Does the oxidation of methionine in thrombomodulin contribute to the hypercoaguable state of smokers and diabetics?

Medical Hypotheses

Volumn 68, Issue 4, 2007, Pages 811-821

  Stites, Wesley E ^a   Froude II, Jeffrey W ^a  

^a UNIVERSITY OF ARKANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METHIONINE; THROMBOMODULIN;

ARTICLE; DIABETES MELLITUS; DISEASE PREDISPOSITION; HEMOSTASIS; HUMAN; HYPERCOAGULABILITY; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; SMOKING; THROMBOSIS;

AMINO ACID SEQUENCE; BLOOD COAGULATION; CARDIOVASCULAR DISEASES; DIABETES MELLITUS; HEMOSTASIS; HUMANS; METHIONINE; MODELS, CHEMICAL; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; OXYGEN; PROTEIN C; SMOKING; THROMBOMODULIN;

EID: 33846369728     PISSN: 03069877     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mehy.2006.09.009     Document Type: Article

References (162)

1. Ambrose J.A., and Barua R.S. The pathophysiology of cigarette smoking and cardiovascular disease: an update. J Am Coll Cardiol 43 (2004) 1731-1737
2. Burns D.M. Epidemiology of smoking-induced cardiovascular disease. Prog Cardiovasc Dis 46 (2003) 11-29
3. Dunn E.J., and Grant P.J. Type 2 diabetes: an atherothrombotic syndrome. Curr Mol Med 5 (2005) 323-332
4. Aras R., Sowers J.R., and Arora R. The proinflammatory and hypercoagulable state of diabetes mellitus. Rev Cardiovasc Med 6 (2005) 84-97
5. Carr M.E. Diabetes mellitus: a hypercoagulable state. J Diabetes Complications 15 (2001) 44-54
6. Dahlback B. Blood coagulation and its regulation by anticoagulant pathways: genetic pathogenesis of bleeding and thrombotic diseases. J Int Med 257 (2005) 209-223
7. Davidson C.J., Tuddenham E.G., and McVey J.H. 450 million years of hemostasis. J Thromb Haemost 1 (2003) 1487-1494
8. Norris L.A. Blood coagulation. Best Pract Res Clin Obstet Gynaecol 17 (2003) 369-383
9. Lasne D., Jude B., and Susen S. From normal to pathological hemostasis. Can J Anaesth 53 (2006) S2-S11
10. Monroe D.M., and Hoffman M. What does it take to make the perfect clot?. Arterioscler Thromb Vasc Biol 26 (2006) 41-48
11. Schenone M., Furie B.C., and Furie B. The blood coagulation cascade. Curr Opin Hematol 11 (2004) 272-277
12. Wu K.K., and Matijevic-Aleksic N. Thrombomodulin: a linker of coagulation and fibrinolysis and predictor of risk of arterial thrombosis. Ann Med 32 Suppl. 1 (2000) 73-77
13. Weiler H., and Isermann B.H. Thrombomodulin. J Thromb Haemost 1 (2003) 1515-1524
14. van de Wouwer M., Collen D., and Conway E.M. Thrombomodulin-protein C-EPCR system: integrated to regulate coagulation and inflammation. Arterioscler Thromb Vasc Biol 24 (2004) 1374-1383
15. Esmon C.T. Crosstalk between inflammation and thrombosis. Maturitas 47 (2004) 305-314
16. Owen W.G., and Esmon C.T. Functional properties of an endothelial cell cofactor for thrombin-catalyzed activation of protein C. J Biol Chem 256 (1981) 5532-5535
17. Esmon C.T. The protein C pathway. Chest 124 (2003) 26S-32S
18. Espana F., Medina P., Navarro S., Estelles A., and Aznar J. Inherited abnormalities in the protein C activation pathway. Pathophysiol Haemost Thromb 32 (2002) 241-244
19. Salomaa V., Matei C., Aleksic N., et al. Soluble thrombomodulin as a predictor of incident coronary heart disease and symptomless carotid artery atherosclerosis in the Atherosclerosis Risk in Communities (ARIC) Study: a case-cohort study. Lancet 353 (1999) 1729-1734
20. Mosnier L.O., Meijers J.C., and Bouma B.N. Regulation of fibrinolysis in plasma by TAFI and protein C is dependent on the concentration of thrombomodulin. Thromb Haemost 85 (2001) 5-11
21. Nesheim M. Thrombin and fibrinolysis. Chest 124 (2003) 33S-39S
22. Nesheim M., Wang W., Boffa M., Nagashima M., Morser J., and Bajzar L. Thrombin, thrombomodulin and TAFI in the molecular link between coagulation and fibrinolysis. Thromb Haemost 78 (1997) 386-391
23. Marx P.F. Thrombin-activatable fibrinolysis inhibitor. Curr Med Chem 11 (2004) 2335-2348
24. Bajzar L., Morser J., and Nesheim M. TAFI, or plasma procarboxypeptidase B, couples the coagulation and fibrinolytic cascades through the thrombin-thrombomodulin complex. J Biol Chem 271 (1996) 16603-16608
25. Song Y.K., Liu D., Maruyama K.Z., and Takizawa T. Antibody mediated lung targeting of long-circulating emulsions. PDA J Pharm Sci Technol 50 (1996) 372-377
26. Ford V.A., Stringer C., and Kennel S.J. Thrombomodulin is preferentially expressed in Balb/c lung microvessels. J Biol Chem 267 (1992) 5446-5450
27. Ishii H., and Majerus P.W. Thrombomodulin is present in human plasma and urine. J Clin Invest 76 (1985) 2178-2181
28. Boffa M.C., and Karmochkine M. Thrombomodulin: an overview and potential implications in vascular disorders. Lupus 7 Suppl. 2 (1998) S120-S125
29. Ishii H., Uchiyama H., and Kazama M. Soluble thrombomodulin antigen in conditioned medium is increased by damage of endothelial cells. Thromb Haemost 65 (1991) 618-623
30. Blann A.D., and McCollum C.N. von Willebrand factor and soluble thrombomodulin as predictors of adverse events among subjects with peripheral or coronary atherosclerosis. Blood Coagul Fibrinolysis 10 (1999) 375-380
31. Blann A.D., McCollum C.N., and Lip G.Y. Relationship between plasma markers of endothelial cell integrity and the Framingham cardiovascular disease risk-factor scores in apparently healthy individuals. Blood Coagul Fibrinolysis 13 (2002) 513-518
32. Nilsson T.K., Hellsten G., and Amiral J. Plasma thrombomodulin concentrations in relation to cardiovascular risk factors in a population sample. Blood Coagul Fibrinolysis 4 (1993) 455-458
33. Glaser C.B., Morser J., Clarke J.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
34. 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
35. Fuentes-Prior P., Iwanaga Y., Huber R., et al. Structural basis for the anticoagulant activity of the thrombin-thrombomodulin complex. Nature 404 (2000) 518-525
36. Wood M.J., Sampoli Benitez B.A., and Komives E.A. Solution structure of the smallest cofactor-active fragment of thrombomodulin. Nat Struct Biol 7 (2000) 200-204
37. Nagashima M., Lundh E., Leonard J.C., Morser J., and Parkinson J.F. Alanine-scanning mutagenesis of the epidermal growth factor-like domains of human thrombomodulin identifies critical residues for its cofactor activity. J Biol Chem 268 (1993) 2888-2892
38. Sadler J.E., Lentz S.R., Sheehan J.P., Tsiang M., and Wu Q. Structure-function relationships of the thrombin-thrombomodulin interaction. Haemostasis 23 Suppl. 1 (1993) 183-193
39. White C.E., Hunter M.J., Meininger D.P., White L.R., and Komives E.A. Large-scale expression, purification and characterization of small fragments of thrombomodulin: the roles of the sixth domain and of methionine 388. Protein Eng 8 (1995) 1177-1187
40. Schenk-Braat E.A., Morser J., and Rijken D.C. Identification of the epidermal growth factor-like domains of thrombomodulin essential for the acceleration of thrombin-mediated inactivation of single-chain urokinase-type plasminogen activator. Eur J Biochem 268 (2001) 5562-5569
41. Brot N., and Weissbach H. Biochemistry of methionine sulfoxide residues in proteins. Biofactors 3 (1991) 91-96
42. Drozdz R., and Naskalski J.W. Inactivation and denaturation of some proteins by enzyme system: myeloperoxidase, chloride and hydrogen peroxide. Folia Histochem Cytobiol 31 (1993) 71-75
43. Stadtman E.R., and Levine R.L. Protein oxidation. Ann N Y Acad Sci 899 (2000) 191-208
44. Naskalski J.W., Marcinkiewicz J., and Drozdz R. Myeloperoxidase-mediated protein oxidation: its possible biological functions. Clin Chem Lab Med 40 (2002) 463-468
45. Levine R.L., Moskovitz J., and Stadtman E.R. Oxidation of methionine in proteins: roles in antioxidant defense and cellular regulation. IUBMB Life 50 (2000) 301-307
46. Vogt W., Damerau B., von Zabern I., Nolte R., and Brunahl D. Non-enzymic activation of the fifth component of human complement, by oxygen radicals. Some properties of the activation product, C5b-like C5. Mol Immunol 26 (1989) 1133-1142
47. Vogt W., and Hesse D. Oxidants generated by the myeloperoxidase-halide system activate the fifth component of human complement, C5. Immunobiology 192 (1994) 1-9
48. Discipio R.G., Daffern P.J., Kawahara M., et al. Cleavage of human complement component C5 by cysteine proteinases from Porphyromonas (Bacteroides) gingivalis. Prior oxidation of C5 augments proteinase digestion of C5. Immunology 87 (1996) 660-667
49. Wang W., Nagashima M., Schneider M., Morser J., and Nesheim M. Elements of the primary structure of thrombomodulin required for efficient thrombin-activable fibrinolysis inhibitor activation. J Biol Chem 275 (2000) 22942-22947
50. Wood M.J., Helena Prieto J., and Komives E.A. Structural and functional consequences of methionine oxidation in thrombomodulin. Biochim Biophys Acta 1703 (2005) 141-147
51. Opal S.M. Interactions between coagulation and inflammation. Scand J Infect Dis 35 (2003) 545-554
52. Esmon C.T. Does inflammation contribute to thrombotic events?. Haemostasis 30 Suppl. 2 (2000) 34-40
53. Esmon C.T. Protein C pathway in sepsis. Ann Med 34 (2002) 598-605
54. Weiler-Guettler H., Christie P.D., Beeler D.L., et al. A targeted point mutation in thrombomodulin generates viable mice with a prethrombotic state. J Clin Invest 101 (1998) 1983-1991
55. Christie P.D., Edelberg J.M., Picard M.H., et al. A murine model of myocardial microvascular thrombosis. J Clin Invest 104 (1999) 533-539
56. Nesheim M. Myocardial infarction and the balance between fibrin deposition and removal. Ital Heart J 2 (2001) 641-645
57. Weiler H., Lindner V., Kerlin B., et al. Characterization of a mouse model for thrombomodulin deficiency. Arterioscler Thromb Vasc Biol 21 (2001) 1531-1537
58. Dorffler-Melly J., de Kruif M., Schwarte L.A., et al. Functional thrombomodulin deficiency causes enhanced thrombus growth in a murine model of carotid artery thrombosis. Basic Res Cardiol 98 (2003) 347-352
59. Dean R.T., Fu S., Stocker R., and Davies M.J. Biochemistry and pathology of radical-mediated protein oxidation. Biochem J 324 Pt 1 (1997) 1-18
60. Stadtman E.R., Van Remmen H., Richardson A., Wehr N.B., and Levine R.L. Methionine oxidation and aging. Biochim Biophys Acta 1703 (2005) 135-140
61. Friguet B. Oxidized protein degradation and repair in ageing and oxidative stress. FEBS Lett 580 (2006) 2910-2916
62. Stadtman E.R., and Levine R.L. Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids 25 (2003) 207-218
63. 2/bicarbonate and hydrogen peroxide. Free Radic Biol Med 35 (2003) 1538-1550
64. Drozdz R., Naskalski J.W., and Sznajd J. Oxidation of amino acids and peptides in reaction with myeloperoxidase, chloride and hydrogen peroxide. Biochim Biophys Acta 957 (1988) 47-52
65. Carr A.C., Hawkins C.L., Thomas S.R., Stocker R., and Frei B. Relative reactivities of N-chloramines and hypochlorous acid with human plasma constituents. Free Radic Biol Med 30 (2001) 526-536
66. Peskin A.V., and Winterbourn C.C. Kinetics of the reactions of hypochlorous acid and amino acid chloramines with thiols, methionine, and ascorbate. Free Radic Biol Med 30 (2001) 572-579
67. Hong J., and Schoneich C. The metal-catalyzed oxidation of methionine in peptides by Fenton systems involves two consecutive one-electron oxidation processes. Free Radic Biol Med 31 (2001) 1432-1441
68. Gadek J.E., Fells G.A., and Crystal R.G. Cigarette smoking induces functional antiprotease deficiency in the lower respiratory tract of humans. Science 206 (1979) 1315-1316
69. Boudier C., Pelletier A., Pauli G., and Bieth J.G. The functional activity of alpha 1-proteinase inhibitor in bronchoalveolar lavage fluids from healthy human smokers and non-smokers. Clin Chim Acta 132 (1983) 309-315
70. Maier K.L., Leuschel L., and Costabel U. Increased oxidized methionine residues in BAL fluid proteins in acute or chronic bronchitis. Eur Respir J 5 (1992) 651-658
71. Evans M.D., Church D.F., and Pryor W.A. Aqueous cigarette tar extracts damage human alpha-1-proteinase inhibitor. Chem Biol Interact 79 (1991) 151-164
72. Evans M.D., and Pryor W.A. Damage to human alpha-1-proteinase inhibitor by aqueous cigarette tar extracts and the formation of methionine sulfoxide. Chem Res Toxicol 5 (1992) 654-660
73. Berlett B.S., Levine R.L., and Stadtman E.R. Comparison of the effects of ozone on the modification of amino acid residues in glutamine synthetase and bovine serum albumin. J Biol Chem 271 (1996) 4177-4182
74. Banerjee S.K., and Mudd J.B. Reaction of ozone with glycophorin in solution and in lipid vesicles. Arch Biochem Biophys 295 (1992) 84-89
75. Blaurock B., Hippeli S., Metz N., and Elstner E.F. Oxidative destruction of biomolecules by gasoline engine exhaust products and detoxifying effects of the three-way catalytic converter. Arch Toxicol 66 (1992) 681-687
76. Maier K.L., Matejkova E., Hinze H., Leuschel L., Weber H., and Beck-Speier I. Different selectivities of oxidants during oxidation of methionine residues in the alpha-1-proteinase inhibitor. FEBS Lett 250 (1989) 221-226
77. Jacob C., Giles G.I., Giles N.M., and Sies H. Sulfur and selenium: the role of oxidation state in protein structure and function. Angew Chem Int Ed Engl 42 (2003) 4742-4758
78. Dalle-Donne I., Rossi R., Giustarini D., et al. Methionine oxidation as a major cause of the functional impairment of oxidized actin. Free Radic Biol Med 32 (2002) 927-937
79. Krishnamurthy R., and Manning M.C. The stability factor: importance in formulation development. Curr Pharm Biotechnol 3 (2002) 361-371
80. Berti P.J., Ekiel I., Lindahl P., Abrahamson M., and Storer A.C. Affinity purification and elimination of methionine oxidation in recombinant human cystatin C. Protein Exp Purif 11 (1997) 111-118
81. Lam X.M., Yang J.Y., and Cleland J.L. Antioxidants for prevention of methionine oxidation in recombinant monoclonal antibody HER2. J Pharm Sci 86 (1997) 1250-1255
82. Fransson J., Florin-Robertsson E., Axelsson K., and Nyhlen C. Oxidation of human insulin-like growth factor I in formulation studies: kinetics of methionine oxidation in aqueous solution and in solid state. Pharm Res 13 (1996) 1252-1257
83. Chen K., Thomas S.R., and Keaney Jr. J.F. Beyond LDL oxidation: ROS in vascular signal transduction. Free Radic Biol Med 35 (2003) 117-132
84. Stadtman E.R., and Levine R.L. Why have cells selected reactive oxygen species to regulate cell signaling events?. Hum Exp Toxicol 21 (2002) 83
85. Klotz L.O. Oxidant-induced signaling: effects of peroxynitrite and singlet oxygen. Biol Chem 383 (2002) 443-456
86. Sauer H., Wartenberg M., and Hescheler J. Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell Physiol Biochem 11 (2001) 173-186
87. Griendling K.K., Sorescu D., Lassegue B., and Ushio-Fukai M. Modulation of protein kinase activity and gene expression by reactive oxygen species and their role in vascular physiology and pathophysiology. Arterioscler Thromb Vasc Biol 20 (2000) 2175-2183
88. Stadtman E.R., Moskovitz J., and Levine R.L. Oxidation of methionine residues of proteins: biological consequences. Antioxid Redox Signal 5 (2003) 577-582
89. Hoshi T., and Heinemann S. Regulation of cell function by methionine oxidation and reduction. J Physiol 531 (2001) 1-11
90. Pattison D.I., and Davies M.J. Absolute rate constants for the reaction of hypochlorous acid with protein side chains and peptide bonds. Chem Res Toxicol 14 (2001) 1453-1464
91. Moskovitz J. Methionine sulfoxide reductases: ubiquitous enzymes involved in antioxidant defense, protein regulation, and prevention of aging-associated diseases. Biochim Biophys Acta 1703 (2005) 213-219
92. Park E.M., Park Y.M., and Gwak Y.S. Oxidative damage in tissues of rats exposed to cigarette smoke. Free Radic Biol Med 25 (1998) 79-86
93. Carnevali S., Petruzzelli S., Longoni B., et al. Cigarette smoke extract induces oxidative stress and apoptosis in human lung fibroblasts. Am J Physiol Lung Cell Mol Physiol 284 (2003) L955-L963
94. Sandhir R., Subramanian S., and Koul A. Long-term smoking and ethanol exposure accentuates oxidative stress in hearts of mice. Cardiovasc Toxicol 3 (2003) 135-140
95. Burke A., and Fitzgerald G.A. Oxidative stress and smoking-induced vascular injury. Prog Cardiovasc Dis 46 (2003) 79-90
96. Alberg A. The influence of cigarette smoking on circulating concentrations of antioxidant micronutrients. Toxicology 180 (2002) 121-137
97. Panda K., Chattopadhyay R., Chattopadhyay D., and Chatterjee I.B. Cigarette smoke-induced protein oxidation and proteolysis is exclusively caused by its tar phase: prevention by vitamin C. Toxicol Lett 123 (2001) 21-32
98. Howard D.J., Ota R.B., Briggs L.A., Hampton M., and Pritsos C.A. Environmental tobacco smoke in the workplace induces oxidative stress in employees, including increased production of 8-hydroxy-2′-deoxyguanosine. Cancer Epidemiol Biomarkers Prev 7 (1998) 141-146
99. Wurzel H., Yeh C.C., Gairola C., and Chow C.K. Oxidative damage and antioxidant status in the lungs and bronchoalveolar lavage fluid of rats exposed chronically to cigarette smoke. J Biochem Toxicol 10 (1995) 11-17
100. Chow C.K. Cigarette smoking and oxidative damage in the lung. Ann N Y Acad Sci 686 (1993) 289-298
101. Cosio M.G., Majo J., and Cosio M.G. Inflammation of the airways and lung parenchyma in COPD: role of T cells. Chest 121 (2002) 160S-165S
102. Jimenez Ruiz C.A., Rajas O., Ruiz A., et al. Bronchoalveolar lavage in smokers: quantification of alveolar macrophages and neutrophils as markers of bronchial obstruction. In Vivo 12 (1998) 427-430
103. Thompson A.B., Bohling T., Heires A., Linder J., and Rennard S.I. Lower respiratory tract iron burden is increased in association with cigarette smoking. J Lab Clin Med 117 (1991) 493-499
104. Mayo J.J., Kohlhepp P., Zhang D., and Winzerling J.J. Effects of sham air and cigarette smoke on A549 lung cells: implications for iron-mediated oxidative damage. Am J Physiol Lung Cell Mol Physiol 286 (2004) L866-L876
105. Swaim M.W., and Pizzo S.V. Methionine sulfoxide and the oxidative regulation of plasma proteinase inhibitors. J Leukoc Biol 43 (1988) 365-379
106. Moraga F., and Janciauskiene S. Activation of primary human monocytes by the oxidized form of alpha1-antitrypsin. J Biol Chem 275 (2000) 7693-7700
107. Shapiro S.D. Evolving concepts in the pathogenesis of chronic obstructive pulmonary disease. Clin Chest Med 21 (2000) 621-632
108. Griffiths S.W., and Cooney C.L. Relationship between protein structure and methionine oxidation in recombinant human alpha 1-antitrypsin. Biochemistry 41 (2002) 6245-6252
109. Taggart C., Cervantes-Laurean D., Kim G., et al. Oxidation of either methionine 351 or methionine 358 in alpha 1-antitrypsin causes loss of anti-neutrophil elastase activity. J Biol Chem 275 (2000) 27258-27265
110. Pryor W.A., Dooley M.M., and Church D.F. The inactivation of alpha-1-proteinase inhibitor by gas-phase cigarette smoke: protection by antioxidants and reducing species. Chem Biol Interact 57 (1986) 271-283
111. Cox D.W., and Billingsley G.D. Oxidation of plasma alpha 1-antitrypsin in smokers and nonsmokers and by an oxidizing agent. Am Rev Respir Dis 130 (1984) 594-599
112. Hubbard R.C., Ogushi F., Fells G.A., et al. Oxidants spontaneously released by alveolar macrophages of cigarette smokers can inactivate the active site of alpha 1-antitrypsin, rendering it ineffective as an inhibitor of neutrophil elastase. J Clin Invest 80 (1987) 1289-1295
113. Churg A., Zay K., and Li K. Mechanisms of mineral dust-induced emphysema. Environ Health Perspect 105 Suppl. 5 (1997) 1215-1218
114. Nedeljkovic Z.S., Gokce N., and Loscalzo J. Mechanisms of oxidative stress and vascular dysfunction. Postgrad Med J 79 (2003) 195-199 quiz 8-200
115. Loscalzo J. Oxidative stress in endothelial cell dysfunction and thrombosis. Pathophysiol Haemost Thromb 32 (2002) 359-360
116. Viles-Gonzalez J.F., Fuster V., and Badimon J.J. Links between inflammation and thrombogenicity in atherosclerosis. Curr Mol Med 6 (2006) 489-499
117. Spronk H.M., van der Voort D., and Ten Cate H. Blood coagulation and the risk of atherothrombosis: a complex relationship. Thromb J 2 (2004) 12
118. Landmesser U., Hornig B., and Drexler H. Endothelial function: a critical determinant in atherosclerosis?. Circulation 109 (2004) II27-II33
119. Voetsch B., and Loscalzo J. Genetics of thrombophilia: impact on atherogenesis. Curr Opin Lipidol 15 (2004) 129-143
120. Ruberg F.L., and Loscalzo J. Prothrombotic determinants of coronary atherothrombosis. Vasc Med 7 (2002) 289-299
121. Christofidou-Solomidou M., Kennel S., Scherpereel A., et al. Vascular immunotargeting of glucose oxidase to the endothelial antigens induces distinct forms of oxidant acute lung injury: targeting to thrombomodulin, but not to PECAM-1, causes pulmonary thrombosis and neutrophil transmigration. Am J Pathol 160 (2002) 1155-1169
122. Fernandez J.A., Gruber A., Heeb M.J., and Griffin J.H. Protein C pathway impairment in nonsymptomatic cigarette smokers. Blood Cells Mol Dis 29 (2002) 73-82
123. Espana F., Vaya A., Mira Y., et al. Low level of circulating activated protein C is a risk factor for venous thromboembolism. Thromb Haemost 86 (2001) 1368-1373
124. Medina P., Navarro S., Estelles A., et al. Contribution of polymorphisms in the endothelial protein C receptor gene to soluble endothelial protein C receptor and circulating activated protein C levels, and thrombotic risk. Thromb Haemost 91 (2004) 905-911
125. Griffin J.H., Fernandez J.A., Liu D., Cheng T., Guo H., and Zlokovic B.V. Activated protein C and ischemic stroke. Crit Care Med 32 (2004) S247-S253
126. De Cristofaro R., Rocca B., Marchioli R., and Landolfi R. Plasma protein oxidation is associated with an increase of procoagulant markers causing an imbalance between pro- and anticoagulant pathways in healthy subjects. Thromb Haemost 87 (2002) 58-67
127. Bayele H.K., Murdock P.J., Perry D.J., and Pasi K.J. Simple shifts in redox/thiol balance that perturb blood coagulation. FEBS Lett 510 (2002) 67-70
128. Ambrosio G., Tritto I., and Golino P. Reactive oxygen metabolites and arterial thrombosis. Cardiovasc Res 34 (1997) 445-452
129. Himmelfarb J., Stenvinkel P., Ikizler T.A., and Hakim R.M. The elephant in uremia: oxidant stress as a unifying concept of cardiovascular disease in uremia. Kidney Int 62 (2002) 1524-1538
130. Obrosova I.G. How does glucose generate oxidative stress in peripheral nerve?. Int Rev Neurobiol 50 (2002) 3-35
131. Lipinski B. Pathophysiology of oxidative stress in diabetes mellitus. J Diabetes Complications 15 (2001) 203-210
132. Bonnefont-Rousselot D. Glucose and reactive oxygen species. Curr Opin Clin Nutr Metab Care 5 (2002) 561-568
133. Biondi-Zoccai G.G., Abbate A., Liuzzo G., and Biasucci L.M. Atherothrombosis, inflammation, and diabetes. J Am Coll Cardiol 41 (2003) 1071-1077
134. Banga J.D. Coagulation and fibrinolysis in diabetes. Semin Vasc Med 2 (2002) 75-86
135. Candido R., Srivastava P., Cooper M.E., and Burrell L.M. Diabetes mellitus: a cardiovascular disease. Curr Opin Investig Drugs 4 (2003) 1088-1094
136. De Cristofaro R., Rocca B., Vitacolonna E., et al. Lipid and protein oxidation contribute to a prothrombotic state in patients with type 2 diabetes mellitus. J Thromb Haemost 1 (2003) 250-256
137. Andreotti F., Burzotta F., Manzoli A., and Robinson K. Homocysteine and risk of cardiovascular disease. J Thromb Thrombolysis 9 (2000) 13-21
138. Cattaneo M. Hyperhomocysteinemia and thrombosis. Lipids 36 Suppl. (2001) S13-S26
139. Lee R., and Frenkel E.P. Hyperhomocysteinemia and thrombosis. Hematol Oncol Clin North Am 17 (2003) 85-102
140. Falk E., Zhou J., and Moller J. Homocysteine and atherothrombosis. Lipids 36 Suppl. (2001) S3-S11
141. den Heijer M., and Keijzer M.B. Hyperhomocysteinemia as a risk factor for venous thrombosis. Clin Chem Lab Med 39 (2001) 710-713
142. Herrmann W. The importance of hyperhomocysteinemia as a risk factor for diseases: an overview. Clin Chem Lab Med 39 (2001) 666-674
143. de Jong S.C., van den Berg M., Rauwerda J.A., and Stehouwer C.D. Hyperhomocysteinemia and atherothrombotic disease. Semin Thromb Hemost 24 (1998) 381-385
144. Guthikonda S., and Haynes W.G. Homocysteine: role and implications in atherosclerosis. Curr Atheroscler Rep 8 (2006) 100-106
145. Undas A., Brozek J., and Szczeklik A. Homocysteine and thrombosis: from basic science to clinical evidence. Thromb Haemost 94 (2005) 907-915
146. Olszewski A.J., and McCully K.S. Homocysteine metabolism and the oxidative modification of proteins and lipids. Free Radic Biol Med 14 (1993) 683-693
147. Widner B., Enzinger C., Laich A., Wirleitner B., and Fuchs D. Hyperhomocysteinemia, pteridines and oxidative stress. Curr Drug Metab 3 (2002) 225-232
148. Cattaneo M., Franchi F., Zighetti M.L., Martinelli I., Asti D., and Mannucci P.M. Plasma levels of activated protein C in healthy subjects and patients with previous venous thromboembolism: relationships with plasma homocysteine levels. Arterioscler Thromb Vasc Biol 18 (1998) 1371-1375
149. Gerdes V.E., Hovinga H.A., ten Cate H., et al. Homocysteine and markers of coagulation and endothelial cell activation. J Thromb Haemost 2 (2004) 445-451
150. Goswami K., Nandakumar D.N., Koner B.C., Bobby Z., and Sen S.K. Oxidative changes and desialylation of serum proteins in hyperthyroidism. Clin Chim Acta 337 (2003) 163-168
151. Bednarek J., Wysocki H., and Sowinski J. Oxidation products and antioxidant markers in plasma of patients with Graves' disease and toxic multinodular goiter: effect of methimazole treatment. Free Radic Res 38 (2004) 659-664
152. Bianchi G., Solaroli E., Zaccheroni V., et al. Oxidative stress and anti-oxidant metabolites in patients with hyperthyroidism: effect of treatment. Horm Metab Res 31 (1999) 620-624
153. Hofbauer L.C., and Heufelder A.E. Coagulation disorders in thyroid diseases. Eur J Endocrinol 136 (1997) 1-7
154. Verberne H.J., Fliers E., Prummel M.F., Stam J., Brandjes D.P., and Wiersinga W.M. Thyrotoxicosis as a predisposing factor for cerebral venous thrombosis. Thyroid 10 (2000) 607-610
155. Parker J.L., and Lawson D.H. Death from thyrotoxicosis. Lancet 302 (1973) 894-895
156. Pawlak K., Naumnik B., Brzosko S., Pawlak D., and Mysliwiec M. Oxidative stress - a link between endothelial injury, coagulation activation, and atherosclerosis in haemodialysis patients. Am J Nephrol 24 (2004) 154-161
157. Locatelli F., Canaud B., Eckardt K.U., Stenvinkel P., Wanner C., and Zoccali C. Oxidative stress in end-stage renal disease: an emerging threat to patient outcome. Nephrol Dial Transplant 18 (2003) 1272-1280
158. Casserly L.F., and Dember L.M. Thrombosis in end-stage renal disease. Semin Dial 16 (2003) 245-256
159. Jikimoto T., Nishikubo Y., Koshiba M., et al. Thioredoxin as a biomarker for oxidative stress in patients with rheumatoid arthritis. Mol Immunol 38 (2002) 765-772
160. Maradit-Kremers H., Crowson C.S., Nicola P.J., et al. Increased unrecognized coronary heart disease and sudden deaths in rheumatoid arthritis: a population-based cohort study. Arthritis Rheum 52 (2005) 402-411
161. Cheras P.A., Whitaker A.N., Blackwell E.A., Sinton T.J., Chapman M.D., and Peacock K.A. Hypercoagulability and hypofibrinolysis in primary osteoarthritis. Clin Orthop Relat Res (1997) 57-67
162. Jurcut C., Jurcut R., and Tanasescu C. Cardiovascular risk and rheumatoid arthritis: from mechanisms of atherosclerosis to therapeutic approach. Rom J Intern Med 42 (2004) 659-669