Allosteric disulfide bonds in thrombosis and thrombolysis

Journal of Thrombosis and Haemostasis

Volumn 4, Issue 12, 2006, Pages 2533-2541

  Chen, V M ^a   Hogg, Philip J ^a,b  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b CHILDREN S CANCER INSTITUTE AUSTRALIA FOR MEDICAL RESEARCH   (Australia)

Author keywords

Glycoprotein 1b ; Integrin 3; Plasminogen; Thrombo modulin; Tissue factor; Vitronectin

Indexed keywords

BETA3 INTEGRIN; BLOOD CLOTTING FACTOR 7A; FIBRONECTIN; GLYCOPROTEIN IB ALPHA; PLASMINOGEN; PROTEIN DISULFIDE ISOMERASE; PROTEINASE ACTIVATED RECEPTOR 2; THROMBOMODULIN; THROMBOPLASTIN; VITRONECTIN;

ALLOSTERISM; ANGIOGENESIS; BLOOD CLOT LYSIS; CELL SURFACE; CONFORMATIONAL TRANSITION; DISULFIDE BOND; HUMAN; INFLAMMATION; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVIEW; THROMBOSIS; TUMOR GROWTH;

ALLOSTERIC SITE; ANIMALS; BLOOD PROTEINS; DISULFIDES; ENZYME ACTIVATION; FIBRINOLYSIS; GLYCOPROTEINS; HUMANS; IMMUNOGLOBULINS; INTEGRIN BETA3; OXIDATION-REDUCTION; PLASMIN; PLASMINOGEN; PROTEIN BINDING; PROTEIN CONFORMATION; THROMBOMODULIN; THROMBOPLASTIN; THROMBOSIS; VITRONECTIN;

EID: 33750985704     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2006.02236.x     Document Type: Review

References (79)

1. Brooks DJ, Fresco JR. Increased frequency of cysteine, tyrosine, and phenylalanine residues since the last universal ancestor. Mol Cell Proteomics 2002; 1: 125-31.
2. Brooks DJ, Fresco JR, Lesk AM, Singh M. Evolution of amino acid frequencies in proteins over deep time: Inferred order of introduction of amino acids into the genetic code. Mol Biol Evol 2002; 19: 1645-55.
3. Jordan IK, Kondrashov FA, Adzhubei IA, Wolf YI, Koonin EV, Kondrashov AS, Sunyaev S. A universal trend of amino acid gain and loss in protein evolution. Nature 2005; 433: 633-8.
4. Thornton JM. Disulphide bridges in globular proteins. J Mol Biol 1981; 151: 261-87.
5. Nakamura H. Thioredoxin and its related molecules: Update 2005. Antioxid Redox Signal 2005; 7: 823-8.
6. Holmgren A. Thioredoxin and glutaredoxin systems. J Biol Chem 1989; 264: 13963-6.
7. Hogg PJ. Disulfide bonds as switches for protein function. Trends Biochem Sci 2003; 28: 210-4.
8. Schmidt B, Ho L, Hogg PJ. Allosteric disulfide bonds. Biochemistry 2006; 45: 7429-33.
9. Weiner SJ, Kollman PA, Case DA, Singh UC, Ghio C, Alagona G, Profeta SJ, Weiner P. A new force field for molecular mechanical simulation of nucleic acids and proteins. J Am Chem Soc 1984; 106: 765-84.
10. Katz BA, Kossiakoff A. The crystallographically determined structures of atypical strained disulfides engineered into subtilisin. J Biol Chem 1986; 261: 15480-5.
11. Wells JA, Powers DB. In vivo formation and stability of engineered disulfide bonds in subtilisin. J Biol Chem 1986; 261: 6564-70.
12. Kuwajima K, Ikeguchi M, Sugawara T, Hiraoka Y, Sugai S. Kinetics of disulfide bond reduction in alpha-lactalbumin by dithiothreitol and molecular basis of superreactivity of the Cys6-Cys120 disulfide bond. Biochemistry 1990; 29: 8240-9.
13. Wetzel R, Perry LJ, Baase WA, Becktel WJ. Disulfide bonds and thermal stability in T4 lysozyme. Proc Natl Acad Sci USA 1988; 85: 401-5.
14. Pjura PE, Matsumura M, Wozniak JA, Matthews BW. Structure of a thermostable disulfide-bridge mutant of phage T4 lysozyme shows that an engineered cross-link in a flexible region does not increase the rigidity of the folded protein. Biochemistry 1990; 29: 2592-8.
15. Richardson J, Richardson D. Prediction of Protein Structure and the Principles of Protein Conformation. New York: Plenum Press, 1989.
16. Wouters MA, Lau KK, Hogg PJ. Cross-strand disulphides in cell entry proteins: Poised to act. Bioessays 2004; 26: 73-9.
17. Erdal E, Bartels F, Binscheck T, Erdmann G, Frevert J, Kistner A, Weller U, Wever J, Bigalke H. Processing of tetanus and botulinum A neurotoxins in isolated chromaffin cells. Naunyn Schmiedebergs Arch Pharmacol 1995; 351: 67-78.
18. Sauer FG, Pinkner JS, Waksman G, Hultgren SJ. Chaperone priming of pilus subunits facilitates a topological transition that drives fiber formation. Cell 2002; 111: 543-51.
19. Haebel PW, Goldstone D, Katzen F, Beckwith J, Metcalf P. The disulfide bond isomerase DsbC is activated by an immunoglobulin-fold thiol oxidoreductase: Crystal structure of the DsbC-DsbDalpha complex. EMBO J 2002; 21: 4774-84.
20. Matthias LJ, Yam PT, Jiang XM, Vandegraaff N, Li P, Poumbourios P, Donoghue N, Hogg PJ. Disulfide exchange in domain 2 of CD4 is required for entry of HIV-1. Nat Immunol 2002; 3: 727-32.
21. Maekawa A, Schmidt B, Fazekas de St Groth B, Sanejouand YH, Hogg PJ. Evidence for a domain-swapped CD4 dimer as the coreceptor for binding to class II MHC. J Immunol 2006; 176: 6873-8.
22. Gallina A, Hanley TM, Mandel R, Trahey M, Broder CC, Viglianti GA, Ryser HJ. Inhibitors of protein-disulfide isomerase prevent cleavage of disulfide bonds in receptor-bound glycoprotein 120 and prevent HIV-1 entry. J Biol Chem 2002; 277: 50579-88.
23. Barbouche R, Miquelis R, Jones IM, Fenouillet E. Protein-disulfide isomerase-mediated reduction of two disulfide bonds of HIV envelope glycoprotein 120 occurs post-CXCR4 binding and is required for fusion. J Biol Chem 2003; 278: 3131-6.
24. Markovic I, Stantchev TS, Fields KH, Tiffany LJ, Tomic M, Weiss CD, Broder CC, Strebel K, Clouse KA. Thiol/disulfide exchange is a prerequisite for CXCR4-tropic HIV-1 envelope-mediated T-cell fusion during viral entry. Blood 2004; 103: 1586-94.
25. Wouters MA, Curmi PM. An analysis of side chain interactions and pair correlations within antiparallel beta-sheets: The differences between backbone hydrogen-bonded and non-hydrogen-bonded residue pairs. Proteins 1995; 22: 119-31.
26. Chen VM, Ahamed J, Versteeg HH, Berndt MC, Ruf W, Hogg PJ. Evidence for activation of tissue factor by an allosteric disulfide bond. Biochemistry 2006; 45: 12020-8.
27. Harlos K, Martin DM, O'Brien DP, Jones EY, Stuart DI, Polikarpov I, Miller A, Tuddenham EG, Boys CW. Crystal structure of the extracellular region of human tissue factor. Nature 1994; 370: 662-6.
28. Bach RR. Tissue factor encryption. Arterioscler Thromb Vasc Biol 2006; 26: 456-61.
29. Maynard JR, Heckman CA, Pitlick FA, Nemerson Y. Association of tissue factor activity with the surface of cultured cells. J Clin Invest 1975; 55: 814-24.
30. Maynard JR, Dreyer BE, Stemerman MB, Pitlick FA. Tissue-factor coagulant activity of cultured human endothelial and smooth muscle cells and fibroblasts. Blood 1977; 50: 387-96.
31. Bach RR, Moldow CF. Mechanism of tissue factor activation on HL-60 cells. Blood 1997; 89: 3270-6.
32. Carson SD, Perry GA,CPirruccello SJ: Fibroblast tissue factor: calcium and ionophore induce shape changes, release of membrane vesicles, and redistribution of tissue factor antigen in addition to increased procoagulant activity. Blood 1994; 84: 526-34.
33. Le DT, Rapaport SI, Rao LV. Studies of the mechanism for enhanced cell surface factor VIIa/tissue factor activation of factor X on fibroblast monolayers after their exposure to N-ethylmaleimide. Thromb Haemost 1994; 72: 848-55.
34. Le DT, Rapaport SI, Rao LV. Relations between factor VIIa binding and expression of factor VIIa/tissue factor catalytic activity on cell surfaces. J Biol Chem 1992; 267: 15447-54.
35. Rao LV, Tait JF, Hoang AD. Binding of annexin V to a human ovarian carcinoma cell line (OC-2008). Contrasting effects on cell surface factor VIIa/tissue factor activity and prothrombinase activity. Thromb Res 1992; 67: 517-31.
36. Wolberg AS, Kon RH, Monroe DM, Ezban M, Roberts HR, Hoffman M. Deencryption of cellular tissue factor is independent of its cytoplasmic domain. Biochem Biophys Res Commun 2000; 272: 332-6.
37. Carson SD, Bromberg ME. Tissue factor encryption/de-encryption is not altered in the absence of the cytoplasmic domain. Thromb Haemost 2000; 84: 657-63.
38. Banner DW, D'Arcy A, Chene C, Winkler FK, Guha A, Konigsberg WH, Nemerson Y, Kirchhofer D. The crystal structure of the complex of blood coagulation factor VIIa with soluble tissue factor. Nature 1996; 380: 41-6.
39. Kirchhofer D, Eigenbrot C, Lipari MT, Moran P, Peek M, Kelley RF. The tissue factor region that interacts with factor Xa in the activation of factor VII. Biochemistry 2001; 40: 675-82.
40. Kirchhofer D, Lipari MT, Moran P, Eigenbrot C, Kelley RF. The tissue factor region that interacts with substrates factor IX and factor X. Biochemistry 2000; 39: 7380-7.
41. Rehemtulla A, Ruf W, Miles DJ, Edgington TS. The third Trp-Lys-Ser (WKS) tripeptide motif in tissue factor is associated with a function site. Biochem J 1992; 282: 737-40.
42. Ahamed J, Versteeg HH, Kerver M, Chen VM, Mueller BM, Hogg PJ, Ruf W. Disulfide isomerization switches tissue factor from coagulation to cell signaling. Proc Natl Acad Sci USA 2006; 103: 13932-7.
43. Rehemtulla A, Ruf W, Edgington TS. The integrity of the cysteine 186-cysteine 209 bond of the second disulfide loop of tissue factor is required for binding of factor VII. J Biol Chem 1991; 266: 10294-9.
44. Jiang XM, Fitzgerald M, Grant CM, Hogg PJ. Redox control of exofacial protein thiols/disulfides by protein disulfide isomerase. J Biol Chem 1999; 274: 2416-23.
45. Ramachandran N, Root P, Jiang XM, Hogg PJ, Mutus B. Mechanism of transfer of NO from extracellular S-nitrosothiols into the cytosol by cell-surface protein disulfide isomerase. Proc Natl Acad Sci USA 2001; 98: 9539-44.
46. O'Reilly MS, Holmgren L, Shing Y, Chen C, Rosenthal RA, Moses M, Lane WS, Cao Y, Sage EH, Folkman J. Angiostatin: A novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 1994; 79: 315-28.
47. Stathakis P, Fitzgerald M, Matthias LJ, Chesterman CN, Hogg PJ. Generation of angiostatin by reduction and proteolysis of plasmin. Catalysis by a plasmin reductase secreted by cultured cells. J Biol Chem 1997; 272: 20641-5.
48. Stathakis P, Lay AJ, Fitzgerald M, Schlieker C, Matthias LJ, Hogg PJ. Angiostatin formation involves disulfide bond reduction and proteolysis in kringle 5 of plasmin. J Biol Chem 1999; 274: 8910-16.
49. Hogg PJ. Plasmin reductase. In: Waisman DM ed. Plasminogen. Kluwer Academic Publishers, 2003; 121-31.
50. Lay AJ, Jiang XM, Kisker O, Flynn E, Underwood A, Condron R, Hogg PJ. Phosphoglycerate kinase acts in tumour angiogenesis as a disulphide reductase. Nature 2000; 408: 869-73.
51. Lay AJ, Jiang XM, Daly E, Sun L, Hogg PJ. Plasmin reduction by phosphoglycerate kinase is a thiol-independent process. J Biol Chem 2002; 277: 9062-8.
52. Wang X, Terzyan S, Tang J, Loy JA, Lin X, Zhang XC. Human plasminogen catalytic domain undergoes an unusual conformational change upon activation. J Mol Biol 2000; 295: 903-14.
53. Preissner KT. Structure and biological role of vitronectin. Annu Rev Cell Biol 1991; 7: 275-310.
54. Mayasundari A, Whittemore NA, Serpersu EH, Peterson CB. The solution structure of the N-terminal domain of human vitronectin: Proximal sites that regulate fibrinolysis and cell migration. J Biol Chem 2004; 279: 29359-66.
55. Kamikubo Y, De Guzman R, Kroon G, Curriden S, Neels JG, Churchill MJ, Dawson P, Oldziej S, Jagielska A, Scheraga HA, Loskutoff DJ, Dyson HJ. Disulfide bonding arrangements in active forms of the somatomedin B domain of human vitronectin. Biochemistry 2004; 43: 6519-34.
56. Andrews RK, Gardiner EE, Shen Y, Whisstock JC, Berndt MC. Glycoprotein Ib-IX-V. Int J Biochem Cell Biol 2003; 35: 1170-4.
57. Celikel R, McClintock RA, Roberts JR, Mendolicchio GL, Ware J, Varughese KI, Ruggeri ZM. Modulation of alpha-thrombin function by distinct interactions with platelet glycoprotein Ibalpha. Science 2003; 301: 218-21.
58. Uff S, Clemetson JM, Harrison T, Clemetson KJ, Emsley J. Crystal structure of the platelet glycoprotein Ib(alpha) N-terminal domain reveals an unmasking mechanism for receptor activation. J Biol Chem 2002; 277: 35657-63.
59. Varughese KI, Ruggeri ZM, Celikel R. Platinum-induced space-group transformation in crystals of the platelet glycoprotein Ib alpha N-terminal domain. Acta Crystallogr D Biol Crystallogr 2004; 60: 405-11.
60. Dumas JJ, Kumar R, McDonagh T, Sullivan F, Stahl ML, Somers WS, Mosyak L. Crystal structure of the wild-type von Willebrand factor A1-glycoprotein Ibalpha complex reveals conformation differences with a complex bearing von Willebrand disease mutations. J Biol Chem 2004; 279: 23327-34.
61. Dumas JJ, Kumar R, Seehra J, Somers WS, Mosyak L. Crystal structure of the GpIbalpha-thrombin complex essential for platelet aggregation. Science 2003; 301: 222-6.
62. Huizinga EG, Tsuji S, Romijn RA, Schiphorst ME, de Groot PG, Sixma JJ, Gros P. Structures of glycoprotein Ibalpha and its complex with von Willebrand factor A1 domain. Science 2002; 297: 1176-9.
63. Burgess JK, Hotchkiss KA, Suter C, Dudman NP, Szollosi J, Chesterman CN, Chong BH, Hogg PJ. Physical proximity and functional association of glycoprotein 1balpha and protein-disulfide isomerase on the platelet plasma membrane. J Biol Chem 2000;275: 9758-66.
64. Takagi J, Petre BM, Walz T, Springer TA. Global conformational rearrangements in integrin extracellular domains in outside-in and inside-out signaling. Cell 2002; 110: 599-611.
65. Beglova N, Blacklow SC, Takagi J, Springer TA. Cysteine-rich module structure reveals a fulcrum for integrin rearrangement upon activation. Nat Struct Biol 2002; 9: 282-7.
66. Essex DW, Li M, Miller A, Feinman RD. Protein disulfide isomerase and sulfhydryl-dependent pathways in platelet activation. Biochemistry 2001; 40: 6070-5.
67. Lahav J, Jurk K, Hess O, Barnes MJ, Farndale RW, Luboshitz J, Kehrel BE. Sustained integrin ligation involves extracellular free sulfhydryls and enzymatically catalyzed disulfide exchange. Blood 2002; 100: 2472-8.
68. Lahav J, Wijnen EM, Hess O, Hamaia SW, Griffiths D, Makris M, Knight CG, Essex DW, Farndale RW. Enzymatically catalyzed disulfide exchange is required for platelet adhesion to collagen via integrin alpha2beta1. Blood 2003; 102: 2085-92.
69. Essex DW, Li M. Redox control of platelet aggregation. Biochemistry 2003; 42: 129-36.
70. Donoghue N, Yam PT, Jiang XM, Hogg PJ. Presence of closely spaced protein thiols on the surface of mammalian cells. Protein Sci 2000; 9: 2436-45.
71. Yan B, Smith JW. Mechanism of integrin activation by disulfide bond reduction. Biochemistry 2001; 40: 8861-7.
72. 3 integrins. Blood 2003; 102: 2491-7.
73. Yan B, Smith JW. A redox site involved in integrin activation. J Biol Chem 2000; 275: 39964-72.
74. Esmon CT. Thrombomodulin as a model of molecular mechanisms that modulate protease specificity and function at the vessel surface. FASEB J 1995; 9: 946-55.
75. Fuentes-Prior P, Iwanaga Y, Huber R, Pagila R, Rumennik G, Seto M, Morser J, Light DR, Bode W. Structural basis for the anticoagulant activity of the thrombin-thrombomodulin complex. Nature 2000; 404: 518-25.
76. White CE, Hunter MJ, Meininger DP, Garrod S, Komives EA. The fifth epidermal growth factor-like domain of thrombomodulin does not have an epidermal growth factor-like disulfide bonding pattern. Proc Natl Acad Sci USA 1996; 93: 10177-82.
77. Sampoli Benitez BA, Hunter MJ, Meininger DP, Komives EA. Structure of the fifth EGF-like domain of thrombomodulin: An EGF-like domain with a novel disulfide-bonding pattern. J Mol Biol 1997; 273: 913-26.
78. Hunter MJ, Komives EA. Thrombin-binding affinities of different disulfide-bonded isomers of the fifth EGF-like domain of thrombomodulin. Protein Sci 1995; 4: 2129-37.
79. Bajaj SP, Schmidt AE, Agah S, Bajaj MS, Padmanabhan K. High resolution structures of p-aminobenzamidine- and benzamidine-VIIa/soluble tissue factor: Unpredicted conformation of the 192-193 peptide bond and mapping of Ca2+, Mg2+, Na+ and Zn2+ sites in factor VIIa. J Biol Chem 2006; 281: 24873-88.