High-fat diet induces changes in adipose tissue trans-4-oxo-2-nonenal and trans-4-hydroxy-2-nonenal levels in a depot-specific manner

Free Radical Biology and Medicine

Volumn 63, Issue , 2013, Pages 390-398

  Long, Eric K ^a   Olson, Dalay M ^a   Bernlohr, David A ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

4 HNE; 4 ONE; Adipose; Free radicals; Gene expression; Obesity; Oxidative stress

Indexed keywords

4 HYDROXYNONENAL; 4 OXO 2 NONENAL; ALDEHYDE DERIVATIVE; GLUTATHIONE TRANSFERASE A4; PEROXIREDOXIN 3; PHOSPHOLIPID HYDROPEROXIDE GLUTATHIONE PEROXIDASE; UNCLASSIFIED DRUG;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EPIDIDYMIS FAT; FAT INTAKE; GENE EXPRESSION; INTRAABDOMINAL FAT; LIPID BLOOD LEVEL; LIPID DIET; LIPID PEROXIDATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN CARBONYLATION; SUBCUTANEOUS FAT; UPREGULATION;

MUS;

EID: 84879487933     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.05.030     Document Type: Article

References (67)

1. Ferroni, P.; Basili, S.; Falco, A.; Davi, G. Inflammation, insulin resistance, and obesity. Curr. Atheroscler. Rep. 6: 424-431; 2004.
2. Furukawa, S.; Fujita, T.; Shimabukuro, M.; Iwaki, M.; Yamada, Y.; Nakajima, Y.; Nakayama, O.; Makishima, M.; Matsuda, M.; Shimomura, I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J. Clin. Invest. 114 : 1752-17 6 1 ; 2 0 0 4 . (Pubitemid 40385531)
3. Sankhla, M.; Sharma, T. K.; Mathur, K.; Rathor, J. S.; Butolia, V.; Gadhok, A. K.; Vardey, S. K.; Sinha, M.; Kaushik, G. G. Relationship of oxidative stress with obesity and its role in obesity induced metabolic syndrome. Clin. Lab. 58: 385-392; 2012.
4. Curtis, J. M.; Grimsrud, P. A.; Wright, W. S.; Xu, X.; Foncea, R. E.; Graham, D. W.; Brestoff, J. R.; Wiczer, B. M.; Ilkayeva, O.; Cianflone, K.; Muoio, D. E.; Arriaga, E. A.; Bernlohr, D. A. Downregulation of adipose glutathione S-transferase A4 leads to increased protein carbonylation, oxidative stress, and mitochondrial dysfunction. Diabetes 59: 113 2 -1142; 2010.
5. Curtis, J. M.; Hahn, W. S.; Long, E. K.; Burrill, J. S.; Arriaga, E. A.; Bernlohr, D. A. Protein carbonylation and metabolic control systems. Trends Endocrinol. Metab. 23: 399-406; 2012.
6. Singh, S. P.; Niemczyk, M.; Saini, D.; Awasthi, Y. C.; Zimniak, L.; Zimniak, P. Role of the electrophilic lipid peroxidation product 4-hydroxynonenal in the development and maintenance of obesity in mice. Biochemistry 47: 3900-3911; 2008. (Pubitemid 351431379)
7. Zimniak, P. 4-Hydroxynonenal and fat storage: a paradoxical pro-obesity mechanism? Cell Cycle 9: 3393-3394; 2010.
8. Oh, D. Y.; Morinaga, H.; Talukdar, S.; Bae, E. J.; Olefsky, J. M. Increased macrophage migration into adipose tissue in obese mice. Diabetes 61: 346-354; 2012.
9. Yuzefovych, L. V.; Musiyenko, S. I.; Wilson, G. L.; Rachek, L. I. Mitochondrial DNA damage and dysfunction, and oxidative stress are associated with endoplasmic reticulum stress, protein degradation and apoptosis in high fat diet-induced insulin resistance mice. PLoS One 8:e54059; 2013.
10. Curtis, J. M.; Hahn, W. S.; Stone, M. D.; Inda, J. J.; Droullard, D. J.; Kuzmicic, J. P.; Donoghue, M. A.; Long, E. K.; Armien, A. G.; Lavandero, S.; Arriaga, E.; Griffin, T. J.; Bernlohr, D. A. Protein carbonylation and adipocyte mitochondria function. J. Biol. Chem. 287: 32967-32980; 2012.
11. Grimsrud, P. A.; Picklo Sr M. J.; Griffin, T. J.; Bernlohr, D. A. Carbonylation of adipose proteins in obesity and insulin resistance: identification of adipocyte fatty acid-binding protein as a cellular target of 4-hydroxynonenal. Mol. Cell. Proteomics 6: 624-637; 2007. (Pubitemid 46630095)
12. Grimsrud, P. A.; Xie, H.; Griffin, T. J.; Bernlohr, D. A. Oxidative stress and covalent modification of protein with bioactive aldehydes. J. Biol. Chem. 283: 21837-21841; 2008.
13. Schaur, R. J. Basic aspects of the biochemical reactivity of 4-hydroxynonenal. Mol. Aspects Med. 24: 149-159; 2003. (Pubitemid 36945015)
14. Bennaars-Eiden, A.; Higgins, L.; Hertzel, A. V.; Kapphahn, R. J.; Ferrington, D. A.; Bernlohr, D. A. Covalent modification of epithelial fatty acid-binding protein by 4-hydroxynonenal in vitro and in vivo: evidence for a role in antioxidant biology. J. Biol. Chem. 277: 50693-50702; 2002. (Pubitemid 36042231)
15. Esterbauer, H.; Schaur, R. J.; Zollner, H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 11 : 81-128; 1991. (Pubitemid 121003917)
16. Stewart, B. J.; Doorn, J. A.; Petersen, D. R. Residue-specific adduction of tubulin by 4-hydroxynonenal and 4-oxononenal causes cross-linking and inhibits polymerization. Chem. Res. Toxicol. 20: 1111 -1119; 2007. (Pubitemid 47372989)
17. Tsuchiya, Y.; Yamaguchi, M.; Chikuma, T.; Hojo, H. Degradation of glyceraldehyde-3-phosphate dehydrogenase triggered by 4-hydroxy-2-nonenal and 4-hydroxy-2-hexenal. Arch. Biochem. Biophys. 438: 217-222; 2005. (Pubitemid 40798021)
18. Picklo, M. J.; Azenkeng, A.; Hoffmann, M. R. Trans-4-oxo-2-nonenal potently alters mitochondrial function. Free Radic. Biol. Med. 50: 400-407; 2011.
19. Picklo Sr M. J.; Montine, T. J. Mitochondrial effects of lipid-derived neurotox-ins. J. Alzheimers Dis. 12: 185-193; 2007.
20. Gardner, H. W. Oxygen radical chemistry of polyunsaturated fatty acids. Free Radic. Biol. Med. 7: 65-86; 1989. (Pubitemid 19165157)
21. Doorn, J. A.; Petersen, D. R. Covalent modification of amino acid nucleophiles by the lipid peroxidation products 4-hydroxy-2-nonenal and 4-oxo-2-nonenal. Chem. Res. Toxicol 15: 1445-1450; 2002. (Pubitemid 35364906)
22. Doorn, J. A.; Petersen, D. R. Covalent adduction of nucleophilic amino acids by 4-hydroxynonenal and 4-oxononenal. Chem. Biol. Interact. 143-144: 93-100; 2003. (Pubitemid 36246435)
23. Uchida, K. A lipid-derived endogenous inducer of COX-2: a bridge between inflammation and oxidative stress. Mol. Cells 25: 347-351; 2008.
24. Frohnert, B. I.; Sinaiko, A. R.; Serrot, F. J.; Foncea, R. E.; Moran, A.; Ikramuddin, S.; Choudry, U.; Bernlohr, D. A. Increased adipose protein carbonylation in human obesity. Obesity (Silver Spring) 19: 17 3 5 -174 1 ; 2 0 11 .
25. Long, E. K.; Smoliakova, I.; Honzatko, A.; Picklo Sr. M. J. Structural characterization of alpha,beta-unsaturated aldehydes by GC/MS is dependent upon ionization method. Lipids 43: 765-774; 2008.
26. Lee, S. H.; Blair, I. A. Characterization of 4-oxo-2-nonenal as a novel product of lipid peroxidation. Chem. Res. Toxicol. 13: 698-702; 2000. (Pubitemid 30663446)
27. Choudhary, S.; Xiao, T.; Vergara, L. A.; Srivastava, S.; Nees, D.; Piatigorsky, J.; Ansari, N. H. Role of aldehyde dehydrogenase isozymes in the defense of rat lens and human lens epithelial cells against oxidative stress. Invest. Ophthal-mol. Visual Sci. 46: 259-267; 2005. (Pubitemid 40044842)
28. Liu, G.; Feinstein, S. I.; Wang, Y.; Dodia, C.; Fisher, D.; Yu, K.; Ho, Y. S.; Fisher, A. B. Comparison of glutathione peroxidase 1 and peroxiredoxin 6 in protection against oxidative stress in the mouse lung. Free Radic. Biol. Med. 49: 117 2 -1181; 2010.
29. Sacks, H. S.; Fain, J. N.; Cheema, P.; Bahouth, S. W.; Garrett, E.; Wolf, R. Y.; Wolford, D.; Samaha, J. Depot-specific overexpression of proinflammatory, redox, endothelial cell, and angiogenic genes in epicardial fat adjacent to severe stable coronary atherosclerosis. Metab. Syndr. Relat. Disord 9: 433-439; 2011.
30. Hjelle, J. J.; Petersen, D. R. Hepatic aldehyde dehydrogenases and lipid peroxidation. Pharmacol. Biochem. Behav. 18(Suppl. 1): 155-160; 1983.
31. Student, A. K.; Hsu, R. Y.; Lane, M. D. Induction of fatty acid synthetase synthesis in differentiating 3T3-L1 preadipocytes. J. Biol. Chem. 255: 4745 4750; 1980. (Pubitemid 10060752)
32. Center for Veterinary Medicine/Center for Drug Evaluation and Research. Guidance for industry: bioanalytical method validation. Rockville, MD: Food and Drug Administration, U.S. Department of Health and Human Services; 2001.
33. Starkenmann, C. Analysis of a model reaction system containing cysteine and (E)-2-methyl-2-butenal, (E)-2-hexenal, or mesityl oxide. J. Agric. Food Chem 51: 7146-7155; 2003.
34. Tanti, J. F.; Ceppo, F.; Jager, J.; Berthou, F. Implication of inflammatory signaling pathways in obesity-induced insulin resistance. Front. Endocrinol. 3: 181; 2012.
35. Wang, X.; Cheng, M.; Zhao, M.; Ge, A.; Guo, F.; Zhang, M.; Yang, Y.; Liu, L.; Yang, N. Differential effects of high-fat-diet rich in lard oil or soybean oil on osteopontin expression and inflammation of adipose tissue in diet-induced obese rats. Eur. J. Nutr. 52: 11 8 1 -1189; 2012.
36. Rossi, M. A.; Fidale, F.; Di Mauro, C.; Esterbauer, H.; Dianzani, M. U. Effect of 4-hydroxy-2,3-trans-nonenal and related aldehydes on phospholipase C activity of rat neutrophils. Int. J. Tissue React. 15: 201-205; 1993. (Pubitemid 24160251)
37. Selley, M. L. Determination of the lipid peroxidation product (E)-4-hydroxy-2-nonenal in clinical samples by gas chromatography - negative-ion chemical ionisation mass spectrometry of the O-pentafluorobenzyl oxime. J. Chroma-togr. B Biomed. Sci. Appl 691: 263-268; 1997. (Pubitemid 27214601)
38. Selley, M. L.; Bartlett, M. R.; McGuiness, J. A.; Hapel, A. J.; Ardlie, N. G. Determination of the lipid peroxidation product trans-4-hydroxy-2-nonenal in biological samples by high-performance liquid chromatography and combined capillary column gas chromatography-negative-ion chemical ionisation mass spectrometry. J. Chromatogr 488: 329-340; 1989. (Pubitemid 19122089)
39. Awasthi, Y. C.; Sharma, R.; Cheng, J. Z.; Yang, Y.; Sharma, A.; Singhal, S. S.; Awasthi, S. Role of 4-hydroxynonenal in stress-mediated apoptosis signaling. Mol. Aspects Med. 24: 219-230; 2003. (Pubitemid 36945022)
40. Bradley, M. A.; Markesbery, W. R.; Lovell, M. A. Increased levels of 4-hydroxynonenal and acrolein in the brain in preclinical Alzheimer disease. Free Radic. Biol. Med. 48: 1570-1576; 2010.
41. Eckl, P. M.; Ortner, A.; Esterbauer, H. Genotoxic properties of 4-hydroxyalkenals and analogous aldehydes. Mutat. Res. 290: 183-192; 1993. (Pubitemid 23355129)
42. Kumagai, T.; Matsukawa, N.; Kaneko, Y.; Kusumi, Y.; Mitsumata, M.; Uchida, K. A lipid peroxidation-derived inflammatory mediator: identification of 4-hydroxy-2-nonenal as a potential inducer of cyclooxygenase-2 in macro-phages. J. Biol. Chem. 279: 48389-48396; 2004. (Pubitemid 39540995)
43. Kumagai, T.; Nakamura, Y.; Osawa, T.; Uchida, K. Role of p38 mitogen-activated protein kinase in the 4-hydroxy-2-nonenal-induced cyclooxygenase-2 expression. Arch. Biochem. Biophys. 397: 240-245; 2002. (Pubitemid 34852286)
44. Minekura, H.; Kumagai, T.; Kawamoto, Y.; Nara, F.; Uchida, K. 4-Hydroxy-2-nonenal is a powerful endogenous inhibitor of endothelial response. Biochem. Biophys. Res. Commun. 282: 557-561; 2001. (Pubitemid 32917907)
45. Poli, G.; Biasi, F.; Leonarduzzi, G. 4-Hydroxynonenal-protein adducts: a reliable biomarker of lipid oxidation in liver diseases. Mol. Aspects Med. 29: 67-71; 2008.
46. Siems, W. G.; Grune, T.; Esterbauer, H. 4-Hydroxynonenal formation during ischemia and reperfusion of rat small intestine. Life Sci. 57: 785-789; 1995.
47. Toyokuni, S.; Yamada, S.; Kashima, M.; Ihara, Y.; Yamada, Y.; Tanaka, T.; Hiai, H.; Seino, Y.; Uchida, K. Serum 4-hydroxy-2-nonenal-modified albumin is elevated in patients with type 2 diabetes mellitus. Antioxid. Redox Signaling 2: 681-685; 2000. (Pubitemid 32062319)
48. Uchida, K.; Stadtman, E. R. Covalent attachment of 4-hydroxynonenal to glyceraldehyde-3-phosphate dehydrogenase: a possible involvement of intra-and intermolecular cross-linking reaction. J. Biol. Chem 268: 6388-6393; 1993. (Pubitemid 23099334)
49. Williams, T. I.; Lynn, B. C.; Markesbery, W. R.; Lovell, M. A. Increased levels of 4-hydroxynonenal and acrolein, neurotoxic markers of lipid peroxidation, in the brain in mild cognitive impairment and early Alzheimer's disease. Neurobiol. Aging 27: 1094-1099; 2006. (Pubitemid 43850642)
50. Liu, Y.; Longmore, R. B. Dietary sandalwood seed oil modifies fatty acid composition of mouse adipose tissue, brain, and liver. Lipids 32: 965-969; 1997. (Pubitemid 27398491)
51. Tallman, D. L.; Taylor, C. G. Effects of dietary fat and zinc on adiposity, serum leptin and adipose fatty acid composition in C57BL/6J mice. J. Nutr. Biochem 14: 17 -23; 2003. (Pubitemid 36143747)
52. Gerard-Monnier, D.; Erdelmeier, I.; Regnard, K.; Moze-Henry, N.; Yadan, J. C.; Chaudiere, J. Reactions of 1-methyl-2-phenylindole with malondialdehyde and 4-hydroxyalkenals: analytical applications to a colorimetric assay of lipid peroxidation. Chem. Res. Toxicol. 11 : 117 6 -1183; 1998. (Pubitemid 28500798)
53. Drechsel, D. A.; Patel, M. Differential contribution of the mitochondrial respiratory chain complexes to reactive oxygen species production by redox cycling agents implicated in parkinsonism. Toxicol. Sci 112 : 427-434; 2009.
54. Kyrou, I.; Chrousos, G. P.; Tsigos, C. Stress, visceral obesity, and metabolic complications. Ann. N. Y. Acad. Sci. 1083: 77-110; 2006.
55. Matsuzawa, Y.; Shimomura, I.; Nakamura, T.; Keno, Y.; Kotani, K.; Tokunaga, K. Pathophysiology and pathogenesis of visceral fat obesity. Obes. Res. 3(Suppl. 2): 187S-194S; 1995.
56. Coate, K. C.; Huggins, K. W. Consumption of a high glycemic index diet increases abdominal adiposity but does not influence adipose tissue pro-oxidant and antioxidant gene expression in C57BL/6 mice. Nutr. Res 30: 141-150; 2010.
57. Huh, J. Y.; Kim, Y.; Jeong, J.; Park, J.; Kim, I.; Huh, K. H.; Kim, Y. S.; Woo, H. A.; Rhee, S. G.; Lee, K. J.; Ha, H. Peroxiredoxin 3 is a key molecule regulating adipocyte oxidative stress, mitochondrial biogenesis, and adipokine expression. Antioxid. Redox Signaling 16: 229-243; 2011.
58. Lee, Y. S.; Kim, A. Y.; Choi, J. W.; Kim, M.; Yasue, S.; Son, H. J.; Masuzaki, H.; Park, K. S.; Kim, J. B. Dysregulation of adipose glutathione peroxidase 3 in obesity contributes to local and systemic oxidative stress. Mol. Endocrinol. 22: 2176-2189; 2008.
59. Balogh, L. M.; Atkins, W. M. Interactions of glutathione transferases with 4-hydroxynonenal. Drug Metab. Rev. 43: 165-178; 2011.
60. Balogh, L. M.; Le Trong, I.; Kripps, K. A.; Shireman, L. M.; Stenkamp, R. E.; Zhang, W.; Mannervik, B.; Atkins, W. M. Substrate specificity combined with stereopromiscuity in glutathione transferase A4-4-dependent metabolism of 4-hydroxynonenal. Biochemistry 49: 1541-1548; 2010.
61. Vatsyayan, R.; Lelsani, P. C.; Chaudhary, P.; Kumar, S.; Awasthi, S.; Awasthi, Y. C. The expression and function of vascular endothelial growth factor in retinal pigment epithelial (RPE) cells is regulated by 4-hydroxynonenal (HNE) and glutathione S-transferaseA4-4. Biochem. Biophys. Res. Commun. 417: 346-351; 2012.
62. Muthukumar, K.; Rajakumar, S.; Sarkar, M. N.; Nachiappan, V. Glutathione peroxidase3 of Saccharomyces cerevisiae protects phospholipids during cadmium-induced oxidative stress. Antonie van Leeuwenhoek 99: 761-771; 2011.
63. Nagy, P.; Karton, A.; Betz, A.; Peskin, A. V.; Pace, P.; O'Reilly, R. J.; Hampton, M. B.; Radom, L.; Winterbourn, C. C. Model for the exceptional reactivity of peroxiredoxins 2 and 3 with hydrogen peroxide: a kinetic and computational study. J. Biol. Chem. 286: 18 0 4 8 -18055; 2011.
64. Korsic, M.; Gotovac, K.; Nikolac, M.; Dusek, T.; Skegro, M.; Muck-Seler, D.; Borovecki, F.; Pivac, N. Gene expression in visceral and subcutaneous adipose tissue in overweight women. Front. Biosci. (Elite edition) 4: 2834-2844; 2012.
65. Alvehus, M.; Buren, J.; Sjostrom, M.; Goedecke, J.; Olsson, T. The human visceral fat depot has a unique inflammatory profile. Obesity (Silver Spring) 18 : 879-883; 2010.
66. Olefsky, J. M.; Glass, C. K. Macrophages, inflammation, and insulin resistance. Annu. Rev. Physiol. 72: 219-246; 2010.
67. Tzanavari, T.; Giannogonas, P.; Karalis, K. P. TNF-alpha and obesity. Curr. Dir. Autoimmun 11 : 145-156; 2010.