RiboAbacus: A model trained on polyribosome images predicts ribosome density and translational efficiency from mammalian transcriptomes

Nucleic Acids Research

Volumn 43, Issue 22, 2015, Pages

  Lauria, Fabio ^a   Tebaldi, Toma ^b   Lunelli, Lorenzo ^c   Struffi, Paolo ^b   Gatto, Pamela ^b   Pugliese, Andrea ^d   Brigotti, Maurizio ^e   Montanaro, Lorenzo ^e   Ciribilli, Yari ^b   Inga, Alberto ^b   Quattrone, Alessandro ^b   Sanguinetti, Guido ^f   Viero, Gabriella ^a  

^a CNR   (Italy)

^b Centre for Integrative Biology CIBIO   (Italy)

^c FONDAZIONE BRUNO KESSLER   (Italy)

^d UNIVERSITY OF TRENTO   (Italy)

^e UNIVERSITY OF BOLOGNA   (Italy)

^f UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEOME; TRANSCRIPTOME;

ANIMAL CELL; ARTICLE; ATOMIC FORCE MICROSCOPY; CODON USAGE; GENETIC TRANSCRIPTION; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMAGE ANALYSIS; MATHEMATICAL MODEL; MEASUREMENT ACCURACY; NONHUMAN; POLYSOME; PREDICTION; PRIORITY JOURNAL; RABBIT; RETICULOCYTE; RNA TRANSLATION; VALIDATION STUDY; ANIMAL; BIOLOGICAL MODEL; COMPUTER PROGRAM; MCF 7 CELL LINE; PROTEIN SYNTHESIS; PROTEOMICS; RIBOSOME; ULTRASTRUCTURE;

ANIMALS; HEK293 CELLS; HUMANS; MCF-7 CELLS; MICROSCOPY, ATOMIC FORCE; MODELS, BIOLOGICAL; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; PROTEOMICS; RABBITS; RETICULOCYTES; RIBOSOMES; SOFTWARE; TRANSCRIPTOME;

EID: 84964621650     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv781     Document Type: Article

References (74)

1. Sonenberg, N. and Hinnebusch, A.G. (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell, 136, 731-745.
2. Aitken, C.E. and Lorsch, J.R. (2012) A mechanistic overview of translation initiation in eukaryotes. Nat. Struct. Mol. Biol., 19, 568-576.
3. Jackson, R.J., Hellen, C.U. and Pestova, T.V. (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol., 324, 113-127.
4. Ingolia, N.T., Lareau, L.F. and Weissman, J.S. (2011) Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell, 147, 789-802.
5. Stadler, M. and Fire, A. (2011) Wobble base-pairing slows in vivo translation elongation in metazoans. RNA, 17, 2063-2073.
6. Li, G.-W., Oh, E. and Weissman, J.S. (2012) The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature, 484, 538-541.
7. Nürenberg, E. and Tampé, R. (2013) Tying up loose ends: ribosome recycling in eukaryotes and archaea. Trends Biochem. Sci., 38, 64-74.
8. des Georges, A., Hashem, Y., Unbehaun, A., Grassucci, R.A., Taylor, D., Hellen, C.U., Pestova, T.V. and Frank, J. (2014) Structure of the mammalian ribosomal pre-termination complex associated with eRF1·eRF3·GDPNP. Nucleic Acids Res., 42, 3409-3418.
9. Novoa, E.M. and Ribas de Pouplana, L. (2012) Speeding with control: codon usage, tRNAs, and ribosomes. Trends Genet., 28, 574-581.
10. Lynn, D.J., Singer, G.A. and Hickey, D.A. (2002) Synonymous codon usage is subject to selection in thermophilic bacteria. Nucleic Acids Res., 30, 4272-4277.
11. Gray, N.K. and Hentze, M.W. (1994) Regulation of protein synthesis by mRNA structure. Mol. Biol. Rep., 19, 195-200.
12. Kudla, G., Murray, A.W., Tollervey, D. and Plotkin, J.B. (2009) Coding-sequence determinants of gene expression in Escherichia coli. Science, 324, 255-258.
13. Pircher, A., Bakowska-Zywicka, K., Schneider, L., Zywicki, M. and Polacek, N. (2014) An mRNA-derived noncoding RNA targets and regulates the ribosome. Mol. Cell, 54, 147-155.
14. Shalgi, R., Hurt, J.A., Krykbaeva, I., Taipale, M., Lindquist, S. and Burge, C.B. (2013) Widespread regulation of translation by elongation pausing in heat shock. Mol. Cell, 49, 439-452.
15. Friend, K., Campbell, Z.T., Cooke, A., Kroll-Conner, P., Wickens, M.P. and Kimble, J. (2012) A conserved PUF-Ago-eEF1A complex attenuates translation elongation. Nat. Struct. Mol. Biol., 19, 176-183.
16. Wolin, S.L. and Walter, P. (1988) Ribosome pausing and stacking during translation of a eukaryotic mRNA. EMBO J., 7, 3559-3569.
17. Ingolia, N.T., Brar, G.A., Rouskin, S., McGeachy, A.M. and Weissman, J.S. (2012) The ribosome profiling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments. Nat. Protoc., 7, 1534-1550.
18. Shah, P., Ding, Y., Niemczyk, M., Kudla, G. and Plotkin, J.B. (2013) Rate-limiting steps in yeast protein translation. Cell, 153, 1589-1601.
19. Noller, H.F. (2012) Evolution of protein synthesis from an RNA World. Cold Spring Harb. Perspect. Biol., 4, a003681.
20. Herr, A.J., Wills, N.M., Nelson, C.C., Gesteland, R.F. and Atkins, J.F. (2001) Drop-off during ribosome hopping. J. Mol. Biol., 311, 445-452.
21. Cruz-Vera, L.R, Magos-Castro, M.A., Zamora-Romo, E. and Guarneros, G. (2004) Ribosome stalling and peptidyl-tRNA drop-off during translational delay at AGA codons. Nucleic Acids Res., 32, 4462-4468.
22. Warner, J.R., Rich, A. and Hall, C.E. (1962) Electron microscope studies of ribosomal clusters synthesizing hemoglobin. Science, 138, 1399-1403.
23. Palade, G.E. (1955) A small particulate component of the cytoplasm. J. Biophys. Biochem. Cytol., 1, 59-68.
24. Wettstein, F.O., Staehelin, T. and Noll, H. (1963) Ribosomal aggregate engaged in protein synthesis: characterization of the ergosome. Nature, 197, 430-435.
25. Gerst, I. and Levine, S.N. (1965) Kinetics of protein synthesis by polyribosomes. J. Theor. Biol., 9, 16-36.
26. MacDonald, C.T. and Gibbs, J.H. (1969) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Biopolymers, 7, 707-725.
27. Gilchrist, M.A. and Wagner, A. (2006) A model of protein translation including codon bias, nonsense errors, and ribosome recycling. J. Theor. Biol., 239, 417-434.
28. Mitarai, N., Sneppen, K. and Pedersen, S. (2008) Ribosome collisions and translation efficiency: optimization by codon usage and mRNA destabilization. J. Theor. Biol., 382, 236-245.
29. Zouridis, H. and Hatzimanikatis, V. (2007) A model for protein translation: polysome self-organization leads to maximum protein synthesis rates. Biophys. J., 92, 717-730.
30. Reuveni, S., Meilijson, I., Kupiec, M., Ruppin, E. and Tuller, T. (2011) Genome-scale analysis of translation elongation with a ribosome flow model. PLoS Comput. Biol., 7, e1002127.
31. Dana, A. and Tuller, T. (2012) Determinants of translation elongation speed and ribosomal profiling biases in mouse embryonic stem cells. PLoS Comput. Biol., 8, e1002755.
32. Ciandrini, L., Stansfield, I. and Romano, M.C. (2013) Ribosome traffic on mRNAs maps to gene ontology: genome-wide quantification of translation initiation rates and polysome size regulation. PLoS Comput. Biol., 9, e1002866.
33. Von der Haar, T. (2012) Mathematical and Computational Modelling of Ribosomal Movement and Protein Synthesis: an overview. Comput. Struct. Biotechnol. J., 1, e20120400.
34. Ingolia, N.T., Ghaemmaghami, S., Newman, J.R. and Weissman, J.S. (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science, 324, 218-223.
35. Tuller, T., Veksler-Lublinsky, I., Gazit, N., Kupiec, M., Ruppin, E. and Ziv-Ukelson, M. (2011) Composite effects of gene determinants on the translation speed and density of ribosomes. Genome Biol., 12, R110.
36. Zupanic, A., Meplan, C., Grellscheid, S.N., Mathers, J.C., Kirkwood, T.B., Hesketh, J.E. and Shanley, D.P. (2014) Detecting translational regulation by change point analysis of ribosome profiling data sets. RNA, 20, 1507-1518.
37. Bohnert, R. and Rätsch, G. (2010) rQuant. web: a tool for RNA-Seq-based transcript quantitation. Nucleic Acids Res., 38, W348-W351.
38. Hansen, K.D., Brenner, S.E. and Dudoit, S. (2010) Biases in Illumina transcriptome sequencing caused by random hexamer priming. Nucleic Acids Res., 38, e131.
39. Roberts, A., Trapnell, C., Donaghey, J., Rinn, J.L. and Pachter, L. (2010) Improving RNA-Seq expression estimates by correcting for fragment bias. Genome Biol., 12, R22.
40. Arava, Y., Wang, Y., Storey, J.D., Liu, C.L., Brown, P.O. and Herschlag, D. (2003) Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A., 100, 3889-3894.
41. MacKay, V.L., Li, X., Flory, M.R., Turcott, E., Law, G.L., Serikawa, K.A., Xu, X.L., Hookeun, L., Goodlett, D.R., Aebersold, R. et al. (2004) Gene expression analyzed by high-resolution state array analysis and quantitative proteomics response of yeast to mating pheromone. Mol. Cell. Proteomics, 3, 478-489.
42. Darnell, J.C., Van Driesche, S.J., Zhang, C., Hung, K. Y.S, 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.
43. Qin, X., Ahn, S., Speed, T.P. and Rubin, G.M. (2007) Global analyses of mRNA translational control during early Drosophila embryogenesis. Genome Biol., 8, R63.
44. Viero, G., Lunelli, L., Passerini, A., Bianchini, P., Gilbert, R.J., Bernabò, P., Tebaldi, T., Diaspro, A., Pederzolli, C. and Quattrone, A. (2015) Three distinct ribosome assemblies modulated by translation are the building blocks of polysomes. J. Cell. Biol., 208, 581-596.
45. Brandt, F., Etchells, S.A., Ortiz, J.O., Elcock, A.H., Hartl, F.U. and Baumeister, W. (2009) The native 3D organization of bacterial polysomes. Cell, 136, 261-271.
46. Brandt, F., Carlson, L.-A., Hartl, F., Baumeister, W. and Grünewald, K. (2010) The three-dimensional organization of polyribosomes in intact human cells. Mol. Cell, 39, 560-569.
47. Afonina, Z.A., Myasnikov, A.G., Shirokov, V.A., Klaholz, B.P. and Spirin, A.S. (2014) Formation of circular polyribosomes on eukaryotic mRNA without cap-structure and poly (A)-tail: a cryo electron tomography study. Nucleic Acids Res., 42, 9461-9469.
48. Myasnikov, A.G., Afonina, Z.A., Ménétret, J.-F., Shirokov, V.A., Spirin, A.S. and Klaholz, B.P. (2014) The molecular structure of the left-handed supra-molecular helix of eukaryotic polyribosomes. Nat. Commun., 5, doi: 10.1038/ncomms6294.
49. Tuller, T. and Zur, H. (2015) Multiple roles of the coding sequence 5' end in gene expression regulation. Nucleic Acids Res., 43, 13-28.
50. Bentele, K., Saffert, P., Rauscher, R., Ignatova, Z. and Blüthgen, N. (2013) Efficient translation initiation dictates codon usage at gene start. Mol. Syst. Biol., 9, doi: 10.1038/msb.2013.32.
51. Li, Q. and Qu, H.-Q. (2013) Human coding synonymous single nucleotide polymorphisms at ramp regions of mRNA translation. PloS One, 8, e59706.
52. Tuller, T., Carmi, A., Vestsigian, K., Navon, S., Dorfan, Y., Zaborske, J., Pan, T., Dahan, O., Furman, I. and Pilpel, Y. (2010) An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell, 141, 344-354.
53. Vogel, C., Abreu Rde, S., Ko, D., Le, S.Y., Shapiro, B.A., Burns, S.C., Sandhu, D., Boutz, D.R., Marcotte, E.M. and Penalva, L.O. (2010) Sequence signatures and mRNA concentration can explain two-thirds of protein abundance variation in a human cell line. Mol. Syst. Biol., 6, doi: 10.1038/msb.2010.59.
54. Hornburg, D., Drepper, C., Butter, F., Meissner, F., Sendtner, M. and Mann, M. (2014) Deep proteomic evaluation of primary and cell line motoneuron disease models delineates major differences in neuronal characteristics. Mol. Cell Proteomics, 13, 3410-3420.
55. Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W. and Selbach, M. (2011) Global quantification of mammalian gene expression control. Nature, 473, 337-342.
56. Jackson, R.J. and Hunt, T. (1983) Preparation and use of nuclease-treated rabbit reticulocyte lysates for the translation of eukaryotic messenger RNA. Methods Enzymol., 96, 50-74.
57. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res., 29, e45.
58. Schneider, C.A., Rasband, W.S. and Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat. Methods, 9, 671-675.
59. Williams, E.J. (1959) Regression Analysis. Wiley, NY.
60. Steiger, J.H. (1980) Tests for comparing elements of a correlation matrix. Psychol. Bull., 87, 245-251.
61. Arava, Y., Boas, F.E., Brown, P.O. and Herschlag, D. (2005) Dissecting eukaryotic translation and its control by ribosome density mapping. Nucleic Acids Res., 33, 2421-2432.
62. Gilchrist, M.A. (2007) Combining models of protein translation and population genetics to predict protein production rates from codon usage patterns. Mol. Biol. Evol., 24, 2362-2372.
63. Warner, J.R. (1999) The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci., 24, 437-440.
64. Frank, J. and Gonzalez, R.L. Jr (2010) Structure and dynamics of a processive Brownian motor: the translating ribosome. Annu. Rev. Biochem., 79, 381-412.
65. Wohlgemuth, I., Pohl, C. and Rodnina, M.V. (2010) Optimization of speed and accuracy of decoding in translation. EMBO J., 29, 3701-3709.
66. Zouridis, H. and Hatzimanikatis, V. (2008) Effects of codon distributions and tRNA competition on protein translation. Biophys. J., 95, 1018-1033.
67. Bilgin, N., Claesens, F., Pahverk, H. and Ehrenberg, M. (1992) Kinetic properties of Escherichia coli ribosomes with altered forms of S12. J. Mol. Biol., 224, 1011-1027.
68. Rodnina, M.V., Pape, T., Fricke, R., Kuhn, L. and Wintermeyer, W. (1996) Initial binding of the elongation factor Tu· GTP· aminoacyl-tRNA complex preceding codon recognition on the ribosome. J. Biol. Chem., 271, 646-652.
69. Pape, T., Wintermeyer, W. and Rodnina, M.V. (1998) Complete kinetic mechanism of elongation factor Tu-dependent binding of aminoacyl-tRNA to the A site of the E. coli ribosome. EMBO J., 17, 7490-7497.
70. Savelsbergh, A., Katunin, V.I., Mohr, D., Peske, F., Rodnina, M.V. and Wintermeyer, W. (2003) An elongation factor G-induced ribosome rearrangement precedes tRNA-mRNA translocation. Mol. Cell, 11, 1517-1523.
71. Soto Rifo, R., Ricci, E.P., Decimo, D., Moncorge, O. and Ohlmann, T. (2007) Back to basics: the untreated rabbit reticulocyte lysate as a competitive system to recapitulate cap/poly(A) synergy and the selective advantage of IRES-driven translation. Nucleic Acids Res., 35, e121.
72. Ghazalpour, A., Bennet, B., Petyuk, V.A., Orozco, L., Hagopian, R., Mungrue, I.N., Farber, C.R., Sinsheimer, J., Kang, H.M., Furlotte, N. et al. (2011) Comparative analysis of proteome and transcriptome variation in Mouse. PLoS Genet., 7, e1001393.
73. Tuller, T., Kupiec, M. and Ruppin, E. (2007) Determinants of protein abundance and translation efficiency in S. cerevisiae. PLoS Comput. Biol., 3, e248.
74. Gunawardana, Y. and Niranjan, M. (2013) Bridging the gap between transcriptome and proteome measurements identifies post-translationally regulated genes. Bioinformatics, 29, 3060-3066.