The production of soluble and correctly folded recombinant bovine β-lactoglobulin variants A and B in Escherichia coli for NMR studies

Protein Expression and Purification

Volumn 70, Issue 2, 2010, Pages 283-289

  Ponniah, Komala ^a   Loo, Trevor S ^a   Edwards, Patrick J B ^a   Pascal, Steven M ^a   Jameson, Geoffrey B ^a   Norris, Gillian E ^a  

^a MASSEY UNIVERSITY   (New Zealand)

Author keywords

Lactoglobulin; Chaperone; Co expression; Disulfide bond; DsbC; Escherichia coli; NMR

Indexed keywords

DISULFIDE; LACTOGLOBULIN; RECOMBINANT PROTEIN;

ANIMAL; ARTICLE; BIOSYNTHESIS; CATTLE; CHEMISTRY; ESCHERICHIA COLI; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PROTEIN FOLDING; SOLUBILITY;

ANIMALS; CATTLE; DISULFIDES; ESCHERICHIA COLI; LACTOGLOBULINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN FOLDING; RECOMBINANT PROTEINS; SOLUBILITY;

BOVINAE; ESCHERICHIA COLI; EUKARYOTA; PROKARYOTA;

EID: 76749159933     PISSN: 10465928     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pep.2009.12.006     Document Type: Article

References (44)

1. Edwards P.J.B., Creamer L.K., and Jameson G.B. Structure and stability of whey proteins. In: Thompson A., Boland M., and Singh H. (Eds). Milk Proteins: From Expression to Food (2009), Elsevier, Inc., San Diego, CA 163-203
2. Sawyer L., and Kontopidis G. The core lipocalin, bovine β-lactoglobulin. Biochim. Biophys. Acta 1482 (2000) 136-148
3. Qin B.Y., Creamer L.K., Baker E.N., and Jameson G.B. 12-Bromododecanoic acid binds inside the calyx of bovine β-lactoglobulin. FEBS Lett. 438 (1998) 272-278
4. Perez M.D., and Calvo M. Interaction of β-lactoglobulin with retinol and fatty acids and its role as a possible biological function for this protein - a review. J. Dairy Sci. 78 (1995) 978-988
5. de Jong P. Impact and control of fouling in milk processing. Trends Food Sci. Technol. 8 (1997) 401-405
6. Hamada D., Segawa S., and Goto Y. Non-native α-helical intermediate in the refolding of β-lactoglobulin, a predominantly β-sheet protein. Nat. Struct. Biol. 3 (1996) 868-873
7. Ragona L., Fogolari F., Romagnoli S., Zetta L., Maubois J.L., and Molinari H. Unfolding and refolding of bovine β-lactoglobulin monitored by hydrogen exchange measurements. J. Mol. Biol. 293 (1999) 953-969
8. Hattori M., Hiramatsu K., Kurata T., Nishiura M., Takahashi K., Ametani A., and Kaminogawa S. Complete refolding of bovine β-lactoglobulin requires disulfide bond formation under strict conditions. Biochim. Biophys. Acta 1752 (2005) 154-165
9. Forge V., Hoshino M., Kuwata K., Arai M., Kuwajima K., Batt C.A., and Goto Y. Is folding of β-lactoglobulin non-hierarchic? Intermediate with native-like β-sheet and non-native α-helix. J. Mol. Biol. 296 (2000) 1039-1051
10. Kuwata K., Shastry R., Cheng H., Hoshino M., Batt C.A., Goto Y., and Roder H. Structural and kinetic characterization of early folding events in β-lactoglobulin. Nat. Struct. Biol. 8 (2001) 151-155
11. Jackson G.S., Hosszu L.L.P., Power A., Hill A.F., Kenney J., Saibil H., Craven C.J., Waltho J.P., Clarke A.R., and Collinge J. Reversible conversion of monomeric human prion protein between native and fibrilogenic conformations. Science 283 (1999) 1935-1937
12. Shiraki K., Nishikawa K., and Goto Y. Trifluoroethanol-induced stabilization of the a-helical structure of β-lactoglobulin - implication for non-hierarchical protein folding. J. Mol. Biol. 245 (1995) 180-194
13. Manderson G.A., Creamer L.K., and Hardman M.J. Effect of heat treatment on the conformation and aggregation of β-lactoglobulin A, B and C. J. Agric. Food Chem. 46 (1998) 5052-5061
14. Batt C.A., Rabson L.D., Wong D.W.S., and Kinsella J.E. Expression of recombinant bovine β-lactoglobulin in Escherichia coli. Agric. Biol. Chem. 54 (1990) 949-955
15. Ariyaratne K.A.N.S., Brown R., Dasgupta A., de Jonge J., Jameson G.B., Loo T.S., Weinberg C., and Norris G.E. Expression of bovine β-lactoglobulin as a fusion protein in Escherichia coli: a tool for investigating how structure affects function. Int. Dairy J. 12 (2002) 311-318
16. Kim T.R., Goto Y., Hirota N., Kuwata K., Denton H., Wu S.Y., Sawyer L., and Batt C.A. High-level expression of bovine β-lactoglobulin in Pichia pastoris and characterization of its physical properties. Protein Eng. 10 (1997) 1339-1345
17. Denton H., Smith M., Husi H., Uhrin D., Barlow P.N., Batt C.A., and Sawyer L. Isotopically labeled bovine β-lactoglobulin for NMR studies expressed in Pichia pastoris. Protein Expression Purif. 14 (1998) 97-103
18. Kuwata K., Hoshino M., Forge V., Era S., Batt C.A., and Goto Y. Solution structure and dynamics of bovine β-lactoglobulin A. Protein Sci. 8 (1999) 2541-2545
19. Uhrinova S., Smith M.H., Jameson G.B., Uhrin D., Sawyer L., and Barlow P.N. Structural changes accompanying pH-induced dissociation of the β-lactoglobulin dimer. Biochemistry 39 (2000) 3565-3574
20. Yagi M., Sakurai K., Kalidas C., Batt C.A., and Goto Y. Reversible unfolding of bovine β-lactoglobulin mutants without a free thiol group. J. Biol. Chem. 278 (2003) 47009-47015
21. Sakurai K., and Goto Y. Dynamics and mechanism of the Tanford transition of bovine β-lactoglobulin studied using heteronuclear NMR spectroscopy. J. Mol. Biol. 356 (2006) 483-496
22. Yagi M., Kameda A., Sakurai K., Nishimura C., and Goto Y. Disulfide-linked bovine β-lactoglobulin dimers fold slowly, navigating a glassy folding landscape. Biochemistry 47 (2008) 5996-6006
23. Bessette P.H., Aslund F., Beckwith J., and Georgiou G. Efficient folding of proteins with multiple disulfide bonds in the Escherichia coli cytoplasm. Proc. Natl. Acad. Sci. USA 96 (1999) 13703-13708
24. Kadokura H., Katzen F., and Beckwith J. Protein disulfide bond formation in prokaryotes. Annu. Rev. Biochem. 72 (2003) 111-135
25. Rietsch A., Belin D., Martin N., and Beckwith J. An in vivo pathway for disulfide bond isomerization in Escherichia coli. Proc. Natl. Acad. Sci. USA 93 (1996) 13048-13053
26. Chen J., Song J.L., Zhang S., Wang Y., Cui D.F., and Wang C.C. Chaperone activity of DsbC. J. Biol. Chem. 274 (1999) 19601-19605
27. Kurokawa Y., Yanagi H., and 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. 66 (2000) 3960-3965
28. Hu X.J., O'Hara L., White S., Magner E., Kane M., and Wall J.G. 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 Expression Purif. 52 (2007) 194-201
29. Jurado P., Ritz D., Beckwith J., de Lorenzo V., and Fernandez L.A. Production of functional single-chain Fv antibodies in the cytoplasm of Escherichia coli. J. Mol. Biol. 320 (2002) 1-10
30. Heo M.A., Kim S.H., Kim S.Y., Kim Y.J., Chung J.H., Oh M.K., and Lee S.G. Functional expression of single-chain variable fragment antibody against c-Met in the cytoplasm of Escherichia coli. Protein Expression Purif. 47 (2006) 203-209
31. Mailliart P., and Ribadeau-Dumas B. Preparation of β-lactoglobulin and β-lactoglobulin-free proteins from whey retentate by NaCl salting out at low pH. J. Food Sci. 53 (1988) 743-752
32. Manderson G.A., Creamer L.K., and Hardman M.J. Effect of heat treatment on the circular dichroism spectra of bovine β-lactoglobulin A, B, and C. J. Agric. Food Chem. 47 (1999) 4557-4567
33. Gething M.J., and Sambrook J. Protein folding in the cell. Nature 355 (1992) 33-45
34. Zapun A., Missiakas D., Raina S., and Creighton T.E. Structural and functional characterization of DsbC, a protein involved in disulfide bond formation in Escherichia coli. Biochemistry 34 (1995) 5075-5089
35. Maskos K., Huber-Wunderlich M., and Glockshuber R. DsbA and DsbC-catalyzed oxidative folding of proteins with complex disulfide bridge patterns in vitro and in vivo. J. Mol. Biol. 325 (2003) 495-513
36. Darby N.J., Raina S., and Creighton T.E. Contributions of substrate binding to the catalytic activity of DsbC. Biochemistry 37 (1998) 783-791
37. Segatori L., Paukstelis P.J., Gilbert H.F., and Georgiou G. Engineered DsbC chimeras catalyze both protein oxidation and disulfide-bond isomerization in Escherichia coli: reconciling two competing pathways. Proc. Natl. Acad. Sci. USA 101 (2004) 10018-10023
38. Schlapschy M., Grimm S., and Skerra A. A system for concomitant overexpression of four periplasmic folding catalysts to improve secretory protein production in Escherichia coli. Protein Eng., Des. Sel. 19 (2006) 385-390
39. Zhang S.T., Shi J., Zhao J., Qi Y.F., and Guo A.G. Expression of soluble and functional snake venom fibrinolytic enzyme fibrolase via the co-expression of DsbC in Escherichia coli. Protein Pept. Lett. 13 (2006) 559-563
40. Invernizzi G., Annoni E., Natalello A., Doglia S.M., and Lotti M. In vivo aggregation of bovine β-lactoglobulin is affected by Cys at position 121. Protein Expression Purif. 62 (2008) 111-115
41. Jayat D., Gaudin J.C., Chobert J.M., Burova T.V., Holt C., McNae I., Sawyer L., and Haertle T. A recombinant C121S mutant of bovine β-lactoglobulin is more susceptible to peptic digestion and to denaturation by reducing agents and heating. Biochemistry 43 (2004) 6312-6321
42. Berkmen M., Boyd D., and Beckwith J. The nonconsecutive disulfide bond of Escherichia coli phytase (AppA) renders it dependent on the protein-disulfide isomerase, DsbC. J. Biol. Chem. 280 (2005) 11387-11394
43. Gleiter S., and Bardwell J.C.A. Disulfide bond isomerization in prokaryotes. Biochim. Biophys.Acta 1783 (2008) 530-534
44. de Marco A. Strategies for successful recombinant expression of disulfide bond-dependent proteins in Escherichia coli. Microb. Cell Fact. 8 (2009) 26