Patterns of microglial cell activation in frontotemporal lobar degeneration

Neuropathology and Applied Neurobiology

Volumn 40, Issue 6, 2014, Pages 686-696

  Lant, Suzannah B ^a   Robinson, Andrew C ^a   Thompson, Jennifer C ^a   Rollinson, Sara ^a   Pickering Brown, Stuart ^a   Snowden, Julie S ^a   Davidson, Yvonne S ^a   Gerhard, Alexander ^a   Mann, David M A ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Alzheimer's disease; CD68 immunohistochemistry; Frontotemporal lobar degeneration; Microglial cells

Indexed keywords

BIOLOGICAL MARKER;

ADULT; AGED; ALZHEIMER DISEASE; BRAIN; FEMALE; FRONTOTEMPORAL DEMENTIA; GRAY MATTER; HUMAN; MALE; MICROGLIA; MIDDLE AGED; PATHOLOGY; VERY ELDERLY; WHITE MATTER;

ADULT; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; BIOLOGICAL MARKERS; BRAIN; FEMALE; FRONTOTEMPORAL LOBAR DEGENERATION; GRAY MATTER; HUMANS; MALE; MICROGLIA; MIDDLE AGED; WHITE MATTER;

EID: 84913536488     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/nan.12092     Document Type: Article

References (40)

1. Neary D, Snowden JS, Mann DMA. Frontotemporal lobar degeneration: clinical and pathological relationships. Acta Neuropathol (Berl) 2007; 114: 31-38
2. Shi J, Shaw CL, Richardson AMT, Bailey K, Tian J, Varma AR, Neary D, Snowden JS, Mann DMA. Histopathological changes underlying frontotemporal lobar degeneration with clinicopathological correlation. Acta Neuropathol (Berl) 2005; 110: 501-512
3. Baborie A, Griffiths TD, Jaros E, Richardson A, Ferrari R, Moreno J, Momeni P, McKeith IG, Burn DJ, Duplessis D, Pal P, Rollinson S, Pickering-Brown SM, Thompson JC, Neary D, Snowden JS, Perry R, Mann DMA. Pathological correlates of frontotemporal lobar degeneration in the elderly. Acta Neuropathol (Berl) 2011; 122: 365-373
4. Mackenzie IRA, Neumann M, Baborie A, Sampathu DM, Du Plessis D, Jaros E, Perry RH, Trojanowski JQ, Mann DMA, Lee VM-Y. A harmonized classification system for FTLD-TDP pathology. Acta Neuropathol (Berl) 2011; 122: 111-113
5. Hutton M, Lendon CL, Rizzu P, Baker M, Froelich S, Houlden M, Pickering-Brown SM, Chakraverty S, Isaacs A, Grover A, Hackett J, Adamson J, Lincoln S, Dickson D, Davies P, Petersen RC, Stevens M, de Graaf E, Wauters E, van Baren J, Hillebrand M, Joosse M, Kwon JM, Nowotny P, Che LK, Norton J, Morris JC, Reed LA, Trojanowski JQ, Basun H, Lannfelt L, Neystat M, Fahn S, Dark F, Tannenberg T, Dodd P, Hayward N, Kwok JBJ, Schofield PR, Andreadis A, Snowden J, Craufurd D, Neary D, Owen F, Oostra BA, Hardy J, Goate A, van Swieten J, Mann DM, Lynch T, Heutink P. Association of missense and 5'-splice-site mutation in tau with inherited dementia FTDP-17. Nature 1998; 393: 702-705
6. Arai T, Hasegawa M, Akiyama H, Ikeda K, Nonaka T, Mori H, Mann D, Tsuchiya K, Yoshida M, Hashizume Y, Oda T. TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem Biophys Res Commun 2006; 351: 602-611
7. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, Bruce J, Schuck T, Grossman M, Clark CM, McCluskey LF, Miller BL, Masliah E, Mackenzie IR, Feldman H, Feiden W, Kretzschmar H, Trojanowski JQ, Lee VM. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006; 314: 130-133
8. Baker M, Mackenzie IRA, Pickering-Brown SM, Gass J, Rademakers R, Lindholm C, Snowden J, Adamson J, Sadovnick AD, Rollinson S, Cannon A, Dwosh E, Neary D, Melquist S, Richardson A, Dickson D, Eriksen J, Robinson T, Zehr C, Dickey CA, Crook R, McGowan E, Mann D, Boeve B, Feldman H, Hutton M. Mutations in Progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature 2006; 442: 916-919
9. Cruts M, Gijselinck I, van der Zee J, Engelborghs S, Wils H, Pirici D, Rademakers R, Vandenberghe R, Dermaut B, Martin JJ, van Duijn C, Peeters K, Sciot R, Santens P, De Pooter T, Mattheijssens M, Van den Broeck M, Cuijt I, Vennekens K, De Deyn PP, Kumar-Singh S, Van Broeckhoven C Null mutations in progranulin cause ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Nature 2006; 442: 920-924
10. DeJesus-Hernandez M, Mackenzie IR, Boeve BF, Boxer AL, Baker M, Rutherford NJ, Nicholson AM, Finch NA, Flynn H, Adamson J, Kouri N, Wojtas A, Sengdy P, Hsiung GY, Karydas A, Seeley WW, Josephs KA, Coppola G, Geschwind DH, Wszolek ZK, Feldman H, Knopman DS, Petersen RC, Miller BL, Dickson DW, Boylan KB, Graff-Radford NR, Rademakers R. Expanded GGGGCC Hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 2011; 72: 245-256
11. Renton AE, Majounie E, Waite A, Simón-Sánchez J, Rollinson S, Gibbs JR, Laaksovirta H, Schymick JC, van Swieten J, Myllykangas L, Kalimo H, Paetau A, Abramzon Y, Remes AM, Kaganovich A, Scholz SW, Duckworth J, Ding J, Harmer DW, Hernandez DG, Johnson JO, Mok K, Ryten M, Trabzuni D, Guerreiro RJ, Orrell RW, Neal J, Murray A, Pearson J, Jansen IE, Sondervan D, Seelaar H, Blake D, Young K, Halliwell N, Callister J, Toulson G, Richardson A, Gerhard A, Snowden J, Mann D, Neary D, Nalls MA, Peuralinna T, Jansson L, Isoviita V-M, Kaivorinne A-L, Holtta-Vuori M, Ikonen E, Sulkava R, Benatar M, Wuu J, Chio A, Restagno G, Borghero G, Sabatelli M, The ITALSGEN Consortium, Heckerman D, Rogaeva E, Zinman L, Rothstein J, Sendtner M, Drepper C, Eichler EE, Alkan C, Abdullaev Z, Pack SD, Dutra A, Pak E, Hardy J, Singleton A, Williams NM, Heutink P, Pickering-Brown S, Morris HR, Tienari PJ, Traynor BJ. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked amyotrophic lateral sclerosis-frontotemporal dementia. Neuron 2011; 72: 257-268
12. Snowden JS, Rollinson S, Thompson JC, Harris J, Stopford CL, Richardson A, Jones M, Gerhard A, Davidson Y, Robinson A, Gibbons L, Hu Q, Halliwell N, DuPlessis D, Neary D, Mann DMA, Pickering-Brown S. Distinct clinical characteristics in patients with frontotemporal dementia and C9ORF72 mutations: a study of demographics, neurology, behaviour, cognition, and histopathology. Brain 2012; 135: 693-708
13. Neumann M, Rademakers R, Roeber S, Baker M, Kretzschmar HA, Mackenzie IR. A new subtype of frontotemporal lobar degeneration with FUS pathology. Brain 2009; 132: 2922-2931
14. Boxer AL, Mackenzie IR, Boeve BF, Baker M, Seeley WW, Crook R, Feldman H, Hsiung G-Y, Rutherford N, Laluz V, Whitwell J, Fote D, McDade E, Molano J, Karydas A, Wojtas A, Goldman J, Mirsky J, Sengdy P, DeArmond S, Miller BL, Rademakers R. Clinical, neuroimaging and neuropathological features of a new chromosome 9p-linked FTD-ALS family. J Neurol Neurosurg Psychiatry 2011; 82: 196-203
15. Al-Sarraj S, King A, Troakes C, Smith B, Maekawa S, Bodi I, Rogelj B, Al-Chalabi A, Hortobagyi T, Shaw CE. p62 positive, TDP-43 negative, neuronal cytoplasmic and intranuclear inclusions in the cerebellum and hippocampus define the pathology of C9orf72-linked FTLD and MNA/ALS. Acta Neuropathol (Berl) 2011; 122: 691-702
16. King A, Maekawa S, Bodi I, Troakes C, Al-Sarraj S. Ubiquitinated, p62 immunopositive cerebellar cortical neuronal inclusions are evident across the spectrum of TDP-43 proteinopathies but are only rarely additionally immunopositive for phosphorylation-dependent TDP-43. Neuropathology 2011; 31: 239-249
17. Pickering-Brown SM, Baker M, Yen S-H, Liu W-K, Hasegawa M, Cairns NJ, Lantos PL, Rossor M, Iwatsubo T, Davies Y, Allsop D, Furlong R, Owen F, Hardy J, Mann DMA, Hutton M. Pick's disease is associated with mutations in the tau gene. Ann Neurol 2000; 48: 859-867
18. Pickering-Brown SM, Richardson AMT, Snowden JS, McDonagh AM, Burns A, Braude W, Baker M, Liu W-K, Yen S-H, Hardy J, Hutton M, Davies Y, Allsop D, Craufurd D, Neary D, Mann DMA. Inherited frontotemporal dementia in 9 British families associated with intronic mutations in the tau gene. Brain 2002; 125: 732-751
19. Hodges JRD, Rhys R, Xuereb J, Casey H, Barney H, Broe M, Bak TH, Kril JJ, Halliday GM. Clinicopathological correlates in frontotemporal dementia. Ann Neurol 2004; 56: 399-406
20. Nordberg A, Carter SF, Rinne J, Drzezga A, Brooks DJ, Vandenberghe R, Perani D, Forsberg A, Langstrom B, Scheinin N, Karrasch M, Nagren K, Grimmer T, Miederer I, Edison P, Okello A, Van Laere K, Nelissen N, Vandenbulcke M, Garibotto V, Almkvist O, Kalbe E, Hinz R, Herholz K. A European multicentre PET study of fibrillar amyloid in Alzheimer's disease. Eur J Nucl Med Mol Imaging 2013; 40: 104-114
21. Kepe V, Bordelon Y, Boxer A, Huang SC, Liu J, Thiede FC, Mazziotta JC, Mendez MF, Donoghue N, Small GW, Barrio JR. PET imaging of neuropathology in tauopathies: progressive supranuclear palsy. J Alzheimers Dis 2013; 36: 145-153
22. Gerhard A, Pavese N, Hotton G, Turkheimer F, Es M, Hammers A, Eggert K, Oertel W, Banati RB, Brooks DJ. In vivo imaging of microglial activation with [(11)C](R)-PK11195 PET in idiopathic Parkinson's disease. Neurobiol Dis 2006; 21: 404-412
23. Edison P, Archer HA, Gerhard A, Hinz R, Pavese N, Turkheimer FE, Hammers A, Tai YF, Fox N, Kennedy A, Rossor M, Brooks DJ. Microglia, amyloid, and cognition in Alzheimer's disease: an [11C](R)PK11195-PET and [11C]PIB-PET study. Neurobiol Dis 2008; 32: 412-419
24. Gerhard A, Trender-Gerhard J, Turkheimer I, Banati F, Quinn NP, Bhatia KP, Brooks DJ. In vivo imaging of microglial activation with [11C](R)-PK11195 PET in progressive supranuclear palsy. Mov Disord 2006; 21: 89-93
25. Gerhard AW, Trender-Gerhard J, Turkheimer I, Banati F, Bhatia KP, Brooks DJ. In vivo imaging of microglial activation with [11C](R)-PK11195 PET in corticobasal degeneration. Mov Disord 2004; 19: 1221-1226
26. Cagnin A, Rossor M, Sampson EL, Mackinnon T, Banati RB. In vivo detection of microglial activation in frontotemporal dementia. Ann Neurol 2004; 56: 894-897
27. Brun A, Englund E, Gustafson L, Passant U, Mann DMA, Neary D, Snowden JS. Clinical, neuropsychological and neuropathological criteria of fronto-temporal dementia. J Neurol Neurosurg Psychiatry 1994; 57: 416-418
28. Neary D, Snowden JS, Gustafson L, Passant U, Stuss D, Black S, Freedman M, Kertesz A, Robert PH, Albert M, Boone K, Miller BL, Cummings J, Benson DF. Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology 1988; 51: 1546-1554
29. Rascovsky K, Hodges JR, Knopman D, Mendez MF, Kramer JH, Neuhaus J, van Swieten JC, Seelaar H, Dopper EG, Onyike CU, Hillis AE, Josephs KA, Boeve BF, Kertesz A, Seeley WW, Rankin KP, Johnson JK, Gorno-Tempini ML, Rosen H, Prioleau-Latham CE, Lee A, Kipps CM, Lillo P, Piguet O, Rohrer JD, Rossor MN, Warren JD, Fox NC, Galasko D, Salmon DP, Black SE, Mesulam M, Weintraub S, Dickerson BC, Diehl-Schmid J, Pasquier F, Deramecourt V, Lebert F, Pijnenburg Y, Chow TW, Manes F, Grafman J, Cappa SF, Freedman M, Grossman M, Miller BL. Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain 2011; 134: 2456-2477
30. Harris JM, Gall C, Thompson JC, Richardson AMT, Neary D, du Plessis D, Pal P, Mann DMA, Snowden JS, Jones M. Sensitivity and specificity of FTDC criteria for behavioral variant Frontotemporal dementia. Neurology 2013; 80: 1881-1887
31. Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brownlee LM. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 1991; 41: 479-486
32. Hyman BT, Phelps CH, Beach TG, Bigio EH, Cairns NJ, Carrillo MC, Dickson DW, Duyckaerts C, Frosch MP, Masliah E, Mirra SS, Nelson PT, Schneider JA, Thal DR, Thies B, Trojanowski JQ, Vinters HV, Montine TJ National institute on aging - Alzsheimer's association guidelines for the neuropathologic assessment of Alzheimer's disease. Alzheimers's and Dementia 2012; 8: 1-13
33. Mann DMA, Younis N, Jones D, Stoddart RW. The time course of pathological events concerned with plaque formation in Down's syndrome with particular reference to the involvement of microglial cells. Neurodegeneration 1992; 1: 201-215
34. Cooper PN, Siddons CA, Mann DMA. Patterns of glial cell activity in fronto-temporal dementia (lobar atrophy). Neuropathol Appl Neurobiol 1996; 22: 17-22
35. Schofield E, Kersaitis C, Shepherd CE, Krill JJ, Halliday GM. Severity of gliosis in Pick's disease and frontotemporal lobar degeneration: tau-positive glia differentiate these disorders. Brain 2003; 126: 827-840
36. Cagnin A, Kassiou M, Meikle SR, Banati RB. In vivo evidence for microglial activation in neurodegenerative dementia. Acta Neurol Scand Suppl 2006; 185: 107-114
37. Bhaskar K, Konerth M, Kokiko-Cochran ON, Cardona A, Ransohoff RM, Lamb BT. Regulation of tau pathology by the microglial fractalkine receptor. Neuron 2010; 68: 19-31
38. Philips T, De Muynck L, Thu HN, Weynants B, Vanacker P, Dhondt J, Sleegers K, Schelhaas HJ, Verbeek M, Vandenberghe R, Sciot R, Van Broeckhoven C, Lambrechts D, Van Leuven F, Van Den Bosch L, Robberecht W, Van Damme P. Microglial upregulation of progranulin as a marker of motor neuron degeneration. J Neuropathol Exp Neurol 2010; 69: 1191-1200
39. Ahmed ZM, Hutton M, Dickson D. Progranulin in frontotemporal lobar degeneration and neuroinflammation. J Neuroinflammation 2007; 4: 7
40. Filiano AJ, Martens LH, Young AH, Warmus BA, Zhou P, Diaz-Ramirez G, Jiao J, Zhang Z, Huang EJ, Gao F-B, Farese RV, Roberson ED. Dissociation of Frontotemporal dementia-related deficits and neuroinflammation in progranulin haploinsufficient mice. J Neurosci 2013; 33: 5352-5361