Receptor for advanced glycation end product-dependent activation of p38 mitogen-activated protein kinase contributes to amyloid-β-mediated cortical synaptic dysfunction

Journal of Neuroscience

Volumn 28, Issue 13, 2008, Pages 3521-3530

  Origlia, Nicola ^a   Righi, Massimo ^b   Capsoni, Simona ^c   Cattaneo, Antonino ^d   Fang, Fang ^e   Stern, David M ^f   Chen, John Xi ^g   Schmidt, Ann Marie ^e   Arancio, Ottavio ^e   Shi, Du Yan ^e   Domenici, Luciano ^a,h  

^a CNR   (Italy)

^b SISSA   (Italy)

^c Lay Line Genomics SpA   (Italy)

^d EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^e Columbia University ^*  (United States)

^f UNIVERSITY OF CINCINNATI   (United States)

^g Harvey Cushing Institutes of Neuroscience   (United States)

^h UNIVERSITY OF L'AQUILA   (Italy)

Author keywords

Alzheimer's disease; Amyloid ; Entorhinal cortex; LTP; p38 MAPK; Protein; RAGE

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ADVANCED GLYCATION END PRODUCT RECEPTOR; AMYLOID BETA PROTEIN; BLOCKING ANTIBODY; MITOGEN ACTIVATED PROTEIN KINASE P38; OLIGOMER; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE INHIBITOR;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; ENTORHINAL CORTEX; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MOUSE; NERVE CELL; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; AMYLOID BETA-PROTEIN; ANIMALS; ANIMALS, NEWBORN; ANTIBODIES; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; ENTORHINAL CORTEX; ENZYME ACTIVATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; LONG-TERM POTENTIATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURAL INHIBITION; NEURONS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PEPTIDE FRAGMENTS; RECEPTORS, IMMUNOLOGIC; SYNAPSES;

EID: 41549089757     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0204-08.2008     Document Type: Article

References (77)

1. Alonso A, de Curtis M, Llinas R (1990) Postsynaptic Hebbian and non-Hebbian long-term potentiation of synaptic efficacy in the entorhinal cortex in slices and in the isolated adult guinea pig brain. Proc Natl Acad Sci USA 87:9280-9284.
2. Anderson WW, Collingridge GL (2001) The LTP program: a data acquisition program for on-line analysis of long-term potentiation and other synaptic events. J Neurosci Methods 108:71-83.
3. 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, et al. (2004) RAGE potentiates Aβ-induced perturbation of neuronal function in transgenic mice. EMBO J 23:4096-4105.
4. Bennett BL, Sasaki DT, Murray BW, O'Leary EC, Sakata ST, Xu W, Leisten JC, Motiwala A, Pierce S, Satoh Y, Bhagwat SS, Manning AM, Anderson DW (2001) SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci USA 98:13681-13686.
5. Braak H, Braak E (1991) Demonstration of amyloid deposits and neurofibrillary changes in whole brain sections. Brain Pathol 3:213-216.
6. Braak H, Braak E (1993) Entorhinal-hippocampal interaction in mnestic disorders. Hippocampus 3:239-246.
7. Chang EH, Savage MJ, Flood DG, Thomas JM, Levy RB, Mahadomrongkul V, Shirao T, Aoki C, Huerta PT (2006) AMPA receptor downscaling at the onset of Alzheimer's disease pathology in double knock-in mice. Proc Natl Acad Sci USA 103:3410-3415.
8. Chapman PF, White GL, Jones MW, Cooper-Blacketer D, Marshall VJ, Irizarry M, Younkin L, Good MA, Bliss TV, Hyman BT, Younkin SG, Hsiao KK (1999) Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci 2:271-276.
9. Chen QS, Wei WZ, Shimahara T, Xie CW (2002) Alzheimer amyloid beta-peptide inhibits the late phase of long-term potentiation through calcineurin-dependent mechanisms in the hippocampal dentate gyrus. Neurobiol Learn Mem 77:354-371.
10. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, Selkoe DJ, Ashe KH (2005) Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 8:79-84.
11. Curran BP, Murray HJ, O'Connor JJ (2003) A role for c-Jun N-terminal kinase in the inhibition of long-term potentiation by interleukin-1β and long-term depression in the rat dentate gyrus in vitro. Neuroscience 118:347-357.
12. 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, et al. (2003) RAGE mediates amyloid-beta peptide transport across the blood-brain barrier and accumulation in brain. Nat Med 9:907-913.
13. Deora A, Win T, Vanhaesebroeck B, Lander H (1998) A redox triggered Ras-effector interaction: recruitment of phosphatidyli-nositol 30-kinase to Ras by redox stress. J Biol Chem 273:29923-29928.
14. D'Hooge R, Nagels G, Westland CE, Mucke L, De Deyn PP (1996) Spatial learning deficit in mice expressing human 751-amino acid beta-amyloid precursor protein. NeuroReport 7:2807-2811.
15. Ding Q, Keller JN (2005) Evaluation of rage isoforms, ligands, and signaling in the brain. Biochim Biophys Acta 1746:1 8-27.
16. Dolorfo CL, Amaral DG (1998) Entorhinal cortex of the rat: organization of intrinsic connections. J Comp Neurol 398:49-82.
17. Domenici L, Harding GW, Burkhalter A (1995) Patterns of synaptic activity in forward and feedback pathways within rat visual cortex. J Neurophysiol 74:2649-2664.
18. Eisenhauer PB, Johnson RJ, Wells JM, Davies TA, Fine RE (2000) Toxicity of various amyloid beta peptide species in cultured human blood-brain barrier endothelial cells: increased toxicity of dutch-type mutant. J Neurosci Res 60:804-810.
19. Giacchino J, Criado JR, Games D, Henriksen S (2000) In vivo synaptic transmission in young and aged amyloid precursor protein transgenic mice. Brain Res 876:185-190.
20. Hensley K, Floyd RA, Zheng NY, Nael R, Robinson KA, Nguyen X, Pye QN, Stewart CA, Geddes J, Markesbery WR, Patel E, Johnson GV, Bing G (1999) p38 kinase is activated in the Alzheimer's disease brain. J Neurochem 72:2053-2058.
21. Hofmann 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 (1999) RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell 97:889-901.
22. Hsia AY, Masliah E, McConlogue L, Yu GQ, Tatsuno G, Hu K, Kholodenko D, Malenka RC, Nicoll RA, Mucke L (1999) Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc Natl Acad Sci USA 96:3228-3233.
23. Hsieh H, Boehm J, Sato C, Iwatsubo T, Tomita T, Sisodia S, Malinow R (2006) AMPAR removal underlies Aβ-induced synaptic depression and dendritic spine loss. Neuron 52:831-843.
24. Huang J, Guh J, Chen H, Hung W, Lai Y, Chuang L (2001) Role of RAGE and the JAK/STAT-signaling pathway in AGE-induced collagen production in NRK-49F cells. J Cell Biochem 81:102-113.
25. Huttunen H, Fages C, Rauvala H (1999) RAGE-mediated neurite outgrowth and activation of NF-κB require the cytoplasmic domain of the receptor but different downstream signaling pathways. J Biol Chem 274:19919-19924.
26. Ingelsson M, Fukumoto H, Newell KL, Growdon JH, Hedley-Whyte ET, Frosch MP, Albert MS, Hyman BT, Irizarry MC (2004) Early Aβ accumulation and progressive synaptic loss, gliosis, and tangle formation in AD brain. Neurology 62:925-931.
27. Johnson LV, Leitner WP, Rivest AJ, Staples MK, Radeke MJ, Anderson DH (2002) The Alzheimer's A β-peptide is deposited at sites of complement activation in pathologic deposits associated with aging and age-related macular degeneration. Proc Natl Acad Sci USA 18:11830-11835.
28. Kelly A, Vereker E, Nolan Y, Brady M, Barry C, Loscher CE, Mills KH, Lynch MA (2003) Activation of p38 plays a pivotal role in the inhibitory effect of lipopolysaccharide and interleukin-1 beta on long term potentiation in rat dentate gyrus. J Biol Chem 278:19453-19462.
29. Kislinger T, Fu C, Huber B, Qu W, Taguchi A, Yan SD, Hofmann M, Yan SF, Pischetsrider M, Stern D, Schmidt AM (1999) Nε (carboxymethyl) lysine modifications of proteins are ligands for RAGE that activate cell signaling pathways and modulate gene expression. J Biol Chem 274:31740-31749.
30. Kourrich S, Chapman CA (2003) NMDA receptor-dependent long-term synaptic depression in the entorhinal cortex in vitro. J Neurophysiol 89:2112-2119.
31. Lali FV, Hunt AE, Turner SJ, Foxwell BM (2000) The pyridinyl imidazole inhibitor SB203580 blocks phosphoinositide-dependent protein kinase activity, protein kinase B phosphorylation, and retinoblastoma hyperphosphorylation in interleukin-2-stimulated T cells independently of p38 mitogen-activated protein kinase. J Biol Chem 275:7395-7402.
32. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trommer B, Viola KL, Wals P, Zhang C, Finch CE, Krafft GA, Klein WL (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 95:6448-6453.
33. Lander H, Tauras J, Ogiste J, Moss R, Schmidt AM (1997) Activation of RAGE triggers a MAP kinase pathway regulated by oxidant stress. J Biol Chem 272:17810-17814.
34. Larson J, Lynch G, Games D, Seubert P (1999) Alterations in synaptic transmission and long-term potentiation in hippocampal slices from young and aged PDAPP mice. Brain Res 840:23-35.
35. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, Gallagher M, Ashe KH (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440:352-357.
36. Li QX, Maynard C, Cappai R, McLean CA, Cherny RA, Lynch T, Culvenor JG, Trevaskis J, Tanner JE, Bailey KA, Czech C, Bush AI, Beyreuther K, Masters CL (1999) Intracellular accumulation of detergent-soluble amyloidogenic A beta fragment of Alzheimer's disease precursor protein in the hippocampus of aged transgenic mice. J Neurochem 72:2479-2487.
37. Lue LF, Walker DG, Brachova L, Beach TG, Rogers J, Schmidt AM, Stern DM, Yan SD (2001) Involvement of microglial receptor for advanced glycation endproducts (RAGE) in Alzheimer's disease: identification of a cellular activation mechanism. Exp Neurol 171:29-45.
38. Lue LF, Yan SD, Stern DM, Walker DG (2005) Preventing activation of receptor for advanced glycation endproducts in Alzheimer's disease. Curr Drug Targets CNS Neurol Disord 4:249-266.
39. Lustbader JW, Cirilli M, Lin C, Xu HW, Takuma K, Wang N, Caspersen C, Chen X, Pollak S, Chaney M, Trinchese F, Liu S, Gunn-Moore F, Lue LF, Walker DG, Kuppusamy P, Zewier ZL, Arancio O, Stern D, Yan SD, Wu H (2004) ABAD directly links Aβ to mitochondrial toxicity in Alzheimer's disease. Science 304:448-452.
40. Mucke L, Masliah E, Yu GQ, Mallory M, Rockenstein EM, Tatsuno G, Hu K, Kholodenko D, Johnson-Wood K, McConlogue L (2000) High-level neuronal expression of Aβ1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J Neurosci 20:4050-4058.
41. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, Metherate R, Mattson MP, Akbari Y, Laferla FM (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Ab and synaptic dysfunction. Neuron 39:409-421.
42. Ono K, Han J (2000) The p38 signal transduction pathway: activation and function. Cell Signal 12:1-13.
43. Parameshwaran K, Sims C, Kanju P, Vaithianathan T, Shonesy BC, Dhanasekaran M, Bahr BA, Suppiramaniam V (2007) Amyloid β-peptide Aβ(1-42) but not Aβ(1-40) attenuates synaptic AMPA receptor function. Synapse 61:367-374.
44. Pei JJ, Braak E, Braak H, Grundke-Iqbal I, Iqbal K, Winblad B, Cowburn RF (2001) Localization of active forms of C-jun kinase (JNK) and p38 kinase in Alzheimer's disease brains at different stages of neurofibrillary degeneration. J Alzheimers Dis 3:41-48.
45. Pesavento E, Capsoni S, Domenici L, Cattaneo A (2002) Acute cholinergic rescue of synaptic plasticity in the neurodegenerating cortex of anti-nerve growth factor mice. Eur J Neurosci 15:1030-1036.
46. Puzzo D, Vitolo O, Trinchese F, Jacob JP, Palmeri A, Arancio O (2005) Amyloid-beta peptide inhibits activation of the nitric oxide/cGMP/cAMP- responsive element-binding protein pathway during hippocampal synaptic plasticity. J Neurosci 25:6887-6897.
47. Raymond CD, Ireland DR, Abraham WC (2003) NMDA receptor regulation by amyloid-b does not account for its inhibition of LTP in rat hippocampus. Brain Res 968:263-272.
48. Sakaguchi T, Yan SF, Yan SD, Belov D, Rong LL, Sousa M, Andrassy M, Marso SP, Duda S, Arnold B, Liliensiek B, Nawroth PP, Stern DM, Schmidt AM, Naka Y (2003) Central role of RAGE-dependent neointimal expansion in arterial restenosis. J Clin Invest Apr 111:959-972.
49. Sasahara M, Fries JWU, Raines EW, Gown AM, Westrum LE, Frosch MP, Bonthron DT, Ross R, Collins T (1991) PDGF B-chain in neurons of the central nervous system, posterior pituitary, and in a transgenic model. Cell 64:217-227.
50. Schmidt AM, Yan SD, Yan SF, Stern DM (2001) The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J Clin Invest 108:949-955.
51. Selkoe DJ (2002) Alzheimer's disease is a synaptic failure. Science 298:789-791.
52. Shemer I, Holmgren C, Min R, Fulop L, Zilberter M, Sousa KM, Farkas T, Hartig W, Penke B, Burnashev N, Tanila H, Zilberter Y, Harkany T (2006) Non-fibrillar beta-amyloid abates spike-timing-dependent synaptic potentiation at excitatory synapses in layer 2/3 of the neocortex by targeting postsynaptic AMPA receptors. Eur J Neurosci 23:2035-2047.
53. Simmons LK, May PC, Tomaselli KJ, Rydel RE, Fuson KS, Brigham EF, Wright S, Lieberburg I, Becker GW, Brems DN (1994) Secondary structure of amyloid beta peptide correlates with neurotoxic activity in vitro. Mol Pharmacol 45:373-379.
54. Snyder EM, Nong Y, Almeida CG, Paul S, Moran T, Choi EY, Nairn AC, Salter MW, Lombroso PJ, Gouras GK, Greengard P (2005) Regulation of NMDA receptor trafficking by amyloid-beta. Nat Neurosci 8:1051-1058.
55. Suzuki WA, Amaral DG (2004) Functional neuroanatomy of the medial temporal lobe memory system. Cortex 40:220-222.
56. Takuma K, Yao J, Huang J, Xu H, Chen X, Luddy J, Trillat AC, Stern DM, Arancio O, Yan SD (2005) ABAD enhances Aβ-induced cell stress via mitochondrial dysfunction. FASEB J 19:597-598.
57. Trinchese F, Liu S, Battaglia F, Walter S, Mathews PM, Arancio O (2004) Progressive age-related development of Alzheimer-like pathology in APP/PS1 mice. Ann Neurol 55:801-814.
58. Troy CM, Rabacchi SA, Xu Z, Maroney AC, Connors TJ, Shelanski ML, Greene LA (2001) beta-Amyloid-induced neuronal apoptosis requires c-Jun N-terminal kinase activation. J Neurochem 77:157-164.
59. Tyszkiewicz JP, Yan Z (2005) Beta-Amyloid peptides impair PKC-dependent functions of metabotropic glutamate receptors in prefrontal cortical neurons. J Neurophysiol 93:3102-3111.
60. Vitolo OV, Sant'Angelo A, Costanzo V, Battaglia F, Arancio O, Shelanski M (2002) Amyloid beta-peptide inhibition of the PKA/CREB pathway and long-term potentiation: reversibility by drugs that enhance cAMP signaling. Proc Natl Acad Sci USA 99:13217-13221.
61. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416:535-539.
62. Walsh DM, Townsend M, Podlisny MB, Shankar GM, Fadeeva JV, El Agnaf O, Hartley DM, Selkoe DJ (2005) Certain inhibitors of synthetic amyloid beta-peptide (Aβ) fibrillogenesis block oligomerization of natural Abeta and thereby rescue long-term potentiation. J Neurosci 25:2455-2462.
63. Wang HW, Pasternak JF, Kuo H, Ristic H, Lambert MP, Chromy B, Viola KL, Klein WL, Stine WB, Krafft GA, Trommer BL (2002) Soluble oligomers of beta amyloid (1-42) inhibit long-term potentiation but not long-term depression in rat dentate gyrus. Brain Res 924:133-140.
64. 2 and NO on apoptosis involving activation of p38 mitogen-activated protein kinase and caspase-3. J Neurosci Res 72:508-519.
65. Wang Q, Walsh DM, Rowan MJ, Selkoe DJ, Anwyl R (2004) Block of longterm potentiation by naturally secreted and synthetic amyloid beta-peptide in hippocampal slices is mediated via activation of the kinases c-Jun N-terminal kinase, cyclin-dependent kinase 5, and p38 mitogen-activated protein kinase as well as metabotropic glutamate receptor type 5. J Neurosci 24:3370-3378.
66. Wendt TM, Tanji N, Guo J, Kislinger TR, Qu W, Lu Y, Bucciarelli LG, Rong LL, Moser B, Markowitz GS, Stein G, Bierhaus A, Liliensiek B, Arnold B, Nawroth PP, Stern DM, D'Agati VD, Schmidt AM (2003) RAGE drives the development of glomerulosclerosis and implicates podocyte activation in the pathogenesis of diabetic nephropathy. Am J Pathol 162:1123-1137.
67. Whitlock JR, Heynen AJ, Shuler MG, Bear MF (2006) Learning induces long-term potentiation in the hippocampus. Science 313:1093-1097.
68. Wirths O, Multhaup G, Czech C, Blanchard V, Moussaoui S, Tremp G, Pradier L, Beyreuther K, Bayer TA (2001) Intraneuronal Abeta accumulation precedes plaque formation in beta-amyloid precursor protein and presenilin-1 double-transgenic mice. Neurosci Lett 306:116-120.
69. Witter MP, Groenewegen HJ, Lopes da Silva FH, Lohman AH (1989) Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol 33:161-253.
70. Yan SD, Yan SF, Chen X, Fu J, Chen M, Kuppusamy P, Smith MA, Perry G, Godman GC, Nawroth P, Zweier J, Stern DM (1995) Non-enzymatically glycated tau in Alzheimer's disease induces neuronal oxidant stress resulting in cytokine gene expression and release of amyloid beta-peptide. Nat Med 1:693-699.
71. 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 (1996) RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature 382:685-691.
72. Yan SD, Stern D, Kane MD, Kuo YM, Lampert HC, Roher AE (1998) RAGE-Abeta interactions in the pathophysiology of Alzheimer's disease. Restor Neurol Neurosci 12:167-173.
73. Yan Y, Liu Y, Sorci M, Belfort G, Lustbader JW, Yan SD, Wang C (2007) Surface plasmon resonance and nuclear magnetic resonance studies of ABAD-Aβ interaction. Biochemistry 46:1724-1731.
74. Yun SH, Huh K, Jung MW (2000) Selective enhancement of non-NMDA receptor-mediated responses following induction of long-term potentiation in entorhinal cortex. Synapse 35:1-7.
75. Yun SH, Jung IM, Jung MW (2002) Variation in effective stimulus pattern for induction of long-term potentiation across different layers of rat entorhinal cortex. J Neurosci 22:RC214.
76. Zhao D, Watson JB, Xie CW (2004) Amyloid beta prevents activation of calcium/calmodulin-dependent protein kinase II and AMPA receptor phosphorylation during hippocampal long-term potentiation. J Neurophysiol 92:2853-2858.
77. Zhu X, Mei M, Lee HG, Wang Y, Han J, Perry G, Smith (2005) MAP38 activation mediates amyloid-beta cytotoxicity. Neurochem Res 30:791-796.