An early and late peak in microglial activation in Alzheimer’s disease trajectory

Brain

Volumn 140, Issue 3, 2017, Pages 792-803

  Fan, Zhen ^a   Brooks, David J ^a,b   Okello, Aren ^a   Edison, Paul ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

Alzheimer s disease; Amyloid imaging; Microglial activation; Mild cognitive impairment; Neuropathology

Indexed keywords

AMYLOID; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE C 11; PIB C 11; RADIOPHARMACEUTICAL AGENT; UNCLASSIFIED DRUG; 2-(4'-(METHYLAMINO)PHENYL)-6-HYDROXYBENZOTHIAZOLE; ANILINE DERIVATIVE; ANTINEOPLASTIC AGENT; CARBON; ISOQUINOLINE DERIVATIVE; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE; THIAZOLE DERIVATIVE;

ADULT; AGED; ALZHEIMER DISEASE; ANTERIOR CINGULATE; ARTICLE; CELL ACTIVATION; CLINICAL ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; FOLLOW UP; FRONTAL CORTEX; FRONTAL LOBE; HIPPOCAMPUS; HUMAN; LONGITUDINAL STUDY; MALE; MICROGLIA; MIDDLE AGED; MILD COGNITIVE IMPAIRMENT; NUCLEAR MAGNETIC RESONANCE IMAGING; OCCIPITAL CORTEX; OCCIPITAL LOBE; PARIETAL CORTEX; PHENOTYPE; POSITRON EMISSION TOMOGRAPHY; POSTERIOR CINGULATE; PRIORITY JOURNAL; TEMPORAL CORTEX; TEMPORAL LOBE; BRAIN MAPPING; COGNITION DISORDERS; COHORT ANALYSIS; DIAGNOSTIC IMAGING; PATHOLOGY; THREE DIMENSIONAL IMAGING;

AGED; ALZHEIMER DISEASE; ANILINE COMPOUNDS; ANTINEOPLASTIC AGENTS; BRAIN MAPPING; CARBON RADIOISOTOPES; COGNITION DISORDERS; COHORT STUDIES; FEMALE; HUMANS; IMAGING, THREE-DIMENSIONAL; ISOQUINOLINES; MAGNETIC RESONANCE IMAGING; MALE; MICROGLIA; MIDDLE AGED; POSITRON-EMISSION TOMOGRAPHY; THIAZOLES;

EID: 85018899137     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aww349     Document Type: Article

References (44)

1. Amor S, Puentes F, Baker D, van der Valk P. Inflammation in neurodegenerative diseases. Immunology 2010; 129: 154–69.
2. Anderson AN, Pavese N, Edison P, Tai YF, Hammers A, Gerhard A, et al. A systematic comparison of kinetic modelling methods generating parametric maps for [(11)C]-(R)-PK11195. Neuroimage 2007; 36: 28–37.
3. Cai Z, Hussain MD, Yan LJ. Microglia, neuroinflammation, and beta-amyloid protein in Alzheimer’s disease. Int J Neurosci 2013; 124: 307–21.
4. Casanova R, Srikanth R, Baer A, Laurienti PJ, Burdette JH, Hayasaka S, et al. Biological parametric mapping: a statistical toolbox for multimodality brain image analysis. Neuroimage 2007; 34: 137–43.
5. Craig-Schapiro R, Perrin RJ, Roe CM, Xiong C, Carter D, Cairns NJ, et al. YKL-40: a novel prognostic fluid biomarker for preclinical Alzheimer’s disease. Biol Psychiatry 2010; 68: 903–12.
6. Cunningham C. Microglia and neurodegeneration: the role of systemic inflammation. Glia 2013; 61: 71–90.
7. Doens D, Fernandez PL. Microglia receptors and their implications in the response to amyloid beta for Alzheimer’s disease pathogenesis. J Neuroinflammation 2014; 11: 48.
8. Edison P, Ahmed I, Fan Z, Hinz R, Gelosa G, Ray Chaudhuri K, et al. Microglia, amyloid, and glucose metabolism in Parkinson’s disease with and without dementia. Neuropsychopharmacology 2013; 38: 938–49.
9. Edison P, Archer HA, Gerhard A, Hinz R, Pavese N, Turkheimer FE, et al. Microglia, amyloid, and cognition in Alzheimer’s disease: an [11C](R)PK11195-PET and [11C]PIB-PET study. Neurobiol Dis 2008; 32: 412–19.
10. Fan Z, Aman Y, Ahmed I, Chetelat G, Landeau B, Ray Chaudhuri K, et al. Influence of microglial activation on neuronal function in Alzheimer’s and Parkinson’s disease dementia. Alzheimers Dement 2015a; 11: 608–21.e7.
11. Fan Z, Okello AA, Brooks DJ, Edison P. Longitudinal influence of microglial activation and amyloid on neuronal function in Alzheimer’s disease. Brain 2015b; 138 (Pt 12): 3685–98.
12. Fraser DA, Pisalyaput K, Tenner AJ. C1q enhances microglial clearance of apoptotic neurons and neuronal blebs, and modulates subsequent inflammatory cytokine production. J Neurochem 2010; 112: 733–43.
13. Guerreiro R, Hardy J. TREM2 and neurodegenerative disease. N Engl J Med 2013; 369: 1569–70.
14. Guerreiro RJ, Hardy J. Alzheimer’s disease genetics: lessons to improve disease modelling. Biochem Soc Trans 2011; 39: 910–16.
15. Hamelin L, Lagarde J, Dorothee G, Leroy C, Labit M, Comley RA, et al. Early and protective microglial activation in Alzheimer’s disease: a prospective study using 18F-DPA-714 PET imaging. Brain 2016; 139 (Pt 4): 1252–64.
16. Heneka MT, Carson MJ, El Khoury J, Landreth GE, Brosseron F, Feinstein DL, et al. Neuroinflammation in Alzheimer’s disease. Lancet Neurol 2015; 14: 388–405.
17. Heslegrave A, Heywood W, Paterson R, Magdalinou N, Svensson J, Johansson P, et al. Increased cerebrospinal fluid soluble TREM2 concentration in Alzheimer’s disease. Mol Neurodegener 2016; 11: 3.
18. Hollingworth P, Harold D, Jones L, Owen MJ, Williams J. Alzheimer’s disease genetics: current knowledge and future challenges. Int J Geriatr Psychiatry 2011a; 26: 793–802.
19. Hollingworth P, Harold D, Sims R, Gerrish A, Lambert JC, Carrasquillo MM, et al. Common variants at ABCA7, MS4A6A/ MS4A4E, EPHA1, CD33 and CD2AP are associated with Alzheimer’s disease. Nat Genet 2011b; 43: 429–35.
20. Jack CR Jr, Knopman DS, Jagust WJ, Shaw LM, Aisen PS, Weiner MW, et al. Hypothetical model of dynamic biomarkers of the Alzheimer’s pathological cascade. Lancet Neurol 2010; 9: 119–28.
21. Jaturapatporn D, Isaac MG, McCleery J, Tabet N. Aspirin, steroidal and non-steroidal anti-inflammatory drugs for the treatment of Alzheimer’s disease. Cochrane Database Syst Rev 2012; 2: CD006378.
22. Jiang T, Yu JT, Zhu XC, Tan L. TREM2 in Alzheimer’s disease. Mol Neurobiol 2013; 48: 180–5.
23. Lim YY, Maruff P, Pietrzak RH, Ames D, Ellis KA, Harrington K, et al. Effect of amyloid on memory and non-memory decline from preclinical to clinical Alzheimer’s disease. Brain 2014; 137: 221–31.
24. Lyman M, Lloyd DG, Ji X, Vizcaychipi MP, Ma D. Neuroinflammation: the role and consequences. Neurosci Res 2014; 79: 1–12.
25. Lynch MA. The impact of neuroimmune changes on development of amyloid pathology; relevance to Alzheimer’s disease. Immunology 2013; 141: 292–301.
26. Mandrekar-Colucci S, Landreth GE. Microglia and inflammation in Alzheimer’s disease. Cns Neurol Disord Drug Targets 2010; 9: 156–67.
27. Okello A, Koivunen J, Edison P, Archer HA, Turkheimer FE, Nagren K, et al. Conversion of amyloid positive and negative MCI to AD over 3 years: an 11C-PIB PET study. Neurology 2009; 73: 754–60.
28. Pan XD, Zhu YG, Lin N, Zhang J, Ye QY, Huang HP, et al. Microglial phagocytosis induced by fibrillar beta-amyloid is attenuated by oligomeric beta-amyloid: implications for Alzheimer’s disease. Mol Neurodegener 2011; 6: 45.
29. Piccio L, Deming Y, Del-Águila JL, Ghezzi L, Holtzman DM, Fagan AM, et al. Cerebrospinal fluid soluble TREM2 is higher in Alzheimer disease and associated with mutation status. Acta Neuropathol 2016; 131: 925–33.
30. Prokop S, Miller KR, Heppner FL. Microglia actions in Alzheimer’s disease. Acta Neuropathol 2013; 126: 461–77.
31. Rogers J, Strohmeyer R, Kovelowski CJ, Li R. Microglia and inflammatory mechanisms in the clearance of amyloid beta peptide. Glia 2002; 40: 260–9.
32. Sanchez-Guajardo V, Barnum CJ, Tansey MG, Romero-Ramos M. Neuroimmunological processes in Parkinson’s disease and their relation to alpha-synuclein: microglia as the referee between neuronal processes and peripheral immunity. ASN Neuro 2013; 5: 113–39.
33. Sastre M, Klockgether T, Heneka MT. Contribution of inflammatory processes to Alzheimer’s disease: molecular mechanisms. Int J Dev Neurosci 2006; 24: 167–76.
34. Schuitemaker A, Kropholler MA, Boellaard R, van der Flier WM, Kloet RW, van der Doef TF, et al. Microglial activation in Alzheimer’s disease: an (R)-[(1)(1)C]PK11195 positron emission tomography study. Neurobiol Aging 2013; 34: 128–36.
35. Shidahara M, Tsoumpas C, Hammers A, Boussion N, Visvikis D, Suhara T, et al. Functional and structural synergy for resolution recovery and partial volume correction in brain PET. Neuroimage 2009; 44: 340–8.
36. Suárez-Calvet M, Kleinberger G, Araque Caballero MÁ, Brendel M, Rominger A, Alcolea D, et al. sTREM2 cerebrospinal fluid levels are a potential biomarker for microglia activity in early-stage Alzheimer’s disease and associate with neuronal injury markers. EMBO Mol Med 2016; 8: 466–76.
37. Turkheimer FE, Edison P, Pavese N, Roncaroli F, Anderson AN, Hammers A, et al. Reference and target region modeling of [11C]-(R)-PK11195 brain studies. J Nucl Med 2007; 48: 158–67.
38. Turkheimer FE, Smith CB, Schmidt K. Estimation of the number of “true” null hypotheses in multivariate analysis of neuroimaging data. Neuroimage 2001; 13: 920–30.
39. Varley J, Brooks DJ, Edison P. Imaging neuroinflammation in Alzheimer’s disease and other dementias: recent advances and future directions. Alzheimers Dement 2015; 11: 1110–20.
40. Varnum MM, Ikezu T. The classification of microglial activation phenotypes on neurodegeneration and regeneration in Alzheimer’s disease brain. Arch Immunol Ther Exp (Warsz) 2012; 60: 251–66.
41. Villemagne VL, Burnham S, Bourgeat P, Brown B, Ellis KA, Salvado O, et al. Amyloid beta deposition, neurodegeneration, and cognitive decline in sporadic Alzheimer’s disease: a prospective cohort study. Lancet Neurol 2013; 12: 357–67.
42. von Bernhardi R, Eugenin-von Bernhardi L, Eugenin J. Microglial cell dysregulation in brain aging and neurodegeneration. Front Aging Neurosci 2015; 7: 124.
43. Yasuno F, Kosaka J, Ota M, Higuchi M, Ito H, Fujimura Y, et al. Increased binding of peripheral benzodiazepine receptor in mild cognitive impairment-dementia converters measured by positron emission tomography with [(1)(1)C]DAA1106. Psychiatry Res 2012; 203: 67–74.
44. Zotova E, Bharambe V, Cheaveau M, Morgan W, Holmes C, Harris S, et al. Inflammatory components in human Alzheimer’s disease and after active amyloid-beta42 immunization. Brain 2013; 136 (Pt 9): 2677–96.