The Pathobiology of Diabetic Complications

The Diabetes Control and Complications Trial Research Group: 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, 1993

UK Prospective Diabetes Study (UKPDS) Group: Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet 352: 837–853, 1998

Kaiser N, Sasson S, Feener EP, Boukobza-Vardi N, Higashi S, Moller DE, Davidheiser S, Przybylski RJ, King GL: Differential regulation of glucose transport and transporters by glucose in vascular endothelial and smooth muscle cells. Diabetes 42: 80–89, 1993

Heilig CW, Concepcion LA, Riser BL, Freytag SO, Zhu M, Cortes P: Overexpression of glucose transporters in rat mesangial cells cultured in a normal glucose milieu mimics the diabetic phenotype. J Clin Invest 96: 1802–1814, 1995

Gabbay KH, Merola LO, Field RA: Sorbitol pathway: presence in nerve and cord with substrate accumulation in diabetes. Science 151: 209–210, 1966

Lee AY, Chung SS: Contributions of polyol pathway to oxidative stress in diabetic cataract. FASEB J 13: 23–30, 1999

Engerman RL, Kern TS, Larson ME: Nerve conduction and aldose reductase inhibition during 5 years of diabetes or galactosaemia in dogs. Diabetologia 37: 141–144, 1994

Giardino I, Edelstein D, Brownlee M: Nonenzymatic glycosylation in vitro and in bovine endothelial cells alters basic fibroblast growth factor activity: a model for intracellular glycosylation in diabetes. J Clin Invest 94: 110–117, 1994

Shinohara M, Thornalley PJ, Giardino I, Beisswenger P, Thorpe SR, Onorato J, Brownlee M: Overexpression of glyoxalase-I in bovine endothelial cells inhibits intracellular advanced glycation endproduct formation and prevents hyperglycemia-induced increases in macromolecular endocytosis. J Clin Invest 101: 1142–1147, 1998

McLellan AC, Thornalley PJ, Benn J, Sonksen PH: Glyoxalase system in clinical diabetes mellitus and correlation with diabetic complications. Clin Sci (Lond) 87: 21–29, 1994

Charonis AS, Reger LA, Dege JE, Kouzi-Koliakos K, Furcht LT, Wohlhueter RM, Tsilibary EC: Laminin alterations after in vitro nonenzymatic glycosylation. Diabetes 39: 807–814, 1990

Li YM, Mitsuhashi T, Wojciechowicz D, Shimizu N, Li J, Stitt A, He C, Banerjee D, Vlassara H: Molecular identity and cellular distribution of advanced glycation endproduct receptors: relationship of p60 to OST-48 and p90 to 80K-H membrane proteins. Proc Natl Acad Sci U S A 93: 11047–11052, 1996

Neeper M, Schmidt AM, Brett J, Yan SD, Wang F, Pan YC, Elliston K, Stern D, Shaw A: Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J Biol Chem 267: 14998–15004, 1992

Smedsrod B, Melkko J, Araki N, Sano H, Horiuchi S: Advanced glycation end products are eliminated by scavenger-receptor-mediated endocytosis in hepatic sinusoidal Kupffer and endothelial cells. Biochem J 322: 567–573, 1997

Vlassara H, Li YM, Imani F, Wojciechowicz D, Yang Z, Liu FT, Cerami A: Identification of galectin-3 as a high-affinity binding protein for advanced glycation end products (AGE): a new member of the AGE-receptor complex. Mol Med 1: 634–646, 1995

Abordo EA, Thornalley PJ: Synthesis and secretion of tumour necrosis factor-alpha by human monocytic THP-1 cells and chemotaxis induced by human serum albumin derivatives modified with methylglyoxal and glucose-derived advanced glycation endproducts. Immunol Lett 58: 139–147, 1997

Doi T, Vlassara H, Kirstein M, Yamada Y, Striker GE, Striker LJ: Receptor-specific increase in extracellular matrix production in mouse mesangial cells by advanced glycosylation end products is mediated via platelet-derived growth factor. Proc Natl Acad Sci U S A 89: 2873–2877, 1992

Kirstein M, Aston C, Hintz R, Vlassara H: Receptor-specific induction of insulin-like growth factor I in human monocytes by advanced glycosylation end product-modified proteins. J Clin Invest 90: 439–446, 1992

Schmidt AM, Hori O, Chen JX, Li JF, Crandall J, Zhang J, Cao R, Yan SD, Brett J, Stern D: Advanced glycation endproducts interacting with their endothelial receptor induce expression of vascular cell adhesion molecule-1 (VCAM-1) in cultured human endothelial cells and in mice: a potential mechanism for the accelerated vasculopathy of diabetes. J Clin Invest 96: 1395–1403, 1995

Skolnik EY, Yang Z, Makita Z, Radoff S, Kirstein M, Vlassara H: Human and rat mesangial cell receptors for glucose-modified proteins: potential role in kidney tissue remodelling and diabetic nephropathy. J Exp Med 174: 931–939, 1991

Vlassara H, Brownlee M, Manogue KR, Dinarello CA, Pasagian A: Cachectin/TNF and IL-1 induced by glucose-modified proteins: role in normal tissue remodeling. Science 240: 1546–1548, 1988

Hammes HP, Martin S, Federlin K, Geisen K, Brownlee M: Aminoguanidine treatment inhibits the development of experimental diabetic retinopathy. Proc Natl Acad Sci U S A 88: 11555–11558, 1991

Koya D, King GL: Protein kinase C activation and the development of diabetic complications. Diabetes 47: 859–866, 1998

DeRubertis FR, Craven PA: Activation of protein kinase C in glomerular cells in diabetes: mechanisms and potential links to the pathogenesis of diabetic glomerulopathy. Diabetes 43: 1–8, 1994

Xia P, Inoguchi T, Kern TS, Engerman RL, Oates PJ, King GL: Characterization of the mechanism for the chronic activation of diacylglycerol-protein kinase C pathway in diabetes and hypergalactosemia. Diabetes 43: 1122–1129, 1994

Koya D, Jirousek MR, Lin YW, Ishii H, Kuboki K, King GL: Characterization of protein kinase C beta isoform activation on the gene expression of transforming growth factor-beta, extracellular matrix components, and prostanoids in the glomeruli of diabetic rats. J Clin Invest 100: 115–126, 1997

Ishii H, Jirousek MR, Koya D, Takagi C, Xia P, Clermont A, Bursell SE, Kern TS, Ballas LM, Heath WF, Stramm LE, Feener EP, King GL: Amelioration of vascular dysfunctions in diabetic rats by an oral PKC beta inhibitor. Science 272: 728–731, 1996

Kuboki K, Jiang ZY, Takahara N, Ha SW, Igarashi M, Yamauchi T, Feener EP, Herbert TP, Rhodes CJ, King GL: Regulation of endothelial constitutive nitric oxide synthase gene expression in endothelial cells and in vivo : a specific vascular action of insulin. Circulation 101: 676–681, 2000

Studer RK, Craven PA, Derubertis FR: Role for protein kinase C in the mediation of increased fibronectin accumulation by mesangial cells grown in high-glucose medium. Diabetes 42: 118–126, 1993

Feener EP, Xia P, Inoguchi T, Shiba T, Kunisaki M, King GL: Role of protein kinase C in glucose- and angiotensin II-induced plasminogen activator inhibitor expression. Contrib Nephrol 118: 180–187, 1996

Bishara NB, Dunlop ME, Murphy TV, Darby IA, Sharmini Rajanayagam MA, Hill MA: Matrix protein glycation impairs agonist-induced intracellular Ca2+ signaling in endothelial cells. J Cell Physiol 193: 80–92, 2002

Koya D, Haneda M, Nakagawa H, Isshiki K, Sato H, Maeda S, Sugimoto T, Yasuda H, Kashiwagi A, Ways DK, King GL, Kikkawa R: Amelioration of accelerated diabetic mesangial expansion by treatment with a PKC beta inhibitor in diabetic db/db mice, a rodent model for type 2 diabetes. FASEB J 14: 439–447, 2000

Kolm-Litty V, Sauer U, Nerlich A, Lehmann R, Schleicher ED: High glucose-induced transforming growth factor beta1 production is mediated by the hexosamine pathway in porcine glomerular mesangial cells. J Clin Invest 101: 160–169, 1998

Sayeski PP, Kudlow JE: Glucose metabolism to glucosamine is necessary for glucose stimulation of transforming growth factor-alpha gene transcription. J Biol Chem 271: 15237–15243, 1996

Wells L, Hart G: O-GlcNAc turns twenty: functional implications for posttranslational modification of nuclear and cytosolic protein with a sugar. FEBS Lett 546: 154–158, 2003

Du XL, Edelstein D, Rossetti L, Fantus IG, Goldberg H, Ziyadeh F, Wu J, Brownlee M: Hyperglycemia-induced mitochondrial superoxide overproduction activates the hexosamine pathway and induces plasminogen activator inhibitor-1 expression by increasing Sp1 glycosylation. Proc Natl Acad Sci U S A 97: 12222–12226, 2000

Clark RJ, McDonough PM, Swanson E, Trost SU, Suzuki M, Fukuda M, Dillmann WH: Diabetes and the accompanying hyperglycemia impairs cardiomyocyte calcium cycling through increased nuclear O-GlcNAcylation. J Biol Chem 278: 44230–44237, 2003

Federici M, Menghini R, Mauriello A, Hribal ML, Ferrelli F, Lauro D, Sbraccia P, Spagnoli LG, Sesti G, Lauro R: Insulin-dependent activation of endothelial nitric oxide synthase is impaired by O-linked glycosylation modification of signaling proteins in human coronary endothelial cells. Circulation 106: 466–472, 2002

Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M: Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404: 787–790, 2000

Giugliano D, Ceriello A, Paolisso G: Oxidative stress and diabetic vascular complications. Diabetes Care 19: 257–267, 1996

Wallace DC: Diseases of the mitochondrial DNA (Review). Annu Rev Biochem 61: 1175–1212, 1992

Trumpower BL: The protonmotive Q cycle: energy transduction by coupling of proton translocation to electron transfer by the cytochrome bc1 complex. J Biol Chem 265: 11409–11412, 1990

Korshunov SS, Skulachev VP, Starkov AA: High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 416: 15–18, 1997

Du XL, Edelstein D, Dimmeler S, Ju Q, Sui C, Brownlee M: Hyperglycemia inhibits endothelial nitric oxide synthase activity by posttranslational modification at the Akt site. J Clin Invest 108: 1341–1348, 2001

DeRubertis FR, Craven PA, Melhem MF, Salah EM: Attenuation of renal injury in db/db mice overexpressing superoxide dismutase: evidence for reduced superoxide–nitric oxide interaction. Diabetes 53: 762–768, 2004

Du X, Matsumura T, Edelstein D, Rossetti L, Zsengeller Z, Szabo C, Brownlee M: Inhibition of GAPDH activity by poly(ADP-ribose) polymerase activates three major pathways of hyperglycemic damage in endothelial cells. J Clin Invest 112: 1049–1057, 2003

Sawa A, Khan AA, Hester LD, Snyder SH: Glyceraldehyde-3-phosphate dehydrogenase: nuclear translocation participates in neuronal and nonneuronal cell death. Proc Natl Acad Sci U S A 94: 11669–11674, 1997

Schmidtz HD: Reversible nuclear translocation of glyceraldehyde-3-phosphate dehydrogenase upon serum depletion. Eur J Cell Biol 80: 419–427, 2001

Hanley AJ, Williams K, Stern MP, Haffner SM: Homeostasis model assessment of insulin resistance in relation to the incidence of cardiovascular disease: the San Antonio Heart Study. Diabetes Care 25: 1177–1184, 2002

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: Benfotiamine blocks three major pathways of hyperglycemic damage and prevents experimental diabetic retinopathy. Nat Med 9: 294–299, 2003

Kuhlencordt PJ, Gyurko R, Han F, Scherrer-Crosbie M, Aretz TH, Hajjar R, Picard MH, Huang PL: Accelerated atherosclerosis, aortic aneurysm formation, and ischemic heart disease in apolipoprotein E/endothelial nitric oxide synthase double-knockout mice. Circulation 104: 448–454, 2001

Kobayashi T, Tahara Y, Matsumoto M, Iguchi M, Sano H, Murayama T, Arai H, Oida H, Yurugi-Kobayashi T, Yamashita JK, Katagiri H, Majima M, Yokode M, Kita T, Narumiya S: Roles of thromboxane A(2) and prostacyclin in the development of atherosclerosis in apoE-deficient mice. J Clin Invest 114: 784–794, 2004

Salvemini D, Wang ZQ, Zweier JL, Samouilov A, Macarthur H, Misko TP, Currie MG, Cuzzocrea S, Sikorski JA, Riley DP: A nonpeptidyl mimic of superoxide dismutase with therapeutic activity in rats. Science 286: 304–306, 1999