Molecular evolution of the vertebrate blood coagulation network

Colin J. Davidson; Robert P. Hirt; Kalpana Lal; Philip Snell; Greg Elgar; Edward G. D. Tuddenham; John H. McVey

doi:10.1055/s-0037-1613369

Thrombosis and Haemostasis, Inhaltsverzeichnis

Thromb Haemost 2003; 89(03): 420-428
DOI: 10.1055/s-0037-1613369

Blood Coagulation, Fibrinolysis and Cellular Haemostasis

Schattauer GmbH

Molecular evolution of the vertebrate blood coagulation network

Colin J. Davidson

¹Haemostasis Group, MRC Clinical Sciences Centre, Faculty of Medicine, Imperial College, Hammersmith Hospital Campus, London, UK

,

Robert P. Hirt

²Department of Zoology, The Natural History Museum, London, UK

,

Kalpana Lal

²Department of Zoology, The Natural History Museum, London, UK

,

Philip Snell

³Fugu Genomics, HGMP Resource Centre, Hinxton, Cambridge, UK

,

Greg Elgar

³Fugu Genomics, HGMP Resource Centre, Hinxton, Cambridge, UK

,

Edward G. D. Tuddenham

¹Haemostasis Group, MRC Clinical Sciences Centre, Faculty of Medicine, Imperial College, Hammersmith Hospital Campus, London, UK

,

John H. McVey

¹Haemostasis Group, MRC Clinical Sciences Centre, Faculty of Medicine, Imperial College, Hammersmith Hospital Campus, London, UK

› Institutsangaben

Abstract

Summary

In mammalian blood coagulation 5 proteases, factor VII (FVII), factor IX (FIX), factor X (FX), protein C (PC) and prothrombin act with two cofactors factor V and factor VIII to control the generation of fibrin. Biochemical evidence and molecular cloning data have previously indicated that blood coagulation involving tissue factor, prothrombin and fibrinogen is present in all vertebrates. Using degenerate RT-PCR we have isolated and characterized novel cDNAs with sequence identity to the blood coagulation serine proteases and cofactors from chicken and the puffer fish (Fugu rubripes). Sequence alignments, phylogenetic and comparative sequence analysis all support the existence of the Gla-EGF1-EGF2-SP domain serine proteases FVII, FIX, FX, PC and the A1-A2-B-A3-C1-C2 domain protein cofactors FV and FVIII in these species. These results strongly suggest that the blood coagulation network is present in all jawed vertebrates and evolved before the divergence of tetrapods and teleosts over 430 million years ago; and that vertebrate blood coagulation may have benefited from two rounds of gene or whole genome duplication. Sequences identified in Fugu coding for additional FVII-like, FIX-like and PC-like sequences support the possibility of further tandem and large-scale duplications in teleosts. Comparative sequence analyses of amino acid residues in the active site region suggest these additional sequences have evolved new and as yet unknown functions.

Supplementary information to this article available at both http://europium.csc.mrc.ac.uk and www.thrombosis-online.com

Keywords

Evolution - serine proteases - blood coagulation - cofactors

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References
1 Doolittle RF. The evolution of vertebrate blood coagulation: a case of Yin and Yang. Thromb Haemost 1993; 70: 24-8.
2 Doolittle RF, Feng DF. Reconstructing the evolution of vertebrate blood coagulation from a consideration of the amino acid sequences of clotting proteins. Cold Spring Harb Symp Quant Biol 1987; 52: 869-74.
3 Patthy L. Evolution of the proteases of blood coagulation and fibrinolysis by assembly from modules. Cell 1985; 41: 657-63.
4 Ryden LG, Hunt LT. Evolution of protein complexity: the blue copper-containing oxidases and related proteins. J Mol Evol 1993; 36: 41-66.
5 Doolittle RF, Sturgenor DM. Blood coagulation in fish. Am J Physiol 1962; 203: 964-70.
6 Banfield DK, MacGillivray RT. Partial characterization of vertebrate prothrombin cDNAs: amplification and sequence analysis of the B chain of thrombin from nine different species. Proc Natl Acad Sci USA 1992; 89: 2779-83.
7 Jagadeeswaran P, Gregory M, Zhou Y, Zon L, Padmanabhan K, Hanumanthaiah R. Characterization of zebrafish full-length prothrombin cDNA and linkage group mapping. Blood Cells Mol Dis 2000; 26: 479-89.
8 Jagadeeswaran P, Sheehan JP. Analysis of blood coagulation in the zebrafish. Blood Cells Mol Dis 1999; 25: 239-49.
9 Sheehan J, Templer M, Gregory M, Hanumanthaiah R, Troyer D, Phan T, Thankavel B, Jagadeeswaran P. Demonstration of the extrinsic coagulation pathway in teleostei: Identification of zebrafish coagulation factor VII. Proc Natl Acad Sci USA 2001; 98: 8768-73.
10 Thompson JD, Higgins DG, Gibson TJ. CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22: 4673-80.
11 Maidak BL, Olsen GJ, Larsen N, Overbeek R, McCaughey MJ, Woese CR. The Ribosomal Database Project (RDP). Nucleic Acids Res 1996; 24: 82-5.
12 Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001; 17: 754-5.
13 Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP. Bayesian inference of phylogeny and its impact on evolutionary biology. Science 2001; 294: 2310-4.
14 Bode W, Brandstetter H, Mather T, Stubbs MT. Comparative analysis of haemostatic proteinases: structural aspects of thrombin, factor Xa, factor IXa and protein C. Thromb Haemost 1997; 78: 501-11.
15 Corey DR, Craik CS. An investigation into the minimum requirements for peptide hydrolysis by mutation of the catalytic triad of trypsin. Journal of American Chemical Society 1992; 114: 1784-90.
16 Dickinson CD, Kelly CR, Ruf W. Identification of surface residues mediating tissue factor binding and catalytic function of the serine protease factor VIIa. Proc Natl Acad Sci USA 1996; 93: 14379-84.
17 Neuenschwander PF, Morrissey JH. Alteration of the substrate and inhibitor specificities of blood coagulation factor VIIa: importance of amino acid residue K192. Biochemistry 1995; 34: 8701-7.
18 Zhang YL, Hervio L, Strandberg L, Madison EL. Distinct contributions of residue 192 to the specificity of coagulation and fibrinolytic serine proteases. J Biol Chem 1999; 274: 7153-6.
19 Graf L, Craik CS, Patthy A, Roczniak S, Fletterick RJ, Rutter WJ. Selective alteration of substrate specificity by replacement of aspartic acid-189 with lysine in the binding pocket of trypsin. Biochemistry 1987; 26: 2616-23.
20 Huber R, Bode W. Structural basis of the activation and action of trypsin. Accounts of Chemical Research 1978; 11: 114-22.
21 Brandstetter H, Bauer M, Huber R, Lollar P, Bode W. X-ray structure of clotting factor IXa: Active site and module structure related to Xase activity and hemophilia B. Proc Natl Acad Sci USA 1995; 92: 9796-800.
22 Abi-Rached L, Gilles A, Shiina T, Pontarotti P, Inoko H. Evidence of en bloc duplication in vertebrate genomes. Nat Genet 2002; 31: 100-5.
23 McLysaght A, Hokamp K, Wolfe KH. Extensive genomic duplication during early chordate evolution. Nat Genet 2002; 31: 200-4.
24 Ohno S. Gene duplication and the uniqueness of vertebrate genomes circa 1970-1999. Semin Cell Dev Biol 1999; 10: 517-22.
25 Smith NG, Knight R, Hurst LD. Vertebrate genome evolution: a slow shuffle or a big bang?. BioEssays 1999; 21: 697-703.
26 Aparicio S, Chapman J, Stupka E, Putnam N, Chia JM, Dehal P. et al Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 2002; 297: 1301-10.
27 Bork P, Bairoch A. Extracellular protein modules: A proposed nomenclature. Trends Biochem Sci 1995; 20 poster C02.