The influence of endotoxemia on the molecular mechanisms of insulin resistance;La influencia de la endotoxemia en los mecanismos moleculares de resistencia a la insulina

Nutricion Hospitalaria

Volumn 27, Issue 2, 2012, Pages 382-390

  Boroni Moreira, A P ^a   de Cassia Goncalves Alfenas R ^a  

^a FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

Author keywords

Endotoxemia; Gut microbiota; Inflammation; Insulin resistance; Lipopolysaccharide

Indexed keywords

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

INSULIN; LIPOPOLYSACCHARIDE;

DIABETES MELLITUS; DIET; ENDOTOXEMIA; HUMAN; INSULIN RESISTANCE; METABOLISM; OBESITY; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION;

DIABETES COMPLICATIONS; DIABETES MELLITUS; DIET; ENDOTOXEMIA; HUMANS; INSULIN; INSULIN RESISTANCE; LIPOPOLYSACCHARIDES; OBESITY; SIGNAL TRANSDUCTION;

EID: 84858735069     PISSN: 02121611     EISSN: 16995198     Source Type: Journal    
DOI: 10.3305/nh.2012.27.2.5543     Document Type: Review

References (96)

1. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest 2006; 116 (7): 1793-801.
2. Milanski M, Degasperi G, Coope A, Morari J, Denis R, Cintra DE et al. Saturated fatty acids produce an inflammatory response predominantly through the activation of 2009 TLR4 signaling in hypothalamus: implications for the pathogenesis of obesity. J Neurosci 2009; 29 (2): 359-70.
3. Moraes JC, Coope A, Morari J, Cintra DE, Roman EA, Pauli JR et al. High-fat diet induces apoptosis of hypothalamic neurons. PLoS One 2009; 4 (4): e5045.
4. Ding S, Lund PK. Role of intestinal inflammation as an early event in obesity and insulin resistance. Curr Opin Clin Nutr Metab Care 2011; 14: 328-33.
5. Manco M, Putignani L, Bottazzo GF. Gut microbiota, lipo -polysaccharides, and innate immunity in the pathogenesis of obesity and cardiovascular risk. Endocr Rev 2010; 31 (6): 817-44.
6. Cani PD, Possemiers S, Van de Wiele T, Guiot Y, Everard A, Rottier O, 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): 1091-103.
7. Shanik MH, Xu Y, Skrha J, Dankner R, Zick Y, Roth J. Insulin resistance and hyperinsulinemia: is hyperinsulinemia the cart or the horse? Diabetes Care 2008; 31 (2): S262-8.
8. Carvalho-Filho MA, Carvalheira JBC, Velloso LA, Saad MJA. Cross-talk das vias de sinalizacao de insulina e angiotensina II: implicacoes com a associacao entre diabetes mellitus e hipertensao arterial e doenca cardiovascular. Arq Bras Endocrinol Metab 2007; 51 (2): 195-203.
9. Carvalheira JBC, Zecchin HG, Saad MJA. Vias de Sinalizacao da Insulina. Arq Bras Endocrinol Metab 2002; 46 (4): 419-25.
10. Pessin JE, Saltiel AR. Signaling pathways in insulin action: molecular targets of insulin resistance. J Clin Invest 2000; 106 (2): 165-9.
11. Shulman GI. Cellular mechanisms of insulin resistance. J Clin Invest 2000; 106 (2): 171-6.
12. Hoehn KL, Salmon AB, Hohnen-Behrens C, Turner N, Hoy AJ, Maghzal GJ et al. Insulin resistance is a cellular antioxidant defense mechanism. Proc Natl Acad Sci 2009; 106 (42): 17787-92.
13. Laron Z. Insulin and the brain. Arch Physiol Biochem 2009; 115 (2): 112-6.
14. Luis DA, Aller R, Izaola O, Sagrado MG, Conde R. Effect of two different hypocaloric diets in transaminases and insulin resistance in nonalcoholic fatty liver disease and obese patients. Nutr Hosp 2010; 25 (5): 730-5.
15. Roith DL, Zick Y. Recent advances in our understanding of insulin action and insulin resistance. Diabetes Care 2001; 24 (3): 588-97.
16. Saltiel AR, Kahn CR. Insulin signaling and the regulation of glucose and lipid metabolism. Nature 2001; 414: 799-806.
17. Velloso LA, Carvalho CR, Rojas FA, Folli F, Saad MJ. Insulin signalling in heart involves insulin receiver substrates-1 and -2, activation of phosphatidylinositol 3-kinase and the JAK 2-growth related pathway. Cardiovasc Res 1998; 40 (1): 96-102.
18. Hotamisligil GS. Inflammatory pathways and insulin action. Int J Obes Relat Metab Disord 2003; 27: S53-5.
19. Gao, Z, Hwang D, Bataille F, Lefevre M, York D, Quon MJ et al. Serine phosphorylation of insulin receiver substrate 1 by inhibitor kappa B kinase complex. J Biol Chem 2002; 277: 48115-21.
20. Hirosumi J, Tuncman G, Chang L, Gorgun CZ, Uysal KT, Maeda K, Karin M, Hotamisligil GS. A central role for JNK in obesity and insulin resistance. Nature 2002; 420 (6913): 333-6.
21. White MF. IRS proteins and the common path to diabetes. Am J Physiol Endocrinol Metab 2002; 283: E413-22.
22. Prada PO, Zecchin HG, Gasparetti AL, Torsoni MA, Ueno M, Hirata AE et al. Western diet modulates insulin signaling, c-Jun N-terminal kinase activity, and insulin receiver substrate-1ser307 phosphorylation in a tissue-specific fashion. Endocrinology 2005; 146 (3): 1576-87.
23. Lin X, Taguchi A, Park S, Kushner JA, Li F, Li Y et al. Dysregulation of insulin receiver substrate 2 in beta cells and brain causes obesity and diabetes. J Clin Invest 2004; 114 (7): 908-16.
24. Tschritter O, Preissl H, Hennige AM, Stumvoll M, Porubska K, Frost R et al. The cerebrocortical response to hyperinsulinemia is reduced in overweight humans: a magnetoencephalographic study. Proc Natl Acad Sci USA 2006; 103 (32): 12103-8.
25. DeFronzo RA. Insulin resistance, lipotoxicity, type 2 diabetes and atherosclerosis: the missing links. The Claude Bernard Lecture 2009. Diabetologia 2010; 53: 1270-87.
26. Weinberg JM. Lipotoxicity. Kidney Int 2006; 70: 1560-6.
27. Shah A, Mehta N, Reilly MP. Adipose Inflammation, insulin resistance, and cardiovascular disease. J Parenter Enteral Nutr 2008; 32 (6): 638-44.
28. Carvalho MHC, Colaco AL, Fortes ZB. Citocinas, disfuncao endotelial e resistencia a insulina. Arq Bras Endocrinol Metab 2006; 50 (2): 304-12.
29. Hattori M, Taylor TD. The human intestinal microbiome: a new frontier of human biology. DNA Res 2009; 16 (1): 1-12.
30. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010; 464 (7285): 59-65.
31. Phillips ML. Gut reaction: environmental effects on the human microbiota. Environ Health Perspect 2009; 117 (5): A198-205.
32. Delzenne NM, Cani PD. Gut microbiota and the pathogenesis of insulin resistance. Curr Diab Rep 2011; 11: 154-9.
33. Cani PD, Delzenne NM. The gut microbiome as therapeutic target. Pharmacol Ther 2011; 130: 202-12.
34. 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 diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 2007a; 50 (11): 2374-83.
35. Brun P, Castagliuolo I, Leo VD, Buda A, Pinzani M, Palu G, Martines D. Increased intestinal permeability in obese mice: new evidence in the pathogenesis of nonalcoholic steatohepatitis. Am J Physiol Gastrointest Liver Physiol 2007; 292: G518-25.
36. Ghoshal S, Witta J, Zhong J, Villiers W, Eckhardt E. Chylomicrons promote intestinal absorption of lipopolysaccharides. J Lipid Res 2009; 50: 90-7.
37. Berg RD. The indigenous gastrointestinal microflora. Trends Microbiol 1996; 4: 430-5.
38. Raetz CRH, Whitfield C. Lipopolysaccharide endotoxins. Annu Rev Biochem 2002; 71: 635-700.
39. Neal MD, Leaphart C, Levy R, Prince J, Billiar TR, Watkins S et al. Enterocyte TLR4 mediates phagocytosis and translocation of bacteria across the intestinal barrier. J Immunol 2006; 176: 3070-9.
40. Schwartz YSH, Dushkin MI. Endotoxin-lipoprotein complex formation as a factor in atherogenesis: associations with hyperlipidemia and with lecithin:cholesterol acyltransferase activity. Biochemistry Mosc 2002; 67: 747-52.
41. Levels JH, Abraham PR, van den Ende A, van Deventer SJ. Distribution and kinetics of lipoprotein-bound endotoxin. Infect Immun 2001; 69 (5): 2821-8.
42. Harris HW, Grunfeld C, Feingold KR, Read TE, Kane JP, Jones AL et al. Chylomicrons alter the fate of endotoxin, decreasing tumor necrosis factor release and preventing death. J Clin Invest 1993; 91: 1028-34.
43. Peri F, Piazza M, Calabrese V, Damore G, Cighetti R. Exploring the LPS/TLR4 signal pathway with small molecules. Biochem Soc Trans 2010; 38 (5): 1390-5.
44. Araki Y, Katoh T, Ogawa A, Bamba S, Andoh A, Koyama S, Fujiyama Y, Bamba T. Bile acid modulates transepithelial permeability via the generation of reactive oxygen species in the Caco-2 cell line. Free Radic Biol Med 2005; 39: 769-80.
45. Shimazu R, Akashi S, Ogata H, Nagai Y, Fukudome K, Miyake K et al. MD-2, a molecule that confers lipopolysaccharide responsiveness on toll-like receiver 4. J Exp Med 1999; 189: 1777-82.
46. Grimaldi E, Donnarumma G, Perfetto B, De Filippis A, Melito A, Tufano MA. Proinflammatory signal transduction pathway induced by shigella flexneri porins in caco-2 cells. Braz Journal Microbiol 2009; 40: 701-9.
47. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007b; 56 (7): 1761-72.
48. Lee JY, Soh KH, Rhee SH, Hwang D. Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase 2 mediated through Toll-like receiver 4. J Biol Chem 2001; 276 (2001): 16683-9.
49. Song MJ, Kim KH, Yoon JM, Kim JB. Activation of Toll-like receiver 4 is associated with insulin resistance in adipocytes. Biochem Biophys Res Commun 2006; 346 (3): 739-45.
50. Bastos DHM, Rogero MM, Areas JAG. Mecanismos de acao de compostos bioativos dos alimentos no contexto de processos inflamatorios relacionados a obesidade. Arq Bras Endocrinol Metab 2009; 53 (5): 646-56.
51. Pan ZK. Toll-like receivers and TLR-mediated signaling: more questions than answers. Am J Physiol Lung Cell Mol Physiol 2004; 286: L918-20.
52. Fujishiro M, Gotoh Y, Katagiri H, Sakoda H, Ogihara T, Anai M, et al. Three mitogen-activated protein kinases inhibit insulin signaling by different mechanisms in 3T3-L1 adipocytes. Mol Endocrinol 2003; 17 (3): 487-7.
53. Wang Q, Dziarski R, Kirschning CJ, Muzio M, Gupta D. Micrococci and peptidoglycan activate TLR2→MyD88→ IRAK→TRAF→NIK→IKK→NF-kB signal transduction pathway that induces transcription of interleukin-8. Infect Immun 2001; 69 (4): 2270-6.
54. Yuan M, Konstantopoulos N, Lee J, Hansen L, Li ZW, Karin M et al. Reversal of obesity- and diet-induced insulin resistance with salicylates or targeted disruption of Ikkbeta. Science 2001; 293 (5535): 1673-7.
55. Kim JK, Kim YJ, Fillmore JJ, Chen Y, Moore I, Lee J et al. Prevention of fat-induced insulin resistance by salicylate. J Clin Invest 2001; 108: 437-46.
56. Cani PD, Bibiloni B, Knauf C, Waget A, Neyrinck AM, Burcelin RG 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): 1470-81.
57. Ma LJ, Mao SL, Taylor KL, Kanjanabuch T, Guan Y, Zhang Y et al. Prevention of obesity and insulin resistance in mice lacking plasminogen activator inhibitor 1. Diabetes 2004; 53 (2): 336-46.
58. Shoelson SE, Lee J, Yuan M. Inflammation and the IKKbeta/IkappaB/NF-kappaB axis in obesity- and diet-induced insulin resistance. Int J Obes Relat Metb Disord 2003; 27: S49-52.
59. Uysal KT, Wiesbrock SM, Marino MW, Hotamisligil GS. Protection from obesity induced insulin resistance in mice lacking TNF-〈 function. Nature 1997; 389 (6651): 610-4.
60. Comalada M, Xaus J, Valledor AF, Lopez-Lopez C, Pennington DJ, Celada A. PKC epsilon is involved in JNK activation that mediates LPS-induced TNF-alpha, which induces apoptosis in macrophages. Am J Physiol Cell Physiol 2003; 285 (5): 1235-45.
61. Carvalho-Filho MA, Ueno M, Carvalheira JBC, Velloso LA, Saad MJA. Targeted disruption of iNOS prevents LPS-induced -nitrosation of IR /IRS-1 and Akt and insulin resistance in muscle of mice. Am J Physiol Endocrinol Metab 2006; 291: E476-82.
62. Park HK, Qatanani M, Briggs ER, Ahima RS, Lazar MA. Inflammatory induction of human resistin causes insulin resistance in endotoxemic mice. Diabetes 2011; 60 (3): 775-83.
63. Luis DA, Sagrado MG, Conde R, Aller R, Izaola O. Resistin levels and inflammatory markers in patients with morbid obesity. Nutr Hosp 2010; 25 (4): 630-4.
64. Agwunobi AO, Reid C, Maycock P, Little RA, Carlson GL. Insulin resistance and substrate utilization in human endotoxemia. J Clin Endocrinol Metab 2000; 85 (10): 3770-8.
65. Dandona P, Ghanim H, Bandyopadhyay A, Korzeniewski K, Ling Sia C, Dhindsa S, et al. Insulin suppresses endotoxininduced oxidative, nitrosative, and inflammatory stress in humans. Diabetes Care 2010; 33 (11); 2416-23.
66. Souza SC, Palmer HJ, Kang YH, Yamamoto MT, Muliro KV, Paulson KE et al. TNF-alpha induction of lipolysis is mediated through activation of the extracellular signal related kinase pathway in 3T3-L1 adipocytes. J Cell Biochem 2003; 89 (6): 1077-86.
67. Kim J, Wei Y, Sowers JR. Role of mitochondrial dysfunction in insulin resistance. Circ Res 2008; 102: 401-14.
68. Chang YH, Chang DM, Lin KC, Shin SJ, Lee YJ. Visfatin in overweight/obesity, type 2 diabetes mellitus, insulin resistance, metabolic syndrome, and cardiovascular diseases: A metaanalysis and systemic review. Diabetes Metab Res Rev 2011.
69. Mehta NN, McGillicuddy FC, Anderson PD, Hinkle CC, Shah R, Pruscino L et al. Experimental endotoxemia induces adipose inflammation and insulin resistance in humans. Diabetes 2010; 59: 172-81.
70. Ueki K, Kondo T, Kahn CR. Suppressor of cytokine signaling 1 (SOCS-1) and SOCS-3 cause insulin resistance through inhibition of tyrosine phosphorylation of insulin receiver substrate proteins by discrete mechanisms. Mol Cell Biol 2004; 24: 5434-46.
71. Rui L, Yuan M, Frantz D, Shoelson S, White MF. SOCS-1 and SOCS-3 block insulin signaling by ubiquitin-mediated degradation of IRS1 and IRS2. J Biol Chem 2002; 277: 42394-8.
72. 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): 392-7.
73. Amar J, Burcelin R, Ruidavets JB, Cani PD, Fauvel J, Alessi MC, Chamontin B, Ferrieres J. Energy intake is associated with endotoxemia in apparently healthy men. Am J Clin Nutr 2008; 87: 1219-23.
74. Sun L, Yu Z, Ye X, Zou S, Li H, Yu D, et al. A marker of endotoxemia is associated with obesity and related metabolic disorders in apparently healthy Chinese. Diabetes Care 2010; 33 (9): 1925-32.
75. Devaraj S, Dasu MR, Park SH, Jialal I. Increased levels of ligands of Toll-like receivers 2 and 4 in type 1 diabetes. Diabetologia 2009; 52 (8): 1665-8.
76. 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: E740-7.
77. Ruiz AG, Casafont F, Crespo J, Cayon A, Mayorga M, Estebanez A et al. Lipopolysaccharide-binding protein plasma levels and liver TNF-alpha gene expression in obese patients: evidence for the potential role of endotoxin in the pathogenesis of non-alcoholic steatohepatitis. Obes Surg 2007; 17: 1374-80.
78. Kueht ML, McFarlin BK, Lee RE. Severely obese have greater LPS-stimulated TNF-〈 production than normal weight africanamerican women. Obesity 2009; 17 (3): 447-51.
79. Van Dielen FM, Buurman WA, Hadfoune M, Nijhuis J, Greve JW. Macrophage inhibitory factor, plasminogen activator inhibitor-1, other acute phase proteins, and inflammatory mediators normalize as a result of weight loss in morbidly obese subjects treated with gastric restrictive surgery. J Clin Endocrinol Metab 2004; 89 (8): 4062-8.
80. Abranches MV, Oliveira FCE, Bressan J. Peroxisome proliferator-activated receptor: effects on nutritional homeostasis, obesity and diabetes mellitus. Nutr Hosp 2011; 26 (2): 271-9.
81. Khovidhunkit W, Kim MS, Memon RA, Shigenaga JK, Moser AH, Feingold KR et al. Effects of infection and inflammation on lipid and lipoprotein metabolism: mechanisms and consequences to the host. J Lipid Res 2004; 45 (7): 1169-96.
82. Birjmohun RS, van Leuven SI, Levels JH, van 't Veer C, Kuivenhoven JA, Meijers JC, et al. High-density lipoprotein attenuates inflammation and coagulation response on endotoxin challenge in humans. Arterioscler Thromb Vasc Biol 2007; 27: 1153-8.
83. Pajkrt D, Doran JE, Koster F, Lerch PG, Arnet B, van der Poll T et al. Antiinflammatory effects of reconstituted high-density lipoprotein during human endotoxemia. J Exp Med 1996; 184 95): 1601-8.
84. Cuoco L, Montalto M, Jorizzo RA, Santarelli L, Arancio F, Cammarota G et al. Eradication of small intestinal bacterial overgrowth and oro-cecal transit in diabetics. Hepatogastroenterology 2002; 49: 1582-6.
85. Byrne MM, Pluntke K, Wank U, Schirra J, Arnold R, Goke B et al. Inhibitory effects of hyperglycaemia on fed jejunal motility: potential role of hyperinsulinaemia. Eur J Clin Invest 1998; 28: 72-8.
86. Yang SQ, Lin HZ, Lane MD, Clemens M, Diehl AM. Obesity increases sensitivity to endotoxin liver injury: implications for the pathogenesis of steatohepatitis. Proc Natl Acad Sci USA 1997; 94: 2557-62.
87. Nymark M, Pussinen PJ, Tuomainen AM, Forsblom C, Groop PH, Lehto M et al. Serum lipopolysaccharide activity is associated with the progression of kidney disease in finnish patients with type 1 diabetes. Diabetes Care 2009; 32: 1689-93.
88. Pussinen PJ, Tuomisto K, Jousilahti P, Havulinna AS, Sundvall J, Salomaa V. Endotoxemia, immune response to periodontal pathogens, and systemic inflammation associate with incident cardiovascular disease events. Arterioscler Thromb Vasc Biol 2007; 27: 1433-9.
89. Geraldo JM, Alfenas RCG. Papel da dieta na prevencao e no controle da inflamacao cronica - evidencias atuais. Arq Bras Endocrinol Metab 2008; 52 (6): 951-67.
90. Kohen VL, Candela CG, Fernandez CF, Rosa LZ, Milla SP, Urbieta M, Lopez LMB. Parametros hormonales e inflamatorios en un grupo de mujeres con sobrepeso/obesidad. Nutr Hosp 2011; 26 (4): 884-9.
91. Ghanim H, Abuaysheh S, Sia CL, Korzeniewski K, Chaudhuri A, Fernandez-Real JM et al. Increase in plasma endotoxin concentrations and the expression of toll-like receivers and suppressor of cytokine signaling-3 in mononuclear cells after a high-fat, high-carbohydrate meal. Diabetes Care 2009; 32 (12): 2281-7.
92. 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: 1286-92.
93. Ghanim H, Sia CL, Upadhyay M, Korzeniewski K, Viswanathan P, Abuaysheh S, et al. Orange juice neutralizes the proinflammatory effect of a high-fat,high-carbohydrate meal and prevents endotoxin increase and Toll-like receiver expression. J Clin Nutr 2010; 91: 940-9.
94. De Bandt JP, Waligora-Dupriet AJ, Butel MJ. Intestinal microbiota in inflammation and insulin resistance: relevance to humans. Curr Opin Clin Nutr Metab Care 2011,14: 334-40.
95. Romeo J, Nova E, Warnberg J, Gomez-Martinez S, Ligia LED, Marcos A. Immunomodulatory effect of fibres, probiotics and synbiotics in different life-stages. Nutr Hosp 2010; 25 (3): 341-9.
96. Laparra JM, Sanz Y. Interactions of gut microbiota with functional food components and nutraceuticals. Pharmacol Res 2010; 61: 219-25.