Top-down lipidomics of low density lipoprotein reveal altered lipid profi les in advanced chronic kidney disease

Journal of Lipid Research

Volumn 56, Issue 2, 2015, Pages 413-422

  Reis, Ana ^a   Rudnitskaya, Alisa ^b   Chariyavilaskul, Pajaree ^c,e   Dhaun, Neeraj ^c,d   Melville, Vanessa ^c   Goddard, Jane ^d   Webb, David J ^c   Pitt, Andrew R ^d   Spickett, Corinne M ^a  

^a ASTON UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF AVEIRO   (Portugal)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d ROYAL INFIRMARY OF EDINBURGH   (United Kingdom)

^e CHULALONGKORN UNIVERSITY   (Thailand)

Author keywords

Cholesterol; Cholesterol sulfate; Dyslipidemias; Inflammation; Mass spectrometry; N acyltaurine; Partial least squares discriminant analysis; Phospholipids

Indexed keywords

C REACTIVE PROTEIN; CERAMIDE; CHOLESTEROL; CHOLESTEROL SULFATE; CREATININE; GLUCOSE; HEMOGLOBIN A1C; HIGH DENSITY LIPOPROTEIN; INTERLEUKIN 6; LIPID; LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; N ACYLTAURINE; OXIDIZED LOW DENSITY LIPOPROTEIN; PHOSPHATIDYLCHOLINE; PLASMENYL ETHANOLAMINE; SULFATIDE; TAURINE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; UNSATURATED PHOSPHOLIPID; CHOLESTEROL ESTER; PHOSPHOLIPID;

ADULT; AGE; ARTICLE; BLOOD PRESSURE MEASUREMENT; BODY MASS; CHEMOMETRICS; CHOLESTEROL BLOOD LEVEL; CHRONIC KIDNEY DISEASE; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GLOMERULUS FILTRATION RATE; GLUCOSE BLOOD LEVEL; HUMAN; INTERMETHOD COMPARISON; LIPID ANALYSIS; LIPID BLOOD LEVEL; LIPIDOMICS; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; MIDDLE AGED; PROTEIN ISOLATION; BLOOD; CHRONIC KIDNEY FAILURE; LIPID METABOLISM; PHYSIOLOGY; RISK FACTOR;

ADULT; CHOLESTEROL; CHOLESTEROL ESTERS; HUMANS; LIPID METABOLISM; LIPIDS; LIPOPROTEINS, LDL; MALE; MASS SPECTROMETRY; MIDDLE AGED; PHOSPHATIDYLCHOLINES; PHOSPHOLIPIDS; RENAL INSUFFICIENCY, CHRONIC; RISK FACTORS; TRIGLYCERIDES;

EID: 84921918212     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M055624     Document Type: Article

References (53)

1. Meguid El Nahas, A., and A. K. Bello . 2005 . Chronic kidney disease: the global challenge. Lancet . 365 : 331-340 .
2. Sarnak, M. J., A. S. Levey, A. C. Schoolwerth, J. Coresh, B. Culleton, L. L. Hamm, P. A. McCullough, B. L. Kasiske, E. Kelepouris, M. J. Klag, et al . 2003 . Kidney disease as a risk factor for development of cardiovascular disease: a statement from the American Heart Association councils on kidney in cardiovascular disease, high blood pressure research, clinical cardiology, and epidemiology and prevention. Circulation . 108 : 2154-2169 .
3. Schiffrin, E. L., M. L. Lipman, and J. F. E. Mann . 2007 . Chronic kidney disease: effects on the cardiovascular system. Circulation . 116 : 85-97 .
4. Zoccali, C. 2006 . Traditional and emerging cardiovascular and renal risk factors: an epidemiologic perspective. Kidney Int. 70 : 26-33 .
5. Steinberg, D. 2005 . Hypercholesterolemia and infl ammation in atherogenesis: two sides of the same coin. Mol. Nutr. Food Res. 49 : 995-998 .
6. Shepherd, J. 2004 . Lipids in health and disease. Biochem. Soc. Trans. 32 : 1051-1056 .
7. Keane, W. F., J. E. Tomassini, and D. R. Neff . 2013 . Lipid abnormalities in patients with chronic kidney disease: implications for the pathophysiology of atherosclerosis. J. Atheroscler. Thromb. 20 : 123-133 .
8. Cheung, A. K. 2009 . Is lipid control necessary in hemodialysis patients?Clin. J. Am. Soc. Nephrol. 4 : S95-S101 .
9. Kaysen, G. A. 2009 . Lipid and lipoprotein metabolism in chronic kidney disease. J. Ren. Nutr. 19 : 73-77 .
10. Vaziri, N. D., and K. Norris . 2011 . Lipid disorders and their relevance to outcomes in chronic kidney disease. Blood Purif. 31 : 189-196 .
11. Lacquaniti, A., D. Bolignano, V. Donato, C. Bono, M. R. Fazio, and M. Buemi . 2010 . Alterations of lipid metabolism in chronic nephropathies: mechanisms, diagnosis and treatment. Kidney Blood Press. Res. 33 : 100-110 .
12. Romanowicz, L., and E. Bankowski . 2010 . Sphingolipids of human umbilical cord vein and their alteration in preeclampsia. Mol. Cell. Biochem. 340 : 81-89 .
13. Barber, M. N., S. Risis, C. Yang, P. J. Meikle, M. Staples, M. A. Febbraio, and C. R. Bruce . 2012 . Plasma lysophosphatidylcholine levels are reduced in obesity and type 2 diabetes. PLoS ONE . 7 : e41456 .
14. Giera, M., A. Ioan-Facsinay, R. Toes, F. Gao, J. Dalli, A. M. Deelder, C. N. Serhan, and O. A. Mayboroda . 2012 . Lipid and lipid mediator profi ling of human synovial fl uid in rheumatoid arthritis patients by means of LC-MS/MS. Biochim. Biophys. Acta . 1821 : 1415-1424 .
15. Sewell, G. W., Y. A. Hannun, X. Han, G. Koster, J. Bielawski, V. Goss, P. J. Smith, F. Z. Rahman, R. Vega, S. L. Bloom, et al . 2012 . Lipidomic profi ling in Crohn's disease: abnormalities in phosphatidylinositols, with preservation of ceramide, phosphatidylcholine and phosphatidylserine composition. Int. J. Biochem. Cell Biol. 44 : 1839-1846 .
16. Jia, L., C. Wang, S. Zhao, X. Lu, and G. Xu . 2007 . Metabolomic identifi cation of potential phospholipid biomarkers for chronic glomerulonephritis by using high performance liquid chromatog-raphy- mass spectrometry. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 860 : 134-140 .
17. Hu, R., G. Li, Y. Kamijo, T. Aoyama, T. Nakajima, T. Inoue, K. Node, R. Kannagi, M. Kyogashima, and A. Hara . 2007 . Serum sulfatides as a novel biomarker for cardiovascular disease in patients with end-stage renal failure. Glycoconj. J. 24 : 565-571 .
18. Han, X., K. Yang, and R. W. Gross . 2012 . Multi-dimensional mass spectrometry-based shotgun lipidomics and novel strategies for lipidomic analyses. Mass Spectrom. Rev. 31 : 134-178 .
19. Lam, S. M., and G. H. Shui . 2013 . Lipidomics as a principal tool for advancing biomedical research. J. Genet. Genomics . 40 : 375-390 .
20. Schwudke, D., K. Schuhmann, R. Herzog, S. R. Bornstein, and A. Shevchenko . 2011 . Shotgun lipidomics on high resolution mass spectrometers. Cold Spring Harb. Perspect. Biol . 3 : a004614 .
21. Schwudke, D., J. T. Hannich, V. Surendranath, V. Grimard, T. Moehring, L. Burton, T. Kurzchalia, and A. Shevchenko . 2007 . Top-down lipidomic screens by multivariate analysis of high-resolution survey mass spectra. Anal. Chem. 79 : 4083-4093 .
22. Stegemann, C., I. Drozdov, J. Shalhoub, J. Humphries, C. Ladroue, A. Didangelos, M. Baumert, M. Allen, A. H. Davies, C. Monaco, et al . 2011 . Comparative lipidomics profi ling of human atherosclerotic plaques. Circ. Cardiovasc. Genet . 4 : 232-242 .
23. Stegemann, C., R. Pechlaner, P. Willeit, S. R. Langley, M. Mangino, U. Mayr, C. Menni, A. Moayyeri, P. Santer, G. Rungger, et al . 2014 . Lipidomics profi ling and risk of cardiovascular disease in the prospective population-based Bruneck study. Circulation . 129 : 1821-1831 .
24. Reis, A., A. Rudnitskaya, G. J. Blackburn, N. M. Fauzi, A. R. Pitt, and C. M. Spickett . 2013 . A comparison of fi ve lipid extraction solvent systems for lipidomic studies of human LDL. J. Lipid Res. 54 : 1812-1824 .
25. Lilitkarntakul, P., N. Dhaun, V. Melville, S. Blackwell, D. K. Talwar, B. Liebman, T. Asai, J. Pollock, J. Goddard, and D. J. Webb . 2011 . Blood pressure and not uraemia is the major determinant of arterial stiffness and endothelial dysfunction in patients with chronic kidney disease and minimal co-morbidity. Atherosclerosis . 216 : 217-225 .
26. Jerlich, A., A. R. Pitt, R. J. Schaur, and C. M. Spickett . 2000 . Pathways of phospholipid oxidation by HOCl in human LDL detected by LC-MS. Free Radic. Biol. Med. 28 : 673-682 .
27. Yue, H., S. A. Jansen, K. I. Strauss, M. R. Borenstein, M. F. Barbe, L. J. Rossi, and E. Murphy . 2007 . A liquid chromatography/mass spectrometric method for simultaneous analysis of arachidonic acid and its endogenous eicosanoid metabolites prostaglandins, dihydroxyeicosatrienoic acids, hydroxyeicosatetraenoic acids, and epoxyeicosatrienoic acids in rat brain tissue. J. Pharm. Biomed. Anal. 43 : 1122-1134 .
28. Mahley, R. W., T. L. Innerarity, S. C. Rall, Jr ., and K. H. Weisgraber . 1984 . Plasma lipoproteins: apolipoprotein structure and function. J. Lipid Res. 25 : 1277-1294 .
29. Zhao, B., S. Y. Tham, J. Lu, M. H. Lai, L. K. Lee, and S. M. Moochhala . 2004 . Simultaneous determination of vitamins C, E and beta-carotene in human plasma by high-performance liquid chromatography with photodiode-array detection. J. Pharm. Pharm. Sci. 7 : 200-204 .
30. Aldred, S., and H. R. Griffiths . 2004 . Oxidation of protein in human low-density lipoprotein exposed to peroxyl radicals facilitates uptake by monocytes; protection by antioxidants in vitro. Environ. Toxicol. Pharmacol. 15 : 111-117 .
31. Wishart, D. S., C. Knox, A. C. Guo, R. Eisner, N. Young, B. Gautam, D. D. Hau, N. Psychogios, E. Dong, S. Bouatra, et al . 2009 . HMDB: a knowledgebase for the human metabolome. Nucleic Acids Res. 37 : D603-D610 .
32. Scheltema, R. A., A. Jankevics, R. C. Jansen, M. A. Swertz, and R. Breitling . 2011 . PeakML/mzMatch: a fi le format, Java library, R library, and tool-chain for mass spectrometry data analysis. Anal. Chem. 83 : 2786-2793 .
33. Tautenhahn, R., G. J. Patti, D. Rinehart, and G. Siuzdak . 2012 . XCMS Online: a web-based platform to process untargeted metabolomic data. Anal. Chem. 84 : 5035-5039 .
34. Wold, S., M. Sjöström, and L. Eriksson . 2001 . PLS-regression: a basic tool of chemometrics. Chemom. Intell. Lab. Syst. 58 : 109-130 .
35. Barker, M., and W. Rayens . 2003 . Partial least squares for discrimination. J. Chemom. 17 : 166-173 .
36. Chi-Hyuck, J., S. H. Lee, H. S. Park, and J. H. Lee . 2009 . Use of partial least squares regression for variable selection and quality prediction. In Computers & Industrial Engineering, 2009. CIE 2009. International Conference on Computers & Industrial Engineering, University of Technology of Troyes. IEEE, New York. 1302-1307.
37. Westerhuis, J. A., H. C. J. Hoefsloot, S. Smit, D. J. Vis, A. K. Smilde, E. J. J. van Velzen, J. P. M. van Duijnhoven, and F. A. van Dorsten . 2008 . Assessment of PLSDA cross validation. Metabolomics . 4 : 81-89 .
38. Westerhuis, J. A., E. J. J. Velzen, H. C. J. Hoefsloot, and A. K. Smilde . 2008 . Discriminant Q 2 (DQ 2) for improved discrimination in PLSDA models. Metabolomics . 4 : 293-296 .
39. Keane, W. F., J. E. Tomassini, and D. R. Neff . 2011 . Lipid abnormalities in patients with chronic kidney disease. Contrib. Nephrol. 171 : 135-142 .
40. Dashti, M., W. Kulik, F. Hoek, E. C. Veerman, M. P. Peppelenbosch, and F. Rezaee . 2011 . A phospholipidomic analysis of all defi ned human plasma lipoproteins. Sci. Rep. 1 : 139 .
41. Flood, C., M. Gustafsson, R. E. Pitas, L. Arnaboldi, R. L. Walzem, and J. Boren . 2004 . Molecular mechanism for changes in proteoglycan binding on compositional changes of the core and the surface of low-density lipoprotein-containing human apolipoprotein B100. Arterioscler. Thromb. Vasc. Biol. 24 : 564-570 .
42. Terpstra, V., D. A. Bird, and D. Steinberg . 1998 . Evidence that the lipid moiety of oxidized low density lipoprotein plays a role in its interaction with macrophage receptors. Proc. Natl. Acad. Sci. USA . 95 : 1806-1811 .
43. Piperi, C., C. Kalofoutis, M. Tzivras, T. Troupis, A. Skenderis, and A. Kalofoutis . 2004 . Effects of hemodialysis on serum lipids and phospholipids of end-stage renal failure patients. Mol. Cell. Biochem. 265 : 57-61 .
44. Yang, W-L., Q. Bai, D-D. Li, T-L. A, S. Wang, R-S. Zhao, H-G. Nie, A-H. Zhang, T. Wang, and M-H. Fan . 2013 . Changes of urinary phospholipids in the chronic kidney disease patients. Biomarkers . 18 : 601-606 .
45. Kyogashima, M. 2004 . The role of sulfatide in thrombogenesis and haemostasis. Arch. Biochem. Biophys. 426 : 157-162 .
46. Sandhoff, R., H. Grieshaber, R. Djafarzadeh, T. P. Sijmonsma, A. E. I. Proudfoot, T. M. Handel, H. Wiegandt, P. J. Nelson, and H. J. Grone . 2005 . Chemokines bind to sulfatides as revealed by surface plasmon resonance. Biochim. Biophys. Acta . 1687 : 52-63 .
47. Blann, A. D., S. K.Nadar, and G. Y.Lip . 2003 . The adhesion molecule P-selectin and cardiovascular disease. Eur. Heart J. 24 : 2166 - 2179 . 48 .
48. Kobayashi, K., E. Nagata, K. Sasaki, M. Harada-Shiba, S. Kojo, and H. Kikuzaki . 2013 . Increase in secretory sphingomyelinase activity and specifi c ceramides in the aorta of apolipoprotein E knockout mice during aging. Biol. Pharm. Bull. 36 : 1192-1196 .
49. Sneck, M., S. D. Nguyen, T. Pihlajamaa, G. Yohannes, M. L. Riekkola, R. Milne, P. T. Kovanen, and K. Oorni . 2012 . Conformational changes of apoB-100 in SMase-modifi ed LDL mediate formation of large aggregates at acidic pH. J. Lipid Res. 53 : 1832-1839 .
50. Tan, B., D. K. O'Dell, Y. W. Yu, M. F. Monn, H. V. Hughes, S. Burstein, and J. M. Walker . 2010 . Identifi cation of endogenous acyl amino acids based on a targeted lipidomics approach. J. Lipid Res. 51 : 112-119 .
51. Yao, L. Y., Q. Lin, Y. Y. Niu, K. M. Deng, J. H. Zhang, and Y. Lu . 2009 . Synthesis of lipoamino acids and their activity against cerebral ischemic injury. Molecules . 14 : 4051-4064 .
52. Takenouchi, R., K. Inoue, Y. Kambe, and A. Miyata . 2012 . N-arachidonoyl glycine induces macrophage apoptosis via GPR18. Biochem. Biophys. Res. Commun. 418 : 366-371 .
53. Brown, J. M., and S. L. Hazen . 2014 . Seeking a unique lipid signature predicting cardiovascular disease risk. Circulation . 129 : 1799-1803 .