Inflammatory signaling in skeletal muscle insulin resistance: Green signal for nutritional intervention?

Current Opinion in Clinical Nutrition and Metabolic Care

Volumn 13, Issue 6, 2010, Pages 647-655

  Hommelberg, Pascal P H ^a,b   Langen, Ramon C J ^a   Schols, Annemie M W J ^a   Mensink, Ronald P ^a,b   Plat, Jogchum ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

Author keywords

fatty acids; inflammation; insulin resistance; polyphenols; skeletal muscle

Indexed keywords

CURCUMIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN KINASE B; QUERCETIN; RESVERATROL; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNSATURATED FATTY ACID;

ADIPOSE TISSUE; CACHEXIA; CURCUMA LONGA; CYTOKINE RELEASE; HUMAN; HYPERLIPIDEMIA; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; INTRACELLULAR SIGNALING; LIPID DIET; MACROPHAGE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUTRITIONAL SUPPORT; OBESITY; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; SKELETAL MUSCLE;

ADIPOSE TISSUE; ANIMALS; CYTOKINES; DIETARY FATS; FATTY ACIDS; FLAVONOIDS; HUMANS; INFLAMMATION; INSULIN RESISTANCE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MACROPHAGES; MUSCLE, SKELETAL; NF-KAPPA B; PHENOLS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 78149284156     PISSN: 13631950     EISSN: 14736519     Source Type: Journal    
DOI: 10.1097/MCO.0b013e32833f1acd     Document Type: Review

References (113)

1. Barton GM, Medzhitov R. Toll-like receptor signaling pathways. Science 2003;300:1524-1525.
2. Medzhitov R. Toll-like receptors and innate immunity. Nat Rev Immunol 2001;1:135-145.
3. Fessler MB, Rudel LL, Brown JM. Toll-like receptor signaling links dietary fatty • acids to the metabolic syndrome. Curr Opin Lipidol 2009;20:379-385. Excellent review discussing the evidence for TLR signaling as the link between dietary FAs and insulin resistance/metabolic syndrome
4. Frost RA, Nystrom G, Burrows PV, Lang CH. Temporal differences in the ability of ethanol to modulate endotoxin-induced increases in inflammatory cytokines in muscle under in vivo conditions. Alcohol Clin Exp Res 2005;29:1247-1256.
5. Frost RA, Nystrom GJ, Lang CH. Multiple Toll-like receptor ligands induce an IL-6 transcriptional response in skeletal myocytes. Am J Physiol Regul Integr Comp Physiol 2006;290:R773-R784.
6. Lang CH, Silvis C, Deshpande N, et al. Endotoxin stimulates in vivo expression of inflammatory cytokines tumor necrosis factor alpha, interleukin-1beta,-6, and high-mobility-group protein-1 in skeletal muscle. Shock 2003;19:538-546.
7. 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;276:16683-16689.
8. Shi H, Kokoeva MV, Inouye K, et al. TLR4 links innate immunity and fatty acidinduced insulin resistance. J Clin Invest 2006;116:3015-3025.
9. Radin MS, Sinha S, Bhatt BA, et al. 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;51:336-346.
10. Tsukumo DM, Carvalho-Filho MA, Carvalheira JB, et al. Loss-of-function mutation in Toll-like receptor 4 prevents diet-induced obesity and insulin resistance. Diabetes 2007;56:1986-1998.
11. Senn JJ. Toll-like receptor-2 is essential for the development of palmitateinduced insulin resistance in myotubes. J Biol Chem 2006;281:26865-26875.
12. Levin MC, Monetti M, Watt MJ, et al. Increased lipid accumulation and insulin resistance in transgenic mice expressing DGAT2 in glycolytic (type II) muscle. Am J Physiol Endocrinol Metab 2007;293:E1772-E1781.
13. Storlien LH, Jenkins AB, Chisholm DJ, et al. Influence of dietary fat composition on development of insulin resistance in rats. Relationship to muscle triglyceride and omega-3 fatty acids in muscle phospholipid. Diabetes 1991;40:280-289.
14. Moro C, Galgani JE, Luu L, et al. Influence of gender, obesity, and muscle lipase activity on intramyocellular lipids in sedentary individuals. J Clin Endocrinol Metab 2009;94:3440-3447.
15. Krssak M, Falk Petersen K, Dresner A, et al. Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. Diabetologia 1999;42:113-116.
16. Perseghin G, Scifo P, De Cobelli F, et al. Intramyocellular triglyceride content is a determinant of in vivo insulin resistance in humans: a 1H-13C nuclear magnetic resonance spectroscopy assessment in offspring of type 2 diabetic parents. Diabetes 1999;48:1600-1606.
17. Bruce CR, Kriketos AD, Cooney GJ, Hawley JA. Disassociation of muscle triglyceride content and insulin sensitivity after exercise training in patients with type 2 diabetes. Diabetologia 2004;47:23-30.
18. Bruce CR, Thrush AB, Mertz VA, et al. Endurance training in obese humans improves glucose tolerance and mitochondrial fatty acid oxidation and alters muscle lipid content. Am J Physiol Endocrinol Metab 2006;291:E99-E107.
19. Goodpaster BH, He J, Watkins S, Kelley DE. Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes. J Clin Endocrinol Metab 2001;86:5755-5761.
20. Itani SI, Ruderman NB, Schmieder F, Boden G. Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha. Diabetes 2002;51:2005-2011.
21. Boden G, Lebed B, Schatz M, et al. Effects of acute changes of plasma free fatty acids on intramyocellular fat content and insulin resistance in healthy subjects. Diabetes 2001;50:1612-1617.
22. Chavez JA, Summers SA. Characterizing the effects of saturated fatty acids on insulin signaling and ceramide and diacylglycerol accumulation in 3T3-L1 adipocytes and C2C12 myotubes. Arch Biochem Biophys 2003;419:101-109.
23. Yu C, Chen Y, Cline GW, et al. Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-1)-associated phosphatidylinositol 3-kinase activity in muscle. J Biol Chem 2002;277:50230-50236.
24. Schmitz-Peiffer C. Signalling aspects of insulin resistance in skeletal muscle: mechanisms induced by lipid oversupply. Cell Signal 2000;12(9-10): 583-594.
25. Schmitz-Peiffer C, Craig DL, Biden TJ. Ceramide generation is sufficient to account for the inhibition of the insulin-stimulated PKB pathway in C2C12 skeletal muscle cells pretreated with palmitate. J Biol Chem 1999;274:24202-24210.
26. Liu L, Zhang Y, Chen N, et al. Upregulation of myocellular DGAT1 augments triglyceride synthesis in skeletal muscle and protects against fat-induced insulin resistance. J Clin Invest 2007;117:1679-1689.
27. Schenk S, Horowitz JF. Acute exercise increases triglyceride synthesis in skeletal muscle and prevents fatty acid-induced insulin resistance. J Clin Invest 2007;117:1690-1698.
28. Pinnamaneni SK, Southgate RJ, Febbraio MA, Watt MJ. Stearoyl CoA desaturase 1 is elevated in obesity but protects against fatty acid-induced skeletal muscle insulin resistance in vitro. Diabetologia 2006;49:3027-3037.
29. Timmers S, Schrauwen P, de Vogel J. Muscular diacylglycerol metabolism and insulin resistance. Physiol Behav 2008;94:242-251.
30. Ragheb R, Shanab GM, Medhat AM, et al. Free fatty acid-induced muscle insulin resistance and glucose uptake dysfunction: evidence for PKC activation and oxidative stress-activated signaling pathways. Biochem Biophys Res Commun 2009;389:211-216.
31. Schmitz-Peiffer C, Browne CL, Oakes ND, et al. Alterations in the expression and cellular localization of protein kinase C isozymes epsilon and theta are associated with insulin resistance in skeletal muscle of the high-fat-fed rat. Diabetes 1997;46:169-178.
32. Itani SI, Zhou Q, Pories WJ, et al. Involvement of protein kinase C in human skeletal muscle insulin resistance and obesity. Diabetes 2000;49:1353-1358.
33. Li Y, Soos TJ, Li X, et al. Protein kinase C theta inhibits insulin signaling by phosphorylating IRS1 at Ser (1101). J Biol Chem 2004;279:45304-45307.
34. Kim JK, Fillmore JJ, Sunshine MJ, et al. PKC-theta knockout mice are protected from fat-induced insulin resistance. J Clin Invest 2004;114:823-827.
35. Gao Z, Wang Z, Zhang X, et al. Inactivation of PKCtheta leads to increased susceptibility to obesity and dietary insulin resistance in mice. Am J Physiol Endocrinol Metab 2007;292:E84-91.
36. Sun Z, Arendt CW, Ellmeier W, et al. PKC-theta is required for TCR-induced NF-kappaB activation in mature but not immature T lymphocytes. Nature 2000;404:402-407.
37. Bhatt BA, Dube JJ, Dedousis N, et al. Diet-induced obesity and acute hyperlipidemia reduce IkappaBalpha levels in rat skeletal muscle in a fiber-type dependent manner. Am J Physiol Regul Integr Comp Physiol 2006;290:R233-R240.
38. Ropelle ER, Pauli JR, Prada PO, et al. Reversal of diet-induced insulin resistance with a single bout of exercise in the rat: the role of PTP1B and IRS-1 serine phosphorylation. J Physiol 2006;577(Pt 3):997-1007.
39. Todd MK, Watt MJ, Le J, et al. Thiazolidinediones enhance skeletal muscle triacylglycerol synthesis while protecting against fatty acid-induced inflammation and insulin resistance. Am J Physiol Endocrinol Metab 2007;292:E485-E493.
40. Hommelberg PP, Plat J, Langen RC, et al. Fatty acid-induced NF-{kappa}B activation and insulin resistance in skeletal muscle are chain length dependent. Am J Physiol Endocrinol Metab 2009;296:E114-E120.
41. Coll T, Eyre E, Rodriguez-Calvo R, et al. Oleate reverses palmitate-induced insulin resistance and inflammation in skeletal muscle cells. J Biol Chem 2008;283:11107-11116.
42. Hommelberg PP, Langen RC, Schols AM, et al. Trans fatty acid-induced NF-kappaB activation does not induce insulin resistance in cultured murine skeletal muscle cells. Lipids 2010;45:285-290.
43. Yuan M, Konstantopoulos N, Lee J, et al. Reversal of obesity-and dietinduced insulin resistance with salicylates or targeted disruption of Ikkbeta. Science 2001;293:1673-1677.
44. Kim JK, Kim YJ, Fillmore JJ, et al. Prevention of fat-induced insulin resistance by salicylate. J Clin Invest 2001;108:437-446.
45. Hundal RS, Petersen KF, Mayerson AB, et al. Mechanism by which high-dose aspirin improves glucose metabolism in type 2 diabetes. J Clin Invest 2002;109:1321-1326.
46. Sinha S, Perdomo G, Brown NF, O'Doherty RM. Fatty acid-induced insulin resistance in l6 myotubes is prevented by inhibition of activation and nuclear localization of nuclear factor kB. J Biol Chem 2004;279:41294-41301.
47. Cai D, Frantz JD, Tawa NE Jr, et al. IKKbeta/NF-kappaB activation causes severe muscle wasting in mice. Cell 2004;119:285-298.
48. Gao Z, Hwang D, Bataille F, et al. Serine phosphorylation of insulin receptor substrate 1 by inhibitor kappa B kinase complex. J Biol Chem 2002;277:48115-48121.
49. Rohl M, Pasparakis M, Baudler S, et al. Conditional disruption of IkappaB kinase 2 fails to prevent obesity-induced insulin resistance. J Clin Invest 2004;113:474-481.
50. Gao Z, Zuberi A, Quon MJ, et al. Aspirin inhibits serine phosphorylation of insulin receptor substrate 1 in tumor necrosis factor-treated cells through targeting multiple serine kinases. J Biol Chem 2003;278:24944-24950.
51. Pillinger MH, Capodici C, Rosenthal P, et al. Modes of action of aspirin-like drugs: salicylates inhibit erk activation and integrin-dependent neutrophil adhesion. Proc Natl Acad Sci U S A 1998;95:14540-14545.
52. Law BK, Waltner-Law ME, Entingh AJ, et al. Salicylate-induced growth arrest is associated with inhibition of p70s6k and down-regulation of c-myc, cyclin D1, cyclin A, and proliferating cell nuclear antigen. J Biol Chem 2000;275:38261-38267.
53. Jiang G, Dallas-Yang Q, Liu F, et al. Salicylic acid reverses phorbol 12-myristate-13-acetate (PMA)-and tumor necrosis factor alpha (TNFalpha) - induced insulin receptor substrate 1 (IRS1) serine 307 phosphorylation and insulin resistance in human embryonic kidney 293 (HEK293) cells. J Biol Chem 2003;278:180-186.
54. Torgerson TR, Colosia AD, Donahue JP, et al. Regulation of NF-kappa B, AP-1, NFAT, and STAT1 nuclear import in T lymphocytes by noninvasive delivery of peptide carrying the nuclear localization sequence of NF-kappa B p50. J Immunol 1998;161:6084-6092.
55. Bandyopadhyay GK, Yu JG, Ofrecio J, Olefsky JM. Increased p85/55/50 expression and decreased phosphotidylinositol 3-kinase activity in insulinresistant human skeletal muscle. Diabetes 2005;54:2351-2359.
56. Hirosumi J, Tuncman G, Chang L, et al. A central role for JNK in obesity and insulin resistance. Nature 2002;420:333-336.
57. Liu G, Rondinone CM. JNK: bridging the insulin signaling and inflammatory pathway. Curr Opin Investig Drugs 2005;6:979-987.
58. Vijayvargia R, Mann K, Weiss HR, et al. JNK deficiency enhances fatty acid utilization and diverts glucose from oxidation to glycogen storage in cultured myotubes. Obesity (Silver Spring) 2010 [Epub ahead of print].
59. Sabio G, Kennedy NJ, Cavanagh-Kyros J, et al. Role of muscle c-Jun. • NH2-terminal kinase 1 in obesity-induced insulin resistance. Mol Cell Biol 2010;30:106-115. This study demonstrates an important role for JNK1 in muscle in peripheral insulin resistance in response to diet-induced obesity.
60. Sabio G, Davis RJ. cJun. NH (2)-terminal kinase 1 (JNK1): roles in metabolic • regulation of insulin resistance. Trends Biochem Sci 2010 [Epub ahead of print]. This clear review describes the multiple roles JNK1 plays in different organs in the regulation of insulin resistance.
61. Galic S, Oakhill JS, Steinberg GR. Adipose tissue as an endocrine organ. Mol • Cell Endocrinol 2010;316:129-139. Complete review that gives a general overview of the most common adipokines, their main source (adipocytes or resident macrophages), and their effects on insulin resistance.
62. Goossens GH. The role of adipose tissue dysfunction in the pathogenesis of obesity-related insulin resistance. Physiol Behav 2008;94:206-218.
63. Sell H, Eckel J, Dietze-Schroeder D. Pathways leading to muscle insulin resistance - the muscle - fat connection. Arch Physiol Biochem 2006;112:105-113.
64. Dietze D, Koenen M, Rohrig K, et al. Impairment of insulin signaling in human skeletal muscle cells by co-culture with human adipocytes. Diabetes 2002;51:2369-2376.
65. Dietze D, Ramrath S, Ritzeler O, et al. Inhibitor kappaB kinase is involved in the paracrine crosstalk between human fat and muscle cells. Int J Obes Relat Metab Disord 2004;28:985-992.
66. Dietze-Schroeder D, Sell H, Uhlig M, et al. Autocrine action of adiponectin on human fat cells prevents the release of insulin resistance-inducing factors. Diabetes 2005;54:2003-2011.
67. Weisberg SP, McCann D, Desai M, et al. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 2003;112:1796-1808.
68. Di Gregorio GB, Yao-Borengasser A, Rasouli N, et al. Expression of CD68 and macrophage chemoattractant protein-1 genes in human adipose and muscle tissues: association with cytokine expression, insulin resistance, and reduction by pioglitazone. Diabetes 2005;54:2305-2313.
69. Xu H, Barnes GT, Yang Q, 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.
70. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 2007;117:175-184.
71. Weisberg SP, Hunter D, Huber R, et al. CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J Clin Invest 2006;116:115-124.
72. Ghanim H, Aljada A, Hofmeyer D, et al. Circulating mononuclear cells in the obese are in a proinflammatory state. Circulation 2004;110:1564-1571.
73. Nguyen MT, Favelyukis S, Nguyen AK, et al. Asubpopulation of macrophages infiltrates hypertrophic adipose tissue and is activated by free fatty acids via Toll-like receptors 2 and 4 and JNK-dependent pathways. J Biol Chem 2007;282:35279-35292.
74. Torres SH, De Sanctis JB, de L'Briceno M, et al. Inflammation and nitric oxide production in skeletal muscle of type 2 diabetic patients. J Endocrinol 2004;181:419-427.
75. 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:E1300-E1310. This study demonstrates that besides the adipose tissue, skeletal muscle of obese persons can also have increased infiltration of macrophages. Furthermore, the authors showed that palmitate could induce skeletal muscle insulin resistance by activation of macrophages via a TLR2/4, JNK signaling pathway.
76. Hevener AL, Olefsky JM, Reichart D, et al. Macrophage PPAR gamma is required for normal skeletal muscle and hepatic insulin sensitivity and full antidiabetic effects of thiazolidinediones. J Clin Invest 2007;117:1658-1669.
77. Samokhvalov V, Bilan PJ, Schertzer JD, et al. Palmitate-and lipopolysaccharide-activated macrophages evoke contrasting insulin responses in muscle cells. Am J Physiol Endocrinol Metab 2009;296:E37-46.
78. Arkan MC, Hevener AL, Greten FR, et al. IKK-beta links inflammation to obesity-induced insulin resistance. Nat Med 2005;11:191-198.
79. Hotamisligil GS. Role of endoplasmic reticulum stress and c-Jun. NH2-terminal kinase pathways in inflammation and origin of obesity and diabetes. Diabetes 2005;54(Suppl 2):S73-S78.
80. Shishodia S, Aggarwal BB. Guggulsterone inhibits NF-kappaB and IkappaBalpha kinase activation, suppresses expression of antiapoptotic gene products, and enhances apoptosis. J Biol Chem 2004;279:47148-47158.
81. Shishodia S, Sethi G, Ahn KS, Aggarwal BB. Guggulsterone inhibits tumor cell proliferation, induces S-phase arrest, and promotes apoptosis through activation of c-Jun. N-terminal kinase, suppression of Akt pathway, and downregulation of antiapoptotic gene products. Biochem Pharmacol 2007;74:118-130.
82. Shishodia S, Majumdar S, Banerjee S, Aggarwal BB. Ursolic acid inhibits nuclear factor-kappaB activation induced by carcinogenic agents through suppression of IkappaBalpha kinase and p65 phosphorylation: correlation with down-regulation of cyclooxygenase 2, matrix metalloproteinase 9, and cyclin D1. Cancer Res 2003;63:4375-4383.
83. Lee TY, Lee KC, Chen SY, Chang HH. 6-Gingerol inhibits ROS and iNOS through the suppression of PKC-alpha and NF-kappaB pathways in lipopolysaccharide-stimulated mouse macrophages. Biochem Biophys Res Commun 2009;382:134-139.
84. Tripathi S, Maier KG, Bruch D, Kittur DS. Effect of 6-gingerol on proinflammatory cytokine production and costimulatory molecule expression in murine peritoneal macrophages. J Surg Res 2007;138:209-213.
85. Surh YJ, Han SS, Keum YS, et al. Inhibitory effects of curcumin and capsaicin on phorbol ester-induced activation of eukaryotic transcription factors, NF-kappaB and AP-1. Biofactors 2000;12:107-112.
86. Kim CS, Kawada T, Kim BS, et al. Capsaicin exhibits anti-inflammatory property by inhibiting IkB-a degradation in LPS-stimulated peritoneal macrophages. Cell Signal 2003;15:299-306.
87. Kang JH, Kim CS, Han IS, et al. Capsaicin, aspicy component ofhot peppers, modulates adipokine gene expression and protein release from obese-mouse adipose tissues and isolated adipocytes, and suppresses the inflammatory responses of adipose tissue macrophages. FEBS Lett 2007;581:4389-4396.
88. Rabi T, Shukla S, Gupta S. Betulinic acid suppresses constitutive and TNFalpha-induced NF-kappaB activation and induces apoptosis in human prostate carcinoma PC-3 cells. Mol Carcinog 2008;47:964-973.
89. Viji V, Shobha B, Kavitha SK, et al. Betulinic acid isolated from Bacopa monniera (L.) Wettst suppresses lipopolysaccharide stimulated interleukin-6 production through modulation of nuclear factor-kappaB in peripheral blood mononuclear cells. Int Immunopharmacol 2010;10:843-849.
90. Wadsworth TL, McDonald TL, Koop DR. Effects of Ginkgo biloba extract (EGb 761) and quercetin on lipopolysaccharide-induced signaling pathways involved in the release of tumor necrosis factor-alpha. Biochem Pharmacol 2001;62:963-974.
91. Puangpraphant S, de Mejia EG. Saponins in yerba mate tea (Ilex paraguariensis A. St.-Hil) and quercetin synergistically inhibit iNOS and COX-2 in lipopolysaccharide-induced macrophages through NFkappaB pathways. J Agric Food Chem 2009;57:8873-8883.
92. Takada Y, Andreeff M, Aggarwal BB. Indole-3-carbinol suppresses NF-kappaB and IkappaBalpha kinase activation, causing inhibition of expression of NF-kappaB-regulated antiapoptotic and metastatic gene products and enhancement of apoptosis in myeloid and leukemia cells. Blood 2005;106:641-649.
93. Cho HJ, Seon MR, Lee YM, et al. 3, 3′-Diindolylmethane suppresses the inflammatory response to lipopolysaccharide in murine macrophages. J Nutr 2008;138:17-23.
94. Joo YE, Karrasch T, Muhlbauer M, et al. Tomato lycopene extract prevents lipopolysaccharide-induced NF-kappaB signaling but worsens dextran sulfate sodium-induced colitis in NF-kappaBEGFP mice. PLoS One 2009;4: e4562.
95. Feng D, Ling WH, Duan RD. Lycopene suppresses LPS-induced NO and IL-6 production by inhibiting the activation of ERK, p38MAPK, and NF-kappaB in macrophages. Inflamm Res 2010;59:115-121.
96. Geng Z, Rong Y, Lau BH. S-allyl cysteine inhibits activation of nuclear factor kappa B in human T cells. Free Radic Biol Med 1997;23:345-350.
97. Chang HP, Huang SY, Chen YH. Modulation of cytokine secretion by garlic oil derivatives is associated with suppressed nitric oxide production in stimulated macrophages. J Agric Food Chem 2005;53:2530-2534.
98. Wang SL, Li Y, Wen Y, et al. Curcumin, a potential inhibitor of up-regulation of TNF-alpha and IL-6 induced by palmitate in 3T3-L1 adipocytes through NF-kappaB and JNK pathway. Biomed Environ Sci 2009;22:32-39.
99. Woo HM, Kang JH, Kawada T, et al. Active spice-derived components can inhibit inflammatory responses of adipose tissue in obesity by suppressing inflammatory actions of macrophages and release of monocyte chemoattractant protein-1 from adipocytes. Life Sci 2007;80:926-931.
100. Kundu JK, Shin YK, Surh YJ. Resveratrol modulates phorbol ester-induced pro-inflammatory signal transduction pathways in mouse skin in vivo: NF-kappaB and AP-1 as prime targets. Biochem Pharmacol 2006;72:1506-1515.
101. Tsai SH, Lin-Shiau SY, Lin JK. Suppression of nitric oxide synthase and the down-regulation of the activation of NFkappaB in macrophages by resveratrol. Br J Pharmacol 1999;126:673-680.
102. Bharti AC, Donato N, Singh S, Aggarwal BB. Curcumin (diferuloylmethane) down-regulates the constitutive activation of nuclear factor-kappa B and IkappaBalpha kinase in human multiple myeloma cells, leading to suppression of proliferation and induction of apoptosis. Blood 2003;101:1053-1062.
103. Han SS, Keum YS, Seo HJ, Surh YJ. Curcumin suppresses activation of NF-kappaB and AP-1 induced by phorbol ester in cultured human promyelocytic leukemia cells. J Biochem Mol Biol 2002;35:337-342.
104. Kundu JK, Surh YJ. Molecular basis of chemoprevention by resveratrol: NF-kappaB and AP-1 as potential targets. Mutat Res 2004;555:65-80.
105. Yang F, Oz HS, Barve S, et al. The green tea polyphenol (-)-epigallocatechin-3-gallate blocks nuclear factor-kappa B activation by inhibiting I kappa B kinase activity in the intestinal epithelial cell line IEC-6. Mol Pharmacol 2001;60:528-533.
106. Gonzales AM, Orlando RA. Curcumin and resveratrol inhibit nuclear factorkappaB-mediated cytokine expression in adipocytes. Nutr Metab (Lond) 2008;5:17.
107. Kang L, Heng W, Yuan A, et al. Resveratrol modulates adipokine expression • and improves insulin sensitivity in adipocytes: relative to inhibition of inflammatory responses. Biochimie 2010;92:789-796. A recent example of how the anti-inflammatory characteristics of polyphenolic compounds (resveratrol) can modulate adipokine expression and insulin sensitivity.
108. Baur JA, Pearson KJ, Price NL, et al. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 2006;444:337-342.
109. Lagouge M, Argmann C, Gerhart-Hines Z, et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 2006;127:1109-1122.
110. Na LX, Zhang YL, Li Y, et al. Curcumin improves insulin resistance in skeletal muscle of rats. Nutr Metab Cardiovasc Dis 2010 [Epub ahead of print].
111. Eid HM, Martineau LC, Saleem A, et al. Stimulation of AMP-activated protein kinase and enhancement of basal glucose uptake in muscle cells by quercetin and quercetin glycosides, active principles of the antidiabetic medicinal plant Vaccinium vitis-idaea. Mol Nutr Food Res 2010;54:991-1003.
112. Tang M, Larson-Meyer DE, Liebman M. Effect of cinnamon and turmeric on urinary oxalate excretion, plasma lipids, and plasma glucose in healthy subjects. Am J Clin Nutr 2008;87:1262-1267.
113. Fukino Y, Shimbo M, Aoki N, et al. Randomized controlled trial for an effect of green tea consumption on insulin resistance and inflammation markers. J Nutr Sci Vitaminol (Tokyo) 2005;51:335-342.