Structural basis of thrombin-mediated factor V activation: The Glu 666-Glu672 sequence is critical for processing at the heavy chain - B domain junction

Blood

Volumn 117, Issue 26, 2011, Pages 7164-7173

  Corral Rodríguez, María Ángeles ^a   Bock, Paul E ^b   Hernández Carvajal, Erick ^a   Gutiérrez Gallego, Ricardo ^c,d   Fuentes Prior, Pablo ^a  

^a HOSPITAL DE LA SANTA CREU I SANT PAU   (Spain)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c INST MUNIC D INVESTIGACIO MEDICA   (Spain)

^d UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; BLOOD CLOTTING FACTOR 5; BLOOD CLOTTING FACTOR 5A; GLUTAMIC ACID; HIRUDIN; PROTEINASE; SERINE; THROMBIN;

AMINO ACID SEQUENCE; ARTICLE; BLOOD CLOTTING; HEAVY CHAIN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN STRUCTURE;

EID: 79959816046     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-10-315309     Document Type: Article

References (50)

1. Davie EW, Fujikawa K, Kisiel W. The coagulation cascade: initiation, maintenance, and regulation. Biochemistry. 1991;30(43):10363-10370.
2. Steen M, Villoutreix BO, Norstrom EA, Yamazaki T, Dahlbäck B. Defining the factor Xa-binding site on factor Va by site-directed glycosylation. J Biol Chem. 2002;277(51):50022-50029. (Pubitemid 36014454)
3. Toso R, Camire RM. Removal of B-domain sequences from factor V rather than specific proteolysis underlies the mechanism by which cofactor function is realized. J Biol Chem. 2004;279(20):21643-21650. (Pubitemid 38656576)
4. Lenting PJ, van de Loo JW, Donath MJ, van Mourik JA, Mertens K. The sequence Glu1811-Lys1818 of human blood coagulation factor VIII comprises a binding site for activated factor IX. J Biol Chem. 1996;271(4):1935-1940.
5. Bode W, Mayr I, Baumann U, Huber R, Stone SR, Hofsteenge J. The refined 1.9 A crystal structure of human alpha-thrombin: interaction with D-Phe-Pro-Arg chloromethylketone and significance of the Tyr-Pro-Pro-Trp insertion segment. EMBO J. 1989;8(11):3467-3475. (Pubitemid 19273577)
6. Bock PE, Panizzi P, Verhamme IMA. Exosites in the substrate specificity of blood coagulation reactions. J Thromb Haemost. 2007;5(s1):81-94. (Pubitemid 46958821)
7. Tsiang M, Jain AK, Dunn KE, Rojas ME, Leung LL, Gibbs CS. Functional mapping of the surface residues of human thrombin. J Biol Chem. 1995;270(28):16854-16863.
8. Pechik I, Madrazo J, Mosesson MW, Hernandez I, Gilliland GL, Medved L. Crystal structure of the complex between thrombin and the central "E" region of fibrin. Proc Natl Acad Sci U S A. 2004;101(9):2718-2723.
9. Rydel TJ, Ravichandran KG, Tulinsky A, et al. The structure of a complex of recombinant hirudin and human alpha-thrombin. Science. 1990;249(4966):277- 280.
10. Corral-Rodríguez MÁ, Macedo-Ribeiro S, Barbosa Pereira PJ, Fuentes-Prior P. Leech-derived thrombin inhibitors: from structures to mechanisms to clinical applications. J Med Chem. 2010;53(10):3847-3861.
11. Fuentes-Prior P, Iwanaga Y, Huber R, et al. Structural basis for the anticoagulant activity of the thrombin-thrombomodulin complex Nature. 2000;404(6777):518-525. (Pubitemid 30186897)
12. Dumas JJ, Kumar R, Seehra J, Somers WS, Mosyak L. Crystal structure of the GpIbalpha-thrombin complex essential for platelet aggregation. Science. 2003;301(5630):222-226. (Pubitemid 36868962)
13. Celikel R, McClintock RA, Roberts JR, et al. Modulation of alpha-thrombin function by distinct interactions with platelet glycoprotein Ibalpha. Science. 2003;301(5630):218-221. (Pubitemid 36858476)
14. Esmon CT, Lollar P. Involvement of thrombin an-ion-binding exosites 1 and 2 in the activation of factor V and factor VIII. J Biol Chem. 1996;271(23):13882-13887. (Pubitemid 26185435)
15. Dharmawardana KR, Bock PE. Demonstration of exosite I-dependent interactions of thrombin with human factor V and factor Va involving the factor Va heavy chain: analysis by affinity chromatography employing a novel method for active-site-selective immobilization of serine proteinases. Biochemistry. 1998;37(38):13143-13152. (Pubitemid 28449558)
16. Dharmawardana KR, Olson ST, Bock PE. Role of regulatory exosite I in binding of thrombin to human factor V, factor Va, factor Va subunits, and activation fragments. J Biol Chem. 1999;274(26):18635-18643.
17. Myles T, Yun TH, Hall SW, Leung LLK. An extensive interaction interface between thrombin and factor V is required for factor V activation. J Biol Chem. 2001;276(27):25143-25149.
18. Segers K, Dahlbäk B, Bock PE, Tans G, Rosing J, Nicolaes GAF. The role of thrombin exosites I and II in the activation of human coagulation factor V. J Biol Chem. 2007;282(47):33915-33924. (Pubitemid 350159447)
19. Beck DO, Bukys MA, Singh LS, Szabo KA, Kalafatis M. The contribution of amino acid region Asp695-Tyr698 of factor V to procofactor activation and factor Va function. J Biol Chem. 2004;279(4):3084-3095. (Pubitemid 38114302)
20. Bukys MA, Orban T, Kim PY, Beck DO, Nesheim ME, Kalafatis M. The structural integrity of anion binding exosite I of thrombin is required and sufficient for timely cleavage and activation of factor V and factor VIII. J Biol Chem. 2006;281(27):18569-18580. (Pubitemid 44035516)
21. Newell JL, Fay PJ. Acidic residues C-terminal to the A2 domain facilitate thrombin-catalyzed activation of factor VIII. Biochemistry. 2008;47(33):8786-8795.
22. Marquette KA, Pittman DD, Kaufman RJ. The factor V B-domain provides two functions to facilitate thrombin cleavage and release of the light chain. Blood. 1995;86(8):3026-3034.
23. Bock PE. Active-site-selective labeling of blood coagulation proteinases with fluorescence probes by the use of thioester peptide chloromethyl ketones. I. Specificity of thrombin labeling. J Biol Chem. 1992;267(21):14963-14973.
24. Bock PE. Active-site-selective labeling of blood coagulation proteinases with fluorescence probes by the use of thioester peptide chloromethyl ketones. II. Properties of thrombin derivatives as reporters of prothrombin fragment 2 binding and specificity of the labeling approach for other proteinases. J Biol Chem. 1992;267(21):14974-14981.
25. Bock PE, Olson ST, Bjork I. Inactivation of thrombin by antithrombin is accompanied by inactivation of regulatory exosite I. J Biol Chem. 1997;272(32):19837-19845. (Pubitemid 27340078)
26. Friedrich R, Panizzi P, Fuentes-Prior P, et al. Staphylocoagulase is a prototype for the mechanism of cofactor-induced zymogen activation. Nature. 2003;425(6957):535-539. (Pubitemid 37237051)
27. Anderson PJ, Nesset A, Dharmawardana KR, Bock PE. Characterization of proexosite I on prothrombin. J Biol Chem. 2000;275(22):16428-16434. (Pubitemid 30398862)
28. Anderson PJ, Nesset A, Dharmawardana KR, Bock PE. Role of proexosite I in factor Vadependent substrate interactions of prothrombin activation. J Biol Chem. 2000;275(22):16435-16442. (Pubitemid 30398863)
29. Anderson PJ, Bock PE. Role of prothrombin fragment 1 in the pathway of regulatory exosite I formation during conversion of human prothrombin to thrombin. J Biol Chem. 2003;278(45):44489-44495. (Pubitemid 37377201)
30. Hirbawi J, Bukys MA, Barhoover MA, Erdogan E, Kalafatis M. Role of the acidic hirudin-like COOH-terminal amino acid region of factor Va heavy chain in the enhanced function of prothrombinase. Biochemistry. 2008;47(30):7963-7974.
31. Bukys MA, Kim PY, Nesheim ME, Kalafatis M. A control switch for prothrombinase: characterization of a hirudin-like pentapeptide from the COOH terminus of factor Va heavy chain that regulates the rate and pathway for prothrombin activation. J Biol Chem. 2006;281(51):39194-39204. (Pubitemid 46041879)
32. Lechtenberg BC, Johnson DJD, Freund SMV, Huntington JA. NMR resonance assignments of thrombin reveal the conformational and dynamic effects of ligation. Proc Natl Acad Sci U S A. 2010;107(32):14087-14092.
33. Toso R, Camire RM. Role of hirudin-like factor Va heavy chain sequences in prothrombinase function. J Biol Chem. 2006;281(13):8773-8779. (Pubitemid 43847983)
34. Padmanabhan K, Padmanabhan KP, Ferrara JD, Sadler JE, Tulinsky A. The structure of alpha-thrombin inhibited by a 15-mer single-stranded DNA aptamer. J Biol Chem. 1993;268(24):17651-17654. (Pubitemid 23260263)
35. Padmanabhan K, Tulinsky A. An ambiguous structure of a DNA 15-mer thrombin complex. Acta Crystallogr D Biol Crystallogr. 1996;52(2):272-282.
36. Liu CC, Brustad E, Liu W, Schultz PG. Crystal structure of a biosynthetic sulfo-hirudin complexed to thrombin. J Am Chem Soc. 2007;129(35):10648-10649. (Pubitemid 350067462)
37. Betz A, Hofsteenge J, Stone SR. Role of interactions involving C-terminal nonpolar residues of hirudin in the formation of the thrombin-hirudin complex. Biochemistry. 1991;30(41):9848-9853.
38. Cheng Y, Slon-Usakiewicz JJ, Wang J, Purisima EO, Konishi Y. Nonpolar interactions of thrombin and its inhibitors at the fibrinogen recognition exosite: thermodynamic analysis. Biochemistry. 1996;35(40):13021-13029. (Pubitemid 26349451)
39. Gandhi PS, Chen Z, Di Cera E. Crystal structure of thrombin bound to the uncleaved extracellular fragment of PAR1. J Biol Chem. 2010;285(20):15393-15398.
40. Krishnan R, Sadler JE, Tulinsky A. Structure of the Ser195Ala mutant of human α-thrombin complexed with fibrinopeptide A(7-16): evidence for residual catalytic activity. Acta Crystallogr D Biol Crystallogr. 2000;56(4):406-410. (Pubitemid 30231220)
41. Stubbs MT, Oschkinat H, Mayr I, et al. The interaction of thrombin with fibrinogen. A structural basis for its specificity. Eur J Biochem. 1992;206(1):187-195.
42. Sadasivan C, Yee VC. Interaction of the factor XIII activation peptide with alpha-thrombin: crystal structure of its enzyme-substrate analog complex. J Biol Chem. 2000;275(47):36942-36948. (Pubitemid 32002108)
43. Martin PD, Malkowski MG, DiMaio J, Konishi Y, Ni F, Edwards BF. Bovine thrombin complexed with an uncleavable analog of residues 7-19 of fibrinogen Aalpha: geometry of the catalytic triad and interactions of the P1′, P2′, and P3′ substrate residues. Biochemistry. 1996;35(40):13030- 13039. (Pubitemid 26349452)
44. Kalafatis M, Beck DO, Mann KG. Structural requirements for expression of factor Va activity. J Biol Chem. 2003;278(35):33550-33561. (Pubitemid 37055809)
45. Hortin GL. Sulfation of tyrosine residues in coagulation factor V. Blood. 1990;76(5):946-952. (Pubitemid 20295506)
46. Pittman DD, Tomkinson KN, Michnick D, Selighsohn U, Kaufman RJ. Posttranslational sulfation of factor V is required for efficient thrombin cleavage and activation and for full procoagulant activity. Biochemistry. 1994;33(22):6952-6959. (Pubitemid 24190820)
47. Long SB, Long MB, White RR, Sullenger BA. Crystal structure of an RNA aptamer bound to thrombin. RNA. 2008;14(12):2504-2512.
48. Suzuki K, Dahlbäck B, Stenflo J. Thrombin-catalyzed activation of human coagulation factor V. J Biol Chem. 1982;257(11):6556-6564. (Pubitemid 12059950)
49. Keller FG, Ortel TL, Quinn-Allen MA, Kane WH. Thrombin-catalyzed activation of recombinant human factor V. Biochemistry. 1995;34(12):4118-4124.
50. Thorelli E, Kaufman RJ, Dahlbäck B. Cleavage requirements for activation of factor V by factor Xa. Eur J Biochem. 1997;247(1):12-20. (Pubitemid 27319480)