Thermodynamic consequences of bipartite immunity protein binding to the ribosomal ribonuclease colicin E3

Biochemistry

Volumn 42, Issue 14, 2003, Pages 4161-4171

  Walker, Daniel ^a   Moore, Geoffrey R ^b   James, Richard ^c   Kleanthous, Colin ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; BACTERIA; DISSOCIATION; ENTHALPY; ENZYME KINETICS; ENZYMES; RATE CONSTANTS; RNA;

THERMODYNAMIC MEASUREMENTS;

BIOCHEMISTRY;

ANTIBIOTIC AGENT; COLICIN E3; IMMUNITY PROTEIN; PROTEIN; RIBONUCLEASE; RNA 16S; TOXIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOTOXICITY; DISSOCIATION; DRUG TARGETING; ENTHALPY; ENZYME ACTIVITY; ESCHERICHIA COLI; MOLECULAR STABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; STEADY STATE; THERMODYNAMICS; TOXIN SYNTHESIS;

BACTERIAL PROTEINS; CALORIMETRY; COLICINS; KINETICS; PLASMIDS; PROTEIN BINDING; PROTEIN FOLDING; SPECTROMETRY, FLUORESCENCE; THERMODYNAMICS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0345701261     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0273720     Document Type: Article

References (45)

1. Parret, A. H. A., and De Mott, R. (2002) Bacteria killing their own kind: novel bacteriocins of Pseudomonas and other γ-proteobacteria, Trends Microbiol. 10, 107-12.
2. Sharma, S., Waterfield, N., Bowen, D., Rocheleau, T., Holland, L., James, R., and French-Constant, R. (2002) The lumicins: novel bacteriocins from Photorhabdus luminescens with similarity to the uropathogenic-specific protein (USP) from uropathogenic, Escherichia coli, FEMS Microbiol. Lett. 214, 241-9.
3. Pommer, A. J., Cal, S., Keeble, A. H., Walker, D., Evens, S. J., Kuhlmann, U. C., Cooper, A., Connolly, B. A., Hemmings, A. M., Moore, G. R., James, R., and Kleanthous, C. (2001) Mechanism and cleavage specificity of the H-N-H endonuclease colicin E9, J. Mol. Biol. 314, 735-49.
4. Tomita, K., Ogawa, T., Uozumi, K., Watanabe, K., and Masaki, H. (2000) A cytotoxic ribonuclease which specifically cleaves four isoaccepting arganine tRNAs at their anticodon loops, Proc. Natl. Acad. Sci. U.S.A. 97, 8278-83.
5. Bowman, C. M., Dahlberg, J. E., Ikemura, T., Konisky, J., and Nomura, M. (1971) Specific inactivation of 16S ribosomal RNA induced by colicin E3 in vivo, Proc. Natl. Acad. Sci. U.S.A. 68, 964-8.
6. Cramer, W. A., Cohen, F. S., Merrill, A. R., and Song, H. Y. (1990) Structure and dynamics of the colicin E1 channel, Mol. Microbiol. 4, 519-26.
7. Harkness, R. E., and Braun, V. (1989) Colicin M inhibits peptidoglycan biosynthesis by interfering with lipid carrier recycling, J. Biol. Chem. 15, 6177-82.
8. Kleanthous, C., Hemmings, A. M., Moore, G. R., and James, R. (1998) Immunity proteins and their specificity for endonuclease colicins: telling right from wrong in protein-protein recognition, Mol. Microbiol. 28, 227-33.
9. Krone, W. J., de Vries, P., Koningstein, G., de Jonge, A. J., de Graaf, F. K., and Oudega, B. (1986) Uptake of cloacin DF13 by susceptible cells: removal of immunity protein and fragmentation of cloacin molecules, J. Bacteriol. 166, 260-268.
10. Ohno, S., Ohno-Iwashita, Y., Suzuki, K., and Imahori, K. (1977) Purification and characterization of active component and active fragment of colicin E3, J. Biochem. (Tokyo) 82, 1045-53.
11. Wallis, R., Moore, G. R., James, R., and Kleanthous, C. (1995) Protein-protein interactions in colicin E9 DNase-immunity protein complexes. 1. Diffusion-controlled association and femtomolar binding for the cognate complex, Biochemistry 34, 13743-50.
12. Schreiber, G., and Fersht, A. R. (1993) Interaction of barnase with its polypeptide inhibitor barstar studied by protein engineering, Biochemistry 32, 5145-50.
13. Lee, F. S., Shapiro, R., and Vallee, B. L. (1989) Tight-binding inhibition of angiogenin and ribonuclease A by placental ribonuclease inhibitor, Biochemistry 28, 225-30.
14. Kleanthous, C., and Walker, D. (2001) Immunity proteins: enzyme inhibitors that avoid the active site, Trends Biochem. Sci. 10, 624-31.
15. Buckle, A. M., Schreiber, G., and Fersht, A. R. (1994) Protein-protein recognition: crystal structural analysis of a barnase-barstar complex at 2.0-Å resolution, Biochemistry 33, 8878-89.
16. Buckle, A. M., and Fersht, A. R. (1994) Subsite binding in an RNase: structure of a barnase-tetranucleotide complex at 1.76-Å resolution, Biochemistry 33, 1644-53.
17. Putnam, C. D., Shroyer, M. J., Lundquist, A. J., Mol, C. D., Arvai, A. S., Mosbaugh, D. W., and Tainer, J. A. (1999) Protein mimicry of DNA from crystal structures of the uracil-DNA glycosylase inhibitor protein and its complex with Escherichia coli uracil-DNA glycosylase, J. Mol. Biol. 287, 331-46.
18. Parikh, S. S., Mol, C. D., Slupphaug, G., Bharati, S., Krokan, H. E., and Tainer, J. A. (1998) Base excision repair initiation revealed by crystal structures and binding kinetics of human uracil-DNA glycosylase with DNA, EMBO J. 17, 5214-26.
19. Noeske-Jungblut, C., Haendler, B., Donner, P., Alagon, A., Possani, L., and Schleuning, W. D. (1995) Triabin, a highly potent exosite inhibitor of thrombin, J. Biol. Chem. 270, 28629-34.
20. Wallis, R., Leung, K. Y., Pommer, A. J., Videler, H., Moore, G. R., James, R., and Kleanthous, C. (1995) Protein-protein interactions in colicin E9 DNase-immunity protein complexes. 2. Cognate and noncognate interactions that span the millimolar to femtomolar affinity range, Biochemistry 34, 13751-9.
21. Senior, B. W., and Holland, I. B. (1971) Effect of colicin E3 upon the 30S ribosomal subunit of Escherichia coli, Proc. Natl. Acad. Sci. U.S.A. 68, 959-63.
22. Cate, J. H., Yusupov, M. M., Yusupova, G. Z., Earnest, T. N., and Noller, H. F. (1999) X-ray crystal structures of 70S ribosome functional complexes, Science 285, 2095-104.
23. Carr, S., Walker, D., James, R., Kleanthous, C., and Hemmings, A. M. (2000) Inhibition of a ribosome-inactivating ribonuclease: the crystal structure of the cytotoxic domain of colicin E3 in complex with its immunity protein, Struct. Fold. Des. 8, 949- 60.
24. Soelaiman, S., Jakes, K., Wu, N., Li, C., and Shoham, M. (2001) Crystal structure of colicin E3: implications for cell entry and ribosome inactivation, Mol. Cell 8, 1053-62.
25. Chak, K. F., and James, R. (1984) Localization and characterization of a gene on the ColE3-CA38 plasmid that confers immunity to colicin E8, J. Gen. Microbiol. 130, 701-10.
26. Garinot-Schneider, C., Pommer, A. J., Moore, G. R., Kleanthous, C., and James, R. (1996) Identification of putative active-site residues in the DNase domain of colicin E9 by random mutagenesis, J. Mol. Biol. 260, 731-42.
27. Wallis, R., Reilly, A., Barnes, K., Abell, C., Campbell, D. G., Moore, G. R., James, R., and Kleanthous, C. (1994) Tandem overproduction and characterisation of the nuclease domain of colicin E9 and its cognate inhibitor protein Im9, Eur. J. Biochem. 220, 447-54.
28. Wallis, R., Reilly, A., Rowe, A., Moore, G. R., James, R., and Kleanthous, C. (1992) In vivo and in vitro characterization of overproduced colicin E9 immunity protein, Eur. J. Biochem. 207, 687-95.
29. Levinson, B. L., Pickover, C. A., and Richards, F. M. (1983) Dimerization by colicin E3 in the absence of immunity protein, J. Biol. Chem. 258, 10967-72.
30. McRorie, D. K., and Voelker, P. J. (1993) Self-associating systems in the analytical ultracentrifuge, Beckman Instruments, Palo Alto, CA.
31. Jakes, K. S., and Zinder, N. D. (1974) Highly purified colicin E3 contains immunity protein, Proc. Natl. Acad. Sci. U.S.A. 71, 3380-4.
32. Fersht, A. R. (1998) Structure and mechanism in protein science, W. H. Freeman, New York.
33. Schreiber, G., and Fersht, A. (1996) Rapid, electrostatically assisted association of proteins, Nature Struct. Biol. 3, 427-431.
34. Vijayakumar, M., Wong, K. Y., Schreiber, G., Fersht, A. R., Szabo, A., and Zhou, H. X. (1998) Electrostatic enhancement of diffusion-controlled protein-protein association: comparison of theory and experiment on barnase and barstar, J. Mol. Biol. 278, 1015-24.
35. Gutfreund, H. (1995) Kinetics for the life sciences, Cambridge University Press, Cambridge.
36. Frisch, C., Fersht, A. R., and Schreiber, G. (2001) Experimental assignment of the structure of the transition state for the association of barnase and barstar, J. Mol. Biol. 308, 69-77.
37. Kleanthous, C., and Pommer, A. (2000) Nuclease inhibitors, in Protein-Protein Recognition (Kleanthous, C., Ed.) pp 280-311, Oxford University Press, Oxford.
38. Frisch, C., Schreiber, G., Johnson, C. M., and Fersht, A. R. (1997) Thermodynamics of the interaction of barnase and barstar: changes in free energy versus changes in enthalpy on mutation, J. Mol. Biol. 267, 696-706.
39. Lee, F. S., Auld, D. S., and Vallee, B. L. (1989) Tryptophan fluorescence as a probe of placental ribonuclease inhibitor binding to angiogenin, Biochemistry 28, 219-24.
40. Lawrence, M. C., and Colman, P. M. (1993) Shape complementarity at protein/protein interfaces, J. Mol. Biol. 234, 946-50.
41. Penfold, C. N., Garinot-Schneider, C., Hemmings, A. M., Moore, G. R., Kleanthous, C., and James, R. (2000) A 76-residue polypeptide of colicin E9 confers receptor specificity and inhibits the growth of vitamin B12-dependent Escherichia coli 113/3 cells, Mol. Microbiol. 38, 639-49.
42. Bouveret, E., Rigal, A., Lazdunski, C., and Bénédetti, H. (1997) The N-terminal domain of colicin E3 interacts with To1B which is involved in the colicin translocation step, Mol. Microbiol. 23, 909-20.
43. Carr, S., Penfold, C. N., Bamford, V., James, R., and Hemmings, A. M. (2000) The structure of To1B, an essential component of the to1-dependent translocation system, and its protein-protein interaction with the translocation domain of colicin E9, Struct. Fold. Des. 8, 57-66.
44. 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 group colicins into Escherichia coli, J. Gen. Microbiol. 135, 3413-20.
45. De Graaf, F. K. (1973) Effects of cloacin DF13 on the functioning of the cytoplasmic membrane, Antonie Van Leeuwenhoek 39, 109-19.