The role of inflammation in vascular insulin resistance with focus on IL-6

Hormone and Metabolic Research

Volumn 40, Issue 9, 2008, Pages 635-639

  Andersen, K ^a   Pedersen, B K ^a  

^a Rigshospitalet   (Denmark)

Author keywords

Cytokines; Insulin resistance; Interleukins; Metabolism; Vascular

Indexed keywords

INFLIXIMAB; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 6; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR;

ATHEROSCLEROSIS; BLOOD FLOW; BLOOD VESSEL TONE; CARDIOVASCULAR RISK; CHRONIC INFLAMMATION; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE MARKER; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM; ENERGY CONSUMPTION; HUMAN; HYPERGLYCEMIA; IN VITRO STUDY; INFLAMMATION; INSULIN RESISTANCE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; SMOOTH MUSCLE FIBER; SYSTEMIC VASCULITIS; VASCULAR INSULIN RESISTANCE; VASCULAR SMOOTH MUSCLE;

ANIMALS; CHRONIC DISEASE; DIABETES MELLITUS, TYPE 2; ENDOTHELIUM, VASCULAR; HUMANS; INFLAMMATION; INSULIN RESISTANCE; INTERLEUKIN-6;

EID: 53649101960     PISSN: 00185043     EISSN: None     Source Type: Journal    
DOI: 10.1055/s-0028-1083810     Document Type: Review

References (88)

1. Landmesser U, Hornig B, Drexler H. Endothelial function: a critical determinant in atherosclerosis? Circulation 2004; 109: II-27
2. Trepels T, Zeiher AM, Fichtlscherer S. The endothelium and inflammation. Endothelium 2006; 13: 423-429
3. Brunner H, Cockcroft JR, Deanfield J, Donald A, Ferrannini E, Halcox J, Kiowski W, Luscher TF, Mancia G, Natali A, Oliver JJ, Pessina AC, Rizzoni D, Rossi GP, Salvetti A, Spieker LE, Taddei S, Webb DJ. Endothelial function and dysfunction. Part II: Association with cardiovascular risk factors and diseases. A statement by the Working Group on Endothelins and Endothelial Factors of the European Society of Hypertension. J Hypertens 2005; 23: 233-246
4. Rask-Madsen C, King GL. Mechanisms of disease: endothelial dysfunction in insulin resistance and diabetes. Nat Clin Pract Endocrinol Metab 2007; 3: 46-56
5. Enderle MD, Benda N, Schmuelling RM, Haering HU, Pfohl M. Preserved endothelial function in IDDM patients, but not in NIDDM patients, compared with healthy subjects. Diabetes Care 1998; 21: 271-277
6. Clarkson P, Celermajer DS, Donald AE, Sampson M, Sorensen KE, Adams M, Yue DK, Betteridge DJ, Deanfield JE. Impaired vascular reactivity in insulin-dependent diabetes mellitus is related to disease duration and low density lipoprotein cholesterol levels. J Am Coll Cardiol 1996; 28: 573-579
7. Arcaro G, Zenere BM, Saggiani F, Zenti MG, Monauni T, Lechi A, Muggeo M, Bonadonna RC. ACE inhibitors improve endothelial function in type 1 diabetic patients with normal arterial pressure and microalbuminuria. Diabetes Care 1999; 22: 1536-1542
8. Celermajer DS, Sorenson KE, Bull C, Robinson J, Deanfield JE. Endothelialdependent dilation in the systemic arteries of asymptomatic subjects relates to coronary risk factors and their interaction. J Am Coll Cardiol 1994; 24: 1468-1474
9. Melikian N, Wheatcroft SB, Ogah OS, Murphy C, Chowienczyk PJ, Wierzbicki AS, Sanders TA, Jiang B, Duncan ER, Shah AM, Kearney MT. Asymmetric dimethylarginine and reduced nitric oxide bioavailability in young Black African men. Hypertension 2007; 49: 873-877
10. Steinberg HO, Chaker H, Learning R. Obesity/insulin resistance is associated with endothelial dysfunction. Implications for the syndrome of insulin resistance. J Clin Invest 1996; 97: 2601-2610
11. Williams IL, Chowienczyk PJ, Wheatcroft SB, Patel AG, Sherwood RA, Momin A, Shah AM, Kearney MT. Endothelial function and weight loss in obese humans. Obes Surg 2005; 15: 1055-1060
12. Hsueh WA, Ouinones MJ. Role of endothelial dysfunction in insulin resistance. The Am J Cardiol 2003; 92: 10-17
13. Vriese AS De, Verbeuren TJ, Van d V, Lameire NH, Vanhoutte PM. Endothelial dysfunction in diabetes. Br J Pharmacol 2000; 130: 963-974
14. MacVeigh GE, Brennan GM, Johnston CD, MacDermott BJ, MacGrath LT, Henry WR, Andrews JW, Hayes JR. Impaired endothelium-dependent and independent vasodilation in patients with type 2 (non-insulindependent) diabetes mellitus. Diabetologia 1992; 35: 771-776
15. Laakso M, Edelman SV, Brechtel G, Baron AD. Decreased effect of insulin to stimulate skeletal muscle blood flow in obese man. A novel mechanism for insulin resistance. J Clin Invest 1990; 85: 1844-1852
16. Laakso M, Edelman SV, Brechtel G, Baron AD. Impaired insulin-mediated skeletal muscle blood flow in patients with NIDDM. Diabetes 1992; 41: 1076-1083
17. Castell JV, Gomez-Lechon MJ, David M, Hirano T, Kishimoto T, Heinrich PC. Recombinant human interleukin-6 (IL-6/BSF-2/HSF) regulates the synthesis of acute phase proteins in human hepatocytes. FEBS Lett 1988; 232: 347-350
18. Morrone G, Ciliberto G, Oliviero S, Arcone R, Dente L, Content J, Cortese R. Recombinant interleukin 6 regulates the transcriptional activation of a set of human acute phase genes. J Biol Chem 1988; 263: 12554-12558
19. Schindler R, Mantilla J, Endres S, Ghorbani R, Clark SC, Dinarello CA. Correlations and interactions in the production of interleukin-6 (IL-6), IL-1, and tumor necrosis factor (TNF) in human blood mononudear cells: IL-6 suppresses IL-1 and TNF. Blood 1990; 75: 40-47
20. Steensberg A, Fischer CP, Keller C, Moller K, Pedersen BK. IL-6 enhances plasma IL-1ra, IL-10, and cortisol in humans. Am J Physiol Endocrinol Metab 2003; 285: E433-E437
21. Tilg H, Dinarello CA, Mier JW. IL-6 and APPs: anti-inflammatory and immunosuppressive mediators. Immunol Today 1997; 18: 428-432
22. Libby P. Inflammation in atherosclerosis. Nature 2002; 420: 868-874
23. Libby P, Ridker PM, Maseri A. Inflammation and atherosclerosis. Circulation 2002; 105: 1135-1143
24. Dandona P, Aljada A, Bandyopadhyay A. Inflammation: the link between insulin resistance, obesity and diabetes. Trends Immunol 2004; 25: 4-7
25. Bruunsgaard H, Pedersen BK. Age-related inflammatory cytokines and disease. Immunol Allergy Clin North Am 2003; 23: 15-39
26. Petersen AM, Pedersen BK. The anti-inflammatory effect of exercise. J Appl Physiol 2005; 98: 1154-1162
27. Duncan BB, Schmidt Ml, Pankow JS, Ballantyne CM, Couper D, Vigo A, Hoogeveen R, Folsom AR, Heiss G. Low-grade systemic inflammation and the development of type 2 diabetes: the atherosclerosis risk in communities study. Diabetes 2003; 52: 1799-1805
28. Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA 2001; 286: 327-334
29. Barzilay JI, Abraham L, Heckbert SR, Cushman M, Kuller LH, Resnick HE, Tracy RP. The relation of markers of inflammation to the development of glucose disorders in the elderly: the Cardiovascular Health Study. Diabetes 2001; 50: 2384-2389
30. Han TS, Sattar N, Williams K, Conzalez-Villalpando C, Lean ME, Haffher SM. Prospective study of C-reactive protein in relation to the development of diabetes and metabolic syndrome in the Mexico City Diabetes Study. Diabetes Care 2002; 25: 2016-2021
31. Lindsay RS, Funahashi T, Hanson RL, Matsuzawa Y, Tanaka S, Tataranni PA, Knowler WC, Krakoff J. Adiponectin and development of type 2 diabetes in the Pima Indian population. Lancet 2002; 360: 57-58
32. Vozarova B, Weyer C, Lindsay RS, Pratley RE, Bogardus C, Tataranni PA. High white blood cell count is associated with a worsening of insulin sensitivity and predicts the development of type 2 diabetes. Diabetes 2002; 51: 455-461
33. Freeman DJ, Norrie J, Caslake MJ, Gaw A, Ford I, Lowe GD, O'Reilly DS, Packard CJ, Sattar N. C-reactive protein is an independent predictor of risk for the development of diabetes in the West of Scotland Coronary Prevention Study. Diabetes 2002; 51: 1596-1600
34. Ford ES. Leukocyte count, erythrocyte sedimentation rate, and diabetes incidence in a national sample of US adults. Am J Epidemiol 2002; 155: 57-64
35. Nakanishi N, Yoshida H, Matsuo Y, Suzuki K, Tatara K. White blood-cell count and the risk of impaired fasting glucose or Type II diabetes in middle-aged Japanese men. Diabetologia 2002; 45: 42-48
36. Festa A, D'Agostino RJr, Tracy RP, Haffner SM. Elevated levels of acutephase proteins and plasminogen activator inhibitor-1 predict the development of type 2 diabetes: the insulin resistance atherosclerosis study. Diabetes 2002; 51: 1131-1137
37. Harris TB, Ferrucd L, Tracy RP, Corti MC, Wacholder S, Ettinger WHJr, Heimovitz H, Cohen HJ, Wallace R. Associations of elevated interleukin-6 and C-reactive protein levels with mortality in the elderly. Am J Med 1999; 106: 506-512
38. Volpato S, Guralnik JM, Ferrucci L, Balfour J, Chaves P, Fried LP, Harris TB. Cardiovascular disease, interleukin-6, and risk of mortality in older women: the women's health and aging study. Circulation 2001; 103: 947-953
39. Reuben DB, Cheh AI, Harris TB, Ferrucd L, Rowe JW, Tracy RP, Seeman TE. Peripheral blood markers of inflammation predict mortality and functional decline in high-functioning community-dwelling older persons. J Am Geriatr Soc 2002; 50: 638-644
40. Roubenoff R, Parise H, Payette HA, Abad LW, D'Agostino R, Jacques PF, Wilson PW, Dinarello CA, Harris TB. Cytokines, insulin-like growth factor 1, sarcopenia, and mortality in very old community-dwelling men and women: the Framingham Heart Study. Am J Med 2003; 115: 429-435
41. Mooradian AD, Reed RL, Osterweil D, Scuderi P. Detectable serum levels of tumor necrosis factor alpha may predict early mortality in elderly institutionalized patients. J Am Geriatr Soc 1991; 39: 891-894
42. Rosenthal AJ, MacMurtry CT, Sanders KM, Jacobs M, Thompson D, Adler RA. The soluble interleukin-2 receptor predicts mortality in older hospitalized men. J Am Geriatr Soc 1997; 45: 1362-1364
43. Weijenberg MP, Feskens EJ, Kromhout D. White blood cell count and the risk of coronary heart disease and all-cause mortality in elderly men. Arterioscler Thromb Vasc Biol 1996; 16: 499-503
44. Cappola AR, Xue QL, Ferrucci L, Guralnik JM, Volpato S, Fried LP. Insulinlike growth factor I and interleukin-6 contribute synergistically to disability and mortality in older women. J Clin Endocrinol Metab 2003; 88: 2019-2025
45. Yeh SS, Hafner A, Chang CK, Levine DM, Parker TS. Schuster MW. Risk factors relating blood markers of inflammation and nutritional status to survival in cachectic geriatric patients in a randomized clinical trial. J Am Geriatr Soc 2004; 52: 1708-1712
46. Bruunsgaard H, Andersen-Ranberg K, Hjelmborg JB, Pedersen BK, Jeune B. Elevated levels of tumor necrosis factor alpha and mortality in centenarians. Am J Med 2003; 115: 278-283
47. Bruunsgaard H, Ladelund S, Pedersen AN, Schroll M, Jorgensen T, Pedersen BK. Predicting death from tumour necrosis factor-alpha and interleukin-6 in 80-year-old people. Clin Exp Immunol 2003; 132: 24-31
48. Lee IM, Paffenbarger RS Jr. Hennekens CH. Physical activity, physical fitness and longevity. Aging (Milano) 1997; 9: 2-11
49. Lamonte MJ, Blair SN, Church TS. Physical activity and diabetes prevention. J Appl Physiol 2005; 99: 1205-1213
50. Thune I, Furberg AS. Physical activity and cancer risk: dose-response and cancer, all sites and site-specific. Med Sci Sports Exerc 2001; 33: S530-S550
51. Clarkson P, Montgomery HE, Mullen MJ, Donald AE, Powe AJ, Bull T, Jubb M, World M, Deanfield JE. Exercise training enhances endothelial function in young men. J Am Coll Cardiol 1999; 33: 1379-1385
52. DeSouza CA, Shapiro LF, Clevenger CM, Dinenno FA Monahan KD, Tanaka H, Seals DR. Regular aerobic exercise prevents and restores agerelated declines in endothelium-dependent vasodilation in healthy men. Circulation 2000; 102: 1351-1357
53. Kingwell BA, Sherrard B, Jennings GL, Dart AM. Four weeks of cycle training increases basal production of nitric oxide from the forearm. Am J Physiol 1997; 272: H1070-H1077
54. Hambrecht R, Fiehn E, Weigl C, Gielen S, Hamann C, Kaiser R, Yu J, Adams V, Niebauer J, Schuler G. Regular physical exercise corrects endothelial dysfunction and improves exercise capacity in patients with chronic heart failure. Circulation 1998; 98: 2709-2715
55. Hambrecht R, Hilbrich L, Erbs S, Gielen S, Fiehn E, Schoene N, Schuler G. Correction of endothelial dysfunction in chronic heart failure: additional effects of exercise training and oral L-arginine supplementation. J Am Coll Cardiol 2000; 35: 706-713
56. Maiorana A, O'Driscoll G, Cheetham C, Collis J, Goodman C, Rankin S, Taylor R, Green D. Combined aerobic and resistance exercise training improves functional capacity and strength in CHF. J Appl Physiol 2000; 88: 1565-1570
57. Sdacqua A, Candigliota M, Ceravolo R, Scozzafava A, Sinopoli F, Corsonello A, Sesti C, Perticone F. Weight loss in combination with physical activity improves endothelial dysfunction in human obesity. Diabetes Care 2003; 26: 1673-1678
58. Andreozzi GM, Leone A, Laudani R, Deinite G, Martini R. Acute impairment of the endothelial function by maximal treadmill exercise in patients with intermittent claudication, and its improvement after supervised physical training. Int Angiol 2007; 26: 12-17
59. Moyna NM, Thompson PD. The effect of physical activity on endothelial function in man. Acta Physiol Scand 2004; 180: 113-123
60. Kado S, Nagase T, Nagata N. Circulating levels of interleukin-6, its soluble receptor and interleukin-6/interleukin-6 receptor complexes in patients with type 2 diabetes mellitus. Acta Diabetol 1999; 36: 67-72
61. Vozarova B, Weyer C, Hanson K, Tataranni PA, Bogardus C, Pratley RE. Circulating interleukin-6 in relation to adiposity, insulin action, and insulin secretion. Obes Res 2001; 9: 414-417
62. Pickup JC, Chusney GD, Thomas SM, Burt D. Plasma interleukin-6, tumour necrosis factor alpha and blood cytokine production in type 2 diabetes. Life Sci 2000; 67: 291-300
63. Mohamed-Ali V, Goodrick S, Rawesh A, Katz DR, Miles JM, Yudkin JS. Klein S, Coppack SW. Subcutaneous adipose tissue releases interleukin-6, but not tumor necrosis factor-alpha, in vivo. J Clin Endocrinol Metab 1997; 82: 4196-4200
64. Petersen KF, Dufour S, Befroy D, Garda R, Shulman Gl. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 2004; 350: 664-671
65. Carey AL, Bruce CR, Sacchetti M, Anderson MJ, Olson D, Saltin B, Hawley JA, Febbraio MA. Interleukin-6 and tumor necrosis factor-alpha are not increased in patients with type 2 diabetes: evidence that plasma IL-6 is related to fat mass and not insulin responsiveness. Diabetologia 2004; 47: 1029-1037
66. Neta R, Sayers TJ, Oppenheim JJ. Relationship of TNF to interleukins. Immunol Ser 1992; 56: 499-566
67. Yudkin JS. Inflammation, obesity, and the metabolic syndrome. Horm Metab Res 2007; 39: 707-709
68. Carey AL. Steinberg GR, Macaulay SL, Thomas WG, Holmes AG, Ramm G, Prelovsek O, Hohnen-Behrens C, Watt MJ, James DE, Kemp BE, Pedersen BK, Febbraio MA. Interleukin-6 increases insulin-stimulated glucose disposal in humans and glucose uptake and fatty acid oxidation in vitro via AMP-activated protein kinase. Diabetes 2006; 55: 2688-2697
69. Al-Khalili L, Bouzakri K, Glund S. Lonnqvist F, Koistinen HA, Krook A. Signaling specificity of interleukin-6 action on glucose and lipid metabolism in skeletal muscle. Mol Endocrinol 2006; 20: 3364-3375
70. Ruderman NB, Keller C, Richard AM, Saha AK, Luo Z, Xiang X, Giralt M, Ritov VB, Menshikova EV, Kelley DE, Hidalgo J, Pedersen BK, Kelly M. Interleukin-6 regulation of AMP-activated protein kinase: Potential role in the systemic response to exercise and prevention of the metabolic syndrome. Diabetes 2006; 55 (Suppl 2): S48-S54
71. Glund S, Deshmukh A, Long YC, Moller T, Koistinen HA, Caidahl K, Zierath JR, Krook A. lnterleukin-6 directly increases glucose metabolism in resting human skeletal muscle. Diabetes 2007; 56: 1630-1637
72. Geiger PC, Hancock C, Wright DC, Han DH, Holloszy JO. IL-6 increases muscle insulin sensitivity only at superphysiological levels. Am J Physiol Endocrinol Metab 2007; 292: E1842-E1846
73. Bhagat K, Moss R, Collier J, Vallance P. Endothelial "stunning" following a brief exposure to endotoxin: a mechanism to link infection and infarction? Cardiovasc Res 1996; 32: 822-829
74. Hingorani AD, Cross J, Kharbanda RK, Mullen MJ, Bhagat K, Taylor M, Donald AE, Palacios M, Griffin GE, Deanfield JE, MacAllister RJ, Vallance P. Acute systemic inflammation impairs endothelium-dependent dilatation in humans. Circulation 2000; 102: 994-999
75. Melikian N, Chowienczyk P, Maccarthy PA, Williams IL, Wheatcroft SB, Sherwood R, Gale C, Shah AM, Kearney MT. Determinants of endothelial function in asymptomatic subjects with and without the metabolic syndrome. Atherosclerosis 2008; 197: 375-382
76. Vita JA, Keaney JF Jr, Larson MG, Keyes MJ, Massaro JM, Lipinska I, Lehman BT, Fan S, Osypiuk E, Wilson PW, Vasan RS, Mitchell GF, Benjamin Ej. Brachial artery vasodilator function and systemic inflammation in the Framingham Offspring Study. Circulation 2004; 110: 3604-3609
77. Esteve E, Castro A, Lopez-Bermejo A, Vendrell J, Ricart W, Fernandez-Real JM. Serum interleukin-6 correlates with endothelial dysfunction in healthy men independently of insulin sensitivity. Diabetes Care 2007; 30: 939-945
78. Kim F, Gallis B, Corson MA. TNF-alpha inhibits flow and insulin signaling leading to NO production in aortic endothelial cells. Am J Physiol Cell Physiol 2001; 280: C1057-C1065
79. Rask-Madsen C, Dominguez H, Ihlemann N, Hermann T, Kober L, Torp-Pedersen C. Tumor necrosis factor-alpha inhibits insulin's stimulating effect on glucose uptake and endothelium-dependent vasodilation in humans. Circulation 2003; 108: 1815-1821
80. Federici M, Hribal ML, Menghini R, Kanno H, Marchetti V, Porzio O, Sunnarborg SW, Rizza S, Serino M, Cunsolo V, Lauro D, Mauriello A, Smookler DS, Sbraccia P, Sesti C, Lee DC, Khokha R, Accili D, Lauro R. Timp3 deficiency in insulin receptor-haploinsufficient mice promotes diabetes and vascular inflammation via increased TNF-alpha. J Clin Invest 2005; 115: 3494-3505
81. Booth AD. Jayne DR, Kharbanda RK, MacEniery CM, Mackenzie IS, Brown J, Wilkinson IB. Infliximab improves endothelial dysfunction in systemic vasculitis: a model of vascular inflammation. Circulation 2004; 109: 1718-1723
82. Branen L, Hovgaard L, Nitulescu M, Bengtsson E, Nilsson J, Jovinge S. Inhibition of tumor necrosis factor-alpha reduces atherosclerosis in apolipoprotein E knockout mice. Arterioscler Thromb Vasc Biol 2004; 24: 2137-2142
83. Andreozzi F, Laratta E, Procopio C, Hribal ML, Sciacqua A, Perticone M, Miele C, Perticone F, Sesti G. Interleukin-6 impairs the insulin signaling pathway, promoting production of nitric oxide in human umbilical vein endothelial cells. Mol Cell Biol 2007; 27: 2372-2383
84. Saura M, Zaragoza C, Bao C, Herranz B, Rodriguez-Puyol M, Lowenstein CJ. Stat3 mediates interleukin-6 [correction of interelukin-6] inhibition of human endothelial nitric-oxide synthase expression. J Biol Chem 2006; 281: 30057-30062
85. Venugopal SK, Devaraj S, Yuhanna I, Shaul P, Jialal I. Demonstration that C-reactive protein decreases eNOS expression and bioactivity in human aortic endothelial cells. Circulation 2002; 106: 1439-1441
86. Verma S, Wang CH, Li SH, Dumont AS, Fedak PW, Badiwala MV, Dhillon B, Weisel RD, Li RK, Mickle DA, Stewart DJ. A self-fulfilling prophecy: C-reactive protein attenuates nitric oxide production and inhibits angiogenesis. Circulation 2002; 106: 913-919
87. Clapp BR, Hirschfield GM, Stony C, Gallimore JR, Stidwill RP, Singer M, Deanfield JE, MacAllister RJ, Pepys MB, Vallance P, Hingorani AD. Inflammation and endothelial function: direct vascular effects of human C-reactive protein on nitric oxide bioavailability. Circulation 2005; 111: 1530-1536
88. Schrader LI, Kinzenbaw DA, Johnson AW, Faraci FM, Didion SP. IL-6 deficiency protects against angiotensin Il induced endothelial dysfunction and hypertrophy. Arterioscler Thromb Vasc Biol 2007; 27: 2576-2581