Cited by 740Amyotrophic Lateral Sclerosis ResearchGenetic Neurodegenerative DiseasesAlzheimer's disease research and treatments

The DOI matches its Crossref record; 37 of the 37 references it cites were found in a registry or an index.

C9orf72 repeat expansions cause neurodegeneration in Drosophila through arginine-rich proteins

Open access

Mizielinska, Sarah, Grönke, Sebastian, Niccoli, Teresa, Ridler, Charlotte E., Clayton, Emma L., Devoy, Anny, Moens, Thomas, Norona, Frances E., Woollacott, Ione O. C., Pietrzyk, Julian, Cleverley, Karen, Nicoll, Andrew J., Pickering-Brown, Stuart, Dols, Jacqueline, Cabecinha, Melissa, Hendrich, Oliver, Fratta, Pietro, Fisher, Elizabeth M. C., Partridge, Linda, Isaacs, Adrian M.·2014·Science

DOI 10.1126/science.1256800PMC PMC4944841

Open this paper in CoChat — free account

Abstract

Dipeptide repeat peptides on the attack: Certain neurodegenerative diseases, including amyotrophic lateral sclerosis (ALS), are associated with expanded dipeptides translated from RNA transcripts of disease-associated genes (see the Perspective by West and Gitler). Kwon et al. show that the peptides encoded by the expanded repeats in the C9orf72 gene interfere with the way cells make RNA and kill cells. These effects may account for how this genetic form of ALS causes disease. Working in Drosophila , Mizielinska et al. aimed to distinguish between the effects of repeat-containing RNAs and the dipeptide repeat peptides that they encode. The findings provide evidence that dipeptide repeat proteins can cause toxicity directly. Science , this issue p. 1139 and p. 1192 ; see also p. 1118

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1126/science.1256800

Cites

37 of 37 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Expanded GGGGCC Hexanucleotide Repeat in Noncoding Region of C9ORF72 Causes Chromosome 9p-Linked FTD and ALS
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) · Neuron · doi:10.1016/j.neuron.2011.09.011 · Cited by 4,936
A Hexanucleotide Repeat Expansion in C9ORF72 Is the Cause of Chromosome 9p21-Linked ALS-FTD
Renton, A. E., Majounie, E., Waite, A., Simón-Sánchez, J., Rollinson, S., Gibbs, J. R., Schymick, J. C., Laaksovirta, H., van Swieten, J. C., Myllykangas, L., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.09.010 · Cited by 4,409
Self-citation
The C9orf72 GGGGCC Repeat Is Translated into Aggregating Dipeptide-Repeat Proteins in FTLD/ALS
Mori, K., Weng, S., Arzberger, T., May, S., Rentzsch, K., Kremmer, E., Schmid, B., Kretzschmar, H. A., Cruts, M., Broeckhoven, C. V., et al. (2013) · Science · doi:10.1126/science.1232927 · Cited by 1,248
Frequency of the C9orf72 hexanucleotide repeat expansion in patients with amyotrophic lateral sclerosis and frontotemporal dementia: a cross-sectional study
Majounie, E., Renton, A. E., Mok, K., Dopper, E. G., Waite, A., Rollinson, S., Chiò, A., Restagno, G., Nicolaou, N., Simon-Sanchez, J., et al. (2012) · The Lancet Neurology · doi:10.1016/s1474-4422(12)70043-1 · Cited by 1,210
Self-citation
Unconventional Translation of C9ORF72 GGGGCC Expansion Generates Insoluble Polypeptides Specific to c9FTD/ALS
Ash, P. E. A., Bieniek, K. F., Gendron, T. F., Caulfield, T. R., Lin, W.-L., DeJesus‐Hernandez, M., van Blitterswijk, M., Jansen‐West, K. R., Paul, J. W., Rademakers, R., et al. (2013) · Neuron · doi:10.1016/j.neuron.2013.02.004 · Cited by 1,127
GAL4 system in drosophila: A fly geneticist's swiss army knife
Duffy, J. B. (2002) · genesis · doi:10.1002/gene.10150 · Cited by 1,099
A Cross-Sectional Study
Drozdzowska, B., Pluskiewicz, W., Halaba, Z. P., Misiołek, H., & Beck, B. R. (2005) · Cited by 984
Non-ATG–initiated translation directed by microsatellite expansions
Zu, T., Gibbens, B. B., Doty, N. S., Gomes-Pereira, M., Huguet-Lachon, A., Stone, M. D., Margolis, J., Peterson, M., Markowski, T. W., Ingram, M. A. C., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1013343108 · Cited by 928
RNA Toxicity from the ALS/FTD C9ORF72 Expansion Is Mitigated by Antisense Intervention
Donnelly, C. J., Zhang, P.-W., Pham, J. T., Haeusler, A. R., Mistry, N. A., Vidensky, S., Daley, E. L., Poth, E. M., Hoover, B., Fines, D. M., et al. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.015 · Cited by 877
A conditional tissue-specific transgene expression system using inducible GAL4
Osterwalder, T., Yoon, K. S., White, B. H., & Keshishian, H. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.221303298 · Cited by 804

Flagged first, then by citations

Show all 37 references

Sorted by citations

Items 101–200 of 739

Modeling Neurodegenerative Disorders in Drosophila melanogaster
Bolus, H., Crocker, K. L., Boekhoff‐Falk, G., & Chtarbanova, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21093055 · Cited by 137
TDP ‐43 binds and transports G ‐quadruplex‐containing m RNA s into neurites for local translation
Ishiguro, A., Kimura, N., Watanabe, Y., Watanabe, S., & Ishihama, A. (2016) · Genes to Cells · doi:10.1111/gtc.12352 · Cited by 127
Genetic Convergence Brings Clarity to the Enigmatic Red Line in ALS
Cook, C. N., & Petrucelli, L. (2019) · Neuron · doi:10.1016/j.neuron.2019.02.032 · Cited by 126
Spt4 selectively regulates the expression of C9orf72 sense and antisense mutant transcripts
Kramer, N. J., Carlomagno, Y., Zhang, Y., Almeida, S., Cook, C. N., Gendron, T. F., Prudencio, M., van Blitterswijk, M., Belzil, V., Couthouis, J., et al. (2016) · Science · doi:10.1126/science.aaf7791 · Cited by 123
Linking hnRNP Function to ALS and FTD Pathology
Purice, M. D., & Taylor, J. P. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00326 · Cited by 128
Poly‐GP in cerebrospinal fluid links C9orf72‐associated dipeptide repeat expression to the asymptomatic phase of ALS/FTD
Lehmer, C., Oeckl, P., Weishaupt, J. H., Volk, A. E., Diehl‐Schmid, J., Schroeter, M. L., Lauer, M., Kornhuber, J., Levin, J., Fassbender, K., et al. (2017) · EMBO Molecular Medicine · doi:10.15252/emmm.201607486 · Cited by 118
Neuropathogenesis-on-chips for neurodegenerative diseases
Amartumur, S., Nguyen, H. M., Huynh, T., Kim, T. S., Woo, R., Oh, E., Kim, K. K., Lee, L. P., & Heo, C. (2024) · Nature Communications · doi:10.1038/s41467-024-46554-8 · Cited by 131
The Hairpin Form of r(G4C2)exp in c9ALS/FTD Is Repeat-Associated Non-ATG Translated and a Target for Bioactive Small Molecules
Wang, Z.-F., Ursu, A., Childs‐Disney, J. L., Guertler, R., Yang, W.-Y., Bernat, V., Rzuczek, S. G., Fuerst, R., Zhang, Y., Gendron, T. F., et al. (2018) · Cell chemical biology · doi:10.1016/j.chembiol.2018.10.018 · Cited by 109
RNA-binding proteins and glycoRNAs form domains on the cell surface for cell-penetrating peptide entry
Perr, J., Langen, A., Almahayni, K., Nestola, G., Chai, P., Lebedenko, C. G., Volk, R. F., Detrés, D., Caldwell, R. M., Spiekermann, M., et al. (2025) · Cell · doi:10.1016/j.cell.2025.01.040 · Cited by 115
Autophagy as a common pathway in amyotrophic lateral sclerosis
Nguyen, D. K. H., Thombre, R., & Wang, J. (2018) · Neuroscience Letters · doi:10.1016/j.neulet.2018.04.006 · Cited by 118
Novel antibodies reveal presynaptic localization of C9orf72 protein and reduced protein levels in C9orf72 mutation carriers
Frick, P., Sellier, C., Mackenzie, I. R., Cheng, C.-Y., Tahraoui‐Bories, J., Martinat, C., Pasterkamp, R. J., Prudlo, J., Edbauer, D., Oulad‐Abdelghani, M., et al. (2018) · Acta Neuropathologica Communications · doi:10.1186/s40478-018-0579-0 · Cited by 118
C9orf72 arginine-rich dipeptide proteins interact with ribosomal proteins in vivo to induce a toxic translational arrest that is rescued by eIF1A
Moens, T. G., Niccoli, T., Wilson, K. M., Atilano, M. L., Birsa, N., Gittings, L. M., Hölbling, B. V., Dyson, M. C., Thoeng, A., Neeves, J., et al. (2019) · Acta Neuropathologica · doi:10.1007/s00401-018-1946-4 · Cited by 110
Self-citation
Cerebellar c9RAN proteins associate with clinical and neuropathological characteristics of C9ORF72 repeat expansion carriers
Gendron, T. F., van Blitterswijk, M., Bieniek, K. F., Daughrity, L. M., Jiang, J., Rush, B. K., Pedraza, O., Lucas, J. A., Murray, M. E., Desaro, P., et al. (2015) · Acta Neuropathologica · doi:10.1007/s00401-015-1474-4 · Cited by 106
Stress granules at the intersection of autophagy and ALS
Monahan, Z. T., Shewmaker, F. P., & Pandey, U. B. (2016) · Brain Research · doi:10.1016/j.brainres.2016.05.022 · Cited by 110
Proteomics and C9orf72 neuropathology identify ribosomes as poly-GR/PR interactors driving toxicity
Hartmann, H., Hornburg, D., Czuppa, M., Bader, J. M., Michaelsen, M., Farny, D., Arzberger, T., Mann, M., Meissner, F., & Edbauer, D. (2018) · Life Science Alliance · doi:10.26508/lsa.201800070 · Cited by 105
The genetics of amyotrophic lateral sclerosis: current insights
Kirby, J., Sultan, A. A., Waller, R., & Heath, P. R. (2016) · Degenerative Neurological and Neuromuscular Disease · doi:10.2147/dnnd.s84956 · Cited by 119
Axonal transport defects are a common phenotype in Drosophila models of ALS
Baldwin, K. R., Godena, V. K., Hewitt, V. L., & Whitworth, A. J. (2016) · Human Molecular Genetics · doi:10.1093/hmg/ddw105 · Cited by 111
Traditional Chinese medicine compounds regulate autophagy for treating neurodegenerative disease: A mechanism review
Wang, Z., Liu, J., Zhu, Z., Su, C.-F., Sreenivasmurthy, S. G., Iyaswamy, A., Lu, J., Chen, G., Song, J., & Li, M. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110968 · Cited by 109
Antibody Therapy Targeting RAN Proteins Rescues C9 ALS/FTD Phenotypes in C9orf72 Mouse Model
Nguyen, L., Montrasio, F., Pattamatta, A., Tusi, S. K., Bardhi, O., Meyer, K. D., Hayes, L. R., Nakamura, K., Báñez-Coronel, M., Coyne, A. N., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.11.007 · Cited by 108
Disease Mechanisms ofC9ORF72Repeat ExpansionsPreprint
Gendron, T. F., & Petrucelli, L. (2017) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a024224 · Cited by 106
A fruitful endeavor: Modeling ALS in the fruit fly
Casci, I., & Pandey, U. B. (2014) · Brain Research · doi:10.1016/j.brainres.2014.09.064 · Cited by 102
RAN translation—What makes it run?
Green, K. M., Linsalata, A. E., & Todd, P. K. (2016) · Brain Research · doi:10.1016/j.brainres.2016.04.003 · Cited by 109
Poly-GR dipeptide repeat polymers correlate with neurodegeneration and Clinicopathological subtypes in C9ORF72-related brain disease
Sakae, N., Bieniek, K. F., Zhang, Y., Ross, K., Gendron, T. F., Murray, M. E., Rademakers, R., Petrucelli, L., & Dickson, D. W. (2018) · Acta Neuropathologica Communications · doi:10.1186/s40478-018-0564-7 · Cited by 103
Evidence that C9ORF72 Dipeptide Repeat Proteins Associate with U2 snRNP to Cause Mis-splicing in ALS/FTD Patients
Yin, S., Lopez-Gonzalez, R., Kunz, R. C., Gangopadhyay, J. P., Borufka, C., Gygi, S. P., Gao, F., & Reed, R. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.05.056 · Cited by 100
Post-transcriptional Inhibition of Hsc70-4/HSPA8 Expression Leads to Synaptic Vesicle Cycling Defects in Multiple Models of ALS
Coyne, A. N., Lorenzini, I., Chou, C., Torvund, M., Rogers, R. S., Starr, A., Zaepfel, B. L., Levy, J., Johannesmeyer, J., Schwartz, J. C., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.09.028 · Cited by 105
Motor dysfunction and neurodegeneration in a C9orf72 mouse line expressing poly-PR
Hao, Z., Liu, L., Tao, Z., Wang, R., Ren, H., Sun, H., Lin, Z., Zhang, Z., Mu, C., Zhou, J., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-10956-w · Cited by 104
RPS25 is required for efficient RAN translation of C9orf72 and other neurodegenerative disease-associated nucleotide repeats
Yamada, S. B., Gendron, T. F., Niccoli, T., Genuth, N. R., Grosely, R., Shi, Y., Glaria, I., Kramer, N. J., Nakayama, L., Fang, S., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0455-7 · Cited by 102
Self-citation
Citrullination of RGG Motifs in FET Proteins by PAD4 Regulates Protein Aggregation and ALS Susceptibility
Tanikawa, C., Ueda, K., Suzuki, A., Iida, A., Nakamura, R., Atsuta, N., Tohnai, G., Sobue, G., Saichi, N., Momozawa, Y., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.01.031 · Cited by 104
Innate Immunity: A Common Denominator between Neurodegenerative and Neuropsychiatric Diseases
Novellino, F., Saccà, V., Donato, A., Zaffino, P., Spadea, M. F., Vismara, M. F. M., Arcidiacono, B., Malara, N., Presta, I., & Donato, G. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21031115 · Cited by 107
A feedback loop between dipeptide-repeat protein, TDP-43 and karyopherin-α mediates C9orf72-related neurodegeneration
Solomon, D. A., Stepto, A., Au, W. H., Adachi, Y., Diaper, D. C., Hall, R., Rekhi, A., Boudi, A., Tziortzouda, P., Lee, Y., et al. (2018) · Brain · doi:10.1093/brain/awy241 · Cited by 105
C9ORF72 Regulates Stress Granule Formation and Its Deficiency Impairs Stress Granule Assembly, Hypersensitizing Cells to Stress
Maharjan, N., Künzli, C., Buthey, K., & Saxena, S. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-9850-1 · Cited by 105
The small heat shock protein B8 (HSPB8) efficiently removes aggregating species of dipeptides produced in C9ORF72-related neurodegenerative diseases
Cristofani, R., Crippa, V., Vezzoli, G., Rusmini, P., Galbiati, M., Cicardi, M. E., Meroni, M., Ferrari, V., Tedesco, B., Piccolella, M., et al. (2017) · Cell Stress and Chaperones · doi:10.1007/s12192-017-0806-9 · Cited by 102
Nuclear pore complexes — a doorway to neural injury in neurodegeneration
Coyne, A. N., & Rothstein, J. D. (2022) · Nature Reviews Neurology · doi:10.1038/s41582-022-00653-6 · Cited by 96
Dipeptide repeat protein inclusions are rare in the spinal cord and almost absent from motor neurons in C9ORF72 mutant amyotrophic lateral sclerosis and are unlikely to cause their degeneration
Gomez-Deza, J., Lee, Y.-B., Troakes, C., Nolan, M., Al-Sarraj, S., Gallo, J.-M., & Shaw, C. E. (2015) · Acta Neuropathologica Communications · doi:10.1186/s40478-015-0218-y · Cited by 93
Genetics insight into the amyotrophic lateral sclerosis/frontotemporal dementia spectrum
Ji, A.-L., Zhang, X., Chen, W., & Huang, W. (2017) · Journal of Medical Genetics · doi:10.1136/jmedgenet-2016-104271 · Cited by 99
Repeat-associated non-ATG (RAN) translation
Cleary, J. D., Pattamatta, A., & Ranum, L. P. W. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.r118.003237 · Cited by 100
GGGGCC microsatellite RNA is neuritically localized, induces branching defects, and perturbs transport granule function
Burguete, A. S., Almeida, S., Gao, F., Kalb, R. G., Akins, M. R., & Bonini, N. M. (2015) · eLife · doi:10.7554/elife.08881 · Cited by 98
C9orf72 -derived arginine-containing dipeptide repeats associate with axonal transport machinery and impede microtubule-based motility
Fumagalli, L., Young, F. L., Boeynaems, S., Decker, M. D., Mehta, A. R., Swijsen, A., Fazal, R., Guo, W., Moisse, M., Beckers, J., et al. (2021) · Science Advances · doi:10.1126/sciadv.abg3013 · Cited by 94
Acetylation mimic of lysine 280 exacerbates human Tau neurotoxicity in vivo
Gorsky, M. K., Burnouf, S., Dols, J., Mandelkow�, E., & Partridge, L. (2016) · Scientific Reports · doi:10.1038/srep22685 · Cited by 94
Self-citation
Dipeptide repeat proteins inhibit homology-directed DNA double strand break repair in C9ORF72 ALS/FTD
Andrade, N. S., Ramic, M., Esanov, R., Liu, W., Rybin, M. J., Gaidosh, G., Abdallah, A., Del’Olio, S., Huff, T. C., Chee, N. T., et al. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00365-9 · Cited by 97
Biological importance of arginine: A comprehensive review of the roles in structure, disorder, and functionality of peptides and proteins
Gupta, M. N., & Uversky, V. N. (2023) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2023.128646 · Cited by 92
RAN translation at CGG repeats induces ubiquitin proteasome system impairment in models of fragile X-associated tremor ataxia syndrome
Oh, S. Y., He, F., Krans, A., Frazer, M. A., Taylor, J. P., Paulson, H. L., & Todd, P. K. (2015) · Human Molecular Genetics · doi:10.1093/hmg/ddv165 · Cited by 92
C9orf72 poly GA RAN-translated protein plays a key role in amyotrophic lateral sclerosis via aggregation and toxicity
Lee, Y., Baskaran, P., Gómez-Deza, J., Chen, H.-J., Nishimura, A. L., Smith, B. N., Troakes, C., Adachi, Y., Stepto, A., Petrucelli, L., et al. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx350 · Cited by 90
Repeat-associated non-AUG (RAN) translation and other molecular mechanisms in Fragile X Tremor Ataxia Syndrome
Glineburg, M. R., Todd, P. K., Charlet‐Berguerand, N., & Sellier, C. (2018) · Brain Research · doi:10.1016/j.brainres.2018.02.006 · Cited by 91
Quantitative Assessment of Eye Phenotypes for Functional Genetic Studies Using Drosophila melanogaster
Iyer, J. S., Wang, Q., Le, T., Pizzo, L., Grönke, S., Ambegaokar, S. S., Imai, Y., Srivastava, A., Troisí, B. L., Mardon, G., et al. (2016) · G3 Genes Genomes Genetics · doi:10.1534/g3.116.027060 · Cited by 92
Self-citation
The Glycine-Alanine Dipeptide Repeat from C9orf72 Hexanucleotide Expansions Forms Toxic Amyloids Possessing Cell-to-Cell Transmission Properties
Chang, Y., Jeng, U., Chiang, Y., Hwang, I., & Chen, Y. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.694273 · Cited by 90
Antibodies inhibit transmission and aggregation of C9orf72 poly‐GA dipeptide repeat proteins
Zhou, Q., Lehmer, C., Michaelsen, M., Mori, K., Alterauge, D., Baumjohann, D., Schludi, M. H., Greiling, J., Farny, D., Flatley, A., et al. (2017) · EMBO Molecular Medicine · doi:10.15252/emmm.201607054 · Cited by 89
Partial inhibition of the overactivated Ku80-dependent DNA repair pathway rescues neurodegeneration in C9ORF72 -ALS/FTD
Lopez-Gonzalez, R., Yang, D., Pribadi, M., Kim, T. S., Krishnan, G., Choi, S. Y., Lee, S., Coppola, G., & Gao, F. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1901313116 · Cited by 85
Synaptic dysfunction and altered excitability in C9ORF72 ALS/FTD
Starr, A., & Sattler, R. (2018) · Brain Research · doi:10.1016/j.brainres.2018.02.011 · Cited by 78
Non-coding RNA in neural function, disease, and aging
Szafranski, K. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00087 · Cited by 86
Gene Therapy for Neurodegenerative Diseases: Slowing Down the Ticking Clock
Martier, R., & Konstantinova, P. S. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.580179 · Cited by 91
FMRpolyG-positive inclusions in CNS and non-CNS organs of a fragile X premutation carrier with fragile X-associated tremor/ataxia syndrome
Buijsen, R. A. M., Sellier, C., Severijnen, L.-A. W. F. M., Oulad‐Abdelghani, M., Verhagen, R. F. M., Berman, R. F., Charlet‐Berguerand, N., Willemsen, R., & Hukema, R. K. (2014) · Acta Neuropathologica Communications · doi:10.1186/s40478-014-0162-2 · Cited by 84
Nucleocytoplasmic Proteomic Analysis Uncovers eRF1 and Nonsense-Mediated Decay as Modifiers of ALS/FTD C9orf72 Toxicity
Ortega, J. A., Daley, E. L., Kour, S., Samani, M., Tellez, L., Smith, H. S., Hall, E., Esengul, Y. T., Tsai, Y., Gendron, T. F., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.01.020 · Cited by 81
Ribosome inhibition by C9ORF72-ALS/FTD-associated poly-PR and poly-GR proteins revealed by cryo-EM
Loveland, A. B., Svidritskiy, E., Susorov, D. S., Lee, S., Park, A., Zvornicanin, S. N., Demo, G., Gao, F., & Korostelev, A. A. (2022) · Nature Communications · doi:10.1038/s41467-022-30418-0 · Cited by 86
Anti-sense DNA d(GGCCCC)n expansions in C9ORF72 form i-motifs and protonated hairpins
Kovanda, A., Zalar, M., Šket, P., Plavec, J., & Rogelj, B. (2015) · Scientific Reports · doi:10.1038/srep17944 · Cited by 82
Biology and Pathobiology of TDP-43 and Emergent Therapeutic StrategiesPreprint
Guo, L. E., & Shorter, J. (2016) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a024554 · Cited by 85
Variant-selective stereopure oligonucleotides protect against pathologies associated with C9orf72-repeat expansion in preclinical models
Liu, Y., Dodart, J., Tran, H., Berkovitch, S. S., Braun, M. C., Byrne, M., Durbin, A. F., Hu, X. S., Iwamoto, N., Jang, H. G., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-21112-8 · Cited by 82
Modeling cell-autonomous motor neuron phenotypes in ALS using iPSCs
Hawrot, J., Imhof, S., & Wainger, B. J. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.104680 · Cited by 74
Neurodegeneration in frontotemporal lobar degeneration and motor neurone disease associated with expansions in C9orf72 is linked to TDP‐43 pathology and not associated with aggregated forms of dipeptide repeat proteins
Davidson, Y., Robinson, A. C., Liu, X., Wu, D., Troakes, C., Rollinson, S., Masuda‐Suzukake, M., Suzuki, G., Nonaka, T., Shi, J., et al. (2016) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12292 · Cited by 77
Self-citation
New pathologic mechanisms in nucleotide repeat expansion disorders
Rodriguez, C. M., & Todd, P. K. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.104515 · Cited by 82
Structure of the C9orf72 ARF GAP complex that is haploinsufficient in ALS and FTD
Su, M.-Y., Fromm, S. A., Zoncu, R., & Hurley, J. H. (2020) · Nature · doi:10.1038/s41586-020-2633-x · Cited by 83
Repeat-Associated Non-ATG Translation: Molecular Mechanisms and Contribution to Neurological Disease
Nguyen, L., Cleary, J. D., & Ranum, L. P. W. (2019) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070918-050405 · Cited by 80
Toxic expanded GGGGCC repeat transcription is mediated by the PAF1 complex in C9orf72-associated FTD
Goodman, L. D., Prudencio, M., Kramer, N. J., Martinez-Ramirez, L. F., Srinivasan, A. R., Lan, M., Parisi, M. J., Zhu, Y., Chew, J., Cook, C. N., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0396-1 · Cited by 75
Nearly 30 Years of Animal Models to Study Amyotrophic Lateral Sclerosis: A Historical Overview and Future Perspectives
Bonifacino, T., Zerbo, R. A., Balbi, M., Torazza, C., Frumento, G., Fedele, E., Bonanno, G., & Milanese, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222212236 · Cited by 82
The roles of intrinsic disorder-based liquid-liquid phase transitions in the “Dr. Jekyll–Mr. Hyde” behavior of proteins involved in amyotrophic lateral sclerosis and frontotemporal lobar degeneration
Uversky, V. N. (2017) · Autophagy · doi:10.1080/15548627.2017.1384889 · Cited by 78
TFEB/Mitf links impaired nuclear import to autophagolysosomal dysfunction in C9-ALS
Cunningham, K. M., Maulding, K., Ruan, K., Şentürk, M., Grima, J. C., Sung, H., Zuo, Z., Song, H., Gao, J., Dubey, S. K., et al. (2020) · eLife · doi:10.7554/elife.59419 · Cited by 80
Disruption of ER−mitochondria signalling in fronto-temporal dementia and related amyotrophic lateral sclerosis
Lau, D. H. W., Hartopp, N., Welsh, N. J., Mueller, S., Glennon, E. B. C., Mórotz, G. M., Annibali, A., Gómez‐Suaga, P., Stoica, R., Paillusson, S., et al. (2018) · Cell Death and Disease · doi:10.1038/s41419-017-0022-7 · Cited by 77
Proteostatic imbalance and protein spreading in amyotrophic lateral sclerosis
Cicardi, M. E., Marrone, L., Azzouz, M., & Trotti, D. (2021) · The EMBO Journal · doi:10.15252/embj.2020106389 · Cited by 75
Studies of neurodegenerative diseases using Drosophila and the development of novel approaches for their analysis
Nitta, Y., & Sugie, A. (2022) · Fly · doi:10.1080/19336934.2022.2087484 · Cited by 81
The Proline/Arginine Dipeptide from Hexanucleotide Repeat Expanded C9ORF72 Inhibits the Proteasome
Gupta, R., Lan, M., Mojsilovic‐Petrovic, J., Choi, W. H., Safren, N., Barmada, S. J., Lee, M. J., & Kalb, R. G. (2017) · eNeuro · doi:10.1523/eneuro.0249-16.2017 · Cited by 74
Insights into the pathogenic mechanisms of chromosome 9 open reading frame 72 (C9orf72) repeat expansions
Todd, T. W., & Petrucelli, L. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13623 · Cited by 73
New insights into nucleolar structure and function
Lam, Y. W., & Trinkle‐Mulcahy, L. (2015) · F1000Prime Reports · doi:10.12703/p7-48 · Cited by 80
Glycine-alanine dipeptide repeat protein contributes to toxicity in a zebrafish model of C9orf72 associated neurodegeneration
Ohki, Y., Wenninger-Weinzierl, A., Hruscha, A., Asakawa, K., Kawakami, K., Haass, C., Edbauer, D., & Schmid, B. (2017) · Molecular Neurodegeneration · doi:10.1186/s13024-016-0146-8 · Cited by 75
CRISPR/Cas9-mediated excision of ALS/FTD-causing hexanucleotide repeat expansion in C9ORF72 rescues major disease mechanisms in vivo and in vitro
Meijboom, K. E., Abdallah, A., Fordham, N. P., Nagase, H., Rodríguez, T., Kraus, C., Gendron, T. F., Krishnan, G., Esanov, R., Andrade, N. S., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33332-7 · Cited by 78
Homeostatic plasticity can be induced and expressed to restore synaptic strength at neuromuscular junctions undergoing ALS-related degeneration
Perry, S., Han, Y., Das, A., & Dickman, D. K. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx304 · Cited by 78
Chimeric Peptide Species Contribute to Divergent Dipeptide Repeat Pathology in c9ALS/FTD and SCA36
McEachin, Z. T., Gendron, T. F., Raj, N., García-Murias, M., Banerjee, A., Purcell, R. H., Ward, P. J., Todd, T. W., Merritt-Garza, M. E., Jansen‐West, K. R., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.04.011 · Cited by 71
NUP62 localizes to ALS/FTLD pathological assemblies and contributes to TDP-43 insolubility
Gleixner, A. M., Verdone, B. M., Otte, C. G., Anderson, E. N., Ramesh, N., Shapiro, O. R., Gale, J. R., Mauna, J. C., Mann, J. R., Copley, K. E., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-31098-6 · Cited by 71
Opposing roles of p38 and JNK in a Drosophila model of TDP-43 proteinopathy reveal oxidative stress and innate immunity as pathogenic components of neurodegeneration
Zhan, L., Xie, Q., & Tibbetts, R. S. (2014) · Human Molecular Genetics · doi:10.1093/hmg/ddu493 · Cited by 70
Sense and antisense RNA are not toxic in Drosophila models of C9orf72-associated ALS/FTD
Moens, T. G., Mizielinska, S., Niccoli, T., Mitchell, J. S., Thoeng, A., Ridler, C. E., Grönke, S., Eßer, J., Heslegrave, A., Zetterberg, H., et al. (2018) · Acta Neuropathologica · doi:10.1007/s00401-017-1798-3 · Cited by 72
Self-citation
Molecular Mechanisms of Neurodegeneration Related to C9orf72 Hexanucleotide Repeat Expansion
Leko, M. B., Župunski, V., Kirincich, J., Smilović, D., Hortobágyi, T., Hof, P. R., & Šimić, G. (2019) · Behavioural Neurology · doi:10.1155/2019/2909168 · Cited by 73
FTD and ALS—translating mouse studies into clinical trials
Ittner, L. M., Halliday, G. M., Kril, J. J., Götz, J., Hodges, J. R., & Kiernan, M. C. (2015) · Nature Reviews Neurology · doi:10.1038/nrneurol.2015.65 · Cited by 70
Stable transgenic C9orf72 zebrafish model key aspects of the ALS/FTD phenotype and reveal novel pathological features
Shaw, M. P., Higginbottom, A., McGown, A., Castelli, L. M., James, E. G., Hautbergue, G. M., Shaw, P. J., & Ramesh, T. (2018) · Acta Neuropathologica Communications · doi:10.1186/s40478-018-0629-7 · Cited by 72
Emerging Perspectives on Dipeptide Repeat Proteins in C9ORF72 ALS/FTD
Schmitz, A., Marques, J. P., Oertig, I., Maharjan, N., & Saxena, S. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.637548 · Cited by 70
Increased expression of the frontotemporal dementia risk factor TMEM106B causes C9orf72-dependent alterations in lysosomes
Busch, J. I., Unger, T. L., Jain, N., Skrinak, R. T., Charan, R. A., & Chen‐Plotkin, A. S. (2016) · Human Molecular Genetics · doi:10.1093/hmg/ddw127 · Cited by 68
ADAR2 mislocalization and widespread RNA editing aberrations in C9orf72-mediated ALS/FTD
Moore, S. R., Alsop, E. B., Lorenzini, I., Starr, A., Rabichow, B. E., Mendez, E. F., Levy, J. L., Burciu, C., Reiman, R. A., Chew, J., et al. (2019) · Acta Neuropathologica · doi:10.1007/s00401-019-01999-w · Cited by 73
Congenic expression of poly-GA but not poly-PR in mice triggers selective neuron loss and interferon responses found in C9orf72 ALS
LaClair, K. D., Zhou, Q., Michaelsen, M., Wefers, B., Brill, M. S., Janjic, A., Rathkolb, B., Farny, D., Cygan, M., de Angelis, M. H., et al. (2020) · Acta Neuropathologica · doi:10.1007/s00401-020-02176-0 · Cited by 68
Expression of C9orf72-related dipeptides impairs motor function in a vertebrate model
Swaminathan, A., Bouffard, M., Liao, M., Ryan, S., Callister, J. B., Pickering-Brown, S. M., Armstrong, G. A. B., & Drapeau, P. (2018) · Human Molecular Genetics · doi:10.1093/hmg/ddy083 · Cited by 71
Self-citation
RNA biology of disease-associated microsatellite repeat expansions
Rohilla, K. J., & Gagnon, K. T. (2017) · Acta Neuropathologica Communications · doi:10.1186/s40478-017-0468-y · Cited by 70
An amyloid-like cascade hypothesis for C9orf72 ALS/FTD
Edbauer, D., & Haass, C. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.10.009 · Cited by 69
DDX3X and specific initiation factors modulate FMR1 repeat‐associated non‐AUG‐initiated translation
Linsalata, A. E., He, F., Malik, A. M., Glineburg, M. R., Green, K. M., Natla, S., Flores, B. N., Krans, A., Archbold, H. C., Fedak, S., et al. (2019) · EMBO Reports · doi:10.15252/embr.201847498 · Cited by 62
Retention of hexanucleotide repeat-containing intron in C9orf72 mRNA: implications for the pathogenesis of ALS/FTD
Niblock, M., Smith, B. N., Lee, Y., Sardone, V., Topp, S. D., Troakes, C., Al‐Sarraj, S., Leblond, C. S., Dion, P. A., Rouleau, G. A., et al. (2016) · Acta Neuropathologica Communications · doi:10.1186/s40478-016-0289-4 · Cited by 64
Unraveling the Role of RNA Mediated Toxicity of C9orf72 Repeats in C9-FTD/ALS
Kumar, V., Hasan, G. M., & Hassan, M. I. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00711 · Cited by 67
Properties of LINE-1 proteins and repeat element expression in the context of amyotrophic lateral sclerosis
Pereira, G., Sánchez, L., Schaughency, P., Rubio-Roldán, A., Choi, J. A., Planet, E., Batra, R., Turelli, P., Trono, D., Ostrow, L. W., et al. (2018) · Mobile DNA · doi:10.1186/s13100-018-0138-z · Cited by 70
C9orf72 plays a central role in Rab GTPase-dependent regulation of autophagy
Webster, C. P., Smith, E. F., Grierson, A. J., & Vos, K. J. D. (2016) · Small GTPases · doi:10.1080/21541248.2016.1240495 · Cited by 70
Hypo- and Hyper-Assembly Diseases of RNA–Protein Complexes
Shukla, S., & Parker, R. (2016) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2016.05.005 · Cited by 64
Nucleo–cytoplasmic transport defects and protein aggregates in neurodegeneration
Bitetto, G., & Fonzo, A. D. (2020) · Translational Neurodegeneration · doi:10.1186/s40035-020-00205-2 · Cited by 68
Disruption of ER‐mitochondria tethering and signalling in C9orf72‐associated amyotrophic lateral sclerosis and frontotemporal dementia
Gómez‐Suaga, P., Mórotz, G. M., Markovinović, A., Martín‐Guerrero, S. M., Preza, E., Arias, N., Mayl, K., Aabdien, A., Gesheva, V., Nishimura, A. L., et al. (2022) · Aging Cell · doi:10.1111/acel.13549 · Cited by 63
Exploring the versatility of Drosophila melanogaster as a model organism in biomedical research: a comprehensive review
Atoki, A. V., Aja, P. M., Shinkafi, T. S., Ondari, E. N., Adeniyi, I. A., Fasogbon, I. V., Dangana, R. S., Shehu, U. U., & Akin-Adewumi, A. (2024) · Fly · doi:10.1080/19336934.2024.2420453 · Cited by 78
Reactivation of nonsense-mediated mRNA decay protects against C9orf72 dipeptide-repeat neurotoxicity
Xu, W., Bao, P., Jiang, X., Wang, H., Qin, M., Wang, R. L., Wang, T., Yang, Y. A., Lorenzini, I., Liao, L., et al. (2019) · Brain · doi:10.1093/brain/awz070 · Cited by 61
Quality-control mechanisms targeting translationally stalled and C-terminally extended poly(GR) associated with ALS/FTD
Li, S., Wu, Z., Tantray, I., Li, Y., Chen, S., Dong, J., Glynn, S. E., Vogel, H. S., Snyder, M. P., & Lu, B. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2005506117 · Cited by 62

Authors: Mizielinska, S., Grönke, S., Niccoli, T., Ridler, C. E., Clayton, E. L., Devoy, A., Moens, T., Norona, F. E., Woollacott, I. O. C., Pietrzyk, J., Cleverley, K., Nicoll, A. J., Pickering-Brown, S., Dols, J., Cabecinha, M., Hendrich, O., Fratta, P., Fisher, E. M. C., Partridge, L., & Isaacs, A. M.
Affiliations: UCL Queen Square Institute of Neurology (GB)
Max Planck Institute for Biology of Ageing (DE)
MRC Prion Unit (GB)
University of Manchester (GB)
University College London (GB)
Corresponding author: Mizielinska, Sarah
Grönke, Sebastian
Niccoli, Teresa
Partridge, Linda
Isaacs, Adrian M.
ORCID: Mizielinska, Sarah
Grönke, Sebastian
Niccoli, Teresa
Clayton, Emma L.
Devoy, Anny
Moens, Thomas
Norona, Frances E.
Woollacott, Ione O. C.
Cleverley, Karen
Nicoll, Andrew J.
Pickering-Brown, Stuart
Cabecinha, Melissa
Hendrich, Oliver
Fratta, Pietro
Fisher, Elizabeth M. C.
Partridge, Linda
Isaacs, Adrian M.
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 2014-09-05
Volume: 345
Issue: 6201
Pages: 1192-1194
ISSN: 0036-8075 (ISSN-L)
1095-9203
DOI: 10.1126/science.1256800
PMC: PMC4944841
OpenAlex: W2137039075
Cited by: 740
References: 37
Citations by year: 2026: 30 · 2025: 44 · 2024: 49 · 2023: 70 · 2022: 57 · 2021: 90 · 2020: 69 · 2019: 62 · 2018: 62 · 2017: 62 · 2016: 68 · 2015: 59 · 2014: 18
FWCI: 45.00
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Science (publishedVersion)
PubMed (publishedVersion)
Research Explorer (The University of Manchester) (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
UCL Discovery (University College London) (submittedVersion)
Research Portal (King's College London) (submittedVersion)
MPG.PuRe (Max Planck Society) (submittedVersion)
Funders: Wellcome Trust (098565, 089701, 081394)
Brain Research UK (13173)
National Institute for Health and Care Research (ACF-2012-18-009)
Motor Neurone Disease Association (ISAACS/APR13/818-791)
Institute on the Environment, University of Minnesota
Medical Research Council (MR/K018523/1, MR/J004022/1, MR/L021056/1)
Topics: Health Sciences › Medicine › Clinical Neurology › Amyotrophic Lateral Sclerosis Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Genetic Neurodegenerative Diseases
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
Keywords: C9orf72, GGGGCC repeat expansion, dipeptide repeat proteins, repeat-associated non-ATG translation, frontotemporal dementia, amyotrophic lateral sclerosis, neurodegeneration, arginine-rich proteins, Drosophila model
MeSH terms: C9orf72 Protein, Amyotrophic Lateral Sclerosis, Animals, Dipeptides, Disease Models, Animal, Drosophila melanogaster, Escherichia coli, Humans, Neurons, Proteins, DNA Repeat Expansion, Cell Line, Tumor, Frontotemporal Dementia

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

C9orf72 repeat expansions cause neurodegeneration in Drosophila through arginine-rich proteins

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks