Structural characterization of both the non-proteolytic and proteolytic activation pathways of coagulation Factor XIII studied by hydrogen-deuterium exchange mass spectrometry

International Journal of Mass Spectrometry

Volumn 302, Issue 1-3, 2011, Pages 139-148

  Andersen, Mette Dahl ^a   Faber, Johan Henrik ^a  

^a NOVO NORDISK A S   (Denmark)

Author keywords

Enzyme activation; Factor XIII; Hydrogen deuterium exchange; rFXIII; Structure activity relationship; Transglutaminases

Indexed keywords

EID: 79954633117     PISSN: 13873806     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijms.2010.09.010     Document Type: Article

References (50)

1. L. Muszbek, R.A. Ariens, and A. Ichinose Factor XIII: recommended terms and abbreviations J. Thromb. Haemost. 5 2007 181 183 (Pubitemid 44921084)
2. G.M. Asijee, L. Muszbek, J. Kappelmayer, J. Polgár, A. Horváth, and A. Sturk Platelet vinculin: a substrate of activated factor XIII Biochim. Biophys. Acta 954 1988 303 308
3. K. Serrano, and D.V. Devine Intracellular factor XIII crosslinks platelet cytoskeletal elements upon platelet activation Thromb. Haemost. 88 2002 315 320 (Pubitemid 34873715)
4. A. Jayo, I. Conde, P. Lastres, V. Jiménez-Yuste, and C. González-Manchón New insights into the expression and role of platelet factor XIII-A J. Thromb. Haemost. 7 2009 1184 1191
5. R.A. Ariëns, T.S. Lai, J.W. Weisel, C.S. Greenberg, and P.J. Grant Role of factor XIII in fibrin clot formation and effects of genetic polymorphisms Blood 100 2002 743 754 (Pubitemid 34832596)
6. L. Lorand Factor XIII: structure, activation, and interactions with fibrinogen and fibrin, Ann N. Y. Acad. Sci. 936 2001 291 311 (Pubitemid 32613915)
7. L. Muszbek, V.C. Yee, and Z. Hevessy Blood coagulation factor XIII: structure and function Thromb. Res. 94 1999 271 305 (Pubitemid 29268348)
8. M. Karimi, Z. Bereczky, N. Cohan, and L. Muszbek Factor XIII deficiency Semin. Thromb. Hemost. 35 2009 426 438
9. A. Ichinose Extracellular transglutaminase: factor XIII Transglutaminases: Family Enzymes Diverse Funct. 38 2005 192 208
10. B.A. Fox, V.C. Yee, L.C. Pedersen, I.L. Trong, P.D. Bishop, R.E. Stenkamp, and D.C. Teller Identification of the calcium binding site and a novel ytterbium site in blood coagulation factor XIII by X-ray crystallography J. Biol. Chem. 274 1999 4917 4923
11. M.S. Weiss, H.J. Metzner, and R. Hilgenfeld Two non-proline cis peptide bonds may be important for factor XIII function FEBS Lett. 423 1998 291 296 (Pubitemid 28129352)
12. V.C. Yee, L.C. Pedersen, I. Le-Trong, P.D. Bishop, R.E. Stenkamp, and D.C. Teller Three-dimensional structure of a transglutaminase: human blood coagulation factor XIII Proc. Natl. Acad. Sci. U. S. A. 91 1994 7296 7300 (Pubitemid 24226850)
13. R.B. Credo, C.G. Curtis, and L. Lorand Ca2+-related regulatory function of fibrinogen Proc. Natl. Acad. Sci. U. S. A. 75 1978 4234 4237
14. C.G. Curtis, K.L. Brown, R.B. Credo, R.A. Domanik, A. Gray, P. Stenberg, and L. Lorand Calcium-dependent unmasking of active center cysteine during activation of fibrin stabilizing factor Biochemistry 13 1974 3774 3780
15. V.C. Yee, L.C. Pedersen, P.D. Bishop, R.E. Stenkamp, and D.C. Teller Structural evidence that the activation peptide is not released upon thrombin cleavage of factor XIII Thromb. Res. 78 1995 389 397
16. T.J. Hornyak, and J.A. Shafer Interactions of factor XIII with fibrin as substrate and cofactor Biochemistry 31 1992 423 429
17. T.J. Janus, S.D. Lewis, L. Lorand, and J.A. Shafer Promotion of thrombin-catalyzed activation of factor XIII by fibrinogen Biochemistry 22 1983 6269 6272 (Pubitemid 14175823)
18. C.S. Greenberg, K.E. Achyuthan, and J.W.d. Fenton Factor XIIIa formation promoted by complexing of alpha-thrombin, fibrin, and plasma factor XIII Blood 69 1987 867 871 (Pubitemid 17057470)
19. L Lorand, R.B. Credo, and T.J. Janus Factor XIII (fibrin-stabilizing factor) Methods Enzymol. 80 1981 333 341
20. J. Polgár, V. Hidasi, and L. Muszbek Non-proteolytic activation of cellular protransglutaminase (placenta macrophage factor XIII) Biochem. J. 267 1990 557 560 (Pubitemid 20136098)
21. L. Muszbek, G. Haramura, and J. Polgar Transformation of cellular factor-XIII into an active zymogen transglutaminase in thrombin-stimulated platelets Thromb. Haemost. 73 1995 702 705
22. L. Muszbek, J. Polgar, and Z. Boda Platelet factor-XIII becomes active without the release of activation peptide during platelet activation Thromb. Haemost. 69 1993 282 285 (Pubitemid 23069009)
23. S. Liu, R.A. Cerione, and J. Clardy 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 2002 2743 2747 (Pubitemid 34240531)
24. L. Lorand, and R.M. Graham Transglutaminases: crosslinking enzymes with pleiotropic functions Nat. Rev. Mol. Cell Biol. 4 2003 140 156 (Pubitemid 36172696)
25. G.E. Begg, L. Carrington, P.H. Stokes, J.M. Matthews, M.A. Wouters, A. Husain, L. Lorand, S.E. Iismaa, and R.M. Graham Mechanism of allosteric regulation of transglutaminase 2 by GTP Proc. Natl. Acad. Sci. U. S. A. 103 2006 19683 19688 (Pubitemid 46037492)
26. D.M. Pinkas, P. Strop, A.T. Brunger, and C. Khosla Transglutaminase 2 undergoes a large conformational change upon activation PLoS Biol. 5 2007 e327
27. A. Hvidt, and K. Linderstrøm-Lang Exchange of hydrogen atoms in insulin with deuterium atoms in aqueous solutions Biochim. Biophys. Acta 14 1954 574 575
28. Z. Zhang, and D.L. Smith Determination of amide hydrogen exchange by mass spectrometry: a new tool for protein structure elucidation Protein Sci. 2 1993 522 531 (Pubitemid 23119303)
29. A. Hvidt, and S.O. Nielsen Hydrogen exchange in proteins Adv. Protein Chem. 1966 Academic Press 287 386
30. K.D. Rand, T.J.D. Jørgensen, O.H. Olsen, E. Persson, O.N. Jensen, H.R. Stennicke, and M.D. Andersen Allosteric activation of coagulation factor VIIa visualized by hydrogen exchange J. Biol. Chem. 281 2006 23018 23024
31. T.E. Wales, and J.R. Engen Hydrogen exchange mass spectrometry for the analysis of protein dynamics Mass Spectrom. Rev. 25 2006 158 170
32. J.J. Englander, C. Del Mar, W. Li, S.W. Englander, J.S. Kim, D.D. Stranz, Y. Hamuro, and V.L. Woods Protein structure change studied by hydrogen-deuterium exchange, functional labeling, and mass spectrometry Proc. Natl. Acad. Sci. U. S. A. 100 2003 7057 7062 (Pubitemid 36706392)
33. C.H. Croy, J.R. Koeppe, S. Bergqvist, and E.A. Komives Allosteric changes in solvent accessibility observed in thrombin upon active site occupation Biochemistry 43 2004 5246 5255 (Pubitemid 38620916)
34. K.L. Hailey, S. Li, M.D. Andersen, M. Roy, V.L. Woods, and P.A. Jennings Pro-interleukin (IL)-1β shares a core region of stability as compared with mature IL-1β while maintaining a distinctly different configurational landscape J. Biol. Chem. 284 2009 26137 26148
35. A.N. Hoofnagle, K.A. Resing, and N.G. Ahn Protein analysis by hydrogen exchange mass spectrometry Annu. Rev. Biophys. Biomol. Struct. 32 2003 1 25 (Pubitemid 37056219)
36. S.W. Englander, and M.M.G. Krishna Hydrogen exchange Nat. Struct. Mol. Biol. 8 2001 741 742 (Pubitemid 32803586)
37. P.D. Bishop, D.C. Teller, R.A. Smith, G.W. Lasser, T. Gilbert, and R.L. Seale Expression, purification, and characterization of human factor XIII in Saccharomyces cerevisiae Biochemistry 29 1990 1861 1869 (Pubitemid 20074732)
38. K Oertel, A. Hunfeld, E. Specker, C. Reiff, R. Seitz, R. Pasternack, and J. Dodt A highly sensitive fluorometric assay for determination of human coagulation factor XIII in plasma Anal. Biochem. 367 2007 152 158 (Pubitemid 47001930)
39. L. Lorand, T. Urayama, J.W.C. de Kiewiet, and H.L. Nossel Diagnostic and genetic studies on fibrin-stabilizing factor with a new assay based on amine incorporation J. Clin. Invest. 48 1969 1054 1064
40. N. Takahashi, Y. Takahashi, and F.W. Putnam Primary structure of blood coagulation factor XIIIa (fibrinoligase, transglutaminase) from human placenta Proc. Natl. Acad. Sci. U. S. A. 83 1986 8019 8023 (Pubitemid 17182435)
41. D.D. Weis, J.R. Engen, and I.J. Kass Semi-automated data processing of hydrogen exchange mass spectra using HX-express J. Am. Soc. Mass Spectrom. 17 2006 1700 1703 (Pubitemid 44809951)
42. D. Houde, J. Arndt, W. Domeier, S. Berkowitz, and J.R. Engen Characterization of IgG1 conformation and conformational dynamics by hydrogen/deuterium exchange mass spectrometry Anal. Chem. 81 2009 5966
43. T.E. Wales, K.E. Fadgen, G.C. Gerhardt, and J.R. Engen High-speed and high-resolution UPLC separation at zero degrees celsius Anal. Chem. 80 2008 6815 6820
44. T.J. Hornyak, and J.A. Shafer Role of calcium ion in the generation of factor XIII activity Biochemistry 30 1991 6175 6182
45. R.A. Garcia, D. Pantazatos, and F.J. Villarreal Hydrogen/deuterium exchange mass spectrometry for investigating protein-ligand interactions ASSAY Drug Dev. Technol. 2 2004 81 91 (Pubitemid 38647419)
46. J.G. Mandell, A.M. Falick, and E.A. Komives Identification of protein-protein interfaces by decreased amide proton solvent accessibility Proc. Natl. Acad. Sci. U. S. A. 95 1998 14705 14710 (Pubitemid 29003694)
47. E. Ortner, V. Schroeder, R. Walser, O. Zerbe, and H.P. Kohler Sensitive and selective detection of free FXIII activation peptide: a potential marker of acute thrombotic events Blood 115 2010 5089 5096
48. T.M. Sabo, P.B. Brasher, and M.C. Maurer Perturbations in factor XIII resulting from activation and inhibition examined by solution based methods and detected by MALDI-TOF MS Biochemistry 46 2007 10089 10101 (Pubitemid 47378601)
49. B.T. Turner, and M.C. Maurer Evaluating the roles of thrombin and calcium in the activation of coagulation factor XIII using H/D exchange and MALDI-TOF MS Biochemistry 41 2002 7947 7954 (Pubitemid 34655160)
50. B.T. Turner, T.M. Sabo, D. Wilding, and M.C. Maurer Mapping of factor XIII solvent accessibility as a function of activation state using chemical modification methods Biochemistry 43 2004 9755 9765 (Pubitemid 38993825)