Table of Contents
Thrombosis
Volume 2010, Article ID 416167, 9 pages
http://dx.doi.org/10.1155/2010/416167
Review Article

Thrombin A-Chain: Activation Remnant or Allosteric Effector?

1Centre for Blood Research, University of British Columbia (UBC), Vancouver, BC, Canada V6T 1Z3
2Department of Biochemistry and Molecular Biology, (UBC), Vancouver, BC, Canada V6T 1Z3
3R and D Canadian Blood Services, Ottawa, ON, Canada K1G 4J5
4Department of Pathology and Laboratory Medicine, (UBC), Vancouver, BC, Canada V6T 1Z3

Received 26 August 2010; Accepted 27 October 2010

Academic Editor: Frank C. Church

Copyright © 2010 Isis S. R. Carter et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. W. Davie and J. D. Kulman, “An overview of the structure and function of thrombin,” Seminars in Thrombosis and Hemostasis, vol. 32, no. 1, pp. 3–15, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. D. M. Monroe and M. Hoffman, What Does It Take to Make the Perfect Clot? Arteriosclerosis, Thrombosis, and Vascular Biology, Lippincott, Williams Wilkins, Philadelphia, Pa, USA, 2006.
  3. M. F. Doyle and K. G. Mann, “Multiple active forms of thrombin. IV. Relative activities of meizothrombins,” Journal of Biological Chemistry, vol. 265, no. 18, pp. 10693–10701, 1990. View at Google Scholar · View at Scopus
  4. R. J. Petrovan, J. W. P. Govers-Riemslag, G. Nowak, H. C. Hemker, G. Tans, and J. Rosing, “Autocatalytic peptide bond cleavages in prothrombin and meizothrombin,” Biochemistry, vol. 37, no. 5, pp. 1185–1191, 1998. View at Publisher · View at Google Scholar · View at Scopus
  5. P. D. Bishop, K. B. Lewis, J. Schultz, and K. M. Walker, “Comparison of recombinant human thrombin and plasma-derived human α-thrombin,” Seminars in Thrombosis and Hemostasis, vol. 32, supplement 1, pp. 86–97, 2006. View at Publisher · View at Google Scholar
  6. W. Bode, D. Turk, and A. Karshikov, “The refined 1.9-Å X-ray crystal structure of D-Phe-Pro-Arg chloromethylketone-inhibited human α-thrombin: structure analysis, overall structure, electrostatic properties, detailed active-site geometry, and structure-function relationships,” Protein Science, vol. 1, no. 4, pp. 426–471, 1992. View at Google Scholar · View at Scopus
  7. W. Bode, I. Mayr, U. Baumann, R. Huber, S. R. Stone, and J. Hofsteenge, “The refined 1.9 Å crystal structure of human α-thrombin: interaction with D-Phe-Pro-Arg chloromethylketone and significance of the Tyr-Pro-Pro-Trp insertion segment,” EMBO Journal, vol. 8, no. 11, pp. 3467–3475, 1989. View at Google Scholar · View at Scopus
  8. T. E. Adams, W. Li, and J. A. Huntington, “Molecular basis of thrombomodulin activation of slow thrombin,” Journal of Thrombosis and Haemostasis, vol. 7, no. 10, pp. 1688–1695, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. D. K. Banfield, D. M. Irwin, D. A. Walz, and R. T. A. MacGillivray, “Evolution of prothrombin: isolation and characterization of the cDNAs encoding chicken and hagfish prothrombin,” Journal of Molecular Evolution, vol. 38, no. 2, pp. 177–187, 1994. View at Google Scholar · View at Scopus
  10. C. Frost, R. Naudé, W. Oelofsen, K. Muramoto, T. Naganuma, and T. Ogawa, “Purification and characterization of ostrich prothrombin,” International Journal of Biochemistry and Cell Biology, vol. 32, no. 11-12, pp. 1151–1159, 2000. View at Publisher · View at Google Scholar
  11. D. K. Banfield and R. T. A. MacGillivray, “Partial characterization of vertebrate prothrombin cDNAs: amplification and sequence analysis of the B chain of thrombin from nine different species,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 7, pp. 2779–2783, 1992. View at Google Scholar · View at Scopus
  12. A. Marchler-Bauer, J. B. Anderson, F. Chitsaz et al., “CDD: specific functional annotation with the Conserved Domain Database,” Nucleic Acids Research, vol. 37, no. 1, pp. D205–D210, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. D. M. Irwin, K. A. Robertson, and R. T. A. MacGillivray, “Structure and evolution of the bovine prothrombin gene,” Journal of Molecular Biology, vol. 200, no. 1, pp. 31–45, 1988. View at Google Scholar · View at Scopus
  14. M. J. Page and E. Di Cera, “Evolution of peptidase diversity,” Journal of Biological Chemistry, vol. 283, no. 44, pp. 30010–30014, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. A. G. Geppert and B. R. Binder, “Allosteric regulation of tPA-mediated plasminogen activation by a modifier mechanism: evidence for a binding site for plasminogen on the tPA A-chain,” Archives of Biochemistry and Biophysics, vol. 297, no. 2, pp. 205–212, 1992. View at Publisher · View at Google Scholar · View at Scopus
  16. L. Summaria and K. C. Robbins, “Isolation of a human plasmin derived, functionally active, light(B) chain capable of forming with streptokinase an equimolar light(B) chain streptokinase complex with plasminogen activator activity,” Journal of Biological Chemistry, vol. 251, no. 18, pp. 5810–5813, 1976. View at Google Scholar · View at Scopus
  17. D. Sinha, M. Marcinkiewicz, D. Navaneetham, and P. N. Walsh, “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, vol. 46, no. 34, pp. 9830–9839, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. B. C. Lechtenberg, D. J. D. Johnson, S. M. V. Freund, and J. A. Huntington, “NMR resonance assignments of thrombin reveal the conformational and dynamic effects of ligation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 32, pp. 14087–14092, 2010. View at Publisher · View at Google Scholar
  19. H. C. Castro, R. B. Zingali, M. G. Albuquerque, M. Pujol-Luz, and C. R. Rodrigues, “Snake venom thrombin-like enzymes: from reptilase to now,” Cellular and Molecular Life Sciences, vol. 61, no. 7-8, pp. 843–856, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. R. C. Maroun, “Molecular basis for the partition of the essential functions of thrombin among snake venom serine proteinases: the case of thrombin-like enzymes,” Haemostasis, vol. 31, no. 3–6, pp. 247–256, 2001. View at Google Scholar · View at Scopus
  21. H. C. Castro, D. M. Silva, C. Craik, and R. B. Zingali, “Structural features of a snake venom thrombin-like enzyme: thrombin and trypsin on a single catalytic platform?” Biochimica et Biophysica Acta, vol. 1547, no. 2, pp. 183–195, 2001. View at Publisher · View at Google Scholar · View at Scopus
  22. N. Itoh, N. Tanaka, S. Mihashi, and I. Yamashina, “Molecular cloning and sequence analysis of cDNA for batroxobin, a thrombin-like snake venom enzyme,” Journal of Biological Chemistry, vol. 262, no. 7, pp. 3132–3135, 1987. View at Google Scholar · View at Scopus
  23. S. M. T. Serrano and R. C. Maroun, “Snake venom serine proteinases: sequence homology vs. substrate specificity, a paradox to be solved,” Toxicon, vol. 45, no. 8, pp. 1115–1132, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Akhavan, P. M. Mannucci, M. Lak et al., “Identification and three-dimensional structural analysis of nine novel mutations in patients with prothrombin deficiency,” Thrombosis and Haemostasis, vol. 84, no. 6, pp. 989–997, 2000. View at Google Scholar · View at Scopus
  25. 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,” Journal of Biological Chemistry, vol. 279, no. 13, pp. 13035–13043, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. R. De Cristofaro, A. Carotti, S. Akhavan et al., “The natural mutation by deletion of Lys9 in the thrombin A-chain affects the pK value of catalytic residues, the overall enzyme's stability and conformational transitions linked to Na binding,” FEBS Journal, vol. 273, no. 1, pp. 159–169, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. C. C. Liu, E. Brustad, W. Liu, and P. G. Schultz, “Crystal structure of a biosynthetic sulfo-hirudin complexed to thrombin,” Journal of the American Chemical Society, vol. 129, no. 35, pp. 10648–10649, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. J. B. Lefkowitz, T. Haver, S. Clarke et al., “The prothrombin Denver patient has two different prothrombin point mutations resulting in Glu-300→Lys and Glu-309→Lys substitutions,” British Journal of Haematology, vol. 108, no. 1, pp. 182–187, 2000. View at Publisher · View at Google Scholar
  29. W. Y. Sun, M. C. Burkart, J. R. Holahan, and S. J. F. Degen, “Prothrombin San Antonio: a single amino acid substitution at a Factor Xa activation site (Arg320 to His) results in dysprothrombinemia,” Blood, vol. 95, no. 2, pp. 711–714, 2000. View at Google Scholar · View at Scopus
  30. S. Akhavan, M. Luciani, S. Lavoretano, and P. M. Mannucci, “Phenotypic and genetic analysis of a compound heterozygote for dys- and hypoprothrombinaemia,” British Journal of Haematology, vol. 120, no. 1, pp. 142–144, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. H. C. F. Cote, W. K. Stevens, L. Bajzar, D. K. Banfield, M. E. Nesheim, and R. T. A. MacGillivray, “Characterization of a stable form of human meizothrombin derived from recombinant prothrombin (R155A, R271A, and R284A),” Journal of Biological Chemistry, vol. 269, no. 15, pp. 11374–11380, 1994. View at Google Scholar · View at Scopus
  32. S. Akhavan, E. Rocha, S. Zeinali, and P. M. Mannucci, “Gly319 → Arg substitution in the dysfunctional prothrombin Segovia,” British Journal of Haematology, vol. 105, no. 3, pp. 667–669, 1999. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Magnusson, T. E. Peterson, L. Sottrup-Jensen, and H. Claeys, “Complete primary structure of prothrombin: structure and reactivity of ten carboxylated glutamic acid residues and regulation of prothrombin activation by thrombin,” in Proteases and Biological Control, E. Reich, D. B. Rifkin, and E. Shaw, Eds., pp. 123–149, Cold Spring Harbor Laboratories, Cold Spring Harbor, NY, USA, 1975. View at Google Scholar
  34. G. F. Endres, M. K. Swenson, and H. A. Scheraga, “Structural aspects of thrombin specificity,” Archives of Biochemistry and Biophysics, vol. 168, no. 1, pp. 180–187, 1975. View at Google Scholar · View at Scopus
  35. K. Fujikawa, M. E. Legaz, H. Kato, and E. W. Davie, “The mechanism of activation of bovine factor IX (Christmas factor) by bovine factor XI (activated plasma thromboplastin antecedent),” Biochemistry, vol. 13, no. 22, pp. 4508–4516, 1974. View at Google Scholar · View at Scopus
  36. T. C. Hageman, G. F. Endres, and H. A. Scheraga, “Mechanism of action of thrombin on fibrinogen. On the role of the A chain of bovine thrombin in specificity and in differentiating between thrombin and trypsin,” Archives of Biochemistry and Biophysics, vol. 171, no. 1, pp. 327–336, 1975. View at Google Scholar · View at Scopus
  37. H. Pirkle, I. Theodor, M. Christofferson, P. Vukasin, and D. Miyada, “On the location in the thrombin B chain of substrate recognition sites for fibrinopeptide release and factor XIII activation,” Thrombosis Research, vol. 55, no. 6, pp. 737–746, 1989. View at Google Scholar · View at Scopus
  38. R. Rajesh Singh and J. Y. Chang, “Structural stability of human alpha-thrombin studied by disulfide reduction and scrambling,” Biochimica et biophysica acta, vol. 1651, no. 1-2, pp. 85–92, 2003. View at Google Scholar · View at Scopus
  39. P. S. Roberts, R. K. Burkat, and W. E. Braxton, “Thrombin's exterase activity in the presence of anticoagulant and other salts,” Thrombosis et diathesis haemorrhagica, vol. 21, no. 1, pp. 103–110, 1969. View at Google Scholar · View at Scopus
  40. E. F. Workman and R. L. Lundblad, “The effect of monovalent cations on the catalytic activity of thrombin,” Archives of Biochemistry and Biophysics, vol. 185, no. 2, pp. 544–548, 1978. View at Google Scholar · View at Scopus
  41. C. L. Orthner and D. P. Kosow, “Evidence that human α-thrombin is a monovalent cation-activated enzyme,” Archives of Biochemistry and Biophysics, vol. 202, no. 1, pp. 63–75, 1980. View at Google Scholar · View at Scopus
  42. B. H. Landis, K. A. Koehler, and J. W. Fenton II, “Human thrombins. Group IA and IIA salt-dependent properties of α-thrombin,” Journal of Biological Chemistry, vol. 256, no. 9, pp. 4604–4610, 1981. View at Google Scholar · View at Scopus
  43. E. Di Cera, R. De Cristofaro, D. J. Albright, and J. W. Fenton II, “Linkage between proton binding and amidase activity in human α-thrombin: effect of ions and temperature,” Biochemistry, vol. 30, no. 32, pp. 7913–7924, 1991. View at Google Scholar
  44. R. De Cristofaro and E. Di Cera, “Effect of protons on the amidase activity of human α-thrombin. Analysis in terms of a general linkage scheme,” Journal of Molecular Biology, vol. 216, no. 4, pp. 1077–1085, 1990. View at Publisher · View at Google Scholar · View at Scopus
  45. R. De Cristofaro and E. Di Cera, “Modulation of thrombin-fibrinogen interaction by specific ion effects,” Biochemistry, vol. 31, no. 1, pp. 257–265, 1992. View at Google Scholar · View at Scopus
  46. R. De Cristofaro, J. W. Fenton II, and E. Di Cera, “Linkage between proton binding and amidase activity in human γ-thrombin,” Biochemistry, vol. 31, no. 4, pp. 1147–1153, 1992. View at Google Scholar · View at Scopus
  47. M. Tsiang, A. K. Jain, K. E. Dunn, M. E. Rojas, L. L. K. Leung, and C. S. Gibbs, “Functional mapping of the surface residues of human thrombin,” Journal of Biological Chemistry, vol. 270, no. 28, pp. 16854–16863, 1995. View at Publisher · View at Google Scholar · View at Scopus
  48. M. E. Papaconstantinou, A. Bah, and E. Di Cera, “Role of the A chain in thrombin function,” Cellular and Molecular Life Sciences, vol. 65, no. 12, pp. 1943–1947, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. C. K. Derian, B. P. Damiano, M. R. D'Andrea, and P. Andrade-Gordon, “Thrombin regulation of cell function through protease-activated receptors: implications for therapeutic intervention,” Biochemistry, vol. 67, no. 1, pp. 56–64, 2002. View at Google Scholar · View at Scopus
  50. M. P. A. Ebert, S. Lamer, J. Meuer et al., “Identification of the thrombin light chain a as the single best mass for differentiation of gastric cancer patients from individuals with dyspepsia by proteome analysis,” Journal of Proteome Research, vol. 4, no. 2, pp. 586–590, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. P. C. Chang, H. L. Wu, H. C. H. Lin, K. C. Wang, and G. Y. Shi, “Human plasminogen kringle1-5 reduces atherosclerosis and neointima formation in mice by suppressing the inflammatory signaling pathway,” Journal of Thrombosis and Haemostasis, vol. 8, no. 1, pp. 194–201, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. S. R. Kim, E. S. Chung, E. Bok et al., “Prothrombin Kringle-2 induces death of mesencephalic dopaminergic neurons in vivo and in vitro via microglial activation,” Journal of Neuroscience Research, vol. 88, no. 7, pp. 1537–1548, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. V. V. Stepanova, I. B. Beloglazova, Y. G. Gursky, R. S. Bibilashvily, Y. V. Parfyonova, and V. A. Tkachuk, “Interaction between kringle and growth-factor-like domains in the urokinase molecule: possible role in stimulation of chemotaxis,” Biochemistry, vol. 73, no. 3, pp. 252–260, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. P. Papareddy, V. Rydengård, M. Pasupuleti et al., “Proteolysis of human thrombin generates novel host defense peptides,” PLoS Pathogens, vol. 6, no. 4, Article ID e1000857, 2010. View at Publisher · View at Google Scholar · View at Scopus