Laminar distribution of the pathological changes in sporadic frontotemporal lobar degeneration with transactive response (TAR) DNA-binding protein of 43kDa (TDP-43) proteinopathy: A quantitative study using polynomial curve fitting

Neuropathology and Applied Neurobiology

Volumn 39, Issue 4, 2013, Pages 335-347

  Armstrong, R A ^a   Hamilton, R L ^c   MacKenzie, I R A ^b   Hedreen, J ^d   Cairns, N J ^e  

^a ASTON UNIVERSITY   (United Kingdom)

^b VANCOUVER GENERAL HOSPITAL   (Canada)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d MCLEAN HOSPITAL   (United States)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Frontotemporal lobar degeneration with TDP 43 proteinopathy (FTLD TDP); FTLD with ubiquitin positive inclusions (FTLD U); Laminar distribution; Neuronal cytoplasmic inclusions (NCI); Transactive response (TAR) DNA binding protein of 43kDa (TDP 43)

Indexed keywords

TAR DNA BINDING PROTEIN;

ADULT; AGED; ARTICLE; CELL INCLUSION; CELL SURVIVAL; CELL VACUOLE; CLINICAL ARTICLE; CURVE FITTING; CYTOPLASM; DENSITY; FEMALE; FRONTAL LOBE; FRONTOTEMPORAL DEMENTIA; GLIA; HUMAN; HUMAN TISSUE; MALE; NEURITE; NEUROPATHOLOGY; NUCLEAR LAMINA; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN POLYMORPHISM; QUANTITATIVE STUDY; TDP 43 PROTEINOPATHY; TEMPORAL LOBE; TISSUE DISTRIBUTION;

AGED; AGED, 80 AND OVER; BRAIN; CELL SURVIVAL; DATA INTERPRETATION, STATISTICAL; DISEASE PROGRESSION; DNA-BINDING PROTEINS; FEMALE; FRONTAL LOBE; FRONTOTEMPORAL LOBAR DEGENERATION; HUMANS; INCLUSION BODIES; MALE; MIDDLE AGED; NEURONS; PARAHIPPOCAMPAL GYRUS; TDP-43 PROTEINOPATHIES; TEMPORAL LOBE;

EID: 84876849906     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/j.1365-2990.2012.01291.x     Document Type: Article

References (62)

1. Tolnay M, Probst A. Frontotemporal lobar degeneration-tau as a pied piper? Neurogenetics 2002; 4: 63-75.
2. Snowden J, Neary D, Mann D. Frontotemporal lobar degeneration: clinical and pathological relationships. Acta Neuropathol 2007; 114: 31-8.
3. Woulfe J, Kertesz A, Munoz DG. Frontotemporal dementia with ubiquinated cytoplasmic and intranuclear inclusions. Acta Neuropathol 2001; 102: 94-102.
4. Kovari E, Gold G, Giannakopoulos P, Bouras C. Cortical ubiquitin positive inclusions in frontotemporal dementia without motor neuron disease: a quantitative immunocytochemical study. Acta Neuropathol 2004; 108: 207-12.
5. Cairns NJ, Neumann M, Bigio EH, Holm IE, Troost D, Hatanpaa KJ, Foong C, White CL III, Schneider JA, Kretzschmar HA, Carter D, Taylor-Reinwald L, Paulsmeyer K, Strider J, Gitcho M, Goate AM, Morris JC, Mishra M, Kwong LK, Steiber A, Xu Y, Forman MS, Trojanowski JQ, Lee VMY, Mackenzie IRA. TDP-43 familial and sporadic frontotemporal lobar degeneration with ubiquitin inclusions. Am J Pathol 2007; 171: 227-40.
6. Armstrong RA, Ellis W, Hamilton RL, Mackenzie IRA, Hedreen J, Gearing M, Montine T, Vonsattel J-P, Head E, Lieberman AP, Cairns NJ. Neuropathological heterogeneity in frontotemporal lobar degeneration with TDP-43 proteinopathy: a quantitative study of 94 cases using principal components analysis. J Neural Transm 2010; 117: 227-39.
7. Mackenzie IR, Baborie A, Pickering-Brown S, Du Plessis D, Jaros E, Perry RH, Neary D, Snowden JS, Mann DMA. Heterogeneity of ubiquitin pathology in frontotemporal lobar degeneration: classification and relation to clinical phenotype. Acta Neuropathol 2006; 112: 539-49.
8. Sampathu DM, Neumann M, Kwong LK, Chou TT, Micsenyi M, Truax A, Bruce J, Grossman M, Trojanowski JQ, Lee VM. Pathological heterogeneity of frontotemporal lobar degeneration with ubiquitin-positive inclusions delineated by ubiquitin immunohistochemistry and novel monoclonal antibodies. Am J Pathol 2006; 169: 1343-52.
9. Neumann M, Igaz LM, Kwong LK, Nakashima-Yasuda H, Kolb SJ, Dreyfuss G, Kretzschmar HA, Trojanowski JQ, Lee VMY. Absence of heterogeneous nuclear riboproteins and survival neuron protein (TDP-43) positive inclusions in frontotemporal lobar degeneration. Acta Neuropathol 2007; 113: 543-8.
10. Cairns NJ, Bigio EH, Mackenzie IRA, Neumann M, Lee VMY, Hatanpaa KJ, White CL, Schneider JA, Grinberg LT, Halliday G, Duyckaerts C, Lowe JS, Holm IE, Tolnay M, Okamoto K, Yokoo H, Murayama S, Woulfe J, Munoz DG, Dickson DW, Ince PG, Trojanowski JQ, Mann DMA. Neuropathologic diagnostic and nosological criteria for frontotemporal lobar degeneration: consensus of the Consortium for Frontotemporal Lobar Degeneration. Acta Neuropathol 2007; 114: 5-22.
11. Armstrong RA. β-amyloid (Aβ) deposits and blood vessels: laminar distribution in the frontal cortex of patients with Alzheimer's disease. Neurosci Res Commun 1996; 18: 19-28.
12. Armstrong RA, Cairns NJ, Lantos PL. Laminar distribution of cortical Lewy bodies and neurofibrillary tangles in dementia with Lewy bodies. Neurosci Res Commun 1997; 21: 145-52.
13. Armstrong RA, Cairns NJ, Lantos PL. Laminar distribution of Pick bodies, Pick cells, and Alzheimer's disease pathology in the frontal and temporal cortex in Pick's disease. Neuropathol Appl Neurobiol 1999; 25: 266-71.
14. Armstrong RA, Lantos PL, Cairns NJ. Laminar distribution of ballooned neurons and tau positive neurons with inclusions in patients with corticobasal degeneration. Neurosci Res 2000; 27: 85-93.
15. Armstrong RA, Lantos PL, Cairns NJ. Multiple system atrophy: laminar distribution of the pathological changes in frontal and temporal neocortex. Clin Neuropathol 2005; 24: 230-5.
16. De Lacoste M, White CL. The role of cortical connectivity in Alzheimer's disease pathogenesis: a review and model system. Neurobiol Aging 1993; 14: 1-16.
17. Armstrong RA, Slaven A. Does the neurodegeneration of Alzheimer's disease spread between visual cortical regions B17 and B18 via the feedforward or feedback short cortico-cortical projections? Neurodegeneration 1994; 3: 191-6.
18. Armstrong RA, Hilton A. Statistical Analysis in Microbiology: Statnotes. Hoboken, NJ, USA: Wiley-Blackwell, 2011.
19. Baker M, Mackenzie IR, 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, Berger Z, 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: 916-19.
20. Cruts M, Gijselink I, van der Zee J, Engelborgs S, Wils H, Pirici D, Radamakers 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: 920-4.
21. Mukherjee O, Pastor P, Cairns NJ, Chakraaverty S, Kauwe JSK, Shears S, Behrens MI, Budde J, Hinrichs AL, Norton J, Levitch D, Taylor-Reinwald L, Gitcho M, Tu PH, Grinberg LT, Liscic RM, Armendariz J, Morris JC, Goate AM. HDDD2 is a familial frontotemporal lobar degeneration with ubiquitin-positive tau-negative inclusions caused by a missense mutation in the signal peptide of progranulin. Ann Neurol 2006; 60: 314-22.
22. Mackenzie IRA, Baker M, Pickering-Brown S, Hsinng GYR, Lindholm C, Dwosh E, Cannon A, Rademakers R, Hutton M, Feldman HH. The neuropathology of frontotemporal lobar degeneration caused by mutations in the progranulin gene. Brain 2006; 129: 3081-90.
23. Rademakers R, Hutton M. The genetics of frontotemporal lobar degeneration. Curr Neurol Neurosci Rep 2007; 7: 434-42.
24. Behrens MI, Mukherjee O, Tu PH, Liscic RM, Grinberg LT, Carter D, Paulsmeyer K, Taylor-Reinwald L, Gitcho M, Norton JB, Chakraverty S, Goate AM, Morris JC, Cairns NJ. Neuropathologic heterogeneity in HDDD1: a familial frontotemporal lobar degeneration with ubiquitin-positive inclusions and progranulin mutation. Alzheimer Dis Assoc Disord 2007; 21: 1-7.
25. Forman MS, Mackenzie IR, Cairns NJ, Swanson E, Boyer PJ, Drachman DA, Jhaveri BS, Karlawish JH, Pestrvik A, Smith TN, Tu PH, Watts GDJ, Markesbery WR, Smith CD, Kimonis VE. Novel ubiquitin neuropathology in frontotemporal dementia with valosin-containing protein gene mutations. J Neuropathol Exp Neurol 2006; 65: 571-81.
26. Gitcho MA, Baloh RH, Chakraverty S, Mayo K, Norton JB, Levitch D, Hatanpaa KJ, White CL III, Bigio EH, Caselli R, Baker M, Al-Lozi MT, Morris JC, Pestronk A, Rademakers R, Goate AM, Cairns NJ. TDP-43 A315T mutation in familial motor neuron disease. Ann Neurol 2008; 63: 535-8.
27. Kabashi E, Valdmanis PN, Dion P, Spiegelman D, McConkey BJ, Vande Velde C, Bouchard J-P, Lacomblez L, Pochigaeva K, Salachas F, Pradat P-F, Camu W, Meininger V, Dupre N, Rouleau GA. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat Genet 2008; 40: 572-4.
28. Benajiba L, Le Ber I, Camuzat A, Lacoste M, Thomas-Anterion C, Couratier P, Legallic S, Salachas F, Hannequin D, Decousus M, Lacomblez L, Guedj E, Golfier V, Camu W, Dubois B, Campion D, Meininger V, Brice A. French Clinical and Genetic Research Network on Frontotemporal Lobar Degeneration/Frontotemporal Lobar Degeneration with Motoneuron Disease TARDBP mutations in motoneuron disease with frontotemporal lobar degeneration. Ann Neurol 2009; 65: 470-4.
29. Gitcho MA, Bigio EH, Mishra M, Johnson N, Weintraub S, Mesulam M, Rademakers R, Chakraverty S, Cruchaga C, Morris JC, Goate AM, Cairns NJ. TARDBP 3-prime-UTR variant in autopsy-confirmed frontotemporal lobar degeneration with TDP-43 proteinopathy. Acta Neuropathol 2009; 118: 633-45.
30. Luty AA, Kwok JBJ, Thompson EM, Blumsbergs P, Brooks WS, Loy CT, Dobson-Stone C, Panegyres PK, Hecker J, Nicholson GA, Halliday GM, Schofield PR. Pedigree with frontotemporal lobar degeneration-motor neuron disease and Tar DNA binding protein-43 positive neuropathology: genetic linkage to chromosome 9. BMC Neurol 2008; 8: 32.
31. Renton AE, Majounie E, Waite A, Simón-Sánchez J, Rollinson S, Gibbs JR, Schymick JC, Laaksovirta H, van Swieten JC, Myllykangas L, Kalimo H, Paetou A, Abramzon Y, Remes AM, Kaganovitch 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 JB, Toulson G, Ricahrdson A, Gerhard A, Snowden J, Mann D, Neary D, Nalls MA, Peuralinna T, Jansson L, Isoviita VM, Kalvorinne AL, Hölttä-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 JD, 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 ALS-FTD. Neuron 2011; 72: 257-68.
32. Josephs KA, Whitwell JL, Jack CR, Parisi JE, Dickson DW. Frontotemporal lobar degeneration without lobar atrophy. Arch Neurol 2006; 63: 1632-8.
33. Kersaitis C, Holliday GM, Xuereb JH, Pamphlett R, Bak TH, Hodges JR, Kril JJ. Ubiquitin-positive inclusions and progression of pathology in frontotemporal dementia and motor neurone disease identifies a group with mainly early pathology. Neuropathol Appl Neurobiol 2006; 32: 83-91.
34. Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brownlee LM, Vogel FS, Hughes JP, van Belle G, Berg L. 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: 479-86.
35. Jellinger KA, Bancher C. Neuropathology of Alzheimer's disease: a critical update. J Neural Transm 1998; 54: 77-95.
36. Newell KL, Hyman BT, Growden JH, Hedley-Whyte ET. Application of the National Institute on Aging (NIA)-Reagan Institute criteria for the neuropathological diagnosis of Alzheimer's disease. J Neuropathol Exp Neurol 1999; 58: 1147-55.
37. Hyman BT, Phelps CH, Beach TG, Bigio EH, Cairns NJ, Carillo MC, Dickson DW, Duyckaerts C, Frosch MP, Masliah E, Mirra SS, Nelson PT, Schneider JA, Thal DR, Theis B, Trojanowski JQ, Vinters HV, Montine TJ. National Institute on Aging-Alzheimer's Association Guidelines for the neuropathological assessment of Alzheimer's disease. Alzheimer & Dem 2012; 8: 1-13.
38. 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.
39. Duyckaerts C, Hauw JJ, Bastenaire F, Piette F, Poulain C, Rainsard V, Javoy-Agid F, Berthaux P. Laminar distribution of neocortical senile plaques in senile dementia of the Alzheimer type. Acta Neuropathol 1986; 70: 249-56.
40. Yaguchi M, Fujita Y, Amari M, Takatama M, Al-Sarraj S, Leigh PN, Okamoto K. Morphological differences of intraneural ubiquitin positive inclusions in the dentate gyrus and parahippocampal gyrus of motor neuron disease with dementia. Neuropathology 2004; 24: 296-301.
41. Davidson Y, Kelley T, Mackenzie IRA, Pickering Brown S, Du Plessis D, Neary D, Snowden JS, Mann DMA. Ubiquinated pathological lesions in frontotemporal lobar degeneration contain TAR DNA-binding protein, TDP-43. Acta Neuropathol 2007; 113: 521-33.
42. Matsumoto S, Udaka F, Kameyama M, Kusaka H, Itoh H, Imai T. Subcortical neurofibrillary tangles, neuropil threads and argentophilic glial inclusions in corticobasal degeneration. Clin Neuropath 1996; 15: 209-14.
43. Armstrong RA, Cairns NJ, Lantos PL. A quantitative study of the pathological lesions in neocortex and hippocampus of 12 patients with corticobasal degeneration. Exp Neurol 2000; 163: 348-56.
44. Yamada T, McGeer PL, McGeer EG. Appearance of paired nucleated tau-positive glia in patients with progressive supranuclear palsy brain tissue. Neurosci Lett 1992; 135: 99-102.
45. Ikeda K, Akiyama H, Kondo H, Haga C, Tanno E, Tokuda T, Ikeda S. Thorn-shaped astrocytes: possibly secondarily induced tau-positive glial fibrillary tangles. Acta Neuropathol 1995; 90: 620-5.
46. Komori T. Tau positive glial inclusions in progressive supranuclear palsy, corticobasal degeneration and Pick's disease. Brain Pathol 1999; 9: 663-79.
47. Probst A, Tolnay M. Argyrophilic grain disease, a frequent and largely underestimated cause of dementia in old patients. Rev Neurol 2002; 158: 155-65.
48. Pirici D, Vandenberghe R, Rademakers R, Dermant B, Cruts M, Vennekens K, Cuijt I, Lubke U, Centerick C, Martin JJ, Van Broeckhoven C, Kumar-Singh S. Characterization of ubiquinated intraneuronal inclusions in a novel Belgian frontotemporal lobar degeneration family. J Neuropath. Exp Neurol 2006; 65: 289-301.
49. Hatanpaa KJ, Bigio EH, Cairns NJ, Womack KB, Weintraub S, Morris JC, Foong C, Xiao GH, Hladik C, Mantanona TY, White CL. TAR DNA-binding protein 43 immunohistochemistry reveals extensive neuritic pathology in FTLD-U: a Midwest-Southwest Consortium for FTLD-U study. J Neuropathol Exp Neurol 2008; 67: 271-9.
50. Armstrong RA. Correlations between the morphology of diffuse and primitive β-amyloid (Aβ) deposits and the frequency of associated cells in Down's syndrome. Neuropathol Appl Neurobiol 1996; 22: 527-30.
51. Armstrong RA, Lantos PL, Cairns NJ. Spatial correlations between the vacuolation, prion protein deposits, and surviving neurons in the cerebral cortex in sporadic Creutzfeldt-Jakob disease. Neuropathology 2001; 21: 266-71.
52. Armstrong RA, Ironside J, Lantos PL, Cairns NJ. A quantitative study of the pathological changes in the cerebellum of 15 cases of variant Creutzfeldt-Jakob disease. Neuropathol Appl Neurobiol 2009; 35: 36-45.
53. Snedecor GW, Cochran WG. Statistical Methods. Ames, IA, USA: Iowa State University Press, 1980.
54. Neumann M, Kwong LK, Lee EB, Kremmer E, Flately A, Xu Y, Forman MS, Troost D, Kretzschmar HA, Trojanoswki JQ, Lee VMY. Phosphorylation of S409/410 of TDP-43 is a consistent feature in all sporadic and familial forms of TDP-43 proteinopathies. Acta Neuropathol 2009; 117: 137-49.
55. Hasegawa M, Arai T, Nonaka T, Kametani F, Yoshida M, Hashizume Y, Beach TG, Buratti E, Baralle F, Morita M, Nakano I, Oda T, Tsuchiya K, Akiyama H. Phosphorylated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Ann Neurol 2008; 64: 60-70.
56. Olive M, Janve A, Moreno D, Gamez J, Torrejon-Escritano B, Ferrer I. TAR DNA-binding protein 43 accumulation in protein aggregate myopathies. J Neuropathol Exp Neurol 2009; 68: 262-73.
57. Schwab C, Arai T, Hasegawa M, Akiyama H, Yu S, McGeer PL. TDP-43 pathology in familial British dementia. Acta Neuropathol 2009; 118: 303-11.
58. Armstrong RA, Carter D, Cairns NJ. A quantitative study of the neuropathology of 32 sporadic and familial cases of frontotemporal lobar degeneration (FTLD) with TDP-43 proteinopathy (FTLD-TDP). Neuropathol Appl Neurobiol 2012; 38: 25-38.
59. Minamu M, Mizutani T, Kawanishi R, Suzuki Y, Mori H. Neuronal expression of alpha B crystallin in cerebral infarction. Acta Neuropathol 2003; 105: 549-54.
60. Pierucci A, de Oliveira AL. Increased sensory neuron apoptotic death two weeks after peripheral axonotomy in C57BL/6J mice compared to A/J mice. Neurosci Lett 2006; 396: 127-31.
61. Kato S, Hirano A, Umahara T, Wena JF, Herz F, Ohama E. Ultrastructural and immunohistochemical studies on ballooned cortical neurons in Creutzfeldt-Jakob disease: expression of alpha-B-crystallin, ubiquitin and stress response protein-27. Acta Neuropathol 1992; 84: 443-8.
62. Goedert M, Clavaguera F, Tolnay M. The propagation of prion-like protein inclusions in neurodegenerative diseases. Trends Neurosci 2010; 33: 317-25.