Human cytotrophoblasts adopt a vascular phenotype as they differentiate: A strategy for successful endovascular invasion?

Journal of Clinical Investigation

Volumn 99, Issue 9, 1997, Pages 2139-2151

  Zhou, Yan ^a   Fisher, Susan J ^a   Janatpour, Mary ^a   Genbacev, Olga ^a   Dejana, Elisabetta ^b   Wheelock, Margaret ^c   Damsky, Caroline H ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^c UNIVERSITY OF TOLEDO   (United States)

^d HSW 604 UCSF   (United States)

Author keywords

cadherins; endothelium; integrins; placentation; trophoblast

Indexed keywords

CADHERIN; CD31 ANTIGEN; INTEGRIN; UVOMORULIN; VASCULAR CELL ADHESION MOLECULE 1;

ANTIGEN EXPRESSION; ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL INVASION; CHORIOCARCINOMA; CHORION VILLUS; CONTROLLED STUDY; CYTOTROPHOBLAST; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; PLACENTA CIRCULATION; PLACENTA DEVELOPMENT; PREECLAMPSIA; PRIORITY JOURNAL; UMBILICAL VEIN;

EID: 0030922747     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119387     Document Type: Article

References (48)

1. Brosens, I., and H.G. Dixon. 1966. The anatomy of the maternal side of the placenta. J. Obstet. Gynaecol. Br. Commonw. 73:357-363.
2. Boyd, J.D., and W.J. Hamilton. 1967. Development and structure of the human placenta from the end of the 3rd month of gestation. J. Obstet. Gynaecol. Br. Commonw. 74:161-226.
3. Enders, A.C. 1976. Anatomical aspects of implantation. J. Reprod. Fertil. (Suppl.)1-15.
4. Enders, A.C., and B.F. King. 1991. Early stages of trophoblastic invasion of the maternal vascular system during implantation in the macaque and baboon. Am. J. Anat. 192:329-346.
5. Damsky, C.H., A.E. Sutherland, and S.J. Fisher. 1993. Adhesive interactions in early mammalian embryogenesis, implantation and placentation. FASEB J. 7:1320-1328.
6. Cross, J.C., Z. Werb, and S.J. Fisher. 1994. Implantation and the placenta: key pieces of the development puzzle. Science (Wash. DC). 266:1508-1518.
7. Genbacev, O., R. Joslin, C.H. Damsky, B.M. Polliotti, and S.J. Fisher. 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.
8. Librach, C.L., Z. Werb, M.L. Fitzgerald, K. Chiu, N.M. Corwin, R.A. Esteves, D. Grobelny, R. Galardy, C.H. Damsky, and S.J. Fisher. 1991. 92-kD type IV collagenase mediates invasion of human cytotrophoblasts. J. Cell Biol. 113:437-449.
9. Kovats, S., C. Librach, P. Fisch, E.K. Main, P.M. Sondel, S.J. Fisher, and R. DeMars. 1990. Expression and possible function of the HLA-G chain in human cytotrophoblasts. Science (Wash. DC). 248:220-222.
10. McMaster, M.T., C.L. Librach, Y. Zhou, K.H. Lim, M.J. Janatpour, R. DeMars, S. Kovats, C. Damsky, and S.J. Fisher. 1995. Human placental HLA-G expression is restricted to differentiated cytotrophoblasts. J. Immunol. 154: 3771-3778.
11. Damsky, C.H., M.L. Fitzgerald, and S.J. Fisher. 1992. Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J. Clin. Invest. 89:210-222.
12. Vicovac, L., C.J. Jones, and J.D. Aplin. 1995. Trophoblast differentiation during formation of anchoring villi in a model of the early human placenta in vitro. Placenta. 16:41-56.
13. Damsky, C.H., C. Librach, K.H. Lim, M.L. Fitzgerald, M.T. McMaster, M. Janatpour, Y. Zhou, S.K. Logan, and S.J. Fisher. 1994. Integrin switching regulates normal trophoblast invasion. Development (Camb.). 120:3657-3666.
14. Brosens, I., W.B. Robertson, and H.G. Dixon. 1972. The role of the spiral arteries in the pathogenesis of pre-eclampsia. Obstet. Gynecol. 88:876-881.
15. Roberts, J.M., R.N. Taylor, S.A. Friedman, and A. Goldfien. 1990. New developments in pre-eclampsia. In Fetal Medical Review. W. Dunlop, editor. Edward Arnold, London. 125-141.
16. Redman, C.W. 1991. Current topic: pre-eclampsia and the placenta. Placenta. 12:301-308.
17. Redline, R.W., and P. Patterson. 1995. Pre-eclampsia is associated with an excess of proliferative immature intermediate trophoblast. Hum. Pathol. 26: 594-600.
18. Damsky, C.H., and S.J. Fisher. 1994. Changes in integrin expression reflect a stepwise differentiation program in mouse and human trophoblast. In Endocrinology of Embryo-Endometrium Interactions. S.R. Glasser, J. Mulholland, and A. Psychoyos, editors. Plenum Publishing Corporation, New York. 353-364.
19. Zhou, Y., C.H. Damsky, K. Chiu, J.M. Roberts, and S.J. Fisher. 1993. Preeclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts. J. Clin. Invest. 91:950-960.
20. Zhou, Y., C.H. Damsky, and S.J. Fisher. 1997. Preeclampsia is associated with failure of cytotrophoblasts to mimic a vascular adhesion phenolype: one cause of defective endovascular invasion in this syndrome? J. Clin. Invest. 99:2152-2164.
21. Fisher, S.J., T-Y. Cui, L. Zhang, L. Hartman, K. Grahl, J. Tarpey, and C. Damsky. 1989. Adhesive and degradative properties of human placental trophoblast cells in vitro. J. Cell Biol. 109:891-902.
22. Gallery, E. 1991. Isolation and purification of microvascular endothelium from human decidual tissue in the late phase of pregnancy. Am. J. Obstet. Gynecol. 165:191-196.
23. Wheelock, M.J., C.A. Buck, K. Bechtol, and C.H. Damsky. 1987. The 80 kD glycopeptide fragment of cell CAM 120/80 inhibits cell-cell adhesion. J. Cell. Biochem. 34:187-204.
24. Damsky, C.H., J. Richa, D. Solter, K.A. Knudsen, and C.A. Buck. 1983. Identification and purification of a cell surface glycoprotein involved in cell-cell interactions. Cell. 34:455-466.
25. Lampugnani, M.G., M. Corada, L. Caveda, F. Breviario, O. Ayalon, B. Geiger, and E. Dejana. 1995. The molecular organization of endothelial cell to cell junctions: differential association of plakoglobin, beta-catenin, and alpha-catenin with vascular endothelial cadherin (VE-cadherin). J. Cell Biol. 129:203-217.
26. Leach, L., P. Cleark, M.G. Lampugnani, A.G. Arroyo, E. Dejana, and J.A. Firth. 1993. Immunoelectron microscope characterization of the interendothelial junctions in human term placenta. J. Cell Sci. 104:1073-1081.
27. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
28. De, S.K., M.T. McMaster, S.K., Dey, and G.K. Andrews. 1989. Cell specific metallothionein gene expression in mouse decidua and placentae. Development (Camb.). 107:611-623.
29. Brooks, P.C., R.A.F. Clark, and D.A. Cheresh. 1994. Requirement of integrin αVβ3 for angiogenesis. Science (Wash. DC). 264:569-571.
30. Albelda, S.M., S.A. Mette, D.E. Elder, R. Stewaart, L. Damjanovich, M. Herlyn, and C.A. Buck. 1990. Integrin distribution in malignant melanoma: association of the beta 3 subunit with tumor progression. Cancer Res. 50:6757-6764.
31. Felding-Habermann, B., B.M. Mueller, C.A. Romerdahl, and D.A. Cheresh. 1992. Involvement of integrin alpha V gene expression in human melanoma tumorgenicity. J. Clin. Invest. 89:2018-2022.
32. Brooks, P.C., A.M.P. Montgomery, M. Rosenfeld, R.A. Reisfeld, T. Hu, G. Klier, and D.A. Cheresh. 1994. Integrin αVβ3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell. 79:1157-1164.
33. Takeichi, M. 1995. Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 7:619-627.
34. Suzuki, S., K. Sano, and H. Tanihara. 1991. Diversity of the cadherin family: evidence for eight new cadherins in nervous tissue. Cell Regul. 2:261-270.
35. Lampugnani, M.G., M. Resnati, M. Raiteri, R. Pigott, A. Pisacane, G. Houen, L.P. Ruco, and E. Dejana. 1992. A novel endothelial-specific membrane protein is a marker of cell-cell contacts. J. Cell Biol. 118:1511-1522.
36. Birchmeier, W. 1995. E-cadherin as a tumor (invasion) suppressor gene. Bioessays. 17:97-99.
37. Gumbiner, B.M. 1996. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell. 84:345-357.
38. Navarro, P., L. Caveda, F. Brevario, L. Mandoteanu, M.-G. Lampugnani, and E. Dejana. 1995. Catenin-dependent and catenin-independent functions of vascular endothelial cadherin. J. Biol. Chem. 270:30965-30972.
39. Hinck, L., I.S. Nathke, J. Papkoff, and W.J. Nelson. 1994. Dynamics of cadherin/catenin complex formation: novel protein interactions and pathways of complex assembly. J. Cell Biol. 125:1327-1340.
40. Blankenship, T.N., A.C. Enders, and B.F. King. 1993. Trophoblastic invasion and the development of uteroplacental arteries in the macaque: immunohistochemical localization of cytokeratins, desmin, type IV collagen, laminin, and fibronectin. Cell Tissue Res. 272:227-236.
41. Blankenship, T.N., A.C. Enders, and B.F. King. 1993. Trophoblastic invasion and modification of uterine veins during placental development in macaques. Cell Tissue Res. 274:135-144.
42. Belkin, V.M., A.M. Belkin, and V.E. Koteliansky. 1990. Human smooth muscle VLA-1 integrin: purification, substrate specificity, localization in aorta, and expression during development. J. Cell Biol. 111:2159-2170.
43. Risau, W., and I. Flamme. 1995. Vasculogenesis. Annu. Rev. Cell Dev. Biol. 11:73-91.
44. Heyward, S.A., N. Dubois-Stringfellow, R. Rapoport, and V.L. Bautch. 1995. Expression and inducibility of vascular adhesion receptors in development. FASEB J. 9:956-962.
45. Vittet, D., M.-H. Prandini, R. Perthier, A. Schweitzer, H. Martin-Sisteron. G. Uzan, and E. Dejana. 1996. Embryonic stem cells differentiate in vitro to endothelial cells through successive maturation steps. Blood. 88:3424-3431.
46. Ahmed, A., X.F. Li, C. Dunk, M.J. Whittle, D.I. Rushton, and T. Rollason. 1995. Colocalisation of vascular endothelial growth factor and its Flt-1 receptor in human placenta. Growth Factors. 12:235-243.
47. Clark, D.E., S.K. Smith, A.M. Sharkey, and D.S. Charnock-Jones. 1996. Localization of vascular endothelial growth factor and expression of its receptors flt and KDR in human placenta throughout pregnancy. Hum. Reprod. (Oxf.). 11:1090-1098.
48. Shiraishi, S., K. Nakagawa, N. Kinukawaf, H. Nakano, and K. Sueishi. 1996. Immunohistochemical localization of vascular endothelial growth factor in the human placenta. Placenta. 17:111-121.