Cited by 117Amyotrophic Lateral Sclerosis ResearchRNA modifications and cancerAlzheimer's disease research and treatments

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RNA methylation influences TDP43 binding and disease pathogenesis in models of amyotrophic lateral sclerosis and frontotemporal dementia

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McMillan, Michael, Gomez, Nicolas, Hsieh, Caroline, Bekier, Michael, Li, Xingli, Miguez, Roberto, Tank, Elizabeth M.H., Barmada, Sami J.·2023·Molecular Cell

DOI 10.1016/j.molcel.2022.12.019PMC PMC9899051

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Abstract

RNA methylation at adenosine N6 (m6A) is one of the most common RNA modifications, impacting RNA stability, transport, and translation. Previous studies uncovered RNA destabilization in amyotrophic lateral sclerosis (ALS) models in association with accumulation of the RNA-binding protein TDP43. Here, we show that TDP43 recognizes m6A RNA and that RNA methylation is critical for both TDP43 binding and autoregulation. We also observed extensive RNA hypermethylation in ALS spinal cord, corresponding to methylated TDP43 substrates. Emphasizing the importance of m6A for TDP43 binding and function, we identified several m6A factors that enhance or suppress TDP43-mediated toxicity via single-cell CRISPR-Cas9 in primary neurons. The most promising modifier-the canonical m6A reader YTHDF2-accumulated within ALS spinal neurons, and its knockdown prolonged the survival of human neurons carrying ALS-associated mutations. Collectively, these data show that m6A modifications modulate RNA binding by TDP43 and that m6A is pivotal for TDP43-related neurodegeneration in ALS.

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Fast and accurate short read alignment with Burrows-Wheeler transform
Li, H., & Durbin, R. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp324 · Cited by 58,607
Cutadapt removes adapter sequences from high-throughput sequencing reads
Martin, M. (2011) · EMBnet.journal · doi:10.14806/ej.17.1.200 · Cited by 33,889
Fast and accurate long-read alignment with Burrows-Wheeler transform.
Li, H., & Durbin, R. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp698 · Cited by 12,063
Genome engineering using the CRISPR-Cas9 system
Ran, F. A., Hsu, P. D., Wright, J., Agarwala, V., Scott, D. A., & Zhang, F. (2013) · Nature Protocols · doi:10.1038/nprot.2013.143 · Cited by 11,133
QuPath: Open source software for digital pathology image analysis
Bankhead, P., Loughrey, M. B., Fernández, J. A., Dombrowski, Y., McArt, D. G., Dunne, P. D., McQuaid, S., Gray, R. T., Murray, L. J., Coleman, H. G., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-17204-5 · Cited by 8,908
The STRING database in 2021: customizable protein–protein networks, and functional characterization of user-uploaded gene/measurement sets
Szklarczyk, D., Gable, A. L., Nastou, K. C., Lyon, D., Kirsch, R., Pyysalo, S., Doncheva, N. T., Legeay, M., Fang, T., Bork, P., et al. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkaa1074 · Cited by 8,056
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
Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq
Dominissini, D., Moshitch-Moshkovitz, S., Schwartz, S., Salmon-Divon, M., Ungar, L., Osenberg, S., Cesarkas, K., Jacob-Hirsch, J., Amariglio, N., Kupiec, M., et al. (2012) · Nature · doi:10.1038/nature11112 · Cited by 4,884
N6-methyladenosine-dependent regulation of messenger RNA stability
Wang, X., Lu, Z., Gomez, A., Hon, G. C., Yue, Y., Han, D., Fu, Y., Parisien, M., Dai, Q., Jia, G., et al. (2014) · Nature · doi:10.1038/nature12730 · Cited by 4,558
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
Comprehensive Analysis of mRNA Methylation Reveals Enrichment in 3′ UTRs and near Stop Codons
Meyer, K. D., Saletore, Y., Zumbo, P., Elemento, O., Mason, C. E., & Jaffrey, S. R. (2012) · Cell · doi:10.1016/j.cell.2012.05.003 · Cited by 4,223
Gene set knowledge discovery with enrichr
Xie, Z., Bailey, A., Kuleshov, M. V., Clarke, D. J. B., Evangelista, J. E., Jenkins, S. L., Lachmann, A., Wojciechowicz, M. L., Kropiwnicki, E., Jagodnik, K. M., et al. (2021) · Current Protocols · doi:10.1002/cpz1.90 · Cited by 3,451
A METTL3–METTL14 complex mediates mammalian nuclear RNA N6-adenosine methylation
Liu, J., Yue, Y., Han, D., Wang, X., Fu, Y., Zhang, L., Jia, G., Yu, M., Lu, Z., Deng, X., et al. (2014) · Nature Chemical Biology · doi:10.1038/nchembio.1432 · Cited by 3,433
Mammalian WTAP is a regulatory subunit of the RNA N6-methyladenosine methyltransferase
Ping, X.-L., Sun, B.-F., Wang, L., Xiao, W., Yang, X., Wang, W.-J., Adhikari, S., Shi, Y., Lv, Y., Chen, Y.-S., et al. (2014) · Cell Research · doi:10.1038/cr.2014.3 · Cited by 2,375
CHOPCHOP v3: expanding the CRISPR web toolbox beyond genome editing
Labun, K., Montague, T. G., Krause, M., Cleuren, Y. N. T., Tjeldnes, H., & Valen, E. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz365 · Cited by 2,075
N6-methyladenosine-dependent RNA structural switches regulate RNA–protein interactions
Liu, N., Dai, Q., Zheng, G., He, C., Parisien, M., & Pan, T. (2015) · Nature · doi:10.1038/nature14234 · Cited by 1,988
Three-dimensional Epigenome Statistical Model: Genome-wide Chromatin Looping Prediction
Bkhetan, Z. A., & Plewczyński, D. (2018) · Scientific Reports · doi:10.1038/s41598-018-23276-8 · Cited by 1,672
Single-nucleotide-resolution mapping of m6A and m6Am throughout the transcriptome
Linder, B., Grozhik, A. V., Olarerin-George, A. O., Meydan, C., Mason, C. E., & Jaffrey, S. R. (2015) · Nature Methods · doi:10.1038/nmeth.3453 · Cited by 1,569
HNRNPA2B1 Is a Mediator of m6A-Dependent Nuclear RNA Processing Events
Alarcón, C. R., Goodarzi, H., Lee, H., Liu, X., Tavazoie, S., & Tavazoie, S. F. (2015) · Cell · doi:10.1016/j.cell.2015.08.011 · Cited by 1,514
Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43
Polymenidou, M., Lagier-Tourenne, C., Hutt, K. R., Huelga, S. C., Moran, J., Liang, T. Y., Ling, S.-C., Sun, E., Wancewicz, E., Mazur, C., et al. (2011) · Nature Neuroscience · doi:10.1038/nn.2779 · Cited by 1,335
m6A RNA Methylation Regulates the Self-Renewal and Tumorigenesis of Glioblastoma Stem Cells
Cui, Q., Shi, H., Ye, P., Li, L., Qu, Q., Sun, G., Sun, G., Lu, Z., Huang, Y., Yang, C., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.02.059 · Cited by 1,255
CHOPCHOP: a CRISPR/Cas9 and TALEN web tool for genome editing
Montague, T. G., Cruz, J. M. B. S., Gagnon, J. A., Church, G. M., & Valen, E. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku410 · Cited by 1,246
Perturbation of m6A Writers Reveals Two Distinct Classes of mRNA Methylation at Internal and 5′ Sites
Schwartz, S., Mumbach, M. R., Jovanović, M., Wang, T., Maciag, K., Bushkin, G. G., Mertins, P., Ter‐Ovanesyan, D., Habib, N., Cacchiarelli, D., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.05.048 · Cited by 1,231
Dynamic m6A mRNA methylation directs translational control of heat shock response
Zhou, J. L., Wan, J., Gao, X., Zhang, X., Jaffrey, S. R., & Qian, S. (2015) · Nature · doi:10.1038/nature15377 · Cited by 1,228
Characterizing the RNA targets and position-dependent splicing regulation by TDP-43
Tollervey, J. R., Curk, T., Rogelj, B., Briese, M., Cereda, M., Kayikci, M., König, J., Hortobágyi, T., Nishimura, A. L., Župunski, V., et al. (2011) · Nature Neuroscience · doi:10.1038/nn.2778 · Cited by 1,165
Purification and cDNA cloning of the AdoMet-binding subunit of the human mRNA (N6-adenosine)-methyltransferase.
Bokar, J. A., Shambaugh, M. E., Polayes, D. A., Matera, A. G., & ROTTMAN, F. M. (1997) · PubMed Central · Cited by 955
CHOPCHOP v2: a web tool for the next generation of CRISPR genome engineering
Labun, K., Montague, T. G., Gagnon, J. A., Thyme, S. B., & Valen, E. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw398 · Cited by 954
VEGF is a modifier of amyotrophic lateral sclerosis in mice and humans and protects motoneurons against ischemic death
Lambrechts, D., Storkebaum, E., Morimoto, M., Del‐Favero, J., Smet, F. D., Marklund, S. L., Wyns, S., Thijs, V., Andersson, J., van Marion, I., et al. (2003) · Nature Genetics · doi:10.1038/ng1211 · Cited by 853
Cloning and characterization of a novel cellular protein, TDP-43, that binds to human immunodeficiency virus type 1 TAR DNA sequence motifs
Ou, S.-H. I., Wu, F. K., Harrich, D., Garcı́a-Martı́nez, L. F., & Gaynor, R. B. (1995) · Journal of Virology · doi:10.1128/jvi.69.6.3584-3596.1995 · Cited by 762
SuperPlots: Communicating reproducibility and variability in cell biology
Lord, S. J., Velle, K. B., Mullins, R. D., & Fritz-Laylin, L. K. (2020) · Journal of Cell Biology · doi:10.1083/jcb.202001064 · Cited by 718
Characterization and Functional Implications of the RNA Binding Properties of Nuclear Factor TDP-43, a Novel Splicing Regulator ofCFTR Exon 9
Buratti, E., & Baralle, F. E. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m104236200 · Cited by 697
A general method to fine-tune fluorophores for live-cell and in vivo imaging
Grimm, J. B., Muthusamy, A. K., Liang, Y., Brown, T. A., Lemon, W. C., Patel, R. H., Lu, R., Macklin, J. J., Keller, P., Ji, N., et al. (2017) · Nature Methods · doi:10.1038/nmeth.4403 · Cited by 665
ALS-implicated protein TDP-43 sustains levels of STMN2, a mediator of motor neuron growth and repair
Klim, J. R., Williams, L. A., Limone, F., Guerra San Juan, I., Davis-Dusenbery, B. N., Mordes, D. A., Burberry, A., Steinbaugh, M. J., Gamage, K. K., Kirchner, R., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-018-0300-4 · Cited by 653
TDP‐43 regulates its mRNA levels through a negative feedback loop
Ayala, Y. M., Conti, L. D., Avendaño-Vázquez, S. E., Dhir, A., Romano, M., D’Ambrogio, A., Tollervey, J. R., Ule, J., Baralle, M., Buratti, E., et al. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.310 · Cited by 649
Premature polyadenylation-mediated loss of stathmin-2 is a hallmark of TDP-43-dependent neurodegeneration
Melamed, Z., López-Erauskin, J., Baughn, M. W., Zhang, O., Drenner, K., Sun, Y., Freyermuth, F., McMahon, M. A., Beccari, M. S., Artates, J. W., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-018-0293-z · Cited by 635
Nuclear factor TDP‐43 and SR proteins promote in vitro and in vivo CFTR exon 9 skipping
Buratti, E., Dörk, T., Zuccato, E., Pagani, F., Romano, M., & Baralle, F. E. (2001) · The EMBO Journal · doi:10.1093/emboj/20.7.1774 · Cited by 633
Endoribonucleolytic Cleavage of m6A-Containing RNAs by RNase P/MRP Complex
Park, O. H., Ha, H., Lee, Y., Boo, S. H., Kwon, D. H., Song, H. K., & Kim, Y. K. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.02.034 · Cited by 587
Therapeutic reduction of ataxin-2 extends lifespan and reduces pathology in TDP-43 mice
Becker, L. A., Huang, B., Bieri, G., Ma, R., Knowles, D. A., Jafar-Nejad, P., Messing, J., Kim, H. J., Soriano, A., Auburger, G., et al. (2017) · Nature · doi:10.1038/nature22038 · Cited by 571
N6-methyladenosine (m6A) recruits and repels proteins to regulate mRNA homeostasis
Edupuganti, R. R., Geiger, S., Lindeboom, R. G. H., Shi, H., Hsu, P. J., Lu, Z., Wang, S.-Y., Baltissen, M. P. A., Jansen, P. W. T. C., Rossa, M., et al. (2017) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3462 · Cited by 568
Cytoplasmic Mislocalization of TDP-43 Is Toxic to Neurons and Enhanced by a Mutation Associated with Familial Amyotrophic Lateral Sclerosis
Barmada, S. J., Skibinski, G., Korb, E., Rao, E. J., Wu, J. Y., & Finkbeiner, S. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4988-09.2010 · Cited by 554
Self-citation
m 6 A mRNA modifications are deposited in nascent pre-mRNA and are not required for splicing but do specify cytoplasmic turnoverPreprint
Ke, S., Pandya‐Jones, A., Saito, Y., Fak, J. J., Vågbø, C. B., Geula, S., Hanna, J. H., Black, D. L., Darnell, J. E., Jr., & Darnell, R. B. (2017) · Genes & Development · doi:10.1101/gad.301036.117 · Cited by 537
Probing N 6 -methyladenosine RNA modification status at single nucleotide resolution in mRNA and long noncoding RNA
Liu, N., Parisien, M., Dai, Q., Zheng, G., He, C., & Pan, T. (2013) · RNA · doi:10.1261/rna.041178.113 · Cited by 530
Global Analysis of TDP-43 Interacting Proteins Reveals Strong Association with RNA Splicing and Translation Machinery
Freibaum, B. D., Chitta, R. K., High, A. A., & Taylor, J. P. (2009) · Journal of Proteome Research · doi:10.1021/pr901076y · Cited by 529
Multiple roles of TDP-43 in gene expression, splicing regulation, and human disease
Buratti, E. (2007) · Frontiers in bioscience · doi:10.2741/2727 · Cited by 493
DART-seq: an antibody-free method for global m6A detection
Meyer, K. D. (2019) · Nature Methods · doi:10.1038/s41592-019-0570-0 · Cited by 490
Transcription factor-mediated differentiation of human iPSCs into neurons
Fernandopulle, M. S., Prestil, R., Grunseich, C., Wang, C., Gan, L., & Ward, M. E. (2018) · Current Protocols in Cell Biology · doi:10.1002/cpcb.51 · Cited by 461
Autophagy induction enhances TDP43 turnover and survival in neuronal ALS models
Barmada, S. J., Serio, A., Arjun, A., Bilican, B., Daub, A., Ando, D. M., Tsvetkov, A., Pleiss, M., Li, X., Peisach, D., et al. (2014) · Nature Chemical Biology · doi:10.1038/nchembio.1563 · Cited by 431
Self-citation
Molecular basis of UG-rich RNA recognition by the human splicing factor TDP-43
Lukavsky, P. J., Daujotyte, D., Tollervey, J. R., Ule, J., Stuani, C., Buratti, E., Baralle, F. E., Damberger, F. F., & Allain, F. H. ‐. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2698 · Cited by 408
YTH Domain: A Family of N 6 -Methyladenosine (m 6 A) Readers
Liao, S., Sun, H., & Xu, C. (2018) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2018.04.002 · Cited by 398
Antisense oligonucleotide therapy for spinocerebellar ataxia type 2
Scoles, D. R., Meera, P., Schneider, M. D., Paul, S., Dansithong, W., Figueroa, K. P., Hung, G., Rigo, F., Bennett, C. F., Otis, T. S., et al. (2017) · Nature · doi:10.1038/nature22044 · Cited by 319
HaloTag Technology: A Versatile Platform for Biomedical Applications
England, C. G., Luo, H., & Cai, W. (2015) · Bioconjugate Chemistry · doi:10.1021/acs.bioconjchem.5b00191 · Cited by 313
Deux cas d'atrophie musculaire progressive avec lésions de la substance grise et des faisceaux antérolatéraux de la moelle épinière
Charcot, J. M. (1869) · Medical Entomology and Zoology · Cited by 305
Genetics of Amyotrophic Lateral SclerosisPreprint
Ghasemi, M., & Brown, R. H. (2017) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a024125 · Cited by 292
TDP-43 gains function due to perturbed autoregulation in a Tardbp knock-in mouse model of ALS-FTD
White, M. A., Kim, E., Duffy, A., Adalbert, R., Phillips, B. U., Peters, O. M., Stephenson, J., Yang, S., Massenzio, F., Lin, Z., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0113-5 · Cited by 289
N6-methyladenosine dynamics in neurodevelopment and aging, and its potential role in Alzheimer’s disease
Shafik, A. M., Zhang, F., Guo, Z., Dai, Q., Pajdzik, K., Li, Y., Kang, Y., Yao, B., Wu, H., He, C., et al. (2021) · Genome biology · doi:10.1186/s13059-020-02249-z · Cited by 264
N6-Methyladenosine Modulates Nonsense-Mediated mRNA Decay in Human Glioblastoma
Li, F., Yang, Y., Miao, Y., Long, W., Long, T., Chen, S., Cheng, W., Zou, C., Zheng, Y., Wu, X., et al. (2019) · Cancer Research · doi:10.1158/0008-5472.can-18-2868 · Cited by 248
Experience-Dependent Accumulation of N 6 -Methyladenosine in the Prefrontal Cortex Is Associated with Memory Processes in Mice
Widagdo, J., Zhao, Q., Kempen, M.-J., Tan, M. C., Ratnu, V. S., Wei, W., Leighton, L. J., Spadaro, P. A., Edson, J., Anggono, V., et al. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.4053-15.2016 · Cited by 247
RNA structure maps across mammalian cellular compartments
Sun, L., Fazal, F. M., Li, P., Broughton, J. P., Lee, B., Tang, L., Huang, W., Kool, E. T., Chang, H. Y., & Zhang, Q. C. (2019) · Nature Structural & Molecular Biology · doi:10.1038/s41594-019-0200-7 · Cited by 245
Transient N-6-Methyladenosine Transcriptome Sequencing Reveals a Regulatory Role of m6A in Splicing Efficiency
Louloupi, A., Ntini, E., Conrad, T., & Ørom, U. A. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.05.077 · Cited by 239
TDP-43 condensation properties specify its RNA-binding and regulatory repertoire
Hallegger, M., Chakrabarti, A. M., Lee, F. C. Y., Lee, B. L., Amalietti, A. G., Odeh, H. M., Copley, K. E., Rubien, J. D., Portz, B., Kuret, K., et al. (2021) · Cell · doi:10.1016/j.cell.2021.07.018 · Cited by 239
Deadenylation is prerequisite for P-body formation and mRNA decay in mammalian cells
Zheng, D., Ezzeddine, N., Chen, C. A., Zhu, W., He, X., & Shyu, A. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200801196 · Cited by 227
Autoregulation of TDP-43 mRNA levels involves interplay between transcription, splicing, and alternative polyA site selectionPreprint
Avendaño-Vázquez, S. E., Dhir, A., Bembich, S., Buratti, E., Proudfoot, N. J., & Baralle, F. E. (2012) · Genes & Development · doi:10.1101/gad.194829.112 · Cited by 212
Atlas of quantitative single-base-resolution N6-methyl-adenine methylomes
Koh, C. W. Q., Goh, Y. T., & Goh, W. S. S. (2019) · Nature Communications · doi:10.1038/s41467-019-13561-z · Cited by 208
A Yeast Model of FUS/TLS-Dependent Cytotoxicity
Ju, S., Tardiff, D. F., Han, H., Divya, K., Zhong, Q., Maquat, L. E., Bosco, D. A., Hayward, L. J., Brown, R. H., Lindquist, S. L., et al. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1001052 · Cited by 208
CLIP Tool Kit (CTK): a flexible and robust pipeline to analyze CLIP sequencing data
Shah, A., Qian, Y., Weyn‐Vanhentenryck, S. M., & Zhang, C. (2016) · Bioinformatics · doi:10.1093/bioinformatics/btw653 · Cited by 182
SuperPlotsOfData—a web app for the transparent display and quantitative comparison of continuous data from different conditions
Goedhart, J. (2021) · Molecular Biology of the Cell · doi:10.1091/mbc.e20-09-0583 · Cited by 181
Interaction of tau with HNRNPA2B1 and N6-methyladenosine RNA mediates the progression of tauopathy
Jiang, L., Lin, W., Zhang, C., Ash, P. E. A., Verma, M., Kwan, J., van Vliet, E., Yang, Z., Cruz, A. L., Boudeau, S., et al. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.07.038 · Cited by 177
ALS mutations of FUS suppress protein translation and disrupt the regulation of nonsense-mediated decay
Kamelgarn, M., Chen, J., Kuang, L., Jin, H., Kasarskis, E. J., & Zhu, H. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1810413115 · Cited by 176
Molecular Neuropathology of TDP-43 Proteinopathies
Neumann, M. (2009) · International Journal of Molecular Sciences · doi:10.3390/ijms10010232 · Cited by 172
p53 is a central regulator driving neurodegeneration caused by C9orf72 poly(PR)
Maor-Nof, M., Shipony, Z., Lopez-Gonzalez, R., Nakayama, L., Zhang, Y., Couthouis, J., Blum, J. A., Castruita, P. A., Linares, G. R., Ruan, K., et al. (2021) · Cell · doi:10.1016/j.cell.2020.12.025 · Cited by 161
TDP43 nuclear export and neurodegeneration in models of amyotrophic lateral sclerosis and frontotemporal dementia
Archbold, H. C., Jackson, K. L., Arora, A., Weskamp, K., Tank, E. M. H., Li, X., Miguez, R., Dayton, R. D., Tamir, S., Klein, R. L., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-22858-w · Cited by 157
Self-citation
m6A modification of non-coding RNA and the control of mammalian gene expression
Coker, H. A., Wei, G., & Brockdorff, N. (2018) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2018.12.002 · Cited by 155
Abnormal RNA stability in amyotrophic lateral sclerosis
Tank, E., Figueroa‐Romero, C., Hinder, L. M., Bedi, K., Archbold, H. C., Li, X., Weskamp, K., Safren, N., Paez-Colasante, X., Pacut, C. M., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05049-z · Cited by 153
Self-citation
Mettl14 Is Essential for Epitranscriptomic Regulation of Striatal Function and Learning
Koranda, J. L., Dore, L., Shi, H., Patel, M. J., Vaasjo, L. O., Rao, M. N., Chen, K., Lu, Z., Yi, Y., Chi, W., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.06.007 · Cited by 144
MetaPlotR: a Perl/R pipeline for plotting metagenes of nucleotide modifications and other transcriptomic sites
Olarerin-George, A. O., & Jaffrey, S. R. (2017) · Bioinformatics · doi:10.1093/bioinformatics/btx002 · Cited by 135
States and traits of neural irregularity in the age-varying human brain
Waschke, L., Wöstmann, M., & Obleser, J. (2017) · Scientific Reports · doi:10.1038/s41598-017-17766-4 · Cited by 132
Shortened TDP43 isoforms upregulated by neuronal hyperactivity drive TDP43 pathology in ALS
Weskamp, K., Tank, E. M. H., Miguez, R., McBride, J. P., Gómez, N., White, M. A., Lin, Z., Moreno-Gonzalez, C., Serio, A., Sreedharan, J., et al. (2019) · Journal of Clinical Investigation · doi:10.1172/jci130988 · Cited by 131
Self-citation
The absolute frequency of labeled N-6-methyladenosine in HeLa cell messenger RNA decreases with label time
Sommer, S. S., Lavi, U., & Darnell, J. E., Jr. (1978) · Journal of Molecular Biology · doi:10.1016/0022-2836(78)90183-3 · Cited by 130
Automated microscope system for determining factors that predict neuronal fate
Arrasate, M., & Finkbeiner, S. M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409777102 · Cited by 126
Amelioration of toxicity in neuronal models of amyotrophic lateral sclerosis by hUPF1
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Self-citation
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Giganti, M. J., Luz, P. M., Caro-Vega, Y. N., César, C., Padgett, D., Koenig, S. P., Echevarria, J. I., McGowan, C. C., & Shepherd, B. E. (2015) · AIDS Research and Human Retroviruses · doi:10.1089/aid.2014.0241 · Cited by 18
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RNA m6A modification, signals for degradation or stabilisation?
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Li, Y., Dou, X., Liu, J., Xiao, Y., Zhang, Z., Hayes, L. R., Wu, R., Fu, X., Ye, Y., Yang, B., et al. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01374-9 · Cited by 85
Membraneless organelles in health and disease: exploring the molecular basis, physiological roles and pathological implications
Li, Y., Liu, Y., Yu, X., Xu, Y., Pan, X., Sun, Y. E., Wang, Y., Song, Y.-H., & Shen, Z. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-02013-w · Cited by 72
RNA dysregulation in neurodegenerative diseases
Li, Y., & Sun, S. (2025) · The EMBO Journal · doi:10.1038/s44318-024-00352-6 · Cited by 65
Aberrant splicing in Huntington’s disease accompanies disrupted TDP-43 activity and altered m6A RNA modification
Nguyen, T. B., Miramontes, R., Chillón-Marinas, C., Maimon, R., Vazquez‐Sanchez, S., Lau, A., McClure, N. R., Wu, Z., Wang, K. Q., England, W., et al. (2025) · Nature Neuroscience · doi:10.1038/s41593-024-01850-w · Cited by 67

See all 117

Authors: McMillan, M., Gomez, N., Hsieh, C., Bekier, M., Li, X., Miguez, R., Tank, E. M. H., & Barmada, S. J.
Affiliations: University of Michigan (US)
Corresponding author: Barmada, Sami J.
ORCID: Bekier, Michael
Tank, Elizabeth M.H.
Barmada, Sami J.
Venue: Molecular Cell
Publisher: Elsevier BV
Published: 2023-01
Volume: 83
Issue: 2
Pages: 219-236.e7
ISSN: 1097-2765 (ISSN-L)
DOI: 10.1016/j.molcel.2022.12.019
PMC: PMC9899051
OpenAlex: W4315928462
Cited by: 112
References: 108
Citations by year: 2026: 31 · 2025: 34 · 2024: 32 · 2023: 15
FWCI: 18.26
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 383 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Molecular Cell (publishedVersion)
bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: University of Michigan (P30AG072931, UL1TR000433)
A. Alfred Taubman Medical Research Institute
National Institutes of Health (1r56ns128110-01, UL1TR000433, CA04659229, P30CA04659229)
Michigan Institute for Clinical and Health Research (MICHR, UL1TR000433, UL1TR000433)
Rogel Cancer Center, University of Michigan
National Institute on Aging (R21AG075368, P30AG072931)
National Cancer Institute (P30CA046592)
National Institute of General Medical Sciences (T32GM007863, T32GM145470)
National Institute of Neurological Disorders and Stroke (R56 NS128110, R01NS113943, R01NS097542)
National Center for Advancing Translational Sciences
Robert Packard Center for ALS Research, Johns Hopkins University
Topics: Health Sciences › Medicine › Clinical Neurology › Amyotrophic Lateral Sclerosis Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA modifications and cancer
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
Keywords: RNA methylation, N6-methyladenosine, TDP-43, amyotrophic lateral sclerosis, frontotemporal dementia, YTHDF2, RNA-binding proteins, RNA destabilization, neurodegeneration, spinal cord neurons
MeSH terms: Amyotrophic Lateral Sclerosis, DNA-Binding Proteins, Humans, Methylation, Neurons, RNA, Frontotemporal Dementia

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RNA methylation influences TDP43 binding and disease pathogenesis in models of amyotrophic lateral sclerosis and frontotemporal dementia

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