Inflammation and immunity in diabetic vascular complications

Current Opinion in Lipidology

Volumn 19, Issue 5, 2008, Pages 519-524

  Nilsson, Jan ^a,b   Bengtsson, Eva ^a   Fredrikson, Gunilla Nordin ^a   Björkbacka, Harry ^a  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Advanced glycation endproducts; Atherosclerosis; Autoimmunity; Complications; Diabetes; Lipoproteins

Indexed keywords

ADVANCED GLYCATION END PRODUCT; C REACTIVE PROTEIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; OXIDIZED LOW DENSITY LIPOPROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ADAPTIVE IMMUNITY; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; AUTOIMMUNITY; CARDIOVASCULAR DISEASE; DIABETES MELLITUS; DIABETIC ANGIOPATHY; DISEASE ASSOCIATION; HUMAN; HUMAN CELL; IMMUNOPATHOLOGY; INFLAMMATION; INNATE IMMUNITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN MODIFICATION; REVIEW; VACCINE PRODUCTION;

ATHEROSCLEROSIS; DIABETIC ANGIOPATHIES; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; IMMUNITY; INFLAMMATION; MODELS, BIOLOGICAL;

ANIMALIA;

EID: 53549101280     PISSN: 09579672     EISSN: None     Source Type: Journal    
DOI: 10.1097/MOL.0b013e32830f47cd     Document Type: Review

References (60)

1. Daneman D. Type 1 diabetes. Lancet 2006; 367:847-858.
2. Beckman JA, Creager MA, Libby P. Diabetes and atherosclerosis: epidemiology, pathophysiology, and management. JAMA 2002; 287:2570-2581.
3. Goldberg IJ. Why does diabetes increase atherosclerosis? I don't know! J Clin Invest 2004; 114:613-615.
4. Clark CM Jr, Lee DA. Prevention and treatment of the complications of diabetes mellitus. N Engl J Med 1995; 332:1210-1217.
5. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 2005; 352:1685-1695.
6. Nilsson J, Hansson GK. Autoimmunity in atherosclerosis: a protective response losing control? J Intern Med 2008; 263:464-478.
7. Palinski W, Witztum JL. Immune responses to oxidative neoepitopes on LDL and phospholipids modulate the development of atherosclerosis. J Intern Med 2000; 247:371-380.
8. 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 1998; 339:229-234.
9. Jamrozik K, Broadhurst RJ, Forbes S, et al. Predictors of death and vascular events in the elderly: the Perth Community Stroke Study. Stroke 2000; 31:863-868.
10. Goldberg IJ, Dansky HM. Diabetic vascular disease: an experimental objective. Arterioscler Thromb Vase Biol 2006; 26:1693-1701.
11. Huang ES, Meigs JB, Singer DE. The effect of interventions to prevent cardiovascular disease in patients with type 2 diabetes mellitus. Am J Med 2001; 111:633-642.
12. Krauss RM. Lipids and lipoproteins in patients with type 2 diabetes. Diabetes Care 2004; 27:1496-1504.
13. Park L, Raman KG, Lee KJ, et al. Suppression of accelerated diabetic atherosclerosis by the soluble receptor for advanced glycation endproducts. Nat Med 1998; 4:1025-1031.
14. Calkin AC, Forbes JM, Smith CM, et al. Rosiglitazone attenuates atherosclerosis in a model of insulin insufficiency independent of its metabolic effects. Arterioscler Thromb Vase Biol 2005; 25:1903-1909.
15. Wu KK, Wu TJ, Chin J, et al. Increased hypercholesterolemia and atherosclerosis in mice lacking both ApoE and leptin receptor. Atherosclerosis 2005; 181:251-259.
16. Gruen ML, Saraswathi V, Nuotio-Antar AM, et al. Plasma insulin levels predict atherosclerotic lesion burden in obese hyperlipidemic mice. Atherosclerosis 2006; 186:54-64.
17. Hsueh W, Abel ED, Breslow JL, et al. Recipes for creating animal models of diabetic cardiovascular disease. Circ Res 2007; 100:1415-1427.
18. Kanter JE, Johansson F, LeBoeuf RC, Bornfeldt KE. Do glucose and lipids exert independent effects on atherosclerotic lesion initiation or progression to advanced plaques? Circ Res 2007; 100:769-781. Reports the development of animal models that makes it possible to distinguish between the roles of hypercholesterolemia and hyperglycemia in the development of diabetic macrovascular complications.
19. Renard CB, Kramer F, Johansson F, et al. Diabetes and diabetes-associated lipid abnormalities have distinct effects on initiation and progression of atherosclerotic lesions. J Clin Invest 2004; 114:659-668.
20. Jovinge S, Hamsten A, Tornvall P, et al. Evidence for a role of tumor necrosis factor alpha in disturbances of triglyceride and glucose metabolism predisposing to coronary heart disease. Metabolism 1998; 47:113-118.
21. Ridker PM, Buring JE, Cook NR, Rifai N. C-reactive protein, the metabolic syndrome, and risk of incident cardiovascular events: an 8-year follow-up of 14 719 initially healthy American women. Circulation 2003; 107:391-397.
22. Fredrikson GN, Hedblad B, Nilsson JA, et al. Association between diet, lifestyle, metabolic cardiovascular risk factors, and plasma C-reactive protein levels. Metabolism 2004; 53:1436-1442.
23. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes 2005; 54:1615-1625.
24. Nilsson J, Nilsson LM, Chen YW, et al. High glucose activates nuclear factor of activated T cells in native vascular smooth muscle. Arterioscler Thromb Vasc Biol 2006; 26:794-800. Demonstrates for the first time a novel pathway for glucose-induced activation of transcription in intact vessels as well as the involvement of extracellular nucleotides in this process.
25. Ceradini DJ, Yao D, Grogan RH, et al. Decreasing intracellular superoxide corrects defective ischemia-induced new vessel formation in diabetic mice. J Biol Chem 2008; 283:10930-10938. The results provide a basis for the rational design of new therapeutics to normalize impaired ischemia-induced vasculaogenesis in diabetes.
26. Berliner J, Navab M, Fogelman A, et al. Atherosclerosis: basic mechanisms. Oxidation, inflammation and genetics. J Clin Invest 1995; 91:2488-2496.
27. Hörkkö S, Binder CJ, Shaw PX, et al. Immunological responses to oxidized LDL. Free Radic Biol Med 2000; 28:1771-1779.
28. Olofsson KE, Andersson L, Nilsson J, Bjorkbacka H. Nanomolar concentrations of lysophosphatidylcholine recruit monocytes and induce pro-inflammatory cytokine production in macrophages. Biochem Biophys Res Commun 2008; 370:348-352. Lysophosphatidylcholine is released by oxidized LDL and can activate macrophages in nanomalar concentrations demonstrating one pathway through which LDL oxidation is proinflammatory.
29. Febbraio M, Podrez EA, Smith JD, et al. Targeted disruption of the class B scavenger receptor CD36 protects against atherosclerotic lesion development in mice. J Clin Invest 2000; 105:1049-1056.
30. Suzuki H, Kurihara Y, Takeya M, et al. A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection. Nature 1997; 386:292-296.
31. Moore KJ, Kunjathoor VV, Koehn SL, et al. Loss of receptor-mediated lipid uptake via scavenger receptor A or CD36 pathways does not ameliorate atherosclerosis in hyperlipidemic mice. J Clin Invest 2005; 115:2192-2201.
32. 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 2004; 10:416-421.
33. Michelsen KS, Wong MH, Shah PK, et al. Lack of Toll-like receptor 4 or myeloid differentiation factor 88 reduces atherosclerosis and alters plaque phenotype in mice deficient in apolipoprotein E. Proc Natl Acad Sci U S A 2004; 101:10679-10684.
34. Mullick AE, Tobias PS, Curtiss LK. Modulation of atherosclerosis in mice by Toll-like receptor 2. J Clin Invest 2005; 115:3149-3156.
35. Shi H, Kokoeva MV, Inouye K, et al. TLR4 links innate immunity and fatty acidinduced insulin resistance. J Clin Invest 2006; 116:3015-3025.
36. Poggi M, Bastelica D, Gual P, et al. C3H/HeJ mice carrying a toll-like receptor 4 mutation are protected against the development of insulin resistance in white adipose tissue in response to a high-fat diet. Diabetologia 2007; 50:1267-1276. This interesting study demonstrates that TLR4 influences white adipose tissue inflammation and insulin sensitivity in response to a high-fat diet.
37. Kim F, Pham M, Luttrell I, et al. Toll-like receptor-4 mediates vascular inflammation and insulin resistance in diet-induced obesity. Circ Res 2007; 100:1589-1596. The TLR4 signaling pathway is identified as a key mediator of the deleterious effects of fatty acids on endothelial nitric oxide signaling.
38. 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 2008; 93:578-583.
39. Methe H, Kim JO, Kofler S, e al. Expansion of circulating Toll-like receptor 4-positive monocytes in patients with acute coronary syndrome. Circulation 2005; 111:2654-2661.
40. Kim HS, Han MS, Chung KW, et al. Toil-like receptor 2 senses beta-cell death and contributes to the initiation of autoimmune diabetes. Immunity 2007; 27:321-333.
41. Binder CJ, Chang MK, Shaw PX, et al. Innate and acquired immunity in atherogenesis. Nat Med 2002; 8:1218-1226.
42. Hansson GK, Libby P, Schonbeck U, Yan ZQ. Innate and adaptive immunity in the pathogenesis of atherosclerosis. Circ Res 2002; 91:281-291.
43. Jonasson L, Holm J, Skalli O, et al. Expression of class II transplantation antigen on vascular smooth muscle cells in human atherosclerosis. J Clin Invest 1985; 76:125-131.
44. Zhou X, Nicoletti A, Elhage R, Hansson GK. Transfer of CD4(+) T cells aggravates atherosclerosis in immunodeficient apolipoprotein E knockout mice. Circulation 2000; 102:2919-2922.
45. Schulte S, Sukhova GK, Libby P. Genetically programmed biases in Th1 and th2 immune responses modulate atherogenesis. Am J Pathol 2008; 172:1500-1508. Although several previous studies have identified distinct components of Th1 immune responses as proatherogenic, this is the first study that systematically evaluates the disease process in Th1 compared with Th2 prone animals.
46. Glass CK, Witztum JL Atherosclerosis: the road ahead. Cell 2001; 104:503-516.
47. Palinski W, Miller E, Witztum JL. Immunization of low density lipoprotein (LDL) receptor-deficient rabbits with homologous malondialdehyde modified LDL reduces atherogenesis. Proc Natl Acad Sci U S A 1995; 92:821-825.
48. Ameli S, Hultgardh-Nilsson A, Regnstrom J, et al. Effect of immunization with homologous LDL and oxidized LDL on early atherosclerosis in hypercholesterolemic rabbits. Arterioscler Thromb Vase Biol 1996; 16:1074-1079.
49. Angeli V, Llodra J, Rong JX, et al. Dyslipidemia associated with atherosclerotic disease systemically alters dendritic cell mobilization. Immunity 2004; 21:561-574.
50. Schiopu A, Bengtsson J, Soderberg I, et al. Recombinant human antibodies against aldehyde-modified apolipoprotein B-100 peptide sequences inhibit atherosclerosis. Circulation 2004; 110:2047-2052.
51. Schiopu A, Frendeus B, Jansson B, et al. Recombinant antibodies to an oxidized low-density lipoprotein epitope induce rapid regression of atherosclerosis in apobec-1 (-/-)flow-density lipoprotein receptorf-/-) mice. J Am Coll Cardiol 2007; 50:2313-2318. The first study to demonstrate that oxidized LDL-specific antibodies can induce regression of pre-existing atherosclerotic plaques. As the antibodies used are human, these results also support the notion that this type of treatment is feasable in humans.
52. Shah PK, Chyu KY, Fredrikson GN, Nilsson J. Immunomodulation of atherosclerosis with a vaccine. Nat Clin Pract Cardiovasc Med 2005; 2:639-646.
53. Thornalley PJ, Langborg A, Minnas HS. Formation of gfyoxat, methylglyoxal and 3-deoxyglucosone in the glycation of proteins by glucose. Biochem J 1999; 344 (Pt 1):109-116.
54. Araki N, Ueno N, Chakrabarti B, et al. Immunochemical evidence for the presence of advanced glycation end products in human lens proteins and its positive correlation with aging. J Biol Chem 1992; 267:10211-10214.
55. Beisswenger PJ, Makrta Z, Curphey TJ, et al. Formation of immunochemical advanced grycosylation end products precedes and correlates with early manifestations of renal and retinal disease in diabetes. Diabetes 1995; 44:824-829.
56. Hammes HP, Brownlee M, Lin J, et al. Diabetic retinopathy risk correlates with intracellular concentrations of the glycoxidation product Nepsilon- (carboxymethyl) lysine independently of glycohaemoglobin concentrations. Diabetologia 1999; 42:603-607.
57. Sakata N, Imanaga Y, Meng J, et al. Immunohistochemical localization of different epitopes of advanced glycation end products in human atherosclerotic lesions. Atherosclerosis 1998; 141:61-75.
58. Vay D, Vidali M, Allochis G, et al. Antibodies against advanced glycation end product Nepsilon-(carboxymethyl)lysine in healthy controls and diabetic patients. Diabetologia 2000; 43:1385-1388.
59. Turk Z, Ljubic S, Turk N, Benko B. Detection of autoantibodies against advanced glycation endproducts and AGE-immune complexes in serum of patients with diabetes mellitus. Clin Chim Acta 2001; 303:105-115.
60. Ge J, Jia Q, Liang C, et al. Advanced glycosylation end products might promote atherosclerosis through inducing the immune maturation of dendritic ceHs. Arterioscler Thromb Vasc Biol 2005; 25:2157-2163.