Neuronal RNP granules: from physiological to pathological assemblies

References

Alami, N.H., Smith, R.B., Carrasco, M.A., Williams, L.A., Winborn, C.S., Han, S.S.W., Kiskinis, E., Winborn, B., Freibaum, B.D., Kanagaraj, A., et al. (2014). Axonal transport of TDP-43 mRNA granules is impaired by ALS-causing mutations. Neuron 81, 536–543.10.1016/j.neuron.2013.12.018Search in Google Scholar PubMed PubMed Central

Alberti, S. (2017). Phase separation in biology. Curr. Biol. 27, R1097–R1102.10.1016/j.cub.2017.08.069Search in Google Scholar PubMed

Baez, M.V., Luchelli, L., Maschi, D., Habif, M., Pascual, M., Thomas, M.G., and Boccaccio, G.L. (2011). Smaug1 mRNA-silencing foci respond to NMDA and modulate synapse formation. J. Cell Biol. 195, 1141–1157.10.1083/jcb.201108159Search in Google Scholar PubMed PubMed Central

Balasanyan, V. and Arnold, D.B. (2014). Actin and myosin-dependent localization of mRNA to dendrites. PLoS One 9, e92349.10.1371/journal.pone.0092349Search in Google Scholar PubMed PubMed Central

Banani, S.F., Lee, H.O., Hyman, A.A., and Rosen, M.K. (2017). Biomolecular condensates: organizers of cellular biochemistry. Nat. Rev. Mol. Cell Biol. 18, 285–298.10.1038/nrm.2017.7Search in Google Scholar PubMed PubMed Central

Batish, M., van den Bogaard, P., Kramer, F.R., and Tyagi, S. (2012). Neuronal mRNAs travel singly into dendrites. Proc. Natl. Acad. Sci. USA 109, 4645–4650.10.1073/pnas.1111226109Search in Google Scholar PubMed PubMed Central

Berger, S.M., Fernandez-Lamo, I., Schonig, K., Fernandez Moya, S.M., Ehses, J., Schieweck, R., Clementi, S., Enkel, T., Grothe, S., von Bohlen Und Halbach, O., et al. (2017). Forebrain-specific, conditional silencing of Staufen2 alters synaptic plasticity, learning, and memory in rats. Genome Biol. 18, 222.10.1186/s13059-017-1350-8Search in Google Scholar PubMed PubMed Central

Besse, F. and Ephrussi, A. (2008). Translational control of localized mRNAs: restricting protein synthesis in space and time. Nat. Rev. Mol. Cell Biol. 9, 971–980.10.1038/nrm2548Search in Google Scholar PubMed

Bianco, A., Dienstbier, M., Salter, H.K., Gatto, G., and Bullock, S.L. (2010). Bicaudal-D regulates fragile X mental retardation protein levels, motility, and function during neuronal morphogenesis. Curr. Biol. 20, 1487–1492.10.1016/j.cub.2010.07.016Search in Google Scholar PubMed PubMed Central

Bowden, H.A. and Dormann, D. (2016). Altered mRNP granule dynamics in FTLD pathogenesis. J. Neurochem. 138(Suppl. 1), 112–133.10.1111/jnc.13601Search in Google Scholar PubMed

Buxbaum, A.R., Wu, B., and Singer, R.H. (2014). Single β-actin mRNA detection in neurons reveals a mechanism for regulating its translatability. Science 343, 419–422.10.1126/science.1242939Search in Google Scholar

Cajigas, I.J., Tushev, G., Will, T.J., tom Dieck, S., Fuerst, N., and Schuman, E.M. (2012). The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging. Neuron 74, 453–466.10.1016/j.neuron.2012.02.036Search in Google Scholar

Calliari, A., Farias, J., Puppo, A., Canclini, L., Mercer, J.A., Munroe, D., Sotelo, J.R., and Sotelo-Silveira, J.R. (2014). Myosin Va associates with mRNA in ribonucleoprotein particles present in myelinated peripheral axons and in the central nervous system. Dev. Neurobiol. 74, 382–396.10.1002/dneu.22155Search in Google Scholar

Campbell, D.S. and Holt, C.E. (2001). Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32, 1013–1026.10.1016/S0896-6273(01)00551-7Search in Google Scholar

Chae, Y.S., Lee, S.H., Cheang, Y.H., Lee, N., Rim, Y.S., Jang, D.J., and Kaang, B.K. (2010). Neuronal RNA granule contains ApCPEB1, a novel cytoplasmic polyadenylation element binding protein, in Aplysia sensory neuron. Exp. Mol. Med. 42, 30–37.10.3858/emm.2010.42.1.003Search in Google Scholar PubMed PubMed Central

Chen, K.H., Boettiger, A.N., Moffitt, J.R., Wang, S., and Zhuang, X. (2015). RNA imaging. Spatially resolved, highly multiplexed RNA profiling in single cells. Science 348, aaa6090.Search in Google Scholar

Christie, S.B., Akins, M.R., Schwob, J.E., and Fallon, J.R. (2009). The FXG: a presynaptic fragile X granule expressed in a subset of developing brain circuits. J. Neurosci. 29, 1514–1524.10.1523/JNEUROSCI.3937-08.2009Search in Google Scholar PubMed PubMed Central

Comery, T.A., Harris, J.B., Willems, P.J., Oostra, B.A., Irwin, S.A., Weiler, I.J., and Greenough, W.T. (1997). Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc. Natl. Acad. Sci. USA 94, 5401–5404.10.1073/pnas.94.10.5401Search in Google Scholar PubMed PubMed Central

Cougot, N., Bhattacharyya, S.N., Tapia-Arancibia, L., Bordonne, R., Filipowicz, W., Bertrand, E., and Rage, F. (2008). Dendrites of mammalian neurons contain specialized P-body-like structures that respond to neuronal activation. J. Neurosci. 28, 13793–13804.10.1523/JNEUROSCI.4155-08.2008Search in Google Scholar PubMed PubMed Central

Courchaine, E.M., Lu, A., and Neugebauer, K.M. (2016). Droplet organelles? EMBO J. 35, 1603–1612.10.15252/embj.201593517Search in Google Scholar PubMed PubMed Central

Davidovic, L., Jaglin, X.H., Lepagnol-Bestel, A.M., Tremblay, S., Simonneau, M., Bardoni, B., and Khandjian, E.W. (2007). The fragile X mental retardation protein is a molecular adaptor between the neurospecific KIF3C kinesin and dendritic RNA granules. Hum. Mol. Genet. 16, 3047–3058.10.1093/hmg/ddm263Search in Google Scholar PubMed

Dictenberg, J.B., Swanger, S.A., Antar, L.N., Singer, R.H., and Bassell, G.J. (2008). A direct role for FMRP in activity-dependent dendritic mRNA transport links filopodial-spine morphogenesis to fragile X syndrome. Dev. Cell. 14, 926–939.10.1016/j.devcel.2008.04.003Search in Google Scholar PubMed PubMed Central

Donlin-Asp, P.G., Bassell, G.J., and Rossoll, W. (2016). A role for the survival of motor neuron protein in mRNP assembly and transport. Curr. Opin. Neurobiol. 39, 53–61.10.1016/j.conb.2016.04.004Search in Google Scholar PubMed

Donlin-Asp, P.G., Fallini, C., Campos, J., Chou, C.C., Merritt, M.E., Phan, H.C., Bassell, G.J., and Rossoll, W. (2017a). The survival of motor neuron protein acts as a molecular chaperone for mRNP assembly. Cell Rep. 18, 1660–1673.10.1016/j.celrep.2017.01.059Search in Google Scholar PubMed PubMed Central

Donlin-Asp, P.G., Rossoll, W., and Bassell, G.J. (2017b). Spatially and temporally regulating translation via mRNA-binding proteins in cellular and neuronal function. FEBS Lett. 591, 1508–1525.10.1002/1873-3468.12621Search in Google Scholar PubMed

Doyle, M. and Kiebler, M.A. (2011). Mechanisms of dendritic mRNA transport and its role in synaptic tagging. EMBO J. 30, 3540–3552.10.1038/emboj.2011.278Search in Google Scholar PubMed PubMed Central

Dynes, J.L. and Steward, O. (2012). Arc mRNA docks precisely at the base of individual dendritic spines indicating the existence of a specialized microdomain for synapse-specific mRNA translation. J. Comp. Neurol. 520, 3105–3119.10.1002/cne.23073Search in Google Scholar PubMed PubMed Central

El Fatimy, R., Davidovic, L., Tremblay, S., Jaglin, X., Dury, A., Robert, C., De Koninck, P., and Khandjian, E.W. (2016). Tracking the fragile X mental retardation protein in a highly ordered neuronal RiboNucleoParticles population: a link between stalled polyribosomes and RNA granules. PLoS Genet. 12, e1006192.10.1371/journal.pgen.1006192Search in Google Scholar PubMed PubMed Central

Elvira, G., Wasiak, S., Blandford, V., Tong, X.K., Serrano, A., Fan, X., del Rayo Sanchez-Carbente, M., Servant, F., Bell, A.W., Boismenu, D., et al. (2006). Characterization of an RNA granule from developing brain. Mol. Cell Proteomics 5, 635–651.10.1074/mcp.M500255-MCP200Search in Google Scholar PubMed

Fallini, C., Donlin-Asp, P.G., Rouanet, J.P., Bassell, G.J., and Rossoll, W. (2016). Deficiency of the survival of motor neuron protein impairs mRNA localization and local translation in the growth cone of motor neurons. J. Neurosci. 36, 3811–3820.10.1523/JNEUROSCI.2396-15.2016Search in Google Scholar PubMed PubMed Central

Fay, M.M., Anderson, P.J., and Ivanov, P. (2017). ALS/FTD-associated C9ORF72 repeat RNA promotes phase transitions in vitro and in cells. Cell Rep. 21, 3573–3584.10.1016/j.celrep.2017.11.093Search in Google Scholar PubMed PubMed Central

Fernandez-Moya, S.M., Bauer, K.E., and Kiebler, M.A. (2014). Meet the players: local translation at the synapse. Front Mol. Neurosci. 7, 84.10.3389/fnmol.2014.00084Search in Google Scholar PubMed PubMed Central

Fritzsche, R., Karra, D., Bennett, K.L., Ang, F.Y., Heraud-Farlow, J.E., Tolino, M., Doyle, M., Bauer, K.E., Thomas, S., Planyavsky, M., et al. (2013). Interactome of two diverse RNA granules links mRNA localization to translational repression in neurons. Cell Rep. 5, 1749–1762.10.1016/j.celrep.2013.11.023Search in Google Scholar PubMed

Gama-Carvalho, M., Garcia-Vaquero, M.L., Pinto, F.R., Besse, F., Weis, J., Voigt, A., Schulz, J.B., and De Las Rivas, J. (2017). Linking amyotrophic lateral sclerosis and spinal muscular atrophy through RNA-transcriptome homeostasis: a genomics perspective. J. Neurochem. 141, 12–30.10.1111/jnc.13945Search in Google Scholar PubMed

Gopal, P.P., Nirschl, J.J., Klinman, E., and Holzbaur, E.L. (2017). Amyotrophic lateral sclerosis-linked mutations increase the viscosity of liquid-like TDP-43 RNP granules in neurons. Proc. Natl. Acad. Sci. USA 114, E2466–E2475.10.1073/pnas.1614462114Search in Google Scholar PubMed PubMed Central

Graber, T.E., Hebert-Seropian, S., Khoutorsky, A., David, A., Yewdell, J.W., Lacaille, J.C., and Sossin, W.S. (2013). Reactivation of stalled polyribosomes in synaptic plasticity. Proc. Natl. Acad. Sci. USA 110, 16205–16210.10.1073/pnas.1307747110Search in Google Scholar PubMed PubMed Central

Gumy, L.F., Yeo, G.S., Tung, Y.C., Zivraj, K.H., Willis, D., Coppola, G., Lam, B.Y., Twiss, J.L., Holt, C.E., and Fawcett, J.W. (2011). Transcriptome analysis of embryonic and adult sensory axons reveals changes in mRNA repertoire localization. RNA 17, 85–98.10.1261/rna.2386111Search in Google Scholar PubMed PubMed Central

Han, T.W., Kato, M., Xie, S., Wu, L.C., Mirzaei, H., Pei, J., Chen, M., Xie, Y., Allen, J., Xiao, G., et al. (2012). Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies. Cell 149, 768–779.10.1016/j.cell.2012.04.016Search in Google Scholar PubMed

Harrison, A.F. and Shorter, J. (2017). RNA-binding proteins with prion-like domains in health and disease. Biochem. J. 474, 1417–1438.10.1042/BCJ20160499Search in Google Scholar PubMed PubMed Central

Heraud-Farlow, J.E., Sharangdhar, T., Li, X., Pfeifer, P., Tauber, S., Orozco, D., Hormann, A., Thomas, S., Bakosova, A., Farlow, A.R., et al. (2013). Staufen2 regulates neuronal target RNAs. Cell Rep. 5, 1511–1518.10.1016/j.celrep.2013.11.039Search in Google Scholar PubMed

Holt, C.E. and Schuman, E.M. (2013). The central dogma decentralized: new perspectives on RNA function and local translation in neurons. Neuron 80, 648–657.10.1016/j.neuron.2013.10.036Search in Google Scholar PubMed PubMed Central

Huang, Y.S., Carson, J.H., Barbarese, E., and Richter, J. D. (2003). Facilitation of dendritic mRNA transport by CPEB. Genes Dev. 17, 638–653.10.1101/gad.1053003Search in Google Scholar PubMed PubMed Central

Huttelmaier, S., Zenklusen, D., Lederer, M., Dictenberg, J., Lorenz, M., Meng, X., Bassell, G.J., Condeelis, J., and Singer, R.H. (2005). Spatial regulation of β-actin translation by Src-dependent phosphorylation of ZBP1. Nature 438, 512–515.10.1038/nature04115Search in Google Scholar PubMed

Ifrim, M.F., Williams, K.R., and Bassell, G.J. (2015). Single-molecule imaging of PSD-95 mRNA translation in dendrites and its dysregulation in a mouse model of fragile X syndrome. J. Neurosci. 35, 7116–7130.10.1523/JNEUROSCI.2802-14.2015Search in Google Scholar PubMed PubMed Central

Jain, A. and Vale, R.D. (2017). RNA phase transitions in repeat expansion disorders. Nature 546, 243–247.10.1038/nature22386Search in Google Scholar PubMed PubMed Central

Jeong, J.H., Nam, Y.J., Kim, S.Y., Kim, E.G., Jeong, J., and Kim, H.K. (2007). The transport of Staufen2-containing ribonucleoprotein complexes involves kinesin motor protein and is modulated by mitogen-activated protein kinase pathway. J. Neurochem. 102, 2073–2084.10.1111/j.1471-4159.2007.04697.xSearch in Google Scholar PubMed

Kanai, Y., Dohmae, N., and Hirokawa, N. (2004). Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 43, 513–525.10.1016/j.neuron.2004.07.022Search in Google Scholar PubMed

Khayachi, A., Gwizdek, C., Poupon, G., Alcor, D., Chafai, M., Casse, F., Maurin, T., Prieto, M., Folci, A., De Graeve, F., et al. (2018). Sumoylation regulates FMRP-mediated dendritic spine elimination and maturation. Nat. Commun. 9, 757.10.1038/s41467-018-03222-ySearch in Google Scholar PubMed PubMed Central

Kiebler, M.A. and Bassell, G.J. (2006). Neuronal RNA granules: movers and makers. Neuron 51, 685–690.10.1016/j.neuron.2006.08.021Search in Google Scholar PubMed

Kim, S. and Martin, K.C. (2015). Neuron-wide RNA transport combines with netrin-mediated local translation to spatially regulate the synaptic proteome. eLife 4.10.7554/eLife.04158.021Search in Google Scholar

Kim, H.J., Kim, N.C., Wang, Y.D., Scarborough, E.A., Moore, J., Diaz, Z., MacLea, K.S., Freibaum, B., Li, S., Molliex, A., et al. (2013). Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS. Nature 495, 467–473.10.1038/nature11922Search in Google Scholar PubMed PubMed Central

Klann, E. and Dever, T.E. (2004). Biochemical mechanisms for translational regulation in synaptic plasticity. Nat. Rev. Neurosci. 5, 931–942.10.1038/nrn1557Search in Google Scholar

Knowles, R.B., Sabry, J.H., Martone, M.E., Deerinck, T.J., Ellisman, M.H., Bassell, G.J., and Kosik, K.S. (1996). Translocation of RNA granules in living neurons. J. Neurosci. 16, 7812–7820.10.1523/JNEUROSCI.16-24-07812.1996Search in Google Scholar

Kohrmann, M., Luo, M., Kaether, C., DesGroseillers, L., Dotti, C.G., and Kiebler, M.A. (1999). Microtubule-dependent recruitment of Staufen-green fluorescent protein into large RNA-containing granules and subsequent dendritic transport in living hippocampal neurons. Mol. Biol. Cell 10, 2945–2953.10.1091/mbc.10.9.2945Search in Google Scholar

Krichevsky, A.M. and Kosik, K.S. (2001). Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation. Neuron 32, 683–696.10.1016/S0896-6273(01)00508-6Search in Google Scholar

Kruttner, S., Stepien, B., Noordermeer, J.N., Mommaas, M.A., Mechtler, K., Dickson, B.J., and Keleman, K. (2012). Drosophila CPEB Orb2A mediates memory independent of Its RNA-binding domain. Neuron 76, 383–395.10.1016/j.neuron.2012.08.028Search in Google Scholar PubMed PubMed Central

Lee, K.H., Zhang, P., Kim, H.J., Mitrea, D.M., Sarkar, M., Freibaum, B.D., Cika, J., Coughlin, M., Messing, J., Molliex, A., et al. (2016). C9orf72 dipeptide repeats impair the assembly, dynamics, and function of membrane-less organelles. Cell 167, 774–788.e717.10.1016/j.cell.2016.10.002Search in Google Scholar PubMed PubMed Central

Lepelletier, L., Langlois, S.D., Kent, C.B., Welshhans, K., Morin, S., Bassell, G.J., Yam, P.T., and Charron, F. (2017). Sonic hedgehog guides axons via zipcode binding protein 1-mediated local translation. J. Neurosci. 37, 1685–1695.10.1523/JNEUROSCI.3016-16.2016Search in Google Scholar PubMed PubMed Central

Leung, K.M., van Horck, F.P., Lin, A.C., Allison, R., Standart, N., and Holt, C.E. (2006). Asymmetrical β-actin mRNA translation in growth cones mediates attractive turning to netrin-1. Nat. Neurosci. 9, 1247–1256.10.1038/nn1775Search in Google Scholar PubMed PubMed Central

Li, P., Banjade, S., Cheng, H.C., Kim, S., Chen, B., Guo, L., Llaguno, M., Hollingsworth, J.V., King, D.S., Banani, S.F., et al. (2012). Phase transitions in the assembly of multivalent signalling proteins. Nature 483, 336–340.10.1038/nature10879Search in Google Scholar PubMed PubMed Central

Li, D.K., Tisdale, S., Lotti, F., and Pellizzoni, L. (2014). SMN control of RNP assembly: from post-transcriptional gene regulation to motor neuron disease. Semin. Cell Dev. Biol. 32, 22–29.10.1016/j.semcdb.2014.04.026Search in Google Scholar PubMed PubMed Central

Lin, Y., Protter, D.S., Rosen, M.K., and Parker, R. (2015). Formation and maturation of phase-separated liquid droplets by RNA-binding proteins. Mol. Cell 60, 208–219.10.1016/j.molcel.2015.08.018Search in Google Scholar PubMed PubMed Central

Ling, S.C., Polymenidou, M., and Cleveland, D.W. (2013). Converging mechanisms in ALS and FTD: disrupted RNA and protein homeostasis. Neuron 79, 416–438.10.1016/j.neuron.2013.07.033Search in Google Scholar PubMed PubMed Central

Lionnet, T., Czaplinski, K., Darzacq, X., Shav-Tal, Y., Wells, A.L., Chao, J.A., Park, H.Y., de Turris, V., Lopez-Jones, M., and Singer, R.H. (2011). A transgenic mouse for in vivo detection of endogenous labeled mRNA. Nat. Methods 8, 165–170.10.1038/nmeth.1551Search in Google Scholar PubMed PubMed Central

Majumdar, A., Cesario, W.C., White-Grindley, E., Jiang, H., Ren, F., Khan, M.R., Li, L., Choi, E.M., Kannan, K., Guo, F., et al. (2012). Critical role of amyloid-like oligomers of Drosophila Orb2 in the persistence of memory. Cell 148, 515–529.10.1016/j.cell.2012.01.004Search in Google Scholar PubMed

Malinovska, L., Kroschwald, S., and Alberti, S. (2013). Protein disorder, prion propensities, and self-organizing macromolecular collectives. Biochim. Biophys. Acta 1834, 918–931.10.1016/j.bbapap.2013.01.003Search in Google Scholar PubMed

Mallardo, M., Deitinghoff, A., Muller, J., Goetze, B., Macchi, P., Peters, C., and Kiebler, M.A. (2003). Isolation and characterization of Staufen-containing ribonucleoprotein particles from rat brain. Proc. Natl. Acad. Sci. USA 100, 2100–2105.10.1073/pnas.0334355100Search in Google Scholar PubMed PubMed Central

Maurin, T., Zongaro, S., and Bardoni, B. (2014). Fragile X syndrome: from molecular pathology to therapy. Neurosci. Biobehav. Rev. 46, 242–255.10.1016/j.neubiorev.2014.01.006Search in Google Scholar PubMed

Mazroui, R., Huot, M.E., Tremblay, S., Filion, C., Labelle, Y., and Khandjian, E.W. (2002). Trapping of messenger RNA by fragile X mental retardation protein into cytoplasmic granules induces translation repression. Hum. Mol. Genet. 11, 3007–3017.10.1093/hmg/11.24.3007Search in Google Scholar PubMed

Medioni, C. and Besse, F. (2018). The secret life of RNA: lessons from emerging methodologies. Methods Mol. Biol. 1649, 1–28.10.1007/978-1-4939-7213-5_1Search in Google Scholar PubMed

Medioni, C., Ramialison, M., Ephrussi, A., and Besse, F. (2014). Imp promotes axonal remodeling by regulating profilin mRNA during brain development. Curr. Biol. 24, 793–800.10.1016/j.cub.2014.02.038Search in Google Scholar PubMed

Mikl, M., Vendra, G., and Kiebler, M.A. (2011). Independent localization of MAP2, CaMKIIα and β-actin RNAs in low copy numbers. EMBO Rep. 12, 1077–1084.10.1038/embor.2011.149Search in Google Scholar PubMed PubMed Central

Mitsumori, K., Takei, Y., and Hirokawa, N. (2017). Components of RNA granules affect their localization and dynamics in neuronal dendrites. Mol. Biol. Cell 28, 1412–1417.10.1091/mbc.e16-07-0497Search in Google Scholar PubMed PubMed Central

Molliex, A., Temirov, J., Lee, J., Coughlin, M., Kanagaraj, A.P., Kim, H.J., Mittag, T., and Taylor, J.P. (2015). Phase separation by low complexity domains promotes stress granule assembly and drives pathological fibrillization. Cell 163, 123–133.10.1016/j.cell.2015.09.015Search in Google Scholar PubMed PubMed Central

Monahan, Z., Ryan, V.H., Janke, A.M., Burke, K.A., Rhoads, S.N., Zerze, G.H., O’Meally, R., Dignon, G.L., Conicella, A.E., Zheng, W., et al. (2017). Phosphorylation of the FUS low-complexity domain disrupts phase separation, aggregation, and toxicity. EMBO J. 36, 2951–2967.10.15252/embj.201696394Search in Google Scholar PubMed PubMed Central

Muddashetty, R.S., Nalavadi, V.C., Gross, C., Yao, X., Xing, L., Laur, O., Warren, S.T., and Bassell, G.J. (2011). Reversible inhibition of PSD-95 mRNA translation by miR-125a, FMRP phosphorylation, and mGluR signaling. Mol. Cell 42, 673–688.10.1016/j.molcel.2011.05.006Search in Google Scholar PubMed PubMed Central

Murakami, T., Qamar, S., Lin, J.Q., Schierle, G.S., Rees, E., Miyashita, A., Costa, A.R., Dodd, R.B., Chan, F.T., Michel, C.H., et al. (2015). ALS/FTD mutation-induced phase transition of FUS liquid droplets and reversible hydrogels into irreversible hydrogels impairs RNP granule function. Neuron 88, 678–690.10.1016/j.neuron.2015.10.030Search in Google Scholar PubMed PubMed Central

Na, Y., Park, S., Lee, C., Kim, D.K., Park, J.M., Sockanathan, S., Huganir, R.L., and Worley, P.F. (2016). Real-time imaging reveals properties of glutamate-induced Arc/Arg 3.1 translation in neuronal dendrites. Neuron 91, 561–573.10.1016/j.neuron.2016.06.017Search in Google Scholar PubMed PubMed Central

Nakayama, K., Ohashi, R., Shinoda, Y., Yamazaki, M., Abe, M., Fujikawa, A., Shigenobu, S., Futatsugi, A., Noda, M., Mikoshiba, K., et al. (2017). RNG105/caprin1, an RNA granule protein for dendritic mRNA localization, is essential for long-term memory formation. eLife 6.10.7554/eLife.29677.029Search in Google Scholar

Nalavadi, V.C., Griffin, L.E., Picard-Fraser, P., Swanson, A.M., Takumi, T., and Bassell, G.J. (2012). Regulation of zipcode binding protein 1 transport dynamics in axons by myosin Va. J. Neurosci. 32, 15133–15141.10.1523/JNEUROSCI.2006-12.2012Search in Google Scholar PubMed PubMed Central

Narayanan, U., Nalavadi, V., Nakamoto, M., Pallas, D.C., Ceman, S., Bassell, G.J., and Warren, S.T. (2007). FMRP phosphorylation reveals an immediate-early signaling pathway triggered by group I mGluR and mediated by PP2A. J. Neurosci. 27, 14349–14357.10.1523/JNEUROSCI.2969-07.2007Search in Google Scholar PubMed PubMed Central

Nott, T.J., Petsalaki, E., Farber, P., Jervis, D., Fussner, E., Plochowietz, A., Craggs, T.D., Bazett-Jones, D.P., Pawson, T., Forman-Kay, J.D., et al. (2015). Phase transition of a disordered nuage protein generates environmentally responsive membraneless organelles. Mol. Cell 57, 936–947.10.1016/j.molcel.2015.01.013Search in Google Scholar PubMed PubMed Central

Park, H.Y., Lim, H., Yoon, Y.J., Follenzi, A., Nwokafor, C., Lopez-Jones, M., Meng, X., and Singer, R.H. (2014). Visualization of dynamics of single endogenous mRNA labeled in live mouse. Science 343, 422–424.10.1126/science.1239200Search in Google Scholar PubMed PubMed Central

Patel, A., Lee, H.O., Jawerth, L., Maharana, S., Jahnel, M., Hein, M.Y., Stoynov, S., Mahamid, J., Saha, S., Franzmann, T.M., et al. (2015). A liquid-to-solid phase transition of the ALS protein FUS accelerated by disease mutation. Cell 162, 1066–1077.10.1016/j.cell.2015.07.047Search in Google Scholar PubMed

Patel, A., Malinovska, L., Saha, S., Wang, J., Alberti, S., Krishnan, Y., and Hyman, A.A. (2017). ATP as a biological hydrotrope. Science 356, 753–756.10.1126/science.aaf6846Search in Google Scholar PubMed

Pimentel, J. and Boccaccio, G.L. (2014). Translation and silencing in RNA granules: a tale of sand grains. Front Mol. Neurosci. 7, 68.10.3389/fnmol.2014.00068Search in Google Scholar PubMed PubMed Central

Ramaswami, M., Taylor, J.P., and Parker, R. (2013). Altered ribostasis: RNA-protein granules in degenerative disorders. Cell 154, 727–736.10.1016/j.cell.2013.07.038Search in Google Scholar PubMed PubMed Central

Rook, M.S., Lu, M., and Kosik, K.S. (2000). CaMKIIα 3′ untranslated region-directed mRNA translocation in living neurons: visualization by GFP linkage. J. Neurosci. 20, 6385–6393.10.1523/JNEUROSCI.20-17-06385.2000Search in Google Scholar

Rossoll, W., Jablonka, S., Andreassi, C., Kroning, A.K., Karle, K., Monani, U.R., and Sendtner, M. (2003). Smn, the spinal muscular atrophy-determining gene product, modulates axon growth and localization of beta-actin mRNA in growth cones of motoneurons. J. Cell Biol. 163, 801–812.10.1083/jcb.200304128Search in Google Scholar PubMed PubMed Central

Sasaki, Y., Welshhans, K., Wen, Z., Yao, J., Xu, M., Goshima, Y., Zheng, J.Q., and Bassell, G.J. (2010). Phosphorylation of zipcode binding protein 1 is required for brain-derived neurotrophic factor signaling of local β-actin synthesis and growth cone turning. J. Neurosci. 30, 9349–9358.10.1523/JNEUROSCI.0499-10.2010Search in Google Scholar PubMed PubMed Central

Shigeoka, T., Jung, H., Jung, J., Turner-Bridger, B., Ohk, J., Lin, J.Q., Amieux, P.S., and Holt, C.E. (2016). Dynamic axonal translation in developing and mature visual circuits. Cell 166, 181–192.10.1016/j.cell.2016.05.029Search in Google Scholar PubMed PubMed Central

Shin, Y., Berry, J., Pannucci, N., Haataja, M.P., Toettcher, J.E., and Brangwynne, C.P. (2017). Spatiotemporal control of intracellular phase transitions using light-activated optodroplets. Cell 168, 159–171.e114.10.1016/j.cell.2016.11.054Search in Google Scholar PubMed PubMed Central

Shukla, S. and Parker, R. (2016). Hypo- and hyper-assembly diseases of RNA-protein complexes. Trends Mol. Med. 22, 615–628.10.1016/j.molmed.2016.05.005Search in Google Scholar PubMed PubMed Central

Si, K., Choi, Y.B., White-Grindley, E., Majumdar, A., and Kandel, E.R. (2010). Aplysia CPEB can form prion-like multimers in sensory neurons that contribute to long-term facilitation. Cell 140, 421–435.10.1016/j.cell.2010.01.008Search in Google Scholar PubMed

Spillane, M., Ketschek, A., Donnelly, C.J., Pacheco, A., Twiss, J.L., and Gallo, G. (2012). Nerve growth factor-induced formation of axonal filopodia and collateral branches involves the intra-axonal synthesis of regulators of the actin-nucleating Arp2/3 complex. J. Neurosci. 32, 17671–17689.10.1523/JNEUROSCI.1079-12.2012Search in Google Scholar PubMed PubMed Central

Strohl, F., Lin, J.Q., Laine, R.F., Wong, H.H., Urbancic, V., Cagnetta, R., Holt, C.E., and Kaminski, C.F. (2017). Single molecule translation imaging visualizes the dynamics of local β-actin synthesis in retinal axons. Sci. Rep. 7, 709.10.1038/s41598-017-00695-7Search in Google Scholar PubMed PubMed Central

Sun, Z., Diaz, Z., Fang, X., Hart, M.P., Chesi, A., Shorter, J., and Gitler, A.D. (2011). Molecular determinants and genetic modifiers of aggregation and toxicity for the ALS disease protein FUS/TLS. PLoS Biol. 9, e1000614.10.1371/journal.pbio.1000614Search in Google Scholar PubMed PubMed Central

Tatavarty, V., Ifrim, M.F., Levin, M., Korza, G., Barbarese, E., Yu, J., and Carson, J.H. (2012). Single-molecule imaging of translational output from individual RNA granules in neurons. Mol. Biol. Cell 23, 918–929.10.1091/mbc.e11-07-0622Search in Google Scholar

Taylor, J.P., Brown, R.H. Jr., and Cleveland, D.W. (2016). Decoding ALS: from genes to mechanism. Nature 539, 197–206.10.1038/nature20413Search in Google Scholar PubMed PubMed Central

Tiruchinapalli, D.M., Oleynikov, Y., Kelic, S., Shenoy, S.M., Hartley, A., Stanton, P.K., Singer, R.H., and Bassell, G.J. (2003). Activity-dependent trafficking and dynamic localization of zipcode binding protein 1 and β-actin mRNA in dendrites and spines of hippocampal neurons. J. Neurosci. 23, 3251–3261.10.1523/JNEUROSCI.23-08-03251.2003Search in Google Scholar

Tolino, M., Kohrmann, M., and Kiebler, M.A. (2012). RNA-binding proteins involved in RNA localization and their implications in neuronal diseases. Eur. J. Neurosci. 35, 1818–1836.10.1111/j.1460-9568.2012.08160.xSearch in Google Scholar PubMed

Tubing, F., Vendra, G., Mikl, M., Macchi, P., Thomas, S., and Kiebler, M.A. (2010). Dendritically localized transcripts are sorted into distinct ribonucleoprotein particles that display fast directional motility along dendrites of hippocampal neurons. J. Neurosci. 30, 4160–4170.10.1523/JNEUROSCI.3537-09.2010Search in Google Scholar

Urbanska, A.S., Janusz-Kaminska, A., Switon, K., Hawthorne, A.L., Perycz, M., Urbanska, M., Bassell, G.J., and Jaworski, J. (2017). ZBP1 phosphorylation at serine 181 regulates its dendritic transport and the development of dendritic trees of hippocampal neurons. Sci. Rep. 7, 1876.10.1038/s41598-017-01963-2Search in Google Scholar

Verkerk, A.J., Pieretti, M., Sutcliffe, J.S., Fu, Y.H., Kuhl, D.P., Pizzuti, A., Reiner, O., Richards, S., Victoria, M.F., Zhang, F.P., et al. (1991). Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome. Cell 65, 905–914.10.1016/0092-8674(91)90397-HSearch in Google Scholar

Voigt, A., Herholz, D., Fiesel, F.C., Kaur, K., Muller, D., Karsten, P., Weber, S.S., Kahle, P. J., Marquardt, T., and Schulz, J.B. (2010). TDP-43-mediated neuron loss in vivo requires RNA-binding activity. PLoS One 5, e12247.10.1371/journal.pone.0012247Search in Google Scholar PubMed PubMed Central

Wang, C., Han, B., Zhou, R., and Zhuang, X. (2016a). Real-time imaging of translation on single mRNA transcripts in live cells. Cell 165, 990–1001.10.1016/j.cell.2016.04.040Search in Google Scholar PubMed PubMed Central

Wang, E.T., Taliaferro, J.M., Lee, J.A., Sudhakaran, I.P., Rossoll, W., Gross, C., Moss, K.R., and Bassell, G.J. (2016b). Dysregulation of mRNA localization and translation in genetic disease. J. Neurosci. 36, 11418–11426.10.1523/JNEUROSCI.2352-16.2016Search in Google Scholar PubMed PubMed Central

Wang, I.F., Wu, L.S., Chang, H.Y., and Shen, C.K. (2008). TDP-43, the signature protein of FTLD-U, is a neuronal activity-responsive factor. J. Neurochem. 105, 797–806.10.1111/j.1471-4159.2007.05190.xSearch in Google Scholar PubMed

Weber, S.C. and Brangwynne, C.P. (2012). Getting RNA and protein in phase. Cell 149, 1188–1191.10.1016/j.cell.2012.05.022Search in Google Scholar PubMed

Wong, H.H., Lin, J.Q., Strohl, F., Roque, C.G., Cioni, J.M., Cagnetta, R., Turner-Bridger, B., Laine, R.F., Harris, W.A., Kaminski, C.F., et al. (2017). RNA docking and local translation regulate site-specific axon remodeling in vivo. Neuron 95, 852–868.e858.10.1016/j.neuron.2017.07.016Search in Google Scholar PubMed PubMed Central

Wu, H. and Fuxreiter, M. (2016). The structure and dynamics of higher-order assemblies: amyloids, signalosomes, and granules. Cell 165, 1055–1066.10.1016/j.cell.2016.05.004Search in Google Scholar PubMed PubMed Central

Wu, B., Eliscovich, C., Yoon, Y.J., and Singer, R.H. (2016). Translation dynamics of single mRNAs in live cells and neurons. Science 352, 1430–1435.10.1126/science.aaf1084Search in Google Scholar PubMed PubMed Central

Yao, J., Sasaki, Y., Wen, Z., Bassell, G.J., and Zheng, J.Q. (2006). An essential role for β-actin mRNA localization and translation in Ca²⁺-dependent growth cone guidance. Nat. Neurosci. 9, 1265–1273.10.1038/nn1773Search in Google Scholar PubMed

Yoon, Y.J., Wu, B., Buxbaum, A.R., Das, S., Tsai, A., English, B.P., Grimm, J.B., Lavis, L.D., and Singer, R.H. (2016). Glutamate-induced RNA localization and translation in neurons. Proc. Natl. Acad. Sci. USA 113, E6877–E6886.10.1073/pnas.1614267113Search in Google Scholar PubMed PubMed Central

Zeitelhofer, M., Karra, D., Macchi, P., Tolino, M., Thomas, S., Schwarz, M., Kiebler, M., and Dahm, R. (2008). Dynamic interaction between P-bodies and transport ribonucleoprotein particles in dendrites of mature hippocampal neurons. J. Neurosci. 28, 7555–7562.10.1523/JNEUROSCI.0104-08.2008Search in Google Scholar PubMed PubMed Central

Zivraj, K.H., Tung, Y.C., Piper, M., Gumy, L., Fawcett, J.W., Yeo, G.S., and Holt, C.E. (2010). Subcellular profiling reveals distinct and developmentally regulated repertoire of growth cone mRNAs. J. Neurosci. 30, 15464–15478.10.1523/JNEUROSCI.1800-10.2010Search in Google Scholar PubMed PubMed Central