Formation of methionine sulfoxide by peroxynitrite at position 1606 of von Willebrand factor inhibits its cleavage by ADAMTS-13: A new prothrombotic mechanism in diseases associated with oxidative stress

Free Radical Biology and Medicine

Volumn 48, Issue 3, 2010, Pages 446-456

  Lancellotti, Stefano ^a   De Filippis, Vincenzo ^b   Pozzi, Nicola ^b   Peyvandi, Flora ^c   Palla, Roberta ^c   Rocca, Bianca ^a   Rutella, Sergio ^a,d   Pitocco, Dario ^a   Mannucci, Pier Mannuccio ^c   De Cristofaro, Raimondo ^a  

^a CATHOLIC UNIVERSITY   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d IRCCS SAN RAFFAELE PISANA   (Italy)

Author keywords

Free radicals; Methionine sulfoxide; Oxidative stress; Peroxynitrite; Thrombotic microangiopathy; Von Willebrand factor, ADAMTS 13

Indexed keywords

3 NITROTYROSINE; ALANINE; ASPARTIC ACID; METHIONINE; METHIONINE SULFOXIDE; PEROXYNITRITE; REACTIVE OXYGEN METABOLITE; RISTOCETIN; TYROSINE; VON WILLEBRAND FACTOR; VON WILLEBRAND FACTOR CLEAVING PROTEINASE;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; HUMAN; HYDROLYSIS; HYPOTHESIS; INHIBITION KINETICS; MICROCIRCULATION; MOLECULAR WEIGHT; NON INSULIN DEPENDENT DIABETES MELLITUS; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOSIS;

ADAM PROTEINS; ADULT; BINDING SITES; BLOOD PLATELETS; CASE-CONTROL STUDIES; DIABETES MELLITUS, TYPE 2; FEMALE; HUMANS; HYDROLYSIS; MALE; METHIONINE; MIDDLE AGED; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; PEROXYNITROUS ACID; PLATELET AGGREGATION; PROTEIN MULTIMERIZATION; RISTOCETIN; TYROSINE; VON WILLEBRAND DISEASES; VON WILLEBRAND FACTOR;

EID: 73649104748     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.11.020     Document Type: Article

References (77)

1. Chung D.W., and Fujikawa K. Processing of von Willebrand factor by ADAMTS-13. Biochemistry 41 (2002) 11065-11070
2. Dent J.A., Berkowitz S.D., Ware J., Kasper C.K., and Ruggeri Z.M. Identification of a cleavage site directing the immunochemical detection of molecular abnormalities in type IIA von Willebrand factor. Proc. Natl. Acad. Sci. USA 87 (1990) 6306-6310
3. Tsai H.M. Physiologic cleavage of von Willebrand factor by a plasma protease is dependent on its conformation and requires calcium ion. Blood 87 (1996) 4235-4244
4. Fischer B.E., Thomas K.B., Schlokat U., and Dorner F. Triplet structure of human von Willebrand factor. Biochem. J. 331 Pt 2 (1998) 483-488
5. Furlan M., Robles R., and Lamie B. Partial purification and characterization of a protease from human plasma cleaving von Willebrand factor to fragments produced by in vivo proteolysis. Blood 87 (1996) 4223-4234
6. Levy G.G., Nichols W.C., Lian E.C., Foroud T., McClintick J.N., McGee B.M., Yang A.Y., Siemieniak D.R., Stark K.R., Gruppo R., Sarode R., Shurin S.B., Chandrasekaran V., Stabler S.P., Sabio H., Bouhassira E.E., Upshaw Jr. J.D., Ginsburg D., and Tsai H.M. Mutations in a member of the ADAMTS gene family cause thrombotic thrombocytopenic purpura. Nature 413 (2001) 488-494
7. Moake J.L. Thrombotic microangiopathies. N. Engl. J. Med. 347 (2002) 589-600
8. O'Brien L.A., Sutherland J.J., Weaver D.F., and Lillicrap D. Theoretical structural explanation for Group I and Group II, type 2A von Willebrand disease mutations. J. Thromb. Haemostasis 3 (2005) 796-797
9. Dong J.F. Cleavage of ultra-large von Willebrand factor by ADAMTS-13 under flow conditions. J. Thromb. Haemostasis 3 (2005) 1710-1716
10. Sutherland J.J., O'Brien L.A., Lillicrap D., and Weaver D.F. Molecular modeling of the von Willebrand factor A2 domain and the effects of associated type 2A von Willebrand disease mutations. J. Mol. Model. (Online) 10 (2004) 259-270
11. O'Brien L.A., James P.D., Othman M., Berber E., Cameron C., Notley C.R., Hegadorn C.A., Sutherland J.J., Hough C., Rivard G.E., O'Shaunessey D., and Lillicrap D. Founder von Willebrand factor haplotype associated with type 1 von Willebrand disease. Blood 102 (2003) 549-557
12. Dong J.F., Moake J.L., Nolasco L., Bernardo A., Arceneaux W., Shrimpton C.N., Schade A.J., McIntire L.V., Fujikawa K., and Lopez J.A. ADAMTS-13 rapidly cleaves newly secreted ultralarge von Willebrand factor multimers on the endothelial surface under flowing conditions. Blood 100 (2002) 4033-4039
13. Tsai H.M., Sussman I.I., and Nagel R.L. Shear stress enhances the proteolysis of von Willebrand factor in normal plasma. Blood 83 (1994) 2171-2179
14. Nishio K., Anderson P.J., Zheng X.L., and Sadler J.E. Binding of platelet glycoprotein Ibalpha to von Willebrand factor domain A1 stimulates the cleavage of the adjacent domain A2 by ADAMTS13. Proc. Natl. Acad. Sci. USA 101 (2004) 10578-10583
15. Shim K., Anderson P.J., Tuley E.A., Wiswall E., and Sadler J.E. Platelet-VWF complexes are preferred substrates of ADAMTS13 under fluid shear stress. Blood 111 (2008) 651-657
16. De Cristofaro R., Peyvandi F., Palla R., Lavoretano S., Lombardi R., Merati G., Romitelli F., Di Stasio E., and Mannucci P.M. Role of chloride ions in modulation of the interaction between von Willebrand factor and ADAMTS-13. J. Biol. Chem 280 (2005) 23295-23302
17. Peyvandi F., Lavoretano S., Palla R., Valsecchi C., Merati G., De Cristofaro R., Rossi E., and Mannuccio Mannucci P. Mechanisms of the interaction between two ADAMTS13 gene mutations leading to severe deficiency of enzymatic activity. Human Mutat. 27 (2006) 330-336
18. Di Stasio E., Lancellotti S., Peyvandi F., Palla R., Mannucci P.M., and De Cristofaro R. Mechanistic studies on ADAMTS13 catalysis. Biophys. J. 95 (2008) 2450-2461
19. Huang R.H., Wang Y., Roth R., Yu X., Purvis A.R., Heuser J.E., Egelman E.H., and Sadler J.E. Assembly of Weibel-Palade body-like tubules from N-terminal domains of von Willebrand factor. Proc. Natl. Acad. Sci. USA 105 (2008) 482-487
20. Zhang X., Halvorsen K., Zhang C.Z., Wong W.P., and Springer T.A. Mechanoenzymatic cleavage of the ultralarge vascular protein von Willebrand factor. Science 324 (2009) 1330-1334
21. Huie R.E., and Padmaja S. The reaction of NO with superoxide. Free Radic. Res. Commun. 18 (1993) 195-199
22. Alvarez M.N., Piacenza L., Irigoin F., Peluffo G., and Radi R. Macrophage-derived peroxynitrite diffusion and toxicity to Trypanosoma cruzi. Arch. Biochem. Biophys. 432 (2004) 222-232
23. Quijano C., Romero N., and Radi R. Tyrosine nitration by superoxide and nitric oxide fluxes in biological systems: modeling the impact of superoxide dismutase and nitric oxide diffusion. Free Radic. Biol. Med. 39 (2005) 728-741
24. Denicola A., Souza J.M., and Radi R. Diffusion of peroxynitrite across erythrocyte membranes. Proc. Natl. Acad. Sci. USA 95 (1998) 3566-3571
25. Alvarez B., Ferrer-Sueta G., Freeman B.A., and Radi R. Kinetics of peroxynitrite reaction with amino acids and human serum albumin. J. Biol. Chem. 274 (1999) 842-848
26. Pryor W.A., Jin X., and Squadrito G.L. One- and two-electron oxidations of methionine by peroxynitrite. Proc. Natl. Acad. Sci. USA 91 (1994) 11173-11177
27. Perrin D., and Koppenol W.H. The quantitative oxidation of methionine to methionine sulfoxide by peroxynitrite. Arch. Biochem. Biophys. 377 (2000) 266-272
28. Alvarez B., and Radi R. Peroxynitrite reactivity with amino acids and proteins. Amino Acids 25 (2003) 295-311
29. Moreno J.J., and Pryor W.A. Inactivation of alpha 1-proteinase inhibitor by peroxynitrite. Chem. Res. Toxicol. 5 (1992) 425-431
30. Berlett B.S., Levine R.L., and Stadtman E.R. Carbon dioxide stimulates peroxynitrite-mediated nitration of tyrosine residues and inhibits oxidation of methionine residues of glutamine synthetase: both modifications mimic effects of adenylylation. Proc. Natl. Acad. Sci. USA 95 (1998) 2784-2789
31. Gow A.J., Duran D., Malcolm S., and Ischiropoulos H. Effects of peroxynitrite-induced protein modifications on tyrosine phosphorylation and degradation. FEBS Lett. 385 (1996) 63-66
32. Fields G.B., and Noble R.L. Solid phase peptide synthesis utilizing 9-fluorenylmethoxycarbonyl amino acids. Int. J. Pept. Protein Res. 35 (1990) 161-214
33. Pace C.N., Vajdos F., Fee L., Grimsley G., and Gray T. How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4 (1995) 2411-2423
34. De Filippis V., Frasson R., and Fontana A. 3-Nitrotyrosine as a spectroscopic probe for investigating protein protein interactions. Protein Sci. 15 (2006) 976-986
35. Beckman J.S., Chen J., Ischiropoulos H., and Crow J.P. Oxidative chemistry of peroxynitrite. Methods Enzymol. 233 (1994) 229-240
36. Zhang P., Pan W., Rux A.H., Sachais B.S., and Zheng X.L. The cooperative activity between the carboxyl-terminal TSP1 repeats and the CUB domains of ADAMTS13 is crucial for recognition of von Willebrand factor under flow. Blood 110 (2007) 1887-1894
37. Reznick A.Z., and Packer L. Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol. 233 (1994) 357-363
38. Kokame K., Matsumoto M., Fujimura Y., and Miyata T. VWF73, a region from D1596 to R1668 of von Willebrand factor, provides a minimal substrate for ADAMTS-13. Blood 103 (2004) 607-612
39. Ewenstein B.M., Warhol M.J., Handin R.I., and Pober J.S. Composition of the von Willebrand factor storage organelle (Weibel-Palade body) isolated from cultured human umbilical vein endothelial cells. J. Cell Biol. 104 (1987) 1423-1433
40. Gokce I., Woody R.W., Anderluh G., and Lakey J.H. Single peptide bonds exhibit poly(pro)II ("random coil") circular dichroism spectra. J. Am. Chem. Soc. 127 (2005) 9700-9701
41. Lakowicz J.R. Principles of Fluorescence Spectroscopy (2006), Springer, New York
42. Sadler J.E., Moake J.L., Miyata T., and George J.N. Recent advances in thrombotic thrombocytopenic purpura. Hematology. Am. Soc. Hematol. Educ. Program (2004) 407-423
43. De Cristofaro R., Rocca B., Vitacolonna E., Falco A., Marchesani P., Ciabattoni G., Landolfi R., Patrono C., and Davi G. Lipid and protein oxidation contribute to a prothrombotic state in patients with type 2 diabetes mellitus. J. Thromb. Haemostasis 1 (2003) 250-256
44. Orasanu G., and Plutzky J. The pathologic continuum of diabetic vascular disease. J. Am. Coll. Cardiol. 53 (2009) S35-42
45. Hink U., Li H., Mollnau H., Oelze M., Matheis E., Hartmann M., Skatchkov M., Thaiss F., Stahl R.A., Warnholtz A., Meinertz T., Griendling K., Harrison D.G., Forstermann U., and Munzel T. Mechanisms underlying endothelial dysfunction in diabetes mellitus. Circ. Res. 88 (2001) E14-22
46. Davi G., Ciabattoni G., Consoli A., Mezzetti A., Falco A., Santarone S., Pennese E., Vitacolonna E., Bucciarelli T., Costantini F., Capani F., and Patrono C. In vivo formation of 8-iso-prostaglandin f2alpha and platelet activation in diabetes mellitus: effects of improved metabolic control and vitamin E supplementation. Circulation 99 (1999) 224-229
47. Gill J.C., Endres-Brooks J., Bauer P.J., Marks Jr. W.J., and Montgomery R.R. The effect of ABO blood group on the diagnosis of von Willebrand disease. Blood 69 (1987) 1691-1695
48. Franchini M., and Mannucci P.M. Von Willebrand factor: another Janus-faced hemostasis protein. Semin. Thromb. Hemostasis 34 (2008) 663-669
49. Spiel A.O., Gilbert J.C., and Jilma B. von Willebrand factor in cardiovascular disease: focus on acute coronary syndromes. Circulation 117 (2008) 1449-1459
50. Frankel D.S., Meigs J.B., Massaro J.M., Wilson P.W., O'Donnell C.J., D'Agostino R.B., and Tofler G.H. Von Willebrand factor, type 2 diabetes mellitus, and risk of cardiovascular disease: the Framingham Offspring Study. Circulation 118 (2008) 2533-2539
51. Zhang Q., Zhou Y.F., Zhang C.Z., Zhang X., Lu C., and Springer T.A. Structural specializations of A2, a force-sensing domain in the ultralarge vascular protein von Willebrand factor. Proc. Natl. Acad. Sci. USA 106 (2009) 9226-9231
52. Sacksteder C.A., Qian W.J., Knyushko T.V., Wang H., Chin M.H., Lacan G., Melega W.P., Camp II D.G., Smith R.D., Smith D.J., Squier T.C., and Bigelow D.J. Endogenously nitrated proteins in mouse brain: links to neurodegenerative disease. Biochemistry 45 (2006) 8009-8022
53. Souza J.M., Peluffo G., and Radi R. Protein tyrosine nitration-functional alteration or just a biomarker?. Free Radic. Biol. Med. 45 (2008) 357-366
54. Fuentes-Prior P., Iwanaga Y., Huber R., Pagila R., Rumennik G., Seto M., Morser J., Light D.R., and Bode W. Structural basis for the anticoagulant activity of the thrombin-thrombomodulin complex. Nature 404 (2000) 518-525
55. Gellman S.H. On the role of methionine residues in the sequence-independent recognition of nonpolar protein surfaces. Biochemistry 30 (1991) 6633-6636
56. Parastatidis I., Thomson L., Burke A., Chernysh I., Nagaswami C., Visser J., Stamer S., Liebler D.C., Koliakos G., Heijnen H.F., Fitzgerald G.A., Weisel J.W., and Ischiropoulos H. Fibrinogen beta-chain tyrosine nitration is a prothrombotic risk factor. J. Biol. Chem. 283 (2008) 33846-33853
57. Vogt W. Oxidation of methionyl residues in proteins: tools, targets, and reversal. Free Radic. Biol. Med. 18 (1995) 93-105
58. Burns E.R., Lou Y., and Pathak A. Morphologic diagnosis of thrombotic thrombocytopenic purpura. Am. J. Hematol. 75 (2004) 18-21
59. Lowther W.T., Brot N., Weissbach H., and Matthews B.W. Structure and mechanism of peptide methionine sulfoxide reductase, an "anti-oxidation" enzyme. Biochemistry 39 (2000) 13307-13312
60. Levine R.L., Mosoni L., Berlett B.S., and Stadtman E.R. Methionine residues as endogenous antioxidants in proteins. Proc. Natl. Acad. Sci. USA 93 (1996) 15036-15040
61. Stadtman E.R., Moskovitz J., Berlett B.S., and Levine R.L. Cyclic oxidation and reduction of protein methionine residues is an important antioxidant mechanism. Mol. Cell. Biochem. 234-235 (2002) 3-9
62. Leopold J.A., and Loscalzo J. Oxidative risk for atherothrombotic cardiovascular disease. Free Radic. Biol. Med. 47 (2009) 1673-1706
63. Glaser C.B., Morser J., Clarke J.H., Blasko E., McLean K., Kuhn I., Chang R.J., Lin J.H., Vilander L., Andrews W.H., et al. Oxidation of a specific methionine in thrombomodulin by activated neutrophil products blocks cofactor activity: a potential rapid mechanism for modulation of coagulation. J. Clin. Invest. 90 (1992) 2565-2573
64. Wood M.J., Becvar L.A., Prieto J.H., Melacini G., and Komives E.A. NMR structures reveal how oxidation inactivates thrombomodulin. Biochemistry 42 (2003) 11932-11942
65. Shacter E., Williams J.A., and Levine R.L. Oxidative modification of fibrinogen inhibits thrombin-catalyzed clot formation. Free Radic. Biol. Med. 18 (1995) 815-821
66. 2-chloride system: structural and functional effects. Thromb. Haemostasis 83 (2000) 253-261
67. Lawrence D.A., and Loskutoff D.J. Inactivation of plasminogen activator inhibitor by oxidants. Biochemistry 25 (1986) 6351-6355
68. Stief T.W., Aab A., and Heimburger N. Oxidative inactivation of purified human alpha-2-antiplasmin, antithrombin III, and C1-inhibitor. Thromb. Res. 49 (1988) 581-589
69. Macfadyen A.J., Reiter C., Zhuang Y., and Beckman J.S. A novel superoxide dismutase-based trap for peroxynitrite used to detect entry of peroxynitrite into erythrocyte ghosts. Chem. Res. Toxicol. 12 (1999) 223-229
70. Pacher P., Beckman J.S., and Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 87 (2007) 315-424
71. Chen, J.; Fu, X.; Wang, Y.; Ling, M.; McMullen, B.; Kulman, J.; Chung, D.W.; Lopez, J.A. Oxidative modification of von Willebrand factor by neutrophil oxidants inhibits its cleavage by ADAMTS13. Blood in press, doi:10.1182/blood-2009-03-213967.
72. Raife T.J., Cao W., Atkinson B.S., Bedell B., Montgomery R.R., Lentz S.R., Johnson G.F., and Zheng X.L. Leukocyte proteases cleave von Willebrand factor at or near the ADAMTS13 cleavage site. Blood 114 (2009) 1666-1674
73. Ogawa H., Nakayama M., Morimoto T., Uemura S., Kanauchi M., Doi N., Jinnouchi H., Sugiyama S., and Saito Y. Low-dose aspirin for primary prevention of atherosclerotic events in patients with type 2 diabetes: a randomized controlled trial. JAMA 300 (2008) 2134-2141
74. Anfossi G., Russo I., and Trovati M. Resistance to aspirin and thienopyridines in diabetes mellitus and metabolic syndrome. Curr. Vasc. Pharmacol. 6 (2008) 313-328
75. Ando K., and Fujita T. Metabolic syndrome and oxidative stress. Free Radic. Biol. Med. 47 (2009) 213-218
76. Yin H., Liu J., Li Z., Berndt M.C., Lowell C.A., and Du X. Src family tyrosine kinase Lyn mediates VWF/GPIb-IX-induced platelet activation via the cGMP signaling pathway. Blood 112 (2008) 1139-1146
77. Yin H., Stojanovic A., Hay N., and Du X. The role of Akt in the signaling pathway of the glycoprotein Ib-IX induced platelet activation. Blood 111 (2008) 658-665