Converting blood coagulation factor IXa into factor Xa: Dramatic increase in amidolytic activity identifies important active site determinants

EMBO Journal

Volumn 16, Issue 22, 1997, Pages 6626-6635

  Hopfner, Karl Peter ^a   Brandstetter, Hans ^c   Karcher, Annette ^b   Kopetzki, Erhard ^b   Huber, Robert ^a   Engh, Richard A ^a,b   Bode, Wolfram ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b Bochringer Mannheim GmbH   (Germany)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Blood coagulation; Factor IX; In vitro folding; Site directed mutagenesis; Specificity

Indexed keywords

BLOOD CLOTTING FACTOR 10A; BLOOD CLOTTING FACTOR 9A; GLUTAMIC ACID; GLYCINE; ISOLEUCINE; VALINE;

AMINO ACID SUBSTITUTION; ARTICLE; CHEMICAL BOND; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; SEQUENCE HOMOLOGY;

ESCHERICHIA COLI;

EID: 0030729772     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.22.6626     Document Type: Article

References (46)

1. Bajaj, S.P., Rapaport, S.I. and Prodanos, C. (1981) A simplified procedure for purification of human prothrombin. factor IX and factor X. Prep. Biochem., 11, 397-412.
2. Bode, W., Mayr, I., Baumann, U., Huber, K., Stone, S.R. and Hofsteenge, J. (1989) The retined L9 A crystal structure of human α-thrombin: interaction with MS-D-Phe-Pro-Arg-chloromethylketone and significance of the Tyr-Pro-Pro-Trp insertion segment. EMBO J., 8, 3467-3475.
3. Brandstetter, H., Bauer, M., Huber, R., Lollar, P. and Bode, W. (1995) X-ray structure of clotting factor IXa: active site and module structure related to Xase activity and hemophilia B. Proc. Natl Acad. Sci. USA. 92, 9796-9800.
4. Brandstetter, H., Kühne, A., Bode, W., Huber, R., von der Saal, W., Wirthensohn, K. and Engh, R. (1996) X-ray structure of the active site-inhibited clotting factor Xa. J. Biol. Chem., 271, 29988-29992.
5. Brinkmann, U., Mattel, R.E. and Buckel, P. (1989) High-level of recombinant genes in Escherichia coli is dependent on the availability of the dnaY gene product. Gene. 85, 109-114.
6. Carter, P.J., Winter, G., Wilkinson, A.J. and Fersht, A.R. (1984) The use of double mutants to detect structural changes in the active site of the tyrosyl-tRNA synthetase (Bacillus stearothermophilus). Cell. 38, 835-840.
7. Castillo, MJ., Kurachi, K., Nishino, N., Ohkubo, I. and Powers, J.C. (1983) Reactivity of bovine coagulation factor IXaβ. factor Xaβ and factor IXa toward fluorogenic peptides containing the activation site sequences of bovine factor IX and factor X. Biochemistry. 22, 1021-1029.
8. Cho, K., Tanaka, T., Cook, R., Kisiel, W., Fujikawa, K., Kurachi, K. and Powers, J.C. (1984) Active-site mapping of bovine and human blood coagulation serine proteases using synthetic peptide 4-nitroanilide and thioester substrates. Biochemistry. 23, 644-650.
9. Dang, Q.D., Guinto, E. and Di Cera, E. (1997) Rational engineering of activity and specificity in a serine prolease. Nature Biotechnol., 15, 146-149.
10. Davie, E.W., Fujikawa, K. and Kisiel, W. (1991) The coagulation cascade: initiation, maintenance, and regulation. Biochemistry, 30, 10363-10370.
11. Di Scipio, R.G., Kurachi, K. and Davie, E.W. (1978) Activation of human factor IX (Christmas factor). J. Clin. Invest., 61, 1528-1538.
12. Di Scipio, R.G., Hermodson, M.A., Yates, S.G. and Davie, E.W. (1977) A comparison of human prothrombin. factor IX (Christmas factor), factor X (Stuart factor) and protein S. Biochemistry, 16, 698-706.
13. Duffy, E.J. and Lollar, P. (1992) Intrinsic pathway activation of factor X and its activation peptide-deficient derivative. factor Xdes-143-191. J. Biol. Chem., 267, 7821-7827.
14. Engh, R.A. et al. (1996) Enzyme flexibility, solvent and 'weak' interactions characterize thrombin-ligand interactions: implications for drug design. Structure. 4, 1353-1362.
15. Esmon, C.T. (1973) Prothrombin activation. Dissertation. Washington University. St Louis, MO, USA.
16. Fujikawa, K., Legaz, M.E., Kato, H. and Davie, E.W. (1974) The mechanism of activtion of bovine factor IX (Christmas factor) by bovine factor XIa (activated plasma thromboplastin antecedent). Biochemistry. 13, 4508-4516.
17. Furie, B. and Furie, B.C. (1988) The molecular basis of blood coagulation, Cell. 53, 505-518.
18. Furie, B.C. and Furie, B. (1976) Coagulant protein of Russell's viper venom. Methods Enzymol., 45, 191-205.
19. Gibbs, C.S. et al. (1995) Conversion of thrombin into an anticoagulant by protein engineering. Nature. 378, 413-416.
20. Grodberg, J. and Dunn, J.J. (1988) OmpT encodes the Escherichia coli outer membrane protease that cleaves T7 RNA polymerase during purification. J. Bacteriol., 170, 1245-1253.
21. Hedstrom, L. (1996) Trypsin: a case study in the structural determinants of enzyme specificity. Biol. Chem., 377, 463-470.
22. Hedstrom, L., Szilagyi, L. and Rutter, W.J. (1992) Converting trypsin to chymotrypsin: the role of surface loops. Science. 255, 1249-1253.
23. Hedstrom, L., Perona, J.J. and Ruaer, W.J. (1994) Converting trypsin to chymotrypsin: residue 172 is a substrate specificity determinant. Biochemistry. 33, 8757-8763.
24. Jackson, C.M. and Nemerson, Y. (1980) Blood coagulation. Annu. Rev. Biochem., 49, 765-811.
25. Kopetzki, E., Rudolph, R. and Grossmann, A. (1993) Recombinant core streptavidin. US patent US5489528 and European patent EP612325.
26. Krishnaswamy, S., Church, W.S., Nesheim, M.E. and Mann, K.G. (1987) Activation of human prothrombin by human prothrombinase. J. Biol. Chem., 262, 3291-3299.
27. Kurachi, K. and Davie, K.W. (1982) Isolation and characterization of a cDNA coding for human factor IX. Proc: Natl Acad. Sci. USA. 79, 6461-6464.
28. Lawson, J.H. and Mann, K.G. (1991) Cooperative activation of human factor IX by the human extrinsic pathway of blood coagulation. J. Biol. Chem., 266, 11317-11327.
29. Lenting, P.J., ter Maat, H., Clijsters, P.P.F.M. Donath, M.-J.S.H., van Mourik, J.A. and Mertens, K. (1995) Cleavage of arginine 145 in human blood coagulation factor IX converts the zymogen into a factor VIII binding enzyme. J. Biol. Chem., 270, 14884-14890.
30. LiCata, V.J. and Ackers, G.K. (1995) Long-range, small magnitude nonadditivity of mutational effects in proteins. Biochemistry. 34, 3133-3139.
31. Lindquist, P.A., Fujikawa, K. and Davie, E.W. (1978) Activation of bovinefactor IX (Christmas factor) by factor XIa (activated plasma thromhoplastin antecedent) and a protease from Russell's viper venom. J. Biol. Chem., 253, 1902-1909.
32. Lottenberg, R., Christensen, U., Jackson, C.M. and Coleman, P.L. (1981) Assay of coagulation proteases using peptide chromogenic and fluorogenic substrates. Methods Enzymol., 80, 341-361.
33. Lozier, J.N., Monroe, D.M., Stanfield-Oakley, S., Lin, S.-W., Smith, K.J., Roberts, H.R. and High, K.A. (1990) Factor IX New London: substitution of proline for glutamine at position 50 causes severe hemophilia B. Blood. 75, 1097-1104.
34. Madison, H. (1994) Probing structure-function relationships of tissue-type plasminogen activator by site-specific mutagenesis. Fibrinolysis. 8, 221-236.
35. Mares-Guia, M. and Shaw, K. (1965) Studies on the active center of trypsin: the binding of amidincs and guanidines as models of the substrate side chain. J. Biol. Chem., 240, 1579-1585.
36. Mather, T., Oganessyan, V. Hof, P., Huber, R., Foundling, S., Esmon, C. and Bode, W. (1996)The 2.8 Á crystal structure of Gla-domainless activated protein C. EMBO J., 15, 6822-6831.
37. McRae, B.J., Kurachi, K., Heimark, R.L., Fujikawa, K., Davie, K.W. and Powers, J.C. (1981) Mapping the active sites of bovine thrombin. factor IXa. factor Xa. factor XIa. factor XIIa. plasma kallikrein and trypsin with amino acid and peptide thioesters: development of new sensitive substrates. Biochemistry. 20, 7196-7206.
38. Padmanabhan, K., Padmanabhan, K.P., Tulinsky, A., Park, C.H., Bode, W., Huber, R., Blankenship, D.T., Cardin, A.D. and Kisiel, W. (1993) Structure of the human des(1-45) factor Xa at 2.2 Å resolution. J. Mol. Biol., 232, 947-966.
39. Perona, J.J. and Craik, C.S. (1995) Structural basis of substrate speciticity in the serine protcases. Protein Sci., 4, 337-360.
40. Rezaie, A.R. (1996) Role of residue 99 at the S2 subsite of factor Xa and activated protein C in enzyme specificity. J. Biol. Chem., 271, 23807-23814.
41. Rezaie, A.R., Neuenschwander, P.F., Morrissey, J.H. and Esmon, C.T. (1993) Analysis of the functions of the first epidermal growth factor-like domain of factor X. J. Mol. Biol., 268, 8176-8180.
42. Roberts, H.R. (1993) Molecular biology of hemophilia B. Thromb. Haemost., 70, 1-9.
43. Sambrook, J., Fritsch, E.F. and Maniatis.T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press. Cold Spring Harbor. NY.
44. Stubbs, M.T. Huber, R. and Bode, W. (1995) Crystal structures of factor Xa specific inhibitors in complex with trypsin: structural grounds for inhibition of factor Xa and selectivity against thrombin. FEBS Lett., 375, 103-107.
45. van Dieijnen, G., Tans, G., Rosing, J. and Hemker, H.C. (1981) The role of phospholipid and factor Villa in the activation of bovine factor X. J. Biol. Chem., 256, 3433-3442.
46. Wells, J.A. (1990) Additivity of mutational effects in proteins. Biochemistry. 29, 8509-8516.