Synaptic control of mRNA translation by reversible assembly of XRN1 bodies

Journal of Cell Science

Volumn 128, Issue 8, 2015, Pages 1542-1554

  Luchelli, Luciana ^a,b   Thomas, María Gabriela ^a   Boccaccio, Graciela L ^a,b  

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

P body; RNA granule; Stress granule; Synapse; XRN1

Indexed keywords

EXORIBONUCLEASE; MESSENGER RNA; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID; SYNAPSIN; UNCLASSIFIED DRUG; XRN1 PROTEIN; DNA BINDING PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; XRN1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL BODY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPAL NEURONAL CULTURE; IMMUNOFLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; RAT; RNA TRANSLATION; SYNAPSE; WESTERN BLOTTING; AMINO ACID SEQUENCE; ANIMAL; CELL CULTURE; CELL ORGANELLE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MOUSE; NERVE CELL; SPRAGUE DAWLEY RAT;

AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; DNA-BINDING PROTEINS; EXORIBONUCLEASES; GENE EXPRESSION REGULATION; MICE; MOLECULAR SEQUENCE DATA; NEURONS; ORGANELLES; PROTEIN BIOSYNTHESIS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, MESSENGER; SYNAPSES;

EID: 84928550463     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.163295     Document Type: Article

References (74)

1. Antar, L. N., Afroz, R., Dictenberg, J. B., Carroll, R. C. and Bassell, G. J. (2004). Metabotropic glutamate receptor activation regulates fragile x mental retardation protein and FMR1 mRNA localization differentially in dendrites and at synapses. J. Neurosci. 24, 2648-2655.
2. Baez, M. V. and Boccaccio, G. L. (2005). Mammalian Smaug is a translational repressor that forms cytoplasmic foci similar to stress granules. J. Biol. Chem. 280, 43131-43140.
3. 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.
4. Bagga, S., Bracht, J., Hunter, S., Massirer, K., Holtz, J., Eachus, R. and Pasquinelli, A. E. (2005). Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation. Cell 122, 553-563.
5. Banko, J. L., Hou, L., Poulin, F., Sonenberg, N. and Klann, E. (2006). Regulation of eukaryotic initiation factor 4E by converging signaling pathways during metabotropic glutamate receptor-dependent long-term depression. J. Neurosci. 26, 2167-2173.
6. Bashkirov, V. I., Scherthan, H., Solinger, J. A., Buerstedde, J. M. and Heyer, W. D. (1997). A mouse cytoplasmic exoribonuclease (mXRN1p) with preference for G4 tetraplex substrates. J. Cell Biol. 136, 761-773.
7. Bossé, G. D., Rüegger, S., Ow, M. C., Vasquez-Rifo, A., Rondeau, E. L., Ambros, V. R., Grosshans, H. and Simard, M. J. (2013). The decapping scavenger enzyme DCS-1 controls microRNA levels in Caenorhabditis elegans. Mol. Cell 50, 281-287.
8. Brangwynne, C. P. (2013). Phase transitions and size scaling of membrane-less organelles. J. Cell Biol. 203, 875-881.
9. Braun, J. E., Truffault, V., Boland, A., Huntzinger, E., Chang, C. T., Haas, G., Weichenrieder, O., Coles, M. and Izaurralde, E. (2012). A direct interaction between DCP1 and XRN1 couples mRNA decapping to 59 exonucleolytic degradation. Nat. Struct. Mol. Biol. 19, 1324-1331.
10. Buchan, J. R. and Parker, R. (2009). Eukaryotic stress granules: the ins and outs of translation. Mol. Cell 36, 932-941.
11. Buxbaum, A. R., Wu, B. and Singer, R. H. (2014). Single b-actin mRNA detection in neurons reveals a mechanism for regulating its translatability. Science 343, 419-422.
12. Castello, A., Fischer, B., Eichelbaum, K., Horos, R., Beckmann, B. M., Strein, C., Davey, N. E., Humphreys, D. T., Preiss, T., Steinmetz, L. M. et al. (2012). Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 149, 1393-1406.
13. Chang, J. H., Xiang, S., Xiang, K., Manley, J. L. and Tong, L. (2011). Structural and biochemical studies of the 59R39 exoribonuclease Xrn1. Nat. Struct. Mol. Biol. 18, 270-276.
14. Cougot, N., Bhattacharyya, S. N., Tapia-Arancibia, L., Bordonné, 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.
15. Darnell, J. C., Jensen, K. B., Jin, P., Brown, V., Warren, S. T. and Darnell, R. B. (2001). Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell 107, 489-499.
16. Darnell, J. C., Van Driesche, S. J., Zhang, C., Hung, K. Y., Mele, A., Fraser, C. E., Stone, E. F., Chen, C., Fak, J. J., Chi, S. W. et al. (2011). FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146, 247-261.
17. di Penta, A., Mercaldo, V., Florenzano, F., Munck, S., Ciotti, M. T., Zalfa, F., Mercanti, D., Molinari, M., Bagni, C. and Achsel, T. (2009). Dendritic LSm1/CBP80-mRNPs mark the early steps of transport commitment and translational control. J. Cell Biol. 184, 423-435.
18. Dieterich, D. C., Hodas, J. J., Gouzer, G., Shadrin, I. Y., Ngo, J. T., Triller, A., Tirrell, D. A. and Schuman, E. M. (2010). In situ visualization and dynamics of newly synthesized proteins in rat hippocampal neurons. Nat. Neurosci. 13, 897-905.
19. Dunn, K. W., Kamocka, M. M. and McDonald, J. H. (2011). A practical guide to evaluating colocalization in biological microscopy. Am. J. Physiol. 300, C723-C742.
20. Eberle, A. B., Lykke-Andersen, S., Mühlemann, O. and Jensen, T. H. (2009). SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat. Struct. Mol. Biol. 16, 49-55.
21. Eulalio, A., Behm-Ansmant, I., Schweizer, D. and Izaurralde, E. (2007). P-body formation is a consequence, not the cause, of RNA-mediated gene silencing. Mol. Cell. Biol. 27, 3970-3981.
22. Farris, S., Lewandowski, G., Cox, C. D. and Steward, O. (2014). Selective localization of arc mRNA in dendrites involves activity- and translation-dependent mRNA degradation. J. Neurosci. 34, 4481-4493.
23. Gatfield, D. and Izaurralde, E. (2004). Nonsense-mediated messenger RNA decay is initiated by endonucleolytic cleavage in Drosophila. Nature 429, 575-578.
24. Giorgi, C., Yeo, G. W., Stone, M. E., Katz, D. B., Burge, C., Turrigiano, G. and Moore, M. J. (2007). The EJC factor eIF4AIII modulates synaptic strength and neuronal protein expression. Cell 130, 179-191.
25. Graber, T. E., Hébert-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.
26. 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.
27. Hillebrand, J., Pan, K., Kokaram, A., Barbee, S., Parker, R. and Ramaswami, M. (2010). The Me31B DEAD-Box helicase localizes to postsynaptic foci and regulates expression of a CaMKII reporter mRNA in dendrites of Drosophila olfactory projection neurons. Front. Neural Circuits 4, 121.
28. Huang, Y. W., Ruiz, C. R., Eyler, E. C., Lin, K. and Meffert, M. K. (2012). Dual regulation of miRNA biogenesis generates target specificity in neurotrophin-induced protein synthesis. Cell 148, 933-946.
29. Hubstenberger, A., Noble, S. L., Cameron, C. and Evans, T. C. (2013). Translation repressors, an RNA helicase, and developmental cues control RNP phase transitions during early development. Dev. Cell 27, 161-173.
30. Huntzinger, E. and Izaurralde, E. (2011). Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat. Rev. Genet. 12, 99-110.
31. Ingelfinger, D., Arndt-Jovin, D. J., Lührmann, R. and Achsel, T. (2002). The human LSm1-7 proteins colocalize with the mRNA-degrading enzymes Dcp1/2 and Xrnl in distinct cytoplasmic foci. RNA 8, 1489-1501.
32. Job, C. and Eberwine, J. (2001). Identification of sites for exponential translation in living dendrites. Proc. Natl. Acad. Sci. USA 98, 13037-13042.
33. Jonas, S. and Izaurralde, E. (2013). The role of disordered protein regions in the assembly of decapping complexes and RNP granules. Genes Dev. 27, 2628-2641.
34. Jones, C. I., Zabolotskaya, M. V. and Newbury, S. F. (2012). The 5' → 3' exoribonuclease XRN1/Pacman and its functions in cellular processes and development. Wiley Interdiscip. Rev. RNA 3, 455-468.
35. Jones, C. I., Grima, D. P., Waldron, J. A., Jones, S., Parker, H. N. and Newbury, S. F. (2013). The 59-39 exoribonuclease Pacman (Xrn1) regulates expression of the heat shock protein Hsp67Bc and the microRNA miR-277-3p in Drosophila wing imaginal discs. RNA Biol. 10, 1345-1355.
36. Kato, M., Han, T. W., Xie, S., Shi, K., Du, X., Wu, L. C., Mirzaei, H., Goldsmith, E. J., Longgood, J., Pei, J. et al. (2012). Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 149, 753-767.
37. Kotani, T., Yasuda, K., Ota, R. and Yamashita, M. (2013). Cyclin B1 mRNA translation is temporally controlled through formation and disassembly of RNA granules. J. Cell Biol. 202, 1041-1055.
38. Kramer, K., Sachsenberg, T., Beckmann, B. M., Qamar, S., Boon, K. L., Hentze, M. W., Kohlbacher, O. and Urlaub, H. (2014). Photo-cross-linking and high-resolution mass spectrometry for assignment of RNA-binding sites in RNAbinding proteins. Nat. Methods 11, 1064-1070.
39. Lejeune, F., Li, X. and Maquat, L. E. (2003). Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities. Mol. Cell 12, 675-687.
40. Leski, M. L. and Steward, O. (1996). Protein synthesis within dendrites: ionic and neurotransmitter modulation of synthesis of particular polypeptides characterized by gel electrophoresis. Neurochem. Res. 21, 681-690.
41. Li, Y., Song, M. and Kiledjian, M. (2011). Differential utilization of decapping enzymes in mammalian mRNA decay pathways. RNA 17, 419-428.
42. Lin, M. D., Jiao, X., Grima, D., Newbury, S. F., Kiledjian, M. and Chou, T. B. (2008). Drosophila processing bodies in oogenesis. Dev. Biol. 322, 276-288.
43. Loschi, M., Leishman, C. C., Berardone, N. and Boccaccio, G. L. (2009). Dynein and kinesin regulate stress-granule and P-body dynamics. J. Cell Sci. 122, 3973-3982.
44. Marin, P., Nastiuk, K. L., Daniel, N., Girault, J. A., Czernik, A. J., Glowinski, J., Nairn, A. C. and Prémont, J. (1997). Glutamate-dependent phosphorylation of elongation factor-2 and inhibition of protein synthesis in neurons. J. Neurosci. 17, 3445-3454.
45. Miller, L. C., Blandford, V., McAdam, R., Sanchez-Carbente, M. R., Badeaux, F., DesGroseillers, L. and Sossin, W. S. (2009). Combinations of DEAD box proteins distinguish distinct types of RNA: protein complexes in neurons. Mol. Cell. Neurosci. 40, 485-495.
46. Nagarajan, V. K., Jones, C. I., Newbury, S. F. and Green, P. J. (2013). XRN 59R39 exoribonucleases: structure, mechanisms and functions. Biochim. Biophys. Acta 1829, 590-603.
47. Newbury, S. and Woollard, A. (2004). The 59-39 exoribonuclease xrn-1 is essential for ventral epithelial enclosure during C. elegans embryogenesis. RNA 10, 59-65.
48. Park, E. and Maquat, L. E. (2013). Staufen-mediated mRNA decay. Wiley Interdiscip Rev. RNA 4, 423-435.
49. Park, S., Park, J. M., Kim, S., Kim, J. A., Shepherd, J. D., Smith-Hicks, C. L., Chowdhury, S., Kaufmann, W., Kuhl, D., Ryazanov, A. G. et al. (2008). Elongation factor 2 and fragile X mental retardation protein control the dynamic translation of Arc/Arg3.1 essential for mGluR-LTD. Neuron 59, 70-83.
50. 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.
51. Pascual, M. L., Luchelli, L., Habif, M. and Boccaccio, G. L. (2012). Synaptic activity regulated mRNA-silencing foci for the fine tuning of local protein synthesis at the synapse. Commun. Integr. Biol. 5, 388-392.
52. Pimentel, J. and Boccaccio, G. L. (2014). Translation and silencing in RNA granules: a tale of sand grains. Front. Mol. Neurosci. 7, 68.
53. Pradhan, S. J., Nesler, K. R., Rosen, S. F., Kato, Y., Nakamura, A., Ramaswami, M. and Barbee, S. A. (2012). The conserved P body component HPat/Pat1 negatively regulates synaptic terminal growth at the larval Drosophila neuromuscular junction. J. Cell Sci. 125, 6105-6116.
54. Raab-Graham, K. F., Haddick, P. C., Jan, Y. N. and Jan, L. Y. (2006). Activity- and mTOR-dependent suppression of Kv1.1 channel mRNA translation in dendrites. Science 314, 144-148.
55. Rymarquis, L. A., Souret, F. F. and Green, P. J. (2011). Evidence that XRN4, an Arabidopsis homolog of exoribonuclease XRN1, preferentially impacts transcripts with certain sequences or in particular functional categories. RNA 17, 501-511.
56. Scheetz, A. J., Nairn, A. C. and Constantine-Paton, M. (2000). NMDA receptor-mediated control of protein synthesis at developing synapses. Nat. Neurosci. 3, 211-216.
57. Schratt, G. (2009). microRNAs at the synapse. Nat. Rev. Neurosci. 10, 842-849.
58. Sinturel, F., Bréchemier-Baey, D., Kiledjian, M., Condon, C. and Bénard, L. (2012). Activation of 59-39 exoribonuclease Xrn1 by cofactor Dcs1 is essential for mitochondrial function in yeast. Proc. Natl. Acad. Sci. USA 109, 8264-8269.
59. Siwaszek, A., Ukleja, M. and Dziembowski, A. (2014). Proteins involved in the degradation of cytoplasmic mRNA in the major eukaryotic model systems. RNA Biol. 11, 1122-1136.
60. Sosanya, N. M., Huang, P. P., Cacheaux, L. P., Chen, C. J., Nguyen, K., Perrone-Bizzozero, N. I. and Raab-Graham, K. F. (2013). Degradation of high affinity HuD targets releases Kv1.1 mRNA from miR-129 repression by mTORC1. J. Cell Biol. 202, 53-69.
61. Souret, F. F., Kastenmayer, J. P. and Green, P. J. (2004). AtXRN4 degrades mRNA in Arabidopsis and its substrates include selected miRNA targets. Mol. Cell 15, 173-183.
62. Sutton, M. A., Wall, N. R., Aakalu, G. N. and Schuman, E. M. (2004). Regulation of dendritic protein synthesis by miniature synaptic events. Science 304, 1979-1983.
63. Sutton, M. A., Ito, H. T., Cressy, P., Kempf, C., Woo, J. C. and Schuman, E. M. (2006). Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis. Cell 125, 785-799.
64. Sutton, M. A., Taylor, A. M., Ito, H. T., Pham, A. and Schuman, E. M. (2007). Postsynaptic decoding of neural activity: eEF2 as a biochemical sensor coupling miniature synaptic transmission to local protein synthesis. Neuron 55, 648-661.
65. 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.
66. Thomas, M. G., Martinez Tosar, L. J., Desbats, M. A., Leishman, C. C. and Boccaccio, G. L. (2009). Mammalian Staufen 1 is recruited to stress granules and impairs their assembly. J. Cell Sci. 122, 563-573.
67. Thomas, M. G., Loschi, M., Desbats, M. A. and Boccaccio, G. L. (2011). RNA granules: the good, the bad and the ugly. Cell. Signal. 23, 324-334.
68. Thomas, M. G., Luchelli, L., Pascual, M., Gottifredi, V. and Boccaccio, G. L. (2012). A monoclonal antibody against p53 cross-reacts with processing bodies. PLoS ONE 7, e36447.
69. Thomas, M. G., Pascual, M. L., Maschi, D., Luchelli, L. and Boccaccio, G. L. (2014). Synaptic control of local translation: the plot thickens with new characters. Cell. Mol. Life Sci. 71, 2219-2239.
70. Toretsky, J. A. and Wright, P. E. (2014). Assemblages: functional units formed by cellular phase separation. J. Cell Biol. 206, 579-588.
71. Weiler, I. J. and Greenough, W. T. (1993). Metabotropic glutamate receptors trigger postsynaptic protein synthesis. Proc. Natl. Acad. Sci. USA 90, 7168-7171.
72. Weiler, I. J., Spangler, C. C., Klintsova, A. Y., Grossman, A. W., Kim, S. H., Bertaina-Anglade, V., Khaliq, H., de Vries, F. E., Lambers, F. A., Hatia, F. et al. (2004). Fragile X mental retardation protein is necessary for neurotransmitter-activated protein translation at synapses. Proc. Natl. Acad. Sci. USA 101, 17504-17509.
73. Yasuda, K., Zhang, H., Loiselle, D., Haystead, T., Macara, I. G. and Mili, S. (2013). The RNA-binding protein Fus directs translation of localized mRNAs in APC-RNP granules. J. Cell Biol. 203, 737-746.
74. 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.