Recombinant protein expression in Escherichia coli: advances and challenges

Germán L. Rosano1, Eduardo A. Ceccarelli1
1Instituto de Biología Molecular y Celular de Rosario, Consejo Nacional de Investigaciones Científicas y Técnicas Rosario, Argentina ; Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario Rosario, Argentina.

Tóm tắt

Từ khóa


Tài liệu tham khảo

Adrio, 2010, Recombinant organisms for production of industrial products., Bioeng. Bugs, 1, 116, 10.4161/bbug.1.2.10484

Alibolandi, 2011, Chemical assistance in refolding of bacterial inclusion bodies., Biochem. Res. Int., 2011:, 10.1155/2011/631607

Andreev, 2010, Cyanogen bromide cleavage of proteins in salt and buffer solutions., Anal. Biochem., 407, 144, 10.1016/j.ab.2010.07.023

Angov, 2011, Adjustment of codon usage frequencies by codon harmonization improves protein expression and folding., Methods Mol. Biol., 705, 1, 10.1007/978-1-61737-967-3_1

Atlas, 2004, Handbook of Microbiological Media, 3rd Edn.

Baker, 1996, Protein expression using ubiquitin fusion and cleavage., Curr. Opin. Biotechnol., 7, 541, 10.1016/S0958-1669(96)80059-0

Baldwin, 1986, Temperature dependence of the hydrophobic interaction in protein folding., Proc. Natl. Acad. Sci. U.S.A., 83, 8069, 10.1073/pnas.83.21.8069

Baneyx, 1999, Recombinant protein expression in Escherichia coli., Curr. Opin. Biotechnol., 10, 411, 10.1016/S0958-1669(99)00003-8

Banki, 2005, Simple bioseparations using self-cleaving elastin-like polypeptide tags., Nat. Methods, 2, 659, 10.1038/nmeth787

Basu, 2011, Refolding of proteins from inclusion bodies: rational design and recipes., Appl. Microbiol. Biotechnol., 92, 241, 10.1007/s00253-011-3513-y

Bentley, 1990, Plasmid-encoded protein: the principal factor in the “metabolic burden” associated with recombinant bacteria., Biotechnol. Bioeng., 35, 668, 10.1002/bit.260350704

Bessette, 1999, Efficient folding of proteins with multiple disulfide bonds in the Escherichia coli cytoplasm., Proc. Natl. Acad. Sci. U.S.A., 96, 13703, 10.1073/pnas.96.24.13703

Bird, 2011, High throughput construction and small scale expression screening of multi-tag vectors in Escherichia coli., Methods, 55, 29, 10.1016/j.ymeth.2011.08.002

Birnbaum, 1991, Plasmid presence changes the relative levels of many host cell proteins and ribosome components in recombinant Escherichia coli., Biotechnol. Bioeng., 37, 736, 10.1002/bit.260370808

Blommel, 2007, Enhanced bacterial protein expression during auto-induction obtained by alteration of lac repressor dosage and medium composition., Biotechnol. Prog., 23, 585, 10.1021/bp070011x

Blommel, 2007, A combined approach to improving large-scale production of tobacco etch virus protease., Protein Expr. Purif., 55, 53, 10.1016/j.pep.2007.04.013

Bolivar, 1977, Construction and characterization of new cloning vehicles. II. A multipurpose cloning system., Gene, 2, 95, 10.1016/0378-1119(77)90000-2

Bornhorst, 2000, Purification of proteins using polyhistidine affinity tags., Methods Enzymol., 326, 245, 10.1016/S0076-6879(00)26058-8

Braun, 2003, High throughput protein production for functional proteomics., Trends Biotechnol., 21, 383, 10.1016/S0167-7799(03)00189-6

Buchan, 2007, Halting a cellular production line: responses to ribosomal pausing during translation., Biol. Cell, 99, 475, 10.1042/BC20070037

Bucher, 2002, Differential effects of short affinity tags on the crystallization of Pyrococcus furiosus maltodextrin-binding protein., Acta Crystallogr. D. Biol. Crystallogr., 58, 392, 10.1107/S0907444901021187

Burgess, 2009, Refolding solubilized inclusion body proteins., Methods Enzymol., 463, 259, 10.1016/S0076-6879(09)63017-2

Burgess-Brown, 2008, Codon optimization can improve expression of human genes in Escherichia coli: a multi-gene study., Protein Expr. Purif., 59, 94, 10.1016/j.pep.2008.01.008

Busso, 2008, A comparison of inoculation methods to simplify recombinant protein expression screening in Escherichia coli., Biotechniques, 44, 101, 10.2144/000112632

Butt, 2005, SUMO fusion technology for difficult-to-express proteins., Protein Expr. Purif., 43, 1, 10.1016/j.pep.2005.03.016

Calos, 1978, DNA sequence for a low-level promoter of the lac repressor gene and an ‘up’ promoter mutation., Nature, 274, 762, 10.1038/274762a0

Campbell, 1978, Genetic recombination and complementation between bacteriophage T7 and cloned fragments of T7 DNA., Proc. Natl. Acad. Sci. U.S.A., 75, 2276, 10.1073/pnas.75.5.2276

Camps, 2010, Modulation of ColE1-like plasmid replication for recombinant gene expression., Recent Pat. DNA Gene Seq., 4, 58, 10.2174/187221510790410822

Carrio, 2001, Protein aggregation as bacterial inclusion bodies is reversible., FEBS Lett., 489, 29, 10.1016/S0014-5793(01)02073-7

Carrio, 2002, Construction and deconstruction of bacterial inclusion bodies., J. Biotechnol., 96, 3, 10.1016/S0168-1656(02)00032-9

Carson, 2007, His-tag impact on structure., Acta Crystallogr. D. Biol. Crystallogr., 63, 295, 10.1107/S0907444906052024

Caspers, 1994, Overproduction of bacterial chaperones improves the solubility of recombinant protein tyrosine kinases in Escherichia coli., Cell. Mol. Biol. (Noisy-le-grand), 40, 635

Chang, 1978, Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid., J. Bacteriol., 134, 1141, 10.1128/JB.134.3.1141-1156.1978

Chant, 2005, Attachment of a histidine tag to the minimal zinc finger protein of the Aspergillus nidulans gene regulatory protein AreA causes a conformational change at the DNA-binding site., Protein Expr. Purif., 39, 152, 10.1016/j.pep.2004.10.017

Choi, 2006, Production of recombinant proteins by high cell density culture of Escherichia coli., Chem. Eng. Sci., 61, 10.1016/j.ces.2005.03.031

Choi, 2004, Secretory and extracellular production of recombinant proteins using Escherichia coli., Appl. Microbiol. Biotechnol., 64, 625, 10.1007/s00253-004-1559-9

Chu, 2014, Translation elongation can control translation initiation on eukaryotic mRNAs., EMBO J., 33, 21, 10.1002/embj.201385651

Clark, 1998, Refolding of recombinant proteins., Curr. Opin. Biotechnol, 9, 157, 10.1016/S0958-1669(98)80109-2

Corchero, 1998, Plasmid maintenance in Escherichia coli recombinant cultures is dramatically, steadily, and specifically influenced by features of the encoded proteins., Biotechnol. Bioeng., 58, 625, 10.1002/(SICI)1097-0290(19980620)58:6625::AID-BIT83.0.CO;2-K

Costa, 2013, 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., 97, 6779, 10.1007/s00253-012-4559-1

Cui, 2006, Optimization of the medium composition for production of mycelial biomass and exo-polymer by Grifola frondosa GF9801 using response surface methodology., Bioresour. Technol., 97, 1209, 10.1016/j.biortech.2005.05.005

Daegelen, 2009, Tracing ancestors and relatives of Escherichia coli B, and the derivation of B strains REL606 and BL21(DE3)., J. Mol. Biol., 394, 634, 10.1016/j.jmb.2009.09.022

Davis, 1999, New fusion protein systems designed to give soluble expression in Escherichia coli., Biotechnol. Bioeng., 65, 382, 10.1002/(SICI)1097-0290(19991120)65:4382::AID-BIT23.0.CO;2-I

de Boer, 1983, The tac promoter: a functional hybrid derived from the trp and lac promoters., Proc. Natl. Acad. Sci. U.S.A., 80, 21, 10.1073/pnas.80.1.21

del Solar, 2000, Plasmid copy number control: an ever-growing story., Mol. Microbiol., 37, 492, 10.1046/j.1365-2958.2000.02005.x

del Solar, 1998, Replication and control of circular bacterial plasmids., Microbiol. Mol. Biol. Rev., 62, 434, 10.1128/MMBR.62.2.434-464.1998

Demain, 2009, Production of recombinant proteins by microbes and higher organisms., Biotechnol. Adv., 27, 297, 10.1016/j.biotechadv.2009.01.008

de Marco, 2009, Strategies for successful recombinant expression of disulfide bond-dependent proteins in Escherichia coli., Microb. Cell Fact., 8, 10.1186/1475-2859-8-26

de Marco, 2004, Bacteria co-transformed with recombinant proteins and chaperones cloned in independent plasmids are suitable for expression tuning., J. Biotechnol., 109, 45, 10.1016/j.jbiotec.2003.10.025

de Marco, 2007, Chaperone-based procedure to increase yields of soluble recombinant proteins produced in E. coli., BMC Biotechnol., 7:, 10.1186/1472-6750-7-32

de Marco, 2005, Native folding of aggregation-prone recombinant proteins in Escherichia coli by osmolytes, plasmid- or benzyl alcohol-overexpressed molecular chaperones., Cell Stress Chaperones, 10, 329, 10.1379/CSC-139R.1

Derman, 1993, Mutations that allow disulfide bond formation in the cytoplasm of Escherichia coli., Science, 262, 1744, 10.1126/science.8259521

Deuschle, 1986, Promoters of Escherichia coli: a hierarchy of in vivo strength indicates alternate structures., EMBO J., 5, 2987, 10.1002/j.1460-2075.1986.tb04596.x

Dodd, 2005, Revisited gene regulation in bacteriophage lambda., Curr. Opin. Genet. Dev., 15, 145, 10.1016/j.gde.2005.02.001

Doherty, 1993, Overproduction of the toxic protein, bovine pancreatic DNaseI, in Escherichia coli using a tightly controlled T7-promoter-based vector., Gene, 136, 337, 10.1016/0378-1119(93)90491-K

Dong, 1995, Gratuitous overexpression of genes in Escherichia coli leads to growth inhibition and ribosome destruction., J. Bacteriol., 177, 1497, 10.1128/jb.177.6.1497-1504.1995

Dubendorff, 1991, Controlling basal expression in an inducible T7 expression system by blocking the target T7 promoter with lac repressor., J. Mol. Biol., 219, 45, 10.1016/0022-2836(91)90856-2

Dumon-Seignovert, 2004, The toxicity of recombinant proteins in Escherichia coli: a comparison of overexpression in BL21(DE3), C41(DE3), and C43(DE3)., Protein Expr. Purif., 37, 203, 10.1016/j.pep.2004.04.025

Epstein, 1975, Adenosine 3‣:5‣-cyclic monophosphate as mediator of catabolite repression in Escherichia coli., Proc. Natl. Acad. Sci. U.S.A., 72, 2300, 10.1073/pnas.72.6.2300

Esposito, 2006, Enhancement of soluble protein expression through the use of fusion tags., Curr. Opin. Biotechnol., 17, 353, 10.1016/j.copbio.2006.06.003

Fernandez-Castane, 2012, Evidencing the role of lactose permease in IPTG uptake by Escherichia coli in fed-batch high cell density cultures., J. Biotechnol., 157, 391, 10.1016/j.jbiotec.2011.12.007

Ferrer, 2003, Chaperonins govern growth of Escherichia coli at low temperatures., Nat. Biotechnol., 21, 1266, 10.1038/nbt1103-1266

Ferrer, 2004, Functional consequences of single: double ring transitions in chaperonins: life in the cold., Mol. Microbiol., 53, 167, 10.1111/j.1365-2958.2004.04077.x

Fong, 2010, Expression and purification of ELP-intein-tagged target proteins in high cell density E. coli fermentation., Microb. Cell Fact., 9, 10.1186/1475-2859-9-77

Galkin, 2009, Cleavage of bacteriophage lambda cI repressor involves the RecA C-terminal domain., J. Mol. Biol., 385, 779, 10.1016/j.jmb.2008.10.081

Galloway, 2003, Increasing the yield of soluble recombinant protein expressed in E. coli by induction during late log phase., Biotechniques, 34, 524, 10.2144/03343st04

Gao, 2004, UpGene: application of a web-based DNA codon optimization algorithm., Biotechnol. Prog., 20, 443, 10.1021/bp0300467

Ge, 2005, Self-cleavable stimulus responsive tags for protein purification without chromatography., J. Am. Chem. Soc., 127, 11228, 10.1021/ja0531125

Georgiou, 2005, Preparative expression of secreted proteins in bacteria: status report and future prospects., Curr. Opin. Biotechnol., 16, 538, 10.1016/j.copbio.2005.07.008

Goldstein, 1995, Prokaryotic promoters in biotechnology., Biotechnol. Annu. Rev., 1, 105, 10.1016/S1387-2656(08)70049-8

Gonzalez-Montalban, 2007, Recombinant protein solubility - does more mean better?, Nat. Biotechnol., 25, 718, 10.1038/nbt0707-718

Goodman, 2013, Causes and effects of N-terminal codon bias in bacterial genes., Science, 342, 475, 10.1126/science.1241934

Gottesman, 1996, Proteases and their targets in Escherichia coli., Annu. Rev. Genet., 30, 465, 10.1146/annurev.genet.30.1.465

Graumann, 2006, Manufacturing of recombinant therapeutic proteins in microbial systems., Biotechnol. J., 1, 164, 10.1002/biot.200500051

Grodberg, 1988, ompT encodes the Escherichia coli outer membrane protease that cleaves T7 RNA polymerase during purification., J. Bacteriol., 170, 1245, 10.1128/jb.170.3.1245-1253.1988

Gustafsson, 2004, Codon bias and heterologous protein expression., Trends Biotechnol., 22, 346, 10.1016/j.tibtech.2004.04.006

Guzman, 1995, Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter., J. Bacteriol., 177, 4121, 10.1128/jb.177.14.4121-4130.1995

Hammarstrom, 2002, Rapid screening for improved solubility of small human proteins produced as fusion proteins in Escherichia coli., Protein Sci., 11, 313, 10.1110/ps.22102

Hammarstrom, 2006, Effect of N-terminal solubility enhancing fusion proteins on yield of purified target protein., J. Struct. Funct. Genomics, 7, 1, 10.1007/s10969-005-9003-7

Hartl, 2002, Molecular chaperones in the cytosol: from nascent chain to folded protein., Science, 295, 1852, 10.1126/science.1068408

Hartley, 1988, Properties of inclusion bodies from recombinant Escherichia coli., Biochem. Soc. Trans., 16, 101, 10.1042/bst0160101

Hayashi, 2008, pCold-GST vector: a novel cold-shock vector containing GST tag for soluble protein production., Protein Expr. Purif., 62, 120, 10.1016/j.pep.2008.07.007

Hopp, 1988, A short polypeptide marker sequence useful for recombinant protein identification and purification., Nat. Biotechnol., 6, 1204, 10.1038/nbt1088-1204

Huber, 2009, Equalizing growth in high-throughput small scale cultivations via precultures operated in fed-batch mode., Biotechnol. Bioeng., 103, 1095, 10.1002/bit.22349

Hwang, 2014, Targeted expression, purification, and cleavage of fusion proteins from inclusion bodies in Escherichia coli., FEBS Lett., 588, 247, 10.1016/j.febslet.2013.09.028

Itakura, 1977, Expression in Escherichia coli of a chemically synthesized gene for the hormone somatostatin., Science, 198, 1056, 10.1126/science.412251

Jana, 2005, Strategies for efficient production of heterologous proteins in Escherichia coli., Appl. Microbiol. Biotechnol., 67, 289, 10.1007/s00253-004-1814-0

Jayaraj, 2005, GeMS: an advanced software package for designing synthetic genes., Nucleic Acids Res., 33, 3011, 10.1093/nar/gki614

Jenny, 2003, A critical review of the methods for cleavage of fusion proteins with thrombin and factor Xa., Protein Expr. Purif., 31, 1, 10.1016/S1046-5928(03)00168-2

Johnson, 1981, lambda Repressor and cro – components of an efficient molecular switch., Nature, 294, 217, 10.1038/294217a0

Kane, 1995, Effects of rare codon clusters on high-level expression of heterologous proteins in Escherichia coli., Curr. Opin. Biotechnol., 6, 494, 10.1016/0958-1669(95)80082-4

Kapust, 2002, The P1‣ specificity of tobacco etch virus protease., Biochem. Biophys. Res. Commun., 294, 949, 10.1016/S0006-291X(02)00574-0

Kapust, 1999, Escherichia coli maltose-binding protein is uncommonly effective at promoting the solubility of polypeptides to which it is fused., Protein Sci., 8, 1668, 10.1110/ps.8.8.1668

Khan, 2012, Histidine affinity tags affect MSP1(42) structural stability and immunodominance in mice., Biotechnol. J., 7, 133, 10.1002/biot.201100331

Khlebnikov, 2002, Effect of lacY expression on homogeneity of induction from the P(tac) and P(trc) promoters by natural and synthetic inducers., Biotechnol. Prog., 18, 672, 10.1021/bp010141k

Klose, 2004, Hexa-histidin tag position influences disulfide structure but not binding behavior of in vitro folded N-terminal domain of rat corticotropin-releasing factor receptor type 2a., Protein Sci., 13, 2470, 10.1110/ps.04835904

Korpimaki, 2003, Surprisingly fast disappearance of beta-lactam selection pressure in cultivation as detected with novel biosensing approaches., J. Microbiol. Methods, 53, 37, 10.1016/S0167-7012(02)00213-0

Kroll, 2010, Plasmid addiction systems: perspectives and applications in biotechnology., Microb. Biotechnol., 3, 634, 10.1111/j.1751-7915.2010.00170.x

Kurokawa, 2000, Overexpression of protein disulfide isomerase DsbC stabilizes multiple-disulfide-bonded recombinant protein produced and transported to the periplasm in Escherichia coli., Appl. Environ. Microbiol., 66, 3960, 10.1128/AEM.66.9.3960-3965.2000

Lanzer, 1988, Promoters largely determine the efficiency of repressor action., Proc. Natl. Acad. Sci. U.S.A., 85, 8973, 10.1073/pnas.85.23.8973

LaVallie, 1993, A thioredoxin gene fusion expression system that circumvents inclusion body formation in the E. coli cytoplasm., Biotechnology (N. Y.), 11, 187, 10.1038/nbt0293-187

Lee, 2006, Absolute and relative QPCR quantification of plasmid copy number in Escherichia coli., J. Biotechnol., 123, 273, 10.1016/j.jbiotec.2005.11.014

Lee, 1996, High cell-density culture of Escherichia coli., Trends Biotechnol., 14, 98, 10.1016/0167-7799(96)80930-9

Lewin, 1989, 4-quinolones and the SOS response., J. Med. Microbiol., 29, 139, 10.1099/00222615-29-2-139

Li, 2012, The anti-Shine–Dalgarno sequence drives translational pausing and codon choice in bacteria., Nature, 484, 538, 10.1038/nature10965

Lin-Chao, 1986, Effect of the bacterial growth rate on replication control of plasmid pBR322 in Escherichia coli., Mol. Gen. Genet., 203, 143, 10.1007/BF00330395

Lobstein, 2012, SHuffle, a novel Escherichia coli protein expression strain capable of correctly folding disulfide bonded proteins in its cytoplasm., Microb. Cell Fact., 11, 10.1186/1475-2859-11-56.

Losen, 2004, Effect of oxygen limitation and medium composition on Escherichia coli fermentation in shake-flask cultures., Biotechnol. Prog., 20, 1062, 10.1021/bp034282t

Madurawe, 2000, A recombinant lipoprotein antigen against Lyme disease expressed in E. coli: fermentor operating strategies for improved yield., Biotechnol. Prog., 16, 571, 10.1021/bp0000555

Makhatadze, 1995, Energetics of protein structure., Adv. Protein Chem., 47, 307, 10.1016/S0065-3233(08)60548-3

Makoff, 1991, High level heterologous expression in E. coli using mutant forms of the lac promoter., Nucleic Acids Res., 19, 2417, 10.1093/nar/19.9.2417

Makrides, 1996, Strategies for achieving high-level expression of genes in Escherichia coli., Microbiol. Rev., 60, 512, 10.1128/MMBR.60.3.512-538.1996

Marisch, 2013, Evaluation of three industrial Escherichia coli strains in fed-batch cultivations during high-level SOD protein production., Microb. Cell Fact., 12, 10.1186/1475-2859-12-58

Martinez-Alonso, 2008, The functional quality of soluble recombinant polypeptides produced in Escherichia coli is defined by a wide conformational spectrum., Appl. Environ. Microbiol., 74, 7431, 10.1128/AEM.01446-08

Martinez-Alonso, 2007, Role of the chaperone DnaK in protein solubility and conformational quality in inclusion body-forming Escherichia coli cells., FEMS Microbiol. Lett., 273, 187, 10.1111/j.1574-6968.2007.00788.x

McCarty, 1991, DnaK as a thermometer: threonine-199 is site of autophosphorylation and is critical for ATPase activity., Proc. Natl. Acad. Sci. U.S.A., 88, 9513, 10.1073/pnas.88.21.9513

McDaniel, 1969, Effect of shaking speed and type of closure on shake flask cultures., Appl. Microbiol., 17, 286, 10.1128/AEM.17.2.286-290.1969

Menart, 2003, Constitutive versus thermoinducible expression of heterologous proteins in Escherichia coli based on strong PR,PL promoters from phage lambda., Biotechnol. Bioeng., 83, 181, 10.1002/bit.10660

Mendoza, 2000, The lower hydrolysis of ATP by the stress protein GroEL is a major factor responsible for the diminished chaperonin activity at low temperature., Cryobiology, 41, 319, 10.1006/cryo.2000.2287

Menzella, 2011, Comparison of two codon optimization strategies to enhance recombinant protein production in Escherichia coli., Microb. Cell Fact., 10, 10.1186/1475-2859-10-15

Menzella, 2003, Novel Escherichia coli strain allows efficient recombinant protein production using lactose as inducer., Biotechnol. Bioeng., 82, 809, 10.1002/bit.10630

Mergulhao, 2005, Recombinant protein secretion in Escherichia coli., Biotechnol. Adv., 23, 177, 10.1016/j.biotechadv.2004.11.003

Messens, 2006, Pathways of disulfide bond formation in Escherichia coli., Int. J. Biochem. Cell Biol., 38, 1050, 10.1016/j.biocel.2005.12.011

Meyer, 1999, Purification of recombinant proteins by fusion with thermally-responsive polypeptides., Nat. Biotechnol., 17, 1112, 10.1038/15100

Mieschendahl, 1986, A novel prophage independent trp regulated lambda PL expression system., Nat. Biotechnol., 4, 10.1038/nbt0986-802

Minton, 1984, Improved plasmid vectors for the isolation of translational lac gene fusions., Gene, 31, 269, 10.1016/0378-1119(84)90220-8

Miroux, 1996, Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels., J. Mol. Biol., 260, 289, 10.1006/jmbi.1996.0399

Moffatt, 1987, T7 lysozyme inhibits transcription by T7 RNA polymerase., Cell, 49, 221, 10.1016/0092-8674(87)90563-0

Moulton, 2013, Fed-Batch Fermentation: A Practical Guide to Scalable Recombinant Protein Production in Escherichia coli.

Müllerller-Hill, 1996, The Lac Operon: A Short History of a Genetic Paradigm, 10.1515/9783110879476

Müllerller-Hill, 1968, Mutants that make more lac repressor., Proc. Natl. Acad. Sci. U.S.A., 59, 1259, 10.1073/pnas.59.4.1259

Nilsson, 1997, Affinity fusion strategies for detection, purification, and immobilization of recombinant proteins., Protein Expr. Purif., 11, 1, 10.1006/prep.1997.0767

Nishihara, 1998, Chaperone coexpression plasmids: differential and synergistic roles of DnaK-DnaJ-GrpE and GroEL-GroES in assisting folding of an allergen of Japanese cedar pollen, Cryj2, in Escherichia coli., Appl. Environ. Microbiol., 64, 1694, 10.1128/AEM.64.5.1694-1699.1998

Nishihara, 2000, Overexpression of trigger factor prevents aggregation of recombinant proteins in Escherichia coli., Appl. Environ. Microbiol., 66, 884, 10.1128/AEM.66.3.884-889.2000

Nordstrom, 2006, Plasmid R1 – replication and its control., Plasmid, 55, 1, 10.1016/j.plasmid.2005.07.002

O’Beirne, 2000, Oxygen availability and the growth of Escherichia coli W3110: a problem exacerbated by scale-up., Bioprocess Eng., 23, 487, 10.1007/s004499900185

Ohana, 2009, HaloTag7: a genetically engineered tag that enhances bacterial expression of soluble proteins and improves protein purification., Protein Expr. Purif., 68, 110, 10.1016/j.pep.2009.05.010

Oresic, 1998, Specific correlations between relative synonymous codon usage and protein secondary structure., J. Mol. Biol., 281, 31, 10.1006/jmbi.1998.1921

Ou, 2004, Stationary phase protein overproduction is a fundamental capability of Escherichia coli., Biochem. Biophys. Res. Commun., 314, 174, 10.1016/j.bbrc.2003.12.077

Palomares, 2004, Production of recombinant proteins: challenges and solutions., Methods Mol. Biol., 267, 15, 10.1385/1-59259-774-2:015

Parks, 1994, Release of proteins and peptides from fusion proteins using a recombinant plant virus proteinase., Anal. Biochem., 216, 413, 10.1006/abio.1994.1060

Pedersen, 1984, Escherichia coli ribosomes translate in vivo with variable rate, EMBO J., 3, 2895, 10.1002/j.1460-2075.1984.tb02227.x

Perron-Savard, 2005, Dimerization and DNA binding of the Salmonella enterica PhoP response regulator are phosphorylation independent., Microbiology, 151, 3979, 10.1099/mic.0.28236-0

Peubez, 2010, Antibiotic-free selection in E. coli: new considerations for optimal design and improved production, Microb. Cell Fact., 9, 10.1186/1475-2859-9-65

Pope, 1996, High efficiency 5 min transformation of Escherichia coli., Nucleic Acids Res., 24, 536, 10.1093/nar/24.3.536

Porath, 1983, Immobilized metal ion affinity adsorption and immobilized metal ion affinity chromatography of biomaterials. Serum protein affinities for gel-immobilized iron and nickel ions, Biochemistry, 22, 1621, 10.1021/bi00276a015

Postma, 1985, Phosphoenolpyruvate: carbohydrate phosphotransferase system of bacteria., Microbiol. Rev., 49, 232, 10.1128/MMBR.49.3.232-269.1985

Puigbo, 2007, OPTIMIZER: a web server for optimizing the codon usage of DNA sequences., Nucleic Acids Res., 35, W126, 10.1093/nar/gkm219

Qing, 2004, Cold-shock induced high-yield protein production in Escherichia coli., Nat. Biotechnol., 22, 877, 10.1038/nbt984

Rais-Beghdadi, 1998, Purification of recombinant proteins by chemical removal of the affinity tag., Appl. Biochem. Biotechnol., 74, 95, 10.1007/BF02787176

Raran-Kurussi, 2012, The ability to enhance the solubility of its fusion partners is an intrinsic property of maltose-binding protein but their folding is either spontaneous or chaperone-mediated., PLoS ONE, 7:, 10.1371/journal.pone.0049589

Roberts, 1996, Tetracycline resistance determinants: mechanisms of action, regulation of expression, genetic mobility, and distribution., FEMS Microbiol. Rev., 19, 1, 10.1111/j.1574-6976.1996.tb00251.x

Rosano, 2011, Insights into the Clp/HSP100 chaperone system from chloroplasts of Arabidopsis thaliana., J. Biol. Chem., 286, 29671, 10.1074/jbc.M110.211946

Rosano, 2009, Rare codon content affects the solubility of recombinant proteins in a codon bias-adjusted Escherichia coli strain., Microb. Cell Fact., 8, 10.1186/1475-2859-8-41

Routledge, 2012, Beyond de-foaming: the effects of antifoams on bioprocess productivity., Comput. Struct. Biotechnol. J., 3, 1, 10.5936/csbj.201210014

Routledge, 2011, Antifoam addition to shake flask cultures of recombinant Pichia pastoris increases yield., Microb. Cell Fact., 10, 10.1186/1475-2859-10-17

Rudolph, 1996, In vitro folding of inclusion body proteins., FASEB J., 10, 49, 10.1096/fasebj.10.1.8566547

Sahdev, 2008, Production of active eukaryotic proteins through bacterial expression systems: a review of the existing biotechnology strategies., Mol. Cell. Biochem., 307, 249, 10.1007/s11010-007-9603-6

Saida, 2006, Expression of highly toxic genes in E. coli: special strategies and genetic tools., Curr. Protein Pept. Sci., 7, 47, 10.2174/138920306775474095

San-Miguel, 2013, Production of soluble eukaryotic recombinant proteins in is favoured in early log-phase cultures induced at low temperature., Springerplus, 2, 10.1186/2193-1801-2-89

Scheidle, 2011, Controlling pH in shake flasks using polymer-based controlled-release discs with pre-determined release kinetics., BMC Biotechnol., 11:, 10.1186/1472-6750-11-25

Schein, 1988, Formation of soluble recombinant proteins in Escherichia coli is favored by lower growth temperature., Nat. Biotechnol., 6, 10.1038/nbt0388-291

Schellman, 1997, Temperature, stability, and the hydrophobic interaction., Biophys. J., 73, 2960, 10.1016/S0006-3495(97)78324-3

Schierle, 2003, The DsbA signal sequence directs efficient, cotranslational export of passenger proteins to the Escherichia coli periplasm via the signal recognition particle pathway., J. Bacteriol., 185, 5706, 10.1128/JB.185.19.5706-5713.2003

Schleif, 2000, Regulation of the L-arabinose operon of Escherichia coli., Trends Genet., 16, 559, 10.1016/S0168-9525(00)02153-3

Schleif, 2010, AraC protein, regulation of the l-arabinose operon in Escherichia coli, and the light switch mechanism of AraC action., FEMS Microbiol. Rev., 34, 779, 10.1111/j.1574-6976.2010.00226.x

Sezonov, 2007, Escherichia coli physiology in Luria-Bertani broth., J. Bacteriol., 189, 8746, 10.1128/JB.01368-07

Shatzman, 2001, Expression using vectors with phage lambda regulatory sequences., Curr. Protoc. Mol. Biol. Chapter 16, Unit16.13., 10.1002/0471142727.mb1603s11

Shaw, 1983, Chloramphenicol acetyltransferase: enzymology and molecular biology., CRC Crit. Rev. Biochem., 14, 1, 10.3109/10409238309102789

Shih, 2002, High-throughput screening of soluble recombinant proteins., Protein Sci., 11, 1714, 10.1110/ps.0205202

Shiloach, 2005, Growing E. coli to high cell density – a historical perspective on method development., Biotechnol. Adv., 23, 345, 10.1016/j.biotechadv.2005.04.004

Shur, 2013, A designed, phase changing RTX-based peptide for efficient bioseparations., Biotechniques, 54, 197, 10.2144/000114010

Siegele, 1997, Gene expression from plasmids containing the araBAD promoter at subsaturating inducer concentrations represents mixed populations., Proc. Natl. Acad. Sci. U.S.A., 94, 8168, 10.1073/pnas.94.15.8168

Silverstone, 1970, Catabolite-insensitive revertants of lac promoter mutants., Proc. Natl. Acad. Sci. U.S.A., 66, 773, 10.1073/pnas.66.3.773

Sivashanmugam, 2009, Practical protocols for production of very high yields of recombinant proteins using Escherichia coli., Protein Sci., 18, 936, 10.1002/pro.102

Smith, 1988, Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase., Gene, 67, 31, 10.1016/0378-1119(88)90005-4

Soares, 2003, Periplasmic expression of human growth hormone via plasmid vectors containing the lambdaPL promoter: use of HPLC for product quantification., Protein Eng., 16, 1131, 10.1093/protein/gzg114

Sorensen, 2005, Advanced genetic strategies for recombinant protein expression in Escherichia coli., J. Biotechnol., 115, 113, 10.1016/j.jbiotec.2004.08.004

Stano, 2004, T7 lysozyme represses T7 RNA polymerase transcription by destabilizing the open complex during initiation., J. Biol. Chem., 279, 16136, 10.1074/jbc.M400139200

Stevens, 2000, Design of high-throughput methods of protein production for structural biology., Structure, 8, R177, 10.1016/S0969-2126(00)00193-3

Stewart, 1998, Disulfide bond formation in the Escherichia coli cytoplasm: an in vivo role reversal for the thioredoxins., EMBO J., 17, 5543, 10.1093/emboj/17.19.5543

Stoker, 1982, Versatile low-copy-number plasmid vectors for cloning in Escherichia coli., Gene, 18, 335, 10.1016/0378-1119(82)90172-X

Strocchi, 2006, Low temperature-induced systems failure in Escherichia coli: insights from rescue by cold-adapted chaperones., Proteomics, 6, 193, 10.1002/pmic.200500031

Studier, 2005, Protein production by auto-induction in high density shaking cultures., Protein Expr. Purif., 41, 207, 10.1016/j.pep.2005.01.016

Studier, 2014, Stable expression clones and auto-induction for protein production in E. coli., Methods Mol. Biol., 1091, 17, 10.1007/978-1-62703-691-7_2

Studier, 1986, Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes., J. Mol. Biol., 189, 113, 10.1016/0022-2836(86)90385-2

Summers, 1993, Multicopy plasmid instability: the dimer catastrophe hypothesis., Mol. Microbiol., 8, 1031, 10.1111/j.1365-2958.1993.tb01648.x

Supek, 2004, INCA: synonymous codon usage analysis and clustering by means of self-organizing map., Bioinformatics, 20, 2329, 10.1093/bioinformatics/bth238

Terpe, 2003, Overview of tag protein fusions: from molecular and biochemical fundamentals to commercial systems., Appl. Microbiol. Biotechnol., 60, 523, 10.1007/s00253-002-1158-6

Thanaraj, 1996, Ribosome-mediated translational pause and protein domain organization., Protein Sci., 5, 1594, 10.1002/pro.5560050814

Tropea, 2009, Expression and purification of soluble His(6)-tagged TEV protease., Methods Mol. Biol., 498, 297, 10.1007/978-1-59745-196-3_19

Tsai, 2008, Synonymous mutations and ribosome stalling can lead to altered folding pathways and distinct minima., J. Mol. Biol., 383, 281, 10.1016/j.jmb.2008.08.012

Tsumoto, 2003, Practical considerations in refolding proteins from inclusion bodies., Protein Expr. Purif., 28, 1, 10.1016/S1046-5928(02)00641-1

Umezawa, 1979, Studies on aminoglycoside antibiotics: enzymic mechanism of resistance and genetics., Jpn. J. Antibiot., 32(Suppl.), S1

Unden, 1995, O2-sensing and O2-dependent gene regulation in facultatively anaerobic bacteria., Arch. Microbiol., 164, 81, 10.1007/s002030050238

Valdez-Cruz, 2010, Production of recombinant proteins in E. coli by the heat inducible expression system based on the phage lambda pL and/or pR promoters, Microb. Cell Fact., 9, 10.1186/1475-2859-9-18

Valent, 1998, The Escherichia coli SRP and SecB targeting pathways converge at the translocon., EMBO J., 17, 2504, 10.1093/emboj/17.9.2504

Vasina, 1997, Expression of aggregation-prone recombinant proteins at low temperatures: a comparative study of the Escherichia coli cspA and tac promoter systems., Protein Expr. Purif., 9, 211, 10.1006/prep.1996.0678

Vasina, 1998, Scale-up and optimization of the low-temperature inducible cspA promoter system., Biotechnol. Prog., 14, 714, 10.1021/bp980061p

Vera, 2007, The conformational quality of insoluble recombinant proteins is enhanced at low growth temperatures., Biotechnol. Bioeng., 96, 1101, 10.1002/bit.21218

Vieira, 1987, Production of single-stranded plasmid DNA., Methods Enzymol., 153, 3, 10.1016/0076-6879(87)53044-0

Voss, 2006, Application of a KDPG-aldolase gene-dependent addiction system for enhanced production of cyanophycin in Ralstonia eutropha strain H16., Metab. Eng., 8, 66, 10.1016/j.ymben.2005.09.003

Wagner, 2008, Tuning Escherichia coli for membrane protein overexpression., Proc. Natl. Acad. Sci. U.S.A., 105, 14371, 10.1073/pnas.0804090105

Wang, 1991, Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli., Gene, 100, 195, 10.1016/0378-1119(91)90366-J

Wanner, 1978, Regulation of lac operon expression: reappraisal of the theory of catabolite repression., J. Bacteriol., 136, 947, 10.1128/JB.136.3.947-954.1978

Waugh, 2011, An overview of enzymatic reagents for the removal of affinity tags., Protein Expr. Purif., 80, 283, 10.1016/j.pep.2011.08.005

Weickert, 1999, A mutation that improves soluble recombinant hemoglobin accumulation in Escherichia coli in heme excess., Appl. Environ. Microbiol., 65, 640, 10.1128/AEM.65.2.640-647.1999

Welch, 2009, Design parameters to control synthetic gene expression in Escherichia coli., PLoS ONE, 4:, 10.1371/journal.pone.0007002

Weuster-Botz, 2001, Parallel substrate feeding and pH-control in shaking-flasks., Biochem. Eng. J., 7, 163, 10.1016/S1369-703X(00)00117-0

Wild, 2002, Conditionally amplifiable BACs: switching from single-copy to high-copy vectors and genomic clones., Genome Res., 12, 1434, 10.1101/gr.130502

Winkler, 1967, Inhibition of beta-galactoside transport by substrates of the glucose transport system in Escherichia coli., Biochim. Biophys. Acta, 135, 1030, 10.1016/0005-2736(67)90073-9

Wu, 1999, Hexahistidine (His6)-tag dependent protein dimerization: a cautionary tale., Acta Biochim. Pol., 46, 591, 10.18388/abp.1999_4131

Yamanè, 1984, “Fed-batch techniques in microbial processes,” in, Bioprocess Parameter Control, 147, 10.1007/BFb0006382

Yang, 2003, High-level expression of a soluble snake venom enzyme, gloshedobin, in E. coli in the presence of metal ions, Biotechnol. Lett., 25, 607, 10.1023/A:1023067626846

Yee, 1992, Recombinant protein expression in high cell density fed-batch cultures of Escherichia coli., Biotechnology (N. Y.), 10, 1550, 10.1038/nbt1292-1550

Yona, 2013, tRNA genes rapidly change in evolution to meet novel translational demands., Elife, 2:, 10.7554/eLife.01339

Zielenkiewicz, 2001, Mechanisms of plasmid stable maintenance with special focus on plasmid addiction systems., Acta Biochim. Pol., 48, 1003, 10.18388/abp.2001_3863