Tetraspanin CD63 promotes vascular endothelial growth factor receptor 2-β1 integrin complex formation, thereby regulating activation and downstream signaling in endothelial cells in Vitro and in Vivo

Journal of Biological Chemistry

Volumn 288, Issue 26, 2013, Pages 19060-19071

  Tugues, Sònia ^a   Honjo, Satoshi ^a   König, Christian ^a   Padhan, Narendra ^a   Kroon, Jeffrey ^a   Gualandi, Laura ^a   Li, Xiujuan ^a   Barkefors, Irmeli ^b   Thijssen, Victor L ^c   Griffioen, Arjan W ^c   Claesson Welsh, Lena ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE EXPRESSION; COMPLEX FORMATIONS; MEMBRANE PROTEINS; RECEPTOR TYROSINE KINASE; SYSTEMIC DELIVERIES; TETRASPANIN; TUBE FORMATION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR;

ADHESION; AMINO ACIDS; CELL MEMBRANES; ENDOTHELIAL CELLS; SIGNALING;

CELL SIGNALING;

BETA1 INTEGRIN; CD63 ANTIGEN; VASCULOTROPIN RECEPTOR 2;

ARTICLE; CAPILLARY SPROUTING; CELL ACTIVATION; CELL ADHESION; CELL MIGRATION; CELL SURFACE; CELLULAR PARAMETERS; COMPLEX FORMATION; CONTROLLED STUDY; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; INTRACELLULAR SIGNALING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TUBE FORMATION; UMBILICAL VEIN ENDOTHELIAL CELL;

ANGIOGENESIS; CD63; ENDOTHELIAL CELL; RECEPTOR TYROSINE KINASE; TETRASPANINS; VASCULAR ENDOTHELIAL GROWTH FACTOR (VEGF);

ANIMALS; ANTIGENS, CD29; ANTIGENS, CD63; CELL ADHESION; CELL MEMBRANE; CHEMOTAXIS; ENDOTHELIAL CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LUNG; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN BINDING; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84879570295     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.468199     Document Type: Article

References (51)

1. Potente, M., Gerhardt, H., and Carmeliet, P. (2011) Basic and therapeutic aspects of angiogenesis. Cell 146, 873-887
2. Eilken, H. M., and Adams, R. H. (2010) Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr. Opin. Cell Biol. 22, 617-625
3. Koch, S., Tugues, S., Li, X., Gualandi, L., and Claesson-Welsh, L. (2011) Signal transduction by vascular endothelial growth factor receptors. Biochem. J. 437, 169-183
4. Margadant, C., Monsuur, H. N., Norman, J. C., and Sonnenberg, A. (2011) Mechanisms of integrin activation and trafficking. Curr. Opin. Cell Biol. 23, 607-614
5. Mitra, S. K., and Schlaepfer, D. D. (2006) Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr. Opin. Cell Biol. 18, 516-523 (Pubitemid 44332916)
6. Ramjaun, A. R., and Hodivala-Dilke, K. (2009) The role of cell adhesion pathways in angiogenesis. Int. J. Biochem. Cell Biol. 41, 521-530
7. Ross, R. S. (2004) Molecular and mechanical synergy. Cross-talk between integrins and growth factor receptors. Cardiovasc. Res. 63, 381-390
8. Hemler, M. E. (2005) Tetraspanin functions and associated microdomains. Nat. Rev. Mol. Cell Biol. 6, 801-811
9. Yunta, M., and Lazo, P. A. (2003) Tetraspanin proteins as organisers of membrane microdomains and signalling complexes. Cell. Signal. 15, 559-564 (Pubitemid 36385161)
10. Yáñez-Mó, M., Barreiro, O., Gordon-Alonso, M., Sala-Valdés, M., and Sánchez-Madrid, F. (2009) Tetraspanin-enriched microdomains. A functional unit in cell plasma membranes. Trends Cell Biol. 19, 434-446
11. Hotta, H., Ross, A. H., Huebner, K., Isobe, M., Wendeborn, S., Chao, M. V., Ricciardi, R. P., Tsujimoto, Y., Croce, C. M., and Koprowski, H. (1988) Molecular cloning and characterization of an antigen associated with early stages of melanoma tumor progression. Cancer Res. 48, 2955-2962
12. Schröder, J., Lüllmann-Rauch, R., Himmerkus, N., Pleines, I., Nieswandt, B., Orinska, Z., Koch-Nolte, F., Schröder, B., Bleich, M., and Saftig, P. (2009) Deficiency of the tetraspanin CD63 associated with kidney pathology but normal lysosomal function. Mol. Cell. Biol. 29, 1083-1094
13. Doyle, E. L., Ridger, V., Ferraro, F., Turmaine, M., Saftig, P., and Cutler, D. F. (2011) CD63 is an essential cofactor to leukocyte recruitment by endothelial P-selectin. Blood 118, 4265-4273
14. Koyama, Y., Suzuki, M., and Yoshida, T. (1998) CD63, a member of tetraspan transmembrane protein family, induces cellular spreading by reaction with monoclonal antibody on substrata. Biochem. Biophys. Res. Commun. 246, 841-846 (Pubitemid 28420946)
15. Toothill, V. J., Van Mourik, J. A., Niewenhuis, H. K., Metzelaar, M. J., and Pearson, J. D. (1990) Characterization of the enhanced adhesion of neutrophil leukocytes to thrombin-stimulated endothelial cells. J. Immunol. 145, 283-291 (Pubitemid 20217413)
16. Skubitz, K. M., Campbell, K. D., Iida, J., and Skubitz, A. P. (1996) CD63 associates with tyrosine kinase activity and CD11/CD18, and transmits an activation signal in neutrophils. J. Immunol. 157, 3617-3626 (Pubitemid 126449176)
17. Mantegazza, A. R., Barrio, M. M., Moutel, S., Bover, L., Weck, M., Brossart, P., Teillaud, J. L., and Mordoh, J. (2004) CD63 tetraspanin slows down cell migration and translocates to the endosomal-lysosomal-MIICs route after extracellular stimuli in human immature dendritic cells. Blood 104, 1183-1190 (Pubitemid 39038041)
18. Radford, K. J., Thorne, R. F., and Hersey, P. (1997) Regulation of tumor cell motility and migration by CD63 in a human melanoma cell line. J. Immunol. 158, 3353-3358 (Pubitemid 127484053)
19. Lee, M., Hadi, M., Halldén, G., and Aponte, G. W. (2005) Peptide YY and neuropeptide Y induce villin expression, reduce adhesion, and enhance migration in small intestinal cells through the regulation of CD63, matrix metalloproteinase-3, and Cdc42 activity. J. Biol. Chem. 280, 125-136 (Pubitemid 40164973)
20. Jung, K. K., Liu, X. W., Chirco, R., Fridman, R., and Kim, H. R. (2006) Identification of CD63 as a tissue inhibitor of metalloproteinase-1 interacting cell surface protein. EMBO J. 25, 3934-3942 (Pubitemid 44338736)
21. Dell'Angelica, E. C., Shotelersuk, V., Aguilar, R. C., Gahl, W. A., and Bonifacino, J. S. (1999) Altered trafficking of lysosomal proteins in Hermansky-Pudlak syndrome due to mutations in the β 3A subunit of the AP-3 adaptor. Mol. Cell 3, 11-21 (Pubitemid 29292473)
22. Bailey, R. L., Herbert, J. M., Khan, K., Heath, V. L., Bicknell, R., and Tomlinson, M. G. (2011) The emerging role of tetraspanin microdomains on endothelial cells. Biochem. Soc. Trans. 39, 1667-1673
23. Vischer, U. M., and Wagner, D. D. (1993) Cd63 Is A Component of Weibel-Palade Bodies of Human Endothelial-Cells. Blood 82, 1184-1191 (Pubitemid 23253992)
24. Söderberg, O., Gullberg, M., Jarvius, M., Ridderstråle, K., Leuchowius, K. J., Jarvius, J., Wester, K., Hydbring, P., Bahram, F., Larsson, L. G., and Landegren, U. (2006) Direct observation in situ of individual endogenous protein complexes by proximity ligation. Nat. Methods 3, 995-1000
25. Israels, S. J., McMillan-Ward, E. M., Easton, J., Robertson, C., and McNicol, A. (2001) CD63 associates with the αIIb β3 integrin-CD9 complex on the surface of activated platelets. Thromb. Haemost. 85, 134-141 (Pubitemid 32050955)
26. Chen, T. T., Luque, A., Lee, S., Anderson, S. M., Segura, T., and Iruela-Arispe, M. L. (2010) Anchorage of VEGF to the extracellular matrix conveys differential signaling responses to endothelial cells. J. Cell Biol. 188, 595-609
27. Latysheva, N., Muratov, G., Rajesh, S., Padgett, M., Hotchin, N. A., Overduin, M., and Berditchevski, F. (2006) Syntenin-1 is a new component of tetraspanin-enriched microdomains. Mechanisms and consequences of the interaction of syntenin-1 with CD63. Mol. Cell. Biol. 26, 7707-7718 (Pubitemid 44547717)
28. Lekishvili, T., Fromm, E., Mujoomdar, M., and Berditchevski, F. (2008) The tumour-associated antigen L6 (L6-Ag) is recruited to the tetraspanin-enriched microdomains. Implication for tumour cell motility. J. Cell Sci. 121, 685-694 (Pubitemid 351524167)
29. Berditchevski, F. (2001) Complexes of tetraspanins with integrins. More than meets the eye. J. Cell Sci. 114, 4143-4151
30. Eliceiri, B. P., and Cheresh, D. A. (2001) Adhesion events in angiogenesis. Curr. Opin. Cell Biol. 13, 563-568 (Pubitemid 32817014)
31. Radford, K. J., Thorne, R. F., and Hersey, P. (1996) CD63 associates with transmembrane 4 superfamily members, CD9 and CD81, and with β1 integrins in human melanoma. Biochem. Biophys. Res. Commun. 222, 13-18 (Pubitemid 26160050)
32. Iizuka, S., Kudo, Y., Yoshida, M., Tsunematsu, T., Yoshiko, Y., Uchida, T., Ogawa, I., Miyauchi, M., and Takata, T. (2011) Ameloblastin regulates osteogenic differentiation by inhibiting Src kinase via cross talk between integrin β1 and CD63. Mol. Cell. Biol. 31, 783-792
33. Berditchevski, F., Bazzoni, G., and Hemler, M. E. (1995) Specific association of Cd63 with the Vla-3 and Vla-6 integrins. J. Biol. Chem. 270, 17784-17790
34. Berditchevski, F., Zutter, M. M., and Hemler, M. E. (1996) Characterization of novel complexes on the cell surface between integrins and proteins with 4 transmembrane domains (TM4 proteins). Mol. Biol. Cell 7, 193-207 (Pubitemid 26064366)
35. Berditchevski, F., Tolias, K. F., Wong, K., Carpenter, C. L., and Hemler, M. E. (1997) A novel link between integrins, transmembrane-4 superfamily proteins (CD63 and CD81), and phosphatidylinositol 4-kinase. J. Biol. Chem. 272, 2595-2598 (Pubitemid 27053987)
36. 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 (Pubitemid 126449679)
37. Calalb, M. B., Polte, T. R., and Hanks, S. K. (1995) Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity. A role for Src family kinases. Mol. Cell. Biol. 15, 954-963
38. Hemler, M. E. (1998) Integrin associated proteins. Curr. Opin. Cell Biol. 10, 578-585
39. Heijnen, H. F., Van Lier, M., Waaijenborg, S., Ohno-Iwashita, Y., Waheed, A. A., Inomata, M., Gorter, G., Möbius, W., Akkerman, J. W., and Slot, J. W. (2003) Concentration of rafts in platelet filopodia correlates with recruitment of c-Src and CD63 to these domains. J. Thromb. Haemost. 1, 1161-1173
40. Ilić, D., Furuta, Y., Kanazawa, S., Takeda, N., Sobue, K., Nakatsuji, N., Nomura, S., Fujimoto, J., Okada, M., Yamamoto, T., and Aizawa, S. (1995) Reduced cell motility and enhanced focal adhesion contact formation in cells from Fak-deficient mice. Nature 377, 539-544
41. Levy, S., and Shoham, T. (2005) Protein-protein interactions in the tetraspanin web. Physiology 20, 218-224 (Pubitemid 41215195)
42. Sundberg, C., and Rubin, K. (1996) Stimulation of β1 integrins on fibroblasts induces PDGF independent tyrosine phosphorylation of PDGF beta-receptors. J. Cell Biol. 132, 741-752
43. Wang, R., Kobayashi, R., and Bishop, J. M. (1996) Cellular adherence elicits ligand-independent activation of the Met cell-surface receptor. Proc. Natl. Acad. Sci. U.S.A. 93, 8425-8430 (Pubitemid 26269574)
44. Zhang, X., Groopman, J. E., and Wang, J. F. (2005) Extracellular matrix regulates endothelial functions through interaction of VEGFR-3 and integrin α5β1. J. Cell Physiol. 202, 205-214 (Pubitemid 39603377)
45. Moro, L., Venturino, M., Bozzo, C., Silengo, L., Altruda, F., Beguinot, L., Tarone, G., and Defilippi, P. (1998) Integrins induce activation of EGF receptor. Role in MAP kinase induction and adhesion-dependent cell survival. EMBO J. 17, 6622-6632 (Pubitemid 28521796)
46. Eliceiri, B. P., Puente, X. S., Hood, J. D., Stupack, D. G., Schlaepfer, D. D., Huang, X. Z., Sheppard, D., and Cheresh, D. A. (2002) Src-mediated coupling of focal adhesion kinase to integrin αvβ5 in vascular endothelial growth factor signaling. J. Cell Biol. 157, 149-160
47. Mahabeleshwar, G. H., Feng, W., Reddy, K., Plow, E. F., and Byzova, T. V. (2007) Mechanisms of integrin-vascular endothelial growth factor receptor cross-activation in angiogenesis. Circ. Res. 101, 570-580 (Pubitemid 351325874)
48. Pols, M. S., and Klumperman, J. (2009) Trafficking and function of the tetraspanin CD63. Exp. Cell Res. 315, 1584-1592
49. Hupalowska, A., and Miaczynska, M. (2012) The new faces of endocytosis in signaling. Traffic 13, 9-18
50. Takeda, Y., Kazarov, A. R., Butterfield, C. E., Hopkins, B. D., Benjamin, L. E., Kaipainen, A., and Hemler, M. E. (2007) Deletion of tetraspanin Cd151 results in decreased pathologic angiogenesis in vivo and in vitro. Blood 109, 1524-1532 (Pubitemid 46239585)
51. Kamisasanuki, T., Tokushige, S., Terasaki, H., Khai, N. C., Wang, Y., Sakamoto, T., and Kosai, K. (2011) Targeting CD9 produces stimulus-independent antiangiogenic effects predominantly in activated endothelial cells during angiogenesis. A novel antiangiogenic therapy. Biochem. Biophys. Res. Commun. 413, 128-135