Tight hydrophobic contacts with the secB chaperone prevent folding of substrate proteins

Biochemistry

Volumn 49, Issue 11, 2010, Pages 2380-2388

  Bechtluft, Philipp ^a   Kedrov, Alexej ^a   Slotboom, Dirk Jan ^b   Nouwen, Nico ^c   Tans, Sander J ^d   Driessen, Arnold J M ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c LABORATOIRE DES SYMBIOSES TROPICALES ET MÉDITERRANÉENNES   (France)

^d FOM INSTITUTE AMOLF   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONIN; HYDROPHOBIC CONTACT; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR CHAPERONES; POLYPEPTIDE BINDING; POLYPEPTIDE CHAIN; SINGLE-MOLECULE; SUBSTRATE PROTEINS; TETRAMERIC STRUCTURES; TRANSLOCASES;

AMINO ACIDS; BINDING ENERGY; ESCHERICHIA COLI; HYDROPHOBICITY;

PROTEINS;

AMINO ACID; ARGININE; CHAPERONE; LEUCINE; MUTANT PROTEIN; POLYPEPTIDE; PROTEIN SECA; PROTEIN SECB; TETRAMER;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENZYME ACTIVITY; HYDROPHOBICITY; ISOTHERMAL TITRATION CALORIMETRY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SUBSTITUTION; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDROPHOBICITY; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MUTATION; PEPTIDES; PERIPLASMIC BINDING PROTEINS; PROTEIN FOLDING; PROTEIN PRECURSORS; PROTEIN STRUCTURE, QUATERNARY; PROTEIN TRANSPORT;

ESCHERICHIA COLI;

EID: 77949510819     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi902051e     Document Type: Article

References (32)

1. Driessen, A. J., and Nouwen, N. (2008) Protein translocation across the bacterial cytoplasmic membrane. Annu. Rev. Biochem. 77, 643667.
2. Randall, L. L., and Hardy, S. J. (1986) Correlation of competence for export with lack of tertiary structure of the mature species: A study in vivo of maltose-binding protein in E. coli. Cell 46, 921-928.
3. van der Sluis, E. O., and Driessen, A. J. (2006) Stepwise evolution of the Sec machinery in Proteobacteria. Trends Microbiol. 14, 105-108.
4. Delepelaire, P., and Wandersman, C. (1998) The SecB chaperone is involved in the secretion of the Serratia marcescens HasA protein through an ABC transporter. EMBO J. 17, 936-944.
5. Xu, Z., Knafels, J. D., and Yoshino, K. (2000) Crystal structure of the bacterial protein export chaperone secB. Nat. Struct. Biol. 7, 1172-1177.
6. Dekker, C., de Kruijff, B., and Gros, P. (2003) Crystal structure of SecB from Escherichia coli. J. Struct. Biol. 144, 313-319.
7. Smith, V. F., Schwartz, B. L., Randall, L. L., and Smith, R. D. (1996) Electrospray mass spectrometric investigation of the chaperone SecB. Protein Sci. 5, 488-494.
8. Topping, T. B., Woodbury, R. L., Diamond, D. L., Hardy, S. J., and Randall, L. L. (2001) Direct demonstration that homotetrameric chaperone SecB undergoes a dynamic dimer-tetramer equilibrium. J. Biol. Chem. 276, 7437-7441.
9. Muren, E. M., Suciu, D., Topping, T. B., Kumamoto, C. A., and Randall, L. L. (1999) Mutational alterations in the homotetrameric chaperone SecB that implicate the structure as dimer of dimers. J. Biol. Chem. 274, 19397-19402.
10. Knoblauch, N. T., Rudiger, S., Schonfeld, H. J., Driessen, A. J., Schneider-Mergener, J., and Bukau, B. (1999) Substrate specificity of the SecB chaperone. J. Biol. Chem. 274, 34219-34225.
11. Randall, L. L., and Hardy, S. J. (1995) High selectivity with low specificity: How SecB has solved the paradox of chaperone binding. Trends Biochem. Sci. 20, 65-69.
12. Topping, T. B., and Randall, L. L. (1997) Chaperone SecB from Escherichia coli mediates kinetic partitioning via a dynamic equilibrium with its ligands. J. Biol. Chem. 272, 19314-19318.
13. Topping, T. B., and Randall, L. L. (1994) Determination of the binding frame within a physiological ligand for the chaperone SecB. Protein Sci. 3, 730-736.
14. Khisty, V. J., Munske, G. R., and Randall, L. L. (1995) Mapping of the binding frame for the chaperone SecB within a natural ligand, galactose-binding protein. J. Biol. Chem. 270, 25920-25927.
15. Hardy, S. J., and Randall, L. L. (1991) A kinetic partitioning model of selective binding of nonnative proteins by the bacterial chaperone SecB. Science 251, 439-443.
16. Kimsey, H. H., Dagarag, M. D., and Kumamoto, C. A. (1995) Diverse effects of mutation on the activity of the Escherichia coli export chaperone SecB. J. Biol. Chem. 270, 22831-22835.
17. Crane, J. M., Suo, Y., Lilly, A. A., Mao, C., Hubbell, W. L., and Randall, L. L. (2006) Sites of interaction of a precursor polypeptide on the export chaperone SecB mapped by site-directed spin labeling. J. Mol. Biol. 363, 63-74.
18. Fekkes, P., de Wit, J. G., van der Wolk, J. P., Kimsey, H. H., Kumamoto, C. A., and Driessen, A. J. (1998) Preprotein transfer to the Escherichia coli translocase requires the co-operative binding of SecB and the signal sequence to SecA. Mol. Microbiol. 29, 1179-1190.
19. Bechtluft, P., van Leeuwen, R. G., Tyreman, M., Tomkiewicz, D., Nouwen, N., Tepper, H. L., Driessen, A. J., and Tans, S. J. (2007) Direct observation of chaperone-induced changes in a protein folding pathway. Science 318, 1458-1461.
20. Crooke, E., Guthrie, B., Lecker, S., Lili, R., and Wickner, W. (1988) ProOmpA is stabilized for membrane translocation by either purified. E. coli trigger factor or canine signal recognition particle. Cell 54, 1003-1011.
21. Cunningham, K., and Wickner, W. T. (1989) Detergent disruption of bacterial inner membranes and recovery of protein translocation activity. Proc. Natl. Acad. Sci. U.S.A. 86, 8673-8677.
22. Fekkes, P., van der Does, C., and Driessen, A. J. (1997) The molecular chaperone SecB is released from the carboxy-terminus of SecA during initiation of precursor protein translocation. EMBO J. 16, 6105-6113.
23. de Keyzer, J., van der Does, C., and Driessen, A. J. (2002) Kinetic analysis of the translocation of fluorescent precursor proteins into Escherichia coli membrane vesicles. J. Biol. Chem. 277, 46059-46065.
24. Ganesh, C., Zaidi, F. N., Udgaonkar, J. B., and Varadarajan, R. (2001) Reversible formation of on-pathway macroscopic aggregates during the folding of maltose binding protein. Protein Sci. 10, 1635-1644.
25. Slotboom, D. J., Duurkens, R. H., Olieman, K., and Erkens, G. B. (2008) Static light scattering to characterize membrane proteins in detergent solution. Methods 46, 73-82.
26. Folta-Stogniew, E. (2006) Oligomeric states of proteins determined by size-exclusion chromatography coupled with light scattering, absorbance, and refractive index detectors. Methods Mol. Biol. 328, 97-112.
27. Zhou, J., and Xu, Z. (2003) Structural determinants of SecB recognition by SecA in bacterial protein translocation. Nat. Struct. Biol. 10, 942-947.
28. Lecker, S. H., Driessen, A. J., and Wickner, W. (1.990) ProOmpA contains secondary and tertiary structure prior to translocation and is shielded from aggregation by association with SecB protein. EMBO J. 9, 2309-2314.
29. Tomkiewicz, D., Nouwen, N., and Driessen, A. J. (2008) Kinetics and energetics of the translocation of maltose binding protein folding mutants. J. Mol. Biol. 377, 83-90.
30. Panse, V. G., Swaminathan, C. P., Surolia, A., and Varadarajan, R. (2000) Thermodynamics of substrate binding to the chaperone SecB. Biochemistry 39, 2420.-2427.
31. Ullers, R. S., Luirink, J., Harms, N., Schwager, F., Georgopoulos, C., and Genevaux, P. (2004) SecB is a bona fide generalized chaperone in Escherichia coli. Proc. Acad. Sci. U.S.A 101, 7583-7588.
32. Krishnan, B., Kulothungan, S. R., Patra, A. K., Udgaonkar, J. B., and Varadarajan, R. (2009) SecB-mediated protein export need not occur via kinetic partitioning. J. Mol. Biol. 385, 1243-1256.