Disulfide bond formation and activation of Escherichia coli β-galactosidase under oxidizing conditions

Applied and Environmental Microbiology

Volumn 78, Issue 7, 2012, Pages 2376-2385

  Seras Franzoso, Joaquin ^a,b   Affentranger, Roman ^a,d   Ferrer Navarro, Mario ^a   Daura, Xavier ^a,c   Villaverde, Antonio ^a,b   García Fruitósa, Elena ^a,b  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^c INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^d R and D Douglas Connect ^*  (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CATALYTIC CENTER; CELL BIOLOGY; CRYSTALLOGRAPHIC STUDIES; DISULFIDE BOND FORMATION; DISULFIDE BONDS; GALACTOSIDASES; HOMOLOGY MODELS; LARGE SIZES; MICROBIAL ENZYMES; OXIDIZING CONDITIONS; REPORTER ENZYMES; TETRAMERIC STRUCTURES;

AMINO ACIDS; CYTOLOGY; ENZYMES; ESCHERICHIA COLI; MOLECULAR BIOLOGY;

COVALENT BONDS;

BETA GALACTOSIDASE; CYSTEINE; DISULFIDE; ESCHERICHIA COLI PROTEIN;

BIOTECHNOLOGY; CELL ORGANELLE; COLIFORM BACTERIUM; ECOLOGICAL MODELING; ENZYME ACTIVITY; HOMOLOGY; MOLECULAR ANALYSIS; NUMERICAL MODEL; OXIDATION; PROTEIN; SPECIES OCCURRENCE; SULFIDE;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVATION; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; GROWTH, DEVELOPMENT AND AGING; MASS SPECTROMETRY; METABOLISM; MUTAGENESIS; OXIDATION REDUCTION REACTION; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; SEQUENCE HOMOLOGY; STRUCTURE ACTIVITY RELATION;

BETA-GALACTOSIDASE; CYSTEINE; DISULFIDES; ENZYME ACTIVATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; MUTAGENESIS; OXIDATION-REDUCTION; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; STRUCTURE-ACTIVITY RELATIONSHIP;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84861153521     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.06923-11     Document Type: Article

References (55)

1. Aslund F, Zheng M, Beckwith J, Storz G. 1999. Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol-disulfide status. Proc. Natl. Acad. Sci. U. S. A. 96:6161- 6165.
2. Barbirz S, Jakob U, Glocker MO. 2000. Mass spectrometry unravels disulfide bond formation as the mechanism that activates a molecular chaperone. J. Biol. Chem. 275:18759 -18766.
3. Bartlett GJ, Porter CT, Borkakoti N, Thornton JM. 2002. Analysis of catalytic residues in enzyme active sites. J. Mol. Biol. 324:105-121.
4. Bessette PH, Aslund F, Beckwith J, Georgiou G. 1999. Efficient folding of proteins with multiple disulfide bonds in the Escherichia coli cytoplasm. Proc. Natl. Acad. Sci. U. S. A. 96:13703-13708.
5. Cassland P, Larsson S, Nilvebrant NO, Jonsson LJ. 2004. Heterologous expression of barley and wheat oxalate oxidase in an E. coli trxB gor double mutant. J. Biotechnol. 109:53- 62.
6. Craven GR, Steers EJ, Anfinsen CB. 1965. Purification, composition, and molecular weight of beta-galactosidase of Escherichia coli K12. J. Biol. Chem. 240:2468 -2477.
7. de Marco A. 2009. Strategies for successful recombinant expression of disulfide bond-dependent proteins in Escherichia coli. Microb. Cell Fact. 8:26.
8. Derman AI, Beckwith J. 1991. Escherichia coli alkaline phosphatase fails to acquire disulfide bonds when retained in the cytoplasm. J. Bacteriol. 173:7719 -7722.
9. Derman AI, Prinz WA, Belin D, Beckwith J. 1993. Mutations that allow disulfide bond formation in the cytoplasm of Escherichia coli. Science 262: 1744-1747.
10. Garcia-Fruitos E, et al. 2005. Aggregation as bacterial inclusion bodies does not imply inactivation of enzymes and fluorescent proteins. Microb. Cell Fact. 4:27.
11. Gebler JC, Aebersold R, Withers SG. 1992. Glu-537, not Glu-461, is the nucleophile in the active site of (lac Z) beta-galactosidase from Escherichia coli. J. Biol. Chem. 267:11126 -11130.
12. Gonzalez-Montalban N, Garcia-Fruitos E, Villaverde A. 2007. Recombinant protein solubility- does more mean better? Nat. Biotechnol. 25: 718-720.
13. Guilhot C, Jander G, Martin NL, Beckwith J. 1995. Evidence that the pathway of disulfide bond formation in Escherichia coli involves interactions between the cysteines of DsbB and DsbA. Proc. Natl. Acad. Sci. U. S. A. 92:9895-9899.
14. Halbmayr EG, et al. 2008. High-level expression of recombinant betagalactosidases in Lactobacillus plantarum and Lactobacillus sakei using a Sakacin P-based expression system. J. Agric. Food Chem. 56:4710-4719.
15. Hu X, et al. 2007. Optimisation of production of a domoic acid-binding scFv antibody fragment in Escherichia coli using molecular chaperones and functional immobilisation on a mesoporous silicate support. Protein Expr. Purif. 52:194 -201.
16. Ibrahim SA, et al. 2010. Enhancement of alpha- and beta-galactosidase activity in Lactobacillus reuteri by different metal ions. Biol. Trace Elem. Res. 136:106 -116.
17. Jacobson RH, Zhang XJ, DuBose RF, Matthews BW. 1994. Threedimensional structure of beta-galactosidase from E. coli. Nature 369:761-766.
18. Jakob U, Muse W, Eser M, Bardwell JC. 1999. Chaperone activity with a redox switch. Cell 96:341-352.
19. Juers DH, et al. 2001. A structural view of the action of Escherichia coli (lacZ) beta-galactosidase. Biochemistry 40:14781-14794.
20. Juers DH, et al. 2000. High resolution refinement of beta-galactosidase in a new crystal form reveals multiple metal-binding sites and provides a structural basis for alpha-complementation. Protein Sci. 9:1685-1699.
21. Juers DH, et al. 2009. Direct and indirect roles of His-418 in metal binding and in the activity of beta-galactosidase (E. coli). Protein Sci. 18: 1281-1292.
22. Jurado P, de Lorenzo V, Fernandez LA. 2006. Thioredoxin fusions increase folding of single chain Fv antibodies in the cytoplasm of Escherichia coli: evidence that chaperone activity is the prime effect of thioredoxin. J. Mol. Biol. 357:49-61.
23. Kadokura H, Katzen F, Beckwith J. 2003. Protein disulfide bond formation in prokaryotes. Annu. Rev. Biochem. 72:111-135.
24. Kang JG, et al. 1999. RsrA, an anti-sigma factor regulated by redox change. EMBO J. 18:4292- 4298.
25. Kim J, Robinson AS. 2006. Dissociation of intermolecular disulfide bonds in P22 tailspike protein intermediates in the presence of SDS. Protein Sci. 15:1791-1793.
26. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
27. Le HV, Trotta PP. 1991. Purification of secreted recombinant proteins from Escherichia coli. Bioprocess Technol. 12:163-181.
28. Locker JK, Griffiths G. 1999. An unconventional role for cytoplasmic disulfide bonds in vaccinia virus proteins. J. Cell Biol. 144:267-279.
29. Makino T, Skretas G, Georgiou G. 2011. Strain engineering for improved expression of recombinant proteins in bacteria. Microb. Cell Fact. 10:32.
30. Martínez-Alonso M, Garcia-Fruitos E, Villaverde A. 2008. Yield, solubility and conformational quality of soluble proteins are not simultaneously favored in recombinant Escherichia coli. Biotechnol. Bioeng. 101: 1353-1358.
31. Martínez-Alonso M, Garcia-Fruitos E, Ferrer N, Rinas U, Villaverde A. 2010. Side effects of chaperone gene co-expression in recombinant protein production. Microb. Cell Fact. 9:64.
32. Messens J, Collet JF. 2006. Pathways of disulfide bond formation in Escherichia coli. Int. J. Biochem. Cell Biol. 38:1050 -1062.
33. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
34. Penner RM, Roth NJ, Rob B, Lay H, Huber RE. 1999. Tyr-503 of beta-galactosidase (Escherichia coli) plays an important role in degalactosylation. Biochem. Cell Biol. 77:229 -236.
35. Platas Rodríguez-Carmona GE, García-Fruitós E, Cano-Garrido O, Villaverde A. 2011. Co-production of GroELS discriminates between intrinsic and thermally-induced recombinant protein aggregation during substrate quality control. Microb. Cell Fact. 10:79.
36. Pollitt S, Zalkin H. 1983. Role of primary structure and disulfide bond formation in beta-lactamase secretion. J. Bacteriol. 153:27-32.
37. Prinz WA, Aslund F, Holmgren A, Beckwith J. 1997. The role of the thioredoxin and glutaredoxin pathways in reducing protein disulfide bonds in the Escherichia coli cytoplasm. J. Biol. Chem. 272:15661-15667.
38. Proba K, Ge L, Pluckthun A. 1995. Functional antibody single-chain fragments from the cytoplasm of Escherichia coli: influence of thioredoxin reductase (TrxB). Gene 159:203-207.
39. Reithel FJ, Newton RM, Eagleson M. 1966. Effects of thiols on Escherichia coli beta-galactosidases. Nature 210:1265.
40. Ring M, Huber RE. 1990. Multiple replacements establish the importance of tyrosine-503 in beta-galactosidase (Escherichia coli). Arch. Biochem. Biophys. 283:342-350.
41. Roth NJ, Penner RM, Huber RE. 2003. Beta-galactosidases (Escherichia coli) with double substitutions show that Tyr-503 acts independently of Glu-461 but cooperatively with Glu-537. J. Protein Chem. 22:663- 668.
42. Sali A, Blundell TL. 1993. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234:779-815.
43. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
44. Schneider EL, Thomas JG, Bassuk JA, Sage EH, Baneyx F. 1997. Manipulating the aggregation and oxidation of human SPARC in the cytoplasm of Escherichia coli. Nat. Biotechnol. 15:581-585.
45. Shen MY, Sali A. 2006. Statistical potential for assessment and prediction of protein structures. Protein Sci. 15:2507-2524.
46. Shifrin S, Grochowski BJ, Luborsky SW. 1970. Dissociation of betagalactosidase by thiols. Nature 227:608-609.
47. Shimizu TH, et al. 2005. Expression, purification, and crystallization of endopolygalacturonase from a pathogenic fungus, Stereum purpureum, in Escherichia coli. Protein Expr. Purif. 44:130 -135.
48. Silhavy TJ, Beckwith J. 1985. Use of lac fusions for the study of biological problems. Microbiol. Rev. 49:398-418.
49. Sorensen HP, Mortensen KK. 2005. Advanced genetic strategies for recombinant protein expression in Escherichia coli. J. Biotechnol. 115:113-128.
50. Sorensen HP, Mortensen KK. 2005. Soluble expression of recombinant proteins in the cytoplasm of Escherichia coli. Microb. Cell Fact. 4:1.
51. Stewart EJ, Aslund F, Beckwith J. 1998. Disulfide bond formation in the Escherichia coli cytoplasm: an in vivo role reversal for the thioredoxins. EMBO J. 17:5543-5550.
52. Terpe K. 2006. Overview of bacterial expression systems for heterologous protein production: from molecular and biochemical fundamentals to commercial systems. Appl. Microbiol. Biotechnol. 72:211-222.
53. Ye T, Lin Z, Lei H. 2008. High-level expression and characterization of an anti-VEGF165 single-chain variable fragment (scFv) by small ubiquitinrelated modifier fusion in Escherichia coli. Appl. Microbiol. Biotechnol. 81:311-317.
54. Yuan J, Martinez-Bilbao M, Huber RE. 1994. Substitutions for Glu-537 of beta-galactosidase from Escherichia coli cause large decreases in catalytic activity. Biochem. J. 299(Pt 2):527-531.
55. Yuan Z, Zhao J, Wang ZX. 2003. Flexibility analysis of enzyme active sites by crystallographic temperature actors. Protein Eng. 16:109 -114