Activity-regulating structural changes and autoantibody epitopes in transglutaminase 2 assessed by hydrogen/deuterium exchange

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 48, 2014, Pages 17146-17151

  Iversena, Rasmus ^a   Myslingb, Simon ^b   Hnidaa, Kathrin ^a   Jørgensenb, Thomas J D ^b   Sollida, Ludvig M ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Autoantibodies; Celiac disease; Hydrogen deuterium exchange; Transglutaminase 2

Indexed keywords

EID: 84914145407     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1407457111     Document Type: Article

References (47)

1. Sollid LM (2002) Coeliac disease: Dissecting a complex inflammatory disorder. Nat Rev Immunol 2(9):647-655.
2. Dieterich W, et al. (1997) Identification of tissue transglutaminase as the autoantigen of celiac disease. Nat Med 3(7):797-801.
3. Lorand L, Graham RM (2003) Transglutaminases: Crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol 4(2):140-156.
4. Molberg O, et al. (1998) Tissue transglutaminase selectively modifies gliadin peptides that are recognized by gut-derived T cells in celiac disease. Nat Med 4(6):713-717.
5. Zemskov EA, Mikhailenko I, Hsia RC, Zaritskaya L, Belkin AM (2011) Unconventional secretion of tissue transglutaminase involves phospholipid-dependent delivery into recycling endosomes. PLoS ONE 6(4):e19414.
6. Aeschlimann D, Thomazy V (2000) Protein crosslinking in assembly and remodelling of extracellular matrices: The role of transglutaminases. Connect Tissue Res 41(1):1-27.
7. Hoffmann BR, Annis DS, Mosher DF (2011) Reactivity of the N-terminal region of fibronectin protein to transglutaminase 2 and factor XIIIA. J Biol Chem 286(37): 32220-32230.
8. Nakaoka H, et al. (1994) Gh: A GTP-binding protein with transglutaminase activity and receptor signaling function. Science 264(5165):1593-1596.
9. Achyuthan KE, Greenberg CS (1987) Identification of a guanosine triphosphatebinding site on guinea pig liver transglutaminase. Role of GTP and calcium ions in modulating activity. J Biol Chem 262(4):1901-1906.
10. Bergamini CM (1988) GTP modulates calcium binding and cation-induced conformational changes in erythrocyte transglutaminase. FEBS Lett 239(2):255-258.
11. Smethurst PA, Griffin M (1996) Measurement of tissue transglutaminase activity in a permeabilized cell system: Its regulation by Ca2+ and nucleotides. Biochem J 313(Pt 3):803-808.
12. Murthy SN, Lomasney JW, Mak EC, Lorand L (1999) Interactions of G(h)/transglutaminase with phospholipase Cdelta1 and with GTP. Proc Natl Acad Sci USA 96(21): 11815-11819.
13. Di Venere A, et al. (2000) Opposite effects of Ca(2+) and GTP binding on tissue transglutaminase tertiary structure. J Biol Chem 275(6):3915-3921.
14. Liu S, Cerione RA, Clardy J (2002) Structural basis for the guanine nucleotide-binding activity of tissue transglutaminase and its regulation of transamidation activity. Proc Natl Acad Sci USA 99(5):2743-2747.
15. Jang TH, et al. (2014) Crystal structure of transglutaminase 2 with GTP complex and amino acid sequence evidence of evolution of GTP binding site. PLoS ONE 9(9): e107005.
16. Pinkas DM, Strop P, Brunger AT, Khosla C (2007) Transglutaminase 2 undergoes a large conformational change upon activation. PLoS Biol 5(12):e327.
17. Stamnaes J, Pinkas DM, Fleckenstein B, Khosla C, Sollid LM (2010) Redox regulation of transglutaminase 2 activity. J Biol Chem 285(33):25402-25409.
18. Jin X, et al. (2011) Activation of extracellular transglutaminase 2 by thioredoxin. J Biol Chem 286(43):37866-37873.
19. Király R, et al. (2009) Functional significance of five noncanonical Ca2+-binding sites of human transglutaminase 2 characterized by site-directed mutagenesis. FEBS J 276(23):7083-7096.
20. Wales TE, Engen JR (2006) Hydrogen exchange mass spectrometry for the analysis of protein dynamics. Mass Spectrom Rev 25(1):158-170.
21. Skinner JJ, Lim WK, Bédard S, Black BE, Englander SW (2012) Protein dynamics viewed by hydrogen exchange. Protein Sci 21(7):996-1005.
22. Malito E, et al. (2013) Defining a protective epitope on factor H binding protein, a key meningococcal virulence factor and vaccine antigen. Proc Natl Acad Sci USA 110(9): 3304-3309.
23. Di Niro R, et al. (2012) High abundance of plasma cells secreting transglutaminase 2-specific IgA autoantibodies with limited somatic hypermutation in celiac disease intestinal lesions. Nat Med 18(3):441-445.
24. Murthy SN, et al. (2002) Conserved tryptophan in the core domain of transglutaminase is essential for catalytic activity. Proc Natl Acad Sci USA 99(5):2738-2742.
25. Ahvazi B, Kim HC, Kee SH, Nemes Z, Steinert PM (2002) Three-dimensional structure of the human transglutaminase 3 enzyme: Binding of calcium ions changes structure for activation. EMBO J 21(9):2055-2067.
26. Stieler M, et al. (2013) Structure of active coagulation factor XIII triggered by calcium binding: Basis for the design of next-generation anticoagulants. Angew Chem Int Ed Engl 52(45):11930-11934.
27. Connellan JM, Folk JE (1969) Mechanism of the inactivation of guinea pig liver transglutaminase by 5,5 ? - dithiobis-(2-nitrobenzoic acid). J Biol Chem 244(12): 3173-3181.
28. Lorand L, Conrad SM (1984) Transglutaminases. Mol Cell Biochem 58(1-2):9-35.
29. Siegel M, et al. (2008) Extracellular transglutaminase 2 is catalytically inactive, but is transiently activated upon tissue injury. PLoS One 3(3):e1861.
30. Iversen R, et al. (2013) Transglutaminase 2-specific autoantibodies in celiac disease target clustered, N-terminal epitopes not displayed on the surface of cells. J Immunol 190(12):5981-5991.
31. Simon-Vecsei Z, et al. (2012) A single conformational transglutaminase 2 epitope contributed by three domains is critical for celiac antibody binding and effects. Proc Natl Acad Sci USA 109(2):431-436.
32. Jeong JM, Murthy SN, Radek JT, Lorand L (1995) The fibronectin-binding domain of transglutaminase. J Biol Chem 270(10):5654-5658.
33. Hang J, Zemskov EA, Lorand L, Belkin AM (2005) Identification of a novel recognition sequence for fibronectin within the NH2-terminal beta-sandwich domain of tissue transglutaminase. J Biol Chem 280(25):23675-23683.
34. Wang Z, et al. (2012) Characterization of heparin-binding site of tissue transglutaminase: Its importance in cell surface targeting, matrix deposition, and cell signaling. J Biol Chem 287(16):13063-13083.
35. Han BG, et al. (2010) Crystal structure of human transglutaminase 2 in complex with adenosine triphosphate. Int J Biol Macromol 47(2):190-195.
36. Halttunen T, Mäki M (1999) Serum immunoglobulin A from patients with celiac disease inhibits human T84 intestinal crypt epithelial cell differentiation. Gastroenterology 116(3):566-572.
37. Barone MV, et al. (2007) Humoral immune response to tissue transglutaminase is related to epithelial cell proliferation in celiac disease. Gastroenterology 132(4): 1245-1253.
38. Cervio E, et al. (2007) Sera of patients with celiac disease and neurologic disorders evoke a mitochondrial-dependent apoptosis in vitro. Gastroenterology 133(1):195-206.
39. Myrsky E, et al. (2008) Coeliac disease-specific autoantibodies targeted against transglutaminase 2 disturb angiogenesis. Clin Exp Immunol 152(1):111-119.
40. Myrsky E, et al. (2009) Celiac disease IgA modulates vascular permeability in vitro through the activity of transglutaminase 2 and RhoA. Cell Mol Life Sci 66(20): 3375-3385.
41. Di Simone N, et al. (2010) Anti-tissue transglutaminase antibodies from celiac patients are responsible for trophoblast damage via apoptosis in vitro. Am J Gastroenterol 105(10):2254-2261.
42. Turner PM, Lorand L (1989) Complexation of fibronectin with tissue transglutaminase. Biochemistry 28(2):628-635.
43. Akimov SS, Krylov D, Fleischman LF, Belkin AM (2000) Tissue transglutaminase is an integrin-binding adhesion coreceptor for fibronectin. J Cell Biol 148(4):825-838.
44. Xu L, Begum S, Hearn JD, Hynes RO (2006) GPR56, an atypical G protein-coupled receptor, binds tissue transglutaminase, TG2, and inhibits melanoma tumor growth and metastasis. Proc Natl Acad Sci USA 103(24):9023-9028.
45. Scarpellini A, et al. (2009) Heparan sulfate proteoglycans are receptors for the cellsurface trafficking and biological activity of transglutaminase-2. J Biol Chem 284(27): 18411-18423.
46. Marzari R, et al. (2001) Molecular dissection of the tissue transglutaminase autoantibody response in celiac disease. J Immunol 166(6):4170-4176.
47. Smith K, et al. (2009) Rapid generation of fully human monoclonal antibodies specific to a vaccinating antigen. Nat Protoc 4(3):372-384.