A reduced astrocyte response to β-amyloid plaques in the ageing brain associates with cognitive impairment

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Mathur, Ryan ^a   Ince, Paul G ^a   Minett, Thais ^b   Garwood, Claire J ^a   Shaw, Pamela J ^a   Matthews, Fiona E ^c   Brayne, Carol ^b   Simpson, Julie E ^a   Wharton, Stephen B ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c MRC BIOSTATISTICS UNIT   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; APOLIPOPROTEIN E4; GLIAL FIBRILLARY ACIDIC PROTEIN;

AGED; AGING; ALZHEIMER DISEASE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; CELL STIMULATION; CINGULATE GYRUS; COGNITIVE DEFECT; CONTROLLED STUDY; CORTEX LAYER VI; DEATH; DISEASE ASSOCIATION; DISEASE CLASSIFICATION; FEMALE; GENE DOSAGE; GENOTYPE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; MINI MENTAL STATE EXAMINATION; NEUROPATHOLOGY; NEUROPROTECTION; QUANTITATIVE ANALYSIS; SEX DIFFERENCE; AMYLOID PLAQUE; METABOLISM; PATHOLOGY; VERY ELDERLY;

AGED; AGED, 80 AND OVER; AGING; AMYLOID BETA-PEPTIDES; ASTROCYTES; COGNITION DISORDERS; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; MALE; PLAQUE, AMYLOID;

EID: 84951077640     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118463     Document Type: Article

References (75)

1. Querfurth HW, LaFerla FM. Alzheimer's disease. N Engl J Med. 2010;362:329-344. doi: 10.1056/NEJMra0909142 PMID: 20107219
2. Rozemuller JM, Eikelenboom P, Stam FC, Beyreuther K, Masters CL. A4 protein in Alzheimer's disease: primary and secondary cellular events in extracellular amyloid deposition. J Neuropathol Exp Neurol. 1989;48:674-691. PMID: 2677252
3. Tagliavini F, Giaccone G, Frangione B, Bugiani O. Preamyloid deposits in the cerebral cortex of patients with Alzheimer's disease and nondemented individuals. Neurosci Lett. 1988;93:191-196. PMID: 3241644
4. Dickson TC, Vickers JC. The morphological phenotype of beta-amyloid plaques and associated neuritic changes in Alzheimer's disease. Neuroscience. 2001;105:99-107. PMID: 11483304
5. Thal DR, Rub U, Schultz C, Sassin I, Ghebremedhin E, Del Tredici K. Sequence of Abeta-protein deposition in the human medial temporal lobe. J Neuropathol Exp Neurol. 2000;59:733-748. PMID: 10952063
6. Matthews F, Brayne C. The incidence of dementia in England and Wales: findings from the five identical sites of the MRC CFA Study. PLoS Med. 2005;2:e193. PMID: 16111436
7. CFANS. Pathological correlates of late-onset dementia in a multicentre, community-based population in England and Wales. Neuropathology Group of the Medical Research Council Cognitive Function and Ageing Study (MRC CFAS). Lancet. 2001;357:169-175. PMID: 11213093
8. Savva GM, Wharton SB, Ince PG, Forster G, Matthews FE, Brayne C. Age, neuropathology, and dementia. N Engl J Med. 2009;360:2302-2309. doi: 10.1056/NEJMoa0806142 PMID: 19474427
9. Maragakis NJ, Rothstein JD. Mechanisms of Disease: astrocytes in neurodegenerative disease. Nat Clin Pract Neurol. 2006;2:679-689. PMID: 17117171
10. Itagaki S, McGeer PL, Akiyama H, Zhu S, Selkoe D. Relationship of microglia and astrocytes to amyloid deposits of Alzheimer disease. J Neuroimmunol. 1989;24:173-182. PMID: 2808689
11. Serrano-Pozo A, Mielke ML, Gomez-Isla T, Betensky RA, Growdon JH, Frosch MP, et al. Reactive glia not only associates with plaques but also parallels tangles in Alzheimer's disease. Am J Pathol 2011;179:1373-1384. doi: 10.1016/j.ajpath.2011.05.047 PMID: 21777559
12. Kamphuis W, Middeldorp J, Kooijman L, Sluijs JA, Kooi EJ, Moeton M, et al. Glial fibrillary acidic protein isoform expression in plaque related astrogliosis in Alzheimer's disease. Neurobiol Aging. 2014;35:492-510. doi: 10.1016/j.neurobiolaging.2013.09.035 PMID: 24269023
13. Thal DR. The role of astrocytes in amyloid beta-protein toxicity and clearance. Exp Neurol. 2012;236:1-5. doi: 10.1016/j.expneurol.2012.04.021 PMID: 22575598
14. Medeiros R, LaFerla FM. Astrocytes: conductors of the Alzheimer disease neuroinflammatory symphony. Exp Neurol. 2013;239:133-138. doi: 10.1016/j.expneurol.2012.10.007 PMID: 23063604
15. Rodriguez JJ, Olabarria M, Chvatal A, Verkhratsky A. Astroglia in dementia and Alzheimer's disease. Cell Death Differ. 2009;16:378-385. doi: 10.1038/cdd.2008.172 PMID: 19057621
16. Sofroniew MV, Vinters HV. Astrocytes: biology and pathology. Acta Neuropathol. 2010;119:7-35. doi: 10.1007/s00401-009-0619-8 PMID: 20012068
17. Broe M, Kril J, Halliday GM. Astrocytic degeneration relates to the severity of disease in frontotemporal dementia. Brain. 2004;127:2214-2220. PMID: 15282215
18. Nagele RG, D'Andrea MR, Lee H, Venkataraman V, Wang HY. Astrocytes accumulate A beta 42 and give rise to astrocytic amyloid plaques in Alzheimer disease brains. Brain Res. 2003;971:197-209. PMID: 12706236
19. Kersaitis C, Halliday GM, Kril JJ. Regional and cellular pathology in frontotemporal dementia: relationship to stage of disease in cases with and without Pick bodies. Acta Neuropathol. 2004;108:515-523. PMID: 15368070
20. DeWitt DA, Perry G, Cohen M, Doller C, Silver J. Astrocytes regulate microglial phagocytosis of senile plaque cores of Alzheimer's disease. Exp Neurol. 1998;149:329-340. PMID: 9500964
21. Bertram L, McQueen MB, Mullin K, Blacker D, Tanzi RE. Systematic meta-analyses of Alzheimer disease genetic association studies: the AlzGene database. Nat Genet. 2007;39:17-23. PMID: 17192785
22. McNamara MJ, Gomez-Isla T, Hyman BT. Apolipoprotein E genotype and deposits of Abeta40 and Abeta42 in Alzheimer disease. Arch Neurol. 1998;55:1001-1004. PMID: 9678319
23. Schmechel DE, Saunders AM, Strittmatter WJ, Crain BJ, Hulette CM, Joo SH, et al. Increased amyloid beta-peptide deposition in cerebral cortex as a consequence of apolipoprotein E genotype in late-onset Alzheimer disease. Proc Natl Acad Sci USA. 1993;90:9649-9653. PMID: 8415756
24. Tiraboschi P, Hansen LA, Masliah E, Alford M, Thal LJ, Corey-Bloom J. Impact of APOE genotype on neuropathologic and neurochemical markers of Alzheimer disease. Neurology. 2004;62:1977-1983. PMID: 15184600
25. Simpson JE, Ince PG, Shaw PJ, Heath PR, Raman R, Garwood CJ, et al. Microarray analysis of the astrocyte transcriptome in the aging brain: relationship to Alzheimer's pathology and APOE genotype. Neurobiol Aging. 2011;32:1795-1807. doi: 10.1016/j.neurobiolaging.2011.04.013 PMID: 21705112
26. Kim J, Basak JM, Holtzman DM. The role of apolipoprotein E in Alzheimer's disease. Neuron. 2009;63:287-303. doi: 10.1016/j.neuron. 2009.06.026 PMID: 19679070
27. Verghese PB, Castellano JM, Holtzman DM. Apolipoprotein E in Alzheimer's disease and other neurological disorders. Lancet Neurol. 2011;10:241-252. doi: 10.1016/S1474-4422 (10) 70325-2 PMID: 21349439
28. Koistinaho M, Lin S, Wu X, Esterman M, Koger D, Hanson J, et al. Apolipoprotein E promotes astrocyte colocalization and degradation of deposited amyloid-beta peptides. Nat Med. 2004;10:719-726. PMID: 15195085
29. Simpson JE, Ince PG, Lace G, Forster G, Shaw PJ, Matthews F, et al. Astrocyte phenotype in relation to Alzheimer-type pathology in the ageing brain. Neurobiol Aging. 2010;31:578-590. doi: 10.1016/j. neurobiolaging.2008.05.015 PMID: 18586353
30. Sutherland RJ, Whishaw IQ, Kolb B. Contributions of cingulate cortex to two forms of spatial learning and memory. J Neurosci. 1988;8:1863-1872. PMID: 3385478
31. Thal DR, Rub U, Orantes M, Braak H. Phases of A beta-deposition in the human brain and its relevance for the development of AD. Neurology. 2002;58:1791-1800. PMID: 12084879
32. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991;82:239-259. PMID: 1759558
33. Huang C, Wahlund LO, Svensson L, Winblad B, Julin P. Cingulate cortex hypoperfusion predicts Alzheimer's disease in mild cognitive impairment. BMC Neurol. 2002;2:9. PMID: 12227833
34. Minoshima S, Giordani B, Berent S, Frey KA, Foster NL, Kuhl DE. Metabolic reduction in the posterior cingulate cortex in very early Alzheimer's disease. Ann Neurol. 1997;42:85-94. PMID: 9225689
35. CFANS. Cognitive function and dementia in six areas of England and Wales: the distribution of MMSE and prevalence of GMS organicity level in the MRC CFA Study. The Medical Research Council Cognitive Function and Ageing Study (MRC CFAS). Psychol Med. 1998;28:319-335. PMID: 9572090
36. Wharton SB, Brayne C, Savva GM, Matthews FE, Forster G, Simpson J, et al. Epidemiological neuropathology: the MRC Cognitive Function and Aging Study experience. J Alzheimers Dis. 2011;25:359-372. doi: 10.3233/JAD-2011-091402 PMID: 21422529
37. Ince PG, McArthur FK, Bjertness E, Torvik A, Candy JM, Edwardson J. Neuropathological diagnoses in elderly patients in Oslo: Alzheimer's disease, Lewy body disease, vascular lesions. Dementia. 1995;6:162-168. PMID: 7620529
38. Mirra SS. The CERAD neuropathology protocol and consensus recommendations for the postmortem diagnosis of Alzheimer's disease: a commentary. Neurobiol Aging. 1997;18:S91-94. PMID: 9330994
39. Braak H, Alafuzoff I, Arzberger T, Kretzschmar H, Del Tredici K. Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol. 2006;112:389-404. PMID: 16906426
40. Nicoll JA, Savva GM, Stewart J, Matthews FE, Brayne C, Ince PG. Association between APOE genotype, neuropathology and dementia in the older population of England and Wales. Neuropathol Appl Neurobiol. 2011;37:285-294. doi: 10.1111/j.1365-2990.2010.01130.x PMID: 20880354
41. Yip AG, Brayne C, Easton D, Rubinsztein DC. Apolipoprotein E4 is only a weak predictor of dementia and cognitive decline in the general population. J Med Genet. 2002;39:639-643. PMID: 12205106
42. Akiyama H, Mori H, Saido T, Kondo H, Ikeda K, McGeer PL. Occurrence of the diffuse amyloid betaprotein (Abeta) deposits with numerous Abeta-containing glial cells in the cerebral cortex of patients with Alzheimer's disease. Glia. 1999;25:324-331. PMID: 10028915
43. Oh D, Prayson RA. Evaluation of epithelial and keratin markers in glioblastoma multiforme: an immunohistochemical study. Arch Pathol Lab Med. 1999;123:917-920. PMID: 10506444
44. Greenfield JG, Love S, Louis DN, Ellison DP. Greenfield's neuropathology. London: Hodder Arnold. 2008.
45. Gwet KL. Computing inter-rater reliability and its variance in the presence of high agreement. Br J Math Stat Psychol. 2008;61:29-48. doi: 10.1348/000711006X126600 PMID: 18482474
46. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33:159-174. PMID: 843571
47. Serrano-Pozo A, Muzikansky A, Gomez-Isla T, Growdon JH, Betensky RA, Frosch MP, et al. Differential relationships of reactive astrocytes and microglia to fibrillar amyloid deposits in Alzheimer disease. J Neuropathol Exp Neurol. 2013;72:462-471. doi: 10.1097/NEN.0b013e3182933788 PMID: 23656989
48. Hardy J. The amyloid hypothesis for Alzheimer's disease: a critical reappraisal. J Neurochem. 2009;110:1129-1134. doi: 10.1111/j.1471-4159.2009.06181.x PMID: 19457065
49. Holmes C, Boche D, Wilkinson D, Yadegarfar G, Hopkins V, Bayer A, et al. Long-term effects of Abeta42 immunisation in Alzheimer's disease: follow-up of a randomised, placebo-controlled phase I trial. Lancet. 2008;372:216-223. doi: 10.1016/S0140-6736 (08) 61075-2 PMID: 18640458
50. Fotuhi M, Hachinski V, Whitehouse PJ. Changing perspectives regarding late-life dementia. Nat Rev Neurol. 2009;5:649-658. doi: 10.1038/nrneurol.2009.175 PMID: 19918254
51. Romito-Di Giacomo RR, Menegay H, Cicero SA, Herrup K. Effects of Alzheimer's disease on different cortical layers: the role of intrinsic differences in Abeta susceptibility. J Neurosci. 2007;27:8496-8504. PMID: 17687027
52. Morgan C, Colombres M, Nunez MT, Inestrosa NC. Structure and function of amyloid in Alzheimer's disease. Prog Neurobiol. 2004;74:323-349. PMID: 15649580
53. Gouras GK, Almeida CG, Takahashi RH. Intraneuronal Abeta accumulation and origin of plaques in Alzheimer's disease. Neurobiol Aging. 2005;26:1235-1244. PMID: 16023263
54. Wirths O, Multhaup G, Bayer TA. A modified beta-amyloid hypothesis: intraneuronal accumulation of the beta-amyloid peptide-The first step of a fatal cascade. J Neurochem. 2004;91:513-520. PMID: 15485483
55. LaFerla FM, Green KN, Oddo S. Intracellular amyloid-beta in Alzheimer's disease. Nat Rev Neurosci. 2007;8:499-509. PMID: 17551515
56. Parpura V, Heneka MT, Montana V, Oliet SH, Schousboe A, Haydon PG, et al. Glial cells in (patho) physiology. J Neurochem. 2012;121:4-27. doi: 10.1111/j.1471-4159.2012.07664.x PMID: 22251135
57. Gozes I, Bassan M, Zamostiano R, Pinhasov A, Davidson A, Giladi E, et al. A novel signaling molecule for neuropeptide action: activity-dependent neuroprotective protein. Ann N Y Acad Sci. 1999;897:125-135. PMID: 10676441
58. Paradisi S, Sacchetti B, Balduzzi M, Gaudi S, Malchiodi-Albedi F. Astrocyte modulation of in vitro betaamyloid neurotoxicity. Glia. 2004;46:252-260. PMID: 15048848
59. Belanger M, Magistretti PJ. The role of astroglia in neuroprotection. Dialogues Clin Neurosci. 2009;11:281-295. PMID: 19877496
60. Serrano-Pozo A, Frosch MP, Masliah E, Hyman BT. Neuropathological alterations in Alzheimer disease. Cold Spring Harb Perspect Med. 2011;1:a006189. doi: 10.1101/cshperspect.a006189 PMID: 22229116
61. Ikeda K, Akiyama H, Haga C, Haga S. (1992) Evidence that neurofibrillary tangles undergo glial modification. Acta Neuropathol. 1992;85:101-104. PMID: 1285492
62. Masliah E. The role of synaptic proteins in Alzheimer's disease. Ann N Y Acad Sci. 2000;924:68-75. PMID: 11193804
63. Crews L, Masliah E. Molecular mechanisms of neurodegeneration in Alzheimer's disease. Hum Mol Genet. 2010;19:R12-20. doi: 10.1093/hmg/ddq160 PMID: 20413653
64. Grutzendler J, Helmin K, Tsai J, Gan WB. Various dendritic abnormalities are associated with fibrillar amyloid deposits in Alzheimer's disease. Ann N Y Acad Sci. 2007;1097:30-39. PMID: 17413007
65. Knobloch M, Mansuy IM. Dendritic spine loss and synaptic alterations in Alzheimer's disease. Mol Neurobiol. 2008;37:73-82. doi: 10.1007/s12035-008-8018-z PMID: 18438727
66. Christensen DZ, Schneider-Axmann T, Lucassen PJ, Bayer TA, Wirths O. Accumulation of intraneuronal Abeta correlates with ApoE4 genotype. Acta Neuropathol. 2010;119:555-566. doi: 10.1007/s00401-010-0666-1 PMID: 20217101
67. Overmyer M, Helisalmi S, Soininen H, Laakso M, Riekkinen P Sr, Alafuzoff I. Astrogliosis and the ApoE genotype. an immunohistochemical study of postmortem human brain tissue. Dement Geriatr Cogn Disord. 1999;10:252-257. PMID: 10364641
68. Olichney JM, Hansen LA, Galasko D, Saitoh T, Hofstetter CR, Katzman R, et al. The apolipoprotein E epsilon 4 allele is associated with increased neuritic plaques and cerebral amyloid angiopathy in Alzheimer's disease and Lewy body variant. Neurology. 1996;47:190-196. PMID: 8710076
69. Sparks DL, Scheff SW, Liu H, Landers T, Danner F, Coyne CM, et al. Increased density of senile plaques (SP), but not neurofibrillary tangles (NFT), in non-demented individuals with the apolipoprotein E4 allele: comparison to confirmed Alzheimer's disease patients. J Neurol Sci. 1996;138:97-104. PMID: 8791246
70. Wyss-Coray T. Inflammation in Alzheimer disease: driving force, bystander or beneficial response? Nat Med. 2006;12:1005-1015. PMID: 16960575
71. Perry VH, Nicoll JA, Holmes C. Microglia in neurodegenerative disease. Nat Rev Neurol. 2010;6:193-201. doi: 10.1038/nrneurol.2010.17 PMID: 20234358
72. Rogers J, Strohmeyer R, Kovelowski CJ, Li R. Microglia and inflammatory mechanisms in the clearance of amyloid beta peptide. Glia. 2002;40:260-269. PMID: 12379913
73. Yang CN, Shiao YJ, Shie FS, Guo BS, Chen PH, Cho CY, et al. Mechanism mediating oligomeric Abeta clearance by naive primary microglia. Neurobiol Dis. 2011;42:221-230. doi: 10.1016/j.nbd. 2011.01.005 PMID: 21220023
74. Marlatt MW, Bauer J, Aronica E, van Haastert ES, Hoozemans JJ, Joels M, et al. Proliferation in the Alzheimer hippocampus is due to microglia, not astroglia, and occurs at sites of amyloid deposition. Neural Plast. 2014:693851. doi: 10.1155/2014/693851 PMID: 25215243
75. Giulian D, Li J, Li X, George J, Rutecki PA. The impact of microglia-derived cytokines upon gliosis in the CNS. Dev Neurosci. 1994;16:128-136. PMID: 7535679