Diabetes is a proinflammatory state: A translational perspective

Expert Review of Endocrinology and Metabolism

Volumn 5, Issue 1, 2010, Pages 19-28

  Devaraj, Sridevi ^a   Dasu, Mohan R ^a   Jialal, Ishwarlal ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Atherosclerosis; C reactive protein; Diabetes; Inflammation; Toll like receptor

Indexed keywords

C REACTIVE PROTEIN; CD40 ANTIGEN; CD40 LIGAND; CHEMOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 6; PLASMINOGEN ACTIVATOR INHIBITOR 1; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ABDOMINAL OBESITY; ADIPOSE TISSUE; ATHEROGENESIS; ATHEROSCLEROSIS; CELL ADHESION; CHEMOTAXIS; CYTOKINE RELEASE; DIABETES MELLITUS; DIABETIC ANGIOPATHY; DIABETOGENESIS; DISEASE ACTIVITY; ENDOTHELIUM; HUMAN; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; MONOCYTE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; RISK FACTOR;

EID: 77949777124     PISSN: 17446651     EISSN: None     Source Type: Journal    
DOI: 10.1586/eem.09.44     Document Type: Review

References (105)

1. American College of Endocrinology. American College of Endocrinology consensus statement on guidelines for glycemic control. Endocr. Pract. 8(Suppl. 1), 5-11 (2002).
2. Narayan KM, Boyle JP, Thompson TJ et al. Lifetime risk for diabetes mellitus in the United States. JAMA 290, 1884-1890 (2003).
3. Centers for Disease Control and Prevention. National Diabetes Fact Sheet: General Information and National Estimates on Diabetes in the United States, 2005. US Dept of Health and Human Services, GA, USA 2005.
4. DeFronzo RA, Ferrannini E. Insulin resistance. A multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease. Diabetes Care 14, 173-194 (1991).
5. Vaccaro O, Eberly LE, Neaton JD et al. Impact of diabetes and previous myocardial infarction on long-term survival: 25-year mortality follow-up of primary screenees of the Multiple Risk Factor Intervention Trial. Arch. Intern. Med. 164, 1438-1443 (2004).
6. Haffner SM, Lehto S, Ronnemaa T et al. Mortality from coronary heart disease in subjects with Type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N. Engl. J. Med. 339, 229-234 (1998).
7. Barrett-Connor EL, Cohn BA, Wingard DL, Edelstein SL. Why is diabetes mellitus a stronger risk factor for fatal ischemic heart disease in women than in men? The Rancho Bernardo Study. JAMA 265, 627-631 (1991).
8. Haffner SM, Lehto S, Ronnemaa T, Pyorala K, Laakso M. Mortality from coronary heart disease in subjects with Type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N. Engl. J. Med. 339, 229-234 (1998).
9. Kannel WB, McGee DL. Diabetes and cardiovascular disease. The Framingham study. JAMA 241, 2035-2038 (1979).
10. Stamler J, Vaccaro O, Neaton JD, Wentworth D. Diabetes, other risk factors, and 12-yr cardiovascular mortality for men screened in the Multiple Risk Factor Intervention Trial. Diabetes Care 16, 434-444 (1993).
11. Després JP, Lemieux I. Abdominal obesity and metabolic syndrome. Nature 444(7121), 881-887 (2006).
12. Packard RR, Libby P. Inflammation in atherosclerosis: from vascular biology to biomarker discovery and risk prediction. Clin. Chem. 54(1), 24-38 (2008).
13. Hansson GK, Libby P, Schönbeck U, Yan ZQ. Innate and adaptive immunity in the pathogenesis of atherosclerosis. Circ. Res. 91(4), 281-291 (2002).
14. Devaraj S, Singh U, Jialal I. The evolving role of C-reactive protein in atherothrombosis. Clin. Chem. 55(2), 229-238 (2009).
15. Ridker PM. C-reactive protein and the prediction of cardiovascular events among those at intermediate risk: moving an inflammatory hypothesis toward consensus. J. Am. Coll. Cardiol. 49(21), 2129-2138 (2007).
16. Pickup JC, Mattock MB, Chusney GD et al. NIDDM as a disease of the innate immune system - association of acute-phase reactants and interleukin-6 with metabolic syndrome. Diabetologia 40, 1286-2129 (1997).
17. Devaraj S, Jialal I. a tocopherol supplementation decreases serum C-reactive protein and monocyte interleukin-6 levels in normal volunteers and Type 2 diabetic patients. Free Radic. Biol. Med. 29(8), 790-792 (2000).
18. Ford ES. The metabolic syndrome and C-reactive protein, fibrinogen, and leukocyte count: findings from the Third National Health and Nutrition Examination. Surv. Atheroscler. 168(2), 351-358 (2003).
19. Tan KC, Chow WS, Tam SC et al. Atorvastatin lowers C-reactive protein and improves endothelium-dependent vasodilation in Type 2 diabetes mellitus. J. Clin. Endocrinol. Metab. 87(2), 563-568 (2002).
20. Jager A, van Hinsbergh VW, Kostense PJ et al. von Willebrand factor, C-reactive protein, and 5-year mortality in diabetic and nondiabetic subjects: the Hoorn Study. Arterioscler. Thromb. Vasc. Biol. 19(12), 3071-3078 (1999).
21. Devaraj S, Singh U, Jialal I. Human C-reactive protein and the metabolic syndrome. Curr. Opin. Lipidol. 20(3), 182-189 (2009).
22. Folsom AR, Aleksic N, Catellier D et al. C-reactive protein and incident coronary heart disease in the Atherosclerosis Risk In Communities (ARIC) study. Am. Heart J. 144(2), 233-238 (2002).
23. Tracy RP, Lemaitre RN, Psaty BM et al. Relationship of C-reactive protein to risk of cardiovascular disease in the elderly. Results from the Cardiovascular Health Study and the Rural Health Promotion Project. Arterioscler. Thromb. Vasc. Biol. 17(6), 1121-1127 (1997).
24. Bermudez EA, Rifai N, Buring J et al. Interrelationships among circulating interleukin-6, C-reactive protein, and traditional cardiovascular risk factors in women. Arterioscler. Thromb. Vasc. Biol. 22(10), 1668-1673 (2002).
25. Freeman DJ, Norrie J, Caslake MJ et al; West of Scotland Coronary Prevention Study. C-reactive protein is an independent predictor of risk for the development of diabetes in the West of Scotland Coronary Prevention Study. Diabetes 51(5), 1596-1600 (2002).
26. Thorand B, Lowel H, Schneider A et al. C-reactive protein as a predictor for incident diabetes mellitus among middle-aged men: results from the MONICA Augsburg cohort study, 1984-1998. Arch. Intern. Med. 163(1), 93-99 (2003).
27. Pradhan AD, Manson JE, Rifai N et al. C-reactive protein, interleukin 6, and risk of developing Type 2 diabetes mellitus. JAMA 286(3), 327-334 (2001).
28. Muntner P, He J, Chen J et al. Prevalence of non-traditional cardiovascular disease risk factors among persons with impaired fasting glucose, impaired glucose tolerance, diabetes, and the metabolic syndrome: analysis of the Third National Health and Nutrition Examination Survey (NHANES III). Ann. Epidemiol. 14(9), 686-695 (2004).
29. Hanley AJ, Festa A, DAgostino RB Jr et al. Metabolic and inflammation variable clusters and prediction of Type 2 diabetes: factor analysis using directly measured insulin sensitivity. Diabetes 53(7), 1773-1781 (2004).
30. Devaraj S, Glaser N, Griffen S et al. Increased monocytic activity and biomarkers of inflammation in patients with Type 1 diabetes. Diabetes 55(3), 774-779. (2006).
31. Schalkwijk CG, Poland DC, van Dijk W et al. Plasma concentration of C-reactive protein is increased in Type I diabetic patients without clinical macroangiopathy and correlates with markers of endothelial dysfunction: evidence for chronic inflammation. Diabetologia 42(3), 351-357 (1999).
32. Schram MT, Chaturvedi N, Schalkwijk CG, Fuller JH, Stehouwer CD; EURODIAB Prospective Complications Study Group. Markers of inflammation are cross-sectionally associated with microvascular complications and cardiovascular disease in Type 1 diabetes - the EURODIAB Prospective Complications Study. Diabetologia 48(2), 370-378 (2005).
33. Hayaishi-Okano R, Yamasaki Y, Katakami N et al. Elevated C-reactive protein associates with early-stage carotid atherosclerosis in young subjects with Type 1 diabetes. Diabetes Care 25(8), 1432-1438 (2002).
34. Moreno PR, Murcia AM, Palacios IF et al. Coronary composition and macrophage infiltration in atherectomy specimens from patients with diabetes mellitus. Circulation 102(18), 2180-2184 (2000).
35. Burke AP, Kolodgie FD, Zieske A et al. Morphologic findings of coronary atherosclerotic plaques in diabetics: a postmortem study. Arterioscler. Thromb. Vasc. Biol. 24(7), 1266-1271 (2004).
36. Rousselot DB, Bastard JP, Jaudon MC, Delattre J. Consequences of the diabetic status on the oxidant/antioxidant balance. Diabetes Metab. 26, 163-176 (2000).
37. Kitahara M, Eyre H, Lynch R et al. Metabolic activity of diabetic monocytes. Diabetes 29, 251-256 (1980).
38. Hill H, Hogan N, Rallison M et al. Functional and metabolic abnormalities of diabetic monocytes. Adv. Expt. Med. Biol. 69, 621-627 (1980).
39. Devaraj S, Cheung AT, Jialal I et al. Evidence of increased inflammation and microcirculatory abnormalities in patients with Type 1 diabetes and their role in microvascular complications. Diabetes 56(11), 2790-2796 (2007).
40. Devaraj S, Glaser N, Griffen S et al. Increased monocytic activity and biomarkers of inflammation in patients with Type 1 diabetes. Diabetes 55(3), 774-779 (2006).
41. Fuller CJ, Agil A, Lender D, Jialal I. Superoxide production and LDL oxidation by diabetic neutrophils. J. Diabetes Complications 10(4), 206-210 (1996).
42. Devaraj S, Jialal I. Low-density lipoprotein postsecretory modification, monocyte function, and circulating adhesion molecules in Type 2 diabetic patients with and without macrovascular complications: the effect of a-tocopherol supplementation. Circulation 102(2), 191-196 (2000).
43. Larsen CM, Faulenbach M, Vaag A, Ehses JA, Donath MY, Mandrup-Poulsen T. Sustained effects of interleukin-1-receptor antagonist treatment in Type 2 diabetes mellitus. Diabetes Care 32(9), 1663-1668 (2009).
44. Desfaits A, Serri O, Renier G. Normalization of plasma lipid peroxides, monocyte adhesion and TNF production in NIDDM patients after gliclazide treatment. Diabetes Care 21, 487-491 (1998).
45. Ross R. Cell biology of atherosclerosis. Ann. Rev. Physiol. 57, 791-804 (1995).
46. Kim J, Berliner J, Natarajan R et al. Evidence that glucose increases monocyte binding to human aortic endothelial cells. Diabetes 43, 1103-1107 (1994).
47. Carantoni M, Abbasi F, Chu L et al. Adherence of mononuclear cells to endothelium in vitro is increased in patients with NIDDM. Diabetes Care 20, 1462-1465 (1997).
48. Hoogerbrugge N, Verkerk A, Jacobs M et al. Hypertriglyceridemia enhances monocyte binding to endothelial cells in NIDDM. Diabetes Care 3, 1122-1124 (1997).
49. Hwang S, Ballantyne CM, Sharrett AR et al. Circulating adhesion molecules VCAM-1-1, ICAM-1-1, and E-selectin in carotid atherosclerosis and incident coronary heart disease cases: the Atherosclerosis Risk In Communities (ARIC) Study. Circulation 96, 4219-4225 (1997).
50. Rohde LE, Lee RT, Jamocochian M et al. Circulating CAMs are correlated with ultrasound measurement of carotid atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 18, 1765-1770 (1998).
51. Ridker PM, Hennekens CH, Roitman JB et al. Plasma concentration of soluble ICAM-1 and risks of future MI in apparently healthy men. Lancet 351, 88-92 (1998).
52. Albertini JP, Valensi P, Lormeau B et al. Elevated concentrations of soluble E-selectin and vascular cell adhesion molecule-1 in NIDDM. Effect of intensive insulin treatment. Diabetes Care 21,1008-1013 (1998).
53. Fasching P, Waldhausl W, Wagner OF. Elevated circulating adhesion molecules in NIDDM-potential mediators in diabetic macroangiopathy. Diabetologia 39, 1242-1244 (1996).
54. Matsumoto K, Sera Y, Abe Y et al. Serum concentrations of soluble vascular cell adhesion molecule-1 and E-selectin are elevated in insulin-resistant patients with Type 2 diabetes. Diabetes Care 24, 1697-1698 (2001).
55. Mocco J, Choudhri TF, Mack WJ et al. Elevation of soluble intercellular adhesion molecule-1 levels in symptomatic and asymptomatic carotid atherosclerosis. Neurosurgery 48, 718-721 (2001).
56. Kulseng B, Vatten L, Espevik T. Soluble tumor necrosis factor receptors in sera from patients with insulin-dependent diabetes mellitus: relations to duration and complications of disease. Acta Diabetol. 36(1-2), 99-105 (1999).
57. Ghosh S, Hayden MS. New regulators of NF-kB in inflammation. Nat. Rev. Immunol. 8(11), 837-848 (2008).
58. Sarkar FH, Li Y, Wang Z, Kong D. NF-kB signaling pathway and its therapeutic implications in human diseases. Int. Rev. Immunol. 27(5), 293-319 (2008).
59. Srivastava SK, Ramana KV. Focus on molecules: nuclear factor-kB. Exp. Eye Res. 88(1), 2-3 (2009).
60. Hofmann MA, Schiekofer S, Isermann B et al. Peripheral blood mononuclear cells isolated from patients with diabetic nephropathy show increased activation of the oxidative-stress sensitive transcription factor NF-kB. Diabetologia 42(2), 222-232 (1999).
61. Sebestjen M, Zegura B, Guzic-Salobir B et al. Fibrinolytic parameters and insulin resistance in young survivors of myocardial infarction with heterozygous familial hypercholesterolemia. Wien Klin. Wochenschr. 113(3-4), 113-118 (2001).
62. Wiman B, Andersson T, Hallqvist J et al. Plasma levels of tissue plasminogen activator/ plasminogen activator inhibitor-1 complex and von Willebrand factor are significant risk markers for recurrent myocardial infarction in the Stockholm Heart Epidemiology Program (SHEEP) study. Arterioscler. Thromb. Vasc. Biol. 20(8), 2019-2023 (2000).
63. Eren M, Painter CA, Atkinson JB et al. Age-dependent spontaneous coronary arterial thrombosis in transgenic mice that express a stable form of human plasminogen activator inhibitor-1. Circulation 106, 491-496 (2002).
64. Schafer K, Muller K, Hecke A et al. Enhanced thrombosis in atherosclerosisprone mice is associated with increased arterial expression of plasminogen activator inhibitor-1. Arterioscler. Thromb. Vasc. Biol. 23(11), 2097-2103 (2003).
65. Eitzman DT, Westrick RJ, Xu Z et al. PAI-1 deficiency protects against atherosclerosis progression in the mouse carotid artery. Blood 96, 4212-4215 (2000).
66. Xiao Q, Danton MJ, Witte DP et al. Plasminogen deficiency accelerates vessel wall disease in mice predisposed to atherosclerosis. Proc. Natl Acad. Sci. USA 94(19), 10335-10340 (1997).
67. Fujii S, Goto D, Zaman T et al. Diminished fibrinolysis and thrombosis: clinical implications for accelerated atherosclerosis. J. Atheroscler. Thromb. 5(2), 76-81 (1998).
68. Alessi MC, Juhan-Vague I. Contribution of PAI-1 in cardiovascular pathology. Arch. Mal. Coeur. Vaiss. 97(6), 673-678 (2004).
69. Festa A, DAgostino R Jr, Mykkanen L et al. Relative contribution of insulin and its precursors to fibrinogen and PAI-1 in a large population with different states of glucose tolerance. The Insulin Resistance Atherosclerosis Study (IRAS). Arterioscler. Thromb. Vasc. Biol. 19(3), 562-568 (1999).
70. Li H, Sun B. Toll-like receptor 4 in atherosclerosis. J. Cell. Mol. Med. 11(1), 88-95 (2007).
71. Trinchieri G, Sher A. Cooperation of Toll-like receptor signals in innate immune defence. Nat. Rev. Immunol. 7(3), 179-190 (2007).
72. Stoll LL, Denning GM, Weintraub NL. Endotoxin, TLR4 signaling and vascular inflammation: potential therapeutic targets in cardiovascular disease. Curr. Pharm. Des. 12(32), 4229-4245 (2006).
73. Uematsu S, Akira S. Toll-like receptors and innate immunity. J. Mol. Med. 84(9), 712-725 (2006).
74. Mullick AE, Tobias PS, Curtiss LK. Toll-like receptors and atherosclerosis: key contributors in disease and health? Immunol. Res. 34(3), 193-209 (2006).
75. Takeda K, Akira S. Roles of Toll-like receptors in innate immune responses. Genes Cells 6(9), 733-742 (2001).
76. Liu X, Ukai T, Yumoto H et al. Toll-like receptor 2 plays a critical role in the progression of atherosclerosis that is independent of dietary lipids. Atherosclerosis 196(1), 146-154 (2009).
77. Mullick AE, Tobias PS, Curtiss LK. Modulation of atherosclerosis in mice by Toll-like receptor 2. J. Clin. Invest. 115(11), 3149-3156 (2005).
78. Bjorkbacka H, Kunjathoor VV, Moore KJ et al. Reduced atherosclerosis in MyD88- null mice links elevated serum cholesterol levels to activation of innate immunity signaling pathways. Nat. Med. 10(4), 416-421 (2004).
79. Song MJ, Kim KH, Yoon JM, Kim JB. Activation of Toll-like receptor 4 is associated with insulin resistance in adipocytes. Biochem. Biophys. Res. Commun. 346(3), 739-745 (2006).
80. Mohammad MK, Morran M, Slotterbeck B et al. Dysregulated Toll-like receptor expression and signaling in bone marrow-derived macrophages at the onset of diabetes in the non-obese diabetic mouse. Int. Immunol. 18(7), 1101-1113 (2006).
81. Kim HS, Han MS, Chung KW et al. Toll-like receptor 2 senses b-cell death and contributes to the initiation of autoimmune diabetes. Immunity 27(2), 321-323 (2007).
82. Wen L, Peng J, Li Z, Wong FS. The effect of innate immunity on autoimmune diabetes and the expression of Toll-like receptors on pancreatic islets. J. Immunol. 172(5), 3173-3180 (2004).
83. Park Y, Park S, Yoo E, Kim D, Shin H. Association of the polymorphism for Toll-like receptor 2 with Type 1 diabetes susceptibility. Ann. NY Acad. Sci. 1037, 170-174 (2004).
84. 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. 292(3), E740-E774 (2007).
85. Devaraj S, Dasu MR, Rockwood J et al. Increased Toll-like receptor (TLR) 2 and TLR4 expression in monocytes from patients with Type 1 diabetes: further evidence of a proinflammatory state. J. Clin. Endocrinol. Metab. 93(2), 578-583 (2008).
86. Devaraj S, Dasu MR, Park SH, Jialal I. Increased levels of ligands of Toll-like receptors 2 and 4 in Type 1 diabetes. Diabetologia 52(8), 1665-1668 (2009).
87. Schonbeck U, Libby P. CD40 signaling and plaque instability. Circ. Res. 89(12), 1092-1103 (2001).
88. Schonbeck U, Libby P. The CD40/CD154 receptor/ligand dyad. Cell. Mol. Life Sci. 58(1), 4-43 (2001).
89. Mach F, Schonbeck U, Libby P. CD40 signaling in vascular cells: a key role in atherosclerosis? Atherosclerosis 137, S89-S95 (1998).
90. Varo N, de Lemos JA, Libby P et al. Soluble CD40L: risk prediction after acute coronary syndromes. Circulation 108(9), 1049-1052 (2003)
91. Varo N, Vicent D, Libby P et al. Elevated plasma levels of the atherogenic mediator soluble CD40 ligand in diabetic patients: a novel target of thiazolidinediones. Circulation 107(21), 2664-2669 (2003).
92. Lim HS, Blann AD, Lip GY. Soluble CD40 ligand, soluble P-selection, interleukin-6, and tissue factor in diabetes mellitus: relationships to cardiovascular disease and risk factor intervention. Circulation 109(21), 2524-2528 (2004).
93. Jinchuan Y, Zonggui W, Jinming C et al. Upregulation of CD40-CD40 ligand system in patients with diabetes mellitus. Clin. Chim. Acta 339(1-2), 85-90 (2004).
94. Venugopal SK, Devaraj S, Yang T, Jialal I. a-tocopherol decreases superoxide anion release in human monocytes under hyperglycemic conditions via inhibition of protein kinase C-alpha. Diabetes 51(10), 3049-3055 (2002).
95. Dasu MR, Devaraj S, Jialal I. High glucose induces IL-1b expression in human monocytes: mechanistic insights. Am. J. Physiol. Endocrinol. Metab. 293(1), E337-E346 (2007)
96. Devaraj S, Venugopal SK, Singh U, Jialal I. Hyperglycemia induces monocytic release of interleukin-6 via induction of protein kinase C-a and -b. Diabetes 54(1), 85-89 (2005).
97. Shanmugam N, Reddy MA, Guha M, Natarajan R. High glucose-induced expression of proinflammatory cytokine and chemokine genes in monocytic cells. Diabetes 52(5), 1256-1264 (2003).
98. Srinivasan S, Bolick DT, Hatley ME et al. Glucose regulates interleukin-8 production in aortic endothelial cells through activation of the p38 mitogen-activated protein kinase pathway in diabetes. J. Biol. Chem. 279(30), 31930-31936 (2004).
99. Dasu MR, Devaraj S, Zhao L et al. High glucose induces Toll-like receptor expression in human monocytes: mechanism of activation. Diabetes 57(11), 3090-3098 (2008).
100. Devaraj S, Jialal I. Increased secretion of IP-10 from monocytes under hyperglycemia is via the TLR2 and TLR4 pathway. Cytokine 47(1), 6-10 (2009).
101. Zeyda M, Stulnig TM. Obesity, inflammation, and insulin resistance - a mini-review. Gerontology 55(4), 379-386 (2009).
102. Rasouli N, Kern PA. Adipocytokines and the metabolic complications of obesity. J. Clin. Endocrinol. Metab. 93(11 Suppl. 1), S64-S73 (2008).
103. Surmi BK, Hasty AH. Macrophage infiltration into adipose tissue: initiation, propagation and remodeling. Future Lipidol. 3(5), 545-556 (2008).
104. Greenfield JR, Samaras K, Jenkins AB et al. Obesity is an important determinant of baseline serum C-reactive protein concentration in monozygotic twins, independent of genetic influences. Circulation 109(24), 3022-3028 (2004).
105. Sam S, Haffner S, Davidson MH et al. Relation of abdominal fat depots to systemic markers of inflammation in Type 2 diabetes. Diabetes Care 32(5), 932-937 (2009).