Saturated long-chain fatty acids activate inflammatory signaling in astrocytes

Journal of Neurochemistry

Volumn 120, Issue 6, 2012, Pages 1060-1071

  Gupta, Sunita ^a   Knight, Alecia G ^a   Gupta, Shruti ^a   Keller, Jeffrey N ^a   Bruce Keller, Annadora J ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

Brain inflammation; Cytokines; Dyslipidemia; Obesity; Reactive gliosis

Indexed keywords

CD36 ANTIGEN; CERVONIC ACID; INTERLEUKIN 1BETA; INTERLEUKIN 6; LAURIC ACID; LEUCINE METHYL ESTER; LONG CHAIN FATTY ACID; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PALMITIC ACID; PALMITOYL COENZYME A; PHOSPHATIDYLINOSITOL 3 KINASE; STEARIC ACID; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL CULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE RELEASE; ENCEPHALITIS; ENZYME INHIBITION; FATTY ACID METABOLISM; FEMALE; GLIOSIS; IN VITRO STUDY; INFLAMMATION; MALE; MICROGLIA; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; BRAIN; CELLS, CULTURED; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ENZYME INHIBITORS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FATTY ACIDS; FEMALE; GENE EXPRESSION REGULATION; MALE; OLEIC ACID; PALMITIC ACID; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4;

EID: 84862812857     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07660.x     Document Type: Article

References (90)

1. Ajuwon K. M. and Spurlock M. E. (2005) Palmitate activates the NFkappaB transcription factor and induces IL-6 and TNFalpha expression in 3T3-L1 adipocytes. J. Nutr. 135, 1841-1846. (Pubitemid 41099739)
2. Akiyama H., Barger S. and Barnum S. et al. (2000) Inflammation and Alzheimer's disease. Neurobiol. Aging 21, 383-421. (Pubitemid 30349107)
3. Allan S. M. and Rothwell N. J. (2003) Inflammation in central nervous system injury. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 1669-1677. (Pubitemid 37298635)
4. Averill M. M. and Bornfeldt K. E. (2009) Lipids versus glucose in inflammation and the pathogenesis of macrovascular disease in diabetes. Curr. Diab. Rep. 9, 18-25.
5. Bellinger F. P., Madamba S. G., Campbell I. L. and Siggins G. R. (1995) Reduced long-term potentiation in the dentate gyrus of transgenic mice with cerebral overexpression of interleukin-6. Neurosci. Lett. 198, 95-98.
6. Bernoud N., Fenart L., Bénistant C., Pageaux J. F., Dehouck M. P., Molière P., Lagarde M., Cecchelli R. and Lecerf J. (1998) Astrocytes are mainly responsible for the polyunsaturated fatty acid enrichment in blood-brain barrier endothelial cells in vitro. J. Lipid Res. 39, 1816-1824. (Pubitemid 28411169)
7. Bourre J. M. (2004) Roles of unsaturated fatty acids (especially omega-3 fatty acids) in the brain at various ages and during ageing. J. Nutr. Health Aging 8, 163-174.
8. Bradley R. L., Fisher F. F. and Maratos-Flier E. (2008) Dietary fatty acids differentially regulate production of TNF-alpha and IL-10 by murine 3T3-L1 adipocytes. Obesity (Silver Spring) 16, 938-944. (Pubitemid 351620481)
9. Bruce-Keller A. J., Barger S. W., Moss N. I., Pham J. T., Keller J. N. and Nath A. (2001) Pro-inflammatory and pro-oxidant properties of the HIV protein Tat in a microglial cell line: attenuation by 17betaestradiol. J. Neurochem. 78, 1315-1324. (Pubitemid 32899763)
10. Bruce-Keller A. J., Keller J. N. and Morrison C. D. (2009) Obesity and vulnerability of the CNS. Biochim. Biophys. Acta 1792, 395-400.
11. Bruce-Keller A. J., White C. L., Gupta S., Knight A. G., Pistell P. J., Ingram D. K., Morrison C. D. and Keller J. N. (2010) NOX activity in brain aging: exacerbation by high fat diet. Free Radic. Biol. Med. 49, 22-30.
12. Calder P. C. (2007) Immunomodulation by omega-3 fatty acids. Prostaglandins Leukot. Essent. Fatty Acids 77, 327-335.
13. Davis J. E., Gabler N. K., Walker-Daniels J. and Spurlock M. E. (2008) Tlr-4 deficiency selectively protects against obesity induced by diets high in saturated fat. Obesity (Silver Spring), 16, 1248-1255. (Pubitemid 351770507)
14. De Smedt-Peyrusse V., Sarqueil F., Moranis A., Harizi H., Mongrand S. and Layé S. (2008) Docosahexaenoic acid prevents lipopolysaccharide- induced cytokine production in microglial cells by inhibiting lipopolysaccharide receptor presentation but not its membrane subdomain localization. J. Neurochem. 105, 296-307. (Pubitemid 351490003)
15. Dhopeshwarkar G. A. and Mead J. F. (1973) Uptake and transport of fatty acids into the brain and role of the blood-brain barrier system. Adv. Lipid Res. 11, 109-142.
16. Dyall S. C. and Michael-Titus A. T. (2008) Neurological benefits of omega-3 fatty acids. Neuromol. Med. 10, 219-235.
17. Eddy D. E. and Harman D. (1977) Free radical theory of aging: effect of age, sex and dietary precursors on rat-brain docosahexanoic acid. J. Am. Geriatr. Soc. 25, 220-229. (Pubitemid 8101973)
18. El-Hage N., Podhaizer E. M., Sturgill J. and Hauser K. F. (2011) Tolllike receptor expression and activation in astroglia: differential regulation by HIV-1 Tat, gp120, and morphine. Immunol. Invest. 40, 498-522.
19. Elias M. F., Elias P. K., Sullivan L. M., Wolf P. A. and D'Agostino R. B. (2003) Lower cognitive function in the presence of obesity and hypertension: the Framingham Heart Study. Int. J. Obes. Relat. Metab. Disord. 27, 260-268. (Pubitemid 36255810)
20. Elias M. F., Elias P. K., Sullivan L. M., Wolf P. A. and D'Agostino R. B. (2005) Obesity, diabetes and cognitive deficit: the Framingham Heart Study. Neurobiol. Aging 26, 11-16.
21. Erridge C., Kennedy S., Spickett C. M. and Webb D. J. (2008) Oxidized phospholipid inhibition of toll-like receptor (TLR) signaling is restricted to TLR2 and TLR4: roles for CD14, LPS-binding protein, and MD2 as targets for specificity of inhibition. J. Biol. Chem. 283, 24748-24759.
22. Farr S. A., Yamada K. A., Butterfield D. A., Abdul H. M., Xu L., Miller N. E., Banks W. A. and Morley J. E. (2008) Obesity and hypertriglyceridemia produce cognitive impairment. Endocrinology 149, 2628-2636. (Pubitemid 351574482)
23. Fedor D. and Kelley D. S. (2009) Prevention of insulin resistance by n-3 polyunsaturated fatty acids. Curr. Opin. Clin. Nutr. Metab. Care 12, 138-146.
24. Fillit H., Nash D. T., Rundek T. and Zuckerman A. (2008) Cardiovascular risk factors and dementia. Am. J. Geriatr. Pharmacother. 6, 100-118.
25. Fontani G., Corradeschi F., Felici A., Alfatti F., Migliorini S. and Lodi L. (2005) Cognitive and physiological effects of omega-3 polyunsaturated fatty acid supplementation in healthy subjects. Eur. J. Clin. Invest. 35, 691-699. (Pubitemid 41640905)
26. Gemma C. and Bickford P. C. (2007) Interleukin-1beta and caspase-1: players in the regulation of age-related cognitive dysfunction. Rev. Neurosci. 18, 137-148.
27. Gorina R., Font-Nieves M., Márquez-Kisinousky L., Santalucia T. and Planas A. M. (2011) Astrocyte TLR4 activation induces a proinflammatory environment through the interplay between MyD88- dependent NFjB signaling, MAPK, and Jak1/Stat1 pathways. Glia 59, 242-255.
28. Grant W. B. (1999) Dietary links to Alzheimer's disease: 1999 update. J. Alzheimer's Dis. 1, 197-201.
29. Haslam D. W. and James W. P. (2005) Obesity. Lancet Neurol. 366, 1197-1209. (Pubitemid 41393598)
30. Hassanali Z., Ametaj B. N., Field C. J., Proctor S. D. and Vine D. F. (2010) Dietary supplementation of n-3 PUFA reduces weight gain and improves postprandial lipaemia and the associated inflammatory response in the obese JCR:LA-cp rat. Diabetes Obes. Metab. 12, 139-147.
31. Håversen L., Danielsson K. N., Fogelstrand L. and Wiklund O. (2009) Induction of proinflammatory cytokines by long-chain saturated fatty acids in human macrophages. Atherosclerosis 202, 382-393.
32. Hotamisligil G. S. (2006) Inflammation and metabolic disorders. Nature 444, 860-867.
33. Jankowsky J. L. and Patterson P. H. (1999) Cytokine and growth factor involvement in long-term potentiation. Mol. Cell. Neurosci. 14, 273-286. (Pubitemid 29506159)
34. Jurdak N., Lichtenstein A. H. and Kanarek R. B. (2008) Diet-induced obesity and spatial cognition in young male rats. Nutr. Neurosci. 11, 48-54.
35. Karmi A., Iozzo P. and Viljanen A. et al. (2010) Increased brain fatty acid uptake in metabolic syndrome. Diabetes 59, 2171-2177.
36. Kennedy A., Martinez K., Chuang C. C., LaPoint K. and McIntosh M. (2009) Saturated fatty acid-mediated inflammation and insulin resistance in adipose tissue: mechanisms of action and implications. J. Nutr. 139, 1-4.
37. Kleinridders A., Schenten D., Könner A. C., Belgardt B. F., Mauer J., Okamura T., Wunderlich F. T., Medzhitov R. and Brüning J. C. (2009) MyD88 signaling in the CNS is required for development of fatty acid-induced leptin resistance and diet-induced obesity. Cell Metab. 10, 249-259.
38. Laine P. S., Schwartz E. A., Wang Y., Zhang W. Y., Karnik S. K., Musi N. and Reaven P. D. (2007) Palmitic acid induces IP-10 expression in human macrophages via NF-kappaB activation. Biochem. Biophys. Res. Commun. 358, 150-155. (Pubitemid 46719095)
39. Lee J. Y., Sohn K. H., Rhee S. H. and Hwang D. (2001) Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J. Biol. Chem. 276, 16683-16689.
40. Lee J. Y., Plakidas A., Lee W. H., Heikkinen A., Chanmugam P., Bray G. and Hwang D. H. (2003) Differential modulation of Toll-like receptors by fatty acids: preferential inhibition by n-3 polyunsaturated fatty acids. J. Lipid Res. 44, 479-486. (Pubitemid 37279695)
41. Martins de Lima-Salgado T., Coccuzzo Sampaio S., Cury-Boaventura M. F. and Curi R. (2011) Modulatory effect of fatty acids on fungicidal activity, respiratory burst and TNF-α and IL-6 production in J774 murine macrophages. Br. J. Nutr. 105, 1173-1179.
42. Mattson M. P., Duan W. and Guo Z. (2003) Meal size and frequency affect neuronal plasticity and vulnerability to disease: cellular and molecular mechanisms. J. Neurochem. 84, 417-431. (Pubitemid 36182240)
43. McNamara R. K. (2010) DHA deficiency and prefrontal cortex neuropathology in recurrent affective disorders. J. Nutr. 140, 864-868.
44. Middleton L. E. and Yaffe K. (2009) Promising strategies for the prevention of dementia. Arch. Neurol. 66, 1210-1215.
45. Miller J. C., Gnaedinger J. M. and Rapoport S. I. (1987) Utilization of plasma fatty acid in rat brain: distribution of [14C]palmitate between oxidative and synthetic pathways. J. Neurochem. 49, 1507-1514. (Pubitemid 17161373)
46. Molteni R., Barnard R., Ying Z., Roberts C. and Gómez-Pinilla F. (2002) A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience 112, 803-814. (Pubitemid 34667045)
47. Monje M. L., Toda H. and Palmer T. D. (2003) Inflammatory blockade restores adult hippocampal neurogenesis. Science 302, 1760-1765. (Pubitemid 37505739)
48. Morand O., Baumann N. and Bourre J. M. (1979) In vivo incorporation of exogenous [1-14C]stearic acid into neurons and astrocytes. Neurosci. Lett. 13, 177-181. (Pubitemid 9232275)
49. Nordvik I., Myhr K. M., Nyland H. and Bjerve K. S. (2000) Effect of dietary advice and n-3 supplementation in newly diagnosed MS patients. Acta Neurol. Scand. 102, 143-149. (Pubitemid 30645133)
50. Opie L. H. and Walfish P. G. (1963) Plasma free fatty acid concentrations in obesity. N. Engl. J. Med. 268, 757-760.
51. Palacios-Pelaez R., Lukiw W. J. and Bazan N. G. (2010) Omega-3 essential fatty acids modulate initiation and progression of neurodegenerative disease. Mol. Neurobiol. 41, 367-374.
52. Pannacciulli N., Del Parigi A., Chen K., Le D. S., Reiman E. M. and Tataranni P. A. (2006) Brain abnormalities in human obesity: a voxel-based morphometric study. Neuroimage 31, 1419-1425. (Pubitemid 43949229)
53. Parnet P., Kelley K. W., Bluthé R. M. and Dantzer R. (2002) Expression and regulation of interleukin-1 receptors in the brain. Role in cytokines-induced sickness behavior. J. Neuroimmunol. 125, 5-14. (Pubitemid 34327448)
54. Patil S. and Chan C. (2005) Palmitic and stearic fatty acids induce Alzheimer-like hyperphosphorylation of tau in primary rat cortical neurons. Neurosci. Lett. 384, 288-293. (Pubitemid 40836016)
55. Patil S., Sheng L., Masserang A. and Chan C. (2006) Palmitic acidtreated astrocytes induce BACE1 upregulation and accumulation of C-terminal fragment of APP in primary cortical neurons. Neurosci. Lett. 406, 55-59. (Pubitemid 44278378)
56. Perry G., Nunomura A. and Raina A. K. et al. (2003) A metabolic basis for Alzheimer disease. Neurochem. Res. 28, 1549-1552. (Pubitemid 37193537)
57. Pistell P. J., Morrison C. D., Gupta S., Knight A. G., Keller J. N., Ingram D. K. and Bruce-Keller A. J. (2010) Cognitive impairment following high fat diet consumption is associated with brain inflammation. J. Neuroimmunol. 219, 25-32.
58. Poggi M., Bastelica D. and Gual P. et al. (2007) C3H/HeJ mice carrying a toll-like receptor 4 mutation are protected against the development of insulin resistance in white adipose tissue in response to a high-fat diet. Diabetologia 50, 1267-1276. (Pubitemid 46701560)
59. Qi K., Hall M. and Deckelbaum R. J. (2002) Long-chain polyunsaturated fatty acid accretion in brain. Curr. Opin. Clin. Nutr. Metab. Care 5, 133-138.
60. Rapoport S. I. (1996) In vivo labeling of brain phospholipids by longchain fatty acids: relation to turnover and function. Lipids 31(Suppl.), S97-S101.
61. Rapoport S. I. (2001) In vivo fatty acid incorporation into brain phosholipids in relation to plasma availability, signal transduction and membrane remodeling. J. Mol. Neurosci. 16, 243-261.
62. Reaven G. M., Hollenbeck C., Jeng C. Y., Wu M. S. and Chen Y. D. (1988) Measurement of plasma glucose, free fatty acid, lactate, and insulin for 24 h in patients with NIDDM. Diabetes 37, 1020-1024. (Pubitemid 19033579)
63. Rossmeisl M., Jelenik T. and Jilkova Z. et al. (2009) Prevention and reversal of obesity and glucose intolerance in mice by DHA derivatives. Obesity (Silver Spring) 17, 1023-1031.
64. Rothwell N. J. (1999) Annual review prize lecture cytokines - killers in the brain? J. Physiol. Pharmacol. (London) 514, 3-17.
65. Rothwell N. J. and Hopkins S. J. (1995) Cytokines and the nervous system II: actions and mechanisms of action. Trends Neurosci., 18, 130-136.
66. Rustan A. C., Christiansen E. N. and Drevon C. A. (1992) Serum lipids, hepatic glycerolipid metabolism and peroxisomal fatty acid oxidation in rats fed omega-3 and omega-6 fatty acids. Biochem. J. 283, 333-339.
67. Scarmeas N., Stern Y., Tang M.-X., Mayeux R. and Luchsinger J. A. (2006) Mediterranean diet and risk for Alzheimer's disease. Ann. Neurol. 59, 912-921. (Pubitemid 43830923)
68. von Schlieffen E., Oskolkova O. V. and Schabbauer G. et al. (2009) Multi-hit inhibition of circulating and cell-associated components of the toll-like receptor 4 pathway by oxidized phospholipids. Arterioscler. Thromb. Vasc. Biol. 29, 356-362.
69. Shi H., Kokoeva M. V., Inouye K., Tzameli I., Yin H. and Flier J. S. (2006) TLR4 links innate immunity and fatty acid-induced insulin resistance. J. Clin. Invest. 116, 3015-3025. (Pubitemid 44684486)
70. Smith Q. R. and Nagura H. (2001) Fatty acid uptake and incorporation in brain: studies with the perfusion model. J. Mol. Neurosci. 16, 167-172. (Pubitemid 32664776)
71. Sofroniew M. V. and Vinters H. V. (2010) Astrocytes: biology and pathology. Acta Neuropathol. 119, 7-35.
72. Solfrizzi V., D'Introno A., Colacicco A. M., Capurso C., Parigi A. D., Capurso S., Gadaleta A., Capurso A. and Panza F. (2005) Dietary fatty acids intake: possible role in cognitive decline and dementia. Exp. Gerontol. 40, 257-270. (Pubitemid 40488193)
73. Souza C. G., Moreira J. D., Siqueira I. R., Pereira A. G., Rieger D. K., Souza D. O., Souza T. M., Portela L. V. and Perry M. L. (2007) Highly palatable diet consumption increases protein oxidation in rat frontal cortex and anxiety-like behavior. Life Sci. 81, 198-203. (Pubitemid 46976978)
74. Stentz F. B. and Kitabchi A. E. (2006) Palmitic acid-induced activation of human T-lymphocytes and aortic endothelial cells with production of insulin receptors, reactive oxygen species, cytokines, and lipid peroxidation. Biochem. Biophys. Res. Commun. 346, 721-726.
75. Stranahan A. M., Norman E. D., Lee K., Cutler R. G., Telljohann R. S., Egan J. M. and Mattson M. P. (2008) Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus 18, 1085-1088.
76. Studzinski C. M., Li F., Bruce-Keller A. J., Fernandez-Kim S. O., Zhang L., Weidner A. M., Markesbery W. R., Murphy M. P. and Keller J. N. (2009) Effects of short-term western diet on cerebral oxidative stress and diabetes related factors in APP x PS1 knock-in mice. J. Neurochem. 108, 860-866.
77. Tappia P. S., Man W. J. and Grimble R. F. (1995) Influence of unsaturated fatty acids on the production of tumour necrosis factor and interleukin-6 by rat peritoneal macrophages. Mol. Cell. Biochem. 14, 89-98.
78. Tsukumo D. M., Carvalho-Filho M. A. and Carvalheira J. B. et al. (2007) Loss-of-function mutation in Toll-like receptor 4 prevents diet-induced obesity and insulin resistance. Diabetes 56, 1986-1998. (Pubitemid 47195825)
79. Turchan-Cholewo J., Dimayuga F. O., Ding Q., Keller J. N., Hauser K. F., Knapp P. E. and Bruce-Keller A. J. (2008) Cell-specific actions of HIV-Tat and morphine on opioid receptor expression in glia. J. Neurosci. Res. 86, 2100-2110.
80. Waldstein S. R. and Katzel L. I. (2006) Interactive relations of central versus total obesity and blood pressure to cognitive function. Int. J. Obes. (Lond.), 30, 201-207. (Pubitemid 41790798)
81. Wang S. W., Wang M., Grossman B. M. and Martin R. J. (1994) Effects of dietary fat on food intake and brain uptake and oxidation of fatty acids. Physiol. Behav. 56, 517-522. (Pubitemid 24269574)
82. Ward M. A., Carlsson C. M., Trivedi M. A., Sager M. A. and Johnson S. C. (2005) The effect of body mass index on global brain volume in middle-aged adults: a cross sectional study. BMC Neurol. 5, 23.
83. Weinstock-Guttman B., Baier M. and Park Y. et al. (2005) Low fat dietary intervention with omega-3 fatty acid supplementation in multiple sclerosis patients. Prostaglandins Leukot. Essent. Fat. Acids 73, 397-404. (Pubitemid 41375637)
84. White C. L., Pistell P. J. and Purpera M. N. et al. (2009) Effects of high fat diet on Morris maze performance, oxidative stress, and inflammation in rats: contributions of maternal diet. Neurobiol. Dis. 35, 3-13.
85. Wilson C. J., Finch C. E. and Cohen H. J. (2002) Cytokines and cognition- the case for a head-to-toe inflammatory paradigm. J. Am. Geriatr. Soc. 50, 2041-2056. (Pubitemid 35462453)
86. Winocur G. and Greenwood C. E. (2005) Studies of the effects of high fat diets on cognitive function in a rat model. Neurobiol. Aging 26, 46-49.
87. Wong S. W., Kwon M. J., Choi A. M., Kim H. P., Nakahira K. and Hwang D. H. (2009) 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. 284, 27384-27392.
88. Xu Z. J., Fan J. G., Ding X. D., Qiao L. and Wang G. L. (2010) Characterization of high-fat, diet-induced, non-alcoholic steatohepatitis with fibrosis in rats. Dig. Dis. Sci. 55, 931-940.
89. Zhang X., Dong F., Ren J., Driscoll M. J. and Culver B. (2005) High dietary fat induces NADPH oxidase-associated oxidative stress and inflammation in rat cerebral cortex. Exp. Neurol. 191, 318-325. (Pubitemid 40092875)
90. Zhang L., Bruce-Keller A. J., Dasuri K., Nguyen A., Liu Y. and Keller J. N. (2009) Diet-induced metabolic disturbances as modulators of brain homeostasis. Biochim. Biophys. Acta 1792, 417-422.