Thrombin-induced shedding of tumour endothelial marker 5 and exposure of its RGD motif are regulated by cell-surface protein disulfide-isomerase

Biochemical Journal

Volumn 441, Issue 3, 2012, Pages 937-944

  Vallon, Mario ^a   Aubele, Philipp ^a   Janssen, Klaus Peter ^a   Essler, Markus ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Cell surface protein disulfide isomerase (PDI); Cryptic RGD motif; Redox regulation; Shedding; Thrombin; Tumour endothelial marker 5 (TEM5)

Indexed keywords

CELL SURFACE PROTEIN; HETERODIMER; PEPTIDE FRAGMENT; PROTEIN DISULFIDE ISOMERASE; PROTEIN TUMOUR ENDOTHELIAL MARKER 5; THROMBIN; TUMOR MARKER; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; CELL SURFACE; CONTROLLED STUDY; DISULFIDE BOND; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN EXPRESSION;

CELLS, CULTURED; HEK293 CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; OLIGOPEPTIDES; PROTEIN DISULFIDE-ISOMERASES; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PROTEOLYSIS; RECEPTORS, G-PROTEIN-COUPLED; THROMBIN; TRANSFECTION;

EID: 84855911678     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111682     Document Type: Article

References (35)

1. Browder, T., Folkman, J. and Pirie-Shepherd, S. (2000) The hemostatic system as a regulator of angiogenesis. J. Biol. Chem. 275, 1521-1524 (Pubitemid 30060762)
2. Bluff, J. E., Brown, N. J., Reed, M. W. and Staton, C. A. (2008) Tissue factor, angiogenesis and tumour progression. Breast Cancer Res. 10, 204
3. Kisucka, J., Butterfield, C. E., Duda, D. G., Eichenberger, S. C., Saffaripour, S., Ware, J., Ruggeri, Z. M., Jain, R. K., Folkman, J. and Wagner, D. D. (2006) Platelets and platelet adhesion support angiogenesis while preventing excessive hemorrhage. Proc. Natl. Acad. Sci. U.S.A. 103, 855-860 (Pubitemid 43212187)
4. Coughlin, S. R. (2000) Thrombin signalling and protease-activated receptors. Nature 407, 258-264
5. Subramanian, S. V., Fitzgerald, M. L. and Bernfield, M. (1997) Regulated shedding of syndecan-1 and -4 ectodomains by thrombin and growth factor receptor activation. J. Biol. Chem. 272, 14713-14720 (Pubitemid 27251736)
6. 130 bonds. J. Biol. Chem. 280, 34441-34446
7. St. Croix, B., Rago, C., Velculescu, V., Traverso, G., Romans, K. E., Montgomery, E., Lal, A., Riggins, G. J., Lengauer, C., Vogelstein, B. and Kinzler, K. W. (2000) Genes expressed in human tumor endothelium. Science 289, 1197-1202 (Pubitemid 30650733)
8. Carson-Walter, E. B., Watkins, D. N., Nanda, A., Vogelstein, B., Kinzler, K. W. and St. Croix, B. (2001) Cell surface tumor endothelial markers are conserved in mice and humans. Cancer Res. 61, 6649-6655 (Pubitemid 32896479)
9. Vallon, M., Rohde, F., Janssen, K.-P. and Essler, M. (2010) Tumor endothelial marker 5 expression in endothelial cells during capillary morphogenesis is induced by the small GTPase Rac and mediates contact inhibition of cell proliferation. Exp. Cell Res. 316, 412-421
10. Kuhnert, F., Mancuso, M. R., Shamloo, A., Wang, H. T., Choksi, V., Florek, M., Su, H., Fruttiger, M., Young, W. L., Heilshorn, S. C. and Kuo, C. J. (2010) Essential regulation of CNS angiogenesis by the orphan G protein-coupled receptor GPR124. Science 330, 985-989
11. Bjarnadóttir, T. K., Fredriksson, R., Höglund, P. J., Gloriam, D. E., Lagerström, M. C. and Schiöth, H. B. (2004) The human and mouse repertoire of the adhesion family of G-protein-coupled receptors. Genomics 84, 23-33
12. Ruoslahti, E. (1996) RGD and other recognition sequences for integrins. Annu. Rev. Cell Dev. Biol. 12, 697-715
13. Senger, D. R., Perruzzi, C. A., Papadopoulos-Sergiou, A. and Van de Water, L. (1994) Adhesive properties of osteopontin: regulation by a naturally occurring thrombin-cleavage in close proximity to the GRGDS cell-binding domain. Mol. Biol. Cell 5, 565-574 (Pubitemid 24183445)
14. Xu, J., Rodriguez, D., Petitclerc, E., Kim, J. J., Hangai, M., Moon, Y. S., Davis, G. E. and Brooks, P. C. (2001) Proteolytic exposure of a cryptic site within collagen type IV is required for angiogenesis and tumor growth in vivo. J. Cell Biol. 154, 1069-1079 (Pubitemid 34286185)
15. Aumailley, M., Gerl, M., Sonnenberg, A., Deutzmann, R. and Timpl, R. (1990) Identification of the Arg-Gly-Asp sequence in laminin A chain as a latent cell-binding site being exposed in fragment P1. FEBS Lett. 262, 82-86 (Pubitemid 20104266)
16. Vallon, M. and Essler, M. (2006) Proteolytically processed soluble tumor endothelial marker (TEM) 5 mediates endothelial cell survival during angiogenesis by linking integrin αvβ3 to glycosaminoglycans. J. Biol. Chem. 281, 34179-34188 (Pubitemid 46036626)
17. Cullen, M., Elzarrad, M. K., Seaman, S., Zudaire, E., Stevens, J., Yang, M. Y., Li, X., Chaudhary, A., Xu, L., Hilton, M. B. et al. (2011) GPR124, an orphan G protein-coupled receptor, is required for CNS-specific vascularization and establishment of the blood-brain barrier. Proc. Natl. Acad. Sci. U.S.A. 108, 5759-5764
18. Anderson, K. D., Pan, L., Yang, X. M., Hughes, V. C., Walls, J. R., Dominguez, M. G., Simmons, M. V., Burfeind, P., Xue, Y., Wei, Y. et al. (2011) Angiogenic sprouting into neural tissue requires Gpr124, an orphan G protein-coupled receptor. Proc. Natl. Acad. Sci. U.S.A. 108, 2807-2812
19. Hatahet, F. and Ruddock, L. W. (2009) Protein disulfide isomerase: a critical evaluation of its function in disulfide bond formation. Antioxid. Redox Signaling 11, 2807-2850
20. Varandani, P. T., Raveed, D. and Nafz, M. A. (1978) Insulin degradation. XXIII. Distribution of glutathione-insulin transhydrogenase in isolated rat hepatocytes as studied by immuno-ferritin and electron microscopy. Biochim. Biophys. Acta 538, 343-353 (Pubitemid 8236708)
21. Yoshimori, T., Semba, T., Takemoto, H., Akagi, S., Yamamoto, A. and Tashiro, Y. (1990) Protein disulfide-isomerase in rat exocrine pancreatic cells is exported from the endoplasmic reticulum despite possessing the retention signal. J. Biol. Chem. 265, 15984-15990
22. Mandel, R., Ryser, H. J., Ghani, F., Wu, M. and Peak, D. (1993) Inhibition of a reductive function of the plasma membrane by bacitracin and antibodies against protein disulfide-isomerase. Proc. Natl. Acad. Sci. U.S.A. 90, 4112-4116 (Pubitemid 23134176)
23. Ryser, H. J., Levy, E. M., Mandel, R. and DiSciullo, G. J. (1994) Inhibition of human immunodeficiency virus infection by agents that interfere with thiol-disulfide interchange upon virus-receptor interaction. Proc. Natl. Acad. Sci. U.S.A. 91, 4559-4563
24. Couët, J., de Bernard, S., Loosfelt, H., Saunier, B., Milgrom, E. and Misrahi, M. (1996) Cell surface protein disulfide-isomerase is involved in the shedding of human thyrotropin receptor ectodomain. Biochemistry 35, 14800-14805
25. Hotchkiss, K. A., Matthias, L. J. and Hogg, P. J. (1998) Exposure of the cryptic Arg-Gly-Asp sequence in thrombospondin-1 by protein disulfide isomerase. Biochim. Biophys. Acta 1388, 478-488 (Pubitemid 28526609)
26. Graham, F. L. and van der Eb, A. J. (1973) A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 52, 456-467
27. Segura, I., González, M. A., Serrano, A., Abad, J. L., Bernad, A. and Riese, H. H. (2001) High transfection efficiency of human umbilical vein endothelial cells using an optimized calcium phosphate method. Anal. Biochem. 296, 143-147 (Pubitemid 32808407)
28. O'Mullan, P., Craft, D., Yi, J. and Gelfand, C. A. (2009) Thrombin induces broad spectrum proteolysis in human serum samples. Clin. Chem. Lab. Med. 47, 685-693
29. Shaw, G., Morse, S., Ararat, M. and Graham, F. L. (2002) Preferential transformation of human neuronal cells by human adenoviruses and the origin of HEK 293 cells. FASEB J. 16, 869-871
30. O'Brien, P. J., Prevost, N., Molino, M., Hollinger, M. K., Woolkalis, M. J., Woulfe, D. S. and Brass, L. F. (2000) Thrombin responses in human endothelial cells. Contributions from receptors other than PAR1 include the transactivation of PAR2 by thrombin-cleaved PAR1. J. Biol. Chem. 275, 13502-13509 (Pubitemid 30257415)
31. Koo, B. H., Park, M. Y., Jeon, O. H. and Kim, D. S. (2009) Regulatory mechanism of matrix metalloprotease-2 enzymatic activity by factor Xa and thrombin. J. Biol. Chem. 284, 23375-23385
32. Grace, C. R., Perrin, M. H., DiGruccio, M. R., Miller, C. L., Rivier, J. E., Vale, W. W. and Riek, R. (2004) NMR structure and peptide hormone binding site of the first extracellular domain of a type B1 G protein-coupled receptor. Proc. Natl. Acad. Sci. U.S.A. 101, 12836-12841 (Pubitemid 39167545)
33. Bush-Pelc, L. A., Marino, F., Chen, Z., Pineda, A. O., Mathews, F. S. and Di Cera, E. (2007) Important role of the Cys-191 Cys-220 disulfide bond in thrombin function and allostery. J. Biol. Chem. 282, 27165-27170 (Pubitemid 47501918)
34. Wang, T., Ward, Y., Tian, L., Lake, R., Guedez, L., Stetler-Stevenson, W. G. and Kelly, K. (2005) CD97, an adhesion receptor on inflammatory cells, stimulates angiogenesis through binding integrin counterreceptors on endothelial cells. Blood 105, 2836-2844 (Pubitemid 40446277)
35. Jasuja, R., Furie, B. and Furie, B. C. (2010) Endothelium-derived but not platelet-derived protein disulfide isomerase is required for thrombus formation in vivo. Blood 116, 4665-4674