Genome engineering for improved recombinant protein expression in escherichia coli

Microbial Cell Factories

Volumn 13, Issue 1, 2014, Pages

  Mahalik, Shubhashree ^a   Sharma, Ashish K ^a   Mukherjee, Krishna J ^a  

^a JAWAHARLAL NEHRU UNIVERSITY   (India)

Author keywords

Escherichia coli; Genome engineering; Metabolic engineering; Recombinant protein expression

Indexed keywords

RECOMBINANT PROTEIN;

ARTICLE; BACTERIAL GENOME; CELL ENGINEERING; CELLULAR STRESS RESPONSE; CYTOPLASM; DNA MODIFICATION; DOWNSTREAM PROCESSING; ESCHERICHIA COLI; GENETIC ENGINEERING; GROWTH INHIBITION; HIGH THROUGHPUT SCREENING; HIGH THROUGHPUT SEQUENCING; HOST CELL; MESSENGER RNA SYNTHESIS; METABOLIC ENGINEERING; MICROBIAL BIOMASS; NEGATIVE FEEDBACK; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FOLDING; TRANSLATION INITIATION; BIOSYNTHESIS; GENE EXPRESSION; GENETICS; METABOLISM; PROCEDURES;

ESCHERICHIA COLI;

ESCHERICHIA COLI; GENE EXPRESSION; GENETIC ENGINEERING; GENOME, BACTERIAL; RECOMBINANT PROTEINS;

EID: 84924033943     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/s12934-014-0177-1     Document Type: Article

References (195)

1. Ajikumar PK, Xiao WH, Tyo KE, Wang Y, Simeon F, Leonard E, Mucha O, Phon TH, Pfeifer B, Stephanopoulos G: Isoprenoid pathway optimization for Taxol precursor overproduction in Escherichia coli . Science 2010, 330:70-74.
2. Bongaerts J, Kramer M, Muller U, Raeven L, Wubbolts M: Metabolic engineering for microbial production of aromatic amino acids and derived compounds. Metab Eng 2001, 3:289-300.
3. Cui YY, Ling C, Zhang YY, Huang J, Liu JZ: Production of shikimic acid from Escherichia coli through chemically inducible chromosomal evolution and cofactor metabolic engineering. Microb Cell Fact 2014, 13:21.
4. Farmer WR, Liao JC: Improving lycopene production in Escherichia coli by engineering metabolic control. Nat Biotechnol 2000, 18:533-537.
5. Flores N, Xiao J, Berry A, Bolivar F, Valle F: Pathway engineering for the production of aromatic compounds in Escherichia coli . Nat Biotechnol 1996, 14:620-623.
6. Paddon CJ, Keasling JD: Semi-synthetic artemisinin: a model for the use of synthetic biology in pharmaceutical development. Nat Rev Micro 2014, 12:355-367.
7. Pitera DJ, Paddon CJ, Newman JD, Keasling JD: Balancing a heterologous mevalonate pathway for improved isoprenoid production in Escherichia coli . Metab Eng 2007, 9:193-207.
8. Kucharova V, Skancke J, Brautaset T, Valla S: Design and Optimization of Short DNA Sequences That Can Be Used as 5' Fusion Partners for High-Level Expression of Heterologous Genes in Escherichia coli . Appl Environ Microbiol 2013, 79:6655-6664.
9. Suzuki M, Zhang J, Liu M, Woychik NA, Inouye M: Single Protein Production in Living Cells Facilitated by an mRNA Interferase. Mol Cell 2005, 18:253-261.
10. Shin J, Noireaux V: Study of messenger RNA inactivation and protein degradation in an Escherichia coli cell-free expression system. J Biol Eng 2010, 4:9.
11. Fakruddin M, Mohammad Mazumdar R, Bin Mannan KS, Chowdhury A, Hossain MN: Critical Factors Affecting the Success of Cloning, Expression, and Mass Production of Enzymes by Recombinant E. coli. ISRN Biotechnology 2012, 2013:7.
12. Cabrita LD, Dai W, Bottomley SP: A family of E. coli expression vectors for laboratory scale and high throughput soluble protein production. BMC Biotechnol 2006, 6:12.
13. Selleck W, Tan S: Recombinant protein complex expression in E. coli. Curr Protoc Protein Sci 2008, 5(21):21-25. 21. 21.
14. Schumann W, Ferreira LCS: Production of recombinant proteins in Escherichia coli . Genet Mol Biol 2004, 27:442-453.
15. Balzer S, Kucharova V, Megerle J, Lale R, Brautaset T, Valla S: A comparative analysis of the properties of regulated promoter systems commonly used for recombinant gene expression in Escherichia coli . Microb Cell Fact 2013, 12:26.
16. Dragosits M, Nicklas D, Tagkopoulos I: A synthetic biology approach to self-regulatory recombinant protein production in Escherichia coli . J Biol Eng 2012, 6:2.
17. Zwick F, Lale R, Valla S: Strong stimulation of recombinant protein production in Escherichia coli by combining stimulatory control elements in an expression cassette. Microb Cell Fact 2012, 11:133.
18. Giacalone MJ, Gentile AM, Lovitt BT, Berkley NL, Gunderson CW, Surber MW: Toxic protein expression in Escherichia coli using a rhamnose-based tightly regulated and tunable promoter system. Biotechniques 2006, 40:355.
19. Marini G, Luchese M, Argondizzo AP, de Goes ACMA, Galler R, Alves TL, Medeiros M, Larentis A: Experimental design approach in recombinant protein expression: determining medium composition and induction conditions for expression of pneumolysin from Streptococcus pneumoniae in Escherichia coli and preliminary purification process. BMC Biotechnol 2014, 14:1.
20. Choi YJ, Morel L, Le François T, Bourque D, Bourget L, Groleau D, Massie B, Míguez CB: Novel, Versatile, and Tightly Regulated Expression System for Escherichia coli Strains. Appl Environ Microbiol 2010, 76:5058-5066.
21. Nallamsetty S, Waugh DS: A generic protocol for the expression and purification of recombinant proteins in Escherichia coli using a combinatorial His6-maltose binding protein fusion tag. Nat Protocols 2007, 2:383-391.
22. Chatterjee DK, Esposito D: Enhanced soluble protein expression using two new fusion tags. Protein Expr Purif 2006, 46:122-129.
23. Costa SJ, Almeida A, Castro A, Domingues L, Besir H: The novel Fh8 and H fusion partners for soluble protein expression in Escherichia coli: a comparison with the traditional gene fusion technology. Appl Microbiol Biotechnol 2013, 97:6779-6791.
24. Kim S, Lee SB: Soluble expression of archaeal proteins in Escherichia coli by using fusion-partners. Protein Expr Purif 2008, 62:116-119.
25. Ideno A, Furutani M, Iwabuchi T, Iida T, Iba Y, Kurosawa Y, Sakuraba H, Ohshima T, Kawarabayashi Y, Maruyama T: Expression of foreign proteins in Escherichia coli by fusing with an archaeal FK506 binding protein. Appl Microbiol Biotechnol 2004, 64:99-105.
26. Esposito D, Chatterjee DK: Enhancement of soluble protein expression through the use of fusion tags. Curr Opin Biotechnol 2006, 17:353-358.
27. Zuo X, Li S, Hall J, Mattern MR, Tran H, Shoo J, Tan R, Weiss SR, Butt TR: Enhanced expression and purification of membrane proteins by SUMO fusion in Escherichia coli . J Struct Funct Genomics 2005, 6:103-111.
28. Nocadello S, Swennen E: The new pLAI (lux regulon based auto-inducible) expression system for recombinant protein production in Escherichia coli . Microb Cell Fact 2012, 11:3.
29. Studier FW: Stable expression clones and auto-induction for protein production in E. coli. In Structural Genomics. Springer; 2014:17-32.
30. da Silva AJ, Horta ACL, Velez AM, Iemma MRC, Sargo CR, Giordano R, Novo MTM, Giordano RC, Zangirolami TC: Non-conventional induction strategies for production of subunit swine erysipelas vaccine antigen in rE. coli fed-batch cultures. Springer Plus 2013, 14:322.
31. Studier FW: Protein production by auto-induction in high-density shaking cultures. Protein Expr Purif 2005, 41:207-234.
32. Sadilkova L, Osicka R, Sulc M, Linhartova I, Novak P, Sebo P: Single-step affinity purification of recombinant proteins using a self-excising module from Neisseria meningitidis FrpC. Protein Sci 2008, 17:1834-1843.
33. Li Y: Self-cleaving fusion tags for recombinant protein production. Biotechnol Lett 2011, 33:869-881.
34. Wu W-Y, Mee C, Califano F, Banki R, Wood DW: Recombinant protein purification by self-cleaving aggregation tag. Nat Protocols 2006, 1:2257-2262.
35. Care S, Bignon C, Pelissier M, Blanc E, Canard B, Coutard B: The translation of recombinant proteins in E. coli can be improved by in silico generating and screening random libraries of a- 70/+ 96 mRNA region with respect to the translation initiation codon. Nucleic Acids Res 2008, 36:e6-e6.
36. Salis HM, Mirsky EA, Voigt CA: Automated design of synthetic ribosome binding sites to control protein expression. Nat Biotechnol 2009, 27:946-950.
37. Berg L, Lale R, Bakke I, Burroughs N, Valla S: The expression of recombinant genes in Escherichia coli can be strongly stimulated at the transcript production level by mutating the DNA-region corresponding to the 5'-untranslated part of mRNA. J Microbial Biotechnol 2009, 2:379-389.
38. Reeve B, Hargest T, Gilbert C, Ellis T: Predicting translation initiation rates for designing synthetic biology. Synthetic Biol 2014, 2:1.
39. Hoffmann F, Rinas U: Stress induced by recombinant protein production in Escherichia coli . Adv Biochem Eng Biotechnol 2004, 89:73-92.
40. Sørensen HP, Mortensen KK: Advanced genetic strategies for recombinant protein expression in Escherichia coli . J Biotechnol 2005, 115:113-128.
41. Piir K, Paier A, Liiv A, Tenson T, Maiväli Ü: Ribosome degradation in growing bacteria. EMBO Rep 2011, 12:458-462.
42. Maruyama H, Mizuno D: Ribosome degradation and the degradation products in starved Escherichia coli . I. Comparison of the degradation rate and of the nucleotide pool between Escherichia coli B and Q-13 strains in phosphate deficiency. Biochim Biophys Acta 1970, 199:159-165.
43. Ben-Hamida F, Schlessinger D: Synthesis and breakdown of ribonucleic acid in Escherichia coli starving for nitrogen. Biochim et Biophysica Acta (BBA)-Nucleic Acids and Protein, Synthesis 1966, 119:183-191.
44. Jacobson A, Gillespie D: Metabolic events occurring during recovery from prolonged glucose starvation in Escherichia coli . J Bacteriol 1968, 95:1030-1039.
45. McCarthy B: The effects of magnesium starvation on the ribosome content of Escherichia coli . Biochim Biophys Acta 1962, 55:880-889.
46. Deutscher MP: Degradation of RNA in bacteria: comparison of mRNA and stable RNA. Nucleic Acids Res 2006, 34:659-666.
47. 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.
48. 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:e7002.
49. Dittmar KA, Sørensen MA, Elf J, Ehrenberg M, Pan T: Selective charging of tRNA isoacceptors induced by amino-acid starvation. EMBO Rep 2005, 6:151-157.
50. 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.
51. Bonomo J, Gill RT: Amino acid content of recombinant proteins influences the metabolic burden response. Biotechnol Bioeng 2005, 90:116-126.
52. Elf J, Nilsson D, Tenson T, Ehrenberg M: Selective charging of tRNA isoacceptors explains patterns of codon usage. Science 2003, 300:1718-1722.
53. Wohlgemuth SE, Gorochowski TE, Roubos JA: Translational sensitivity of the Escherichia coli genome to fluctuating tRNA availability. Nucleic Acids Res 2013, 41:8021-8033.
54. Gustafsson C, Govindarajan S, Minshull J: Codon bias and heterologous protein expression. Trends Biotechnol 2004, 22:346-353.
55. Puigbò P, Guzmán E, Romeu A, Garcia-Vallvé S: OPTIMIZER: a web server for optimizing the codon usage of DNA sequences. Nucleic Acids Res 2007, 35:W126-W131.
56. Reuveni S, Meilijson I, Kupiec M, Ruppin E, Tuller T: Genome-scale analysis of translation elongation with a ribosome flow model. PLoS Comput Biol 2011, 7:e1002127.
57. Komar AA: A pause for thought along the co-translational folding pathway. Trends Biochem Sci 2009, 34:16-24.
58. Dubey AK, Baker CS, Romeo T, Babitzke P: RNA sequence and secondary structure participate in high-affinity CsrA-RNA interaction. RNA 2005, 11:1579-1587.
59. Suzuki K, Babitzke P, Kushner SR, Romeo T: Identification of a novel regulatory protein (CsrD) that targets the global regulatory RNAs CsrB and CsrC for degradation by RNase E. Genes Dev 2006, 20:2605-2617.
60. Weilbacher T, Suzuki K, Dubey AK, Wang X, Gudapaty S, Morozov I, Baker CS, Georgellis D, Babitzke P, Romeo T: A novel sRNA component of the carbon storage regulatory system of Escherichia coli . Mol Microbiol 2003, 48:657-670.
61. Richins R, Chen W: Effects of FIS Overexpression on Cell Growth, rRNA Synthesis, and Ribosome Content in Escherichiacoli. Biotechnol Prog 2001, 17:252-257.
62. George H, Powell A, Dahlgren M, Herber W, Maigetter R, Burgess B, Stirdivant S, Greasham R: Physiological effects of TGFα-PE40 expression in recombinant Escherichia coli JM109. Biotechnol Bioeng 1992, 40:437-445.
63. Hoffmann F, Rinas U: On-line estimation of the metabolic burden resulting from the synthesis of plasmid-encoded and heat-shock proteins by monitoring respiratory energy generation. Biotechnol Bioeng 2001, 76:333-340.
64. Hoffmann F, Weber J, Rinas U: Metabolic adaptation of Escherichia coli during temperature-induced recombinant protein production: 1. Readjustment of metabolic enzyme synthesis. Biotechnol Bioeng 2002, 80:313-319.
65. Heyland J, Blank LM, Schmid A: Quantification of metabolic limitations during recombinant protein production in Escherichia coli . J Biotechnol 2011, 155:178-184.
66. Tempest D, Neijssel O: Growth yield and energy distribution. In Escherichia coli and Salmonella typhimurium: cellular and molecular biology American Society for Microbiology. Washington, DC: ; 1987:797-806.
67. Kim HJ, Kwon YD, Lee SY, Kim P: An engineered Escherichia coli having a high intracellular level of ATP and enhanced recombinant protein production. Appl Microbiol Biotechnol 2012, 94:1079-1086.
68. Ingraham J, Maaloe O, Neidhardt FC: Growth of the Bacterial Cell. Sunderland, MA: Sinauer; 1983:381-383.
69. Elf J, Ehrenberg M: Near-Critical Behavior of Aminoacyl-tRNA Pools in E. coli at Rate-Limiting Supply of Amino Acids. Biophys J 2005, 88:132-146.
70. Sorensen H, Mortensen K: Soluble expression of recombinant proteins in the cytoplasm of Escherichia coli . Microb Cell Fact 2005, 4:1.
71. King ZA, Feist AM: Optimizing Cofactor Specificity of Oxidoreductase Enzymes for the Generation of Microbial Production Strains-OptSwap. Ind Biotechnol 2013, 9:236-246.
72. Lakshmanan M, Chung BK, Liu C, Kim SW, Lee DY: Cofactor modification analysis: a computational framework to identify cofactor specificity engineering targets for strain improvement. J Bioinform Comput Biol 2013, 11:1343006.
73. Wang Y, San K-Y, Bennett GN: Cofactor engineering for advancing chemical biotechnology. Curr Opin Biotechnol 2013, 24:994-999.
74. Bastian S, Arnold FH: Reversal of NAD(P)H cofactor dependence by protein engineering. Methods Mol Biol 2012, 834:17-31.
75. Berrios-Rivera SJ, Bennett GN, San KY: Metabolic engineering of Escherichia coli: increase of NADH availability by overexpressing an NAD(+)-dependent formate dehydrogenase. Metab Eng 2002, 4:217-229.
76. Fan Z, Yuan L, Chatterjee R: Increased Hydrogen Production by Genetic Engineering of Escherichia coli . PLoS One 2009, 4:e4432.
77. de Marco A, Deuerling E, Mogk A, Tomoyasu T, Bukau B: Chaperone-based procedure to increase yields of soluble recombinant proteins produced in E. coli. BMC Biotechnol 2007, 7:32.
78. Nannenga BL, Baneyx F: Reprogramming chaperone pathways to improve membrane protein expression in Escherichia coli . Protein Sci 2011, 20:1411-1420.
79. Martin J, Ulrich Hartl F: Chaperone-assisted protein folding. Curr Opin Struct Biol 1997, 7:41-52.
80. Hartl FU, Hayer-Hartl M: Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 2002, 295:1852-1858.
81. Messens J, Collet J-F: Pathways of disulfide bond formation in Escherichia coli . Int J Biochem Cell Biol 2006, 38:1050-1062.
82. Masip L, Pan JL, Haldar S, Penner-Hahn JE, DeLisa MP, Georgiou G, Bardwell JCA, Collet J-F: An Engineered Pathway for the Formation of Protein Disulfide Bonds. Science 2004, 303:1185-1189.
83. Bessette PH, Åslund F, Beckwith J, Georgiou G: Efficient folding of proteins with multiple disulfide bonds in the Escherichia coli cytoplasm. Proc Natl Acad Sci 1999, 96:13703-13708.
84. Hortsch R, Weuster-Botz D: Growth and recombinant protein expression with Escherichia coli in different batch cultivation media. Appl Microbiol Biotechnol 2011, 90:69-76.
85. Lobstein J, Emrich CA, Jeans C, Faulkner M, Riggs P, Berkmen M: SHuffle, a novel Escherichia coli protein expression strain capable of correctly folding disulfide bonded proteins in its cytoplasm. Microb Cell Fact 2012, 11:56-56.
86. Zhan X, Schwaller M, Gilbert HF, Georgiou G: Facilitating the formation of disulfide bonds in the Escherichia coli periplasm via coexpression of yeast protein disulfide isomerase. Biotechnol Prog 1999, 15:1033-1038.
87. Kurokawa Y, Yanagi H, Yura T: Overexpression of Protein Disulfide Isomerase DsbC Stabilizes Multiple-Disulfide-Bonded Recombinant Protein Produced and Transported to the Periplasm in Escherichia coli . Appl Environ Microbiol 2000, 66:3960-3965.
88. Matos CF, Robinson C, Alanen HI, Prus P, Uchida Y, Ruddock LW, Freedman RB, Keshavarz-Moore E: Efficient export of prefolded, disulfide-bonded recombinant proteins to the periplasm by the Tat pathway in Escherichia coli CyDisCo strains. Biotechnol Prog 2014, 30:281-290.
89. Su L, Chen S, Yi L, Woodard R, Chen J, Wu J: Extracellular overexpression of recombinant Thermobifida fusca cutinase by alpha-hemolysin secretion system in E. coli BL21(DE3). Microb Cell Fact 2012, 11:8.
90. Sugamata Y, Shiba T: Improved Secretory Production of Recombinant Proteins by Random Mutagenesis of hlyB, an Alpha-Hemolysin Transporter from Escherichia coli . Appl Environ Microbiol 2005, 71:656-662.
91. Pugsley AP: The complete general secretory pathway in gram-negative bacteria. Microbiol Rev 1993, 57:50.
92. Mergulhao F, Summers D, Monteiro G: Recombinant protein secretion in Escherichia coli . Biotechnol Adv 2005, 23:177-202.
93. Choi J, Lee S: Secretory and extracellular production of recombinant proteins using Escherichia coli . Appl Microbiol Biotechnol 2004, 64:625-635.
94. Liu CC, Schultz PG: Recombinant expression of selectively sulfated proteins in Escherichia coli . Nat Biotechnol 2006, 24:1436-1440.
95. Su L, Xu C, Woodard RW, Chen J, Wu J: A novel strategy for enhancing extracellular secretion of recombinant proteins in Escherichia coli . Appl Microbiol Biotechnol 2013, 97:6705-6713.
96. Douville K, Price A, Eichler J, Economou A, Wickner W: SecYEG and SecA are the stoichiometric components of preprotein translocase. J Biol Chem 1995, 270:20106-20111.
97. Khushoo A, Pal Y, Mukherjee KJ: Optimization of extracellular production of recombinant asparaginase in Escherichia coli in shake-flask and bioreactor. Appl Microbiol Biotechnol 2005, 68:189-197.
98. Khushoo A, Pal Y, Singh BN, Mukherjee KJ: Extracellular expression and single step purification of recombinant Escherichia coli L-asparaginase II. Protein Expr Purif 2004, 38:29-36.
99. Ni Y, Chen R: Extracellular recombinant protein production from Escherichia coli . Biotechnol Lett 2009, 31:1661-1670.
100. Matos CF, Branston SD, Albiniak A, Dhanoya A, Freedman RB, Keshavarz-Moore E, Robinson C: High-yield export of a native heterologous protein to the periplasm by the tat translocation pathway in Escherichia coli . Biotechnol Bioeng 2012, 109:2533-2542.
101. Chung CW, You J, Kim K, Moon Y, Kim H, Ahn JH: Export of recombinant proteins in Escherichia coli using ABC transporter with an attached lipase ABC transporter recognition domain (LARD). Microb Cell Fact 2009, 8:
102. Bentley WE, Mirjalili N, Andersen DC, Davis RH, Kompala DS: Plasmid-encoded protein: the principal factor in the "metabolic burden" associated with recombinant bacteria. Biotechnol Bioeng 1990, 35:668-681.
103. Panda AK, Khan RH, Rao KB, Totey SM: Kinetics of inclusion body production in batch and high cell density fed-batch culture of Escherichia coli expressing ovine growth hormone. J Biotechnol 1999, 75:161-172.
104. Vaiphei ST, Pandey G, Mukherjee KJ: Kinetic studies of recombinant human interferon-gamma expression in continuous cultures of E. coli. J Ind Microbiol Biotechnol 2009, 36:1453-1458.
105. Srivastava P, Mukherjee KJ: Kinetic studies of recombinant human interferon-alpha (rhIFN-α) expression in transient state continuous cultures. Biochem Eng J 2005, 26:50-58.
106. Shin CS, Hong MS, Bae CS, Lee J: Enhanced Production of Human Mini-Proinsulin in Fed-Batch Cultures at High Cell Density of Escherichia coli BL21(DE3) [pET-3aT2M2]. Biotechnol Prog 1997, 13:249-257.
107. Bhattacharya P, Pandey G, Srivastava P, Mukherjee K: Combined effect of protein fusion and signal sequence greatly enhances the production of recombinant human GM-CSF in Escherichia coli . Mol Biotechnol 2005, 30:103-115.
108. Khasa YP, Khushoo A, Mukherjee KJ: Enhancing toxic protein expression in Escherichia coli fed-batch culture using kinetic parameters: Human granulocyte-macrophage colony-stimulating factor as a model system. J Biosci Bioeng 2013, 115:291-297.
109. Yazdani S, Mukherjee K: Continuous-culture studies on the stability and expression of recombinant streptokinase in Escherichia coli . Bioprocess Biosyst Eng 2002, 24:341-346.
110. Balagurunathan B, Jayaraman G: Cellular response to accumulation of recombinant proteins in the E. coli inner membrane: Implications for proteolysis and productivity of the secretory expression system. Biochem Eng J 2008, 39:74-83.
111. Khasa YP, Khushoo A, Tapryal S, Mukherjee K: Optimization of Human Granulocyte Macrophage-Colony Stimulating Factor (hGM-CSF) Expression Using Asparaginase and Xylanase Gene's Signal Sequences in Escherichia coli . Appl Biochem Biotechnol 2011, 165:523-537.
112. Ramalingam S, Gautam P, Mukherjee KJ, Jayaraman G: Effects of post-induction feed strategies on secretory production of recombinant streptokinase in Escherichia coli . Biochem Eng J 2007, 33:34-41.
113. Marisch K, Bayer K, Scharl T, Mairhofer J, Krempl PM, Hummel K, Razzazi-Fazeli E, Striedner G: A Comparative Analysis of Industrial Escherichia coli K-12 and B Strains in High-Glucose Batch Cultivations on Process-, Transcriptome-and Proteome Level. PloS one 2013, 8:e70516.
114. Carneiro S, Ferreira EC, Rocha I: Metabolic responses to recombinant bioprocesses in Escherichia coli . J Biotechnol 2013, 164:396-408.
115. Enfors SO: Physiological Stress Responses in Bioprocesses. Springer; 2004.
116. Sharma AK, Mahalik S, Ghosh C, Singh AB, Mukherjee KJ: Comparative transcriptomic profile analysis of fed-batch cultures expressing different recombinant proteins in Escherichia coli . AMB express 2011, 1:33.
117. Fong B, Wood D: Expression and purification of ELP-intein-tagged target proteins in high cell density E. coli fermentation. Microb Cell Fact 2010, 9:77.
118. Losen M, Frölich B, Pohl M, Büchs J: Effect of Oxygen Limitation and Medium Composition on Escherichia coli Fermentation in Shake-Flask Cultures. Biotechnol Prog 2004, 20:1062-1068.
119. Saraswat V, Kim DY, Lee J, Park Y: Effect of specific production rate of recombinant protein on multimerization of plasmid vector and gene expression level. FEMS Microbiol Lett 1999, 179:367-373.
120. Hellmuth K, Korz DJ, Sanders EA, Deckwer WD: Effect of growth rate on stability and gene expression of recombinant plasmids during continuous and high cell density cultivation of Escherichia coli TG1. J Biotechnol 1994, 32:289-298.
121. Singh AB, Sharma AK, Mukherjee KJ: Analyzing the metabolic stress response of recombinant Escherichia coli cultures expressing human interferon-beta in high cell density fed batch cultures using time course transcriptomic data. Mol Biosyst 2012, 8:615-628.
122. Baig F, Fernando LP, Salazar MA, Powell RR, Bruce TF, Harcum SW: Dynamic transcriptional response of Escherichia coli to inclusion body formation. Biotechnol Bioeng 2014, 111:980-999.
123. Lesley SA, Graziano J, Cho CY, Knuth MW, Klock HE: Gene expression response to misfolded protein as a screen for soluble recombinant protein. Protein Eng 2002, 15:153-160.
124. Smith HE: The transcriptional response of Escherichia coli to recombinant protein insolubility. J Struct Funct Genomics 2007, 8:27-35.
125. Bordbar A, Monk JM, King ZA, Palsson BO: Constraint-based models predict metabolic and associated cellular functions. Nat Rev Genet 2014, 15:107-120.
126. Orth JD, Thiele I, Palsson BO: What is flux balance analysis? Nat Biotechnol 2010, 28:245-248.
127. Orth JD, Palsson B: Gap-filling analysis of the iJO1366 Escherichia coli metabolic network reconstruction for discovery of metabolic functions. BMC Syst Biol 2012, 6:30.
128. Feist AM, Henry CS, Reed JL, Krummenacker M, Joyce AR, Karp PD, Broadbelt LJ, Hatzimanikatis V, Palsson BØ: A genome-scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information. Mol Syst Biol 2007, 3.
129. Covert MW, Palsson BØ: Transcriptional regulation in constraints-based metabolic models of Escherichia coli . J Biol Chem 2002, 277:28058-28064.
130. Covert MW, Xiao N, Chen TJ, Karr JR: Integrating metabolic, transcriptional regulatory and signal transduction models in Escherichia coli . Bioinformatics 2008, 24:2044-2050.
131. Kim J, Reed JL: OptORF: Optimal metabolic and regulatory perturbations for metabolic engineering of microbial strains. BMC Syst Biol 2010, 4:53.
132. Shlomi T, Berkman O, Ruppin E: Regulatory on/off minimization of metabolic flux changes after genetic perturbations. Proc Natl Acad Sci U S A 2005, 102:7695-7700.
133. Singh AB, Mukherjee KJ: Supplementation of substrate uptake gene enhances the expression of rhIFN-beta in high cell density fed-batch cultures of Escherichia coli . Mol Biotechnol 2013, 54:692-702.
134. Choi JH, Lee SJ, Lee SJ, Lee SY: Enhanced Production of Insulin-Like Growth Factor I Fusion Protein in Escherichia coli by Coexpression of the Down-Regulated Genes Identified by Transcriptome Profiling. Appl Environ Microbiol 2003, 69:4737-4742.
135. Chang DE, Shin S, Rhee JS, Pan JG: Acetate metabolism in a pta mutant of Escherichia coli W3110: importance of maintaining acetyl coenzyme A flux for growth and survival. J Bacteriol 1999, 181:6656-6663.
136. Chou CH, Bennett GN, San KY: Effect of modified glucose uptake using genetic engineering techniques on high-level recombinant protein production in Escherichia coli dense cultures. Biotechnol Bioeng 1994, 44:952-960.
137. De Anda R, Lara AR, Hernandez V, Hernandez-Montalvo V, Gosset G, Bolivar F, Ramirez OT: Replacement of the glucose phosphotransferase transport system by galactose permease reduces acetate accumulation and improves process performance of Escherichia coli for recombinant protein production without impairment of growth rate. Metab Eng 2006, 8:281-290.
138. Dittrich CR, Vadali RV, Bennett GN, San KY: Redistribution of metabolic fluxes in the central aerobic metabolic pathway of E. coli mutant strains with deletion of the ackA-pta and poxB pathways for the synthesis of isoamyl acetate. Biotechnol Prog 2005, 21:627-631.
139. Flores S, de Anda-Herrera R, Gosset G, Bolivar FG: Growth-rate recovery of Escherichia coli cultures carrying a multicopy plasmid, by engineering of the pentose-phosphate pathway. Biotechnol Bioeng 2004, 87:485-494.
140. Yang YT, Bennett GN, San KY: Effect of inactivation of nuo and ackA-pta on redistribution of metabolic fluxes in Escherichia coli . Biotechnol Bioeng 1999, 65:291-297.
141. Brown L, Gentry D, Elliott T, Cashel M: DksA affects ppGpp induction of RpoS at a translational level. J Bacteriol 2002, 184:4455-4465.
142. Dedhia N, Richins R, Mesina A, Chen W: Improvement in recombinant protein production in ppGpp-deficient Escherichia coli . Biotechnol Bioeng 1997, 53:379-386.
143. Jeong KJ, Choi JH, Yoo WM, Keum KC, Yoo NC, Lee SY, Sung MH: Constitutive production of human leptin by fed-batch culture of recombinant rpoS- Escherichia coli . Protein Expr Purif 2004, 36:150-156.
144. Rahman M, Hasan MR, Oba T, Shimizu K: Effect of rpoS gene knockout on the metabolism of Escherichia coli during exponential growth phase and early stationary phase based on gene expressions, enzyme activities and intracellular metabolite concentrations. Biotechnol Bioeng 2006, 94:585-595.
145. Waegeman H, Soetaert W: Increasing recombinant protein production in Escherichia coli through metabolic and genetic engineering. J Ind Microbiol Biotechnol 2011, 38:1891-1910.
146. Rowe DC, Summers DK: The quiescent-cell expression system for protein synthesis in Escherichia coli . Appl Environ Microbiol 1999, 65:2710-2715.
147. Mukherjee K, Rowe D, Watkins N, Summers D: Studies of single-chain antibody expression in quiescent Escherichia coli . Appl Environ Microbiol 2004, 70:3005-3012.
148. Chant EL, Summers DK: Indole signalling contributes to the stable maintenance of Escherichia coli multicopy plasmids. Mol Microbiol 2007, 63:35-43.
149. Lee JH, Lee J: Indole as an intercellular signal in microbial communities. FEMS Microbiol Rev 2010, 34:426-444.
150. Bury-Mone S, Nomane Y, Reymond N, Barbet R, Jacquet E, Imbeaud S, Jacq A, Bouloc P: Global analysis of extracytoplasmic stress signaling in Escherichia coli . PLoS Genet 2009, 5:e1000651.
151. Garbe TR, Kobayashi M, Yukawa H: Indole-inducible proteins in bacteria suggest membrane and oxidant toxicity. Arch Microbiol 2000, 173:78-82.
152. Huang LC, Wood EA, Cox MM: Convenient and reversible site-specific targeting of exogenous DNA into a bacterial chromosome by use of the FLP recombinase: the FLIRT system. J Bacteriol 1997, 179:6076-6083.
153. De Mey M, Maertens J, Boogmans S, Soetaert WK, Vandamme EJ, Cunin R, Foulquie-Moreno MR: Promoter knock-in: a novel rational method for the fine tuning of genes. BMC Biotechnol 2010, 10:26.
154. Alper H, Fischer C, Nevoigt E, Stephanopoulos G: Tuning genetic control through promoter engineering. Proc Natl Acad Sci U S A 2005, 102:12678-12683.
155. Datsenko KA, Wanner BL: One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci 2000, 97:6640-6645.
156. Marx CJ, Lidstrom ME: Broad-host-range cre-lox system for antibiotic marker recycling in gram-negative bacteria. Biotechniques 2002, 33:1062-1067.
157. Yang J, Sun B, Huang H, Jiang Y, Diao L, Chen B, Xu C, Wang X, Liu J, Jiang W: High-Efficiency Scarless Genetic Modification in Escherichia coli by Using Lambda Red Recombination and I-SceI Cleavage. Appl Environ Microbiol 2014, 80:3826-3834.
158. McCloskey D, Palsson BØ, Feist AM: Basic and applied uses of genome-scale metabolic network reconstructions of Escherichia coli . Mol Syst Biol 2013, 9:661.
159. Chemler JA, Fowler ZL, McHugh KP, Koffas MA: Improving NADPH availability for natural product biosynthesis in Escherichia coli by metabolic engineering. Metab Eng 2010, 12:96-104.
160. Ryu YS, Biswas RK, Shin K, Parisutham V, Kim SM, Lee SK: A simple and effective method for construction of Escherichia coli strains proficient for genome engineering. PLoS One 2014, 9:e94266.
161. Jeong J, Cho N, Jung D, Bang D: Genome-scale genetic engineering in Escherichia coli . Biotechnol Adv 2013, 31:804-810.
162. Donath MJ, Dominguez MA, Withers ST: Development of an automated platform for high-throughput P1-phage transduction of Escherichia coli . J Association for Laboratory Automation 2011, 16:141-147.
163. Kim HJ, Hou BK, Lee SG, Kim JS, Lee D-W, Lee SJ: Genome-wide analysis of redox reactions reveals metabolic engineering targets for d-lactate overproduction in Escherichia coli . Metab Eng 2013, 18:44-52.
164. Chin JW, Cirino PC: Strain engineering strategies for improving whole-cell biocatalysis: engineering Escherichia coli to overproduce xylitol as an example. In Nanoscale Biocatalysis.: Springer; 2011:185-203.
165. Meynial-Salles I, Soucaille P: Creation of new metabolic pathways or improvement of existing metabolic enzymes by in vivo evolution in Escherichia coli. In Microbial Metabolic Engineering.: Springer; 2012:75-86.
166. Zhu J, Sanchez A, Bennett GN, San K-Y: Manipulating respiratory levels in Escherichia coli for aerobic formation of reduced chemical products. Metab Eng 2011, 13:704-712.
167. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H: Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2006, 2:2006-0008.
168. Link AJ, Phillips D, Church GM: Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: application to open reading frame characterization. J Bacteriol 1997, 179:6228-6237.
169. Na D, Yoo SM, Chung H, Park H, Park JH, Lee SY: Metabolic engineering of Escherichia coli using synthetic small regulatory RNAs. Nat Biotechnol 2013, 31:170-174.
170. Wang HH, Isaacs FJ, Carr PA, Sun ZZ, Xu G, Forest CR, Church GM: Programming cells by multiplex genome engineering and accelerated evolution. Nature 2009, 460:894-898.
171. Warner JR, Reeder PJ, Karimpour-Fard A, Woodruff LB, Gill RT: Rapid profiling of a microbial genome using mixtures of barcoded oligonucleotides. Nat Biotechnol 2010, 28:856-862.
172. Yoo SM, Na D, Lee SY: Design and use of synthetic regulatory small RNAs to control gene expression in Escherichia coli . Nat Protoc 2013, 8:1694-1707.
173. Waegeman H, De Lausnay S, Beauprez J, Maertens J, De Mey M, Soetaert W: Increasing recombinant protein production in Escherichia coli K12 through metabolic engineering. N Biotechnol 2013, 30:255-261.
174. Lajoie MJ, Rovner AJ, Goodman DB, Aerni HR, Haimovich AD, Kuznetsov G, Mercer JA, Wang HH, Carr PA, Mosberg JA, Rohland N, Schultz PG, Jacobson JM, Rinehart J, Church GM, Isaacs FJ: Genomically recoded organisms expand biological functions. Science 2013, 342:357-360.
175. Isaacs FJ, Carr PA, Wang HH, Lajoie MJ, Sterling B, Kraal L, Tolonen AC, Gianoulis TA, Goodman DB, Reppas NB, Emig CJ, Bang D, Hwang SJ, Jewett MC, Jacobson JM, Church GM: Precise Manipulation of Chromosomes in Vivo Enables Genome-Wide Codon Replacement. Science 2011, 333:348-353.
176. Pal C, Papp B, Posfai G: The dawn of evolutionary genome engineering. Nat Rev Genet 2014, 15:504-512.
177. Shoemaker DD, Lashkari DA, Morris D, Mittmann M, Davis RW: Quantitative phenotypic analysis of yeast deletion mutants using a highly parallel molecular bar-coding strategy. Nat Genet 1996, 14:450-456.
178. Ghosh C, Gupta R, Mukherjee KJ: An inverse metabolic engineering approach for the design of an improved host platform for over-expression of recombinant proteins in Escherichia coli . Microb Cell Fact 2012, 11:93.
179. Crameri A, Whitehorn EA, Tate E, Stemmer WP: Improved green fluorescent protein by molecular evolution using DNA shuffling. Nat Biotechnol 1996, 14:315-319.
180. Maksimow M, Hakkila K, Karp M, Virta M: Simultaneous detection of bacteria expressing GFP and DsRed genes with a flow cytometer. Cytometry 2002, 47:243-247.
181. Cormack BP, Valdivia RH, Falkow S: FACS-optimized mutants of the green fluorescent protein (GFP). Gene 1996, 173:33-38.
182. Lissemore JL, Jankowski JT, Thomas CB, Mascotti DP, De Haseth PL: Green fluorescent protein as a quantitative reporter of relative promoter activity in E. coli. Biotechniques 2000, 28:82-84. 86, 88-89.
183. Burke C, Liu M, Britton W, Triccas JA, Thomas T, Smith AL, Allen S, Salomon R, Harry E: Harnessing single cell sorting to identify cell division genes and regulators in bacteria. PLoS One 2013, 8:e60964.
184. Kensy F, Engelbrecht C, Buchs J: Scale-up from microtiter plate to laboratory fermenter: evaluation by online monitoring techniques of growth and protein expression in Escherichia coli and Hansenula polymorpha fermentations. Microb Cell Fact 2009, 8:68.
185. Kensy F, Zang E, Faulhammer C, Tan RK, Buchs J: Validation of a high-throughput fermentation system based on online monitoring of biomass and fluorescence in continuously shaken microtiter plates. Microb Cell Fact 2009, 8:31.
186. Fernandez-Ricaud L, Warringer J, Ericson E, Glaab K, Davidsson P, Nilsson F, Kemp GJ, Nerman O, Blomberg A: PROPHECY-a yeast phenome database, update 2006. Nucleic Acids Res 2007, 35:D463-D467.
187. Fong SS, Marciniak JY, Palsson BO: Description and interpretation of adaptive evolution of Escherichia coli K-12 MG1655 by using a genome-scale in silico metabolic model. J Bacteriol 2003, 185:6400-6408.
188. Jasnos L, Korona R: Epistatic buffering of fitness loss in yeast double deletion strains. Nat Genet 2007, 39:550-554.
189. Korch SB, Henderson TA, Hill TM: Characterization of the hipA7 allele of Escherichia coli and evidence that high persistence is governed by (p)ppGpp synthesis. Mol Microbiol 2003, 50:1199-1213.
190. Warringer J, Ericson E, Fernandez L, Nerman O, Blomberg A: High-resolution yeast phenomics resolves different physiological features in the saline response. Proc Natl Acad Sci U S A 2003, 100:15724-15729.
191. Bareither R, Pollard D: A review of advanced small-scale parallel bioreactor technology for accelerated process development: current state and future need. Biotechnol Prog 2011, 27:2-14.
192. Blomberg A: Measuring growth rate in high-throughput growth phenotyping. Curr Opin Biotechnol 2011, 22:94-102.
193. Klockner W, Buchs J: Advances in shaking technologies. Trends Biotechnol 2012, 30:307-314.
194. Suresh S, Srivastava VC, Mishra IM: Techniques for oxygen transfer measurement in bioreactors: a review. J Chem Technol Biotechnol 2009, 84:1091-1103.
195. Duetz WA: Microtiter plates as mini-bioreactors: miniaturization of fermentation methods. Trends Microbiol 2007, 15:469-47.