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Table 1 Proteins whose total and/or functional yields increase upon co-production of GroESL

From: Use of folding modulators to improve heterologous protein production in Escherichia coli

Recombinant protein Effect of co-production of GroESL chaperones Reference
Human procollagenase GroESL increased production levels by 10-fold, solubility and half-life [68]
p50csk Protein-Tyrosine Kinase Co-production enhanced solubility and activity of the protein by up to >50% [69]
Candida albicans PMI metalloenzyme 2-fold increase in protein solubility [70]
α and β subunits of human propionyl-CoA carboxylase (PCC) Several hundred-fold increase in PCC specific activity; most of the protein produced in soluble form [71]
Human electron transfer flavoprotein (ETF) Co-production required for stable expression of ETF α G116R mutant [72]
β-glucosidase from Cellovibrio gilvus and Agrobacterium tumefaciens Co-production resulted in slower growth rate and reduced yield but increased solubility of the proteins by 20–60% at 37°C and up to 70% at 25°C [64]
Cryj2 Japanese cedar pollen Increased yield and solubility of expressed protein; 4-fold stabilisation of the protein in the presence of a 10-fold chaperone excess [36]
Human kinase inhibitor-GST fusion Solubility of otherwise mostly insoluble protein enhanced by 5–6-fold [73]
Eukaryotic phenylalanine ammonia-lyase Dramatically improved yield and activity of the protein after engineering of gene to remove E. coli rare codons [74]
Bovine adrenodoxin reductase (AdR) Increased soluble AdR yield to 10 mg/l, compared with 4 mg/l with Hsp70 [75]
Cyanobacterium transcription factor 3–4-fold increase in solubility [76]
Thermococcus litoralis 4-α-glucanotransferase (GTase) Co-production of GroESL with tRNAAGA and tRNAAGG led to 5-fold increase in GTase activity in soluble fraction; yield otherwise lower and 60% insoluble [77]
Agrobacterium radiobacter carbamoylase 4-fold increase in activity due to improved solubility [39]
Human cytochrome P450 3A7 (CYP3A7) Increased expression levels and activity of the otherwise inactive protein [78]
Decarboxylase component of human α-keto acid dehydrogenase complex Co-production of GroEL or GroES resulted in increase in decarboxylase activity by 500-fold and 30-fold, respectively [79]
Maize plastidic protoporphyrinogen IX oxidase (PPO) 6-fold increase in soluble PPO yield [80]
Manganese catalase from Thermus sp. Increased solubility (up to 50%) with GroESL [81]
p66 and p51 subunits of HIV-1 RTase Yield and nucleic acid affinity increased by 4–5- and 1.6-fold, respectively [82]
Anti-digoxin Fab antibody fragment 4-fold increase in solubility of the Fab produced in E. coli Origami strain [19]
Agrobacterium tumefaciens D-carbamoylase (DCB) Increase in solubility of DCB up to 60% and activity by 6.2-fold at 28°C; at 25°C protein solubility increased to 75% and activity by 4.5-fold [83]
Guinea pig NADPH:quinone oxidoreductase 3-fold increase in solubility [84]
Aconitase Solubility and activity increased to 40% and by 1.5-fold, respectively [58]
Rhodococcus erythropolis desulfinase Solubility of the protein increased up to 40–50% and activity by 25-fold [85]
E. coli glutamate racemase (GluR) Growth of host cells improved; 2.2-fold increase in yield of active GluR [86]
Pseudomonas putida F61 nicotinoprotein formaldehyde dismutase (NDF) With tac promoter, increased solubility (up to 80%) and 6-fold higher enzyme activity; lesser effect when NDF expressed under the lac promoter [61]
Human PP2A methyltransferase 24-fold increase in solubility [87]
Oligo-1,6-glucosidase from Bacillus thermoglucosidasius Specific activity increased by 44%, 56% and 56% with co-production of GroES, GroEL and GroESL, respectively [43]
Cyclodextrin gluanotransferase (CGTase) from Bacillus macerans Increase in solubility and activity of CGTase by 12% and 1.5-fold, respectively, at 37°C and by 22% and 1.3-fold, respectively, at 25°C [88, 89]
Rhizobium sp. α-1,6-fucosyltransferase At 30°C, improved folding and an increase in specific activity by 1.76-fold [90]
Mouse CYP27B1 protein 10-fold increase in the yield of stable and active protein [91]
Pyridoxine 4-oxidase (PNO) from Microbacterium luteolum No benefit of GroESL at 37°C; co-production at 23°C enhanced solubility and specific activity of PNO by 1.9-fold and 3.9-fold, respectively [92]
Pyridoxal 4-dehydrogenase from Microbacterium luteolum Co-production at 20°C led to reduced amounts of insoluble protein and increased specific activity by 9.1-fold [93]
Alcaligenes xylosoxydans N-acyl-D-amino acid amidohydrolases Enzymatic activity of the proteins increased from 7.8 to 72.4 U/mg and 7.1 to 22.7 U/mg, respectively, at 30°C [21]
Human aromatase (P450arom, CYP19) NmA264C and NmA264R mutants No improvement with NmA264C; production of NmA264R greatly enhanced (up to 400 nmol/l) [94]
scFv specific for c-Met Solubility increased 2-fold in E. coli Origami2(DE3) but not in BL21(DE3) [95]
Yeast mitochondrial aconitase Increased solubility at 25°C with no change in total yield [96]
human prolyl hydroxylase isoenzyme 2-fold increase in solubility when produced at 30°C [97]
Pig liver esterase γ-isoenzyme (PLE) Enhanced yield of soluble and active PLE in E. coli Origami (DE3) [98]
Soybean seed ferritin complex Increased solubility of H-1 subunit from 4 to 39% and H-2 subunit from 19 to 85% [99]
Human 11β hydroxylase 20- to 40-fold increase in yield in half the production time [100]
Human glucose 6-phosphate dehydrogenase (G6PD) and mutants Negligible effect on expression of wild type G6PD but activities of two mutants were enhanced by 48–160% and 39–118% at 37°C and 31°C, respectively [101]