Efficient soluble expression of disulfide bonded proteins in the cytoplasm of Escherichia coli in fed-batch fermentations on chemically defined minimal media

Microbial Cell Factories

Volumn 16, Issue 1, 2017, Pages

  Gaciarz, Anna ^a   Khatri, Narendar Kumar ^a   Velez Suberbie, M Lourdes ^b   Saaranen, Mirva J ^a   Uchida, Yuko ^a   Keshavarz Moore, Eli ^b   Ruddock, Lloyd W ^a  

^a UNIVERSITY OF OULU   (Finland)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Avidin; Cytoplasm; Disulfide bonds; Escherichia coli; Fed batch; Fermentation; Growth hormone; Interleukin 6; ScFv

Indexed keywords

AVIDIN; DISULFIDE; ESCHERICHIA COLI PROTEIN; GLUCOSE; GLYCEROL; HUMAN GROWTH HORMONE; IMMUNOGLOBULIN FRAGMENT; INTERLEUKIN 6; RECOMBINANT PROTEIN;

ANIMAL; BIOREACTOR; BIOSYNTHESIS; CELL INCLUSION; CHEMISTRY; CHICKEN; CULTURE MEDIUM; CYTOLOGY; CYTOPLASM; ESCHERICHIA COLI; FEMALE; FERMENTATION; GENETICS; HUMAN; METABOLISM; OXIDATION REDUCTION REACTION;

ANIMALS; AVIDIN; BIOREACTORS; CHICKENS; CULTURE MEDIA; CYTOPLASM; DISULFIDES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FEMALE; FERMENTATION; GLUCOSE; GLYCEROL; HUMAN GROWTH HORMONE; HUMANS; IMMUNOGLOBULIN FRAGMENTS; INCLUSION BODIES; INTERLEUKIN-6; OXIDATION-REDUCTION; RECOMBINANT PROTEINS;

EID: 85027546516     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/s12934-017-0721-x     Document Type: Article

References (53)

1. Bulleid NJ. Disulfide bond formation in the mammalian endoplasmic reticulum. Cold Spring Harb Perspect Biol 2012; 4: a013219. 10.1101/cshperspect.a013219
2. Mamathambika BS, Bardwell JC. Disulfide-linked protein folding pathways. Annu Rev Cell Dev Biol 2008; 24: 211-235. 10.1146/annurev.cellbio.24.110707.175333
3. Prinz WA, Aslund F, Holmgren A, Beckwith J. The role of the thioredoxin and glutaredoxin pathways in reducing protein disulfide bonds in the Escherichia coli cytoplasm. J Biol Chem 1997; 272: 15661-15667. 10.1074/jbc.272.25.15661
4. Huang C-J, Lin H, Yang X. Industrial production of recombinant therapeutics in Escherichia coli and its recent advancements. J Ind Microbiol Biotechnol 2012; 39: 383-399. 10.1007/s10295-011-1082-9
5. Graham LL, Beveridge TJ, Nanninga N. Periplasmic space and the concept of the periplasm. Trends Biochem Sci 1991; 16: 328-329. 10.1016/0968-0004(91)90135-I
6. Schlegel S, Rujas E, Ytterberg AJ, Zubarev RA, Luirink J, Gier J-W. Optimizing heterologous protein production in the periplasm of E. coli by regulating gene expression levels. Microb Cell Fact 2013; 12: 24. 10.1186/1475-2859-12-24
7. Schmidt FR. Recombinant expression systems in the pharmaceutical industry. Appl Microbiol Biotechnol 2004; 65: 363-372. 10.1007/s00253-004-1656-9
8. Sahdev S, Khattar SK, Saini KS. Production of active eukaryotic proteins through bacterial expression systems: a review of the existing biotechnology strategies. Mol Cell Biochem 2007; 307: 249-264. 10.1007/s11010-007-9603-6
9. Singh A, Panda AK. Solubilization and refolding of inclusion body proteins. Insoluble Proteins Methods Protoc 2005; 99: 283-291
10. Graumann K, Premstaller A. Manufacturing of recombinant therapeutic proteins in microbial systems. Biotechnol J 2006; 1: 164-186. 10.1002/biot.200500051
11. Bessette PH, Aslund 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. 10.1073/pnas.96.24.13703
12. Yamamoto Y, Ritz D, Planson A-G, Jönsson TJ, Faulkner MJ, Boyd D. Mutant AhpC peroxiredoxins suppress thiol-disulfide redox deficiencies and acquire deglutathionylating activity. Mol Cell 2008; 29: 36-45. 10.1016/j.molcel.2007.11.029
13. Levy R, Weiss R, Chen G, Iverson BL, Georgiou G. Production of correctly folded Fab antibody fragment in the cytoplasm of Escherichia coli trxB gor mutants via the coexpression of molecular chaperones. Protein Expr Purif 2001; 23: 338-347. 10.1006/prep.2001.1520
14. 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: 753. 10.1186/1475-2859-11-56
15. Samuelson J, Causey T, Berkmen M. Disulfide-bonded protein production in E. coli. Involvement of disulfide bond isomerase improves protein folding. Gen 2012; 32: 35-36
16. Hatahet F, Nguyen VD, Salo KEH, Ruddock LW. Disruption of reducing pathways is not essential for efficient disulfide bond formation in the cytoplasm of E. coli. Microb Cell Fact 2010; 9: 67
17. Gaciarz A, Veijola J, Uchida Y, Saaranen MJ, Wang C, Hörkkö S. Systematic screening of soluble expression of antibody fragments in the cytoplasm of E. coli. Microb Cell Fact 2016; 15: 22. 10.1186/s12934-016-0419-5
18. Nguyen VD, Hatahet F, Salo KEH, Enlund E, Zhang C, Ruddock LW. Pre-expression of a sulfhydryl oxidase significantly increases the yields of eukaryotic disulfide bond containing proteins expressed in the cytoplasm of E. coli. Microb Cell Fact 2011; 10: 1. 10.1186/1475-2859-10-1
19. Matos CFRO, Robinson C, Alanen HI, Prus P, Uchida Y, Ruddock LW. 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. 10.1002/btpr.1858
20. Hatahet F, Ruddock LW. Topological plasticity of enzymes involved in disulfide bond formation allows catalysis in either the periplasm or the cytoplasm. J Mol Biol 2013; 425: 3268-3276. 10.1016/j.jmb.2013.04.034
21. Korz DJ, Rinas U, Hellmuth K, Sanders EA, Deckwer WD. Simple fed-batch technique for high cell density cultivation of Escherichia coli. J Biotechnol 1995; 39: 59-65. 10.1016/0168-1656(94)00143-Z
22. Chung W-J, Huang C-L, Gong H-Y, Ou T-Y, Hsu J-L, Hu S-Y. Recombinant production of biologically active giant grouper (Epinephelus lanceolatus) growth hormone from inclusion bodies of Escherichia coli by fed-batch culture. Protein Expr Purif 2015; 110: 79-88. 10.1016/j.pep.2015.02.012
23. Brüsehaber E, Schwiebs A, Schmidt M, Böttcher D, Bornscheuer UT. Production of pig liver esterase in batch fermentation of E. coli Origami. Appl Microbiol Biotechnol 2010; 86: 1337-1344. 10.1007/s00253-009-2392-y
24. Lamppa JW, Tanyos SA, Griswold KE. Engineering Escherichia coli for soluble expression and single step purification of active human lysozyme. J Biotechnol 2013; 164: 1-8. 10.1016/j.jbiotec.2012.11.007
25. Cronin MJ. Pioneering recombinant growth hormone manufacturing: pounds produced per mile of height. J Pediatr 1997; 131: S5-S7. 10.1016/S0022-3476(97)70002-7
26. Drug Bank. http://www.drugbank.ca/drugs/DB00052
27. Ejima D, Watanabe M, Sato Y, Date M, Yamada N, Takahara Y. High yield refolding and purification process for recombinant human interleukin-6 expressed in Escherichia coli. Biotechnol Bioeng 1999; 62: 301-310. 10.1002/(SICI)1097-0290(19990205)62:3<301::AID-BIT6>3.0.CO;2-W
28. Kim TW, Chung BH, Chang YK. Production of soluble human interleukin-6 in cytoplasm by fed-batch culture of recombinant E. coli. Biotechnol Prog 2008; 21: 524-531. 10.1021/bp049645j
29. Lee EG, Baek J-E, Lee S-H, Kim T-W, Choi JH, Rho M-C. Efficient proteolytic cleavage by insertion of oligopeptide linkers and its application to production of recombinant human interleukin-6 in Escherichia coli. Enzyme Microb Technol 2009; 44: 254-262. 10.1016/j.enzmictec.2008.12.014
30. Nausch H, Huckauf J, Koslowski R, Meyer U, Broer I, Mikschofsky H. Recombinant production of human interleukin 6 in Escherichia coli. PLoS ONE 2013; 8: e54933. 10.1371/journal.pone.0054933
31. Li Y, Chen CX, Specht B-U, Hahn HP. Cloning and hemolysin-mediated secretory expression of a codon-optimized synthetic human interleukin-6 gene in Escherichia coli. Protein Expr Purif 2002; 25: 437-447. 10.1016/S1046-5928(02)00028-1
32. Nelson AL, Reichert JM. Development trends for therapeutic antibody fragments. Nat Biotechnol 2009; 27: 331-337. 10.1038/nbt0409-331
33. Skerra A, Pluckthun A. Assembly of a functional immunoglobulin Fv fragment in Escherichia coli. Science 1988; 240: 1038. 10.1126/science.3285470
34. Proba K, Wörn A, Honegger A, Plückthun A. Antibody scFv fragments without disulfide bonds, made by molecular evolution. J Mol Biol 1998; 275: 245-253. 10.1006/jmbi.1997.1457
35. Livnah O, Bayer EA, Wilchek M, Sussman JL. Three-dimensional structures of avidin and the avidin-biotin complex. Proc Natl Acad Sci USA 1993; 90: 5076-5080. 10.1073/pnas.90.11.5076
36. Hiller Y, Gershoni JM, Bayer EA, Wilchek M. Biotin binding to avidin. Oligosaccharide side chain not required for ligand association. Biochem J 1987; 248: 167-171. 10.1042/bj2480167
37. Kovacs-Nolan J, Phillips M, Mine Y. Advances in the value of eggs and egg components for human health. J Agric Food Chem 2005; 53: 8421-8431. 10.1021/jf050964f
38. Nardone E, Rosano C, Santambrogio P, Curnis F, Corti A, Magni F. Biochemical characterization and crystal structure of a recombinant hen avidin and its acidic mutant expressed in Escherichia coli. Eur J Biochem 1998; 256: 453-460. 10.1046/j.1432-1327.1998.2560453.x
39. Hytönen VP, Lattinen OH, Airenne TT, Kidron H, Meltola NJ, Porkka EJ. Efficient production of active chicken avidin using a bacterial signal peptide in Escherichia coli. Biochem J 2004; 384: 385. 10.1042/BJ20041114
40. Overton TW. Recombinant protein production in bacterial hosts. Drug Discov Today 2014; 19: 590-601. 10.1016/j.drudis.2013.11.008
41. Kim JY, Kim YG, Lee GM. CHO cells in biotechnology for production of recombinant proteins: current state and further potential. Appl Microbiol Biotechnol 2012; 93: 917-930. 10.1007/s00253-011-3758-5
42. Hossler P, Khattak SF, Li ZJ. Optimal and consistent protein glycosylation in mammalian cell culture. Glycobiology 2009; 19: 936-949. 10.1093/glycob/cwp079
43. Miesegaes G, Lute S, Brorson K. Analysis of viral clearance unit operations for monoclonal antibodies. Biotechnol Bioeng 2010; 106: 238-246
44. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2006; 2006(2): 0008
45. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 2000; 97: 6640-6645. 10.1073/pnas.120163297
46. Bachmann BJ. Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriol Rev 1972; 36: 525-557
47. Hill CW, Harnish BW. Inversions between ribosomal RNA genes of Escherichia coli. Proc Natl Acad Sci USA 1981; 78: 7069-7072. 10.1073/pnas.78.11.7069
48. Alanen HI, Salo KEH, Pekkala M, Siekkinen HM, Prineskoski A, Ruddock LW. Defining the domain boundaries of the human protein disulfide isomerases. Antioxid Redox Signal 2003; 5: 367-374. 10.1089/152308603768295096
49. Neubauer P, Häggström L, Enfors S-O. Influence of substrate oscillations on acetate formation and growth yield in Escherichia coli glucose limited fed-batch cultivations. Biotechnol Bioeng 1995; 47: 139-146. 10.1002/bit.260470204
50. Holme T, Arvidson S, Lindholm B, Pavlu B. Enzymes-laboratory-scale production. Process Biochem 1970; 5: 62-66
51. Tripathi N, Sathyaseelan K, Jana A, Rao PVL. High yield production of heterologous proteins with Escherichia coli. Def Sci J 2009; 59: 137-146. 10.14429/dsj.59.1501
52. Boychyn M, Yim SSS, Bulmer M, More J, Bracewell DG, Hoare M. Performance prediction of industrial centrifuges using scale-down models. Bioprocess Biosyst Eng 2004; 26: 385-391. 10.1007/s00449-003-0328-y
53. Branston SD, Matos CFRO, Freedman RB, Robinson C, Keshavarz-Moore E. Investigation of the impact of Tat export pathway enhancement on E. coli culture, protein production and early stage recovery. Biotechnol Bioeng 2012; 109: 983-991. 10.1002/bit.24384