Hypoxia-induced changes in the bioactivity of cytotrophoblast-derived exosomes

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Salomon, Carlos ^a   Kobayashi, Miharu ^a   Ashman, Keith ^a   Sobrevia, Luis ^a,b   Mitchell, Murray D ^a   Rice, Gregory E ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE; DISPASE; GELATINASE B; MITOGEN ACTIVATED PROTEIN KINASE P38; TRANSFORMING GROWTH FACTOR BETA; TRYPSIN; VASCULOTROPIN; OXYGEN; PROTEOME;

ARTICLE; BIOLOGICAL ACTIVITY; CELL COMMUNICATION; CELL CULTURE; CELL HYPOXIA; CELL INVASION; CELL ISOLATION; CELL MIGRATION; CELL PROLIFERATION; CELL RELEASE; CELLULAR DISTRIBUTION; CELLULAR PARAMETERS; CENTRIFUGATION; CONTROLLED STUDY; CORRELATIONAL STUDY; CYTOTROPHOBLAST; EXOSOME; EXTRAVILLOUS TROPHOBLAST; FEMALE; FETOPLACENTAL UNIT; FETUS (ANATOMY); FIRST TRIMESTER PREGNANCY; HUMAN; HUMAN CELL; MOLECULAR IMAGING; OXYGEN TENSION; PHENOTYPE; PROTEIN CONTENT; PROTEIN LOCALIZATION; PROTEIN SECRETION; TROPHOBLAST; ANOXIA; CELL MOTION; METABOLISM; PREGNANCY; PROTEIN PROTEIN INTERACTION; PROTEOMICS; SIGNAL TRANSDUCTION;

ANOXIA; CELL MOVEMENT; CELL PROLIFERATION; EXOSOMES; FEMALE; HUMANS; OXYGEN; PREGNANCY; PROTEIN INTERACTION MAPS; PROTEOME; PROTEOMICS; SIGNAL TRANSDUCTION; TROPHOBLASTS;

EID: 84892676248     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079636     Document Type: Article

References (37)

1. Burton GJ, Jauniaux E, Charnock-Jones DS (2010) The influence of the intrauterine environment on human placental development. Int J Dev Biol 54: 303-312.
2. Rodesch F, Simon P, Donner C, Jauniaux E (1992) Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet Gynecol 80: 283-285.
3. Jauniaux E, Gulbis B, Burton GJ (2003) Physiological implications of the materno-fetal oxygen gradient in human early pregnancy. Reprod Biomed Online 7: 250-253. (Pubitemid 37121075)
4. Kaufmann P, Black S, Huppertz B (2003) Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol Reprod 69: 1-7. (Pubitemid 36806800)
5. Lyall F (2006) Mechanisms regulating cytotrophoblast invasion in normal pregnancy and pre-eclampsia. Aust N Z J Obstet Gynaecol 46: 266-273.
6. Jauniaux E, Van Oppenraaij RH, Burton GJ (2010) Obstetric outcome after early placental complications. Curr Opin Obstet Gynecol 22: 452-457.
7. Barker DJ (2007) The origins of the developmental origins theory. J Intern Med 261: 412-417.
8. Lash GE, Otun HA, Innes BA, Bulmer JN, Searle RF, et al. (2006) Low oxygen concentrations inhibit trophoblast cell invasion from early gestation placental explants via alterations in levels of the urokinase plasminogen activator system. Biol Reprod 74: 403-409. (Pubitemid 43122292)
9. Zhao H, Jiang Y, Cao Q, Hou Y, Wang C (2012) Role of integrin switch and transforming growth factor Beta 3 in hypoxia-induced invasion inhibition of human extravillous trophoblast cells. Biol Reprod 87: 47.
10. Salomon C, Ryan J, Sobrevia L, Kobayashi M, Ashman K, et al. (2013) Exosomal Signaling during Hypoxia Mediates Microvascular Endothelial Cell Migration and Vasculogenesis. PLoS One 8: e68451.
11. Ludwig AK, Giebel B (2012) Exosomes: small vesicles participating in intercellular communication. Int J Biochem Cell Biol 44: 11-15.
12. Yang C, Robbins PD (2011) The roles of tumor-derived exosomes in cancer pathogenesis. Clin Dev Immunol 2011: 842849.
13. Yang M, Chen J, Su F, Yu B, Su F, et al. (2011) Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer 10: 117.
14. Thery C, Zitvogel L, Amigorena S (2002) Exosomes: composition, biogenesis and function. Nat Rev Immunol 2: 569-579. (Pubitemid 37328732)
15. Mincheva-Nilsson L, Baranov V (2010) The role of placental exosomes in reproduction. Am J Reprod Immunol 63: 520-533.
16. Redman CW, Sargent IL (2008) Circulating microparticles in normal pregnancy and pre-eclampsia. Placenta 29 Suppl A: S73-77.
17. Hedlund M, Nagaeva O, Kargl D, Baranov V, Mincheva-Nilsson L (2011) Thermal- and oxidative stress causes enhanced release of NKG2D ligand-bearing immunosuppressive exosomes in leukemia/lymphoma T and B cells. PLoS One 6: e16899.
18. Maloyan A, Mele J, Muralimanohara B, Myatt L (2012) Measurement of mitochondrial respiration in trophoblast culture. Placenta 33: 456-458.
19. Thery C, Amigorena S, Raposo G, Clayton A (2006) Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol Chapter 3: Unit 3 22.
20. Mincheva-Nilsson L, Nagaeva O, Chen T, Stendahl U, Antsiferova J, et al. (2006) Placenta-derived soluble MHC class I chain-related molecules downregulate NKG2D receptor on peripheral blood mononuclear cells during human pregnancy: a possible novel immune escape mechanism for fetal survival. J Immunol 176: 3585-3592. (Pubitemid 43364006)
21. Graham CH, Hawley TS, Hawley RG, MacDougall JR, Kerbel RS, et al. (1993) Establishment and characterization of first trimester human trophoblast cells with extended lifespan. Exp Cell Res 206: 204-211. (Pubitemid 23212937)
22. Irving JA, Lysiak JJ, Graham CH, Hearn S, Han VK, et al. (1995) Characteristics of trophoblast cells migrating from first trimester chorionic villus explants and propagated in culture. Placenta 16: 413-433.
23. Thon JN, Devine MT, Jurak Begonja A, Tibbitts J, Italiano JE, Jr. (2012) High-content live-cell imaging assay used to establish mechanism of trastuzumab emtansine (T-DM1) -mediated inhibition of platelet production. Blood 120: 1975-1984.
24. Soares MJ, Chakraborty D, Renaud SJ, Kubota K, Bu P, et al. (2012) Regulatory pathways controlling the endovascular invasive trophoblast cell lineage. J Reprod Dev 58: 283-287.
25. Rosario GX, Konno T, Soares MJ (2008) Maternal hypoxia activates endovascular trophoblast cell invasion. Dev Biol 314: 362-375.
26. Lunghi L, Ferretti ME, Medici S, Biondi C, Vesce F (2007) Control of human trophoblast function. Reprod Biol Endocrinol 5: 6.
27. Lasser C, Eldh M, Lotvall J (2012) Isolation and characterization of RNA-containing exosomes. J Vis Exp: e3037.
28. King HW, Michael MZ, Gleadle JM (2012) Hypoxic enhancement of exosome release by breast cancer cells. BMC Cancer 12: 421.
29. Zhang HC, Liu XB, Huang S, Bi XY, Wang HX, et al. (2012) Microvesicles Derived from Human Umbilical Cord Mesenchymal Stem Cells Stimulated by Hypoxia Promote Angiogenesis Both In Vitro and In Vivo. Stem Cells Dev.
30. Park JE, Tan HS, Datta A, Lai RC, Zhang H, et al. (2010) Hypoxic tumor cell modulates its microenvironment to enhance angiogenic and metastatic potential by secretion of proteins and exosomes. Mol Cell Proteomics 9: 1085-1099.
31. Jauniaux E, Watson AL, Hempstock J, Bao YP, Skepper JN, et al. (2000) Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. Am J Pathol 157: 2111-2122.
32. Harris LK (2010) Review: Trophoblast-vascular cell interactions in early pregnancy: how to remodel a vessel. Placenta 31 Suppl: S93-98.
33. Crocker IP, Wareing M, Ferris GR, Jones CJ, Cartwright JE, et al. (2005) The effect of vascular origin, oxygen, and tumour necrosis factor alpha on trophoblast invasion of maternal arteries in vitro. J Pathol 206: 476-485. (Pubitemid 41025351)
34. Vitoratos N, Hassiakos D, Iavazzo C (2012) Molecular mechanisms of preeclampsia. J Pregnancy 2012: 298343.
35. Genbacev O, Joslin R, Damsky CH, Polliotti BM, Fisher SJ (1996) Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J Clin Invest 97: 540-550. (Pubitemid 26039422)
36. Onogi A, Naruse K, Sado T, Tsunemi T, Shigetomi H, et al. (2011) Hypoxia inhibits invasion of extravillous trophoblast cells through reduction of matrix metalloproteinase (MMP)-2 activation in the early first trimester of human pregnancy. Placenta 32: 665-670.
37. Graham CH, Fitzpatrick TE, McCrae KR (1998) Hypoxia stimulates urokinase receptor expression through a heme protein-dependent pathway. Blood 91: 3300-3307. (Pubitemid 28193880)