Skip to main content
SpringerLink
Log in

Molecular chaperones, folding catalysts, and the recovery of active recombinant proteins fromE. coli

To fold or to refold

  • Accelerated Article
  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

The high-level expression of recombinant gene products in the gramnegative bacteriumEscherichia coli often results in the misfolding of the protein of interest and its subsequent degradation by cellular proteases or its deposition into biologically inactive aggregates known as inclusion bodies. It has recently become clear that in vivo protein folding is an energy-dependent process mediated by two classes of folding modulators. Molecular chaperones, such as the DnaK-DnaJ-GrpE and GroEL-GroES systems, suppress off-pathway aggregation reactions and facilitate proper folding through ATP-coordinated cycles of binding and release of folding intermediates. On the other hand, folding catalysts (foldases) accelerate rate-limiting steps along the protein folding pathway such as thecis/trans isomerization of peptidyl-prolyl bonds and the formation and reshuffling of disulfide bridges. Manipulating the cytoplasmic folding environment by increasing the intracellular concentration of all or specific folding modulators, or by inactivating genes encoding these proteins, holds great promise in facilitating the production and purification of heterologous proteins. Purified folding modulators and artificial systems that mimic their mode of action have also proven useful in improving the in vitro refolding yields of chemically denatured polypeptides. This review examines the usefulness and limitations of molecular chaperones and folding catalysts in both in vivo and in vitro folding processes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Swartz, J. R. (1996), inEscherichia coli and Salmonella Cellular and Molecular Biology, Neidhardt, F. C. Ingraham, J. L., Low, K. B., Magasanik, B., Schaecter, M., Umbarger, H. E., eds. American Society of Microbiology, Washington, D. C., pp. 1693–1711.

    Google Scholar 

  2. Hockney, R. C. (1994),Trends Biotechnol. 12, 456–463.

    Article  CAS  Google Scholar 

  3. Georgiou, G. (1995), inPrinciples and Practice of Protein Engineering, Cleland, J. L. and Craik, C. S., eds. Butterworths, New York, pp. 101–127.

    Google Scholar 

  4. Georgiou, G. and Valax, P. (1996),Curr. Opin. Biotechnol. 7, 190–197.

    Article  CAS  Google Scholar 

  5. Makrides, S. C. (1996),Microbiol. Rev. 60, 512–538.

    CAS  Google Scholar 

  6. Rudolph, R. and Lilie, H. (1996),FASEB J. 10, 49–56.

    CAS  Google Scholar 

  7. Roman, L. J., Sheta, E. A., Martasek, P., Gross, S. S., Liu, Q., and Masters, B. S. S. (1995),Proc. Natl. Acad. Sci. USA 92, 8428–8432.

    Article  CAS  Google Scholar 

  8. Marston, F. A. (1986),Biochem. J. 240, 1–12.

    CAS  Google Scholar 

  9. Georgiou, G. and Bowden, G. A. (1990), inRecombinant DNA Technology and Applications, Prokop, A., Bajpai, R. K., and Ho, C., eds. McGraw-Hill, New York, pp. 333–356.

    Google Scholar 

  10. Blum, P., Velligan, M., Lin, N., and Matin, A. (1992),Bio/Technology 10, 301–304.

    Article  CAS  Google Scholar 

  11. Wilkinson, D. L. and Harrison, R. G. (1991),Bio/Technology 9, 443–448.

    Article  CAS  Google Scholar 

  12. Mitraki, A. and King, J. (1989),Bio/Technology 7, 690–697.

    Article  CAS  Google Scholar 

  13. Wetzel, R. (1994),Trends Biotechnol. 12, 193–198.

    Article  CAS  Google Scholar 

  14. Oberg, K., Chrunyk, B. A., Wetzel, R., and Fink, A. L. (1994),Biochemistry 33, 2628–2634.

    Article  CAS  Google Scholar 

  15. Przybycien, T. M., Dunn, J. P., Valax, P., and Georgiou, G. (1994),Protein Eng. 7, 131–136.

    Article  CAS  Google Scholar 

  16. Georgopoulos, C. and Welch, W. J. (1993),Annu. Rev. Cell Biol. 9, 601–634.

    Article  CAS  Google Scholar 

  17. Bardwell, J. C. (1994),Mol. Microbiol. 14, 199–205.

    Article  CAS  Google Scholar 

  18. Fischer, G. (1994),Angew. Chem. Int. Ed. Engl. 33, 1415–1436.

    Article  Google Scholar 

  19. Freedman, R. B., Hirst, T. R., and Tuite, M. F. (1994),Trends Biochem. Sci. 19, 331–336.

    Article  CAS  Google Scholar 

  20. Galat, A. and Metcalfe, S. M. (1995),Prog. Biophys. Mol. Biol. 63, 67–118.

    Article  CAS  Google Scholar 

  21. Hartl, F.-U. and Martin, J. (1995),Curr. Opin. Struct. Biol. 5, 92–102.

    Article  CAS  Google Scholar 

  22. Buchner, J. (1996),FASEB J. 10, 10–19.

    CAS  Google Scholar 

  23. Hartl, F. U. (1996),Nature 381, 571–579.

    Article  CAS  Google Scholar 

  24. Mitraki, A. and King, J. (1992),FEBS Lett. 307, 20–25.

    Article  CAS  Google Scholar 

  25. Wetzel, R., Perry, L. J., and Veilleux, C. (1991),Bio/Technology 9, 731–777.

    Article  CAS  Google Scholar 

  26. Chrunyk, B. A., Evans, J., Lillquist, J., Young, P., and Wetzel, R. (1993),J. Biol. Chem. 268, 18,053–18,061.

    CAS  Google Scholar 

  27. Wetzel, R. and Chrunyk, B. A. (1994),FEBS Lett. 350, 245–248.

    Article  CAS  Google Scholar 

  28. Dale, G. E., Broger, C., Langen, H., D’Arcy, A., and Stuber, D. (1994),Protein Eng. 7, 933–939.

    Article  CAS  Google Scholar 

  29. LaVallie, E. R. and McCoy, J. M. (1995),Curr. Opin. Biotechnol. 6, 501–506.

    Article  CAS  Google Scholar 

  30. LaVallie, E. R., DiBlasio, E. A., Kovacic, S., Grant, K. L., Schendel, P. F., and McCoy, J. M. (1993),Bio/Technology 11, 187–193.

    Article  CAS  Google Scholar 

  31. Wall, J. G. and Plückthun, A. (1995),Curr. Opin. Biotechnol. 6, 507–516.

    Article  CAS  Google Scholar 

  32. Guise, A. D., West, S. M., and Chaudhuri, J. B. (1996),Mol. Biotechnol. 6, 53–64.

    Article  CAS  Google Scholar 

  33. Neidhardt, F. C. and VanBogelen, R. A. (1987), inEscherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, Neidhardt, F. C., Ingraham, J. L., Low, K. B., Magasanik, B., Schaecter, M., and Umbarger, H. E., eds. American Society for Microbiology, Washington D.C., pp. 1334, 1345.

    Google Scholar 

  34. Parsell, D. A. and Sauer, R. T. (1989),Genes Dev. 3, 1226–1232.

    Article  CAS  Google Scholar 

  35. Betton, J. M. and Hofnung, M. (1996),J. Biol. Chem. 271, 8046–8052.

    Article  CAS  Google Scholar 

  36. Rinas, U. (1996),Biotechnol. Prog. 12, 196–200.

    Article  CAS  Google Scholar 

  37. Gross, C. A. (1996),Escherichia coli and Salmonella Cellular and Molecular Biology, Neidhardt, F. C. ???Ingraham, J. L., Low, K. B., Magasanik, B., Schaecter, M., Umbarger, H. E. eds. American Society of Microbiology, Washington, D. C., pp. 1382–1399.

    Google Scholar 

  38. Herman, C., Thévenet, D., D’Ari, R., and Bouloc, P. (1995),Proc. Natl. Acad. Sci. USA 92, 3516–3520.

    Article  CAS  Google Scholar 

  39. Craig, E. A. and Gross, C. A. (1991),Trends Biochem. Sci. 16, 135–140.

    Article  CAS  Google Scholar 

  40. Gragerov, A. L., Nudler, E., Komissarova, E., Gaitanaris, G. A., Gottesman, M. E., and Nikiforov, V. G. (1992),Proc. Natl. Acad. Sci. USA 89, 10,341–10,344.

    Article  CAS  Google Scholar 

  41. Langer, T., Lu, C., Echols, H., Flanagan, J., Hayer, M. K., and Hartl, F.-U. (1992),Nature 356, 683–689.

    Article  CAS  Google Scholar 

  42. Petit, M.-A., Bedale, W., Osipiuk, J., Lu, C., Rajagopalan, M., McInerney, P., Goodman, M. F., and Echols, H. (1994),J. Biol. Chem. 269, 23,824–23,829.

    CAS  Google Scholar 

  43. Buchberger, A., Schröder, H., Hesterkamp, T., Schönfeld, H.-J., and Bukau, B. (1996),J. Mol. Biol. 261, 328–333.

    Article  CAS  Google Scholar 

  44. Schröder, H., Langer, T., Hartl, F.-U., and Bukau, B. (1993),EMBO J. 12, 4137–4144.

    Google Scholar 

  45. Gaitanaris, G. A., Vysokanov, A., Hung, S. C., Gottesman, M. E., and Gragerov, A. (1994),Mol. Microbiol. 14, 861–869.

    Article  CAS  Google Scholar 

  46. Thomas, J. G. and Baneyx, F. (1996),Mol. Microbiol. 21, 1185–1196.

    Article  CAS  Google Scholar 

  47. Szabo, A., Langer, T., Schröder, H., Flanagan, J., Bukau, B., and Hartl, F.-U. (1994),Proc. Natl. Acad. Sci. USA 91, 10,345–10,349.

    CAS  Google Scholar 

  48. Thomas, J. G. and Baneyx, F. (1996),J. Biol. Chem. 271, 11,141–11,147.

    CAS  Google Scholar 

  49. Goloubinoff, P., Gatenby, A. A., and Lorimer, G. H. (1989),Nature 337, 44–47.

    Article  CAS  Google Scholar 

  50. Lee, S. C. and Olins, P. O. (1992),J. Biol. Chem. 267, 2849–2852.

    CAS  Google Scholar 

  51. Battistoni, A., Carri, M. T., Steinkuhler, C., and Rotilio, G. (1993),FEBS Lett. 322, 6–9.

    Article  CAS  Google Scholar 

  52. Dale, G. E., Schönfeld, H. J., Langen, H., and Stieger, M. (1994),Protein Eng. 7, 925–931.

    Article  CAS  Google Scholar 

  53. Caspers, P., Stieger, M., and Burn, P. (1994),Cell. Mol. Biol. 40, 635–644.

    CAS  Google Scholar 

  54. Schneider, E. L., Thomas, J. G., Bassuk, J. A., Sage, E. H., and Baneyx, F. submitted for publication.

  55. Hendrick, J. P., Langer, T., Davis, T. A., Hartl, F. U., and Wiedmann, M. (1993),Proc. Natl. Acad. Sci. USA 90, 10,216–10,220.

    Article  CAS  Google Scholar 

  56. Kudlicki, W., Odom, O. W., Kramer, G., and Hardesty, B. (1994),J. Mol. Biol. 244, 319–331.

    Article  CAS  Google Scholar 

  57. Fong, G. and Bridger, W. A. (1992),Biochemistry 31, 5661–5664.

    Article  CAS  Google Scholar 

  58. Horwich, A. L., Low, K. B., Fenton, W. A., Hirshfield, I. N., and Furtak, K. (1993),Cell 74, 909–917.

    Article  CAS  Google Scholar 

  59. Weissman, J. S., Hohl, C. M., Kovalenko, O., Kashi, Y., Chen, S., Braig, K., Saibil, H. R., Fenton, W. A., and Horwich, A. L. (1995),Cell 83, 577–587.

    Article  CAS  Google Scholar 

  60. Mayhew, M., daSilva, A. C. R., Martin, J., ErdjumentBromage, H., Tempst, P., and Hartl, F.-U. (1996),Nature 379, 420–126.

    Article  CAS  Google Scholar 

  61. Blum, P., Ory, J., Bauernfeind, J., and Krska, J. (1992),J. Bacteriol. 174, 7436–7444.

    CAS  Google Scholar 

  62. Liberek, K., Marzlalek, J., Ang, D., and Georgopoulos, C. (1991),Proc. Natl. Acad. Sci. USA 88, 2874–2878.

    Article  CAS  Google Scholar 

  63. Davie, J. R., Wynn, R. M., Meng, M., Huang, Y. S., Aalund, G., Chuang, D. T., and Lau, K. S. (1995),J. Biol. Chem. 270, 19,861–19,867.

    CAS  Google Scholar 

  64. Martasek, P., Liu, Q., Liu, J., Roman, L. J., Gross, S. S., Sessa, W. C., and Masters, B. S. (1996),Biochem. Biophys. Res. Comm. 219, 359–365.

    Article  CAS  Google Scholar 

  65. Ueguchi, C. and Ito, K. (1992),J. Bacteriol. 174, 1454–1461.

    CAS  Google Scholar 

  66. Shirai, Y., Akiyama, Y., and Ito, K. (1996),J. Bacteriol. 178, 1141–1145.

    CAS  Google Scholar 

  67. Gottesman, S. (1996),Ann. Rev. Genet. 30, 465–506.

    Article  CAS  Google Scholar 

  68. Wawrzynów, A., Banecki, B., and Zylicz, M. (1996),Mol. Microbiol. 21, 895–899.

    Article  Google Scholar 

  69. Wickner, S., Gottesman, S., Skowyra, D., Hoskins, J., McKenney, K., and Maurizi, M. R. (1994),Proc. Natl. Acad. Sci. USA 91, 12,218–12,222.

    Article  CAS  Google Scholar 

  70. Wawrzynów, A., Wojtkowiak, D., Marszalek, J., Banecki, B., Jonsen, M., Graves, B., Georgopoulos, C., and Zylicz, M. (1995),EMBO J. 14, 1867–1877.

    Google Scholar 

  71. Allen, S. P., Polazzi, J. O., Gierse, J. K., and Easton, A. M. (1992),J. Bacteriol. 174, 6938–6947.

    CAS  Google Scholar 

  72. Laskowska, E., Wawrzynów, A., and Taylor, A. (1996),Biochimie 78, 117–122.

    Article  CAS  Google Scholar 

  73. Wülfing, C. and Plückthun, A. (1994),Mol. Microbiol. 12, 685–692.

    Article  Google Scholar 

  74. Nossal, N. G. and Heppel, L. A. (1966),J. Biol. Chem. 241, 3055–3062.

    CAS  Google Scholar 

  75. Pugsley, A. P. (1993),Microbiol. Rev. 57, 50–108.

    CAS  Google Scholar 

  76. BlaauwendenT, Driessen A. J. (1996),Arch. Microbiol. 165, 1–8.

    Article  Google Scholar 

  77. Kusukawa, N., Yura, T., Ueguchi, C., Akiyama, Y., and Ito, K. (1989),EMBO J. 8, 3517–3521.

    CAS  Google Scholar 

  78. Wild, J., Altman, E., Yura, T., and Gross, C. A. (1992),Genes Dev. 6, 1165–1172.

    Article  CAS  Google Scholar 

  79. Wild, J., Rossmeissl, P., Walter, W. A., and Gross, C. A. (1996),J. Bacteriol. 178, 3608–3613.

    CAS  Google Scholar 

  80. Bergès, H., Joseph-Liauzun, E., and Fayet, O. (1996),Appl. Environ. Microbiol. 62, 55–60.

    Google Scholar 

  81. Thomas, J. G. and Baneyx, F. submitted for publication.

  82. Bowden, G. A. and Georgiou, G. (1990),J. Biol. Chem. 265, 16,760–16,766.

    CAS  Google Scholar 

  83. Pérez-Pérez, J., M’Arquez, G., Barbero, J. L., and Gutiérrez, J. (1994),Bio/Technology 12, 178–180.

    Article  Google Scholar 

  84. Kiino, D. R., Phillips, G. J., and Silhavy, T. J. (1990),J. Bacteriol. 172, 185–192.

    CAS  Google Scholar 

  85. Minas, W. and Bailey, J. E. (1995),Biotechnol. Prog. 11, 403–411.

    Article  CAS  Google Scholar 

  86. Missiakas, D., Betton, J.-M., and Raina, S. (1996),Mol. Microbiol. 21, 871–884.

    Article  CAS  Google Scholar 

  87. Kalbach, C. E. and Gatenby, A. A. (1993),Enzyme Microb. Technol. 15, 730–735.

    Article  CAS  Google Scholar 

  88. Straus, D. B., Walter, W. A., and Gross, C. A. (1989),Genes Dev. 3, 2003–2010.

    Article  CAS  Google Scholar 

  89. Tilly, K., Spence, J., and Georgopoulos, C. (1989),J. Bacteriol. 171, 1585–1589.

    CAS  Google Scholar 

  90. Straus, D., Walter, W., and Gross, C. A. (1990),Genes Dev. 4, 2202–2209.

    Article  CAS  Google Scholar 

  91. Yoo, S. J., Soel, H. J., Shin, D. H., Rohrwild, M., Kang, M.-S., Tanaka, K., Goldberg, A. L., and Chung, C. H. (1996),J. Biol. Chem. 271, 14,035–14,040.

    CAS  Google Scholar 

  92. Missiakas, D., Schwager, F., Betton, J.-M., Georgopoulos, C., and Raina, S. (1996),EMBO J. 15, 6899–6909.

    CAS  Google Scholar 

  93. Sherman, M. Y. and Goldberg, A. L. (1996),EXS 77, 57–78.

    CAS  Google Scholar 

  94. Gottesman, S. (1991), inGene Expression Technology, Goeddel, D. V., ed. Academic, New York, pp. 119–129.

    Google Scholar 

  95. Meerman, H. J. and Georgiou, G. (1994),Bio/Technology 12, 1107–1110.

    Article  CAS  Google Scholar 

  96. Kiselev, V. I. and Tarasova, I. M. (1988),Biotech. Appl. Biochem. 10, 59–62.

    CAS  Google Scholar 

  97. Baneyx, F. and Georgiou, G. (1992), inStability of Protein Pharmaceuticals. Part A: Chemical and Physical Pathways of Protein Degradation, Ahern, T. J. and Manning, M. C., eds. Plenum, New York, pp. 69–108.

    Google Scholar 

  98. Lim, V. I. and Spirin, A. S. (1986),J. Mol. Biol. 188, 565–574.

    Article  CAS  Google Scholar 

  99. MacArthur, M. W. and Thornton, J. M. (1991),J. Mol. Biol. 218, 397–412.

    Article  CAS  Google Scholar 

  100. Kleerebezem, M., Heutink, M., and Tommassen, J. (1995),Mol. Microbiol. 18, 313–320.

    Article  CAS  Google Scholar 

  101. Beck, R., Crooke, H., Jarsch, M., Cole, J., and Burtscher, H. (1994),FEMS Microbiol. Lett. 124, 209–214.

    Article  CAS  Google Scholar 

  102. Knappik, A., Krebber, C., and Plückthun, A. (1993),Bio/Technology 11, 77–83.

    Article  CAS  Google Scholar 

  103. Rouvière, P. E. and Gross, C. A. (1996),Genes Dev. 10, 3170–3182.

    Article  Google Scholar 

  104. Lazar, S. W. and Kolter, R. (1996),J. Bacteriol. 178, 1770–1773.

    CAS  Google Scholar 

  105. Home, S. M. and Young, K. D. (1994),Arch. Microbiol. 163, 357–365.

    Google Scholar 

  106. Crooke, E. and Wickner, W. (1987),Proc. Natl. Acad. Sci. USA 84, 5216–5220.

    Article  CAS  Google Scholar 

  107. Hesterkamp, T., Hauser, S., Lütcke, H., and Bukau, B. (1996),Proc. Natl. Acad. Sci. USA 93, 4437–4441.

    Article  CAS  Google Scholar 

  108. Zapun, A., Missiakas, D., Raina, S., and Creighton, T. E. (1995),Biochemistry 34, 5075–5089.

    Article  CAS  Google Scholar 

  109. Missiakas, D., Schwager, F., and Raina, S. (1995),EMBO J. 14, 3415–3424.

    CAS  Google Scholar 

  110. Wülfing, C. and Plückthun, A. (1994),J. Mol. Biol. 242, 655–669.

    Article  Google Scholar 

  111. Wunderlich, M. and Glockshunber, R. (1993),J. Biol. Chem. 268, 24,547–24,550.

    CAS  Google Scholar 

  112. Alksne, L. E., Keeney, D., and Rasmunssen, B. A. (1995),J. Bacteriol. 177, 462–464.

    CAS  Google Scholar 

  113. Georgiou, G. (1996), personal communication (University of Texas, Austin).

  114. Ostermeier, M., De Sutter, K., and Georgiou, G. (1996),J. Biol. Chem. 271, 10,616–10,622.

    CAS  Google Scholar 

  115. Humphreys, D. P., Weir, N., Mountain, A., and Lund, P. A. (1995),J. Biol. Chem. 270, 28,210–28,215.

    CAS  Google Scholar 

  116. Humphreys, D. P., Weir, N., Lawson, A., Mountain, A., and Lund, P. A. (1996),FEBS Lett. 380, 194–197.

    Article  Google Scholar 

  117. Derman, A. I., Prinz, W. A., Belin, D., and Beckwith, J. (1993),Science 262, 1744–1747.

    Article  CAS  Google Scholar 

  118. Proba, K., Ge, L., and Plückthun, A. (1995),Gene 159, 203–207.

    Article  CAS  Google Scholar 

  119. Yasukawa, T., Kanei-Ishii, C., Maekawa, T., Fujimoto, J., Yamamoto, T., and Ishii, S. (1995),J. Biol. Chem. 270, 25,328–25,331.

    CAS  Google Scholar 

  120. Thomas, J. G. and Baneyx, F. (1996),Ann. NY Acad. Sci. 782, 478–485.

    Article  CAS  Google Scholar 

  121. Rudolph, R. (1990), inModern Methods in Protein and Nucleic Acid Research, Tschesche, H., ed. de Gruyter, Berlin, pp. 149–171.

    Google Scholar 

  122. Buchner, J., Pastan, I., and Brinkmann, U. (1992),Anal. Biochem. 205, 263–270.

    Article  CAS  Google Scholar 

  123. Chaudhuri, J. B. (1994),Ann. NY Acad. Sci. 721, 374–385.

    Article  CAS  Google Scholar 

  124. Buchner, J. and Rudolph, R. (1991),Bio/Technology 9, 157–162.

    Article  CAS  Google Scholar 

  125. Cleland, J. L. and Wang, D. I. C. (1990),Bio/Technology 8, 1274–1278.

    Article  CAS  Google Scholar 

  126. Cleland, J. L., Builder, S. E., Swartz, J. R., Winkler, M., Chang, J. Y., and Wang, D. I. (1992),Bio/Technology 10, 1013–1019.

    Article  CAS  Google Scholar 

  127. Hagen, A. J., Hatton, T. A., and Wang, D. I. C. (1990),Biotechnol. Bioeng. 35, 955–965.

    Article  CAS  Google Scholar 

  128. Ellis, R. J. and Hartl, F.-U. (1996),FASEB J. 10, 20–26.

    CAS  Google Scholar 

  129. Brunschier, R., Danner, M., and Seckler, R. (1993),J. Biol. Chem. 268, 2767–2772.

    CAS  Google Scholar 

  130. Hansen, J. E. and Gafni, A. (1993),J. Biol. Chem. 268, 21,632–21,636.

    CAS  Google Scholar 

  131. Schmidt, M., Buchner, J., Todd, M. J., Lorimer, G. H., and Viitanen, P. V. (1994),J. Biol. Chem. 269, 10,304–10,311.

    CAS  Google Scholar 

  132. Ayling, A. and Baneyx, F. (1996),Protein Sci. 5, 478–487.

    CAS  Google Scholar 

  133. Gray, T. E. and Fersht, A. R. (1993),J. Mol. Biol. 232, 1197–1207.

    Article  CAS  Google Scholar 

  134. Tian, G., Vainberg, I. E., Tap, W. D., Lewis, S. A., and Cowan, N. J. (1995),Nature 375, 250–253.

    Article  CAS  Google Scholar 

  135. Buchner, J., Brinkmann, U., and Pastan, I. (1992),Bio/Technology 10, 682–685.

    Article  CAS  Google Scholar 

  136. Jakob, U. and Buchner, J. (1994),Trends Biochem. Sci. 19, 205–211.

    Article  CAS  Google Scholar 

  137. Wiech, H., Buchner, J., Zimmermann, R., and Jakob, U. (1992),Nature 358, 169–170.

    Article  CAS  Google Scholar 

  138. Jakob, U., Lilie, H., Meyer, I., and Buchner, J. (1995),J. Biol. Chem. 270, 7288–7294.

    Article  CAS  Google Scholar 

  139. Freeman, B. C. and Morimoto, R. I. (1996),EMBO J. 15, 2969–2979.

    CAS  Google Scholar 

  140. Noiva, R. and Lennarz, W. J. (1992),J. Biol. Chem. 267, 3553–3556.

    CAS  Google Scholar 

  141. Puig, A. and Gilbert, H. F. (1994),J. Biol. Chem. 269, 7764–7771.

    CAS  Google Scholar 

  142. Joly, J. C. and Swartz, J. R. (1994),Biochemistry 33, 4231–4236.

    Article  CAS  Google Scholar 

  143. Crouy-Chanel, de A., Kohiyama, M., and Richarme, G. (1995),J. Biol. Chem. 270, 22,669–22,672.

    Google Scholar 

  144. Lilie, H., Lang, K., Rudolph, R., and Buchner, J. (1993),Protein Sci. 2, 1490–1496.

    Article  CAS  Google Scholar 

  145. Freskgard, P. O., Bergenhem, N., Jonsson, B. H., Svensson, M., and Carlsson, U. (1992),Science 258, 466–468.

    Article  CAS  Google Scholar 

  146. Phadtare, S., Fisher, M. T., and Yarbrough, L. R. (1994),Biochim. Biophys. Acta 1208, 189–192.

    CAS  Google Scholar 

  147. Makino, Y., Taguchi, H., and Yoshida, M. (1993),FEBS Lett. 336, 363–367.

    Article  CAS  Google Scholar 

  148. Zahn, R., Buckle, A. M., Perrett, S., Johnson, C. M., Corrales, F. J., Golbik, R., and Fersht, A. R. (1996),Proc. Natl. Acad. Sci. USA 93, 15,024–15,029.

    Article  CAS  Google Scholar 

  149. Taguchi, H., Makino, Y., and Yoshida, M. (1994),J. Biol. Chem. 269, 8529–8534.

    CAS  Google Scholar 

  150. Rozema, D. and Gellman, S. H. (1995),J. Am. Chem. Soc. 117, 2373–2374.

    Article  CAS  Google Scholar 

  151. Rozema, D. and Gellman, S. H. (1996),J. Biol. Chem. 271, 3478–3487.

    Article  CAS  Google Scholar 

  152. Rozema, D. and Gellman, S. H. (1996),Biochemistry 35, 15,760–15,771.

    Article  CAS  Google Scholar 

  153. Zardeneta, G. and Horowitz, P. M. (1992),J. Biol. Chem. 267, 5811–5816.

    CAS  Google Scholar 

  154. Karuppiah, N. and Sharma, A. (1995),Biochem. Biophys. Res. Comm. 211, 60–66.

    Article  CAS  Google Scholar 

  155. Xie, Y. and Wetlaufer, D. B. (1996),Protein Sci. 5, 517–523.

    CAS  Google Scholar 

  156. Stempfer, G., HollNeugebauer, B., and Rudolph, R. (1996),Nature Biotech. 14, 329–334.

    Article  CAS  Google Scholar 

  157. Hsu, T. A., Eiden, J. J., and Betenbaugh, M. J. (1994),Ann. NY Acad. Sci. 721, 208–217.

    Article  CAS  Google Scholar 

  158. Chen, Y., Pioli, D., and Piper, P. W. (1994),Bio/Technology 12, 819–823.

    Article  CAS  Google Scholar 

  159. Robinson, A. S., Hines, V., and Wittrup, K. D. (1994),Bio/Technology 12, 381–384.

    Article  CAS  Google Scholar 

  160. Voellmy, R. (1996),Cell Stress Chap. 1, 29–32.

    Article  CAS  Google Scholar 

  161. Peek, J. A. and Taylor, R. K. (1992),Proc. Natl. Acad. Sci. USA 89, 6210–6214.

    Article  CAS  Google Scholar 

  162. Ferreyra, R. G., Soncini, F. C., and Viale, A. M. (1993),J. Bacterial. 175, 1514–1523.

    CAS  Google Scholar 

  163. Carrillo, N., Ceccarelli, E. A., Krapp, A. R., Boggio, S., Ferreyra, R. G., and Viale, A. M. (1992),J. Biol. Chem. 267, 15,537–15,541.

    CAS  Google Scholar 

  164. Escher, A. and Szalay, A. A. (1993),Mol. Gen. Genet. 238, 65–73.

    CAS  Google Scholar 

  165. Wynn, R. M., Davie, J. R., Cox, R. P., and Chuang, D. T. (1992),J. Biol. Chem. 267, 12,400–12,403.

    CAS  Google Scholar 

  166. Chuang, D. T., Davie, J. R., Wynn, R. M., Chuang, J. L., Koyata, H., and Cox, R. P. (1995),J. Nutr. 125, 1766S-1772S.

    CAS  Google Scholar 

  167. Andresen, B. S., Bross, P., Jensen, T. G., Knudsen, I., Winter, V., Kølvraa, S., Bolund, L., and Gregersen, N. (1995),Scand. J. Clin. Lab. Invest. Suppl. 220, 9–25.

    CAS  Google Scholar 

  168. Bross, P., Andresen, B. S., Winter, V., Kräulte, F., Jensen, T. G., Nandy, A., Kølvraa, S., Ghisla, S., Bolund, L., and Gregersen, N. (1993),Biochim. Biophys. Acta 1192, 264–274.

    Google Scholar 

  169. Lawson, J. E., Niu, X. D., Browning, K. S., Trong, H. L., Yan, J., and Reed, L. J. (1993),Biochemistry 32, 8987–8993.

    Article  CAS  Google Scholar 

  170. Amrein, K. E., Takacs, B., Stieger, M., Molnos, J., Flint, N. A., and Burn, P. (1995),Proc. Natl. Acad. Sci. USA 92, 1048–1052.

    Article  CAS  Google Scholar 

  171. Dueñas, M., Vázquez, J., Ayala, M., Söderlind, E., Ohlin, M., Pérez, L., Borrebaeck, C. A. K., and Gavilondo, J. V. (1994),BioTechniques 16, 476–483.

    Google Scholar 

  172. Gordon, C. L., Sather, S. K., Casjens, S., and King, J. (1994),J. Biol. Chem. 269, 27,941–27,951.

    CAS  Google Scholar 

  173. Ashiuchi, M., Yoshimura, T., Kitamura, T., Kawata, Y., Nagai, J., Gorlatov, S., Esaki, N., and Soda, K. (1995),J. Biochem. 117, 495–498.

    CAS  Google Scholar 

  174. Phillips, G. J. and Silhavy, T. J. (1990),Nature 344, 882–884.

    Article  CAS  Google Scholar 

  175. Fraipont, C., Adam, M., Nguyen-Disteche, M., Keck, W., Van-Beeumen, J., Ayala, J. A., Granier, B., Hara, H., and Ghuysen, J. M. (1994),Biochem. J. 298, 189–195.

    CAS  Google Scholar 

  176. Sato, K., Sato, M. H., Yamaguchi, A., and Yoshida, M. (1994),Biochem. Biophys. Res. Comm. 202, 258–264.

    Article  CAS  Google Scholar 

  177. Battistoni, A., Mazzetti, A. P., Petruzzelli, R., Muramatsu, M., Federici, G., Ricci, G., and Lo-Bello, M. (1995),Protein Expr. Purif. 6, 579–587.

    Article  CAS  Google Scholar 

  178. Pérez-Pérez, J., Martínez-Caja, C., Barbero, J. L., and Gutiérrez, J. (1995),Biochem. Biophys. Res. Comm. 210, 524–529.

    Article  Google Scholar 

  179. Kashlev, M. V., Gragerov, A. I., and Nikiforov, V. G. (1989),Mol. Gen. Genet. 216, 469–474.

    Article  CAS  Google Scholar 

  180. Steczko, J., Donoho, G. A., Dixon, J. E., Sugimoto, T., and Axelrod, B. (1991),Protein Expr. Purif. 2, 221–227.

    Article  CAS  Google Scholar 

  181. Wynn, R. M., Davie, J. R., Zhi, W., Cox, R. P., and Chuang, D. T. (1994),Biochemistry 33, 8962–8968.

    Article  CAS  Google Scholar 

  182. Mendoza, J. A., Rogers, E., Lorimer, G. H., and Horowitz, P. M. (1991),J. Biol. Chem. 266, 13,044–13,049.

    CAS  Google Scholar 

  183. Martin, J., Langer, T., Boteva, R., Schramel, A., Horwich, A. L., and Hartl, F.-U. (1991),Nature 352, 36–42.

    Article  CAS  Google Scholar 

  184. Zheng, X., Rosenberg, L. E., Kalousek, F., and Fenton, W. A. (1993),J. Biol. Chem. 268, 7489–7493.

    CAS  Google Scholar 

  185. Viitanen, P. V., Gatenby, A. A., and Lorimer, G. H. (1992),Protein Sci. 1, 363–369.

    CAS  Google Scholar 

  186. Baneyx, F. and Gatenby, A. A. (1992),J. Biol. Chem. 267, 11,637–11,644.

    CAS  Google Scholar 

  187. Goloubinoff, P., Christeller, J. T., Gatenby, A. A., and Lorimer, G. H. (1989),Nature 342, 884–889.

    Article  CAS  Google Scholar 

  188. Grimm, R., Donaldson, G. K., van der Vies, S. M., Schafer, E., and Gatenby, A. A. (1993),J. Biol. Chem. 268, 5220–5226.

    CAS  Google Scholar 

  189. Mizobata, T., Akiyama, Y., Ito, K., Yumoto, N., and Kawata, Y. (1992),J. Biol. Chem. 267, 17,773–17,779.

    CAS  Google Scholar 

  190. Miller, A. D., Maghlaoui, K., Albanese, G., Kleinjan, D. A., and Smith, C. (1993),Biochem. J. 291, 139–144.

    CAS  Google Scholar 

  191. Peralta, D., Hartman, D. J., Hoogenrad, N. J., and Hoj, P. B. (1994),FEBS Lett. 339, 49–45.

    Article  Google Scholar 

  192. Fisher, M. T. (1992),Biochemistry 31, 3955–3963.

    Article  CAS  Google Scholar 

  193. Fisher, M. T. (1993),J. Biol. Chem. 268, 13,777–13,779.

    CAS  Google Scholar 

  194. Fisher, M. T. (1994),J. Biol. Chem. 269, 13,629–13,636.

    CAS  Google Scholar 

  195. Buchner, J., Schmidt, M., Fuchs, M., Jaenicke, R., Rudolph, R., Schmid, F. X., and Kiefhaber, T. (1991),Biochemistry 30, 1586–1591.

    Article  CAS  Google Scholar 

  196. Zhi, W., Landry, S. J., Gierasch, L. M., and Srere, P. A. (1992),Protein Sci. 1, 522–529.

    Article  CAS  Google Scholar 

  197. Kern, G., Schmidt, M., Buchner, J., and Jaenicke, R. (1992),FEBS Lett. 305, 203–205.

    Article  CAS  Google Scholar 

  198. Jackson, G. S., Staniforth, R. A., Halsall, D. J., Atkinson, T., Holbrook, J. J., Clarke, A. R., and Burston, S. G. (1993),Biochemistry 32, 2554–2563.

    Article  CAS  Google Scholar 

  199. Badcoe, I. G., Smith, C. J., Wood, S., Halsall, D. J., Holbrook, J. J., Lund, P., and Clarke, A. R. (1991),Biochemistry 30, 9195–9200.

    Article  CAS  Google Scholar 

  200. Schmidt, M. and Buchner, J. (1992),J. Biol. Chem. 267, 16,829–16,833.

    CAS  Google Scholar 

  201. Laminet, A. A., Ziegelhoffer, T., Georgopoulos, C., and Pluckthun, A. (1990),EMBO J. 9, 2315–2319.

    CAS  Google Scholar 

  202. Holl-Neugebauer, B. and Rudolph, R. (1991),Biochemistry 30, 11,609–11,614.

    Article  CAS  Google Scholar 

  203. Levy, E. J., McCarty, J., Bukau, B., and Chiciro, W. J. (1995),FEBS Lett. 368, 435–440.

    Article  CAS  Google Scholar 

  204. Freeman, B. C., Myers, M. P., Schumacher, R., and Morimoto, R. I. (1995),EMBO J. 14, 2281–2292.

    CAS  Google Scholar 

  205. Ziemienowicz, A., Zylicz, M., Floth, C., and Hubscher, U. (1995),J. Biol. Chem. 270, 15,479–15,484.

    CAS  Google Scholar 

  206. Jakob, U., Gaestel, M., Engel, K., and Buchner, J. (1993),J. Biol. Chem. 268, 1517–1520.

    CAS  Google Scholar 

  207. Lee, G. J., Pakala, N., and Vierling, E. (1995),J. Biol. Chem. 270, 10,432–10,438.

    CAS  Google Scholar 

  208. Horwitz, J. (1992),Proc. Natl. Acad. Sci. USA 89, 10,449–10,453.

    Article  CAS  Google Scholar 

  209. Lilie, H., McLaughlin, S., Freedman, R., and Buchner, J. (1994),J. Biol. Chem. 269, 14,290–14,296.

    CAS  Google Scholar 

  210. Creighton, T. E., Bagley, C. J., Cooper, L., Darby, N. J., Freedman, R. B., Kemmink, J., and Sheikh, A. (1993),J. Mol. Biol. 232, 1176–1196.

    Article  CAS  Google Scholar 

  211. Song, J. and Wang, C. (1995),Eur. J. Biochem. 231, 312–316.

    Article  CAS  Google Scholar 

  212. Cai, H., Wang, C. C., and Tsou, C.-L. (1994),J. Biol. Chem. 269, 24,550–24,552.

    CAS  Google Scholar 

  213. Akiyama, Y., Kamitani, S., Kusukawa, N., and Ito, K. (1992),J. Biol. Chem. 267, 22,440–22,445.

    CAS  Google Scholar 

  214. Zapun, A. and Creighton, T. E. (1994),Biochemistry 33, 5202–5211.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Chemical Engineering, University of Washington, Box 351750, 98195-1750, Seattle, WA

    Jeffrey G. Thomas, Amanda Ayling & François Baneyx

Authors
  1. Jeffrey G. Thomas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amanda Ayling
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. François Baneyx
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Thomas, J.G., Ayling, A. & Baneyx, F. Molecular chaperones, folding catalysts, and the recovery of active recombinant proteins fromE. coli . Appl Biochem Biotechnol 66, 197–238 (1997). https://doi.org/10.1007/BF02785589

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02785589

Index Entries

Search

Navigation