Crosstalk between intestinal microbiota, adipose tissue and skeletal muscle as an early event in systemic low-grade inflammation and the development of obesity and diabetes

Diabetes/Metabolism Research and Reviews

Volumn 31, Issue 6, 2015, Pages 545-561

  Bleau, Christian ^a   Karelis, Antony D ^a   St Pierre, David H ^a   Lamontagne, Lucie ^a  

^a UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

Author keywords

Adipose cells; Cytokines; Gut peptides; High fat diet; Inflammation; Intestinal epithelial cells; Microbiota; Muscular cells; Obesity; TLR; Type 2 diabetes

Indexed keywords

ANTIINFLAMMATORY GUT PEPTIDE; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG; GASTROINTESTINAL HORMONE;

ADIPOSE TISSUE; ADIPOSE TISSUE CELL; ARTICLE; DIABETES MELLITUS; DISEASE ASSOCIATION; HOMEOSTASIS; HUMAN; IMMUNE SYSTEM; INFLAMMATION; INTESTINE EPITHELIUM; INTESTINE FLORA; LIPID DIET; METABOLIC DISORDER; MUSCLE CELL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PRIORITY JOURNAL; SKELETAL MUSCLE; ADVERSE EFFECTS; ANIMAL; BIOLOGICAL MODEL; DIABETES MELLITUS, TYPE 2; ENTERITIS; IMMUNOLOGY; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; MUCOSAL IMMUNITY; MYOSITIS; PANNICULITIS; PATHOPHYSIOLOGY; SECRETION (PROCESS); SYSTEMIC VASCULITIS; WHITE ADIPOSE TISSUE;

ADIPOSE TISSUE, WHITE; ANIMALS; DIABETES MELLITUS, TYPE 2; DIET, HIGH-FAT; ENTERITIS; GASTROINTESTINAL HORMONES; GASTROINTESTINAL MICROBIOME; HUMANS; IMMUNITY, MUCOSAL; INTESTINAL MUCOSA; MODELS, BIOLOGICAL; MUSCLE, SKELETAL; MYOSITIS; OBESITY; PANNICULITIS; SYSTEMIC VASCULITIS;

EID: 84941259141     PISSN: 15207552     EISSN: 15207560     Source Type: Journal    
DOI: 10.1002/dmrr.2617     Document Type: Article

References (154)

1. Kahn SE, Hull RL, Utzschneider KM. Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 2006; 444(7121): 840-846.
2. Greenberg AS, Obin MS. Obesity and the role of adipose tissue in inflammation and metabolism. Am J Clin Nutr 2006; 83(2): 461S-465S.
3. Hotamisligil GS. Inflammation and metabolic disorders. Nature 2006; 444(7121): 860-867.
4. Maury E, Brichard SM. Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome. Mol Cell Endocrinol 2010; 314(1): 1-16.
5. Sell H, Eckel J. Adipose tissue inflammation: novel insight into the role of macrophages and lymphocytes. Curr Opin Clin Nutr Metab Care 2010; 13(4): 366-370.
6. Ding S, Chi MM, Scull BP, et al. High-fat diet: bacteria interactions promote intestinal inflammation which precedes and correlates with obesity and insulin resistance in mouse. PLoS One 2010; 5(8): e12191.
7. Cani PD, Bibiloni R, Knauf C, et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 2008; 57(6): 1470-1481.
8. de La Serre CB, Ellis CL, Lee J, et al. Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. Am J Physiol Gastrointest Liver Physiol 2010; 299(2): G440-G448.
9. Mehta NN, McGillicuddy FC, Anderson PD, et al. Experimental endotoxemia induces adipose inflammation and insulin resistance in humans. Diabetes 2010; 59(1): 172-181.
10. Raybould HE. Gut microbiota, epithelial function and derangements in obesity. J Physiol 2012; 590(Pt 3): 441-446.
11. Shen J, Obin MS, Zhao L. The gut microbiota, obesity and insulin resistance. Mol Aspects Med 2013; 34(1): 39-58.
12. Alonzo VR, Guarner R. Linging the gut microbiota to human health. Br J Nutr 2013; 109: S21-S26.
13. Little TJ, Feinle-Bisset C. Effects of dietary fat on appetite and energy intake in health and obesity--oral and gastrointestinal sensory contributions. Physiol Behav 2011; 104(4): 613-620.
14. Erridge C. Endogenous ligands of TLR2 and TLR4: agonists or assistants? J Leukoc Biol 2010; 87(6): 989-999.
15. Davis JE, Gabler NK, Walker-Daniels J, Spurlock ME. Tlr-4 deficiency selectively protects against obesity induced by diets high in saturated fat. Obesity (Silver Spring) 2008; 16(6): 1248-1255.
16. Ahmad R, Al-Mass A, Atizado V, et al. Elevated expression of the toll like receptors 2 and 4 in obese individuals: its significance for obesity-induced inflammation. J Inflamm (Lond) 2012; 9(1): 48.
17. Pillon NJ, Bilan PJ, Fink LN, Klip A. Cross-talk between skeletal muscle and immune cells: muscle-derived mediators and metabolic implications. Am J Physiol Endocrinol Metab 2013; 304(5): E453-E465.
18. Langlet C, Tamoutounour S, Henri S, et al. CD64 expression distinguishes monocyte-derived and conventional dendritic cells and reveals their distinct role during intramuscular immunization. J Immunol 2012; 188(4): 1751-1760.
19. Chmelar J, Chung KJ, Chavakis T. The role of innate immune cells in obese adipose tissue inflammation and development of insulin resistance. Thromb Haemost 2013; 109(3): 399-406.
20. Guillet C, Masgrau A, Walrand S, Boirie Y. Impaired protein metabolism: interlinks between obesity, insulin resistance and inflammation. Obes Rev 2012; 13(Suppl 2): 51-57.
21. Trayhurn P, Drevon CA, Eckel J. Secreted proteins from adipose tissue and skeletal muscle - adipokines, myokines and adipose/muscle cross-talk. Arch Physiol Biochem 2011; 117(2): 47-56.
22. Pedersen BK, Febbraio MA. Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol 2012; 8(8): 457-465.
23. Kinnebrew MA, Pamer EG. Innate immune signaling in defense against intestinal microbes. Immunol Rev 2012; 245(1): 113-131.
24. Wu GD, Chen J, Hoffmann C, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011; 334(6052): 105-108.
25. Macpherson AJ, Harris NL. Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 2004; 4(6): 478-485.
26. Sansonetti PJ, Di Santo JP. Debugging how bacteria manipulate the immune response. Immunity 2007; 26(2): 149-161.
27. Wells JM, Rossi O, Meijerink M, van Baarlen P. Epithelial crosstalk at the microbiota-mucosal interface. Proc Natl Acad Sci U S A 2011; 108(Suppl 1): 4607-4614.
28. Sharma R, Young C, Neu J. Molecular modulation of intestinal epithelial barrier: contribution of microbiota. J Biomed Biotechnol 2010; 2010: 305879.
29. Tanoue T, Honda K. Induction of Treg cells in the mouse colonic mucosa: a central mechanism to maintain host-microbiota homeostasis. Semin Immunol 2012; 24(1): 50-57.
30. Pastorelli L, De Salvo C, Mercado JR, Vecchi M, Pizarro TT. Central Role of the Gut Epithelial Barrier in the Pathogenesis of Chronic Intestinal Inflammation: Lessons Learned from Animal Models and Human Genetics. Front Immunol 2013; 4: 280.
31. Natividad JM, Verdu EF. Modulation of intestinal barrier by intestinal microbiota: pathological and therapeutic implications. Pharmacol Res 2013; 69(1): 42-51.
32. Howe KL, Reardon C, Wang A, Nazli A, McKay DM. Transforming growth factor-beta regulation of epithelial tight junction proteins enhances barrier function and blocks enterohemorrhagic Escherichia coli O157:H7-induced increased permeability. Am J Pathol 2005; 167(6): 1587-1597.
33. Weiner HL, da Cunha AP, Quintana F, Wu H. Oral tolerance. Immunol Rev 2011; 241(1): 241-259.
34. Tyrer P, Foxwell AR, Cripps AW, Apicella MA, Kyd JM. Microbial pattern recognition receptors mediate M-cell uptake of a gram-negative bacterium. Infect Immun 2006; 74(1): 625-631.
35. Suzuki T, Yoshida S, Hara H. Physiological concentrations of short-chain fatty acids immediately suppress colonic epithelial permeability. Br J Nutr 2008; 100(2): 297-305.
36. Madara JL, Stafford J. Interferon-gamma directly affects barrier function of cultured intestinal epithelial monolayers. J Clin Invest 1989; 83(2): 724-727.
37. Bleau C, Savard R, Lamontagne L. Murine immunomodulation of IL-10 and IL-12 induced by new isolates from avian type 2 Lactobacillus acidophilus. Can J Microbiol 2007; 53(8): 944-956.
38. Cario E. Barrier-protective function of intestinal epithelial Toll-like receptor 2. Mucosal Immunol 2008; 1(Suppl 1): S62-S66.
39. Murphy KG, Bloom SR. Gut hormones and the regulation of energy homeostasis. Nature 2006; 444(7121): 854-859.
40. Duca FA, Covasa M. Current and emerging concepts on the role of peripheral signals in the control of food intake and development of obesity. Br J Nutr 2012; 108(5): 778-793.
41. Gonzalez-Rey E, Chorny A, Delgado M. Therapeutic action of ghrelin in a mouse model of colitis. Gastroenterology 2006; 130(6): 1707-1720.
42. Abad C, Martinez C, Juarranz MG, et al. Therapeutic effects of vasoactive intestinal peptide in the trinitrobenzene sulfonic acid mice model of Crohn's disease. Gastroenterology 2003; 124(4): 961-971.
43. Chorny A, Anderson P, Gonzalez-Rey E, Delgado M. Ghrelin protects against experimental sepsis by inhibiting high-mobility group box 1 release and by killing bacteria. J Immunol 2008; 180(12): 8369-8377.
44. Wu R, Dong W, Qiang X, et al. Orexigenic hormone ghrelin ameliorates gut barrier dysfunction in sepsis in rats. Crit Care Med 2009; 37(8): 2421-2426.
45. Saia RS, Bertozi G, Mestriner FL, et al. Cardiovascular and inflammatory response to cholecystokinin during endotoxemic shock. Shock 2013; 39(1): 104-113.
46. Lubbers T, de Haan JJ, Luyer MD, et al. Cholecystokinin/Cholecystokinin-1 receptor-mediated peripheral activation of the afferent vagus by enteral nutrients attenuates inflammation in rats. Ann Surg 2010; 252(2): 376-382.
47. Chandra R, Liddle RA. Cholecystokinin. Curr Opin Endocrinol Diabetes Obes 2007; 14(1): 63-67.
48. Hornby PJ, Moore BA. The therapeutic potential of targeting the glucagon-like peptide-2 receptor in gastrointestinal disease. Expert Opin Ther Targets 2011; 15(5): 637-646.
49. Moran GW, O'Neill C, McLaughlin JT. GLP-2 enhances barrier formation and attenuates TNFalpha-induced changes in a Caco-2 cell model of the intestinal barrier. Regul Pept 2012; 178(1-3): 95-101.
50. Li WG, Gavrila D, Liu X, et al. Ghrelin inhibits proinflammatory responses and nuclear factor-kappaB activation in human endothelial cells. Circulation 2004; 109(18): 2221-2226.
51. Dixit VD, Schaffer EM, Pyle RS, et al. Ghrelin inhibits leptin- and activation-induced proinflammatory cytokine expression by human monocytes and T cells. J Clin Invest 2004; 114(1): 57-66.
52. Baatar D, Patel K, Taub DD. The effects of ghrelin on inflammation and the immune system. Mol Cell Endocrinol 2011; 340(1): 44-58.
53. Souza-Moreira L, Campos-Salinas J, Caro M, Gonzalez-Rey E. Neuropeptides as pleiotropic modulators of the immune response. Neuroendocrinology 2011; 94(2): 89-100.
54. Yusta B, Baggio LL, Estall JL, et al. GLP-1 receptor activation improves beta cell function and survival following induction of endoplasmic reticulum stress. Cell Metab 2006; 4(5): 391-406.
55. Alosi JA, McFadden DW. Peptide YY mediates inhibition of tumor growth and inflammation. Methods Mol Biol 2009; 512: 377-394.
56. Cunha DA, Ladriere L, Ortis F, et al. Glucagon-like peptide-1 agonists protect pancreatic beta-cells from lipotoxic endoplasmic reticulum stress through upregulation of BiP and JunB. Diabetes 2009; 58(12): 2851-2862.
57. Daousi C, Pinkney JH, Cleator J, Wilding JP, Ranganath LR. Acute peripheral administration of synthetic human GLP-1 (7-36 amide) decreases circulating IL-6 in obese patients with type 2 diabetes mellitus: A potential role for GLP-1 in modulation of the diabetic pro-inflammatory state? Regul Pept 2013; 183C: 54-61.
58. Lee YS, Park MS, Choung JS, et al. Glucagon-like peptide-1 inhibits adipose tissue macrophage infiltration and inflammation in an obese mouse model of diabetes. Diabetologia 2012; 55(9): 2456-2468.
59. Turnbaugh PJ, Ley RE, Mahowald MA, et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006; 444(7122): 1027-1031.
60. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 2008; 3(4): 213-223.
61. Amar J, Chabo C, Waget A, et al. Intestinal mucosal adherence and translocation of commensal bacteria at the early onset of type 2 diabetes: molecular mechanisms and probiotic treatment. EMBO Mol Med 2011; 3(9): 559-572.
62. Turnbaugh PJ, Hamady M, Yatsunenko T, et al. A core gut microbiome in obese and lean twins. Nature 2009; 457(7228): 480-484.
63. Ley RE, Backhed F, Turnbaugh P, et al. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 2005; 102(31): 11070-11075.
64. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature 2006; 444(7122): 1022-1023.
65. Duncan SH, Lobley GE, Holtrop G, et al. Human colonic microbiota associated with diet, obesity and weight loss. Int J Obes (Lond) 2008; 32(11): 1720-1724.
66. Le Chatelier E, Nielsen T, Qin J, et al. Richness of human gut microbiome correlates with metabolic markers. Nature 2013; 500(7464): 541-546.
67. Santacruz A, Collado MC, Garcia-Valdes L, et al. Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. Br J Nutr 2010; 104(1): 83-92.
68. Awada M, Soulage CO, Meynier A, et al. Dietary oxidized n-3 PUFA induce oxidative stress and inflammation: role of intestinal absorption of 4-HHE and reactivity in intestinal cells. J Lipid Res 2012; 53(10): 2069-2080.
69. Hodin CM, Verdam FJ, Grootjans J, et al. Reduced Paneth cell antimicrobial protein levels correlate with activation of the unfolded protein response in the gut of obese individuals. J Pathol 2011; 225(2): 276-284.
70. Cani PD, Amar J, Iglesias MA, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007; 56(7): 1761-1772.
71. Sokol H, Pigneur B, Watterlot L, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A 2008; 105(43): 16731-16736.
72. Furet JP, Kong LC, Tap J, et al. Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes 2010; 59(12): 3049-3057.
73. Fei N, Zhao L. An opportunistic pathogen isolated from the gut of an obese human causes obesity in germfree mice. ISME J 2013; 7(4): 880-884.
74. Malo MS, Alam SN, Mostafa G, et al. Intestinal alkaline phosphatase preserves the normal homeostasis of gut microbiota. Gut 2010; 59(11): 1476-1484.
75. Kim KA, Gu W, Lee IA, Joh EH, Kim DH. High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. PLoS One 2012; 7(10): e47713.
76. Spagnuolo MI, Cicalese MP, Caiazzo MA, et al. Relationship between severe obesity and gut inflammation in children: what's next? Ital J Pediatr 2010; 36: 66.
77. Pendyala S, Neff LM, Suarez-Farinas M, Holt PR. Diet-induced weight loss reduces colorectal inflammation: implications for colorectal carcinogenesis. Am J Clin Nutr 2011; 93(2): 234-242.
78. Daly DM, Park SJ, Valinsky WC, Beyak MJ. Impaired intestinal afferent nerve satiety signalling and vagal afferent excitability in diet induced obesity in the mouse. J Physiol 2011; 589(Pt 11): 2857-2870.
79. Poutahidis T, Kleinewietfeld M, Smillie C, et al. Microbial reprogramming inhibits Western diet-associated obesity. PLoS One 2013; 8(7): e68596.
80. Deiuliis J, Shah Z, Shah N, et al. Visceral adipose inflammation in obesity is associated with critical alterations in tregulatory cell numbers. PLoS One 2011; 6(1): e16376.
81. Wagner NM, Brandhorst G, Czepluch F, et al. Circulating regulatory T cells are reduced in obesity and may identify subjects at increased metabolic and cardiovascular risk. Obesity (Silver Spring) 2013; 21(3): 461-468.
82. Ma X, Torbenson M, Hamad AR, Soloski MJ, Li Z. High-fat diet modulates non-CD1d-restricted natural killer T cells and regulatory T cells in mouse colon and exacerbates experimental colitis. Clin Exp Immunol 2008; 151(1): 130-138.
83. Wang B, Sun J, Ma Y, et al. Increased oxidative stress and the apoptosis of regulatory T cells in obese mice but not resistant mice in response to a high-fat diet. Cell Immunol 2014; 288(1-2): 39-46.
84. Suzuki T, Hara H. Dietary fat and bile juice, but not obesity, are responsible for the increase in small intestinal permeability induced through the suppression of tight junction protein expression in LETO and OLETF rats. Nutr Metab (Lond) 2010; 7: 19.
85. Lam YY, Ha CW, Campbell CR, et al. Increased gut permeability and microbiota change associate with mesenteric fat inflammation and metabolic dysfunction in diet-induced obese mice. PLoS One 2012; 7(3): e34233.
86. Erridge C, Attina T, Spickett CM, Webb DJ. A high-fat meal induces low-grade endotoxemia: evidence of a novel mechanism of postprandial inflammation. Am J Clin Nutr 2007; 86(5): 1286-1292.
87. Amar J, Burcelin R, Ruidavets JB, et al. Energy intake is associated with endotoxemia in apparently healthy men. Am J Clin Nutr 2008; 87(5): 1219-1223.
88. Sun L, Yu Z, Ye X, et al. A marker of endotoxemia is associated with obesity and related metabolic disorders in apparently healthy Chinese. Diabetes Care 2010; 33(9): 1925-1932.
89. Osbak PS, Bindslev N, Hansen MB. Relationships between body mass index and short-circuit current in human duodenal and colonic mucosal biopsies. Acta Physiol (Oxf) 2011; 201(1): 47-53.
90. Ghoshal S, Witta J, Zhong J, de Villiers W, Eckhardt E. Chylomicrons promote intestinal absorption of lipopolysaccharides. J Lipid Res 2009; 50(1): 90-97.
91. Moreira AP, Texeira TF, Ferreira AB, Peluzio Mdo C, Alfenas RC. Influence of a high-fat diet on gut microbiota, intestinal permeability and metabolic endotoxaemia. Br J Nutr 2012; 108(5): 801-809.
92. Teixeira TF, Collado MC, Ferreira CL, Bressan J, Peluzio Mdo C. Potential mechanisms for the emerging link between obesity and increased intestinal permeability. Nutr Res 2012; 32(9): 637-647.
93. Resta-Lenert S, Barrett KE. Probiotics and commensals reverse TNF-alpha- and IFN-gamma-induced dysfunction in human intestinal epithelial cells. Gastroenterology 2006; 130(3): 731-746.
94. Ji Y, Sakata Y, Tso P. Nutrient-induced inflammation in the intestine. Curr Opin Clin Nutr Metab Care 2011; 14(4): 315-321.
95. Fujiyama Y, Hokari R, Miura S, et al. Butter feeding enhances TNF-alpha production from macrophages and lymphocyte adherence in murine small intestinal microvessels. J Gastroenterol Hepatol 2007; 22(11): 1838-1845.
96. Hara Y, Miura S, Komoto S, et al. Exposure to fatty acids modulates interferon production by intraepithelial lymphocytes. Immunol Lett 2003; 86(2): 139-148.
97. Cani PD, Possemiers S, Van de Wiele T, et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 2009; 58(8): 1091-1103.
98. Duca FA, Swartz TD, Sakar Y, Covasa M. Decreased intestinal nutrient response in diet-induced obese rats: role of gut peptides and nutrient receptors. Int J Obes (Lond) 2013; 37(3): 375-381.
99. Cani PD, Delzenne NM. The role of the gut microbiota in energy metabolism and metabolic disease. Curr Pharm Des 2009; 15(13): 1546-1558.
100. le Roux CW, Patterson M, Vincent RP, et al. Postprandial plasma ghrelin is suppressed proportional to meal calorie content in normal-weight but not obese subjects. J Clin Endocrinol Metab 2005; 90(2): 1068-1071.
101. Tschop M, Weyer C, Tataranni PA, et al. Circulating ghrelin levels are decreased in human obesity. Diabetes 2001; 50(4): 707-709.
102. Perreault M, Istrate N, Wang L, et al. Resistance to the orexigenic effect of ghrelin in dietary-induced obesity in mice: reversal upon weight loss. Int J Obes Relat Metab Disord 2004; 28(7): 879-885.
103. Williams DL, Hyvarinen N, Lilly N, et al. Maintenance on a high-fat diet impairs the anorexic response to glucagon-like-peptide-1 receptor activation. Physiol Behav 2011; 103(5): 557-564.
104. le Roux CW, Batterham RL, Aylwin SJ, et al. Attenuated peptide YY release in obese subjects is associated with reduced satiety. Endocrinology 2006; 147(1): 3-8.
105. Batterham RL, Cohen MA, Ellis SM, et al. Inhibition of food intake in obese subjects by peptide YY3-36. N Engl J Med 2003; 349(10): 941-948.
106. Bertrand RL, Senadheera S, Markus I, et al. A Western diet increases serotonin availability in rat small intestine. Endocrinology 2011; 152(1): 36-47.
107. Laberge S, Cruikshank WW, Beer DJ, Center DM. Secretion of IL-16 (lymphocyte chemoattractant factor) from serotonin-stimulated CD8+ T cells in vitro. J Immunol 1996; 156(1): 310-315.
108. Ghia JE, Li N, Wang H, et al. Serotonin has a key role in pathogenesis of experimental colitis. Gastroenterology 2009; 137(5): 1649-1660.
109. Ghanim H, Abuaysheh S, Sia CL, et al. Increase in plasma endotoxin concentrations and the expression of Toll-like receptors and suppressor of cytokine signaling-3 in mononuclear cells after a high-fat, high-carbohydrate meal: implications for insulin resistance. Diabetes Care 2009; 32(12): 2281-2287.
110. Deopurkar R, Ghanim H, Friedman J, et al. Differential effects of cream, glucose, and orange juice on inflammation, endotoxin, and the expression of Toll-like receptor-4 and suppressor of cytokine signaling-3. Diabetes Care 2010; 33(5): 991-997.
111. Pussinen PJ, Havulinna AS, Lehto M, Sundvall J, Salomaa V. Endotoxemia is associated with an increased risk of incident diabetes. Diabetes Care 2011; 34(2): 392-397.
112. Creely SJ, McTernan PG, Kusminski CM, 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(3): E740-E747.
113. Senn JJ. Toll-like receptor-2 is essential for the development of palmitate-induced insulin resistance in myotubes. J Biol Chem 2006; 281(37): 26865-26875.
114. Shi H, Kokoeva MV, Inouye K, et al. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest 2006; 116(11): 3015-3025.
115. Davis JE, Gabler NK, Walker-Daniels J, Spurlock ME. The c-Jun N-terminal kinase mediates the induction of oxidative stress and insulin resistance by palmitate and toll-like receptor 2 and 4 ligands in 3 T3-L1 adipocytes. Horm Metab Res 2009; 41(7): 523-530.
116. Brown J, Wang H, Hajishengallis GN, Martin M. TLR-signaling networks: an integration of adaptor molecules, kinases, and cross-talk. J Dent Res 2011; 90(4): 417-427.
117. Piya MK, McTernan PG, Kumar S. Adipokine inflammation and insulin resistance: the role of glucose, lipids and endotoxin. J Endocrinol 2013; 216(1): T1-T15.
118. Harwood HJ Jr. The adipocyte as an endocrine organ in the regulation of metabolic homeostasis. Neuropharmacology 2012; 63(1): 57-75.
119. de Heredia FP, Gomez-Martinez S, Marcos A. Obesity, inflammation and the immune system. Proc Nutr Soc 2012; 71(2): 332-338.
120. Lee JY, Zhao L, Hwang DH. Modulation of pattern recognition receptor-mediated inflammation and risk of chronic diseases by dietary fatty acids. Nutr Rev 2010; 68(1): 38-61.
121. Huang S, Rutkowsky JM, Snodgrass RG, et al. Saturated fatty acids activate TLR-mediated proinflammatory signaling pathways. J Lipid Res 2012; 53(9): 2002-2013.
122. Lee JY, Sohn KH, Rhee SH, Hwang D. Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J Biol Chem 2001; 276(20): 16683-16689.
123. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 2007; 117(1): 175-184.
124. Martinez FO, Sica A, Mantovani A, Locati M. Macrophage activation and polarization. Front Biosci 2008; 13: 453-461.
125. Talukdar S, Oh da Y, Bandyopadhyay G, et al. Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase. Nat Med 2012; 18(9): 1407-1412.
126. Sarraf P, Frederich RC, Turner EM, et al. Multiple cytokines and acute inflammation raise mouse leptin levels: potential role in inflammatory anorexia. J Exp Med 1997; 185(1): 171-175.
127. Grunfeld C, Zhao C, Fuller J, et al. Endotoxin and cytokines induce expression of leptin, the ob gene product, in hamsters. J Clin Invest 1996; 97(9): 2152-2157.
128. Bleau C, Lamontagne L, Savard R. New Lactobacillus acidophilus isolates reduce the release of leptin by murine adipocytes leading to lower interferon-gamma production. Clin Exp Immunol 2005; 140(3): 427-435.
129. Kusminski CM, da Silva NF, Creely SJ, et al. The in vitro effects of resistin on the innate immune signaling pathway in isolated human subcutaneous adipocytes. J Clin Endocrinol Metab 2007; 92(1): 270-276.
130. Rourke JL, Dranse HJ, Sinal CJ. Towards an integrative approach to understanding the role of chemerin in human health and disease. Obes Rev 2013; 14(3): 245-262.
131. Wolf AM, Wolf D, Rumpold H, Enrich B, Tilg H. Adiponectin induces the anti-inflammatory cytokines IL-10 and IL-1RA in human leukocytes. Biochem Biophys Res Commun 2004; 323(2): 630-635.
132. Gregor MF, Hotamisligil GS. Thematic review series: Adipocyte Biology. Adipocyte stress: the endoplasmic reticulum and metabolic disease. J Lipid Res 2007; 48(9): 1905-1914.
133. Hussey SE, Liang H, Costford SR, et al. TAK-242, a small-molecule inhibitor of Toll-like receptor 4 signalling, unveils similarities and differences in lipopolysaccharide- and lipid-induced inflammation and insulin resistance in muscle cells. Biosci Rep 2013; 33(1): 37-47.
134. Hong EG, Ko HJ, Cho YR, et al. Interleukin-10 prevents diet-induced insulin resistance by attenuating macrophage and cytokine response in skeletal muscle. Diabetes 2009; 58(11): 2525-2535.
135. Radin MS, Sinha S, Bhatt BA, Dedousis N, O'Doherty RM. Inhibition or deletion of the lipopolysaccharide receptor Toll-like receptor-4 confers partial protection against lipid-induced insulin resistance in rodent skeletal muscle. Diabetologia 2008; 51(2): 336-346.
136. Varma V, Yao-Borengasser A, Rasouli N, 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(6): E1300-E1310.
137. Green CJ, Macrae K, Fogarty S, et al. 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(2): 463-474.
138. Pillon NJ, Arane K, Bilan PJ, Chiu TT, Klip A. Muscle cells challenged with saturated fatty acids mount an autonomous inflammatory response that activates macrophages. Cell Commun Signal 2012; 10(1): 30.
139. Sell H, Dietze-Schroeder D, Eckel J. The adipocyte-myocyte axis in insulin resistance. Trends Endocrinol Metab 2006; 17(10): 416-422.
140. Liu Y, Chewchuk S, Lavigne C, et al. Functional significance of skeletal muscle adiponectin production, changes in animal models of obesity and diabetes, and regulation by rosiglitazone treatment. Am J Physiol Endocrinol Metab 2009; 297(3): E657-E664.
141. Quinn LS, Strait-Bodey L, Anderson BG, Argiles JM, Havel PJ. Interleukin-15 stimulates adiponectin secretion by 3 T3-L1 adipocytes: evidence for a skeletal muscle-to-fat signaling pathway. Cell Biol Int 2005; 29(6): 449-457.
142. Yang H, Chang J, Chen W, et al. Treadmill exercise promotes interleukin 15 expression in skeletal muscle and interleukin 15 receptor alpha expression in adipose tissue of high-fat diet rats. Endocrine 2013; 43(3): 579-585.
143. Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 2011; 11(2): 98-107.
144. Montane J, Cadavez L, Novials A. Stress and the inflammatory process: a major cause of pancreatic cell death in type 2 diabetes. Diabetes Metab Syndr Obes 2014; 7: 25-34.
145. Shu CJ, Benoist C, Mathis D. The immune system's involvement in obesity-driven type 2 diabetes. Semin Immunol 2012; 24(6): 436-442.
146. Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 1993; 259(5091): 87-91.
147. Rask-Madsen C, Dominguez H, Ihlemann N, et al. Tumor necrosis factor-alpha inhibits insulin's stimulating effect on glucose uptake and endothelium-dependent vasodilation in humans. Circulation 2003; 108(15): 1815-1821.
148. Bastard JP, Maachi M, Lagathu C, et al. Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw 2006; 17(1): 4-12.
149. Wallenius V, Wallenius K, Ahren B, et al. Interleukin-6-deficient mice develop mature-onset obesity. Nat Med 2002; 8(1): 75-79.
150. Sabio G, Das M, Mora A, et al. A stress signaling pathway in adipose tissue regulates hepatic insulin resistance. Science 2008; 322(5907): 1539-1543.
151. Solinas G, Vilcu C, Neels JG, et al. JNK1 in hematopoietically derived cells contributes to diet-induced inflammation and insulin resistance without affecting obesity. Cell Metab 2007; 6(5): 386-397.
152. Karelis AD, Rabasa-Lhoret R. Obesity: Can inflammatory status define metabolic health? Nat Rev Endocrinol 2013; 9(12): 694-695.
153. Karelis AD. Metabolically healthy but obese individuals. Lancet 2008; 372(9646): 1281-1283.
154. Plourde G, Karelis AD. Current issues in the identification and treatment of metabolically healthy but obese individuals. Nutr Metab Cardiovasc Dis 2014; 24(5): 455-459.