Isoform-specific antibodies reveal distinct subcellular localizations of C9orf72 in amyotrophic lateral sclerosis

Annals of Neurology

Volumn 78, Issue 4, 2015, Pages 568-583

  Xiao, Shangxi ^a   MacNair, Laura ^a,b   McGoldrick, Philip ^a   McKeever, Paul M ^a,b   McLean, Jesse R ^a   Zhang, Ming ^a   Keith, Julia ^b,c   Zinman, Lorne ^b,c   Rogaeva, Ekaterina ^a   Robertson, Janice ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c SUNNYBROOK RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; IMPORTIN BETA1; ISOPROTEIN; KARYOPHERIN BETA; MEMBRANE PROTEIN; NUCLEOCYTOPLASMIC TRANSPORT PROTEIN; PROTEIN ANTIBODY; PROTEIN C9ORF72; PROTEIN C9ORF72 LONG FORM; PROTEIN C9ORF72 SHORT FORM; RAN GTPASE; UNCLASSIFIED DRUG; ANTIBODY; C9ORF72 PROTEIN, HUMAN; PROTEIN;

ADULT; AGED; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL NUCLEUS MEMBRANE; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MIDDLE AGED; MOTONEURON; NERVE CELL; NONHUMAN; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PURKINJE CELL; VERY ELDERLY; WESTERN BLOTTING; AMINO ACID SEQUENCE; BIOSYNTHESIS; CEREBELLUM; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; PATHOLOGY;

AGED; AGED, 80 AND OVER; AMINO ACID SEQUENCE; AMYOTROPHIC LATERAL SCLEROSIS; ANTIBODIES; CEREBELLUM; FEMALE; HUMANS; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; MOTOR NEURONS; PROTEIN ISOFORMS; PROTEINS;

EID: 84942369240     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.24469     Document Type: Article

References (48)

1. DeJesus-Hernandez M, Mackenzie IR, Boeve BF, et al., Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 2011; 72: 245-256.
2. Renton AE, Majounie E, Waite A, et al., A Hexanucleotide Repeat Expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 2011; 72: 257-268.
3. Xi Z, Zinman L, Grinberg Y, et al., Investigation of C9orf72 in 4 neurodegenerative disorders. Arch Neurol 2012; 69: 1583.
4. Cruts M, Gijselinck I, Van Langenhove T, et al., Current insights into the C9orf72 repeat expansion diseases of the FTLD/ALS spectrum. Trends Neurosci 2013; 36: 450-459.
5. Mackenzie IR, Frick P, Neumann M,. The neuropathology associated with repeat expansions in the C9ORF72 gene. Acta Neuropathol 2014; 127: 347-357.
6. Hardy J, Rogaeva E,. Motor neuron disease and frontotemporal dementia: sometimes related, sometimes not. Exp Neurol 2014; 262: 75-83.
7. Rutherford NJ, Heckman MG, DeJesus-Hernandez M, et al., Length of normal alleles of C9orf72 GGGGCC repeat do not influence disease phenotype. Neurobiol Aging 2012; 33: 2950.e5-2950.e7.
8. Beck J, Poulter M, Hensman D, 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: 345-353.
9. Boeve BF, Boylan KB, Graff-Radford NR, et al., Characterization of frontotemporal dementia and/or amyotrophic lateral sclerosis associated with the GGGGCC repeat expansion in C9ORF72. Brain 2012; 135: 765-783.
10. Chiò A, Borghero G, Restagno G, et al., Clinical characteristics of patients with familial amyotrophic lateral sclerosis carrying the pathogenic GGGGCC hexanucleotide repeat expansion of C9ORF72. Brain 2012; 135: 784-793.
11. Cooper-Knock J, Hewitt C, Highley JR, et al., Clinico-pathological features in amyotrophic lateral sclerosis with expansions in C9ORF72. Brain 2012; 135: 751-764.
12. Hsiung GYR, DeJesus-Hernandez M, Feldman HH, et al., Clinical and pathological features of familial frontotemporal dementia caused by C9ORF72 mutation on chromosome 9p. Brain 2012; 135: 709-722.
13. Mahoney CJ, Beck J, Rohrer JD, et al., Frontotemporal dementia with the C9ORF72 hexanucleotide repeat expansion: clinical, neuroanatomical and neuropathological features. Brain 2012; 135: 736-750.
14. Murray ME, DeJesus-Hernandez M, Rutherford NJ, et al., Clinical and neuropathologic heterogeneity of c9FTD/ALS associated with hexanucleotide repeat expansion in C9ORF72. Acta Neuropathol 2011; 122: 673-690.
15. Simón-Sánchez J, Dopper EGP, Cohn-Hokke PE, et al., The clinical and pathological phenotype of C9ORF72 hexanucleotide repeat expansions. Brain 2012; 135: 723-735.
16. Snowden JS, Rollinson S, Thompson JC, et al., Distinct clinical and pathological characteristics of frontotemporal dementia associated with C9ORF72 mutations. Brain 2012; 135: 693-708.
17. Majounie E, Abramzon Y, Renton AE, et al., Repeat expansion in C9ORF72 in Alzheimer's disease. N Engl J Med 2012; 366: 283-284.
18. Lesage S, Le Ber I, Condroyer C, et al., C9orf72 repeat expansions are a rare genetic cause of parkinsonism. Brain 2013; 136: 385-391.
19. Coon EA, Daube JR, DeJesus-Hernandez M, et al., Clinical and electrophysiologic variability in amyotrophic lateral sclerosis within a kindred harboring the C9ORF72repeat expansion. Amyotroph Lateral Scler Frontotemporal Degener 2013; 14: 132-137.
20. Gendron TF, Belzil VV, Zhang YJ, Petrucelli L,. Mechanisms of toxicity in C9FTLD/ALS. Acta Neuropathol 2014; 127: 359-376.
21. Stepto A, Gallo JM, Shaw CE, Hirth F,. Modelling C9ORF72 hexanucleotide repeat expansion in amyotrophic lateral sclerosis and frontotemporal dementia. Acta Neuropathol 2013; 127: 377-389.
22. Ash PE, Bieniek KF, Gendron TF, et al., Unconventional translation of C9ORF72 GGGGCC expansion generates insoluble polypeptides specific to c9FTD/ALS. Neuron 2013; 77: 639-646.
23. Mori K, Weng SM, Arzberger T, et al., The C9orf72 GGGGCC repeat is translated into aggregating dipeptide-repeat proteins in FTLD/ALS. Science 2013; 339: 1335-1338.
24. Belzil VV, Bauer PO, Prudencio M, et al., Reduced C9orf72 gene expression in c9FTD/ALS is caused by histone trimethylation, an epigenetic event detectable in blood. Acta Neuropathol 2013; 126: 895-905.
25. Gijselinck I, Van Langenhove T, van der Zee J, 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; 11: 54-65.
26. Fratta P, Poulter M, Lashley T, et al., Homozygosity for the C9orf72 GGGGCC repeat expansion in frontotemporal dementia. Acta Neuropathol 2013; 126: 401-409.
27. Almeida S, Gascon E, Tran H, et al., Modeling key pathological features of frontotemporal dementia with C9ORF72 repeat expansion in iPSC-derived human neurons. Acta Neuropathol 2013; 126: 385-399.
28. Donnelly CJ, Zhang P-W, Pham JT, et al., RNA toxicity from the ALS/FTD C9ORF72 expansion is mitigated by antisense intervention. Neuron 2013; 80: 415-428.
29. Waite AJ, Baümer D, East S, et al., Reduced C9orf72 protein levels in frontal cortex of amyotrophic lateral sclerosis and frontotemporal degeneration brain with the C9ORF72 hexanucleotide repeat expansion. Neurobiol Aginh 2014; 35: 1779.e5-1779.e13.
30. Ciura S, Lattante S, Le Ber I, et al., Loss of function of C9orf72 causes motor deficits in a zebrafish model of amyotrophic lateral sclerosis. Ann Neurol 2013; 74: 180-187.
31. Liu EY, Russ J, Wu K, et al., C9orf72 hypermethylation protects against repeat expansion-associated pathology in ALS/FTD. Acta Neuropathol 2014; 128: 525-541.
32. Therrien M, Rouleau GA, Dion PA, Parker JA,. Deletion of C9ORF72 results in motor neuron degeneration and stress sensitivity in C. elegans. PLoS ONE 2013; 8: e83450.
33. Levine TP, Daniels RD, Gatta AT, et al., The product of C9orf72, a gene strongly implicated in neurodegeneration, is structurally related to DENN Rab-GEFs. Bioinformatics 2013; 29: 499-503.
34. Farg MA, Sundaramoorthy V, Sultana JM, et al., C9ORF72, implicated in amytrophic lateral sclerosis and frontotemporal dementia, regulates endosomal trafficking. Hum Mol Genet 2014; 23: 3579-3595.
35. Brooks BR, Miller RG, Swash M, Munsat TL,. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 2000; 1: 293-299.
36. Mackenzie IR, Arzberger T, Kremmer E, et al., Dipeptide repeat protein pathology in C9ORF72 mutation cases: clinico-pathological correlations. Acta Neuropathol 2013; 126: 859-879.
37. Haeusler AR, Donnelly CJ, Periz G, et al., C9orf72 nucleotide repeat structures initiate molecular cascades of disease. Nature 2014; 507: 195-200.
38. Xi Z, Rainero I, Rubino E, et al., Hypermethylation of the CpG-island near the C9orf72 G4C2-repeat expansion in FTLD patients. Hum Mol Genet 2014; 23: 5630-5637.
39. Xi Z, Zinman L, Moreno D, et al., Hypermethylation of the CpG island near the G4C2 repeat in ALS with a C9orf72 expansion. Am J Hum Genet 2013; 92: 981-989.
40. Belzil VV, Bauer PO, Gendron TF, et al., Characterization of DNA hypermethylation in the cerebellum of c9FTD/ALS patients. Brain Res 2014; 1584: 15-21.
41. Stewart H, Rutherford NJ, Briemberg H, et al., Clinical and pathological features of amyotrophic lateral sclerosis caused by mutation in the C9ORF72 gene on chromosome 9p. Acta Neuropathol 2012; 123: 409-417.
42. Satoh JI, Tabunoki H, Ishida T, et al., Dystrophic neurites express C9orf72 in Alzheimer's disease brains. Alzheimers Res Ther 2012; 4: 33.
43. Ito D, Suzuki N,. Conjoint pathologic cascades mediated by ALS/FTLD-U linked RNA-binding proteins TDP-43 and FUS. Neurology 2011; 77: 1636-1643.
44. Nishimura AL, Zupunski V, Troakes C, et al., Nuclear import impairment causes cytoplasmic trans-activation response DNA-binding protein accumulation and is associated with frontotemporal lobar degeneration. Brain 2010; 133: 1763-1771.
45. Melchior F, Guan T, Paschal B, Gerace L,. Biochemical and structural analysis of nuclear protein import. Cold Spring Harb Symp Quant Biol 1995; 60: 707-716.
46. Ward ME, Taubes A, Chen R, et al., Early retinal neurodegeneration and impaired Ran-mediated nuclear import of TDP-43 in progranulin-deficient FTLD. J Exp Med 2014; 211: 1937-1945.
47. Zhang J, Ito H, Wate R, et al., Altered distributions of nucleocytoplasmic transport-related proteins in the spinal cord of a mouse model of amyotrophic lateral sclerosis. Acta Neuropathol 2006; 112: 673-680.
48. Tran D, Chalhoub A, Schooley A, et al., A mutation in VAPB that causes amyotrophic lateral sclerosis also causes a nuclear envelope defect. J Cell Sci 2012; 125: 2831-2836.