The "Metabolic memory": Is more than just tight glucose control necessary to prevent diabetic complications?

Journal of Clinical Endocrinology and Metabolism

Volumn 94, Issue 2, 2009, Pages 410-415

  Ceriello, Antonio ^a,b,d   Ihnat, Michael A ^c   Thorpe, Jessica E ^c  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b Ist Naz Ricovero/Cura per Anziani   (Italy)

^c UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^d WALSGRAVE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; GLUCOSE; LIPID; MITOCHONDRIAL PROTEIN; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; ADVANCED GLYCATION END PRODUCT;

GLYCATION; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; MEDICAL RESEARCH; MEMORY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROPHYLAXIS; REVIEW; BIOLOGICAL MODEL; BLOOD; CARDIOVASCULAR DISEASE; DIABETES MELLITUS; GLUCOSE BLOOD LEVEL; METABOLISM; PHYSIOLOGY;

ANIMALIA;

BLOOD GLUCOSE; CARDIOVASCULAR DISEASES; DIABETES COMPLICATIONS; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; METABOLIC NETWORKS AND PATHWAYS; MODELS, BIOLOGICAL; OXIDATIVE STRESS;

EID: 59749094860     PISSN: 0021972X     EISSN: 0021972X     Source Type: Journal    
DOI: 10.1210/jc.2008-1824     Document Type: Review

References (50)

1. The Diabetes Control and Complications Trial Research Group 1993 The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 329:977-986
2. U.K. Prospective Diabetes Study 1998 Intensive blood glucose control with sulfonylureas or insulin compared with conventional treatment and risk for complications in patients with type 2 diabetes (UKPDS 33). Lancet 352:837-853
3. The ADVANCE Collaborative Group 2008 Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes. N Engl J Med 358: 2560-2572
4. The Action to Control Cardiovascular Risk in Diabetes Study Group 2008 Effects of intensive glucose lowering in type 2 diabetes. N Engl J Med 358: 2545-2559
5. Holman RR, Paul SK, Bethel MA, Matthews DR, Neil HA 2008 10-Year follow-up of intensive glucose control in type 2 diabetes. N Engl J Med 359: 1565-1576
6. Nathan DM, Cleary PA, Backlund JY, Genuth SM, Lachin JM, Orchard TJ, Raskin P, Zinman B, Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications (DCCT/EDIC) Study Research Group 2005 Intensive diabetes treatment and cardiovascular disease in patients with type 1 diabetes. N Engl J Med 353:2643-2653
7. Engerman RL, Kern TS 1987 Progression of incipient diabetic retinopathy during good glycemic control. Diabetes 36:808-812
8. Roy S, Sala R, Cagliero E, Lorenzi M 1990 Overexpression of fibronectin induced by diabetes or high glucose: phenomenon with a memory. Proc Natl Acad Sci USA 87:404-408
9. Hammes HP, Klinzing I, Wiegand S, Bretzel RG, Cohen AM, Federlin K 1993 Islet transplantation inhibits diabetic retinopathy in the sucrose-fed diabetic Cohen rat. Invest Ophthalmol Vis Sci 34:2092-2096
10. Writing Team for the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group 2002 Effect of intensive therapy on the microvascular complications of type 1 diabetes mellitus. JAMA 287:2563-2569
11. Writing Team for the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group 2003 Sustained effect of intensive treatment of type 1 diabetes mellitus on development and progression of diabetic nephropathy: the Epidemiology of Diabetes Interventions and Complications (EDIC) study. JAMA 290:2159-2167
12. Nathan DM, Lachin J, Cleary P, Orchard T, Brillon DJ, Backlund JY, O'Leary DH, Genuth S, Diabetes Control and Complications Trial, Epidemiology of Diabetes Interventions and Complications Research Group 2003 Intensive diabetes therapy and carotid intima-media thickness in type 1 diabetes mellitus. N Engl J Med 348:2294-2303
13. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M 2000 Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404:787-790
14. Brownlee M 2005 The pathobiology of diabetic complications: a unifying mechanism. Diabetes 54:1615-1625
15. Beckman JS, Koppenol WH 1996 Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 271:C1424-C1437
16. Julius U, Drel VR, Gräßler J, Obrosova IG 25 August 2008 Nitrosylated proteins in monocytes as a new marker of oxidative-nitrosative stress in diabetic subjects with macroangiopathy. Exp Clin Endocrinol Diabetes. [Epub ahead of print]
17. Foury F, Hu J, Vanderstraeten S 2004 Mitochondrial DNA mutators. Cell Mol Life Sci 61:2799-2811
18. Kowluru RA 2003 Effect of reinstitution of good glycemic control on retinal oxidative stress and nitrative stress in diabetic rats. Diabetes 52:818-823
19. Kowluru RA, Chakrabarti S, Chen S 2004 Re-institution of good metabolic control in diabetic rats and activation of caspase-3 and nuclear transcriptional factor (NFκB) in the retina. Acta Diabetol 41:194-199
20. Kowluru RA, Kanwar M, Kennedy A 2007 Metabolic memory phenomenon and accumulation of peroxynitrite in retinal capillaries. Exp Diabetes Res 2007:21976
21. Ihnat MA, Thorpe JE, Kamat CD, Szabo C, Green DE, Warnke LA, Lacza Z, Cselenyak A, Ross K, Shakir S, Piconi L, Kaltreider RC, Ceriello A 2007 Reactive oxygen species mediate a cellular 'memory' of high glucose stress signalling. Diabetologia 50:1523-1531
22. El-Osta A, Brasacchio D, Yao D, Pocai A, Jones PL, Roeder RG, Cooper ME, Brownlee M 2008 Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J Exp Med 205:2409-2417
23. Radford CR, Schisano B, McTernan PG, Ceriello A 2008 The impact of oscillating glucose and the metabolic memory effect on oxidative stress in human endothelial cells. Diabetologia 51(Suppl 1):57 (Abstract)
24. Ceriello A, Kumar S, Piconi L, Esposito K, Giugliano D 2007 Simultaneous control of hyperglycemia and oxidative stress normalizes endothelial function in type 1 diabetes. Diabetes Care 30:649-654
25. Piconi L, Ihnat MA, Ceriello A 2007 Oxidative stress in the pathogenesis/ treatment of diabetes. Curr Clin Food Sci 3:194-199
26. Ceriello A, Esposito K, Piconi L, Ihnat MA, Thorpe JE, Testa R, Boemi M, Giugliano D 2008 Oscillating glucose is more deleterious to endothelial function and oxidative stress than mean glucose in normal and type 2 diabetic patients. Diabetes 57:1349-1354
27. Beisswenger PJ, Howell SK, Nelson RG, Mauer M, Szwergold BS 2003 α-Oxoaldehyde metabolism and diabetic complications. Biochem Soc Trans 31:1358-1363
28. Lo TW, Westwood ME, McLellan AC, Selwood T, Thornalley PJ 1994 Binding and modification of proteins by methylglyoxal under physiological conditions. A kinetic and mechanistic study with Nα-acetylarginine, Nα-acetylcysteine, and N α-acetyllysine, and bovine serum albumin. J Biol Chem 269: 32299-32305
29. Papoulis A, al-Abed Y, Bucala R 1995 Identification of N2-(1-carboxyethyl-)guanine (CEG) as a guanine advanced glycosylation end product. Biochemistry 34:648-655
30. Goldin A, Beckman JA, Schmidt AM, Creager MA 2006 Advanced glycation end products: sparking the development of diabetic vascular injury. Circulation 114:597-605
31. Rosca MG, Monnier VM, Szweda LI, Weiss MF 2002 Alterations in renal mitochondrial respiration in response to the reactive oxoaldehyde methylglyoxal. Am J Physiol Renal Physiol 283:F52-F59
32. Rosca MG, Mustata TG, Kinter MT, Ozdemir AM, Kern TS, Szweda LI, Brownlee M, Monnier VM, Weiss MF 2005 Glycation of mitochondrial proteins from diabetic rat kidney is associated with excess superoxide formation. Am J Physiol Renal Physiol 289:F420-F430
33. Reznick RM, Shulman GI 2006 The role of AMP-activated protein kinase in mitochondrial biogenesis. J Physiol 574:33-39
34. Gibson BW 2005 The human mitochondrial proteome: oxidative stress, protein modifications and oxidative phosphorylation. Int J Biochem Cell Biol 37:927-934
35. Elfering SL, Haynes VL, Traaseth NJ, Ettl A, Giulivi C 2004 Aspects, mechanism, and biological relevance of mitochondrial protein nitration sustained by mitochondrial nitric oxide synthase. Am J Physiol Heart Circ Physiol 286: H22-H29
36. Wautier MP, Chappey O, Corda S, Stern DM, Schmidt AM, Wautier JL 2001 Activation of NADPH oxidase by AGE links oxidant stress to altered gene expression via RAGE. Am J Physiol Endocrinol Metab 280:E685-E694
37. Genuth S, Sun W, Cleary P, Sell DR, Dahms W, Malone J, Sivitz W, Monnier VM, DCCT Skin Collagen Ancillary Study Group 2005 Glycation and carboxymethyllysine levels in skin collagen predict the risk of future 10-year progression of diabetic retinopathy and nephropathy in the diabetes control and complications trial and epidemiology of diabetes interventions and complications participants with type 1 diabetes. Diabetes 54:3103-3111
38. Monnier VM, Bautista O, Kenny D, Sell DR, Fogarty J, Dahms W, Cleary PA, Lachin J, Genuth S 1999 Skin collagen glycation, glycoxidation, and cross-linking are lower in subjects with long-term intensive versus conventional therapy of type 1 diabetes: relevance of glycated collagen products versus HbA1c as markers of diabetic complications. DCCT Skin Collagen Ancillary Study Group. Diabetes Control and Complications Trial. Diabetes 48:870-880
39. Lander HM, Tauras JM, Ogiste JS, Hori O, Moss RA, Schmidt AM 1997 Activation of the receptor for advanced glycation end products triggers a p21(ras)-dependent mitogen-activated protein kinase pathway regulated by oxidant stress. J Biol Chem 272:17810-17814
40. Tanaka N, Yonekura H, Yamagishi S, Fujimori H, Yamamoto Y, Yamamoto H 2000 The receptor for advanced glycation end products is induced by the glycation products themselves and tumor necrosis factor-α through nuclear factor-κB, and by 17β-estradiol through Sp-1 in human vascular endothelial cells. J Biol Chem 275:25781-25790
41. Willcox BJ, Curb JD, Rodriguez BL 2008 Antioxidants in cardiovascular health and disease: key lessons from epidemiologic studies. Am J Cardiol 101: 75D-86D
42. Ceriello A 2003 New insights on oxidative stress and diabetic complications may lead to a "causal" antioxidant therapy. Diabetes Care 26:1589-1596
43. Rahbar S, Natarajan R, Yerneni K, Scott S, Gonzales N, Nadler JL 2000 Evidence that pioglitazone, metformin and pentoxifylline are inhibitors of glycation. Clin Chim Acta 301:65-77
44. Miyata T, van Ypersele de Strihou C, Ueda Y, Ichimori K, Inagi R, Onogi H, Ishikawa N, Nangaku M, Kurokawa K 2002 Angiotensin II receptor antagonists and angiotensin-converting enzyme inhibitors lower in vitro the formation of advanced glycation end products: biochemical mechanisms. J Am Soc Nephrol 13:2478-2487
45. Yoshida T, Yamagishi S, Nakamura K, Matsui T, Imaizumi T, Takeuchi M, Koga H, Ueno T, Sata M 2006 Telmisartan inhibits AGE-induced C-reactive protein production through downregulation of the receptor for AGE via peroxisome proliferator-activated receptor-γ activation. Diabetologia 49:3094-3099
46. Ceriello A, Assaloni R, Da Ros R, Maier A, Piconi L, Quagliaro L, Esposito K, Giugliano D 2005 Effect of atorvastatin and irbesartan, alone and in combination, on postprandial endothelial dysfunction, oxidative stress, and inflammation in type 2 diabetic patients. Circulation 111:2518-2524
47. Ceriello A, Piconi L, Esposito K, Giugliano D 2007 Telmisartan shows an equivalent effect of vitamin C in further improving endothelial dysfunction after glycemia normalization in type 1 diabetes. Diabetes Care 30:1694-1698
48. Corgnali M, Piconi L, Ihnat M, Ceriello A 2007 Evaluation of gliclazide ability to attenuate the hyperglycaemic 'memory' induced by high glucose in isolated human endothelial cells. Diabetes Metab Res Rev 24:301-309
49. Hammes HP, Du X, Edelstein D, Taguchi T, Matsumura T, Ju Q, Lin J, Bierhaus A, Nawroth P, Hannak D, Neumaier M, Bergfeld R, Giardino I, Brownlee M 2003 Benfotiamine blocks three major pathways of hyperglycemic damage and prevents experimental diabetic retinopathy. Nat Med 9:294-299
50. Du X, Edelstein D, Brownlee M 2008 Oral benfotiamine plus α-lipoic acid normalises complication-causing pathways in type 1 diabetes. Diabetologia 51:1930-1932