Motor neuron disease clinically limited to the lower motor neuron is a diffuse TDP-43 proteinopathy

Acta Neuropathologica

Volumn 121, Issue 4, 2011, Pages 509-517

  Geser, Felix ^a,b   Stein, Beth ^c   Partain, Michael ^a   Elman, Lauren B ^a   McCluskey, Leo F ^a   Xie, Sharon X ^a   Van Deerlin, Vivianna M ^a   Kwong, Linda K ^a   Lee, Virginia M Y ^a   Trojanowski, John Q ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b GOETHE UNIVERSITY   (Germany)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Motor neuron disease clinically limited to the lower motor neuron; Pathological 43 kDa transactive responsive sequence DNA binding protein; Progressive muscular atrophy

Indexed keywords

TAR DNA BINDING PROTEIN;

ADULT; AGED; ARTICLE; AUTOPSY; BRAIN REGION; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE CLASSIFICATION; DISEASE DURATION; FEMALE; GLIA CELL; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LIMBIC CORTEX; LONGITUDINAL STUDY; MALE; MEDICAL RECORD REVIEW; MOTOR CORTEX; MOTOR NEURON DISEASE; NEOCORTEX; NERVE CELL; NERVE DEGENERATION; PRIORITY JOURNAL; PROGRESSIVE MUSCULAR ATROPHY; RETROSPECTIVE STUDY;

AGED; AGED, 80 AND OVER; BRAIN; CELL COUNT; DNA-BINDING PROTEINS; FEMALE; HUMANS; MALE; MIDDLE AGED; MOTOR NEURON DISEASE; MOTOR NEURONS; STATISTICS, NONPARAMETRIC;

EID: 79954616367     PISSN: 00016322     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00401-011-0797-z     Document Type: Article

References (35)

1. H Braak E Braak 1991 Neuropathological stageing of Alzheimer-related changes Acta Neuropathol 82 239 259 1759558 10.1007/BF00308809 1:STN:280:DyaK387gtFOiug%3D%3D
2. H Braak K Del Tredici H Bratzke J Hamm-Clement D Sandmann-Keil U Rub 2002 Staging of the intracerebral inclusion body pathology associated with idiopathic Parkinson's disease (preclinical and clinical stages) J Neurol 249 Suppl 3:III 1 5 10.1007/s00415-002-1301-4
3. H Braak A Ludolph DR Thal K Del Tredici 2010 Amyotrophic lateral sclerosis: dash-like accumulation of phosphorylated TDP-43 in somatodendritic and axonal compartments of somatomotor neurons of the lower brainstem and spinal cord Acta Neuropathol 120 67 74 20379728 10.1007/s00401-010-0683-0 1:CAS:528:DC%2BC3cXns1ymurY%3D
4. NJ Brandmeir F Geser LK Kwong E Zimmerman J Qian VM Lee JQ Trojanowski 2008 Severe subcortical TDP-43 pathology in sporadic frontotemporal lobar degeneration with motor neuron disease Acta Neuropathol 115 123 131 18004574 10.1007/s00401-007-0315-5 (Pubitemid 50003187)
5. BR Brooks 1994 El Escorial World Federation of Neurology criteria for the diagnosis of amyotrophic lateral sclerosis. Subcommittee on motor neuron diseases/amyotrophic lateral sclerosis of the World Federation of Neurology Research Group on neuromuscular diseases and the El Escorial "Clinical limits of amyotrophic lateral sclerosis" workshop contributors J Neurol Sci 124 Suppl 96 107 7807156 10.1016/0022-510X(94)90191-0
6. BR Brooks RG Miller M Swash TL Munsat 2000 El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis Amyotroph Lateral Scler Other Motor Neuron Disord 1 293 299 11464847 10.1080/146608200300079536 1:STN:280:DC%2BD3Mvhs1Ghsg%3D%3D
7. LK Clinton M Blurton-Jones K Myczek JQ Trojanowski FM LaFerla 2010 Synergistic Interactions between Abeta, tau, and alpha-synuclein: acceleration of neuropathology and cognitive decline J Neurosci 30 7281 7289 20505094 10.1523/JNEUROSCI.0490-10.2010 1:CAS:528:DC%2BC3cXovVOisLw%3D
8. DW Dickson KA Josephs C Amador-Ortiz 2007 TDP-43 in differential diagnosis of motor neuron disorders Acta Neuropathol 114 71 79 17569066 10.1007/s00401-007-0234-5 1:CAS:528:DC%2BD2sXmvFals7g%3D (Pubitemid 47029062)
9. MS Forman J Farmer JK Johnson CM Clark SE Arnold HB Coslett A Chatterjee HI Hurtig JH Karlawish HJ Rosen V Van Deerlin VM Lee BL Miller JQ Trojanowski M Grossman 2006 Frontotemporal dementia: clinicopathological correlations Ann Neurol 59 952 962 16718704 10.1002/ana.20873 (Pubitemid 43830927)
10. F Geser NJ Brandmeir LK Kwong M Martinez-Lage L Elman L McCluskey SX Xie VM Lee JQ Trojanowski 2008 Evidence of multisystem disorder in whole-brain map of pathological TDP-43 in amyotrophic lateral sclerosis Arch Neurol 65 636 641 18474740 10.1001/archneur.65.5.636 (Pubitemid 351679659)
11. F Geser M Martinez-Lage J Robinson K Uryu M Neumann NJ Brandmeir SX Xie LK Kwong L Elman L McCluskey CM Clark J Malunda BL Miller EA Zimmerman J Qian V Van Deerlin M Grossman VM Lee JQ Trojanowski 2009 Clinical and pathological continuum of multisystem TDP-43 proteinopathies Arch Neurol 66 180 189 19204154 10.1001/archneurol.2008.558
12. F Geser JL Robinson JA Malunda SX Xie CM Clark LK Kwong PJ Moberg EM Moore VM Van Deerlin VM Lee SE Arnold JQ Trojanowski 2010 Pathological 43-kDa transactivation response DNA-binding protein in older adults with and without severe mental illness Arch Neurol 67 1238 1250 20937952 10.1001/archneurol.2010. 254
13. PH Gordon B Cheng IB Katz M Pinto AP Hays H Mitsumoto LP Rowland 2006 The natural history of primary lateral sclerosis Neurology 66 647 653 16534101 10.1212/01.wnl.0000200962.94777.71 1:STN:280:DC%2BD287ks1SrtA%3D%3D (Pubitemid 43739816)
14. M Grossman EM Wood P Moore M Neumann L Kwong MS Forman CM Clark LF McCluskey BL Miller VM Lee JQ Trojanowski 2007 TDP-43 pathologic lesions and clinical phenotype in frontotemporal lobar degeneration with ubiquitin-positive inclusions Arch Neurol 64 1449 1454 17923628 10.1001/archneur.64.10.1449 (Pubitemid 47572668)
15. JR Hodges R Davies J Xuereb J Kril G Halliday 2003 Survival in frontotemporal dementia Neurology 61 349 354 12913196 1:STN:280: DC%2BD3sznslOrsQ%3D%3D (Pubitemid 36975964)
16. WT Hu KA Josephs DS Knopman BF Boeve DW Dickson RC Petersen JE Parisi 2008 Temporal lobar predominance of TDP-43 neuronal cytoplasmic inclusions in Alzheimer disease Acta Neuropathol 116 215 220 18592255 10.1007/s00401-008-0400- 4 1:CAS:528:DC%2BD1cXosVyisLk%3D
17. WT Hu H Seelaar KA Josephs DS Knopman BF Boeve EJ Sorenson L McCluskey L Elman HJ Schelhaas JE Parisi B Kuesters VM Lee JQ Trojanowski RC Petersen JC van Swieten M Grossman 2009 Survival profiles of patients with frontotemporal dementia and motor neuron disease Arch Neurol 66 1359 1364 19901167 10.1001/archneurol.2009.253
18. PG Ince J Evans M Knopp G Forster HH Hamdalla SB Wharton PJ Shaw 2003 Corticospinal tract degeneration in the progressive muscular atrophy variant of ALS Neurology 60 1252 1258 12707426 1:STN:280:DC%2BD3s7ovVKitQ%3D%3D (Pubitemid 36460979)
19. KA Josephs DW Dickson 2007 Frontotemporal lobar degeneration with upper motor neuron disease/primary lateral sclerosis Neurology 69 1800 1801 17967995 10.1212/01.wnl.0000277270.99272.7e (Pubitemid 350059309)
20. KA Josephs DS Knopman JL Whitwell BF Boeve JE Parisi RC Petersen DW Dickson 2005 Survival in two variants of tau-negative frontotemporal lobar degeneration: FTLD-U vs. FTLD-MND Neurology 65 645 647 16116138 10.1212/01.wnl.0000173178.67986.7f 1:STN:280:DC%2BD2MvkvFCmsw%3D%3D (Pubitemid 41170737)
21. WK Kim X Liu J Sandner M Pasmantier J Andrews LP Rowland H Mitsumoto 2009 Study of 962 patients indicates progressive muscular atrophy is a form of ALS Neurology 73 1686 1692 19917992 10.1212/WNL.0b013e3181c1dea3 1:CAS:528:DC%2BD1MXhtlyrtLzN
22. IR Mackenzie A Baborie S Pickering-Brown D Du Plessis E Jaros RH Perry D Neary JS Snowden DM Mann 2006 Heterogeneity of ubiquitin pathology in frontotemporal lobar degeneration: classification and relation to clinical phenotype Acta Neuropathol 112 539 549 17021754 10.1007/s00401-006-0138-9 (Pubitemid 44550678)
23. LF McCluskey LB Elman M Martinez-Lage V Van Deerlin W Yuan D Clay A Siderowf JQ Trojanowski 2009 Amyotrophic lateral sclerosis-plus syndrome with TAR DNA-binding protein-43 pathology Arch Neurol 66 121 124 19139310 10.1001/archneur.66.1.121
24. IG McKeith DW Dickson J Lowe M Emre JT O'Brien H Feldman J Cummings JE Duda C Lippa EK Perry D Aarsland H Arai CG Ballard B Boeve DJ Burn D Costa T Del Ser B Dubois D Galasko S Gauthier CG Goetz E Gomez-Tortosa G Halliday LA Hansen J Hardy T Iwatsubo RN Kalaria D Kaufer RA Kenny A Korczyn K Kosaka VM Lee A Lees I Litvan E Londos OL Lopez S Minoshima Y Mizuno JA Molina EB Mukaetova-Ladinska F Pasquier RH Perry JB Schulz JQ Trojanowski M Yamada 2005 Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium Neurology 65 1863 1872 16237129 10.1212/01.wnl.0000187889.17253.b1 1:STN:280:DC%2BD2Mnpt1GqsQ%3D%3D (Pubitemid 43970103)
25. F Mori K Tanji HX Zhang Y Nishihira CF Tan H Takahashi K Wakabayashi 2008 Maturation process of TDP-43-positive neuronal cytoplasmic inclusions in amyotrophic lateral sclerosis with and without dementia Acta Neuropathol 116 193 203 18560845 10.1007/s00401-008-0396-9 1:CAS:528:DC%2BD1cXosVyisb4%3D
26. M Neumann LK Kwong EB Lee E Kremmer A Flatley Y Xu MS Forman D Troost HA Kretzschmar JQ Trojanowski VM Lee 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 19125255 10.1007/s00401-008-0477-9 1:CAS:528:DC%2BD1MXhtVCltLw%3D
27. M Neumann DM Sampathu LK Kwong AC Truax MC Micsenyi TT Chou J Bruce T Schuck M Grossman CM Clark LF McCluskey BL Miller E Masliah IR Mackenzie H Feldman W Feiden HA Kretzschmar JQ Trojanowski VM Lee 2006 Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis Science 314 130 133 17023659 10.1126/science.1134108 1:CAS:528:DC%2BD28XhtVCiurrL (Pubitemid 44547757)
28. Y Nishihira CF Tan Y Hoshi K Iwanaga M Yamada I Kawachi M Tsujihata I Hozumi T Morita O Onodera M Nishizawa A Kakita H Takahashi 2009 Sporadic amyotrophic lateral sclerosis of long duration is associated with relatively mild TDP-43 pathology Acta Neuropathol 117 45 53 18923836 10.1007/s00401-008- 0443-6 1:CAS:528:DC%2BD1cXhsVeksrfJ
29. DM Sampathu M Neumann LK Kwong TT Chou M Micsenyi A Truax J Bruce M Grossman JQ Trojanowski VM Lee 2006 Pathological heterogeneity of frontotemporal lobar degeneration with ubiquitin-positive inclusions delineated by ubiquitin immunohistochemistry and novel monoclonal antibodies Am J Pathol 169 1343 1352 17003490 10.2353/ajpath.2006.060438 1:CAS:528:DC%2BD28XhtFeitLbJ (Pubitemid 351194368)
30. Tan C-F, Yamada M, Toyoshima Y, Yokoseki A, Miki Y, Hoshi Y, Kaneko H, Ikeuchi T, Onodera O, Kakita A, Takahashi H (2009) Selective occurrence of TDP-43-immunoreactive inclusions in the lower motor neurons in Machado-Joseph disease. Acta Neuropathol 118:553-560
31. K Tsuchiya M Sano H Shiotsu H Akiyama S Watabiki K Taki H Kondo I Nakano K Ikeda 2004 Sporadic amyotrophic lateral sclerosis of long duration mimicking spinal progressive muscular atrophy exists: additional autopsy case with a clinical course of 19 years Neuropathology 24 228 235 15484701 10.1111/j.1440-1789.2004.00546.x (Pubitemid 39279683)
32. K Uryu H Nakashima-Yasuda MS Forman LK Kwong CM Clark M Grossman BL Miller HA Kretzschmar VM Lee JQ Trojanowski M Neumann 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 18520774 10.1097/NEN.0b013e31817713b5 1:CAS:528:DC%2BD1cXotVant7g%3D (Pubitemid 351787082)
33. RM Van den Berg-Vos J Visser S Kalmijn K Fischer M de Visser V de Jong RJ de Haan H Franssen JH Wokke LH Van den Berg 2009 A long-term prospective study of the natural course of sporadic adult-onset lower motor neuron syndromes Arch Neurol 66 751 757 19506135 10.1001/archneurol.2009.91
34. O Yokota Y Davidson T Arai M Hasegawa H Akiyama H Ishizu S Terada S Sikkink S Pickering-Brown DM Mann 2010 Effect of topographical distribution of alpha-synuclein pathology on TDP-43 accumulation in Lewy body disease Acta Neuropathol 120 789 801 20669025 10.1007/s00401-010-0731-9 1:CAS:528: DC%2BC3cXhsVymsLrN
35. O Yokota Y Davidson EH Bigio H Ishizu S Terada T Arai M Hasegawa H Akiyama S Sikkink S Pickering-Brown DM Mann 2010 Phosphorylated TDP-43 pathology and hippocampal sclerosis in progressive supranuclear palsy Acta Neuropathol 120 55 66 20512649 10.1007/s00401-010-0702-1