Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGFβ3

Journal of Clinical Investigation

Volumn 105, Issue 5, 2000, Pages 577-587

  Caniggia, Isabella ^a,b,c,e   Mostachfi, Homa ^b   Winter, Jennifer ^b,c   Gassmann, Max ^d   Lye, Stephen J ^b,c   Kuliszewski, Maciej ^a   Post, Martin ^a,c  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF ZURICH   (Switzerland)

^e MOUNT SINAI HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRONECTIN; GELATINASE A; HYPOXIA INDUCIBLE FACTOR 1; INTEGRIN; TRANSFORMING GROWTH FACTOR BETA3;

ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; ENZYME ACTIVITY; HUMAN; HUMAN TISSUE; OXYGEN TENSION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; TROPHOBLAST;

EID: 0034100836     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI8316     Document Type: Article

References (46)

1. Cross, J.C., Werb, Z., and Fisher, S.J. 1994. Implantation and the placenta: key pieces of the development puzzle. Science. 266:1508 1518.
2. Strickland, S., and Richards, W.G. 1992. Invasion of trophoblasts. Cell. 71:355 357.
3. Aplin, J.D. 1991. Implantation, trophoblast differentiation and haemochorial placentation: mechanistic evidence in vivo and in vitro. J. Cell Sci. 99:681-692.
4. Rodesch, F., Simon, P., Donner, C., and Jaumaux, E. 1992. Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet. Gynecol. 80:283-285.
5. Genbacev, O., Joslin, R., Damsky, C.H., Polliotti, B.M., and Fisher, S.J. 1996. Hypoxia alters early gestation human cytotrophoblast ditterentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J. Clin. Invest. 97:540 550.
6. Semenza, G.L., and Wang, G.L. 1992. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriprional activation. Mol. Cell. Biol. 12:5447 5454.
7. Forsythe, J.A,. et al. 1996. Activation of vascular endothelial growth factor gene transcription by hypoxia inducible factor 1. Mol. Cell. Biol. 16:4604-4613.
8. Semenza, G.L., Roth, P.H., Fang, H.-M., and Wang, G.L. 1994. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia inducible factor 1. J. Biol. Chem. 269:23757-23763.
9. Melillo, G., et al. 1995. A hypoxia responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J. Exp. Med. 182:1683-1693.
10. Wenger, R.H., and Gassmann, M. 1997. Oxygen(es) and tinhypoxia-inducible factor-1. J. Biol. Chem. 378:609-616.
11. Wang, G.L., and Semenza, G.L. 1993. General involvement of hypoxia inducible factor 1 in transcriptional response to hypoxia. Proc. Natl. Acad. Sci. USA. 90:4304-4308.
12. Wang, G.L., Jiang, B.H., Rueand, E.A., and Semenza, G.L. 1995. Hypoxia inducible factor 1 is a basic helix-loop-helix PAS hererodimer regulated by cellular O2 tension. Proc. Natl Acad. Sci. USA. 92:5510-5514.
13. Maxwell, P.H., et al. 1999. The tumor suppressor protein VHL targets hypoxia-inducihle factors for oxygen-dependent proteolysis. Nature. 399:271-275.
14. Caniggia, I., Grisaru-Gravnoskt, S., Kuliszewski, M., Post, M., and Lye, S.J. 1999. Inhibition of TGFβ, restores the invasive capability of extravillous trophoblast in preeclamptic pregnancies. J. Clin. Invest. 103:1641-1650.
15. Caniggia, I., Taylor, C.V., Ritchie, J.W.K.. Lye, S.J., and Letarte, M. 1997. Endoglin regulates trophoblast differentiation along the invasive pathway in human placental villous expiants. Endocrinology. 138:4977-4988.
16. Malcolm, A.D. 1992. Uses of antisense nucleic acids: an introduction. Biochem. Soc. Trans. 20:745-746.
17. Wang, J., et al. 1995. Cloning and characterization of glucocorticoids induced genes in feral rat lung fibroblasts: transforming growth factor β3. J. Biol. Chem. 270:2722-2728.
18. Camenisch, G., et al. 1999. General applicability of chicken egg yolk antibodies: the performance of IgY immunoglobulins raised against the hypoxia-inducible factor Iα. FASEB J. 13:81-88.
19. Braissant, O., and Wahli, W. 1998. A simplified in situ hybridisation protocol using non-radioactive labeled probes to detect abundant and rare mRNAs on tissue sections. Biochemica. 1:10-16.
20. Engvall, E., and Ruoslhati, F., 1977. Binding of soluble form of fibroblast surface protein, fibronectin, to collagen. Int. J. Cancer. 20:1 -5.
21. Caniggia, I., Lye, S. J. L., and Cross, J.C. 1997. Activin is a local regulator of human cytotrophoblast cell differentiation. Endocrinology. 138:3976-3986.
22. Zhou, Y., Genbacev, O., Damsky, C.H., and Fisher, S.J. 1998. Oxygen regulates human cytotrophoblast differentiation and invasion: implications for endovascular invasion in normal pregnancy and in pre-eclampsia. J Reprod. Immunol. 39:197-213.
23. Fisher, S.J., et al. 1989. Adhesive and degradative properties of human placental cytotrophoblast cells in vitro. J. Cell Biol. 109:891-902.
24. Librach, C.L., et al. 1991. 92-kD type IV collagenase mediates invasion of human cytotrophoblast. J. Cell Biol. 113:437-449.
25. Zhou, Y., et al. 1997. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. J. Clin. Invest. 99:2139 2151.
26. Damsky, C.H., et al. 1994. Integrin switching regulates normal trophoblast invasion. Development. 120:3657-3666.
27. Bischof, P., Redard, M., Gindre, P., Vassilakos, P., and Campana, A. 1993. Localization of alpha2, alpha5 and alpha6 inregrin subunits in human endometrium. decidua and trophoblast. Eur. J. Obstet. Gynecol. Reprod. Biol. 51:217-226.
28. Fox, H., and Path, M.C. 1970. Effect of hypoxia on trophoblast in organ culture. Am. J. Obstet. Gynecol. 107:1058-1064.
29. Aplin, J.D., Haigh, T., Jones, C.J.P., Church, H.J., and Vicovac, L. 1999. Development of cytorrophoblast columns from explanted first-trimester human placental villi: role of fibronectin and integrin α5β1. Biol. Reprod. 60:828 838.
30. Benyo, D.F., Miles, T.M., and Conrad, K.P. 1997. Hypoxia stimulates cytokine production by villous explants from the human placenta. J. Clin. Enadocrinol. Metab. 82:1582 1588.
31. Conrad, K.P., and Benyo, D.B. 1997. Placental cytokines and the pathogenesis ot preeclampsia. Am. J. Reprod. Immunol. 37:240-249.
32. Taylor, C.M., Stevens, H., Anthony, F.W., and Wheeler, T. 1997. Influence of hypoxia on vascular endothelial growth factor and chorionic gonadotrophin production in trophoblast-derived cell lines: JEG,Jar and BeWo. Placenta. 18:451-458.
33. Fitzpatrick, T.E., and Graham, C.H. 1998. Stimulation of plasminogen activator inhihitor-1 expression in ummortalized human trophoblast cells cultured under low levels of oxygen. Exp. Cell Res. 245:155-162.
34. Alsat, E., et al. 1996. Hypoxia impairs cell fusion and differentiation process in human cytotrophoblast, in vitro. J. Cell. Physiol. 168:346 353.
35. Janatpour, M.J., et al. 1999. A repertoire of differentially expressed transcription factors that offers insight into mechanisms of human cytotrophoblast differentiation. Dev. Genet. 25:146 157.
36. Carmeliet, P., et al. 1998. Role of HIF-1α in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature. 394:485 490.
37. Genbacev, O., Zhou, Y., Ludlow, J.W., and Fisher, S.J. 1997. Regulation of human placental development by oxygen tension. Science. 277:1669-1672.
38. Ryan, H.E., Lo, J., and Johnson, R.S. 1988. HIF-1α is required for solid tumor formation and embryonic vascularization. EMBO J. 17:3005 3015.
39. Maltepe, E., Schmidt, J.V., Baunoch, D., Bradfieldand, C.A., and Simon, M.C, 1997. Abnormal angiogenesis and response to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature. 386:403 407.
40. Kozak, K.R., Abbott, B., and Hankinson, O. 1997. ARNT deficient mice and placental differentiation. Dev. Biol. 191:297 305.
41. Salceda, S., and Caro, J. 1997. Hypoxia-inducible factor 1α (HIF-1α) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilizatoin by hypoxia depends on redox-induced changes. J. Biol. Chem. 272:22642 22647.
42. Goldberg, M.A., Dunning, S.P., and Bunn, H.F. 1988. Regulation of the erythropoietin gene: evidence that the oxygen sensor is a heme protein. Science 242:1412-1415.
43. Zhou, Y., Damsky, C.H., Chiu, K., Roberts, J. M., and Fisher, S.J. 1993. Preeclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts. J. Clin. Invest. 91:950-960.
44. Zhou, Y., Damsky, C.H., and Fisher, S.J. 1997. Preeclampsia is associated with failure of human cytotrophoblast to mimic a vascular adhesion phenotype. J. Clin. Invest. 99:2152-2164.
45. Redline, R.W., and Patterson, P. 1995. Pre-eclampsia is associated with an excess ot proliferative immature intermediate trophoblast. Hum. Pathol. 26:594 600.
46. Kupferminc, M.J., Peaceman, A.M., Wigton, T.R., Rehnberg, K.A., and Socol, M.A. 1995. Fetal fibronectin levels are elevated in maternal plasma and anmiotic fluid of patients with severe preeclampsia. Am. J. Obstet. Gynecol. 172:649 653.