Primary events in the colicin translocon: FRET analysis of colicin unfolding initiated by binding to BtuB and OmpF

Biochemistry

Volumn 47, Issue 48, 2008, Pages 12802-12809

  Zakharov, Stanislav D ^a,b   Sharma, Onkar ^a   Zhalnina, Mariya V ^a   Cramer, William A ^a  

^a PURDUE UNIVERSITY   (United States)

^b INSTITUTE OF BASIC BIOLOGICAL PROBLEMS   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; CELL MEMBRANES; ELECTROSTATICS; ESCHERICHIA COLI; FLOW INTERACTIONS; MODEL STRUCTURES; MOLECULAR INTERACTIONS; PORT TERMINALS;

COLICIN; CYTOTOXIC; DO-MAINS; DONOR AND ACCEPTORS; ELECTROSTATIC COMPONENTS; ELECTROSTATIC INTERACTIONS; FLUORESCENT DYES; GENETIC ANALYSES; HIGH AFFINITY BINDINGS; IN VITRO; NOVEL METHODS; NUCLEASE DOMAINS; OUTER MEMBRANES; POLYPEPTIDE CHAINS; TRANSLOCON; VITAMIN B;

BINDING ENERGY;

COLICIN; CYANOCOBALAMIN RECEPTOR; MEMBRANE RECEPTOR; OUTER MEMBRANE PROTEIN F; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL OUTER MEMBRANE; CONFORMATIONAL TRANSITION; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN TARGETING; RECEPTOR AFFINITY;

BACTERIAL OUTER MEMBRANE PROTEINS; BINDING SITES; COLICINS; CYSTEINE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; KINETICS; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; MUTATION; OXIDATION-REDUCTION; PORINS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN TRANSPORT; STAINING AND LABELING; STATIC ELECTRICITY; SULFHYDRYL COMPOUNDS; THERMODYNAMICS;

ESCHERICHIA COLI;

EID: 57049103480     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800865h     Document Type: Article

References (33)

1. Mock, M., and Pugsley, A. P. (1982) The BtuB group Col plasmids and homology between the colicins they encode. J. Bacteriol. 150, 1069-1076.
2. Benedetti, H., Frenette, M., Baty, D., Lloubes, R., Geli, V., and Lazdunski, C. (1989) Comparison of the uptake systems for the entry of various BtuB groups colicins into Escherichia coli. J. Gen. Microbiol. 135, 3413-3420.
3. 12 receptor with high affinity for colicin E3. J. Biol. Chem. 273, 31113-31118.
4. Kurisu, G., Zakharov, S. D., Zhalnina, M. V., Bano, S., Eroukova, V. Y., Rokitskaya, T. I., Antonenko, Y. N., Wiener, M. C., and Cramer, W. A. (2003) The structure of BtuB with bound colicin E3 R-domain implies a translocon. Nat. Struct. Biol. 10, 948-954.
5. Housden, N. G., Loftus, S. R., Moore, G. R., James, R., and Kleanthous, C. (2005) Cell entry mechanism of enzymatic bacterial colicins: Porin recruitment and the thermodynamics of receptor binding. Proc. Natl Acad. Sci. U.S.A. 102, 13849-13854.
6. Yamashita, E., Zhalnina, M. V., Zakharov, S. D., Sharma, O., and Cramer, W. A. (2008) Crystal structures of the OmpF porin: function in a colicin translocon. EMBO J. 27, 2171-2180.
7. Soelaiman, S., Jakes, K., Wu, N., Li, C. M., and Shoham, M. (2001) Crystal structure of colicin E3: Implications for cell entry and ribosome inactivation. Mol. Cell 8, 1053-1062.
8. Penfold, C. N., Healy, B., Housden, N. G., Boetzel, R., Vankemmelbeke, M., Moore, G. R., Kleanthous, C., and James, R. (2004) Flexibility in the receptor-binding domain of the enzymatic colicin E9 is required for toxicity against Escherichia coli cells. J. Bacteriol. 186, 4520-4527.
9. Zakharov, S. D. v., Zhalnina, M. V., Sharma, O., and Cramer, W. A. (2006) The colicin E3 outer membrane translocon: immunity protein release allows interaction of the cytotoxic domain with OmpF porin. Biochemistry 45, 10199-10207.
10. Haugland, R. P. (2005) The Handbook. A guide to fluorescent probes and labeling technologies, Invitrogen Corp.
11. Jullien, M., and Garel, J.-R. (1983) Energy-transfer measurements on a double fluorescent labeled ribonuclease A. Biochemistry 22, 3829-3836.
12. Lakowicz, J. R. (1999) in Principles of fluorescence spectroscopy, pp 367-394, Kluwer Academic/Plenum Publishers, New York.
13. Rye, H. S. (2001) Application of fluorescence resonance energy transfer to the GroEL-GroES chaperonin reaction. Methods 24, 278-288.
14. Sharma, S., Chakraborty, K., Muller, B. K., Astola, N., Tang, Y.-C., Lamb, D. C., Hayer-Hartl, M., and Hartl, F. U. (2008) Monitoring protein conformation along the pathway of chaperonin-assisted folding. Cell 133, 142-153.
15. Sharma, O., and Cramer, W. A. (2007) Minimum length requirement of the flexible N-terminal translocation subdomain of colicin E3. J. Bacteriol. 189, 363-368.
16. Zakharov, S. D., Eroukova, V. Y., Rokitskaya, T. I., Zhalnina, M. V., Sharma, O., Loll, P. J., Zgurskaya, H. I., Antonenko, Y. N., and Cramer, W. A. (2004) Colicin occlusion of OmpF and TolC channels: outer membrane translocons for colicin import. Biophys. J. 87, 3901-3911.
17. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
18. Lowry, O. H., Rosengrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein measurement with the Folin reagent. J. Biol. Chem. 193, 265-275.
19. Ellman, G. L. (1959) Tissue sulfhydryl groups. Arch. Biochem. Biophys. 82, 70-77.
20. Jocelyn, P. C. (1987) Spectrophotometric assay of thiols. Methods Enzymol. 143, 44-67.
21. Coligan, J. E., Dunn, B. M., Ploegh, H. L., Speicher, D. W., and Wingfield, P. T. (2001) in Current Protocols in Protein Sciences, pp 18.16.11-18.16.19, John Wiley & Sons, Inc., New York.
22. Wiener, M., Freymann, D., Ghosh, P., and Stroud, R. M. (1997) Crystal structure of colicin Ia. Nature 385, 461-464.
23. Schuler, B., Lipman, E. A., and Eaton, W. A. (2002) Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy. Nature 419, 743-747.
24. Merchant, K. A., Best, R. B., Louis, J. M., Gopich, I. V., and Eaton, W. A. (2007) Characterizing the unfolded states of proteins using single-molecule FRET spectroscopy and molecular simulations. Proc. Natl Acad. Sci. U.S.A. 104, 1528-1533.
25. Lin, Z., and Rye, H. S. (2004) Expansion and compression of a protein folding intermediate by GroEL. Mol. Cell 16, 23-34.
26. Krishnan, B., Szymanska, A., and Gierasch, L. M. (2007) Site-specific fluorescent labeling of poly-histidine sequences using a metal-chelating cysteine. Chem. Biol. Drug Des. 69, 31-40.
27. Sowdhamini, R., Srinivasan, N., Shoichet, B., Santi, D. V., Ramakrishnan, C., and Balaram, P. (1989) Stereochemical modelling of disulfide bridges: criteria for introduction into proteins by site-directed mutagenesis. Protein Eng. 3, 95-103.
28. James, R., Penfold, C. N., Moore, G. R., and Kleanthous, C. (2002) Killing of E. coli cells by E group nuclease colicins. Biochimie 84, 381-389.
29. Walker, D., Moore, G. R., James, R., and Kleanthous, C. (2003) Thermodynamic consequences of bipartite immunity protein binding to the ribosomal ribonuclease colicin E3. Biochemistry 42, 4161-4171.
30. Indyk, L., and Fisher, H. F. (1998) Theoretical aspects of isothermal titration calorimetry. Methods Enzymol. 295, 350-364.
31. Pierce, M. M., Raman, C. S., and Nall, B. T. (1999) Isothermal titration calorimetry of protein-protein interactions. Methods 19, 213-221.
32. Sharma, O., Yamashita, E., Zhalnina, M. V., Zakharov, S. D., Datsenko, K. A., Wanner, B. L., and Cramer, W. A. (2007) Structure of the complex of the colicin E2 R-domain and its BtuB receptor. The outer membrane colicin translocon. J. Biol. Chem. 282, 23163-23170.
33. Buchanan, S. K., Lukacik, P., Grizot, S., Ghirlando, R., Ali, M. M., Barnard, T. J., Jakes, K. S., Kienker, P. K., and Esser, L. (2007) Structure of colicin I receptor bound to the R-domain of colicin Ia: implications for protein import. EMBO J. 26, 2594-2604.