Microglial activation and TDP-43 pathology correlate with executive dysfunction in amyotrophic lateral sclerosis (original) (raw)

References

  1. Abrahams S, Goldstein LH, Suckling J, Ng V, Simmons A, Chitnis X, Atkins L, Williams SC, Leigh PN (2005) Frontotemporal white matter changes in amyotrophic lateral sclerosis. J Neurol 252:321–331
    Article PubMed Google Scholar
  2. Alexianu ME, Kozovska M, Appel SH (2001) Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology 57:1282–1289
    PubMed CAS Google Scholar
  3. Arai T, Hasegawa M, Nonoka T, Kametani F, Yamashita M, Hosokawa M, Niizato K, Tsuchiya K, Kobayashi Z, Ikeda K, Yoshida M, Onaya M, Fujishiro H, Akiyama H (2010) Phosphorylated and cleaved TDP-43 in ALS, FTLD and other neurodegenerative disorders and in cellular models of TDP-43 proteinopathy. Neuropathology 30:170–181
    Article PubMed Google Scholar
  4. Avants B, Khan A, McCluskey L, Elman L, Grossman M (2009) Longitudinal cortical atrophy in amyotrophic lateral sclerosis with frontotemporal dementia. Arch Neurol 66:138–139
    Article PubMed Google Scholar
  5. Ayala YM, Misteli T, Baralle FE (2008) TDP-43 regulates retinoblastoma protein phosphorylation through the repression of cyclin-dependent kinase 6 expression. Proc Natl Acad Sci USA 105:3785–3789
    Article PubMed CAS Google Scholar
  6. Bellucci A, Bugiani O, Ghetti B, Spillantini MG (2011) Presence of reactive microglia and neuroinflammatory mediators in a case of frontotemporal dementia with P301S mutation. Neurodegener Dis 8:221–229
    Article PubMed Google Scholar
  7. Braak H, Alafuzoff I, Arzberger T, Kretzschmar H, Del Tredici K (2006) Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol 112:389–404
    Article PubMed Google Scholar
  8. Braak H, Braak E (1991) Neuropathological staging of Alzheimer-related changes. Acta Neuropathol 82:239–259
    Article PubMed CAS Google Scholar
  9. Brooks BR, Miller RG, Swash M, Munsat TL (2000) El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 1:293–299
    Article PubMed CAS Google Scholar
  10. Canning SJ, Leach L, Stuss D, Ngo L, Black SE (2004) Diagnostic utility of abbreviated fluency measures in Alzheimer disease and vascular dementia. Neurology 62:556–562
    PubMed Google Scholar
  11. Cedarbaum JM, Stambler N, Malta E, Fuller C, Hilt D, Thurmond B, Nakanishi A (1999) The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J Neurol Sci 169:13–21
    Article PubMed CAS Google Scholar
  12. Consensus recommendations for the postmortem diagnosis of Alzheimer’s disease. The National Institute on Aging, and Reagan Institute Working Group on Diagnostic Criteria for the Neuropathological Assessment of Alzheimer’s Disease (1997). Neurobiol Aging 18:S1–2
    Google Scholar
  13. Crum RM, Anthony JC, Bassett SS, Folstein MF (1993) Population-based norms for the Mini-Mental State Examination by age and educational level. JAMA 269:2386–2391
    Article PubMed CAS Google Scholar
  14. Davidson Y, Kelley T, Mackenzie IR, Pickering-Brown S, Du Plessis D, Neary D, Snowden JS, Mann DM (2007) Ubiquitinated pathological lesions in frontotemporal lobar degeneration contain the TAR DNA-binding protein, TDP-43. Acta Neuropathol 113:521–533
    Article PubMed CAS Google Scholar
  15. Drachman DB, Frank K, Dykes-Hoberg M, Teismann P, Almer G, Przedborski S, Rothstein JD (2002) Cyclooxygenase 2 inhibition protects motor neurons and prolongs survival in a transgenic mouse model of ALS. Ann Neurol 52:771–778
    Article PubMed CAS Google Scholar
  16. Engelhardt JI, Tajti J, Appel SH (1993) Lymphocytic infiltrates in the spinal cord in amyotrophic lateral sclerosis. Arch Neurol 50:30–36
    Article PubMed CAS Google Scholar
  17. Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198
    Article PubMed CAS Google Scholar
  18. Garraux G, Salmon E, Degueldre C, Lemaire C, Franck G (1999) Medial temporal lobe metabolic impairment in dementia associated with motor neuron disease. J Neurol Sci 168:145–150
    Article PubMed CAS Google Scholar
  19. Geser F, Lee VM, Trojanowski JQ (2010) Amyotrophic lateral sclerosis and frontotemporal lobar degeneration: a spectrum of TDP-43 proteinopathies. Neuropathology 30:103–112
    Article PubMed Google Scholar
  20. Geser F, Martinez-Lage M, Robinson J, Uryu K, Neumann M, Brandmeir NJ, Xie SX, Kwong LK, Elman L, McCluskey L, Clark CM, Malunda J, Miller BL, Zimmerman EA, Qian J, Van Deerlin V, Grossman M, Lee VM, Trojanowski JQ (2009) Clinical and pathological continuum of multisystem TDP-43 proteinopathies. Arch Neurol 66:180–189
    Article PubMed Google Scholar
  21. Geser F, Robinson JL, Malunda JA, Xie SX, Clark CM, Kwong LK, Moberg PJ, Moore EM, Van Deerlin VM, Lee VM, Arnold SE, Trojanowski JQ (2010) Pathological 43-kDa transactivation response DNA-binding protein in older adults with and without severe mental illness. Arch Neurol 67:1238–1250
    Article PubMed Google Scholar
  22. Gregory CA, Orrell M, Sahakian B, Hodges JR (1997) Can frontotemporal dementia and Alzheimer’s disease be differentiated using a brief battery of tests? Int J Geriatr Psychiatry 12:375–383
    Article PubMed CAS Google Scholar
  23. Hall ED, Oostveen JA, Gurney ME (1998) Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia 23:249–256
    Article PubMed CAS Google Scholar
  24. Hamilton RL, Bowser R (2004) Alzheimer disease pathology in amyotrophic lateral sclerosis. Acta Neuropathol 107:515–522
    Article PubMed Google Scholar
  25. Hu WT, Seelaar H, Josephs KA, Knopman DS, Boeve BF, Sorenson EJ, McCluskey L, Elman L, Schelhaas HJ, Parisi JE, Kuesters B, Lee VM, Trojanowski JQ, Petersen RC, van Swieten JC, Grossman M (2009) Survival profiles of patients with frontotemporal dementia and motor neuron disease. Arch Neurol 66:1359–1364
    Article PubMed Google Scholar
  26. Hudson AJ (1981) Amyotrophic lateral sclerosis and its association with dementia, parkinsonism and other neurological disorders: a review. Brain 104:217–247
    Article PubMed CAS Google Scholar
  27. Hyman BT, Trojanowski JQ (1997) Consensus recommendations for the postmortem diagnosis of Alzheimer disease from the National Institute on Aging and the Reagan Institute Working Group on diagnostic criteria for the neuropathological assessment of Alzheimer disease. J Neuropathol Exp Neurol 56:1095–1097
    Article PubMed CAS Google Scholar
  28. Igaz LM, Kwong LK, Chen-Plotkin A, Winton MJ, Unger TL, Xu Y, Neumann M, Trojanowski JQ, Lee VM (2009) Expression of TDP-43 C-terminal fragments in vitro recapitulates pathological features of TDP-43 proteinopathies. J Biol Chem 284:8516–8524
    Article PubMed CAS Google Scholar
  29. Iguchi Y, Katsuno M, Niwa J, Yamada S, Sone J, Waza M, Adachi H, Tanaka F, Nagata K, Arimura N, Watanabe T, Kaibuchi K, Sobue G (2009) TDP-43 depletion induces neuronal cell damage through dysregulation of Rho family GTPases. J Biol Chem 284:22059–22066
    Article PubMed CAS Google Scholar
  30. Imai Y, Kohsaka S (2002) Intracellular signaling in M-CSF-induced microglia activation: role of Iba1. Glia 40:164–174
    Article PubMed Google Scholar
  31. Ince PG, Highley JR, Kirby J, Wharton SB, Takahashi H, Strong MJ, Shaw PJ (2011) Molecular pathology and genetic advances in amyotrophic lateral sclerosis: an emerging molecular pathway and the significance of glial pathology. Acta Neuropathol 122:657–671
    Article PubMed CAS Google Scholar
  32. Kertesz A, Davidson W, Fox H (1997) Frontal behavioral inventory: diagnostic criteria for frontal lobe dementia. Can J Neurol Sci 24:29–36
    PubMed CAS Google Scholar
  33. Kiernan MC, Vucic S, Cheah BC, Turner MR, Eisen A, Hardiman O, Burrell JR, Zoing MC (2011) Amyotrophic lateral sclerosis. Lancet 377:942–955
    Article PubMed CAS Google Scholar
  34. Kim SH, Shi Y, Hanson KA, Williams LM, Sakasai R, Bowler MJ, Tibbetts RS (2009) Potentiation of amyotrophic lateral sclerosis (ALS)-associated TDP-43 aggregation by the proteasome-targeting factor, ubiquilin 1. J Biol Chem 284:8083–8092
    Article PubMed CAS Google Scholar
  35. Kriz J, Nguyen MD, Julien JP (2002) Minocycline slows disease progression in a mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 10:268–278
    Article PubMed CAS Google Scholar
  36. Lezak M (1983) Neuropsychological assessment. Oxford University Press, New York
    Google Scholar
  37. Libon DJ, Massimo L, Moore P, Coslett HB, Chatterjee A, Aguirre GK, Rice A, Vesely L, Grossman M (2007) Screening for frontotemporal dementias and Alzheimer’s disease with the Philadelphia Brief Assessment of Cognition: a preliminary analysis. Dement Geriatr Cogn Disord 24:441–447
    Article PubMed Google Scholar
  38. Lomen-Hoerth C, Murphy J, Langmore S, Kramer JH, Olney RK, Miller B (2003) Are amyotrophic lateral sclerosis patients cognitively normal? Neurology 60:1094–1097
    PubMed CAS Google Scholar
  39. Mackenzie IR, Bigio EH, Ince PG, Geser F, Neumann M, Cairns NJ, Kwong LK, Forman MS, Ravits J, Stewart H, Eisen A, McClusky L, Kretzschmar HA, Monoranu CM, Highley JR, Kirby J, Siddique T, Shaw PJ, Lee VM, Trojanowski JQ (2007) Pathological TDP-43 distinguishes sporadic amyotrophic lateral sclerosis from amyotrophic lateral sclerosis with SOD1 mutations. Ann Neurol 61:427–434
    Article PubMed CAS Google Scholar
  40. McGeer PL, McGeer EG (2002) Inflammatory processes in amyotrophic lateral sclerosis. Muscle Nerve 26:459–470
    Article PubMed CAS Google Scholar
  41. Miller BL, Cummings JL, Villanueva-Meyer J, Boone K, Mehringer CM, Lesser IM, Mena I (1991) Frontal lobe degeneration: clinical, neuropsychological, and SPECT characteristics. Neurology 41:1374–1382
    PubMed CAS Google Scholar
  42. Miller JW, Urbinati CR, Teng-Umnuay P, Stenberg MG, Byrne BJ, Thornton CA, Swanson MS (2000) Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. EMBO J 19:4439–4448
    Article PubMed CAS Google Scholar
  43. Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brownlee LM, Vogel FS, Hughes JP, van Belle G, Berg L (1991) The consortium to establish a registry for Alzheimer’s Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer’s disease. Neurology 41:479–486
    PubMed CAS Google Scholar
  44. Morita K, Kaiya H, Ikeda T, Namba M (1987) Presenile dementia combined with amyotrophy: a review of 34 Japanese cases. Arch Gerontol Geriatr 6:263–277
    Article PubMed CAS Google Scholar
  45. 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 (1998) Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology 51:1546–1554
    Google Scholar
  46. Neumann M, Kwong LK, Lee EB, Kremmer E, Flatley A, Xu Y, Forman MS, Troost D, Kretzschmar HA, Trojanowski JQ, Lee VM (2009) Phosphorylation of S409/410 of TDP-43 is a consistent feature in all sporadic and familial forms of TDP-43 proteinopathies. Acta Neuropathol 117:137–149
    Article PubMed CAS Google Scholar
  47. 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 HA, Trojanowski JQ, Lee VM (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314:130–133
    Article PubMed CAS Google Scholar
  48. Nishimura AL, Zupunski V, Troakes C, Kathe C, Fratta P, Howell M, Gallo JM, Hortobagyi T, Shaw CE, Rogelj B (2010) Nuclear import impairment causes cytoplasmic trans-activation response DNA-binding protein accumulation and is associated with frontotemporal lobar degeneration. Brain 133:1763–1771
    Article PubMed Google Scholar
  49. Nonaka T, Kametani F, Arai T, Akiyama H, Hasegawa M (2009) Truncation and pathogenic mutations facilitate the formation of intracellular aggregates of TDP-43. Hum Mol Genet 18:3353–3364
    Article PubMed CAS Google Scholar
  50. Ohsawa K, Imai Y, Kanazawa H, Sasaki Y, Kohsaka S (2000) Involvement of Iba1 in membrane ruffling and phagocytosis of macrophages/microglia. J Cell Sci 113:3073–3084
    PubMed CAS Google Scholar
  51. Olney RK, Murphy J, Forshew D, Garwood E, Miller BL, Langmore S, Kohn MA, Lomen-Hoerth C (2005) The effects of executive and behavioral dysfunction on the course of ALS. Neurology 65:1774–1777
    Article PubMed CAS Google Scholar
  52. Phukan J, Pender NP, Hardiman O (2007) Cognitive impairment in amyotrophic lateral sclerosis. Lancet Neurol 6:994–1003
    Article PubMed CAS Google Scholar
  53. Strong MJ, Grace GM, Orange JB, Leeper HA, Menon RS, Aere C (1999) A prospective study of cognitive impairment in ALS. Neurology 53:1665–1670
    PubMed CAS Google Scholar
  54. Takeda T, Uchihara T, Arai N, Mizutani T, Iwata M (2009) Progression of hippocampal degeneration in amyotrophic lateral sclerosis with or without memory impairment: distinction from Alzheimer disease. Acta Neuropathol 117:35–44
    Article PubMed CAS Google Scholar
  55. Thal DR, Rub U, Orantes M, Braak H (2002) Phases of A beta-deposition in the human brain and its relevance for the development of AD. Neurology 58:1791–1800
    PubMed Google Scholar
  56. Thal DR, Rub U, Schultz C, Sassin I, Ghebremedhin E, Del Tredici K, Braak E, Braak H (2000) Sequence of Abeta-protein deposition in the human medial temporal lobe. J Neuropathol Exp Neurol 59:733–748
    PubMed CAS Google Scholar
  57. Turner MR, Cagnin A, Turkheimer FE, Miller CC, Shaw CE, Brooks DJ, Leigh PN, Banati RB (2004) Evidence of widespread cerebral microglial activation in amyotrophic lateral sclerosis: an [11C](R)-PK11195 positron emission tomography study. Neurobiol Dis 15:601–609
    Article PubMed CAS Google Scholar
  58. Uryu K, Nakashima-Yasuda H, Forman MS, Kwong LK, Clark CM, Grossman M, Miller BL, Kretzschmar HA, Lee VM, Trojanowski JQ, Neumann M (2008) Concomitant TAR-DNA-binding protein 43 pathology is present in Alzheimer disease and corticobasal degeneration but not in other tauopathies. J Neuropathol Exp Neurol 67:555–564
    Article PubMed CAS Google Scholar
  59. Vass R, Ashbridge E, Geser F, Hu WT, Grossman M, Clay-Falcone D, Elman L, McCluskey L, Lee VM, Van Deerlin VM, Trojanowski JQ, Chen-Plotkin AS (2011) Risk genotypes at TMEM106B are associated with cognitive impairment in amyotrophic lateral sclerosis. Acta Neuropathol 121:373–380
    Article PubMed Google Scholar
  60. Wikstrom J, Paetau A, Palo J, Sulkava R, Haltia M (1982) Classic amyotrophic lateral sclerosis with dementia. Arch Neurol 39:681–683
    Article PubMed CAS Google Scholar
  61. Wilson CM, Grace GM, Munoz DG, He BP, Strong MJ (2001) Cognitive impairment in sporadic ALS: a pathologic continuum underlying a multisystem disorder. Neurology 57:651–657
    PubMed CAS Google Scholar
  62. Yoshida M (2004) Amyotrophic lateral sclerosis with dementia: the clinicopathological spectrum. Neuropathology 24:87–102
    Article PubMed Google Scholar
  63. Yoshida M, Murakami N, Hashizume Y, Takahashi A (1992) A clinicopathological study on 13 cases of motor neuron disease with dementia. Rinsho Shinkeigaku 32:1193–1202
    PubMed CAS Google Scholar
  64. Zhu X, Hill RA, Nishiyama A (2008) NG2 cells generate oligodendrocytes and gray matter astrocytes in the spinal cord. Neuron Glia Biol 4:19–26
    Article PubMed Google Scholar

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