EMILIN1 represents a major stromal element determining human trophoblast invasion of the uterine wall

Journal of Cell Science

Volumn 119, Issue 21, 2006, Pages 4574-4584

  Spessotto, Paola ^a   Bulla, Roberta ^b   Danussi, Carla ^a   Radillo, Oriano ^b   Cervi, Marta ^a   Monami, Giada ^a,d   Bossi, Fleur ^b   Tedesco, Francesco ^b   Doliana, Roberto ^a   Colombatti, Alfonso ^a,c  

^a CENTRO DI RIFERIMENTO ONCOLOGICO   (Italy)

^b UNIVERSITY OF TRIESTE   (Italy)

^c UNIVERSITY OF UDINE   (Italy)

^d THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

4 integrin; EMILIN1; Migration; MMP; Trophoblast

Indexed keywords

ALPHA4 INTEGRIN; EMILIN 1; GELATINASE A; GLYCOPROTEIN; INTERSTITIAL COLLAGENASE; MONOCLONAL ANTIBODY; SMALL INTERFERING RNA;

ARTICLE; CELL INTERACTION; CHORION VILLUS; COCULTURE; CONNECTIVE TISSUE; CONTROLLED STUDY; DECIDUA; ELASTIC FIBER; EMBRYO; ENZYME REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MYOMETRIUM; PLACENTA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; STROMA; STROMA CELL; TROPHOBLAST; UPREGULATION;

CELL ADHESION; CELL MOVEMENT; CHORIONIC VILLI; DECIDUA; FEMALE; HUMANS; INTEGRIN ALPHA4BETA1; MATRIX METALLOPROTEINASES, MEMBRANE-ASSOCIATED; MEMBRANE GLYCOPROTEINS; NEOPLASM INVASIVENESS; PLACENTA; PREGNANCY; PREGNANCY TRIMESTER, FIRST; RNA, SMALL INTERFERING; STROMAL CELLS; TROPHOBLASTS; UTERUS;

EID: 33751541732     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.03232     Document Type: Article

References (46)

1. Aplin, J. D. (1993). Expression of integrin α6β4 in human trophoblast and its loss from extravillous cells. Placenta 14, 203-215.
2. Aplin, J. D., Haigh, T., Lacey, H., Chen, C. P. and Jones, C. J. (2000). Tissue interactions in the control of trophoblast invasion. J. Reprod. Fertil. Suppl. 55, 57-64.
3. Braghetta, P., Ferrari, A., de Gemmis, P., Zanetti, M., Volpin, D., Bonaldo, P. and Bressan, G. M. (2002). Expression of the EMILIN-1 gene during mouse development. Matrix Biol. 21, 603-609.
4. Bulla, R., de Guarrini, F., Pausa, M., Fischetti, F., Meroni, P. L., De Seta, F., Guaschino, S. and Tedesco, F. (1999). Inhibition of trophoblast adhesion to endothelial cells by sera of women with recurrent spontaneous abortions. Am. J. Reprod. Immunol. 42, 116-123.
5. Bulla, R., Villa, A., Bossi, F., Cassetti, A., Radillo, O., Spessotto, P., De Seta, F., Guaschino, S. and Tedesco, F. (2005). VE-cadherin is a critical molecule for trophoblast-endothelial cell interaction in decisula spiral arteries. Exp. Cell Res. 303, 101-113.
6. Campbell, S., Rowe, J., Jackson, C. J. and Gallery, E. D. (2003). In vitro migration of cytotrophoblasts through a decidual endothelial cell monolayer: the role of matrix metalloproteinases. Placenta 24, 306-315.
7. Chen, C. P. and Aplin, J. D. (2003). Placental extracellular matrix: gene expression, deposition by placental fibroblasts and the effect of oxygen. Placenta 24, 316-325.
8. Colombatti, A., Doliana, R., Bot, S., Canton, A., Mongiat, M., Mungiguerra, G., Paron-Cilli, S. and Spessotto, P. (2000). The EMILIN protein family. Matrix Biol. 19, 289-301.
9. Cowell, S., Knauper, V., Stewart, M. L., D'Ortho, M. P., Stanton, H., Hembry, R. M., Lopez-Otin, C., Reynolds, J. J. and Murphy, G. (1998). Induction of matrix metalloproteinase activation cascades based on membrane-type 1 matrix metalloproteinase: associated activation of gelatinase A, gelatinase B and collagenase 3. Biochem. J. 331, 453-458.
10. Damsky, C. H., Fitzgerald, M. L. and Fisher, S. J. (1992). Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during the first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J. Clin. Invest. 89, 210-222.
11. Deryugina, E. I., Ratnikov, B., Monosov, E., Postnova, T. I., DiScipio, R., Smith, J. W. and Strongin, A. Y. (2001). MT1-MMP initiates activation of pro-MMP-2 and integrin alphavbeta3 promotes maturation of MMP-2 in breast carcinoma cells. Exp. Cell Res. 263, 209-223.
12. Doliana, R., Mongiat, M., Bucciotti, F., Giacomello, E., Deutzmann, R., Volpin, D., Bressan, G. M. and Colombatti, A. (1999). EMILIN, a component of the elastic fiber and a new member of the C1q/tumor necrosis factor superfamily of proteins. J. Biol. Chem. 274, 16773-16781.
13. Engvall, E., Krusius, T., Wewer, U. and Ruoslahti, E. (1983). Laminin from rat yolk sac tumor: isolation, partial characterization, and comparison with mouse laminin. Arch. Biochem. Biophys. 222, 649-656.
14. Even-Ram, S., Uziely, B., Cohen, P., Grisaru-Granovsky, S., Maoz, M., Ginzburg, Y., Reich, R., Vlodavsky, I. and Bar-Shavit, R. (1998). Thrombin receptor overexpression in malignant and physiological invasion processes. Nat. Med. 4, 909-914.
15. Giacomello, E., Neumayer, J., Colombatti, A. and Perris, R. (1999). Centrifugal assay for fluorescence-based cell adhesion adapted to the analysis of ex vivo cells and capable of determining relative binding strengths. Biotechniques 26, 758-762, 764-766.
16. Graham, C. H. and Lala, P. K. (1992). Mechanisms of placental invasion of the uterus and their control. Biochem. Cell Biol. 70, 867-870.
17. Graham, C. H., Hawley, T. S., Hawley, R. G., MacDougall, J. R., Kerbel, R. S., Khoo, N. and Lala, P. K. (1993). Establishment and characterization of first trimester human trophoblast cells with extended life span. Exp. Cell Res. 206, 204-211.
18. Hamilton, G. S., Lysiak, J. J., Han, V. K. M. and Lala, P. K. (1998). Autocrine-paracrine regulation of human trophoblast invasiveness by insulin-like growth factor (IGF)-II and IGF-binding protein (IGFBP)-1. Exp. Cell Res. 244, 147-156.
19. Hotary, K. B., Allen, E. D., Brooks, P. C., Datta, N. S., Long, M. W. and Weiss, S. J. (2003). Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell 114, 33-45.
20. Ilic, D., Genbacev, O., Jin, F., Caceres, E., Almeida, E. A., Bellingard-Dubouchaud, V., Schaefer, E. M., Damsky, C. H. and Fisher, S. J. (2001). Plasma membrane-associated pY397FAK is a marker of cytotrophoblast invasion in vivo and in vitro. Am. J. Pathol. 159, 93-108.
21. Irving, J. A. and Lala, P. K. (1995). Functional role of cell surface integrins on human trophoblast cell migration: regulation by TGF-ß, IGF-II, and IGFBP-1. Exp. Cell Res. 217, 419-427.
22. Irving, J. A., Lysiak, J. J., Graham, C. H., Hearn, S., Han, V. K. and Lala, P. K. (1995). Characteristics of trophoblast cells migrating from first trimester chorionic villus explants and propagated in culture. Placenta 16, 413-433.
23. Kaufmann, P. and Castellucci, M. (1997). Extravillous trophoblast in the human placenta. Trophoblast Res. 10, 21-65.
24. Kilburn, B. A., Wang, J., Duniec-Dmuchkowski, Z. M., Leach, R. E., Romero, R. and Armant, D. R. (2000). Extracellular matrix composition and hypoxia regulate the expression of HLA-G and integrins in trophoblast cell line. Biol. Reprod. 62, 739-747.
25. Korhonen, M., Ylanne, J., Laitinen, L., Cooper, H. M., Quaranta, V. and Virtanen, I. (1991). Distribution of the α1-6 integrin subunits in human developing and term placenta. Lab. Invest. 65, 347-356.
26. Lorenzon, P., Vecile, E., Nardon, E., Ferrero, E., Harlan, J. M., Tedesco, F. and Dobrina, A. (1998). Endothelial cell E- and P-selectin and vascular cell adhesion molecule- 1 function as signaling receptors. J. Cell Biol. 142, 1381-1391.
27. MacPhee, D. J., Mostachfi, H., Han, R., Lye, S. J., Post, M. and Caniggia, I. (2001). Focal adhesion kinase is a key mediator of human trophoblast development. Lab. Invest. 81, 1469-1483.
28. Maldonado-Estrada, J., Menu, E., Roques, P., Barré-Sinoussi, F. and Chaouat, G. (2004). Evaluation of Cytokeratin 7 as an accurate intracellular marker with which to assess the purify of human placental villous trophoblast cells by flow cytometry. J. Immunol. Methods 286, 21-34.
29. Mazzucato, M., Spessotto, P., Masotti, A., De Appollonia, L., Cozzi, M. R., Yoshioka, A., Perris, R., Colombatti, A. and De Marco, L. (1999). Identification of domains responsible for von Willebrand factor type VI collagen interaction mediating platelet adhesion under high flow. J. Biol. Chem. 274, 3033-3041.
30. McCarthy, J. B. and Furcht, L. T. (1984). Laminin and fibronectin promote the haptotactic migration of B16 mouse melanoma cells in vitro. J. Cell Biol. 98, 1474-1486.
31. Miyamoto, S., Katz, B. Z., Lafrenie, R. M. and Yamada, K. M. (1998). Fibronectin and integrins in cell adhesion, signaling, and morphogenesis. Ann. N. Y. Acad. Sci. 857, 119-129.
32. Mongiat, M., Mungiguerra, G., Bot, S., Mucignat, M. T., Giacomello, E., Doliana, R. and Colombatti, A. (2000). Self-assembly and supramolecular organization of EMILIN. J. Biol. Chem. 275, 25471-25480.
33. Murdoch, A., Jenkinson, E. J., Johnson, G. D. and Owen, J. J. T. (1990). Alkaline phosphatase-fast red, a new fluorescent label: Application in double labelling for cell surface antigen and cell cycle analysis. J. Immunol. Methods 132, 45-49.
34. Nardo, L. G., Nikas, G. and Makrigiannakis, A. (2003). Molecules in blastocyst implantation. Role of matrix metalloproteinases, cytokines and growth factors. J. Reprod. Med. 48, 137-147.
35. Norwitz, E. R., Schust, D. J. and Fisher, S. J. (2001). Implantation and the survival of early pregnancy. N. Engl. J. Med. 345, 1400-1408.
36. Pender, S. L., Salmela, M. T., Monteleone, G., Schnapp, D., McKenzie, C., Spencer, J., Fong, S., Saarialho-Kere, U. and MacDonald, T. T. (2000). Ligation of alpha4ss1 integrin on human intestinal mucosal mesenchymal cells selectively up-regulates membrane type-1 matrix metalloproteinase and confers a migratory phenotype. Am. J. Pathol. 157, 1955-1962.
37. Queenan, J. T., Jr. Kao, L. C., Arboleda, C. E., Ulloa-Aguirre, A., Golos, T. G., Cines, D. B. and Strauss, J. F. D. (1987). Regulation of urokinase-type plasminogen activator production by cultured human cytotrophoblasts. J. Biol. Chem. 262, 10903-10906.
38. Rose, D. M., Han, J. and Ginsberg, M. H. (2002). Alpha 4 integrins and the immune response. Immunol. Rev. 186, 118-124.
39. Seiki, M. (1999). Membrane-type matrix metalloproteinases. Acta Pathol. Microbiol. Immunol. Scand. 107, 137-143.
40. Spessotto, P., Giacomello, E. and Perris, R. (2000). Fluorescence assays to study cell adhesion and migration in vitro. Methods Mol. Biol. 139, 321-343.
41. Spessotto, P., Cervi, M., Mucignat, M. T., Mungiguerra, G., Sartoretto, I., Doliana, R. and Colombatti, A. (2003a). beta 1 integrin-dependent cell adhesion to EMILIN-1 is mediated by the gC1q domain. J. Biol. Chem. 278, 6160-6167.
42. Spessotto, P., Gronkowska, A., Deutzmann, R., Perris, R. and Colombatti, A. (2003b). Preferential locomotion of leukemic cells towards laminin isoforms 8 and 10. Matrix Biol. 22, 351-361.
43. Strongin, A. Y., Collier, I., Bannikov, G., Marmer, B. L., Grant, G. A. and Goldberg, G. I. (1995). Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J. Biol. Chem. 270, 5331-5338.
44. Tedesco, F., Narchi, G., Radillo, O., Meri, S., Ferrone, S. and Betterle, C. (1993). Susceptibility of human trophoblast to killing by human complement and the role of the complement regulatory proteins. J. Immunol. 151, 1562-1570.
45. Tedesco, F., Pausa, M., Nardon, E., Introna, M., Mantovani, A. and Dobrina, A. (1997). The cytolytically inactive terminal complement complex activates endothelial cells to express adhesion molecules and tissue factor procoagulant activity. J. Exp. Med. 185, 1619-1627.
46. Zhou, Y., Fisher, S., Janatpour, M., Genbacev, O., Dejana, E., Wheelock, M. and Damsky, C. (1997). Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion? J. Clin. Invest. 99, 2139-2151.