Frontotemporal dementia with the C9ORF72 hexanucleotide repeat expansion: Clinical, neuroanatomical and neuropathological features

Brain

Volumn 135, Issue 3, 2012, Pages 736-750

  Mahoney, Colin J ^a   Beck, Jon ^a   Rohrer, Jonathan D ^a   Lashley, Tammaryn ^a   Mok, Kin ^b   Shakespeare, Tim ^a   Yeatman, Tom ^a   Warrington, Elizabeth K ^a   Schott, Jonathan M ^a   Fox, Nick C ^a   Rossor, Martin N ^a   Hardy, John ^b   Collinge, John ^a   Revesz, Tamas ^a   Mead, Simon ^a   Warren, Jason D ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

frontotemporal lobar degeneration; genetics; motor neuron disease; neurodegenerative disorders; neuroimaging

Indexed keywords

ADULT; AGED; AGITATION; ANXIETY; ARTICLE; BRAIN ATROPHY; C9ORF72 GENE; CEREBELLUM; FEMALE; FRONTAL CORTEX; FRONTOTEMPORAL DEMENTIA; GENE; GENE MUTATION; GENETIC HETEROGENEITY; GRAY MATTER; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MEMORY DISORDER; MOTOR NEURON DISEASE; NEUROANATOMY; NEUROIMAGING; NEUROPATHOLOGY; PARIETAL CORTEX; PRIORITY JOURNAL; TEMPORAL CORTEX; THALAMUS;

EID: 84857517997     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awr361     Document Type: Article

References (55)

1. Al-Sarraj S, King A, Troakes C, Smith B, Maekawa S, Bodi I, et al. p62 positive, TDP-43 negative, neuronal cytoplasmic and intranuclear inclusions in the cerebellum and hippocampus define the pathology of C9orf72-linked FTLD and MND/ALS [Internet]. Acta Neuropathologica 2011. Available from: http://www.springerlink.com/index/10.1007/s00401-011-0911-2 (23 November 2011, date last accessed).
2. Andreasen NC, O'Leary DS, Cizadlo T, Arndt S, Rezai K, Ponto LL, et al. Schizophrenia and cognitive dysmetria: a positron-emission tomography study of dysfunctional prefrontal-thalamic-cerebellar circuitry. Proc Natl Acad Sci USA 1996;93:9985-90.
3. Beck J, King A, Scahill R, Warren JD, Fox NC, Rossor MN, et al. A distinct clinical, neuropsychological and radiological phenotype is associated with progranulin gene mutations in a large UK series. Brain 2008;131:706-20.
4. Boeve BF, Lang AE, Litvan I. Corticobasal degeneration and its relationship to progressive supranuclear palsy and frontotemporal dementia. Ann Neurol 2003;54(Suppl 5): S15-S19.
5. Boxer AL, Mackenzie IR, Boeve BF, Baker M, Seeley WW, Crook R, et al. Clinical, neuroimaging and neuropathological features of a new chromosome 9p-linked FTD-ALS family. J Neurol Neurosurg Psychiatr 2011;82:196-203.
6. Cook P, Bai Y, Nedjati-Gilani S, Seunarine K, Hall M, Parker G, et al. Camino: open-source diffusion-MRI reconstruction and processing. Seattle, WA, USA: International Society for Magnetic Resonance in Medicine; 2006. p. 2759.
7. Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 1999;9:179-94.
8. de Jong LW, van der Hiele K, Veer IM, Houwing JJ, Westendorp R G J, Bollen E L E M, et al. Strongly reduced volumes of putamen and thalamus in Alzheimer's disease: an MRI study. Brain 2008;131:3277-85.
9. Dejesus-Hernandez M, Mackenzie IR, Boeve BF, Boxer AL, Baker M, Rutherford NJ, et al. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS [Internet]. Neuron 2011. Available from: http://www.ncbi. nlm.nih.gov/pubmed/21944778 (19 October 2011, date last accessed).
10. Fischl B, Dale AM. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 2000;97:11050-5.
11. Fletcher PD, Warren JD. Semantic Dementia: a specific network-opathy [Internet]. J Mol Neurosci 2011. Available from: http://www.ncbi.nlm. nih.gov/pubmed/21710360 (17 August 2011, date last accessed).
12. Freeborough PA, Fox NC. The boundary shift integral: an accurate and robust measure of cerebral volume changes from registered repeat MRI. IEEE Trans Med Imaging 1997;16:623-9.
13. Freeborough PA, Fox NC, Kitney RI. Interactive algorithms for the segmentation and quantitation of 3-D MRI brain scans. Comput Methods Programs Biomed 1997;53:15-25.
14. Gijselinck I, Engelborghs S, Maes G, Cuijt I, Peeters K, Mattheijssens M, et al. Identification of 2 Loci at chromosomes 9 and 14 in a multiplex family with frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Arch Neurol 2010;67:606-16.
15. Gijselinck I, Van Langenhove T, van der Zee J, Sleegers K, Philtjens S, Kleinberger G, et al. A C9orf72 promoter repeat expansion in a Flanders-Belgian cohort with disorders of the frontotemporal lobar degeneration-amyotrophic lateral sclerosis spectrum: a gene identification study. Lancet Neurol 2011. Dec. 7 [Epub ahead of print].
16. Goldman JS, Farmer JM, Wood EM, Johnson JK, Boxer A, Neuhaus J, et al. Comparison of family histories in FTLD subtypes and related tauopathies. Neurology 2005;65:1817-9.
17. Goossens L, Schruers K, Peeters R, Griez E, Sunaert S. Visual presentation of phobic stimuli: amygdala activation via an extrageniculostriate pathway? Psychiatry Res 2007;155:113-20.
18. Gorno-Tempini ML, Hillis AE, Weintraub S, Kertesz A, Mendez M, Cappa SF, et al. Classification of primary progressive aphasia and its variants. Neurology 2011;76:1006-14.
19. Hornberger M, Piguet O, Graham AJ, Nestor PJ, Hodges JR. How preserved is episodic memory in behavioral variant frontotemporal dementia? Neurology 2010;74:472-9.
20. Kessler RM, Woodward ND, Riccardi P, Li R, Ansari MS, Anderson S, et al. Dopamine D2 receptor levels in striatum, thalamus, substantia nigra, limbic regions, and cortex in schizophrenic subjects. Biol Psychiatr 2009;65:1024-31.
21. 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;31:239-49.
22. Lashley T, Rohrer JD, Bandopadhyay R, Fry C, Ahmed Z, Isaacs AM, et al. A comparative clinical, pathological, biochemical and genetic study of fused in sarcoma proteinopathies. Brain 2011;134:2548-64.
23. Le Ber I, Camuzat A, Berger E, Hannequin D, Laquerriè re A, Golfier V, et al. Chromosome 9p-linked families with frontotemporal dementia associated with motor neuron disease. Neurology 2009;72:1669-76.
24. Le Ber I, Camuzat A, Hannequin D, Pasquier F, Guedj E, Rovelet-Lecrux A, et al. Phenotype variability in progranulin mutation carriers: a clinical, neuropsychological, imaging and genetic study. Brain 2008;131:732-46.
25. Lillo P, Garcin B, Hornberger M, Bak TH, Hodges JR. Neurobehavioral features in frontotemporal dementia with amyotrophic lateral sclerosis. Arch Neurol 2010;67:826-30.
26. Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC, et al. Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology 1996;47:1-9.
27. Loy CT, Kril JJ, Trollor JN, Kiernan MC, Kwok JB, Vucic S, et al. The case of a 48 year-old woman with bizarre and complex delusions. Nat Rev Neurol 2010;6:175-9.
28. Luty AA, Kwok J B J, Thompson EM, Blumbergs P, Brooks WS, Loy CT, et al. 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.
29. Mackenzie I R A, Neumann M, Baborie A, Sampathu DM, Plessis D, Jaros E, et al. A harmonized classification system for FTLD-TDP pathology. Acta Neuropathologica 2011;122:111-3.
30. Momeni P, Schymick J, Jain S, Cookson MR, Cairns NJ, Greggio E, et al. Analysis of IFT74 as a candidate gene for chromosome 9p-linked ALS-FTD. BMC Neurol 2006;6:44.
31. Morita M, Al-Chalabi A, Andersen PM, Hosler B, Sapp P, Englund E, et al. A locus on chromosome 9p confers susceptibility to ALS and frontotemporal dementia. Neurology 2006;66:839-44.
32. Murray ME, Dejesus-Hernandez M, Rutherford NJ, Baker M, Duara R, Graff-Radford NR, et al. Clinical and neuropathologic heterogeneity of c9FTD/ALS associated with hexanucleotide repeat expansion in C9ORF72 [Internet]. Acta Neuropathologica 2011. Available from: http://www.ncbi.nlm.nih.gov/pubmed/ 22083254 (21 November 2011, date last accessed).
33. Omar R, Sampson EL, Loy CT, Mummery CJ, Fox NC, Rossor MN, et al. Delusions in frontotemporal lobar degeneration. J Neurol 2009;256:600-7.
34. Pearson JP, Williams NM, Majounie E, Waite A, Stott J, Newsway V, et al. Familial frontotemporal dementia with amyotrophic lateral sclerosis and a shared haplotype on chromosome 9p. J Neurol 2011;258:647-55.
35. Pikkarainen M, Hartikainen P, Alafuzoff I. Neuropathologic features of frontotemporal lobar degeneration with ubiquitin-positive inclusions visualized with ubiquitin-binding protein p62 immunohistochemistry. J Neuropathol Exp Neurol 2008;67:280-98.
36. Rademakers R, Baker M, Gass J, Adamson J, Huey ED, Momeni P, et al. Phenotypic variability associated with progranulin haploinsufficiency in patients with the common 1477C-4T (Arg493X) mutation: an international initiative. Lancet Neurol 2007;6:857-68.
37. Rascovsky K, Hodges JR, Knopman D, Mendez MF, Kramer JH, Neuhaus J, et al. Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain 2011;134:2456-77.
38. Ratnavalli E, Brayne C, Dawson K, Hodges JR. The prevalence of frontotemporal dementia. Neurology 2002;58:1615-21.
39. Renton AE, Majounie E, Waite A, Simón-Sánchez J, Rollinson S, Gibbs JR, et al. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD [Internet]. Neuron 2011. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21944779 (19 October 2011, date last accessed).
40. Ridgway GR, Omar R, Ourselin S, Hill D L G, Warren JD, Fox NC. Issues with threshold masking in voxel-based morphometry of atrophied brains. Neuroimage 2009;44:99-111.
41. Rohrer JD, Guerreiro R, Vandrovcova J, Uphill J, Reiman D, Beck J, et al. The heritability and genetics of frontotemporal lobar degeneration. Neurology 2009;73:1451-6.
42. Rohrer J, Lashley T, Schott J. Clinical and neuroanatomical signatures of tissue pathology in fontotemporal lobar degeneration. Brain 2011;134:2565-81.
43. Rohrer JD, Ridgway GR, Modat M, Ourselin S, Mead S, Fox NC, et al. Distinct profiles of brain atrophy in frontotemporal lobar degeneration caused by progranulin and tau mutations. Neuroimage 2010;53:1070-6.
44. Rohrer JD, Warren JD. Phenotypic signatures of genetic frontotemporal dementia [Internet]. Curr Opin Neurol 2011. Available from: http://www.ncbi.nlm. nih.gov/pubmed/21986680 (9 November 2011, date last accessed).
45. Rohrer JD, Warren JD, Omar R, Mead S, Beck J, Revesz T, et al. Parietal lobe deficits in frontotemporal lobar degeneration caused by a mutation in the progranulin gene. Arch Neurol 2008;65:506-13.
46. Schmahmann JD. Cognition, emotion and the cerebellum. Brain 2005;129:290-2.
47. Schmahmann J, Pandya D. Disconnection syndromes of basal ganglia, thalamus, and cerebrocerebellar systems. Cortex 2008;44:1037-66.
48. Seelaar H, Rohrer JD, Pijnenburg Y A L, Fox NC, van Swieten JC. Clinical, genetic and pathological heterogeneity of frontotemporal dementia: a review. J Neurol Neurosurg Psychiatr 2011;82:476-86.
49. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, et al. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 2006;31:1487-505.
50. Smith SM, Nichols TE. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 2009;44:83-98.
51. Straube T, Mentzel H-J, Miltner W H R. Waiting for spiders: brain activation during anticipatory anxiety in spider phobics. Neuroimage 2007;37:1427-36.
52. Tedesco AM, Chiricozzi FR, Clausi S, Lupo M, Molinari M, Leggio MG. The cerebellar cognitive profile [Internet]. Brain 2011. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22036960 (9 November 2011, date last accessed).
53. Valdmanis PN, Dupre N, Bouchard J-P, Camu W, Salachas F, Meininger V, et al. Three families with amyotrophic lateral sclerosis and frontotemporal dementia with evidence of linkage to chromosome 9p. Arch Neurol 2007;64:240-5.
54. Van der Werf YD, Scheltens P, Lindeboom J, Witter MP, Uylings H B M, Jolles J. Deficits of memory, executive functioning and attention following infarction in the thalamus; a study of 22 cases with localised lesions. Neuropsychologia 2003;41:1330-44.
55. Vance C, Al-Chalabi A, Ruddy D, Smith BN, Hu X, Sreedharan J, et al. Familial amyotrophic lateral sclerosis with frontotemporal dementia is linked to a locus on chromosome 9p13.2-21.3. Brain 2006;129:868-76.