Prolylpeptide binding by the prokaryotic SH3-like domain of the diphtheria toxin repressor: A regulatory switch

Biochemistry

Volumn 44, Issue 1, 2005, Pages 40-51

  Wylie, Gregory P ^a   Rangachari, Vijayaraghavan ^a   Bienkiewicz, Ewa A ^a   Marin, Vedrana ^a   Bhattacharya, Nilakshee ^a   Love, John F ^b   Murphy, John R ^b   Logan, Timothy M ^a,c  

^a FLORIDA STATE UNIVERSITY   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c FLORIDA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CALORIMETRY; COMPLEXATION; DIMERIZATION; DNA; ISOTHERMS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; TITRATION;

BINDING AFFINITY; DOMAIN COMPLEXES; INTRAMOLECULAR COMPLEX; TOXIN GENES;

GENES;

ALIPHATIC CARBOXYLIC ACID; DIPHTHERIA TOXIN; DNA BINDING PROTEIN; REPRESSOR PROTEIN; STEROID RECEPTOR COACTIVATOR 3; SYNTHETIC PEPTIDE;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CORYNEBACTERIUM DIPHTHERIAE; DIMERIZATION; DNA BINDING; ENZYME REGULATION; EUKARYOTE; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR INTERACTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN EXPRESSION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BINDING SITES; CALORIMETRY; CORYNEBACTERIUM DIPHTHERIAE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PEPTIDE FRAGMENTS; PROLINE; PROTEIN CONFORMATION; RECEPTORS, CELL SURFACE; RECOMBINANT PROTEINS;

CORYNEBACTERIUM; CORYNEBACTERIUM DIPHTHERIAE; EUKARYOTA; PROKARYOTA;

EID: 11844280282     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048035p     Document Type: Article

References (64)

1. Jakubovics, N. S., and Jenkinson, H. F. (2001) Out of the iron age: new insights into the critical role of manganese homeostasis in bacteria, Microbiology 147, 1709-1718.
2. Tao, X., Schiering, N., Zeng, H.-Y., Ringe, D., and Murphy, J. R. (1994) Iron, DtxR, and the regulation of diphtheria toxin expression, Mol. Microbiol. 14, 191-197.
3. Boyd, J., Oza, M. N., and Murphy, J. R. (1990) Molecular cloning and DNA sequence analysis of a diptheria tox iron-dependent regulatory element (dtxR) from Cornybacterium diptheriae, Proc. Natl. Acad. Sci. U.S.A. 87, 5968-5972.
4. Lee, J. H., and Holmes, R. K. (2000) Characterization of specific nucleotide substitutions in DtxR-specific operators of Corynebacterium diphtheriae that dramatically affect DtxR binding, operator function, and promoter strength, J. Bacteriol. 182, 432-438.
5. Schmitt, M. P. (1997) Transcription of the Corynebacterium diphtheriae humO gene is regulated by iron and heme, Infect. Immun. 65, 4634-4641.
6. Braun, V., and Killmann, H. (1999) Bacterial solutions to the iron-supply problem, Trends. Biochem. Sci. 24, 104-109.
7. Braun, V. (2001) Iron uptake mechanisms and their regulation in pathogenic bacteria, Int. J. Med. Microbiol. 291, 67-79.
8. Ratledge, C., and Dover, L. G. (2000) Iron metabolism in pathogenic bacteria, Annu. Rev. Microbiol. 54, 881-941.
9. Schiering, N., Tao, X., Zeng, H., Murphy, J. R., Petsko, G. A., and Ringe, D. (1995) Structures of the apo- and metal ion-activated forms of the diphtheria tox repressor from Corynebacterium diphtheriae, Proc. Natl. Acad. Sci. U.S.A. 92, 9843-9850.
10. Qiu, X., Verlinde, C. L. M. J., Zhang, S., Schmitt, M. P., Holmes, R. K., and Hol, W. G. J. (1995) Three-dimensional structure of the diphtheria toxin repressor in complex with divalent cation co-repressors, Structure 3, 87-100.
11. Qiu, X., Pohl, E., Holmes, R. K., and Hol, W. G. J. (1996) High-resolution structure of the diptheria toxin repressor complexed with cobalt and manganese reveals an SH3-like third domain and suggests a possible role of phosphate as co-corepressor, Biochemistry 35, 12292-12302.
12. Pohl, E., Holmes, R. K., and Hol, W. G. J. (1999) Crystal structure of a cobalt-activated diphtheria toxin repressor-DNA complex reveals a metal-binding SH3-like domain, J. Mol. Biol. 292, 653-667.
13. Wang, G., Wylie, G. P., Twigg, P. D., Caspar, D. L. D., Murphy, J. R., and Logan, T. M. (1999) Solution structure and peptide binding studies of the C-terminal Src homology 3-like domain of the diphtheria toxin repressor protein, Proc. Natl. Acad. Sci., U.S.A. 90, 6119-6124.
14. Tao, X., and Murphy, J. R. (1992) Binding of the metaolloregulatory protein DtxR to the Diptheria tox operator requires divalent heavy metal ion and protects the palindromic sequence from DNase I digestion, J. Biol. Chem. 267, 21761-21764.
15. Ding, X., Zeng, H., Schiering, N., Ringe, D., and Murphy, J. R. (1996) Identification of the primary metal ion-activation sites of the diphtheria tox repressor by X-ray crystallography and site-directed mutagenesis, Nat. Struct. Biol. 3, 382-387.
16. Pohl, E., Holmes, R. K., and Hol, W. G. (1999) Crystal structure of the iron-dependent regulator (IdeR) from Mycobacterium tuberculosis shows both metal binding sites fully occupied, J. Mol. Biol. 285, 1145-1156.
17. Love, J. F., VanderSpek, J. C., and Murphy, J. R. (2003) The src homology 3-like domain of the diphtheria toxin repressor (DtxR) modulates repressor activation through interaction with the ancillary metal ion-binding site, J. Bacteriol. 185, 2251-2258.
18. Twigg, P. D., Parthasarathy, G., Guerrero, L., Logan, T. M., and Caspar, D. L. (2001) Disordered to ordered folding in the regulation of diphtheria toxin repressor activity, Proc. Natl. Acad. Sci. U.S.A. 98, 11259-11264.
19. Spiering, M. M., Ringe, D., Murphy, J. R., and Marietta, M. A. (2003) Metal stoichiometry and functional studies of the diphtheria toxin repressor, Proc. Natl. Acad. Sci. U.S.A. 100, 3808-3813.
20. Xu, W., Harrison, S. C., and Eck, M. L. (1997) Three-dimensional structure of the tyrosine kinase c-Src, Nature 385, 595-602.
21. Sicheri, F., Maorefi, I., and Kuriyan, J. (1997) Crystal structure of the Src family tyrosine kinase Hck, Nature 385, 602-609.
22. 1H nuclear magnetic resonance studies of receptor-bound cyclosporin, J. Am. Chem. Soc. 112, 9015-9016.
23. Wu, D., Chen, A., and C. S. Johnson, J. (1995) An improved diffusion-ordered spectroscopy experiment incorporating bipolar-gradient pulses, J. Magn. Reson. A115, 260-264.
24. Stapley, B. J., and Creamer, T. P. (1999) A survey of left-handed polyproline II helices, Protein Sci. 8, 587-595.
25. Kuriyan, J., and Cowburn, D. (1997) Modular peptide recognition domains in eukaryotic signaling, Annu. Rev. Biophys. Biomol. Struct. 26, 259-288.
26. Reed, J., and Kinzel, V. (1991) A conformational switch is associated with receptor affinity in peptides derived from the CD4-binding domain of gp120 from HIV I, Biochemistry 30, 4521-4528.
27. Fukada, H., and Takahashi, K. (1998) Enthalpy and heat capacity changes for the proton dissociation of various buffer components in 0.1 M potassium chloride, Proteins 33, 159-166.
28. Parker, M. H., Brouillette, C. G., and Prevelige, P. E., Jr. (2001) Kinetic and calorimetric evidence for two distinct scaffolding protein binding populations within the bacteriophage P22 procapsid, Biochemistry 40, 8962-8970.
29. Graversen, J. H., Sigurskjold, B. W., Thogersen, H. C., and Etzerodt, M. (2000) Tetranectin-binding site on plasminogen kringle 4 involves the lysine-binding pocket and at least one additional amino acid residue, Biochemistry 39, 7414-7419.
30. Wiseman, T., Williston, S., Brandts, J. F., and Lin, L.-N. (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter, Anal. Biochem. 179, 131-137.
31. Love, J. F., and Murphy, J. R. (2002) Design and development of a novel genetic probe for the analysis of repressor-operator interactions, J. Microbiol. Methods 51, 63-72.
32. Saraste, M., and Musacchio, A. (1994) Backwards and forwards binding, Nat. Struct. Biol. 1, 835-837.
33. Kay, B. K., Williamson, M. P., and Sudol, M. (2000) The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains, FASEB J. 14, 231-241.
34. Kang, H., Freund, C., Duke-Cohan, J. S., Musacchio, A., Wagner, G., and Rudd, C. E. (2000) SH3 domain recognition of a proline-independent tyrosine-based RKxxYxxY motif in immune cell adaptor SKAP55, EMBO J. 19, 2889-2899.
35. Kami, K., Takeya, R., Sumimoto, H., and Kohda, D. (2002) Diverse recognition of non-PxxP peptide ligands by the SH3 domains from p67(phox), Grb2 and Pex13p, EMBO J. 21, 4268-4276.
36. Gorina, S., and Pavletich, N. P. (1996) Structure of the p53 tumor suppressor bound to the ankyrin and SH3 domains of 53bp2, Science 274, 1001-1005.
37. Berry, D. M., Nash, P., Liu, S. K., Pawson, T., and McGlade, C. J. (2002) A high-affinity Arg-X-X-Lys SH3 binding motif confers specificity for the interaction between Gads and SLP-76 in T cell signaling, Curr. Biol. 12, 1336-1341.
38. Brazin, K. N., Fulton, D. B., and Andreotti, A. H. (2000) A specific intermolecular association between the regulatory domains of a Tec family kinase, J. Mol. Biol. 302, 607-623.
39. Stock, A. M., Robinson, V. L., and Goudreau, P. N. (2000) Two-component signal transduction, Annu. Rev. Biochem. 69, 183-215.
40. Ponting, C. P., Aravind, L., Schultz, J., Bork, P., and Koonin, E. V. (1999) Eukaryotic signalling domain homologues in archaea and bacteria. Ancient ancestry and horizontal gene transfer, J. Mol. Biol. 289, 729-745.
41. Whisstock, J. C., and Lesk, A. M. (1999) SH3 domains in prokaryotes, Trends. Biochem. Sci. 24, 132-133.
42. Ferreon, J. C., and Hilser, V. J. (2003) Ligand-induced changes in dynamics in the RT loop of the C-terminal SH3 domain of Sem-5 indicate cooperative conformational coupling, Protein Sci. 12, 982-996.
43. Paras-Lutzke, R. A., Vink, C., and Plasternak, R. H. A. (1994) Characterization of the minimal DNA-binding domain of the HIV integrase protein, Nucl. Acids Res. 22, 4125-4131.
44. Wittekind, M., Mapelli, C., Farmer, B. T, II, Suen, K.-L., Goldfarb, V., Tsao, J., Lavoie, T., Barbacid, M., Meyers, C. A., and Mueller, L. (1994) Orientation of peptide fragments from Sos protein bound to the N-terminal SH3 domain of Grb2 determined by NMR spectroscopy, Biochemistry 33, 13531-13539.
45. Petrella, E. C., Machesky, L. M., Kaiser, D. A., and Pollard, T. D. (1996) Structural requirements and thermodynamics of the interaction of proline peptides with profilin, Biochemistry 35, 16535-16543.
46. Makhatadze, G. I., and Privalov, P. L. (1994) Energetics of interactions of aromatic hydrocarbons with water, Biophys. Chem. 50, 285-291.
47. II) helix formation, Biochemistry 43, 7787-7797.
48. Zhou, H.-X. (2001) Loops in proteins can be modeled as worm-like chains, J. Phys. Chem. B 105, 6763-6736.
49. Goranson-Siekierke, J., Pohl, E., Hol, W. J. G., and Holmes, R. K. (1999) Anion-coordinating residues at binding site 1 are essential for the biological activity of the diphtheria toxin repressor, Infect. Immun. 67, 1806-1811.
50. Hantke, K. (2001) Iron and metal regulation in bacteria, Curr. Opin. Microbiol. 4, 172-177.
51. Muhandiram, D. R., and Kay, L. E. (1994) Gradient-enhanced triple-resonance three-dimensional NMR experiments with improved sensitivity, J. Magn. Reson. 103B, 203-216.
52. 13C resonances of the C-terminal domain of diphtheria toxin repressor, J. Biomol. NMR 13, 197-198.
53. Kuboniwa, H., Grzesiek, S., Delagio, F., and Bax, A. (1994) Measurement of Hn-Ha J couplings in calcium-free calmodulin using new 2D and 3D water flip-back methods, J. Biomol. NMR 4, 871-878.
54. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectra processing system based on UNIX pipes, J. Biomol. NMR 6, 277-293.
55. Johnson, B. A., and Blevins, R. A. (1994) NMRView: A computer program for the visualization and analysis of NMR data, J. Biomol. NMR 4, 603-614.
56. Fletcher, C. M., Jones, D. N. M., Diamond, R., and Neuhaus, D. (1996) Treatment of NOE constraints involving equivalent or nonstereoassigned protons in calculations of biomacromolecular structures, J. Biomol. NMR 8, 292-310.
57. Stein, E. G., Rice, L. M., and Brünger, A. T. (1997) Torsion-angle molecular dynamics as a new efficient tool for NMR structure calculation, J. Magn. Reson. 124, 154-164.
58. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr. D Biol. Crystallogr. 54, 905-921.
59. Linge, J. P., and Nilges, M. (1999) Influence of nonbonded parameters on the quality of NMR structures: a new force field for NMR structure calculation, J. Biomol. NMR 13, 51-59.
60. Laskowski, R. A., Rullmann, J. A. C., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: Programs for checking the quality of protein structuers solved by NMR, J. Biomol. NMR. 8, 477-486.
61. Korepanova, A., Douglas, C., and Logan, T. M. (2002) Glutamine 53 is a gatekeeper residue in the FK506 binding protein, J. Mol. Biol. 323, 285-296.
62. Mulder, F. A. A., Schipper, D., Bott, R., and Boelens, R. (1999) Altered flexibility in the substrate-binding site of related native and engineered high-alkaline Bacillus subtilisins, J. Mol. Biol. 292, 111-123.
63. Eldridge, A. M., Kang, H. S., Johnson, E., Gunsalus, R., and Dahlquist, F. W. (2002) Effect of phosphorylation on the interdomain interaction of the response regulator, NarL, Biochemistry 41, 15173-15180.
64. Koradi, R., Billeter, M., and Wüthrich, K. (1996) MOLMOL: A program for display and analysis of macromolecular structures, J. Mol. Graphics 14, 51-55.