Oleate prevents palmitate-induced mitochondrial dysfunction, insulin resistance and inflammatory signaling in neuronal cells

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 7, 2014, Pages 1402-1413

  Kwon, Bumsup ^a   Lee, Han Kyu ^a   Querfurth, Henry W ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Inflammation; Insulin resistance; Mitochondrial dysfunction; Oleate; Palmitate

Indexed keywords

CERAMIDE; CYCLIC AMP DEPENDENT PROTEIN KINASE; DIACYLGLYCEROL; DOCOSAHEXAENOIC ACID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LINOLEIC ACID; MITOGEN ACTIVATED PROTEIN KINASE; OLEIC ACID; PALMITIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; SUPEROXIDE; TRIACYLGLYCEROL; BOVINE SERUM ALBUMIN; PPARGC1A PROTEIN, HUMAN; RELA PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RELA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CELL; CELL PROTECTION; CONTROLLED STUDY; CYTOTOXICITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME INHIBITION; INFLAMMATION; INSULIN RESISTANCE; INTRACELLULAR SIGNALING; MOUSE; NERVE CELL; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; ANIMAL; ANIMAL EMBRYO; ANTAGONISTS AND INHIBITORS; BOVINAE; BRAIN CORTEX; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MITOCHONDRION; RAT; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; TUMOR CELL LINE;

ANIMALS; CATTLE; CELL LINE, TUMOR; CELL SURVIVAL; CEREBRAL CORTEX; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DOCOSAHEXAENOIC ACIDS; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSULIN RESISTANCE; LINOLEIC ACID; MICE; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASES; NEURONS; OLEIC ACID; PALMITIC ACID; RATS; RATS, SPRAGUE-DAWLEY; SERUM ALBUMIN, BOVINE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTORS;

EID: 84899548867     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.04.004     Document Type: Article

References (67)

1. Zeyda M., Stulnig T.M. Obesity, inflammation, and insulin resistance-a mini-review. Gerontology 2009, 55:379-386.
2. Funaki M. Saturated fatty acids and insulin resistance. J. Med. Investig. 2009, 56:88-92.
3. Boden G. Fatty acid-induced inflammation and insulin resistance in skeletal muscle and liver. Curr. Diab. Rep. 2006, 6:177-181.
4. Xu H., Barnes G.T., Yang Q., Tan G., Yang D., Chou C.J., Sole J., Nichols A., Ross J.S., Tartaglia L.A., Chen H. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Invest. 2003, 112:1821-1830.
5. De Souza C.T., Araujo E.P., Bordin S., Ashimine R., Zollner R.L., Boschero A.C., Saad M.J., Velloso L.A. Consumption of a fat-rich diet activates a proinflammatory response and induces insulin resistance in the hypothalamus. Endocrinology 2005, 146:4192-4199.
6. Posey K.A., Clegg D.J., Printz R.L., Byun J., Morton G.J., Vivekanandan-Giri A., Pennathur S., Baskin D.G., Heinecke J.W., Woods S.C., Schwartz M.W., Niswender K.D. Hypothalamic proinflammatory lipid accumulation, inflammation, and insulin resistance in rats fed a high-fat diet. Am. J. Physiol. Endocrinol. Metab. 2009, 296:E1003-E1012.
7. Coll T., Jove M., Rodriguez-Calvo R., Eyre E., Palomer X., Sanchez R.M., Merlos M., Laguna J.C., Vazquez-Carrera M. Palmitate-mediated downregulation of peroxisome proliferator-activated receptor-gamma coactivator 1alpha in skeletal muscle cells involves MEK1/2 and nuclear factor-kappaB activation. Diabetes 2006, 55:2779-2787.
8. Jove M., Planavila A., Sanchez R.M., Merlos M., Laguna J.C., Vazquez-Carrera M. Palmitate induces tumor necrosis factor-alpha expression in C2C12 skeletal muscle cells by a mechanism involving protein kinase C and nuclear factor-kappaB activation. Endocrinology 2006, 147:552-561.
9. Green C.J., Macrae K., Fogarty S., Hardie D.G., Sakamoto K., Hundal H.S. Counter-modulation of fatty acid-induced pro-inflammatory nuclear factor kappaB signalling in rat skeletal muscle cells by AMP-activated protein kinase. Biochem. J. 2011, 435:463-474.
10. Ajuwon K.M., Spurlock M.E. Palmitate activates the NF-kappaB transcription factor and induces IL-6 and TNFalpha expression in 3T3-L1 adipocytes. J. Nutr. 2005, 135:1841-1846.
11. Maloney E., Sweet I.R., Hockenbery D.M., Pham M., Rizzo N.O., Tateya S., Handa P., Schwartz M.W., Kim F. Activation of NF-kappaB by palmitate in endothelial cells: a key role for NADPH oxidase-derived superoxide in response to TLR4 activation. Arterioscler. Thromb. Vasc. Biol. 2009, 29:1370-1375.
12. Cai D. NFkappaB-mediated metabolic inflammation in peripheral tissues versus central nervous system. Cell Cycle 2009, 8:2542-2548.
13. Burstein E., Duckett C.S. Dying for NF-kappaB? Control of cell death by transcriptional regulation of the apoptotic machinery. Curr. Opin. Cell Biol. 2003, 15:732-737.
14. Hayden M.S., Ghosh S. Signaling to NF-kappaB. Genes Dev. 2004, 18:2195-2224.
15. Barnes P.J., Karin M. Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. N. Engl. J. Med. 1997, 336:1066-1071.
16. Li Y.P., Schwartz R.J., Waddell I.D., Holloway B.R., Reid M.B. Skeletal muscle myocytes undergo protein loss and reactive oxygen-mediated NF-kappaB activation in response to tumor necrosis factor alpha. FASEB J. 1998, 12:871-880.
17. Staiger K., Staiger H., Weigert C., Haas C., Haring H.U., 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.
18. Miller T.A., LeBrasseur N.K., Cote G.M., Trucillo M.P., Pimentel D.R., Ido Y., Ruderman N.B., Sawyer D.B. Oleate prevents palmitate-induced cytotoxic stress in cardiac myocytes. Biochem. Biophys. Res. Commun. 2005, 336:309-315.
19. Piro S., Maniscalchi E.T., Monello A., Pandini G., Mascali L.G., Rabuazzo A.M., Purrello F. Palmitate affects insulin receptor phosphorylation and intracellular insulin signal in a pancreatic alpha-cell line. Endocrinology 2010, 151:4197-4206.
20. Gao D., Nong S., Huang X., Lu Y., Zhao H., Lin Y., Man Y., Wang S., Yang J., Li J. The effects of palmitate on hepatic insulin resistance are mediated by NADPH oxidase 3-derived reactive oxygen species through JNK and p38MAPK pathways. J. Biol. Chem. 2010, 285:29965-29973.
21. Kaminska B. MAPK signalling pathways as molecular targets for anti-inflammatory therapy-from molecular mechanisms to therapeutic benefits. Biochim. Biophys. Acta 2005, 1754:253-262.
22. Tanti J.F., Jager J. Cellular mechanisms of insulin resistance: role of stress-regulated serine kinases and insulin receptor substrates (IRS) serine phosphorylation. Curr. Opin. Pharmacol. 2009, 9:753-762.
23. Mayer C.M., Belsham D.D. Palmitate attenuates insulin signaling and induces endoplasmic reticulum stress and apoptosis in hypothalamic neurons: rescue of resistance and apoptosis through adenosine 5' monophosphate-activated protein kinase activation. Endocrinology 2010, 151:576-585.
24. Choi S.J., Kim F., Schwartz M.W., Wisse B.E. Cultured hypothalamic neurons are resistant to inflammation and insulin resistance induced by saturated fatty acids. Am. J. Physiol. Endocrinol. Metab. 2010, 298:E1122-E1130.
25. Lee J.S., Pinnamaneni S.K., Eo S.J., Cho I.H., Pyo J.H., Kim C.K., Sinclair A.J., Febbraio M.A., Watt M.J. Saturated, but not n-6 polyunsaturated, fatty acids induce insulin resistance: role of intramuscular accumulation of lipid metabolites. J. Appl. Physiol. 2006, 100:1467-1474.
26. Rachek L.I., Musiyenko S.I., LeDoux S.P., Wilson G.L. Palmitate induced mitochondrial deoxyribonucleic acid damage and apoptosis in l6 rat skeletal muscle cells. Endocrinology 2007, 148:293-299.
27. Yuzefovych L., Wilson G., Rachek L. Different effects of oleate vs. palmitate on mitochondrial function, apoptosis, and insulin signaling in L6 skeletal muscle cells: role of oxidative stress. Am. J. Physiol. Endocrinol. Metab. 2010, 299:E1096-E1105.
28. Coll T., Eyre E., Rodriguez-Calvo R., Palomer X., Sanchez R.M., Merlos M., Laguna J.C., Vazquez-Carrera M. Oleate reverses palmitate-induced insulin resistance and inflammation in skeletal muscle cells. J. Biol. Chem. 2008, 283:11107-11116.
29. Nakamura S., Takamura T., Matsuzawa-Nagata N., Takayama H., Misu H., Noda H., Nabemoto S., Kurita S., Ota T., Ando H., Miyamoto K., Kaneko S. Palmitate induces insulin resistance in H4IIEC3 hepatocytes through reactive oxygen species produced by mitochondria. J. Biol. Chem. 2009, 284:14809-14818.
30. Kim J.A., Wei Y., Sowers J.R. Role of mitochondrial dysfunction in insulin resistance. Circ. Res. 2008, 102:401-414.
31. Liu S., Okada T., Assmann A., Soto J., Liew C.W., Bugger H., Shirihai O.S., Abel E.D., Kulkarni R.N. Insulin signaling regulates mitochondrial function in pancreatic beta-cells. PLoS One 2009, 4:e7983.
32. Calder P.C. Fatty acids and inflammation: the cutting edge between food and pharma. Eur. J. Pharmacol. 2011, 668(Suppl. 1):S50-S58.
33. Kalupahana N.S., Claycombe K.J., Moustaid-Moussa N. (n-3) Fatty acids alleviate adipose tissue inflammation and insulin resistance: mechanistic insights. Adv. Nutr. 2011, 2:304-316.
34. Peng G., Li L., Liu Y., Pu J., Zhang S., Yu J., Zhao J., Liu P. Oleate blocks palmitate-induced abnormal lipid distribution, endoplasmic reticulum expansion and stress, and insulin resistance in skeletal muscle. Endocrinology 2011, 152:2206-2218.
35. Gao D., Griffiths H.R., Bailey C.J. Oleate protects against palmitate-induced insulin resistance in L6 myotubes. Br. J. Nutr. 2009, 102:1557-1563.
36. de la Monte S.M. Brain insulin resistance and deficiency as therapeutic targets in Alzheimer's disease. Curr. Alzheimer Res. 2012, 9:35-66.
37. Hildreth K.L., Van Pelt R.E., Schwartz R.S. Obesity, insulin resistance, and Alzheimer's disease. Obesity (Silver Spring) 2012, 20:1549-1557.
38. Kim H.J., Magrane J. Isolation and culture of neurons and astrocytes from the mouse brain cortex. Methods Mol. Biol. 2011, 793:63-75.
39. Cistola D.P., Small D.M. Fatty acid distribution in systems modeling the normal and diabetic human circulation. A 13C nuclear magnetic resonance study. J. Clin. Invest. 1991, 87:1431-1441.
40. Folch J., Lees M., Sloane Stanley G.H. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 1957, 226:497-509.
41. Clogston J.D., Patri A.K. Lipid component quantitation by thin layer chromatography. Methods Mol. Biol. 2011, 697:109-117.
42. Gum E.T., Swanson R.A., Alano C., Liu J., Hong S., Weinstein P.R., Panter S.S. Human serum albumin and its N-terminal tetrapeptide (DAHK) block oxidant-induced neuronal death. Stroke 2004, 35:590-595.
43. Zoellner H., Hofler M., Beckmann R., Hufnagl P., Vanyek E., Bielek E., Wojta J., Fabry A., Lockie S., Binder B.R. Serum albumin is a specific inhibitor of apoptosis in human endothelial cells. J. Cell Sci. 1996, 109(Pt 10):2571-2580.
44. Mishra R., Simonson M.S. Saturated free fatty acids and apoptosis in microvascular mesangial cells: palmitate activates pro-apoptotic signaling involving caspase 9 and mitochondrial release of endonuclease G. Cardiovasc. Diabetol. 2005, 4:2.
45. Corsetto P.A., Montorfano G., Zava S., Jovenitti I.E., Cremona A., Berra B., Rizzo A.M. Effects of n-3 PUFAs on breast cancer cells through their incorporation in plasma membrane. Lipids Health Dis. 2011, 10:73.
46. Lu X.F., He G.Q., Yu H.N., Ma Q., Shen S.R., Das U.N. Colorectal cancer cell growth inhibition by linoleic acid is related to fatty acid composition changes. J. Zhejiang Univ. Sci. B 2010, 11:923-930.
47. Savary S., Trompier D., Andreoletti P., Le Borgne F., Demarquoy J., Lizard G. Fatty acids-induced lipotoxicity and inflammation. Curr. Drug Metab. 2012, 13:1358-1370.
48. Cascio G., Schiera G., Di Liegro I. Dietary fatty acids in metabolic syndrome, diabetes and cardiovascular diseases. Curr. Diabetes Rev. 2012, 8:2-17.
49. Morris M.C., Evans D.A., Bienias J.L., Tangney C.C., Bennett D.A., Aggarwal N., Schneider J., Wilson R.S. Dietary fats and the risk of incident Alzheimer disease. Arch. Neurol. 2003, 60:194-200.
50. Solfrizzi V., Panza F., Frisardi V., Seripa D., Logroscino G., Imbimbo B.P., Pilotto A. Diet and Alzheimer's disease risk factors or prevention: the current evidence. Expert. Rev. Neurother. 2011, 11:677-708.
51. Delarue J., Magnan C. Free fatty acids and insulin resistance. Curr. Opin. Clin. Nutr. Metab. Care 2007, 10:142-148.
52. Handschin C., Spiegelman B.M. Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr. Rev. 2006, 27:728-735.
53. Johnson R.F., Witzel I.I., Perkins N.D. p53-dependent regulation of mitochondrial energy production by the RelA subunit of NF-kappaB. Cancer Res. 2011, 71:5588-5597.
54. St-Pierre J., Drori S., Uldry M., Silvaggi J.M., Rhee J., Jager S., Handschin C., Zheng K., Lin J., Yang W., Simon D.K., Bachoo R., Spiegelman B.M. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 2006, 127:397-408.
55. Lennon R., Pons D., Sabin M.A., Wei C., Shield J.P., Coward R.J., Tavare J.M., Mathieson P.W., Saleem M.A., Welsh G.I. Saturated fatty acids induce insulin resistance in human podocytes: implications for diabetic nephropathy. Nephrol. Dial. Transplant. 2009, 24:3288-3296.
56. Yang L., Qian Z., Ji H., Yang R., Wang Y., Xi L., Sheng L., Zhao B., Zhang X. Inhibitory effect on protein kinase Ctheta by Crocetin attenuates palmitate-induced insulin insensitivity in 3T3-L1 adipocytes. Eur. J. Pharmacol. 2010, 642:47-55.
57. Salvado L., Coll T., Gomez-Foix A.M., Salmeron E., Barroso E., Palomer X., Vazquez-Carrera M. Oleate prevents saturated-fatty-acid-induced ER stress, inflammation and insulin resistance in skeletal muscle cells through an AMPK-dependent mechanism. Diabetologia 2013, 56:1372-1382.
58. Samad F., Badeanlou L., Shah C., Yang G. Adipose tissue and ceramide biosynthesis in the pathogenesis of obesity. Adv. Exp. Med. Biol. 2011, 721:67-86.
59. de la Monte S.M. Triangulated mal-signaling in Alzheimer's disease: roles of neurotoxic ceramides, ER stress, and insulin resistance reviewed. J. Alzheimers Dis. 2012, 30(Suppl. 2):S231-S249.
60. Pickersgill L., Litherland G.J., Greenberg A.S., Walker M., Yeaman S.J. Key role for ceramides in mediating insulin resistance in human muscle cells. J. Biol. Chem. 2007, 282:12583-12589.
61. Lee J.Y., Cho H.K., Kwon Y.H. Palmitate induces insulin resistance without significant intracellular triglyceride accumulation in HepG2 cells. Metabolism 2010, 59:927-934.
62. Peterson J.M., Wang Y., Bryner R.W., Williamson D.L., Alway S.E. Bax signaling regulates palmitate-mediated apoptosis in C(2)C(12) myotubes. Am. J. Physiol. Endocrinol. Metab. 2008, 295:E1307-E1314.
63. Maedler K., Oberholzer J., Bucher P., Spinas G.A., Donath M.Y. Monounsaturated fatty acids prevent the deleterious effects of palmitate and high glucose on human pancreatic beta-cell turnover and function. Diabetes 2003, 52:726-733.
64. Listenberger L.L., Han X., Lewis S.E., Cases S., Farese R.V., Ory D.S., Schaffer J.E. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:3077-3082.
65. Bazan N.G., Molina M.F., Gordon W.C. Docosahexaenoic acid signalolipidomics in nutrition: significance in aging, neuroinflammation, macular degeneration, Alzheimer's, and other neurodegenerative diseases. Annu. Rev. Nutr. 2011, 31:321-351.
66. Quinn J.F., Raman R., Thomas R.G., Yurko-Mauro K., Nelson E.B., Van Dyck C., Galvin J.E., Emond J., Jack C.R., Weiner M., Shinto L., Aisen P.S. Docosahexaenoic acid supplementation and cognitive decline in Alzheimer disease: a randomized trial. JAMA 2010, 304:1903-1911.
67. Sinn N., Milte C.M., Street S.J., Buckley J.D., Coates A.M., Petkov J., Howe P.R. Effects of n-3 fatty acids, EPA v. DHA, on depressive symptoms, quality of life, memory and executive function in older adults with mild cognitive impairment: a 6-month randomised controlled trial. Br. J. Nutr. 2012, 107:1682-1693.