Structural basis for O2 sensing by the hemerythrin-like domain of a bacterial chemotaxis protein: Substrate tunnel and fluxional N terminus

Biochemistry

Volumn 45, Issue 30, 2006, Pages 9023-9031

  Isaza, Clara E ^a   Silaghi Dumitrescu, Radu ^b   Iyer, Ramesh B ^b   Kurtz Jr , Donald M ^b,c   Chan, Michael K ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BIOCHEMISTRY; CRYSTAL STRUCTURE; OXIDATION; REDOX REACTIONS; X RAY ANALYSIS;

ANAEROBIC SULFATE; CHEMOTAXIS PROTEIN; CONFORMATIONAL DIFFERENCES; CYTOPLASMIC LOCALIZATION;

PROTEINS;

BACTERIAL PROTEIN; HEMERYTHRIN; PROTEIN DCRH; UNCLASSIFIED DRUG; OXYGEN; PEPTIDE FRAGMENT;

AMINO TERMINAL SEQUENCE; ARTICLE; AUTOOXIDATION; CARBOXY TERMINAL SEQUENCE; DESULFOVIBRIO VULGARIS; METHYLATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXYGEN AFFINITY; OXYGEN SENSING; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; X RAY CRYSTALLOGRAPHY; BINDING SITE; CHEMISTRY; CHEMOTAXIS; COMPARATIVE STUDY; CRYSTALLIZATION; ENZYME SPECIFICITY; GENETICS; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION;

BACTERIA (MICROORGANISMS); DESULFOVIBRIO VULGARIS; INVERTEBRATA;

BACTERIAL PROTEINS; BINDING SITES; CHEMOTAXIS; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; DESULFOVIBRIO VULGARIS; HEMERYTHRIN; OXIDATION-REDUCTION; OXYGEN; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

EID: 33746661497     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0607812     Document Type: Article

References (49)

1. Falke, J. J., and Hazelbauer, G. L. (2001) Transmembrane signaling in bacterial chemoreceptors, Trends Biochem. Sci. 26, 257-265.
2. Wadhams, G. H., and Armitage, J. P. (2004) Making sense of it all: Bacterial chemotaxis, Nat. Rev. Mol. Cell Biol. 5, 1024-1037.
3. Taylor, B. L., Zhulin, I. B., and Johnson, M. S. (1999) Aerotaxis and other energy-sensing behavior in bacteria, Annu. Rev. Microbiol. 53, 103-128.
4. Cypionka, H. (2000) Oxygen respiration by Desulfovibrio species, Annu. Rev. Microbiol. 54, 827-848.
5. 2-regulated prolyl hydroxylation, Science 292, 468-472.
6. Gilles-Gonzalez, M. A., Ditta, G. S., and Helinski, D. R. (1991) A hemoprotein with kinase activity encoded by the oxygen sensor of Rhizobium meliloti, Nature 350, 170-117 172.
7. Gilles-Gonzalez, M. A., Gonzalez, G., Perutz, M. F., Kiger, L., Marden, M. C., and Poyart, C. (1994) Heme-based sensors, exemplified by the kinase FixL, are a new class of heme protein with distinctive ligand binding and autoxidation, Biochemistry 33, 8067-8073.
8. Gong, W., Hao, B., Mansy, S. S., Gonzalez, G., Gilles-Gonzalez, M.-A., and Chan, M. K. (1998) Structure of a biological oxygen sensor: A new mechanism for heme-driven signal transduction, Proc. Natl. Acad. Sci. U.S.A. 95, 15177-15182.
9. 2 sensing and ligand discrimination by the FixL heme domain of Bradyrhizobium japonicum, Biochemistry 41, 12952-12958.
10. Delgado-Nixon, V. M., Gonzalez, G., and Gilles-Gonzalez, M.-A. (2000) Dos, a heme-binding PAS protein from Escherichia coli, is a direct oxygen sensor, Biochemistry 39, 2685-2691.
11. Kurokawa, H., Lee, D. S., Watanabe, M., Sagami, I., Mikami, B., Raman, C. S., and Shimizu, T. (2004) A redox-controlled molecular switch revealed by the crystal structure of a bacterial heme PAS sensor, J. Biol. Chem. 279, 20186-20193.
12. Park, H., Suquet, C., Satterlee, J. D., and Rang, C. (2004) Insights into signal transduction involving PAS domain oxygen-sensing heme proteins from the X-ray crystal structure of Escherichia coli Dos heme domain (Ec DosH), Biochemistry 43, 2738-2746.
13. Hou, S., Larsen, R. W., Boudko, D., Riley, C. W., Karatan, E., Zimmer, M., Ordal, G. W., and Alam, M. (2000) Myoglobin-like aerotaxis transducers in archaea and bacteria, Nature 403, 540-544.
14. Zhang, W., and Phillips, G. N., Jr. (2003) Structure of the oxygen sensor in Bacillus subtilis: Signal transduction of chemotaxis by control of symmetry, Structure 11, 1097-1111.
15. Pellicena, P., Karow, D. S., Boon, E. M., Marletta, M. A., and Kuriyan, J. (2004) Crystal structure of an oxygen-binding heme domain related to soluble guanylate cyclases, Proc. Natl. Acad. Sci. U.S.A. 101, 12854-12859.
16. Jain, R., and Chan, M. K. (2003) Mechanisms of ligand discrimination by heme proteins, J. Biol. Inorg. Chem. 8, 1-11.
17. Deckers, H. M., and Voordouw, G. (1996) The dcr gene family of Desulfovibrio: Implications from the sequence of dcrH and phylogenetic comparison with other mcp genes, Antonie Van Leeuwenhoek 70, 21-29.
18. Xiong, J., Farmer, C. S., and Kurtz, D. M., Jr. (1997) The C-terminal domain of Desulfovibrio vulgar is dcrH gene product is a hemerythrin homolog, FASEB J. 11, A1340.
19. Mangum, C. P. (1992) Physiological function of the hemerythrins, in Advances in Comparative and Environmental Physiology (Mangum, C. P., Ed.) Vol. 13, pp 173-192, Springer-Verlag, New York.
20. Stenkamp, R. E. (1994) Dioxygen and hemerythrin, Chem. Rev. 94, 715-726.
21. Kurtz, D. M., Jr. (2004) Dioxygen-binding proteins, in Comprehensive Coordination Chemistry II (McCleverty, J. A., and Meyer, T. J., Eds.) Vol. 8, pp 229-260, Elsevier, Oxford, U.K.
22. Xiong, J., Kurtz, D. M., Jr., Ai, J., and Sanders-Loehr, J. (2000) A hemerythrin-like domain in a bacterial chemotaxis protein, Biochemistry 39, 5117-5125.
23. 2 access to the binding pocket of Phascolopsis gouldii hemerythrin, J. Biol. Chem. 275, 17043-17050.
24. Feig, A. L., and Lippard, S. J. (1994) Reactions of non-heme iron-(II) centers with dioxygen in biology and chemistry, Chem. Rev. 94, 759-805.
25. Martins, L. J., Hill, C. P., and Ellis, W. R., Jr. (1997) Structures of wild-type chloromet and L103N hydroxomet Themiste zostericola myohemerythrins at 1.8 Å resolution, Biochemistry 36, 7044-7049.
26. 2 binding pocket, J. Biol. Inorg. Chem. 6, 418-429.
27. Wistam, M., Lippard, S. J., and Friesner, R. A. (2003) Reversible dioxygen binding to hemerythrin, J. Am. Chem. Soc. 125, 3980-3987.
28. Sheriff, S., Hendrickson, W. A., and Smith, J. L. (1987) Structure of myohemerythrin in the azidomet state at 1.7/1.3 Å resolution, J. Mol. Biol. 197, 273-296.
29. 2 binding pocket of myohemerythrin: Role of a conserved leucine, Biochemistry 39, 8526-8536.
30. 2 release and autoxidation, J. Inorg. Biochem. 81, 293-300.
31. Kurtz, D. M., Jr. (1990) Oxo- and hydroxo-bridged diiron complexes: A chemical perspective on a biological unit, Chem. Rev. 90, 585-606.
32. Eschemann, A., Kuhl, M., and Cypionka, H. (1999) Aerotaxis in Desulfovibrio, Environ. Microbiol. 1, 489-494.
33. Fu, R., and Voordouw, G. (1997) Targeted gene-replacement mutagenesis of dcrA, encoding an oxygen sensor of the sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough, Microbiology 143, 1815-1826.
34. Johnson, M. S., Zhulin, I. B., Gapuzan, M.-E. R., and Taylor, B. L. (1997) Oxygen-dependent growth of the obligate anaerobe Desulfovibrio vulgaris Hildenborough, J. Bacteriol. 179, 5598-5601.
35. Deckers, H. M., and Voordouw, G. (1994) Membrane topology of the methyl-accepting chemotaxis protein DcrA from Desulfovibrio vulgaris Hildenborough, Antonie Van Leeuwenhoek 65, 7-12.
36. Fu, R., Wall, J. D., and Voordouw, G. (1994) DcrA, a c-type heme-containing methyl-accepting protein from Desulfovibrio vulgaris Hildenborough, senses the oxygen concentration or redox potential of the environment, J. Bacteriol. 176, 344-350.
37. McPhillips, T. M., McPhillips, S. E., Chiu, H. J., Cohen, A. E., Deacon, A. M., Ellis, P. J., Garman, E., Gonzalez, A., Sauter, N. K., Phizackerley, R. P., Soltis, S. M., and Kuhn P. (2002) Bluice and the distributed control system: Software for data acquisition and instrument control at macromolecular crystallography beamlines, J. Synchrotron Radiat. 9, 401-406.
38. Evans, G., and Pettifer, R. F. (2001) CHOOCH: A program for deriving anomalous scattering factors from X-ray fluorescence spectra, J. Appl. Crystallogr. 34, 82-86.
39. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode, Methods Enzymol. 276, 307-326.
40. Leslie, A. G. W. (1992) Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 and ESF-EAMCB Newsletter on Protein Crystallogr.
41. 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 and NMR system, Acta Crystallogr., Sect. D: Biol. Crystallogr. 54, 905-921.
42. Read, R. J., and Kleywegt, G. J. (2001) Density modification: Theory and practice, in Methods in Macromolecular Crystallography (Turk, D., and Johnson, L., Eds.) pp 123-135, IOS Press, Amsterdam, The Netherlands.
43. Kleywegt, G. J. (1999) Experimental assessment of differences between related protein crystal structures, Acta Crystallogr., Sect. D: Biol. Crystallogr. 55, 1857-1878.
44. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard, M. (1992) A, yaap, asap, @#*? A set of averaging programs, in Molecular Replacement (Dodson, E. J., Gover, S., and Wolf, W., Eds.) pp 91-105, SERC Daresbury Laboratory, Warrington, U.K.
45. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models, Acta Crystallogr., Sect. A: Found. Crystallogr. 47, 110-119.
46. Storoni, L. C., McCoy, A. J., and Read, R. J. (2004) Likehood-enhanced fast rotation functions, Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 432-438.
47. Potterton, E., Briggs, P., Turkenburg, M., and Dodson, E. (2003) A graphical user interface to the CCP4 program suite, Acta Crystallogr., Sect. D: Biol. Crystallogr. 59, 1131-1137.
48. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: A program to check the stereochemical quality of protein structures, J. Appl. Crystallogr. 26, 283-291.
49. DeLano, W. L. (2002) The PyMOL molecular graphics system, DeLano Scientific, San Carlos, CA.