Syntenin-1 is a new component of tetraspanin-enriched microdomains: Mechanisms and consequences of the interaction of syntenin-1 with CD63

Molecular and Cellular Biology

Volumn 26, Issue 20, 2006, Pages 7707-7718

  Latysheva, Nadya ^a   Muratov, Gairat ^a   Rajesh, Sundaresan ^a   Padgett, Matthew ^a   Hotchin, Neil A ^a   Overduin, Michael ^a   Berditchevski, Fedor ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CD63 ANTIGEN; CELL RECEPTOR; INTEGRIN; MEMBRANE PROTEIN; PDZ PROTEIN; PDZ1 PROTEIN; PROTEIN TYROSINE KINASE; REGULATOR PROTEIN; SYNTENIN 1; TETRASPANIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOCHEMISTRY; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CONTROLLED STUDY; ENDOCYTOSIS; HUMAN; HUMAN CELL; INTERNALIZATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTON NUCLEAR MAGNETIC RESONANCE; TETRASPANIN ENRICHED MICRODOMAIN;

ANIMALS; ANTIGENS, CD; CERCOPITHECUS AETHIOPS; CRICETINAE; CYTOSOL; HUMANS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PLATELET MEMBRANE GLYCOPROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; SYNTAXIN 1;

EID: 33749635768     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00849-06     Document Type: Article

References (45)

1. Adey, N. B., L. Huang, P. A. Ormonde, M. L. Baumgard, R. Pero, D. V. Byreddy, S. V. Tavtigian, and P. L. Bartel. 2000. Threonine phosphorylation of the MMAC1/PTEN PDZ binding domain both inhibits and stimulates PDZ binding. Cancer Res. 60:35-37.
2. Amezcua, C. A., S. M. Harper, J. Rutter, and K. H. Gardner. 2002. Structure and interactions of PAS kinase N-terminal PAS domain: model for intramolecular kinase regulation. Structure 10:1349-1361.
3. Berditchevski, F. 2001. Complexes of tetraspanins with integrins: more than meets the eye. J. Cell Sci. 115:4143-4151.
4. 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.
5. Berditchevski, F., S. Chang, J. Bodorova, and M. E. Hemler. 1997. Generation of monoclonal antibodies to integrin-associated proteins. Evidence that alpha3beta1 complexes with EMMPRIN/basigin/OX47/M6. J. Biol. Chem. 272:29174-29180.
6. Berditchevski, F., and E. Odintsova. 1999. Characterization of integrin/tetraspanin adhesion complexes: role of tetraspanins in integrin signaling. J. Cell Biol. 146:477-492.
7. Berditchevski, F., K. F. Tolias, K. Wong, C. L. Carpenter, and M. E. Hemler. 1997. Novel link between integrins, TM4SF proteins (CD63, CD81) and phosphatidylinositol 4-kinase. J. Biol. Chem. 272:2595-2598.
8. Boukerche, H., Z. Z. Su, L. Emdad, P. Baril, B. Balme, L. Thomas, A. Randolph, K. Valerie, D. Sarkar, and P. B. Fisher. 2005. mda-9/syntenin: a positive regulator of melanoma metastasis. Cancer Res. 65:10901-10911.
9. Cierpicki, T., J. H. Bushweller, and Z. S. Derewenda. 2005. Probing the supramodular architecture of a multidomain protein: the structure of syntenin in solution. Structure 13:319-327.
10. Doyle, D. A., A. Lee, J. Lewis, E. Kim, M. Sheng, and R. MacKinnon. 1996. Crystal structures of a complexed and peptide-free membrane protein-binding domain: molecular basis of peptide recognition by PDZ. Cell 85:1067-1076.
11. Duffield, A., E. J. Kamsteeg, A. N. Brown, P. Pagel, and M. J. Caplan. 2003. The tetraspanin CD63 enhances the internalization of the H,K-ATPase beta-subunit. Proc. Natl. Acad. Sci. USA 100:15560-15565.
12. Escola, J.-M., M. J. Kleijmeer, W. Stoorvogel, J. Griffith, O. Yoshie, and H. J. Geuze. 1998. Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and exosomes secreted by human B-lymphocytes. J. Biol. Chem. 273:20121-20127.
13. Fernandez-Larrea, J., A. Merlos-Suarez, J. M. Urena, J. Baselga, and J. Arribas. 1999. A role for a PDZ protein in the early secretory pathway for the targeting of proTGF-alpha to the cell surface. Mol. Cell 3:423-433.
14. Fialka, I., P. Steinlein, H. Ahorn, G. Bock, P. D. Burbelo, M. Haberfellner, F. Lottspeich, K. Paiha, C. Pasquali, and L. A. Huber. 1999. Identification of syntenin as a protein of the apical early endocytic compartment in Madin-Darby canine kidney cells. J. Biol. Chem. 274:26233-26239.
15. Gimferrer, I., A. Ibanez, M. Farnos, M. R. Sarrias, R. Fenutria, S. Rosello, P. Zimmermann, G. David, J. Vives, C. Serra-Pages, and F. Lozano. 2005. The lymphocyte receptor CD6 interacts with syntenin-1, a scaffolding protein containing PDZ domains. J. Immunol. 175:1406-1414.
16. Grembecka, J., T. Cierpicki, Y. Devedjiev, U. Derewenda, B. S. Kang, J. H. Bushweller, and Z. S. Derewenda. 2006. The binding of the PDZ tandem of syntenin to target proteins. Biochemistry 45:3674-3683.
17. Grootjans, J. J., P. Zimmermann, G. Reekmans, A. Smets, G. Degeest, J. Durr, and G. David. 1997. Syntenin, a PDZ protein that binds syndecan cytoplasmic domains. Proc. Natl. Acad. Sci. USA 94:13683-13688.
18. 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.
19. Hemler, M. E. 2005. Tetraspanin functions and associated microdomains. Nat. Rev. Mol. Cell Biol. 6:801-811.
20. Hirbec, H., O. Perestenko, A. Nishimune, G. Meyer, S. Nakanishi, J. M. Henley, and K. K. Dev. 2002. The PDZ proteins PICK1, GRIP, and syntenin bind multiple glutamate receptor subtypes. Analysis of PDZ binding motifs. J. Biol. Chem. 277:15221-15224.
21. Jannatipour, M., P. Dion, S. Khan, H. Jindal, X. Fan, J. Laganiere, A. H. Chishti, and G. A. Rouleau. 2001. Schwannomin isoform-1 interacts with syntenin via PDZ domains. J. Biol. Chem. 276:33093-33100.
22. Janvier, K., and J. S. Bonifacino. 2005. Role of the endocytic machinery in the sorting of lysosome-associated membrane proteins. Mol. Biol. Cell. 16:4231-4242.
23. Kang, B. S., D. R. Cooper, Y. Devedjiev, U. Derewenda, and Z. S. Derewenda. 2003. Molecular roots of degenerate specificity in syntenin's PDZ2 domain: reassessment of the PDZ recognition paradigm. Structure 11:845-853.
24. Kang, B. S., D. R. Cooper, F. Jelen, Y. Devedjiev, U. Derewenda, Z. Dauter, J. Otlewski, and Z. S. Derewenda. 2003. PDZ tandem of human syntenin: crystal structure and functional properties. Structure 11:459-468.
25. Rarthikeyan, S., T. Leung, G. Birrane, G. Webster, and J. A. Ladias. 2001. Crystal structure of the PDZ1 domain of human Na(+)/H(+) exchanger regulatory factor provides insights into the mechanism of carboxyl-terminal leucine recognition by class I PDZ domains. J. Mol. Biol. 308:963-973.
26. Koo, T. H., J. J. Lee, E. M. Kim, R. W. Kim, H. D. Kim, and J. H. Lee. 2002. Syntenin is overexpressed and promotes cell migration in metastatic human breast and gastric cancer cell lines. Oncogene 21:4080-4088.
27. Koroll, M., F. G. Rathjen, and H. Volkmer. 2001. The neural cell recognition molecule neurofascin interacts with syntenin-1 but not with syntenin-2, both of which reveal self-associating activity. J. Biol. Chem. 276:10646-10654.
28. Kraulis, P. J., P. J. Domaille, S. L. Campbell-Burk, T. Van Aken, and E. D. Laue. 1994. Solution structure and dynamics of ras p21.GDP determined by heteronuclear three- and four-dimensional NMR spectroscopy. Biochemistry 33:3515-3531.
29. Levy, S., and T. Shoham. 2005. The tetraspanin web modulates immune-signalling complexes. Nat. Rev. Immunol. 5:136-148.
30. Lin, D., G. D. Gish, Z. Songyang, and T. Pawson. 1999. The carboxyl terminus of B class ephrins constitutes a PDZ domain binding motif. J. Biol. Chem. 274:3726-3733.
31. Long, J. F., W. Feng, R. Wang, L. N. Chan, F. C. Ip, J. Xia, N. Y. Ip, and M. Zhang. 2005. Autoinhibition of X11/Mint scaffold proteins revealed by the closed conformation of the PDZ tandem. Nat. Struct. Mol. Biol. 12:722-728.
32. Owen, D. J., and P. R. Evans. 1998. A structural explanation for the recognition of tyrosine-based endocytotic signals. Science 282:1327-1332.
33. Pelchen-Matthews, A., G. Raposo, and M. Marsh. 2004. Endosomes, exosomes and Trojan viruses. Trends Microbiol. 12:310-316.
34. Rous, B. A., B. J. Reaves, G. Ihrke, J. A. Briggs, S. R. Gray, D. J. Stephens, G. Banting, and J. P. Luzio. 2002. Role of adaptor complex AP-3 in targeting wild-type and mutated CD63 to lysosomes. Mol. Biol. Cell 13:1071-1082.
35. Royle, S. J., O. S. Qureshi, L. K. Bobanovic, P. R. Evans, D. J. Owen, and R. D. Murrell-Lagnado. 2005. Non-canonical YXXGPhi endocytic motifs: recognition by AP2 and preferential utilization in P2X4 receptors. J. Cell Sci. 118:3073-3080.
36. Sarkar, D., H. Boukerche, Z. Z. Su, and P. B. Fisher. 2004. mda-9/syntenin: recent insights into a novel cell signaling and metastasis-associated gene. Pharmacol. Ther. 104:101-115.
37. Shoham, T., R. Rajapaksa, C. Boucheix, E. Rubinstein, J. C. Poe, T. F. Tedder, and S. Levy. 2003. The tetraspanin CD81 regulates the expression of CD 19 during B cell development in a postendoplasmic reticulum compartment. J. Immunol. 171:4062-4072.
38. Takino, T., H. Miyamori, N. Kawaguchi, T. Uekita, M. Seiki, and H. Sato. 2003. Tetraspanin CD63 promotes targeting and lysosomal proteolysis of membrane-type 1 matrix metalloproteinase. Biochem. Biophys. Res. Commun. 304:160-166.
39. Then, C., M. Boussac, P. Veron, P. Ricciardi-Castagnoli, G. Raposo, J. Garin, and S. Amigorena. 2001. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J. Immunol. 166:7309-7318.
40. Tomoda, T., J. H. Kim, C. Zhan, and M. E. Hatten. 2004. Role of Unc51.1 and its binding partners in CNS axon outgrowth. Genes Dev. 18:541-558.
41. Vazquez, F., S. R. Grossman, Y. Takahashi, M. V. Rokas, N. Nakamura, and W. R. Sellers. 2001. Phosphorylation of the PTEN tail acts as an inhibitory switch by preventing its recruitment into a protein complex. J. Biol. Chem. 276:48627-48630.
42. Zhang, X. A., A. L. Bontrager, and M. E. Hemler. 2001. Transmembrane-4 superfamily proteins associate with activated protein kinase C (PKC) and link PKC to specific beta(1) integrins. J. Biol. Chem. 276:25005-25013.
43. Zimmermann, P., K. Meerschaert, G. Reekmans, I. Leenaerts, J. V. Small, J. Vandekerckhove, G. David, and J. Gettemans. 2002. PIP(2)-PDZ domain binding controls the association of syntenin with the plasma membrane. Mol. Cell 9:1215-1225.
44. Zimmermann, P., D. Tomatis, M. Rosas, J. Grootjans, I. Leenaerts, G. Degeest, G. Reekmans, C. Coomans, and G. David. 2001. Characterization of syntenin, a syndecan-binding PDZ protein, as a component of cell adhesion sites and microfilaments. Mol. Biol. Cell 12:339-350.
45. Zimmermann, P., Z. Zhang, G. Degeest, E. Mortier, I. Leenaerts, C. Coomans, J. Schulz, F. N'Kuli, P. J. Courtoy, and G. David. 2005. Syndecan recyling [sic] is controlled by syntenin-PIP2 interaction and Arf6. Dev. Cell 9:377-388.