TLS (FUS) binds RNA in vivo and engages in nucleo-cytoplasmic shuttling
Abstract
TLS, the product of a gene commonly translocated in liposarcomas (TLS), is prototypical of a newly identified class of nuclear proteins that contain a C-terminal domain with a distinct RNA recognition motif (RRM) surrounded by Arg-Gly-Gly (RGG) repeats. Its unique N terminus serves as an essential transforming domain for a number of fusion oncoproteins in human sarcomas and leukemias. In this study we use an in vivo UV crosslinking procedure to probe the interactions of TLS with RNA. TLS is found to bind RNA in vivo and the association of TLS with RNA is rapidly diminished by treating cells with transcriptional inhibitors. This suggests that the species bound by TLS turns over rapidly. Surprisingly, the RRM was found to be dispensable for RNA binding by TLS in vivo, suggesting that at any one time most of the interactions between TLS and RNA in the cell are not sequence specific. Analysis of inter specific heterokaryons formed between human and mouse or Xenopus cells revealed that TLS engages in rapid nucleocytoplasmic shuttling, a finding confirmed by the ability of anti-TLS antibodies to trap TLS when injected into the cytoplasm of HeLa cells. Cellular fractionation experiments suggest that TLS binds to RNA in both the nucleus and cytoplasm and support the hypothesis that TLS functions as a heterogeneous ribonuclear protein (hnRNP)-like chaperone of RNA. These findings are discussed in the context of the role altered forms of TLS play in cellular transformation.
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FUS is a widely expressed, predominantly nuclear RNA-binding protein.
“Another ALS and FTLD gene, FUS156, is a widely expressed, predominantly nuclear RNA-binding protein176,177”
From The neurogenetics of alternative splicing (2016) · cites this paper as [177]
Cites
Schreiber, E. H., Matthias, P., Müller, M. M., & Schaffner, W. (1989) · Nucleic Acids Research · doi:10.1093/nar/17.15.6419 · Cited by 4,179 · see citing works
Gene fusion with an ETS DNA-binding domain caused by chromosome translocation in human tumours
Delattre, O., Zucman, J., Plougastel, B., Desmaze, C., Melot, T., Peter, M., Kovar, H., Joubert, I., de Jong, P., Rouleau, G., et al. (1992) · Nature · doi:10.1038/359162a0 · Cited by 1,907 · see citing works
Conserved Structures and Diversity of Functions of RNA-Binding Proteins
Burd, C. G., & Dreyfuss, G. (1994) · Science · doi:10.1126/science.8036511 · Cited by 1,878 · see citing works
Chromosomal translocations in human cancer
Rabbitts, T. H. (1994) · Nature · doi:10.1038/372143a0 · Cited by 1,490 · see citing works
Major nucleolar proteins shuttle between nucleus and cytoplasm
Borer, R. A., Lehner, C. F., Eppenberger, H. M., & Nigg, E. A. (1989) · Cell · doi:10.1016/0092-8674(89)90241-9 · Cited by 1,113 · see citing works
The C-terminal domain of RNA polymerase II couples mRNA processing to transcription
McCracken, S. A., Fong, N., Yankulov, K., Ballantyne, S. M., Pan, G., Greenblatt, J., Patterson, S. D., Wickens, M., & Bentley, D. L. (1997) · Nature · doi:10.1038/385357a0 · Cited by 925 · see citing works
Fusion of CHOP to a novel RNA-binding protein in human myxoid liposarcoma
Crozat, A., Åman, P., Mandahl, N., & Ron, D. (1993) · Nature · doi:10.1038/363640a0 · Cited by 893 · see citing works
Self-citationShuttling of pre-mRNA binding proteins between nucleus and cytoplasm
Piñol-Roma, S., & Dreyfuss, G. (1992) · Nature · doi:10.1038/355730a0 · Cited by 842 · see citing works
RNA recognition: towards identifying determinants of specificity
Kenan, D. J., Query, C. C., & Keene, J. D. (1991) · Trends in Biochemical Sciences · doi:10.1016/0968-0004(91)90088-d · Cited by 748 · see citing works
May, W. A., Gishizky, M. L., Lessnick, S. L., Lunsford, L. B., Lewis, B. C., Delattre, O., Zucman‐Rossi, J., Thomas, G. D., & Denny, C. T. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.12.5752 · Cited by 572 · see citing works
Michael, W. M., Choi, M., & Dreyfuss, G. (1995) · Cell · doi:10.1016/0092-8674(95)90119-1 · Cited by 528 · see citing works
May, W. A., Lessnick, S. L., Braun, B. S., Klemsz, M., Lewis, B. C., Lunsford, L. B., Hromas, R., & Denny, C. T. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.12.7393 · Cited by 497 · see citing works
Bertolotti, A., Lutz, Y., Heard, D. J., Chambon, P., & Tora, L. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00882.x · Cited by 364 · see citing works
Barone, M. V., Crozat, A., Tabaee, A., Philipson, L., & Ron, D. (1994) · Genes & Development · doi:10.1101/gad.8.4.453 · Cited by 336 · see citing works
Self-citationDreyfuss, G., Adam, S. A., & Choi, Y. D. (1984) · Molecular and Cellular Biology · doi:10.1128/mcb.4.3.415 · Cited by 326 · see citing works
Zinszner, H., Albalat, R., & Ron, D. (1994) · Genes & Development · doi:10.1101/gad.8.21.2513 · Cited by 261 · see citing works
Self-citationVisa, N., Alzhanova-Ericsson, A. T., Sun, X., Владимировна, К. Е., Björkroth, B., Wurtz, T., & Daneholt, B. (1996) · Cell · doi:10.1016/s0092-8674(00)80980-0 · Cited by 218 · see citing works
Ohno, T., Ouchida, M., Lee, L., Gatalica, Z., Rao, V. N., & Reddy, E. S. P. (1994) · PubMed · Cited by 188 · see citing works
hnRNP proteins:Localization and transport between the nucleus and the cytoplasm
Piñol-Roma, S., & Dreyfuss, G. (1993) · Trends in Cell Biology · doi:10.1016/0962-8924(93)90135-n · Cited by 160 · see citing works
Prasad, D. D. K., Ouchida, M., Lee, L., Rao, V. N., & Reddy, E. S. P. (1994) · PubMed · Cited by 147 · see citing works
Characterization of the major hnRNP proteins from Drosophila melanogaster.
Matunis, E. L., Matunis, M. J., & Dreyfuss, G. (1992) · The Journal of Cell Biology · doi:10.1083/jcb.116.2.257 · Cited by 133 · see citing works
Cross‐linking of mRNA to Proteins by Irradiation of Intact Cells with Ultraviolet Light
Wagenmakers, A. J. M., Reinders, R. J., & VENROOIJ, W. J. V. (1980) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1980.tb07207.x · Cited by 128 · see citing works
Identification of hnRNP P2 as TLS/FUS using electrospray mass spectrometry.
Calvio, C., Neubauer, G., Mann, M., & Lamond, A. I. (1995) · PubMed Central · Cited by 113 · see citing works
Sánchez-Garcı́a, I., & Rabbitts, T. H. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.17.7869 · Cited by 93 · see citing works
Economidis, I. V., & Pederson, T. (1983) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.80.6.1599 · Cited by 85 · see citing works
How fixed is the differentiated state?
Blau, H. M. (1989) · Trends in Genetics · doi:10.1016/0168-9525(89)90100-5 · Cited by 75 · see citing works
Stolow, D. T., & Haynes, S. R. (1995) · Nucleic Acids Research · doi:10.1093/nar/23.5.835 · Cited by 70 · see citing works
Zinszner, H., Immanuel, D., Yin, Y., Liang, F., & Ron, D. (1997) · Oncogene · doi:10.1038/sj.onc.1200854 · Cited by 66 · see citing works
Self-citationImmanuel, D., Zinszner, H., & Ron, D. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.8.4562 · Cited by 57 · see citing works
Self-citationTLS-CHOP and the Role of RNA-Binding Proteins in Oncogenic Transformation
Ron, D. (1997) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-60479-9_8 · Cited by 37 · see citing works
Self-citationHaynes (1992) · PubMed · Cited by 32 · see citing works
van Eekelen, C. A. G., Buijtels, H., Linné, T., OHLSSON, R. I., Philipson, L., & Venrooij, W. V. (1982) · Nucleic Acids Research · doi:10.1093/nar/10.10.3039 · Cited by 28 · see citing works
Chromosomal Translocations and Oncogenic Transcription Factors
Rauscher, F. J., & Vogt, P. K. (1997) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-60479-9 · Cited by 12 · see citing works
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3 of the 36 references couldn’t be matched to a known paper.
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Converging Mechanisms in ALS and FTD: Disrupted RNA and Protein Homeostasis
Ling, S.-C., Polymenidou, M., & Cleveland, D. W. (2013) · Neuron · doi:10.1016/j.neuron.2013.07.033 · Cited by 1,811 · see citing works
TDP-43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration
Lagier-Tourenne, C., Polymenidou, M., & Cleveland, D. W. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq137 · Cited by 1,021 · see citing works
TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia
Mackenzie, I. R., Rademakers, R., & Neumann, M. (2010) · The Lancet Neurology · doi:10.1016/s1474-4422(10)70195-2 · Cited by 977 · see citing works
The changing scene of amyotrophic lateral sclerosis
Robberecht, W., & Philips, T. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3430 · Cited by 957 · see citing works
ALS‐associated fused in sarcoma (FUS) mutations disrupt Transportin‐mediated nuclear import
Dormann, D., Rodde, R., Edbauer, D., Bentmann, E., Fischer, I., Hruscha, A., Than, M. E., Mackenzie, I. R. A., Capell, A., Schmid, B., et al. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.143 · Cited by 836 · see citing works
Han, T. W., Kato, M., Xie, S., Wu, L. C., Mirzaei, H., Pei, J., Chen, M., Xie, Y., Allen, J. D., Xiao, G., et al. (2012) · Cell · doi:10.1016/j.cell.2012.04.016 · Cited by 758 · see citing works
ALS Genetics, Mechanisms, and Therapeutics: Where Are We Now?
Mejzini, R., Flynn, L. L., Pitout, I. L., Fletcher, S., Wilton, S. D., & Akkari, P. A. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01310 · Cited by 755 · see citing works
A new subtype of frontotemporal lobar degeneration with FUS pathology
Neumann, M., Rademakers, R., Roeber, S., Baker, M., Kretzschmar, H. A., & Mackenzie, I. R. A. (2009) · Brain · doi:10.1093/brain/awp214 · Cited by 722 · see citing works
The tip of the iceberg: RNA-binding proteins with prion-like domains in neurodegenerative disease
King, O. D., Gitler, A. D., & Shorter, J. (2012) · Brain Research · doi:10.1016/j.brainres.2012.01.016 · Cited by 637 · see citing works
Protein aggregation in amyotrophic lateral sclerosis
Blokhuis, A. M., Groen, E. J. N., Koppers, M., van den Berg, L. H., & Pasterkamp, R. J. (2013) · Acta Neuropathologica · doi:10.1007/s00401-013-1125-6 · Cited by 573 · see citing works
Mutant FUS proteins that cause amyotrophic lateral sclerosis incorporate into stress granules
Bosco, D. A., Lemay, N., Ko, H. K., Zhou, H., Burke, C., Kwiatkowski, T. J., Sapp, P. C., McKenna-Yasek, D. M., Brown, R. H., & Hayward, L. J. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq335 · Cited by 520 · see citing works
Sun, Z., Diaz, Z., Fang, X., Hart, M. P., Chesi, A., Shorter, J., & Gitler, A. D. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1000614 · Cited by 448 · see citing works
ALS Genetics: Gains, Losses, and Implications for Future Therapies
Kim, G., Gautier, O., Tassoni-Tsuchida, E., Ma, X. R., & Gitler, A. D. (2020) · Neuron · doi:10.1016/j.neuron.2020.08.022 · Cited by 370 · see citing works
The role of FUS gene variants in neurodegenerative diseases
Deng, H., Gao, K., & Jankovic, J. J. (2014) · Nature Reviews Neurology · doi:10.1038/nrneurol.2014.78 · Cited by 357 · see citing works
The neurogenetics of alternative splicing
Vuong, C. K., Black, D. L., & Zheng, S. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.27 · Cited by 340 · see citing works
Biology of EWS/ETS fusions in Ewing's family tumors
Arvand, A., & Denny, C. T. (2001) · Oncogene · doi:10.1038/sj.onc.1204598 · Cited by 347 · see citing works
Andersson, M. K., Ståhlberg, A., Arvidsson, Y., Olofsson, A., Semb, H., Stenman, G., Nilsson, O., & Åman, P. (2008) · BMC Cell Biology · doi:10.1186/1471-2121-9-37 · Cited by 346 · see citing works
Mutations in TDP-43 link glycine-rich domain functions to amyotrophic lateral sclerosis
Pesiridis, G. S., Lee, V. M.-Y., & Trojanowski, J. Q. (2009) · Human Molecular Genetics · doi:10.1093/hmg/ddp303 · Cited by 324 · see citing works
Fujii, R., Okabe, S., Urushido, T., Inoue, K., Yoshimura, A., Tachibana, T., Nishikawa, T., Hicks, G. G., & Takumi, T. (2005) · Current Biology · doi:10.1016/j.cub.2005.01.058 · Cited by 322 · see citing works
Neumann, M., Bentmann, E., Dormann, D., Jawaid, A., DeJesus‐Hernandez, M., Ansorge, O., Roeber, S., Kretzschmar, H. A., Muñoz, D. G., Kusaka, H., et al. (2011) · Brain · doi:10.1093/brain/awr201 · Cited by 302 · see citing works
The TET Family of Proteins: Functions and Roles in Disease
Tan, A. Y., & Manley, J. L. (2009) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjp025 · Cited by 271 · see citing works
Mastrocola, A. S., Kim, S. H., Trinh, A. T., Rodenkirch, L. A., & Tibbetts, R. S. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.497974 · Cited by 262 · see citing works
Abundant FUS-immunoreactive pathology in neuronal intermediate filament inclusion disease
Neumann, M., Roeber, S., Kretzschmar, H. A., Rademakers, R., Baker, M. C., & Mackenzie, I. R. (2009) · Acta Neuropathologica · doi:10.1007/s00401-009-0581-5 · Cited by 257 · see citing works
FUS pathology in basophilic inclusion body disease
Muñoz, D. G., Neumann, M., Kusaka, H., Yokota, O., Ishihara, K., Terada, S., Kuroda, S., & Mackenzie, I. R. (2009) · Acta Neuropathologica · doi:10.1007/s00401-009-0598-9 · Cited by 253 · see citing works
TLS facilitates transport of mRNA encoding an actin-stabilizing protein to dendritic spines
Fujii, R., & Takumi, T. (2005) · Journal of Cell Science · doi:10.1242/jcs.02692 · Cited by 245 · see citing works
Male sterility and enhanced radiation sensitivity in TLS−/− mice
Kuroda, M., Sok, J., Webb, L., Baechtold, H., Urano, F., Yin, Y., Chung, P., de Rooij, D. G., Akhmedov, A., Ashley, T., et al. (2000) · The EMBO Journal · doi:10.1093/emboj/19.3.453 · Cited by 244 · see citing works
Self-citationFUS stimulates microRNA biogenesis by facilitating co‐transcriptional Drosha recruitment
Morlando, M., Modigliani, S. D., Torrelli, G., Rosa, A., Carlo, V. D., Caffarelli, E., & Bozzoni, I. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.319 · Cited by 229 · see citing works
Biochemical Properties and Biological Functions of FET Proteins
Schwartz, J. C., Cech, T. R., & Parker, R. (2014) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-060614-034325 · Cited by 230 · see citing works
Atasoy, U., Watson, J., Patel, D. D., & Keene, J. D. (1998) · Journal of Cell Science · doi:10.1242/jcs.111.21.3145 · Cited by 226 · see citing works
SARS-CoV-2 requires cholesterol for viral entry and pathological syncytia formation
Sanders, D. W., Jumper, C. C., Ackerman, P. J., Bracha, D., Donlic, A., Kim, H., Kenney, D., Castello-Serrano, I., Suzuki, S., Tamura, T., et al. (2021) · eLife · doi:10.7554/elife.65962 · Cited by 215 · see citing works
Oncoprotein TLS Interacts with Serine-Arginine Proteins Involved in RNA Splicing
Yang, L., Embree, L. J., Tsai, S., & Hickstein, D. D. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.43.27761 · Cited by 224 · see citing works
Lashley, T., Rohrer, J. D., Mead, S., & Révész, T. (2015) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12250 · Cited by 217 · see citing works
Nuclear localization sequence of FUS and induction of stress granules by ALS mutants
Gál, J., Zhang, J. Y., Kwinter, D. M., Zhai, J., Jia, H., Jia, J., & Zhu, H. (2010) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2010.06.010 · Cited by 215 · see citing works
Kim, S. H., Shanware, N. P., Bowler, M. J., & Tibbetts, R. S. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.154831 · Cited by 213 · see citing works
TDP-43 and FUS: a nuclear affair
Dormann, D., & Haass, C. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.05.002 · Cited by 214 · see citing works
ALS-Associated FUS Mutations Result in Compromised FUS Alternative Splicing and Autoregulation
Zhou, Y., Liu, S., Liu, G., Öztürk, A., & Hicks, G. G. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003895 · Cited by 210 · see citing works
Liposarcoma: Molecular Genetics and Therapeutics
Conyers, R. K., Young, S., & Thomas, D. M. (2010) · Sarcoma · doi:10.1155/2011/483154 · Cited by 213 · see citing works
Huang, C., Zhou, H., Tong, J., Chen, H., Liu, Y., Wang, D., Wei, X., & Xia, X. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002011 · Cited by 206 · see citing works
Daigle, J. G., Lanson, N. A., Smith, R. B., Casci, I., Maltare, A., Monaghan, J., Nichols, C. D., Kryndushkin, D. S., Shewmaker, F. P., & Pandey, U. B. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds526 · Cited by 206 · see citing works
Lanson, N. A., Maltare, A., King, H., Smith, R. B., Kim, J. H., Taylor, J. P., Lloyd, T. E., & Pandey, U. B. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr150 · Cited by 198 · see citing works
TLS, EWS and TAF15: a model for transcriptional integration of gene expression
Law, W. J. (2006) · Briefings in Functional Genomics and Proteomics · doi:10.1093/bfgp/ell015 · Cited by 200 · see citing works
FUS Interacts with HSP60 to Promote Mitochondrial Damage
Deng, J., Yang, M., Chen, Y., Chen, X., Liu, J., Sun, S., Cheng, H., Li, Y., Bigio, E. H., Mesulam, M. M., et al. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005357 · Cited by 188 · see citing works
Identification of an RNA Binding Specificity for the Potential Splicing Factor TLS
Lerga, A., Hallier, M., Delva, L., Orvain, C., Gallais, I., Marie, J., & Moreau-Gachelin, F. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m008304200 · Cited by 189 · see citing works
Mackenzie, I. R. A., Ansorge, O., Strong, M., Bilbao, J., Zinman, L., Ang, L.-C., Baker, M., Stewart, H., Eisen, A., Rademakers, R., et al. (2011) · Acta Neuropathologica · doi:10.1007/s00401-011-0838-7 · Cited by 183 · see citing works
FUS/TLS assembles into stress granules and is a prosurvival factor during hyperosmolar stress
Sama, R. R. K., Ward, C. L., Kaushansky, L. J., Lemay, N., Ishigaki, S., Urano, F., & Bosco, D. A. (2013) · Journal of Cellular Physiology · doi:10.1002/jcp.24395 · Cited by 178 · see citing works
EWS–ETS oncoproteins: The linchpins of Ewing tumors
Janknecht, R. (2005) · Gene · doi:10.1016/j.gene.2005.08.007 · Cited by 173 · see citing works
Baechtold, H., Kuroda, M., Sok, J. C., Ron, D., López, B. S., & Akhmedov, A. T. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.48.34337 · Cited by 171 · see citing works
Self-citationDomain Architectures and Characterization of an RNA-binding Protein, TLS
Iko, Y., Kodama, T. S., Kasai, N., Oyama, T., Morita, E. H., Muto, T., Okumura, M., Fujii, R., Takumi, T., Tate, S.-I., et al. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m408552200 · Cited by 168 · see citing works
Mutations of FUS gene in sporadic amyotrophic lateral sclerosis
Corrado, L., Bo, R. D., Castellotti, B., Ratti, A., Cereda, C., Penco, S., Sorarú, G., Carlomagno, Y., Ghezzi, S., Pensato, V., et al. (2009) · Journal of Medical Genetics · doi:10.1136/jmg.2009.071027 · Cited by 170 · see citing works
Distinct pathological subtypes of FTLD-FUS
Mackenzie, I. R., Muñoz, D. G., Kusaka, H., Yokota, O., Ishihara, K., Roeber, S., Kretzschmar, H. A., Cairns, N. J., & Neumann, M. (2010) · Acta Neuropathologica · doi:10.1007/s00401-010-0764-0 · Cited by 168 · see citing works
TDP ‐43 and FUS en route from the nucleus to the cytoplasm
Ederle, H., & Dormann, D. (2017) · FEBS Letters · doi:10.1002/1873-3468.12646 · Cited by 169 · see citing works
Ticozzi, N., Vance, C. A., LeClerc, A. L., Keagle, P. J., Glass, J. D., McKenna‐Yasek, D., Sapp, P. C., Silani, V., Bosco, D. A., Shaw, C. E., et al. (2011) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.31158 · Cited by 168 · see citing works
FUS is Phosphorylated by DNA-PK and Accumulates in the Cytoplasm after DNA Damage
Deng, Q., Holler, C. J., Taylor, G., Hudson, K. F., Watkins, W., Gearing, M., Ito, D., Murray, M. E., Dickson, D. W., Seyfried, N. T., et al. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0172-14.2014 · Cited by 161 · see citing works
Analysis of FUS gene mutation in familial amyotrophic lateral sclerosis within an Italian cohort
Ticozzi, N., Silani, V., LeClerc, A. L., Keagle, P. J., Gellera, C., Ratti, A., Taroni, F., Kwiatkowski, T. J., McKenna‐Yasek, D., Sapp, P. C., et al. (2009) · Neurology · doi:10.1212/wnl.0b013e3181bbff05 · Cited by 160 · see citing works
Nomura, T., Watanabe, S., Kaneko, K., Yamanaka, K., Nukina, N., & Furukawa, Y. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.516492 · Cited by 160 · see citing works
Amyotrophic lateral sclerosis-linked FUS/TLS alters stress granule assembly and dynamics
Baron, D. M., Kaushansky, L. J., Ward, C. L., Sama, R. R. K., Chian, R.-J., Boggio, K. J., Quaresma, A. J. C., Nickerson, J. A., & Bosco, D. A. (2013) · Molecular Neurodegeneration · doi:10.1186/1750-1326-8-30 · Cited by 154 · see citing works
Mechanisms of FUS mutations in familial amyotrophic lateral sclerosis
Shang, Y., & Huang, E. J. (2016) · Brain Research · doi:10.1016/j.brainres.2016.03.036 · Cited by 154 · see citing works
ALS-associated mutations in FUS disrupt the axonal distribution and function of SMN
Groen, E. J. N., Fumoto, K., Blokhuis, A. M., Engelen-Lee, J.-Y., Zhou, Y., van den Heuvel, D. M. A., Koppers, M., van Diggelen, F., van Heest, J., Demmers, J., et al. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt222 · Cited by 152 · see citing works
De novo truncating FUS gene mutation as a cause of sporadic amyotrophic lateral sclerosis
DeJesus‐Hernandez, M., Kocerha, J., Finch, N. A., Crook, R., Baker, M. C., Desaro, P., Johnston, A., Rutherford, N. J., Wojtas, A., Kennelly, K. D., et al. (2010) · Human Mutation · doi:10.1002/humu.21241 · Cited by 150 · see citing works
Ewing sarcoma gene EWS is essential for meiosis and B lymphocyte development
Li, K., Watford, W. T., Li, C., Parmelee, A., Bryant, M., Deng, C., O’Shea, J. J., & Lee, S. B. (2007) · Journal of Clinical Investigation · doi:10.1172/jci31222 · Cited by 151 · see citing works
Lee, S., Neumann, M., Stearman, R. S., Stauber, R. H., Pause, A., Pavlakis, G. N., & Klausner, R. D. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.2.1486 · Cited by 142 · see citing works
Uversky, V. N. (2010) · Expert Review of Proteomics · doi:10.1586/epr.10.36 · Cited by 141 · see citing works
Lenzi, J., Santis, R. D., de Turris, V., Morlando, M., Laneve, P., Calvo, A., Caliendo, V., Chiò, A., Rosa, A., & Bozzoni, I. (2015) · Disease Models & Mechanisms · doi:10.1242/dmm.020099 · Cited by 140 · see citing works
Novel FUS/TLS Mutations and Pathology in Familial and Sporadic Amyotrophic Lateral Sclerosis
Hewitt, C., Kirby, J., Highley, J. R., Hartley, J. A., Hibberd, R., Hollinger, H. C., Williams, T. L., Ince, P. G., McDermott, C. J., & Shaw, P. J. (2010) · Archives of Neurology · doi:10.1001/archneurol.2010.52 · Cited by 139 · see citing works
Fused in sarcoma (FUS): An oncogene goes awry in neurodegeneration
Dormann, D., & Haass, C. (2013) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2013.03.006 · Cited by 134 · see citing works
Dr. Jekyll and Mr. Hyde: The Two Faces of the FUS/EWS/TAF15 Protein Family
Kovar, H. (2010) · Sarcoma · doi:10.1155/2011/837474 · Cited by 137 · see citing works
TLS-ERG Leukemia Fusion Protein Inhibits RNA Splicing Mediated by Serine-Arginine Proteins
Yang, L., Embree, L. J., & Hickstein, D. D. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.10.3345-3354.2000 · Cited by 129 · see citing works
Functions of FUS/TLS From DNA Repair to Stress Response: Implications for ALS
Sama, R. R. K., Ward, C. L., & Bosco, D. A. (2014) · ASN NEURO · doi:10.1177/1759091414544472 · Cited by 128 · see citing works
Perrotti, D., Bonatti, S., Trotta, R., Martinez, R., Skorski, T., Salomoni, P., Grassilli, E., Iozzo, R. V., Cooper, D. R., & Calabretta, B. (1998) · The EMBO Journal · doi:10.1093/emboj/17.15.4442 · Cited by 128 · see citing works
Saunders, L. R., Perkins, D. J., Balachandran, S., Michaels, R., Ford, R. J., Mayeda, A., & Barber, G. N. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m104207200 · Cited by 126 · see citing works
Fus gene mutations in familial and sporadic amyotrophic lateral sclerosis
Rademakers, R., Stewart, H. G., DeJesus‐Hernandez, M., Krieger, C., Graff‐Radford, N. R., Fabros, M., Briemberg, H., Cashman, N. R., Eisen, A., & Mackenzie, I. R. (2010) · Muscle & Nerve · doi:10.1002/mus.21665 · Cited by 126 · see citing works
Kamelgarn, M., Chen, J., Kuang, L., Arenas, A., Zhai, J., Zhu, H., & Gál, J. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2016.07.015 · Cited by 125 · see citing works
The Ewing's sarcoma gene product functions as a transcriptional activator.
Rossow, K. L., & Janknecht, R. (2001) · PubMed · Cited by 121 · see citing works
Minor intron splicing is regulated by FUS and affected by ALS‐associated FUS mutants
Reber, S., Stettler, J., Filosa, G., Colombo, M., Jutzi, D., Lenzken, S. C., Schweingruber, C., Bruggmann, R., Bachi, A., Barabino, S. M. L., et al. (2016) · The EMBO Journal · doi:10.15252/embj.201593791 · Cited by 120 · see citing works
Doi, H., Okamura, K., Bauer, P. O., Furukawa, Y., Shimizu, H., Kurosawa, M., Machida, Y., Miyazaki, H., Mitsui, K., Kuroiwa, Y., et al. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m705306200 · Cited by 120 · see citing works
Iervolino, A., Santilli, G., Trotta, R., Guerzoni, C., Cesi, V., Bergamaschi, A., Gambacorti-Passerini, C. B., Calabretta, B., & Perrotti, D. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.7.2255-2266.2002 · Cited by 120 · see citing works
The role of hnRNPs in frontotemporal dementia and amyotrophic lateral sclerosis
Bampton, A., Gittings, L. M., Fratta, P., Lashley, T., & Gatt, A. P. (2020) · Acta Neuropathologica · doi:10.1007/s00401-020-02203-0 · Cited by 118 · see citing works
Rhoads, S. N., Monahan, Z. T., Yee, D. S., & Shewmaker, F. P. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19030886 · Cited by 115 · see citing works
Identification of Mammalian Proteins Cross-linked to DNA by Ionizing Radiation
Barker, S., Weinfeld, M., Zheng, J., Li, L., & Murray, D. L. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m502477200 · Cited by 115 · see citing works
Identification and characterization of FUS/TLS as a new target of ATM
Gardiner, M., Toth, R., Vandermoere, F., Morrice, N. A., & Rouse, J. (2008) · Biochemical Journal · doi:10.1042/bj20081135 · Cited by 111 · see citing works
Åman, P. (1999) · Seminars in Cancer Biology · doi:10.1006/scbi.1999.0130 · Cited by 111 · see citing works
Meißner, M., Lopato, S., Gotzmann, J., Sauermann, G., & Barta, A. (2003) · Experimental Cell Research · doi:10.1016/s0014-4827(02)00046-0 · Cited by 109 · see citing works
Role of FET proteins in neurodegenerative disorders
Svetoni, F., Frisone, P., & Paronetto, M. P. (2016) · RNA Biology · doi:10.1080/15476286.2016.1211225 · Cited by 107 · see citing works
Lee, M., Ghosh, U., Thurber, K. R., Kato, M., & Tycko, R. (2020) · Nature Communications · doi:10.1038/s41467-020-19512-3 · Cited by 107 · see citing works
Belly, A., Moreau-Gachelin, F., Sadoul, R., & Goldberg, Y. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2004.12.071 · Cited by 107 · see citing works
Zhang, D., Paley, A. J., & Childs, G. J. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.29.18086 · Cited by 107 · see citing works
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 107 · see citing works
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 105 · see citing works
Fushimi, K., Long, C., Jayaram, N., Chen, X., Li, L., & Wu, J. Y. (2011) · Protein & Cell · doi:10.1007/s13238-011-1014-5 · Cited by 104 · see citing works
Koyuncu, S., Saez, I., Lee, H. J., Gutiérrez-García, R., Pokrzywa, W., Fatima, A., Hoppe, T., & Vilchez, D. (2018) · Nature Communications · doi:10.1038/s41467-018-05320-3 · Cited by 97 · see citing works
Halliday, G. M., Bigio, E. H., Cairns, N. J., Neumann, M., Mackenzie, I. R., & Mann, D. M. A. (2012) · Acta Neuropathologica · doi:10.1007/s00401-012-1030-4 · Cited by 98 · see citing works
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 98 · see citing works
Expression of human FUS protein in Drosophila leads to progressive neurodegeneration
Chen, Y., Yang, M., Deng, J., Chen, X., Ye, Y., Zhu, L., Liu, J., Ye, H., Shen, Y., Li, Y., et al. (2011) · Protein & Cell · doi:10.1007/s13238-011-1065-7 · Cited by 103 · see citing works
Xia, R., Liu, Y., Yang, L., Gál, J., Zhu, H., & Jia, J. (2012) · Molecular Neurodegeneration · doi:10.1186/1750-1326-7-10 · Cited by 102 · see citing works
Farg, M. A., Soo, K. Y., Walker, A. K., Pham, H., Orian, J. M., Horne, M. K., Warraich, S. T., Williams, K. L., Blair, I. P., & Atkin, J. D. (2012) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2012.02.009 · Cited by 101 · see citing works
Fused in Sarcoma: Properties, Self-Assembly and Correlation with Neurodegenerative Diseases
Chen, C., Ding, X., Akram, N., Xue, S., & Luo, S. (2019) · Molecules · doi:10.3390/molecules24081622 · Cited by 96 · see citing works
Liu, C., Zhang, Y., She, X., Li, F., Li, P., Feng, J., Fu, H., Liu, Q., Liu, Q., Zhao, C., et al. (2018) · Journal of Hematology & Oncology · doi:10.1186/s13045-018-0619-z · Cited by 93 · see citing works
Lashley, T., Rohrer, J. D., Bandopadhyay, R., Fry, C., Ahmed, Z., Isaacs, A. M., Brelstaff, J., Borroni, B., Warren, J. D., Troakes, C., et al. (2011) · Brain · doi:10.1093/brain/awr160 · Cited by 93 · see citing works
PRMT1 mediated methylation of TAF15 is required for its positive gene regulatory function
Jobert, L., Argentini, M., & Tora, L. (2008) · Experimental Cell Research · doi:10.1016/j.yexcr.2008.12.008 · Cited by 91 · see citing works
Kryndushkin, D. S., Wickner, R. B., & Shewmaker, F. P. (2011) · Protein & Cell · doi:10.1007/s13238-011-1525-0 · Cited by 88 · see citing works
- Authors
- Zinszner, H., Sok, J., Immanuel, D., Yin, Y., & Ron, D.
- Affiliations
- Skirball Institute of Biomolecular Medicine, the Departments of Medicine, Cell Biology and the Kaplan Cancer Center, NYU Medical Center, New York, NY 10016, USA
- NYU Langone Health (US)
- ORCID
- Venue
- Journal of Cell Science
- Publisher
- The Company of Biologists
- Published
- 1997-08-01
- Volume
- 110
- Issue
- 15
- Pages
- 1741-1750
- ISSN
- 0021-9533 (ISSN-L)
- 1477-9137
- OpenAlex
- W2115670698
- Cited by
- 350
- References
- 36
- Citations by year
- 2026: 2 · 2025: 12 · 2024: 5 · 2023: 14 · 2022: 17 · 2021: 19 · 2020: 22 · 2019: 13 · 2018: 21 · 2017: 14 · 2016: 18 · 2015: 15 · 2014: 18 · 2013: 17 · 2012: 29
- FWCI
- 1.90
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Cell Science (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ca060945-09)
- National Cancer Institute (CA-60945)
- National Institute of General Medical Sciences (5T32GM07038)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Sarcoma Diagnosis and Treatment
- Keywords
- TLS, RNA recognition motif, RNA binding, nucleocytoplasmic shuttling, fusion oncoproteins, cell transformation, transcription inhibitors, heterokaryons, UV crosslinking
- MeSH terms
- Animals, Cell Nucleus, Centrifugation, Density Gradient, Cytoplasm, Dactinomycin, HeLa Cells, Humans, Ribonucleoproteins, RNA, Ultraviolet Rays, Xenopus, RNA-Binding Proteins, Coculture Techniques, Nucleic Acid Synthesis Inhibitors, COS Cells, Heterogeneous-Nuclear Ribonucleoproteins, RNA-Binding Protein FUS, Mice
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