Pausing on Polyribosomes: Make Way for Elongation in Translational Control

Cell

Volumn 163, Issue 2, 2015, Pages 292-300

  Richter, Joel D ^a   Coller, Jeff ^b  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; TRANSFER RNA; CODON;

CARCINOGENESIS; CELL STRESS; CODON USAGE; FRAGILE X SYNDROME; NERVE CELL; NERVE CELL PLASTICITY; NERVE DEGENERATION; NEUROLOGIC DISEASE; NONHUMAN; POLYSOME; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; RIBOSOME; RNA TRANSLATION; TRANSCRIPTION ELONGATION; TRANSCRIPTION TERMINATION; TRANSLATION INITIATION; ANIMAL; CODON; DISEASES; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM;

ANIMALS; CODON; DISEASE; GENE EXPRESSION REGULATION; HUMANS; PEPTIDE CHAIN ELONGATION, TRANSLATIONAL; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; POLYRIBOSOMES; RNA, MESSENGER; RNA, TRANSFER;

EID: 84943742690     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.09.041     Document Type: Review

References (71)

1. H. Akashi Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy Genetics 136 1994 927 935
2. P. Anderson, and N. Kedersha RNA granules: post-transcriptional and epigenetic modulators of gene expression Nat. Rev. Mol. Cell Biol. 10 2009 430 436
3. S. Andrews, D.R. Snowflack, I.E. Clark, and E.R. Gavis Multiple mechanisms collaborate to repress nanos translation in the Drosophila ovary and embryo RNA 17 2011 967 977
4. D.G. Ballinger, and M.L. Pardue The control of protein synthesis during heat shock in Drosophila cells involves altered polypeptide elongation rates Cell 33 1983 103 113
5. B. Baragaña, I. Hallyburton, M.C.S. Lee, N.R. Norcross, R. Grimaldi, T.D. Otto, W.R. Proto, A.M. Blagborough, S. Meister, G. Wirjanata, and et al. A novel multiple-stage antimalarial agent that inhibits protein synthesis Nature 522 2015 315 320
6. A.A. Bazzini, M.T. Lee, and A.J. Giraldez Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in zebrafish Science 336 2012 233 237
7. A. Bhattacharya, H. Kaphzan, A.C. Alvarez-Dieppa, J.P. Murphy, P. Pierre, and E. Klann Genetic removal of p70 S6 kinase 1 corrects molecular, synaptic, and behavioral phenotypes in fragile X syndrome mice Neuron 76 2012 325 337
8. A.K. Braat, N. Yan, E. Arn, D. Harrison, and P.M. Macdonald Localization-dependent oskar protein accumulation; control after the initiation of translation Dev. Cell 7 2004 125 131
9. J.W. Brandis, and R.A. Raff Translation of oogenetic mRNA in sea urchin eggs and early embryos. Demonstration of a change in translational efficiency following fertilization Dev. Biol. 67 1978 99 113
10. A.R. Buxbaum, B. Wu, and R.H. Singer Single β-actin mRNA detection in neurons reveals a mechanism for regulating its translatability Science 343 2014 419 422
11. C.T.Y. Chan, Y.L.J. Pang, W. Deng, I.R. Babu, M. Dyavaiah, T.J. Begley, and P.C. Dedon Reprogramming of tRNA modifications controls the oxidative stress response by codon-biased translation of proteins Nat. Commun. 3 2012 937
12. R.E. Chapman, and P. Walter Translational attenuation mediated by an mRNA intron Curr. Biol. 7 1997 850 859
13. E. Chen, M.R. Sharma, X. Shi, R.K. Agrawal, and S. Joseph Fragile X mental retardation protein regulates translation by binding directly to the ribosome Mol. Cell 54 2014 407 417
14. I.E. Clark, D. Wyckoff, and E.R. Gavis Synthesis of the posterior determinant Nanos is spatially restricted by a novel cotranslational regulatory mechanism Curr. Biol. 10 2000 1311 1314
15. F. Corbin, M. Bouillon, A. Fortin, S. Morin, F. Rousseau, and E.W. Khandjian The fragile X mental retardation protein is associated with poly(A)+ mRNA in actively translating polyribosomes Hum. Mol. Genet. 6 1997 1465 1472
16. F.H. Crick The origin of the genetic code J. Mol. Biol. 38 1968 367 379
17. J.C. Darnell Molecular biology. Ribosome rescue and neurodegeneration Science 345 2014 378 379
18. J.C. Darnell, S.J. Van Driesche, C. Zhang, K.Y. Hung, A. Mele, C.E. Fraser, E.F. Stone, C. Chen, J.J. Fak, S.W. Chi, and et al. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism Cell 146 2011 247 261
19. C.J. Decker, and R. Parker P-bodies and stress granules: possible roles in the control of translation and mRNA degradation Cold Spring Harb. Perspect. Biol. 4 2012 a012286
20. G. Dölen, E. Osterweil, B.S. Rao, G.B. Smith, B.D. Auerbach, S. Chattarji, and M.F. Bear Correction of fragile X syndrome in mice Neuron 56 2007 955 962
21. D.A. Drummond, and C.O. Wilke Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution Cell 134 2008 341 352
22. W.J. Faller, T.J. Jackson, J.R. Knight, R.A. Ridgway, T. Jamieson, S.A. Karim, C. Jones, S. Radulescu, D.J. Huels, K.B. Myant, and et al. mTORC1-mediated translational elongation limits intestinal tumour initiation and growth Nature 517 2015 497 500
23. Y. Feng, D. Absher, D.E. Eberhart, V. Brown, H.E. Malter, and S.T. Warren FMRP associates with polyribosomes as an mRNP, and the I304N mutation of severe fragile X syndrome abolishes this association Mol. Cell 1 1997 109 118
24. H. Gingold, D. Tehler, N.R. Christoffersen, M.M. Nielsen, F. Asmar, S.M. Kooistra, N.S. Christophersen, L.L. Christensen, M. Borre, K.D. Sørensen, and et al. A dual program for translation regulation in cellular proliferation and differentiation Cell 158 2014 1281 1292
25. T.E. Graber, S. Hébert-Seropian, A. Khoutorsky, A. David, J.W. Yewdell, J.C. Lacaille, and W.S. Sossin Reactivation of stalled polyribosomes in synaptic plasticity Proc. Natl. Acad. Sci. USA 110 2013 16205 16210
26. C. Gross, N. Raj, G. Molinaro, A.G. Allen, A.J. Whyte, J.R. Gibson, K.M. Huber, S.L. Gourley, and G.J. Bassell Selective role of the catalytic PI3K subunit p110β in impaired higher order cognition in fragile X syndrome Cell Rep. 11 2015 681 688
27. W. Gu, T. Zhou, and C.O. Wilke A universal trend of reduced mRNA stability near the translation-initiation site in prokaryotes and eukaryotes PLoS Comput. Biol. 6 2010 e1000664
28. E. Gutierrez, B.-S. Shin, C.J. Woolstenhulme, J.-R. Kim, P. Saini, A.R. Buskirk, and T.E. Dever eIF5A promotes translation of polyproline motifs Mol. Cell 51 2013 35 45
29. M. Halic, T. Becker, M.R. Pool, C.M.T. Spahn, R.A. Grassucci, J. Frank, and R. Beckmann Structure of the signal recognition particle interacting with the elongation-arrested ribosome Nature 427 2004 808 814
30. A.G. Hinnebusch The scanning mechanism of eukaryotic translation initiation Annu. Rev. Biochem. 83 2014 779 812
31. J. Huang, Y. Ikeuchi, M. Malumbres, and A. Bonni A Cdh1-APC/FMRP ubiquitin signaling link drives mGluR-dependent synaptic plasticity in the mammalian brain Neuron 86 2015 726 739
32. N.T. Ingolia, S. Ghaemmaghami, J.R. Newman, and J.S. Weissman Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling Science 324 2009 218 223
33. R. Ishimura, G. Nagy, I. Dotu, H. Zhou, X.L. Yang, P. Schimmel, S. Senju, Y. Nishimura, J.H. Chuang, and S.L. Ackerman RNA function. Ribosome stalling induced by mutation of a CNS-specific tRNA causes neurodegeneration Science 345 2014 455 459
34. Y. Kanai, N. Dohmae, and N. Hirokawa Kinesin transports RNA: isolation and characterization of an RNA-transporting granule Neuron 43 2004 513 525
35. H. Kang, and E.M. Schuman A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity Science 273 1996 1402 1406
36. K.S. Koutmou, A.P. Schuller, J.L. Brunelle, A. Radhakrishnan, S. Djuranovic, and R. Green Ribosomes slide on lysine-encoding homopolymeric A stretches eLife 4 2015 10.7554/eLife.05534
37. A.M. Krichevsky, and K.S. Kosik Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation Neuron 32 2001 683 696
38. A. Krisko, T. Copic, T. Gabaldón, B. Lehner, and F. Supek Inferring gene function from evolutionary change in signatures of translation efficiency Genome Biol. 15 2014 R44
39. R.C. Lee, R.L. Feinbaum, and V. Ambros The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14 Cell 75 1993 843 854
40. J.W. Lee, K. Beebe, L.A. Nangle, J. Jang, C.M. Longo-Guess, S.A. Cook, M.T. Davisson, J.P. Sundberg, P. Schimmel, and S.L. Ackerman Editing-defective tRNA synthetase causes protein misfolding and neurodegeneration Nature 443 2006 50 55
41. G. Leprivier, M. Remke, B. Rotblat, A. Dubuc, A.R. Mateo, M. Kool, S. Agnihotri, A. El-Naggar, B. Yu, S.P. Somasekharan, and et al. The eEF2 kinase confers resistance to nutrient deprivation by blocking translation elongation Cell 153 2013 1064 1079
42. B. Liu, Y. Han, and S.B. Qian Cotranslational response to proteotoxic stress by elongation pausing of ribosomes Mol. Cell 49 2013 453 463
43. Y. Mamane, E. Petroulakis, L. Rong, K. Yoshida, L.W. Ler, and N. Sonenberg eIF4E - from translation to transformation Oncogene 23 2004 3172 3179
44. P.A. Maroney, Y. Yu, J. Fisher, and T.W. Nilsen Evidence that microRNAs are associated with translating messenger RNAs in human cells Nat. Struct. Mol. Biol. 13 2006 1102 1107
45. K.C. Martin, A. Casadio, H. Zhu, E. Yaping, J.C. Rose, M. Chen, C.H. Bailey, and E.R. Kandel Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: a function for local protein synthesis in memory storage Cell 91 1997 927 938
46. V.C. Nalavadi, R.S. Muddashetty, C. Gross, and G.J. Bassell Dephosphorylation-induced ubiquitination and degradation of FMRP in dendrites: a role in immediate early mGluR-stimulated translation J. Neurosci. 32 2012 2582 2587
47. S. Nottrott, M.J. Simard, and J.D. Richter Human let-7a miRNA blocks protein production on actively translating polyribosomes Nat. Struct. Mol. Biol. 13 2006 1108 1114
48. E.M. Novoa, and L. Ribas de Pouplana Speeding with control: codon usage, tRNAs, and ribosomes Trends Genet. 28 2012 574 581
49. P.H. Olsen, and V. Ambros The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation Dev. Biol. 216 1999 671 680
50. J.L. Parmley, J.V. Chamary, and L.D. Hurst Evidence for purifying selection against synonymous mutations in mammalian exonic splicing enhancers Mol. Biol. Evol. 23 2006 301 309
51. S. Pechmann, and J. Frydman Evolutionary conservation of codon optimality reveals hidden signatures of cotranslational folding Nat. Struct. Mol. Biol. 20 2013 237 243
52. J. Pelletier, J. Graff, D. Ruggero, and N. Sonenberg Targeting the eIF4F translation initiation complex: a critical nexus for cancer development Cancer Res. 75 2015 250 263
53. C.P. Petersen, M.E. Bordeleau, J. Pelletier, and P.A. Sharp Short RNAs repress translation after initiation in mammalian cells Mol. Cell 21 2006 533 542
54. V. Presnyak, N. Alhusaini, Y.H. Chen, S. Martin, N. Morris, N. Kline, S. Olson, D. Weinberg, K.E. Baker, B.R. Graveley, and J. Coller Codon optimality is a major determinant of mRNA stability Cell 160 2015 1111 1124
55. C.G. Proud eIF2 and the control of cell physiology Semin. Cell Dev. Biol. 16 2005 3 12
56. M.D. Reis, R. Savva, and L. Wernisch Solving the riddle of codon usage preferences: a test for translational selection Nucleic Acids Res. 32 2004 5036 5044
57. J.D. Richter, and N. Sonenberg Regulation of cap-dependent translation by eIF4E inhibitory proteins Nature 433 2005 477 480
58. J.D. Richter, W.J. Wasserman, and L.D. Smith The mechanism for increased protein synthesis during Xenopus oocyte maturation Dev. Biol. 89 1982 159 167
59. U. Rüegsegger, J.H. Leber, and P. Walter Block of HAC1 mRNA translation by long-range base pairing is released by cytoplasmic splicing upon induction of the unfolded protein response Cell 107 2001 103 114
60. A.J. Scheetz, A.C. Nairn, and M. Constantine-Paton NMDA receptor-mediated control of protein synthesis at developing synapses Nat. Neurosci. 3 2000 211 216
61. B.M. Schmitt, K.L.M. Rudolph, P. Karagianni, N.A. Fonseca, R.J. White, I. Talianidis, D.T. Odom, J.C. Marioni, and C. Kutter High-resolution mapping of transcriptional dynamics across tissue development reveals a stable mRNA-tRNA interface Genome Res. 24 2014 1797 1807
62. R. Shalgi, J.A. Hurt, I. Krykbaeva, M. Taipale, S. Lindquist, and C.B. Burge Widespread regulation of translation by elongation pausing in heat shock Mol. Cell 49 2013 439 452
63. V. Siegel, and P. Walter Each of the activities of signal recognition particle (SRP) is contained within a distinct domain: analysis of biochemical mutants of SRP Cell 52 1988 39 49
64. G. Stefani, C.E. Fraser, J.C. Darnell, and R.B. Darnell Fragile X mental retardation protein is associated with translating polyribosomes in neuronal cells J. Neurosci. 24 2004 7272 7276
65. M.A. Sutton, A.M. Taylor, H.T. Ito, A. Pham, and E.M. Schuman Postsynaptic decoding of neural activity: eEF2 as a biochemical sensor coupling miniature synaptic transmission to local protein synthesis Neuron 55 2007 648 661
66. S. Takyar, R.P. Hickerson, and H.F. Noller mRNA helicase activity of the ribosome Cell 120 2005 49 58
67. T. Tuller, A. Carmi, K. Vestsigian, S. Navon, Y. Dorfan, J. Zaborske, T. Pan, O. Dahan, I. Furman, and Y. Pilpel An evolutionarily conserved mechanism for controlling the efficiency of protein translation Cell 141 2010 344 354
68. T. Udagawa, N.G. Farny, M. Jakovcevski, H. Kaphzan, J.M. Alarcon, S. Anilkumar, M. Ivshina, J.A. Hurt, K. Nagaoka, V.C. Nalavadi, and et al. Genetic and acute CPEB1 depletion ameliorate fragile X pathophysiology Nat. Med. 19 2013 1473 1477
69. B. Wightman, I. Ha, and G. Ruvkun Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans Cell 75 1993 855 862
70. J.M. Zaborske, V.L.B. DuMont, E.W.J. Wallace, T. Pan, C.F. Aquadro, and D.A. Drummond A nutrient-driven tRNA modification alters translational fidelity and genome-wide protein coding across an animal genus PLoS Biol. 12 2014 e1002015
71. Y. Zhang, C. Ma, Y. Yuan, J. Zhu, N. Li, C. Chen, S. Wu, L. Yu, J. Lei, and N. Gao Structural basis for interaction of a cotranslational chaperone with the eukaryotic ribosome Nat. Struct. Mol. Biol. 21 2014 1042 1046