TspanC8 tetraspanins and a disintegrin and metalloprotease 10 (ADAM10) interact via their extracellular regions: Evidence for distinct binding mechanisms for different TspanC8 proteins

Journal of Biological Chemistry

Volumn 291, Issue 7, 2016, Pages 3145-3157

  Noy, Peter J ^a   Yang, Jing ^a   Reyat, Jasmeet S ^a   Matthews, Alexandra L ^a   Charlton, Alice E ^a   Furmston, Joanna ^a   Rogers, David A ^a   Ed Rainger, G ^a   Tomlinson, Michael G ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINS; CELL MEMBRANES; DISEASES; PROTEINS; SUBSTRATES;

CO-IMMUNOPRECIPITATIONS; EMBRYONIC DEVELOPMENT; ENDOPLASMIC RETICULUM; INTERACTION MECHANISMS; INTRACELLULAR TRAFFICKING; OVEREXPRESSION SYSTEMS; SUBSTRATE SELECTIVITY; TRANS-MEMBRANE PROTEINS;

ENZYME ACTIVITY;

ADAM10 ENDOPEPTIDASE; NERVE CELL ADHESION MOLECULE; TETRASPANIN; TETRASPANIN 14; UNCLASSIFIED DRUG; ADAM PROTEIN; ADAM10 PROTEIN, HUMAN; ADAM10 PROTEIN, MOUSE; CD9 ANTIGEN; CD9 PROTEIN, HUMAN; HYBRID PROTEIN; MEMBRANE PROTEIN; PEPTIDE FRAGMENT; SECRETASE; TSPAN14 PROTEIN, HUMAN; TSPAN17 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; CELL MATURATION; CELL MIGRATION; CELL SURFACE; CELLULAR DISTRIBUTION; COIMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM; ENDOTHELIUM CELL; EXTRACELLULAR SPACE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; THROMBOCYTE; ANIMAL; CELL CULTURE; CELL LINE; CELL MEMBRANE; CHEMISTRY; COMPARATIVE STUDY; CYTOLOGY; ENZYME ACTIVATION; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; METABOLISM; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; SURFACE PROPERTY; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR ENDOTHELIUM;

ADAM PROTEINS; ADAM10 PROTEIN; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ANTIGENS, CD9; BLOOD PLATELETS; CELL LINE; CELL MEMBRANE; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MEMBRANE PROTEINS; MICE; PEPTIDE FRAGMENTS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PROTEOLYSIS; RECOMBINANT FUSION PROTEINS; SUBSTRATE SPECIFICITY; SURFACE PROPERTIES; TETRASPANINS;

EID: 84966293694     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.703058     Document Type: Article

References (40)

1. Saftig, P., and Reiss, K. (2011) The "A Disintegrin And Metalloproteases" ADAM10 and ADAM17: Novel drug targets with therapeutic potential? Eur. J. Cell Biol. 90, 527-535
2. Dreymueller, D., Pruessmeyer, J., Groth, E., and Ludwig, A. (2012) The role of ADAM-mediated shedding in vascular biology. Eur. J. CellBiol. 91, 472-485
3. Hartmann, D., de Strooper, B., Serneels, L., Craessaerts, K., Herreman, A., Annaert, W., Umans, L., Lübke, T., Lena Illert, A., Figura, von, K., and Saftig, P. (2002) The disintegrin/metalloprotease ADAM 10 is essential for Notch signalling but not for a-secretase activity in fibroblasts. Hum. Mol. Genet 11, 2615-2624
4. Bender, M., Hofmann, S., Stegner, D., Chalaris, A., Bösl, M., Braun, A., Scheller, J., Rose-John, S., and Nieswandt, B. (2010) Differentially regulated GPVI ectodomain shedding by multiple platelet-expressed proteinases. Blood 116, 3347-3355
5. Gardiner, E. E., Karunakaran, D., Shen, Y., Arthur, J. F., Andrews, R. K., and Berndt, M. C. (2007) Controlled shedding of platelet glycoprotein (GP) VI and GPIb-IX-V by ADAM family metalloproteinases. J. Thromb. Haemost. 5, 1530-1537
6. van der Vorst, E. P. C., Keijbeck, A. A., de Winther, M. P., and Donners, M. M. (2012) A disintegrin and metalloproteases: Molecular scissors in angiogenesis, inflammation and atherosclerosis. Atherosclerosis 224, 302-308
7. Murphy, G. (2008) The ADAMs: signalling scissors in the tumour microenvironment. Nat. Rev. Cancer. 8, 932-941
8. Haining, E. J., Yang, J., Bailey, R. L., Khan, K., Collier, R., Tsai, S., Watson, S. P., Frampton, J., Garcia, P., and Tomlinson, M. G. (2012) The TspanC8 subgroup of tetraspanins interacts with A disintegrin and metalloprotease 10 (ADAM10) and regulates its maturation and cell surface expression. J. Biol. Chem. 287, 39753-39765
9. Prox, J., Willenbrock, M., Weber, S., Lehmann, T., Schmidt-Arras, D., Schwanbeck, R., Saftig, P., and Schwake, M. (2012) Tetraspanin15 regulates cellular trafficking and activity of the ectodomain sheddase ADAM10. Cell Mol. Life Sci. 69, 2919-2932
10. Dornier, E., Coumailleau, F., Ottavi, J.-F., Moretti, J., Boucheix, C, Maudui, P., Schweisgut, F., and Rubinstein, E. (2012) TspanC8 tetraspanins regulate ADAM10/Kuzbanian trafficking and promote Notch activation in flies and mammals. J. Cell Biol. 199, 481-496
11. Charrin, S., Jouannet, S., Boucheix, C, and Rubinstein, E. (2014) Tetraspanins at a glance. J. Cell Sci. 127, 3641-3648
12. Hemler, M. E. (2014) Tetraspanin proteins promote multiple cancer stages. Nat Rev. Cancer. 14, 49-60
13. Zhou, J., Fujiwara, T., Ye, S., Li, X., and Zhao, H. (2014) Downregulationof Notch Modulators, Tetraspanin 5 and 10, Inhibits Osteoclastogenesis in Vitro. Calcif. Tissue Int. 95, 209-217
14. 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
15. Protty, M. B., Watkins, N A., Colombo, D., Thomas, S. G., Heath, V. L., Herbert, J. M. J., Bicknell, R., Senis, Y. A., Ashman, L. K., Berditchevski, F., Ouwehand, W. H, Watson, S. P., and Tomlinson, M. G. (2009) Identification of Tspan9 as a novel platelet tetraspanin and the collagen receptor GPVI as a component of tetraspanin microdomains. Biochem. J. 417, 391-400
16. Tomlinson, M. G., Woods, D. B., McMahon, M., Wahl, M. I., Witte, O.., Kurosaki, T., Bolen, J. B., and Johnston, J. A. (2001) A conditional form of Bruton's tyrosine kinase is sufficient to activate multiple downstream signaling pathways via PLC γ2 in B cells. BMC Immunol. 2, 4
17. Horiuchi, K., Le Gall, S., Schulte, M., Yamaguchi, T., Reiss, K., Murphy, G., Toyama, Y., Hartmann, D., Saftig, P., and Blobel, C. P. (2007) Substrate selectivity of epidermal growth factor-receptor ligand sheddases and their regulation by phorbol esters and calcium influx. Mol. Biol. Cell 18, 176-188
18. Liu, C, Xu, P., Lamouille, S., Xu, J., and Derynck, R. (2009) TACE-mediated ectodomain shedding of the type I TGF-β receptor downregulates TGF-β signaling. Mol. Cell 35, 26-36
19. Berlanga, O., Bori-Sanz, T., James, J. R., Frampton, J., Davis, S. J., Tomlinson, M. G., and Watson, S. P. (2007) Glycoprotein VI oligomerization in cell lines and platelets. J. Thromb. Haemost. 5, 1026-1033
20. Ehrhardt, C, Schmolk, M., Matzk, A., Knoblauch, A., Will, C, Wixler, V., and Ludwig, S. (2006) Polyethylenimine, a cost-effective transfection reagent. Signal Transduct. 6, 179-184
21. Noy, P. J., Lodhia, P., Khan, K., Zhuang, X., Ward, D. G., Verissimo, A. R., Bacon, A., and Bicknell, R. (2015) Blocking CLEC14A-MMRN2 binding inhibits sprouting angiogenesis and tumour growth. Oncogene 34, 5821-5831
22. Wilson, E., Leszczynska, K., Poulter, N. S., Edelmann, F., Salisbury, V. A., Noy, P. J., Bacon, A., Rappoport, J. Z., Heath, J. K., Bicknell, R., and Heath, V. L. (2014) RhoJ interacts with the GIT-PIX complex and regulates focal adhesion disassembly. J. Cell Sci. 127, 3039-3051
23. McCarty, O. J. T., Calaminus, S. D. J., Berndt, M.., Machesky, L. M., and Watson, S. P. (2006) von Willebrand factor mediates platelet spreading through glycoprotein Ib and α (IIb) β3 in the presence of botrocetin and ristocetin, respectively. J. Thromb. Haemost. 4, 1367-1378
24. Pearce, A.., Senis, Y. A., Billadeau, D. D., Turner, M., Watson, S. P., and Vigorito, E. (2004) Vav1 and vav3 have critical but redundant roles in mediating platelet activation by collagen. J. Biol. Chem. 279, 53955-53962
25. 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
26. Tomlinson, M. G. (2009) Platelet tetraspanins: small but interesting. J. Thromb. Haemost. 7, 2070-2073
27. Seigneuret, M., Conjeaud, H., Zhang, H.-T., and Kong, X.-P. (2013) Structural Bases for Tetraspanin Functions in Tetraspanins, Springer Netherlands, Dordrecht
28. Reiss, K., Maretzky, T., Ludwig, A., Tousseyn, T., de Strooper, B., Hartmann, D., and Saftig, P. (2005) ADAM10 cleavage of N-cadherin and regulation of cell-cell adhesion and beta-catenin nuclear signalling. EMBO J. 24, 742-752
29. Rubinstein, E., Charrin, S., and Tomlinson, M. G. (2013) Organisation of the Tetraspanin Web in Tetraspanins, Springer Netherlands, Dordrecht
30. Stipp, C. S., Kolesnikova, T. V., and Hemler, M. E. (2003) Functional domains in tetraspanin proteins. Trends Biochem. Sci. 28, 106-112
31. Huang, S., Yuan, S., Dong, M., Su, J., Yu, C, Shen, Y., Xie, X., Yu, Y., Yu, X., Chen, S., Zhang, S., Pontarotti, P., and Xu, A. (2005) The phylogenetic analysis of tetraspanins projects the evolution of cell-cell interactions from unicellular to multicellular organisms. Genomics 86, 674-684
32. Min, G., Wang, H., Sun, T.-T., and Kong, X.-P. (2006) Structural basis for tetraspanin functions as revealed by the cryo-EM structure of uroplakin complexes at 6-A resolution. J. CellBiol. 173, 975-983
33. Yauch, R. L., Kazarov, A. R., Desai, B., Lee, R. T., and Hemler, M. E. (2000) Direct extracellular contact between integrin α (3) β (1) and TM4SF protein CD151. J. Biol. Chem. 275, 9230-9238
34. Berditchevski, F., Gilbert, E., Griffiths, M. R., Fitter, S., Ashman, L., and Jenner, S. J. (2001) Analysis of the CD151-α3β1 integrin and CD151-tetraspanin interactions by mutagenesis. J. Biol. Chem. 276, 41165-41174
35. Yáñez-Mó, M., Alfranca, A., Cabañas, C., Marazuela, M., Tejedor, R., Ursa, M. A., Ashman, L. K., de Landázuri, M. O., and Sánchez-Madrid, F. (1998) Regulation of endothelial cell motility by complexes of tetraspan molecules CD81/TAPA-1 and CD151/PETA-3 with α3 β1 integrin localized at endothelial lateral junctions. J. Cell Biol. 141, 791-804
36. Shoham, T., Rajapaksa, R., Kuo, C.-C., Haimovich, J., and Levy, S. (2006) Building of the tetraspanin web: distinct structural domains of CD81 function in different cellular compartments. Mol. Cell Biol. 26, 1373-1385
37. Shoham, T., Rajapaksa, R., Boucheix, C., Rubinstein, E., Poe, J. C., Tedder, T. F., and Levy, S. (2003) The tetraspanin CD81 regulates the expression of CD19 during B cell development in a postendoplasmic reticulum compartment. J. Immunol. 171, 4062-4072
38. Montpellier, C., Tews, B. A., Poitrimole, J., Rocha-Perugini, V., D'Arienzo, V., Potel, J., Zhang, X. A., Rubinstein, E., Dubuisson, J., and Cocquerel, L. (2011) Interacting regions of CD81 and two of its partners, EWI-2 and EWI-2wint, and their effect on hepatitis C virus infection. J. Biol. Chem. 286, 13954-13965
39. Charrin, S., Le Naour, F., Labas, V., Billard, M., Le Caer, J.-P., Emile, J.-F., Petit, M.-A., Boucheix, C., and Rubinstein, E. (2003) EWI-2 is a new component of the tetraspanin web in hepatocytes and lymphoid cells. Biochem. J. 373, 409-421
40. Metharom, P., Berndt, M. C., Baker, R. I., and Andrews, R. K. (2015) Current state and novel approaches of antiplatelet therapy. Arterioscler. Thromb. Vasc. Biol. 35, 1327-1338 10.1074/jbc. M115.703058