{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,31]],"date-time":"2026-03-31T14:39:16Z","timestamp":1774967956442,"version":"3.50.1"},"reference-count":56,"publisher":"Springer Science and Business Media LLC","issue":"1","content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Syst Biol"],"published-print":{"date-parts":[[2010,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n          <jats:sec>\n            <jats:title>Background<\/jats:title>\n            <jats:p>Within the emerging field of synthetic biology, engineering paradigms have recently been used to design biological systems with novel functionalities. One of the essential challenges hampering the construction of such systems is the need to precisely optimize protein expression levels for robust operation. However, it is difficult to design mRNA sequences for expression at targeted protein levels, since even a few nucleotide modifications around the start codon may alter translational efficiency and dramatically (up to 250-fold) change protein expression. Previous studies have used <jats:italic>ad hoc<\/jats:italic> approaches (e.g., random mutagenesis) to obtain the desired translational efficiencies for mRNA sequences. Hence, the development of a mathematical methodology capable of estimating translational efficiency would greatly facilitate the future design of mRNA sequences aimed at yielding desired protein expression levels.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Results<\/jats:title>\n            <jats:p>We herein propose a mathematical model that focuses on translation initiation, which is the rate-limiting step in translation. The model uses mRNA-folding dynamics and ribosome-binding dynamics to estimate translational efficiencies solely from mRNA sequence information. We confirmed the feasibility of our model using previously reported expression data on the MS2 coat protein. For further confirmation, we used our model to design 22 <jats:italic>luxR<\/jats:italic> mRNA sequences predicted to have diverse translation efficiencies ranging from 10<jats:sup>-5<\/jats:sup> to 1. The expression levels of these sequences were measured in <jats:italic>Escherichia coli<\/jats:italic> and found to be highly correlated (<jats:italic>R<\/jats:italic>\n              <jats:sup>\n                <jats:italic>2<\/jats:italic>\n              <\/jats:sup>= 0.87) with their estimated translational efficiencies. Moreover, we used our computational method to successfully transform a low-expressing DsRed2 mRNA sequence into a high-expressing mRNA sequence by maximizing its translational efficiency through the modification of only eight nucleotides upstream of the start codon.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Conclusions<\/jats:title>\n            <jats:p>We herein describe a mathematical model that uses mRNA sequence information to estimate translational efficiency. This model could be used to design best-fit mRNA sequences having a desired protein expression level, thereby facilitating protein over-production in biotechnology or the protein expression-level optimization necessary for the construction of robust networks in synthetic biology.<\/jats:p>\n          <\/jats:sec>","DOI":"10.1186\/1752-0509-4-71","type":"journal-article","created":{"date-parts":[[2010,5,26]],"date-time":"2010-05-26T18:15:01Z","timestamp":1274897701000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":81,"title":["Mathematical modeling of translation initiation for the estimation of its efficiency to computationally design mRNA sequences with desired expression levels in prokaryotes"],"prefix":"10.1186","volume":"4","author":[{"given":"Dokyun","family":"Na","sequence":"first","affiliation":[]},{"given":"Sunjae","family":"Lee","sequence":"additional","affiliation":[]},{"given":"Doheon","family":"Lee","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2010,5,26]]},"reference":[{"issue":"10","key":"460_CR1","doi-asserted-by":"publisher","first-page":"1211","DOI":"10.1038\/nbt1004-1211","volume":"22","author":"R Brent","year":"2004","unstructured":"Brent R: A partnership between biology and engineering. Nat Biotech. 2004, 22 (10): 1211-1214. 10.1038\/nbt1004-1211.","journal-title":"Nat Biotech"},{"issue":"7009","key":"460_CR2","doi-asserted-by":"publisher","first-page":"624","DOI":"10.1038\/431624a","volume":"431","author":"P Ball","year":"2004","unstructured":"Ball P: Synthetic biology: Starting from scratch. Nature. 2004, 431 (7009): 624-626. 10.1038\/431624a","journal-title":"Nature"},{"issue":"5655","key":"460_CR3","doi-asserted-by":"publisher","first-page":"158","DOI":"10.1126\/science.303.5655.158","volume":"303","author":"D Ferber","year":"2004","unstructured":"Ferber D: Synthetic biology: Microbes made to order. Science. 2004, 303 (5655): 158-161. 10.1126\/science.303.5655.158","journal-title":"Science"},{"issue":"7","key":"460_CR4","doi-asserted-by":"publisher","first-page":"533","DOI":"10.1038\/nrg1637","volume":"6","author":"SA Benner","year":"2005","unstructured":"Benner SA, Sismour AM: Synthetic biology. Nat Rev Genet. 2005, 6 (7): 533-543. 10.1038\/nrg1637","journal-title":"Nat Rev Genet"},{"issue":"3","key":"460_CR5","doi-asserted-by":"publisher","first-page":"431","DOI":"10.1016\/j.jtbi.2005.01.023","volume":"235","author":"M Chaves","year":"2005","unstructured":"Chaves M, Albert Ra, Sontag ED: Robustness and fragility of Boolean models for genetic regulatory networks. J Theor Biol. 2005, 235 (3): 431-449. 10.1016\/j.jtbi.2005.01.023","journal-title":"J Theor Biol"},{"issue":"2","key":"460_CR6","doi-asserted-by":"publisher","first-page":"348","DOI":"10.1016\/j.jtbi.2005.05.032","volume":"238","author":"T Lipniacki","year":"2006","unstructured":"Lipniacki T, Paszek P, Marciniak-Czochra A, Brasier AR, Kimmel M: Transcriptional stochasticity in gene expression. J Theor Biol. 2006, 238 (2): 348-367. 10.1016\/j.jtbi.2005.05.032","journal-title":"J Theor Biol"},{"issue":"5","key":"460_CR7","doi-asserted-by":"publisher","first-page":"553","DOI":"10.1002\/bit.20630","volume":"92","author":"BF Pfleger","year":"2005","unstructured":"Pfleger BF, Fawzi NJ, Keasling JD: Optimization of DsRed production in Escherichia coli: Effect of ribosome binding site sequestration on translation efficiency. Biotechnol Bioeng. 2005, 92 (5): 553-558. 10.1002\/bit.20630","journal-title":"Biotechnol Bioeng"},{"issue":"5","key":"460_CR8","doi-asserted-by":"publisher","first-page":"1933","DOI":"10.1093\/nar\/17.5.1933","volume":"17","author":"JM Chernak","year":"1989","unstructured":"Chernak JM, Hamilton OS: Use of synthetic ribosome binding site for overproduction of the 5B protein of Insertion sequence IS5. Nucleic Acids Res. 1989, 17 (5): 1933-1951. 10.1093\/nar\/17.5.1933","journal-title":"Nucleic Acids Res"},{"issue":"7","key":"460_CR9","doi-asserted-by":"publisher","first-page":"2605","DOI":"10.1073\/pnas.89.7.2605","volume":"89","author":"J Zhang","year":"1992","unstructured":"Zhang J, Deutscher MP: A uridine-rich sequence required for translation of prokaryotic mRNA. Proc Natl Acad Sci USA. 1992, 89 (7): 2605-2609. 10.1073\/pnas.89.7.2605","journal-title":"Proc Natl Acad Sci USA"},{"issue":"5924","key":"460_CR10","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1126\/science.1170160","volume":"324","author":"G Kudla","year":"2009","unstructured":"Kudla G, Murray AW, Tollervey D, Plotkin JB: Coding-sequence determinants of gene expression in Escherichia coli. Science. 2009, 324 (5924): 255-258. 10.1126\/science.1170160","journal-title":"Science"},{"issue":"1","key":"460_CR11","doi-asserted-by":"publisher","first-page":"94","DOI":"10.1016\/j.pep.2008.01.008","volume":"59","author":"NA Burgess-Brown","year":"2008","unstructured":"Burgess-Brown NA, Sharma S, Sobott F, Loenarz C, Oppermann U, Gileadi O: Codon optimization can improve expression of human genes in Escherichia coli: A multi-gene study. Protein Expr Purif. 2008, 59 (1): 94-102. 10.1016\/j.pep.2008.01.008","journal-title":"Protein Expr Purif"},{"issue":"1","key":"460_CR12","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1016\/j.bbrc.2006.07.209","volume":"349","author":"W Zhang","year":"2006","unstructured":"Zhang W, Xiao W, Wei H, Zhang J, Tian Z: mRNA secondary structure at start AUG codon is a key limiting factor for human protein expression in Escherichia coli. Biochem Biophys Res Comm. 2006, 349 (1): 69-78. 10.1016\/j.bbrc.2006.07.209","journal-title":"Biochem Biophys Res Comm"},{"issue":"26","key":"460_CR13","doi-asserted-by":"publisher","first-page":"16587","DOI":"10.1073\/pnas.252535999","volume":"99","author":"Y Yokobayashi","year":"2002","unstructured":"Yokobayashi Y, Weiss R, Arnold FH: Directed evolution of a genetic circuit. Proc Natl Acad Sci USA. 2002, 99 (26): 16587-16591. 10.1073\/pnas.252535999","journal-title":"Proc Natl Acad Sci USA"},{"issue":"1","key":"460_CR14","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1146\/annurev.biophys.36.040306.132600","volume":"36","author":"EL Haseltine","year":"2007","unstructured":"Haseltine EL, Arnold FH: Synthetic gene circuits: Design with directed evolution. Annu Rev Bioph Biom. 2007, 36 (1): 1-19. 10.1146\/annurev.biophys.36.040306.132600.","journal-title":"Annu Rev Bioph Biom"},{"issue":"11","key":"460_CR15","doi-asserted-by":"publisher","first-page":"5075","DOI":"10.1093\/nar\/16.11.5075","volume":"16","author":"KT Min","year":"1988","unstructured":"Min KT, Kim MH, Lee DS: Search for the optimal sequence of the ribosome binding site by random oligonucleotide-directed mutagenesis. Nucleic Acids Res. 1988, 16 (11): 5075-5088. 10.1093\/nar\/16.11.5075","journal-title":"Nucleic Acids Res"},{"issue":"5","key":"460_CR16","doi-asserted-by":"publisher","first-page":"e52","DOI":"10.1093\/nar\/gnh050","volume":"32","author":"OB Zhelyabovskaya","year":"2004","unstructured":"Zhelyabovskaya OB, Berlin YA, Birikh KR: Artificial genetic selection for an efficient translation initiation site for expression of human RACK1 gene in Escherichia coli. Nucleic Acids Res. 2004, 32 (5): e52- 10.1093\/nar\/gnh050","journal-title":"Nucleic Acids Res"},{"issue":"4","key":"460_CR17","doi-asserted-by":"publisher","first-page":"619","DOI":"10.1016\/j.jmb.2005.10.076","volume":"355","author":"JC Anderson","year":"2006","unstructured":"Anderson JC, Clarke EJ, Arkin AP, Voigt CA: Environmentally controlled invasion of cancer cells by engineered bacteria. J Mol Biol. 2006, 355 (4): 619-627. 10.1016\/j.jmb.2005.10.076","journal-title":"J Mol Biol"},{"issue":"1","key":"460_CR18","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1128\/MMBR.69.1.101-123.2005","volume":"69","author":"BS Laursen","year":"2005","unstructured":"Laursen BS, Sorensen HP, Mortensen KK, Sperling-Petersen HU: Initiation of protein synthesis in bacteria. Microbiol Mol Biol Rev. 2005, 69 (1): 101-123. 10.1128\/MMBR.69.1.101-123.2005","journal-title":"Microbiol Mol Biol Rev"},{"issue":"7","key":"460_CR19","doi-asserted-by":"publisher","first-page":"1063","DOI":"10.1111\/j.1365-2958.1990.tb00679.x","volume":"4","author":"N Jacques","year":"1990","unstructured":"Jacques N, Dreyfus M: Translation initiation in Escherichia coli: old and new questions. Mol Microbiol. 1990, 4 (7): 1063-1067. 10.1111\/j.1365-2958.1990.tb00679.x","journal-title":"Mol Microbiol"},{"issue":"1-2","key":"460_CR20","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/0378-1119(80)90163-8","volume":"9","author":"D Iserentant","year":"1980","unstructured":"Iserentant D, Fiers W: Secondary structure of mRNA and efficiency of translation initiation. Gene. 1980, 9 (1-2): 1-12. 10.1016\/0378-1119(80)90163-8","journal-title":"Gene"},{"issue":"13","key":"460_CR21","doi-asserted-by":"publisher","first-page":"5481","DOI":"10.1093\/nar\/14.13.5481","volume":"14","author":"AC Looman","year":"1986","unstructured":"Looman AC, Bodlaender J, de Gruyter M, Vogelaar A, van Knippenberg PH: Secondary structure as primary determinant of the efficiency of ribosome binding sites in Escherichia coli. Nucleic Acids Res. 1986, 14 (13): 5481-5497. 10.1093\/nar\/14.13.5481","journal-title":"Nucleic Acids Res"},{"issue":"2","key":"460_CR22","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1016\/0378-1119(84)90255-5","volume":"28","author":"JL Schottel","year":"1984","unstructured":"Schottel JL, Sninsky JJ, Cohen SN: Effects of alterations in the translation control region on bacterial gene expression: use of cat gene constructs transcribed from the lac promoter as a model system. Gene. 1984, 28 (2): 177-193. 10.1016\/0378-1119(84)90255-5","journal-title":"Gene"},{"issue":"19","key":"460_CR23","doi-asserted-by":"publisher","first-page":"7668","DOI":"10.1073\/pnas.87.19.7668","volume":"87","author":"MH de Smit","year":"1990","unstructured":"de Smit MH, van Duin J: Secondary structure of the ribosome binding site determines translational efficiency: A quantitative analysis. Proc Natl Acad Sci USA. 1990, 87 (19): 7668-7672. 10.1073\/pnas.87.19.7668","journal-title":"Proc Natl Acad Sci USA"},{"issue":"17","key":"460_CR24","doi-asserted-by":"publisher","first-page":"4019","DOI":"10.1093\/nar\/21.17.4019","volume":"21","author":"T Schurr","year":"1993","unstructured":"Schurr T, Nadir E, Margalit H: Identification and characterization of E.coli ribosomal binding sites by free energy computation. Nucleic Acids Res. 1993, 21 (17): 4019-4023. 10.1093\/nar\/21.17.4019","journal-title":"Nucleic Acids Res"},{"issue":"3","key":"460_CR25","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1128\/jb.175.3.597-603.1993","volume":"175","author":"NF Habib","year":"1993","unstructured":"Habib NF, Jackson MP: Roles of a ribosome-binding site and mRNA secondary structure in differential expression of Shiga toxin genes. J Bacteriol. 1993, 175 (3): 597-603.","journal-title":"J Bacteriol"},{"issue":"3","key":"460_CR26","doi-asserted-by":"crossref","first-page":"512","DOI":"10.1128\/mr.60.3.512-538.1996","volume":"60","author":"SC Makrides","year":"1996","unstructured":"Makrides SC: Strategies for achieving high-level expression of genes in Escherichia coli. Microbiol Rev. 1996, 60 (3): 512-538.","journal-title":"Microbiol Rev"},{"issue":"1","key":"460_CR27","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1016\/0022-2836(85)90332-8","volume":"181","author":"J Coleman","year":"1985","unstructured":"Coleman J, Inouye M, Nakamura K: Mutations upstream of the ribosome-binding site affect translational efficiency. J Mol Biol. 1985, 181 (1): 139-143. 10.1016\/0022-2836(85)90332-8","journal-title":"J Mol Biol"},{"issue":"3","key":"460_CR28","doi-asserted-by":"publisher","first-page":"284","DOI":"10.1006\/prep.1995.1037","volume":"6","author":"G Wang","year":"1995","unstructured":"Wang G, Liu NJ, Yang KY: High-level expression of prochymosin in Escherichia coli: Effect of the secondary structure of the ribosome binding site. Protein Expr Purif. 1995, 6 (3): 284-290. 10.1006\/prep.1995.1037","journal-title":"Protein Expr Purif"},{"issue":"3","key":"460_CR29","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1016\/j.str.2006.12.008","volume":"15","author":"T Kaminishi","year":"2007","unstructured":"Kaminishi T, Wilson DN, Takemoto C, Harms JM, Kawazoe M, Schluenzen F, Hanawa-Suetsugu K, Shirouzu M, Fucini P, Yokoyama S: A snapshot of the 30S ribosomal subunit capturing mRNA via the Shine-Dalgarno interaction. Structure. 2007, 15 (3): 289-297. 10.1016\/j.str.2006.12.008","journal-title":"Structure"},{"issue":"9","key":"460_CR30","doi-asserted-by":"publisher","first-page":"751","DOI":"10.1016\/S0969-2126(01)00649-9","volume":"9","author":"GM Culver","year":"2001","unstructured":"Culver GM: Meanderings of the mRNA through the ribosome. Structure. 2001, 9 (9): 751-758. 10.1016\/S0969-2126(01)00649-9","journal-title":"Structure"},{"issue":"38","key":"460_CR31","doi-asserted-by":"publisher","first-page":"10254","DOI":"10.1021\/bi00089a048","volume":"32","author":"S Ringquist","year":"1993","unstructured":"Ringquist S, MacDonald M, Gibson T, Gold L: Nature of the ribosomal mRNA track: Analysis of ribosome-binding sites containing different sequences and secondary structures. Biochemistry. 1993, 32 (38): 10254-10262. 10.1021\/bi00089a048","journal-title":"Biochemistry"},{"issue":"5","key":"460_CR32","doi-asserted-by":"publisher","first-page":"834","DOI":"10.1073\/pnas.51.5.834","volume":"51","author":"M Takanami","year":"1964","unstructured":"Takanami M, Zubay G: An estimate of the size of the ribosomal site for messenger RNA binding. Proc Natl Acad Sci USA. 1964, 51 (5): 834-839. 10.1073\/pnas.51.5.834","journal-title":"Proc Natl Acad Sci USA"},{"issue":"1","key":"460_CR33","doi-asserted-by":"publisher","first-page":"173","DOI":"10.1016\/S0022-2836(05)80024-5","volume":"235","author":"MH de Smit","year":"1994","unstructured":"de Smit MH, van Duin J: Translational initiation on structured messengers: Another role for the shine-dalgarno interaction. J Mol Biol. 1994, 235 (1): 173-184. 10.1016\/S0022-2836(05)80024-5","journal-title":"J Mol Biol"},{"issue":"8","key":"460_CR34","doi-asserted-by":"publisher","first-page":"1178","DOI":"10.1261\/rna.7650904","volume":"10","author":"DH Mathews","year":"2004","unstructured":"Mathews DH: Using an RNA secondary structure partition function to determine confidence in base pairs predicted by free energy minimization. RNA. 2004, 10 (8): 1178-1190. 10.1261\/rna.7650904","journal-title":"RNA"},{"issue":"7134","key":"460_CR35","doi-asserted-by":"publisher","first-page":"454","DOI":"10.1038\/nature05625","volume":"446","author":"S Uemura","year":"2007","unstructured":"Uemura S, Dorywalska M, Lee TH, Kim HD, Puglisi JD, Chu S: Peptide bond formation destabilizes Shine-Dalgarno interaction on the ribosome. Nature. 2007, 446 (7134): 454-457. 10.1038\/nature05625","journal-title":"Nature"},{"issue":"20","key":"460_CR36","doi-asserted-by":"publisher","first-page":"7706","DOI":"10.1073\/pnas.86.20.7706","volume":"86","author":"JA Jaeger","year":"1989","unstructured":"Jaeger JA, Turner DH, Zuker M: Improved predictions of secondary structures for RNA. Proc Natl Acad Sci USA. 1989, 86 (20): 7706-7710. 10.1073\/pnas.86.20.7706","journal-title":"Proc Natl Acad Sci USA"},{"issue":"1","key":"460_CR37","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1093\/nar\/9.1.133","volume":"9","author":"M Zuker","year":"1981","unstructured":"Zuker M, Stiegler P: Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acids Res. 1981, 9 (1): 133-148. 10.1093\/nar\/9.1.133","journal-title":"Nucleic Acids Res"},{"issue":"suppl_2","key":"460_CR38","doi-asserted-by":"publisher","first-page":"W577","DOI":"10.1093\/nar\/gki591","volume":"33","author":"NR Markham","year":"2005","unstructured":"Markham NR, Zuker M: DINAMelt web server for nucleic acid melting prediction. Nucleic Acids Res. 2005, 33 (suppl_2): W577-581. 10.1093\/nar\/gki591","journal-title":"Nucleic Acids Res"},{"issue":"13","key":"460_CR39","doi-asserted-by":"publisher","first-page":"3406","DOI":"10.1093\/nar\/gkg595","volume":"31","author":"M Zuker","year":"2003","unstructured":"Zuker M: Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003, 31 (13): 3406-3415. 10.1093\/nar\/gkg595","journal-title":"Nucleic Acids Res"},{"issue":"1","key":"460_CR40","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1016\/j.cell.2004.11.042","volume":"120","author":"S Takyar","year":"2005","unstructured":"Takyar S, Hickerson RP, Noller HF: mRNA helicase activity of the ribosome. Cell. 2005, 120 (1): 49-58. 10.1016\/j.cell.2004.11.042","journal-title":"Cell"},{"issue":"8","key":"460_CR41","doi-asserted-by":"publisher","first-page":"1713","DOI":"10.1093\/nar\/21.8.1713","volume":"21","author":"J van Himbergen","year":"1993","unstructured":"van Himbergen J, van Geffen B, van Duin J: Translational control by a long range RNA-RNA interaction; a basepair substitution analysis. Nucl Acids Res. 1993, 21 (8): 1713-1717. 10.1093\/nar\/21.8.1713","journal-title":"Nucl Acids Res"},{"key":"460_CR42","doi-asserted-by":"publisher","first-page":"82","DOI":"10.1038\/237082a0","volume":"237","author":"W Jou","year":"1972","unstructured":"Jou W, Haegeman G, Ysebaert M, Fiers W: Nucleotide sequence of the gene coding for the bacteriophage MS2 coat protein. Nature. 1972, 237: 82-88. 10.1038\/237082a0","journal-title":"Nature"},{"issue":"4","key":"460_CR43","doi-asserted-by":"publisher","first-page":"1342","DOI":"10.1073\/pnas.71.4.1342","volume":"71","author":"J Shine","year":"1974","unstructured":"Shine J, Dalgarno L: The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: Complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci USA. 1974, 71 (4): 1342-1346. 10.1073\/pnas.71.4.1342","journal-title":"Proc Natl Acad Sci USA"},{"issue":"7","key":"460_CR44","doi-asserted-by":"publisher","first-page":"578","DOI":"10.1093\/bioinformatics\/15.7.578","volume":"15","author":"Y Osada","year":"1999","unstructured":"Osada Y, Saito R, Tomita M: Analysis of base-pairing potentials between 16S rRNA and 5' UTR for translation initiation in various prokaryotes. Bioinformatics. 1999, 15 (7): 578-581. 10.1093\/bioinformatics\/15.7.578","journal-title":"Bioinformatics"},{"issue":"25","key":"460_CR45","doi-asserted-by":"publisher","first-page":"5864","DOI":"10.1021\/bi00566a031","volume":"19","author":"JD Gralla","year":"1980","unstructured":"Gralla JD, Carpousis AJ, Stefano JE: Productive and abortive initiation of transcription in vitro at the lac UV5 promoter. Biochemistry. 1980, 19 (25): 5864-5869. 10.1021\/bi00566a031","journal-title":"Biochemistry"},{"issue":"15","key":"460_CR46","doi-asserted-by":"publisher","first-page":"9697","DOI":"10.1073\/pnas.112318199","volume":"99","author":"JA Bernstein","year":"2002","unstructured":"Bernstein JA, Khodursky AB, Lin PH, Lin-Chao S, Cohen SN: Global analysis of mRNA decay and abundance in Escherichia coli at single-gene resolution using two-color fluorescent DNA microarrays. Proc Natl Acad Sci USA. 2002, 99 (15): 9697-9702. 10.1073\/pnas.112318199","journal-title":"Proc Natl Acad Sci USA"},{"issue":"2","key":"460_CR47","doi-asserted-by":"publisher","first-page":"216","DOI":"10.1101\/gr.912603","volume":"13","author":"DW Selinger","year":"2003","unstructured":"Selinger DW, Saxena RM, Cheung KJ, Church GM, Rosenow C: Global RNA half-life analysis in Escherichia coli reveals positional patterns of transcript degradation. Genome Res. 2003, 13 (2): 216-223. 10.1101\/gr.912603","journal-title":"Genome Res"},{"issue":"5","key":"460_CR48","doi-asserted-by":"publisher","first-page":"615","DOI":"10.1002\/(SICI)1097-0290(19961205)52:5<615::AID-BIT9>3.0.CO;2-M","volume":"52","author":"HS Yun","year":"1996","unstructured":"Yun HS, Hong J, Lim HC: Regulation of ribosome synthesis in Escherichia coli Effects of temperature and dilution rate changes. Biotechnol Bioeng. 1996, 52 (5): 615-624. 10.1002\/(SICI)1097-0290(19961205)52:5<615::AID-BIT9>3.0.CO;2-M","journal-title":"Biotechnol Bioeng"},{"issue":"7082","key":"460_CR49","doi-asserted-by":"publisher","first-page":"358","DOI":"10.1038\/nature04599","volume":"440","author":"L Cai","year":"2006","unstructured":"Cai L, Friedman N, Xie XS: Stochastic protein expression in individual cells at the single molecule level. Nature. 2006, 440 (7082): 358-362. 10.1038\/nature04599","journal-title":"Nature"},{"issue":"4","key":"460_CR50","doi-asserted-by":"publisher","first-page":"1344","DOI":"10.1128\/JB.187.4.1344-1349.2005","volume":"187","author":"A Komarova","year":"2005","unstructured":"Komarova A, Tchufistova L, Dreyfus M, Boni I: AU-rich sequences within 5'untranslated leaders enhance translation and stabilize mRNA in Escherichia coli. J Bacteriol. 2005, 187 (4): 1344- 10.1128\/JB.187.4.1344-1349.2005","journal-title":"J Bacteriol"},{"issue":"12","key":"460_CR51","doi-asserted-by":"publisher","first-page":"4038","DOI":"10.1093\/nar\/gkn354","volume":"36","author":"L Chubiz","year":"2008","unstructured":"Chubiz L, Rao C: Computational design of orthogonal ribosomes. Nucleic Acids Res. 2008, 36 (12): 4038- 10.1093\/nar\/gkn354","journal-title":"Nucleic Acids Res"},{"issue":"9","key":"460_CR52","doi-asserted-by":"publisher","first-page":"1219","DOI":"10.1111\/j.1365-2958.1992.tb01561.x","volume":"6","author":"S Ringquist","year":"1992","unstructured":"Ringquist S, Shinedling S, Barrick D, Green L, Binkley J, Stormo GD, Gold L: Translation initiation in Escherichia coli: sequences within the ribosome-binding site. Mol Microbiol. 1992, 6 (9): 1219-1229. 10.1111\/j.1365-2958.1992.tb01561.x","journal-title":"Mol Microbiol"},{"key":"460_CR53","volume-title":"Experiments in molecular genetics","author":"J Miller","year":"1972","unstructured":"Miller J: Experiments in molecular genetics. 1972, New York: Cold Spring Harbor Laboratory Press,"},{"issue":"10","key":"460_CR54","doi-asserted-by":"publisher","first-page":"946","DOI":"10.1038\/nbt.1568","volume":"27","author":"HM Salis","year":"2009","unstructured":"Salis HM, Mirsky EA, Voigt CA: Automated design of synthetic ribosome binding sites to control protein expression. Nat Biotech. 2009, 27 (10): 946-950. 10.1038\/nbt.1568.","journal-title":"Nat Biotech"},{"issue":"1","key":"460_CR55","doi-asserted-by":"publisher","first-page":"303","DOI":"10.1146\/annurev.micro.58.030603.123841","volume":"58","author":"S Gottesman","year":"2004","unstructured":"Gottesman S: The small RNA regulators of Escherichia coli: Roles and mechanisms. Annu Rev Microbiol. 2004, 58 (1): 303-328. 10.1146\/annurev.micro.58.030603.123841","journal-title":"Annu Rev Microbiol"},{"issue":"2","key":"460_CR56","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1016\/0022-2836(89)90329-X","volume":"210","author":"S Altuvia","year":"1989","unstructured":"Altuvia S, Kornitzer D, Teff D, Oppenheim AB: Alternative mRNA structures of the cIII gene of bacteriophage \u03bb determine the rate of its translation initiation. J Mol Biol. 1989, 210 (2): 265-280. 10.1016\/0022-2836(89)90329-X","journal-title":"J Mol Biol"}],"container-title":["BMC Systems Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/1752-0509-4-71.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,9,1]],"date-time":"2021-09-01T05:08:27Z","timestamp":1630472907000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcsystbiol.biomedcentral.com\/articles\/10.1186\/1752-0509-4-71"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2010,5,26]]},"references-count":56,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2010,12]]}},"alternative-id":["460"],"URL":"https:\/\/doi.org\/10.1186\/1752-0509-4-71","relation":{},"ISSN":["1752-0509"],"issn-type":[{"value":"1752-0509","type":"electronic"}],"subject":[],"published":{"date-parts":[[2010,5,26]]},"assertion":[{"value":"1 September 2009","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"26 May 2010","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"26 May 2010","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}}],"article-number":"71"}}