Endothelial Acyl-CoA synthetase 1 is not required for inflammatory and apoptotic effects of a saturated fatty acid-rich environment

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 2, 2013, Pages 232-240

  Li, Xin ^a   Gonzalez, Oscar ^a   Shen, Xia ^a   Barnhart, Shelley ^a   Kramer, Farah ^a   Kanter, Jenny E ^a   Vivekanandan Giri, Anuradha ^b   Tsuchiya, Kyoichiro ^c   Handa, Priya ^a   Pennathur, Subramaniam ^b   Kim, Francis ^a   Coleman, Rosalind A ^d   Schaffer, Jean E ^e   Bornfeldt, Karin E ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c Surgeons of Columbia University ^*  (United States)

^d IL   (United States)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

acyl CoA synthetase; apoptosis; endothelium; inflammation

Indexed keywords

ACYL COENZYME A SYNTHETASE 1; LIGASE; LONG CHAIN FATTY ACID COENZYME A LIGASE; SATURATED FATTY ACID; UNCLASSIFIED DRUG;

ADIPOSE TISSUE; ANIMAL CELL; APOPTOSIS; ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIUM CELL; FEMALE; GENE OVEREXPRESSION; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ACYL COENZYME A; ADIPOSE TISSUE; ANIMALS; AORTA; APOPTOSIS; CATTLE; CELLS, CULTURED; COENZYME A LIGASES; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIAL CELLS; ENZYME ACTIVATION; FATTY ACIDS; INFLAMMATION; INSULIN RESISTANCE; INTERCELLULAR ADHESION MOLECULE-1; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OBESITY; PALMITOYL COENZYME A; RNA INTERFERENCE; TIME FACTORS; TRANSFECTION; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84872930995     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.252239     Document Type: Article

References (34)

1. Versari D, Daghini E, Virdis A, Ghiadoni L, Taddei S. Endothelial dysfunction as a target for prevention of cardiovascular disease. Diabetes Care. 2009;32(Suppl 2):S314-S321.
2. Kanda T, Brown JD, Orasanu G, Vogel S, Gonzalez FJ, Sartoretto J, Michel T, Plutzky J. PPARgamma in the endothelium regulates metabolic responses to high-fat diet in mice. J Clin Invest. 2009;119:110-124.
3. Steinberg HO, Tarshoby M, Monestel R, Hook G, Cronin J, Johnson A, Bayazeed B, Baron AD. Elevated circulating free fatty acid levels impair endothelium-dependent vasodilation. J Clin Invest. 1997;100: 1230-1239.
4. Cacicedo JM, Benjachareowong S, Chou E, Ruderman NB, Ido Y. Palmitate-induced apoptosis in cultured bovine retinal pericytes: roles of NAD(P)H oxidase, oxidant stress, and ceramide. Diabetes. 2005;54: 1838-1845.
5. Kim F, Pham M, Luttrell I, Bannerman DD, Tupper J, Thaler J, Hawn TR, Raines EW, Schwartz MW. Toll-like receptor-4 mediates vascular infammation and insulin resistance in diet-induced obesity. Circ Res. 2007;100:1589-1596.
6. Harvey KA, Walker CL, Pavlina TM, Xu Z, Zaloga GP, Siddiqui RA. Long-chain saturated fatty acids induce pro-infammatory responses and impact endothelial cell growth. Clin Nutr. 2010;29:492-500.
7. Schaeffer A, Gross P, Buettner R, Bollheimer C, Buechler C, Neumeier M, Kopp A, Schoelmerich J, Falk W. Fatty acid-induced induction of Tolllike receptor-4/nuclear factor-kappaB pathway in adipocytes links nutritional signalling with innate immunity. Immunology. 2009;126:233-245.
8. Dasu MR, Jialal I. Free fatty acids in the presence of high glucose amplify monocyte infammation via Toll-like receptors. Am J Physiol Endocrinol Metab. 2011;300:E145-E154.
9. Wong SW, Kwon MJ, Choi AM, Kim HP, Nakahira K, Hwang DH. Fatty acids modulate Toll-like receptor 4 activation through regulation of receptor dimerization and recruitment into lipid rafts in a reactive oxygen species-dependent manner. J Biol Chem. 2009;284:27384-27392.
10. Schwartz EA, Zhang WY, Karnik SK, Borwege S, Anand VR, Laine PS, Su Y, Reaven PD. Nutrient modifcation of the innate immune response: a novel mechanism by which saturated fatty acids greatly amplify mono-cyte infammation. Arterioscler Thromb Vasc Biol. 2010;30:802-808.
11. Erridge C, Samani NJ. Saturated fatty acids do not directly stimulate Toll-like receptor signaling. Arterioscler Thromb Vasc Biol. 2009;29: 1944-1949.
12. Borradaile NM, Han X, Harp JD, Gale SE, Ory DS, Schaffer JE. Disruption of endoplasmic reticulum structure and integrity in lipotoxic cell death. J Lipid Res. 2006;47:2726-2737.
13. Staiger K, Staiger H, Weigert C, Haas C, Häring HU, Kellerer M. Saturated, but not unsaturated, fatty acids induce apoptosis of human coronary artery endothelial cells via nuclear factor-kappaB activation. Diabetes. 2006;55:3121-3126.
14. Eizirik DL, Cardozo AK, Cnop M. The role for endoplasmic reticulum stress in diabetes mellitus. Endocr Rev. 2008;29:42-61.
15. Li LO, Klett EL, Coleman RA. Acyl-CoA synthesis, lipid metabolism and lipotoxicity. Biochim Biophys Acta. 2010;1801:246-251.
16. Sandoval A, Fraisl P, Arias-Barrau E, Dirusso CC, Singer D, Sealls W, Black PN. Fatty acid transport and activation and the expression patterns of genes involved in fatty acid traffcking. Arch Biochem Biophys. 2008;477:363-371.
17. Chiu HC, Kovacs A, Ford DA, Hsu FF, Garcia R, Herrero P, Safftz JE, Schaffer JE. A novel mouse model of lipotoxic cardiomyopathy. J Clin Invest. 2001;107:813-822.
18. Kanter JE, Kramer F, Barnhart S, et al. Diabetes promotes an infam-matory macrophage phenotype and atherosclerosis through acyl-CoA synthetase 1. Proc Natl Acad Sci USA. 2012;109:E715-E724.
19. Li LO, Ellis JM, Paich HA, Wang S, Gong N, Altshuller G, Thresher RJ, Koves TR, Watkins SM, Muoio DM, Cline GW, Shulman GI, Coleman RA. Liver-specifc loss of long chain acyl-CoA synthetase-1 decreases triacylglycerol synthesis and beta-oxidation and alters phospholipid fatty acid composition. J Biol Chem. 2009;284:27816-27826.
20. Subramanian S, Han CY, Chiba T, McMillen TS, Wang SA, Haw A 3rd, Kirk EA, O'Brien KD, Chait A. Dietary cholesterol worsens adipose tissue macrophage accumulation and atherosclerosis in obese LDL receptor-defcient mice. Arterioscler Thromb Vasc Biol. 2008;28: 685-691.
21. Averill MM, Barnhart S, Becker L, Li X, Heinecke JW, Leboeuf RC, Hamerman JA, Sorg C, Kerkhoff C, Bornfeldt KE. S100A9 differentially modifes phenotypic states of neutrophils, macrophages, and dendritic cells: implications for atherosclerosis and adipose tissue infammation. Circulation. 2011;123:1216-1226.
22. Ieronimakis N, Balasundaram G, Reyes M. Direct isolation, culture and transplant of mouse skeletal muscle derived endothelial cells with angio-genic potential. PLoS ONE. 2008;3:e0001753.
23. Tsuchiya K, Tanaka J, Shuiqing Y, Welch CL, DePinho RA, Tabas I, Tall AR, Goldberg IJ, Accili D. FoxOs integrate pleiotropic actions of insulin in vascular endothelium to protect mice from atherosclerosis. Cell Metab. 2012;15:372-381.
24. Psychogios N, Hau DD, Peng J, et al. The human serum metabolome. PLoS ONE. 2011;6:e16957.
25. Yamagishi S, Okamoto T, Amano S, Inagaki Y, Koga K, Koga M, Choei H, Sasaki N, Kikuchi S, Takeuchi M, Makita Z. Palmitate-induced apoptosis of microvascular endothelial cells and pericytes. Mol Med. 2002;8:179-184.
26. Ciapaite J, van Bezu J, van Eikenhorst G, Bakker SJ, Teerlink T, Diamant M, Heine RJ, Krab K, Westerhoff HV, Schalkwijk CG. Palmitate and oleate have distinct effects on the infammatory phenotype of human endothelial cells. Biochim Biophys Acta. 2007;1771:147-154.
27. Cnop M, Welsh N, Jonas JC, Jörns A, Lenzen S, Eizirik DL. Mechanisms of pancreatic beta-cell death in type 1 and type 2 diabetes: many differences, few similarities. Diabetes. 2005;54(Suppl 2):S97-107.
28. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science. 2000;287:664-666.
29. Pfaffenbach KT, Gentile CL, Nivala AM, Wang D, Wei Y, Pagliassotti MJ. Linking endoplasmic reticulum stress to cell death in hepato-cytes: roles of C/EBP homologous protein and chemical chaperones in palmitate-mediated cell death. Am J Physiol Endocrinol Metab. 2010;298:E1027-E1035.
30. Huang S, Rutkowsky JM, Snodgrass RG, Ono-Moore KD, Schneider DA, Newman JW, Adams SH, Hwang DH. Saturated fatty acids activate TLR-mediated proinfammatory signaling pathways. J Lipid Res. 2012;53:2002-2013.
31. Watt MJ, Hoy AJ, Muoio DM, Coleman RA. Distinct roles of spe-cifc fatty acids in cellular processes: implications for interpreting and reporting experiments. Am J Physiol Endocrinol Metab. 2012;302:E1-E3.
32. Liu L, Shi X, Bharadwaj KG, Ikeda S, Yamashita H, Yagyu H, Schaffer JE, Yu YH, Goldberg IJ. DGAT1 expression increases heart triglyceride content but ameliorates lipotoxicity. J Biol Chem. 2009;284:36312-36323.
33. Ellis JM, Li LO, Wu PC, Koves TR, Ilkayeva O, Stevens RD, Watkins SM, Muoio DM, Coleman RA. Adipose acyl-CoA synthetase-1 directs fatty acids toward beta-oxidation and is required for cold thermogenesis. Cell Metab. 2010;12:53-64.
34. Ellis JM, Mentock SM, Depetrillo MA, Koves TR, Sen S, Watkins SM, Muoio DM, Cline GW, Taegtmeyer H, Shulman GI, Willis MS, Coleman RA. Mouse cardiac acyl coenzyme a synthetase 1 defciency impairs Fatty Acid oxidation and induces cardiac hypertrophy. Mol Cell Biol. 2011;31:1252-1262.