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http://dx.doi.org/10.5808/GI.2013.11.4.224

Receptor for Advanced Glycation Endproducts (RAGE), Its Ligands, and Soluble RAGE: Potential Biomarkers for Diagnosis and Therapeutic Targets for Human Renal Diseases  

Lee, Eun Ji (Department of Biological Science, Sookmyung Women's University)
Park, Jong Hoon (Department of Biological Science, Sookmyung Women's University)
Abstract
Receptor for advanced glycation endproducts (RAGE) is a multi-ligand receptor that is able to bind several different ligands, including advanced glycation endproducts, high-mobility group protein (B)1 (HMGB1), S-100 calcium-binding protein, amyloid-${\beta}$-protein, Mac-1, and phosphatidylserine. Its interaction is engaged in critical cellular processes, such as inflammation, proliferation, apoptosis, autophagy, and migration, and dysregulation of RAGE and its ligands leads to the development of numerous human diseases. In this review, we summarize the signaling pathways regulated by RAGE and its ligands identified up to date and demonstrate the effects of hyper-activation of RAGE signals on human diseases, focused mainly on renal disorders. Finally, we propose that RAGE and its ligands are the potential targets for the diagnosis, monitoring, and treatment of numerous renal diseases.
Keywords
advanced glycosylation end-product receptor; kidney diseases; signal transduction;
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1 Willemsen S, Hartog JW, Hummel YM, van Ruijven MH, van der Horst IC, van Veldhuisen DJ, et al. Tissue advanced glycation end products are associated with diastolic function and aerobic exercise capacity in diabetic heart failure patients. Eur J Heart Fail 2011;13:76-82.   DOI   ScienceOn
2 Yamada K, Miyahara Y, Hamaguchi K, Nakayama M, Nakano H, Nozaki O, et al. Immunohistochemical study of human advanced glycosylation end-products (AGE) in chronic renal failure. Clin Nephrol 1994;42:354-361.
3 Harris PC, Torres VE. Polycystic kidney disease. Annu Rev Med 2009;60:321-337.   DOI   ScienceOn
4 Ye M, Grant M, Sharma M, Elzinga L, Swan S, Torres VE, et al. Cyst fluid from human autosomal dominant polycystic kidneys promotes cyst formation and expansion by renal epithelial cells in vitro. J Am Soc Nephrol 1992;3:984-994.
5 Sparvero LJ, Asafu-Adjei D, Kang R, Tang D, Amin N, Im J, et al. RAGE (Receptor for Advanced Glycation Endproducts), RAGE ligands, and their role in cancer and inflammation. J Transl Med 2009;7:17.   DOI   ScienceOn
6 Higashi T, Sano H, Saishoji T, Ikeda K, Jinnouchi Y, Kanzaki T, et al. The receptor for advanced glycation end products mediates the chemotaxis of rabbit smooth muscle cells. Diabetes 1997;46:463-472.   DOI
7 Schmidt AM, Yan SD, Wautier JL, Stern D. Activation of receptor for advanced glycation end products: a mechanism for chronic vascular dysfunction in diabetic vasculopathy and atherosclerosis. Circ Res 1999;84:489-497.   DOI   ScienceOn
8 Monnier VM, Sell DR, Nagaraj RH, Miyata S, Grandhee S, Odetti P, 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.   DOI
9 Tanji N, Markowitz GS, Fu C, Kislinger T, Taguchi A, Pischetsrieder M, 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.
10 Bohlender JM, Franke S, Stein G, Wolf G. Advanced glycation end products and the kidney. Am J Physiol Renal Physiol 2005; 289:F645-F659.   DOI   ScienceOn
11 Vlassara H. The AGE-receptor in the pathogenesis of diabetic complications. Diabetes Metab Res Rev 2001;17:436-443.   DOI   ScienceOn
12 Simm A, Munch G, Seif F, Schenk O, Heidland A, Richter H, et al. Advanced glycation endproducts stimulate the MAP-kinase pathway in tubulus cell line LLC-PK1. FEBS Lett 1997;410: 481-484.   DOI   ScienceOn
13 Ulloa L, Batliwalla FM, Andersson U, Gregersen PK, Tracey KJ. High mobility group box chromosomal protein 1 as a nuclear protein, cytokine, and potential therapeutic target in arthritis. Arthritis Rheum 2003;48:876-881.   DOI   ScienceOn
14 Gugliucci A, Bendayan M. Renal fate of circulating advanced glycated end products (AGE): evidence for reabsorption and catabolism of AGE-peptides by renal proximal tubular cells. Diabetologia 1996;39:149-160.   DOI
15 Zhu P, Xie L, Ding HS, Gong Q, Yang J, Yang L. High mobility group box 1 and kidney diseases (Review). Int J Mol Med 2013;31:763-768.   DOI
16 Calcutt NA, Cooper ME, Kern TS, Schmidt AM. Therapies for hyperglycaemia-induced diabetic complications: from animal models to clinical trials. Nat Rev Drug Discov 2009;8:417-429.   DOI   ScienceOn
17 Donato R, Cannon BR, Sorci G, Riuzzi F, Hsu K, Weber DJ, et al. Functions of S100 proteins. Curr Mol Med 2013;13:24-57.   DOI
18 Salama I, Malone PS, Mihaimeed F, Jones JL. A review of the S100 proteins in cancer. Eur J Surg Oncol 2008;34:357-364.   DOI   ScienceOn
19 Sugaya K, Fukagawa T, Matsumoto K, Mita K, Takahashi E, Ando A, et al. Three genes in the human MHC class III region near the junction with the class II: gene for receptor of advanced glycosylation end products, PBX2 homeobox gene and a notch homolog, human counterpart of mouse mammary tumor gene int-3. Genomics 1994;23:408-419.   DOI   ScienceOn
20 González I, Romero J, Rodríguez BL, Pérez-Castro R, Rojas A. The immunobiology of the receptor of advanced glycation end-products: trends and challenges. Immunobiology 2013;218: 790-797.   DOI   ScienceOn
21 Hudson BI, Carter AM, Harja E, Kalea AZ, Arriero M, Yang H, et al. Identification, classification, and expression of RAGE gene splice variants. FASEB J 2008;22:1572-1580.   DOI
22 Maillard-Lefebvre H, Boulanger E, Daroux M, Gaxatte C, Hudson BI, Lambert M. Soluble receptor for advanced glycation end products: a new biomarker in diagnosis and prognosis of chronic inflammatory diseases. Rheumatology (Oxford) 2009;48:1190-1196.   DOI   ScienceOn
23 Huttunen HJ, Kuja-Panula J, Sorci G, Agneletti AL, Donato R, Rauvala H. Coregulation of neurite outgrowth and cell survival by amphoterin and S100 proteins through receptor for advanced glycation end products (RAGE) activation. J Biol Chem 2000;275:40096-40105.   DOI   ScienceOn
24 Schmidt AM, Yan SD, Yan SF, Stern DM. The biology of the receptor for advanced glycation end products and its ligands. Biochim Biophys Acta 2000;1498:99-111.   DOI   ScienceOn
25 Barnes PJ, Karin M. Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. N Engl J Med 1997;336:1066-1071.   DOI   ScienceOn
26 Yao D, Brownlee M. Hyperglycemia-induced reactive oxygen species increase expression of the receptor for advanced glycation end products (RAGE) and RAGE ligands. Diabetes 2010;59:249-255.   DOI   ScienceOn
27 Neeper M, Schmidt AM, Brett J, Yan SD, Wang F, Pan YC, et al. Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J Biol Chem 1992;267: 14998-15004.
28 Reddy S, Bichler J, Wells-Knecht KJ, Thorpe SR, Baynes JW. N epsilon-(carboxymethyl)lysine is a dominant advanced glycation end product (AGE) antigen in tissue proteins. Biochemistry 1995;34:10872-10878.   DOI   ScienceOn
29 Ramasamy R, Yan SF, Schmidt AM. The diverse ligand repertoire of the receptor for advanced glycation endproducts and pathways to the complications of diabetes. Vascul Pharmacol 2012;57:160-167.   DOI   ScienceOn
30 Xie J, Méndez JD, Méndez-Valenzuela V, Aguilar-Hernández MM. Cellular signalling of the receptor for advanced glycation end products (RAGE). Cell Signal 2013;25:2185-2197.   DOI   ScienceOn
31 Brett J, Schmidt AM, Yan SD, Zou YS, Weidman E, Pinsky D, et al. Survey of the distribution of a newly characterized receptor for advanced glycation end products in tissues. Am J Pathol 1993;143:1699-1712.
32 Ramasamy R, Yan SF, Schmidt AM. RAGE: therapeutic target and biomarker of the inflammatory response: the evidence mounts. J Leukoc Biol 2009;86:505-512.   DOI   ScienceOn
33 Chuah YK, Basir R, Talib H, Tie TH, Nordin N. Receptor for advanced glycation end products and its involvement in inflammatory diseases. Int J Inflam 2013;2013:403460.
34 Li G, Gentil-Perret A, Lambert C, Genin C, Tostain J. S100A1 and KIT gene expressions in common subtypes of renal tumours. Eur J Surg Oncol 2005;31:299-303.   DOI   ScienceOn
35 Lan HY. Transforming growth factor-beta/Smad signalling in diabetic nephropathy. Clin Exp Pharmacol Physiol 2012;39: 731-738.   DOI   ScienceOn
36 Norman J. Fibrosis and progression of autosomal dominant polycystic kidney disease (ADPKD). Biochim Biophys Acta 2011;1812:1327-1336.   DOI   ScienceOn
37 Vernon MA, Mylonas KJ, Hughes J. Macrophages and renal fibrosis. Semin Nephrol 2010;30:302-317.   DOI   ScienceOn
38 Nakamura T, Sato E, Fujiwara N, Kawagoe Y, Yamada S, Ueda Y, et al. Changes in urinary albumin excretion, inflammatory and oxidative stress markers in ADPKD patients with hypertension. Am J Med Sci 2012;343:46-51.   DOI   ScienceOn
39 Park EY, Seo MJ, Park JH. Effects of specific genes activating RAGE on polycystic kidney disease. Am J Nephrol 2010;32: 169-178.   DOI   ScienceOn
40 Lin F, Yang W, Betten M, Teh BT, Yang XJ; French Kidney Cancer Study Group. Expression of S-100 protein in renal cell neoplasms. Hum Pathol 2006;37:462-470.   DOI   ScienceOn
41 Hamberg AP, Korse CM, Bonfrer JM, de Gast GC. Serum S100B is suitable for prediction and monitoring of response to chemoimmunotherapy in metastatic malignant melanoma. Melanoma Res 2003;13:45-49.   DOI   ScienceOn
42 Lee SW, Park KH, Park S, Kim JH, Hong SY, Lee SK, et al. Soluble receptor for advanced glycation end products alleviates nephritis in (NZB/NZW)F1 mice. Arthritis Rheum 2013;65:1902-1912.   DOI   ScienceOn
43 Lin L, Zhong K, Sun Z, Wu G, Ding G. Receptor for advanced glycation end products (RAGE) partially mediates HMGB1- ERKs activation in clear cell renal cell carcinoma. J Cancer Res Clin Oncol 2012;138:11-22.   DOI   ScienceOn
44 Hallam KM, Li Q, Ananthakrishnan R, Kalea A, Zou YS, Vedantham S, et al. Aldose reductase and AGE-RAGE pathways: central roles in the pathogenesis of vascular dysfunction in aging rats. Aging Cell 2010;9:776-784.   DOI   ScienceOn
45 Bolton WK, Cattran DC, Williams ME, Adler SG, Appel GB, Cartwright 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.   DOI   ScienceOn
46 Williams ME, Bolton WK, Khalifah RG, Degenhardt TP, Schotzinger RJ, McGill JB. Effects of pyridoxamine in combined phase 2 studies of patients with type 1 and type 2 diabetes and overt nephropathy. Am J Nephrol 2007;27:605-614.   DOI   ScienceOn
47 Arora MK, Singh UK. Molecular mechanisms in the pathogenesis of diabetic nephropathy: an update. Vascul Pharmacol 2013;58:259-271.   DOI   ScienceOn
48 Ohshiro Y, Ma RC, Yasuda Y, Hiraoka-Yamamoto J, Clermont AC, Isshiki K, et al. Reduction of diabetes-induced oxidative stress, fibrotic cytokine expression, and renal dysfunction in protein kinase Cbeta-null mice. Diabetes 2006;55:3112-3120.   DOI   ScienceOn
49 Asaba K, Tojo A, Onozato ML, Goto A, Quinn MT, Fujita T, et al. Effects of NADPH oxidase inhibitor in diabetic nephropathy. Kidney Int 2005;67:1890-1898.   DOI   ScienceOn
50 Ronco C, Haapio M, House AA, Anavekar N, Bellomo R. Cardiorenal syndrome. J Am Coll Cardiol 2008;52:1527-1539.   DOI   ScienceOn
51 Vlassara H, Uribarri J, Cai W, Goodman S, Pyzik R, Post J, et al. Effects of sevelamer on HbA1c, inflammation, and advanced glycation end products in diabetic kidney disease. Clin J Am Soc Nephrol 2012;7:934-942.   DOI
52 Willemsen S, Hartog JW, Heiner-Fokkema MR, van Veldhuisen DJ, Voors AA. Advanced glycation end-products, a pathophysiological pathway in the cardiorenal syndrome. Heart Fail Rev 2012;17:221-228.   DOI   ScienceOn
53 Bierhaus A, Humpert PM, Morcos M, Wendt T, Chavakis T, Arnold B, et al. Understanding RAGE, the receptor for advanced glycation end products. J Mol Med (Berl) 2005;83: 876-886.   DOI   ScienceOn
54 Nakamura T, Kawagoe Y, Ueda Y, Yamada S, Koide H. Hemoperfusion treatment in a septic shock patient with autosomal dominant polycystic kidney disease and increased HMGB1 protein levels. Blood Purif 2011;32:139-142.   DOI   ScienceOn
55 Singh R, Alavi N, Singh AK, Leehey DJ. Role of angiotensin II in glucose-induced inhibition of mesangial matrix degradation. Diabetes 1999;48:2066-2073.   DOI   ScienceOn
56 Saito A, Takeda T, Sato K, Hama H, Tanuma A, Kaseda R, et al. Significance of proximal tubular metabolism of advanced glycation end products in kidney diseases. Ann N Y Acad Sci 2005; 1043:637-643.   DOI   ScienceOn