Recombinant protein folding and misfolding in Escherichia coli

Nature Biotechnology

Volumn 22, Issue 11, 2004, Pages 1399-1407

  Baneyx, François ^a   Mujacic, Mirna ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLATION; BACTERIA; BIODEGRADATION; BIOTECHNOLOGY; ESCHERICHIA COLI;

GLYOCOSYLATION; PROTEIN FOLDING; PROTEIN TRANSLOCATION;

PROTEINS;

CHAPERONE; CHAPERONIN; CYTOPLASM PROTEIN; GLYCOPROTEIN; N ACETYLGLUCOSAMINE; PERIPLASMIC BINDING PROTEIN; PROTEIN DNAJ; PROTEIN DNAK; RECOMBINANT PROTEIN;

BACTERIAL TRANSLOCATION; CELL INCLUSION; COMMODIFICATION; DISULFIDE BOND; ESCHERICHIA COLI; GLYCOSYLATION; HETEROLOGOUS EXPRESSION; ISOMERIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN INTERACTION; REVIEW;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; INCLUSION BODIES; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN TRANSPORT; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 8344256552     PISSN: 10870156     EISSN: None     Source Type: Journal    
DOI: 10.1038/nbt1029     Document Type: Review

References (90)

1. Baneyx, F. Protein expression technologies: current status and future trends (Horizon Biosciences, Norfolk, 2004).
2. Lorimer, G.H. A quantitative assessment of the role of the chaperonin proteins in protein folding in vivo. FASEB J. 10, 5-9 (1996).
3. Ellis, R.J. & Minton, A.P. Join the crowd. Nature 425, 27-28 (2003).
4. Valax, P. & Georgiou, G. Molecular characterization of β-lactamase inclusion bodies produced in Escherichia coli. 1. Composition. Biotechnol. Prog. 9, 539-547 (1993).
5. Allen, S.P., Polazzi, J.O., Gierse, J.K. & Easton, A.M. Two novel heat shock genes encoding proteins produced in response to heterologous protein expression in Escherichia coli. J. Bacteriol. 174, 6938-6947 (1992).
6. Carrió, M. M., Corchero, J.L. & Villaverde, A. Dynamics of in vivo protein aggregation: building inclusion bodies in recombinant bacteria. FEMS Microbiol. Lett. 169, 9-15 (1998).
7. Bowden, G.A., Paredes, A.M. & Georgiou, G. Structure and morphology of inclusion bodies in Escherichia coli. Bio/Technology 9, 725-730 (1991).
8. Taylor, G., Hoare, M., Gray, D.R. & Martson, F.A.O. Size and density of inclusion bodies. Bio/Technology 4, 553-557 (1986).
9. Oberg, K., Chrunyk, B.A., Wetzel, R. & Fink, A.L. Nativelike secondary structure in interleukin 1-β inclusion bodies by attenuated total reflectance FTIR. Biochemistry 33, 2628-2634 (1994).
10. Tsumoto, K., Ejima, D., Kumagai, I. & Arakawa, T. Practical considerations in refolding proteins from inclusion bodies. Protein Expr. Purif. 28, 1-8 (2003).
11. Hoffmann, F. & Rinas, U. Kinetics of heat-shock response and inclusion body formation during temperature-induced production of basic fibroblast growth factor in high-cell-density cultures of recombinant Escherichia coli. Biotechnol. Prog. 16, 1000-1007 (2000).
12. Hartl, F.U. & Hayer-Hartl, M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295, 1852-1858 (2002).
13. Mujacic, M. & Baneyx, F. in Protein expression technologies: current status and future trends. (ed. Baneyx, F.) 85-148 (Horizon Biosciences, Norfolk, UK, 2004).
14. Patzelt, H. et al. Binding specificity of Escherichia coli trigger factor. Proc. Natl. Acad. Sci. USA 98, 14244-14249 (2001).
15. Deuerling, E. et al. Trigger factor and DnaK possess overlapping substrate pools and binding specificities. Mol. Microbiol. 47, 1317-1328 (2003).
16. Ewalt, K.L., Hendrick, J.P., Houry, W.A. & Hartl, F.U. In vivo observation of polypeptide flux through the bacterial chaperonin system. Cell 90, 491-500 (1997).
17. Narberhaus, F. Alpha-crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol. Mol. Biol. Rev. 66, 64-93 (2002).
18. Shearstone, J.R. & Baneyx, F. Biochemical characterization of the small heat shock protein IbpB from Escherichia coli. J. Biol. Chem. 274, 9937-9945 (1999).
19. Veinger, L., Diamant, S., Buchner, J. & Goloubinoff, P. The small heat-shock protein IbpB from Escherichia coli stabilizes stress-denatured proteins for subsequent refolding by a multichaperone network. J. Biol. Chem. 273, 11032-11037 (1998).
20. Graf, P.C. & Jakob, U. Redox-regulated molecular chaperones. Cell. Mol. Life Sci. 59, 1624-1631 (2002).
21. Hoffmann, J.H., Linke, K., Graf, P.C., Lilie, H. & Jakob, U. Identification of a redox-regulated chaperone network. EMBO J. 23, 160-168 (2004).
22. Malki, A., Kern, R., Abdallah, J. & Richarme, G. Characterization of the Escherichia coli YedU protein as a molecular chaperone. Biochem. Biophys. Res. Commun. 301, 430-436 (2003).
23. Sastry, M.S.R., Korotkov, K., Brodsky, Y. & Baneyx, F. Hsp31, the Escherichia coli yedU gene product, is a molecular chaperone whose activity is inhibited by ATP at high temperatures. J. Biol. Chem. 277, 46026-46034 (2002).
24. Mujacic, M., Bader, M.W. & Baneyx, F. Escherichia coli Hsp31 functions as a holding chaperone that cooperates with the DnaK-DnaJ-GrpE system in the management of protein misfolding under severe thermal stress conditions. Mol. Microbiol. 51, 849-859 (2004).
25. Quigley, P.M., Korotkov, K., Baneyx, F. & Hol, W.G.J. The 1.6-Å crystal structure of the class of chaperones represented by Escherichia coli Hsp31 reveals a putative catalytic triad. Proc. Natl. Acad. Sci. USA 100, 3137-3142 (2003).
26. Quigley, P.M., Korotkov, K., Baneyx, F. & Hol, W.G.J. A new native EcHsp31 crystal structure suggests key role of structural flexibility for chaperone function. Protein Sci. 13, 269-277 (2004).
27. Sastry, M.S.R., Quigley, P.M., Hol, W.G.J. & Baneyx, F. The linker-loop region of E. coli chaperone Hsp31 functions as a thermal gate that modulates high affinity substrate binding at elevated temperatures. Proc. Natl. Acad. Sci. USA 101, 8587-8592 (2004).
28. Weibezahn, J., Bukau, B. & Mogk, A. Unscrambling an egg: protein disaggregation by AAA+ proteins. Microb. Cell Fact. 3, 1 (2004).
29. Lee, S. et al. The structure of ClpB. A molecular chaperone that rescues proteins from an aggregated state. Cell 115, 229-240 (2003).
30. Schlieker, C. et al. Substrate recognition by the AAA+ chaperone ClpB. Nat. Struct. Mol. Biol. 11, 607-615 (2004).
31. Mogk, A., Deuerling, E., Vorderwulbecke, S., Vierling, E. & Bukau, B. Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Mol. Microbiol. 50, 585-595 (2003).
32. Goloubinoff, P., Mogk, A., Ben Zvi, A.P., Tomoyasu, T. & Bukau, B. Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc. Natl. Acad. Sci. USA 96, 13732-13737 (1999).
33. Zolkiewski, M. ClpB cooperates with DnaK, DnaJ and GrpE in suppressing protein aggregation. J. Biol. Chem. 274, 28083-28086 (1999).
34. Diamant, S., Ben-Zvi, A.P., Bukau, B. & Goloubinoff, P. Size-dependent disaggregation of stable protein aggregates by the DnaK chaperone machinery. J. Biol. Chem. 275, 21107-21113 (2000).
35. Zietkiewicz, S., Krzewska, J. & Liberek, K. Successive and synergistic action of the Hsp70 and Hsp100 chaperones in protein disaggregation. J. Biol. Chem. (in the press) (2004).
36. de Keyzer, J., van der Does, C. & Driessen, A.J. The bacterial translocase: a dynamic protein channel complex. Cell. Mol. Life Sci. 60, 2034-2052 (2003).
37. Xu, Z., Knafels, J.D. & Yoshino, K. Crystal structure of the bacterial protein export chaperone SecB. Nat. Struct. Biol. 7, 1172-1177 (2000).
38. Altman, E., Kumamoto, C.A. & Emr, S.D. Heat-shock proteins can substitute for SecB function during protein export in Escherichia coli. EMBO J. 10, 239-245 (1991).
39. Harms, N., Luirink, J. & Oudega, B. in Molecular chaperones in the cell (ed. Lund, P.) 35-60 (Oxford University Press, New York, 2001).
40. Driessen, A.J.M., Manting, E.H. & van der Does, C. The structural basis of protein targeting and translocation in bacteria. Nat. Struct. Biol. 8, 492-498 (2001).
41. Buskiewicz, I. et al. Trigger factor binds to ribosome-signal recognition particle (SRP) complexes and is excluded by binding of the SRP receptor. Proc. Natl. Acad. Sci. USA 101, 7902-7906 (2004).
42. DeLisa, M.P., Samuelson, P., Palmer, T. & Georgiou, G. Genetic analysis of the twin arginine translocator secretion pathway in bacteria. J. Biol. Chem. 277, 29825-29831 (2002).
43. Brüser, T. & Sanders, C. An alternative model of the twin arginine translocation system. Mircobiol. Res. 158, 7-17 (2003).
44. Palmer, T. & Berks, B.C. Moving folded protein across the bacterial cell membrane. Microbiology 149, 547-556 (2003).
45. Sargent, F. et al. Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J. 17, 3640-3650 (1998).
46. Chen, R. & Henning, U. A periplasmic protein (Skp) of Escherichia coli selectively binds a class of outer membrane proteins. Mol. Microbiol. 19, 1287-1294 (1996).
47. Schafer, U., Beck, K. & Muller, M. Skp, a molecular chaperone of gram-negative bacteria is required for the formation of soluble periplasmic intermediates of outer membrane proteins. J. Biol. Chem. 274, 24567-24574 (1999).
48. Walton, T.A. & Sousa, M.C. Crystal structure of Skp, a prefoldin-like chaperone that protects soluble and membrane proteins from aggregation. Mol. Cell 15, 367-374 (2004).
49. Missiakas, D., Betton, J.M. & Raina, S. New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA and Skp/OmpH. Mol. Microbiol. 21, 871-884 (1996).
50. Arie, J.P., Sassoon, N. & Betton, J.M. Chaperone function of FkpA, a heat shock prolyl isomerase, in the periplasm of Escherichia coli. Mol. Microbiol. 39, 199-210 (2001).
51. Saul, F.A. et al. Structural and functional studies of FkpA from Escherichia coli, a cis/trans peptidyl-prolyl isomerase with chaperone activity. J. Mol. Biol. 335, 595-608 (2004).
52. Behrens, S., Maier, R., de Cock, H., Schmid, F.X. & Gross, C.A. The SurA periplasmic PPlase lacking its parvulin domains functions in vivo and has chaperone activity. EMBO J. 20, 285-294 (2001).
53. Bitto, E. & McKay, D.B. Crystallographic structure of SurA, a molecular chaperone that facilitates folding of outer membrane porins. Structure 10, 1489-1498 (2002).
54. Bitto, E. & McKay, D.B. The periplasmic molecular chaperone protein SurA binds a peptide motif that is characteristic of integral outer membrane proteins. J. Biol. Chem. 278, 49316-49322 (2003).
55. Hiniker, A. & Bardwell, J.C.A. Disulfide bond isomerization in prokaryotes. Biochemistry 42, 1179-1185 (2003).
56. Kadokura, H., Katzen, F. & Beckwith, J. Protein disulfide bond formation in prokaryotes. Annu. Rev. Biochem. 72, 111-135 (2003).
57. McCarthy, A.A. et al. Crystal structure of the protein disulfide bond isomerase, DsbC, from Escherichia coli. Nat. Struct. Biol. 7, 196-199 (2000).
58. Missiakas, D., Schwager, F., Betton, J.M., Georgopoulos, C. & Raina, S. Identification and characterization of HsIV HsIU (ClpQ ClpY) proteins involved in overall proteolysis of misfolded proteins in Escherichia coli. EMBO J. 15, 6899-6909 (1996).
59. Tomoyasu, T., Mogk, A., Langen, H., Goloubinoff, P. & Bukau, B. Genetic dissection of the roles of chaperones and proteases in protein folding and degradation in the Escherichia coli cytosol. Mol. Microbiol. 40, 397-413 (2001).
60. Matouschek, A. Protein unfolding - an important process in vivo? Curr. Opin. Struct. Biol. 13, 98-109 (2003).
61. Kim, Y.-I. et al. Molecular determinants of complex formation between Clp/Hsp100 ATPases and the ClpP peptidase. Nat. Struct. Biol. 8, 230-233 (2001).
62. Ortega, J., Lee, H.S., Maurizi, M.R. & Steven, A.C. ClpA and ClpX ATPases bind simultaneously to opposite ends of ClpP peptidase to form active hybrid complexes. J. Struct. Biol. 146, 217-226 (2004).
63. Bochtler, M. et al. The structure of HsIU and the ATP-dependent protease HsIU-HsIV. Nature 403, 800-805 (2000).
64. Gottesman, S., Roche, E., Zhou, Y.N. & Sauer, R.T. The ClpXP and ClpAP proteases degrade proteins with carboxyl-terminal peptide tails added by the SsrA-tagging system. Genes Dev. 12, 1338-1347 (1998).
65. Dougan, D.A., Weber-Ban, E. & Bukau, B. Targeted delivery of an ssrA-tagged substrate by the protein SspB to it cognate AAA+ protein ClpX. Mol. Cell 12, 373-380 (2003).
66. Dougan, D.A., Reid, B.G., Horwich, A.L. & Bukau, B. ClpS, a substrate modulator of the ClpAP machine. Mol. Cell 9, 673-683 (2002).
67. Saikawa, N. & Akiyama, Y. & Ito, K. FtsH exists as an exceptionally large complex containing HflKC in the plasma membrane of Escherichia coli. J. Struct. Biol. 146, 123-129 (2004).
68. Krojer, T., Garrido-Franco, M., Huber, R., Ehrmann, M. & Clausen, T. Crystal structure of DegP (HtrA) reveals a new protease-chaperone machine. Nature 416, 455-459 (2002).
69. Jones, C.H. et al. Escherichia coli DegP protease cleaves between paired hydrophobic residues in a natural substrate: the PapA pilin. J. Bacteriol. 184, 5762-5771 (2002).
70. Spiess, C., Beil, A. & Ehrmann, M. A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97, 339-347 (1999).
71. Keiler, K.C. et al. C-terminal specific protein degradation: activity and substrate specificity of the Tsp protease. Protein Sci. 4, 1507-1515 (1995).
72. Spiers, A. et al. PDZ domains facilitate binding of high temperature requirement protease A (HtrA) and tail-specific protease (Tsp) to heterologous substrates through recognition of the small stable RNA A (ssrA)-encoded peptide. J. Biol. Chem. 277, 39443-39449 (2002).
73. Walsh, N.P., Alba, B.M., Bose, B., Gross, C.A. & Sauer, R.T. OMP peptide signals initiate the envelope-stress response by activating DegS protease via relief of inhibition mediated by its PDZ domain. Cell 113, 61-71 (2003).
74. Waller, P.R. & Sauer, R.T. Characterization of degQ and degS, Escherichia coli genes encoding homologs of the DegP protease. J. Bacteriol. 178, 1146-1153 (1996).
75. Baneyx, F. & Georgiou, G. Construction and characterization of Escherichia coli strains deficient in multiple secreted proteases: protease III degrades high molecular weight substrates in vivo. J. Bacteriol. 173, 2696-2703 (1991).
76. Vandeputte-Rutten, L. et al. Crystal structure of the outer membrane protease OmpT from Escherichia coli suggests a novel catalytic site. EMBO J. 20, 5033-5039 (2001).
77. White, C.B., Chen, Q., Kenyon, G.L. & Babbitt, P.C. A novel activity of OmpT. Proteolysis under extreme denaturing conditions. J. Biol. Chem. 270, 12990-12994 (1995).
78. BAD promoter in Escherichia coli by constitutive expression of the low-affinity high-capacity AraE transporter. Microbiology 147, 3241-3247 (2001).
79. Morgan-Kiss, R.M., Wadler, C. & Cronan, J.E.J. Long-term and homogeneous regulation of the Escherichia coli araBAD promoter by use of a lactose transporter of relaxed specificity. Proc. Natl. Acad. Sci. USA 99, 7373-7377 (2002).
80. Vasina, J.A. & Baneyx, F. Expression of aggregation-prone proteins at low temperatures: a comparative study of the E. coli cspA and tac promoter systems. Protein Expr. Purif. 9, 211-218 (1997).
81. Mujacic, M., Cooper, K.W. & Baneyx, F. Cold-inducible cloning vectors for low-temperature protein expression in Escherichia coli: application to the production of a toxic and proteolytically sensitive fusion protein. Gene 238, 325-332 (1999).
82. Vasina, J. A., Peterson, M.S. & Baneyx, F. Scale-up and optimization of the low-temperature inducible cspA promoter system. Biotechnol. Prog. 14, 714-721 (1998).
83. Qing, G. et al. Cold-shock induced high-yield protein production in Escherichia coli. Nat. Biotechnol. 22, 877-882 (2004).
84. Baneyx, F. & Palumbo, J.L. Improving heterologous protein folding via molecular chaperone and foldase co-expression. Methods Mol. Biol. 205, 171-197 (2003).
85. Nishihara, K., Kanemori, M., Yanagi, H. & Yura, T. Overexpression of trigger factor prevents aggregation of recombinant proteins in Escherichia coli. Appl. Environ. Microbiol. 66, 884-889 (2000).
86. Roman, L.J. et al. High-level expression of functional rat neuronal nitric oxide synthase in Escherichia coli. Proc. Natl. Acad. Sci. USA 92, 8428-8432 (1995).
87. Ayling, A. & Baneyx, F. Influence of the GroE molecular chaperone machine on the in vitro folding of Escherichia coli β-galactosidase. Protein Sci. 5, 478-487 (1996).
88. Nishihara, K., Kanemori, M., Kitagawa, M., Yanaga, H. & Yura, T. 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, 1694-1699 (1998).
89. Agashe, V.R. et al. Function of trigger factor and DnaK in multidomain protein folding: increase in yield at the expense of folding speed. Cell 117, 199-209 (2004).
90. Schneider, E.L., Thomas, J.G., Bassuk, J.A., Sage, E.H. & Baneyx, F. Manipulating the aggregation and oxidation of human SPARC in the cytoplasm of Escherichia coli.