Proteomics of plaques and novel sources of potential biomarkers for atherosclerosis

Proteomics - Clinical Applications

Volumn 7, Issue 7-8, 2013, Pages 490-503

  Bleijerveld, Onno B ^a   Zhang, Ya Nan ^b   Beldar, Serap ^c   Hoefer, Imo E ^a   Sze, Siu K ^c   Pasterkamp, Gerard ^a   De Kleijn, Dominique P V ^a,b,d  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d ROYAL NETHERLANDS ACADEMY OF ARTS AND SCIENCES   (Netherlands)

Author keywords

Atherosclerosis; Atherosclerotic plaque; Biomarkers; Circulating cells; Plasma extracellular vesicles

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ADVANCED GLYCATION END PRODUCT RECEPTOR; ATORVASTATIN; BIOLOGICAL MARKER; C REACTIVE PROTEIN; CATHEPSIN D; CD40 LIGAND; FATTY ACID BINDING PROTEIN 4; HEAT SHOCK PROTEIN 27; HIGH DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; MYELOPEROXIDASE; OSTEOPONTIN; TROPONIN I;

ACUTE CORONARY SYNDROME; ATHEROSCLEROTIC PLAQUE; CARBAMOYLATION; CARDIOVASCULAR DISEASE; CAROTID ATHEROSCLEROSIS; CORONARY ARTERY ATHEROSCLEROSIS; CORONARY ARTERY DISEASE; CORONARY ARTERY OBSTRUCTION; ENDOTHELIUM CELL; GRANULOCYTE; HUMAN; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; OXIDATION REDUCTION POTENTIAL; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN PHOSPHORYLATION; PROTEOMICS; REVIEW; TWO DIMENSIONAL ELECTROPHORESIS;

ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BIOMARKERS; CIRCULATING CELLS; PLASMA EXTRACELLULAR VESICLES;

ANIMALS; BIOLOGICAL MARKERS; EXTRACELLULAR SPACE; HUMANS; OXIDATION-REDUCTION; PHOSPHOLIPIDS; PLAQUE, ATHEROSCLEROTIC; PROTEOMICS;

EID: 84881535285     PISSN: 18628346     EISSN: 18628354     Source Type: Journal    
DOI: 10.1002/prca.201200119     Document Type: Review

References (115)

1. Kim, A. S., Johnston, S. C., Global variation in the relative burden of stroke and ischemic heart disease. Circulation 2011, 124, 314-323.
2. Kolodgie, F. D., Gold, H. K., Burke, A. P., Fowler, D. R. et al., Intraplaque hemorrhage and progression of coronary atheroma. N. Engl. J. Med. 2003, 349, 2316-2325.
3. Libby, P., Inflammation in atherosclerosis. Nature 2002, 420, 868-874.
4. Libby, P., Ridker, P. M., Hansson, G. K., Progress and challenges in translating the biology of atherosclerosis. Nature 2011, 473, 317-325.
5. Vivanco, F., Mas, S., Darde, V. M., De la Cuesta, F. et al., Vascular proteomics. Proteomics Clin. Appl. 2007, 1, 1102-1122.
6. Burke, A. P., Farb, A., Malcom, G. T., Liang, Y. H. et al., Coronary risk factors and plaque morphology in men with coronary disease who died suddenly. N. Engl. J. Med. 1997, 336, 1276-1282.
7. Naghavi, M., Libby, P., Falk, E., Casscells, S. W. et al., From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: part I. Circulation 2003, 108, 1664-1672.
8. Naghavi, M., Libby, P., Falk, E., Casscells, S. W. et al., From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: part II. Circulation 2003, 108, 1772-1778.
9. Schwartz, S. M., Galis, Z. S., Rosenfeld, M. E., Falk, E., Plaque rupture in humans and mice. Arterioscler. Thromb. Vasc. Biol. 2007, 27, 705-713.
10. Shah, P. K., Falk, E., Badimon, J. J., Fernandez-Ortiz, A. et al., Human monocyte-derived macrophages induce collagen breakdown in fibrous caps of atherosclerotic plaques. Potential role of matrix-degrading metalloproteinases and implications for plaque rupture. Circulation 1995, 92, 1565-1569.
11. Mathers, C. D., Boerma, T., Ma Fat, D., Global and regional causes of death. Br. Med. Bull. 2009, 92, 7-32.
12. Executive Summary of The Third Report of The National Cholesterol Education Program (NCEP) Expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (adult treatment panel III). JAMA 2001, 285, 2486-2497.
13. Greenland, P., Knoll, M. D., Stamler, J., Neaton, J. D. et al., Major risk factors as antecedents of fatal and nonfatal coronary heart disease events. JAMA 2003, 290, 891-897.
14. Khot, U. N., Khot, M. B., Bajzer, C. T., Sapp, S. K. et al., Prevalence of conventional risk factors in patients with coronary heart disease. JAMA 2003, 290, 898-904.
15. Magnus, P., Beaglehole, R., The real contribution of the major risk factors to the coronary epidemics: time to end the "only-50%" myth. Arch. Intern. Med. 2001, 161, 2657-2660.
16. Ridker, P. M., Brown, N. J., Vaughan, D. E., Harrison, D. G. et al., Established and emerging plasma biomarkers in the prediction of first atherothrombotic events. Circulation 2004, 109, IV6-19.
17. Danesh, J., Wheeler, J. G., Hirschfield, G. M., Eda, S. et al., C-reactive protein and other circulating markers of inflammation in the prediction of coronary heart disease. N. Engl. J. Med. 2004, 350, 1387-1397.
18. de Lemos, J. A., Morrow, D. A., Sabatine, M. S., Murphy, S. A. et al., Association between plasma levels of monocyte chemoattractant protein-1 and long-term clinical outcomes in patients with acute coronary syndromes. Circulation 2003, 107, 690-695.
19. van Wijk, D. F., van Leuven, S. I., Sandhu, M. S., Tanck, M. W. et al., Chemokine ligand 2 genetic variants, serum monocyte chemoattractant protein-1 levels, and the risk of coronary artery disease. Arterioscler. Thromb. Vasc. Biol. 2010, 30, 1460-1466.
20. Heeschen, C., Dimmeler, S., Hamm, C. W., van den Brand, M. J. et al., Soluble CD40 ligand in acute coronary syndromes. N. Engl. J. Med. 2003, 348, 1104-1111.
21. Meuwese, M. C., Stroes, E. S., Hazen, S. L., van Miert, J. N. et al., Serum myeloperoxidase levels are associated with the future risk of coronary artery disease in apparently healthy individuals: the EPIC-Norfolk Prospective Population Study. J. Am. Coll. Cardiol. 2007, 50, 159-165.
22. Kullo, I. J., Cooper, L. T., Early identification of cardiovascular risk using genomics and proteomics. Nat. Rev. Cardiol. 2010, 7, 309-317.
23. Zethelius, B., Berglund, L., Sundstrom, J., Ingelsson, E. et al., Use of multiple biomarkers to improve the prediction of death from cardiovascular causes. N. Engl. J. Med. 2008, 358, 2107-2116.
24. Wang, T. J., Gona, P., Larson, M. G., Tofler, G. H. et al., Multiple biomarkers for the prediction of first major cardiovascular events and death. N. Engl. J. Med. 2006, 355, 2631-2639.
25. Van Eyk, J. E., Overview: the maturing of proteomics in cardiovascular research. Circ. Res. 2011, 108, 490-498.
26. Duran, M. C., Mas, S., Martin-Ventura, J. L., Meilhac, O. et al., Proteomic analysis of human vessels: application to atherosclerotic plaques. Proteomics 2003, 3, 973-978.
27. Martin-Ventura, J. L., Duran, M. C., Blanco-Colio, L. M., Meilhac, O. et al., Identification by a differential proteomic approach of heat shock protein 27 as a potential marker of atherosclerosis. Circulation 2004, 110, 2216-2219.
28. Duran, M. C., Martin-Ventura, J. L., Mohammed, S., Barderas, M. G. et al., Atorvastatin modulates the profile of proteins released by human atherosclerotic plaques. Eur. J. Pharmacol. 2007, 562, 119-129.
29. Brioschi, M., Lento, S., Tremoli, E., Banfi, C., Proteomic analysis of endothelial cell secretome: A means of studying the pleiotropic effects of Hmg-CoA reductase inhibitors. J. Proteomics 2012, 78, 346-361.
30. Porcelli, B., Ciari, I., Felici, C., Pagani, R. et al., Proteomic analysis of atherosclerotic plaque. Biomed. Pharmacother. 2010, 64, 369-372.
31. de la Cuesta, F., Barderas, M. G., Calvo, E., Zubiri, I. et al., Secretome analysis of atherosclerotic and non-atherosclerotic arteries reveals dynamic extracellular remodeling during pathogenesis. J. Proteom. 2012, 75, 2960-2971.
32. Donners, M. M., Verluyten, M. J., Bouwman, F. G., Mariman, E. C. et al., Proteomic analysis of differential protein expression in human atherosclerotic plaque progression. J. Pathol. 2005, 206, 39-45.
33. Lepedda, A. J., Cigliano, A., Cherchi, G. M., Spirito, R. et al., A proteomic approach to differentiate histologically classified stable and unstable plaques from human carotid arteries. Atherosclerosis 2009, 203, 112-118.
34. de la Cuesta, F., Alvarez-Llamas, G., Maroto, A. S., Donado, A. et al., A proteomic focus on the alterations occurring at the human atherosclerotic coronary intima. Mol. Cell Proteom. 2011, 10, M110 003517.
35. Malaud, E., Piquer, D., Merle, D., Molina, L. et al., Carotid atherosclerotic plaques: proteomics study after a low-abundance protein enrichment step. Electrophoresis 2012, 33, 470-482.
36. Bagnato, C., Thumar, J., Mayya, V., Hwang, S. I. et al., Proteomics analysis of human coronary atherosclerotic plaque: a feasibility study of direct tissue proteomics by liquid chromatography and tandem mass spectrometry. Mol. Cell Proteom. 2007, 6, 1088-1102.
37. Kardys, I., Rifai, N., Meilhac, O., Michel, J. B. et al., Plasma concentration of heat shock protein 27 and risk of cardiovascular disease: a prospective, nested case-control study. Clin. Chem. 2008, 54, 139-146.
38. Petrak, J., Ivanek, R., Toman, O., Cmejla, R. et al., Deja vu in proteomics. A hit parade of repeatedly identified differentially expressed proteins. Proteomics 2008, 8, 1744-1749.
39. Blanco-Colio, L. M., Martin-Ventura, J. L., Carrero, J. J., Yilmaz, M. I. et al., Vascular proteomics and the discovery process of clinical biomarkers: the case of TWEAK. Proteom. Clin. Appl. 2011, 5, 281-288.
40. Pasterkamp, G., Schoneveld, A. H., van der Wal, A. C., Hijnen, D. J. et al., Inflammation of the atherosclerotic cap and shoulder of the plaque is a common and locally observed feature in unruptured plaques of femoral and coronary arteries. Arterioscler. Thromb. Vasc. Biol. 1999, 19, 54-58.
41. Hellings, W. E., Peeters, W., Moll, F. L., Piers, S. R. et al., Composition of carotid atherosclerotic plaque is associated with cardiovascular outcome: a prognostic study. Circulation 2010, 121, 1941-1950.
42. Verhoeven, B. A., Velema, E., Schoneveld, A. H., de Vries, J. P. et al., Athero-express: differential atherosclerotic plaque expression of mRNA and protein in relation to cardiovascular events and patient characteristics. Rationale and design. Eur. J. Epidemiol. 2004, 19, 1127-1133.
43. de Kleijn, D. P., Moll, F. L., Hellings, W. E., Ozsarlak-Sozer, G. et al., Local atherosclerotic plaques are a source of prognostic biomarkers for adverse cardiovascular events. Arterioscler. Thromb. Vasc. Biol. 2010, 30, 612-619.
44. Peeters, W., de Kleijn, D. P., Vink, A., van de Weg, S. et al., Adipocyte fatty acid binding protein in atherosclerotic plaques is associated with local vulnerability and is predictive for the occurrence of adverse cardiovascular events. Eur. Heart. J. 2011, 32, 1758-1768.
45. Furuhashi, M., Tuncman, G., Gorgun, C. Z., Makowski, L. et al., Treatment of diabetes and atherosclerosis by inhibiting fatty-acid-binding protein aP2. Nature 2007, 447, 959-965.
46. Mause, S. F., Weber, C., Microparticles: protagonists of a novel communication network for intercellular information exchange. Circ. Res. 2010, 107, 1047-1057.
47. Jy, W., Horstman, L. L., Jimenez, J. J., Ahn, Y. S. et al., Measuring circulating cell-derived microparticles. J. Thromb. Haemost. 2004, 2, 1842-1851.
48. Morel, O., Morel, N., Hugel, B., Jesel, L. et al., The significance of circulating microparticles in physiology, inflammatory and thrombotic diseases. Rev. Med. Intern. 2005, 26, 791-801.
49. Davila, M., Amirkhosravi, A., Coll, E., Desai, H. et al., Tissue factor-bearing microparticles derived from tumor cells: impact on coagulation activation. J. Thromb. Haemost. 2008, 6, 1517-1524.
50. Mack, M., Kleinschmidt, A., Bruhl, H., Klier, C. et al., Transfer of the chemokine receptor CCR5 between cells by membrane-derived microparticles: a mechanism for cellular human immunodeficiency virus 1 infection. Nat. Med. 2000, 6, 769-775.
51. Bernal-Mizrachi, L., Jy, W., Jimenez, J. J., Pastor, J. et al., High levels of circulating endothelial microparticles in patients with acute coronary syndromes. Am. Heart J. 2003, 145, 962-970.
52. Boulanger, C. M., Amabile, N., Tedgui, A., Circulating microparticles: a potential prognostic marker for atherosclerotic vascular disease. Hypertension 2006, 48, 180-186.
53. Boulanger, C. M., Scoazec, A., Ebrahimian, T., Henry, P. et al., Circulating microparticles from patients with myocardial infarction cause endothelial dysfunction. Circulation 2001, 104, 2649-2652.
54. Martinez, M. C., Tual-Chalot, S., Leonetti, D., Andriantsitohaina, R., Microparticles: targets and tools in cardiovascular disease. Trends Pharmacol. Sci. 2011, 32, 659-665.
55. Rautou, P. E., Vion, A. C., Amabile, N., Chironi, G. et al., Microparticles, vascular function, and atherothrombosis. Circ. Res. 2011, 109, 593-606.
56. Gyorgy, B., Szabo, T. G., Pasztoi, M., Pal, Z. et al., Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol. Life Sci. 2011, 68, 2667-2688.
57. VanWijk, M. J., VanBavel, E., Sturk, A., Nieuwland, R., Microparticles in cardiovascular diseases. Cardiovasc. Res. 2003, 59, 277-287.
58. Mallat, Z., Benamer, H., Hugel, B., Benessiano, J. et al., Elevated levels of shed membrane microparticles with procoagulant potential in the peripheral circulating blood of patients with acute coronary syndromes. Circulation 2000, 101, 841-843.
59. Morel, O., Pereira, B., Averous, G., Faure, A. et al., Increased levels of procoagulant tissue factor-bearing microparticles within the occluded coronary artery of patients with ST-segment elevation myocardial infarction: role of endothelial damage and leukocyte activation. Atherosclerosis 2009, 204, 636-641.
60. Sinning, J. M., Losch, J., Walenta, K., Bohm, M. et al., Circulating CD31+/annexin V+ microparticles correlate with cardiovascular outcomes. Eur. Heart J. 2011, 32, 2034-2041.
61. Garcia, B. A., Smalley, D. M., Cho, H., Shabanowitz, J. et al., The platelet microparticle proteome. J. Proteome. Res. 2005, 4, 1516-1521.
62. Dean, W. L., Lee, M. J., Cummins, T. D., Schultz, D. J., Powell, D. W., Proteomic and functional characterisation of platelet microparticle size classes. Thromb. Haemost. 2009, 102, 711-718.
63. Peterson, D. B., Sander, T., Kaul, S., Wakim, B. T. et al., Comparative proteomic analysis of PAI-1 and TNF-alpha-derived endothelial microparticles. Proteomics 2008, 8, 2430-2446.
64. Rubin, O., Crettaz, D., Tissot, J. D., Lion, N., Pre-analytical and methodological challenges in red blood cell microparticle proteomics. Talanta 2010, 82, 1-8.
65. Pasterkamp, G., Daemen, M., Circulating cells: the biofactory for markers of atherosclerotic disease. Eur. Heart J. 2008, 29, 2701-2702.
66. Liuzzo, G., Angiolillo, D. J., Buffon, A., Rizzello, V. et al., Enhanced response of blood monocytes to in vitro lipopolysaccharide-challenge in patients with recurrent unstable angina. Circulation 2001, 103, 2236-2241.
67. Versteeg, D., Hoefer, I. E., Schoneveld, A. H., de Kleijn, D. P. et al., Monocyte toll-like receptor 2 and 4 responses and expression following percutaneous coronary intervention: association with lesion stenosis and fractional flow reserve. Heart 2008, 94, 770-776.
68. Barderas, M. G., Tunon, J., Darde, V. M., De la Cuesta, F. et al., Circulating human monocytes in the acute coronary syndrome express a characteristic proteomic profile. J. Proteome Res. 2007, 6, 876-886.
69. Barderas, M. G., Tunon, J., Darde, V. M., De la Cuesta, F. et al., Atorvastatin modifies the protein profile of circulating human monocytes after an acute coronary syndrome. Proteomics 2009, 9, 1982-1993.
70. Bleijerveld, O. B., Wijten, P., Cappadona, S., McClellan, E. A. et al., Deep proteome profiling of circulating granulocytes reveals bactericidal/permeability-increasing protein as a biomarker for severe atherosclerotic coronary stenosis. J. Proteome. Res. 2012, 11, 5235-5244.
71. Farley, A. R., Link, A. J., Identification and quantification of protein posttranslational modifications. Methods Enzymol. 2009, 463, 725-763.
72. Van Eyk, J. E., Overview: the maturing of proteomics in cardiovascular research. Circ. Res. 2011, 108, 490-498.
73. Baynes, J. W., The clinical chemome: a tool for the diagnosis and management of chronic disease. Clin. Chem. 2004, 50, 1116-1117.
74. Izquierdo-Alvarez, A., Martinez-Ruiz, A., Thiol redox proteomics seen with fluorescent eyes: the detection of cysteine oxidative modifications by fluorescence derivatization and 2-DE. J. Proteom. 2011, 75, 329-338.
75. Butterfield, D. A., Dalle-Donne, I., Redox proteomics. Antioxid. Redox. Signal 2012, 17, 1487-1489.
76. Fu, C., Hu, J., Liu, T., Ago, T. et al., Quantitative analysis of redox-sensitive proteome with DIGE and ICAT. J. Proteome Res. 2008, 7, 3789-3802.
77. Held, J. M., Gibson, B. W., Regulatory control or oxidative damage? Proteomic approaches to interrogate the role of cysteine oxidation status in biological processes. Mol. Cell Proteomics 2012, 11, R111 013037.
78. Izquierdo-Alvarez, A., Ramos, E., Villanueva, J., Hernansanz-Agustin, P. et al., Differential redox proteomics allows identification of proteins reversibly oxidized at cysteine residues in endothelial cells in response to acute hypoxia. J. Proteom. 2012, 75, 5449-5462.
79. Chen, S. C., Huang, B., Liu, Y. C., Shyu, K. G. et al., Acute hypoxia enhances proteins' S-nitrosylation in endothelial cells. Biochem. Biophys. Res. Comm. 2008, 377, 1274-1278.
80. Zimman, A., Chen, S. S., Komisopoulou, E., Titz, B. et al., Activation of aortic endothelial cells by oxidized phospholipids: a phosphoproteomic analysis. J. Proteome. Res. 2010, 9, 2812-2824.
81. Ashraf, M. Z., Kar, N. S., Podrez, E. A., Oxidized phospholipids: biomarker for cardiovascular diseases. Int. J. Biochem. Cell Biol. 2009, 41, 1241-1244.
82. Lee, S., Birukov, K. G., Romanoski, C. E., Springstead, J. R. et al., Role of phospholipid oxidation products in atherosclerosis. Circ. Res. 2012, 111, 778-799.
83. Smith, J. D., Dysfunctional HDL as a diagnostic and therapeutic target. Arterioscler. Thromb. Vasc. Biol. 2010, 30, 151-155.
84. Navab, M., Reddy, S. T., Van Lenten, B. J., Fogelman, A. M., HDL and cardiovascular disease: atherogenic and atheroprotective mechanisms. Nat. Rev. Cardiol. 2011, 8, 222-232.
85. Thorne, R. F., Mhaidat, N. M., Ralston, K. J., Burns, G. F., CD36 is a receptor for oxidized high density lipoprotein: implications for the development of atherosclerosis. FEBS Lett. 2007, 581, 1227-1232.
86. Zalewski, A., Macphee, C., Role of lipoprotein-associated phospholipase A2 in atherosclerosis: biology, epidemiology, and possible therapeutic target. Arterioscler. Thromb. Vasc. Biol. 2005, 25, 923-931.
87. Garcia-Arguinzonis, M., Padro, T., Lugano, R., Llorente-Cortes, V. et al., Low-density lipoproteins induce heat shock protein 27 dephosphorylation, oligomerization, and subcellular relocalization in human vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 2010, 30, 1212-1219.
88. Ghayour-Mobarhan, M., Saber, H., Ferns, G. A., The potential role of heat shock protein 27 in cardiovascular disease. Clinica Chimica Acta: Int. J. Clin. Chem. 2012, 413, 15-24.
89. Trott, D., McManus, C. A., Martin, J. L., Brennan, B. et al., Effect of phosphorylated hsp27 on proliferation of human endothelial and smooth muscle cells. Proteomics 2009, 9, 3383-3394.
90. Park, H. K., Park, E. C., Bae, S. W., Park, M. Y. et al., Expression of heat shock protein 27 in human atherosclerotic plaques and increased plasma level of heat shock protein 27 in patients with acute coronary syndrome. Circulation 2006, 114, 886-893.
91. Almofti, M. R., Huang, Z., Yang, P., Rui, Y., Proteomic analysis of rat aorta during atherosclerosis induced by high cholesterol diet and injection of vitamin D3. Clin. Exp. Pharmacol. Physiol. 2006, 33, 305-309.
92. Kilhovd, B. K., Juutilainen, A., Lehto, S., Ronnemaa, T. et al., High serum levels of advanced glycation end products predict increased coronary heart disease mortality in nondiabetic women but not in nondiabetic men: a population-based 18-year follow-up study. Arterioscler. Thromb. Vasc. Biol. 2005, 25, 815-820.
93. Sims, T. J., Rasmussen, L. M., Oxlund, H., Bailey, A. J., The role of glycation cross-links in diabetic vascular stiffening. Diabetologia 1996, 39, 946-951.
94. Basta, G., Schmidt, A. M., De Caterina, R., Advanced glycation end products and vascular inflammation: implications for accelerated atherosclerosis in diabetes. Cardiovasc. Res. 2004, 63, 582-592.
95. Hegab, Z., Gibbons, S., Neyses, L., Mamas, M. A., Role of advanced glycation end products in cardiovascular disease. World J. Cardiol. 2012, 4, 90-102.
96. Maillard-Lefebvre, H., Boulanger, E., Daroux, M., Gaxatte, C. et al., Soluble receptor for advanced glycation end products: a new biomarker in diagnosis and prognosis of chronic inflammatory diseases. Rheumatology 2009, 48, 1190-1196.
97. Wendt, T., Harja, E., Bucciarelli, L., Qu, W. et al., RAGE modulates vascular inflammation and atherosclerosis in a murine model of type 2 diabetes. Atherosclerosis 2006, 185, 70-77.
98. Jaisson, S., Pietrement, C., Gillery, P., Carbamylation-derived products: bioactive compounds and potential biomarkers in chronic renal failure and atherosclerosis. Clin. Chem. 2011, 57, 1499-1505.
99. Apostolov, E. O., Ray, D., Savenka, A. V., Shah, S. V., Basnakian, A. G., Chronic uremia stimulates LDL carbamylation and atherosclerosis. J. Am. Soc. Nephrol.: JASN 2010, 21, 1852-1857.
100. Holzer, M., Gauster, M., Pfeifer, T., Wadsack, C. et al., Protein carbamylation renders high-density lipoprotein dysfunctional. Antioxidant. Redox Signal. 2011, 14, 2337-2346.
101. Apostolov, E. O., Shah, S. V., Ray, D., Basnakian, A. G., Scavenger receptors of endothelial cells mediate the uptake and cellular proatherogenic effects of carbamylated LDL. Arterioscler. Thromb. Vasc. Biol. 2009, 29, 1622-1630.
102. Apostolov, E. O., Shah, S. V., Ok, E., Basnakian, A. G., Quantification of carbamylated LDL in human sera by a new sandwich ELISA. Clin. Chem. 2005, 51, 719-728.
103. Karsdal, M. A., Henriksen, K., Leeming, D. J., Woodworth, T. et al., Novel combinations of post-translational modification (PTM) neo-epitopes provide tissue-specific biochemical markers-are they the cause or the consequence of the disease? Clin. Biochem. 2010, 43, 793-804.
104. Zhang, P., Kirk, J. A., Ji, W., Dos Remedios, C. G. et al., Multiple reaction monitoring to identify site-specific troponin I phosphorylated residues in the failing human heart. Circulation 2012, 126, 1828-1837.
105. Cima, I., Schiess, R., Wild, P., Kaelin, M. et al., Cancer genetics-guided discovery of serum biomarker signatures for diagnosis and prognosis of prostate cancer. Proc. Natl. Acad. Sci. U S A 2011, 108, 3342-3347.
106. Schiess, R., Wollscheid, B., Aebersold, R., Targeted proteomic strategy for clinical biomarker discovery. Mol. Oncol. 2009, 3, 33-44.
107. Surinova, S., Schiess, R., Huttenhain, R., Cerciello, F. et al., On the development of plasma protein biomarkers. J. Proteome. Res. 2011, 10, 5-16.
108. Roth, J., Protein N-glycosylation along the secretory pathway: relationship to organelle topography and function, protein quality control, and cell interactions. Chem. Rev. 2002, 102, 285-303.
109. Poste, G., Bring on the biomarkers. Nature 2011, 469, 156-157.
110. Delles, C., Schiffer, E., von Zur Muhlen, C., Peter, K. et al., Urinary proteomic diagnosis of coronary artery disease: identification and clinical validation in 623 individuals. J. Hypertens. 2010, 28, 2316-2322.
111. von zur Muhlen, C., Schiffer, E., Sackmann, C., Zurbig, P. et al., Urine proteome analysis reflects atherosclerotic disease in an ApoE-/- mouse model and allows the discovery of new candidate biomarkers in mouse and human atherosclerosis. Mol. Cell Proteom. 2012, 11, M111 013847.
112. Blanco-Colio, L. M., Martin-Ventura, J. L., Munoz-Garcia, B., Orbe, J. et al., Identification of soluble tumor necrosis factor-like weak inducer of apoptosis (sTWEAK) as a possible biomarker of subclinical atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2007, 27, 916-922.
113. Urbonaviciene, G., Martin-Ventura, J. L., Lindholt, J. S., Urbonavicius, S. et al., Impact of soluble TWEAK and CD163/TWEAK ratio on long-term cardiovascular mortality in patients with peripheral arterial disease. Atherosclerosis 2011, 219, 892-899.
114. Nishinari, M., Aoyama, N., Ogawa, Z., Yukino, S. et al., Phosphoglucomutase activity as a novel biomarker in patients with acute myocardial infarction. Circ. J. 2012, 76, 2197-2203.
115. Cubedo, J., Padro, T., Alonso, R., Cinca, J. et al., Differential proteomic distribution of TTR (pre-albumin) forms in serum and HDL of patients with high cardiovascular risk. Atherosclerosis 2012, 222, 263-269.