Timing and significance of pathological features in C9orf72 expansion-associated frontotemporal dementia

Brain

Volumn 139, Issue 12, 2016, Pages 3202-3216

  Vatsavayai, Sarat C ^a   Yoon, Soo Jin ^b   Gardner, Raquel C ^a   Gendron, Tania F ^c   Vargas, Jose Norberto S ^a   Trujillo, Andrew ^a   Pribadi, Mochtar ^d   Phillips, Joanna J ^a   Gaus, Stephanie E ^a   Hixson, John D ^e   Garcia, Paul A ^e   Rabinovici, Gil D ^a   Coppola, Giovanni ^d   Geschwind, Daniel H ^d   Petrucelli, Leonard ^c   Miller, Bruce L ^a   Seeley, William W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Eulji University School of Medicine   (South Korea)

^c MAYO CLINIC   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Frontotemporal dementia; Protein aggregation; TDP 43

Indexed keywords

LAMOTRIGINE; PHENYTOIN; QUETIAPINE; TAR DNA BINDING PROTEIN; C9ORF72 PROTEIN, HUMAN; DNA BINDING PROTEIN; PROTEIN; REPETITIVE DNA; TDP-43 PROTEIN, HUMAN;

ADULT; AGITATION; AMYGDALA; ANTERIOR CINGULATE; ANTICONVULSANT THERAPY; ARTICLE; AUTOPSY; BIPOLAR DISORDER; BLUNTED AFFECT; BRAIN REGION; C9ORF72 GENE; CASE REPORT; CLINICAL FEATURE; COMPLEX PARTIAL SEIZURE; DEMENTIA; DEPRESSION; ELECTROENCEPHALOGRAM; EPILEPTIC DISCHARGE; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; FRONTAL VARIANT FRONTOTEMPORAL DEMENTIA; GENE; GENETIC ANALYSIS; HAND TREMOR; HIPPOCAMPUS; HOSPICE CARE; HUMAN; HYPERREFLEXIA; IMMUNOHISTOCHEMISTRY; LIBIDO; MIDDLE AGED; MINI MENTAL STATE EXAMINATION; MOOD DISORDER; MOTOR NEURON DISEASE; NERVE DEGENERATION; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; OVERNUTRITION; PANIC; PARKINSONISM; PERSONAL HYGIENE; PRIORITY JOURNAL; PROTEIN AGGREGATION; TDP 43 PROTEINOPATHY; TELEMETRY; TEMPORAL LOBE EPILEPSY; TEMPORAL LOBECTOMY; TONIC CLONIC SEIZURE; TRAUMATIC BRAIN INJURY; TREMOR; VERBAL MEMORY; AGED; FRONTOTEMPORAL DEMENTIA; GENETICS; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY;

AGED; DNA REPEAT EXPANSION; DNA-BINDING PROTEINS; FEMALE; FRONTOTEMPORAL DEMENTIA; HUMANS; PROTEINS;

EID: 85014016605     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aww250     Document Type: Article

References (41)

1. Abbruzzese G, Arata L, Bino G, Dall'Agata D, Leonardi A. Thalamic dementia: report of a case with unusual lesion location. Ital J Neurol Sci 1986; 7: 155-9.
2. Ash PE, Bieniek KF, Gendron TF, Caulfield T, Lin WL, Dejesus-Hernandez M, et al. Unconventional translation of C9ORF72 GGGGCC expansion generates insoluble polypeptides specific to c9FTD/ALS. Neuron 2013; 77: 639-46.
3. Baborie A, Griffiths TD, Jaros E, Perry R, McKeith IG, Burn DJ, et al. Accumulation of dipeptide repeat proteins predates that of TDP-43 in frontotemporal lobar degeneration associated with hexanucleotide repeat expansions in C9ORF72 gene. Neuropathol Appl Neurobiol 2015; 41: 601-12.
4. Boeve BF, Boylan KB, Graff-Radford NR, DeJesus-Hernandez M, Knopman DS, Pedraza O, et al. Characterization of frontotemporal dementia and/or amyotrophic lateral sclerosis associated with the GGGGCC repeat expansion in C9ORF72. Brain 2012; 135(Pt 3): 765-83.
5. Cooper-Knock J, Higginbottom A, Stopford MJ, Highley JR, Ince PG, Wharton SB, et al. Antisense RNA foci in the motor neurons of C9ORF72-ALS patients are associated with TDP-43 proteinopathy. Acta Neuropathol 2015; 130: 63-75.
6. 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. Neuron 2011; 72: 245-56.
7. Donnelly CJ, Zhang PW, Pham JT, Haeusler AR, Mistry NA, Vidensky S, et al. RNA toxicity from the ALS/FTD C9ORF72 expansion is mitigated by antisense intervention. Neuron 2013; 80: 415-28.
8. Freibaum BD, Lu Y, Lopez-Gonzalez R, Kim NC, Almeida S, Lee KH, et al. GGGGCC repeat expansion in C9orf72 compromises nucleocytoplasmic transport. Nature 2015; 525: 129-33.
9. Gendron TF, Bieniek KF, Zhang YJ, Jansen-West K, Ash PE, Caulfield T, et al. Antisense transcripts of the expanded C9ORF72 hexanucleotide repeat form nuclear RNA foci and undergo repeat-associated non-ATG translation in c9FTD/ALS. Acta Neuropathol 2013; 126: 829-44.
10. 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 2012; 11: 54-65.
11. Haeusler AR, Donnelly CJ, Periz G, Simko EA, Shaw PG, Kim MS, et al. C9orf72 nucleotide repeat structures initiate molecular cascades of disease. Nature 2014; 507: 195-200.
12. Hetman M, Pietrzak M. Emerging roles of the neuronal nucleolus. Trends Neurosci 2012; 35: 305-14.
13. Janssen P, Houben M, Hoff E. Photosensitivity in a patient with C9orf72 repeat expansion. Amyotroph Lateral Scler Frontotemporal Degener 2016; 17: 266-9.
14. Jovicic A, Mertens J, Boeynaems S, Bogaert E, Chai N, Yamada SB, et al. Modifiers of C9orf72 dipeptide repeat toxicity connect nucleocytoplasmic transport defects to FTD/ALS. Nat Neurosci 2015; 18: 1226-9.
15. Karageorgiou E, Miller BL. Frontotemporal lobar degeneration: a clinical approach. Semin Neurol 2014; 34: 189-201.
16. Khan BK, Yokoyama JS, Takada LT, Sha SJ, Rutherford NJ, Fong JC, et al. Atypical, slowly progressive behavioural variant frontotemporal dementia associated with C9ORF72 hexanucleotide expansion. J Neurol Neurosurg Psychiatry 2012; 83: 358-64.
17. Kwon I, Xiang S, Kato M, Wu L, Theodoropoulos P, Wang T, et al. Poly-dipeptides encoded by the C9orf72 repeats bind nucleoli, impede RNA biogenesis, and kill cells. Science 2014; 345: 1139-45.
18. Lee SE, Khazenzon AM, Trujillo AJ, Guo CC, Yokoyama JS, Sha SJ, et al. Altered network connectivity in frontotemporal dementia with C9orf72 hexanucleotide repeat expansion. Brain 2014; 137(Pt 11): 3047-60.
19. Lee YB, Chen HJ, Peres JN, Gomez-Deza J, Attig J, Stalekar M, et al. Hexanucleotide repeats in ALS/FTD form length-dependent RNA foci, sequester RNA binding proteins, and are neurotoxic. Cell Rep 2013; 5: 1178-86.
20. Mackenzie IR, Arzberger T, Kremmer E, Troost D, Lorenzl S, Mori K, et al. Dipeptide repeat protein pathology in C9ORF72 mutation cases: clinico-pathological correlations. Acta Neuropathol 2013; 126: 859-79.
21. Mackenzie IR, Frick P, Grasser FA, Gendron TF, Petrucelli L, Cashman NR, et al. Quantitative analysis and clinico-pathological correlations of different dipeptide repeat protein pathologies in C9ORF72 mutation carriers. Acta Neuropathol 2015; 130: 845-61.
22. Mahoney CJ, Beck J, Rohrer JD, Lashley T, Mok K, Shakespeare T, et al. Frontotemporal dementia with the C9ORF72 hexanucleotide repeat expansion: clinical, neuroanatomical and neuropathological features. Brain 2012; 135(Pt 3): 736-50.
23. Mann DM, Rollinson S, Robinson A, Bennion Callister J, Thompson JC, Snowden JS, et al. Dipeptide repeat proteins are present in the p62 positive inclusions in patients with frontotemporal lobar degeneration and motor neurone disease associated with expansions in C9ORF72. Acta Neuropathol Commun 2013; 1: 68.
24. Miki Y, Mori F, Tanji K, Kurotaki H, Kakita A, Takahashi H, et al. An autopsy case of incipient Pick's disease: immunohistochemical profile of early-stage Pick body formation. Neuropathology 2014; 34: 386-91.
25. Mizielinska S, Gronke S, Niccoli T, Ridler CE, Clayton EL, Devoy A, et al. C9orf72 repeat expansions cause neurodegeneration in Drosophila through arginine-rich proteins. Science 2014; 345: 1192-4.
26. Mizielinska S, Lashley T, Norona FE, Clayton EL, Ridler CE, Fratta P, et al. C9orf72 frontotemporal lobar degeneration is characterised by frequent neuronal sense and antisense RNA foci. Acta Neuropathol 2013; 126: 845-57.
27. Mori K, Lammich S, Mackenzie IR, Forne I, Zilow S, Kretzschmar H, et al. hnRNP A3 binds to GGGGCC repeats and is a constituent of p62-positive/TDP43-negative inclusions in the hippocampus of patients with C9orf72 mutations. Acta neuropathologica 2013a; 125: 413-23.
28. Mori K, Weng SM, Arzberger T, May S, Rentzsch K, Kremmer E, et al. The C9orf72 GGGGCC repeat is translated into aggregating dipeptide-repeat proteins in FTLD/ALS. Science 2013b; 339: 1335-8.
29. Proudfoot M, Gutowski NJ, Edbauer D, Hilton DA, Stephens M, Rankin J, et al. Early dipeptide repeat pathology in a frontotemporal dementia kindred with C9ORF72 mutation and intellectual disability. Acta Neuropathol 2014; 127: 451-8.
30. Renton AE, Majounie E, Waite A, Simon-Sanchez J, Rollinson S, Gibbs JR, et al. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 2011; 72: 257-68.
31. Rohrer JD, Nicholas JM, Cash DM, van Swieten J, Dopper E, Jiskoot L, et al. Presymptomatic cognitive and neuroanatomical changes in genetic frontotemporal dementia in the Genetic Frontotemporal dementia Initiative (GENFI) study: a cross-sectional analysis. Lancet Neurol 2015; 14: 253-62.
32. Sareen D, O'Rourke JG, Meera P, Muhammad AK, Grant S, Simpkinson M, et al. Targeting RNA foci in iPSC-derived motor neurons from ALS patients with a C9ORF72 repeat expansion. Sci Trans Med 2013; 5: 208ra149.
33. Schludi MH, May S, Grasser FA, Rentzsch K, Kremmer E, Kupper C, et al. Distribution of dipeptide repeat proteins in cellular models and C9orf72 mutation cases suggests link to transcriptional silencing. Acta Neuropathol 2015; 130: 537-55.
34. Sha SJ, Takada LT, Rankin KP, Yokoyama JS, Rutherford NJ, Fong JC, et al. Frontotemporal dementia due to C9ORF72 mutations: clinical and imaging features. Neurology 2012; 79: 1002-11.
35. Suhonen NM, Kaivorinne AL, Moilanen V, Bode M, Takalo R, Hanninen T, et al. Slowly progressive frontotemporal lobar degeneration caused by the C9ORF72 repeat expansion: a 20-year followup study. Neurocase 2015; 21: 85-9.
36. Szirmai I, Vastagh I, Szombathelyi E, Kamondi A. Strategic infarcts of the thalamus in vascular dementia. J Neurol Sci 2002; 203-204: 91-7.
37. Wen X, Tan W, Westergard T, Krishnamurthy K, Markandaiah SS, Shi Y, et al. Antisense proline-arginine RAN dipeptides linked to C9ORF72-ALS/FTD form toxic nuclear aggregates that initiate in vitro and in vivo neuronal death. Neuron 2014; 84: 1213-25.
38. Zhang K, Donnelly CJ, Haeusler AR, Grima JC, Machamer JB, Steinwald P, et al. The C9orf72 repeat expansion disrupts nucleocytoplasmic transport. Nature 2015; 525: 56-61.
39. Zhang YJ, Jansen-West K, Xu YF, Gendron TF, Bieniek KF, Lin WL, et al. Aggregation-prone c9FTD/ALS poly(GA) RAN-translated proteins cause neurotoxicity by inducing ER stress. Acta Neuropathol 2014; 128: 505-24.
40. Zu T, Gibbens B, Doty NS, Gomes-Pereira M, Huguet A, Stone MD, et al. Non-ATG-initiated translation directed by microsatellite expansions. Proc Natl Acad Sci USA 2011; 108: 260-5.
41. Zu T, Liu Y, Banez-Coronel M, Reid T, Pletnikova O, Lewis J, et al. RAN proteins and RNA foci from antisense transcripts in C9ORF72 ALS and frontotemporal dementia. Proc Natl Acad Sci USA 2013; 110: E4968-77.