Heme inhibits the DNA binding properties of the cytoplasmic heme binding protein of Shigella dysenteriae (ShuS)

Biochemistry

Volumn 46, Issue 11, 2007, Pages 2994-3000

  Kaur, Ajinder P ^a   Wilks, Angela ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF PHARMACY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING AFFINITY; CYTOPLASMIC HEME BINDING PROTEINS; FLUORESCENCE ANISOTROPY; SHIGELLA DYSENTERIAE (SHUS); VIRULENCE;

ATOMIC FORCE MICROSCOPY; DISEASES; ENZYME INHIBITION; ESCHERICHIA COLI; GENETIC ENGINEERING; PATHOGENS;

DNA;

APOPROTEIN; BACTERIAL DNA; BINDING PROTEIN; CELL DNA; DPS PROTEIN; HEME; PROTEIN SHUS; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANISOTROPY; ARTICLE; ATOMIC FORCE MICROSCOPY; BACTERIAL OUTER MEMBRANE; BACTERIAL VIRULENCE; COMPLEX FORMATION; CYTOPLASM; FLUORESCENCE; GEL PERMEATION CHROMATOGRAPHY; IMAGE ANALYSIS; MOLECULAR WEIGHT; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DNA BINDING; SHIGELLA DYSENTERIAE;

CHROMATOGRAPHY, GEL; DNA; DNA-BINDING PROTEINS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCENCE POLARIZATION; HEME; HEMEPROTEINS; MICROSCOPY, ATOMIC FORCE; OXIDATIVE STRESS; SHIGELLA DYSENTERIAE;

ESCHERICHIA COLI; SHIGELLA DYSENTERIAE;

EID: 33947402707     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061722r     Document Type: Article

References (35)

1. Ratledge, C., and Dover, L. G. (2000) Iron metabolism in pathogenic bacteria, Annu. Rev. Microbiol. 54, 881-941.
2. Otto, B. R., Verweij-van Vught, A. M., and MacLaren, D. M. (1992) Transferrins and heme-compounds as iron sources for pathogenic bacteria, Crit. Rev. Microbiol. 18, 217-233.
3. Braun, V. (2005) Bacterial iron transport related to virulence, Contrib. Microbiol. 12, 210-233.
4. Wandersman, C., and Stojiljkovic, I. (2000) Bacterial heme sources: The role of heme, hemoprotein receptors and hemophores, Curr. Opin. Microbiol. 3, 215-220.
5. Wandersman, C., and Delepelaire, P. (2004) Bacterial iron sources: From siderophores to hemophores, Annu. Rev. Microbiol. 58, 611-647.
6. Vanderpool, C. K., and Armstrong, S. K. (2001) The Bordetella bhu locus is required for heme iron utilization, J. Bacteriol. 183, 4278-4287.
7. Torres, A. G., and Payne, S. M. (1997) Haem iron-transport system in enterohaemorrhagic Escherichia coli O157:H7, Mol. Microbiol. 23, 825-833.
8. Sanders, J. D., Cope, L. D., and Hansen, E. J. (1994) Identification of a locus involved in the utilization of iron by Haemophilus influenzae, Infect. Immun. 62, 4515-4525.
9. Hanson, M. S., Pelzel, S. E., Latimer, J., Muller-Eberhard, U., and Hansen, E. J. (1992) Identification of a genetic locus of Haemophilus influenzae type b necessary for the binding and utilization of heme bound to human hemopexin, Proc. Natl. Acad. Sci. U.S.A. 89, 1973-1977.
10. Cope, L. D., Yogev, R., Muller-Eberhard, U., and Hansen, E. J. (1995) A gene cluster involved in the utilization of both free heme and heme:hemopexin by Haemophilus influenzae type b, J. Bacteriol. 177, 2644-2653.
11. Stojiljkovic, I., Hwa, V., de Saint Martin, L., O'Gaora, P., Nassif, X., Heffron, F., and So, M. (1995) The Neisseria meningitidis haemoglobin receptor: Its role in iron utilization and virulence, Mol. Microbiol. 15, 531-541.
12. Schryvers, A. B., and Stojiljkovic, I. (1999) Iron acquisition systems in the pathogenic Neisseria, Mol. Microbiol. 32, 1117-1123.
13. Mills, M., and Payne, S. M. (1995) Genetics and regulation of heme iron transport in Shigella dysenteriae and detection of an analogous system in Escherichia coli O157:H7, J. Bacteriol. 177, 3004-3009.
14. Henderson, D. P., and Payne, S. M. (1994) Vibrio cholerae iron transport systems: Roles of heme and siderophore iron transport in virulence and identification of a gene associated with multiple iron transport systems, Infect. Immun. 62, 5120-5125.
15. Stojiljkovic, I., and Hantke, K. (1992) Hemin uptake system of Yersinia enterocolitica: Similarities with other TonB-dependent systems in Gram-negative bacteria, EMBO J. 11, 4359-4367.
16. Hornung, J. M., Jones, H. A., and Perry, R. D. (1996) The hmu locus of Yersinia pestis is essential for utilization of free haemin and haem-protein complexes as iron sources, Mol. Microbiol. 20, 725-739.
17. Ochsner, U. A., Johnson, Z., and Vasil, M. L. (2000) Genetics and regulation of two distinct haem-uptake systems, phu and has, in Pseudomonas aeruginosa, Microbiology 146 (Part 1), 185-198.
18. Wyckoff, E. E., Duncan, D., Torres, A. G., Mills, M., Maase, K., and Payne, S. M. (1998) Structure of the Shigella dysenteriae haem transport locus and its phylogenetic distribution in enteric bacteria, Mol. Microbiol. 28, 1139-1152.
19. Mills, M., and Payne, S. M. (1997) Identification of shuA, the gene encoding the heme receptor of Shigella dysenteriae, and analysis of invasion and intracellular multiplication of a shuA mutant, Infect. Immun. 65, 5358-5363.
20. Eakanunkul, S., Lukat-Rodgers, G. S., Sumithran, S., Ghosh, A., Rodgers, K. R., Dawson, J. H., and Wilks, A. (2005) Characterization of the Periplasmic Heme-Binding Protein ShuT from the Heme Uptake System of Shigella dysenteriae, Biochemistry 44, 13179-13191.
21. Shea, C. M., and McIntosh, M. A. (1991) Nucleotide sequence and genetic organization of the ferric enterobactin transport system: Homology to other periplasmic binding protein-dependent systems in Escherichia coli, Mol. Microbiol. 5, 1415-1428.
22. Linton, K. J., and Higgins, C. F. (1998) The Escherichia coli ATP-binding cassette (ABC) proteins, Mol. Microbiol. 28, 5-13.
23. Wilks, A. (2001) The ShuS protein of Shigella dysenteriae is a heme-sequestering protein that also binds DNA, Arch. Biochem. Biophys. 387, 137-142.
24. Wyckoff, E. E., Lopreato, G. F., Tipton, K. A., and Payne, S. M. (2005) Shigella dysenteriae ShuS promotes utilization of heme as an iron source and protects against heme toxicity, J. Bacteriol. 187, 5658-5664.
25. Stojiljkovic, I., and Hantke, K. (1994) Transport of haemin across the cytoplasmic membrane through a haemin-specific periplasmic binding-protein- dependent transport system in Yersinia enterocolitica, Mol. Microbiol. 13, 719-732.
26. Suits, M. D., Pal, G. P., Nakatsu, K., Matte, A., Cygler, M., and Jia, Z. (2005) Identification of an Escherichia coli O157:H7 heme oxygenase with tandem functional repeats, Proc. Natl. Acad. Sci. U.S.A. 102, 16955-16960.
27. Lansky, I. B., Lukat-Rodgers, G. S., Block, D., Rodgers, K. R., Ratliff, M., and Wilks, A. (2006) The Cytoplasmic Heme-binding Protein (PhuS) from the Heme Uptake System of Pseudomonas aeruginosa Is an Intracellular Heme-trafficking Protein to the δ-Regioselective Heme Oxygenase, J. Biol. Chem. 281, 13652-13662.
28. Almiron, M., Link, A. J., Furlong, D., and Kolter, R. (1992) A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli, Genes Dev. 6, 2646-2654.
29. Wolf, S. G., Frenkiel, D., Arad, T., Finkel, S. E., Kolter, R., and Minsky, A. (1999) DNA protection by stress-induced biocrystallization, Nature 400, 83-85.
30. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Plainview, NY.
31. Yanisch-Perron, C., Vieira, J., and Messing, J. (1985) Improved M13 phage cloning vectors and host strains: Nucleotide sequences of the M13mp18 and pUC19 vectors, Gene 33, 103-119.
32. Michel, S. L., Guerrerio, A. L., and Berg, J. M. (2003) Selective RNA binding by a single CCCH zinc-binding domain from Nup475 (Tristetraprolin), Biochemistry 42, 4626-4630.
33. Martinez, A., and Kolter, R. (1997) Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps, J. Bacteriol. 179, 5188-5194.
34. Schneider, S., Sharp, K. H., Barker, P. D., and Paoli, M. (2006) An Induced Fit Conformational Change Underlies the Binding Mechanism of the Heme Transport Proteobacteria-Protein HemS, J. Biol. Chem. 281, 32606-32610.
35. Ceci, P., Cellai, S., Falvo, E., Rivetti, C., Rossi, G. L., and Chiancone, E. (2004) DNA condensation and self-aggregation of Escherichia coli Dps are coupled phenomena related to the properties of the N-terminus, Nucleic Acids Res. 32, 5935-5944.