Quantitative Metabolomic Profiling of Plasma, Urine, and Liver Extracts by 1H NMR Spectroscopy Characterizes Different Stages of Atherosclerosis in Hamsters

Journal of Proteome Research

Volumn 15, Issue 10, 2016, Pages 3500-3510

  Guo, Wei ^a   Jiang, Chunying ^a   Yang, Liu ^a   Li, Tianqi ^a   Liu, Xia ^a   Jin, Mengxia ^a   Qu, Kai ^a   Chen, Huili ^a   Jin, Xiangju ^a   Liu, Hongyue ^a   Zhu, Haibo ^a   Wang, Yinghong ^a  

^a INSTITUTE OF MATERIA MEDICA   (China)

Author keywords

atherosclerosis; hamsters; high fat and high cholesterol diet; NMR; quantitative metabolomics

Indexed keywords

AMINO ACID; CARBOHYDRATE; CHOLESTEROL; CHOLESTEROL 7ALPHA MONOOXYGENASE; CHOLINE; FATTY ACID; LOW DENSITY LIPOPROTEIN RECEPTOR; NUCLEOTIDE; PHOSPHATIDYLCHOLINE STEROL ACYLTRANSFERASE; SCAVENGER RECEPTOR BI; STEROL REGULATORY ELEMENT BINDING PROTEIN 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROSIS; BIOCHEMICAL ANALYSIS; CHOLESTEROL DIET; CHOLESTEROL METABOLISM; CONTROLLED STUDY; DOWN REGULATION; ENERGY METABOLISM; HAMSTER MODEL; HISTOPATHOLOGY; INFLAMMATORY INFILTRATE; INTESTINE FLORA; LIPID DIET; LIPID STORAGE; LIVER LEVEL; MALE; METABOLIC DISORDER; METABOLOMICS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN URINE LEVEL; PROTON NUCLEAR MAGNETIC RESONANCE; QUANTITATIVE ANALYSIS; ANIMAL; DISEASE COURSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; HAMSTER; HOMEOSTASIS; LIVER; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PLASMA; URINE;

ANIMALS; ATHEROSCLEROSIS; CHOLESTEROL; CRICETINAE; DISEASE PROGRESSION; FATTY ACIDS; GENE EXPRESSION REGULATION; HOMEOSTASIS; LIVER; MAGNETIC RESONANCE SPECTROSCOPY; METABOLOMICS; PLASMA; URINE;

EID: 84990817443     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.6b00179     Document Type: Article

References (50)

1. Ramsey, S. A.; Gold, E. S.; Aderem, A. A systems biology approach to understanding atherosclerosis EMBO Mol. Med. 2010, 2, 79-89 10.1002/emmm.201000063
2. Yusuf, S.; Hawken, S.; Ounpuu, S.; Dans, T.; Avezum, A.; Lanas, F.; McQueen, M.; Budaj, A.; Pais, P.; Varigos, J.; Lisheng, L. Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case-control study Lancet 2004, 364, 937-952 10.1016/S0140-6736(04)17018-9
3. Gerszten, R. E.; Wang, T. J. The search for new cardiovascular biomarkers Nature 2008, 451, 949-952 10.1038/nature06802
4. Vasan, R. S. Biomarkers of cardiovascular disease: molecular basis and practical considerations Circulation 2006, 113, 2335-2362 10.1161/CIRCULATIONAHA.104.482570
5. Moe, K. T.; Wong, P. Current trends in diagnostic biomarkers of acute coronary syndrome Ann. Acad. Med. Singapore 2010, 39, 210-215
6. Auger, C.; Gerain, P.; Laurent, B. F.; Portet, K.; Bornet, A.; Caporiccio, B.; Cros, G.; Teissédre, P. L.; Rouanet, J. M. Phenolics from commercialized grape extracts prevent early atherosclerotic lesions in hamsters by mechanisms other than antioxidant effect J. Agric. Food Chem. 2004, 52, 5297-5302 10.1021/jf040125d
7. Jové, M.; Pamplona, R.; Prat, J.; Arola, L.; Portero-Otin, O. M. Atherosclerosis prevention by nutritional factors: a meta-analysis in small animal models Nutr., Metab. Cardiovasc. Dis. 2013, 23, 84-93 10.1016/j.numecd.2012.09.006
8. Uehara, Y.; Urata, H.; Ideishi, M.; Arakawa, K.; Saku, K. Chymase inhibition suppresses highcholesterol diet-induced lipid accumulation in the hamster aorta Cardiovasc. Res. 2002, 55, 870-876 10.1016/S0008-6363(02)00458-3
9. -/- mice J. Proteome Res. 2015, 14, 2237-2254 10.1021/acs.jproteome.5b00032
10. -/- mice reveals progression axes for atherosclerosis based on NMR spectroscopy Mol. BioSyst. 2014, 10, 3170-3178 10.1039/C4MB00334A
11. Jové, M.; Ayala, V.; Ramírez, N. O.; Serrano, J. C.; Cassanyé, A.; Arola, L.; Caimari, A.; Del Bas, J. M.; Crescenti, A.; Pamplona, R.; Portero-Otín, M. Lipidomic and metabolomic analyses reveal potential plasma biomarkers of early atheromatous plaque formation in hamsters Cardiovasc. Res. 2013, 97, 642-652 10.1093/cvr/cvs368
12. 1HNMR-based metabolomics Expert Rev. Mol. Diagn. 2006, 6, 717-731 10.1586/14737159.6.5.717
13. Guo, T.; Chen, W. Q.; Zhang, C.; Zhao, Y. X.; Zhang, Y. Chymase activity is closely related with plaque vulnerability in a hamster model of atherosclerosis Atherosclerosis 2009, 207, 59-67 10.1016/j.atherosclerosis.2009.04.014
14. Dillard, A.; Matthan, N. R.; Lichtenstein, A. H. Use of hamster as a model to study diet-induced atherosclerosis Nutr. Metab. 2010, 7, 89 10.1186/1743-7075-7-89
15. Li, L.; Wang, Y.; Xu, Y.; Chen, L. F. Atorvastatin inhibits CD68 expression in aortic root through a GRP78-involved pathway Cardiovasc. Drugs Ther. 2014, 28, 523-532 10.1007/s10557-014-6556-3
16. 1H NMR-based metabonomic investigation of time-related metabolic trajectories of the plasma, urine and liver extracts of hyperlipidemic hamsters PLoS One 2013, 8, e66786 10.1371/journal.pone.0066786
17. 1H NMR metabolomics data Anal. Chem. 2006, 78, 4430-4442 10.1021/ac060209g
18. 1H NMR metabonomics of plasma lipoprotein subclasses: elucidation of metabolic clustering by self-organising maps NMR Biomed. 2007, 20, 658-672 10.1002/nbm.1123
19. Vinaixa, M.; Rodríguez, M. A.; Rull, A.; Beltrán, R.; Bladé, C.; Brezmes, J.; Cañellas, N.; Joven, J.; Correig, X. Metabolomic assessment of the effect of dietary cholesterol in the progressive development of fatty liver disease J. Proteome Res. 2010, 9, 2527-2538 10.1021/pr901203w
20. 1H-NMR metabonomic data BMC Bioinf. 2007, 8, S8 10.1186/1471-2105-8-S2-S8
21. Eberle, D.; Hegarty, B.; Bossard, P.; Ferre, P.; Foufelle, F. SREBP transcription factors: master regulators of lipid homeostasis Biochimie 2004, 86, 839-848 10.1016/j.biochi.2004.09.018
22. Tang, J. J.; Li, J. G.; Qi, W.; Qiu, W. W.; Li, P. S.; Li, B. L.; Song, B. L. Inhibition of SREBP by a small molecule, betulin, improves hyperlipidemia and insulin resistance and reduces atherosclerotic plaques Cell Metab. 2011, 13, 44-56 10.1016/j.cmet.2010.12.004
23. Princen, H. M.; Post, S. M.; Twisk, J. Regulation of bile acid synthesis Curr. Pharm. Design 1997, 3, 59-84
24. Tastesen, H. S.; Keenan, A. H.; Madsen, L.; Kristiansen, K.; Liaset, B. Scallop protein with endogenous high taurine and glycine content prevents high-fat, high-sucrose-induced obesity and improves plasma lipid profile in male C57BL/6J mice Amino Acids 2014, 46, 1659-1671 10.1007/s00726-014-1715-1
25. Leiva, A.; Verdejo, H.; Benítez, M. L.; Martínez, A.; Busso, D.; Rigotti, A. Mechanisms regulating hepatic SR-BI expression and their impact on HDL metabolism Atherosclerosis 2011, 217, 299-307 10.1016/j.atherosclerosis.2011.05.036
26. Rogers, M. A.; Liu, J.; Song, B. L.; Li, B. L.; Chang, C. C.; Chang, T. Y. Acyl-CoA:cholesterol acyltransferases (ACATs/SOATs): Enzymes with multiple sterols as substrates and as activators J. Steroid Biochem. Mol. Biol. 2015, 151, 102-107 10.1016/j.jsbmb.2014.09.008
27. Calabresi, L.; Simonelli, S.; Gomaraschi, M.; Franceschini, G. Genetic lecithin:cholesterol acyltransferase deficiency and cardiovascular disease Atherosclerosis 2012, 222, 299-306 10.1016/j.atherosclerosis.2011.11.034
28. Mayr, M.; Chung, Y. L.; Mayr, U.; Yin, X.; Ly, L.; Troy, H.; Fredericks, S.; Hu, Y.; Griffiths, J. R.; Xu, Q. Proteomic and metabolomic analyses of atherosclerotic vessels from apolipoprotein E-deficient mice reveal alterations in inflammation, oxidative Stress, and energy metabolism Arterioscler. Thromb. Vasc. Biol. 2005, 25, 2135-2142
29. Browning, J. D.; Horton, J. D. Molecular mediators of hepatic steatosis and liver injury J. Clin. Invest. 2004, 114, 147-152 10.1172/JCI200422422
30. Ribas, G. S.; Vargas, C. R.; Wajner, M. L-carnitine supplementation as a potential antioxidant therapy for inherited neurometabolic disorders Gene 2014, 533, 469-476 10.1016/j.gene.2013.10.017
31. He, W.; Miao, F. J.; Lin, D. C.; Schwandner, R. T.; Wang, Z.; Gao, J.; Chen, J. L.; Tian, H.; Ling, L. Citric acid cycle intermediates as ligands for orphan G-protein-coupled receptors Nature 2004, 429, 188-193 10.1038/nature02488
32. Catala, A. A synopsis of the process of lipid peroxidation since the discovery of the essential fatty acids Biochem. Biophys. Res. Commun. 2010, 399, 318-323 10.1016/j.bbrc.2010.07.087
33. Wang, Z.; Klipfell, E.; Bennett, B. J.; Koeth, R.; Levison, B. S.; Dugar, B.; Feldstein, A. E.; Britt, E. B.; Fu, X.; Chung, Y. M.; Wu, Y.; Schauer, P.; Smith, J. D.; Allayee, H.; Tang, W. H.; DiDonato, J. A.; Lusis, A. J.; Hazen, S. L. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease Nature 2011, 472, 57-63 10.1038/nature09922
34. Dumas, M. E.; Barton, R. H.; Toye, A.; Cloarec, O.; Blancher, C.; Rothwell, A.; Fearnside, J.; Tatoud, R.; Blanc, V.; Lindon, J. C.; Mitchell, S. C.; Holmes, E.; McCarthy, M. I.; Scott, J.; Gauguier, D.; Nicholson, J. K. Metabolic profiling reveals a contribution of gut microbiota to fatty liver phenotype in insulin-resistant mice Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 12511-12516 10.1073/pnas.0601056103
35. 1H NMR based metabonomics approach to progression of coronary atherosclerosis in a rabbit model Process Biochem. 2011, 46, 2240-2247 10.1016/j.procbio.2011.08.016
36. Mestdagh, R.; Dumas, M. E.; Rezzi, S.; Kochhar, S.; Holmes, E.; Claus, S. P.; Nicholson, J. K. Gut microbiota modulate the metabolism of brown adipose tissue in mice J. Proteome Res. 2012, 11, 620-630 10.1021/pr200938v
37. Zhang, Q.; Wang, G. J.; A, J.; Ma, B.; Dua, Y.; Zhu, L.; Wu, D. Metabonomic profiling of diet-induced hyperlipidaemia in a rat model Biomarkers 2010, 15, 205-216 10.3109/13547500903419049
38. Lu, J.; Xie, G.; Jia, W.; Jia, W. Insulin resistance and the metabolism of branched-chain amino acids Front. Med. 2013, 7, 53-59 10.1007/s11684-013-0255-5
39. 1H NMR metabonomics can differentiate the early atherogenic effect of dairy products in hyperlipidemic hamsters Atherosclerosis 2009, 206, 127-133 10.1016/j.atherosclerosis.2009.01.040
40. Lescano-De-Souza, A. J.; Curi, R. Cholesterol inhibits glutamine metabolism in LLC WRC256 tumour cells but does not affect it in lymphocytes: possible implications for tumour cell proliferation Cell Biochem. Funct. 1999, 17, 223-238 10.1002/(SICI)1099-0844(199912)17:4<223::AID-CBF832>3.0.CO;2-8
41. Swierkosz, T. A.; Mitchell, J. A.; Sessa, W. C.; Hecker, M.; Vane, J. R. L-Glutamine inhibits the release of endothelium-derived relaxing factor from the rabbits aorta Biochem. Biophys. Res. Commun. 1990, 172, 143-148 10.1016/S0006-291X(05)80184-6
42. Cai, H.; Harrison, D. G. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress Circ. Res. 2000, 87, 840-844 10.1161/01.RES.87.10.840
43. Bell, J. D.; Lee, J. A.; Lee, H. A.; Sadler, P. J.; Wilkie, D. R.; Woodham, R. H. Nuclear magnetic resonance studies of blood plasma and urine from subjects with chronic renal failure: identification of trimethylamine-N-oxide Biochim. Biophys. Acta, Mol. Basis Dis. 1991, 1096, 101-107 10.1016/0925-4439(91)90046-C
44. Hauet, T.; Baumert, H.; Gibelin, H.; Hameury, F.; Goujon, J. M.; Carretier, M.; Eugene, M. Noninvasive monitoring of citrate, acetate, lactate, and renal medullary osmolyte excretion in urine as biomarkers of exposure to ischemic reperfusion injury Cryobiology 2000, 41, 280-291 10.1006/cryo.2000.2291
45. Swann, J. R.; Tuohy, K. M.; Lindfors, P.; Brown, D. T.; Gibson, G. R.; Wilson, I. D.; Sidaway, J.; Nicholson, J. K.; Holmes, E. Variation in antibiotic-induced microbial recolonization impacts on the host metabolic phenotypes of rats J. Proteome Res. 2011, 10, 3590-3603 10.1021/pr200243t
46. Williams, H. R.; Cox, I. J.; Walker, D. G.; North, B. V.; Patel, V. M.; Marshall, S. E.; Jewell, D. P.; Ghosh, S.; Thomas, H. J.; Teare, J. P.; Jakobovits, S.; Zeki, S.; Welsh, K. I.; Taylor-Robinson, S. D.; Orchard, T. R. Characterization of inflammatory bowel disease with urinary metabolic profiling Am. J. Gastroenterol. 2009, 104, 1435-1444 10.1038/ajg.2009.175
47. Bell, J. D.; Brown, J. C.; Nicholson, J. K.; Sadler, P. J. Assignment of resonances for acutephase' glycoproteins in high resolution proton NMR spectra of human blood plasma FEBS Lett. 1987, 215, 311-315 10.1016/0014-5793(87)80168-0
48. Lord, R. S.; Bralley, J. A. Clinical applications of urinary organic acids. Part I: Detoxification markers Altern. Med. Rev. 2008, 13, 205-215
49. Grootveld, M.; Halliwell, B. Measurement of allantoin and uric acid in human body fluids. A potential index of free-radical reactions in vivo? Biochem. J. 1987, 243, 803-808 10.1042/bj2430803
50. Chaykin, S.; Bloch, K. The metabolism of nicotinamide-N-oxide Biochim. Biophys. Acta 1959, 31, 213-216 10.1016/0006-3002(59)90458-5