Palmitoylation supports assembly and function of integrin-tetraspanin complexes

Journal of Cell Biology

Volumn 167, Issue 6, 2004, Pages 1231-1240

  Yang, Xiuwei ^a   Kovalenko, Oleg V ^a   Tang, Wei ^a   Claas, Christoph ^a   Stipp, Christopher S ^a   Hemler, Martin E ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA3 INTEGRIN; ALPHA6 INTEGRIN; ALPHA6BETA4 INTEGRIN; ANTIBODY; BETA4 INTEGRIN; CD151 ANTIGEN; CD63 ANTIGEN; CD81 ANTIGEN; CD9 ANTIGEN; CRK ASSOCIATED SUBSTRATE PROTEIN; DETERGENT; INTEGRIN; LAMININ; MEMBRANE ANTIGEN; PROTEIN P130; TETRASPANIN; UNCLASSIFIED DRUG;

ARTICLE; CELL SPREADING; COMPLEX FORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; LIPID MEMBRANE; MOUSE; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SUCROSE GRADIENT;

ANIMALS; ANTIGENS, CD; CELL LINE; HUMANS; INTEGRIN BETA3; INTEGRINS; MACROMOLECULAR SUBSTANCES; MEMBRANE GLYCOPROTEINS; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; PALMITIC ACID; PROTEIN SUBUNITS; RECEPTORS, GROWTH FACTOR; SRC-FAMILY KINASES;

EID: 11244304502     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200404100     Document Type: Article

References (58)

1. Adelsman, M.A., J.B. McCarthy, and Y. Shimizu. 1999. Stimulation of β1-integrin function by epidermal growth factor and heregulin-β has distinct requirements for erbB2 but a similar dependence on phosphoinositide 3-OH kinase. Mol. Biol. Cell. 10:2861-2878.
2. Anzai, N., Y. Lee, B.S. Youn, S. Fukuda, Y.J. Kim, C. Mantel, M. Akashi, and H.E. Broxmeyer. 2002. C-kit associated with the transmembrane 4 superfamily proteins constitutes a functionally distinct subunit in human hematopoietic progenitors. Blood. 99:4413-4421.
3. Baudoux, B., D. Castanares-Zapatero, M. Leclercq-Smekens, N. Berna, and Y. Poumay. 2000. The tetraspanin CD9 associates with the integrin alpha6beta4 in cultured human epidermal keratinocytes and is involved in cell motility. Eur. J. Cell Biol. 79:41-51.
4. Belkin, A.M., and M.A. Stepp. 2000. Integrins as receptors for laminins. Microsc. Res. Tech. 51:280-301.
5. Berditchevski, F. 2001. Complexes of tetraspanins with integrins: more than meets the eye. J. Cell Sci. 114:4143-4151.
6. 1 integrin and CD151-tetraspanin interactions by mutagenesis. J. Biol. Chem. 276:41165-41174.
7. 1 integrin with the tetraspanin-enriched microdomains and affects integrin-dependent signalling. J. Biol. Chem. 277:36991-37000.
8. Boucheix, C., and E. Rubinstein. 2001. Tetraspanins. Cell. Mol. Life Sci. 58:1189-1205.
9. Chapman, E.R., J. Blasi, S. An, N. Brose, P.A. Johnston, T.C. Sudhof, and R. Jahn. 1996. Fatty acylation of synaptotagmin in PC12 cells and synaptosomes. Biochem. Biophys. Res. Commun. 225:326-332.
10. Charrin, S., S. Manie, M. Oualid, M. Billard, C. Boucheix, and E. Rubinstein. 2002. Differential stability of tetraspanin/tetraspanin interactions: role of palmitoylation. FEBS Lett. 516:139-144.
11. Claas, C., C.S. Stipp, and M.E. Hemler. 2001. Evaluation of prototype TM4SF protein complexes and their relation to lipid rafts. J. Biol. Chem. 276:7974-7984.
12. Dipersio, C.M., S. Shah, and R.O. Hynes. 1995. α3Aβ1 integrin localizes to focal contacts in response to diverse extracellular matfix proteins. J. Cell Sci. 108:2321-2336.
13. Drbal, K., P. Angelisova, A.M. Rasmussen, I. Hilgert, S. Funderud, and V. Horejsi. 1999. The nature of the subset of MHC class II molecules carrying the CDw78 epitopes. Int. Immunol. 11:491-498.
14. Dunphy, J.T., and M.E. Linder. 1998. Signalling functions of protein palmitoylation. Biochim. Biophys. Acta. 1436:245-261.
15. Foster, L.J., C.L. De Hoog, and M. Mann. 2003. Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc. Natl. Acad. Sci. USA. 100:5813-5818.
16. Gagnoux-Palacios, L., M. Dans, W. van't Hof, A. Mariotti, A. Pepe, G. Meneguzzi, M.D. Resh, and F.G. Giancotti. 2003. Compartmentalization of integrin α6β4 signaling in lipid rafts. J. Cell Biol. 162:1189-1196.
17. 4 integrin and ErbB-2 receptor is required to promote phosphatidylinositol 3-kinase-dependent invasion. J. Biol. Chem. 275:10604-10610.
18. Cas-CrkII-DOCK180 pathway. J. Biol. Chem. 276:27090-27097.
19. Gundersen, C.B., A. Mastrogiacomo, K. Faull, and J.A. Umbach. 1994. Extensive lipidation of a Torpedo cysteine string protein. J. Biol. Chem. 269:19197-19199.
20. Hanke, J.H., J.P. Gardner, R.L. Dow, P.S. Changelian, W.H. Brissette, E.J. Weringer, B.A. Pollok, and P.A. Connelly. 1996. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck-and FynT-dependent T cell activation. J. Biol. Chem. 271:695-701.
21. Hemler, M.E. 1998. Integrin-associated proteins. Curr. Opin. Cell Biol. 10:578-585.
22. Hemler, M.E. 2001. Specific tetraspanin functions. J. Cell Biol. 155:1103-1107.
23. Hemler, M.E. 2003. Tetraspanin proteins mediate cellular penetration, invasion and fusion events, and define a novel type of membrane microdomain. Annu. Rev. Cell Dev. Biol. 19:397-422.
24. Higashiyama, S., R. Iwamoto, K. Goishi, G. Raab, N. Taniguchi, M. Klagsbrun, and E. Mekada. 1995. The membrane protein CD9/DRAP27 potentiates the juxtacrine growth factor activity of the membrane-anchored heparin-binding EGF-like growth factor. J. Cell Biol. 128:929-938.
25. Hintermann, E., M. Bilban, A. Sbarabi, and V. Quaranta. 2001. Inhibitory role of α6β4-associated erbB-2 and phosphoinositide 3-kinase in keratinocyte haptotactic migration dependent on α3β1 integrin. J. Cell Biol. 153:465-478.
26. 1 integrins in human epidermal keratinocytes. Cell Adhes. Commun. 4:297-305.
27. Kazarov, A.R., X. Yang, C.S. Stipp, B. Sehgal, and M.E. Hemler. 2002. An extracellular site on tetraspanin CD151 determines α3 and α6 integrin-dependent cellular morphology. J. Cell Biol. 158:1299-1309.
28. Koch, C., G. Staffler, R. Huttinger, I. Hilgert, E. Prager, J. Cerny, P. Steinlein, O. Majdic, V. Horejsi, and H. Stockinger. 1999. T cell activation-associated epitopes of CD147 in regulation of the T cell response, and their definition by antibody affinity and antigen density. Int. Immunol. 11:777-786.
29. Kolesnikova, T.V., C.S. Stipp, R.M. Rao, W.S. Lane, F.W. Luscinskas, and M.E. Hemler. 2004. EWI-2 modulates lymphocyte integrin α4β1 functions. Blood. 103:3013-3019.
30. Kovalenko, O.V., X. Yang, T.V. Kolesnikova, and M.E. Hemler. 2004. Evidence for specific tetraspanin homodimers: inhibition of palmitoylation makes cysteine residues available for cross-linking. Biochem. J. 377:407-417.
31. 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.
32. Levy, S., S.C. Todd, and H.T. Maecker. 1998. CD81 (TAPA-1): a molecule involved in signal transduction and cell adhesion in the immune system. Annu. Rev. Immunol. 16:89-109.
33. 4 integrin are regulated by EGF. J. Cell Biol. 134:241-253.
34. Mariotti, A., P.A. Kedeshian, M. Dans, A.M. Curatola, L. Gagnoux-Palacios, and F.G. Giancotti. 2001. EGF-R signaling through Fyn kinase disrupts the function of integrin α6β4 at hemidesmosomes: role in epithelial cell migration and carcinoma invasion. J. Cell Biol. 155:447-458.
35. Mercurio, A.M., I. Rabinovitz, and L.M. Shaw. 2001. The α6β4 integrin and epithelial cell migration. Curr. Opin. Cell Biol. 13:541-545.
36. Nojima, Y., T. Mimura, N. Morino, K. Hamasaki, H. Furuya, R. Sakai, T. Nakamoto, Y. Yazaki, and H. Hirai. 1996. Tyrosine phosphorylation of p130Cas in cell adhesion and transformation. Hum. Cell. 9:169-174.
37. O'Neill, G.M., S.J. Fashena, and E.A. Golemis. 2000. Integrin signalling: a new Cas(t) of characters enters the stage. Trends Cell Biol. 10:111-119.
38. Panetti, T.S. 2002. Tyrosine phosphorylation of paxillin, FAK, and p130CAS: effects on cell spreading and migration. Front. Biosci. 7:d143-d150.
39. Rabinovitz, I., A. Toker, and A.M. Mercurio. 1999. Protein kinase C-dependent mobilization of the α6β4 integrin from hemidesmosomes and its association with actin-rich cell protrusions drive the chemotactic migration of carcinoma cells. J. Cell Biol. 146:1147-1160.
40. Resh, M.D. 1999. Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim. Biophys. Acta. 1451:1-16.
41. Santoro, M.M., G. Gaudino, and P.C. Marchisio. 2003. The MSP receptor regulates α6β4 and α3β1 integrins via 14-3-3 proteins in keratinocyte migration. Dev. Cell. 5:257-271.
42. Serru, V., F.L. Naour, M. Billard, D.O. Azorsa, F. Lanza, C. Boucheix, and E. Rubinstein. 1999. Selective tetraspan-integrin complexes (CD81/α4β1, CD151/α3β1, CD151/α6β1) under conditions disrupting tetraspan interactions. Biochem. J. 340:103-111.
43. Shaw, L.M., I. Rabinovitz, H.H. Wang, A. Toker, and A.M. Mercurio. 1997. Activation of phosphoinositide 3-OH kinase by the alpha6beta4 integrin promotes carcinoma invasion. Cell. 91:949-960.
44. Shi, W., H. Fan, L. Shum, and R. Derynck. 2000. The tetraspanin CD9 associates with transmembrane TGF-α and regulates TGF-α-induced EGF receptor activation and cell proliferation. J. Cell Biol. 148:591-602.
45. 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 α6β4 and may regulate the spatial organization of hemidesmosomes. J. Cell Biol. 149:969-982.
46. Sterk, L.M., C.A. Geuijen, J.G. van den Berg, N. Claessen, J.J. Weening, and A. Sonnenberg. 2002. Association of the tetraspanin CD151 with the laminin-binding integrins α3β1, α6β1, α6β4 and α7β1 in cells in culture and in vivo. J. Cell Sci. 115:1161-1173.
47. Stipp, C.S., and M.E. Hemler. 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.
48. Stipp, C.S., T.V. Kolesnikova, and M.E. Hemler. 2003a. EWI-2 regulates α3β1 integrin-dependent cell functions on laminin-5. J. Cell Biol. 163:1167-1177.
49. Stipp, C.S., T.V. Kolesnikova, and M.E. Hemler. 2003b. Functional domains in tetraspanin proteins. Trends Biochem. Sci. 28:106-112.
50. Trusolino, L., A. Bertotti, and P.M. Comoglio. 2001. A signaling adapter function for α6β4 integrin in the control of HGF-dependent invasive growth. Cell. 107:643-654.
51. Wang, Z., J.M. Symons, S.L. Goldstein, A. McDonald, J.H. Miner, and J.A. Kreidberg. 1999. α3β1 integrin regulates epithelial cytoskeletal organization. J. Cell Sci. 112:2925-2935.
52. Yánez-Mó, M., A. Alfranca, C. Cabañas, 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.
53. 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.
54. Yauch, R.L., and M.E. Hemler. 2000. Specific interactions among transmembrane 4 superfamily (TM4SF) proteins and phosphatidylinositol 4-kinase. Biochem. J. 351:629-637.
55. Yauch, R.L., F. Berditchevski, 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.
56. 1 and TM4SF protein CD151. J. Biol. Chem. 275:9230-9238.
57. 1 integrins. J. Biol. Chem. 276:25005-25013.
58. Zhang, X.A., A.R. Kazarov, X. Yang, A.L. Bontrager, C.S. Stipp, and M.E. Hemler. 2002. Function of the tetraspanin CD151-α6β1 integrin complex during cellular morphogenesis. Mol. Biol. Cell. 13:1-11.