Comprehensive metabolomics identified lipid peroxidation as a prominent feature in human plasma of patients with coronary heart diseases

Redox Biology

Volumn 12, Issue , 2017, Pages 899-907

  Lu, Jianhong ^a,b,c   Chen, Buxing ^d   Chen, Tingting ^e   Guo, Shuyuan ^a,b,c,f   Xue, Xinli ^a,b,c   Chen, Qun ^a,b,c   Zhao, Mingming ^g   Xia, Lin ^a,c   Zhu, Zhengjiang ^e   Zheng, Lemin ^g   Yin, Huiyong ^a,b,c,f  

^a Chinese Academy of Sciences   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c BEIJING HOSPITAL   (China)

^d CAPITAL MEDICAL UNIVERSITY   (China)

^e SHANGHAI INSTITUTE OF ORGANIC CHEMISTRY   (China)

^f SHANGHAITECH UNIVERSITY   (China)

^g Peking University Health Science Center   (China)

Author keywords

Coronary heart disease (CHD); Isoprostanes; Lipid peroxidation; Lipidomics; Metabolomics; Myocardial infarction

Indexed keywords

ARACHIDONIC ACID; BIOLOGICAL MARKER; GLYCEROPHOSPHOLIPID; ISOPROSTANE DERIVATIVE; LINOLEIC ACID; PHOSPHOLIPID; POLYUNSATURATED FATTY ACID; PROSTAGLANDIN;

ADULT; AGED; ARTICLE; BLOOD ANALYSIS; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; FEMALE; HEART INFARCTION; HUMAN; ISCHEMIC HEART DISEASE; ISOMER; LIPID ANALYSIS; LIPID PEROXIDATION; MALE; METABOLITE; METABOLOMICS; MIDDLE AGED; OXIDATIVE STRESS; PATHOGENESIS; STABLE ANGINA PECTORIS; BLOOD; CASE CONTROL STUDY; CHEMISTRY; METABOLISM; PATHOLOGY; PLASMA; PROCEDURES;

ADULT; ANGINA, STABLE; BIOMARKERS; CASE-CONTROL STUDIES; FEMALE; GLYCEROPHOSPHOLIPIDS; HUMANS; LIPID PEROXIDATION; MALE; METABOLOMICS; MIDDLE AGED; MYOCARDIAL INFARCTION; OXIDATIVE STRESS; PLASMA;

EID: 85018441512     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2017.04.032     Document Type: Article

References (64)

1. [1] Steinberg, D., Witztum, J.L., Oxidized low-density lipoprotein and atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 30 (2010), 2311–2316.
2. [2] Steinbrecker, U.P., Parthasarathy, S., Leake, D.S., Witztum, J.L., Steinberg, D., Modification of low density lipoprotein by endothelial cells involves lipid peroxidation and degradation of low density lipoprotein phospholipids. Proc. Natl. Acad. Sci. USA 81 (1984), 3883–3887.
3. [3] Mozaffarian, D., Benjamin, E.J., Go, A.S., Arnett, D.K., Blaha, M.J., Cushman, M., Das, S.R., de Ferranti, S., Després, J.-P., Fullerton, H.J., Howard, V.J., Huffman, M.D., Isasi, C.R., Jiménez, M.C., Judd, S.E., Kissela, B.M., Lichtman, J.H., Lisabeth, L.D., Liu, S., Mackey, R.H., Magid, D.J., McGuire, D.K., Mohler, E.R., Moy, C.S., Muntner, P., Mussolino, M.E., Nasir, K., Neumar, R.W., Nichol, G., Palaniappan, L., Pandey, D.K., Reeves, M.J., Rodriguez, C.J., Rosamond, W., Sorlie, P.D., Stein, J., Towfighi, A., Turan, T.N., Virani, S.S., Woo, D., Yeh, R.W., Turner, M.B., Executive summary: heart disease and stroke statistics—2016 update: a report from the American Heart Association. Circulation 133 (2016), 447–454.
4. [4] Mozaffarian, D., Benjamin, E.J., Go, A.S., Arnett, D.K., Blaha, M.J., Cushman, M., Das, S.R., de Ferranti, S., Després, J.-P., Fullerton, H.J., Howard, V.J., Huffman, M.D., Isasi, C.R., Jiménez, M.C., Judd, S.E., Kissela, B.M., Lichtman, J.H., Lisabeth, L.D., Liu, S., Mackey, R.H., Magid, D.J., McGuire, D.K., Mohler, E.R., Moy, C.S., Muntner, P., Mussolino, M.E., Nasir, K., Neumar, R.W., Nichol, G., Palaniappan, L., Pandey, D.K., Reeves, M.J., Rodriguez, C.J., Rosamond, W., Sorlie, P.D., Stein, J., Towfighi, A., Turan, T.N., Virani, S.S., Woo, D., Yeh, R.W., Turner, M.B., heart disease and stroke statistics—2016 update: a report from the American Heart Association. Circulation 133 (2016), e38–e360.
5. [5] Glass, C.K., Witztu, J.L., Atherosclerosis: the road ahead. Cell 104 (2001), 503–516.
6. [6] Tsimikas, S., Lipoprotein(a): novel target and emergence of novel therapies to lower cardiovascular disease risk. Curr. Opin. Endocrinol. Diabetes Obes., 2016.
7. [7] Berliner, J.A., Navab, M., Folgelman, A.M., Frank, J.S., Demer, L.L., Edwards, P.A., Watson, A.D., Lusis, A.J., Atherosclerosis: basic mechanisms: oxidation, inflammation, and genetics. Circulation 91 (1995), 2488–2496.
8. [8] Berliner, J.A., Watson, A.D., A role for oxidized phospholipids in atherosclerosis. N. Engl. J. Med. 353 (2005), 9–11.
9. [9] Lee, S., Birukov, K.G., Romanoski, C.E., Springstead, J.R., Lusis, A.J., Berliner, J.A., Role of phospholipid oxidation products in atherosclerosis. Circ. Res. 111 (2012), 778–799.
10. [10] Tsimikas, S., Oxidative biomarkers in the diagnosis and prognosis of cardiovascular disease. Am. J. Cardiol. 98 (2006), 9P–17P.
11. [11] Yin, H., Xu, L., Porter, N.A., Free radical lipid peroxidation: mechanisms and analysis. Chem. Rev. 111 (2011), 5944–5972.
12. [12] Yin, H., Porter, N.A., New insights regarding the autoxidation of polyunsaturated fatty acids. Antioxid. Redox Signal. 7 (2005), 170–184.
13. [13] Moore, Kathryn J., and Tabas, I, Macrophages in the pathogenesis of atherosclerosis. Cell 145 (2011), 341–355.
14. [14] Podrez, E.A., Abu-Soud, H.M., Hazen, S.L., Myeloperoxidase-generated oxidants and atherosclerosis. Free Radic. Biol. Med. 28 (2000), 1717–1725.
15. [15] Podrez, E.A., Schmitt, D., Hoff, H.F., Hazen, S.L., Myeloperoxidase-generated reactive nitrogen species convert LDL into an atherogenic form in vitro. J. Clin. Investig. 103 (1999), 1547–1560.
16. [16] Hazell, L.J., Davies, M.J., Stocker, R., Secondary radicals derived from chloramines of apolipoprotein B-100 contribute to HOCl-induced lipid peroxidation of low-density lipoproteins. Biochem. J. 339 (1999), 489–495.
17. [17] Malle, E., Marsche, G., Arnhold, J., Davies, M.J., Modification of low-density lipoprotein by myeloperoxidase-derived oxidants and reagent hypochlorous acid. Biochim. Et. Biophys. Acta (BBA) - Mol. Cell Biol. Lipids 1761 (2006), 392–415.
18. [18] McIntyre, T.M., Prescott, S.M., Stafforini, D.M., The emerging roles of PAF acetylhydrolase. J. Lipid Res. 50 (2009), S255–S259.
19. [19] Milne, G.L., Yin, H., Hardy, K.D., Davies, S.S., Roberts, L.J., Isoprostane generation and function. Chem. Rev. 111 (2011), 5973–5996.
20. [20] Yin, H., Zhou, Y., Zhu, M., Hou, S., Li, Z., Zhong, H., Lu, J., Meng, T., Wang, J., Xia, L., Xu, Y., Wu, Y., Role of mitochondria in programmed cell death mediated by arachidonic acid-derived eicosanoids. Mitochondrion 13 (2013), 209–224.
21. [21] Funk, C.D., Prostaglandins and Leukotrienes: advances in eicosanoid biology. Science 294 (2001), 1871–1875.
22. [22] Lu, J., Guo, S., Xue, X., Chen, Q., Ge, J., Zhuo, Y., Zhong, H., Chen, B., Zhao, M., Han, W., Suzuki, T., Zhu, M., Xia, L., Schneider, C., Blackwell, T.S., Porter, N.A., Zheng, L., Tsimikas, S., Yin, H., Identification of a novel series of anti-inflammatory and anti-oxidative phospholipid oxidation products containing cyclopentenone moiety in vitro and in vivo: implication in atherosclerosis. J. Biol. Chem., 2017.
23. [23] Rhee, E.P., Gerszten, R.E., Metabolomics and cardiovascular biomarker discovery. Clin. Chem. 58 (2012), 139–147.
24. [24] Martinez-Gonzalez, M.A., Ruiz-Canela, M., Hruby, A., Liang, L., Trichopoulou, A., Hu, F.B., Intervention trials with the mediterranean diet in cardiovascular prevention: understanding potential mechanisms through metabolomic profiling. J. Nutr., 2016.
25. [25] Shah, S.H., Bain, J.R., Muehlbauer, M.J., Stevens, R.D., Crosslin, D.R., Haynes, C., Dungan, J., Newby, L.K., Hauser, E.R., Ginsburg, G.S., Newgard, C.B., Kraus, W.E., Association of a peripheral blood metabolic profile with coronary artery disease and risk of subsequent cardiovascular events. Circ.-Cardiovasc. Genet. 3 (2010), 207–U233.
26. [26] Liu, X., Gao, J., Chen, J., Wang, Z., Shi, Q., Man, H., Guo, S., Wang, Y., Li, Z., Wang, W., Identification of metabolic biomarkers in patients with type 2 diabetic coronary heart diseases based on metabolomic approach. Sci. Rep., 6, 2016, 30785.
27. [27] Guo, W., Jiang, C., Yang, L., Li, T., Liu, X., Jin, M., Qu, K., Chen, H., Jin, X., Liu, H., Zhu, H., Wang, Y., Quantitative metabolomic profiling of plasma, urine, and liver extracts by 1H NMR spectroscopy characterizes different stages of atherosclerosis in hamsters. J. Proteome Res. 15 (2016), 3500–3510.
28. [28] Garcia-Fontana, B., Morales-Santana, S., Diaz Navarro, C., Rozas-Moreno, P., Genilloud, O., Vicente Perez, F., Perez del Palacio, J., Munoz-Torres, M., Metabolomic profile related to cardiovascular disease in patients with type 2 diabetes mellitus: a pilot study. Talanta 148 (2016), 135–143.
29. [29] Barallobre-Barreiro, J., Chung, Y.L., Mayr, M., Proteomics and metabolomics for mechanistic insights and biomarker discovery in cardiovascular disease. Rev. Esp. De. Cardiol. 66 (2013), 657–661.
30. [30] Fan, Y., Li, Y., Chen, Y., Zhao, Y.J., Liu, L.W., Li, J., Wang, S.L., Alolga, R.N., Yin, Y., Wang, X.M., Zhao, D.S., Shen, J.H., Meng, F.Q., Zhou, X., Xu, H., He, G.P., Lai, M.D., Li, P., Zhu, W., Qi, L.W., Comprehensive metabolomic characterization of coronary artery diseases. J. Am. Coll. Cardiol. 68 (2016), 1281–1293.
31. [31] Baig, F., Pechlaner, R., Mayr, M., Caveats of untargeted metabolomics for biomarker discovery∗. J. Am. Coll. Cardiol. 68 (2016), 1294–1296.
32. [32] Wang, J.L., Zhang, T., Shen, X.T., Liu, J., Zhao, D.L., Sun, Y.W., Wang, L., Liu, Y.J., Gong, X.Y., Liu, Y.X., Zhu, Z.J., Xue, F.Z., Serum metabolomics for early diagnosis of esophageal squamous cell carcinoma by UHPLC-QTOF/MS. Metabolomics, 12, 2016.
33. [33] Kuhl, C., Tautenhahn, R., Bottcher, C., Larson, T.R., Neumann, S., CAMERA: an integrated strategy for compound spectra extraction and annotation of liquid chromatography/mass spectrometry data sets. Anal. Chem. 84 (2012), 283–289.
34. [34] Dunn, W.B., Broadhurst, D., Begley, P., Zelena, E., Francis-McIntyre, S., Anderson, N., Brown, M., Knowles, J.D., Halsall, A., Haselden, J.N., Nicholls, A.W., Wilson, I.D., Kell, D.B., Goodacre, R., H. S. M. H, C., Procedures for large-scale metabolic profiling of serum and plasma using gas chromatography and liquid chromatography coupled to mass spectrometry. Nat. Protoc. 6 (2011), 1060–1083.
35. [35] Yin, H., Cox, B.E., Liu, W., Porter, N.A., Morrow, J.D., Milne, G.L., Identification of intact oxidation products of glycerophospholipids in vitro and in vivo using negative ion electrospray iontrap mass spectrometry. J. Mass Spectrom. 44 (2009), 672–680.
36. [36] Huang, Y., Zhu, M., Li, Z., Sa, R., Chu, Q., Zhang, Q., Zhang, H., Tang, W., Zhang, M., Yin, H., Mass spectrometry-based metabolomic profiling identifies alterations in salivary redox status and fatty acid metabolism in response to inflammation and oxidative stress in periodontal disease. Free Radic. Biol. Med. 70 (2014), 223–232.
37. [37] Yao, X., Sa, R., Ye, C., Zhang, D., Zhang, S., Xia, H., Wang, Y.-c., Jiang, J., Yin, H., Ying, H., Effects of thyroid hormone status on metabolic pathways of arachidonic acid in mice and humans: a targeted metabolomic approach. Prostaglandins Other Lipid Mediat. 118–119 (2015), 11–18.
38. [38] Kurano, M., Kano, K., Dohi, T., Matsumoto, H., Igarashi, K., Nishikawa, M., Ohkawa, R., Ikeda, H., Miyauchi, K., Daida, H., Aoki, J., Yatomi, Y., Different origins of lysophospholipid mediators between coronary and peripheral arteries in acute coronary syndrome. J. Lipid Res. 58 (2017), 433–442.
39. [39] Norris, P.C., Gosselin, D., Reichart, D., Glass, C.K., Dennis, E.A., Phospholipase A2 regulates eicosanoid class switching during inflammasome activation. Proc. Natl. Acad. Sci. USA, 2014.
40. [40] Dennis, E.A., Norris, P.C., Eicosanoid storm in infection and inflammation. Nat. Rev. Immunol. 15 (2015), 511–523.
41. [41] Kougias, P., Chai, H., Lin, P.H., Lumsden, A.B., Yao, Q., Chen, C., Lysophosphatidylcholine and secretory phospholipase A2 in vascular disease: mediators of endothelial dysfunction and atherosclerosis. Med. Sci. Monit.: Int. Med. J. Exp. Clin. Res. 12 (2006), RA5–RA16.
42. [42] Schmitz, G., Ruebsaamen, K., Metabolism and atherogenic disease association of lysophosphatidylcholine. Atherosclerosis 208 (2010), 10–18.
43. [43] Morrow, J.D., Quantification of isoprostanes as indices of oxidant stress and the risk of atherosclerosis in humans. Arterioscler. Thromb. Vasc. Biol. 25 (2005), 279–286.
44. [44] Witztum, J.L., Lichtman, A.H., The influence of innate and adaptive immune responses on atherosclerosis. Annu. Rev. Pathol. 9 (2014), 73–102.
45. [45] Fraley, A.E., Schwartz, G.G., Olsson, A.G., Kinlay, S., Szarek, M., Rifai, N., Libby, P., Ganz, P., Witztum, J.L., Tsimikas, S., Relationship of oxidized phospholipids and biomarkers of oxidized low-density lipoprotein with cardiovascular risk factors, inflammatory biomarkers, and effect of statin therapy in patients with acute coronary syndromes: results from the MIRACL (Myocardial Ischemia Reduction with Aggressive Cholesterol Lowering) trial. J. Am. Coll. Cardiol. 53 (2009), 2186–2196.
46. [46] Tsimikas, S., Brilakis, E.S., Miller, E.R., McConnell, J.P., Lennon, R.J., Kornman, K.S., Witztum, J.L., Berger, P.B., Oxidized phospholipids, Lp(a) lipoprotein, and coronary artery disease. N. Engl. J. Med. 353 (2005), 46–57.
47. [47] Tsimikas, S., Witztum, J.L., The role of oxidized phospholipids in mediating lipoprotein(a) atherogenicity. Curr. Opin. Lipidol. 19 (2008), 369–377.
48. [48] Bretscher, P., Egger, J., Shamshiev, A., Trotzmuller, M., Kofeler, H., Carreira, E.M., Kopf, M., Freigang, S., Phospholipid oxidation generates potent anti-inflammatory lipid mediators that mimic structurally related pro-resolving eicosanoids by activating Nrf2. EMBO Mol. Med. 7 (2015), 593–607.
49. [49] Kadl, A., Sharma, P.R., Chen, W.S., Agrawal, R., Meher, A.K., Rudraiah, S., Grubbs, N., Sharma, R., Leitinger, N., Oxidized phospholipid-induced inflammation is mediated by Toll-like receptor 2. Free Radic. Biol. Med. 51 (2011), 1903–1909.
50. [50] Podrez, E.A., Poliakov, E., Shen, Z., Zhang, R., Deng, Y., Sun, M., Finton, P.J., Shan, L., Febbraio, M., Hajjar, D.P., Silverstein, R.L., Hoff, H.F., Salomon, R.G., Hazen, S.L., A novel family of atherogenic oxidized phospholipids promotes macrophage foam cell formation via the scavenger receptor CD36 and is enriched in atherosclerotic lesions. J. Biol. Chem. 277 (2002), 38517–38523.
51. [51] Liu, W., Morrow, J.D., Yin, H., Quantification of F2-isoprostanes as a reliable index of oxidative stress in vivo using gas chromatography-mass spectrometry (GC-MS) method. Free Radic. Biol. Med. 47 (2009), 1101–1107.
52. [52] Spiteller, G., Linoleic acid peroxidation - the dominant lipid peroxidation process in low density lipoprotein - and its relationship to chronic diseases. Chem. Phys. Lipids 95 (1998), 105–162.
53. [53] Liu, W., Yin, H., Akazawa, Y.O., Yoshida, Y., Niki, E., Porter, N.A., Ex vivo oxidation in tissue and plasma assays of Hydroxyoctadecadienoates: Z,E/E,E stereoisomer ratios. Chem. Res. Toxicol. 23 (2010), 986–995.
54. [54] Ravandi, A., Leibundgut, G., Hung, M.Y., Patel, M., Hutchins, P.M., Murphy, R.C., Prasad, A., Mahmud, E., Miller, Y.I., Dennis, E.A., Witztum, J.L., Tsimikas, S., Release and capture of bioactive oxidized phospholipids and oxidized cholesteryl esters during percutaneous coronary and peripheral arterial interventions in humans. J. Am. Coll. Cardiol. 63 (2014), 1961–1971.
55. [55] Choi, S.H., Yin, H., Ravandi, A., Armando, A., Dumlao, D., Kim, J., Almazan, F., Taylor, A.M., McNamara, C.A., Tsimikas, S., Dennis, E.A., Witztum, J.L., Miller, Y.I., Polyoxygenated cholesterol ester hydroperoxide activates TLR4 and SYK dependent signaling in macrophages. PLoS One, 8, 2013, e83145.
56. [56] Yin, H., Davis, T., Porter, N.A., Simultaneous analysis of multiple lipid oxidation products in vivo by liquid chromatographic-mass spectrometry (LC-MS). Methods Mol. Biol. 610 (2010), 375–386.
57. 2 is generated from the isoprostane pathway and not the cyclooxygenase in humans. J. Biol. Chem. 282 (2007), 329–336.
58. [58] Zhang, S., Zhang, S., Wang, H., Wu, W., Ye, Y., Arginine methylation dysfunction increased risk of acute coronary syndrome in coronary artery disease population: a case-control study. Medicine, 96, 2017, e6074.
59. [59] Polyzos, K.A., Ketelhuth, D.F.J., The role of the kynurenine pathway of tryptophan metabolism in cardiovascular disease. An emerging field. Hamostaseologie 35 (2015), 128–136.
60. [60] Murr, C., Grammer, T.B., Kleber, M.E., Meinitzer, A., Marz, W., Fuchs, D., Low serum tryptophan predicts higher mortality in cardiovascular disease. Eur. J. Clin. Investig. 45 (2015), 247–254.
61. [61] Yu, E., Ruiz-Canela, M., Guasch-Ferre, M., Zheng, Y., Toledo, E., Clish, C.B., Salas-Salvado, J., Liang, L., Wang, D.D., Corella, D., Fito, M., Gomez-Gracia, E., Lapetra, J., Estruch, R., Ros, E., Cofan, M., Aros, F., Romaguera, D., Serra-Majem, L., Sorli, J.V., Hu, F.B., Martinez-Gonzalez, M.A., Increases in plasma tryptophan are inversely associated with incident cardiovascular disease in the Prevencion con Dieta Mediterranea (PREDIMED) Study. J. Nutr., 2017.
62. [62] FitzGerald, Garret A, Human platelet lipidomics: variance, visualization, flux, and fuel. Cell Metab. 23 (2016), 757–759.
63. [63] Capoulade, R., Chan, K.L., Yeang, C., Mathieu, P., Bossé, Y., Dumesnil, J.G., Tam, J.W., Teo, K.K., Mahmut, A., Yang, X., Witztum, J.L., Arsenault, B.J., Després, J.-P., Pibarot, P., Tsimikas, S., Oxidized phospholipids, lipoprotein(a), and progression of calcific aortic valve stenosis. J. Am. Coll. Cardiol. 66 (2015), 1236–1246.
64. [64] S. Li, Q. Chu, J. Ma, Y. Sun, T. Tao, R. Huang, Y. Liao, J. Yue, J. Zheng, L. Wang, X. Xue, M. Zhu, X. Kang, H. Yin, W. Liu, Discovery of novel lipid profiles in PCOS: Do insulin and androgen oppositely regulate bioactive lipid production? J. Clin. Endocrinol. Metab. 2016. jc20162692.