The RNA-binding protein Fus directs translation of localized mrnas in APC-RNP granules

Journal of Cell Biology

Volumn 203, Issue 5, 2013, Pages 737-746

  Yasuda, Kyota ^a   Zhang, Huaye ^b   Loiselle, David ^c   Haystead, Timothy ^c   Macara, Ian G ^d   Mili, Stavroula ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; FUSED IN SARCOMA PROTEIN; GREEN FLUORESCENT PROTEIN; MESSENGER RNA; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ARTICLE; CELL GRANULE; COMPLEX FORMATION; CONTROLLED STUDY; CYTOPLASM; GENE EXPRESSION; GENE SILENCING; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN RNA BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSLATION; WESTERN BLOTTING;

EID: 84890819735     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201306058     Document Type: Article

References (39)

1. Anderson, P., and N. Kedersha. 2008. Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 33:141-150. http://dx.doi.org/10.1016/j.tibs.2007.12.003
2. Andersson, M.K., A. Ståhlberg, Y. Arvidsson, A. Olofsson, H. Semb, G. Stenman, O. Nilsson, and P. Aman. 2008. The multifunctional FUS, EWS and TAF15 proto-oncoproteins show cell type-specific expression patterns and involvement in cell spreading and stress response. BMC Cell Biol. 9:37. http://dx.doi.org/10.1186/1471-2121-9-37
3. Bassell, G.J., and S.T. Warren. 2008. Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function. Neuron. 60:201- 214. http://dx.doi.org/10.1016/j.neuron.2008.10.004
4. Besse, F., S. Lopez de Quinto, V. Marchand, A. Trucco, and A. Ephrussi. 2009. Drosophila PTB promotes formation of high-order RNP particles and represses oskar translation. Genes Dev. 23:195-207. http://dx.doi.org/10.1101/gad.505709
5. Blower, M.D., E. Feric, K. Weis, and R. Heald. 2007. Genome-wide analysis demonstrates conserved localization of messenger RNAs to mitotic microtubules. J. Cell Biol. 179:1365-1373. http://dx.doi.org/10.1083/jcb.200705163
6. Bosco, D.A., N. Lemay, H.K. Ko, H. Zhou, C. Burke, T.J. Kwiatkowski Jr., P. Sapp, D. McKenna-Yasek, R.H. Brown Jr., and L.J. Hayward. 2010. Mutant FUS proteins that cause amyotrophic lateral sclerosis incorporate into stress granules. Hum. Mol. Genet. 19:4160-4175. http://dx.doi.org/10.1093/hmg/ddq335
7. Buchan, J.R., and R. Parker. 2009. Eukaryotic stress granules: the ins and outs of translation. Mol. Cell. 36:932-941. http://dx.doi.org/10.1016/j.molcel.2009.11.020
8. Buchan, J.R., D. Muhlrad, and R. Parker. 2008. P bodies promote stress granule assembly in Saccharomyces cerevisiae. J. Cell Biol. 183:441-455. http://dx.doi.org/10.1083/jcb.200807043
9. Buchan, J.R., J.H. Yoon, and R. Parker. 2011. Stress-specific composition, assembly and kinetics of stress granules in Saccharomyces cerevisiae. J. Cell Sci. 124:228-239. http://dx.doi.org/10.1242/jcs.078444
10. Damgaard, C.K., and J. Lykke-Andersen. 2011. Translational coregulation of 5'TOP mRNAs by TIA-1 and TIAR. Genes Dev. 25:2057-2068. http://dx.doi.org/10.1101/gad.17355911
11. David, A., B.P. Dolan, H.D. Hickman, J.J. Knowlton, G. Clavarino, P. Pierre, J.R. Bennink, and J.W. Yewdell. 2012. Nuclear translation visualized by ribosome-bound nascent chain puromycylation. J. Cell Biol. 197:45- 57. http://dx.doi.org/10.1083/jcb.201112145
12. Dieterich, D.C., J.J. Lee, A.J. Link, J. Graumann, D.A. Tirrell, and E.M. Schuman. 2007. Labeling, detection and identification of newly synthesized proteomes with bioorthogonal non-canonical amino-acid tagging. Nat. Protoc. 2:532-540. http://dx.doi.org/10.1038/nprot.2007.52
13. Dormann, D., R. Rodde, D. Edbauer, E. Bentmann, I. Fischer, A. Hruscha, M.E. Than, I.R. Mackenzie, A. Capell, B. Schmid, et al. 2010. ALSassociated fused in sarcoma (FUS) mutations disrupt Transportin-mediated nuclear import. EMBO J. 29:2841-2857. http://dx.doi.org/10.1038/emboj.2010.143
14. Gilks, N., N. Kedersha, M. Ayodele, L. Shen, G. Stoecklin, L.M. Dember, and P. Anderson. 2004. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol. Biol. Cell. 15:5383-5398. http://dx.doi.org/10.1091/mbc.E04-08-0715
15. Harris, E.S., and W.J. Nelson. 2010. Adenomatous polyposis coli regulates endothelial cell migration independent of roles in beta-catenin signaling and cell-cell adhesion. Mol. Biol. Cell. 21:2611-2623. http://dx.doi.org/10.1091/mbc.E10-03-0235
16. Hengst, U., A. Deglincerti, H.J. Kim, N.L. Jeon, and S.R. Jaffrey. 2009. Axonal elongation triggered by stimulus-induced local translation of a polarity complex protein. Nat. Cell Biol. 11:1024-1030. http://dx.doi.org/10.1038/ncb1916
17. Holt, C.E., and S.L. Bullock. 2009. Subcellular mRNA localization in animal cells and why it matters. Science. 326:1212-1216. http://dx.doi.org/10.1126/science.1176488
18. Huang, C., H. Zhou, J. Tong, H. Chen, Y.J. Liu, D. Wang, X. Wei, and X.G. Xia. 2011. FUS transgenic rats develop the phenotypes of amyotrophic lateral sclerosis and frontotemporal lobar degeneration. PLoS Genet. 7:e1002011. http://dx.doi.org/10.1371/journal.pgen.1002011
19. Kedersha, N., M.R. Cho, W. Li, P.W. Yacono, S. Chen, N. Gilks, D.E. Golan, and P. Anderson. 2000. Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J. Cell Biol. 151:1257-1268. http://dx.doi.org/10.1083/jcb.151.6.1257
20. Kennell, J., and K.M. Cadigan. 2009. APC and beta-catenin degradation. Adv. Exp. Med. Biol. 656:1-12. http://dx.doi.org/10.1007/978-1-4419-1145-2_1
21. Kroboth, K., I.P. Newton, K. Kita, D. Dikovskaya, J. Zumbrunn, C.M. Waterman-Storer, and I.S. Näthke. 2007. Lack of adenomatous polyposis coli protein correlates with a decrease in cell migration and overall changes in microtubule stability. Mol. Biol. Cell. 18:910-918. http://dx.doi.org/10.1091/mbc.E06-03-0179
22. Lagier-Tourenne, C., M. Polymenidou, and D.W. Cleveland. 2010. TDP-43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration. Hum. Mol. Genet. 19(R1):R46-R64. http://dx.doi.org/10.1093/hmg/ddq137
23. Lagier-Tourenne, C., M. Polymenidou, K.R. Hutt, A.Q. Vu, M. Baughn, S.C. Huelga, K.M. Clutario, S.C. Ling, T.Y. Liang, C. Mazur, et al. 2012. Divergent roles of ALS-linked proteins FUS/TLS and TDP-43 intersect in processing long pre-mRNAs. Nat. Neurosci. 15:1488-1497. http://dx.doi.org/10.1038/nn.3230
24. Leung, K.M., F.P. van Horck, A.C. Lin, R. Allison, N. Standart, and C.E. Holt. 2006. Asymmetrical beta-actin mRNA translation in growth cones mediates attractive turning to netrin-1. Nat. Neurosci. 9:1247-1256. http://dx.doi.org/10.1038/nn1775
25. Li, Z., L. Wang, T.S. Hays, and Y. Cai. 2008. Dynein-mediated apical localization of crumbs transcripts is required for Crumbs activity in epithelial polarity. J. Cell Biol. 180:31-38. http://dx.doi.org/10.1083/jcb.200707007
26. Liu-Yesucevitz, L., G.J. Bassell, A.D. Gitler, A.C. Hart, E. Klann, J.D. Richter, S.T. Warren, and B. Wolozin. 2011. Local RNA translation at the synapse and in disease. J. Neurosci. 31:16086-16093. http://dx.doi.org/10.1523/JNEUROSCI.4105-11.2011
27. Mackenzie, I.R., R. Rademakers, and M. Neumann. 2010. TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia. Lancet Neurol. 9:995-1007. http://dx.doi.org/10.1016/S1474-4422(10)70195-2
28. Meerbrey, K.L., G. Hu, J.D. Kessler, K. Roarty, M.Z. Li, J.E. Fang, J.I. Herschkowitz, A.E. Burrows, A. Ciccia, T. Sun, et al. 2011. The pINDUCER lentiviral toolkit for inducible RNA interference in vitro and in vivo. Proc. Natl. Acad. Sci. USA. 108:3665-3670. http://dx.doi.org/10.1073/pnas.1019736108
29. Mili, S., K. Moissoglu, and I.G. Macara. 2008. Genome-wide screen reveals APC-associated RNAs enriched in cell protrusions. Nature. 453:115-119. http://dx.doi.org/10.1038/nature06888
30. Mitchell, J.C., P. McGoldrick, C. Vance, T. Hortobagyi, J. Sreedharan, B. Rogelj, E.L. Tudor, B.N. Smith, C. Klasen, C.C. Miller, et al. 2013. Overexpression of human wild-type FUS causes progressive motor neuron degeneration in an age- and dose-dependent fashion. Acta Neuropathol. 125:273-288. http://dx.doi.org/10.1007/s00401-012-1043-z
31. Nagaoka, K., T. Udagawa, and J.D. Richter. 2012. CPEB-mediated ZO-1 mRNA localization is required for epithelial tight-junction assembly and cell polarity. Nat Commun. 3:675. http://dx.doi.org/10.1038/ncomms1678
32. Näthke, I.S. 2004. The adenomatous polyposis coli protein: the Achilles heel of the gut epithelium. Annu. Rev. Cell Dev. Biol. 20:337-366. http://dx.doi.org/10.1146/annurev.cellbio.20.012103.094541
33. Rogelj, B., L.E. Easton, G.K. Bogu, L.W. Stanton, G. Rot, T. Curk, B. Zupan, Y. Sugimoto, M. Modic, N. Haberman, et al. 2012. Widespread binding of FUS along nascent RNA regulates alternative splicing in the brain. Sci Rep. 2:603. http://dx.doi.org/10.1038/srep00603
34. Sabatelli, M., A. Moncada, A. Conte, S. Lattante, G. Marangi, M. Luigetti, M. Lucchini, M. Mirabella, A. Romano, A. Del Grande, et al. 2013. Mutations in the 3 untranslated region of FUS causing FUS overexpression are associated with amyotrophic lateral sclerosis. Hum. Mol. Genet. 22:4748-4755. http://dx.doi.org/10.1093/hmg/ddt328
35. Sansom, O.J., K.R. Reed, A.J. Hayes, H. Ireland, H. Brinkmann, I.P. Newton, E. Batlle, P. Simon-Assmann, H. Clevers, I.S. Nathke, et al. 2004. Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev. 18:1385-1390. http://dx.doi.org/10.1101/gad.287404
36. Schmidt, E.K., G. Clavarino, M. Ceppi, and P. Pierre. 2009. SUnSET, a nonradioactive method to monitor protein synthesis. Nat. Methods. 6:275-277. http://dx.doi.org/10.1038/nmeth.1314
37. Shestakova, E.A., R.H. Singer, and J. Condeelis. 2001. The physiological significance of beta -actin mRNA localization in determining cell polarity and directional motility. Proc. Natl. Acad. Sci. USA. 98:7045-7050. http://dx.doi.org/10.1073/pnas.121146098
38. Vainer, G., E. Vainer-Mosse, A. Pikarsky, S.M. Shenoy, F. Oberman, A. Yeffet, R.H. Singer, E. Pikarsky, and J.K. Yisraeli. 2008. A role for VICKZ proteins in the progression of colorectal carcinomas: regulating lamellipodia formation. J. Pathol. 215:445-456. http://dx.doi.org/10.1002/path.2376
39. Weil, T.T., R.M. Parton, B. Herpers, J. Soetaert, T. Veenendaal, D. Xanthakis, I.M. Dobbie, J.M. Halstead, R. Hayashi, C. Rabouille, and I. Davis. 2012. Drosophila patterning is established by differential association of mRNAs with P bodies. Nat. Cell Biol. 14:1305-1313. http://dx.doi.org/10.1038/ncb2627