Productive recognition of factor IX by factor XIa exosites requires disulfide linkage between heavy and light chains of factor XIa

Journal of Biological Chemistry

Volumn 287, Issue 9, 2012, Pages 6187-6195

  Marcinkiewicz, Mariola M ^a   Sinha, Dipali ^a   Walsh, Peter N ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION PEPTIDE; BLOOD COAGULATION; CLEAVAGE RATES; DISULFIDE LINKAGES; ELISA ASSAY; ENZYME-SUBSTRATE INTERACTIONS; EXOSITES; HEAVY AND LIGHT CHAINS; HEAVY CHAIN; HIGH AFFINITY; LIGHT CHAIN; PARTIAL REDUCTION; PRE-INCUBATION; SATURATING CONCENTRATION; SCISSILE BOND; SUBSTRATE RECOGNITION;

CHEMICAL ACTIVATION;

SULFUR COMPOUNDS;

BLOOD CLOTTING FACTOR 11A; BLOOD CLOTTING FACTOR 9;

ALLOSTERISM; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DISULFIDE BOND; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME SUBSTRATE COMPLEX; HUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN;

BINDING, COMPETITIVE; BLOOD COAGULATION; CATALYTIC DOMAIN; DISULFIDES; ENZYME ACTIVATION; FACTOR IX; FACTOR XIA; HEK293 CELLS; HUMANS; MUTAGENESIS, SITE-DIRECTED; OXIDATION-REDUCTION; PEPTIDE HYDROLASES; SUBSTRATE SPECIFICITY;

EID: 84857496038     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.291989     Document Type: Article

References (37)

1. Davie, E. W., Fujikawa, K., and Kisiel, W. (1991) The coagulation cascade. Initiation, maintenance, and regulation. Biochemistry 30, 10363-10370
2. Nemerson, Y. (1992) The tissue factor pathway of blood coagulation. Semin. Hematol. 29, 170-176
3. Edgington, T. S., Dickinson, C. D., and Ruf, W. (1997) The structural basis of function of the TF. VIIa complex in the cellular initiation of coagulation. Thromb. Haemost. 78, 401-405 (Pubitemid 27289275)
4. Mann, K. G., Butenas, S., and Brummel, K. (2003) The dynamics of thrombin formation. Arterioscler. Thromb. Vasc. Biol. 23, 17-25 (Pubitemid 36091621)
5. Fujikawa, K., Legaz, M. E., Kato, H., and Davie, E. W. (1974) The mechanism of activation of bovine factor IX (Christmas factor) by bovine factor XIa (activated plasma thromboplastin antecedent). Biochemistry 13, 4508-4516
6. Di Scipio, R. G., Kurachi, K., and Davie, E. W. (1978) Activation of human factor IX (Christmas factor). J. Clin. Invest. 61, 1528-1538 (Pubitemid 8361879)
7. Lindquist, P. A., Fujikawa, K., and Davie, E. W. (1978) Activation of bovine factor IX (Christmas factor) by factor XIa (activated plasma thromboplastin antecedent) and a protease from Russell's viper venom. J. Biol. Chem. 253, 1902-1909 (Pubitemid 8299515)
8. Naito, K., and Fujikawa, K. (1991) Activation of human blood coagulation factor XI independent of factor XII. Factor XI is activated by thrombin and factor XIa in the presence of negatively charged surfaces. J. Biol. Chem. 266, 7353-7358 (Pubitemid 21906372)
9. Gailani, D., and Broze, G. J., Jr. (1991) Factor XI activation in a revised model of blood coagulation. Science 253, 909-912 (Pubitemid 21917236)
10. Broze, G. J., Jr., Warren, L. A., Novotny, W. F., Higuchi, D. A., Girard, J. J., and Miletich, J. P. (1988) The lipoprotein-associated coagulation inhibitor that inhibits the factor VII-tissue factor complex also inhibits factor Xa. Insight into its possible mechanism of action. Blood 71, 335-343 (Pubitemid 18089519)
11. Broze, G. J., Jr., Girard, T. J., and Novotny, W. F. (1990) Regulation of coagulation by a multivalent Kunitz-type inhibitor. Biochemistry 29, 7539-7546 (Pubitemid 20279168)
12. Fujikawa, K., Chung, D. W., Hendrickson, L. E., and Davie, E. W. (1986) Amino acid sequence of human factor XI, a blood coagulation factor with four tandem repeats that are highly homologous with plasma prekallikrein. Biochemistry 25, 2417-2424
13. McMullen, B. A., Fujikawa, K., and Davie, E. W. (1991) Location of the disulfide bonds in human coagulation factor XI. The presence of tandem apple domains. Biochemistry 30, 2056-2060
14. Sinha, D., Koshy, A., Seaman, F. S., and Walsh, P. N. (1985) Functional characterization of human blood coagulation factor XIa using hybridoma antibodies. J. Biol. Chem. 260, 10714-10719 (Pubitemid 16252253)
15. Sinha, D., Seaman, F. S., and Walsh, P. N. (1987) Role of calcium ions and the heavy chain of factor XIa in the activation of human coagulation factor IX. Biochemistry 26, 3768-3775 (Pubitemid 17127449)
16. Sun, Y., and Gailani, D. (1996) Identification of a factor IX binding site on the third apple domain of activated factor XI. J. Biol. Chem. 271, 29023-29028 (Pubitemid 26382607)
17. Sun, M. F., Zhao, M., and Gailani, D. (1999) Identification of amino acids in the factor XI apple 3 domain required for activation of factor IX. J. Biol. Chem. 274, 36373-36378
18. Ogawa, T., Verhamme, I. M., Sun, M. F., Bock, P. E., and Gailani, D. (2005) Exosite-mediated substrate recognition of factor IX by factor XIa. The factor XIa heavy chain is required for initial recognition of factor IX. J. Biol. Chem. 280, 23523-23530 (Pubitemid 40884830)
19. Sinha, D., Marcinkiewicz, M., Navaneetham, D., and Walsh, P. N. (2007) Macromolecular substrate-binding exosites on both the heavy and light chains of factor XIa mediate the formation of the Michaelis complex required for factor IX-activation. Biochemistry 46, 9830-9839 (Pubitemid 47328589)
20. van der Graaf, F., Greengard, J. S., Bouma, B. N., Kerbiriou, D. M., and Griffin, J. H. (1983) Isolation and functional characterization of the active light chain of activated human blood coagulation factor XI. J. Biol. Chem. 258, 9669-9675 (Pubitemid 13049099)
21. Miller, T. N., Sinha, D., Baird, T. R., and Walsh, P. N. (2007) A catalytic domain exosite (Cys527-Cys542) in factor XIa mediates binding to a site on activated platelets. Biochemistry 46, 14450-14460 (Pubitemid 350276352)
22. Sinha, D., Marcinkiewicz, M., Lear, J. D., and Walsh, P. N. (2005) Factor XIa dimer in the activation of factor IX. Biochemistry 44, 10416-10422 (Pubitemid 41076837)
23. Wagenvoord, R., Hendrix, H., Tran, T., and Hemker, H. C. (1990) Development of a sensitive and rapid chromogenic factor IX assay for clinical use. Haemostasis 20, 276-288. (Pubitemid 20378318)
24. Thompson, R. E., Mandle, R., Jr., and Kaplan, A. P. (1977) Association of factor XI and high molecular weight kininogen in human plasma. J. Clin. Invest. 60, 1376-1380 (Pubitemid 8238653)
25. Renné, T., Gailani, D., Meijers, J. C., and Müller-Esterl, W. (2002) Characterization of the H-kininogen-binding site on factor XI. A comparison of factor XI and plasma prekallikrein. J. Biol. Chem. 277, 4892-4899
26. Betz, A., Vlasuk, G. P., Bergum, P. W., and Krishnaswamy, S. (1997) Selective inhibition of the prothrombinase complex. Factor Va alters macromolecular recognition of a tick anticoagulant peptide mutant by factor Xa. Biochemistry 36, 181-191 (Pubitemid 27024691)
27. Krishnaswamy, S., and Betz, A. (1997) Exosites determine macromolecular substrate recognition by prothrombinase. Biochemistry 36, 12080-12086 (Pubitemid 27440946)
28. Baugh, R. J., Dickinson, C. D., Ruf, W., and Krishnaswamy, S. (2000) Exosite interactions determine the affinity of factor X for the extrinsic Xase complex. J. Biol. Chem. 275, 28826-28833
29. Osterud, B., and Rapaport, S. I. (1977) Activation of factor IX by the reaction product of tissue factor and factor VII. Additional pathway for initiating blood coagulation. Proc. Natl. Acad. Sci. U.S.A. 74, 5260-5264
30. Bajaj, S. P., Rapaport, S. I., and Russell, W. A. (1983) Redetermination of the rate-limiting step in the activation of factor IX by factor XIa and by factor VIIa/tissue factor. Explanation for different electrophoretic radioactivity profiles obtained on activation of 3H- and 125I-labeled factor IX. Biochemistry 22, 4047-4053 (Pubitemid 13047082)
31. Wolberg, A. S., Morris, D. P., and Stafford, D. W. (1997) Factor IX activation by factor XIa proceeds without release of a free intermediate. Biochemistry 36, 4074-4079 (Pubitemid 27171578)
32. Samuel, D., Cheng, H., Riley, P. W., Canutescu, A. A., Nagaswami, C., Weisel, J. W., Bu, Z., Walsh, P. N., and Roder, H. (2007) Solution structure of the A4 domain of factor XI sheds light on the mechanism of zymogen activation. Proc. Natl. Acad. Sci. U.S.A. 104, 15693-15698 (Pubitemid 350035362)
33. Wu, W., Sinha, D., Shikov, S., Yip, C. K., Walz, T., Billings, P. C., Lear, J. D., and Walsh, P. N. (2008) Factor XI homodimer structure is essential for normal proteolytic activation by factor XIIa, thrombin, and factor XIa. J. Biol. Chem. 283, 18655-18664
34. Smith, S. B., Verhamme, I. M., Sun, M. F., Bock, P. E., and Gailani, D. (2008) Characterization of Novel Forms of Coagulation Factor XIa: independence of factor XIa subunits in factor IX activation. J. Biol. Chem. 283, 6696-6705
35. Papagrigoriou, E., McEwan, P. A., Walsh, P. N., and Emsley, J. (2006) Crystal structure of the factor XI zymogen reveals a pathway for transactivation. Nat. Struct. Mol. Biol. 13, 557-558 (Pubitemid 43848912)
36. Jin, L., Pandey, P., Babine, R. E., Gorga, J. C., Seidl, K. J., Gelfand, E., Weaver, D. T., Abdel-Meguid, S. S., and Strickler, J. E. (2005) Crystal structures of the FXIa catalytic domain in complex with ecotin mutants reveal substrate-like interactions. J. Biol. Chem. 280, 4704-4712 (Pubitemid 40288640)
37. Navaneetham, D., Jin, L., Pandey, P., Strickler, J. E., Babine, R. E., Abdel-Meguid, S. S., and Walsh, P. N. (2005) Structural and mutational analyses of the molecular interactions between the catalytic domain of factor XIa and the Kunitz protease inhibitor domain of protease nexin 2. J. Biol. Chem. 280, 36165-36175 (Pubitemid 41633889)