Hypermethylation of the CpG-island near the C9orf72 G4C2-repeat expansion in FTLD patients

Human Molecular Genetics

Volumn 23, Issue 21, 2014, Pages 5630-5637

  Xi, Zhengrui ^a   Rainero, Innocenzo ^b   Rubino, Elisa ^b   Pinessi, Lorenzo ^b   Bruni, Amalia C ^c   Maletta, Raffaele G ^c   Nacmias, Benedetta ^d   Sorbi, Sandro ^d   Galimberti, Daniela ^e   Surace, Ezequiel I ^f   Zheng, Yonglan ^g   Moreno, Danielle ^a   Sato, Christine ^a   Liang, Yan ^a   Zhou, Ye ^a   Robertson, Janice ^a   Zinman, Lorne ^h,i   Tartaglia, Maria Carmela ^a,i   St George Hyslop, Peter ^a,i,j   Rogaeva, Ekaterina ^a,i  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TURIN   (Italy)

^c Department of Neonatology   (Italy)

^d UNIVERSITY OF FLORENCE   (Italy)

^e UNIVERSITY OF MILAN   (Italy)

^f Instituto de Investigaciones Neurologicas Raul Carrera   (Argentina)

^g UNIVERSITY OF CHICAGO   (United States)

^h SUNNYBROOK RESEARCH INSTITUTE   (Canada)

ⁱ UNIVERSITY OF TORONTO   (Canada)

^j UNIVERSITY OF CAMBRIDGE   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ALLELE; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BLOOD; BRAIN; CLONE; CONTROLLED STUDY; COPY NUMBER VARIATION; CPG ISLAND; DNA METHYLATION; DNA MODIFICATION; DNA SEQUENCE; DNA STRAND; EPIGENETICS; FEMALE; FRONTOTEMPORAL DEMENTIA; GENOTYPE; HETEROZYGOTE; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; NUCLEOTIDE REPEAT; PHENOTYPE; POLYMERASE CHAIN REACTION; SPINAL CORD; AGED; GENETICS; INFORMATION PROCESSING; MIDDLE AGED; ONSET AGE;

C9ORF72 PROTEIN, HUMAN; PROTEIN; REPETITIVE DNA;

AGE OF ONSET; AGED; AMYOTROPHIC LATERAL SCLEROSIS; CPG ISLANDS; DATASETS AS TOPIC; DNA METHYLATION; DNA REPEAT EXPANSION; FEMALE; FRONTOTEMPORAL LOBAR DEGENERATION; GENOTYPE; HUMANS; MALE; MIDDLE AGED; PROTEINS; SEQUENCE ANALYSIS, DNA;

EID: 84911382953     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu279     Document Type: Article

References (41)

1. Cruts, M., Gijselinck, I., Van Langenhove, T., van der Zee, J. and Van Broeckhoven, C. (2013) Current insights into the C9orf72 repeat expansion diseases of the FTLD/ALS spectrum. Trends Neurosci., 36, 450-459.
2. Mackenzie, I.R., Rademakers, R. and Neumann,M. (2010) TDP-43 andFUS in amyotrophic lateral sclerosis and frontotemporal dementia. Lancet Neurol., 9, 995-1007.
3. Rademakers, R., Neumann, M. and Mackenzie, I.R. (2012) Advances in understanding the molecular basis of frontotemporal dementia. Nat. Rev. Neurol., 8, 423-434.
4. Van Langenhove, T., van der Zee, J. and Van Broeckhoven, C. (2012) The molecular basis of the frontotemporal lobar degeneration-amyotrophic lateral sclerosis spectrum. Ann. Med., 44, 817-828.
5. Neary, D., Snowden, J.S., Gustafson, L., Passant, U., Stuss, D., Black, S., Freedman, M., Kertesz, A., Robert, P.H., Albert, M. et al. (1998) Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology, 51, 1546-1554.
6. Brooks, B.R., Miller, R.G., Swash, M. and Munsat, T.L. (2000) El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. Other Motor Neuron Disord., 1, 293-299.
7. Hardy, J. and Rogaeva, E. (2013) Motor neuron disease and frontotemporal dementia: sometimes related, sometimes not. Exp. Neurol. [Epub ahead of print].
8. 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. et al. (2011) Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron, 72, 245-256.
9. 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. et al. (2011) A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron, 72, 257-268.
10. Gijselinck, I.,VanLangenhove, T., van der Zee, J., Sleegers, K., Philtjens, S., Kleinberger, G., Janssens, J., Bettens, K., Van Cauwenberghe, C., Pereson, S. et al. (2012) 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., 11, 54-65.
11. Mori, K., Weng, S.M., Arzberger, T., May, S., Rentzsch, K., Kremmer, E., Schmid, B., Kretzschmar, H.A., Cruts, M., Van Broeckhoven, C. et al. (2013) The C9orf72 GGGGCC repeat is translated into aggregating dipeptide-repeat proteins in FTLD/ALS. Science, 339, 1335-1338.
12. Ash, P.E., Bieniek, K.F., Gendron, T.F., Caulfield, T., Lin, W.L., Dejesus-Hernandez, M., van Blitterswijk, M.M., Jansen-West, K., Paul, J.W. 3rd, Rademakers, R. et al. (2013) Unconventional translation of C9ORF72 GGGGCC expansion generates insoluble polypeptides specific to c9FTD/ALS. Neuron, 77, 639-646.
13. Levine, T.P., Daniels, R.D., Gatta, A.T., Wong, L.H. and Hayes, M.J. (2013) The product of C9orf72, a gene strongly implicated in neurodegeneration, is structurally related to DENN Rab-GEFs. Bioinformatics, 29, 499-503.
14. Zhang, D., Iyer, L.M., He, F. and Aravind, L. (2012) Discovery of novel DENN proteins: implications for the evolution of eukaryotic intracellular membrane structures and human disease. Front Genet., 3, 283.
15. Xi, Z., Zinman, L., Moreno, D., Schymick, J., Liang, Y., Sato, C., Zheng, Y., Ghani, M., Dib, S., Keith, J. et al. (2013) Hypermethylation of theCpGIsland Near the GC Repeat in ALS with a C9orf72 Expansion. Am. J. Hum. Genet., 92, 981-989.
16. Al-Mahdawi, S., Pinto,R.M., Ismail,O.,Varshney,D.,Lymperi, S., Sandi,C., Trabzuni, D. and Pook,M. (2008) The Friedreich ataxia GAA repeat expansion mutation induces comparable epigenetic changes in human and transgenic mouse brain and heart tissues. Hum. Mol. Genet., 17, 735-746.
17. Greene, E., Mahishi, L., Entezam, A., Kumari, D. and Usdin, K. (2007) Repeat-induced epigenetic changes in intron 1 of the frataxin gene and its consequences in Friedreich ataxia. Nucleic Acids Res., 35, 3383-3390.
18. Evans-Galea, M.V., Carrodus, N., Rowley, S.M., Corben, L.A., Tai, G., Saffery, R., Galati, J.C., Wong, N.C., Craig, J.M., Lynch, D.R. et al. (2012) FXN methylation predicts expression and clinical outcome in Friedreich ataxia. Ann. Neurol., 71, 487-497.
19. Sutcliffe, J.S., Nelson, D.L., Zhang, F., Pieretti, M., Caskey, C.T., Saxe, D. and Warren, S.T. (1992)DNAmethylation represses FMR-1transcription in fragile X syndrome. Hum. Mol. Genet., 1, 397-400.
20. Pieretti, M., Zhang, F.P., Fu, Y.H., Warren, S.T., Oostra, B.A., Caskey, C.T. and Nelson, D.L. (1991) Absence of expression of the FMR-1 gene in fragile X syndrome. Cell, 66, 817-822.
21. Bell, M.V., Hirst, M.C., Nakahori, Y., MacKinnon, R.N., Roche, A., Flint, T.J., Jacobs, P.A., Tommerup, N., Tranebjaerg, L., Froster-Iskenius, U. et al. (1991) Physical mapping across the fragile X: hypermethylation and clinical expression of the fragile X syndrome. Cell, 64, 861-866.
22. Klesert, T.R., Otten, A.D., Bird, T.D. and Tapscott, S.J. (1997) Trinucleotide repeat expansion at the myotonic dystrophy locus reduces expression of DMAHP. Nat. Genet., 16, 402-406.
23. Thornton, C.A., Wymer, J.P., Simmons, Z., McClain, C. and Moxley, R.T. 3rd (1997) Expansion of the myotonic dystrophy CTG repeat reduces expression of the flanking DMAHP gene. Nat. Genet., 16, 407-409.
24. Korade-Mirnics, Z., Tarleton, J., Servidei, S., Casey, R.R., Gennarelli, M., Pegoraro, E., Angelini, C. and Hoffman, E.P. (1999) Myotonic dystrophy: tissue-specific effect of somatic CTG expansions on allele-specific DMAHP/SIX5 expression. Hum. Mol. Genet., 8, 1017-1023.
25. Ciura, S., Lattante, S., Le Ber, I., Latouche, M., Tostivint, H., Brice, A. and Kabashi, E. (2013) Loss of function of C9orf72 causes motor deficits in a zebrafish model of Amyotrophic Lateral Sclerosis. Ann. Neurol., 74, 180-187.
26. Therrien, M., Rouleau, G.A., Dion, P.A. and Parker, J.A. (2013) Deletion of C9ORF72 results in motor neuron degeneration and stress sensitivity in C. elegans. PLoS One, 8, e83450.
27. Xi, Z., Zinman, L., Grinberg, Y., Moreno, D., Sato, C., Bilbao, J.M., Ghani, M., Hernandez, I., Ruiz, A., Boada, M. et al. (2012) Investigation of C9orf72 in 4 neurodegenerative disorders. Arch. Neurol., 69, 1583-1590.
28. Arand, J., Spieler, D., Karius, T., Branco, M.R., Meilinger, D., Meissner, A., Jenuwein, T., Xu, G., Leonhardt, H., Wolf, V. et al. (2012) In vivo control of CpG and non-CpG DNA methylation by DNA methyltransferases. PLoS Genet., 8, e1002750.
29. Laird, C.D., Pleasant, N.D., Clark, A.D., Sneeden, J.L., Hassan, K.M., Manley, N.C., Vary, J.C. Jr, Morgan, T., Hansen, R.S. and Stoger, R. (2004) Hairpin-bisulfite PCR: assessing epigenetic methylation patterns on complementary strands of individualDNAmolecules. Proc. Natl. Acad. Sci. U.S.A., 101, 204-209.
30. Ehrlich, M. and Lacey, M. (2013) DNA hypomethylation and hemimethylation in cancer. Adv. Exp. Med. Biol., 754, 31-56.
31. Belzil, V.V., Bauer, P.O., Gendron, T.F., Murray, M.E., Dickson, D. and Petrucelli, L. (2014) Characterization of DNA hypermethylation in the cerebellum of c9FTD/ALS patients. Brain Res. [Epub ahead of print].
32. Castaldo, I., Pinelli, M., Monticelli, A., Acquaviva, F., Giacchetti, M., Filla, A., Sacchetti, S., Keller, S., Avvedimento, V.E., Chiariotti, L. et al. (2008) DNA methylation in intron 1 of the frataxin gene is related to GAA repeat length and age of onset in Friedreich ataxia patients. J. Med. Genet., 45, 808-812.
33. Dols-Icardo, O., Garcia-Redondo, A., Rojas-Garcia, R., Sanchez-Valle, R., Noguera, A., Gomez-Tortosa, E., Pastor, P., Hernandez, I., Esteban-Perez, J., Suarez-Calvet, M. et al. (2013) Characterization of the repeat expansion size in C9orf72 in amyotrophic lateral sclerosis and frontotemporal dementia. Hum. Mol. Genet., 23, 749-754.
34. van Blitterswijk, M., Dejesus-Hernandez, M., Niemantsverdriet, E., Murray, M.E., Heckman, M.G., Diehl, N.N., Brown, P.H., Baker, M.C., Finch, N.A., Bauer, P.O. et al. (2013) Association between repeat sizes and clinical and pathological characteristics in carriers of C9ORF72 repeat expansions (Xpansize-72): a cross-sectional cohort study. Lancet Neurol., 12, 978-988.
35. Fratta, P., Poulter, M., Lashley, T., Rohrer, J.D., Polke, J.M., Beck, J., Ryan, N., Hensman, D., Mizielinska, S., Waite, A.J. et al. (2013)Homozygosity for the C9orf72 GGGGCC repeat expansion in frontotemporal dementia. Acta Neuropathol., 126, 401-409.
36. Cooper-Knock, J., Higginbottom, A., Connor-Robson, N., Bayatti, N., Bury, J.J., Kirby, J., Ninkina, N., Buchman, V.L. and Shaw, P.J. (2013) C9ORF72 transcription in a frontotemporal dementia case with two expanded alleles. Neurology, 81, 1719-1721.
37. Donnelly, C.J., Zhang, P.W., Pham, J.T., Heusler, A.R., Mistry, N.A., Vidensky, S., Daley, E.L., Poth, E.M., Hoover, B., Fines, D.M. et al. (2013) RNA Toxicity from the ALS/FTD C9ORF72 Expansion Is Mitigated by Antisense Intervention. Neuron, 80, 415-428.
38. Belzil, V.V., Bauer, P.O., Prudencio, M., Gendron, T.F., Stetler, C.T., Yan, I.K., Pregent, L., Daughrity, L., Baker, M.C., Rademakers, R. et al. (2013) Reduced C9orf72 gene expression in c9FTD/ALS is caused by histone trimethylation, an epigenetic event detectable in blood. Acta Neuropathol., 126, 895-905.
39. Cedar, H. and Bergman, Y. (2009) Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet., 10, 295-304.
40. Fraga, M.F. and Esteller,M. (2007) Epigenetics and aging: the targets and the marks. Trends Genet., 23, 413-418.
41. [1994] Clinical and neuropathological criteria for frontotemporal dementia. The Lund and Manchester Groups. J. Neurol. Neurosurg. Psychiatry, 57, 416-418.