Activation of NF-κB by palmitate in endothelial cells: A key role for NADPH oxidase-derived superoxide in response to TLR4 activation

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 29, Issue 9, 2009, Pages 1370-1375

  Maloney, Ezekiel ^a   Sweet, Ian R ^b   Hockenbery, David M ^a,c   Pham, Matilda ^a   Rizzo, Norma O ^a,b   Tateya, Sanshiro ^a,b   Handa, Priya ^a,b   Schwartz, Michael W ^a,b   Kim, Francis ^a,b  

^a Department of Medicine ^*  (United States)

^b Diabetes and Obesity Center of Excellence   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Endothelial cells; NADPH oxidase; Toll like receptor 4; Vascular inflammation

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; DIPHENYLIODONIUM SALT; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; PALMITIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SUPEROXIDE; SUPEROXIDE DISMUTASE; TOLL LIKE RECEPTOR 4; BMP4 PROTEIN, MOUSE; CATION; I KAPPA B; IL6 PROTEIN, HUMAN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE; MESSENGER RNA; MYD88 PROTEIN, HUMAN; MYELOID DIFFERENTIATION FACTOR 88; NF KAPPAB INHIBITOR ALPHA; NF-KAPPAB INHIBITOR ALPHA; NOX4 PROTEIN, HUMAN; NOX4 PROTEIN, MOUSE; TLR4 PROTEIN, HUMAN; TLR4 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; INFLAMMATION; LIPID DIET; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; CELL CULTURE; DRUG EFFECT; ENZYMOLOGY; FAT INTAKE; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; THORACIC AORTA; TIME;

ANIMALS; AORTA, THORACIC; BONE MORPHOGENETIC PROTEIN 4; CELLS, CULTURED; DIETARY FATS; ENDOTHELIAL CELLS; HUMANS; I-KAPPA B PROTEINS; INTERCELLULAR ADHESION MOLECULE-1; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; INTERLEUKIN-6; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; NADPH OXIDASE; NF-KAPPA B; ONIUM COMPOUNDS; PALMITIC ACID; PHOSPHORYLATION; RNA INTERFERENCE; RNA, MESSENGER; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE; SUPEROXIDES; TIME FACTORS; TOLL-LIKE RECEPTOR 4;

EID: 69849111863     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.109.188813     Document Type: Article

References (33)

1. Kim F, Pham M, Luttrell I, Bannerman DD, Tupper J, Thaler J, Hawn TR, Raines EW, Schwartz MW. Toll-like receptor-4 mediates vascular inflammation and insulin resistance in diet-induced obesity. Circ Res. 2007;100:1589-1596.
2. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxi-dases: physiology and pathophysiology. Physiol Rev. 2007;87:245-313.
3. San Martin A, Du P, Dikalova A, Lassegue B, Aleman M, Gongora MC, Brown K, Joseph G, Harrison DG, Taylor WR, Jo H, Griendling KK. Reactive oxygen species-selective regulation of aortic inflammatory gene expression in Type 2 diabetes. Am J Physiol Heart Circ Physiol. 2007;292: H2073-H2082.
4. Inoguchi T, Li P, Umeda F, Yu HY, Kakimoto M, Imamura M, Aoki T, Etoh T, Hashimoto T, Naruse M, Sano H, Utsumi H, Nawata H. High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase C-dependent activation of NAD(P)H oxidase in cultured vascular cells. Diabetes. 2000;49:1939-1945.
5. Park HS, Chun JN, Jung HY, Choi C, Bae YS. Role of NADPH oxidase 4 in lipopolysaccharide-induced proinflammatory responses by human aortic endothelial cells. Cardiovasc Res. 2006;72:447-455.
6. Cousin SP, Hugl SR, Wrede CE, Kajio H, Myers MG Jr, Rhodes CJ. Free fatty acid-induced inhibition of glucose and insulin-like growth factor I-induced deoxyribonucleic acid synthesis in the pancreatic beta-cell line INS-1. Endocrinology. 2001;142:229-240.
7. Gallis B, Corthals GL, Goodlett DR, Ueba H, Kim F, Presnell SR, Figeys D, Harrison DG, Berk BC, Aebersold R, Corson MA. Identification of flow-dependent endothelial nitric-oxide synthase phosphorylation sites by mass spectrometry and regulation of phosphorylation and nitric oxide production by the phosphatidylinositol 3-kinase inhibitor LY294002. J Biol Chem. 1999;274:30101-30108.
8. Bannerman DD, Erwert RD, Winn RK, Harlan JM. TIRAP mediates endotoxin-induced NF-kappaB activation and apoptosis in endothelial cells. Biochem Biophys Res Commun. 2002;295:157-162.
9. Bannerman DD, Tupper JC, Erwert RD, Winn RK, Harlan JM. Divergence of bacterial lipopolysaccharide pro-apoptotic signaling downstream of IRAK-1. J Biol Chem. 2002;277:8048-8053.
10. Ferri N, Garton KJ, Raines EW. An NF-kappaB-dependent transcriptional program is required for collagen remodeling by human smooth muscle cells. J Biol Chem. 2003;278:19757-19764.
11. Landmesser U, Cai H, Dikalov S, McCann L, Hwang J, Jo H, Holland SM, Harrison DG. Role of p47(phox) in vascular oxidative stress and hypertension caused by angiotensin II. Hypertension. 2002;40:511-515.
12. Dikalov SI, Li W, Mehranpour P, Wang SS, Zafari AM. Production of extracellular superoxide by human lymphoblast cell lines: comparison of electron spin resonance techniques and cytochrome C reduction assay. Biochem Pharmacol. 2007;73:972-980.
13. Chalupsky K, Cai H. Endothelial dihydrofolate reductase: critical for nitric oxide bioavailability and role in angiotensin II uncoupling of endothelial nitric oxide synthase. Proc Natl Acad Sci U S A. 2005;102:9056-9061.
14. Kim F, Tysseling KA, Rice J, Pham M, Haji L, Gallis BM, Baas AS, Paramsothy P, Giachelli CM, Corson MA, Raines EW. Free fatty acid impairment of nitric oxide production in endothelial cells is mediated by IKKbeta. Arterioscler Thromb Vasc Biol. 2005;25:989-994.
15. Miriyala S, Gongora Nieto MC, Mingone C, Smith D, Dikalov S, Harrison DG, Jo H. Bone morphogenic protein-4 induces hypertension in mice: role of noggin, vascular NADPH oxidases, and impaired vasore-laxation. Circulation. 2006;113:2818-2825.
16. Beckman JA, Creager MA, Libby P. Diabetes and atherosclerosis: epidemiology, pathophysiology, and management. JAMA. 2002;287:2570-2581.
17. Williams IL, Wheatcroft SB, Shah AM, Kearney MT. Obesity, atherosclerosis and the vascular endothelium: mechanisms of reduced nitric oxide bioavailability in obese humans. Int J Obes Relat Metab Disord. 2002;26:754-764.
18. Yki-Jarvinen H. Insulin resistance and endothelial dysfunction. Best Pract Res Clin Endocrinol Metab. 2003;17:411-430.
19. Kim F, Pham M, Maloney E, Rizzo NO, Morton GJ, Wisse BE, Kirk EA, Chait A, Schwartz MW. Vascular inflammation, insulin resistance, and reduced nitric oxide production precede the onset of peripheral insulin resistance. Arterioscler Thromb Vasc Biol. 2008;28:1982-1988.
20. Mokdad AH, Serdula MK, Dietz WH, Bowman BA, Marks JS, Koplan JP. The spread of the obesity epidemic in the United States, 1991-1998. JAMA. 1999;282:1519-1522.
21. Yli-Jama P, Meyer HE, Ringstad J, Pedersen JI. Serum free fatty acid pattern and risk of myocardial infarction: a case-control study. J Intern Med. 2002;251:19-28.
22. Knopp RH, Retzlaff B, Walden C, Fish B, Buck B, McCann B. One-year effects of increasingly fat-restricted, carbohydrate-enriched diets on lipoprotein levels in free-living subjects. Proc Soc Exp Biol Med. 2000;225:191-199.
23. Artwohl M, Roden M, Waldhausl W, Freudenthaler A, Baumgartner-Parzer SM. Free fatty acids trigger apoptosis and inhibit cell cycle progression in human vascular endothelial cells. Faseb J. 2004;18:146-148.
24. Schreck R, Rieber P, Baeuerle PA. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J. 1991;10:2247-2258.
25. Lum H, Roebuck KA. Oxidant stress and endothelial cell dysfunction. Am J Physiol Cell Physiol. 2001;280:C719-C741.
26. Chen XL, Zhang Q, Zhao R, Ding X, Tummala PE, Medford RM. Rac1 and superoxide are required for the expression of cell adhesion molecules induced by tumor necrosis factor-alpha in endothelial cells. J Pharmacol Exp Ther. 2003;305:573-580.
27. Chen XL, Zhang Q, Zhao R, Medford RM. Superoxide, H2O2, and iron are required for TNF-alpha-induced MCP-1 gene expression in endothe-lial cells: role of Rac1 and NADPH oxidase. Am J Physiol Heart Circ Physiol. 2004;286:H1001-H1007.
28. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest. 2006;116:1793-1801.
29. Remer KA, Brcic M, Jungi TW. Toll-like receptor-4 is involved in eliciting an LPS-induced oxidative burst in neutrophils. Immunol Lett. 2003;85:75-80.
30. Ryan KA, Smith MF Jr, Sanders MK, Ernst PB. Reactive oxygen and nitrogen species differentially regulate Toll-like receptor 4-mediated activation of NF-kappa B and interleukin-8 expression. Infect Immun. 2004; 72:2123-2130.
31. Lopez JA, del Conde I, Shrimpton CN. Receptors, rafts, and microvesicles in thrombosis and inflammation. J Thromb Haemost. 2005;3:1737-1744.
32. Yvan-Charvet L, Welch C, Pagler TA, Ranalletta M, Lamkanfi M, Han S, Ishibashi M, Li R, Wang N, Tall AR. Increased inflammatory gene expression in ABC transporter-deficient macrophages: free cholesterol accumulation, increased signaling via toll-like receptors, and neutrophil infiltration of atherosclerotic lesions. Circulation. 2008;118:1837-1847.
33. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature. 2000;404:787-790.