Asymmetric mRNA localization contributes to fidelity and sensitivity of spatially localized systems

Nature Structural and Molecular Biology

Volumn 21, Issue 9, 2014, Pages 833-839

  Weatheritt, Robert J ^a,c   Gibson, Toby J ^b   Babu, M Madan ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH FACTOR; MESSENGER RNA; PROTEIN; PROTEOME;

ADULT; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FEMALE; GENOME ANALYSIS; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; RAT; RNA TRANSCRIPTION; RNA TRANSPORT; SIGNAL TRANSDUCTION; SPATIOTEMPORAL ANALYSIS; TRANSLATION REGULATION; ANIMAL; METABOLISM;

MAMMALIA;

ANIMALS; MICE; PROTEIN BIOSYNTHESIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEINS; RATS; RNA TRANSPORT; RNA, MESSENGER;

EID: 84921951502     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2876     Document Type: Article

References (85)

1. Martin, K.C. & Ephrussi, A. mRNA localization: gene expression in the spatial dimension. Cell 136, 719-730 (2009).
2. Scott, J.D. & Pawson, T. Cell signaling in space and time: where proteins come together and when they're apart. Science 326, 1220-1224 (2009).
3. Ephrussi, A., Dickinson, L.K. & Lehmann, R. Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 66, 37-50 (1991).
4. Holt, C.E. & Bullock, S.L. Subcellular mRNA localization in animal cells and why it matters. Science 326, 1212-1216 (2009).
5. Jung, H., Gkogkas, C.G., Sonenberg, N. & Holt, C.E. Remote control of gene function by local translation. Cell 157, 26-40 (2014).
6. Lecuyer, E. Et al. Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131, 174-187 (2007).
7. Pertz, O.C. Et al. Spatial mapping of the neurite and soma proteomes reveals a functional Cdc42/Rac regulatory network. Proc. Natl. Acad. Sci. USA 105, 1931-1936 (2008).
8. Wang, Y. Et al. Profiling signaling polarity in chemotactic cells. Proc. Natl. Acad. Sci. USA 104, 8328-8333 (2007).
9. Cajigas, I.J. Et al. The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging. Neuron 74, 453-466 (2012).
10. Nevo-Dinur, K., Nussbaum-Shochat, A., Ben-Yehuda, S. & Amster-Choder, O. Translation-independent localization of mRNA in E. Coli. Science 331, 1081-1084 (2011).
11. Huttelmaier, S. Et al. Spatial regulation of beta-actin translation by Src-dependent phosphorylation of ZBP1. Nature 438, 512-515 (2005).
12. Weis, B.L., Schleiff, E. & Zerges, W. Protein targeting to subcellular organelles via MRNA localization. Biochim. Biophys. Acta 1833, 260-273 (2013).
13. Feltrin, D. Et al. Growth cone MKK7 mRNA targeting regulates MAP1b-dependent microtubule bundling to control neurite elongation. PLoS Biol. 10, e1001439 (2012).
14. van der Lee, R. Et al. Classification of intrinsically disordered regions and proteins. Chem. Rev. 114, 6589-6631 (2014).
15. Van Roey, K. Et al. Short linear motifs: ubiquitous and functionally diverse protein interaction modules directing cell regulation. Chem. Rev. 114, 6733-6778 (2014).
16. Bockers, T.M. Et al. Differential expression and dendritic transcript localization of Shank family members: identification of a dendritic targeting element in the 3′ untranslated region of Shank1 mRNA. Mol. Cell. Neurosci. 26, 182-190 (2004).
17. Davey, N.E. Et al. Attributes of short linear motifs. Mol. Biosyst. 8, 268-281 (2012).
18. Dosztanyi, Z., Meszaros, B. & Simon, I. ANCHOR: web server for predicting protein binding regions in disordered proteins. Bioinformatics 25, 2745-2746 (2009).
19. Van Roey, K., Dinkel, H., Weatheritt, R.J., Gibson, T.J. & Davey, N.E. The switches.ELM Resource: A Compendium of Conditional Regulatory Interaction Interfaces. Sci. Signal. 6, rs7 (2013).
20. Li, P. Et al. Phase transitions in the assembly of multivalent signalling proteins. Nature 483, 336-340 (2012).
21. Cumberworth, A., Lamour, G., Babu, M.M. & Gsponer, J. Promiscuity as a functional trait: intrinsically disordered regions as central players of interactomes. Biochem. J. 454, 361-369 (2013).
22. Wu, H. Higher-order assemblies in a new paradigm of signal transduction. Cell 153, 287-292 (2013).
23. Takenawa, T. & Suetsugu, S. The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat. Rev. Mol. Cell Biol. 8, 37-48 (2007).
24. Van Roey, K., Gibson, T.J. & Davey, N.E. Motif switches: decision-making in cell regulation. Curr. Opin. Struct. Biol. 22, 378-385 (2012).
25. Honnappa, S. Et al. An EB1-binding motif acts as a microtubule tip localization signal. Cell 138, 366-376 (2009).
26. Mili, S., Moissoglu, K. & Macara, I.G. Genome-wide screen reveals APC-associated RNAs enriched in cell protrusions. Nature 453, 115-119 (2008).
27. Nozumi, M. Et al. Identification of functional marker proteins in the mammalian growth cone. Proc. Natl. Acad. Sci. USA 106, 17211-17216 (2009).
28. Xiong, X. Et al. Enrichment and proteomic analysis of plasma membrane from rat dorsal root ganglions. Proteome Sci. 7, 41 (2009).
29. Gumy, L.F. Et al. Transcriptome analysis of embryonic and adult sensory axons reveals changes in mRNA repertoire localization. RNA 17, 85-98 (2011).
30. Schwanhausser, B. Et al. Global quantification of mammalian gene expression control. Nature 473, 337-342 (2011).
31. Gsponer, J. & Babu, M.M. Cellular strategies for regulating functional and nonfunctional protein aggregation. Cell Reports 2, 1425-1437 (2012).
32. Sasaki, Y., Gross, C., Xing, L., Goshima, Y. & Bassell, G.J. Identification of axon-enriched MicroRNAs localized to growth cones of cortical neurons. Dev. Neurobiol. 74, 397-406 (2014).
33. Gsponer, J., Futschik, M.E., Teichmann, S.A. & Babu, M.M. Tight regulation of unstructured proteins: from transcript synthesis to protein degradation. Science 322, 1365-1368 (2008).
34. Gibson, T.J., Seiler, M. & Veitia, R.A. The transience of transient overexpression. Nat. Methods 10, 715-721 (2013).
35. von Kriegsheim, A. Et al. Cell fate decisions are specified by the dynamic ERK interactome. Nat. Cell Biol. 11, 1458-1464 (2009).
36. Christensen, G.L. Et al. Quantitative phosphoproteomics dissection of seven-transmembrane receptor signaling using full and biased agonists. Mol. Cell. Proteomics 9, 1540-1553 (2010).
37. Mausbacher, N., Schreiber, T.B., Machatti, M., Schaab, C. & Daub, H. Proteome-wide analysis of temporal phosphorylation dynamics in lysophosphatidic acid-induced signaling. Proteomics 12, 3485-3498 (2012).
38. Olsen, J.V. Et al. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648 (2006).
39. Buxbaum, A.R., Wu, B. & Singer, R.H. Single beta-actin mRNA detection in neurons reveals a mechanism for regulating its translatability. Science 343, 419-422 (2014).
40. Yoon, B.C. Et al. Local translation of extranuclear lamin B promotes axon maintenance. Cell 148, 752-764 (2012).
41. Scott, D.A., Das, U., Tang, Y. & Roy, S. Mechanistic logic underlying the axonal transport of cytosolic proteins. Neuron 70, 441-454 (2011).
42. Vavouri, T., Semple, J.I., Garcia-Verdugo, R. & Lehner, B. Intrinsic protein disorder and interaction promiscuity are widely associated with dosage sensitivity. Cell 138, 198-208 (2009).
43. Babu, M.M., van der Lee, R., de Groot, N.S. & Gsponer, J. Intrinsically disordered proteins: regulation and disease. Curr. Opin. Struct. Biol. 21, 432-440 (2011).
44. Jones, R.B., Gordus, A., Krall, J.A. & MacBeath, G. A quantitative protein interaction network for the ErbB receptors using protein microarrays. Nature 439, 168-174 (2006).
45. Roux, P.P. & Topisirovic, I. Regulation of mRNA translation by signaling pathways. Cold Spring Harb. Perspect. Biol. 4, a012252 (2012).
46. Xue, S. & Barna, M. Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat. Rev. Mol. Cell Biol. 13, 355-369 (2012).
47. Marc, P. Et al. Genome-wide analysis of mRNAs targeted to yeast mitochondria. EMBO Rep. 3, 159-164 (2002).
48. Gibson, T.J. Cell regulation: determined to signal discrete cooperation. Trends Biochem. Sci. 34, 471-482 (2009).
49. Hyman, A.A. & Brangwynne, C.P. Beyond stereospecificity: liquids and mesoscale organization of cytoplasm. Dev. Cell 21, 14-16 (2011).
50. Ladbury, J.E. & Arold, S.T. Noise in cellular signaling pathways: causes and effects. Trends Biochem. Sci. 37, 173-178 (2012).
51. Darnell, J.C. Et al. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146, 247-261 (2011).
52. Zheng, Y. Et al. Temporal regulation of EGF signalling networks by the scaffold protein Shc1. Nature 499, 166-171 (2013).
53. Ji, S.J. & Jaffrey, S.R. Intra-axonal translation of SMAD1/5/8 mediates retrograde regulation of trigeminal ganglia subtype specification. Neuron 74, 95-107 (2012).
54. Kundel, M., Jones, K.J., Shin, C.Y. & Wells, D.G. Cytoplasmic polyadenylation element-binding protein regulates neurotrophin-3-dependent beta-catenin mRNA translation in developing hippocampal neurons. J. Neurosci. 29, 13630-13639 (2009).
55. Yudin, D. Et al. Localized regulation of axonal RanGTPase controls retrograde injury signaling in peripheral nerve. Neuron 59, 241-252 (2008).
56. Hengst, U., Deglincerti, A., Kim, H.J., Jeon, N.L. & Jaffrey, S.R. Axonal elongation triggered by stimulus-induced local translation of a polarity complex protein. Nat. Cell Biol. 11, 1024-1030 (2009).
57. Gavis, E.R. & Lehmann, R. Localization of nanos RNA controls embryonic polarity. Cell 71, 301-313 (1992).
58. Han, T.W. Et al. Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies. Cell 149, 768-779 (2012).
59. Ostlund, G. Et al. InParanoid 7: new algorithms and tools for eukaryotic orthology analysis. Nucleic Acids Res. 38, D196-D203 (2010).
60. Schwanhausser, B. Et al. Corrigendum: Global quantification of mammalian gene expression control. Nature 495, 126-127 (2013).
61. Kinsella, R.J. Et al. Ensembl BioMarts: a hub for data retrieval across taxonomic space. Database (Oxford) 2011, bar030 (2011).
62. Dennis, G. Et al. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4, 3 (2003).
63. Bult, C.J., Eppig, J.T., Blake, J.A., Kadin, J.A. & Richardson, J.E. The mouse genome database: genotypes, phenotypes, and models of human disease. Nucleic Acids Res. 41, D885-D891 (2013).
64. Franceschini, A. Et al. STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 41, D808-D815 (2013).
65. Ruepp, A. Et al. CORUM: the comprehensive resource of mammalian protein complexes-2009. Nucleic Acids Res. 38, D497-D501 (2010).
66. Dosztanyi, Z., Csizmok, V., Tompa, P. & Simon, I. The pairwise energy content estimated from amino acid composition discriminates between folded and intrinsically unstructured proteins. J. Mol. Biol. 347, 827-839 (2005).
67. Weatheritt, R.J., Luck, K., Petsalaki, E., Davey, N.E. & Gibson, T.J. The identification of short linear motif-mediated interfaces within the human interactome. Bioinformatics 28, 976-982 (2012).
68. Punta, M. Et al. The Pfam protein families database. Nucleic Acids Res. 40, D290-D301 (2012).
69. Alberti, S., Halfmann, R., King, O., Kapila, A. & Lindquist, S. A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 137, 146-158 (2009).
70. Halfmann, R. Et al. Opposing effects of glutamine and asparagine govern prion formation by intrinsically disordered proteins. Mol. Cell 43, 72-84 (2011).
71. Michelitsch, M.D. & Weissman, J.S. A census of glutamine/asparagine-rich regions: implications for their conserved function and the prediction of novel prions. Proc. Natl. Acad. Sci. USA 97, 11910-11915 (2000).
72. Toombs, J.A., McCarty, B.R. & Ross, E.D. Compositional determinants of prion formation in yeast. Mol. Cell. Biol. 30, 319-332 (2010).
73. Ader, C. Et al. Amyloid-like interactions within nucleoporin FG hydrogels. Proc. Natl. Acad. Sci. USA 107, 6281-6285 (2010).
74. Kato, M. Et al. Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 149, 753-767 (2012).
75. Updike, D.L., Hachey, S.J., Kreher, J. & Strome, S. P granules extend the nuclear pore complex environment in the C. Elegans germ line. J. Cell Biol. 192, 939-948 (2011).
76. Malinovska, L., Kroschwald, S. & Alberti, S. Protein disorder, prion propensities, and self-organizing macromolecular collectives. Biochim. Biophys. Acta 1834, 918-931 (2013).
77. Hornbeck, P.V. Et al. PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res. 40, D261-D270 (2012).
78. UniProt Consortium. Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res. 40, D71-D75 (2012).
79. Griffiths-Jones, S., Saini, H.K., van Dongen, S. & Enright, A.J. miRBase: tools for microRNA genomics. Nucleic Acids Res. 36, D154-D158 (2008).
80. Lewis, B.P., Burge, C.B. & Bartel, D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20 (2005).
81. Halees, A.S., El-Badrawi, R. & Khabar, K.S. ARED organism: expansion of ARED reveals AU-rich element cluster variations between human and mouse. Nucleic Acids Res. 36, D137-D140 (2008).
82. Pique, M., Lopez, J.M., Foissac, S., Guigo, R. & Mendez, R. A combinatorial code for CPE-mediated translational control. Cell 132, 434-448 (2008).
83. Gupta, R., Bhattacharyya, A., Agosto-Perez, F.J., Wickramasinghe, P. & Davuluri, R.V. MPromDb update 2010: an integrated resource for annotation and visualization of mammalian gene promoters and ChIP-seq experimental data. Nucleic Acids Res. 39, D92-D97 (2011).
84. McGraw, K.O. & Wong, S.P. A common language effect size statistic. Psychol. Bull. 111, 361-365 (1992).
85. Grissom, R.J. & Kim, J.J. Effect Sizes for Research: Univariate and Multivariate Applications (Routledge, 2012).