A condition-specific codon optimization approach for improved heterologous gene expression in Saccharomyces cerevisiae

BMC Systems Biology

Volumn 8, Issue 1, 2014, Pages

  Lanza, Amanda M ^a,c   Curran, Kathleen A ^a   Rey, Lindsey G ^a   Alper, Hal S ^a,b  

^a The University of Texas at Austin   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c Bristol Myers Squibb Company   (United States)

Author keywords

Codon bias; Codon optimization; Heterologous expression; Saccharomyces cerevisiae; Synthetic biology

Indexed keywords

CATECHOL 1,2 DIOXYGENASE; GREEN FLUORESCENT PROTEIN;

ARTICLE; CODON; GENE EXPRESSION; GENETIC DATABASE; GENETICS; METABOLIC ENGINEERING; METHODOLOGY; SACCHAROMYCES CEREVISIAE;

CATECHOL 1,2-DIOXYGENASE; CODON; DATABASES, GENETIC; GENE EXPRESSION; GREEN FLUORESCENT PROTEINS; METABOLIC ENGINEERING; SACCHAROMYCES CEREVISIAE;

EID: 84899155758     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-8-33     Document Type: Article

References (46)

1. Gustafsson C, Govindarajan S, Minshull J. Codon bias and heterologous protein expression. Trends Biotechnol 2004, 22:346-353. 10.1016/j.tibtech.2004.04.006, 15245907.
2. Young E, Alper H. Synthetic biology: tools to design, build, and optimize cellular processes. J Biomed Biotechnol 2010, 2010:130781. 2817555, 20150964.
3. 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, 59:94-102. 10.1016/j.pep.2008.01.008, 18289875.
4. Anthony JR, Anthony LC, Nowroozi F, Kwon G, Newman JD, Keasling JD. Optimization of the mevalonate-based isoprenoid biosynthetic pathway in Escherichia coli for production of the anti-malarial drug precursor amorpha-4,11-diene. Metab Eng 2009, 11:13-19. 10.1016/j.ymben.2008.07.007, 18775787.
5. Maertens B, Spriestersbach A, von Groll U, Roth U, Kubicek J, Gerrits M, Graf M, Liss M, Daubert D, Wagner R, Schafer F. Gene optimization mechanisms: a multi-gene study reveals a high success rate of full-length human proteins expressed in Escherichia coli. Protein Sci 2010, 19:1312-1326. 10.1002/pro.408, 2970903,2970903, 20506237.
6. Wiedemann B, Boles E. Codon-optimized bacterial genes improve L-Arabinose fermentation in recombinant Saccharomyces cerevisiae. Appl Environ Microbiol 2008, 74:2043-2050. 10.1128/AEM.02395-07, 2292587, 18263741.
7. Kotula L, Curtis PJ. Evaluation of foreign gene codon optimization in yeast: expression of a mouse IG kappa chain. Biotechnology (N Y) 1991, 9:1386-1389. 10.1038/nbt1291-1386, 1367771.
8. Partow S, Siewers V, Daviet L, Schalk M, Nielsen J. Reconstruction and evaluation of the synthetic bacterial MEP pathway in Saccharomyces cerevisiae. PLoS One 2012, 7:e52498. 10.1371/journal.pone.0052498, 3532213, 23285068.
9. Hershberg R, Petrov DA. General rules for optimal codon choice. PLoS Genet 2009, 5:e1000556. 10.1371/journal.pgen.1000556, 2700274, 19593368.
10. Plotkin JB, Kudla G. Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet 2011, 12:32-42. 10.1038/nrg2899, 3074964, 21102527.
11. Fox JM, Erill I. Relative codon adaptation: a generic codon bias index for prediction of gene expression. DNA Res 2010, 17:185-196. 10.1093/dnares/dsq012, 2885275, 20453079.
12. 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, 107:3645-3650. 10.1073/pnas.0909910107, 2840511, 20133581.
13. Nakamura Y, Gojobori T, Ikemura T. Codon usage tabulated from international DNA sequence databases: status for the year 2000. Nucleic Acids Res 2000, 28:292. 10.1093/nar/28.1.292, 102460, 10592250.
14. Jansen R, Bussemaker HJ, Gerstein M. Revisiting the codon adaptation index from a whole-genome perspective: analyzing the relationship between gene expression and codon occurrence in yeast using a variety of models. Nucleic Acids Res 2003, 31:2242-2251. 10.1093/nar/gkg306, 153734, 12682375.
15. Sharp PM, Li WH. The codon adaptation index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 1987, 15:1281-1295. 10.1093/nar/15.3.1281, 340524, 3547335.
16. Sharp PM, Tuohy TM, Mosurski KR. Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes. Nucleic Acids Res 1986, 14:5125-5143. 10.1093/nar/14.13.5125, 311530, 3526280.
17. Wright F. The 'effective number of codons' used in a gene. Gene 1990, 87:23-29. 10.1016/0378-1119(90)90491-9, 2110097.
18. Puigbo P, Guzman E, Romeu A, Garcia-Vallve S. OPTIMIZER: a web server for optimizing the codon usage of DNA sequences. Nucleic Acids Res 2007, 35:W126-W131. 10.1093/nar/gkm219, 1933141, 17439967.
19. Puigbo P, Bravo IG, Garcia-Vallve S. E-CAI: a novel server to estimate an expected value of Codon Adaptation Index (eCAI). BMC Bioinformatics 2008, 9:65. 10.1186/1471-2105-9-65, 2246156, 18230160.
20. Wang TT, Cheng WC, Lee BH. A simple program to calculate codon bias index. Mol Biotechnol 1998, 10:103-106. 10.1007/BF02760858, 9819810.
21. Alexeyev MF, Winkler HH. Gene synthesis, bacterial expression and purification of the Rickettsia prowazekii ATP/ADP translocase. Biochim Biophys Acta 1999, 1419:299-306. 10.1016/S0005-2736(99)00078-4, 10407080.
22. Curran KA, Leavitt JM, Karim AS, Alper HS. Metabolic engineering of muconic acid production in Saccharomyces cerevisiae. Metab Eng 2013, 15:55-66.
23. Agashe D, Martinez-Gomez NC, Drummond DA, Marx CJ. Good codons, Bad transcript: large reductions in gene expression and fitness arising from synonymous mutations in a Key enzyme. Mol Biol Evol 2013, 30(3):549-560. doi:10.1093/molbev/mss273, 10.1093/molbev/mss273, 3563975, 23223712.
24. Forster AC. Synthetic biology challenges long-held hypotheses in translation, codon bias and transcription. Biotechnol J 2012, 7:835-845.
25. Dong H, Nilsson L, Kurland CG. Co-variation of tRNA abundance and codon usage in Escherichia coli at different growth rates. J Mol Biol 1996, 260:649-663. 10.1006/jmbi.1996.0428, 8709146.
26. Frenkel-Morgenstern M, Danon T, Christian T, Igarashi T, Cohen L, Hou YM, Jensen LJ. Genes adopt non-optimal codon usage to generate cell cycle-dependent oscillations in protein levels. Mol Syst Biol 2012, 8:572. 3293633, 22373820.
27. Gingold H, Pilpel Y. Determinants of translation efficiency and accuracy. Mol Syst Biol 2011, 7:481. 3101949, 21487400.
28. Hershberg R, Petrov DA. Selection on codon bias. Annu Rev Genet 2008, 42:287-299. 10.1146/annurev.genet.42.110807.091442, 18983258.
29. Yarus M, Folley LS. Sense codons are found in specific contexts. J Mol Biol 1985, 182:529-540. 10.1016/0022-2836(85)90239-6, 3892014.
30. Chung BK, Lee DY. Computational codon optimization of synthetic gene for protein expression. BMC Syst Biol 2012, 6:134. 10.1186/1752-0509-6-134, 3495653, 23083100.
31. Tats A, Tenson T, Remm M. Preferred and avoided codon pairs in three domains of life. BMC Genomics 2008, 9:463. 10.1186/1471-2164-9-463, 2585594, 18842120.
32. Chung BK, Yusufi FN, Mariati, Yang Y, Lee DY. Enhanced expression of codon optimized interferon gamma in CHO cells. J Biotechnol 2013, 167:326-333. 10.1016/j.jbiotec.2013.07.011, 23876479.
33. Coleman JR, Papamichail D, Skiena S, Futcher B, Wimmer E, Mueller S. Virus attenuation by genome-scale changes in codon pair bias. Science 2008, 320:1784-1787. 10.1126/science.1155761, 2754401, 18583614.
34. Owrutsky P, Khaneja N. Control of inhomogeneous ensembles in the presence of a random periodic drift. American Control Conference (ACC), 2012; 27-29 June 2012 2012, 5090-5095.
35. Holstege FC, Jennings EG, Wyrick JJ, Lee TI, Hengartner CJ, Green MR, Golub TR, Lander ES, Young RA. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 1998, 95:717-728. 10.1016/S0092-8674(00)81641-4, 9845373.
36. Karim AS, Curran KA, Alper HS. Characterization of plasmid burden and copy number in Saccharomyces cerevisiae for optimization of metabolic engineering applications. Fems Yeast Res 2013, 13:107-116. 10.1111/1567-1364.12016, 3546148, 23107142.
37. Menzella HG. Comparison of two codon optimization strategies to enhance recombinant protein production in Escherichia coli. Microb Cell Fact 2011, 10:15. 10.1186/1475-2859-10-15, 3056764, 21371320.
38. Westholm JO, Nordberg N, Muren E, Ameur A, Komorowski J, Ronne H. Combinatorial control of gene expression by the three yeast repressors Mig1, Mig2 and Mig3. BMC Genomics 2008, 9:601. 10.1186/1471-2164-9-601, 2631581, 19087243.
39. Norkiene M, Gedvilaite A. Influence of codon bias on heterologous production of human papillomavirus type 16 major structural protein L1 in yeast. Scientific World J 2012, 2012:979218.
40. Curran KA, Alper HS. Expanding the chemical palate of cells by combining systems biology and metabolic engineering. Metab Eng 2012, 14:289-297. 10.1016/j.ymben.2012.04.006, 22595280.
41. Krivoruchko A, Siewers V, Nielsen J. Opportunities for yeast metabolic engineering: Lessons from synthetic biology. Biotechnol J 2011, 6:262-276.
42. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. Summaries of affymetrix GeneChip probe level data. Nucleic Acids Res 2003, 31:e15. 10.1093/nar/gng015, 150247, 12582260.
43. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4:249-264. 10.1093/biostatistics/4.2.249, 12925520.
44. Bolstad BM, Irizarry RA, Astrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003, 19:185-193. 10.1093/bioinformatics/19.2.185, 12538238.
45. Mumberg D, Müller R, Funk M. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 1995, 156:119-122. 10.1016/0378-1119(95)00037-7, 7737504.
46. Andersen JB, Sternberg C, Poulsen LK, Bjorn SP, Givskov M, Molin S. New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Appl Environ Microbiol 1998, 64:2240-2246. 106306, 9603842.