1,540
Views
35
CrossRef citations to date
0
Altmetric
Research Paper

Rationally designed, heterologous S. cerevisiae transcripts expose novel expression determinants

, , , , , , , , , & show all
Pages 972-984 | Received 04 May 2015, Accepted 07 Jul 2015, Published online: 18 Sep 2015

References

  • Lithwick G, Margalit H. Hierarchy of sequence-dependent features associated with prokaryotic translation. Genome Res (2003) 13:2665-73; PMID:14656971; http://dx.doi.org/10.1101/gr.1485203
  • Zur H, Tuller T. Transcript features enable accurate prediction and understanding of gene expression in S. cerevisiae. BMC Bioinfomatics. (2013) 14:S1; http://dx.doi.org/10.1186/1471-2105-14-S15-S1
  • Tuller T, Kupiec M, Ruppin E. Determinants of protein abundance and translation efficiency in S. cerevisiae. PLoS Comput Biol (2007) 3:2510-19; http://dx.doi.org/10.1371/journal.pcbi.0030248
  • Vogel C. Abreu Rde S, Ko D, Le SY, Shapiro BA, Burns SC, Sandhu D, Boutz DR, Marcotte EM, Penalva LO. Sequence signatures and mRNA concentration can explain two-thirds of protein abundance variation in a human cell line. Mol Syst Biol (2010) 6:1-9; http://dx.doi.org/10.1038/msb.2010.59
  • Huang T, Wan S, Xu Z, Zheng Y, Feng KY, Li HP, Kong X, Cai YD. Analysis and prediction of translation rate based on sequence and functional features of the mRNA. PLoS One (2011) 6:e16036; PMID:21253596; http://dx.doi.org/10.1371/journal.pone.0016036
  • Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O'Shea EK, Weissman JS. Global analysis of protein expression in yeast. Nature (2003) 425:737-41; PMID:14562106; http://dx.doi.org/10.1038/nature02046
  • Gygi SP, Rochon Y, Franza BR, Aebersold R. Correlation between protein and mRNA abundance in yeast. Mol Cell Biol (1999) 19:1720-30; PMID:10022859
  • Schwanhausser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M. Global quantification of mammalian gene expression control. Nature (2011) 473:337-42; PMID:21593866; http://dx.doi.org/10.1038/nature10098
  • Lu P, Vogel C, Wang R, Yao X, Marcotte EM. Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat Biotechnol (2007) 25:117-24; PMID:17187058; http://dx.doi.org/10.1038/nbt1270
  • Wang M, Weiss M, Simonovic M, Haertinger G, Schrimpf SP, Hengartner MO, von Mering C. PaxDb, a Database of Protein Abundance Averages Across All Three Domains of Life. Mol Cell Proteomics (2012) 11:492-500; http://dx.doi.org/10.1074/mcp.O111.014704
  • Kudla G, Murray AW, Tollervey D, Plotkin JB. Coding-sequence determinants of gene expression in Escherichia coli. Science (2009) 324:255-8; PMID:19359587; http://dx.doi.org/10.1126/science.1170160
  • Welch M, Govindarajan S, Ness JE, Villalobos A, Gurney A, Minshull J, Gustafsson C. Design parameters to control synthetic gene expression in Escherichia coli. PLoS One (2009) 4:1-10; http://dx.doi.org/10.1371/journal.pone.0007002
  • Goodman DB, Church GM, Kosuri S. Causes and effects of N-terminal codon bias in bacterial genes. Science. (2013) 342:475-9; http://dx.doi.org/10.1126/science.1241934
  • Allert M, Cox JC, Hellinga HW. Multifactorial determinants of protein expression in prokaryotic open reading frames. J Mol Biol (2010) 402:905-918; http://dx.doi.org/10.1016/j.jmb.2010.08.010
  • Bentele K, Saffert P, Rauscher R, Ignatova Z, Bluthgen N. Efficient translation initiation dictates codon usage at gene start. Mol Syst Biol (2013) 9:675., 10.1038/msb.2013.1032.; PMID:23774758; http://dx.doi.org/10.1038/msb.2013.32
  • Tuller T, Zur H. Multiple Roles of the Coding Sequence 5′ End in Gene Expression Regulation. Nucleic Acids Res (2015) 43:13-28; PMID:25505165; http://dx.doi.org/10.1093/nar/gku1313
  • Supek F, Smuc T. On relevance of codon usage to expression of synthetic and natural genes in Escherichia coli. Genetics (2010) 185:1129-34; PMID:20421604; http://dx.doi.org/10.1534/genetics.110.115477
  • Ingolia NT, Lareau LF, Weissman JS. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell (2011) 147:789-802; PMID:22056041; http://dx.doi.org/10.1016/j.cell.2011.10.002
  • Qian W, Yang J-R, Pearson NM, Maclean C, Zhang J. Balanced codon usage optimizes eukaryotic translational efficiency. PLoS genetics (2012) 8:e1002603; PMID:22479199; http://dx.doi.org/10.1371/journal.pgen.1002603
  • Dana A, Tuller T. The effect of tRNA levels on decoding times of mRNA codons. Nucleic Acids Res. (2014) 42:9171-81; PMID:25056313
  • Chu D, Kazana E, Bellanger N, Singh T, Tuite MF, von der Haar T. Translation elongation can control translation initiation on eukaryotic mRNAs. EMBO J. (2014) 33:21-34. Epub 201382013 Dec 201385619; PMID:24357599; http://dx.doi.org/10.1002/embj.201385651
  • Gardin J, Yeasmin R, Yurovsky A, Cai Y, Skiena S, Futcher B. Measurement of average decoding rates of the 61 sense codons in vivo. Elife. (2014); 3 10.7554/eLife.03735.; PMID:25347064; http://dx.doi.org/10.7554/eLife.03735
  • Tuller T, Waldman YY, Kupiec M, Ruppin E. Translation efficiency is determined by both codon bias and folding energy. Proc Natl Acad Sci U S A (2010) 107:3645-50; PMID:20133581; http://dx.doi.org/10.1073/pnas.0909910107
  • Plotkin JB, Kudla G. Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet (2010) 12:32-42; PMID:21102527; http://dx.doi.org/10.1038/nrg2899
  • Chamary JV, Parmley JL, Hurst LD. Hearing silence: non-neutral evolution at synonymous sites in mammals. Nat Rev Genet (2006) 7:98-108; PMID:16418745; http://dx.doi.org/10.1038/nrg1770
  • Sauna ZE, Kimchi-Sarfaty C. Understanding the contribution of synonymous mutations to human disease. Nat Rev Genet (2013) 12:683-91; http://dx.doi.org/10.1038/nrg3051
  • Hershberg R, Petrov DA. Selection on codon bias. Annu Rev Genet (2008) 42:287-99; PMID:18983258; http://dx.doi.org/10.1146/annurev.genet.42.110807.091442
  • Gingold H, Pilpel Y. Determinants of translation efficiency and accuracy. Mol Syst Biol. (2011) 7:481., 10.1038/msb.2011.1014.; PMID:21487400; http://dx.doi.org/10.1038/msb.2011.14
  • Novoa EM, Ribas de Pouplana L. Speeding with control: codon usage, tRNAs, and ribosomes. Trends Genet. (2012) 28:574-81; http://dx.doi.org/10.1016/j.tig.2012.07.006
  • Kozak M. Point mutations close to the AUG initiator codon affect the efficiency of translation of rat preproinsulin in vivo. Nature (1984) 308:241-6; PMID:6700727; http://dx.doi.org/10.1038/308241a0
  • Kozak M. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell (1986) 44:283-92; PMID:3943125; http://dx.doi.org/10.1016/0092-8674(86)90762-2
  • Gu W, Zhou T, Wilke CO. A universal trend of reduced mRNA stability near the translation-initiation site in prokaryotes and eukaryotes. PLoS Comput Biol. 2010 6:1-8 (2010); http://dx.doi.org/10.1371/journal.pcbi.1000664
  • Hamilton R, Watanabe CK, de Boer HA. Compilation and comparison of the sequence context around the AUG startcodons in Saccharomyces cerevisiae mRNAs. Nucleic Acids Res. (1987) 15:3581-93.; PMID:3554144
  • Zur H, Tuller T. New Universal Rules of Eukaryotic Translation Initiation Fidelity. PLoS Comput Biol (2013) 9:e1003136; PMID:23874179; http://dx.doi.org/10.1371/journal.pcbi.1003136
  • Li X, Quon G, Lipshitz HD, Morris Q. Predicting in vivo binding sites of RNA-binding proteins using mRNA secondary structure. RNA. (2010) 16:1096-107. Epub 2012010 Apr 2017223.; PMID:20418358
  • Ingolia NT. Ribosome profiling: new views of translation, from single codons to genome scale. Nat Rev Genet. (2014) 15:205-13; PMID:24468696; http://dx.doi.org/10.1038/nrg3645
  • Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science (2009) 324:218-23; PMID:19213877; http://dx.doi.org/10.1126/science.1168978
  • dos Reis M, Savva R, Wernisch L. Solving the riddle of codon usage preferences: a test for translational selection. Nucleic Acids Res (2004) 32:5036-44; PMID:15448185; http://dx.doi.org/10.1093/nar/gkh834
  • Dana A, Tuller T. Properties and Determinants of Codon Translation Speed Distributions. BMC Genomics (2014); 15 Suppl 6:S13; PMID:25572668
  • Tuller T, Veksler-Lublinsky I, Gazit N, Kupiec M, Ruppin E, Ziv-Ukelson M. Composite effects of gene determinants on the translation speed and density of ribosomes Genome Biol (2011) 12:R110; PMID:22050731
  • Kozak M. Regulation of translation via mRNA structure in prokaryotes and eukaryotes. Gene (2005) 361:13-37; PMID:16213112; http://dx.doi.org/10.1016/j.gene.2005.06.037
  • Kozak M. Downstream secondary structure facilitates recognition of initiator codons by eukaryotic ribosomes. Proc Natl Acad Sci (1990) 87:8301-05; http://dx.doi.org/10.1073/pnas.87.21.8301
  • Kochetov AV, Palyanov A, Titov II, Grigorovich D, Sarai A, Kolchanov NA. AUG_hairpin: prediction of a downstream secondary structure influencing the recognition of a translation start site. BMC Bioinformatics. (2007) 8:318.; PMID:17760957; http://dx.doi.org/10.1186/1471-2105-8-318
  • Robbins-Pianka A, Rice MD, Weir MP. The mRNA landscape at yeast translation initiation sites. Bioinformatics. (2010) 26:2651-2655; PMID:20861026; http://dx.doi.org/10.1093/bioinformatics/btq509
  • Eyre-Walker A, Bulmer M. Reduced synonymous substitution rate at the start of enterobacterial genes. Nucl. Acids Res. (1993) 21:4599-603; http://dx.doi.org/10.1093/nar/21.19.4599
  • Nakagawa S, Niimura Y, Gojobori T, Tanaka H, Miura K. Diversity of preferred nucleotide sequences around the translation initiation codon in eukaryote genomes. Nucleic Acids Res (2008) 36:861-71; http://dx.doi.org/10.1093/nar/gkm1102
  • Man O, Pilpel Y. Differential translation efficiency of orthologous genes is involved in phenotypic divergence of yeast species. Nat Genet (2007) 39:415-21; PMID:17277776; http://dx.doi.org/10.1038/ng1967
  • Drummond DA, Wilke CO. The evolutionary consequences of erroneous protein synthesis. Nat Rev Genet (2009) 10:715-724; PMID:19763154; http://dx.doi.org/10.1038/nrg2662
  • Frith MC, Forrest AR, Nourbakhsh E, Pang KC, Kai C, Kawai J, Carninci P, Hayashizaki Y, Bailey TL, Grimmond SM. The abundance of short proteins in the mammalian proteome. PLoS Genet. (2006) 2:e52. Epub 2006 Apr 2028.; PMID:16683031; http://dx.doi.org/10.1371/journal.pgen.0020052
  • Charneski CA, Hurst LD. Positively charged residues are the major determinants of ribosomal velocity. PLoS Biol (2013) 11:e1001508; PMID:23554576; http://dx.doi.org/10.1371/journal.pbio.1001508
  • Jacques N, Dreyfus M. Translation initiation in Escherichia coli: old and new questions. Mol Microbiol (1990) 4:1063-7; PMID:1700254; http://dx.doi.org/10.1111/j.1365-2958.1990.tb00679.x
  • Poker G, Margaliot M, Tuller T. Sensitivity of mRNA Translation. in review (2014).
  • Shields DC, Sharp PM, Higgins DG, Wright F. “Silent” sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol Biol Evol. (1988) 5:704-16.; PMID:3146682
  • Linshiz G, Yehezkel TB, Kaplan S, Gronau I, Ravid S, Adar R, Shapiro E. Recursive construction of perfect DNA molecules from imperfect oligonucleotides. Mol Syst Biol (2008) 4:191; PMID:18463615; http://dx.doi.org/10.1038/msb.2008.26
  • Shabi U, Kaplan S, Linshiz G, Benyehezkel T, Buaron H, Mazor Y, Shapiro E. Processing DNA molecules as text. Syst Synth Biol (2010) 4:227-36; PMID:21189843; http://dx.doi.org/10.1007/s11693-010-9059-y
  • Gietz RD, Woods RA. Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol (2002) 350:87-96.; PMID:12073338; http://dx.doi.org/10.1016/S0076-6879(02)50957-5
  • Ingolia NT, Ghaemmaghami S, Newman JRS, Weissman JS. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science (2009) 324:218; PMID:19213877; http://dx.doi.org/10.1126/science.1168978
  • Damelin SB, Miller Jr W. The mathematics of signal processing. (Cambridge University Press, 2011).
  • Grushka E. Characterization of exponentially modified Gaussian peaks in chromatography. Anal Chem (1972) 44:1733-38; PMID:22324584; http://dx.doi.org/10.1021/ac60319a011
  • Lorenz R, Bernhart SH, Höner Zu Siederdissen C, Tafer H, Flamm C, Stadler PF, Hofacker IL. ViennaRNA Package 2.0. Algorithms Mol Biol. (2011) 6:26; PMID:22115189; http://dx.doi.org/10.1186/1748-7188-6-26
  • Zur H, Tuller, T. Strong association between mRNA folding strength and protein abundance in S. cerevisiae. EMBO Rep. (2012); 13(3):272-7; PMID:22249164
  • Newman JR, Ghaemmaghami S, Ihmels J, Breslow DK, Noble M, DeRisi JL, Weissman JS. Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature (2006) 441:840-6; PMID:16699522; http://dx.doi.org/10.1038/nature04785
  • Lee MV, Topper SE, Hubler SL, Hose J, Wenger CD, Coon JJ, Gasch AP. A dynamic model of proteome changes reveals new roles for transcript alteration in yeast. Mol Syst Biol (2011) 7:514; PMID:21772262; http://dx.doi.org/10.1038/msb.2011.48
  • Benjamini Y, Hochberg Y. Controlling the False Discovery Rate - a Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B-Methodological (1995) 57:289-300
  • Storey JD. A direct approach to false discovery rates. J. R. Stat. Soc. (2002) 64:479-98; http://dx.doi.org/10.1111/1467-9868.00346
  • Sabi RTT. Modeling the efficiency of codon-tRNA interactions based on codon usage bias. DNA Res (2014); 21(5):511-26; PMID:24906480

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.