C9orf72 G4C2 repeat expansions in Alzheimer's disease and mild cognitive impairment

Neurobiology of Aging

Volumn 34, Issue 6, 2013, Pages 1712.e1-1712.e7

  Cacace, Rita ^a,b   Van Cauwenberghe, Caroline ^a,b   Bettens, Karolien ^a,b   Gijselinck, Ilse ^a,b   van der Zee, Julie ^a,b   Engelborghs, Sebastiaan ^b,c   Vandenbulcke, Mathieu ^d   Van Dongen, Jasper ^a,b   Bäumer, Veerle ^a,b   Dillen, Lubina ^a,b   Mattheijssens, Maria ^a,b   Peeters, Karin ^a,b   Cruts, Marc ^a,b   Vandenberghe, Rik ^e   De Deyn, Peter P ^b,c,f   Van Broeckhoven, Christine ^a,b   Sleegers, Kristel ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b UNIVERSITY OF ANTWERP   (Belgium)

^c Hospital Network Antwerp   (Belgium)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^f UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

AD; C9orf72; Genetic association study; MCI

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; APOLIPOPROTEIN E4; TAU PROTEIN; THREONINE; C9ORF72 PROTEIN, HUMAN; PROTEIN; REPETITIVE DNA;

ADULT; ALZHEIMER DISEASE; ARTICLE; CAG REPEAT; CEREBROSPINAL FLUID; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; DISEASE PREDISPOSITION; FEMALE; GENE FREQUENCY; GENOTYPE; HUMAN; MAJOR CLINICAL STUDY; MALE; MILD COGNITIVE IMPAIRMENT; MOTOR NEURON DISEASE; MULTIINFARCT DEMENTIA; NERVE DEGENERATION; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; ONSET AGE; OPEN READING FRAME; PATHOGENESIS; PHENOTYPE; PREVALENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RISK FACTOR; AGED; BELGIUM; COHORT ANALYSIS; GENETICS; PROSPECTIVE STUDY; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; BELGIUM; COHORT STUDIES; DNA REPEAT EXPANSION; FEMALE; HUMANS; MALE; MILD COGNITIVE IMPAIRMENT; PROSPECTIVE STUDIES; PROTEINS;

EID: 84875267247     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2012.12.019     Document Type: Article

References (33)

1. Arighi A., Fumagalli G.G., Jacini F., Fenoglio C., Ghezzi L., Pietroboni A.M., De Riz M., Serpente M., Ridolfi E., Bonsi R., Bresolin N., Scarpini E., Galimberti D. Early onset behavioral variant frontotemporal dementia due to the C9ORF72 hexanucleotide repeat expansion: Psychiatric clinical presentations. J. Alzheimers Dis. 2012, 31:447-452.
2. Bettens K., Brouwers N., Van Miegroet H., Gil A., Engelborghs S., De Deyn P.P., Vandenberghe R., Van Broeckhoven C., Sleegers K. Follow-up study of susceptibility loci for Alzheimer's disease and onset age identified by genome-wide association. J. Alzheimers Dis. 2010, 19:1169-1175.
3. Boeve B.F., Boylan K.B., Graff-Radford N.R., DeJesus-Hernandez M., Knopman D.S., Pedraza O., Vemuri P., Jones D., Lowe V., Murray M.E., Dickson D.W., Josephs K.A., Rush B.K., Machulda M.M., Fields J.A., Ferman T.J., Baker M., Rutherford N.J., Adamson J., Wszolek Z.K., Adeli A., Savica R., Boot B., Kuntz K.M., Gavrilova R., Reeves A., Whitwell J., Kantarci K., Jack C.R., Parisi J.E., Lucas J.A., Petersen R.C., Rademakers R. Characterization of frontotemporal dementia and/or amyotrophic lateral sclerosis associated with the GGGGCC repeat expansion in C9ORF72. Brain 2012, 135:765-783.
4. Brouwers N., Nuytemans K., van der Zee J., Gijselinck I., Engelborghs S., Theuns J., Kumar-Singh S., Pickut B.A., Pals P., Dermaut B., Bogaerts V., De Pooter T., Serneels S., Van den Broeck M., Cuijt I., Mattheijssens M., Peeters K., Sciot R., Martin J.J., Cras P., Santens P., Vandenberghe R., De Deyn P.P., Cruts M., Van Broeckhoven C., Sleegers K. Alzheimer and Parkinson diagnoses in progranulin null mutation carriers in an extended founder family. Arch. Neurol. 2007, 64:1436-1446.
5. Chio A., Borghero G., Restagno G., Mora G., Drepper C., Traynor B.J., Sendtner M., Brunetti M., Ossola I., Calvo A., Pugliatti M., Sotgiu M.A., Murru M.R., Marrosu M.G., Marrosu F., Marinou K., Mandrioli J., Sola P., Caponnetto C., Mancardi G., Mandich P., La Bella V., Spataro R., Conte A., Monsurro M.R., Tedeschi G., Pisano F., Bartolomei I., Salvi F., Lauria Pinter G., Simone I., Logroscino G., Gambardella A., Quattrone A., Lunetta C., Volanti P., Zollino M., Penco S., Battistini S., Renton A.E., Majounie E., Abramzon Y., Conforti F.L., Giannini F., Corbo M., Sabatelli M. Clinical characteristics of patients with familial amyotrophic lateral sclerosis carrying the pathogenic GGGGCC hexanucleotide repeat expansion of C9ORF72. Brain 2012, 135:784-793.
6. DeJesus-Hernandez M., Mackenzie I.R., Boeve B.F., Boxer A.L., Baker M., Rutherford N.J., Nicholson A.M., Finch N.A., Flynn H., Adamson J., Kouri N., Wojtas A., Sengdy P., Hsiung G.Y., Karydas A., Seeley W.W., Josephs K.A., Coppola G., Geschwind D.H., Wszolek Z.K., Feldman H., Knopman D.S., Petersen R.C., Miller B.L., Dickson D.W., Boylan K.B., Graff-Radford N.R., Rademakers R. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 2011, 72:245-256.
7. Engelborghs S., Dermaut B., Goeman J., Saerens J., Marien P., Pickut B.A., Van den Broeck M., Serneels S., Cruts M., Van Broeckhoven C., De Deyn P.P. Prospective Belgian study of neurodegenerative and vascular dementia: APOE genotype effects. J. Neurol. Neurosurg. Psychiatry 2003, 74:1148-1151.
8. Engelborghs S., Dermaut B., Marien P., Symons A., Vloeberghs E., Maertens K., Somers N., Goeman J., Rademakers R., Van den Broeck M., Pickut B., Cruts M., Van Broeckhoven C., De Deyn P.P. Dose dependent effect of APOE epsilon4 on behavioral symptoms in frontal lobe dementia. Neurobiol. Aging 2006, 27:285-292.
9. Ferrari R., Mok K., Moreno J.H., Cosentino S., Goldman J., Pietrini P., Mayeux R., Tierney M.C., Kapogiannis D., Jicha G.A., Murrell J.R., Ghetti B., Wassermann E.M., Grafman J., Hardy J., Huey E.D., Momeni P. Screening for C9ORF72 repeat expansion in FTLD. Neurobiol. Aging 2012, 33:1850. e1-11.
10. Folstein M.F., Folstein S.E., McHugh P.R. "Mini-Mental State". A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 1975, 12:189-198.
11. Gijselinck I., Van Langenhove T., van der Zee J., Sleegers K., Philtjens S., Kleinberger G., Janssens J., Bettens K., Van Cauwenberghe C., Pereson S., Engelborghs S., Sieben A., De Jonghe P., Vandenberghe R., Santens P., De Bleecker J., Maes G., Baumer V., Dillen L., Joris G., Cuijt I., Corsmit E., Elinck E., Van Dongen J., Vermeulen S., Van den Broeck M., Vaerenberg C., Mattheijssens M., Peeters K., Robberecht W., Cras P., Martin J.J., De Deyn P.P., Cruts M., Van Broeckhoven C. 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.
12. Khan B.K., Yokoyama J.S., Takada L.T., Sha S.J., Rutherford N.J., Fong J.C., Karydas A.M., Wu T., Ketelle R.S., Baker M.C., Hernandez M.D., Coppola G., Geschwind D.H., Rademakers R., Lee S.E., Rosen H.J., Rabinovici G.D., Seeley W.W., Rankin K.P., Boxer A.L., Miller B.L. Atypical, slowly progressive behavioural variant frontotemporal dementia associated with C9ORF72 hexanucleotide expansion. J. Neurol. Neurosurg. Psychiatry 2012, 83:358-364.
13. Kohli, M.A., John-Williams, K., Rajbhandary, R., Naj, A., Whitehead, P., Hamilton, K., Carney, R.M., Wright, C., Crocco, E., Gwirtzman, H.E., Lang, R., Beecham, G., Martin, E.R., Gilbert, J., Benatar, M., Small, G.W., Mash, D., Byrd, G., Haines, J.L., Pericak-Vance, M.A., Zuchner, S. 2012. Repeat expansions in the C9ORF72 gene contribute to Alzheimer's disease in Caucasians. Neurobiol. Aging. http://dx.doi.org/10.1016/j.neurobiolaging.2012.10.003.
14. Laaksovirta H., Peuralinna T., Schymick J.C., Scholz S.W., Lai S.L., Myllykangas L., Sulkava R., Jansson L., Hernandez D.G., Gibbs J.R., Nalls M.A., Heckerman D., Tienari P.J., Traynor B.J. Chromosome 9p21 in amyotrophic lateral sclerosis in Finland: a genome-wide association study. Lancet Neurol. 2010, 9:978-985.
15. Lindquist, S., Duno, M., Batbayli, M., Puschmann, A., Braendgaard, H., Mardosiene, S., Svenstrup, K., Pinborg, L., Vestergaard, K., Hjermind, L., Stokholm, J., Andersen, B., Johannsen, P., Nielsen, J. 2012. Corticobasal and ataxia syndromes widen the spectrum of C9ORF72 hexanucleotide expansion disease. Clin. Genet. 9999, http://dx.doi.org/10.1111/j.1399-0004.2012.01903.x.
16. Mahoney C.J., Beck J., Rohrer J.D., Lashley T., Mok K., Shakespeare T., Yeatman T., Warrington E.K., Schott J.M., Fox N.C., Rossor M.N., Hardy J., Collinge J., Revesz T., Mead S., Warren J.D. Frontotemporal dementia with the C9ORF72 hexanucleotide repeat expansion: clinical, neuroanatomical and neuropathological features. Brain 2012, 135:736-750.
17. Majounie E., Abramzon Y., Renton A.E., Perry R., Bassett S.S., Pletnikova O., Troncoso J.C., Hardy J., Singleton A.B., Traynor B.J. Repeat expansion in C9ORF72 in Alzheimer's disease. N. Engl. J. Med. 2012, 366:283-284.
18. Majounie E., Renton A.E., Mok K., Dopper E.G., Waite A., Rollinson S., Chio A., Restagno G., Nicolaou N., Simon-Sanchez J., van Swieten J.C., Abramzon Y., Johnson J.O., Sendtner M., Pamphlett R., Orrell R.W., Mead S., Sidle K.C., Houlden H., Rohrer J.D., Morrison K.E., Pall H., Talbot K., Ansorge O., Hernandez D.G., Arepalli S., Sabatelli M., Mora G., Corbo M., Giannini F., Calvo A., Englund E., Borghero G., Floris G.L., Remes A.M., Laaksovirta H., McCluskey L., Trojanowski J.Q., Van Deerlin V.M., Schellenberg G.D., Nalls M.A., Drory V.E., Lu C.S., Yeh T.H., Ishiura H., Takahashi Y., Tsuji S., Le Ber I., Brice A., Drepper C., Williams N., Kirby J., Shaw P., Hardy J., Tienari P.J., Heutink P., Morris H.R., Pickering-Brown S., Traynor B.J. Frequency of the C9orf72 hexanucleotide repeat expansion in patients with amyotrophic lateral sclerosis and frontotemporal dementia: a cross-sectional study. Lancet Neurol. 2012, 11:323-330.
19. McKhann G., Drachman D., Folstein M., Katzman R., Price D., Stadlan E.M. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 1984, 34:939-944.
20. Murray M.E., DeJesus-Hernandez M., Rutherford N.J., Baker M., Duara R., Graff-Radford N.R., Wszolek Z.K., Ferman T.J., Josephs K.A., Boylan K.B., Rademakers R., Dickson D.W. Clinical and neuropathologic heterogeneity of c9FTD/ALS associated with hexanucleotide repeat expansion in C9ORF72. Acta Neuropathol. 2011, 122:673-690.
21. Petersen R.C. Mild cognitive impairment as a diagnostic entity. J. Intern. Med. 2004, 256:183-194.
22. Rademakers R., Dermaut B., Peeters K., Cruts M., Heutink P., Goate A., Van Broeckhoven C. Tau (MAPT) mutation Arg406Trp presenting clinically with Alzheimer disease does not share a common founder in Western Europe. Hum. Mutat. 2003, 22:409-411.
23. Renton A.E., Majounie E., Waite A., Simon-Sanchez J., Rollinson S., Gibbs J.R., Schymick J.C., Laaksovirta H., van Swieten J.C., Myllykangas L., Kalimo H., Paetau A., Abramzon Y., Remes A.M., Kaganovich A., Scholz S.W., Duckworth J., Ding J., Harmer D.W., Hernandez D.G., Johnson J.O., Mok K., Ryten M., Trabzuni D., Guerreiro R.J., Orrell R.W., Neal J., Murray A., Pearson J., Jansen I.E., Sondervan D., Seelaar H., Blake D., Young K., Halliwell N., Callister J.B., Toulson G., Richardson A., Gerhard A., Snowden J., Mann D., Neary D., Nalls M.A., Peuralinna T., Jansson L., Isoviita V.M., Kaivorinne A.L., Holtta-Vuori M., Ikonen E., Sulkava R., Benatar M., Wuu J., Chio A., Restagno G., Borghero G., Sabatelli M., Heckerman D., Rogaeva E., Zinman L., Rothstein J.D., Sendtner M., Drepper C., Eichler E.E., Alkan C., Abdullaev Z., Pack S.D., Dutra A., Pak E., Hardy J., Singleton A., Williams N.M., Heutink P., Pickering-Brown S., Morris H.R., Tienari P.J., Traynor B.J. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 2011, 72:257-268.
24. Rollinson S., Halliwell N., Young K., Callister J.B., Toulson G., Gibbons L., Davidson Y.S., Robinson A.C., Gerhard A., Richardson A., Neary D., Snowden J., Mann D.M., Pickering-Brown S.M. Analysis of the hexanucleotide repeat in C9ORF72 in Alzheimer's disease. Neurobiol. Aging 2012, 33:1846. e5-6.
25. Satoh J.I., Tabunoki H., Ishida T., Saito Y., Arima K. Dystrophic neurites express C9orf72 in Alzheimer's disease brains. Alzheimers Res. Ther. 2012, 4:33.
26. Shatunov A., Mok K., Newhouse S., Weale M.E., Smith B., Vance C., Johnson L., Veldink J.H., van Es M.A., van den Berg L.H., Robberecht W., Van D.P., Hardiman O., Farmer A.E., Lewis C.M., Butler A.W., Abel O., Andersen P.M., Fogh I., Silani V., Chio A., Traynor B.J., Melki J., Meininger V., Landers J.E., McGuffin P., Glass J.D., Pall H., Leigh P.N., Hardy J., Brown R.H., Powell J.F., Orrell R.W., Morrison K.E., Shaw P.J., Shaw C.E., Al-Chalabi A. Chromosome 9p21 in sporadic amyotrophic lateral sclerosis in the UK and seven other countries: a genome-wide association study. Lancet Neurol. 2010, 9:986-994.
27. Snowden J.S., Rollinson S., Thompson J.C., Harris J.M., Stopford C.L., Richardson A.M., Jones M., Gerhard A., Davidson Y.S., Robinson A., Gibbons L., Hu Q., DuPlessis D., Neary D., Mann D.M., Pickering-Brown S.M. Distinct clinical and pathological characteristics of frontotemporal dementia associated with C9ORF72 mutations. Brain 2012, 135:693-708.
28. Stewart H., Rutherford N.J., Briemberg H., Krieger C., Cashman N., Fabros M., Baker M., Fok A., DeJesus-Hernandez M., Eisen A., Rademakers R., Mackenzie I.R. Clinical and pathological features of amyotrophic lateral sclerosis caused by mutation in the C9ORF72 gene on chromosome 9p. Acta Neuropathol. 2012, 123:409-417.
29. van der Zee, J., Gijselinck, I., Dillen, L., Van Langenhove, T., Theuns, J., Engelborghs, S., Philtjens, S., Vandenbulcke, M., Sleegers, K., Sieben, A., Baumer, V., Maes, G., Corsmit, E., Borroni, B., Padovani, A., Archetti, S., Perneczky, R., Diehl-Schmid, J., de, M.A., Miltenberger-Miltenyi, G., Pereira, S., Pimentel, J., Nacmias, B., Bagnoli, S., Sorbi, S., Graff, C., Chiang, H.H., Westerlund, M., Sanchez-Valle, R., Llado, A., Gelpi, E., Santana, I., Almeida, M.R., Santiago, B., Frisoni, G., Zanetti, O., Bonvicini, C., Synofzik, M., Maetzler, W., vom Hagen, J.M., Schols, L., Heneka, M.T., Jessen, F., Matej, R., Parobkova, E., Kovacs, G.G., Strobel, T., Sarafov, S., Tournev, I., Jordanova, A., Danek, A., Arzberger, T., Fabrizi, G.M., Testi, S., Salmon, E., Santens, P., Martin, J.J., Cras, P., Vandenberghe, R., De Deyn, P.P., Cruts, M., Van Broeckhoven C. 2012. A Pan-European study of the C9orf72 Repeat Associated with FTLD: Geographic Prevalence, Genomic Instability and Intermediate Repeats. Hum. Mutat, http://dx.doi.org/10.1002/humu.22244.
30. van Es M.A., Veldink J.H., Saris C.G., Blauw H.M., van Vught P.W., Birve A., Lemmens R., Schelhaas H.J., Groen E.J., Huisman M.H., van der Kooi A.J., de V.M., Dahlberg C., Estrada K., Rivadeneira F., Hofman A., Zwarts M.J., van Doormaal P.T., Rujescu D., Strengman E., Giegling I., Muglia P., Tomik B., Slowik A., Uitterlinden A.G., Hendrich C., Waibel S., Meyer T., Ludolph A.C., Glass J.D., Purcell S., Cichon S., Nothen M.M., Wichmann H.E., Schreiber S., Vermeulen S.H., Kiemeney L.A., Wokke J.H., Cronin S., McLaughlin R.L., Hardiman O., Fumoto K., Pasterkamp R.J., Meininger V., Melki J., Leigh P.N., Shaw C.E., Landers J.E., Al-Chalabi A., Brown R.H., Robberecht W., Andersen P.M., Ophoff R.A., van den Berg L.H. Genome-wide association study identifies 19p13.3 (UNC13A) and 9p21.2 as susceptibility loci for sporadic amyotrophic lateral sclerosis. Nat. Genet. 2009, 41:1083-1087.
31. Wallon D., Rovelet-Lecrux A., Deramecourt V., Pariente J., Auriacombe S., Le Ber I., Schraen S., Pasquier F., Campion D., Hannequin D. Definite behavioral variant of frontotemporal dementia with C9ORF72 expansions despite positive Alzheimer's disease cerebrospinal fluid biomarkers. J. Alzheimers Dis. 2012, 32:19-22.
32. Weckx S., Del Favero J., Rademakers R., Claes L., Cruts M., De Jonghe P., Van Broeckhoven C., De Rijk P. novoSNP, a novel computational tool for sequence variation discovery. Genome Res. 2005, 15:436-442.
33. Xi Z., Zinman L., Grinberg Y., Moreno D., Sato C., Bilbao J.M., Ghani M., Hernandez I., Ruiz A., Boada M., Moron F.J., Lang A.E., Marras C., Bruni A., Colao R., Maletta R.G., Puccio G., Rainero I., Pinessi L., Galimberti D., Morrison K.E., Moorby C., Stockton J.D., Masellis M., Black S.E., Hazrati L.N., Liang Y., van Haersma de W.J., Fornazzari L., Villagra R., Rojas-Garcia R., Clarimon J., Mayeux R., Robertson J., St George-Hyslop P., Rogaeva E. Investigation of C9orf72 in 4 Neurodegenerative Disorders. Arch. Neurol. 2012, 69:1583-1590.