The significance of neuroinflammation in understanding Alzheimer's disease

Journal of Neural Transmission

Volumn 113, Issue 11, 2006, Pages 1685-1695

  Eikelenboom, P ^a,b,c   Veerhuis, R ^b   Scheper, W ^a   Rozemuller, A J M ^b   Van Gool, W A ^a   Hoozemans, J J M ^a,b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c Valerriuskliniek   (Netherlands)

Author keywords

A associated proteins; Acute phase proteins; Alzheimer's disease; Microglia; Neuroinflammation

Indexed keywords

ACUTE PHASE PROTEIN; AMYLOID BETA PROTEIN; ANTIINFLAMMATORY AGENT; CELECOXIB; CURCUMIN; CYTOKINE; HYDROXYCHLOROQUINE; LURBIPROFEN; NAPROXEN; NONSTEROID ANTIINFLAMMATORY AGENT; PREDNISONE; ROFECOXIB; UNCLASSIFIED DRUG; VACCINE;

ALZHEIMER DISEASE; CELL REGENERATION; CLINICAL TRIAL; COMPLEMENT FACTOR; HUMAN; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MENINGOENCEPHALITIS; MICROGLIA; NEUROFIBRILLARY TANGLE; NONHUMAN; PATHOGENESIS; PHYSICIAN; PLAQUE FORMING CELL; PRIORITY JOURNAL; REVIEW; SENILE PLAQUE;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; BRAIN; HUMANS; INFLAMMATION; SENILE PLAQUES;

EID: 33750461977     PISSN: 03009564     EISSN: 14351463     Source Type: Journal    
DOI: 10.1007/s00702-006-0575-6     Document Type: Review

References (102)

1. H Akiyama S Barker S Barnum B Bradt J Bauer GM Cole NR Cooper P Eikelenboom M Emmerling BL Fiebich 2000 Inflammation and Alzheimer's disease Neurobiol Aging 21 383 421
2. YM Arends C Duyckaerts JM Rozemuller P Eikelenboom J-J Hauw 2000 Microglia, amyloid and dementia in Alzheimer's disease. A correlative study Neurobiol Aging 21 39 47
3. T Arendt 2001 Alzheimer's disease as a disorder of mechanisms underlying structural brain self-organization Neuroscience 102 723 765
4. KR Bales T Verina RC Dodel YS Du L Altstiel M Bender P Hyslop EM Johnstone SP Little DJ Cummins P Ricardo B Ghetti SM Paul 1997 Lack of apoliprotein E dramatically reduces amyloid β-peptide deposition Nature Genet 17 263 264
5. C Bate R Veerhuis P Eikelenboom A Williams 2004 Microglia kill Aβ1-42 damaged neurons by a CD14 dependent process Neuroreport 28 1427 1430
6. RJ Bateman LY Munsell JC Morris R Swarm KE Yarasheski DM Holzman 2006 Human amyloid-β synthesis and clearance rates as measured in cerebrospinal fluid in vivo Nat Med 12 856 861
7. D Beher EE Clarke JD Wrigley AC Martin A Nadin I Churcher MS Shearman 2004 Selected non-steroidal anti-inflammatory drugs and their derivates target γ-secretase at a novel site. Evidence for an allosteric mechanism J Biol Chem 279 43419 43426
8. EM Blalock JW Geddes KC Chen NM Porter WR Markesbery PW Landfield 2004 Incipient Alzheimer's disease: microarray correlation analyses reveal major transcriptional and tumor suppressor responses Proc Natl Acad Sci USA 101 2173 2178
9. L Bouman 1934 Senile plaques Brain 57 128 142
10. H Braak E Braak 1996 Staging of Alzheimer's disease-related neurofibrillary changes Neurobiol Aging 16 271 278
11. KC Breen 1992 APP-collagen interaction is mediated by a heparin bridge mechanism Mol Chem Neuropathol 16 109 121
12. RP Brendza BJ Bacskai JR Cirrito KA Simmons JM Skoch WE Klunk CA Mathis KR Bales SM Paul BT Hyman DM Holtzman 2005 Anti-β antibody treatment promotes the rapid recovery of amyloid-associated neuritic dystrophy in PDAPP transgenic mice J Clin Invest 115 428 433
13. A Cagnin DJ Brooks AM Kennedy RN Gunn R Myers FE Turkheimer T Jones RB Banati 2001 In-vivo measurement of microglia in dementia Lancet 358 461 467
14. B Cannella CS Raine 1995 The adhesion molecule and cytokine profile of multiple sclerosis lesions Ann Neurol 37 424 435
15. CW Cotman 1997 Beta-amyloid peptide, peptide self-assembly, and the emergence of biological activities. A new principle in peptide function and the induction of neuropathology Ann NY Acad Sci 814 1 16
16. P del Rio-Hortega 1932 Microglia W Penfield Cytology and cellular pathology of the nervous system PB Hoeber New York 483 534
17. RB DeMattos MA O'dell M Parsadanian JW Taylor JA Harmony KR Bales SM Paul BJ Aronow DM Holtzman 2002 Clusterin promotes amyloid plaque formation and it is critical for neuritic toxicity in a mouse model of Alzheimer's disease Proc Natl Acad Sci USA 99 10843 10848
18. MG Dik C Jonker CE Hack JH Smit HC Comijs P Eikelenboom 2005 Serum inflammatory proteins and cognitive decline in older patients Neurology 64 1371 1377
19. P Eikelenboom FC Stam 1982 Immunoglobulins and complements factors in senile plaques Acta Neuropathol (Berl) 57 239 242
20. P Eikelenboom CE Hack JM Rozemuller FC Stam 1989 Complement activation in amyloid plaques in Alzheimer's disease Virchows Arch B (Cell Pathol) 56 259 262
21. P Eikelenboom JM Rozemuller G Kraal FC Stam PA [tmp] McBride ME Bruce H Fraser 1991 Cerebral amyloid plaques in Alzheimer's disease but not in scrapie-affected mice are closely associated with an chronic inflammatory process Virchows Arch B (Cell Pathol) 60 329 336
22. P Eikelenboom SS Zhan W Kamphorst P Van der Valk JM Rozemuller 1994 Cellular and substrate adhesion molecules (integrins) and their ligands in cerebral amyloid plaques in Alzheimer's disease Virchows Arch 424 421 427
23. P Eikelenboom R Veerhuis 1996 The role of complement and activated microglia in the pathogenesis of Alzheimer's disease Neurobiol Aging 17 673 680
24. P Eikelenboom WJG Hoogendijk C Jonker W van Tilburg 2002 Immunological mechanisms and the spectrum of psychiatric syndromes in Alzheimer's disease J Psychiat Res 36 269 280
25. P Eikelenboom WA van Gool 2004 Neuroinflammatory perspectives on the two faces of Alzheimer's disease J Neural Transm 111 281 294
26. J El Khoury SE Hickman CA Thomas L Cao SC Silverstein J Loike 1996 Scavenger receptor mediated adhesion of micoglia to amyloid-β fibrils Nature 382 716 719
27. MJ Engelhart MI Geerlings J Meijer A Kilaan A Ruitenberg JC van Swieten T Stijnen A Hofman JC Witteman MMB Breteler 2004 Inflammatory proteins in plasma and the risk of dementia: the Rotterdam study Arch Neurol 61 668 672
28. S Familian RS Boshuizen P Eikelenboom R Veerhuis 2006 Inhibitory effect of minocycline on amyloid-β fibril formation and human microglia activation Glia 53 223 240
29. K Fassbender S Walter S Kuhl R Landmann K Ishii T Bertsch AK Stalder F Muehlhauser Y Liu AJ Ulmer S Rivest A Lentschat E Guulbins M Jucker M Staufenbiel K Brechtel J Walter G Multhaup B Penke Y Adachi T Hartmann K Beyreuther 2004 The LPS receptor (CD14) links innate immunity with Alzheimer's disease Faseb J 18 203 205
30. O Fischer 1907 Miliare Nekrosen mit drusigen Wucherungen der Neurofibrillen, eine regelmässige Veränderung der Hirnrinde bei seniler Demenz Monatsch f Psychiat u Neurol 22 361 372
31. O Fischer 1910 Die presbyophrene Demenz, deren anatomische Grundlage und klinische Abgrenzung Z Ges Neurol u Psychiat 3 371 471
32. L Gasparini E Ongini G Wenk 2004 Non-steroidal anti-inflammatory drugs (NSAIDs) in Alzheimer's disease: old and new mechanisms of action J Neurochem 91 521 536
33. JW Geddes DT Monaghan CW Cotman IT Lou RC Kim HC Chui 1995 Plasticity of hippocampal circuitry in Alzheimer's disease Science 230 1179 1181
34. JP Godbout J Chen J Abraham AF Richwine BM Berg KW Kelley RW Johnson 2005 Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system FASEB J 19 1329 1331
35. EA Grace J Busciglio 2003 Aberrant activation of focal adhesion proteins mediates fibrillar amyloid-β-induced neuronal dystrophy J Neurosci 23 493 502
36. EST Griffin LC Stanley C Ling L White V [tmp] MacLeod LJ Perrot CL White C Araoz 1989 Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer's disease Proc Natl Acad Sci 86 7611 7615
37. JJM Hoozemans MK Brückner AJM Rozemuller R Veerhuis P Eikelenboom T Arendt 2002 Cyclin D1 and cyclin E are co-localized with cyclooxygenase-2 in pyramidal neurons in Alzheimer's disease temporal cortex J Neuropathol Exp Neurol 61 678 688
38. JJM Hoozemans R Veerhuis AJM Rozemuller T Arendt P Eikelenboom 2004 Neuronal COX-2 expression and phosphorylation of pRb precede p38∈MAPK activation and neurofibrillary changes in AD temporal cortex Neurobiol Dis 15 492 499
39. JJM Hoozemans ES van Haastert R Veerhuis T Arendt W Scheper P Eikelenboom AJM Rozemuller 2005a Maximal COX-2 and ppRb expression in neurons occurs during early Braak stages prior to the maximal activation of astrocytes and microglia in Alzheimer's disease J Neuroinflammation 2 27
40. JJM Hoozemans R Veerhuis JM Rozemuller F Baas P Eikelenboom W Scheper 2005b The unfolded protein is activated in Alzheimer's disease Acta Neuropathol 110 165 172
41. JJM Hoozemans SM Chafekar F Baas P Eikelenboom W Scheper 2006a Always around, never the same: pathways of amyuloid-β induced neurodgeneration throughout the pathogenic cascade of Alzheimer's Curr Med Chem 13 2599 2605
42. JJM Hoozemans R Veerhuis JM Rozemuller P Eikelenboom 2006b Neuroinflammation and regeneration in the early stages of Alzheimer's disease pathology Int J Devl Neurosci 24 157 165
43. T Ishii S Haga 1984 Immuno-electron-microscopic localization of complement in amyloid fibrils of senile plaques Acta Neuropathol 63 296 300
44. S Itagaki PL [tmp] McGeer H Akiyama S Zhu D Selkoe 1989 Relationship of microglia and astrocytes to amyloid deposits of Alzheimer's disease J Neuroimmunol 24 173 182
45. N Iwata M Higuchi TC Saido 2005 Metabolism of amyloid-β peptide and Alzheimer's disease Pharmacol Ther 108 129 148
46. PT Jantzen KE Connor G DiCarlo GL Wenk JL Wallace AM Rojiani D Coppola D Morgan MN Gordon 2002 Microglial activation and β-amyloid deposit reduction caused by nitric oxide-releasing ninsteroidal anti-inflammatory drug in amyloid precursor protein plus presenelin-1 transgenic mice J Neurosci 22 2246 2254
47. WL Klein GA Krafft CE Finch 2001 Targetting small oligomers: the solution to an Alzheimer's disease conundrum? Trends Neurosci 2001 219 224
48. EH Koo L Park DJ Selkoe 1993 Amyloid-β protein as substrate interacts with extracellular matrix to promote neurite outgrowth Proc Natl Acad Sci USA 90 1564 1568
49. GE Landreth MT Heneka 2001 Anti-inflammatory actions of peroxisome proliferator-activated receptor γ agonists in Alzheimer's disease Neurobiol Aging 22 937 944
50. GP Lim T Chu F Yang W Beech SA Frautschy GM Cole 2001 The curry spice curcumin reduces oxidative damage and amyloid pathology in Alzheimer transgenic mice J Neurosci 21 8370 8377
51. PL [tmp] McGeer S Itagaki H Tago EG [tmp] McGeer 1987 Reactive microglia in patients with senile dementia of Alzheimer-type are positive for the histocompatibility glycoprotein HLA-DR Neurosci Lett 79 195 200
52. PL [tmp] McGeer H Akiyama S Itgaki EG [tmp] McGeer 1989 Immune system response in Alzheimer's disease Can J Neurol Sci 16 516 527
53. JP Melchor R Pawlak S Strickland 2003 The tissue plasminogen activator-plasminogen proteolytic cascade accelerates amyloid-β (Aβ) degredation and inhibits Aβ-induced neurodegeneration J Neurosci 23 8867 8871
54. D Morgan 2006 Modulation of microglial activation state following passive immunization in amyloid deposing transgenic mice Neurochem Int 49 190 194
55. S Narindrasorasak DE Lowery RA Altman PA Gonzalez-DeWhitt BD Greenberg R Kisilevsky 1992 Characterization of high affinity binding between laminin and Alzheimer's amyloid precursor proteins Lab Invest 67 643 652
56. JA Nicoll D Wilkinson C Holmes P Steart H Markham RO Weller 2003 Neuropathology of human Alzheimer's disease after immunization with amyloid-β peptide; a case study Nat Med 9 448 452
57. LNG Nilsson KR Bales G DiCarlo MN Gordon SM Paul H Potter 2001 α-1 Antichymotrypsin promotes β-sheet amyloid plaque formation in a transgenic mouse model of Alzheimer's disease J Neurochem 21 1444 1451
58. HS Nottet Y Persidsky VG Sasseville AN Nukuna P Bock H Zhai LR Sharer RD [tmp] McComb S Swindels C Soderland HE Gentleman 1996 Mechanisms for the transendothelial migration of HIV-1-infected monocytes into the brain J Immunol 156 1284 1295
59. K Oshima H Akiyam K Tsuchiya H Kondo C Haga Y Shimomura E Iseki H Uchikado M Kato K Niizato H Arai 2006 Relatively paucity of tau accumulation in the small areas with abundant Aβ42-positive caplliary amyloid angiopathy within a given cortical region in the brain of patients with Alzheimer pathology Acta Neuropathol 111 510 518
60. DM Paresce RN Ghosh FR Maxfield 1996 Microglial cells internalize aggregates of the Alzheimer's disease amyloid-β-protein via a scavenger receptor Neuron 17 553 565
61. VH Perry TA Newman C Cunningham 2003 The impact of systemic infection on the progression of neurodegenerative disease Nat Rev Neurisci 4 103 112
62. A Poulard-Barthelaix F Dubas W Jabbour I Maher J Emile 1986 An immunological view on the etiology and pathogenesis of Alzheimer's disease A Bes Senile dementia early detection John Libbey Eurotext, Paris 216 222
63. A Pouplard J Emile 1985 New immunological findings in senile dementia Interdiscipl Topics Geront 19 62 71
64. WQ Qiu DM Walsh Z Ye K Vekrelis J Zhang MB Podlisny MR Rosner A Safavi LB Hersh DJ Selkoe 1998 Insulin-degrading enzyme regulates extracellular levels of amyloid-β protein by degredation J Biol Chem 273 32370 32738
65. A Reichenberg R Yirmiya AM Schuld T Kraus M Haack A Morag T Pollmacher 2001 Cytokine-associated emotional and cognitive disturbances in humans Arch Gen Psychiat 56 445 452
66. KP Riley DA Snowdon WR Markesberry 2002 Alzheimer's neurofibrillary pathology and the spectrum of cognitive function: findings from the Nun Study Ann Neurol 51 567 577
67. BR Rock G Gekker S Hu WS Sheng M Cheeran JR Lokensgaard PK Peterson 2004 Role of microglia in central nervous infections Clin Microbiol Rev 17 942 964
68. J Rogers J Luber-Narod SD Styren WH Civin 1988 Expression of the immune system-associated antigen by cells of the human central nervous system. Relationship to the pathology of Alzheimer's disease Neurobiol Aging 9 339 349
69. J Rogers NR Cooper S Webster J Schulz PL [tmp] McGeer SD Styren WH Civin L Brachova B Bradt I Lieberburg 1992 Complement activation by β-amyloid in Alzheimer's disease Proc Natl Acad Sci USA 89 10016 10020
70. JM Rozemuller P Eikelenboom ST Pals FC Stam 1989a Microglial cells around plaques in Alzheimer's disease express leucocyte adhesion of the LFA/1 family Neurosci Lett 101 288 292
71. JM Rozemuller P Eikelenboom FC Stam K Beyreuther CL Masters 1989b A4 protein in Alzheimer's disease: primary and secondary cellular events in extracellular amyloid depostion J Neuropathol Exp Neurol 48 647 663
72. Saido TC, Overview-Aβ metabolism: From Alzheimer research to brain aging control (2003) In: Saido TC (ed) Aβ metabolism and Alzheimer's disease. Landes Bioscience Georgetown, Texas USA, pp 1-16
73. D Schenk R Barbour W Dunn G Gordon H Grajeda T Guido K Hu J Huang K Johnson-Wood K Khan 1999 Immunisation with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse Nature 400 173 177
74. R Schmidt H Schmidt JD Curb K Masaki LR White LJ Launer 2002 Early inflammation and dementia: a 25-year follow-up of the Honolul-asian aging study Ann Neurol 52 168 174
75. J Schnabel 1998 Forever young Science and the search for immortality Bloomsburry Publishing Plc London
76. LM Shaffer MD Dority R Gupta-Bansal RC Frederickson SG Younkin KR Brunden 1995 Amyloid-β protein (Aβ) removal by neuroglial cells in the culture Neurobiol Aging 16 737 745
77. AD Snow R Sekiguchi D Nochlin P Fraser K Kimata A Mizutani M Arai WA Schreier DG Morgan 1994 An important role of heparan sulphate proteoglycan (Perlecan) in a model system for the deposition and persistence of fibrillar β-amyloid in the rat brain Neuron 12 219 234
78. SW Snyder GT Wang L Barrett US Ladror D Casuto CM Lee GA Kraft RB Holzman TF Holzman 1994 Complement C1q does not bind monomeric β-amyloid Exp Neurol 128 136 142
79. WJ Streit 2002 Microglia as neuroprotective, immunocompetent cells of the CNS Glia 40 133 139
80. GA Tennent LB Lovat MB Pepys 1995 Serum amyloid-P component prevents proteolysis of the amyloid fibrils of alzheimer disease and systemic amyloidosis Proc Natl Acad Sci USA 92 4299 4303
81. AP Timmer 1925 Der Anteil der Mikroglia und Makroglia am Afbau der senile Plaques Z Neurol 98 43 58
82. KP Townsend D Pratico 2005 Novel therapeutic options for Alzheimer's disease: focus on nonsteroidal anti-inflammatory drugs FASEB J 19 1592 1601
83. WA Van Gool PS Aisen P Eikelenboom 2003 Anti-inflammatory therapy in Alzheimer's disease: is hope still alive J Neurol 250 788 792
84. J Van Horssen P Wesseling LP van den Heuvel RM de Waal MM Verbeek 2003 Heparan sulphate proteoglycans in Alzheimer's disease and amyloid-related disorders Lancet Neurol 2 482 492
85. R Veerhuis MJ van Breemen JJM Hoozemans M Morbin J Ouladhadj F Tagliavini P Eikelenboom 2003 Amyloid β-associated proteins C1q and SAP enhance the Aβ1-42 peptide-induced cytokine secretion by adult human microglia in vitro Acta Neuropathol 105 135 144
86. R Veerhuis RS Boshuizen A Familian 2005 Amyloid associated proteins in Alzheimer's and prion disease Curr Drug Targets CNS Neurol Disord 4 325 348
87. R Veerhuis A Familian P Eikelenboom 2006 Minocycline attenuates the amyloid-β (Aβ) mediated activation of human microglia without affecting microglial Aβ phagocytosis in vitro Alzheimer's & Dementia 2 S607
88. AK Vehmas CH Kawas WF Stewart JC Troncoso 2003 Immune reactive cells in senile plaque and cognitive decline in Alzheimer's disease Neurobiol Aging 24 321 331
89. S Weggen JL Eriksen P Das SA Sagi R Wang CU Pietrzik KA Findl TE Smith MP Murphy T Bulter DE Kang N Marquez-Sterling TE Golde EH Koo 2001 A subset of NSAIDs lower amyloidogenic Abeta42 independently of cyclooxygenase activity Nature 414 212 216
90. S Weggen JL Eriksen SA Sagi CU Pietrzik V Ozols A Fauq TE Golde EH Koo 2003 Evidence that nonsteroidal anti-inflammatory drugs decrease amyloid-β 42 production by direct modulation of γ-secretase activity J Biol Chem 278 31831 31837
91. S Webster J Rogers 1997 Relative efficacies of amyloid-β peptide (Aβ) binding proteins in Aβ aggregation J Neurosci Res 46 58 66
92. SD Webster AJ Yang L Margol W Garzon-Rodriquez CG Glabe AJ Tenner 2000 Complement component C1q modulates the phagocytosis of Aβ by microglia Exp Neurol 161 127 138
93. DM Wilcock A Rojiani A Rosenthal S Subbarao MJ Freeman MN Gordon D Morgan 2004 O Passive immunotherapy against Aβ in aged APP-transgenic mice reverses cognitive deficits and depletes parenchymal amyloid deposits in spite of increased vascular amyloid and microhemorrhage J Neuroinflammation 1 24
94. AE Williams A-M Van Dam P Eikelenboom H Fraser 1997 Immunocytochemical appearance of cytokines, prostaglandin E2 and lipocortin-1 in the CNS during the incuabation period of mrine scrapie correlates with progressive PrP accumulations Brain Res 754 171 180
95. T Wyss-Coray L Mucke 2002 Inflammation in neurodegenerative disease: a double-edged sword Neuron 35 419 432
96. T Wyss-Coray F Yan AH Lin JD Lambris JJ Alexander RJ Quigg E Masliah 2002 Prominent neurodegeneration and increased plaque formation in complement inhibited Alzheimer's mice Proc Natl Acad Sci USA 99 10837 10842
97. K Yaffe K Lindquist BW Penninx EM Simonsick M Pahor S Kritchevsky L Launer L Kuller S Rubin T Harris 2003 Inflammation and cognition in well-functioning African-American and white elders Neurology 61 76 80
98. K Yaffe A Kanaya K Lindquist EM Simonsick T Harris RI Shorr FA Tylavsky AB Newman 2004 The metabolic syndrome, inflammation, and risk of cognitive decline JAMA 292 2237 2242
99. SS Zhan W Kamphorst WE VanNostrand P Eikelenboom 1995a Distribution of neuronal growth-promoting factors and cytoskeletal proteins in altered neurites in Alzheimer's disease and non-demented elderly Acta Neuropathol (Berl) 89 356 362
100. SS Zhan R Veerhuis W Kamphorst P Eikelenboom 1995b Distribution of beta amyloid associated proteins in plaques in Alzheimer's disease and in non-demented elderly Neurodegeneration 4 291 297
101. BV Zlokovic 2004 Clearing amyloid through the blood-brain barrier J Neurochem 89 807 811
102. BV Zlokovic B Frangione 2003 Transport clearance hypothesis for Alzheimer's disease and potential implications TC Saido Aβ metabolism and Alzheimer's disease Landes Bioscience Georgetown Texas, USA 117 125