An extracellular site on tetraspanin CD151 determines α3 and α6 integrin-dependent cellular morphology

Journal of Cell Biology

Volumn 158, Issue 7, 2002, Pages 1299-1309

  Kazarov, Alexander R ^a   Yang, Xiuwei ^a   Stipp, Christopher S ^a   Sehgal, Bantoo ^a   Hemler, Martin E ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA3 INTEGRIN; ALPHA6 INTEGRIN; CD151 PROTEIN; CELL PROTEIN; EPITOPE; TETRASPANIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BASEMENT MEMBRANE; BIOSYNTHESIS; CELL SPREADING; CELL STRAIN 3T3; CELL STRAIN COS7; CELL STRUCTURE; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; EXTRACELLULAR MATRIX; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; STOICHIOMETRY;

ANIMALS; ANTIGENS, CD; CELL ADHESION; CELLS, CULTURED; EPITOPES; EXTRACELLULAR SPACE; HUMANS; IMMUNOBLOTTING; INTEGRIN ALPHA3BETA1; INTEGRIN ALPHA6BETA1; MUTAGENESIS, SITE-DIRECTED; OCTOXYNOL; PEPTIDE FRAGMENTS; PLASMIDS; PRECIPITIN TESTS; PROTEIN BINDING; SEQUENCE DELETION;

ANIMALIA;

EID: 0037144837     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200204056     Document Type: Article

References (60)

1. Anton, E.S., J.A. Kreidberg, and P. Rakic. 1999. Distinct functions of alpha3 and alpha(v) integrin receptors in neuronal migration and laminar organization of the cerebral cortex. Neuron. 22:277-289.
2. Belkin, A.M., and M.A. Stepp. 2000. Integrins as receptors for laminins. Microsc. Res. Tech. 51:280-301.
3. Bell, E., B. Ivarsson, and C. Merrill. 1979. Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc. Natl. Acad. Sci. USA. 76:1274-1278.
4. Berditchevski, F. 2001. Complexes of tetraspanins with integrins: more than meets the eye. J. Cell Sci. 114:4143-4151.
5. Berditchevski, F., G. Bazzoni, and M.E. Hemler. 1995. Specific association of CD63 with the VLA-3 and VLA-6 integrins. J. Biol. Chem. 270:17784-17790.
6. Berditchevski, F., M.M. Zutter, and M.E. Hemler. 1996. Characterization of novel complexes on the cell surface between integrins and proteins with 4 transmembranes (TM4 proteins). Mol. Biol. Cell 7:193-207.
7. Berditchevski, F., S. Chang, J. Bodorova, and M.E. Hemler. 1997. Generation ofmonoclonal antibodies to integrin-associated proteins: evidence that α3β1 complexes with EMMPRIN/basigin/OX47/M6. J. Biol. Chem. 272:29174-29180.
8. Berditchevski, F., E. Gilbert, M.R. Griffiths, S. Fitter, L. Ashman, and S.J. Jenner. 2001. Analysis of the CD151-{alpha}3{beta}1 integrin and CD151-tetraspanin interactions by mutagenesis. J. Biol. Chem. 276:41165-41174.
9. Bergelson, J.M., N.F. St. John, S. Kawaguchi, R. Pasqualini, F. Berdichevsky, M.E. Hemler, and R.W. Finberg. 1994. The I domain is essential for echovirus I interaction with VLA-2. Cell Adhes. Commun. 2:455-464.
10. Boucheix, C., and E. Rubinstein. 2001. Tetraspanins. Cell. Mol. Life Sci. 58:1189-1205.
11. Burkin, D.J., and S.J. Kaufman. 1999. The alpha7beta1 integrin in muscle development and disease. Cell Tissue Res. 296:183-190.
12. Chan, B.M.C., P.D, Kassner, J.A, Schiro, H.R. Byers, T.S. Kupper, and M.E. Hemler. 1992. Distinct cellular functions mediated by different VLA integrin α subunit cytoplasmic domains. Cell. 68:1051-1060.
13. Davis, G.E., and C.W. Camarillo. 1995. Regulation of endothelial cell morphogenesis by integrins, mechanical forces, and matrix guidance pathways. Exp. Cell Res. 216:113-123.
14. Delwel, G.O., A.A. de Melker, F. Hogervorst, L.H. Jaspars, D.L.A. Fles, I. Kuikman, A. Lindblom, M. Paulsson, R. Timpl, and A. Sonnenberg. 1994. Distinct and overlapping ligand specificities of the α3Aβ1 and α6Aβ1 integrins: recognition of laminin isoforms. Mol. Biol. Cell. 5:203-215.
15. Dipersio, C.M., S. Shah, and R.O. Hynes. 1995. α3Aβ1 integrin localizes to focal contacts in response to diverse extracellular matrix proteins. J. Cell Sci. 108:2321-2336.
16. Dipersio, C.M., K.M. Hodivala-Dilke, R. Jaenisch, and J.A. Kreidberg. 1997. Alpha-3-Beta-1 integrin is required for normal development of the epidermal basement membrane. J. Cell Biol. 137:729-742.
17. Eble, J.A., K.W. Wucherpfennig, L. Gauthier, P. Dersch, E. Krukonis, R.R. Isberg, and M.E. Hemler. 1998. Recombinant soluble human α3β1 integrin: purification, processing, regulation, and specific binding to laminin-5 and invasin in a mutually exclusive manner. Biochemistry. 37:10945-10955.
18. Fitter, S., T.H. Tetaz, M.C. Berndt, and L.K. Ashman. 1995. Molecular cloning of cDNA encoding a novel platelet-endothelial cell tetra-span antigen, PETA-3. Blood. 86:1348-1355.
19. Georges-Labouesse, E.N., N. Messaddeq, G. Yehia, L. Cadalbert, A. Dierich, and M. Le Meur. 1996. Absence of the alpha-6 integrin leads to epidermolysis bullosa and neonatal death in mice. Nat. Genet. 13:370-373.
20. Harris, A.K., D. Stopak, and P. Wild. 1981. Fibroblast traction as a mechanism for collagen morphogenesis. Nature. 290:249-251.
21. Hasegawa, H., Y. Utsunomiya, K. Kishimoto, K. Yanagisawa, and S. Fujita. 1996. SFA-1, a novel cellular gene induced by human T-cell leukemia virus type 1, is a member of the transmembrane 4 superfamily. J. Virol. 70:3258-3263.
22. Hemler, M.E. 1998. Integrin-associated proteins. Curr. Opin. Cell Biol. 10:578-585.
23. Hemler, M.E. 2001. Specific tetraspanin functions. J. Cell Biol. 155:1103-1107.
24. Hemler, M.E., B.A. Mannion, and F. Berditchevski. 1996. Association of TM4SF proteins with integrins: relevance to cancer. Biochim. Biophys. Acta. 1287:67-71.
25. Hynes, R.O. 1992. Integrins: versatility, modulation and signalling in cell adhesion. Cell. 69:11-25.
26. Indig, F.E., R. Diaz-Gonzalez, and M.H. Ginsberg. 1997. Analysis of the tetraspanin CD9-integrin αIIbβ3 (GPIIb-Illa) complex in platelet membranes and transfected cells. Biochem. J. 327:291-298.
27. Kohno, M., H. Hasegawa, M. Miyake, T. Yamamoto, and S. Fujita. 2002. CD151 enhances cell motility and metastasis of cancer cells in the presence of focal adhesion kinase. Int. J. Cancer. 97:336-343.
28. Korff, T., and H.G. Augustin. 1999. Tensional forces in fibrillar extracellular matrices control directional capillary sprouting. J. Cell Sci. 112(Pt 19):3249-3258.
29. Kreidberg, J.A. 2000. Functions of alpha3beta1 integrin. Curr. Opin. Cell Biol. 12:548-553.
30. Kreidberg, J.A., M.J. Donovan, S.L. Goldstein, H. Rennke, K. Shepherd, R.C. Jones, and R. Jaenisch. 1996. α3β1 integrin has a crucial role in kidney and lung organogenesis. Development. 122:3537-3547.
31. Lee, R.T., F. Berditchevski, G.C. Cheng, and M.E. Hemler. 1995. Integrin-mediated collagen matrix reorganization by cultured human vascular smooth muscle cells. Circ. Res. 76:209-214.
32. Mayer, U., G. Saher, R. Fässler, A. Bornemann, R. Echtermeyer, K. Von der Mark, N. Miosge, and E. Poeschl, 1997. Absence of integrin α7 causes a novel form of muscular dystrophy. Nat. Genet. 17:318-323.
33. McCaffrey, P.G., D.A. Newsome, E. Fibach, M. Yoshida, and M.S. Su. 1997. Induction of gamma-globin by histone deacetylase inhibitors. Blood. 90:2075-2083.
34. Mercurio, A.M., I. Rabinovitz, and L.M. Shaw. 2001. The alpha 6 beta 4 integrin and epithelial cell migration. Curr. Opin. Cell Biol. 13:541-545.
35. Penas, P.F., A. Garcia-Diez, F. Sanchez-Madrid, and M. Yanez-Mo. 2000. Tetraspanins are localized at motility-related structures and involved in normal human keratinocyte wound healing migration. J. Invest. Dermatol. 114:1126-1135.
36. Pesando, J.M., P. Hoffman, and T. Conrad. 1986. Malignant human B cells express two populations of p24 surface antigens. J. Immunol. 136:2709-2714.
37. Rabinovitz, I., I.K. Gipson, and A.M. Mercurio. 2001. Traction forces mediated by alpha6beta4 integrin: implications for basement membrane organization and tumor invasion. Mol. Biol. Cell. 12:4030-4043.
38. Serru, V., F.L. Naour, M. Billard, D.O. Azorsa, F. Lanza, C. Boucheix, and E. Ruinstein. 1999. Selective tetraspan-integrin complexes (CD81/alpha4beta1, CD151/alpha3beta1, CD151/alpha6beta1) under conditions disrupting tetraspan interactions. Biochem. J. 340:103-111.
39. Sincock, P.M., S. Fitter, R.G. Patton, M.C. Berndt, J.R. Gamble, and L.K. Ashman. 1999. PETA-3/CD151, a member of the transmembrane 4 superfamily, is localised to the plasma membrane and endocytic system of endothelial cells, associates with multiple integrins and modulates cell function. J. Cell Sci. 112:833-844.
40. Sterk, L.M., C.A. Geuijen, L.C. Oomen, J. Calafat, H. Janssen, and A. Sonnenberg. 2000. The tetraspan molecule CD151, a novel constituent of hemidesmosomes, associates with the integrin alpha6bera4 and may regulate the spatial organization of hemidesmosomes. J. Cell Biol. 149:969-982.
41. Sterk, L.M., C.A. Geuijen, J.G. van Den Berg, N. Claessen, J.J. Weening, and A. Sonnenberg. 2002. Association of the tetraspanin C D151 with the laminin-binding integrins alpha3beta1, alpha6beta1, alpha6beta4 and alpha7beta1 in cells in culture and in vivo. J. Cell Sci. 115:1161-1173.
42. Stipp, C.S., and M.E. Hernler. 2000. Transmembrane-4-Superfamily proteins CD151 and CD81 associate with α3β1. integrin, and selectively contribute to α3β1-dependent neurite outgrowth. J. Cell Sci. 113:1871-1882.
43. Stipp, C.S., D. Orlicky, and M.E. Hemler. 2001. FPRP: A major, higly stoichiometric, highly specific CD81 and CD9-associated protein. J. Biol. Chem. 276:4853-4862.
44. Tachibana, I., J. Bodorova, F. Berditchevski, M.M. Zutter, and M.E. Hemler. 1997. NAG-2, a novel transmembrane-4 superfamily (TM4SF) protein that complexes with integrins and other TM4SF proteins. J. Biol. Chem. 272:29181-29189.
45. Testa, J.E., P.C. Brooks, J.M. Lin, and J.P. Quigley. 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.
46. Tokuhara, T., H. Hasegawa, N. Hattori, H. Ishida, T. Taki, S. Tachibana, S. Sasaki, and M. Miyake. 2001. Clinical significance of CD151 gene expression in non-small cell lung cancer. Clin. Cancer Res. 7:4109-4114.
47. Vernon, R.B., and E.H. Sage. 1995. Between molecules and morphology. Extracellular matrix and creation of vascular form. Am. J. Pathol. 147:873-883.
48. Vernon, R.B., J.C. Angello, M.L. Iruela-Arispe, T.F. Lane, and E.H. Sage. 1992. Reorganization of basement membrane matrices by cellular traction promotes the formation of cellular networks in vitro. Lab. Invest. 66:536-547.
49. Wei, J., L.M. Shaw, and A.M. Mercurio. 1997. Integrin signaling in leukocytes: lessons from the α6β1 integrin. J. Leukoc. Biol. 61:397-407.
50. Weitzman, J.B., R. Pasqualini, Y. Takada, and M.E. Hemler. 1993. The function and distinctive regulation of the integrin VLA-3 in cell adhesion, spreading and homotypic cell aggregation. J. Biol. Chem. 268:8651-8657.
51. 3 integrin. Cell Adhes. Commun. 4:41-52.
52. Woods, A., and J.R. Couchman. 2000. Integrin modulation by lateral association. J. Biol. Chem. 275:24233-24236.
53. Wu, X.-R., J.J. Medina, and T.-T. Sun. 1995. Selective interactions of UPIa and UPIb, two members of the transmembrane 4 superfamily, with distinct single transmembrane-domained proteins in differentiated urothelial cells. J. Biol. Chem. 270:29752-29759.
54. Yánez-Mó, M., A. Alfranca, C. Cabahas, M. Marazuela, R. Tejedor, M.A. Ursa, L.K. Ashman, M.O. De Landázuri, and F. Sánchez-Madrid. 1998. Regulation of endothelial cell motility by complexes of tetraspan molecules CD81/TAPA-1 and CD151/PETA-3 with α3β1 integrin localized at endothelial lateral junctions. J. Cell Biol. 141:791-804.
55. Yánez-Mó, M., M. Mittelbrunn, and F. Sanchez-Madrid. 2001. Tetraspanins and intercellular interactions. Microcirculation. 8:153-168.
56. Yang, X., C. Claas, S.-K. Kraeft, L.B. Chen, Z. Wang, J.A. Kreidberg, and M.E. Hemler. 2002. Palmitoylation of tetraspanin proteins: modulation of CD151 lateral interactions, subcellular distribution, and integrin-dependent cell morphology. Mol. Biol. Cell. 13:767-781.
57. Yauch, R.L., F. Berdirchevski, M.B. Harler, J. Reichner, and M.E. Hemler. 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.
58. Yauch, R.L., A.R. Kazarov, B. Desai, R.T. Lee, and M.E. Hemler. 2000. Direct extracellular contact between integrin α3β1 and TM4SF protein CD151. J. Biol. Chem. 275:9230-9238.
59. Zhang, X.A., A.L. Bontrager, and M.E. Hemler. 2001. TM4SF proteins associate with activated PKC and link PKC to specific betal integrins. J. Biol. Chem. 276:25005-25013.
60. Zhang, X.A., A.R. Kazarov, X. Yang, A.L. Bontrager, C.S. Stipp, and M.E. Hemler. 2002. Function of the tetraspanin CD15 I-a6bl integrin complex during cellular morphogenesis. Mol. Biol. Cell. 13:1-11.