A recurrent Gly43Asp substitution in coagulation Factor X rigidifies its catalytic pocket and impairs catalytic activity and intracellular trafficking

Thrombosis Research

Volumn 133, Issue 3, 2014, Pages 481-487

  Menegatti, Marzia ^a,e   Vangone, Anna ^b   Palla, Roberta ^a,e   Milano, Giuseppe ^b   Cavallo, Luigi ^b   Oliva, Romina ^c   De Cristofaro, Raimondo ^d   Peyvandi, Flora ^a,e  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF SALERNO   (Italy)

^c UNIVERSITY OF NAPLES PARTHENOPE   (Italy)

^d CATHOLIC UNIVERSITY   (Italy)

^e FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

Author keywords

Amidolytic activity; Catalytic activity; Factor X deficiency; Factor X Gly43Asp mutation; Molecular dynamics

Indexed keywords

BLOOD CLOTTING FACTOR 10;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BLOOD CLOTTING FACTOR 10 DEFICIENCY; CATALYSIS; CHEMISTRY; ENZYME ACTIVE SITE; GENETICS; HEK293 CELL LINE; HUMAN; INTRACELLULAR SPACE; METABOLISM; MOLECULAR DYNAMICS; MUTATION; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CATALYSIS; CATALYTIC DOMAIN; FACTOR X; FACTOR X DEFICIENCY; HEK293 CELLS; HUMANS; INTRACELLULAR SPACE; MOLECULAR DYNAMICS SIMULATION; MUTATION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84893915820     PISSN: 00493848     EISSN: 18792472     Source Type: Journal    
DOI: 10.1016/j.thromres.2013.12.020     Document Type: Article

References (35)

1. M. Menegatti, and F. Peyvandi Factor X deficiency Semin Thromb Hemost 35 2009 407 415
2. J. Greer Comparative modeling methods: application to the family of the mammalian serine proteases Proteins 7 1990 317 334
3. W. Bode, H. Brandstetter, T. Mather, and M.T. Stubbs Comparative analysis of haemostatic proteinases: structural aspects of thrombin, factor Xa, factor IXa and protein C Thromb Haemost 78 1997 501 511
4. M. Pinotti, M. Monti, M. Baroni, G. Marchetti, and F. Bernardi Molecular characterization of factor X deficiency associated with borderline plasma factor X level Haematologica 89 2004 501 502
5. W.B. Wang, Q.H. Fu, R.F. Zhou, W.M. Wu, Q.L. Ding, and Y.Q. Hu et al. Molecular characterization of two novel mutations causing factor X deficiency in a Chinese pedigree Haemophilia 11 2005 31 37
6. I. Isshiki, R. Favier, T. Moriki, T. Uchida, H. Ishihara, and P. Van Dreden et al. Genetic analysis of hereditary factor X deficiency in a French patient of Sri Lankan ancestry: in vitro expression study identified Gly366Ser substitution as the molecular basis of the dysfunctional factor X Blood Coagul Fibrinolysis 16 2005 9 16
7. M. Pinotti, R.M. Camire, M. Baroni, A. Rajab, G. Marchetti, and F. Bernardi Impaired prothrombinase activity of factor X Gly381Asp results in severe familial CRM + FX deficiency Thromb Haemost 89 2003 243 248
8. F. Peyvandi, M. Menegatti, E. Santagostino, S. Akhavan, J. Uprichard, and D.J. Perry et al. Gene mutations and three-dimensional structural analysis in 13 families with severe factor X deficiency Br J Haematol 117 2002 685 692
9. B. Furie, D.H. Bing, R.J. Feldmann, D.J. Robison, J.P. Burnier, and B.C. Furie Computer-generated models of blood coagulation factor Xa, factor IXa, and thrombin based upon structural homology with other serine proteases J Biol Chem 257 1982 3875 3882
10. R. Palla, S. Lavoretano, R. Lombardi, I. Garagiola, M. Karimi, and A. Afrasiabi et al. The first deletion mutation in the TSP1-6 repeat domain of ADAMTS13 in a family with inherited thrombotic thrombocytopenic purpura Haematologica 94 2009 289 293
11. D. Zhang, and I.M. Kovach Deuterium solvent isotope effect and proton-inventory studies of factor Xa-catalyzed reactions Biochemistry 45 2006 14175 14182
12. R. De Cristofaro, S. Akhavan, C. Altomare, A. Carotti, F. Peyvandi, and P.M. Mannucci A natural prothrombin mutant reveals an unexpected influence of A-chain structure on the activity of human α-thrombin J Biol Chem 279 2004 13035 13043
13. M. Nazaré, D.W. Will, H. Matter, H. Schreuder, K. Ritter, and M. Urmann et al. Probing the subpockets of factor Xa reveals two binding modes for inhibitors based on a 2-carboxyindole scaffold: a study combining structure-activity relationship and X-ray crystallography J Med Chem 48 2005 4511 4525
14. H.G. Wallnoefer, S. Handschuh, K.R. Liedl, and T. Fox Stabilizing of a globular protein by a highly complex water network: a molecular dynamics simulation study on factor Xa J Phys Chem B 114 2010 7405 7412
15. D. Van Der Spoel, E. Lindahl, B. Hess, G. Groenhof, A.E. Mark, and H.J. Berendsen GROMACS: fast, flexible, and free J Comput Chem 26 2005 1701 1718
16. V. Hornak, R. Abel, A. Okur, B. Strockbine, A. Roitberg, and C. Simmerling Comparison of multiple Amber force fields and development of improved protein backbone parameters Proteins 65 2006 712 725
17. N.A. Baker, D. Sept, S. Joseph, M.J. Holst, and J.A. McCammon Electrostatics of nanosystems: Application to microtubules and the ribosome Proc Natl Acad Sci U S A 98 2001 10037 10041
18. V. Chantarangkul, M. Clerici, A. Bressi, P.L. Giesen, and A. Tripodi Thrombin generation assessed as endogenous thrombin potential (ETP) in patients with hypo- or hyper-coagulability. Effects of phospholipids, tissue factor and residual platelets on the measurement performed in platelet-poor and platelet-rich plasma Haematologica 88 2003 547 554
19. S. Epcacan, A. Cairo, M. Menegatti, S. Akbayram, F. Peyvandi, and A.F. Oner Recurrence of the p.Gly262Asp mutation and a novel p.Thr176-Gln186 deletion in twelve patients with congenital Factor X deficiency J Thromb Haemost 9 Suppl. 2 2011 934
20. M. Krawczak, A. Wacey, and D.N. Cooper Molecular reconstruction and homology modelling of the catalytic domain of the common ancestor of the haemostatic vitamin-K-dependent serine proteinases Hum Genet 98 1996 351 370
21. S. Akhavan, P.M. Mannucci, M. Lak, G. Mancuso, M.G. Mazzucconi, and A. Rocino et al. Identification and three-dimensional structural analysis of nine novel mutations in patients with prothrombin deficiency Throm Haemost 84 2000 989 997
22. D.S. Millar, G. Kemball-Cook, J.H. McVey, E.G. Tuddenham, A.D. Mumford, and G.B. Attock et al. Molecular analysis of the genotype-phenotype relationship in factor VII deficiency Hum Genet 107 2000 327 342
23. F. Giannelli, P.M. Green, S.S. Sommer, D.P. Lillicrap, M. Ludwig, and R. Schwaab et al. Haemophilia B: database of point mutations and short additions and deletions, fifth editon, 1994 Nucl Acid Res 22 1994 3534 3546
24. S. Gandrille, and M. Aiach The French INSERM Network on Molecular Abnormalities Responsible for Protein C and Protein S Deficiencies. Identification of mutations in 90 of 121 consecutive symptomatic french patients with a type I protein C deficiency Blood 86 1995 2598 2605
25. F. Peyvandi, M. Menegatti, K. Kavakli, M. Karimi, and P.M. Mannucci Molecular evaluation of a naturally occuring mutation on Factor X gene (Gly222Asp) causing severe FX deficiency Haemophilia 10 Suppl. 3 2004 15
26. R.W. Ruddon, and E. Bedows Assisted protein folding J Biol Chem 272 1997 3125 3128
27. C. Sidrauski, R. Chapman, and P. Walter The unfolded protein response: an intracellular signalling pathway with many surprising features Trends Cell Biol 8 1998 245 249
28. M.J. Gething Role and regulation of the ER chaperone BiP Semin Cell Dev Biol 10 1999 465 472
29. Y. Argon, and B.B. Simen GRP94, an ER chaperone with protein and peptide binding properties Semin Cell Dev Biol 10 1999 495 505
30. W. Bode, D. Turk, and A. Karshikov The refined 1.9-A X-ray crystal structure of D-Phe-Pro-Arg chloromethylketone-inhibited human alpha-thrombin: structure analysis, overall structure, electrostatic properties, detailed active-site geometry, and structure-function relationships Protein Sci 1 1992 426 471
31. S. Mine, T. Yamazaki, T. Miyata, S. Hara, and H. Kato Structural mechanism for heparin-binding of the third Kunitz domain of human tissue factor pathway inhibitor Biochemistry 41 2002 78 85
32. S. Krishnaswamy, and A. Betz Exosites determine macromolecular substrate recognition by prothrombinase Biochemistry 36 1997 12080 12086
33. M. Wilkens, and S. Krishnaswamy The contribution of factor Xa to exosite-dependent substrate recognition by prothrombinase J Biol Chem 277 2002 9366 9374
34. E.Z. Eisenmesser, O. Millet, W. Labeikovsky, D.M. Korzhnev, M. Wolf-Watz, and D.A. Bosco et al. Intrinsic dynamics of an enzyme underlies catalysis Nature 438 2005 117 121
35. D. Banerjee, and S.K. Pal Conformational dynamics at the active site of alpha-chymotrypsin and enzymatic activity Langmuir 24 2008 8163 8168