Crosstalk between calcium, amyloid β and the receptor for advanced glycation endproducts in Alzheimer's disease

Reviews in the Neurosciences

Volumn 20, Issue 2, 2009, Pages 95-110

  Leclerc, Estelle ^a   Sturchler, Emmanuel ^b   Vetter, Stefan W ^a   Heizmann, Claus W ^c  

^a FLORIDA ATLANTIC UNIVERSITY   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

AGEs; Alzheimer's disease; Calcium; Neurodegenerative diseases; RAGE; S100 proteins; amyloid peptide

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ADVANCED GLYCATION END PRODUCT RECEPTOR; AMYLOID BETA PROTEIN; CALCIUM; CALCIUM BINDING PROTEIN; HIGH MOBILITY GROUP B1 PROTEIN; PROTEIN S 100; PROTEIN S100B; TAU PROTEIN;

ALZHEIMER DISEASE; BLOOD BRAIN BARRIER; HIPPOCAMPUS; HUMAN; INFLAMMATION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RECEPTOR UPREGULATION; REVIEW; SIGNAL TRANSDUCTION;

EID: 69749096429     PISSN: 03341763     EISSN: None     Source Type: Journal    
DOI: 10.1515/REVNEURO.2009.20.2.95     Document Type: Review

References (164)

1. Akiyama H, Ikeda K, Katoh M, McGeer EG, McGeer PL. Expression of MRP14, 27E10, interferon-alpha and leukocyte common antigen by reactive microglia in postmortem human brain tissue. J Neuroimmunol 1994; 50: 195-201.
2. Arancio O, Zhang HP, Chen X, Lin C, Trinchese F, Puzzo D, Liu S, Hegde A, Yan SF, Stern A, Luddy JS, Lue LF, Walker DG, Roher A, Buttini M, Mucke L, Li W, Schmidt AM, Kindy M, Hyslop PA, Stern DM, Du Yan SS. RAGE potentiates Abeta-induced perturbation of neuronal function in transgenic mice. EMBO J 2004; 23: 4096-4105. (Pubitemid 39472430)
3. Arispe N, Pollard HB, Rojas E. Giant multilevel cation channels formed by Alzheimer disease amyloid beta-protein [A beta P-(1-40)] in bilayer membranes. Proc Natl Acad Sci USA 1993; 90: 10573-10577. (Pubitemid 23347084)
4. 2+/ calmodulin-dependent protein kinase II. J Biol Chem 1988; 263: 5876-5883. (Pubitemid 18122937)
5. Bernstein HG, Blazejczyk M, Rudka T, Gundelfinger ED, Dobrowolny H, Bogerts B, Kreutz MR, Kuznicki J, Wojda U. The Alzheimer disease-related calcium-binding protein calmyrin is present in human forebrain with an altered distribution in Alzheimer's as compared to normal ageing brains. Neuropathol Appl Neurobiol 2005; 31: 314-324. (Pubitemid 40769530)
6. Boom A, Pochet R, Authelet M, Pradier L, Borghgraef P, Van Leuven F, Heizmann CW, Brion JP. Astrocytic calcium/zinc binding protein S100A6 overexpression in Alzheimer's disease and in PS1/APP transgenic mice models. Biochim Biophys Acta 2004; 1742: 161-168. (Pubitemid 39601776)
7. Boyd JH, Kan B, Roberts H, Wang Y, Walley KR. S100A8 and S100A9 mediate endotoxin-induced cardiomyocyte dysfunction via the receptor for advanced glycation end products. Circ Res 2008; 102: 1239-1246.
8. Brett J, Schmidt AM, Yan SD, Zou YS, Weidman E, Pinsky D, Nowygrod R, Neeper M, Przysiecki C, Shaw A, 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. (Pubitemid 24058273)
9. Businaro R, Leone S, Fabrizi C, Sorci G, Donato R, Lauro GM, Fumagalli L. S100B protects LAN-5 neuroblastoma cells against Abeta amyloid-induced neurotoxicity via RAGE engagement at low doses but increases Abeta amyloid neurotoxicity at high doses. J Neurosci Res 2006; 83: 897-906.
10. Buxbaum JD. A role for calsenilin and related proteins in multiple aspects of neuronal function. Biochem Biophys Res Commun 2004; 322: 1140-1144.
11. Buxbaum JN, Ye Z, Reixach N, Friske L, Levy C, Das P, Golde T, Masliah E, Roberts AR, Bartfai T. Transthyretin protects Alzheimer's mice from the behavioral and biochemical effects of Abeta toxicity. Proc Natl Acad Sci USA 2008; 105: 2681-2686.
12. Casley CS, Canevari L, Land JM, Clark JB, Sharpe MA. Beta-amyloid inhibits integrated mitochondrial respiration and key enzyme activities. J Neurochem 2002; 80: 91-100. (Pubitemid 34614581)
13. Caso JR, Pradillo JM, Hurtado O, Leza JC, Moro MA, Lizasoain I. Toll-like receptor 4 is involved in subacute stress-induced neuroinflammation and in the worsening of experimental stroke. Stroke 2008; 39: 1314-1320.
14. Chaney MO, Stine WB, Kokjohn TA, Kuo YM, Esh C, Rahman A, Luehrs DC, Schmidt AM, Stem D, Yan SD, Roher AE. RAGE and amyloid beta interactions: atomic force microscopy and molecular modeling. Biochim Biophys Acta 2005; 1741: 199-205. (Pubitemid 40825005)
15. Chavakis T, Bierhaus A, Al-Fakhri N, Schneider D, Witte S, Linn T, Nagashima M, Morser J, Arnold B, Preissner KT, Nawroth PP. 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. (Pubitemid 37467165)
16. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, Selkoe DJ, Ashe KH. Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 2005; 8: 79-84.
17. Cole SL, Vassar R. The role of amyloid precursor protein processing by BACE1, the beta-secretase, in Alzheimer disease pathophysiology. J Biol Chem 2008; 283: 29621-29625.
18. Craft JM, Watterson DM, Marks A, Van Eldik LJ. Enhanced susceptibility of S-100B transgenic mice to neuroinflammation and neuronal dysfunction induced by intracerebroventricular infusion of human beta-amyloid. Glia 2005; 51: 209-216. (Pubitemid 41297427)
19. Curtain CC, Ali F, Volitakis I, Cherny RA, Norton RS, Beyreuther K, Barrow CJ, Masters CL, Bush AI, Barnham KJ. Alzheimer's disease amyloid-beta binds copper and zinc to generate an allosterically ordered membrane-penetrating structure containing superoxide dismutase-like subunits. J Biol Chem 2001; 276: 20466-20473. (Pubitemid 37411129)
20. Dahlgren KN, Manelli AM, Stine WB Jr, Baker LK, Krafft GA, LaDu MJ. Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. J Biol Chem 2002; 277: 32046-32053.
21. 2+ levels regulate the alternative cell density-dependent secretion of S100B in human glioblastoma cells. J Biol Chem 2001; 276: 30819-30826. (Pubitemid 37384941)
22. Deane R, Du Yan S, Submamaryan RK, LaRue B, Jovanovic S, Hogg E, Welch D, Manness L, Lin C, Yu J, Zhu H, Ghiso J, Frangione B, Stern A, Schmidt AM, Armstrong DL, Arnold B, Liliensiek B, Nawroth P, Hofman F, Kindy M, Stern D, Zlokovic B. RAGE mediates amyloid-beta peptide transport across the blood-brain barrier and accumulation in brain. Nat Med 2003; 9: 907-913. (Pubitemid 36889934)
23. Demuro A, Mina E, Kayed R, Milton SC, Parker I, Glabe CG. Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers. J Biol Chem 2005; 280: 17294-17300. (Pubitemid 41389198)
24. Deshpande A, Mina E, Glabe C, Busciglio J. Different conformations of amyloid beta induce neurotoxicity by distinct mechanisms in human cortical neurons. J Neurosci 2006; 26: 6011-6018. (Pubitemid 44318367)
25. Dickson DW, Sinicropi S, Yen SH, Ko LW, Mattiace LA, Bucala R, Vlassara H. Glycation and microglial reaction in lesions of Alzheimer's disease. Neurobiol Aging 1996; 17: 733-743. (Pubitemid 26348874)
26. Ding Q, Keller JN. Splice variants of the receptor for advanced glycosylation end products (RAGE) in human brain. Neurosci Lett 2005; 373: 67-72. (Pubitemid 39536223)
27. Donato R. Intracellular and extracellular roles of S100 proteins. Microsc Res Tech 2003; 60: 540-551.
28. Donato R. RAGE: a single receptor for several ligands and different cellular responses: the case of certain SlOO proteins. Curr Mol Med 2007; 7: 711-724.
29. Donato R. S100B's double life: intracellular and extracellular signal. Biochim Biophys Acta: Mol Cell Res 2009; in press.
30. Dougherty JJ, Wu J, Nichols RA. Beta-amyloid regulation of presynaptic nicotinic receptors in rat hippocampus and neocortex. J Neurosci 2003; 23: 6740-6747.
31. Du Yan S, Zhu H, Fu J, Yan SF, Roher A, Tourtellotte WW, Rajavashisth T, Chen X, Godman GC, Stern D, Schmidt AM. Amyloid-beta 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: 5296-5301. (Pubitemid 27214777)
32. Dyck RH, Bogoch H, Marks A, Melvin NR, Teskey GC. Enhanced epileptogenesis in S100B knockout mice. Brain Res Mol Brain Res 2002; 106: 22-29. (Pubitemid 35223276)
33. Emanuele E, D'Angelo A, Tomaino C, Binetti G, Ghidoni R, Politi P, Bemardi 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: 1734-1736. (Pubitemid 41626671)
34. Esposito G, Scuderi C, Lu J, Savani C, De Filippis D, Iuvone T, Steardo L Jr, Sheen V, Steardo L. S100B induces tau protein hyperphosphorylation via Dickopff-1 up-regulation and disrupts the Wnt pathway in human neural stem cells. J Cell Mol Med 2008; 12: 914-927. (Pubitemid 351718070)
35. Foell D, Wittkowski H, Vogl T, Roth J. S100 proteins expressed in phagocytes: a novel group of damage-associated molecular pattern molecules. J Leukoc Biol 2007; 81: 28-37. (Pubitemid 46021248)
36. Fritz G, Heizmann CW. 3D structures of the calcium and zinc binding S100 proteins. In: Messerschmidt A, Bode W, Cygler M, eds. Handbook of Metalloproteins, Vol.3. Chichester: Wiley, 2004; 529-540.
37. Galichet A, Weibel M, Heizmann CW. Calcium-regulated intramembrane proteolysis of the RAGE receptor. Biochem Biophys Res Commun 2008; 370: 1-5.
38. Gasic-Milenkovic J, Dukic-Stefanovic S, Deuther-Conrad W, Gartner U, Munch G. Beta-amyloid peptide potentiates inflammatory responses induced by lipopolysaccharide, interferon-gamma and 'advanced glycation endproducts' in a murine microglia cell line. Eur J Neurosci 2003; 17: 813-821. (Pubitemid 36315251)
39. Ghavami S, Rashedi I, Dattilo BM, Eshraghi M, Chazin WJ, Hashemi M, Wesselborg S, Kerkhoff C, Los M. S100A8/A9 at low concentration promotes tumor cell growth via RAGE ligation and MAP kinase-dependent pathway. J Leukoc Biol 2008; 83: 1484-1492. (Pubitemid 351960330)
40. 2+-binding helix-loop-helix EF-hand motifs. Biochem J 2007; 405: 199-201.
41. Glenner GG, Wong CW. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 1984; 120: 885-890. (Pubitemid 14104991)
42. 2+ channels. J Neurochem 2001; 77: 953-956. (Pubitemid 32466792)
43. Guo Q, Christakos S, Robinson N, Mattson MP. Calbindin D28k blocks the proapoptotic actions of mutant presenilin 1: reduced oxidative stress and preserved mitochondrial function. Proc Natl Acad Sci USA 1998; 95: 3227-3232. (Pubitemid 28135884)
44. Haass C, Schlossmacher MG, Hung AY, Vigo-Pelfrey C, Mellon A, Ostaszewski BL, Lieberburg I, Koo EH, Schenk D, Teplow DB, et al. Amyloid beta-peptide is produced by cultured cells during normal metabolism. Nature 1992; 359: 322-325.
45. Hadding A, Kaltschmidt B, Kaltschmidt C. Overexpression of receptor of advanced glycation end products hypersensitizes cells for amyloid beta peptide-induced cell death. Biochim Biophys Acta 2004; 1691: 67-72. (Pubitemid 38410951)
46. Hara MR, Snyder SH. Cell signaling and neuronal death. Annu Rev Pharmacol Toxicol 2007; 47: 117-141.
47. Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002; 297: 353-356. (Pubitemid 34790756)
48. Hardy JA, Higgins GA. Alzheimer's disease: the amyloid cascade hypothesis. Science 1992; 256: 184-185.
49. Hartley DM, Walsh DM, Ye CP, Diehl T, Vasquez S, Vassilev PM, Teplow DB, Selkoe DJ. Protofibrillar intermediates of amyloid beta-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons. J Neurosci 1999; 19: 8876-8884. (Pubitemid 30226709)
50. Heizmann CW, Ackermann GE, Galichet A. Pathologies involving the S100 proteins and RAGE. Subcell Biochem 2007; 45: 93-138.
51. Heizmann CW, Fritz G, Schäfer BW. S100 proteins: structure, functions and pathology. Front Biosci 2002; 7: d1356-1368.
52. Hensley K, Carney JM, Mattson MP, Aksenova M, Harris M, Wu JF, Floyd RA, Butterfield DA. A model for beta-amyloid aggregation and neurotoxicity based on free radical generation by the peptide: relevance to Alzheimer disease. Proc Natl Acad Sci USA 1994; 91: 3270-3274. (Pubitemid 24130218)
53. Hickman SE, Allison EK, El Khoury J. Microglial dysfunction and defective beta-amyloid clearance pathways in aging Alzheimer's disease mice. J Neurosci 2008; 28: 8354-8360.
54. Hofrnann MA, Drury S, Fu C, Qu W, Taguchi A, Lu Y, Avila C, Kambham N, Bierhaus A, Nawroth P, Neurath MF, Slattery T, Beach D, McClary J, Nagashima M, Morser J, Stern D, Schmidt AM. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell 1999; 97: 889-901. (Pubitemid 29375048)
55. Hori O, Brett J, Slattery T, Cao R, Zhang J, Chen JX, Nagashima M, Lundh ER, Vijay S, Nitecki D, et al. The receptor for advanced glycation end products (RAGE) is a cellular binding site for amphoteric Mediation of neurite outgrowth and co-expression of RAGE and amphoterin in the developing nervous system. J Biol Chem 1995; 270: 25752-25761.
56. Hou X, Parkington HC, Coleman HA, Mechler A, Martin LL, Aguilar MI, Small DH. Transthyretin oligomers induce calcium influx via voltage-gated calcium channels. J Neurochem 2007; 100: 446-457. (Pubitemid 46011005)
57. Hoyaux D, Alao J, Fuchs J, Kiss R, Keller B, Heizmann CW, Pochet R, Frermann D. S100A6, a calcium- and zinc-binding protein, is overexpressed in SOD1 mutant mice, a model for amyotrophic lateral sclerosis. Biochim Biophys Acta 2000; 1498: 264-272.
58. Hsia AY, Masliah E, McConlogue L, Yu GQ, Tatsuno G, Hu K, Kholodenko D, Malenka RC, Nicoll RA, Mucke L. Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc Natl Acad Sci USA 1999; 96: 3228-3233. (Pubitemid 29148873)
59. Huang TH, Yang DS, Fraser PE, Chakrabartty A. Alternate aggregation pathways of the Alzheimer beta-amyloid peptide. An in vitro model of preamyloid. J Biol Chem 2000; 275: 36436-36440. (Pubitemid 30841201)
60. 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: 1572-1580. (Pubitemid 351656797)
61. 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: 34457-34468.
62. 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. (Pubitemid 32064635)
63. Iribarren P, Zhou Y, Hu J, Le Y, Wang JM. Role of formyl peptide receptor-like 1 (FPRL1/FPR2) in mononuclear phagocyte responses in Alzheimer disease. Immunol Res 2005; 31: 165-176. (Pubitemid 40628955)
64. Ishihara K, Tsutsumi K, Kawane S, Nakajima M, Kasaoka T. The receptor for advanced glycation end-products (RAGE) directly binds to ERK by a D-domain-like docking site. FEBS Lett 2003; 550: 107-113. (Pubitemid 37281366)
65. Jhamandas JH, MacTavish D. Antagonist of the amylin receptor blocks beta-amyloid toxicity in rat cholinergic basal forebrain neurons. J Neurosci 2004; 24: 5579-5584. (Pubitemid 38812640)
66. Kagan BL, Hirakura Y, Azimov R, Azimova R, Lin MC. The channel hypothesis of Alzheimer's disease: current status. Peptides 2002; 23: 1311-1315. (Pubitemid 34786709)
67. 2+ modulator matures human hair cuticle. J Biol Chem 2008; 283: 5004-5013.
68. Klein WL. Abeta toxicity in Alzheimer's disease: globular oligomers (ADDLs) as new vaccine and drug targets. Neurochem Int 2002; 41: 345-352.
69. Kögel D, Peters M, König HG, Hashemi SMA, Bui NT, Arolt V, Rothermundt M, Prehn JHM. S100B potently activates p65/c-Rel transcriptional complexes in hippocampal neurons: clinical implications for the role of S100B in excitotoxic brain injury. Neuroscience 2004; 127: 913-920. (Pubitemid 39099556)
70. Kosik KS, Joachim CL, Selkoe DJ. Microtubule-associated protein tau (tau) is a major antigenic component of paired helical filaments in Alzheimer disease. Proc Natl Acad Sci USA 1986; 83: 4044-4048. (Pubitemid 16062419)
71. Krebs J, Heizmann CW. Calcium-binding proteins and the EF-hand principle. In: Krebs J, Michalak M, eds. Calcium: A Matter of Life or Death. Amsterdam: Elsevier, 2007; 51-93.
72. Kyriakis JM, Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 2001; 81: 807-869. (Pubitemid 32267078)
73. LaFerla FM, Green KN, Oddo S. Intracellular amyloid-beta in Alzheimer's disease. Nat Rev Neurosci 2007; 8: 499-509. (Pubitemid 46985362)
74. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trammer B, Viola KL, Wals P, Zhang C, Finch CE, Krafft GA, Klein WL. Diffusible, nonfibrillar ligands derived from Abeta 1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 1998; 95: 6448-6453. (Pubitemid 28249033)
75. Lashuel HA, Hartley D, Petre BM, Walz T, Lansbury PT Jr. Neurodegenerative disease: amyloid pores from pathogenic mutations. Nature 2002; 418: 291. (Pubitemid 34790672)
76. Leclerc E, Fritz G, Vetter SW, Heizmann CW. Binding of S100 proteins to RAGE: an update. Biochim Biophys Acta: Mol Cell Res 2009; in press.
77. 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: 31317-31331. (Pubitemid 350044892)
78. Leclerc E, Starchler, E., Heizmann, CW. The EF-hand calcium-binding sensor in the CNS. In: Mikoshiba K, ed. Handbook of Neurochemistry and Molecular Neurobiology. New York: Springer Publishers, 2008.
79. Leissring MA. The AbetaCs of Abeta-cleaving proteases. J Biol Chem 2008; 283: 29645-29649.
80. Leukert N, Vogl T, Strupat K, Reichelt R, Sorg C, Roth J. Calcium-dependent tetramer formation of S100A8 and S100A9 is essential for biological activity. J Mol Biol 2006; 359: 961-972. (Pubitemid 43831924)
81. Li Y, Wang J, Sheng JG, Liu L, Barger SW, Jones RA, Van Eldik LJ, Mrak RE, Griffin WS. SlOO beta increases levels of beta-amyloid precursor protein and its encoding mRNA in rat neuronal cultures. J Neurochem 1998; 71: 1421-1428. (Pubitemid 28443012)
82. Lian Q, Ladner CJ, Magnuson D, Lee JM. Selective changes of calcineurin (protein phosphatase 2B) activity in Alzheimer's disease cerebral cortex. Exp Neurol 2001; 167: 158-165. (Pubitemid 32066418)
83. Link CD. Expression of human beta-amyloid peptide in transgenic Caenorhabditis elegans. Proc Natl Acad Sci USA 1995; 92: 9368-9372.
84. Lovell MA, Robertson JD, Teesdale WJ, Campbell JL, Markesbery WR. Copper, iron and zinc in Alzheimer's disease senile plaques. J Neurol Sci 1998; 158: 47-52.
85. Lue LF, Walker DG, Brachova L, Beach TG, Rogers J, Schmidt AM, Stem 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: 29-45. (Pubitemid 32848443)
86. Malherbe P, Richards JG, Gaillard H, Thompson A, Diener C, Schuler A, Huber G. 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 1999; 71: 159-170. (Pubitemid 29492960)
87. Marenholz I, Heizmann CW, Fritz G. S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature). Biochem Biophys Res Commun 2004; 322: 1111-1122. (Pubitemid 39164640)
88. Marenholz I, Lovering RC, Heizmann CW. An update of the S100 nomenclature. Biochim Biophys Acta 2006; 1763: 1282-1283.
89. Marshak DR, Pesce SA, Stanley LC, Griffin WS. Increased S100 beta neurotrophic activity in Alzheimer's disease temporal lobe. Neurobiol Aging 1992; 13: 1-7.
90. Mattson MP, Chan SL. Neuronal and glial calcium signaling in Alzheimer's disease. Cell Calcium 2003; 34: 385-397. (Pubitemid 37021231)
91. McLean CA, Cherny RA, Fraser FW, Fuller SJ, Smith MJ, Beyreuther K, Bush AI, Masters CL. Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol 1999; 46: 860-866.
92. 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.
93. Minkeviciene R, Banerjee P, Tanila H. Memantine improves spatial learning in a transgenic mouse model of Alzheimer's disease. J Pharmacol Exp Ther 2004; 311: 677-682. (Pubitemid 39391555)
94. Moroz OV, Dodson GG, Wilson KS, Lukanidin E, Bronstein IB. Multiple structural states of S100A12: a key to its functional diversity. Microsc Res Tech 2003; 60: 581-592.
95. Mrak RE, Griffin WS. The role of activated astrocytes and of the neurotrophic cytokine S100B in the pathogenesis of Alzheimer's disease. Neurobiol Aging 2001; 22: 915-922.
96. Mruthinti S, Sood A, Humphrey CL, Swamy-Mruthinti S, Buccafusco JJ. The induction of surface beta-amyloid binding proteins and enhanced cytotoxicity in cultured PC-12 and IMR-32 cells by advanced glycation end products. Neuroscience 2006; 142: 463-473. (Pubitemid 44415326)
97. Muller-Hill B, Beyreuther K. Molecular biology of Alzheimer's disease. Annu Rev Biochem 1989; 58: 287-307.
98. Nagele RG, D'Andrea MR, Anderson WJ, Wang HY. Intracellular accumulation of beta-amyloid(1-42) in neurons is facilitated by the alpha 7 nicotinic acetylcholine receptor in Alzheimer's disease. Neuroscience 2002; 110: 199-211.
99. Neeper M, Schmidt AM, Brett J, Yan SD, Wang F, Pan YC, Elliston K, Stem D, Shaw A. Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J Biol Chem 1992; 267: 14998-15004.
100. Nozaki I, Watanabe T, Kawaguchi M, Akatsu H, Tsuneyama K, Yamamoto Y, Ohe K, Yonekura H, Yamada M, Yamamoto H. Reduced expression of endogenous secretory receptor for advanced glycation endproducts in hippocampal neurons of Alzheimer's disease brains. Arch Histol Cytol 2007; 70: 279-290. (Pubitemid 351594919)
101. Onyango IG, Tuttle JB, Bennett JP Jr. Altered intracellular signaling and reduced viability of Alzheimer's disease neuronal cybrids is reproduced by beta-amyloid peptide acting through receptor for advanced glycation end products (RAGE). Mol Cell Neurosci 2005; 29: 333-343.
102. Origlia N, Righi M, Capsoni S, Cattaneo A, Fang F, Stem 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-beta-mediated cortical synaptic dysfunction. J Neurosci 2008; 28: 3521-3530.
103. 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: 3868-3878 (Pubitemid 47295872)
104. Peretz D, Scott MR, Groth D, Williamson RA, Burton DR, Cohen FE, Prusiner SB. Strain-specified relative conformational stability of the scrapie prion protein. Protein Sci 2001; 10: 854-863. (Pubitemid 32240511)
105. Perrone L, Peluso G, Melone MA. RAGE recycles at the plasma membrane in S100B secretory vesicles and promotes Schwann cells morphological changes. J Cell Physiol 2008; 217: 60-71.
106. Peskind ER, Griffin WS, Akama KT, Raskind MA, Van Eldik LJ. Cerebrospinal fluid S100B is elevated in the earlier stages of Alzheimer's disease. Neurochem Int 2001; 39: 409-413. (Pubitemid 32907405)
107. Petkova AT, Leapman RD, Guo Z, Yau WM, Mattson MP, Tycko R. Self-propagating, molecular-level polymorphism in Alzheimer's beta-amyloid fibrils. Science 2005; 307: 262-265. (Pubitemid 40116242)
108. Ponath G, Schettler C, Kaestner F, Voigt B, Wentker D, Arolt V, Rothermundt M. Autocrine S100B effects on astrocytes are mediated via RAGE. J Neuroimmunol 2007; 184: 214-222. (Pubitemid 46366005)
109. Quist A, Doudevski I, Lin H, Azimova R, Ng D, Frangione B, Kagan B, Ghiso J, Lal R. Amyloid ion channels: a common structural link for protein-misfolding disease. Proc Natl Acad Sci USA 2005; 102: 10427-10432. (Pubitemid 41061570)
110. Ramasamy R, Vannucci SJ, Yan SS, Herold K, Yan SF, Schmidt AM. Advanced glycation end products and RAGE: a common thread in aging, diabetes, neurodegeneration, and inflammation. Glycobiology 2005; 15: 16R-28R. (Pubitemid 41417992)
111. 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 a disintegrin and metalloprotease 10 (ADAM10). FASEB J 2008; 22: 3716-3727.
112. Reisberg B, Doody R, Stoffler A, Schmitt F, Ferris S, Mobius HJ. Memantine in moderate-to-severe Alzheimer's disease. N Engl J Med 2003; 348: 1333-1341. (Pubitemid 36384100)
113. Rothermundt M, Peters M, Prehn JH, Arolt V. S100B in brain damage and neurodegeneration. Microsc Res Tech 2003; 60: 614-632.
114. Santamaria-Kisiel L, Rintala-Dempsey AC, Shaw GS. Calcium-dependent and -independent interactions of the S100 protein family. Biochem J 2006; 396: 201-214. (Pubitemid 43837235)
115. Sasaki N, Fukatsu R, Tsuzuki K, Hayashi Y, Yoshida T, Fujii N, Koike T, Wakayama I, Yanagihara R, Garruto R, Amano N, Makita Z. Advanced glycation end products in Alzheimer's disease and other neurodegenerative diseases. Am J Pathol 1998; 153: 1149-1155. (Pubitemid 28465838)
116. Sasaki N, Takeuchi M, Chowei H, Kikuchi S, Hayashi Y, Nakano N, Ikeda H, Yamagishi S, Kitamoto T, Saito T, Makita Z. Advanced glycation end products (AGE) and their receptor (RAGE) in the brain of patients with Creutzfeldt-Jakob disease with prion plaques. Neurosci Lett 2002; 326: 117-120. (Pubitemid 34607573)
117. Schaub MC, Heizmann CW. Calcium, troponin, calmodulin, S100 proteins: from myocardial basics to new therapeutic strategies. Biochem Biophys Res Commun 2008; 369: 247-264.
118. 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 2003; 1630: 1-6.
119. Schmidt A, Kuhla B, Bigl K, Munch G, Arendt T. Cell cycle related signaling in Neuro2a cells proceeds via the receptor for advanced glycation end products. J Neural Transm 2007; 114: 1413-1424. (Pubitemid 350112287)
120. Schmidt AM, Hofmann M, Taguchi A, Yan SD, Stem DM. RAGE: a multiligand receptor contributing to the cellular response in diabetic vasculopathy and inflammation. Semin Thromb Heniost 2000; 26: 485-493.
121. Schmidt AM, Vianna M, Gerlach M, Brett J, Ryan J, Kao J, Esposito C, Hegarty H, Hurley W, Clauss 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.
122. Schmidt AM, Yan SD, Yan SF, Stem DM. The biology of the receptor for advanced glycation end products and its ligands. Biochim Biophys Acta 2000; 1498: 99-111.
123. Schwaller B, Meyer M, Schiffmann S. 'New' functions for 'old' proteins: the role of the calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum 2002; 1: 241-258.
124. Schwarzman AL, Tsiper M, Wente H, Wang A, Vitek MP, Vasiliev V, Goldgaber D. Amyloidogenic and anti-amyloidogenic properties of recombinant transthyretin variants. Amyloid 2004; 11: 1-9. (Pubitemid 38680232)
125. Seubert P, Vigo-Pelfrey C, Esch F, Lee M, Dovey H, Davis D, Sinha S, Schlossmacher M, Whaley J, Swindlehurst C, et al. Isolation and quantification of soluble Alzheimer's beta-peptide from biological fluids. Nature 1992; 359: 325-327.
126. Sevillano N, Giron MD, Salido M, Vargas AM, Vilches J, Salto R. Internalization of the receptor for advanced glycation end products (RAGE) is required to mediate intracellular responses. J Biochem 2009; 145: 21-30.
127. Shepherd CE, Goyette J, Utter V, Rahimi F, Yang Z, Geczy CL, Halliday GM. Inflammatory S100A9 and S100A12 proteins in Alzheimer's disease. Neurobiol Aging 2006; 27: 1554-1563. (Pubitemid 44344843)
128. Shoji M, Golde TE, Ghiso J, Cheung TT, Estus S, Shaffer LM, Cai XD, McKay DM, Tintner R, Frangione B, et al. Production of the Alzheimer amyloid beta protein by normal proteolytic processing. Science 1992; 258: 126-129.
129. Simard AR, Soulet D, Gowing G, Julien JP, Rivest S. Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron 2006; 49: 89-502. (Pubitemid 43221886)
130. 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: 5710-5714. (Pubitemid 24174398)
131. Snyder EM, Nong Y, Almeida CG, Paul S, Moran T, Choi EY, Nairn AC, Salter MW, Lombroso PJ, Gouras GK, Greengard P. Regulation of NMDA receptor trafficking by amyloid-beta. Nat Neurosci 2005; 8: 1051-1058. (Pubitemid 41061516)
132. Sousa MM, Du Yan S, Fernandes R, Guimaraes A, Stem D, Saraiva MJ. Familial amyloid polyneuropathy: receptor for advanced glycation end products-dependent triggering of neuronal inflammatory and apoptotic pathways. J Neurosci 2001; 21: 7576-7586. (Pubitemid 32904957)
133. Sousa MM, Yan SD, Stem 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: 1101-1110.
134. Srikrishna G, Huttunen HJ, Johansson L, Weigle B, Yamaguchi Y, Rauvala H, Freeze HH. N-Glycans on the receptor for advanced glycation end products influence amphoterin binding and neurite outgrowth. J Neurochem 2002; 80: 998-1008. (Pubitemid 34809952)
135. Stein TD, Anders NJ, DeCarli C, Chan SL, Mattson MP, Johnson JA. Neutralization of transthyretin reverses the neuroprotective effects of secreted amyloid precursor protein (APP) in APPSW mice resulting in tau phosphorylation and loss of hippocampal neurons: support for the amyloid hypothesis. J Neurosci 2004; 24: 7707-7717. (Pubitemid 39186826)
136. Sturchler E, Galichet A, Weibel M, Leclerc E, Heizmann CW. Site-specific blockade of RAGE-Vd prevents amyloid-beta oligomer neurotoxicity. J Neurosci 2008; 28: 5149-5158.
137. Sugaya K, Fukagawa T, Matsumoto K, Mita K, Takahashi E, Ando A, Inoko H, Ikemura T. 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
138. Sweatt JD. The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 2001; 76: 1-10.
139. Thies E, Mandelkow EM. Missorting of tau in neurons causes degeneration of synapses that can be rescued by the kinase MARK2/Par-1. J Neurosci 2007; 27: 2896-2907. (Pubitemid 46438993)
140. Thinakaran G, Koo EH. Amyloid precursor protein trafficking, processing, and function. J Biol Chem 2008; 283: 29615-29619.
141. Thomas T, Thomas G, McLendon C, Sutton T, Mullan M. Beta-Amyloid-mediated vasoactivity and vascular endothelial damage. Nature 1996; 380: 168-171. (Pubitemid 26085884)
142. Trinchese F, Fa M, Liu S, Zhang H, Hidalgo A, Schmidt SD, Yamaguchi H, Yoshii N, Mathews PM, Nixon RA, Arancio O. Inhibition of calpains improves memory and synaptic transmission in a mouse model of Alzheimer disease. J Clin Invest 2008; 118: 2796-2807.
143. 2+ channels: a possible involvement of free radicals. J Neurochem 1997; 68: 265-271. (Pubitemid 26427316)
144. Vega IE, Traverso EE, Ferrer-Acosta Y, Matos E, Colon M, Gonzalez J, Dickson D, Hutton M, Lewis J, Yen SH. A novel calcium-binding protein is associated with tau proteins in tauopathy. J Neurochem 2008; 106: 96-106. (Pubitemid 351840193)
145. Vincent AM, Perrone L, Sullivan KA, Backus C, Sastry AM, Lastoskie C, Feldman EL. Receptor for advanced glycation end products activation injures primary sensory neurons via oxidative stress. Endocrinology 2007; 148: 548-558. (Pubitemid 46143159)
146. Vogl T, Tenbrock K, Ludwig S, Leukert N, Ehrhardt C, van Zoelen MA, Nacken W, Foell D, van der Poll T, Sorg C, Roth J. Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat Med 2007; 13: 1042-1049. (Pubitemid 47517513)
147. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002; 416: 535-539. (Pubitemid 34288854)
148. Walsh DM, Klyubin I, Fadeeva JV, Rowan MJ, Selkoe DJ. Amyloid-beta oligomers: their production, toxicity and therapeutic inhibition. Biochem Soc Trans 2002; 30: 552-557. (Pubitemid 35001597)
149. Westermark P, Benson MD, Buxbaum JN, Cohen AS, Frangione B, Ikeda S, Masters CL, Merlini G, Saraiva MJ, Sipe JD. A primer of amyloid nomenclature. Amyloid 2007; 14: 179-183.
150. Wilton R, Yousef MA, Saxena P, Szpunar M, Stevens FJ. Expression and purification of recombinant human receptor for advanced glycation endproducts in Escherichia coli. Protein Expr Purif 2006; 47: 25-35.
151. Wogulis M, Wright S, Cunningham D, Chilcote T, Powell K, Rydel RE. Nucleation-dependent polymerization is an essential component of amyloid-mediated neuronal cell death. J Neurosci 2005; 25: 1071-1080. (Pubitemid 41741352)
152. Wu J, Anwyl R, Rowan MJ. Beta-Amyloid selectively augments NMDA receptor-mediated synaptic transmission in rat hippocampus. NeuroReport 1995; 6: 2409-2413. (Pubitemid 3011537)
153. Xia Z, Storm DR. The role of calmodulin as a signal integrator for synaptic plasticity. Nat Rev Neurosci 2005; 6: 267-276. (Pubitemid 40469981)
154. 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: 4218-4231. (Pubitemid 47084493)
155. 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: 27255-27269.
156. Yamaguchi H, Nakazato Y, Hirai S, Shoji M, Harigaya Y. Electron micrograph of diffuse plaques. Initial stage of senile plaque formation in the Alzheimer brain. Am J Pathol 1989; 135: 593-597. (Pubitemid 19268015)
157. Yamashita N, Ilg EC, Schafer BW, Heizmann CW, Kosaka T. Distribution of a specific calcium-binding protein of the S100 protein family, S100A6 (calcyclin), in subpopulations of neurons and glial cells of the adult rat nervous system. J Comp Neurol 1999; 404: 235-257. (Pubitemid 29086548)
158. Yan SD, Chen X, Fu J, Chen M, Zhu H, Roher A, Slattery T, Zhao L, Nagashima M, Morser J, Migheli A, Nawroth P, Stern D, Schmidt AM. RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature 1996; 382: 685-691. (Pubitemid 26282167)
159. Yonekura H, Yamamoto Y, Sakurai S, Petrova RG, Abedin MJ, Li H, Yasui K, Takeuchi M, Makita Z, Takasawa S, Okamoto H, Watanabe T, Yamamoto H. 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: 1097-1109. (Pubitemid 36399105)
160. Zatz M, Starling A. Calpains and disease. N Engl J Med 2005; 352: 2413-2423.
161. Zerbinatti CV, Wahrle SE, Kim H, Cam JA, Bales K, Paul SM, Holtzman DM, Bu G. Apolipoprotein E and low density lipoprotein receptor-related protein facilitate intraneuronal Abeta42 accumulation in amyloid model mice. J Biol Chem 2006; 281: 36180-36186. (Pubitemid 46041352)
162. Zhang L, Bukulin M, Kojro E, Roth A, Metz VV, Fahrenholz F, Nawroth PP, Bierhaus A, Postina R. Receptor for advanced glycation end products is subjected to protein ectodomain shedding by metalloproteinases. J Biol Chem 2008; 283: 35507-35516.
163. 2+ sensor VILIP-1 leads to the upregulation of functional alpha4beta2 nicotinic acetylcholine receptors in hippocampal neurons. Mol Cell Neurosci 2009; 40: 280-292.
164. Zimmer DB, Wright Sadosky P, Weber DJ. Molecular mechanisms of S100-target protein interactions. Microsc Res Tech 2003; 60: 552-559.