Characterization of heparin-binding site of tissue transglutaminase: Its importance in cell surface targeting, matrix deposition, and cell signaling

Journal of Biological Chemistry

Volumn 287, Issue 16, 2012, Pages 13063-13083

  Wang, Zhuo ^a   Collighan, Russell J ^a   Pytel, Kamila ^a   Rathbone, Daniel L ^a   Li, Xiaoling ^a   Griffin, Martin ^a  

^a ASTON UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN CYTOSKELETON; ACTIVATED PROTEINS; CELIAC DISEASE; CELL SIGNALING; CELL SURFACES; EXTRACELLULAR; EXTRACELLULAR COMPARTMENTS; EXTRACELLULAR MATRICES; FOCAL ADHESIONS; HEPARAN SULFATES; HEPARIN-BINDING SITE; INTEGRINS; MATRIX DEPOSITION; METASTATIC CANCERS; PATHOLOGICAL FUNCTIONS; REGULATORY MECHANISM; TISSUE TRANSGLUTAMINASE; WOUND HEALING;

CELL ADHESION; CELL MEMBRANES; ENZYME INHIBITION; PEPTIDES;

TISSUE;

ARGINYLGLYCYLASPARTYLSERINE; FIBRONECTIN; HEPARAN SULFATE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PROTEIN KINASE C ALPHA; SYNDECAN 4;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; BINDING SITE; CELL ADHESION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FOCAL ADHESION; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REGULATORY MECHANISM;

ANIMALS; ANTIGENS, SURFACE; CATALYTIC DOMAIN; CELL ADHESION; CHO CELLS; CRICETINAE; EXTRACELLULAR MATRIX; HEK293 CELLS; HEPARIN; HEPARITIN SULFATE; HUMANS; MICE; MODELS, MOLECULAR; MUTAGENESIS; NIH 3T3 CELLS; OLIGOPEPTIDES; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SYNDECAN-4; TRANSGLUTAMINASES;

EID: 84859644032     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.294819     Document Type: Article

References (44)

1. Iismaa, S. E., Mearns, B. M., Lorand, L., and Graham, R. M. (2009) Transglutaminases and disease. Lessons from genetically engineered mouse models and inherited disorders. Physiol. Rev. 89, 991-1023
2. Griffin, M., Casadio, R., and Bergamini, C. M. (2002) Transglutaminases. Nature's biological glues. Biochem. J. 368, 377-396
3. Zemskov, E. A., Mikhailenko, I., Hsia, R. C., Zaritskaya, L., and Belkin, A. M. (2011) Unconventional secretion of tissue transglutaminase involves phospholipid-dependent delivery into recycling endosomes. PLoS One 6, e19414
4. Gaudry, C. A., Verderio, E., Aeschlimann, D., Cox, A., Smith, C., and Griffin, M. (1999) Cell surface localization of tissue transglutaminase is dependent on a fibronectin-binding site in its N-terminal β-sandwich domain. J. Biol. Chem. 274, 30707-30714
5. Wang, Z., Telci, D., and Griffin, M. (2011) Importance of syndecan-4 and syndecan-2 in osteoblast cell adhesion and survival mediated by a tissue transglutaminase-fibronectin complex. Exp. Cell Res. 317, 367-381
6. Wang, Z., Collighan, R. J., Gross, S. R., Danen, E. H., Orend, G., Telci, D., and Griffin, M. (2010) RGD-independent cell adhesion via a tissue transglutaminase-fibronectin matrix promotes fibronectin fibril deposition and requires syndecan-4/2 and α5β1 integrin co-signaling. J. Biol. Chem. 285, 40212-40229
7. Wang, Z., and Griffin, M. (2011) TG2, a novel extracellular protein with multiple functions. Review article. Amino Acids 42, 939-949
8. Mahtouk, K., Hose, D., Raynaud, P., Hundemer, M., Jourdan, M., Jourdan, E., Pantesco, V., Baudard, M., De Vos, J., Larroque, M., Moehler, T., Rossi, J. F., Rème, T., Goldschmidt, H., and Klein, B. (2007) Heparanase influences expression and shedding of syndecan-1, and its expression by the bone marrow environment is a bad prognostic factor in multiple myeloma. Blood 109, 4914-4923 (Pubitemid 46827789)
9. Manon-Jensen, T., Itoh, Y., and Couchman, J. R. (2010) Proteoglycans in health and disease: the multiple roles of syndecan shedding. Review article. FEBS J. 277, 3786-3889
10. Tsanou, E., Ioachim, E., Briasoulis, E., Charchanti, A., Damala, K., Karavasilis, V., Pavlidis, N., and Agnantis, N. J. (2004) Clinicopathological study of the expression of syndecan-1 in invasive breast carcinomas. Correlation with extracellular matrix components. J. Exp. Clin. Cancer Res. 23, 641-650
11. Fuster, M. M., and Wang, L. (2010) Endothelial heparan sulfate in angiogenesis. Prog. Mol. Biol. Transl. Sci. 93, 179-212
12. Brule, S., Charnaux, N., Sutton, A., Ledoux, D., Chaigneau, T., Saffar, L., and Gattegno, L. (2006) The shedding of syndecan-4 and syndecan-1 from HeLa cells and human primary macrophages is accelerated by SDF-1/CXCL12 and mediated by the matrix metalloproteinase-9. Glycobiology 16, 488-501 (Pubitemid 43779045)
13. Verderio, E., Nicholas, B., Gross, S., and Griffin, M. (1998) Regulated expression of tissue transglutaminase in Swiss 3T3 fibroblasts. Effects on the processing of fibronectin, cell attachment, and cell death. Exp. Cell Res. 239, 119-138 (Pubitemid 28368484)
14. Leblanc, A., Day, N., Ménard, A., and Keillor, J. W. (1999) Guinea pig liver transglutaminase. A modified purification procedure affording enzyme with superior activity in greater yield. Protein Expr. Purif. 17, 89-95 (Pubitemid 29504382)
15. Parsons, M., Keppler, M. D., Kline, A., Messent, A., Humphries, M. J., Gilchrist, R., Hart, I. R., Quittau-Prevostel, C., Hughes, W. E., Parker, P. J., and Ng, T. (2002) Site-directed perturbation of protein kinase C-integrin interaction blocks carcinoma cell chemotaxis. Mol. Cell. Biol. 22, 5897-5911 (Pubitemid 34815838)
16. Gentile, V., Saydak, M., Chiocca, E. A., Akande, O., Birckbichler, P. J., Lee, K. N., Stein, J. P., and Davies, P. J. (1991) Isolation and characterization of cDNA clones to mouse macrophage and human endothelial cell tissue transglutaminases. J. Biol. Chem. 266, 478-483 (Pubitemid 21906147)
17. Lee, K. N., Arnold, S. A., Birckbichler, P. J., Patterson, M. K., Jr., Fraij, B. M., Takeuchi, Y., and Carter, H. A. (1993) Site-directed mutagenesis of human tissue transglutaminase. Cys-277 is essential for transglutaminase activity but not for GTPase activity. Biochim. Biophys. Acta 1202, 1-6 (Pubitemid 23269739)
18. Akimov, S. S., Krylov, D., Fleischman, L. F., and Belkin, A. M. (2000) Tissue transglutaminase is an integrin-binding adhesion coreceptor for fibronectin. J. Cell Biol. 148, 825-838
19. Telci, D., Wang, Z., Li, X., Verderio, E. A., Humphries, M. J., Baccarini, M., Basaga, H., and Griffin, M. (2008) Fibronectin-tissue transglutaminase matrix rescues RGD-impaired cell adhesion through syndecan-4 and β1 integrin co-signaling. J. Biol. Chem. 283, 20937-20947
20. Griffin, M., Mongeot, A., Collighan, R., Saint, R. E., Jones, R. A., Coutts, I. G., and Rathbone, D. L. (2008) Synthesis of potent water-soluble tissue transglutaminase inhibitors. Bioorg. Med. Chem. Lett. 18, 5559-5562
21. Jones, R. A., Nicholas, B., Mian, S., Davies, P. J., and Griffin, M. (1997) Reduced expression of tissue transglutaminase in a human endothelial cell line leads to changes in cell spreading, cell adhesion, and reduced polymerization of fibronectin. J. Cell Sci. 110, 2461-2472 (Pubitemid 127699160)
22. Nicholas, B., Smethurst, P., Verderio, E., Jones, R., and Griffin, M. (2003) Cross-linking of cellular proteins by tissue transglutaminase during necrotic cell death. A mechanism for maintaining tissue integrity. Biochem. J. 371, 413-422 (Pubitemid 36547624)
23. Cardin, A. D., and Weintraub, H. J. (1989) Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis 9, 21-32 (Pubitemid 19046087)
24. Verderio, E. A., Scarpellini, A., and Johnson, T. S. (2009) Novel interactions of TG2 with heparan sulfate proteoglycans. Reflection on physiological implications. Amino Acids 36, 671-677
25. Margalit, H., Fischer, N., and Ben-Sasson, S. A. (1993) Comparative analysis of structurally defined heparin-binding sequences reveals a distinct spatial distribution of basic residues. J. Biol. Chem. 268, 19228-19231 (Pubitemid 23270692)
26. Hileman, R. E., Fromm, J. R., Weiler, J. M., and Linhardt, R. J. (1998) Glycosaminoglycan-protein interactions. Definition of consensus sites in glycosaminoglycan-binding proteins. BioEssays 20, 156-167
27. Verderio, E. A., Telci, D., Okoye, A., Melino, G., and Griffin, M. (2003) A novel RGD-independent cel adhesion pathway mediated by fibronectin-bound tissue transglutaminase rescues cells from anoikis. J. Biol. Chem. 278, 42604-42614 (Pubitemid 37310534)
28. 2-terminal β-sandwich domain of tissue transglutaminase. J. Biol. Chem. 280, 23675-23683
29. Scarpellini, A., Germack, R., Lortat-Jacob, H., Muramatsu, T., Billett, E., Johnson, T., and Verderio, E. A. (2009) Heparan sulfate proteoglycans are receptors for the cell-surface trafficking and biological activity of transglutaminase-2. J. Biol. Chem. 284, 18411-18423
30. Salo, T., Mäkelä, M., Kylmäniemi, M., Autio-Harmainen, H., and Larjava, H. (1994) Expression of matrix metalloproteinase-2 and -9 during early human wound healing. Lab. Invest. 70, 176-182 (Pubitemid 24090099)
31. Fitzgerald, M. L., Wang, Z., Park, P. W., Murphy, G., and Bernfield, M. (2000) Shedding of syndecan-1 and -4 ectodomains is regulated by multiple signaling pathways and mediated by a TIMP-3-sensitive metalloproteinase. J. Cell Biol. 148, 811-824
32. Ritchie, J. P., Ramani, V. C., Ren, Y., Naggi, A., Torri, G., Casu, B., Penco, S., Pisano, C., Carminati, P., Tortoreto, M., Zunino, F., Vlodavsky, I., Sanderson, R. D., and Yang, Y. (2011) SST0001, a chemically modified heparin, inhibits myeloma growth and angiogenesis via disruption of the heparanase/syndecan-1 axis. Clin. Cancer Res. 17, 1382-1393
33. Pinkas, D. M., Strop, P., Brunger, A. T., and Khosla, C. (2007) Transglutaminase 2 undergoes a large conformational change upon activation. PLoS Biol. 5, e327
34. Liu, S., Cerione, R. A., and Clardy, J. (2002) Structural basis for the guanine nucleotide-binding activity of tissue transglutaminase and its regulation of transamidation activity. Proc. Natl. Acad. Sci. U.S.A. 99, 2743-2747 (Pubitemid 34240531)
35. Chou, C. Y., Streets, A. J., Watson, P. F., Huang, L., Verderio, E. A., and Johnson, T. S. (2011) A crucial sequence for transglutaminase type 2 extracellular trafficking in renal tubular epithelial cells lies in its N-terminal β-sandwich domain. J. Biol. Chem. 286, 27825-27835
36. Lidholt, K., Weinke, J. L., Kiser, C. S., Lugemwa, F. N., Bame, K. J., Cheifetz, S., Massagué, J., Lindahl, U., and Esko, J. D. (1992) A single mutation affects both N-acetylglucosaminyltransferase and glucuronosyltransferase activities in a Chinese hamster ovary cell mutant defective in heparan sulfate biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 89, 2267-2271
37. Alexopoulou, A. N., Multhaupt, H. A., and Couchman, J. R. (2007) Syndecans in wound healing, inflammation, and vascular biology. Int. J. Biochem. Cell Biol. 39, 505-528 (Pubitemid 46099032)
38. Okina, E., Manon-Jensen, T., Whiteford, J. R., and Couchman, J. R. (2009) Syndecan proteoglycan contributions to cytoskeletal organization and contractility. Scand. J. Med. Sci. Sports 19, 479-489
39. Su, G., Blaine, S. A., Qiao, D., and Friedl, A. (2008) Membrane type 1 matrix metalloproteinase-mediated stromal syndecan-1 shedding stimulates breast carcinoma cell proliferation. Cancer Res. 68, 9558-9565
40. Verderio, E. A., Johnson, T., and Griffin, M. (2004) Tissue transglutaminase in normal and abnormal wound healing. Review article. Amino Acids 26, 387-404 (Pubitemid 39093142)
41. Johnson, K. A., and Terkeltaub, R. A. (2005) External GTP-bound transglutaminase 2 is a molecular switch for chondrocyte hypertrophic differentiation and calcification. J. Biol. Chem. 280, 15004-15012 (Pubitemid 40562853)
42. LeMosy, E. K., Erickson, H. P., Beyer, W. F., Jr., Radek, J. T., Jeong, J. M., Murthy, S. N., and Lorand, L. (1992) Visualization of purified fibronectin-transglutaminase complexes. J. Biol. Chem. 267, 7880-7885
43. Stamnaes, J., Pinkas, D. M., Fleckenstein, B., Khosla, C., and Sollid, L. M. (2010) Redox regulation of transglutaminase 2 activity. J. Biol. Chem. 285, 25402-25409
44. Telci, D., Collighan, R. J., Basaga, H., and Griffin, M. (2009) Increased TG2 expression can result in induction of transforming growth factorß1, causing increased synthesis and deposition of matrix proteins, which can be regulated by nitric oxide. J. Biol. Chem. 284, 29547-29558