The diverse ligand repertoire of the receptor for advanced glycation endproducts and pathways to the complications of diabetes

Vascular Pharmacology

Volumn 57, Issue 5-6, 2012, Pages 160-167

  Ramasamy, Ravichandran ^a   Yan, Shi Fang ^a   Schmidt, Ann Marie ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Complications; Diabetes; Glycation; RAGE

Indexed keywords

ADVANCED GLYCATION END PRODUCT; BIOLOGICAL MARKER; LIGAND;

ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; DIABETES MELLITUS; DIABETIC NEPHROPATHY; DIABETIC NEUROPATHY; DIABETIC RETINOPATHY; HEART DISEASE; HUMAN; INFLAMMATION; LIGAND BINDING; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; REVIEW; SIGNAL TRANSDUCTION; SWINE;

ANIMALS; DIABETES COMPLICATIONS; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; INFLAMMATION; MICE; RATS; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; SWINE;

EID: 84865647121     PISSN: 15371891     EISSN: 18793649     Source Type: Journal    
DOI: 10.1016/j.vph.2012.06.004     Document Type: Review

References (73)

1. Anand D.V., et al. Determinants of progression of coronary artery calcification in type 2 diabetes role of glycemic control and inflammatory/vascular calcification markers. J. Am. Coll. Cardiol. 2007, 50:2218-2225.
2. Araki N., et al. Macrophage scavenger receptor mediates the endocytic uptake and degradation of advanced glycation endproducts of the Maillard reaction. Eur. J. Biochem. 1995, 230:408-415.
3. Barile G.R., et al. The RAGE axis in early diabetic retinopathy. Invest Ophthalmol. Vis. Sci. 2005, 46:2916-2924.
4. Beisswenger P.J., et al. Formation of immunochemical advanced glycosylation end products precedes and correlates with early manifestations of renal and retinal disease in diabetes. Diabetes 1995, 44:824-829.
5. Bierhaus A., et al. Loss of pain perception in diabetes is dependent on a receptor of the immunoglobulin superfamily. J. Clin. Invest. 2004, 114:1741-1751.
6. Bolton W.K., et al. Randomized trial of an inhibitor of formation of advanced glycation end products in diabetic nephropathy. Am. J. Nephrol. 2004, 24:32-40.
7. Bu D.X., et al. Activation of the ROCK1 branch of the TGF-beta pathway contributes to RAGE-dependent acceleration of atherosclerosis in diabetic ApoE null mice. Circ. Res. 2010, 106:1040-1051.
8. Bucciarelli L.G., et al. RAGE and modulation of ischemic injury in the diabetic myocardium. Diabetes 2008, 57:1941-1951.
9. Burke A.P., et al. Morphologic findings of coronary atherosclerotic plaques in diabetics: a postmortem study. Arterioscler. Thromb. Vasc. Biol. 2004, 24:1266-1271.
10. Calcutt N.A., Cooper M.E., Kern T.S., Schmidt A.M. Therapies for hyperglycaemia-induced diabetic complications: from animal models to clinical trials. Nat. Rev. Drug Discov. 2009, 8:417-429.
11. Chang J.S., et al. Oxygen deprivation triggers upregulation of early growth response-1 by the receptor for advanced glycation endproducts. Circ. Res. 2008, 102:905-913.
12. Chavakis T., et al. The pattern recognition receptor (RAGE) is a counterreceptor for leukocyte integrins: a novel pathway for inflammatory cell recruitment. J. Exp. Med. 2003, 198:1507-1515.
13. Chen J., et al. Advanced glycation endproducts alter functions and promote apoptosis in endothelial progenitor cells through receptor for advanced glycation endproducts mediate overexpression of cell oxidant stress. Mol. Cell. Biochem. 2010, 335:137-146.
14. Chen J., Jin J., Song M., Dong H., Zhao G., Huang L. C-reactive protein down-regulates endothelial nitric oxide synthase expression and promotes apoptosis in endothelial progenitor cells through receptor for advanced glycation endproducts. Gene 2012, 496:128-135.
15. Distler M.G., et al. Glyoxalase 1 increases anxiety by reducing GABAA receptor agonist methylglyoxal. J. Clin. Invest. 2012, 122(6):2306-2315. (Jun 1, Epub 2012 May 15). http://dx.doi.org/10.1172/JCI61319.
16. El-Asrar A.M., et al. High mobility group box 1 and biomarkers of inflammation in the vitreous from patients with proliferative diabetic retinopathy. Mol. Vis. 2011, 17:1829-1838.
17. El-Mesallamy H.O., et al. Levels of soluble advanced glycation end products receptors and other soluble serum markers as indicators of diabetic neuropathy in the foot. J. Investig. Med. 2011, 59:1233-1238.
18. Forbes J.M., et al. Modulation of soluble receptor for advanced glycation end products by angiotensin-converting enzyme-1 inhibition in diabetic nephropathy. J. Am. Soc. Nephrol. 2005, 16:2363-2372.
19. Grossin N., Boulanger E., Wautier M.P., Wautier J.L. The different isoforms of the receptor for advanced glycation end products are modulated by pharmacological agents. Clin. Hemorheol. Microcirc. 2010, 45:143-153.
20. Harja E., et al. Vascular and inflammatory stresses mediate atherosclerosis via RAGE in apo E deficient mice. J. Clin. Invest. 2008, 1118:183-194.
21. Herman W.H., Zimmet P. Type 2 diabetes: an epidemic requiring global attention and urgent action. Diabetes Care 2012, 35:943-944.
22. Hofmann M.A., et al. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell 1999, 97:889-901.
23. Huang J.S., Guh J.Y., Chen H.C., Hung W.C., Lai Y.H., Chuang L.Y. Role of receptor for advanced glycation endproduct (RAGE) and the Jak/STAT signaling pathway in AGE-induced collagen production in NRK-49F cells. J. Cell. Biochem. 2001, 81:102-113.
24. Hudson B.I., et al. Interaction of the RAGE cytoplasmic domain with diaphanous-1 is required for ligand-stimulated cellular migration through activation of Rac1 and Cdc42. J. Biol. Chem. 2008, 283:34457-34468.
25. Humpert P.M., et al. sRAGE and esRAGE are not associated with peripheral or autonomic neuropathy in type 2 diabetes. Horm. Metab. Res. 2007, 39:899-902.
26. Huttunen H.J., Fages C., Rauvala H. Receptor for advanced glycation endproducts (RAGE)-mediated neurite outgrowth and activation of NF-kB require the cytoplasmic domain of the receptor but different downstream signaling pathways. J. Biol. Chem. 1999, 274:19919-19924.
27. Huttunen H.J., Kuja-Panula J., Rauvala H. Receptor for advanced glycation endproduct (RAGE) signaling induces CREB-dependent chromogranin expression during neuronal differentiation. J. Biol. Chem. 2002, 277:38635-38646.
28. Juranek J., et al. Morphological changes and immunohistochemical expression of RAGE and its ligands in the sciatic nerve of hyperglycemic pig (Sus scrofa). Biochem. Insights 2010, 47-59.
29. Kalousová M., et al. Soluble receptor for advanced glycation end products in patients with decreased renal function. Am. J. Kidney Dis. 2006, 47:406-411.
30. Kislinger T.K., et al. N(epsilon)-(carboxymethyl)lysine adducts of proteins are ligands for advanced glycation end products that activate cell signaling pathways and modulate gene expression. J. Biol. Chem. 1999, 274:31740-31749.
31. Kosaki A., et al. Increased plasma S100A12 (EN-RAGE) levels in patients with type 2 diabetes. J. Clin. Endocrinol. Metab. 2004, 89:5423-5428.
32. Lander H.M., Tauras J.M., Ogiste J.S., Hori O., Moss R.A., Schmidt A.M. Activation of the receptor for advanced glycation endproducts triggers a p21(ras) dependent mitogen activated protein kinase pathway regulated by oxidant stress. J. Biol. Chem. 1997, 272:17810-17814.
33. Ma H., et al. Advanced glycation endproduct (AGE) accumulation and AGE receptor (RAGE) upregulation contribute to the onset of diabetic cardiomyopathy. J. Cell. Mol. Med. 2009, 13:1751-1764.
34. Monnier V.M., et al. Maillard reaction-mediated molecular damage to extracellular matrix and other tissue proteins in diabetes, aging and uremia. Diabetes 1992, 41(Suppl. 2):36-41.
35. Morris-Rosenfeld S., et al. Deletion of bone marrow-derived receptor for advanced glycation end products inhibits atherosclerotic plaque progression. Eur. J. Clin. Invest. 2011, 41:1164-1171.
36. Myint K.M., et al. RAGE control of diabetic nephropathy in a mouse model: effects of RAGE gene disruption and administration of low molecular weight heparin. Diabetes 2006, 55:2510-2522.
37. Nakamura K., Adachi H., Matsui T., Kurita Y., Takeuchi M., Yamagishi S. Independent determinants of soluble form of receptor for advanced glycation end products in elderly hypertensive patients. Metabolism 2009, 58:421-425.
38. Nathan D.M., et al. Intensive diabetes therapy and carotid intima-media thickness in type 1 diabetes mellitus. N. Engl. J. Med. 2003, 348:2294-2303.
39. Nielsen J.M., et al. Blockage of receptor for advanced glycation endproducts prevents development of cardiac dysfunction in db/db type 2 diabetic mice. Eur. J. Heart Fail. 2009, 11:638-647.
40. Nin J.W., et al. Serum high-mobility group box-1 levels are positively associated with micro- and macroalbuminuria but not with cardiovascular disease in type 1 diabetes: the EURODIAB Prospective Complications Study. Eur. J. Endocrinol. 2012, 166:325-332.
41. Ohgami N., et al. CD36, a member of the class b scavenger receptor family, as a receptor for advanced glycation endproducts. J. Biol. Chem. 2001, 276:3195-3202.
42. Parathath S., et al. Diabetes adversely affects macrophages during atherosclerotic plaque regression in mice. Diabetes 2011, 60:1759-1769.
43. Park L., et al. Suppression of accelerated diabetic atherosclerosis by soluble Receptor for AGE (sRAGE). Nat. Med. 1998, 4:1025-1031.
44. Rai V., et al. Signal transduction in receptor for advanced glycation end products (RAGE): solution structure of C-terminal rage (ctRAGE) and its binding to mDia1. J. Biol. Chem. 2012, 287:5133-5144.
45. Ramasamy R., Goldberg I.J. Aldose reductase and cardiovascular diseases, creating human-like diabetic complications in an experimental model. Circ. Res. 2010, 106:1449-1458.
46. Raucci A., et al. A soluble form of the receptor for advanced glycation endproducts (RAGE) is produced by proteolytic cleavage of the membrane-bound form by the sheddase a disintegrin and metalloprotease 10 (ADAM10). FASEB J. 2008, 22:3716-3727.
47. Reiniger N., et al. Deletion of the receptor for advanced glycation endproducts reduces glomerulosclerosis and preserves renal function in the diabetic OVE26 mouse. Diabetes 2010, 59:2043-2054.
48. Rudijanto A. The expression and down stream effect of lectin-like oxidized low density lipoprotein (Lox-1) in hyperglycemic state. Acta Med. Indones. 2007, 39:36-43.
49. Sakaguchi T., et al. Central role of RAGE-dependent neointimal expansion in arterial restenosis. J. Clin. Invest. 2003, 111:959-972.
50. Santilli F., et al. Decreased plasma soluble RAGE in patients with hypercholesterolemia: effects of statins. Free Radic. Biol. Med. 2007, 43:1255-1262.
51. Schmidt A.M., et al. Isolation and characterization of two binding proteins for advanced glycosylation end products from bovine lung which are present on the endothelial cell surface. J. Biol. Chem. 1992, 267:14987-14997.
52. Schmidt A.M., et al. Regulation of human mononuclear phagocyte migration by cell-surface binding proteins for advanced glycation end products. J. Clin. Invest. 1993, 91:2155-2168.
53. Shang L., et al. RAGE modulates hypoxia/reoxygenation injury in adult murine cardiomyocytes via JNK and GSK-3beta signaling pathways. PLoS One 2010, 5:e10092.
54. Soro-Paavonen A., et al. RAGE deficiency attenuates the development of atherosclerosis in diabetes. Diabetes 2008, 57:2461-2469.
55. Taguchi A., et al. Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases. Nature 2000, 405:354-360.
56. Tan A.L., et al. Disparate effects on renal and oxidative parameters following RAGE deletion, AGE accumulation inhibition, or dietary AGE control in experimental diabetic nephropathy. Am. J. Physiol. Renal Physiol. 2010, 298:F763-F770.
57. Tanji N., et al. Expression of advanced glycation end products and their cellular receptor RAGE in diabetic nephropathy and nondiabetic renal disease. J. Am. Soc. Nephrol. 2000, 11:1656-1666.
58. Thornalley P.J. The glyoxalase system: new developments toward functional characterization of a metabolic pathway fundamental to life. Biochem. J. 1990, 269:1-11.
59. Thornalley P.J. Glycation in diabetic neuropathy: characteristics, consequences, causes and therapeutic options. Int. Rev. Neurobiol. 2002, 50:37-57.
60. Thornalley P.J. Dicarbonyl intermediates in the Maillard reaction. Ann. N. Y. Acad. Sci. 2005, 1043:111-117. (8)).
61. Toth C., et al. Receptor for advanced glycation endproducts (RAGEs) and experimental diabetic neuropathy. Diabetes 2008, 57:1002-1017.
62. Toure F., et al. Formin mDia1 mediates vascular remodeling via integration of oxidative and signal transduction pathways. Circ. Res. 2012, 110:1279-1293.
63. Vazzana N., Santilli F., Cuccurullo C., Davì G. Soluble forms of RAGE in internal medicine. Intern. Emerg. Med. 2009, 4:389-401.
64. Vikramadithyan R.K. Human aldose reductase expression accelerates diabetic atherosclerosis in transgenic mice. J. Clin. Invest. 2005, 115:2434-2443.
65. Wendt T.M., et al. RAGE drives the development of glomerulosclerosis and implicates podocyte activation in the pathogenesis of diabetic nephropathy. Am. J. Pathol. 2003, 162:1123-1137.
66. Witzke K.A., et al. Loss of RAGE defense: a cause of Charcot neuroarthropathy?. Diabetes Care 2011, 34:1617-1621.
67. Xu Y., et al. Advanced glycation end product (AGE)-receptor for AGE (RAGE) signaling and up-regulation of Egr-1 in hypoxic macrophages. J. Biol. Chem. 2010, 285:23233-23240.
68. Yan S.F., Ramasamy R., Schmidt A.M. The RAGE axis: a fundamental axis signaling danger to the vulnerable vasculature. Circ. Res. 2010, 106:842-853.
69. Yanagisawa K., et al. Specific fluorescence assay for advanced glycation end products in blood and urine of diabetic patients. Metabolism 1998, 47:1348-1353.
70. Yonekura H., Yamamoto Y., Sakurai S., Watanabe T., Yamamoto H. Roles of the receptor for advanced glycation endproducts in diabetes-induced vascular injury. J. Pharmacol. Sci. 2005, 97:305-311.
71. Zeng S., et al. Opposing roles of RAGE and Myd88 signaling in extensive liver resection. FASEB J. 2012, 26:882-893.
72. Zhang X., et al. Prevalence of diabetic retinopathy in the United States, 2005-2008. JAMA 2010, 304:649-656.
73. Zong H., Ward M., Stitt A.W. AGEs, RAGE and diabetic retinopathy. Curr. Diab. Rep. 2011, 11:244-252.