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The finding that a GGGGCC (G4C2) hexanucleotide repeat expansion in the chromosome 9 ORF 72 (C9ORF72) gene is a common cause of amyotrophic lateral sclerosis (ALS) and frontotemporal dementia (FTD) links ALS/FTD to a large group of unstable microsatellite diseases. Previously, we showed that microsatellite expansion mutations can be bidirectionally transcribed and that these mutations express unexpected proteins by a unique mechanism, repeat-associated non-ATG (RAN) translation. In this study, we show that C9ORF72 antisense transcripts are elevated in the brains of C9ORF72 expansion-positive [C9(+)] patients, and antisense GGCCCC (G2C4) repeat-expansion RNAs accumulate in nuclear foci in brain. Additionally, sense and antisense foci accumulate in blood and are potential biomarkers of the disease. Furthermore, we show that RAN translation occurs from both sense and antisense expansion transcripts, resulting in the expression of six RAN proteins (antisense: Pro-Arg, Pro-Ala, Gly-Pro; and sense: Gly-Ala, Gly-Arg, Gly-Pro).

These proteins accumulate in cytoplasmic aggregates in affected brain regions, including the frontal and motor cortex, hippocampus, and spinal cord neurons, with some brain regions showing dramatic RAN protein accumulation and clustering. The finding that unique antisense G2C4 RNA foci and three unique antisense RAN proteins accumulate in patient tissues indicates that bidirectional transcription of expanded alleles is a fundamental pathologic feature of C9ORF72 ALS/FTD. Additionally, these findings suggest the need to test therapeutic strategies that target both sense and antisense RNAs and RAN proteins in C9ORF72 ALS/FTD, and to more broadly consider the role of antisense expression and RAN translation across microsatellite expansion diseases.

G 2C 4 antisense transcripts accumulate as RNA foci in C9ORF72 patient tissues. ( A) Schematic diagram of C9ORF72 gene and antisense transcripts and relative location of primers for strand-specific RT-PCR and RACE primers. ( B) Strand-specific RT-PCR of sense (S) and antisense (AS) transcripts (across intron 1b and exon 1a) from FCX of C9(+) and C9(−) ALS patients. ( C) Strand-specific qRT-PCR showing elevated antisense mRNA in C9(+) compared with C9(−) ALS patients and a healthy control (HC). ( D) FISH with G 4C 2-Cy3 probe showing G 2C 4 antisense RNA foci (red) in C9(+)FCX and PBLs which are absent in C9(−) cases.

Nuclear foci in FCX are indicated by arrowheads. In vitro evidence for RAN translation of antisense G 2C 4 expansion and dual immunological detection strategy. ( A) Diagram of putative proteins translated from sense and antisense transcripts. Sequences highlighted in red were used to generate antibodies.

CT, C-terminal; f1–3, reading frames 1–3; *, stop codon. ( B) Abbreviated example of validation of α-PA AS rabbit polyclonal antibody.

Immunoblots ( Lower Left) and IF staining ( Lower Right) of HEK293T cells transfected with Flag-PA AS construct ( Upper) and probed with α-Flag and α-PA AS antibodies. S4 and S5 for additional controls and validation of eight additional antibodies generated against RAN repeat motifs and CT regions. ( C) Immunoblots ( Lower Left) and IF staining ( Lower Right) of HEK293T cells 48 h posttransfection with the AS-(G 2C 4) EXP-3T construct ( Upper). PR AS and GP AS expansion proteins were detected by Western blot and PA AS, PR AS and GP AS proteins were detected by IF in transfected cells. In vivo evidence for RAN-translation of the G 2C 4 AS repeat and toxicity studies. ( A) Dot blots containing frontal cortex lysates from four different C9(−) and four different C9(+) ALS/FTD patients were probed with α-PA AS, α-PA-CT AS, α-PR AS, and α-PR-CT AS antibodies. Results show evidence of RAN protein accumulation with all four antibodies in two of four C9(+) samples and weaker positive staining in one sample with α-PA AS.