The association of the tetraspanin D6.1A with the α6β4 integrin supports cell motility and liver metastasis formation

Journal of Cell Science

Volumn 116, Issue 21, 2003, Pages 4373-4390

  Herlevsen, Mikael ^a,d   Schmidt, Dirk Steffen ^a   Miyazaki, Kaoru ^b   Zöller, Margot ^a,c  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b YOKOHAMA CITY UNIVERSITY   (Japan)

^c UNIVERSITY OF KARLSRUHE   (Germany)

^d UNIVERSITY OF VIRGINIA   (United States)

Author keywords

6 4 integrin; Adhesion; Metastasis; Motility; Tetrasparin

Indexed keywords

ALPHA6 INTEGRIN; BETA4 INTEGRIN; CD44V ANTIGEN; CELL ADHESION MOLECULE; KALININ; TETRASPANIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ADHESION; CELL MIGRATION; CELL MOTILITY; CELL STIMULATION; CELL SUBPOPULATION; CELL TRANSPLANTATION; CELL TRANSPORT; COMPLEX FORMATION; CONTROLLED STUDY; GENE OVEREXPRESSION; GENETIC TRANSFECTION; LIVER METASTASIS; MASS SPECTROMETRY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PANCREAS ADENOCARCINOMA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; TUMOR GROWTH;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD44; CELL ADHESION MOLECULES; CELL MOVEMENT; CLONING, MOLECULAR; ENZYME INDUCTION; HEMIDESMOSOMES; INTEGRIN ALPHA6BETA4; LIVER NEOPLASMS; MASS SPECTROMETRY; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; NEOPLASM PROTEINS; PROTEIN BINDING; PROTEIN KINASE C; PSEUDOPODIA; RATS; RECEPTORS, CELL SURFACE; TUMOR CELLS, CULTURED;

ANIMALIA;

EID: 0242720078     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00760     Document Type: Article

References (78)

1. Aplin, J. D., Dawson, S. and Seif, M. W. (1996). Abnormal expression of integrin alpha 6 beta 4 in cervical intraepithelial neoplasia. Br. J. Cancer 74, 240-245.
2. Baudoux, B., Castanares-Zapatero, D., Leclercq-Smekens, M., Berna, N. and Poumay, Y. (2000). The tetraspanin CD9 associates with the integrin alpha6beta4 in cultures human epidermal keratinocytes and is involved in cell motility. Eur J. Cell Biol. 79, 41-51.
3. Belkin, A. M. and Stepp, M. A. (1999). Integrins as receptors for laminin. Microsc. Res. Tech. 51, 280-301.
4. Berditchevski, F. and Odintsova, E. (1999). Characterization of integrin-tetraspanin adhesion complexes: role of tetraspanins in integrin signaling. J. Cell Biol. 146, 477-492.
5. Borradori, L. and Sonnenberg, A. (1999). Structure and function of hemidesmosomes: more than simple adhesion complexes. J. Invest. Dermatol. 112, 411-418.
6. Bretscher, M. S. (1992). Circulating integrins: α5β1, α6β4 and Mac-1, but not α3β1, α4β1 or LFA-1 EMBO J. 11, 405-410.
7. Charrin, S., LeNaour, F., Oualid, M., Billard, M., Faure, G., Hanash, S. M., Boucheix, C. and Rubinstein, E. (2001). The major cd9 and cd81 molecular partner. identification and characterization of the complexes. J. Biol. Chem. 276, 14329-14337.
8. Chomzynski, P. and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
9. Claas, C., Herrmann, K., Matzku, M., Möller, P. and Zöller, M. (1996). Developmentally regulated expression of metastasis-associated antigens in the rat. Cell Growth Diff. 7, 663-678.
10. Claas, C., Seiter, S., Claas, A., Savelyeva, L., Schwab, M. and Zöller, M. (1998). Identification of the rat homologue of CO-029, a metastasis-associated tetraspan molecule. J. Cell Biol. 141, 267-280.
11. Claas, C., Stipp, C. S. and Hemler, M. E. (2001). Evaluation of prototype transmembrane 4 superfamily protein complexes and their relation to lipid rafts. J. Biol. Chem. 276, 7974-7984.
12. Daemi, N., Thomasset, N., Lissitzky, J. C., Dumortier, J., Jacquier, M. F., Pourreyron, C., Rousselle, P., Chayvialle, J. A. and Remy, L. (2000). Anti-beta4 integrin antibodies enhance migratory and invasive abilities of human colon adenocarcinoma cells and their MMP-2 expression. Int. J. Cancer 85, 850-856.
13. DeMelker, A. A. and Sonnenberg, A. (1999). Integrins: alternative splicing as a mechanism to regulate ligand binding and integrin signaling events. BioEssays 21, 499-509.
14. Domanico, S. Z., Pelletier, A. J., Havran, W. L. and Quaranta, V. (1997). Integrin alpha6A beta1 induces CD81-dependent cell-motility without engaging the extracellular matrix migration substrate. Mol. Biol. Cell 8, 2253-2265.
15. Dowling, J., Yu, Q. C. and Fuchs, E. (1996). β4 integrin is required for hemidesmosome formation, cell adhesion and cell survival J. Cell Biol. 134, 559-572.
16. Falk-Marzillier, J., Domanico, S. Z., Pelletier, A., Mullen, L. and Quaranta, V. (1998). Characterization of a tight molecular complex between integrin alpha 6 beta 4 and laminin-5 extracellular matrix. Biochem. Biphys. Res. Commun. 251, 49-55.
17. Feltri, M. L., Arona, M., Scherer, S. S. and Wrabetz, L. (1997). Cloning and sequence of the cDNA encoding the beta 4 integrin subunit in rat peripheral nerve. Gene 186, 299-304.
18. Fitter, S., Sincock, P. M., Joliffe, C. N. and Ashman, L. K. (1999). Transmembrane 4 superfamily protein CD151 (PETA-3) associates with beta1 and alpha IIb beta3 integrins in haematopoietic cell lines and modulates cell-cell adhesion. Biochem. J. 338, 61-70.
19. Fontao, L., Dirrig, S., Owaribe, K., Kedinger, M. and Launay, J. F. (1997). Polarized expression of HD1: relationship with the cytoskeleton in cultured human colonic carcinoma cells. Exp. Cell. Res. 231, 319-327.
20. Fornaro, M. and Languino, L. R. (1997). Alternatively spliced variants: a new view of the integrin cytoplasmic domain. Matrix Biol. 16, 185-193.
21. Friedl, P., Brocker, E. B. and Zanker, K. S. (1998). Integrins, cell matrix interactions and cell migration strategies: fundamental differences in leukocytes and tumor cells. Cell Adhes. Commun. 6, 225-236.
22. Gaietta, G., Redelmeier, T. E., Jackson, M. R., Tamura, R. N. and Quaranta, V. (1994). Quantitative measurement of α6β1 and α6β4 integrin internalization under cross-linking conditions: a possible role for the α6 cytoplasmic domains. J. Cell. Sci. 107, 3339-3349.
23. Gambaletta, D., Marchetti, A., Benedetti, L., Mercurion, A. M., Sacchi, A. and Falcioni, R. (2000). Cooperative signaling between alpha(6)beta(4) integrin and ErbB-2 receptor is required to promote phosphatidylinositol 3-kinase-dependent invasion. J. Biol. Chem. 275, 10604-10610.
24. Grassi, M., Moens, G., Rousselle, P., Thiery, J. P. and Jouanneau, J. (1999). The SFL activity secreted by metastatic carcinoma cells is related to laminin 5 and mediates cell scattering in an integrin-independent manner. J. Cell. Sci. 112, 2511-2520.
25. Günthert, U., Hofman, M., Rudy, W., Reber, S., Zöller, M., Haußmann, I., Matzku, S., Wenzel, A., Ponta, H. and Herrlich, P. (1991). A new variant of glycoprotein CD44 confers metastatic potential to rat carcinoma cells. Cell 65, 13-24.
26. Hemler, M. E. (2001). Specific tetraspanin functions. J. Cell Biol. 155, 1103-1108.
27. Hermanek, P. (1998). Pathology and biology of pancreatic ductal adenocarcinoma. Langenbecks Arch. Surg. 383, 116-120.
28. Hintermann, E., Bilban, M., Sharabi, A. and Quaranta, V. (2001). Inhibitory role of alpha6 beta4-associated erbB-2 and phosphoinositide 3-kinase in keratinocyte haptotactic migration dependent on alpha3 beta1 integrin. J. Cell Biol. 153, 465-478.
29. Horvath, G., Serru, V., Clay, D., Billard, M., Boucheix, C. and Rubinstein, E. (1998). CD19 is linked to the integrin-associated tetraspans CD9, CD81, and CD82. J. Biol. Chem. 273, 30537-30543.
30. Indig, F. E., Diaz-Gonzales, F. and Ginsberg, M. H. (1997). Analysis of the tetraspanin CD9-integrin alphaIIbbeta3 (GPIIb-IIIa) complex in pletelet membranes and transfected cells. Biochem. J. 327, 291-298.
31. Jones, J. C., Hopkinson, S. B. and Goldfinger, L. E. (1998). Structure and assembly of hemidesmosomes. BioEssays 20, 488-494.
32. Jones, P. H., Bishop, L. A. and Watt, F. M. (1996). Functional significance of CD9 association with beta1 integrins in human epidermal keratinocytes. Cell Adhes. Commun. 4, 297-305.
33. Kariya, Y., Ishida, K., Tsubota, Y., Nakashima, V., Hirosaki, T., Ogawa, T. and Miyazaki, K. (2002). Efficient expression system of human recombinant laminin-5. J. Biochem. (Tokyo) 132, 607-612.
34. Lee, E. C., Lotz, M. M., Steele, G. D. and Mercurio, A. M. (1992). The integrin alpha 6 beta 4 is a laminin receptor. J. Cell Biol. 117, 671-678.
35. Levy, S., Todd, S. C. and Maecker, H. T. (1998). CD81 (TAPA-1): a molcule involved in signal transduction and cell adhesion in the immune system. Ann. Rev. Immunol. 16, 89-109.
36. Lozahic, S., Christiansen, D., Manie, S., Gerlier, D., Billard, M., Boucheix, C. and Rubinstein, E. (2000). CD46 (membrane cofactor protein) associates with multiple beta1 integrins and tetraspans. Eur. J. Immunol. 30, 900-907.
37. MacDonald, N. J. and Steeg, P. S. (1997). Molecular basis of tumour metastasis. Cancer Surv. 16, 175-199.
38. Maecker, H. T., Todd, S. C. and Levy, S. (1997). The tetraspanin superfamily: molecular facilitators. FASEB J. 11, 428-442.
39. Maniero, F., Pepe, A., Yeon, M., Ren, Y. and Giancotti, F. G. (1996). The intracellular functions of alpha6beta4 integrin are regulated by EGF. J. Cell Biol. 134, 241-253.
40. Mannion, B. A., Berditchevski, F., Kraeft, S. K., Chen, L. B. and Hemler, M. E. (1996). Transmembrane-4 superfamily proteins CD81 (TAPA-1), CD82, CD63, and CD53 specifically associate with integrin α4β1 (CD49d/CD29). J. Immunol. 157, 2039-2047.
41. Mareel, M. M., VanRoy, F. M. and Bracke, M. E. (1993). How and when do tumor cells metastasize? Crit. Rev. Oncol. 4, 559-594.
42. Matzku, S., Komitowski, D., Miltenberger, M. and Zöller, M. (1983). Characterization of BSp73, a spontaneous rat tumour and its in vivo selected variants showing different metastasizing capacity. Invasion Metast. 3, 109-123.
43. Matzku, S., Wenzel, A., Liu, S. and Zöller, M. (1989). Antigenic differences between metastatic and non-metastatic rat tumour variants characterized by monoclonal antibodies. Cancer Res. 49, 1294-1299
44. Mercurio, A. M. and Rabinovitz, I. (2001). Towards a mechanistic understanding of tumor invasion - lessons from the alpha6 beta4 integrin. Semin. Cancer Biol. 11, 129-141.
45. Nath, D., Slocombe, P. M., Webster, A., Stephens, P. E., Docherty, A. J. and Murphy, G. (2000). Meltrin gamma(ADAM-9) mediates cellular adhesion through alpha(6)beta(1)integrin, leading to a marked induction of fibroblast cell motility. J. Cell Sci. 113, 2319-2328.
46. Ng, T., Shima, D., Squire, A., Bastiaens, P. I. H., Gschmeissner, S., Humphries, M. J. and Parker, P. J. (1999). PKCa regulates β1 integrin-dependent cell motility through association and control of integrin traffic. EMBO J. 18, 3909-3923.
47. Nguyen, B. P., Gil, S. G. and Carter, W. G. (2000). Deposition of laminin 5 by keratinocytes regulates integrin adhesion and signaling. J. Biol. Chem. 275, 31896-31907.
48. Niessen, C. M., Hulsman, E. H., Oomen, L. C., Kuikman, I. and Sonnenberg, A. (1997). A minimal region on the integrin beta4 subunit that is critical to its localization in hemidesmosomes regulates the distribution of HD1/plectin in COS-7 cells. J. Cell. Sci. 110, 1705-1716.
49. Nievers, M. G., Schaapveld, R. Q., Oomen, L. C., Fontao, L., Geerts, D. and Sonnenberg, A. (1998). Ligand-independent role of the beta 4 integrin subunit in the formation of hemidesmosomes. J. Cell Sci. 111, 1659-1672.
50. O'Connor, K. L., Nguyen, B. K. and Mercurio, A. M. (2000). RhoA function in lamellae formation and migration is regulated by the alpha6 beta4 integrin and cAMP metabolism. J. Cell Biol. 148, 253-258.
51. Odintsova, E., Sugiura, T. and Berditchevski, F. (2000). Attenuation of EGF receptor signaling by a metastasis suppressor, the tetraspanin CD82/KAI-1. Curr. Biol. 10, 1009-1012.
52. Penas, P. F., Garzia-Diez, A., Sanchez-Madrid, F. and Yanez-Mo, M. (2000). Tetraspanins are localized at motility-related structures and involved in normal human keratinocyte wound healing migration. J. Invest. Dermatol. 114, 1126-1135.
53. Poste, G. and Fidler, I. J. (1980). The pathogenesis of cancer metastasis. Nature 283, 139-146.
54. Rabinovitz, I., Toker, A. and Mercurio, A. M. (1999). Protein kinase C-dependent mobilization of the alpha6beta4 integrin from hemodesmosomes and ist association with actin-rich cell protrusions drive the chemotactic migration of carcinoma cells. J. Cell Biol. 146, 1147-1160.
55. Rabinovitz, I. and Mercurio, A. M. (1997). The interin α6β4 functions in carcinoma cell migration on laminin-1 by mediating the formation and stabilization of actin-containing motility structures. J. Cell Biol. 139, 1873-1884.
56. Reisser, D., Olsson, N. O. and Martin, F. (1993). In vivo and in vitro reactivity of rat spleen cells against regressor and progressor colon-cancer cell variants. Int. J. Cancer 53, 651-656.
57. Riddelle, K. S., Green, K. J. and Jones, J. C. (1991). Formation of hemidesomosomes in vitro by a transformed rat bladder cell line. J. Cell Biol. 112, 159-168.
58. Rigot, V., Lehmann, M., Andre, F., Daemi, N., Marvaldi, J. and Luis, J. (1998). Integrin ligation and PKC activation are required for migration of colon carcinoma cells. J. Cell. Sci. 111, 3119-3127.
59. Rösel, M., Claas, C., Herlevsen, M., Seiter, S. and Zöller, M. (1998). Identification of a new phosphatidyl-inositol anchored member of the family of plasminogen activators as metastasis-associated molecule. Oncogene 17, 1989-2002.
60. Rubinstein, E., Poindessous-Jazat, V., LeNaour, F., Billard, M. and Boucheix, C. (1997). CD9, but not other tetraspans, associate with the beta1 integrin precursor. Eur. J. Immunol. 27, 1919-1927.
61. Scherberich, A., Moog, S., Haan-Archipoff, G., Azorsa, D. O., Lanza, F. and Beretz, A. (1998). Tetraspanin CD9 is associated with vary late-acting integrins in human vascular smooth muscle cells and modulates collagen matrix reorganization. Arterioscler. Thromb. Vasc. Biol. 18, 1691-1697.
62. Serru, V., LeNaour, F., Billard, M., Azorsa, D. O., Lanza, F., Boucheix, C. and Rubinstein, F. (1999). Selective tetraspan-integrin complexes (CD81/alpha4beta1, CD151/alpha3beta1, CD151/alpha6beta1) under conditions disrupting tetraspan interactions. Biochem. J. 340, 103-111.
63. Shaw, L. M., Chao, C., Wewer, U. M. and Mercurio, A. M. (1996). Function of the integrin alpha 6 beta 1 in metastatic breast carcinoma cells assessed by expression of a dominant-negative receptor. Cancer Res. 56, 563-959.
64. Shaw, L. M., Rabinovitz, I., Wang, H. H., Toker, A. and Mercurio, A. M. (1997). Activation of phosphoinositide 3-OH kinase by the alpha6 beta4 integrin promotes carcinoma invasion. Cell 91, 949-960.
65. Sincock, P. M., Fitter, S., Parton, R. G., Berndt, M. C., Gamble, J. R. and Ashman, L. K. (1999). PETA-3/CD151, a member of the transmembrane 4 superfamily, is localised to the plasma membrane and endocytotic system of endothelial cells, associates with multiple integrins and modulates cell function. J. Cell. Sci. 112, 833-844.
66. Stahl, S., Weitzman, S. and Jones, J. C. (1997). The role of laminin-5 and its receptor in mammary epithelial cell branching morphogenesis. J. Cell. Sci. 110, 55-63.
67. Sterk, L. M. T., Geuijen, C. A. W., Oomen, L. C. J. M., Cafat, J., Janssen, H. and Sonneberg, A. (2000). The tetraspanin molecule CD151, a novel constituent of hemidesmosomes, associates with the integrin α6β4 and may regulate the spatial organization of hemidesmosomes. J. Cell Biol. 149, 969-982.
68. Sugiura, T. and Berditchevski, F. (1999). Function of alpha3beta1-tetraspanin protein complexes in tumor cell invasion. Evidence for the role of the complexes in production of matrix metalloproteinase 2 (MMP-2). J. Cell Biol. 146, 1375-1389.
69. Testa, J. E., Brooks, P. C., Lin, J. M. and Quigle, J. P. (1999). Eukaryotic expression cloning with an antimetastatic monoclonal antibody identifies a tetraspanin (PETA-3/CD151) as an effector of human tumor cell migration and metastasis. Cancer Res. 59, 3812-3820.
70. Tiwari-Woodruff, S. K., Buznikov, A. G., Vu, T. Q., Micevych, P. E., Chen, K., Kornblum, H. I. and Bronstein, J. M. (2001). OSP/claudin-11 forms a complex with a novel member of the tetraspanin super family and beta1 integrin and regulates proliferation and migration of oligodendrocytes. J. Cell Biol. 153, 295-305.
71. Todres, E., Nardi, J. B. and Robertson, H. M. (2000). The tetraspanin superfamily in insects. Insect. Mol. Biol. 9, 581-590.
72. Vogelmann, R., Kreuser, E. D., Adler, G. and Lutz, M. P. (1999). Integrin alpha6beta1 role in metastatic behavior of human pancreatic carcinoma cells. Int. J. Cancer 80, 791-795.
73. Würfel, J., Rösel, M., Seiter, S., Claas, C., Herlevsen, M., Weth, R. and Zöller, M. (1999). Metastasis association of the rat orthologue of the human epithelial glycoprotein antigen EGP314. Oncogene 18, 2323-2334.
74. Yauch, R. L., Berditchevski, F., Harler, M. B., Reichner, J. and Hemler, M. E. (1998). Highly stoichiometric, stable, and specific association of integrin α3β1 with CD151 provides a major link to phosphatidylinositol 4-kinase, and may regulate cell migration. Mol. Biol. Cell 9, 2751-2765.
75. Yauch, R. L., Kazarov, A. R., Desai, B., Lee, R. T. and Hemler, M. E. (2000). Direct extracellular contact between integrin alpha(3)beta(1) and TM4SF protein CD151. J. Biol. Chem. 275, 9230-9238.
76. Z'graggen, K., Centeno, B. A., Fernandez-delCastillo, C., Jimenez, R. E., Werner, J. and Warshaw, A. L. (2001). Biological implications of tumor cells in blood and bone marrow of pancreatic cancer patients. Surgery 129, 537-546.
77. Zöller, M. (1998). Metastasierung als physiologisches Programm. Nova Acta Leopoldina 78, 55-102.
78. Zutter, M. M., Sun, H. and Santoro, S. A. (1998). Altered integrin expression and the malignant phenotype: the contribution of multiple integrated integrin receptors. J. Mammary Gland Biol. Neoplasia 3, 191-200.