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Research Paper

Deciphering the rules of mRNA structure differentiation in Saccharomyces cerevisiae in vivo and in vitro with deep neural networks

ORCID Icon, , ORCID Icon, , &
Pages 1044-1054 | Received 22 Sep 2018, Accepted 23 Apr 2019, Published online: 23 May 2019

References

  • Mortimer SA, Kidwell MA, Doudna JA. Insights into RNA structure and function from genome-wide studies. Nat Rev Genet. 2014 Jul;15(7):469–479. PubMed PMID: 24821474; English.
  • Mustoe AM, Busan S, Rice GM, et al. Pervasive regulatory functions of mrna structure revealed by high-resolution SHAPE probing. Cell. 2018 Mar 22;173(1):181–195 e18. PubMed PMID: 29551268; PubMed Central PMCID: PMCPMC5866243.
  • Espah Borujeni A, Cetnar D, Farasat I, et al. Precise quantification of translation inhibition by mRNA structures that overlap with the ribosomal footprint in N-terminal coding sequences. Nucleic Acids Res. 2017 May 19;45(9):5437–5448. PubMed PMID: 28158713; PubMed Central PMCID: PMCPMC5435973.
  • Rouskin S, Zubradt M, Washietl S, et al. Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo. Nature. 2014 Jan 30;505(7485):701–705. PubMed PMID: 24336214; PubMed Central PMCID: PMCPMC3966492.
  • Ding Y, Tang Y, Kwok CK, et al. In vivo genome-wide profiling of RNA secondary structure reveals novel regulatory features. Nature. 2014 Jan 30;505(7485):696–700. PubMed PMID: 24270811. English.
  • Zubradt M, Gupta P, Persad S, et al. DMS-MaPseq for genome-wide or targeted RNA structure probing in vivo. Nat Methods. 2017 Jan;14(1):75–82. PubMed PMID: 27819661.
  • Spitale RC, Flynn RA, Zhang QC, et al. Structural imprints in vivo decode RNA regulatory mechanisms. Nature. 2015 Mar 26;519(7544):486–490. PubMed PMID: 25799993; PubMed Central PMCID: PMCPMC4376618.
  • Ingolia NT, Ghaemmaghami S, Newman JR, et al. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science. 2009 Apr 10;324(5924):218–223. PubMed PMID: 19213877; PubMed Central PMCID: PMCPMC2746483.
  • Ingolia NT. Ribosome profiling: new views of translation, from single codons to genome scale. Nat Rev Genet. 2014 Mar;15(3):205–213. PubMed PMID: 24468696.
  • Sabi R, Tuller T. A comparative genomics study on the effect of individual amino acids on ribosome stalling. Bmc Genomics. 2015;16 Suppl 10:S5. PubMed PMID: 26449596; PubMed Central PMCID: PMCPMC4602185.
  • Zur H, Tuller T. Strong association between mRNA folding strength and protein abundance in S. cerevisiae. EMBO Rep. 2012 Mar 01;13(3):272–277. PubMed PMID: 22249164; PubMed Central PMCID: PMCPMC3323128. English.
  • Tuller T, Waldman YY, Kupiec M, et al. Translation efficiency is determined by both codon bias and folding energy. Proc Natl Acad Sci U S A. 2010 Feb 23;107(8):3645–3650. PubMed PMID: 20133581; PubMed Central PMCID: PMCPMC2840511. English.
  • Doan S, Conway M, Phuong TM, et al. Natural language processing in biomedicine: a unified system architecture overview. Methods Mol Biol. 2014;1168:275–294. PubMed PMID: 24870142.
  • Hinton G, Deng L, Yu D, et al. Deep neural networks for acoustic modeling in speech recognition. Ieee Signal Proc Mag. 2012 Nov;29(6):82–97. PubMed PMID: WOS:000310345000010. English.
  • Silver D, Huang A, Maddison CJ, et al. Mastering the game of go with deep neural networks and tree search. Nature. 2016 Jan 28;529(7587):484–489. PubMed PMID: WOS:000368673800028. English.
  • Ciresan DC, Giusti A, Gambardella LM, et al. Mitosis detection in breast cancer histology images with deep neural networks. Med Image Comput Comput Assist Interv. 2013;16(Pt 2):411–418. PubMed PMID: 24579167.
  • Zhang S, Hu H, Zhou J, et al. Analysis of Ribosome stalling and translation elongation dynamics by deep learning. Cell Syst. 2017 Sep 27;5(3):212–220 e6. PubMed PMID: 28957655.
  • Alipanahi B, Delong A, Weirauch MT, et al. Predicting the sequence specificities of DNA- and RNA-binding proteins by deep learning. Nat Biotechnol. 2015 Aug;33(8):831–838. PubMed PMID: 26213851.
  • Ouyang Z, Snyder MP, Chang HY. SeqFold: genome-scale reconstruction of RNA secondary structure integrating high-throughput sequencing data. Genome Res. 2013 Feb;23(2):377–387. PubMed PMID: 23064747; PubMed Central PMCID: PMCPMC3561878.
  • Pop C, Rouskin S, Ingolia NT, et al. Causal signals between codon bias, mRNA structure, and the efficiency of translation and elongation. Mol Syst Biol. 2014 Dec 23;10:770. PubMed PMID: 25538139; PubMed Central PMCID: PMCPMC4300493.
  • Lorenz R, Bernhart SH, Honer Zu Siederdissen C, et al. ViennaRNA package 2.0. Algorithms Mol Biol. 2011 Nov 24;6:26. PubMed PMID: 22115189; PubMed Central PMCID: PMCPMC3319429.
  • Zinshteyn B, Gilbert WV. Loss of a conserved tRNA anticodon modification perturbs cellular signaling. PLoS Genet. 2013;9(8):e1003675. PubMed PMID: 23935536; PubMed Central PMCID: PMCPMC3731203.
  • Lareau LF, Hite DH, Hogan GJ, et al. Distinct stages of the translation elongation cycle revealed by sequencing ribosome-protected mRNA fragments. Elife. 2014 May 09;3:e01257. PubMed PMID: 24842990; PubMed Central PMCID: PMCPMC4052883.
  • Albert FW, Muzzey D, Weissman JS, et al. Genetic influences on translation in yeast. PLoS Genet. 2014 Oct;10(10):e1004692. PubMed PMID: 25340754; PubMed Central PMCID: PMCPMC4207643.
  • Young SK, Palam LR, Wu C, et al. Ribosome elongation stall directs gene-specific translation in the integrated stress response. J Biol Chem. 2016 Mar 18;291(12):6546–6558. PubMed PMID: 26817837; PubMed Central PMCID: PMCPMC4813566.
  • Nissley DA, Sharma AK, Ahmed N, et al. Accurate prediction of cellular co-translational folding indicates proteins can switch from post- to co-translational folding. Nat Commun. 2016 Feb 18;7:10341. PubMed PMID: 26887592; PubMed Central PMCID: PMCPMC4759629.
  • Abadi M, Barham P, Chen J, et al. TensorFlow: a system for large-scale machine learning. In: Software available from tensorfloworg; Savannah, GA; 2016. p. 265–283.
  • Nair V, Hinton GE, editors. Rectified linear units improve restricted boltzmann machines. International Conference on International Conference on Machine Learning; Haifa, Israel; 2010. p. 807–814.
  • Kingma DP, Ba J. Adam: A method for stochastic optimization. Computer Sci.  San Diego, CA; 2015.
  • Ioffe S, Szegedy C Batch normalization: accelerating deep network training by reducing internal covariate shift; 2015. p.448–456.
  • Bengio Y. Practical recommendations for gradient-based training of deep architectures. In K.-R. Müller, G. Montavon, and G. B. Orr, editors, Neural Networks: Tricks of the Trade. Springer; 2012. p. 437–478. doi:10.1007/978-3-642-35289-8_26.
  • Gorochowski TE, Ignatova Z, Bovenberg RA, et al. Trade-offs between tRNA abundance and mRNA secondary structure support smoothing of translation elongation rate. Nucleic Acids Res. 2015 Mar 31;43(6):3022–3032. PubMed PMID: 25765653; PubMed Central PMCID: PMCPMC4381083.
  • Kertesz M, Wan Y, Mazor E, et al. Genome-wide measurement of RNA secondary structure in yeast. Nature. 2010 Sep 2;467(7311):103–107. PubMed PMID: 20811459; PubMed Central PMCID: PMCPMC3847670.
  • Kudla G, Murray AW, Tollervey D, et al. Coding-sequence determinants of gene expression in escherichia coli. Science. 2009 Apr 10;324(5924):255–258. PubMed PMID: WOS:000265024400047. English.
  • Tuller T, Carmi A, Vestsigian K, et al. An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell. 2010 Apr 16;141(2):344–354. PubMed PMID: 20403328.
  • Wan Y, Qu K, Ouyang Z, et al. Genome-wide measurement of RNA folding energies. Mol Cell. 2012 Oct 26;48(2):169–181. PubMed PMID: 22981864; PubMed Central PMCID: PMC3483374. English.
  • Martin KC, Ephrussi A. mRNA localization: gene expression in the spatial dimension. Cell. 2009 Feb 20;136(4):719–730. PubMed PMID: WOS:000263688200021. English.
  • Gandin V, Miluzio A, Barbieri AM, et al. Eukaryotic initiation factor 6 is rate-limiting in translation, growth and transformation. Nature. 2008 Oct 2;455(7213):684–688. PubMed PMID: 18784653; PubMed Central PMCID: PMCPMC2753212.
  • Mao Y, Liu H, Liu Y, et al. Deciphering the rules by which dynamics of mRNA secondary structure affect translation efficiency in Saccharomyces cerevisiae. Nucleic Acids Res. 2014 Apr;42(8):4813–4822. PubMed PMID: 24561808; PubMed Central PMCID: PMCPMC4005662.
  • Boel G, Letso R, Neely H, et al. Codon influence on protein expression in E. coli correlates with mRNA levels. Nature. 2016 Jan 21;529(7586):358–363. PubMed PMID: 26760206; PubMed Central PMCID: PMCPMC5054687.
  • Mao Y, Li Q, Wang W, et al. Number variation of high stability regions is correlated with gene functions. Genome Biol Evol. 2013;5(3):484–493. PubMed PMID: 23407773; PubMed Central PMCID: PMCPMC3622296.
  • Mao Y, Li Q, Zhang Y, et al. Genome-wide analysis of selective constraints on high stability regions of mRNA reveals multiple compensatory mutations in escherichia coli. Plos One. 2013 Sep 27;8(9):e73299. PubMed PMID: 24086278; PubMed Central PMCID: PMC3785496. English.
  • Zhang J, Kuo CCJ, Chen LA. GC content around splice sites affects splicing through pre-mRNA secondary structures. Bmc Genomics. 2011 Jan 31;12. PubMed PMID: WOS:000287481000001. English. DOI:10.1186/1471-2164-12-90
  • Supek F. The code of silence: widespread associations between synonymous codon biases and gene function. J Mol Evol. 2016 Jan;82(1):65–73. PubMed PMID: 26538122.
  • Ingolia NT, Brar GA, Rouskin S, et al. The ribosome profiling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments. Nat Protoc. 2012 Jul 26;7(8):1534–1550. PubMed PMID: 22836135; PubMed Central PMCID: PMCPMC3535016. English.
  • Ingolia NT, Lareau LF, Weissman JS. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell. 2011 Nov 11;147(4):789–802. PubMed PMID: 22056041; PubMed Central PMCID: PMCPMC3225288.
  • Li GW, Burkhardt D, Gross C, et al. Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell. 2014 Apr 24;157(3):624–635. PubMed PMID: 24766808; PubMed Central PMCID: PMCPMC4006352.
  • Reuter JS, Mathews DH. RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinformatics. 2010 Mar 15;11:129. PubMed PMID: 20230624; PubMed Central PMCID: PMCPMC2984261.
  • Murtagh F, Legendre P. Ward‘s Hierarchical agglomerative clustering method: which algorithms implement ward‘s criterion? J Classif. 2014 Oct;31(3):274–295. PubMed PMID: WOS:000345142200002. English.