Regulation of thrombosis and vascular function by protein methionine oxidation

Blood

Volumn 125, Issue 25, 2015, Pages 3851-3859

  Gu, Sean X ^a   Stevens, Jeff W ^a   Lentz, Steven R ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN A1; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; METHIONINE; METHIONINE SULFOXIDE; METHIONINE SULFOXIDE REDUCTASE; THROMBOMODULIN; VON WILLEBRAND FACTOR; PROTEIN; REACTIVE OXYGEN METABOLITE;

CARDIOVASCULAR FUNCTION; HUMAN; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; REVIEW; THROMBOSIS; VASCULAR DISEASE; ANIMAL; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY;

ANIMALS; HUMANS; METHIONINE; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEINS; REACTIVE OXYGEN SPECIES; THROMBOSIS; VASCULAR DISEASES;

EID: 84934905054     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2015-01-544676     Document Type: Review

References (106)

1. Taniyama Y, Griendling KK. Reactive oxygen species in the vasculature: molecular and cellular mechanisms. Hypertension. 2003;42(6):1075-1081.
2. Kim YW, Byzova TV. Oxidative stress in angiogenesis and vascular disease. Blood. 2014;123(5):625-631.
3. Dikalov SI, Harrison DG. Methods for detection of mitochondrial and cellular reactive oxygen species. Antioxid Redox Signal. 2014;20(2): 372-382.
4. Sugamura K, Keaney JF Jr. Reactive oxygen species in cardiovascular disease. Free Radic Biol Med. 2011;51(5):978-992.
5. Sesso HD, Buring JE, Christen WG, et al. Vitamins E and C in the prevention of cardiovascular disease in men: the Physicians' Health Study II randomized controlled trial. JAMA. 2008;300(18):2123-2133.
6. Cook NR, Albert CM, Gaziano JM, et al. A randomized factorial trial of vitamins C and E and beta carotene in the secondary prevention of cardiovascular events in women: results from the Women's Antioxidant Cardiovascular Study. Arch Intern Med. 2007;167(15):1610-1618.
7. Mueller CF, Laude K, McNally JS, Harrison DG. ATVB in focus: redox mechanisms in blood vessels. Arterioscler Thromb Vasc Biol. 2005;25(2):274-278.
8. Thomas SR, Witting PK, Drummond GR. Redox control of endothelial function and dysfunction: molecular mechanisms and therapeutic opportunities. Antioxid Redox Signal. 2008;10(10):1713-1765.
9. Buettner GR. The pecking order of free radicals and antioxidants: lipid peroxidation, alpha-tocopherol, and ascorbate. Arch Biochem Biophys. 1993;300(2):535-543.
10. Reczek CR, Chandel NS. ROS-dependent signal transduction. Curr Opin Cell Biol. 2015;33:8-13.
11. Burgoyne JR, Oka S, Ale-Agha N, Eaton P. Hydrogen peroxide sensing and signaling by protein kinases in the cardiovascular system. Antioxid Redox Signal. 2013;18(9):1042-1052.
12. Kim G, Weiss SJ, Levine RL. Methionine oxidation and reduction in proteins. Biochim Biophys Acta. 2014;1840(2):901-905.
13. Black SD, Mould DR. Development of hydrophobicity parameters to analyze proteins which bear post- or cotranslational modifications. Anal Biochem. 1991;193(1):72-82.
14. Chao CC, Ma YS, Stadtman ER. Modification of protein surface hydrophobicity and methionine oxidation by oxidative systems. Proc Natl Acad Sci USA. 1997;94(7):2969-2974.
15. Hoshi T, Heinemann S. Regulation of cell function by methionine oxidation and reduction. J Physiol. 2001;531(Pt 1):1-11.
16. Kim HY, Gladyshev VN. Methionine sulfoxide reductases: selenoprotein forms and roles in antioxidant protein repair in mammals. Biochem J. 2007;407(3):321-329.
17. Lee BC, Dikiy A, Kim HY, Gladyshev VN. Functions and evolution of selenoprotein methionine sulfoxide reductases. Biochim Biophys Acta. 2009;1790(11):1471-1477.
18. St John G, Brot N, Ruan J, et al. Peptide methionine sulfoxide reductase from Escherichia coli and Mycobacterium tuberculosis protects bacteria against oxidative damage from reactive nitrogen intermediates. Proc Natl Acad Sci USA. 2001;98(17):9901-9906.
19. Moskovitz J, Bar-Noy S, Williams WM, Requena J, Berlett BS, Stadtman ER. Methionine sulfoxide reductase (MsrA) is a regulator of antioxidant defense and lifespan in mammals. Proc Natl Acad Sci USA. 2001;98(23):12920-12925.
20. De Luca A, Sanna F, Sallese M, et al. Methionine sulfoxide reductase A down-regulation in human breast cancer cells results in a more aggressive phenotype. Proc Natl Acad Sci USA. 2010;107(43):18628-18633.
21. Lee BC, Péterfi Z, Hoffmann FW, et al. MsrB1 and MICALs regulate actin assembly and macrophage function via reversible stereoselective methionine oxidation. Mol Cell. 2013;51(3):397-404.
22. Butterfield DA, Galvan V, Lange MB, et al. In vivo oxidative stress in brain of Alzheimer disease transgenic mice: Requirement for methionine 35 in amyloid beta-peptide of APP. Free Radic Biol Med. 2010;48(1):136-144.
23. Nan C, Li Y, Jean-Charles PY, et al. Deficiency of methionine sulfoxide reductase A causes cellular dysfunction and mitochondrial damage in cardiac myocytes under physical and oxidative stresses. Biochem Biophys Res Commun. 2010;402(4):608-613.
24. Prentice HM, Moench IA, Rickaway ZT, Dougherty CJ, Webster KA, Weissbach H. MsrA protects cardiac myocytes against hypoxia/reoxygenation induced cell death. Biochem Biophys Res Commun. 2008;366(3):775-778.
25. Zhao H, Sun J, Deschamps AM, et al. Myristoylated methionine sulfoxide reductase A protects the heart from ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol. 2011;301(4):H1513-H1518.
26. García-Bermúdez M, López-Mejías R, González-Juanatey C, et al. Association of the methionine sulfoxide reductase A rs10903323 gene polymorphism with cardiovascular disease in patients with rheumatoid arthritis. Scand J Rheumatol. 2012;41(5):350-353.
27. Gu H, Chen W, Yin J, Chen S, Zhang J, Gong J. Methionine sulfoxide reductase A rs10903323 G/A polymorphism is associated with increased risk of coronary artery disease in a Chinese population. Clin Biochem. 2013;46(16-17):1668-1672.
28. Ghesquiere B, Jonckheere V, Colaert N, et al. Redox proteomics of protein-bound methionine oxidation. Mol Cell Proteomics. 2011;10(5):M110006866.
29. Anderson ME, Brown JH, Bers DM. CaMKII in myocardial hypertrophy and heart failure. J Mol Cell Cardiol. 2011;51(4):468-473.
30. Hudmon A, Schulman H. Structure-function of the multifunctional Ca2+/calmodulin-dependent protein kinase II. Biochem J. 2002;364(Pt 3):593-611.
31. Erickson JR, Joiner ML, Guan X, et al. A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell. 2008;133(3):462-474.
32. He BJ, Joiner ML, Singh MV, et al. Oxidation of CaMKII determines the cardiotoxic effects of aldosterone. Nat Med. 2011;17(12):1610-1618.
33. Swaminathan PD, Purohit A, Soni S, et al. Oxidized CaMKII causes cardiac sinus node dysfunction in mice. J Clin Invest. 2011;121(8):3277-3288.
34. Purohit A, Rokita AG, Guan X, et al. Oxidized Ca(2+)/calmodulin-dependent protein kinase II triggers atrial fibrillation. Circulation. 2013;128(16):1748-1757.
35. Luo M, Guan X, Luczak ED, et al. Diabetes increases mortality after myocardial infarction by oxidizing CaMKII. J Clin Invest. 2013;123(3):1262-1274.
36. House SJ, Singer HA. CaMKII-delta isoform regulation of neointima formation after vascular injury. Arterioscler Thromb Vasc Biol. 2008;28(3):441-447.
37. Singer HA. Ca2+/calmodulin-dependent protein kinase II function in vascular remodelling. J Physiol. 2012;590(Pt 6):1349-1356.
38. Papaharalambus CA, Griendling KK. Basic mechanisms of oxidative stress and reactive oxygen species in cardiovascular injury. Trends Cardiovasc Med. 2007;17(2):48-54.
39. Scott JA, Xie L, Li H, et al. The multifunctional Ca2+/calmodulin-dependent kinase II regulates vascular smooth muscle migration through matrix metalloproteinase 9. Am J Physiol Heart Circ Physiol. 2012;302(10):H1953-H1964.
40. Zhu LJ, Klutho PJ, Scott JA, et al. Oxidative activation of the Ca(2+)/calmodulin-dependent protein kinase II (CaMKII) regulates vascular smooth muscle migration and apoptosis. Vascul Pharmacol. 2014;60(2):75-83.
41. Sanders PN, Koval OM, Jaffer OA, et al. CaMKII is essential for the proasthmatic effects of oxidation. Sci Transl Med. 2013;5(195):195ra197.
42. Fielding CJ, Fielding PE. Molecular physiology of reverse cholesterol transport. J Lipid Res. 1995;36(2):211-228.
43. Garner B, Witting PK, Waldeck AR, Christison JK, Raftery M, Stocker R. Oxidation of high density lipoproteins. I. Formation of methionine sulfoxide in apolipoproteins AI and AII is an early event that accompanies lipid peroxidation and can be enhanced by alpha-tocopherol. J Biol Chem. 1998;273(11):6080-6087.
44. Garner B, Waldeck AR, Witting PK, Rye KA, Stocker R. Oxidation of high density lipoproteins. II. Evidence for direct reduction of lipid hydroperoxides by methionine residues of apolipoproteins AI and AII. J Biol Chem. 1998;273(11):6088-6095.
45. Shao B, Oda MN, Bergt C, et al. Myeloperoxidase impairs ABCA1-dependent cholesterol efflux through methionine oxidation and site-specific tyrosine chlorination of apolipoprotein A-I. J Biol Chem. 2006;281(14):9001-9004.
46. Shao B, Cavigiolio G, Brot N, Oda MN, Heinecke JW. Methionine oxidation impairs reverse cholesterol transport by apolipoprotein A-I. Proc Natl Acad Sci USA. 2008;105(34):12224-12229.
47. Shao B, Tang C, Sinha A, et al. Humans with atherosclerosis have impaired ABCA1 cholesterol efflux and enhanced high-density lipoprotein oxidation by myeloperoxidase. Circ Res. 2014;114(11):1733-1742.
48. Martin FA, Murphy RP, Cummins PM. Thrombomodulin and the vascular endothelium: insights into functional, regulatory, and therapeutic aspects. Am J Physiol Heart Circ Physiol. 2013;304(12):H1585-H1597.
49. Esmon CT. Thrombomodulin as a model of molecular mechanisms that modulate protease specificity and function at the vessel surface. FASEB J. 1995;9(10):946-955.
50. Danese S, Vetrano S, Zhang L, Poplis VA, Castellino FJ. The protein C pathway in tissue inflammation and injury: pathogenic role and therapeutic implications. Blood. 2010;115(6):1121-1130.
51. Kearon C, Crowther M, Hirsh J. Management of patients with hereditary hypercoagulable disorders. Annu Rev Med. 2000;51:169-185.
52. Goldenberg NA, Manco-Johnson MJ. Protein C deficiency. Haemophilia. 2008;14(6):1214-1221.
53. Seehaus S, Shahzad K, Kashif M, et al. Hypercoagulability inhibits monocyte transendothelial migration through protease-activated receptor-1-, phospholipase-Cbeta-, phosphoinositide 3-kinase-, and nitric oxide-dependent signaling in monocytes and promotes plaque stability. Circulation. 2009;120(9):774-784.
54. Zlokovic BV, Griffin JH. Cytoprotective protein C pathways and implications for stroke and neurological disorders. Trends Neurosci. 2011;34(4):198-209.
55. Isermann B, Hendrickson SB, Zogg M, et al. Endothelium-specific loss of murine thrombomodulin disrupts the protein C anticoagulant pathway and causes juvenile-onset thrombosis. J Clin Invest. 2001;108(4):537-546.
56. Wood MJ, Sampoli Benitez BA, Komives EA. Solution structure of the smallest cofactor-active fragment of thrombomodulin. Nat Struct Biol. 2000;7(3):200-204.
57. Glaser CB, Morser J, Clarke JH, 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. 1992;90(6):2565-2573.
58. Prieto JH, Sampoli Benitez BA, Melacini G, Johnson DA, Wood MJ, Komives EA. Dynamics of the fragment of thrombomodulin containing the fourth and fifth epidermal growth factor-like domains correlate with function. Biochemistry. 2005;44(4):1225-1233.
59. Clarke JH, Light DR, Blasko E, et al. The short loop between epidermal growth factor-like domains 4 and 5 is critical for human thrombomodulin function. J Biol Chem. 1993;268(9):6309-6315.
60. Wood MJ, Becvar LA, Prieto JH, Melacini G, Komives EA. NMR structures reveal how oxidation inactivates thrombomodulin. Biochemistry. 2003;42(41):11932-11942.
61. Lentz SR, Fernández JA, Griffin JH, et al. Impaired anticoagulant response to infusion of thrombin in atherosclerotic monkeys associated with acquired defects in the protein C system. Arterioscler Thromb Vasc Biol. 1999;19(7):1744-1750.
62. Lentz SR, Miller FJ Jr, Piegors DJ, et al. Anticoagulant responses to thrombin are enhanced during regression of atherosclerosis in monkeys. Circulation. 2002;106(7):842-846.
63. Wilson KM, McCaw RB, Leo L, et al. Prothrombotic effects of hyperhomocysteinemia and hypercholesterolemia in ApoE-deficient mice. Arterioscler Thromb Vasc Biol. 2007;27(1):233-240.
64. Raife TJ, Dwyre DM, Stevens JW, et al. Human thrombomodulin knock-in mice reveal differential effects of human thrombomodulin on thrombosis and atherosclerosis. Arterioscler Thromb Vasc Biol. 2011;31(11):2509-2517.
65. Wilson KM, Leo L, Lentz SR. Gene transfer of human ECSOD enhances protein C activation in hypercholesterolemic mice. Arterioscler Thromb Vasc Biol. 2009;29(7):e8.
66. Dayal S, Gu S. X.; Wilson, K.M., Hutchins, R.; Lentz, S.R. Endogenous superoxide dismutase protects from impaired generation of activated protein C and enhanced susceptibility to experimental thrombosis in mice. Arterioscler Thromb Vasc Biol. 2014;34(Suppl 1):A34.
67. Nalian A, Iakhiaev AV. Possible mechanisms contributing to oxidative inactivation of activated protein C: molecular dynamics study. Thromb Haemost. 2008;100(1):18-25.
68. Denis CV. Molecular and cellular biology of von Willebrand factor. Int J Hematol. 2002;75(1):3-8.
69. Sadler JE. New concepts in von Willebrand disease. Annu Rev Med. 2005;56:173-191.
70. Sadler JE. Von Willebrand factor, ADAMTS13, and thrombotic thrombocytopenic purpura. Blood. 2008;112(1):11-18.
71. George JN, Nester CM. Syndromes of thrombotic microangiopathy. N Engl J Med. 2014;371(19):1847-1848.
72. Hanson E, Jood K, Nilsson S, Blomstrand C, Jern C. Association between genetic variation at the ADAMTS13 locus and ischemic stroke. J Thromb Haemost. 2009;7(12):2147-2148.
73. Miura M, Kaikita K, Matsukawa M, et al. Prognostic value of plasma von Willebrand factor-cleaving protease (ADAMTS13) antigen levels in patients with coronary artery disease. Thromb Haemost. 2010;103(3):623-629.
74. Furlan M, Robles R, Lämmle B. Partial purification and characterization of a protease from human plasma cleaving von Willebrand factor to fragments produced by in vivo proteolysis. Blood. 1996;87(10):4223-4234.
75. Chen J, Fu X, Wang Y, et al. Oxidative modification of von Willebrand factor by neutrophil oxidants inhibits its cleavage by ADAMTS13. Blood. 2010;115(3):706-712.
76. Lancellotti S, De Filippis V, Pozzi N, et al. 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 Radic Biol Med. 2010;48(3):446-456.
77. Fu X, Chen J, Gallagher R, Zheng Y, Chung DW, López JA. Shear stress-induced unfolding of VWF accelerates oxidation of key methionine residues in the A1A2A3 region. Blood. 2011;118(19):5283-5291.
78. Chen J, Ling M, Fu X, López JA, Chung DW. Simultaneous exposure of sites in von Willebrand factor for glycoprotein Ib binding and ADAMTS13 cleavage: studies with ristocetin. Arterioscler Thromb Vasc Biol. 2012;32(11):2625-2630.
79. De Filippis V, Lancellotti S, Maset F, et al. Oxidation of Met1606 in von Willebrand factor is a risk factor for thrombotic and septic complications in chronic renal failure. Biochem J. 2012;442(2):423-432.
80. Wang Y, Chen J, Ling M, López JA, Chung DW, Fu X. Hypochlorous acid generated by neutrophils inactivates ADAMTS13: an oxidative mechanism for regulating ADAMTS13 proteolytic activity during inflammation. J Biol Chem. 2015;290(3):1422-1431.
81. Raife TJ, Cao W, Atkinson BS, et al. Leukocyte proteases cleave von Willebrand factor at or near the ADAMTS13 cleavage site. Blood. 2009;114(8):1666-1674.
82. Lancellotti S, De Filippis V, Pozzi N, et al. Oxidized von Willebrand factor is efficiently cleaved by serine proteases from primary granules of leukocytes: divergence from ADAMTS-13. J Thromb Haemost. 2011;9(8):1620-1627.
83. Taggart C, Cervantes-Laurean D, Kim G, et al. Oxidation of either methionine 351 or methionine 358 in alpha 1-antitrypsin causes loss of antineutrophil elastase activity. J Biol Chem. 2000;275(35):27258-27265.
84. Weigandt KM, White N, Chung D, et al. Fibrin clot structure and mechanics associated with specific oxidation of methionine residues in fibrinogen. Biophys J. 2012;103(11):2399-2407.
85. Burney PR, White N, Pfaendtner J. Structural effects of methionine oxidation on isolated subdomains of human fibrin D and αC regions. PLoS ONE. 2014;9(1):e86981.
86. Stief TW, Martín E, Jimenez J, Digón J, Rodriguez JM. Effect of oxidants on proteases of the fibrinolytic system: possible role for methionine residues in the interaction between tissue type plasminogen activator and fibrin. Thromb Res. 1991;61(3):191-200.
87. Lawrence DA, Loskutoff DJ. Inactivation of plasminogen activator inhibitor by oxidants. Biochemistry. 1986;25(21):6351-6355.
88. Strandberg L, Lawrence DA, Johansson LB, Ny T. The oxidative inactivation of plasminogen activator inhibitor type 1 results from a conformational change in the molecule and does not require the involvement of the P1′ methionine. J Biol Chem. 1991;266(21):13852-13858.
89. Kornfelt T, Persson E, Palm L. Oxidation of methionine residues in coagulation factor VIIa. Arch Biochem Biophys. 1999;363(1):43-54.
90. Stief TW, Aab A, Heimburger N. Oxidative inactivation of purified human alpha-2-antiplasmin, antithrombin III, and C1-inhibitor. Thromb Res. 1988;49(6):581-589.
91. Van Patten SM, Hanson E, Bernasconi R, et al. Oxidation of methionine residues in antithrombin. Effects on biological activity and heparin binding. J Biol Chem. 1999;274(15):10268-10276.
92. Sroussi HY, Berline J, Palefsky JM. Oxidation of methionine 63 and 83 regulates the effect of S100A9 on the migration of neutrophils in vitro. J Leukoc Biol. 2007;81(3):818-824.
93. Hung RJ, Spaeth CS, Yesilyurt HG, Terman JR. SelR reverses Mical-mediated oxidation of actin to regulate F-actin dynamics. Nat Cell Biol. 2013;15(12):1445-1454.
94. Kanayama A, Inoue J, Sugita-Konishi Y, Shimizu M, Miyamoto Y. Oxidation of Ikappa Balpha at methionine 45 is one cause of taurine chloramine-induced inhibition of NF-kappa B activation. J Biol Chem. 2002;277(27):24049-24056.
95. Midwinter RG, Cheah FC, Moskovitz J, Vissers MC, Winterbourn CC. IkappaB is a sensitive target for oxidation by cell-permeable chloramines: inhibition of NF-kappaB activity by glycine chloramine through methionine oxidation. Biochem J. 2006;396(1):71-78.
96. Nomura T, Kamada R, Ito I, Chuman Y, Shimohigashi Y, Sakaguchi K. Oxidation of methionine residue at hydrophobic core destabilizes p53 tetrameric structure. Biopolymers. 2009;91(1):78-84.
97. Schieber M, Chandel NS. ROS function in redox signaling and oxidative stress. Curr Biol. 2014;24(10):R453-R462.
98. Oien DB, Canello T, Gabizon R, et al. Detection of oxidized methionine in selected proteins, cellular extracts and blood serums by novel anti-methionine sulfoxide antibodies. Arch Biochem Biophys. 2009;485(1):35-40.
99. Ghesquière B, Gevaert K. Proteomics methods to study methionine oxidation. Mass Spectrom Rev. 2014;33(2):147-156.
100. Gevaert K, Ghesquière B, Staes A, et al. Reversible labeling of cysteine-containing peptides allows their specific chromatographic isolation for non-gel proteome studies. Proteomics. 2004;4(4):897-908.
101. Seraglia R, Sartore G, Marin R, et al. An effective and rapid determination by MALDI/TOF/TOF of methionine sulphoxide content of ApoA-I in type 2 diabetic patients. J Mass Spectrom. 2013;48(1):105-110.
102. Oggianu L, Lancellotti S, Pitocco D, et al. The oxidative modification of von Willebrand factor is associated with thrombotic angiopathies in diabetes mellitus. PLoS ONE. 2013;8(1):e55396.
103. Su EJ, Geyer M, Wahl M, et al. The thrombomodulin analog Solulin promotes reperfusion and reduces infarct volume in a thrombotic stroke model. J Thromb Haemost. 2011;9(6):1174-1182.
104. Carnemolla R, Greineder CF, Chacko AM, et al. Platelet endothelial cell adhesion molecule targeted oxidant-resistant mutant thrombomodulin fusion protein with enhanced potency in vitro and in vivo. J Pharmacol Exp Ther. 2013;347(2):339-345.
105. van Iersel T, Stroissnig H, Giesen P, Wemer J, Wilhelm-Ogunbiyi K. Phase I study of Solulin, a novel recombinant soluble human thrombomodulin analogue. Thromb Haemost. 2011;105(2):302-312.
106. Hood ED, Chorny M, Greineder CF, S Alferiev I, Levy RJ, Muzykantov VR. Endothelial targeting of nanocarriers loaded with antioxidant enzymes for protection against vascular oxidative stress and inflammation. Biomaterials. 2014;35(11):3708-3715.