Lu, L.; Zheng, L.; Si, Y.; Luo, W.; Dujardin, G.; Kwan, T.; Potochick, N.R.; Thompson, S.R.; Schneider, D.A.; King, P.H. "Hu antigen R (HuR) is a positive regulator of the RNA-binding proteins TDP-43 and FUS/TLS: Implications for amyotrophic lateral sclerosis" (2014) Journal of Biological Chemistry. 289(46):31792-31804
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Posttranscriptional gene regulation is governed by a network of RNA-binding proteins (RBPs) that interact with regulatory elements in the mRNA to modulate multiple molecular processes, including splicing, RNA transport, RNA stability, and translation. Mounting evidence indicates that there is a hierarchy within this network whereby certain RBPs cross-regulate other RBPs to coordinate gene expression. HuR, an RNA-binding protein we linked previously to aberrant VEGF mRNA metabolism in models of SOD1-associated amyotrophic lateral sclerosis, has been identified as being high up in this hierarchy, serving as a regulator of RNA regulators. Here we investigated the role of HuR in regulating two RBPs, TDP-43 and FUS/TLS, that have been linked genetically to amyotrophic lateral sclerosis. Wefound thatHuRpromotes the expression of both RBPs in primary astrocytes and U251 cells under normal and stressed (hypoxic) conditions. For TDP-43, we found that HuR binds to the 3' untranslated region (UTR) and regulates its expression through translational efficiency rather than RNA stability. With HuR knockdown, there was a shift of TDP-43 and FUS mRNAs away from polysomes, consistent with translational silencing. The TDP-43 splicing function was attenuated upon HuR knockdown and could be rescued by ectopic TDP-43 lacking the 3' UTR regulatory elements. Finally, conditioned medium from astrocytes in which HuR or TDP-43 was knocked down produced significant motor neuron and cortical neuron toxicity in vitro. These findings indicate that HuR regulates TDP-43 and FUS/TLS expression and that loss of HuR-mediated RNA processing in astrocytes can alter the molecular and cellular landscape to produce a toxic phenotype. © 2014 by The American Society for Biochemistry and Molecular Biology, Inc.


Documento: Artículo
Título:Hu antigen R (HuR) is a positive regulator of the RNA-binding proteins TDP-43 and FUS/TLS: Implications for amyotrophic lateral sclerosis
Autor:Lu, L.; Zheng, L.; Si, Y.; Luo, W.; Dujardin, G.; Kwan, T.; Potochick, N.R.; Thompson, S.R.; Schneider, D.A.; King, P.H.
Filiación:Department of Neurology, University of Alabama at Birmingham, Sparks Center, 1720 7th Ave. S., Birmingham, AL 35294, 35233-0017, United States
Department of Genetics, University of Alabama at Birmingham, Birmingham, AL 35294, United States
Department of Cell, Developmental, and Integrative Biolog, University of Alabama at Birmingham, Birmingham, AL 35294, United States
Department of Microbiology, University of Alabama at Birmingham, Birmingham, AL 35294, United States
Department of Biochemistry and Molecular Genetics, University of Alabama at Birmingham, Birmingham, AL 35294, United States
Birmingham Veterans Affairs Medical Center, Birmingham, AL 35294, United States
Facultad de Ciencias Exactas, Naturales Universidad de Buenos Aires, Buenos Aires, C1428EHA, Argentina
Palabras clave:Gene expression; Genes; Neurodegenerative diseases; Neurons; Proteins; RNA; Amyotrophic lateral sclerosis; Conditioned medium; Molecular process; Post-transcriptional gene regulation; Regulatory elements; RNA-binding protein; Translational efficiencies; Untranslated regions; Nucleic acids; cystic fibrosis transmembrane conductance regulator; fused in sarcoma protein; Hu antigen R; RNA binding protein; TAR DNA binding protein; unclassified drug; 3' untranslated region; CFTR protein, human; culture medium; cystic fibrosis transmembrane conductance regulator; DNA binding protein; ELAVL1 protein, human; Hu antigen; protein TDP-43; RNA; RNA binding protein; 3' untranslated region; amyotrophic lateral sclerosis; animal cell; Article; astrocyte; autoregulation; binding affinity; biotinylation; cell viability; controlled study; densitometry; immunoprecipitation; motoneuron; mouse; nonhuman; open reading frame; phenotype; polyadenylation; polysome; protein analysis; protein binding; protein expression; protein function; RNA isolation; RNA processing; amyotrophic lateral sclerosis; animal; anoxia; cell line; cell survival; chemistry; culture medium; cytology; gene expression regulation; genetics; human; metabolism; tumor cell line; 3' Untranslated Regions; Amyotrophic Lateral Sclerosis; Animals; Anoxia; Astrocytes; Cell Line; Cell Line, Tumor; Cell Survival; Culture Media, Conditioned; Cystic Fibrosis Transmembrane Conductance Regulator; DNA-Binding Proteins; Gene Expression Regulation; Hu Paraneoplastic Encephalomyelitis Antigens; Humans; Mice; Motor Neurons; Phenotype; RNA; RNA-Binding Protein FUS
Página de inicio:31792
Página de fin:31804
Título revista:Journal of Biological Chemistry
Título revista abreviado:J. Biol. Chem.
CAS:cystic fibrosis transmembrane conductance regulator, 126880-72-6; RNA, 63231-63-0; 3' Untranslated Regions; CFTR protein, human; Culture Media, Conditioned; Cystic Fibrosis Transmembrane Conductance Regulator; DNA-Binding Proteins; ELAVL1 protein, human; Hu Paraneoplastic Encephalomyelitis Antigens; protein TDP-43; RNA; RNA-Binding Protein FUS


  • Robberecht, W., Philips, T., The changing scene of amyotrophic lateral sclerosis (2013) Nat. Rev. Neurosci., 14, pp. 248-264
  • Buratti, E., Baralle, F.E., TDP-43: New aspects of autoregulation mechanisms in RNA binding proteins and their connection with human disease (2011) FEBS J., 278, pp. 3530-3538
  • Zhou, Y., Liu, S., Liu, G., Oztürk, A., Hicks, G.G., ALS-associated FUS mutations result in compromised FUS alternative splicing and autoregulation (2013) PLoS Genet, 9, p. e1003895
  • Huelga, S.C., Vu, A.Q., Arnold, J.D., Liang, T.Y., Liu, P.P., Yan, B.Y., Donohue, J.P., Yeo, G.W., Integrative genome-wide analysis reveals cooperative regulation of alternative splicing by hnRNP proteins (2012) Cell Rep, 1, pp. 167-178
  • Pullmann, R., Jr., Kim, H.H., Abdelmohsen, K., Lal, A., Martindale, J.L., Yang, X., Gorospe, M., Analysis of turnover and translation regulatory RNA-binding protein expression through binding to cognate mRNAs (2007) Mol. Cell Biol., 27, pp. 6265-6278
  • Ni, J.Z., Grate, L., Donohue, J.P., Preston, C., Nobida, N., O'Brien, G., Shiue, L., Ares, M., Jr., Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay (2007) Genes Dev, 21, pp. 708-718
  • Polymenidou, M., Lagier-Tourenne, C., Hutt, K.R., Huelga, S.C., Moran, J., Liang, T.Y., Ling, S.C., Cleveland, D.W., Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43 (2011) Nat. Neurosci., 14, pp. 459-468
  • Dassi, E., Zuccotti, P., Leo, S., Provenzani, A., Assfalg, M., D'Onofrio, M., Riva, P., Quattrone, A., Hyper conserved elements in vertebrate mRNA 3'-UTRs reveal a translational network of RNA-binding proteins controlled by HuR (2013) Nucleic Acids Res, 41, pp. 3201-3216
  • Mukherjee, N., Corcoran, D.L., Nusbaum, J.D., Reid, D.W., Georgiev, S., Hafner, M., Ascano, M., Jr., Keene, J.D., Integrative regulatory mapping indicates that the RNA-binding protein HuR couples pre-mRNA processing and mRNA stability (2011) Mol. Cell., 43, pp. 327-339
  • Abdelmohsen, K., Kuwano, Y., Kim, H.H., Gorospe, M., Posttranscriptional gene regulation by RNA-binding proteins during oxidative stress: Implications for cellular senescence (2008) Biol. Chem., 389, pp. 243-255
  • Srikantan, S., Gorospe, M., HuR function in disease (2012) Front. Biosci. (Landmark Ed), 17, pp. 189-205
  • Brennan, C.M., Steitz, J.A., HuR andmRNAstability (2001) Cell. Mol. Life Sci., 58, pp. 266-277
  • Burkhart, R.A., Pineda, D.M., Chand, S.N., Romeo, C., Londin, E.R., Karoly, E.D., Cozzitorto, J.A., Winter, J.M., HuR is a post-transcriptional regulator of core metabolic enzymes in pancreatic cancer (2013) RNA Biol, 10, pp. 1312-1323
  • Lu, L., Wang, S., Zheng, L., Li, X., Suswam, E.A., Zhang, X., Wheeler, C.G., King, P.H., Amyotrophic lateral sclerosis-linked mutant SOD1 sequesters Hu antigen R (HuR) and TIA-1 related protein (TIAR): Implications for impaired posttranscriptional regulation of vascular endothelial growth factor (2009) J. Biol. Chem., 284, pp. 33989-33998
  • Lu, L., Zheng, L., Viera, L., Suswam, E., Li, Y., Li, X., Estévez, A.G., King, P.H., Mutant Cu/Zn-superoxide dismutase associated with amyotrophic lateral sclerosis destabilizes vascular endothelial growth factor mRNA and downregulates its expression (2007) J. Neurosci., 27, pp. 7929-7938
  • Li, X., Lin, W.J., Chen, C.Y., Si, Y., Zhang, X., Lu, L., Suswam, E., King, P.H., KSRP: A checkpoint for inflammatory cytokine production in astrocytes (2012) Glia, 60, pp. 1773-1784
  • Fallini, C., Bassell, G.J., Rossoll, W., High-efficiency transfection of cultured primary motor neurons to study protein localization, trafficking, and function (2010) Mol. Neurodegener., 5, p. 17
  • Kaech, S., Banker, G., Culturing hippocampal neurons (2006) Nat. Protoc., 1, pp. 2406-2415
  • Nabors, L.B., Suswam, E., Huang, Y., Yang, X., Johnson, M.J., King, P.H., Tumor necrosis factor-α induces angiogenic factor up-regulation in malignant glioma cells: A role for RNA stabilization and HuR (2003) Cancer Res, 63, pp. 4181-4187
  • Lin, W.-J., Duffy, A., Chen, C.-Y., Localization of AU-rich elementcontaining mRNA in cytoplasmic granules containing exosome subunits (2007) J. Biol. Chem., 282, pp. 19958-19968
  • Dujardin, G., Buratti, E., Charlet-Berguerand, N., Martins De Araujo, M., Mbopda, A., Le Jossic-Corcos, C., Pagani, F., Corcos, L., CELF proteins regulate CFTR pre-mRNA splicing: Essential role of the divergent domain of ETR-3 (2010) Nucleic Acids Res, 38, pp. 7273-7285
  • Suswam, E.A., Shacka, J.J., Walker, K., Lu, L., Li, X., Si, Y., Zhang, X., King, P.H., Mutant tristetraprolin: A potent inhibitor of malignant glioma cell growth (2013) J. Neurooncol., 113, pp. 195-205
  • Suswam, E.A., Nabors, L.B., Huang, Y., Yang, X., King, P.H., IL-1β induces stabilization of IL-8 mRNA in malignant breast cancer cells via the 3' untranslated region: Involvement of divergent RNA-binding factors HuR, KSRP and TIAR (2005) Int. J. Cancer., 113, pp. 911-919
  • Iguchi, Y., Katsuno, M., Niwa, J., Yamada, S., Sone, J., Waza, M., Adachi, H., Sobue, G., TDP-43 depletion induces neuronal cell damage through dysregulation of Rho family GTPases (2009) J. Biol. Chem., 284, pp. 22059-22066
  • Filippova, N., Yang, X., Wang, Y., Gillespie, G.Y., Langford, C., King, P.H., Wheeler, C., Nabors, L.B., The RNA-binding protein HuR promotes glioma growth and treatment resistance (2011) Mol. Cancer Res., 9, pp. 648-659
  • King, P.H., RNA-binding analyses of HuC and HuD with the VEGF and c-myc 3'-untranslated regions using a novel ELISA-based assay (2000) Nucleic Acids Res, 28, p. E20
  • Nabors, L.B., Gillespie, G.Y., Harkins, L., King, P.H., HuR, an RNA stability factor, is expressed in malignant brain tumors and binds to adenine and uridine-rich elements within the 3' untranslated regions of cytokine and angiogenic factor mRNAs (2001) Cancer Res, 61, pp. 2154-2161
  • Filippova, N., Yang, X., King, P., Nabors, L.B., Phosphoregulation of the RNA-binding protein Hu antigen R (HuR) by Cdk5 affects centrosome function (2012) J. Biol. Chem., 287, pp. 32277-32287
  • Henics, T., Nagy, E., Oh, H.J., Csermely, P., Von Gabain, A., Subjeck, J.R., Mammalian Hsp70 and Hsp110 proteins bind to RNA motifs involved in mRNA stability (1999) J. Biol. Chem., 274, pp. 17318-17324
  • Meisner, N.-C., Hintersteiner, M., Mueller, K., Bauer, R., Seifert, J.-M., Naegeli, H.-U., Ottl, J., Auer, M., Identification and mechanistic characterization of low-molecular-weight inhibitors for HuR (2007) Nat. Chem. Biol., 3, pp. 508-515
  • Lin, W.J., Zheng, X., Lin, C.C., Tsao, J., Zhu, X., Cody, J.J., Coleman, J.M., Chen, C.Y., Posttranscriptional control of type I interferon genes by KSRP in the innate immune response against viral infection (2011) Mol. Cell Biol., 31, pp. 3196-3207
  • Avendaño-Vázquez, S.E., Dhir, A., Bembich, S., Buratti, E., Proudfoot, N., Baralle, F.E., Autoregulation of TDP-43 mRNA levels involves interplay between transcription, splicing, and alternative polyA site selection (2012) Genes Dev, 26, pp. 1679-1684
  • Ray, D., Kazan, H., Chan, E.T., Peña Castillo, L., Chaudhry, S., Talukder, S., Blencowe, B.J., Hughes, T.R., Rapid and systematic analysis of the RNA recognition specificities of RNA-binding proteins (2009) Nat. Biotechnol., 27, pp. 667-670
  • Lebedeva, S., Jens, M., Theil, K., Schwanhäusser, B., Selbach, M., Landthaler, M., Rajewsky, N., Transcriptome-wide analysis of regulatory interactions of the RNA-binding protein HuR (2011) Mol. Cell., 43, pp. 340-352
  • Ayala, Y.M., De Conti, L., Avendaño-Vázquez, S.E., Dhir, A., Romano, M., D'Ambrogio, A., Tollervey, J., Baralle, F.E., TDP-43 regulates its mRNA levels through a negative feedback loop (2011) EMBO J., 30, pp. 277-288
  • Vasudevan, S., Steitz, J.A., AU-rich-element-mediated upregulation of translation by FXR1 and Argonaute 2 (2007) Cell, 128, pp. 1105-1118
  • Li, X., Lu, L., Bush, D.J., Zhang, X., Zheng, L., Suswam, E.A., King, P.H., Mutant copper-zinc superoxide dismutase associated with amyotrophic lateral sclerosis binds to adenine/uridine-rich stability elements in the vascular endothelial growth factor 3'-untranslated region (2009) J. Neurochem., 108, pp. 1032-1044
  • Fialcowitz, E.J., Brewer, B.Y., Keenan, B.P., Wilson, G.M., A Hairpin-like structure within an AU-rich mRNA-destabilizing element regulates trans-factor binding selectivity andmRNAdecay kinetics (2005) J. Biol. Chem., 280, pp. 22406-22417
  • Ma, W.-J., Cheng, S., Campbell, C., Wright, A., Furneaux, H., Cloning and characterization of HuR, a ubiquitously expressed Elav-like protein (1996) J. Biol. Chem., 271, pp. 8144-8151
  • Buratti, E., Dörk, T., Zuccato, E., Pagani, F., Romano, M., Baralle, F.E., Nuclear factor TDP-43 and SR proteins promote in vitro and in vivo CFTR exon 9 skipping (2001) EMBO J., 20, pp. 1774-1784
  • Buratti, E., Baralle, F.E., Characterization and functional implications of the RNA binding properties of nuclear factor TDP-43, a novel splicing regulator of CFTR exon 9 (2001) J. Biol. Chem., 276, pp. 36337-36343
  • Pagani, F., Buratti, E., Stuani, C., Romano, M., Zuccato, E., Niksic, M., Giglio, L., Baralle, F.E., Splicing factors induce cystic fibrosis transmembrane regulator exon 9 skipping through a nonevolutionary conserved intronic element (2000) J. Biol. Chem., 275, pp. 21041-21047
  • Lagier-Tourenne, C., Polymenidou, M., Hutt, K.R., Vu, A.Q., Baughn, M., Huelga, S.C., Clutario, K.M., Yeo, G.W., Divergent roles of ALS-linked proteins FUS/TLS and TDP-43 intersect in processing long pre-mRNAs (2012) Nat. Neurosci., 15, pp. 1488-1497
  • Simone, L.E., Keene, J.D., Mechanisms coordinating ELAV/Hu mRNA regulons (2013) Curr. Opin. Genet. Dev., 23, pp. 35-43
  • Tollervey, J.R., Curk, T., Rogelj, B., Briese, M., Cereda, M., Kayikci, M., König, J., Ule, J., Characterizing the RNA targets and position-dependent splicing regulation by TDP-43 (2011) Nat. Neurosci., 14, pp. 452-458
  • Keene, J.D., Tenenbaum, S.A., Eukaryotic mRNPs may represent posttranscriptional operons (2002) Mol. Cell., 9, pp. 1161-1167
  • Mansfield, K.D., Keene, J.D., The ribonome: A dominant force in co-ordinating gene expression (2009) Biol. Cell., 101, pp. 169-181
  • Blackburn, D., Sargsyan, S., Monk, P.N., Shaw, P.J., Astrocyte function and role in motor neuron disease: A future therapeutic target? (2009) Glia, 57, pp. 1251-1264
  • Sofroniew, M.V., Vinters, H.V., Astrocytes: Biology and pathology (2010) Acta Neuropathol, 119, pp. 7-35
  • Dong, Y., Benveniste, E.N., Immune function of astrocytes (2001) Glia, 36, pp. 180-190
  • Haidet-Phillips, A.M., Hester, M.E., Miranda, C.J., Meyer, K., Braun, L., Frakes, A., Song, S., Kaspar, B.K., Astrocytes from familial and sporadic ALS patients are toxic to motor neurons (2011) Nat. Biotechnol., 29, pp. 824-828
  • Nagai, M., Re, D.B., Nagata, T., Chalazonitis, A., Jessell, T.M., Wichterle, H., Przedborski, S., Astrocytes expressing ALS-linked mutated SOD1release factors selectively toxic to motor neurons (2007) Nat. Neurosci., 10, pp. 615-622
  • Yamanaka, K., Chun, S.J., Boillee, S., Fujimori-Tonou, N., Yamashita, H., Gutmann, D.H., Takahashi, R., Cleveland, D.W., Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis (2008) Nat. Neurosci., 11, pp. 251-253
  • Bi, F., Huang, C., Tong, J., Qiu, G., Huang, B., Wu, Q., Li, F., Zhou, H., Reactive astrocytes secrete lcn2 to promote neuron death (2013) Proc. Natl. Acad. Sci. U. S. A., 110, pp. 4069-4074
  • Yang, C., Wang, H., Qiao, T., Yang, B., Aliaga, L., Qiu, L., Tan, W., Xu, Z., Partial loss of TDP-43 function causes phenotypes of amyotrophic lateral sclerosis (2014) Proc. Natl. Acad. Sci. U. S. A., 111, pp. E1121-E1129
  • Di Giorgio, F.P., Carrasco, M.A., Siao, M.C., Maniatis, T., Eggan, K., Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model (2007) Nat. Neurosci., 10, pp. 608-614
  • Haidet-Phillips, A.M., Gross, S.K., Williams, T., Tuteja, A., Sherman, A., Ko, M., Jeong, Y.H., Maragakis, N.J., Altered astrocytic expression of TDP-43 does not influence motor neuron survival (2013) Exp. Neurol., 250, pp. 250-259
  • Buratti, E., Baralle, F.E., TDP-43: Gumming up neurons through protein-protein and protein-RNA interactions (2012) Trends Biochem. Sci., 37, pp. 237-247
  • Barreau, C., Paillard, L., Osborne, H.B., AU-rich elements and associated factors: Are there unifying principles? (2005) Nucleic Acids Res, 33, pp. 7138-7150
  • Kawai, T., Lal, A., Yang, X., Galban, S., Mazan-Mamczarz, K., Gorospe, M., Translational control of cytochrome c by RNA-binding proteins TIA-1 and HuR (2006) Mol. Cell Biol., 26, pp. 3295-3307
  • Kullmann, M., Göpfert, U., Siewe, B., Hengst, L., ELAV/Hu proteins inhibit p27 translation via an IRES element in the p27 5'UTR (2002) Genes Dev, 16, pp. 3087-3099
  • Meng, Z., Jackson, N.L., Choi, H., King, P.H., Emanuel, P.D., Blume, S.W., Alterations in RNA-binding activities of IRES-regulatory proteins as a mechanism for physiological variability and pathological dysregulation of IGF-IR translational control in human breast tumor cells (2008) J. Cell Physiol., 217, pp. 172-183
  • Durie, D., Lewis, S.M., Liwak, U., Kisilewicz, M., Gorospe, M., Holcik, M., RNA-binding protein HuR mediates cytoprotection through stimulation of XIAP translation (2011) Oncogene, 30, pp. 1460-1469
  • Meisner, N.-C., Filipowicz, W., (2011) Properties of the Regulatory RNA-binding Protein HuR and its Role in Controlling MiRNA Repression, pp. 106-123. , Großhans, H. ed., Springer, New York
  • Gorospe, M., Tominaga, K., Wu, X., Fähling, M., Ivan, M., Post-transcriptional control of the hypoxic response by RNA-binding proteins and microRNAs (2011) Front. Mol. Neurosci., 4, p. 7
  • Sama, R.R., Ward, C.L., Kaushansky, L.J., Lemay, N., Ishigaki, S., Urano, F., Bosco, D.A., FUS/TLS assembles into stress granules and is a prosurvival factor during hyperosmolar stress (2013) J. Cell Physiol., 228, pp. 2222-2231
  • Bosco, D.A., Lemay, N., Ko, H.K., Zhou, H., Burke, C., Kwiatkowski, T.J., Jr., Sapp, P., Hayward, L.J., Mutant FUS proteins that cause amyotrophic lateral sclerosis incorporate into stress granules (2010) Hum. Mol. Genet., 19, pp. 4160-4175
  • Colombrita, C., Zennaro, E., Fallini, C., Weber, M., Sommacal, A., Buratti, E., Silani, V., Ratti, A., TDP-43 is recruited to stress granules in conditions of oxidative insult (2009) J. Neurochem., 111, pp. 1051-1061
  • Vaccaro, A., Tauffenberger, A., Ash, P.E., Carlomagno, Y., Petrucelli, L., Parker, J.A., TDP-1/TDP-43 regulates stress signaling and agedependent proteotoxicity in Caenorhabditis elegans (2012) PLoS Genet, 8, p. e1002806
  • Anderson, P., Kedersha, N., RNA granules (2006) J. Cell Biol., 172, pp. 803-808


---------- APA ----------
Lu, L., Zheng, L., Si, Y., Luo, W., Dujardin, G., Kwan, T., Potochick, N.R.,..., King, P.H. (2014) . Hu antigen R (HuR) is a positive regulator of the RNA-binding proteins TDP-43 and FUS/TLS: Implications for amyotrophic lateral sclerosis. Journal of Biological Chemistry, 289(46), 31792-31804.
---------- CHICAGO ----------
Lu, L., Zheng, L., Si, Y., Luo, W., Dujardin, G., Kwan, T., et al. "Hu antigen R (HuR) is a positive regulator of the RNA-binding proteins TDP-43 and FUS/TLS: Implications for amyotrophic lateral sclerosis" . Journal of Biological Chemistry 289, no. 46 (2014) : 31792-31804.
---------- MLA ----------
Lu, L., Zheng, L., Si, Y., Luo, W., Dujardin, G., Kwan, T., et al. "Hu antigen R (HuR) is a positive regulator of the RNA-binding proteins TDP-43 and FUS/TLS: Implications for amyotrophic lateral sclerosis" . Journal of Biological Chemistry, vol. 289, no. 46, 2014, pp. 31792-31804.
---------- VANCOUVER ----------
Lu, L., Zheng, L., Si, Y., Luo, W., Dujardin, G., Kwan, T., et al. Hu antigen R (HuR) is a positive regulator of the RNA-binding proteins TDP-43 and FUS/TLS: Implications for amyotrophic lateral sclerosis. J. Biol. Chem. 2014;289(46):31792-31804.