Strategies of codon optimization for high-level heterologous protein expression in microbial expression systems

Gene Reports

Volumn 9, Issue , 2017, Pages 46-53

  Al Hawash, Adnan B ^a,b   Zhang, Xiaoyu ^a   Ma, Fuying ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b MINISTRY OF EDUCATION   (Iraq)

Author keywords

Codon optimization; Gene engineering; Microbial systems; Synthetic biology

Indexed keywords

PROTEIN; SYNTHETIC DNA; TRANSFER RNA;

CODON; CODON FREQUENCY; CODON OPTIMIZATION; CODON USAGE; CODON USAGE BIAS; GENE EXPRESSION SYSTEM; GENETIC ANALYSIS; HETEROLOGOUS EXPRESSION; MICROBIAL EXPRESSION SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; RECOMBINANT DNA TECHNOLOGY; REVIEW; STATISTICAL BIAS; SYNTHETIC BIOLOGY;

EID: 85028708204     PISSN: 24520144     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.genrep.2017.08.006     Document Type: Review

References (107)

1. Agashe, D., Martinez-Gomez, N.C., Drummond, D.A., Marx, C.J., Good codons, bad transcript: large reductions in gene expression and fitness arising from synonymous mutations in a key enzyme. Mol. Biol. Evol. 30 (2013), 549–560.
2. Allert, M., Cox, J.C., Hellinga, H.W., Multifactorial determinants of protein expression in prokaryotic open reading frames. J. Mol. Biol. 402 (2010), 905–918.
3. Andersson, S., Kurland, C., Codon preferences in free-living microorganisms. Microbiol. Rev. 54 (1990), 198–210.
4. Angov, E., Hillier, C.J., Kincaid, R.L., Lyon, J.A., Heterologous protein expression is enhanced by harmonizing the codon usage frequencies of the target gene with those of the expression host. PLoS One, 3, 2008, e2189.
5. Basu, S., Gerchman, Y., Collins, C.H., Arnold, F.H., Weiss, R., A synthetic multicellular system for programmed pattern formation. Nature 434 (2005), 1130–1134.
6. Becker, J., Wittmann, C., Bio-based production of chemicals, materials and fuels–Corynebacterium glutamicum as versatile cell factory. Curr. Opin. Biotechnol. 23 (2012), 631–640.
7. Bennetzen, J.L., Hall, B., Codon selection in yeast. J. Biol. Chem. 257 (1982), 3026–3031.
8. Bond-Watts, B.B., Bellerose, R.J., Chang, M.C., Enzyme mechanism as a kinetic control element for designing synthetic biofuel pathways. Nat. Chem. Biol. 7 (2011), 222–227.
9. Bonekamp, F., Dalbøge, H., Christensen, T., Jensen, K.F., Translation rates of individual codons are not correlated with tRNA abundances or with frequencies of utilization in Escherichia coli. J. Bacteriol. 171 (1989), 5812–5816.
10. Boyle, P.M., Silver, P.A., Parts plus pipes: synthetic biology approaches to metabolic engineering. Metab. Eng. 14 (2012), 223–232.
11. Bradel-Tretheway, B.G., Zhen, Z., Dewhurst, S., Effects of codon-optimization on protein expression by the human herpesvirus 6 and 7 U51 open reading frame. J. Virol. Methods 111 (2003), 145–156.
12. Bulmer, M., Coevolution of codon usage and transfer RNA abundance. Nature 325 (1987), 728–730.
13. Burgess-Brown, N.A., 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. 59 (2008), 94–102.
14. Charneski, C.A., Hurst, L.D., Positively Charged Residues are the Major Determinants of Ribosomal Velocity. 2013.
15. Chen, Q., Nimal, J., Li, W., Liu, X., Cao, W., Delta-6 desaturase from borage converts linoleic acid to gamma-linolenic acid in HEK293 cells. Biochem. Biophys. Res. Commun. 410 (2011), 484–488.
16. Chen, C., Zhang, H., Broitman, S.L., Reiche, M., Farrell, I., Cooperman, B.S., Goldman, Y.E., Dynamics of translation by single ribosomes through mRNA secondary structures. Nat. Struct. Mol. Biol. 20 (2013), 582–588.
17. Coleman, J.R., Papamichail, D., Skiena, S., Futcher, B., Wimmer, E., Mueller, S., Virus attenuation by genome-scale changes in codon pair bias. Science 320 (2008), 1784–1787.
18. Constante, M., Grunberg, R., Isalan, M., A biobrick library for cloning custom eukaryotic plasmids. PLoS One, 6, 2011, e23685.
19. Crick, F., Barnett, L., Brenner, S., Watts-Tobin, R.J., General nature of the genetic code for proteins. Nature 192 (1961), 1227–1232.
20. Curran, J.F., Yarus, M., Rates of aminoacyl-tRNA selection at 29 sense codons in vivo. J. Mol. Biol. 209 (1989), 65–77.
21. Dellomonaco, C., Fava, F., Gonzalez, R., The path to next generation biofuels: successes and challenges in the era of synthetic biology. Microb. Cell Factories 9 (2010), 1–15.
22. Dong, H., Nilsson, L., Kurland, C.G., Co-variation of tRNA abundance and codon usage in Escherichia coli at different growth rates. J. Mol. Biol. 260 (1996), 649–663.
23. dos Reis, M., Savva, R., Wernisch, L., Solving the riddle of codon usage preferences: a test for translational selection. Nucleic Acids Res. 32 (2004), 5036–5044.
24. Duan, H., Wang, H., Ma, B., Jiang, P., Tu, P., Ni, Z., Li, X., Li, M., Ma, X., Wang, B., Codon optimization and expression of irisin in Pichia pastoris GS115. Int. J. Biol. Macromol. 79 (2015), 21–26.
25. Duret, L., Evolution of synonymous codon usage in metazoans. Curr. Opin. Genet. Dev. 12 (2002), 640–649.
26. Duret, L., Mouchiroud, D., Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 96 (1999), 4482–4487.
27. Feng, Z., Zhang, L., Han, X., Zhang, Y., Codon optimization of the calf prochymosin gene and its expression in Kluyveromyces lactis. World J. Microbiol. Biotechnol. 26 (2010), 895–901.
28. Fletcher, S.P., Muto, M., Mayfield, S.P., Optimization of recombinant protein expression in the chloroplasts of green algae. Adv. Exp. Med. Biol. 616 (2007), 90–98.
29. Gaspar, P., Oliveira, J.L., Frommlet, J., Santos, M.A., Moura, G., EuGene: maximizing synthetic gene design for heterologous expression. Bioinformatics 28 (2012), 2683–2684.
30. George, H.J., L'ITALIEN, J.J., PILACINSKI, W.P., GLASSMAN, D.L., KRZYZEK, R.A., High-level expression in Escherichia coli of biologically active bovine growth hormone. DNA 4 (1985), 273–281.
31. Ghaemmaghami, S., Huh, W.-K., Bower, K., Howson, R.W., Belle, A., Dephoure, N., O'Shea, E.K., Weissman, J.S., Global analysis of protein expression in yeast. Nature 425 (2003), 737–741.
32. Gimpel, J.A., Specht, E.A., Georgianna, D.R., Mayfield, S.P., Advances in microalgae engineering and synthetic biology applications for biofuel production. Curr. Opin. Chem. Biol. 17 (2013), 489–495.
33. Goetz, R.M., Fuglsang, A., Correlation of codon bias measures with mRNA levels: analysis of transcriptome data from Escherichia coli. Biochem. Biophys. Res. Commun. 327 (2005), 4–7.
34. Gong, M., Gong, F., Yanofsky, C., Overexpression of tnaC of Escherichia coli inhibits growth by depleting tRNA2Pro availability. J. Bacteriol. 188 (2006), 1892–1898.
35. Goodman, D.B., Church, G.M., Kosuri, S., Causes and effects of N-terminal codon bias in bacterial genes. Science 342 (2013), 475–479.
36. Hale, R.S., Thompson, G., Codon optimization of the gene encoding a domain from human type 1 neurofibromin protein results in a threefold improvement in expression level in Escherichia coli. Protein Expr. Purif. 12 (1998), 185–188.
37. Hansen, M.E., Wangari, R., Hansen, E.B., Mijakovic, I., Jensen, P.R., Engineering of Bacillus subtilis 168 for increased nisin resistance. Appl. Environ. Microbiol. 75 (2009), 6688–6695.
38. Hershberg, R., Petrov, D.A., Selection on codon bias. Annu. Rev. Genet. 42 (2008), 287–299.
39. Hershey, J.W., Sonenberg, N., Mathews, M.B., Principles of translational control: an overview. Cold Spring Harb. Perspect. Biol., 4, 2012, a011528.
40. Hoekema, A., Kastelein, R., Vasser, M., De Boer, H., Codon replacement in the PGK1 gene of Saccharomyces cerevisiae: experimental approach to study the role of biased codon usage in gene expression. Mol. Cell. Biol. 7 (1987), 2914–2924.
41. Hoover, D.M., Lubkowski, J., DNAWorks: an automated method for designing oligonucleotides for PCR-based gene synthesis. Nucleic Acids Res. 30 (2002), 1–7 e43.
42. Hu, X., Shi, Q., Yang, T., Jackowski, G., Specific replacement of consecutive AGG codons results in high-level expression of human cardiac troponin T in Escherichia coli. Protein Expr. Purif. 7 (1996), 289–293.
43. Ikemura, T., Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes. J. Mol. Biol. 146 (1981), 1–21.
44. Inouye, S., Sahara-Miura, Y., Sato, J.-I., Suzuki, T., Codon optimization of genes for efficient protein expression in mammalian cells by selection of only preferred human codons. Protein Expr. Purif. 109 (2015), 47–54.
45. Itakura, K., Hirose, T., Crea, R., Riggs, A.D., Heyneker, H.L., Bolivar, F., Boyer, H.W., Expression in Escherichia coli of a chemically synthesized gene for the hormone somatostatin. Science 198 (1977), 1056–1063.
46. Jayaraj, S., Reid, R., Santi, D.V., GeMS: an advanced software package for designing synthetic genes. Nucleic Acids Res. 33 (2005), 3011–3016.
47. Jia, H., Fan, G., Yan, Q., Liu, Y., Yan, Y., Jiang, Z., High-level expression of a hyperthermostable Thermotoga maritima xylanase in Pichia pastoris by codon optimization. J. Mol. Catal. B Enzym. 78 (2012), 72–77.
48. Kanaya, S., Yamada, Y., Kudo, Y., Ikemura, T., Studies of codon usage and tRNA genes of 18 unicellular organisms and quantification of Bacillus subtilis tRNAs: gene expression level and species-specific diversity of codon usage based on multivariate analysis. Gene 238 (1999), 143–155.
49. Kane, J.F., Effects of rare codon clusters on high-level expression of heterologous proteins in Escherichia coli. Curr. Opin. Biotechnol. 6 (1995), 494–500.
50. Keasling, J.D., Synthetic biology and the development of tools for metabolic engineering. Metab. Eng. 14 (2012), 189–195.
51. Klumpp, S., Dong, J., Hwa, T., On ribosome load, codon bias and protein abundance. PLoS One, 7, 2012, e48542.
52. Kocharin, K., Siewers, V., Nielsen, J., Improved polyhydroxybutyrate production by Saccharomyces cerevisiae through the use of the phosphoketolase pathway. Biotechnol. Bioeng. 110 (2013), 2216–2224.
53. Kodumal, S.J., Patel, K.G., Reid, R., Menzella, H.G., Welch, M., Santi, D.V., Total synthesis of long DNA sequences: synthesis of a contiguous 32-kb polyketide synthase gene cluster. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 15573–15578.
54. Komar, A.A., A pause for thought along the co-translational folding pathway. Trends Biochem. Sci. 34 (2009), 16–24.
55. Kosuri, S., Goodman, D.B., Cambray, G., Mutalik, V.K., Gao, Y., Arkin, A.P., Endy, D., Church, G.M., Composability of regulatory sequences controlling transcription and translation in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 14024–14029.
56. Kotula, L., Curtis, P.J., Evaluation of foreign gene codon optimization in yeast: expression of a mouse IG kappa chain. Nat. Biotechnol. 9 (1991), 1386–1389.
57. Krivoruchko, A., Siewers, V., Nielsen, J., Opportunities for yeast metabolic engineering: lessons from synthetic biology. Biotechnol. J. 6 (2011), 262–276.
58. Kurland, C., Gallant, J., Errors of heterologous protein expression. Curr. Opin. Biotechnol. 7 (1996), 489–493.
59. Lanza, A.M., Curran, K.A., Rey, L.G., Alper, H.S., A condition-specific codon optimization approach for improved heterologous gene expression in Saccharomyces cerevisiae. BMC Syst. Biol., 8, 2014, 33.
60. Li, G.-W., Oh, E., Weissman, J.S., The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature 484 (2012), 538–541.
61. Lithwick, G., Margalit, H., Hierarchy of sequence-dependent features associated with prokaryotic translation. Genome Res. 13 (2003), 2665–2673.
62. Marlatt, N.M., Spratt, D.E., Shaw, G.S., Codon optimization for enhanced Escherichia coli expression of human S100A11 and S100A1 proteins. Protein Expr. Purif. 73 (2010), 58–64.
63. Massey, S.E., Moura, G., Beltrão, P., Almeida, R., Garey, J.R., Tuite, M.F., Santos, M.A., Comparative evolutionary genomics unveils the molecular mechanism of reassignment of the CTG codon in Candida spp. Genome Res. 13 (2003), 544–557.
64. Medema, M.H., Breitling, R., Takano, E., Synthetic biology in Streptomyces bacteria. Methods Enzymol. 497 (2011), 485–502.
65. Meng, H., Wang, J., Xiong, Z., Xu, F., Zhao, G., Wang, Y., Quantitative design of regulatory elements based on high-precision strength prediction using artificial neural network. PLoS One, 8, 2013, e60288.
66. Menzella, H.G., Comparison of two codon optimization strategies to enhance recombinant protein production in Escherichia coli. Microb. Cell Factories, 10, 2011, 10.1186.
67. Novoa, E.M., Pavon-Eternod, M., Pan, T., de Pouplana, L.R., A role for tRNA modifications in genome structure and codon usage. Cell 149 (2012), 202–213.
68. Paddon, C.J., Westfall, P., Pitera, D., Benjamin, K., Fisher, K., McPhee, D., Leavell, M., Tai, A., Main, A., Eng, D., High-level semi-synthetic production of the potent antimalarial artemisinin. Nature 496 (2013), 528–532.
69. Peralta-Yahya, P.P., Ouellet, M., Chan, R., Mukhopadhyay, A., Keasling, J.D., Lee, T.S., Identification and microbial production of a terpene-based advanced biofuel. Nat. Commun., 2, 2011, 483.
70. Pertzev, A.V., Nicholson, A.W., Characterization of RNA sequence determinants and antideterminants of processing reactivity for a minimal substrate of Escherichia coli ribonuclease III. Nucleic Acids Res. 34 (2006), 3708–3721.
71. Pfleger, B.F., Pitera, D.J., Smolke, C.D., Keasling, J.D., Combinatorial engineering of intergenic regions in operons tunes expression of multiple genes. Nat. Biotechnol. 24 (2006), 1027–1032.
72. Plotkin, J.B., Kudla, G., Synonymous but not the same: the causes and consequences of codon bias. Nat. Rev. Genet. 12 (2011), 32–42.
73. Puigbo, P., Guzman, E., Romeu, A., Garcia-Vallve, S., OPTIMIZER: a web server for optimizing the codon usage of DNA sequences. Nucleic Acids Res. 35 (2007), W126–W131.
74. Qian, W., Yang, J.-R., Pearson, N.M., Maclean, C., Zhang, J., Balanced codon usage optimizes eukaryotic translational efficiency. PLoS Genet. 8 (2012), 1–18 e1002603.
75. Raab, D., Graf, M., Notka, F., Schödl, T., Wagner, R., The GeneOptimizer Algorithm: using a sliding window approach to cope with the vast sequence space in multiparameter DNA sequence optimization. Syst. Synth. Biol. 4 (2010), 215–225.
76. Richardson, S.M., Wheelan, S.J., Yarrington, R.M., Boeke, J.D., GeneDesign: rapid, automated design of multikilobase synthetic genes. Genome Res. 16 (2006), 550–556.
77. Rocha, E.P., Codon usage bias from tRNA's point of view: redundancy, specialization, and efficient decoding for translation optimization. Genome Res. 14 (2004), 2279–2286.
78. Rosano, G.L., Ceccarelli, E.A., Rare codon content affects the solubility of recombinant proteins in a codon bias-adjusted Escherichia coli strain. Microb. Cell Factories, 8, 2009, 41.
79. Salis, H.M., Mirsky, E.A., Voigt, C.A., Automated design of synthetic ribosome binding sites to control protein expression. Nat. Biotechnol. 27 (2009), 946–950.
80. Sander, I.M., Chaney, J.L., Clark, P.L., Expanding Anfinsen's principle: contributions of synonymous codon selection to rational protein design. J. Am. Chem. Soc. 136 (2014), 858–861.
81. Santos, M.A., Moura, G., Massey, S.E., Tuite, M.F., Driving change: the evolution of alternative genetic codes. Trends Genet. 20 (2004), 95–102.
82. Sharp, P.M., Li, W.-H., The codon adaptation index—a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 15 (1987), 1281–1295.
83. Sharp, P.M., Tuohy, T.M., Mosurski, K.R., Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes. Nucleic Acids Res. 14 (1986), 5125–5143.
84. Sharp, P.M., Emery, L.R., Zeng, K., Forces that influence the evolution of codon bias. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 365 (2010), 1203–1212.
85. Shetty, R., Lizarazo, M., Rettberg, R., Knight, T.F., Assembly of BioBrick standard biological parts using three antibiotic assembly. Methods Enzymol. 498 (2011), 311–326.
86. Steen, E.J., Kang, Y., Bokinsky, G., Hu, Z., Schirmer, A., McClure, A., Del Cardayre, S.B., Keasling, J.D., Microbial production of fatty-acid-derived fuels and chemicals from plant biomass. Nature 463 (2010), 559–562.
87. Studier, F.W., Moffatt, B.A., Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189 (1986), 113–130.
88. Subramanian, S., Nearly neutrality and the evolution of codon usage bias in eukaryotic genomes. Genetics 178 (2008), 2429–2432.
89. Tschopp, J.F., Brust, P.F., Cregg, J.M., Stillman, C.A., Gingeras, T.R., Expression of the lacZ gene from two methanol-regulated promoters in Pichia pastoris. Nucleic Acids Res. 15 (1987), 3859–3876.
90. Vervoort, E.B., van Ravestein, A., van Peij, N.N., Heikoop, J.C., van Haastert, P.J., Verheijden, G.F., Linskens, M.H., Optimizing heterologous expression in Dictyostelium: importance of 5′ codon adaptation. Nucleic Acids Res. 28 (2000), 2069–2074.
91. Villalobos, A., Ness, J.E., Gustafsson, C., Minshull, J., Govindarajan, S., Gene Designer: a synthetic biology tool for constructing artificial DNA segments. BMC Bioinf., 7, 2006, 285.
92. Vogl, T., Ruth, C., Pitzer, J., Kickenweiz, T., Glieder, A., Synthetic core promoters for Pichia pastoris. ACS Synth. Biol. 3 (2013), 188–191.
93. Wang, X., Li, X., Zhang, Z., Shen, X., Zhong, F., Codon optimization enhances secretory expression of Pseudomonas aeruginosa exotoxin A in E. coli. Protein Expr. Purif. 72 (2010), 101–106.
94. Wang, B., Wang, J., Zhang, W., Meldrum, D.R., Application of synthetic biology in cyanobacteria and algae. Front. Microbiol. 3 (2012), 1–15.
95. Welch, M., Govindarajan, S., Ness, J.E., Villalobos, A., Gurney, A., Minshull, J., Gustafsson, C., Design parameters to control synthetic gene expression in Escherichia coli. PLoS One 4 (2009), 1–10 e7002.
96. Williams, D., Regier, D., Akiyoshi, D., Genbauffe, F., Murphy, J., Design, synthesis and expression of a human interteukin-2 gene incorporating the codon usage bias found in highly expressed Escherichia coli genes. Nucleic Acids Res. 16 (1988), 10453–10468.
97. Wright, F., The ‘effective number of codons’ used in a gene. Gene 87 (1990), 23–29.
98. Wu, G., Bashir-Bello, N., Freeland, S.J., The synthetic gene designer: a flexible web platform to explore sequence manipulation for heterologous expression. Protein Expr. Purif. 47 (2006), 441–445.
99. Wu, Y., Zhang, Y., Tu, R., Liu, H., Wang, Q., Construction of synthetic promoters for Escherichia coli and application in the biosynthesis of cis, cis-muconic acid. Chin. J. Biotechnol. 29 (2013), 760–771.
100. Yadava, A., Ockenhouse, C.F., Effect of codon optimization on expression levels of a functionally folded malaria vaccine candidate in prokaryotic and eukaryotic expression systems. Infect. Immun. 71 (2003), 4961–4969.
101. Yang, J.-K., Liu, L.-Y., Dai, J.-H., Li, Q., De novo design and synthesis of Candida antarctica lipase B gene and α-factor leads to high-level expression in Pichia pastoris. PLoS One, 8, 2013, e53939.
102. Yim, S.S., An, S.J., Kang, M., Lee, J., Jeong, K.J., Isolation of fully synthetic promoters for high-level gene expression in Corynebacterium glutamicum. Biotechnol. Bioeng. 110 (2013), 2959–2969.
103. Yu, P., Yan, Y., Gu, Q., Wang, X., Codon optimisation improves the expression of Trichoderma viride sp. endochitinase in Pichia pastoris. Sci Rep 3 (2013), 1–6.
104. Zhou, J., Liu, W.J., Peng, S.W., Sun, X.Y., Frazer, I., Papillomavirus capsid protein expression level depends on the match between codon usage and tRNA availability. J. Virol. 73 (1999), 4972–4982.
105. Zhou, T., Weems, M., Wilke, C.O., Translationally optimal codons associate with structurally sensitive sites in proteins. Mol. Biol. Evol. 26 (2009), 1571–1580.
106. Zhou, W.-J., Yang, J.-K., Mao, L., Miao, L.-H., Codon optimization, promoter and expression system selection that achieved high-level production of Yarrowia lipolytica lipase in Pichia pastoris. Enzym. Microb. Technol. 71 (2015), 66–72.
107. Zolotukhin, S., Potter, M., Hauswirth, W.W., Guy, J., Muzyczka, N., A “humanized” green fluorescent protein cDNA adapted for high-level expression in mammalian cells. J. Virol. 70 (1996), 4646–4654.