The role of RAGE in amyloid-β peptide-mediated pathology in Alzheimer's disease

Current Opinion in Investigational Drugs

Volumn 10, Issue 7, 2009, Pages 672-680

  Schmidt, Ann Marie ^a   Sahagan, Barbara ^b   Nelson, Robert B ^b   Selmer, Johan ^c   Rothlein, Robert ^c   Bell, Joanne M ^b  

^a Department of Surgery ^*  (United States)

^b PFIZER INC   (United States)

^c TransTech Pharma Inc   (United States)

Author keywords

Alzheimer's disease; Amyloid ; Blood brain barrier; Inflammation; LDL receptor related protein; RAGE; Receptor for advanced glycation endproducts

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; AMYLOID BETA PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; HYBRID PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PF 4494700; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR; TTP 4000; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; BLOOD BRAIN BARRIER; BRAIN REGION; CLINICAL TRIAL; DISEASE COURSE; HUMAN; INFLAMMATION; LEARNING DISORDER; MEDIATOR RELEASE; MEMORY DISORDER; MICROGLIA; MONOCYTE; NEUROPATHOLOGY; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; HUMANS; INFLAMMATION; MICE; MODELS, BIOLOGICAL; NEURODEGENERATIVE DISEASES; RECEPTORS, IMMUNOLOGIC;

EID: 68149132859     PISSN: 14724472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (98)

1. Alzheimer's Assocation: 2009 Alzheimer's disease facts and figures. Alzheimers Demen. (2009) 5(3):234-270.
2. Cummings J, Doody R, Clark C: Disease-modifying therapies for Alzheimer disease: Challenges to early intervention. Neurology. (2007) 69(16):1622-1634.
3. Nunomora A, Moreira PI, Lee HG, Zhu X, Castellani RJ, Smith MA, Perry G: Neuronal death and survival under oxidative stress in Alzheimer and Parkinson diseases. CNS Neurol Disord Drug Targets. (2007) 6(6):411-423
4. Stuchbury G, Munch G: Alzheimer's associated inflammation, potential drug targets and future therapies. J Neural Transm. (2005) 112(3):429-453..
5. Schmidt AM, Vianna M, Gerlach M, Brett J, Ryan J, Kao J, Esposito C, Hegarty H, Hurley H, Clauss M, Wang F 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(21):14987-14997.
6. 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. (1992) 267(21):14998-15004.
7. Moroz OV, Antson AA, Dodson EJ, Burrell HJ, Grist SJ, Lloyd RM, Maitland NJ, Dodson GG, Wilson KS, Lukanidin E, Bronstein IB: The structure of S100A12 in a hexameric form and its proposed role in receptor signalling. Acta Crystallogr D Biol Crystallogr. (2002) 58(Pt 3):407-413.
8. Xie J, Burz DS, He W, Bronstein IB, Lednev I, Shekhtman A: Hexameric calgranulin C (S100A12) binds to the receptor for advanced glycated end products (RAGE) using symmetric hydrophobic target-binding patches. J Biol Chem. (2007) 282(6):4218-4231.
9. Dattilo BM, Fritz G, Leclerc E, Kooi CW, Heizmann CW, Chazin WJ: The extracellular region of the receptor for advanced glycation end products is composed of two independent structural units. Biochemistry. (2007) 46(23):6957-6970.
10. Ostendorp T, Leclerc E, Galichet A, Koch M, Demling N, Weigle B, Heizmann CW, Kroneck PM, Fritz G: Structural and functional insights into RAGE activation by multimeric S100B. EMBO J. (2007) 26(16):3868- 3878.
11. Leclerc E, Fritz G, Weibel M, Heizmann CW, Galichet A: S100B and S100A6 differentially modulate cell survival by interacting with distinct RAGE (receptor for advanced glycation end products) immunoglobulin domains. J Biol Chem. (2007) 282(43):31317-31331.
12. Struchler E, Galichet A, Weibel M, Leclerc E, Heizmann CW: Site-specific blockade of RAGE-Vd prevents amyloid-β oligomer neurotoxicity. J Neurosci. (2008) 28(20):5149-5158.
13. Xie J, Reverdatto S, Frolov A, Hoffmann R, Burz DS, Shekhtman A: Structural basis for pattern recognition by the receptor for advanced glycation end products (RAGE). J Biol Chem. (2008) 283(40):27255-27269.
14. Matsumoto S, Yoshida T, Murata H, Harada S, Fujita N, Nakamura S, Yamamoto Y, Watanabe T, Yonekura H, Yamamoto H, Ohkubo T et al:. Solution structure of the variable-type domain of the receptor for advanced glycation end products: New insights into AGE-RAGE interaction. Biochemistry. (2008) 47(47):12299-12311.
15. Chavakis T, Bierhaus A, Nawroth PP: RAGE (receptor for advanced glycation end products): A central player in the inflammatory response. Microbes Infect. (2004) 6(13):1219-1225.
16. Kokkola R, Andersson A, Mullins G, Ostberg T, Treutiger CJ, Arnold B, Nawroth P, Andersson U, Harris RA, Harris HE: RAGE is the major receptor for the proinflammatory activity of HMGB1 in rodent macrophages. Scand J Immunol. (2005) 61(1):1-9.
17. Schmidt AM, Yan SD, Yan SF, Stern DM: The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J Clin Invest. (2001) 108(7):949-955.
18. Röcken C, Kientsch-Engel R, Mansfeld S, Stix B, Stubenrauch K, Weigle B, Bühling F, Schwan M, Saeger W: Advanced glycation end products and receptor for advanced glycation end products in AA amyloidosis. Am J Pathol. (2003) 162(4):1213-1220.
19. Smith MA, Taneda S, Richey PL, Miyata S, Yan SD, Stern D, Sayre LM, Monnier VM, Perry G: Advanced Maillard reaction end products are associated with Alzheimer disease pathology. Proc Natl Acad Sci USA. (1994) 91(12):5710-5714.
20. Yeh CH, Sturgis L, Haidacher J, Zhang XN, Sherwood SJ, Bjercke RJ, Juhasz 0, Crow MT, Tilton RG, Denner L: Requirement for p38 and p44/p42 mitogen-activated protein kinases in RAGE-mediated nuclear factor- B transcriptional activation and cytokine secretion. Diabetes. (2001) 50(6):1495-1504.
21. Hudson BI, Kalea AZ, Del Mar Arriero M, Harja E, Boulanger E, D'Agati V, Schmidt AM: 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(49):34457-34468.
22. Chang JS, Wendt T, Qu W, Kong L, Zou YS, Schmidt AM, Yan SF: Oxygen deprivation triggers upregulation of early growth response-1 by the receptor for advanced glycation end products. Circ Res. (2008) 102(8):905-913.
23. Tanaka N, Yonekura H, Yamagishi S, Fujimori H, Yamamoto Y, Yamamoto H: The receptor for advanced glycation end products is induced by the glycation products themselves and tumor necrosis factor-α through nuclear factor-κ B, and by 17|β-estradiol through Sp-1 in human vascular endothelial cells. J Biol Chem. (2000) 275(33): 25781-25790.
24. Chen X, Walker DG, Schmidt AM, Arancio O, Lue LF, Yan SD: RAGE: A potential target for A| -mediated cellular perturbation in Alzheimer's disease. Curr Mol Med. (2007) 7(8):735-742.
25. Yan SD, Chen X, Fu J, Chen M, Zhu H, Roher A, Slattery T, Zhao L, Nagashima M, Morser J, Migheli A et al:. RAGE and amyloid-| peptide neurotoxicity in Alzheimer's disease. Nature. (1996) 382(6593):685-691.
26. Du Yan S, Zhu H, Fu J, Yan SF, Roher A, Tourtellotte WW, Rajavashisth T, Chen X, Godman GC, Stern D, Schmidt AM: Amyloid-| peptide-receptor for advanced glycation endproduct interaction elicits neuronal expression of macrophage-colony stimulating factor: A proinflammatory pathway in Alzheimer disease. Proc Natl Acad Sci USA. (1997) 94(10):5296-5301.
27. Yan SD, Zhu H, Zhu A, Golabek A, Du H, Roher A, Yu J, Soto C, Schmidt AM, Stern D, Kindy M: Receptor-dependent cell stress and amyloid accumulation in systemic amyloidosis. Nat Med. (2000) 6(6):643-651.
28. Sousa MM, Yan SD, Stern D, Saraiva MJ: Interaction of the receptor for advanced glycation end products (RAGE) with transthyretin triggers nuclear transcription factor&κB (NF-κB) activation. Lab Invest. (2000) 80(7):1101-1110.
29. Lüth HJ, Ogunlade V, Kuhla B, Kientsch-Engel R, Stahl P, Webster J, Arendt T, Münch G: Age- and stage-dependent accumulation of advanced glycation end products in intracellular deposits in normal and Alzheimer's disease brains. Cereb Cortex. (2005) 15(2):211-220.
30. Petzold A, Jenkins R, Watt HC, Green AJ, Thompson EJ, Keir G, Fox NC, Rossor MN: Cerebrospinal fluid S100B correlates with brain atrophy in Alzheimer's disease. Neurosci Lett. (2003) 336(3):167-170.
31. Sasaki N, Toki S, Chowei H, Saito T, Nakano N, Hayashi Y, Takeuchi M, Makita Z: Immunohistochemical distribution of the receptor for advanced glycation end products in neurons and astrocytes in Alzheimer's disease. Brain Res. (2001) 888(2):256-262.
32. d value close to that observed in mouse endothelial cells and rat cortical neurons and induces oxidative stress.
33. Lue LF, Walker DG, Brachova L, Beach TG, Rogers J, Schmidt AM, Stern DM, Yan SD: Involvement of microglial receptor for advanced glycation endproducts (RAGE) in Alzheimer's disease: Identification of a cellular activation mechanism. Exp Neurol. (2001) 171(1):29-45.Data suggest a positive feedback loop by which Aβ-RAGE-mediated microglial activation enhances the expression of M-CSFs and RAGE, potentially initiating a spiral of cellular activation.
34. Deane R, Du Yan S, Submamaryan RK, LaRue B, Jovanovic S, Hogg E, Welch D, Manness L, Lin C, Yu J, Zhu H et al:. RAGE mediates amyloid-β peptide transport across the blood-brain barrier and accumulation in brain. Nat Med. (2003) 9(7):907-913. Describes the Aβ-RAGE interaction in transgenic mice at the level of the BBB by demonstrating that systemic Aβ infusion interacts with RAGE- bearing cells in vessel walls, culminating in BBB transport of Aβ with the induction of proinflammatory cytokines.
35. Miller MC, Tavares R, Johanson CE, Hovanesian V, Donahue JE, Gonzalez L, Silverberg GD, Stopa EG: Hippocampal RAGE immunoreactivity in early and advanced Alzheimer's disease. Brain Res. (2008) 1230:273-280.
36. Yonekura H, Yamamoto Y, Sakurai S, Petrova RG, Abedin MJ, Li H, Yasui K, Takeuchi M, Makita Z, Takasawa S, Okamoto H 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. (2003) 370(Pt 3):1097-1109.
37. Hudson BI, Carter AM, Harja E, Kalea AZ, Arriero M, Yang H, Grant PJ, Schmidt AM: Identification, classification, and expression of RAGE gene splice variants. FASEB J. (2008) 22(5):1572-1580.
38. Raucci A, Cugusi S, Antonelli A, Barabino SM, Monti L, Bierhaus A, Reiss K, Saftig P, Bianchi ME: A soluble form of the receptor for advanced glycation endproducts (RAGE) is produced by proteolytic cleavage of the membrane-bound form by the sheddase disintegrin and metalloprotease 10 (ADAM10). FASEB J. (2008) 22(10):3716-3727.
39. Emanuele E, D'Angelo A, Tomaino C, Binetti G, Ghidoni R, Politi P, Bernardi L, Maletta R, Bruni AC, Geroldi D: Circulating levels of soluble receptor for advanced glycation end products in Alzheimer disease and vascular dementia. Arch Neurol. (2005) 62(11):1734-1736.
40. Ghidoni R, Benussi L, Glionna M, Franzoni M, Geroldi D, Emanuele E, Binetti G: Decreased plasma levels of soluble receptor for advanced glycation end products in mild cognitive impairment. J Neural Transm. (2008) 115(7):1047-1050.
41. Deane R, Wu Z, Zlokovic B: RAGE (yin) versus LRP (yang) balance regulates Alzheimer amyloidβ-peptide clearance through transport across the blood-brain barrier. Stroke. (2004) 35(Suppl 1):2628-2631.
42. Deane R, Sagare A, Zlokovic B: The role of the cell surface LRP and soluble LRP in blood-brain barrier Aβ clearance in Alzheimer's disease. Curr Pharm Des. (2008) 14(16):1601-1605. A thorough discussion of several mechanisms that lead to high levels of neurotoxic A. p in the AD brain; levels of LRP at the BBB are reduced in the AD brain, which leads to the decreased efflux of brain Aβ and the reduced sequestration of plasma Abeta;, with the subsequent increased re-entry of Aβ into the brain via RAGE.
43. Shibata M, Yamada S, Kumar SR, Calero M, Bading J, Frangione B, Holtzman DM, Miller CA, Strickland DK, Ghiso J, Zlokovic BV: Clearance of Alzheimer's amyloid-β 1-40 peptide from brain by LDL receptor-related protein-1 at the blood brain barrier. J Clin Invest. (2000) 106(12):1489-1499.
44. Deane R, Wu Z, Sagare A, Davis J, Du Yan S, Hamm K, Xu F, Parisi M, LaRue B, Hu HW, Spijkers P et al:. LRP/amyloidβ-protein mediates differential brain efflux of Aβ isoforms. Neuron. (2004) 43(3):333-344.
45. Donahue JE, Flaherty SL, Johanson CE, Duncan JA 3rd, Silverberg GD, Miller MC, Tavares R, Yang W, Wu Q, Sabo E, Hovanesian V et al:. RAGE, LRP-1, and amyloid-β protein in Alzheimer's disease. Acta Neuropathol. (2006) 112(4):405-415.
46. Herring A, Yasin H, Ambree O, Sachser N, Paulus W, Keyvani K: Environmental enrichment counteracts Alzheimer's neurovascular dysfunction in TgCRND8 mice. Brain Pathol. (2008) 18(1):32-39.
47. Arancio O, Zhang HP, Chen X, Lin C, Trinchese F, Puzzo D, Liu S, Hegde A, Yan SF, Stern A, Luddy JS et al:. RAGE potentiates Ap-induced perturbation of neuronal function in transgenic mice. EMBO J. (2004) 23(20):4096-4105.
48. Origlia N, Righi M, Capsoni S, Cattaneo A, Fang F, Stern DM, Chen JX, Schmidt AM, Arancio O, Yan SD, Domenici L: Receptor for advanced glycation end product- dependent activation of p38 mitogen-activated protein kinase contributes to amyloid-β-mediated cortical synaptic dysfunction. J Neurosci. (2008) 28(13):3521-3530.
49. Pfizer Inc: Pfizer and TransTech Pharma enter into agreement for the development and commercialization of RAGE modulators. Press Release. (2006): September 18.
50. Stalder AK, Ermini F, Bondolfi L, Krenger W, Burbach GJ, Deller T, Coomaraswamy J, Staufenbiel M, Landmann R, Jucker M: Invasion of hematopoietic cells into the brain of amyloid precursor protein transgenic mice. J Neurosci. (2005) 25(48):11125-11132.
51. Wegiel J, Imaki H, Wang K-C, Wegiel J, Wronska A, Osuchowski M, Rubenstein R: Origin and turnover of microglial cells in fibrillar plaques of APPsw transgenic mice. Acta Neuropathol. (2003) 105(4):393- 402.
52. Nagele RG, Wegiel J, Venkataraman V, Imaki H, Wang K-C, Wegiel J: Contribution of glial cells to the development of amyloid plaques in Alzheimer's disease. Neurobiol Aging. (2004) 25(5):663-674.
53. Gellermann GP, Ullrich K, Tannert A, Unger C, Habicht G, Sauter SR, Hortschansky P, Horn U, Mollmann U, Decker M, Lehmann J et al:. Alzheimer-like plaque formation by human macrophages is reduced by fibrillation inhibitors and lovastatin. J Mol Biol. (2006) 360(2):251-257.
54. Hickman SE, Allison EK, El KJ: Microglial dysfunction and defectiveβ-amyloid clearance pathways in aging Alzheimer's disease mice. J Neurosci. (2008) 28(33):8354-8360.
55. Simard AR, Soulet D, Gowing G, Julien J-P, Rivest S: Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron. (2006) 49(4):489- 502.
56. Jimenez S, Baglietto-Vargas D, Caballero C, Moreno-Gonzalez I, Torres M, Sanchez-Varo R, Ruano D, Vizuete M, Gutierrez A, Vitorica J: Inflammatory response in the hippocampus of PS1M146L/APP751SL mouse model of Alzheimer's disease: Age-dependent switch in the microglial phenotype from alternative to classic. J Neurosci. (2008) 28(45):11650-11661.
57. Gu L, Hagiwara S, Fan Q, Tanimoto M, Kobata M, Yamashita M, Nishitani T, Gohda T, Ni Z, Qian J, Horikoshi S et al:. Role of receptor for advanced glycation end-products and signalling events in advanced glycation end-product- induced monocyte chemoattractant protein-1 expression in differentiated mouse podocytes. Nephrol Dial Transplant. (2006) 21(2):299-313.
58. Giri R, Shen Y, Stins M, Du Yan S, Schmidt AM, Stern D, Kim KS, Zlokovic B, Kalra VK: β-Amyloid-induced migration of monocytes across human brain endothelial cells involves RAGE and PECAM-1. Am J Physiol. (2000) 279(6):C1772-C1781.
59. Miyata T, Hori O, Zhang J, Yan SD, Ferran L, Iida Y, Schmidt AM: The receptor for advanced glycation end products (RAGE) is a central mediator of the interaction of AGE-2 microglobulin with human mononuclear phagocytes via an oxidant-sensitive pathway: Implications for the pathogenesis of dialysis-related amyloidosis. J Clin Invest. (1996) 98(5):1088-1094.
60. Park L, Anrather J, Forster C, Kazama K, Carlson GA, Iadecola C: A| -induced vascular oxidative stress and attenuation of functional hyperemia in mouse somatosensory cortex. J Cereb Blood Flow Metab. (2004) 24(3):334-342.
61. Paris D, Quadros A, Humphrey J, Patel N, Crescentini R, Crawford F, Mullan M: Nilvadipine antagonizes both A| vasoactivity in isolated arteries, and the reduced cerebral blood flow in APPsw transgenic mice. Brain Res. (2004) 999(1):53-61.
62. Iadecola C: Cerebrovascular effects of amyloid-| peptides: Mechanisms and implications for Alzheimer's dementia. Cell Mol Neurobiol. (2003) 23(4/5):681-689.Reviews the experimental evidence indicating that. Ap exerts profound effects on the regulation of cerebral circulation.
63. Park L, Anrather J, Zhou P, Frys K, Pitstick R, Younkin S, Carlson GA, Iadecola C: NADPH oxidase-derived reactive oxygen species mediate the cerebrovascular dysfunction induced by the amyloidβ peptide. J Neurosci. (2005) 25(7):1769-1777.
64. Wautier M-P, Chappey O, Corda S, Stern DM, Schmidt AM, Wautier J-L: Activation of NADPH oxidase by AGE links oxidant stress to altered gene expression via RAGE. Am J Physiol Endocrinol Metab. (2001) 280(5):E685-E694.
65. -mice. J Clin Invest. (2008) 118(1):183- 194.
66. Chappey 0, Dosquet C, Wautier MP, Wautier JL: Advanced glycation end products, oxidant stress and vascular lesions. Eur J Clin Invest. (1997) 27(2):97-108.
67. Datla SR, Dusting GJ, Mori TA, Taylor CJ, Croft KD, Jiang F: Induction of heme oxygenase-1in vivosuppresses NADPH oxidase-derived oxidative stress. Hypertension. (2007) 50(4):636-642.
68. Pratico D, Uryu K, Leight S, Trojanoswki JQ, Lee VM: Increased lipid peroxidation precedes amyloid plaque formation in an animal model of Alzheimer amyloidosis. J Neurosci. (2001) 21(12):4183-4187.
69. Deane R, Sagare A, Hamm K, Parisi M, Lane S, Finn MB, Holtzman DM, Zlokovic BV: ApoE isoform-specific disruption of amyloidβ peptide clearance from mouse brain. J Clin Invest. (2008) 118(12):4002-4013.
70. Deane R, Zlokovic BV: Role of the blood-brain barrier in the pathogenesis of Alzheimer's disease. Curr Alzheimer Res. (2007) 4(2):191-197.Based upon the neurovascular hypothesis of AD, this review suggests several potential therapeutic approaches for treatment, with RAGE- and LRP1-based strategies as the focus for controlling brain Ap in AD and possibly familial cerebrovascular. p-amyloidoses.
71. Zlokovic BV: Neurovascular mechanisms of Alzheimer's neurodegeneration. Trends Neurosci. (2005) 28(4):202-208An excellent overview of how neurovascular dysfunction contributes to cognitive decline and neurodegeneration in AD.
72. Li M, Shang DS, Zhao WD, Tian L, Li B, Fang WG, Zhu L, Man SM, Chen YH: Amyloidβ interaction with receptor for advanced glycation end products up-regulates brain endothelial CCR5 expression and promotes T cells crossing the blood-brain barrier. J Immunol. (2009) 182(9):5778-5788.
73. Clynes R, Herold K, Schmidt AM: RAGE: Exacting a toll on the host in response to polymicrobial sepsis andListeria monocytogenes.Crit Care. (2007) 11(6):183.
74. Yan SF, Barile GR, D'Agati V, Yan SD, Ramasamy R, Schmidt AM: The biology of RAGE and its ligands: Uncovering mechanisms at the heart of diabetes and its complications. Curr Diab Rep. (2007) 7(2):146-153.
75. Klein WL, Stine WB Jr, Teplow DB: Small assemblies of unmodified amyloidβ-protein are the proximate neurotoxin in Alzheimer's disease. Neurobiol Aging. (2004) 25(5):569-580.
76. Lin L: RAGE on the toll road?Cell Mol Immunol. (2006) 3(5):351-358.
77. Ishihara K, Tsutsumi K, Kawane S, Nakajima M, Kasaoka T: The receptor for advanced glycation endproducts (RAGE) directly binds to ERK by a D-domain like docking site. FEBS Lett. (2003) 550(1-3):107-113.
78. Hofmann MA, Drury S, Fu C, Qu W, Taguchi A, Lu Y, Avila C, Kambham N, Bierhaus A, Nawroth P, Neurath MF et al:. RAGE mediates a novel proinflammatory axis: A central cell surface receptor for S100/calgranulin polypeptides. Cell. (1999) 97(7):889-901.
79. Moser B, Szabolcs MJ, Ankersmit HJ, Lu Y, Qu W, Weinberg A, Herold KC, Schmidt AM: Blockade of RAGE suppresses alloimmune reactionsin vitroand delays allograft rejection in murine heart transplantation. Am J Transplant. (2007) 7(2):293-302.
80. Moser B, Desai DD, Downie MP, Chen Y, Yan SF, Herold K, Schmidt AM, Clynes R: Receptor for advanced glycation end products expression on T cells contributes to antigen-specific cellular expansionin vivo.J Immunol. (2007) 179(12):8051-8058.
81. Collison KS, Parhar RS, Saleh SS, Meyer BF, Kwaasi AA, Hammami MM, Schmidt AM, Stern DM, Al-Mohanna FA:RAGE-mediated neutrophil dysfunction is evoked by advanced glycation endproducts (AGEs). J Leukoc Biol. (2002) 71(3):433-444.
82. Schmidt AM, Yan SD, Brett J, Mora R, Nowygrod R, Stern D:Regulation of human mononuclear phagocyte migration by cell surface-binding proteins for advanced glycation end products. J Clin Invest. (1993) 91(5):2155-2168.
83. Hofmann MA, Drury S, Hudson BI, Gleason MR, Qu W, Lu Y, Lalla E, Chitnis S, Monteiro J, Stickland MH, Bucciarelli LG et al:. RAGE and arthritis: The G82 polymorphism amplifies the inflammatory response. Genes Immun. (2002) 3(3):123-135.
84. Cataldegirmen G, Zeng S, Feirt N, Ippagunta N, Dun H, Qu W, Lu Y, Rong LL, Hofmann MA, Kislinger T, Pachydaki SI et al:. RAGE limits regeneration after massive liver injury by coordinated suppression of TNF-α andNF-kB. J Exp Med. (2005) 201(3):473-484.
85. Toth C, Rong LL, Yang C, Martinez J, Song F, Ramji N, Brussee V, Liu W, Durand J, Nguyen MD, Schmidt AM et al:. Receptor for advanced glycation endproducts (RAGE) and experimental diabetic neuropathy. Diabetes. (2008) 57(4):1002-1017.
86. Bierhaus A, Haslbeck KM, Humpert PM, Liliensiek B, Dehmer T, Morcos M, Sayed AA, Andrassy M, Schiekofer S, Schneider JG, Schulz JB et al:. Loss of pain perception in diabetes is dependent on a receptor of the immunoglobulin superfamily. J Clin Invest. (2004) 114(12):1741-1751.
87. Chou SM, Wang HS, Taniguchi A, Bucala R: Advanced glycation endproducts in neurofilament conglomeration of motoneurons in familial and sporadic amyotrophic lateral sclerosis. Mol Med. (1998) 4(5):324-332.
88. Shibata N, Hirano A, Kato S, Nagai R, Horiuchi S, Komori T, Umahara T, Asayama K, Kobayashi M: Advanced glycation endproducts are deposited in neuronal hyaline inclusions: A study on familial amyotrophic lateral sclerosis with superoxide dismutase-1 mutation. Acta Neuropathol. (1999) 97(3):240-246.
89. Shibata N, Nagai R, Miyata S, Jono T, Horiuchi S, Hirano A, Kato S, Sasaki S, Asayama K, Kobayashi M: Nonoxidative protein glycation is implicated in familial amyotrophic lateral sclerosis with superoxide dismutase-1 mutation. Acta Neuropathol. (2000) 100(3):275-284.
90. Shibata N, Nagai R, Uchida K, Horiuchi S, Yamada S, Hirano A, Kawaguchi M, Yamamoto T, Sasaki S, Kobayashi M:Morphological evidence for lipid peroxidation and protein glycoxidation in spinal cords from sporadic amyotrophic lateral sclerosis patients. Brain Res. (2001) 917(1):97-104.
91. Shibata N, Hirano A, Hedley-Whyte ET, Dal Canto MC, Nagai R, Uchida K, Horiuchi S, Kawaguchi M, Yamamoto T, Kobayashi M: Selective formation of certain advanced glycation endproducts in spinal cord astrocytes of humans and mice with superoxide dismutase-1 mutation. Acta Neuropathol. (2002) 104(2):171-178.
92. Kikuchi S, Shinpo K, Ogata A, Tsuji S, Takeuchi M, Makita Z, Tashiro K: Detection of N&epsi'-(carboxymethyl)lysine (CML) and non-CML advanced glycation end-products in the anterior horn of the amyotrophic lateral sclerosis spinal cord. Amyotroph Lateral Scler Other Motor Neuron Disord. (2002) 3(2): 63-68.
93. Kaufmann E, Boehm BO, Sussmuth SD, Kientsch-Engel R, Sperfeld A, Ludolph AC, Tumani H: The advanced glycation endproduct Nε- (carboxymethyl)lysine level is elevated in cerebrospinal fluid of patients with amyotrophic lateral sclerosis. Neurosci Lett. (2004) 371(2-3):226-229.
94. Kislinger T, Fu C, Huber B, Qu W, Taguchi A, Yan SD, Hofmann M, Yan SF, Pischetsrieder M, Stern D, Schmidt AM: N(ε)-(carboxymethyl)lysine adducts of proteins are ligands for receptor for advanced glycation end products that activate cell signaling pathways and modulate gene expression. J Biol Chem. (1999) 274(44):31740-31749.
95. LoCoco D, Veglianese P, Allievi E, Bendotti C: Distribution and cellular localization of high mobility group box protein 1 (HMGB1) in the spinal cord of a transgenic mouse model of ALS. Neurosci Lett. (2007) 412(1):73-77.
96. Hori O, Brett J, Slattery T, Cao R, Zhang J, Chen, JX, Nagashima M, Lundh ER, Vijay S, Nitecki D, Morser J et al:. The receptor for advanced glycation endproducts (RAGE) is a cellular binding site for amphoterin: Mediation of neurite outgrowth and co-expression of RAGE and amphoterin in the developing nervous system. J Biol Chem. (1995) 270(43):25752- 25761.
97. Izecka J: Serum-soluble receptor for advanced glycation end product levels in patients with amyotrophic lateral sclerosis. Acta Neurol Scand. (2008):doi:10.1111/j.1600-0404.2008.01133.x.
98. Taguchi A, Blood DC, del Toro G, Canet A, Lee DC, Qu W, Tanji N, Lu Y, Lalla E, Fu C, Hofmann MA et al:. Blockade of RAGE- amphoterin signaling suppresses tumour growth and metastases. Nature. (2000) 405(6784):354-360.