Cytokine and cytokine-like inflammation markers, endothelial dysfunction, and imbalanced coagulation in development of diabetes and its complications

Journal of Clinical Endocrinology and Metabolism

Volumn 94, Issue 9, 2009, Pages 3171-3182

  Goldberg, Ronald B ^a,b  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b Department of Medicine ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTOKINE; ADIPONECTIN; ANTIDIABETIC AGENT; BIOLOGICAL MARKER; C REACTIVE PROTEIN; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; FIBRINOGEN; GLITAZONE DERIVATIVE; INSULIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; METFORMIN; PADGEM PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA ANTAGONIST; PLASMINOGEN ACTIVATOR INHIBITOR 1; REPAGLINIDE; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; VON WILLEBRAND FACTOR;

ADIPOSE TISSUE; ATHEROSCLEROSIS; BLOOD CLOTTING DISORDER; CARDIOVASCULAR DISEASE; COMORBIDITY; DIABETES CONTROL; DIABETIC MICROANGIOPATHY; DIABETIC NEPHROPATHY; DIABETIC NEUROPATHY; DIABETIC RETINOPATHY; DRUG MECHANISM; DYSLIPIDEMIA; ENDOTHELIAL DYSFUNCTION; HUMAN; HYPERGLYCEMIA; HYPERTENSION; IMPAIRED GLUCOSE TOLERANCE; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RESISTANCE; LIFESTYLE MODIFICATION; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; OVARY POLYCYSTIC DISEASE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW;

EID: 69949093803     PISSN: 0021972X     EISSN: 0021972X     Source Type: Journal    
DOI: 10.1210/jc.2008-2534     Document Type: Article

References (137)

1. Ballantyne CM, Nambi V 2005 Markers of inflammation and their clinical significance. Atheroscler Suppl 6:21-29 (Review) (Pubitemid 40501306)
2. Cardozo AK, Kruhøffer M, Leeman R, Orntoft T, Eizirik DL 2001 Identification of novel cytokine-induced genes in pancreatic β-cells by high-density oligonucleotide arrays. Diabetes 50:909-920 (Pubitemid 32374519)
3. Christiansen T, Richelsen B, Bruun JM 2005 Monocyte chemoattractant protein-1 is produced in isolated adipocytes, associated with adiposity and reduced after weight loss in morbid obese subjects. Int J Obes (Lond) 29:146-150 (Pubitemid 40065478)
4. Libby P 2002 Inflammation in atherosclerosis. Nature 420:868-874
5. Ehses JA, Böni-Schnetzler M, Faulenbach M, Donath MY 2008 Macrophages, cytokines and beta-cell death in type 2 diabetes. Biochem Soc Trans 36(Pt 3):340-342 (Pubitemid 351839327)
6. Griendling KK, FitzGerald GA 2003 Oxidative stress and cardiovascular injury: part I: basic mechanisms and in vivo monitoring of ROS. Circulation 108:1912-1916
7. Ceriello A, Motz E 2004 Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler Thromb Vasc Biol 24:816-823 (Pubitemid 38620857)
8. Papanicolaou DA, Vgontzas AN 2000 Interleukin-6: the endocrine cytokine. J Clin Endocrinol Metab 85:1331-1333
9. Libby P, Ridker PM 2004 Inflammation and atherosclerosis: role of C-reactive protein in risk assessment. Am J Med 116(Suppl 6A): 9S-16S (Pubitemid 38402010)
10. Rajala MW, Scherer PE 2003 Minireview: the adipocyte - at the crossroads of energy homeostasis, inflammation, and atherosclerosis. Endocrinology 144:3765-3773
11. Suganami T, Nishida J, Ogawa Y 2005 A paracrine loop between adipocytes and macrophages aggravates inflammatory changes. Role of free fatty acids and tumor necrosis factor α. Arterioscler Thromb Vasc Biol 25:2062-2068
12. Berg AH, Combs TP, Du X, Brownlee M, Scherer PE 2001 The adipocyte-secreted protein Acrp30 enhances hepatic insulin action. Nat Med 7:947-953 (Pubitemid 32756433)
13. Ouchi N, Kihara S, Arita Y, Okamoto Y, Maeda K, Kuriyama H, Hotta K, Nishida M, Takahashi M, Muraguchi M, Ohmoto Y, Nakamura T, Yamashita S, Funahashi T, Matsuzawa Y 2000 Adiponectin, adipocyte-derived plasma protein, inhibits endothelial NF-κB signaling through cAMP-dependent pathway. Circulation 102:1296-1301 (Pubitemid 30728130)
14. Rakatzi I, Mueller H, Ritzeler O, Tennagels N, Eckel J 2004 Adiponectin counteracts cytokine- and fatty acid-induced apoptosis in the pancreatic β-cell line INS-1. Diabetologia 47:249-258 (Pubitemid 38315361)
15. Matsuzawa Y 2005 Adiponectin: Identification, physiology and clinical relevance in metabolic and vascular disease. Atheroscler Suppl 6:7-14 (Pubitemid 40501304)
16. Toso C, Emamaullee A, Merani S, Sapiro AMJ 2008 The role of macrophage migration inhibition factor on glucose metabolism and diabetes. Diabetologia 51:1937-1946
17. Nicoletti F, Conget I, Di Marco R, Speciale AM, Morìnigo R, Bendtzen K, Gomis R 2001 Serum levels of the interferon-γ-inducing cytokine interleukin-18 are increased in individuals at high risk of developing type I diabetes. Diabetologia 44:309-311 (Pubitemid 32234456)
18. Nicoletti F, Conget I, Di Mauro M, Di Marco R, Mazzarino MC, Bendtzen K, Messina A, Gomis R 2002 Serum concentrations of the interferon-γ-inducible chemokine IP-10/CXCL10 are augmented in both newly diagnosed type I diabetes mellitus patients and subjects at risk of developing the disease. Diabetologia 45:1107-1110 (Pubitemid 34985286)
19. Hanifi-Moghaddam P, Kappler S, Seissler J, Müller-Scholze S, Martin S, Roep BO, Strassburger K, Kolb H, Schloot NC 2006 Altered chemokine levels in individuals at risk of type 1 diabetes mellitus. Diabet Med 23:156-163
20. Chase HP, Cooper S, Osberg I, Stene LC, Barriga K, Norris J, Eisenbarth GS, Rewers M 2004 Elevated C-reactive protein levels in the development of type 1 diabetes. Diabetes 53:2569-2573 (Pubitemid 39299263)
21. Pickup JC, Mattock MB, Chusney GD, Burt D 1997 NIDDM as a disease of the innate immune system: association of acute-phase reactants and interleukin-6 with metabolic syndrome X. Diabetologia 40:1286-1292 (Pubitemid 27469668)
22. Shoelson SE, Lee J, Goldfine AB 2006 Inflammation and insulin resistance. J Clin Invest 116:1793-1801
23. Varma V, Yao-Borengasser A, Rasouli N, Nolen GT, Phanavanh B, Starks T, Gurley CM, Simpson PM, McGehee Jr RE, Kern PA, Peterson CA 2009 Muscle inflammatory response and insulin resistance: synergistic interaction between macrophages and fatty acids leads to impaired insulin action. Am J Physiol Endocrinol Metab 296:E1300-E1310
24. Schmidt MI, Duncan BB, Sharrett AR, Lindberg G, Savage PJ, Offenbacher S, Azambuja MI, Tracy RP, Heiss G 1999 Markers of inflammation and prediction of diabetes mellitus in adults (Atherosclerosis Risk in Communities study): a cohort study. Lancet 353:1649-1652 (Pubitemid 29224520)
25. Duncan BB, Schmidt MI, Offenbacher S, Wu KK, Savage PJ, Heiss G 1999 Factor VIII and other hemostasis variables are related to incident diabetes in adults. The Atherosclerosis Risk in Communities (ARIC) Study. Diabetes Care 22:767-772
26. Festa A, D'Agostino Jr R, Tracy RP, Haffner SM; Insulin Resistance Atherosclerosis Study 2002 Elevated levels of acute-phase proteins andplasminogenactivator inhibitor-1 predict thedevelopmentof type 2 diabetes: the insulin resistance atherosclerosis study. Diabetes 51:1131-1137 (Pubitemid 34438360)
27. Liu S, Tinker L, Song Y, Rifai N, Bonds DE, Cook NR, Heiss G, Howard BV, Hotamisligil GS, Hu FB, Kuller LH, Manson JE 2007 A prospective study of inflammatory cytokines and diabetes mellitus in a multiethnic cohort of postmenopausal women. Arch Intern Med 167:1676-1685 (Pubitemid 47280350)
28. Eliasson MC, Jansson JH, Lindahl B, Stegmayr B 2003 High levels of tissue plasminogen activator (tPA) antigen precede the development of type 2 diabetes in a longitudinal population study. The Northern Sweden MONICA study. Cardiovasc Diabetol 2:19 (Pubitemid 38751094)
29. Meigs JB, O'Donnell CJ, Tofler GH, Benjamin EJ, Fox CS, Lipinska I, Nathan DM, Sullivan LM, D'Agostino RB, Wilson PW 2006 Hemostatic markers of endothelial dysfunction and risk of incident type 2 diabetes: the Framingham Offspring Study. Diabetes 55:530-537 (Pubitemid 43343286)
30. Festa A, Williams K, Tracy RP, Wagenknecht LE, Haffner SM 2006 Progression of plasminogen activator inhibitor-1 and fibrinogen levels in relation to incident type 2 diabetes. Circulation. 113:1753-1759 (Pubitemid 43958468)
31. Lee CC, Adler AI, Sandhu MS, Sharp SJ, Forouhi NG, Erqou S, Luben R, Bingham S, Khaw KT, Wareham NJ 2009 Association of C-reactive protein with type 2 diabetes: prospective analysis and meta-analysis. Diabetologia 52:1040-1047
32. Herder C, Baumert J, Thorand B, Koenig W, de Jager W, Meisinger C, Illig T, Martin S, Kolb H 2006 Chemokines as risk factors for type 2 diabetes: results from the MONICA/KORA Augsburg study, 1984-2002. Diabetologia 49:921-929
33. Rosen P, Nawroth PP, King G, Moller W, Tritschler HJ, Packer L 2001 The role of oxidative stress in the onset and progression of diabetes and its complications: a summary of a Congress Series sponsored by UNESCO-MCBN, the American Diabetes Association and the German Diabetes Society. Diabetes Metab Res Rev 17:189-212 (Pubitemid 32624602)
34. Schwenke DC, D'Agostino Jr RB, Goff Jr DC, Karter AJ, Rewers MJ, Wagenknecht LE; Insulin Resistance Atherosclerosis Study 2003 Differences in LDL oxidizability by glycemic status: the insulin resistance atherosclerosis study. Diabetes Care 26:1449-1455 (Pubitemid 36929177)
35. Il'yasova D, Morrow JD, Wagenknecht LE 2005 Urinary F2-isoprostanes are not associated with increased risk of type 2 diabetes. Obes Res 13:1638-1644
36. Ceriello A, Mercuri F, Quagliaro L, Assaloni R, Motz E, Tonutti L, Taboga C 2001 Detection of nitrotyrosine in the diabetic plasma: evidence of oxidative stress. Diabetologia 44:834-838 (Pubitemid 32642455)
37. Bo S, Gambino R, Guidi S, Silli B, Gentile L, Cassader M, Pagano GF 2005 Plasma nitrotyrosine levels, antioxidant vitamins and hyperglycaemia. Diabet Med 22:1185-1189 (Pubitemid 41224178)
38. Meigs JB, Larson MG, Fox CS, Keaney Jr JF, Vasan RS, Benjamin EJ 2007 Association of oxidative stress, insulin resistance, and diabetes risk phenotypes: the Framingham Offspring Study. Diabetes Care 30:2529-2535
39. de Jager J, Dekker JM, Kooy A, Kostense PJ, Nijpels G, Heine RJ, Bouter LM, Stehouwer CD 2006 Endothelial dysfunction and low-grade inflammation explain much of the excess cardiovascular mortality in individuals with type 2 diabetes: the Hoorn Study. Arterioscler Thromb Vasc Biol 26:1086-1093 (Pubitemid 43732116)
40. Meigs JB, Hu FB, Rifai N, Manson JE 2004 Biomarkers of endothelial dysfunction and risk of type 2 diabetes mellitus. JAMA 291:1978-1986 (Pubitemid 38544279)
41. Lindsay RS, Funahashi T, Hanson RL, Matsuzawa Y, Tanaka S, Tataranni PA, Knowler WC, Krakoff J 2002 Adiponectin and development of type 2 diabetes in the Pima Indian population. Lancet 360:57-58 (Pubitemid 34756495)
42. Duncan BB, Schmidt MI, Pankow JS, Bang H, Couper D, Ballantyne CM, Hoogeveen RC, Heiss G 2004 Adiponectin and the development of type 2 diabetes: the atherosclerosis risk in communities study. Diabetes 53:2473-2478 (Pubitemid 39145606)
43. Snehalatha C, Mukesh B, Simon M, Viswanathan V, Haffner SM, Ramachandran A 2003 Plasma adiponectin is an independent predictor of type 2 diabetes in Asian Indians. Diabetes Care 26:3226-3229 (Pubitemid 37466879)
44. Mather KJ, Funahashi T, Matsuzawa Y, Edelstein S, Bray GA, Kahn SE, Crandall J, Marcovina S, Goldstein B, Goldberg R; Diabetes Prevention Program 2008 Adiponectin, change in adiponectin, and progression to diabetes in the Diabetes Prevention Program. Diabetes 57:980-986
45. Kanaya AM, Wassel Fyr C, Vittinghoff E, Harris TB, Park SW, Goodpaster BH, Tylavsky F, Cummings SR 2006 Adipocytokines and incident diabetes mellitus in older adults: the independent effect of plasminogen activator inhibitor 1. Arch Intern Med 166:350-356 (Pubitemid 43244324)
46. Hoo RL, Chow WS, Yau MH, Xu A, Tso AW, Tse HF, Fong CH, Tam S, Chan L, Lam KS 2007 Adiponectin mediates the suppressive effect of rosiglitazone on plasminogen activator inhibitor-1 production. Arterioscler Thromb Vasc Biol 27:2777-2782 (Pubitemid 350158936)
47. Hivert MF, Sullivan LM, Fox CS, Nathan DM, D'Agostino RB Sr, Wilson PW, Meigs JB 2008 Associations of adiponectin, resistin, and tumor necrosis factor-α with insulin resistance. J Clin Endocrinol Metab 93:3165-3172
48. Graham TE, Yang Q, Blüher M, Hammarstedt A, Ciaraldi TP, Henry RR, Wason CJ, Oberbach A, Jansson PA, Smith U, Kahn BB 2006 Retinol-binding protein 4 and insulin resistance in lean, obese, and diabetic subjects. N Engl J Med 354:2552-2563 (Pubitemid 43882351)
49. Silha JV, Nyomba BL, Leslie WD, Murphy LJ 2007 Ethnicity, insulin resistance, and inflammatory adipokines in women at high and low risk for vascular disease. Diabetes Care 30:286-291
50. Tso AW, Xu A, Sham PC, Wat NM, Wang Y, Fong CH, Cheung BM, Janus ED, Lam KS 2007 Serum adipocyte fatty acid binding protein as a new biomarker predicting the development of type 2 diabetes: a 10-year prospective study in a Chinese cohort. Diabetes Care 30:2667-2672 (Pubitemid 47547818)
51. Stefan N, Fritsche A, Weikert C, Boeing H, Joost HG, Häring HU, Schulze MB 2008 Plasma fetuin-A levels and the risk of type 2 diabetes. Diabetes 57:2762-2767
52. Fleischman A, Shoelson SE, Bernier R, Goldfine AB 2008 Salsalate improves glycemia and inflammatory parameters in obese young adults. Diabetes Care 31:289-294 (Pubitemid 351213338)
53. Goldfine AB, Silver R, Aldhahi W, Cai D, Tatro E, Lee J, Shoelson SE 2008 Use of salsalate to target inflammation in the treatment of insulin resistance and type 2 diabetes. Clin Transl Sci 1:36-43
54. Dandona P, Chaudhuri A, Ghanim H, Mohanty P 2007 Proinflammatory effects of glucose and anti-inflammatory effect of insulin: relevance to cardiovascular disease. Am J Cardiol 99:15B-26B (Pubitemid 46239948)
55. Lindmark S, Burén J, Eriksson JW 2006 Insulin resistance, endocrine function and adipokines in type 2 diabetes patients at different glycaemic levels: potential impact for glucotoxicity in vivo. Clin Endocrinol (Oxf) 65:301-309 (Pubitemid 44244919)
56. King DE, Mainous 3rd AG, Buchanan TA, Pearson WS 2003 Creactive protein and glycemic control in adults with diabetes. Diabetes Care 26:1535-1539 (Pubitemid 36929192)
57. Mantzoros CS, Li T, Manson JE, Meigs JB, Hu FB 2005 Circulating adiponectin levels are associated with better glycemic control, more favorable lipid profile, and reduced inflammation in women with type 2 diabetes. J Clin Endocrinol Metab 90:4542-4548 (Pubitemid 41159340)
58. Stentz FB, Umpierrez GE, Cuervo R, Kitabchi AE 2004 Proinflammatory cytokines, markers of cardiovascular risks, oxidative stress, and lipid peroxidation in patients with hyperglycemic crises. Diabetes 53:2079-2086 (Pubitemid 38970758)
59. Heliövaara MK, Teppo AM, Karonen SL, Tuominen JA, Ebeling P 2006 Improved glycaemia in type 1 diabetes results in decreased levels of soluble adhesion molecules with no change in serum adiponectin or most acute phase proteins. Exp Clin Endocrinol Diabetes 114:295-300 (Pubitemid 44166175)
60. Schulze MB, Rimm EB, Shai I, Rifai N, Hu FB 2004 Relationship between adiponectin and glycemic control, blood lipids, and inflammatory markers in men with type 2 diabetes. Diabetes Care 27:1680-1687 (Pubitemid 38857444)
61. Barnes MM, Curran-Everett D, Hamman RF, Maahs D, Mayer- Davis EJ, D'Agostino Jr RB, West N, Dabelea D 2008 Determinants of adiponectin levels in young people with type 1 diabetes. Diabet Med 25:365-369 (Pubitemid 351322711)
62. John S Yudkin, Stehouwer CDA, Emeis JJ, Coppack SW 1999 C-reactive protein in healthy subjects: associations with obesity, insulin resistance, and endothelial dysfunction: a potential role for cytokines originating from adipose tissue? Arterioscler Thromb Vasc Biol 19:972-978
63. Godsland IF, Crook D, Proudler AJ, Stevenson JC 2005 Hemostatic risk factors and insulin sensitivity, regional body fat distribution, and the metabolic syndrome. J Clin Endocrinol Metab 90:190-197 (Pubitemid 40116656)
64. Urakawa H, Katsuki A, Sumida Y, Gabazza EC, Murashima S, Morioka K, Maruyama N, Kitagawa N, Tanaka T, Hori Y, Nakatani K, Yano Y, Adachi Y 2003 Oxidative stress is associated with adiposity and insulin resistance in men. J Clin Endocrinol Metab 88:4673-4676 (Pubitemid 37357510)
65. Dandona P, Aljada A, Bandyopadhyay A 2004 Inflammation: the link between insulin resistance, obesity and diabetes Trends Immunol 25:4-7
66. Festa A, D'Agostino Jr R, Howard G, Mykkanen L, Tracy RP, Haffner SM 2000 Chronic subclinical inflammation as part of the insulin resistance syndrome: the Insulin Resistance Atherosclerosis Study (IRAS). Circulation 102:42-47 (Pubitemid 30430551)
67. The Diabetes Prevention Program Research Group 2005 Lipid, lipoproteins, C-reactive protein, and hemostatic factors at baseline in the diabetes prevention program. Diabetes Care 28:2472-2479
68. Natali A, Toschi E, Baldeweg S, Ciociaro D, Favilla S, Sacca L, Ferrannini E 2006 Clustering of insulin resistance with vascular dysfunction and low-grade inflammation in type 2 diabetes. Diabetes 55:1133-1140 (Pubitemid 44100192)
69. Hung J, McQuillan BM, Thompson PL, Beilby JP 2008 Circulating adiponectin levels associate with inflammatory markers, insulin resistance and metabolic syndrome independent of obesity. Int J Obes (Lond) 32:772-779 (Pubitemid 351670618)
70. van Oostrom AJ, van Wijk J, Cabezas MC 2004 Lipaemia, inflammation and atherosclerosis: novel opportunities in the understanding and treatment of atherosclerosis. Drugs 64(Suppl 2):19-41
71. Savoia C, Schiffrin EL 2006 Inflammation in hypertension. Curr Opin Nephrol Hypertens 15:152-158
72. Dietrich M, Jialal I 2005 The effect of weight loss on a stable biomarker of inflammation, C-reactive protein. Nutr Rev 63:22-28
73. Ziccardi P, Nappo F, Giugliano G, Esposito K, Marfella R, Cioffi M, D'Andrea F, Molinari AM, Giugliano D 2002 Reduction of inflammatory cytokine concentrations and improvement of endothelial functions in obese women after weight loss over one year. Circulation 105:804-809 (Pubitemid 34174919)
74. Plaisance EP, Grandjean PW 2006 Physical activity and high-sensitivity C-reactive protein. Sports Med 36:443-458
75. Esposito K, Marfella R, Ciotola M, Di Palo C, Giugliano F, Giugliano G, D'Armiento M, D'Andrea F, Giugliano D 2004 Effect of a Mediterranean-style diet on endothelial dysfunction and markers of vascular inflammation in the metabolic syndrome: a randomized trial. JAMA 292:1440-1446 (Pubitemid 39258336)
76. Roberts CK, Won D, Pruthi S, Lin SS, Barnard RJ 2006 Effect of a diet and exercise intervention on oxidative stress, inflammation and monocyte adhesion in diabetic men. Diabetes Res Clin Pract 73:249-259 (Pubitemid 44107591)
77. Pischon T, Girman CJ, Rifai N, Hotamisligil GS, Rimm EB 2005 Association between dietary factors and plasma adiponectin concentrations in men. Am J Clin Nutr 81:780-786 (Pubitemid 41724983)
78. Kasim-Karakas SE, Tsodikov A, Singh U, Jialal I 2006 Responses of inflammatory markers to a low-fat, high-carbohydrate diet: effects of energy intake. Am J Clin Nutr 83:774-779 (Pubitemid 44713139)
79. Haffner S, Temprosa M, Crandall J, Fowler S, Goldberg R, Horton E, Marcovina S, Mather K, Orchard T, Ratner R, Barrett-Connor E; Diabetes Prevention Program Research Group 2005 Intensive lifestyle intervention or metformin on inflammation and coagulation in participants with impaired glucose tolerance. Diabetes 54:1566-1572 (Pubitemid 40586691)
80. Hamalainen H, Ronnemaa T, Virtanen A, Lindstrom J, Eriksson JG, Valle TT, Ilanne-Parikka P, Keinanen-Kiukaanniemi S, Rastas M, Aunola S, Uusitupa M, Tuomilehto J; Finnish Diabetes Prevention Study Group 2005 Improved fibrinolysis by an intensive lifestyle intervention in subjects with impaired glucose tolerance. The Finnish Diabetes Prevention Study. Diabetologia 48:2248-2253
81. Nagi DK, Yudkin JS 1993 Effects of metformin on insulin resistance, risk factors for cardiovascular disease, and plasminogen activator inhibitor in NIDDM subjects. A study of two ethnic groups. Diabetes Care 16:621-629
82. Lund SS, Tarnow L, Stehouwer CD, Schalkwijk CG, Teerlink T, Gram J, Winther K, Frandsen M, Smidt UM, Pedersen O, Parving HH, Vaag AA 2008 Impact of metformin versus repaglinide on non-glycaemic cardiovascular risk markers related to inflammation and endothelial dysfunction in non-obese patients with type 2 diabetes. Eur J Endocrinol 158:631-641 (Pubitemid 351639600)
83. Caballero AE, Delgado A, Aguilar-Salinas CA, Herrera AN, Castillo JL, Cabrera T, Gomez-Perez FJ, Rull JA 2004 The differential effects of metformin on markers of endothelial activation and inflammation in subjects with impaired glucose tolerance: a placebo-controlled, randomized clinical trial. J Clin Endocrinol Metab 89:3943-3948 (Pubitemid 39071497)
84. Jensterle M, Sebestjen M, Janez A, Prezelj J, Kocjan T, Keber I, Pfeifer M 2008 Improvement of endothelial function with met-formin and rosiglitazone treatment in women with polycystic ovary syndrome. Eur J Endocrinol 159:399-406 (Pubitemid 351837367)
85. Reynolds K, Goldberg RB 2006 Thiazolidinediones: beyond glycemic control. Treat Endocrinol 5:25-36
86. Pfützner A, Marx N, Lübben G, Langenfeld M, Walcher D, Konrad T, Forst T 2005 Improvement of cardiovascular risk markers by pioglitazone is independent from glycemic control: results from the pioneer study. J Am Coll Cardiol 45:1925-1931 (Pubitemid 40814110)
87. Fonseca VA, Theuma P, Mudaliar S, Leissinger CA, Clejan S, Henry RR 2006 Diabetes treatments have differential effects on nontraditional cardiovascular risk factors. J Diabetes Complications 20:14-20 (Pubitemid 43028408)
88. Albertini JP, Valensi P, Lormeau B, Aurousseau MH, Ferrière F, Attali JR, Gattegno L 1998 Elevated concentrations of soluble E-selectin and vascular cell adhesion molecule-1 in NIDDM. Effect of intensive insulin treatment. Diabetes Care 21:1008-1013
89. Giugliano D, Ceriello A, Esposito K 2008 Glucose metabolism and hyperglycemia. Am J Clin Nutr 87:217S-222S
90. Landmesser U, Drexler H 2007 Endothelial function and hypertension. Curr Opin Cardiol 22:316-320
91. Orasanu G, Plutzky J 2009 The pathologic continuum of diabetic vascular disease. J Am Coll Cardiol 53(Suppl 5):S35-S42
92. Costa LA, Canani LH, Lisbôa HR, Tres GS, Gross JL 2004 Aggregation of features of the metabolic syndrome is associated with increased prevalence of chronic complications in type 2 diabetes. Diabet Med 21:252-255
93. De Block CE, De Leeuw IH, Van Gaal LF 2005 Impact of overweight on chronic microvascular complications in type 1 diabetic patients. Diabetes Care 28:1649-1655 (Pubitemid 41340904)
94. Kang ES, Kim HJ, Ahn CW, Park CW, Cha BS, Lim SK, Kim KR, Lee HC 2005 Relationship of serum high sensitivity C-reactive protein to metabolic syndrome and microvascular complications in type 2 diabetes. Diabetes Res Clin Pract 69:151-159 (Pubitemid 40943480)
95. Mora C, Navarro JF 2006 Inflammation and diabetic nephropathy. Curr Diab Rep 6:463-468
96. Targher G, Bertolini L, Zoppini G, Zenari L, Falezza G 2005 Increased plasma markers of inflammation and endothelial dysfunction and their association with microvascular complications in type 1 diabetic patients without clinically manifest macroangiopathy. Diabet Med 22:999-1004 (Pubitemid 41025995)
97. Matsumoto K, Sera Y, Ueki Y, Inukai G, Niiro E, Miyake S 2002 Comparison of serum concentrations of soluble adhesion molecules in diabetic microangiopathy and macroangiopathy. Diabet Med 19:822-826 (Pubitemid 35177180)
98. Lopes-Virella MF, Carter RE, Gilbert GE, Klein RL, Jaffa M, Jenkins AJ, Lyons TJ, Garvey WT, Virella G; Diabetes Control and Complications Trial/Epidemiology of Diabetes Intervention and Complications Cohort Study Group 2008 Risk factors related to inflammation and endothelial dysfunction in the DCCT/EDIC cohort and their relationship with nephropathy and macrovascular complications. Diabetes Care 31:2006-2012
99. Astrup AS, Tarnow L, Pietraszek L, Schalkwijk CG, Stehouwer CD, Parving HH, Rossing P 2008 Markers of endothelial dysfunction and inflammation in type 1 diabetic patients with or without diabetic nephropathy followed for 10 years: association with mortality and decline of glomerular filtration rate. Diabetes Care 31:1170-1176
100. Persson F, Rossing P, Hovind P, Stehouwer CD, Schalkwijk CG, Tarnow L, Parving HH 2008 Endothelial dysfunction and inflammation predict development of diabetic nephropathy in the Irbesartan in Patients with Type 2 Diabetes and Microalbuminuria (IRMA 2) study. Scand J Clin Lab Invest 68:731-738
101. Araki S, Haneda M, Koya D, Sugimoto T, Isshiki K, Chin-Kanasaki M, Uzu T, Kashiwagi A 2007 Predictive impact of elevated serum level of IL-18 for early renal dysfunction in type 2 diabetes: an observational follow-up study. Diabetologia 50:867-873 (Pubitemid 46355823)
102. Kamgar M, Nobakhthaghighi N, Shamshirsaz AA, Estacio RO, McFann KK, Schrier RW 2006 Impaired fibrinolytic activity in type II diabetes: correlation with urinary albumin excretion and progression of renal disease. Kidney Int 69:1899-1903 (Pubitemid 43739222)
103. Tesch GH 2008 MCP-1/CCL2: a new diagnostic marker and therapeutic target for progressive renal injury in diabetic nephropathy. Am J Physiol Renal Physiol 294:F697-F701
104. Hwang JS, Shin CH, Yang SW, Jung SY, Huh N 2005 Clinical implications of N ε-(carboxymethyl)lysine, advanced glycation end product, in children and adolescents with type 1 diabetes. Diabetes Obes Metab 7:263-267
105. Yenicesu M, Yilmaz MI, Caglar K, Sonmez A, Eyileten T, Kir T, Acikel C, Bingol N, Oguz Y, Ikizler TA, Vural A 2005 Adiponectin level is reduced and inversely correlated with the degree of proteinuria in type 2 diabetic patients. Clin Nephrol 64:12-19 (Pubitemid 40975060)
106. Lin J, Hu FB, Curhan G 2007 Serum adiponectin and renal dysfunction in men with type 2 diabetes. Diabetes Care 30:239-244 (Pubitemid 46198325)
107. Kato K, Osawa H, Ochi M, Kusunoki Y, Ebisui O, Ohno K, Ohashi J, Shimizu I, Fujii Y, Tanimoto M, Makino H 2008 Serum total and high molecular weight adiponectin levels are correlated with the severity of diabetic retinopathy and nephropathy. Clin Endocrinol (Oxf) 68:442-449 (Pubitemid 351257865)
108. Hadjadj S, Aubert R, Fumeron F, Pean F, Tichet J, Roussel R, Marre M; SURGENE Study Group; DESIR Study Group 2005 Increased plasma adiponectin concentrations are associated with microangiopathy in type 1 diabetic subjects. Diabetologia 48:1088-1092 (Pubitemid 40909643)
109. Briley LP, Szczech LA 2006 Leptin and renal disease. Semin Dial 19:54-59
110. Kern TS 2007 Contributions of inflammatory processes to the development of the early stages of diabetic retinopathy. Exp Diabetes Res 2007:1-14
111. van Hecke MV, Dekker JM, Nijpels G, Moll AC, Heine RJ, Bouter LM, Polak BC, Stehouwer CD 2005 Inflammation and endothelial dysfunction are associated with retinopathy: the Hoorn Study. Diabetologia 48:1300-1306 (Pubitemid 41186094)
112. Spijkerman AM, Gall MA, Tarnow L, Twisk JW, Lauritzen E, Lund-Andersen H, Emeis J, Parving HH, Stehouwer CD 2007 Endothelial dysfunction and low-grade inflammation and the progression of retinopathy in type 2 diabetes. Diabet Med 24:969-976 (Pubitemid 47301646)
113. Ersanli D, Top C, Oncül O, Aydin A, Terekeci H 2007 Relationship between serum soluble E-selectin levels and development of diabetic retinopathy in patients with type 2 diabetes. Scand J Clin Lab Invest 67:474-479 (Pubitemid 47344350)
114. Yilmaz MI, Sonmez A, Acikel C, Celik T, Bingol N, Pinar M, Bayraktar Z, Ozata M 2004 Adiponectin may play a part in the pathogenesis of diabetic retinopathy. Eur J Endocrinol 151:135-140 (Pubitemid 39117376)
115. González-Clemente JM, Mauricio D, Richart C, Broch M, Caixàs A, Megia A, Giménez-Palop O, Simón I, Martínez-Riquelme A, Giménez-Pérez G, Vendrell 2005 Diabetic neuropathy is associated with activation of the TNF-α system in subjects with type 1 diabetes mellitus. J Clin Endocrinol (Oxf) 63:525-529
116. Herder C, Lankisch M, Ziegler D, Rathmann W, Koenig W, Illig T, Döring A, Thorand B, Holle R, Giani G, Martin S, Meisinger C 2009 Subclinical inflammation and diabetic polyneuropathy: MONICA/KORA Survey F3 (Augsburg, Germany). Diabetes Care 32:680-682
117. Gruden G, Bruno G, Chaturvedi N, Burt D, Schalkwijk C, Pinach S, Stehouwer CD, Witte DR, Fuller JH, Perin PC; EURODIAB Prospective Complications Study Group 2008 Serum heat shock protein 27 and diabetes complications in the EURODIAB prospective complications study: a novel circulating marker for diabetic neuropathy. Diabetes 57:1966-1970
118. Staels B, Maes M, Zambon A 2008 Fibrates and future PPARα agonists in the treatment of cardiovascular disease. Nat Clin Pract Cardiovasc Med 5:542-553
119. Jager A, van Hinsbergh VW, Kostense PJ, Emeis JJ, Yudkin JS, Nijpels G, Dekker JM, Heine RJ, Bouter LM, Stehouwer CD 1999 von Willebrand factor, C-reactive protein, and 5-year mortality in diabetic and nondiabetic subjects: the Hoorn Study. Arterioscler Thromb Vasc Biol 19:3071-3078
120. Jager A, van Hinsbergh VW, Kostense PJ, Emeis JJ, Nijpels G, Dekker JM, Heine RJ, Bouter LM, Stehouwer CD 2000 Increased levels of soluble vascular cell adhesion molecule 1 are associated with risk of cardiovascular mortality in type 2 diabetes: the Hoorn study Diabetes 49:485-491
121. Stehouwer CD, Gall MA, Twisk JW, Knudsen E, Emeis JJ, Parving HH 2002 Increased urinary albumin excretion, endothelial dysfunction, and chronic low-grade inflammation in type 2 diabetes: progressive, interrelated, and independently associated with risk of death. Diabetes 51:1157-1165 (Pubitemid 34438363)
122. Schulze MB, Rimm EB, Li T, Rifai N, Stampfer MJ, Hu FB 2004 C-reactive protein and incident cardiovascular events among men with diabetes. Diabetes Care 27:889-894 (Pubitemid 38420210)
123. Soinio M, Marniemi J, Laakso M, Lehto S, Rönnemaa T 2006 High-sensitivity C-reactive protein and coronary heart disease mortality in patients with type 2 diabetes: a 7-year follow-up study. Diabetes Care 29:329-333 (Pubitemid 44106513)
124. Sattar N, Nelson SM 2008 Adiponectin, diabetes, and coronary heart disease in older persons: unraveling the paradox. J Clin Endocrinol Metab 93:3299-3301
125. Schulze MB, Shai I, Rimm EB, Li T, Rifai N, Hu FB 2005 Adiponectin and future coronary heart disease events among men with type 2 diabetes. Diabetes 54:534-539:889-894
126. Stephens JW, Gable DR, Hurel SJ, Miller GJ, Cooper JA, Humphries SE 2006 Increased plasma markers of oxidative stress are associated with coronary heart disease in males with diabetes mellitus and with 10-year risk in a prospective sample of males. Clin Chem 52:446-452
127. Schram MT, Chaturvedi N, Schalkwijk CG, Fuller JH, Stehouwer CD; EURODIAB Prospective Complications Study Group 2005 Markers of inflammation are cross-sectionally associated with microvascular complications and cardiovascular disease in type 1 diabetes - the EURODIAB Prospective Complications Study. Diabetologia 48:370-378 (Pubitemid 40543311)
128. Soedamah-Muthu SS, Chaturvedi N, Schalkwijk CG, Stehouwer CD, Ebeling P, Fuller JH; The EURODIAB Prospective Complications Study group 2006 Soluble vascular cell adhesion molecule-1 and soluble E-selectin are associated with micro- and macrovascular complications in type 1 diabetic patients. J Diabetes Complications 20:188-195
129. Epidemiology of Diabetes Interventions and Complications (EDIC) Research Group 1999 Effect of intensive diabetes treatment on carotid artery wall thickness in the epidemiology of diabetes interventions and complications. Diabetes 48:383-390
130. Hayaishi-Okano R, Yamasaki Y, Katakami N, Ohtoshi K, Gorogawa S, Kuroda A, Matsuhisa M, Kosugi K, Nishikawa N, Kajimoto Y, Hori M 2002 Elevated C-reactive protein associates with early-stage carotid atherosclerosis in young subjects with type 1 diabetes. Diabetes Care 25:1432-1438 (Pubitemid 41071157)
131. Sigurdardottir V, Fagerberg B, Hulthe J 2004 Preclinical atherosclerosis and inflammation in 61-year-old men with newly diagnosed diabetes and
132. Saremi A, Anderson RJ, Luo P, Moritz TE, Schwenke DC, Allison M, Reaven PD; for the VADT 2009 Association between IL-6 and the extent of coronary atherosclerosis in the veterans affairs diabetes trial (VADT). Atherosclerosis 203:610-614
133. Katakami N, Kaneto H, Matsuhisa M, Miyatsuka T, Sakamoto K, Kawamori D, Yoshiuchi K, Nakamura Y, Kato K, Yamamoto K, Kosugi K, Hori M, Yamasaki Y 2006 Association of soluble CD40 ligand with carotid atherosclerosis in Japanese type 1 diabetic patients. Diabetologia 49:1670-1676 (Pubitemid 43848105)
134. Reilly MP, Iqbal N, Schutta M, Wolfe ML, Scally M, Localio AR, Rader DJ, Kimmel SE 2004 Plasma leptin levels are associated with coronary atherosclerosis in type 2 diabetes. J Clin Endocrinol Metab 89:3872-3878 (Pubitemid 39071487)
135. Maahs DM, Ogden LG, Kretowski A, Snell-Bergeon JK, Kinney GL, Berl T, Rewers M 2007 Serum cystatin C predicts progression of subclinical coronary atherosclerosis in individuals with type 1 diabetes. Diabetes 56:2774-2779 (Pubitemid 350044921)
136. Lajer M, Tarnow L, Jorsal A, Teerlink T, Parving HH, Rossing P 2008 Plasma concentration of asymmetric dimethylarginine (ADMA) predicts cardiovascular morbidity and mortality in type 1 diabetic patients with diabetic nephropathy. Diabetes Care 31:747-752
137. Yoshida N, Okumura K, Aso Y 2005 High serum pentosidine concentrations are associated with increased arterial stiffness and thickness in patients with type 2 diabetes. Metabolism 54:345-350 (Pubitemid 40250094)