PPAR-pan activation induces hepatic oxidative stress and lipidomic remodelling

Free Radical Biology and Medicine

Volumn 95, Issue , 2016, Pages 357-368

  Ament, Zsuzsanna ^a,b,c   West, James A ^a,b,c   Stanley, Elizabeth ^a,b,c   Ashmore, Tom ^a,b,c   Roberts, Lee D ^a,b,c   Wright, Jayne ^d   Nicholls, Andrew W ^e   Griffin, Julian L ^a,b,c  

^a MEDICAL RESEARCH COUNCIL   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d Jayne Wright Ltd   (United Kingdom)

^e GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Eicosanoids; Lipidomics; Metabolomics; Peroxisome proliferator activated receptors; Oxidation

Indexed keywords

CYTOSINE; FATTY ACID; ICOSANOID; METHIONINE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR AGONIST; PHOSPHOLIPID; S ADENOSYLMETHIONINE; TRIACYLGLYCEROL; LIPID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA DAMAGE; HEPATOMEGALY; IMMUNE STATUS; LIPIDOMICS; MALE; METABOLOMICS; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; AGONISTS; ANIMAL; BIOSYNTHESIS; DRUG EFFECTS; GENETICS; LIPID METABOLISM; LIVER; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; DIABETES MELLITUS, TYPE 2; FATTY ACIDS, NONESTERIFIED; LIPID METABOLISM; LIPIDS; LIVER; OXIDATIVE STRESS; PPAR ALPHA; PPAR GAMMA; PPAR-BETA; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84964952471     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.11.033     Document Type: Article

References (44)

1. Z. Ament, M. Masoodi, and J.L. Griffin Applications of metabolomics for understanding the action of peroxisome proliferator-activated receptors (PPARs) in diabetes, obesity and cancer Genome Med. 4 2012 32
2. L.D. Roberts, A.J. Murray, D. Menassa, T. Ashmore, A.W. Nicholls, and J.L. Griffin The contrasting roles of PPARδ and PPARγ in regulating the metabolic switch between oxidation and storage of fats in white adipose tissue Genome Biol. 12 2011
3. G. Leonardsson, J.H. Steel, M. Christian, V. Pocock, S. Milligan, J. Bell, P.-W. So, G. Medina-Gomez, A. Vidal-Puig, and R. White Nuclear receptor corepressor RIP140 regulates fat accumulation Proc. Natl. Acad. Sci. USA 101 2004 8437 8442
4. P. Escher, O. Braissant, S. Basu-Modak, L. Michalik, W. Wahli, and B. Desvergne Rat PPARs: quantitative analysis in adult rat tissues and regulation in fasting and refeeding Endocrinology 142 2001 4195 4202
5. S.A. Kliewer, B.M. Forman, B. Blumberg, E.S. Ong, U. Borgmeyer, D.J. Mangelsdorf, K. Umesono, R.M. Evans, Differential expression and activation of a family of murine peroxisome proliferator-activated receptors. Proc. Natl. Acad. Sci. 91 (1994) 7355-7355.
6. O. Braissant, F. Foufelle, C. Scotto, M. Dauca, W. Wahli, Differential expression of peroxisome proliferator-activated receptors (PPARs): tissue distribution of PPAR-alpha,-beta, and-gamma in the adult rat. Endocrinology 137 (1996) 354-354.
7. D. Patsouris Nuclear control of the inflammatory response in mammals by peroxisome proliferator-activated receptors PPAR Res. 2013 2013
8. B. Staels, J. Dallongeville, J. Auwerx, K. Schoonjans, E. Leitersdorf, and J.-C. Fruchart Mechanism of action of fibrates on lipid and lipoprotein metabolism Circulation 98 1998 2088 2093
9. M. Guerre-Millo, P. Gervois, E. Raspé, L. Madsen, P. Poulain, B. Derudas, J.-M. Herbert, D.A. Winegar, T.M. Willson, and J.-C. Fruchart Peroxisome proliferator-activated receptor α activators improve insulin sensitivity and reduce adiposity J. Biol. Chem. 275 2000 16638 16642
10. A. Minnich, N. Tian, L. Byan, and G. Bilder A potent PPARalpha agonist stimulates mitochondrial fatty acid beta-oxidation in liver and skeletal muscle Am. J. Physiol. Endocrinol. Metab. 280 2001 E270 E279
11. H.J. Atherton, N.J. Bailey, W. Zhang, J. Taylor, H. Major, J. Shockcor, K. Clarke, and J.L. Griffin A combined 1H-NMR spectroscopy- and mass spectrometry-based metabolomic study of the PPAR-{alpha} null mutant mouse defines profound systemic changes in metabolism linked to the metabolic syndrome Physiol. Genom. 27 2006 178 186
12. H. Kim, M. Haluzik, Z. Asghar, D. Yau, J.W. Joseph, A.M. Fernandez, M.L. Reitman, S. Yakar, B. Stannard, and L. Heron-Milhavet Peroxisome proliferator-activated receptor-α agonist treatment in a transgenic model of type 2 diabetes reverses the lipotoxic state and improves glucose homeostasis Diabetes 52 2003 1770 1778
13. L.D. Roberts, D.G. Hassall, D.A. Winegar, J.N. Haselden, A.W. Nicholls, J.L. Griffin, Increased hepatic oxidative metabolism distinguishes the action of Peroxisome proliferator-activated receptor delta from Peroxisome proliferator-activated receptor gamma in the ob/ob mouse. Genome Med. 1:115-115, 2009.
14. J.L. Griffin, and A. Vidal-Puig Current challenges in metabolomics for diabetes research: a vital functional genomic tool or just a ploy for gaining funding? Physiol. Genom. 34 2008 1 5
15. K. Matsusue, M. Haluzik, G. Lambert, S.-H. Yim, O. Gavrilova, J.M. Ward, B. Brewer Jr, M.L. Reitman, and F.J. Gonzalez Liver-specific disruption of PPARgamma in leptin-deficient mice improves fatty liver but aggravates diabetic phenotypes J. Clin. Invest. 111 2003 737 747
16. L.S. Mackenzie, and L. Lione Harnessing the benefits of PPARβ/δ agonists Life Sci. 93 2013 963 967
17. M. Vacca, C. Degirolamo, V. Massafra, L. Polimeno, R. Mariani-Costantini, G. Palasciano, and A. Moschetta Nuclear receptors in regenerating liver and hepatocellular carcinoma Mol. Cell. Endocrinol. 368 2013 108 119
18. M. Vacca, C. Degirolamo, R. Mariani-Costantini, G. Palasciano, and A. Moschetta Lipid-sensing nuclear receptors in the pathophysiology and treatment of the metabolic syndrome Wiley Interdiscip. Rev.: Syst. Biol. Med. 3 2011 562 587
19. Z. Ament, C.L. Waterman, J.A. West, C. Waterfield, R.A. Currie, J. Wright, and J.L. Griffin A metabolomics investigation of non-genotoxic carcinogenicity in the rat J. Proteome Res. 12 2013 5775 5790
20. C. Waterman, R. Currie, L. Cottrell, J. Dow, J. Wright, C. Waterfield, J. Griffin, An integrated functional genomic study of acute phenobarbital exposure in the rat. BMC Genomics 11:9-9; 2010.
21. L.D. Roberts, J.A. West, A. Vidal-Puig, and J.L. Griffin Methods for performing lipidomics in white adipose tissue Methods Enzym. 538 2014 211 231
22. S. Azhar Peroxisome proliferator-activated receptors, metabolic syndrome and cardiovascular disease Future Cardiol. 6 2010 657 691
23. S.K. Ramaiah A toxicologist guide to the diagnostic interpretation of hepatic biochemical parameters Food Chem. Toxicol. 45 2007 1551 1557
24. Z. Ament, J.A. West, S. Elizabeth, T. Ashmore, L.D. Roberts, A.W. Nicholls, and J.L. Griffin Metabolomics of PPAR-pan treated rat liver Data Brief. 2015
25. R. Wall, R.P. Ross, G.F. Fitzgerald, and C. Stanton Fatty acids from fish: the anti-inflammatory potential of long-chain omega-3 fatty acids Nutr. Rev. 68 2010 280 289
26. S.C. Larsson, M. Kumlin, M. Ingelman-Sundberg, and A. Wolk Dietary long-chain n-3 fatty acids for the prevention of cancer: a review of potential mechanisms Am. J. Clin. Nutr. 79 2004 935 945
27. M. Vagner, and E. Santigosa Characterization and modulation of gene expression and enzymatic activity of delta-6 desaturase in teleosts: a review Aquaculture 315 2011 131 143
28. M.T. Nakamura, and T.Y. Nara Structure, function, and dietary regulation of Δ6, Δ5, and Δ9 desaturases Nutrition 24 2004
29. J.E. Klaunig, M.A. Babich, K.P. Baetcke, J.C. Cook, J.C. Corton, R.M. David, J.G. DeLuca, D.Y. Lai, R.H. McKee, J.M. Peters, R.A. Roberts, and P.A. Fenner-Crisp PPARalpha agonist-induced rodent tumors: modes of action and human relevance Crit. Rev. Toxicol. 33 2003 655 780
30. E.A. Ortlund, Y. Lee, I.H. Solomon, J.M. Hager, R. Safi, Y. Choi, Z. Guan, A. Tripathy, C.R. Raetz, and D.P. McDonnell Modulation of human nuclear receptor LRH-1 activity by phospholipids and SHP Nat. Struct. Mol. Biol. 12 2005 357 363
31. S. Stein, and K. Schoonjans Molecular basis for the regulation of the nuclear receptor LRH-1 Curr. Opin. Cell. Biol. 33 2015 26 34
32. X. Wang, J.A. West, A.J. Murray, and J.L. Griffin A comprehensive metabolic profiling of age-related mitochondrial dysfunction in the high-fat fed ob/ob mouse heart J. Proteome Res. 2015
33. S.H. Adams, C.L. Hoppel, K.H. Lok, L. Zhao, S.W. Wong, P.E. Minkler, D.H. Hwang, J.W. Newman, and W.T. Garvey Plasma acylcarnitine profiles suggest incomplete long-chain fatty acid beta-oxidation and altered tricarboxylic acid cycle activity in type 2 diabetic African-American women J. Nutr. 139 2009 1073 1081
34. T.R. Koves, J.R. Ussher, R.C. Noland, D. Slentz, M. Mosedale, O. Ilkayeva, J. Bain, R. Stevens, J.R.B. Dyck, C.B. Newgard, G.D. Lopaschuk, and D.M. Muoio Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance Cell Metab. 7 2008 45 56
35. C.L. Ulrey, L. Liu, L.G. Andrews, and T.O. Tollefsbol The impact of metabolism on DNA methylation Hum. Mol. Genet. 14 2005 R139 R147
36. M. Akkaoui, I. Cohen, C. Esnous, V. Lenoir, M. Sournac, J. Girard, and C. Prip-Buus Modulation of the hepatic malonyl-CoA-carnitine palmitoyltransferase 1A partnership creates a metabolic switch allowing oxidation of de novo fatty acids1 Biochem. J. 420 2009 429 438
37. T.C. Leone, C.J. Weinheimer, and D.P. Kelly A critical role for the peroxisome proliferator-activated receptor α (PPARα) in the cellular fasting response: the PPARα-null mouse as a model of fatty acid oxidation disorders Proc. Natl. Acad. Sci. 96 1999 7473 7478
38. S.A. Kliewer, S.S. Sundseth, S.A. Jones, P.J. Brown, G.B. Wisely, C.S. Koble, P. Devchand, W. Wahli, T.M. Willson, J.M. Lenhard, and J.M. Lehmann Fatty acids and eicosanoids regulate gene expression through direct interactions with peroxisome proliferator-activated receptors α and γ Proc. Natl. Acad. Sci. USA 94 1997 4318 4323
39. B.M. Forman, J. Chen, and R.M. Evans Hypolipidemic drugs, polyunsaturated fatty acids, and eicosanoids are ligands for peroxisome proliferator-activated receptors alpha and delta Proc. Natl. Acad. Sci. USA 94 1997 4312 4317
40. A.A. Spector, and A.W. Norris Action of epoxyeicosatrienoic acids on cellular function Am. J. Physiol. Cell. Physiol. 292 2007 C996 1012
41. C. Jiang, A.T. Ting, and B. Seed PPAR-γ agonists inhibit production of monocyte inflammatory cytokines Nature 391 1998 82 86
42. M. Ricote, A.C. Li, T.M. Willson, C.J. Kelly, and C.K. Glass The peroxisome proliferator-activated receptor-γ is a negative regulator of macrophage activation Nature 391 1998 79 82
43. M.E. Poynter, and R.A. Daynes Peroxisome proliferator-activated receptor α activation modulates cellular redox status, represses nuclear factor-κB signaling, and reduces inflammatory cytokine production in aging J. Biol. Chem. 273 1998 32833 32841
44. J.K. Reddy, and M.S. Rao Lipid metabolism and liver inflammation. II. Fatty liver disease and fatty acid oxidation Am. J. Physiol. Gastrointest. Liver Physiol. 290 2006 G852 G858