Receptor for advanced glycation end products: Its role in Alzheimer's disease and other neurological diseases

Future Neurology

Volumn 4, Issue 2, 2009, Pages 167-177

  Lue, Lih Fen ^a   Walker, Douglas Gordon ^a   Jacobson, Sandra ^a   Sabbagh, Marwan ^a  

^a SUN HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

Advanced glycation end products; Alzheimer's disease; Amyloid peptide; RAGE; RAGE inhibitors; S100 calgranulins; Secreted; Transcript variants

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; AMYLOID BETA PROTEIN; HIGH MOBILITY GROUP B1 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38;

BINDING SITE; BLOOD BRAIN BARRIER; BRAIN ISCHEMIA; CELL ACTIVATION; CELL TYPE; GENE ACTIVATION; GENE EXPRESSION; GENE FUNCTION; GENE INTERACTION; HUMAN; IMMUNOREACTIVITY; LIGAND BINDING; NERVE CELL; NEUROLOGIC DISEASE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW;

EID: 67149113327     PISSN: 14796708     EISSN: None     Source Type: Journal    
DOI: 10.2217/14796708.4.2.167     Document Type: Review

References (89)

1. Schmidt AM, Vianna M, Gerlach 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. 267(21), 14987-14997 (1992).
2. Neeper M, Schmidt AM, Brett J et al.: Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J. Biol. Chem. 267(21), 14998-15004 (1992).
3. Chen X, Walker DG, Schmidt AM, Arancio O, Lue LF, Yan SD: RAGE: a potential target for Aβ-mediated cellular perturbation in Alzheimer's disease: Curr. Mol. Med. 7(8), 735-742 (2007).
4. Deane R, Wu Z, Zlokovic BV: RAGE (yin) versus LRP (yang) balance regulates Alzheimer amyloid β-peptide clearance through transport across the blood-brain barrier. Stroke 35(11 Suppl. 1), 2628-2631 (2004).
5. Maczurek A, Shanmugam K, Munch G: Inflammation and the redox-sensitive AGE-RAGE pathway as a therapeutic target in Alzheimer's disease. Ann. NY Acad. Sci. 1126, 147-151 (2008).
6. Muhammad S, Barakat W, Stoyanov S et al.: The HMGB1 receptor RAGE mediates ischemic brain damage. J. Neurosci. 28(46), 12023-12031 (2008).
7. Qiu J, Nishimura M, Wang Y et al.: Early release of HMGB-1 from neurons after the onset of brain ischemia. J. Cereb. Blood Flow Metab. 28(5), 927-938 (2008).
8. Yan SS, Wu ZY, Zhang HP et al.: Suppression of experimental autoimmune encephalomyelitis by selective blockade of encephalitogenic T-cell infiltration of the central nervous system. Nat. Med. 9(3), 287-293 (2003).
9. Qin J, Goswami R, Dawson S, Dawson G: Expression of the receptor for advanced glycation end products in oligodendrocytes in response to oxidative stress. J. Neurosci. Res. 86(11), 2414-2422 (2008).
10. Iłzecka J: Serum-soluble receptor for advanced glycation endproducts levels in patients with amytrophic lateral sclerosis. Acta Neurol. Scand. DOI: 10.1111/J.1600-0404.2008.011.33.x (2008).
11. Toth C, Martinez J, Zochodne DW: RAGE, diabetes, and the nervous system. Curr. Mol. Med. 7(8), 766-776 (2007).
12. Clynes R, Moser B, Yan SF, Ramasamy R, Herold K, Schmidt AM: Receptor for AGE (RAGE), weaving tangled webs within the inflammatory response. Curr. Mol. Med. 7(8), 743-751 (2007).
13. Logsdon CD, Fuentes MK, Huang EH, Arumugam T: RAGE and RAGE ligands in cancer. Curr. Mol. Med. 7(8), 777-789 (2007).
14. Yamamoto H, Watanabe T, Yamamoto Y et al.: RAGE in diabetic nephropathy. Curr. Mol. Med. 7(8), 752-757 (2007).
15. Hofmann MA, Drury S, Fu C et al.: RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/ calgranulin polypeptides. Cell 97(7), 889-901 (1999).
16. 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. 275(51), 40096-40105 (2000).
17. Wautier JL, Zoukourian C, Chappey O et al.: Receptor-mediated endothelial cell dysfunction in diabetic vasculopathy. Soluble receptor for advanced glycation end products blocks hyperpermeability in diabetic rats. J. Clin. Invest. 97(1), 238-243 (1996).
18. Yan SD, Chen X, Fu J et al.: RAGE and amyloid-β peptide neurotoxicity in Alzheimer's disease. Nature 382(6593), 685-691 (1996).
19. Li J, Schmidt AM: Characterization and functional analysis of the promoter of RAGE, the receptor for advanced glycation end products. J. Biol. Chem. 272(26), 16498-16506 (1997).
20. Bucciarelli LG, Wendt T, Qu W et al.: RAGE blockade stabilizes established atherosclerosis in diabetic apolipoprotein E-null mice. Circulation 106(22), 2827-2835 (2002).
21. Goova MT, Li J, Kislinger T et al.: Blockade of receptor for advanced glycation end-products restores effective wound healing in diabetic mice. Am. J. Pathol. 159(2), 513-525 (2001).
22. Yan SD, Zhu H, Zhu A et al.: Receptor-dependent cell stress and amyloid accumulation in systemic amyloidosis. Nat. Med. 6(6), 643-651 (2000).
23. Wautier JL, Zoukourian C, Chappey O et al.: Receptor-mediated endothelial cell dysfunction in diabetic vasculopathy. Soluble receptor for advanced glycation end products blocks hyperpermeability in diabetic rats. J. Clin. Invest. 97(1), 238-243 (1996).
24. Hudson BI, Carter AM, Harja E et al.: Identification, classification, and expression of RAGE gene splice variants. FASEB J. 22(5), 1572-1580 (2008).
25. Cheng C, Tsuneyama K, Kominami R et al.: Expression profiling of endogenous secretory receptor for advanced glycation end products in human organs. Mod. Pathol. 18(10), 1385-1396 (2005).
26. Raucci A, Cugusi S, Antonelli 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. 22(10), 3716-3727 (2008).
27. Zhang L, Bukulin M, Kojro E et al.: Receptor for advanced glycation end products is subjected to protein ectodomain shedding by metalloproteinases. J. Biol. Chem. 283(51), 35507-35516 (2008).
28. Yonekura H, Yamamoto Y, Sakurai S et al.: Novel splice variants of the receptor for advanced glycation end-products expressed in human vascular endothelial cells and pericytes, and their putative roles in diabetes-induced vascular injury. Biochem. J. 370(Pt 3), 1097-1109 (2003).
29. Sugaya K, Fukagawa T, Matsumoto K 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 23(2), 408-419 (1994).
30. Park IH, Yeon SI, Youn JH et al.: Expression of a novel secreted splice variant of the receptor for advanced glycation end products (RAGE) in human brain astrocytes and peripheral blood mononuclear cells. Mol. Immunol. 40(16), 1203-1211 (2004).
31. Ding Q, Keller JN: Splice variants of the receptor for advanced glycosylation end products (RAGE) in human brain. Neurosci. Lett. 373(1), 67-72 (2005).
32. Malherbe P, Richards JG, Gaillard H et al.: cDNA cloning of a novel secreted isoform of the human receptor for advanced glycation end products and characterization of cells co-expressing cell-surface scavenger receptors and Swedish mutant amyloid precursor protein. Brain Res. Mol. Brain Res. 71(2), 159-170 (1999).
33. Schlueter C, Hauke S, Flohr AM, Rogalla P, Bullerdiek J: Tissue-specific expression patterns of the RAGE receptor and its soluble forms - a result of regulated alternative splicing? Biochim. Biophys. Acta 1630(1), 1-6 (2003).
34. Lue LF, Walker DG, Brachova L et al.: Involvement of microglial receptor for advanced glycation endproducts (RAGE) in Alzheimer's disease: identification of a cellular activation mechanism. Exp. Neurol. 171(1), 29-45 (2001).
35. Jeynes B, Provias J: Evidence for altered expression in Alzheimer lesion pathogenesis. Curr. Alzheimer Res. 5(5), 432-437 (2008).
36. Yan SD, Zhu H, Fu J et al.: Amyloid-β peptide-receptor for advanced glycation endproduct interaction elicits neurottal expression of macrophage-colony stimulating factor: a proinflammatory pathway in Alzheimer disease. Proc. Natl Acad. Sci. USA 94(10), 5296-5301 (1997).
37. Yan SD, Stern D, Kane MD, Kuo YM, Lampert HC, Roher AE: RAGE-Aβ interactions in the pathophysiology of Alzheimer's disease. Restor. Neurol. Neurosci. 12(2-3), 167-173 (1998).
38. Yan SD, Roher A, Chaney M, Zlokovic B, Schmidt AM, Stern D: Cellular cofactors potentiating induction of stress and cytotoxicity by amyloid β-peptide. Biochim. Biophys. Acta 1502(1), 145-157 (2000).
39. Sasaki N, Toki S, Chowei H et al.: Immunohistochemical distribution of the receptor for advanced glycation end products in neurons and astrocytes in Alzheimer's disease. Brain Res. 888(2), 256-262 (2001).
40. Nozaki I, Watanabe T, Kawaguchi M et al.: Reduced expression of endogenous secretory receptor for advanced glycation endproducts in hippocampal neurons of Alzheimer's disease brains. Arch. Histol. Cytol. 70(5), 279-290 (2007).
41. Deane R, Du YS, Submamaryan RK et al.: RAGE mediates amyloid-β peptide transport across the blood-brain barrier and accumulation in brain. Nat. Med. 9(7), 907-913 (2003).
42. Miller MC, Tavares R, Johanson CE et al.: Hippocampal RAGE immunoreactivity in early and advanced Alzheimer's disease. Brain Res. 1230, 273-280 (2008).
43. Donahue JE, Flaherty SL, Johanson CE et al.: RAGE, LRP-1, and amyloid-β protein in Alzheimer's disease. Acta Neuropathol. 112(4), 405-415 (2006).
44. Mackic JB, Stins M, McComb JG et al.: Human blood-brain barrier receptors for Alzheimer's amyloid-β 1-40. Asymmetrical binding, endocytosis, and transcytosis at the apical side of brain microvascular endothelial cell monolayer. J. Clin. Invest. 102(4), 734-743 (1998).
45. Deane R, Zlokovic BV: Role of the blood-brain barrier in the pathogenesis of Alzheimer's disease. Curr. Alzheimer Res. 4(2), 191-197 (2007).
46. Deane R, Sagare A, Zlokovic BV: The role of the cell surface LRP and soluble LRP in blood-brain barrier Aβ clearance in Alzheimer's disease. Curr. Pharm. Des. 14(16), 1601-1605 (2008).
47. Arancio O, Zhang HP, Chen X et al.: RAGE potentiates Aβ-induced perturbation of neuronal function in transgenic mice. EMBO J. 23(20), 4096-4105 (2004).
48. Origlia N, Righi M, Capsoni S et al.: Receptor for advanced glycation end product-dependent activation of p38 mitogen-activated protein kinase contributes to amyloid-β-mediated cortical synaptic dysfunction. J. Neurosci. 28(13), 3521-3530 (2008).
49. Southern L, Williams J, Esiri MM: Immunohistochemical study of N--̇carboxymethyl lysine (CML) in human brain: relation to vascular dementia. BMC Neurol. 7, 35 (2007).
50. Choei H, Sasaki N, Takeuchi M et al.: Glyceraldehyde-derived advanced glycation end products in Alzheimer's disease. Acta Neuropathol. 108(3), 189-193 (2004).
51. Ko LW, Ko EC, Nacharaju P et al.: An immunochemical study on tau glycation in paired helical filaments. Brain Res. 830(2), 301-313 (1999).
52. Sato T, Shimogaito N, Wu X, Kikuchi S, Yamagishi S, Takeuchi M: Toxic advanced glycation end products (TAGE) theory in Alzheimer's disease. Am. J. Alzheimers Dis. Other Demen. 21(3), 197-208 (2006).
53. Shepherd CE, Goyette J, Utter V et al.: Inflammatory S100A9 and S100A12 proteins in Alzheimer's disease. Neurobiol. Aging 27(11), 1554-1563 (2006).
54. Donato R: RAGE: a single receptor for several ligands and different cellular responses: the case of certain S100 proteins. Curr. Mol. Med. 7(8), 711-724 (2007).
55. Businaro R, Leone S, Fabrizi C et al.: S100B protects LAN-5 neuroblastoma cells against Aβ amyloid-induced neurotoxicity via RAGE engagement at low doses but increases Aβ amyloid neurotoxicity at high doses. J. Neurosci. Res. 83(5), 897-906 (2006).
56. Chaney MO, Stine WB, Kokjohn TA et al.: RAGE and amyloid β interactions: atomic force microscopy and molecular modeling. Biochim. Biophys. Acta 1741(1-2), 199-205 (2005).
57. Hudson BI, Wendt T, Bucciarelli LG et al.: Diabetic vascular disease: it's all the RAGE. Antioxid. Redox Signal. 7(11-12), 1588-1600 (2005).
58. Hudson BI, Schmidt AM: RAGE: a novel target for drug intervention in diabetic vascular disease. Pharm. Res. 21(7), 1079-1086 (2004).
59. Kim W, Hudson BI, Moser B et al.: Receptor for advanced glycation end products and its ligands: a journey from the complications of diabetes to its pathogenesis. Ann. NY Acad. Sci. 1043, 553-561 (2005).
60. Myint KM, Yamamoto Y, Sakurai S et al.: Blockade of diabetic vascular injury by controlling of AGE-RAGE system. Curr. Drug Targets 6(4), 447-452 (2005).
61. Sakurai S, Yonekura H, Yamamoto Y et al.: The AGE-RAGE system and diabetic nephropathy. J. Am. Soc. Nephrol. 14(8 Suppl. 3), S259-S263 (2003).
62. Wendt T, Tanji N, Guo J et al.: Glucose, glycation, and RAGE: implications for amplification of cellular dysfunction in diabetic nephropathy. J. Am. Soc. Nephrol. 14(5), 1383-1395 (2003).
63. Yan SF, Ramasamy R, Bucciarelli LG et al.: RAGE and its ligands: a lasting memory in diabetic complications? Diab. Vasc. Dis. Res. 1(1), 10-20 (2004).
64. Jongen C, van der Grand J, Kappelle LJ, Biessels GJ, Viergever MA, Pluim JP: Automated measurement of brain and white matter lesion volume in Type 2 diabetes mellitus. Diabetologia 50(7), 1509-1516 (2007).
65. Brands AM, Biessels GJ, Kappelle LJ et al.: Cognitive functioning and brain MRI in patients with Type 1 and Type 2 diabetes mellitus: a comparative study. Dement. Geriatr. Cogn. Disord. 23(5), 343-350 (2007).
66. Toth C, Schmidt AM, Tuor UI et al.: Diabetes, leukoencephalopathy and RAGE. Neurobiol. Dis. 23(2), 445-461 (2006).
67. Huttunen HJ, Fages C, Rauvala H: Receptor for advanced glycation end products (RAGE)-mediated neurite outgrowth and activation of NF-κB require the cytoplasmic domain of the receptor but different downstream signaling pathways. J. Biol. Chem. 274(28), 19919-19924 (1999).
68. Hermani A, De SB, Medunjanin S, Tessier PA, Mayer D: S100A8 and S100A9 activate MAP kinase and NF-κB signaling pathways and trigger translocation of RAGE in human prostate cancer cells. Exp. Cell Res. 312(2), 184-197 (2006).
69. Yeh CH, Sturgis L, Haidacher J et al.: Requirement for p38 and p44/p42 mitogen-activated protein kinases in RAGE-mediated nuclear factor-κB transcriptional activation and cytokine secretion. Diabetes 50(6), 1495-1504 (2001).
70. Fuentes MK, Nigavekar SS, Arumugam T et al.: RAGE activation by S100P in colon cancer stimulates growth, migration, and cell signaling pathways. Dis. Colon Rectum. 50(8), 1230-1240 (2007).
71. Huang JS, Guh JY, Chen HC, Hung WC, Lai YH, Chuang LY: Role of receptor for advanced glycation end-product (RAGE) and the JAK/STAT-signaling pathway in AGE-induced collagen production in NRK-49F cells. J. Cell Biochem. 81(1), 102-113 (2001).
72. Onyango IG, Tuttle JB, Bennett JP Jr: Altered intracellular signaling and reduced viability of Alzheimer's disease neuronal cybrids is reproduced by β-amyloid peptide acting through receptor for advanced glycation end products (RAGE). Mol. Cell. Neurosci. 29(2), 333-343 (2005).
73. Humpert PM, Djuric Z, Kopf S et al.: Soluble RAGE but not endogenous secretory RAGE is associated with albuminuria in patients with Type 2 diabetes. Cardiovasc. Diabetol. 6, 9 (2007).
74. Katakami N, Matsuhisa M, Kaneto H et al.: Endogenous secretory RAGE but not soluble RAGE is associated with carotid atherosclerosis in Type 1 diabetes patients. Diab. Vasc. Dis. Res. 5(3), 190-197 (2008).
75. Raucci A, Cugusi S, Antonelli 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. 22(10), 3716-3727 (2008).
76. Galichet A, Weibel M, Heizmann CW: Calcium-regulated intramembrane proteolysis of the RAGE receptor. Biochem. Biophys. Res. Commun. 370(1), 1-5 (2008).
77. Bopp C, Hofer S, Weitz J et al.: sRAGE is elevated in septic patients and associated with patients outcome. J. Surg. Res. 147(1), 79-83 (2008).
78. Choi KM, Yoo HJ, Kim HY et al.: Association between endogenous secretory RAGE, inflammatory markers and arterial stiffness. Int. J. Cardiol. 132(1), 96-101 (2009).
79. Emanuele E, D'Angelo A, Tomaino C et al.: Circulating levels of soluble receptor for advanced glycation end products in Alzheimer disease and vascular dementia. Arch. Neurol. 62(11), 1734-1736 (2005).
80. Geroldi D, Falcone C, Emanuele E: Soluble receptor for advanced glycation end products: from disease marker to potential therapeutic target. Curr. Med. Chem. 13(17), 1971-1978 (2006).
81. Ghidoni R, Benussi L, Glionna M et al.: Decreased plasma levels of soluble receptor for advanced glycation end products in mild cognitive impairment. J. Neural. Transm. 115(7), 1047-1050 (2008).
82. Katakami N, Matsuhisa M, Kaneto H et al.: Endogenous secretory RAGE but not soluble RAGE is associated with carotid atherosclerosis in Type 1 diabetes patients. Diab. Vasc. Dis. Res. 5(3), 190-197 (2008).
83. Moser B, Hudson BI, Schmidt AM: Soluble RAGE: a hot new biomarker for the hot joint? Arthritis Res. Ther. 7(4), 142-144 (2005).
84. Nakamura K, Yamagishi S, Adachi H et al.: Serum levels of sRAGE, the soluble form of receptor for advanced glycation end products, are associated with inflammatory markers in patients with Type 2 diabetes. Mol. Med. 13(3-4), 185-189 (2007).
85. Sternberg Z, Weinstock-Guttman B, Hojnacki D et al.: Soluble receptor for advanced glycation end products in multiple sclerosis: a potential marker of disease severity. Mult. Scler. 14(6), 759-763 (2008).
86. Stewart C, Cha S, Caudle RM, Berg K, Katz J: Decreased levels of soluble receptor for advanced glycation end products in patients with primary Sjogren's syndrome. Rheumatol. Int. 28(8), 771-776 (2008).
87. Zhang H, Tasaka S, Shiraishi Y et al.: Role of soluble receptor for advanced glycation end products on endotoxin-induced lung injury. Am. J. Respir. Crit. Care Med. 178(4), 356-362 (2008).
88. Geroldi D, Falcone C, Minoretti P, Emanuele E, Arra M, D'Angelo A: High levels of soluble receptor for advanced glycation end products may be a marker of extreme longevity in humans. J. Am. Geriatr. Soc. 54(7), 1149-1150 (2006).
89. Norata GD, Garlaschelli K, Grigore L et al.: Circulating soluble receptor for advanced glycation end products is inversely associated with body mass index and waist/hip ratio in the general population. Nutr. Metab. Cardiovasc. Dis. DOI: 10.1016/j.numecd.2008.03.004 (2008).