. Contributions from self-renewal and trafficking to the uterine NK cell population of early pregnancy. J. Immunol. 2002, 168:22.
10. Cheng S.B., Sharma S. Interleukin-10: a pleiotropic regulator in pregnancy. Am. J. Reprod. Immunol. 2014.
11. Chernyshov V.P., Dons'koi B.V., Sudoma I.O., Goncharova Y.O. Favorable immune phenotype predicts successful implantation and pregnancy. Immunol. Lett. 2014, 162:217.
12. Clark D.A., Coker R. Transforming growth factor-beta (TGF-beta). Int. J. Biochem. Cell Biol. 1998, 30:293.
13. Cooper M.A., Fehniger T.A., Caligiuri M.A. The biology of human natural killer-cell subsets. Trends Immunol. 2001, 22:633.
14. Dai C., Krantz S.B. Interferon gamma induces upregulation and activation of caspases 1, 3, and 8 to produce apoptosis in human erythroid progenitor cells. Blood 1999, 93:3309.
15. Dragovic R.A., Southcombe J.H., Tannetta D.S., Redman C.W., Sargent I.L. Multicolor flow cytometry and nanoparticle tracking analysis of extracellular vesicles in the plasma of normal pregnant and pre-eclamptic women. Biol. Reprod. 2013, 89:151.
16. Frangsmyr L., Baranov V., Nagaeva O., Stendahl U., Kjellberg L., Mincheva-Nilsson L. Cytoplasmic microvesicular form of Fas ligand in human early placenta: switching the tissue immune privilege hypothesis from cellular to vesicular level. Mol. Hum. Reprod. 2005, 11:35.
17. Franzen C.A., Simms P.E., Van Huis A.F., Foreman K.E., Kuo P.C., Gupta G.N. Characterization of uptake and internalization of exosomes by bladder cancer cells. Biomed. Res. Int. 2014, 2014:619829.
18. Germain S.J., Sacks G.P., Sooranna S.R., Sargent I.L., Redman C.W. Systemic inflammatory priming in normal pregnancy and preeclampsia: the role of circulating syncytiotrophoblast microparticles. J. Immunol. 2007, 178:5949.
19. Gotsch F., Romero R., Friel L., Kusanovic J.P., Espinoza J., Erez O., Than N.G., Mittal P., Edwin S., Yoon B.H., Kim C.J., Mazaki-Tovi S., Chaiworapongsa T., Hassan S.S. CXCL10/IP-10: a missing link between inflammation and anti-angiogenesis in preeclampsia?. J. Maternal-Fetal Neonatal Med. 2007, 20:777.
20. Graham C.H., Lysiak J.J., McCrae K.R., Lala P.K. Localization of transforming growth factor-beta at the human fetal-maternal interface: role in trophoblast growth and differentiation. Biol. Reprod. 1992, 46:561.
21. Hanna N., Hanna I., Hleb M., Wagner E., Dougherty J., Balkundi D., Padbury J., Sharma S. Gestational age-dependent expression of IL-10 and its receptor in human placental tissues and isolated cytotrophoblasts. J. Immunol. 2000, 164:5721.
22. Hedlund M., Stenqvist A.C., Nagaeva O., Kjellberg L., Wulff M., Baranov V., Mincheva-Nilsson L. 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.
23. Hernandez-Valencia M., Zarate A., Ochoa R., Fonseca M.E., Amato D., De Jesus Ortiz M. Insulin-like growth factor I, epidermal growth factor and transforming growth factor beta expression and their association with intrauterine fetal growth retardation, such as development during human pregnancy. Diabetes Obes. Metab. 2001, 3:457.
24. Holder B.S., Tower C.L., Jones C.J., Aplin J.D., Abrahams V.M. Heightened pro-inflammatory effect of preeclamptic placental microvesicles on peripheral blood immune cells in humans. Biol. Reprod. 2012, 86:103.
25. Hunter C.A., Reiner S.L. Cytokines and T cells in host defense. Curr. Opin. Immunol. 2000, 12:413.
26. Hunter M.P., Ismail N., Zhang X., Aguda B.D., Lee E.J., Yu L., Xiao T., Schafer J., Lee M.L., Schmittgen T.D., Nana-Sinkam S.P., Jarjoura D., Marsh C.B. Detection of microRNA expression in human peripheral blood microvesicles. PLoS One 2008, 3:e3694.
27. Keller S., Rupp C., Stoeck A., Runz S., Fogel M., Lugert S., Hager H.D., Abdel-Bakky M.S., Gutwein P., Altevogt P. CD24 is a marker of exosomes secreted into urine and amniotic fluid. Kidney Int. 2007, 72:1095.
28. Kharaziha P., Ceder S., Li Q., Panaretakis T. Tumor cell-derived exosomes: a message in a bottle. Biochim. Biophys. Acta 2012, 1826:103.
29. Kordelas L., Rebmann V., Ludwig A.K., Radtke S., Ruesing J., Doeppner T.R., Epple M., Horn P.A., Beelen D.W., Giebel B. MSC-derived exosomes: a novel tool to treat therapy-refractory graft-versus-host disease. Leukemia 2014, 28:970.
30. Liu Y., Lu Q. Extracellular vesicle microRNAs: biomarker discovery in various diseases based on RT-qPCR. Biomark. Med. 2015, 9:791.
31. Lotvall J., Hill A.F., Hochberg F., Buzas E.I., Di Vizio D., Gardiner C., Gho Y.S., Kurochkin I.V., Mathivanan S., Quesenberry P., Sahoo S., Tahara H., Wauben M.H., Witwer K.W., Thery C. Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the international society for extracellular vesicles. J. Extracell. Vesicles 2014, 3:26913.
32. Ludwig A.K., Giebel B. Exosomes: small vesicles participating in intercellular communication. Int. J. Biochem. Cell Biol. 2012, 44:11.
33. 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.
34. Mulcahy L.A., Pink R.C., Carter D.R. Routes and mechanisms of extracellular vesicle uptake. J. Extracell. Vesicles 2014, 3.
35. Redman C.W., Sargent I.L. Microparticles and immunomodulation in pregnancy and pre-eclampsia. J. Reprod. Immunol. 2007, 76:61.
36. Salomon C., Torres M.J., Kobayashi M., Scholz-Romero K., Sobrevia L., Dobierzewska A., Illanes S.E., Mitchell M.D., Rice G.E. A gestational profile of placental exosomes in maternal plasma and their effects on endothelial cell migration. PLoS One 2014, 9:e98667.
37. Sarker S., Scholz-Romero K., Perez A., Illanes S.E., Mitchell M.D., Rice G.E., Salomon C. Placenta-derived exosomes continuously increase in maternal circulation over the first trimester of pregnancy. J. Transl. Med. 2014, 12:204.
38. Simpson H., Robson S.C., Bulmer J.N., Barber A., Lyall F. Transforming growth factor beta expression in human placenta and placental bed during early pregnancy. Placenta 2002, 23:44.
39. Singh M., Orazulike N.C., Ashmore J., Konje J.C. Changes in maternal serum transforming growth factor beta-1 during pregnancy: a cross-sectional study. Biomed. Res. Int. 2013, 2013:318464.
40. Sohda M., Misumi Y., Oda K. TNFalpha triggers release of extracellular vesicles containing TNFR1 and TRADD, which can modulate TNFalpha responses of the parental cells. Arch. Biochem. Biophys. 2015, 587:31.
41. 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 2011, 87:146.
42. Southcombe J., Tannetta D., Redman C., Sargent I. The immunomodulatory role of syncytiotrophoblast microvesicles. PLoS One 2011, 6:e20245.
43. Stenqvist A.C., 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.
44. Tannetta D., Dragovic R., Alyahyaei Z., Southcombe J. Extracellular vesicles and reproduction-promotion of successful pregnancy. Cell. Mol. Immunol. 2014, 11:548.
45. Taylor D.D., Akyol S., Gercel-Taylor C. Pregnancy-associated exosomes and their modulation of T cell signaling. J. Immunol. 2006, 176:1534.
46. Tessier D.R., Yockell-Lelievre J., Gruslin A. Uterine spiral artery remodeling: the role of uterine natural killer cells and extravillous trophoblasts in normal and high-risk human pregnancies. Am. J. Reprod. Immunol. 2014.
47. Thery C., Duban L., Segura E., Veron P., Lantz O., Amigorena S. Indirect activation of naive CD4+ T cells by dendritic cell-derived exosomes. Nat. Immunol. 2002, 3:1156.
48. Thery C., Ostrowski M., Segura E. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 2009, 9:581.
49. Toth B., Lok C.A., Boing A., Diamant M., van der Post J.A., Friese K., Nieuwland R. Microparticles and exosomes: impact on normal and complicated pregnancy. Am. J. Reprod. Immunol. 2007, 58:389.
50. Van Deun J., Mestdagh P., Sormunen R., Cocquyt V., Vermaelen K., Vandesompele J., Bracke M., De Wever O., Hendrix A. The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling. J. Extracell. Vesicles 2014, 3.
51. Vlassov A.V., Magdaleno S., Setterquist R., Conrad R. Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim. Biophys. Acta 2012, 1820:940.
52. Yagel S., Goldman-Wohl D.S., Mandelboim O., Hanna Y., Hochner-Celnikier D. Maternal adaptation to vasculogenesis and angiogenesis at the feto-maternal interface. Thromb. Res. 2005, 115(Suppl. 1):97.
53. Yuana Y., Sturk A., Nieuwland R. Extracellular vesicles in physiological and pathological conditions. Blood Rev. 2013, 27:31.
54. Zhang H.G., Zhuang X., Sun D., Liu Y., Xiang X., Grizzle W.E. Exosomes and immune surveillance of neoplastic lesions: a review. Biotech. Histochem. 2012, 87:161.
55. Zlotogorski-Hurvitz A., Dayan D., Chaushu G., Korvala J., Salo T., Sormunen R., Vered M. Human saliva-derived exosomes: comparing methods of isolation. J. Histochem. Cytochem. 2014.
56. van Dommelen S.M., Vader P., Lakhal S., Kooijmans S.A., van Solinge W.W., Wood M.J., Schiffelers R.M. Microvesicles and exosomes: opportunities for cell-derived membrane vesicles in drug delivery. J. Controlled Release 2012, 161:635.