Biomarkers of Vascular Inflammation and Cardiovascular Disease

  • Paul Welsh
  • David Preiss
  • Sofia Tsiropoulou
  • Francisco J. Rios
  • Adam Harvey
  • Maria G. Dulak-Lis
  • Augusto C. Montezano
  • Rhian M. Touyz
Chapter

Abstract

Cardiovascular disease is the major cause of morbidity and mortality globally. As such better approaches for early detection and mechanism-targeted therapies are key priorities in cardiovascular research. Growing evidence indicates that vascular inflammation and oxidative stress may play an important role in the genesis and progression of cardiovascular disease. Accordingly identification of markers reflecting these processes may be useful early predictors of vascular damage and could provide insights into mechanisms, risk and targeted treatment. The present chapter provides a brief overview of vascular damage in cardiovascular disease and discusses recently identified novel biomarkers of vascular inflammation and oxidative stress. The potential clinical relevance is also highlighted.

Keywords

Inflammation Vascular remodelling Cytokines Oxidative stress Endothelial dysfunction 

References

  1. 1.
    Shimokawa H (2014) 2014 Williams Harvey Lecture: importance of coronary vasomotion abnormalities-from bench to bedside. Eur Heart J 35:3180–3193. doi:10.1093/eurheartj/ehu427 PubMedGoogle Scholar
  2. 2.
    Savoia C, Burger D, Nishigaki N et al (2011) Angiotensin II and the vascular phenotype in hypertension. Expert Rev Mol Med 13:e11PubMedGoogle Scholar
  3. 3.
    Chaudhari N, Talwar P, Parimisetty A et al (2014) A molecular web: endoplasmic reticulum stress, inflammation, and oxidative stress. Front Cell Neurosci 8:213PubMedCentralPubMedGoogle Scholar
  4. 4.
    Harrison DG, Widder J, Grumbach I et al (2006) Endothelial mechanotransduction, nitric oxide and vascular inflammation. J Intern Med 259(4):351–363PubMedGoogle Scholar
  5. 5.
    De Ciuceis C, Amiri F, Brassard P et al (2005) Reduced vascular remodeling, endothelial dysfunction, and oxidative stress in resistance arteries of angiotensin II-infused macrophage colony-stimulating factor-deficient mice: evidence for a role in inflammation in angiotensin-induced vascular injury. Arterioscler Thromb Vasc Biol 25:2106–2113PubMedGoogle Scholar
  6. 6.
    Tano JY, Schleifenbaum J, Gollasch M (2014) Perivascular adipose tissue, potassium channels, and vascular dysfunction. Arterioscler Thromb Vasc Biol 34(9):1827–1830PubMedGoogle Scholar
  7. 7.
    Sedeek M, Montezano AC, Hebert RL et al (2012) Oxidative stress, Nox isoforms and complications of diabetes–potential targets for novel therapies. J Cardiovasc Transl Res 5(4):509–518PubMedGoogle Scholar
  8. 8.
    Usui F, Shirasuna K, Kimura H et al (2015) Inflammasome activation by mitochondrial oxidative stress in macrophages leads to the development of angiotensin II-induced aortic aneurysm. Arterioscler Thromb Vasc Biol 35:127–136. doi:10.1161/ATVBAHA.114.303763 PubMedGoogle Scholar
  9. 9.
    Wang Y, Wang GZ, Rabinovitch PS, Tabas I (2014) Macrophage mitochondrial oxidative stress promotes atherosclerosis and nuclear factor-κB-mediated inflammation in macrophages. Circ Res 114(3):421–433PubMedCentralPubMedGoogle Scholar
  10. 10.
    Paneni F, Costantino S, Cosentino F (2014) Molecular mechanisms of vascular dysfunction and cardiovascular biomarkers in type 2 diabetes. Cardiovasc Diagn Ther 4(4):324–332PubMedCentralPubMedGoogle Scholar
  11. 11.
    Signorelli SS, Fiore V, Malaponte G (2014) Inflammation and peripheral arterial disease: the value of circulating biomarkers. Int J Mol Med 33(4):777–783PubMedGoogle Scholar
  12. 12.
    Koenig W (2013) High-sensitivity C-reactive protein and atherosclerotic disease: from improved risk prediction to risk-guided therapy. Int J Cardiol 168(6):5126–5134PubMedGoogle Scholar
  13. 13.
    Galano JM, Mas E, Barden A et al (2013) Isoprostanes and neuroprostanes: total synthesis, biological activity and biomarkers of oxidative stress in humans. Prostaglandins Other Lipid Mediat 107:95–102PubMedGoogle Scholar
  14. 14.
    Biomarkers Definitions Working Group (2001) Biomarkers and surrogate endpoints: preferred definitions and conceptual framework. Clin Pharmacol Ther 69(3):89–95Google Scholar
  15. 15.
    Wang TJ (2011) Assessing the role of circulating, genetic, and imaging biomarkers in cardiovascular risk prediction. Circulation 123:551–565PubMedCentralPubMedGoogle Scholar
  16. 16.
    Weber M, Hamm C (2006) Role of B-type natriuretic peptide (BNP) and NT-proBNP in clinical routine. Heart 92:843–849PubMedCentralPubMedGoogle Scholar
  17. 17.
    Ho E, Karimi Galougahi K, Liu CC et al (2013) Biological markers of oxidative stress: applications to cardiovascular research and practice. Redox Biol 1(1):483–491PubMedCentralPubMedGoogle Scholar
  18. 18.
    Rodrigo R, Libuy M, Feliú F, Hasson D (2013) Oxidative stress-related biomarkers in essential hypertension and ischemia-reperfusion myocardial damage. Dis Markers 35(6):773–790PubMedCentralPubMedGoogle Scholar
  19. 19.
    Sherwood MW, Kristin Newby L (2014) High-sensitivity troponin assays: evidence, indications, and reasonable use. J Am Heart Assoc 3(1):e000403PubMedCentralPubMedGoogle Scholar
  20. 20.
    Viel EC, Lemarié CA, Benkirane K et al (2010) Immune regulation and vascular inflammation in genetic hypertension. Am J Physiol Heart Circ Physiol 298:H938–H944PubMedGoogle Scholar
  21. 21.
    Sadat U, Jaffer FA, van Zandvoort MA et al (2014) Inflammation and neovascularization intertwined in atherosclerosis: imaging of structural and molecular imaging targets. Circulation 130(9):786–794PubMedGoogle Scholar
  22. 22.
    von Hundelshausen P, Schmitt MM (2014) Platelets and their chemokines in atherosclerosis-clinical applications. Front Physiol 5:294Google Scholar
  23. 23.
    Tuttolomondo A, Di Raimondo D, Pecoraro R et al (2012) Atherosclerosis as an inflammatory disease. Curr Pharm Des 18(28):4266–4288PubMedGoogle Scholar
  24. 24.
    Pitocco D, Tesauro M, Alessandro R et al (2013) Oxidative stress in diabetes: implications for vascular and other complications. Int J Mol Sci 14(11):21525–21550PubMedCentralPubMedGoogle Scholar
  25. 25.
    Schiffrin EL (2010) T Lymphocytes: a role in hypertension? Curr Opin Nephrol Hypertens 19:181–186PubMedGoogle Scholar
  26. 26.
    Guzik TJ, Hoch NE, Brown KA (2007) Role of T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J Exp Med 204:2449–2460PubMedCentralPubMedGoogle Scholar
  27. 27.
    Marvar PJ, Thabet SR, Guzik TJ et al (2010) Central and peripheral mechanisms of T-lymphocyte activation and vascular inflammation produced by angiotensin II-induced hypertension. Circ Res 107(2):263–270PubMedCentralPubMedGoogle Scholar
  28. 28.
    Barhoumi T, Kasal DAB, Li MW et al (2011) T regulatory lymphocytes prevent angiotensin II-induced hypertension and vascular injury. Hypertension 57:469–476PubMedGoogle Scholar
  29. 29.
    Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82(1):47–95PubMedGoogle Scholar
  30. 30.
    Brandes RP, Weissmann N, Schröder K (2014) Nox family NADPH oxidases: molecular mechanisms of activation. Free Radic Biol Med 76C:208–226Google Scholar
  31. 31.
    Montezano AC, Touyz RM (2014) Reactive oxygen species, vascular Noxs, and hypertension: focus on translational and clinical research. Antioxid Redox Signal 20(1):164–182PubMedCentralPubMedGoogle Scholar
  32. 32.
    Lassègue B, San Martín A, Griendling KK (2012) Biochemistry, physiology, and pathophysiology of NADPH oxidases in the cardiovascular system. Circ Res 110(10):1364–1390PubMedCentralPubMedGoogle Scholar
  33. 33.
    Liu J, Ormsby A, Oja-Tebbe N, Pagano PJ (2004) Gene transfer of NAD(P)H oxidase inhibitor to the vascular adventitia attenuates medial smooth muscle hypertrophy. Circ Res 95(6):587–594PubMedGoogle Scholar
  34. 34.
    Mochin MT, Underwood KF, Cooper B et al (2014) Hyperglycemia and redox status regulate RUNX2 DNA-binding and an angiogenic phenotype in endothelial cells. Microvasc Res 97C:55–64Google Scholar
  35. 35.
    Ali ZA, de Jesus Perez V, Yuan K et al (2014) Oxido-reductive regulation of vascular remodeling by receptor tyrosine kinase ROS1. J Clin Invest 124:5159–5174. pii:77484Google Scholar
  36. 36.
    Chen J, Xu L, Huang C (2014) DHEA inhibits vascular remodeling following arterial injury: a possible role in suppression of inflammation and oxidative stress derived from vascular smooth muscle cells. Mol Cell Biochem 388(1–2):75–84PubMedGoogle Scholar
  37. 37.
    Nguyen Dinh Cat A, Montezano AC, Burger D, Touyz RM (2013) Angiotensin II, NADPH oxidase, and redox signaling in the vasculature. Antioxid Redox Signal 19(10):1110–1120PubMedCentralPubMedGoogle Scholar
  38. 38.
    Al Ghouleh I, Khoo NK, Knaus UG et al (2011) Oxidases and peroxidases in cardiovascular and lung disease: new concepts in reactive oxygen species signaling. Free Radic Biol Med 51(7):1271–1288PubMedGoogle Scholar
  39. 39.
    Touyz RM (2005) Reactive oxygen species as mediators of calcium signalling by angiotensin II: implications in vascular physiology and pathophysiology. Antioxid Redox Signal 7(9–10):1302–1314PubMedGoogle Scholar
  40. 40.
    Bruder-Nascimento T, Callera GE, Montezano AC et al (2015) Vascular injury in diabetic db/db mice is ameliorated by atorvastatin: role of Rac1/2-sensitive Nox-dependent pathways. Clin Sci (Lond) 128:411–423. doi:10.1042/cs20140456 Google Scholar
  41. 41.
    Heneberg P (2014) Reactive nitrogen species and hydrogen sulfide as regulators of protein tyrosine phosphatase activity. Antioxid Redox Signal 20(14):2191–2209PubMedGoogle Scholar
  42. 42.
    Tabet F, Savoia C, Schiffrin EL, Touyz RM (2004) Differential calcium regulation by hydrogen peroxide and superoxide in vascular smooth muscle cells from spontaneously hypertensive rats. J Cardiovasc Pharmacol 44(2):200–208PubMedGoogle Scholar
  43. 43.
    Pastore A, Piemonte F (2013) Protein glutathionylation in cardiovascular diseases. Int J Mol Sci 14(10):20845–20876PubMedCentralPubMedGoogle Scholar
  44. 44.
    Iqbal A, Paviani V, Moretti AI et al (2014) Oxidation, inactivation and aggregation of protein disulfide isomerase promoted by the bicarbonate-dependent peroxidase activity of human superoxide dismutase. Arch Biochem Biophys 557:72–81PubMedGoogle Scholar
  45. 45.
    Touyz RM, Briones AM (2011) Reactive oxygen species and vascular biology: implications in human hypertension. Hypertens Res 34(1):5–14PubMedGoogle Scholar
  46. 46.
    Kleikers PW, Wingler K, Hermans JJ et al (2012) NADPH oxidases as a source of oxidative stress and molecular target in ischemia/reperfusion injury. J Mol Med (Berl) 90(12):1391–1406Google Scholar
  47. 47.
    Maghzal GJ, Krause KH, Stocker R, Jaquet V (2012) Detection of reactive oxygen species derived from the family of NOX NADPH oxidases. Free Radic Biol Med 53(10):1903–1918PubMedGoogle Scholar
  48. 48.
    Kaludercic N, Deshwal S, Di Lisa F (2014) Reactive oxygen species and redox compartmentalization. Front Physiol 5:285PubMedCentralPubMedGoogle Scholar
  49. 49.
    McNeill E, Channon KM (2012) The role of tetrahydrobiopterin in inflammation and cardiovascular disease. Thromb Haemost 108(5):832–839PubMedGoogle Scholar
  50. 50.
    Lassegue B, Clempus RE (2003) Vascular NAD(P)H oxidases: specific features, expression, and regulation. Am J Physiol Regul Integr Comp Physiol 285:R277–R297PubMedGoogle Scholar
  51. 51.
    Kietadisorn R, Juni RP, Moens AL (2012) Tackling endothelial dysfunction by modulating NOS uncoupling: new insights into its pathogenesis and therapeutic possibilities. Am J Physiol Endocrinol Metab 302(5):E481–E495PubMedGoogle Scholar
  52. 52.
    Cai H, Harrison DG (2000) Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res 87:840–844PubMedGoogle Scholar
  53. 53.
    Zhang YH, Casadei B (2012) Sub-cellular targeting of constitutive NOS in health and disease. J Mol Cell Cardiol 52(2):341–350PubMedGoogle Scholar
  54. 54.
    Nagababu E, Rifkind JM (2010) Measurement of plasma nitrite by chemiluminescence. Methods Mol Biol 610:41–49PubMedCentralPubMedGoogle Scholar
  55. 55.
    Bouras G, Deftereos S, Tousoulis D et al (2013) Asymmetric Dimethylarginine (ADMA): a promising biomarker for cardiovascular disease? Curr Top Med Chem 13(2):180–200PubMedGoogle Scholar
  56. 56.
    Juonala M (2007) Brachial artery flow-mediated dilation and asymmetrical dimethylarginine in the cardiovascular risk in young Finns study. Circulation 116(12):1367–1373PubMedGoogle Scholar
  57. 57.
    Paiva H (2010) Levels of asymmetrical dimethylarginine are predictive of brachial artery flow-mediated dilation 6 years later. The Cardiovascular Risk in Young Finns Study. Atherosclerosis 212(2):512–515PubMedGoogle Scholar
  58. 58.
    Wolin MS, Gupte SA, Neo BH et al (2010) Oxidant-redox regulation of pulmonary vascular responses to hypoxia and nitric oxide-cGMP signaling. Cardiol Rev 18(2):89–93PubMedCentralPubMedGoogle Scholar
  59. 59.
    O’Donnell VB (1997) Nitric oxide inhibition of lipid peroxidation: kinetics of reaction with lipid peroxyl radicals and comparison with alpha-tocopherol. Biochemistry 36(49):15216–15223PubMedGoogle Scholar
  60. 60.
    Roberts LJ, Morrow JD (2000) Measurement of F(2)-isoprostanes as an index of oxidative stress in vivo. Free Radic Biol Med 28(4):505–513PubMedGoogle Scholar
  61. 61.
    Armstrong D, Browne R (1994) The analysis of free radicals, lipid peroxides, antioxidant enzymes and compounds related to oxidative stress as applied to the clinical chemistry laboratory. Adv Exp Med Biol 366:43–58PubMedGoogle Scholar
  62. 62.
    Heitzer T, Schlinzig T, Krohn K et al (2001) Endothelial dysfunction, oxidative stress, and risk of cardiovascular events in patients with coronary artery disease. Circulation 104(22):2673–2678PubMedGoogle Scholar
  63. 63.
    Annuk M, Zilmer M, Lind L et al (2001) Oxidative stress and endothelial function in chronic renal failure. J Am Soc Nephrol 12(12):2747–2752PubMedGoogle Scholar
  64. 64.
    Annuk M, Zilmer M, Fellstrom B (2003) Endothelium-dependent vasodilation and oxidative stress in chronic renal failure: impact on cardiovascular disease. Kidney Int Suppl 84:S50–S53PubMedGoogle Scholar
  65. 65.
    Guarneri M (2010) Flow mediated dilation, endothelial and inflammatory biomarkers in hypertensives with chronic kidney disease. J Hypertens 28:e118Google Scholar
  66. 66.
    Recio-Mayoral A, Banerjee D, Streather C, Kaski JC (2011) Endothelial dysfunction, inflammation and atherosclerosis in chronic kidney disease – a cross-sectional study of predialysis, dialysis and kidney-transplantation patients. Atherosclerosis 216:446–451PubMedGoogle Scholar
  67. 67.
    Yeun JY, Levine RA, Mantadilok V, Kaysen GA (2000) C-Reactive protein predicts all-cause and cardiovascular mortality in hemodialysis patients. Am J Kidney Dis 35(3):469–476PubMedGoogle Scholar
  68. 68.
    Ferroni P, Guadagni F (2008) Soluble CD40L and its role in essential hypertension: diagnostic and therapeutic implications. Cardiovasc Hematol Disord Drug Targets 8(3):194–202PubMedGoogle Scholar
  69. 69.
    Goldberg RB (2009) Cytokine and cytokine-like inflammation markers, endothelial dysfunction, and imbalanced coagulation in development of diabetes and its complications. J Clin Endocrinol Metab 94(9):3171–3182PubMedGoogle Scholar
  70. 70.
    Binder BR, Christ G, Gruber F et al (2002) Plasminogen activator inhibitor 1: physiological and pathophysiological roles. News Physiol Sci 17:56–61PubMedGoogle Scholar
  71. 71.
    Yang P, Liu YF, Yang L et al (2010) Mechanism and clinical significance of the prothrombotic state in patients with essential hypertension. Clin Cardiol 33(6):E81–E86PubMedGoogle Scholar
  72. 72.
    Paulinska P, Spiel A, Jilma B (2009) Role of von Willebrand factor in vascular disease. Hamostaseologie 29(1):32–38PubMedGoogle Scholar
  73. 73.
    Dignat-George F, Boulanger CM (2011) The many faces of endothelial microparticles. Arterioscler Thromb Vasc Biol 31(1):27–33PubMedGoogle Scholar
  74. 74.
    Beyer C, Pisetsky DS (2010) The role of microparticles in the pathogenesis of rheumatic diseases. Nat Rev Rheumatol 6(1):21–29PubMedGoogle Scholar
  75. 75.
    Jy W, Horstman LL, Jimenez JJ et al (2004) Measuring circulating cell-derived microparticles. J Thromb Haemost 2(10):1842–1851PubMedGoogle Scholar
  76. 76.
    Lacroix R, Robert S, Poncelet P, Dignat-George F (2010) Overcoming limitations of microparticle measurement by flow cytometry. Semin Thromb Hemost 36(8):807–818PubMedGoogle Scholar
  77. 77.
    Burger D, Montezano AC, Nishigaki N et al (2011) Endothelial microparticle formation by angiotensin II is mediated via AT1R/NADPH Oxidase/Rho kinase pathways targeted to lipid rafts. Arterioscler Thromb Vasc Biol 31:1898–1907PubMedGoogle Scholar
  78. 78.
    Burger D, Schock S, Thompson CS et al (2013) Microparticles: biomarkers and beyond. Clin Sci (Lond) 124(7):423–441Google Scholar
  79. 79.
    Burger D, Touyz RM (2012) Cellular biomarkers of endothelial health: microparticles, endothelial progenitor cells, and circulating endothelial cells. J Am Soc Hypertens 6(2):85–99PubMedGoogle Scholar
  80. 80.
    Burger D, Kwart DG, Montezano AC et al (2012) Microparticles induce cell cycle arrest through redox-sensitive processes in endothelial cells: implications in vascular senescence. J Am Heart Assoc 1(3):e001842PubMedCentralPubMedGoogle Scholar
  81. 81.
    Leroyer AS, Anfosso F, Lacroix R et al (2010) Endothelial-derived microparticles: biological conveyors at the crossroad of inflammation, thrombosis and angiogenesis. Thromb Haemost 104(3):456–463PubMedGoogle Scholar
  82. 82.
    Shantsila E, Kamphuisen PW, Lip GY (2010) Circulating microparticles in cardiovascular disease: implications for atherogenesis and atherothrombosis. J Thromb Haemost 8(11):2358–2368PubMedGoogle Scholar
  83. 83.
    Boulanger CM, Amabile N, Tedgui A (2006) Circulating microparticles: a potential prognostic marker for atherosclerotic vascular disease. Hypertension 48(2):180–186PubMedGoogle Scholar
  84. 84.
    Azevedo LC, Pedro MA, Laurindo FR (2007) Circulating microparticles as therapeutic targets in cardiovascular diseases. Recent Pat Cardiovasc Drug Discov 2(1):41–51PubMedGoogle Scholar
  85. 85.
    Ridker PM, Lüscher TF (2014) Anti-inflammatory therapies for cardiovascular disease. Eur Heart J 35(27):1782–1791PubMedGoogle Scholar
  86. 86.
    Kaptoge S, Di AE, Pennells L, Wood AM (2012) C-reactive protein, fibrinogen, and cardiovascular disease prediction. N Engl J Med 367:1310–1320PubMedGoogle Scholar
  87. 87.
    Gillett MJ (2009) International Expert Committee report on the role of the A1C assay in the diagnosis of diabetes. Diabetes Care 32:1327–1334Google Scholar
  88. 88.
    Ridker PM (2003) Clinical application of C-reactive protein for cardiovascular disease detection and prevention. Circulation 107:363–369PubMedGoogle Scholar
  89. 89.
    Kaptoge S, Di Angelantonio E, Lowe G et al (2010) C-reactive protein concentration and risk of coronary heart disease, stroke, and mortality: an individual participant meta-analysis. Emerging Risk Factors Collaboration. Lancet 375(9709):132–140PubMedGoogle Scholar
  90. 90.
    Meisinger C, Heier M, von Scheidt W, Kuch B (2010) Admission C-reactive protein and short- as well as long-term mortality in diabetic versus non-diabetic patients with incident myocardial infarction. MONICA/KORA Myocardial Infarction Registry. Clin Res Cardiol 99(12):817–823PubMedGoogle Scholar
  91. 91.
    Miyazaki T, Chiuve S, Sacks FM et al (2014) Plasma pentraxin 3 levels do not predict coronary events but reflect metabolic disorders in patients with coronary artery disease in the CARE trial. PLoS One 9(4):e94073PubMedCentralPubMedGoogle Scholar
  92. 92.
    Dubin R, Li Y, Ix JH et al (2012) Associations of pentraxin-3 with cardiovascular events, incident heart failure, and mortality among persons with coronary heart disease: data from the Heart and Soul Study. Am Heart J 163(2):274–279PubMedCentralPubMedGoogle Scholar
  93. 93.
    Xanthakis V, Enserro DM, Murabito JM et al (2014) Ideal cardiovascular health: associations with biomarkers and subclinical disease and impact on incidence of cardiovascular disease in the Framingham offspring study. Circulation 130(19):1676–1683PubMedGoogle Scholar
  94. 94.
    Keller T, Zeller T, Peetz D et al (2009) Sensitive troponin I assay in early diagnosis of acute myocardial infarction. N Engl J Med 361:868–877PubMedGoogle Scholar
  95. 95.
    Kotzé RC, Ariëns RA, de Lange Z, Pieters M (2014) CVD risk factors are related to plasma fibrin clot properties independent of total and or γ′ fibrinogen concentration. Thromb Res 134:963–969. pii:S0049-3848(14)00454-XGoogle Scholar
  96. 96.
    Tecchio C, Micheletti A, Cassatella MA (2014) Neutrophil-derived cytokines: facts beyond expression. Front Immunol 5:508PubMedCentralPubMedGoogle Scholar
  97. 97.
    Kaptoge S, Seshasai SR, Gao P et al (2014) Inflammatory cytokines and risk of coronary heart disease: new prospective study and updated meta-analysis. Eur Heart J 35(9):578–589PubMedCentralPubMedGoogle Scholar
  98. 98.
    Su D, Li Z, Li X et al (2013) Association between serum interleukin-6 concentration and mortality in patients with coronary artery disease. Mediators Inflamm 2013:726178PubMedCentralPubMedGoogle Scholar
  99. 99.
    Murdaca G, Spanò F, Cagnati P, Puppo F (2013) Free radicals and endothelial dysfunction: potential positive effects of TNF-α inhibitors. Redox Rep 18(3):95–99PubMedGoogle Scholar
  100. 100.
    Tam LS, Kitas GD, González-Gay MA (2014) Can suppression of inflammation by anti-TNF prevent progression of subclinical atherosclerosis in inflammatory arthritis? Rheumatology (Oxford) 53(6):1108–1119Google Scholar
  101. 101.
    Garlanda C, Dinarello CA, Mantovani A (2013) The interleukin-1 family: back to the future. Immunity 39(6):1003–1018PubMedCentralPubMedGoogle Scholar
  102. 102.
    Dinarello CA, van der Meer JW (2013) Treating inflammation by blocking interleukin-1 in humans. Semin Immunol 25(6):469–484PubMedCentralPubMedGoogle Scholar
  103. 103.
    Garbers C, Scheller J (2013) Interleukin-6 and interleukin-11: same same but different. Biol Chem 394(9):1145–1161PubMedGoogle Scholar
  104. 104.
    Bustamante A, Sobrino T, Giralt D et al (2014) Prognostic value of blood interleukin-6 in the prediction of functional outcome after stroke: a systematic review and meta-analysis. J Neuroimmunol 274(1–2):215–224PubMedGoogle Scholar
  105. 105.
    Trott DW, Harrison DG (2014) The immune system in hypertension. Adv Physiol Educ 38(1):20–24PubMedGoogle Scholar
  106. 106.
    Gomolak JR, Didion SP (2014) Angiotensin II-induced endothelial dysfunction is temporally linked with increases in interleukin-6 and vascular macrophage accumulation. Front Physiol 5:396PubMedCentralPubMedGoogle Scholar
  107. 107.
    Spranger J, Kroke A, Möhlig M et al (2003) Inflammatory cytokines and the risk to develop type 2 diabetes: results of the prospective population-based European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study. Diabetes 52(3):812–817PubMedGoogle Scholar
  108. 108.
    Lowe G, Woodward M, Hillis G et al (2014) Circulating inflammatory markers and the risk of vascular complications and mortality in people with type 2 diabetes and cardiovascular disease or risk factors: the ADVANCE study. Diabetes 63(3):1115–1123PubMedGoogle Scholar
  109. 109.
    Kawai VK, Chung CP, Solus JF et al (2014) The ability of the 2013 ACC/AHA cardiovascular risk score to identify rheumatoid arthritis patients with high coronary artery calcification scores. Arthritis Rheumatol. doi:10.1002/art.38944
  110. 110.
    Puttevils D, De Vusser P, Geusens P, Dens J (2014) Increased cardiovascular risk in patients with rheumatoid arthritis: an overview. Acta Cardiol 69(2):111–118PubMedGoogle Scholar
  111. 111.
    Damjanov N, Nurmohamed MT, Szekanecz Z (2014) Biologics, cardiovascular effects and cancer. BMC Med 12:48PubMedCentralPubMedGoogle Scholar
  112. 112.
    Greenberg JD, Kremer JM, Curtis JR, CORRONA Investigators (2011) Tumour necrosis factor antagonist use and associated risk reduction of cardiovascular events among patients with rheumatoid arthritis. Ann Rheum Dis 70(4):576–582PubMedGoogle Scholar
  113. 113.
    Desai RJ, Rao JK, Hansen RA et al (2014) Tumor necrosis factor-α inhibitor treatment and the risk of incident cardiovascular events in patients with early rheumatoid arthritis: a nested case-control study. J Rheumatol 41(11):2129–2136PubMedGoogle Scholar
  114. 114.
    Niki E (2014) Biomarkers of lipid peroxidation in clinical material. Biochim Biophys Acta 1840(2):809–817PubMedGoogle Scholar
  115. 115.
    Del Rio D, Stewart AJ, Pellegrini N (2005) A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr Metab Cardiovasc Dis 15(4):316–328PubMedGoogle Scholar
  116. 116.
    Yagi K (1998) Simple assay for the level of total lipid peroxides in serum or plasma. Methods Mol Biol 108:101–106PubMedGoogle Scholar
  117. 117.
    White M, Ducharme A, Ibrahim R et al (2006) Increased systemic inflammation and oxidative stress in patients with worsening congestive heart failure: improvement after short-term inotropic support. Clin Sci (Lond) 110(4):483–489Google Scholar
  118. 118.
    White M, Cantin B, Haddad H et al (2013) Cardiac signaling molecules and plasma biomarkers after cardiac transplantation: impact of tacrolimus versus cyclosporine. J Heart Lung Transplant 32(12):1222–1232PubMedGoogle Scholar
  119. 119.
    Kurlak LO, Green A, Loughna P et al (2014) Oxidative stress markers in hypertensive states of pregnancy: preterm and term disease. Front Physiol 5:310PubMedCentralPubMedGoogle Scholar
  120. 120.
    da Cruz AC, Petronilho F, Heluany CC et al (2014) Oxidative stress and aging: correlation with clinical parameters. Aging Clin Exp Res 26(1):7–12PubMedGoogle Scholar
  121. 121.
    Lee WC, Wong HY, Chai YY et al (2012) Lipid peroxidation dysregulation in ischemic stroke: plasma 4-HNE as a potential biomarker? Biochem Biophys Res Commun 425(4):842–847PubMedGoogle Scholar
  122. 122.
    Tanaka S, Miki T, Sha S et al (2011) Serum levels of thiobarbituric acid-reactive substances are associated with risk of coronary heart disease. J Atheroscler Thromb 18(7):584–591PubMedGoogle Scholar
  123. 123.
    Salonen JT, Nyyssonen K, Salonen R et al (1997) Lipoprotein oxidation and progression of carotid atherosclerosis. Circulation 95:840–845PubMedGoogle Scholar
  124. 124.
    Zhang ZJ (2013) Systematic review on the association between F2-isoprostanes and cardiovascular disease. Ann Clin Biochem 50(Pt 2):108–114PubMedGoogle Scholar
  125. 125.
    Lee R, Margaritis M, Channon KM, Antoniades C (2012) Evaluating oxidative stress in human cardiovascular disease: methodological aspects and considerations. Curr Med Chem 19(16):2504–2520PubMedCentralPubMedGoogle Scholar
  126. 126.
    Campos C, Guzmán R, López-Fernández E, Casado Á (2011) Urinary biomarkers of oxidative/nitrosative stress in healthy smokers. Inhal Toxicol 23(3):148–156PubMedGoogle Scholar
  127. 127.
    Morrow JD, Frei B, Longmire AW et al (1995) Increase in circulating products of lipid peroxidation (F2-isoprostanes) in smokers. Smoking as a cause of oxidative damage. N Engl J Med 332(18):1198–1203PubMedGoogle Scholar
  128. 128.
    Davies SS, Roberts LJ 2nd (2011) F2-isoprostanes as an indicator and risk factor for coronary heart disease. Free Radic Biol Med 50(5):559–566PubMedCentralPubMedGoogle Scholar
  129. 129.
    Basu S (2010) Bioactive eicosanoids: role of prostaglandin F(2α) and F2-isoprostanes in inflammation and oxidative stress related pathology. Mol Cells 30(5):383–391PubMedGoogle Scholar
  130. 130.
    Tsimikas S (2006) Oxidative biomarkers in the diagnosis and prognosis of cardiovascular disease. Am J Cardiol 98(11A):9P–17PPubMedGoogle Scholar
  131. 131.
    Pignatelli P, Pastori D, Carnevale R et al (2014) Serum NOX2 and urinary isoprostanes predict vascular events in patients with atrial fibrillation. Thromb Haemost. doi:10.1160/TH14-07-0571
  132. 132.
    Spickett CM (2013) The lipid peroxidation product 4-hydroxy-2-nonenal: advances in chemistry and analysis. Redox Biol 1(1):145–152PubMedCentralPubMedGoogle Scholar
  133. 133.
    Asselin C, Shi Y, Clément R et al (2007) Higher circulating 4-hydroxynonenal-protein thioether adducts correlate with more severe diastolic dysfunction in spontaneously hypertensive rats. Redox Rep 12(1):68–72PubMedGoogle Scholar
  134. 134.
    Mali VR, Ning R, Chen J et al (2014) Impairment of aldehyde dehydrogenase-2 by 4-hydroxy-2-nonenal adduct formation and cardiomyocyte hypertrophy in mice fed a high-fat diet and injected with low-dose streptozotocin. Exp Biol Med 239(5):610–618Google Scholar
  135. 135.
    Zhang Y, Sano M, Shinmura K et al (2010) 4-hydroxy-2-nonenal protects against cardiac ischemia-reperfusion injury via the Nrf2-dependent pathway. J Mol Cell Cardiol 49(4):576–586PubMedGoogle Scholar
  136. 136.
    Usberti M, Gerardi GM, Gazzotti RM et al (2002) Oxidative stress and cardiovascular disease in dialyzed patients. Nephron 91(1):25–33PubMedGoogle Scholar
  137. 137.
    Gerardi G, Usberti M, Martini G et al (2002) Plasma total antioxidant capacity in hemodialyzed patients and its relationships to other biomarkers of oxidative stress and lipid peroxidation. Clin Chem Lab Med 40(2):104–110PubMedGoogle Scholar
  138. 138.
    Fraga CG, Oteiza PI, Galleano M (2014) In vitro measurements and interpretation of total antioxidant capacity. Biochim Biophys Acta 1840(2):931–934PubMedGoogle Scholar
  139. 139.
    Pinchuk I, Shoval H, Dotan Y, Lichtenberg D (2012) Evaluation of antioxidants: scope, limitations and relevance of assays. Chem Phys Lipids 165(6):638–647PubMedGoogle Scholar
  140. 140.
    Lotito SB, Frei B (2006) Consumption of flavonoid-rich foods and increased plasma antioxidant capacity in humans: cause, consequence, or epiphenomenon? Free Radic Biol Med 41(12):1727–1746PubMedGoogle Scholar
  141. 141.
    Hollman PC, Cassidy A, Comte B et al (2011) The biological relevance of direct antioxidant effects of polyphenols for cardiovascular health in humans is not established. J Nutr 141(5):989S–1009SPubMedGoogle Scholar
  142. 142.
    Wang Y, Chun OK, Song WO (2013) Plasma and dietary antioxidant status as cardiovascular disease risk factors: a review of human studies. Nutrients 5(8):2969–3004PubMedCentralPubMedGoogle Scholar
  143. 143.
    Bartosz G (2010) Non-enzymatic antioxidant capacity assays: limitations of use in biomedicine. Free Radic Res 44(7):711–720PubMedGoogle Scholar
  144. 144.
    Gedikli O, Ozturk S, Yilmaz H et al (2009) Low total antioxidative capacity levels are associated with augmentation index but not pulse-wave velocity. Heart Vessels 24(5):366–370PubMedGoogle Scholar
  145. 145.
    Dean RT, Fu S, Stocker R, Davies MJ (1997) Biochemistry and pathology of radical-mediated protein oxidation. Biochem J 324(Pt 1):1–18PubMedCentralPubMedGoogle Scholar
  146. 146.
    Shacter E (2000) Quantification and significance of protein oxidation in biological samples. Drug Metab Rev 32(3–4):307–326PubMedGoogle Scholar
  147. 147.
    Cai Z, Yan LJ (2013) Protein oxidative modifications: beneficial roles in disease and health. J Biochem Pharmacol Res 1(1):15–26PubMedCentralPubMedGoogle Scholar
  148. 148.
    Dalle-Donne I, Giustarini D, Colombo R, Rossi R, Milzani A (2003) Protein carbonylation in human diseases. Trends Mol Med 9:169–176PubMedGoogle Scholar
  149. 149.
    Kojer K, Riemer J (2014) Balancing oxidative protein folding: the influences of reducing pathways on disulfide bond formation. Biochim Biophys Acta 1844(8):1383–1390PubMedGoogle Scholar
  150. 150.
    Rhee SG, Jeong W, Chang TS, Woo HA (2007) Sulfiredoxin, the cysteine sulfinic acid reductase specific to 2-Cys peroxiredoxin: its discovery, mechanism of action, and biological significance. Kidney Int Suppl 106:S3–S8PubMedGoogle Scholar
  151. 151.
    Arai H (2014) Oxidative modification of lipoproteins. Subcell Biochem 77:103–114PubMedGoogle Scholar
  152. 152.
    Collins AR (2005) Assays for oxidative stress and antioxidant status: applications to research into the biological effectiveness of polyphenols. Am J Clin Nutr 81(1 Suppl):261S–267SPubMedGoogle Scholar
  153. 153.
    Haque A, Andersen JN, Salmeen A et al (2011) Conformation-sensing antibodies stabilize the oxidized form of PTP1B and inhibit its phosphatase activity. Cell 147(1):185–198PubMedCentralPubMedGoogle Scholar
  154. 154.
    Nelson KJ, Klomsiri C, Codreanu SG et al (2010) Use of dimedone-based chemical probes for sulfenic acid detection methods to visualize and identify labeled proteins. Methods Enzymol 473:95–115PubMedGoogle Scholar
  155. 155.
    Paulsen CE, Truong TH, Garcia FJ et al (2012) Peroxide-dependent sulfenylation of the EGFR catalytic site enhances kinase activity. Nat Chem Biol 8(1):57–64Google Scholar
  156. 156.
    Ckless K (2014) Redox proteomics: from bench to bedside. Adv Exp Med Biol 806:301–317PubMedGoogle Scholar
  157. 157.
    Groitl B, Jakob U (2014) Thiol-based redox switches. Biochim Biophys Acta 1844(8):1335–1343PubMedGoogle Scholar
  158. 158.
    Becatti M, Marcucci R, Bruschi G et al (2014) Oxidative modification of fibrinogen is associated with altered function and structure in the subacute phase of myocardial infarction. Arterioscler Thromb Vasc Biol 34(7):1355–1361PubMedGoogle Scholar
  159. 159.
    Goff DC Jr, Lloyd-Jones DM, Bennett G, American College of Cardiology/American Heart Association Task Force on Practice Guidelines et al (2014) 2013 ACC/AHA guideline on the assessment of cardiovascular risk: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. Circulation 129(25 Suppl 2):S49–S73PubMedGoogle Scholar
  160. 160.
    Davies KJ, Thapar A, Kasivisvanathan V et al (2013) Review of trans-atlantic cardiovascular best medical therapy guidelines – recommendations for asymptomatic carotid atherosclerosis. Curr Vasc Pharmacol 11(4):514–523PubMedGoogle Scholar
  161. 161.
    Davidson MH, Corson MA, Alberts MJ et al (2008) Consensus panel recommendation for incorporating lipoprotein-associated phospholipase A2 testing into cardiovascular disease risk assessment guidelines. Am J Cardiol 101(12A):51F–57FPubMedGoogle Scholar
  162. 162.
    Paynter NP, Everett BM, Cook NR (2014) Cardiovascular disease risk prediction in women: is there a role for novel biomarkers? Clin Chem 60(1):88–97PubMedGoogle Scholar
  163. 163.
    Abbasi A, Corpeleijn E, Meijer E et al (2012) Sex differences in the association between plasma copeptin and incident type 2 diabetes: the Prevention of Renal and Vascular Endstage Disease (PREVEND) study. Diabetologia 55(7):1963–1970PubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Paul Welsh
    • 1
  • David Preiss
    • 1
  • Sofia Tsiropoulou
    • 1
  • Francisco J. Rios
    • 1
  • Adam Harvey
    • 1
  • Maria G. Dulak-Lis
    • 1
  • Augusto C. Montezano
    • 1
  • Rhian M. Touyz
    • 1
  1. 1.Institute of Cardiovascular and Medical Sciences, British Heart Foundation (BHF) Glasgow Cardiovascular Research CentreUniversity of GlasgowGlasgowUK

Personalised recommendations