Comprehensive genotyping of the C9orf72 hexanucleotide repeat region in 2095 ALS samples from the NINDS collection using a two-mode, long-read PCR assay

References

• 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.
   PubMed Web of Science ®Google Scholar
• Beck J, Poulter M, Hensman D, Rohrer JD, Mahoney CJ, Adamson G, et al. Large C9orf72 hexanucleotide repeat expansions are seen in multiple neurodegenerative syndromes and are more frequent than expected in the UK population. Am J Hum Genet. 2013;92:345–53.
   PubMed Web of Science ®Google Scholar
• Benussi L, Rossi G, Glionna M, Tonoli E, Piccoli E, Fostinelli S, et al. C9ORF72 hexanucleotide repeat number in frontotemporal lobar degeneration: a genotype–phenotype correlation study. J Alzheimer's Dis: JAD. 2015;45:319.
   PubMed Web of Science ®Google Scholar
• Majounie E, Renton AE, Mok K, Dopper EG, Waite A, Rollinson S, et al. Frequency of the C9orf72 hexanucleotide repeat expansion in patients with amyotrophic lateral sclerosis and frontotemporal dementia: a cross-sectional study. Lancet Neurol. 2012;2012:170–30.
   Google Scholar
• van der Zee J, Gijselinck I, Dillen L, Van Langenhove T, Theuns J, Engelborghs S, et al. A pan-European study of the C9orf72 repeat associated with FTLD: geographic prevalence, genomic instability, and intermediate repeats. Hum Mutat. 2013;34:363–73.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Zhang M, Tartaglia MC, Moreno D, Sato C, McKeever P, Weichert A, et al. DNA methylation age-acceleration is associated with disease duration and age at onset in C9orf72 patients. Acta Neuropathol. 2017;134:271–9.
   PubMed Web of Science ®Google Scholar
• Akimoto C, Volk AE, van Blitterswijk M, Van den Broeck M, Leblond CS, Lumbroso S, et al. A blinded international study on the reliability of genetic testing for GGGGCC-repeat expansions in C9orf72 reveals marked differences in results among 14 laboratories. J Med Genet. 2014;51:419–24.
   PubMed Web of Science ®Google Scholar
• Rollinson S, Bennion Callister J, Young K, Ryan SJ, Druyeh R, Rohrer JD, et al. Small deletion in C9orf72 hides a proportion of expansion carriers in FTLD. Neurobiol Aging. 2015;36:1601 e1–5.
   Web of Science ®Google Scholar
• Nordin A, Akimoto C, Wuolikainen A, Alstermark H, Forsberg K, Baumann P, et al. Sequence variations in C9orf72 downstream of the hexanucleotide repeat region and its effect on repeat-primed PCR interpretation: a large multinational screening study. Amyotroph Lat Scler Frontotemp Degener. 2017;18:256–64.
   PubMed Web of Science ®Google Scholar
• Rutherford NJ, DeJesus-Hernandez M, Baker MC, Kryston TB, Brown PE, Lomen-Hoerth C, et al. C9ORF72 hexanucleotide repeat expansions in patients with ALS from the Coriell Cell Repository. Neurology. 2012;79:482–3.
   PubMed Web of Science ®Google Scholar
• Theuns J, Verstraeten A, Sleegers K, Wauters E, Gijselinck I, Smolders S, et al. Global investigation and meta-analysis of the C9orf72 (G4C2)n repeat in Parkinson disease. Neurology. 2014;83:1906–13.
   PubMed Web of Science ®Google Scholar
• Filipovic-Sadic S, Sah S, Chen L, Krosting J, Sekinger E, Zhang W, et al. A novel FMR1 PCR method for the routine detection of low abundance expanded alleles and full mutations in fragile X syndrome. Clin Chem. 2010;56:399–408.
   PubMed Web of Science ®Google Scholar
• Chen L, Hadd A, Sah S, Filipovic-Sadic S, Krosting J, Sekinger E, et al. An information-rich CGG repeat primed PCR that detects the full range of fragile X expanded alleles and minimizes the need for southern blot analysis. J Mol Diagnost: JMD. 2010;12:589–600.
   PubMed Web of Science ®Google Scholar
• Biasiotto G, Archetti S, Di Lorenzo D, Merola F, Paiardi G, Borroni B, et al. A PCR-based protocol to accurately size C9orf72 intermediate-length alleles. Mol Cell Probes. 2017;32:60–4.
   PubMed Web of Science ®Google Scholar
• Cleary EM, Pal S, Azam T, Moore DJ, Swingler R, Gorrie G, et al. Improved PCR based methods for detecting C9orf72 hexanucleotide repeat expansions. Mol Cell Probes. 2016;30:218–24.
   PubMed Web of Science ®Google Scholar
• Yrigollen CM, Durbin-Johnson B, Gane L, Nelson DL, Hagerman R, Hagerman PJ, et al. AGG interruptions within the maternal FMR1 gene reduce the risk of offspring with fragile X syndrome. Genet Med. 2012;14:729–36.
   PubMed Web of Science ®Google Scholar
• Ohshima K, Sakamoto N, Labuda M, Poirier J, Moseley ML, Montermini L, et al. A nonpathogenic GAAGGA repeat in the Friedreich gene: implications for pathogenesis. Neurology. 1999;53:1854–7.
   PubMed Web of Science ®Google Scholar
• Musova Z, Mazanec R, Krepelova A, Ehler E, Vales J, Jaklova R, et al. Highly unstable sequence interruptions of the CTG repeat in the myotonic dystrophy gene. Am J Med Genet. 2009;149A:1365–74.
   PubMed Web of Science ®Google Scholar
• Bachinski LL, Czernuszewicz T, Ramagli LS, Suominen T, Shriver MD, Udd B, et al. Premutation allele pool in myotonic dystrophy type 2. Neurology. 2009;72:490–7.
   PubMed Web of Science ®Google Scholar
• Bean L, Bayrak-Toydemir P. American College of Medical Genetics and Genomics Standards and Guidelines for Clinical Genetics Laboratories, 2014 edition: technical standards and guidelines for Huntington disease. Genet Med. 2014;16:e2.
   PubMedGoogle Scholar
• Xi Z, van Blitterswijk M, Zhang M, McGoldrick P, McLean JR, Yunusova Y, et al. Jump from pre-mutation to pathologic expansion in C9orf72. Am J Hum Genet. 2015;96:962–70.
   PubMed Web of Science ®Google Scholar
• Dols-Icardo O, Garcia-Redondo A, Rojas-Garcia R, Sanchez-Valle R, Noguera A, Gomez-Tortosa E, et al. Characterization of the repeat expansion size in C9orf72 in amyotrophic lateral sclerosis and frontotemporal dementia. Hum Mol Genet. 2014;23:749–54.
   PubMed Web of Science ®Google Scholar
• Dobson-Stone C, Hallupp M, Loy CT, Thompson EM, Haan E, Sue CM, et al. C9ORF72 repeat expansion in Australian and Spanish frontotemporal dementia patients. PLoS One. 2013;8:e56899.
   PubMed Web of Science ®Google Scholar
• Xi Z, Zinman L, Grinberg Y, Moreno D, Sato C, Bilbao JM, et al. Investigation of c9orf72 in 4 neurodegenerative disorders. Arch Neurol. 2012;69:1583–90.
   PubMedGoogle Scholar
• Suh E, Grando K, Van Deerlin VM. Validation of a long-read PCR assay for sensitive detection and sizing of C9orf72 hexanucleotide repeat expansions. J Mol Diagn. 2018;pii:S1525-1578(18)30116–8. doi: 10.1016/j.jmoldx.2018.07.001.
   Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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 Transl Med. 2013;5:208ra149.
   PubMed Web of Science ®Google Scholar
• Jiang J, Zhu Q, Gendron TF, Saberi S, McAlonis-Downes M, Seelman A, et al. Gain of toxicity from ALS/FTD-linked repeat expansions in C9ORF72 is alleviated by antisense oligonucleotides targeting GGGGCC-containing RNAs. Neuron. 2016;90:535–50.
   PubMed Web of Science ®Google Scholar
• Yeo EH, Goh WL, Chow SC. The aminopeptidase inhibitor, z-L-CMK, is toxic and induces cell death in Jurkat T cells through oxidative stress. Toxicol Mech Methods. 2018;28:157–166.
   PubMed Web of Science ®Google Scholar
• Pinto BS, Saxena T, Oliveira R, Mendez-Gomez HR, Cleary JD, Denes LT, et al. Impeding transcription of expanded microsatellite repeats by deactivated Cas9. Mol Cell. 2017;68:479–90.e5.
   PubMed Web of Science ®Google Scholar