Potential role of omega-3-derived resolution mediators in metabolic inflammation

Immunology and Cell Biology

Volumn 92, Issue 4, 2014, Pages 324-330

  White, Phillip J ^a,b   Marette, André ^a  

^a LAVAL UNIVERSITY   (Canada)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adipose tissue; inflammation; insulin resistance; microbiota; obesity; omega 3 fatty acids

Indexed keywords

OMEGA 3 FATTY ACID; PATTERN RECOGNITION RECEPTOR;

ADAPTIVE IMMUNITY; HUMAN; HYPOTHALAMUS; INFLAMMATION; INNATE IMMUNITY; LIPID ANALYSIS; MEDIATOR; METABOLIC DISORDER; NONHUMAN; NUTRIENT; REVIEW; SKELETAL MUSCLE; ANIMAL; ANTIBODY SPECIFICITY; BIOLOGICAL MODEL; METABOLISM;

ANIMALS; FATTY ACIDS, OMEGA-3; HUMANS; INFLAMMATION; MODELS, BIOLOGICAL; ORGAN SPECIFICITY; RECEPTORS, PATTERN RECOGNITION;

EID: 84899434055     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2013.112     Document Type: Review

References (99)

1. Ginter E, Simko V. Type 2 diabetes mellitus, pandemic in 21st century. Adv Exp Med Biol 2012; 771: 42-50.
2. Wang YC, McPherson K, Marsh T, Gortmaker SL, Brown M. Health and economic burden of the projected obesity trends in the USA and the UK. Lancet 2011; 378: 815-825.
3. Holland WL, Miller RA, Wang ZV, Sun K, Barth BM, Bui HH et al. Rece ptor-mediated activation of ceramidase activity initiates the pleiotropic actions of adiponectin. Nat Med 2011; 17: 55-63.
4. Tchernof A, Despres JP. Pathophysiology of human visceral obesity: an update. Physiol Rev 2013; 93: 359-404.
5. Hotamisligil GS Shargill NS Spiegelman BM Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance Science 1993 259 87-91.
6. Legein B, Temmerman L, Biessen EA, Lutgens E. Inflammation and immune system interactions in atherosclerosis. Cell Mol Life Sci 2013; 70: 3847-3869.
7. Tilg H, Moschen AR. Evolution of inflammation in nonalcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology 2010; 52: 1836-1846.
8. Karelis AD, Faraj M, Ba stard JP, St-Pierre DH, Brochu M, Prud'homme D et al. The metabolically healthy but obese individual presents a favorable inflammation profile. J Clin Endocrinol Metab 2005; 90: 4145-4150.
9. Koster A, Stenholm S, Alley DE, Kim LJ, Simonsick EM, Kanaya AM et al. Body fat distribution and inflammation among obese older adults with and without metabolic syndrome. Obesity (Silver Spring) 2010; 18: 2354-2361.
10. Barbarroja N, Lopez-Pedrera R, Mayas MD, Garcia-Fuentes E, Garrido-Sanchez L, Macias-Gonzalez M et al. The obese healthy paradox: is inflammation the answer Biochem J 2010; 430: 141-149.
11. Wildman RP. Healthy obesity. Curr Opin Clin Nutr Metab Care 2009; 12: 438-443.
12. Aguirre V, Uchida T, Yenush L, Davis R, White MF. The c-Jun NH(2)-terminal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser(307). J Bio l Chem 2000; 275: 9047-9054.
13. Hirosumi J, Tuncman G, Chang L, Gorgun CZ, Uysal KT, Maeda K et al. A central role for JNK in obesity and insulin resistance. Nature 2002; 420: 333-336.
14. Charbonneau A, Marette A. Inducible nitric oxide synthase induction underlies lipidinduced hepatic insulin resistance in mice: potential role of tyrosine nitration of insulin signaling proteins. Diabetes 2010; 59: 861-871.
15. Pilon G, Charbonneau A, White PJ, Dallaire P, Perreault M, Kapur S et al. Endotoxin mediated-iNOS induction causes insulin resistance via ONOO(-) induced tyrosine n itration of IRS-1 in skeletal muscle. PLoS One 2010; 5: e15912.
16. Carvalho-Filho MA, Ueno M, Hirabara SM, Seabra AB, Carvalheira JB, de Oliveira MG et al. S-nitrosation of the insul in receptor, insulin receptor substrate 1, and protein kinase B/Akt: a novel mechanism of insulin resistance. Diabetes 2005; 54: 959-967.
17. Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 2003; 112: 1821-1830.
18. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 2003; 112: 1796-1808.
19. Cinti S, Mitchell G, Barbatelli G, Murano I, Ceresi E, Faloia E et al. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res 2005; 46: 2347-2355.
20. Strissel KJ, Stancheva Z, Miyoshi H, Perfield JW 2nd, DeFuria J, Jick Z et al. Adipocyte death, adipose tissue remodeling, and obesity complications. Diabetes 2007; 56: 2910-2918.
21. Nishimura S, Manabe I, Nagasaki M, Eto K, Yamashita H, Ohsugi M et al. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med 2009; 15: 914-920.
22. Winer S, Chan Y, Paltser G, Truong D, Tsui H, Bahrami J et al. Normalization of obesityassociated insulin resistance through immunotherapy. Nat Med 2009; 15: 921-929.
23. Feuerer M, Herrero L, Cipolletta D, Naaz A, Wong J, Nayer A et al. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat Med 2009; 15: 930-939.
24. Ohmura K, Ishimori N, Ohmura Y, Tokuhara S, Nozawa A, Horii S et al. Natural killer T cells are involved in adipose tissues inflammation and glucose intolerance in diet-induced obese mice. Arterioscler Thromb Vas c Biol 2010; 30: 193-199.
25. Winer DA, Winer S, Shen L, Wadia PP, Yantha J, Paltser G et al. B cells promote insulin resistance through modulation of T cells and production of pathogenic I gG antibodies. Nat Med 2011; 17: 610-617.
26. Pickup JC, Mattock MB, Chusney GD, Burt D. NIDDM as a disease of the innate immune system: association of acute-phase reactants and interleukin-6 with metabolic syndrome X. Diabetologia 1997; 40: 128 6-1292.
27. Visser M Bouter LM McQuillan GM Wener MH Harris TB Elevated C-reactive protein levels in overweight and obese adults JAMA 1999 282 2131-2135.
28. Yudk in JS, Stehouwer CD, Emeis JJ, Coppack SW. C-reactive protein in healthy subjects: associations with obesity, insulin resistance, and endothelial dysfunction: a potential role for cytokines originating from adipose tissue Arterioscl er Thromb Vasc Biol 1999; 19: 972-978.
29. Cook DG, Mendall MA, Whincup PH, Carey IM, Ballam L, Morris JE et al. C-reactive protein concentration in children: relationship to adiposity and o ther cardiovascular risk factors. Atherosclerosis 2000; 149: 139-150.
30. Elgazar-Carmon V, Rudich A, Hadad N, Levy R. Neutrophils transiently infiltrate intra-abdominal fat early in the course of high-fat feeding. J Lipid Res 2008; 49: 1894-1903.
31. Talukdar S, Oh da Y, Bandyopadhyay G, Li D, Xu J, McNelis J et al. Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase. Nat Med 2012; 18: 1407-1412.
32. Wu D, Molofsky AB, Liang HE, Ricardo-Gonzalez RR, Jouihan HA, Bando JK et al. Eosinophils sustain adipose alternative ly activated macrophages associated with glucose homeostasis. Science 2011; 332: 243-247.
33. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 2007; 117: 175-184.
34. Nijhuis J, Rensen SS, Slaats Y, van Dielen FM, Buurman WA, Greve JW. Neutrophil activation in morbid obesity, chronic activation of acute infl ammation. Obesity (Silver Spring) 2009; 17: 2014-2018.
35. Magne J, Mariotti F, Fischer R, Mathe V, Tome D, Huneau JF. Early postprandial lowgrade inflammation after high-fat meal in healthy rats: po ssible involvement of visceral adipose tissue. J Nutr Biochem 2010; 21: 550-555.
36. Soehnlein O, Lindbom L, Weber C. Mechanisms underlying neutrophil-mediated monocyte recruitment. Blood 2009; 114: 4613-4623.
37. Miller R, Wen X, Dunford B, Wang X, Suzuki Y. Cytokine production of CD8+ immune T cells but not of CD4+ T cells from Toxoplasma gondii-infected mice is polarized to a type 1 re sponse following stimulation with tachyzoite-infected macrophages. J Interferon Cytokine Res 2006; 26: 787-792.
38. Defuria J, Belkina AC, Jagannathan-Bogdan M, Snyder-Cappione J, Carr JD, Ners esova YR et al. B cells promote inflammation in obesity and type 2 diabetes through regulation of T-cell function and an inflammatory cytokine profile. Proc Natl Acad Sci USA 2013; 110: 5133-5138.
39. We isberg SP, Hunter D, Huber R, Lemieux J, Slaymaker S, Vaddi K et al. CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J Clin Invest 2006; 116: 115-124.
40. Creely SJ, McTernan PG, Kusminski CM, Fisher M, Da Silva NF, Khanolkar M et al. Lipopolysaccharide activates an innate immune system response in human adipose tissue in obesity and type 2 diabetes. Am J Physiol Endocrinol Metab 2007; 292: E740-E747.
41. Reyna SM, Ghosh S, Tantiwong P, Meka CS, Eagan P, Jenkinson CP et al. Elevated toll-like receptor expression and signaling in muscle from insulin-resistant subjects. Diabetes 2008; 57: 2595-2602.
42. Caricilli AM, Nascimento PH, Pauli JR, Tsukumo DM, Velloso LA, Carvalheira JB et al. Inhibition of toll-like receptor 2 expression improves insulin sensitivity and signaling in muscle and white adipose tissue of mice fed a high-fat diet. J Endocrinol 2008; 199: 399-406.
43. Himes RW, Smith CW. Tlr2 is critical for diet-induced metabolic syndrome in a murine model. FASEB J 2010; 24: 731-739.
44. Shi H, Kokoeva MV, Inouye K, Tzameli I, Y in H, Flier JS. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest 2006; 116: 3015-3025.
45. Tsukumo DM, Carvalho-Filho MA, Carvalheira JB, Prada PO, Hirab ara SM, Schenka AA et al. Loss-of-function mutation in Toll-like receptor 4 prevents diet-induced obesity and insulin resistance. Diabetes 2007; 56: 1986-1998.
46. Schertzer JD Tamrakar AK Magalhaes JG Pereira S Bilan PJ Fullerton MD et al. NOD1 activators link innate immunity to insulin resistance Diabetes 2011 60 2206-2215.
47. Vandanmagsar B, Youm YH, Ravussin A, Galgani JE, Stadler K, Mynatt RL et al. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat Med 2011; 17: 179-188.
48. Takeuchi O, Akira S. T oll-like receptors; their physiological role and signal transduction system. Int Immunopharmacol 2001; 1: 625-635.
49. Drexler SK, Foxwell BM. The role of toll-like receptors in chronic inflammation. Int J Biochem Cell Biol 2010; 42: 506-518.
50. Opitz B, Eitel J, Meixenberger K, Suttorp N. Role of Toll-like receptors, NOD-like receptors and RIG-I-like receptors in endothelial cells and syst emic infections. Thromb Haemost 2009; 102: 1103-1109.
51. Lin Y, Lee H, Berg AH, Lisanti MP, Shapiro L, Scherer PE. The lipopolysaccharideactivated toll-like receptor (TLR)-4 induces synthesis of the closely related receptor TLR-2 in adipocytes. J Biol Chem 2000; 275: 24255-24263.
52. Zhou YJ, Zhou H, Li Y, Song YL. NOD1 activation induces innate immune responses and insulin resistance in human adipocytes. Diabetes Metab 2012; 38: 538-543.
53. Stienstra R, Joosten LA, Koenen T, van Tits B, van Diepen JA, van den Berg SA et al. The inflammasome-mediated caspase-1 activation controls adipocyte differentiation and insulin sensitivity. Cell Metab 2010; 12: 593-605.
54. Senn JJ. Toll-like receptor-2 is essential for the development of palmitate-induced insulin resistance in myotubes. J Biol Chem 2006; 281: 26865-26875.
55. Tamrakar AK, Schertzer JD, Chiu TT, Foley KP, Bilan PJ, Philpott DJ et al. NOD2 activation induces muscle cell-autonomous innate immune responses and insulin resistance. Endocrinology 2010; 151: 5624-5637.
56. Matsumura T, Ito A, Takii T, Hayashi H, Onozaki K. Endotoxin and cytokine regulation of toll-like receptor (TLR) 2 and TLR4 gene expression in murine liver and hepatocytes. J Interferon Cytokine Res 2000; 20: 915-921.
57. Ehses JA, Meier DT, Wueest S, Rytka J, Boller S, Wielinga PY et al. Toll-like receptor 2-deficient mice are protected from insulin resistance and beta cell dysfunction induced by a high-fat diet. Diabetologia 2010; 53: 1795-1806.
58. Saberi M, Woods NB, de Luca C, Schenk S, Lu JC, Bandyopadhyay G et al. Hematopoietic cell-specific deletion of toll-like receptor 4 ameliorates h epatic and adipose tissue insulin resistance in high-fat-fed mice. Cell Metab 2009; 10: 419-429.
59. Zhao L, Kwon MJ, Huang S, Lee JY, Fukase K, Inohara N et al. Differential modulatio n of Nods signaling pathways by fatty acids in human colonic epithelial HCT116 cells. J Biol Chem 2007; 282: 11618-11628.
60. Wen H, Gris D, Lei Y, Jha S, Zhang L, Huang MT et al. Fatt y acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol 2011; 12: 408-415.
61. Schwartz EA, Zhang WY, Karnik SK, Borwege S, Anand VR, Laine PS et al. . Nutrient modification of the innate immune response: a novel mechanism by which saturated fatty acids greatly amplify monocyte inflammation. Arterioscler Thromb Vasc Biol 2010; 30: 802-808.
62. Fischer H, Ellstrom P, Ekstrom K, Gustafsson L, Gustafsson M, Svanborg C. Ceramide as a TLR4 agonist; a putative signalling intermediate between sphingolipid receptors for microbial ligands and TLR4. Cell Microbiol 2007; 9: 1239-1251.
63. Kosteli A, Sugaru E, Haemmerle G, Martin JF, Lei J, Zechner R et al. Weight loss and lipolysis promote a dynamic immune response in murine adipose tissue. J Clin Invest 2010; 120: 3466-3479.
64. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesityassociated gut microbiome with increased capacity for energy harvest. Nature 2006; 444 1027-1031.
65. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007; 56: 1761-1772.
66. Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat dietinduced obesity and diabetes in mice. D iabetes 2008; 57: 1470-1481.
67. Cani PD Neyrinck AM Fava F Knauf C Burcelin RG Tuohy KM et al. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced di abetes in mice through a mechanism associated with endotoxaemia Diabetologia 2007 50 2374-2383.
68. Piccinini AM, Midwood KS. DAMPening inflammation by modulating TLR signalling. Mediators Inflamm 2010; 2010: 672395.
69. Varma V, Yao-Borengasser A, Rasouli N, Nolen GT, Phanavanh B, Starks T et al. Muscle inflammatory response and insulin resistance: synergistic interaction between macrophages and fatty acids leads to impaired insulin action. Am J Physiol Endocrinol Metab 2009; 296: E1300-E1310.
70. Bigorgne AE, Bouchet-Delbos L, Naveau S, Dagher I, Prevot S, Durand-Gasse lin I et al. Obesity-induced lymphocyte hyperresponsiveness to chemokines: a new mechanism of fatty liver inflammation in obese mice. Gastroenterology 2008; 134: 1459-1469.
71. Deng ZB, Liu Y, Liu C, Xiang X, Wang J, Cheng Z et al. Immature myeloid cells induced by a high-fat diet contribute to liver inflammation. Hepatology 2009; 50: 1412-1420.
72. Rensen SS, Slaats Y, Nijhuis J, Jans A, Bieghs V, Driessen A et al. Increased hepatic myeloperoxidase activity in obese subjects with nonalcoholic steatohepatitis. Am J Pathol 2009; 175: 1473-1482.
73. Stanton MC, Ch en SC, Jackson JV, Rojas-Triana A, Kinsley D, Cui L et al. Inflammatory signals shift from adipose to liver during high fat feeding and influence the development of steatohepatitis in mice. J Inflamm (Lond) 2011; 8 8.
74. Thaler JP, Yi CX, Schur EA, Guyenet SJ, Hwang BH, Dietrich MO et al. Obesity is associated with hypothalamic injury in rodents and humans. J Clin Invest 2012; 122: 153-1 62.
75. De Souza CT, Araujo EP, Bordin S, Ashimine R, Zollner RL, Boschero AC et al. Consumption of a fat-rich diet activates a proinflammatory response and induces insulin resistance in the hypothalamus. Endocrinology 2005; 146: 4192-4199.
76. Milanski M, Arruda AP, Coope A, Ignacio-Souza LM, Nunez CE, Roman EA et al. Inhibition of hypothalamic inflammation reverses diet-induced insuli n resistance in the liver. Diabetes 2012; 61: 1455-1462.
77. Zhang X, Zhang G, Zhang H, Karin M, Bai H, Cai D. Hypothalamic IKKbeta/NF-kappaB and ER stress link overnutrition to energy im balance and obesity. Cell 2008; 135: 61-73.
78. Yi CX, Tschop MH, Woods SC, Hofmann SM. High-fat-diet exposure induces IgG accumulation in hypothalamic microglia. Dis Model Mech 2012; 5: 686-690.
79. Kleinridders A, Schenten D, Konner AC, Belgardt BF, Mauer J, Okamura T et al. MyD88 signaling in the CNS is required for development of fatty acid-induced leptin resistance and di et-induced obesity. Cell Metab 2009; 10: 249-259.
80. Goldfine AB, Fonseca V, Shoelson SE. Therapeutic approaches to target inflammation in type 2 diabetes. Clin Chem 2011; 57: 162-167.
81. Buckley CD, Gilroy DW, Serhan CN, Stockinger B, Tak PP. The resolution of inflammation. Nat Rev Immunol 2013; 13: 59-66.
82. Levy BD, Clish CB, Schmidt B, Gronert K, Serhan CN. Lipid mediator class switching during acute inflammation: signals in resolution. Nat Immunol 2001; 2: 612-619.
83. Serhan CN, Petasis NA. Resolvins and protectins in inflammation resolution. Chem Rev 2011; 111: 5922-5943.
84. Serhan CN, Hong S, Gronert K, Colgan SP, Devchand PR, Mirick G et al. Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that coun ter proinflammation signals. J Exp Med 2002; 196: 1025-1037.
85. 5 Ariel A, Fredman G, Sun YP, Kantarci A, Van Dyke TE, Luster AD et al. Apoptotic neutrophils and T cells sequester chemokines during immune response resolution through modulation of CCR5 expression. Nat Immunol 2006; 7: 1209-1216.
86. Dalli J, Serhan CN. Specific lipid mediator signatures of human phagocytes: microparticles stimulate macrophage efferocytosis and pro-resolving mediators. Blood 2012; 120: e60-e72.
87. Oh DY, Talukdar S, Bae EJ, Imamura T, Morinaga H, Fan W et al. GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell 20 10; 142: 687-698.
88. White PJ, Arita M, Taguchi R, Kang JX, Marette A. Transgenic restoration of long-chain n-3 fatty acids in insulin target tissues improves resolution capacity and alleviates obesit y-linked inflammation and insulin resistance in high-fat-fed mice. Diabetes 2010; 59: 3066-3073.
89. Gonzalez-Periz A Horrillo R Ferre N Gronert K Dong B Moran-Salvador E et al. Obesity-induced insulin resistance and hepatic steatosis are alleviated by omega-3 fatty acids: a role for resolvins and protectins FASEB J 2009 23: 1946-1957.
90. Hudert CA, Weylandt KH, Lu Y, Wang J, Hong S, Dignass A et al. Transgenic mice rich in endogenous omega-3 fatty acids are protected from colitis. Proc Natl Acad Sci USA 2006; 103: 11276-11281.
91. Lukiw WJ, Cui JG, Marches elli VL, Bodker M, Botkjaer A, Gotlinger K et al. A role for docosahexaenoic acid-derived neuroprotectin D1 in neural cell survival and Alzheimer disease. J Clin Invest 2005; 115: 2774-2783.
92. Claria J, Dalli J, Yacoubian S, Gao F, Serhan CN. Resolvin D1 and resolvin D2 govern local inflammatory tone in obese fat. J Immunol 2012; 189: 2597-2605.
93. Tang Y, Zhang MJ, Hellmann J, Kosuri M, Bhatnagar A, Spite M. Proresolution therapy for the treatment of delayed healing of diabetic wounds. Diabetes 2013; 62: 618-627.
94. Neuhofer A, Zeyda M, Mascher D, Itariu BK, Murano I, Leitner L et al. Impaired local production of proresolving lipid mediators in obesity and 17-HDHA as a potential treatment for obesity-associated inflammat ion. Diabetes 2013; 62: 1945-1956.
95. Claria J, Nguyen BT, Madenci AL, Ozaki CK, Serhan CN. Diversity of lipid mediators in human adipose tissue depots. Am J Physiol Cell Physiol 2013; 304: C1141-C1149.
96. Li S, Sun Y, Liang CP, Thorp EB, Han S, Jehle AW et al. Defective phagocytosis of apoptotic cells by macrophages in atherosclerotic lesions of ob/ob mice and reve rsal by a fish oil diet. Circ Res 2009; 105: 1072-1082.
97. Hellmann J, Tang Y, Kosuri M, Bhatnagar A, Spite M. Resolvin D1 decreases adipose tissue macrophage accumulation and improves insuli n sensitivity in obese-diabetic mice. FASEB J 2011; 25: 2399-2407.
98. Titos E, Rius B, Gonzalez-Periz A, Lopez-Vicario C, Moran-Salvador E, Martinez-Clemente M et al. Resolvin D1 and its precursor docosahexaenoic acid promote resolution of adipose tissue inflammation by eliciting macrophage polarization toward an M2-like phenotype. J Immunol 2011; 187: 5408-5418.
99. Birnbaum Y, Ye Y, Lin Y, Freeberg SY, Nishi SP, Martinez JD et al. Augmentation of myocardial production of 15-epi-lipoxin-a4 by pioglitazone and atorvastatin in the rat. Circulation 2006; 114: 929-935.