A heme-responsive regulator controls synthesis of staphyloferrin B in staphylococcus aureus

Journal of Biological Chemistry

Volumn 291, Issue 1, 2016, Pages 29-40

  Laakso, Holly A ^a   Marolda, Cristina L ^a   Pinter, Tyler B ^a   Stillman, Martin J ^a   Heinrichs, David E ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BINS; BIOSYNTHESIS; CARBOXYLATION; DNA; ENCODING (SYMBOLS); GENE ENCODING; GENE EXPRESSION; GENES; IRON; PORPHYRINS; PROTEINS;

ACQUISITION SYSTEMS; CODING REGION; GENES ENCODING; IRON ACQUISITION; REGULATORY PROTEIN; SIDEROPHORE SYNTHESIS; STAPHYLOCOCCUS AUREUS; STARVATION CONDITIONS;

GENE EXPRESSION REGULATION;

DIMER; DNA BINDING PROTEIN; HEME; REGULATOR PROTEIN; SBNI PROTEIN; SIDEROPHORE; STAPHYLOFERRIN B; TETRAMER; UNCLASSIFIED DRUG; BACTERIAL DNA; BACTERIAL PROTEIN; CITRIC ACID; IRON; PROTEIN BINDING;

ARTICLE; BACTERIAL GROWTH; CONTROLLED STUDY; GENE EXPRESSION REGULATION; IRON METABOLISM; IRON TRANSPORT; NONHUMAN; OPERON; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN SYNTHESIS; SBN OPERON; STAPHYLOCOCCUS AUREUS; BINDING SITE; BIOLOGICAL MODEL; BIOSYNTHESIS; DRUG EFFECTS; GENE LOCUS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PROTEIN MULTIMERIZATION;

BACTERIAL PROTEINS; BASE SEQUENCE; BINDING SITES; BIOSYNTHETIC PATHWAYS; CITRATES; DNA, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC LOCI; HEME; IRON; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; OPEN READING FRAMES; OPERON; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN MULTIMERIZATION; STAPHYLOCOCCUS AUREUS;

EID: 84952942675     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.696625     Document Type: Article

References (49)

1. Mediavilla, J. R., Chen, L., Mathema, B., and Kreiswirth, B. N. (2012) Global epidemiology of community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA). Curr. Opin. Microbiol. 15, 588-595
2. Nichol, K. A., Adam, H. J., Hussain, Z., Mulvey, M. R., McCracken, M., Mataseje, L. F., Thompson, K., Kost, S., Lagacé-Wiens, P. R., Hoban, D. J., Zhanel, G. G., and Canadian Antimicrobial Resistance Alliance (CARA). (2011) Comparison of community-associated and health care-associated methicillin-resistant Staphylococcus aureus in Canada: results of the CANWARD 2007-2009 study. Diagn. Microbiol. Infect. Dis. 69, 320-325
3. Garnier, F., Tristan, A., François, B., Etienne, J., Delage-Corre, M., Martin, C., Liassine, N., Wannet, W., Denis, F., and Ploy, M. C. (2006) Pneumonia and new methicillin-resistant Staphylococcus aureus clone. Emerg. Infect. Dis. 12, 498-500
4. Moreillon, P., Que, Y. A., and Bayer, A. S. (2002) Pathogenesis of streptococcal and staphylococcal endocarditis. Infect. Dis. Clin. North Am. 16, 297-318
5. Johnson, A. P., Pearson, A., and Duckworth, G. (2005) Surveillance and epidemiology of MRSA bacteraemia in the UK. J. Antimicrob. Chemother. 56, 455-462
6. Posey, J. E., and Gherardini, F. C. (2000) Lack of a role for iron in the Lyme disease pathogen. Science 288, 1651-1653
7. Imbert, M., and Blondeau, R. (1998) On the iron requirement of lactobacilli grown in chemically defined medium. Curr. Microbiol. 37, 64-66
8. Ratledge, C., and Dover, L. G. (2000) Iron metabolism in pathogenic bacteria. Annu. Rev. Microbiol. 54, 881-941
9. Hentze, M. W., Muckenthaler, M. U., and Andrews, N. C. (2004) Balancing acts: molecular control of mammalian iron metabolism. Cell 117, 285-297
10. Hammer, N. D., and Skaar, E. P. (2011) Molecular mechanisms of Staphylococcus aureus iron acquisition. Annu. Rev. Microbiol. 65, 129-147
11. Sheldon, J. R., and Heinrichs, D. E. (2015) Recent developments in understanding the iron acquisition strategies of Gram-positive pathogens. FEMS Microbiol. Rev. 39, 592-630
12. Skaar, E. P., Humayun, M., Bae, T., DeBord, K. L., and Schneewind, O. (2004) Iron-source preference of Staphylococcus aureus infections. Science 305, 1626-1628
13. Mazmanian, S. K., Skaar, E. P., Gaspar, A. H., Humayun, M., Gornicki, P., Jelenska, J., Joachmiak, A., Missiakas, D. M., and Schneewind, O. (2003) Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299, 906-909
14. Muryoi, N., Tiedemann, M. T., Pluym, M., Cheung, J., Heinrichs, D. E., and Stillman, M. J. (2008) Demonstration of the iron-regulated surface determinant (Isd) heme transfer pathway in Staphylococcus aureus. J. Biol. Chem. 283, 28125-28136
15. Grigg, J. C., Ukpabi, G., Gaudin, C. F., and Murphy, M. E. (2010) Structural biology of heme binding in the Staphylococcus aureus Isd system. J. Inorg. Biochem. 104, 341-348
16. Pishchany, G., Sheldon, J. R., Dickson, C. F., Alam, M. T., Read, T. D., Gell, D. A., Heinrichs, D. E., and Skaar, E. P. (2014) IsdB-dependent hemoglobin binding is required for acquisition of heme by Staphylococcus aureus. J. Infect. Dis. 209, 1764-1772
17. Challis, G. L. (2005) A widely distributed bacterial pathway for siderophore biosynthesis independent of nonribosomal peptide synthetases. ChemBioChem. 6, 601-611
18. Raymond, K. N., Dertz, E. A., and Kim, S. S. (2003) Enterobactin: an archetype for microbial iron transport. Proc. Natl. Acad. Sci. U.S.A. 100, 3584-3588
19. Cheung, J., Beasley, F. C., Liu, S., Lajoie, G. A., and Heinrichs, D. E. (2009) Molecular characterization of staphyloferrin B biosynthesis in Staphylococcus aureus. Mol. Microbiol. 74, 594-608
20. Beasley, F. C., Cheung, J., and Heinrichs, D. E. (2011) Mutation of L-2, 3- diaminopropionic acid synthase genes blocks staphyloferrin B synthesis in Staphylococcus aureus. BMC Microbiol. 11, 199
21. Kobylarz, M. J., Grigg, J. C., Takayama, S. J., Rai, D. K., Heinrichs, D. E., and Murphy, M. E. (2014) Synthesis of L-2, 3-diaminopropionic acid, a siderophore, and antibiotic precursor. Chem. Biol. 21, 379-388
22. Cotton, J. L., Tao, J., and Balibar, C. J. (2009) Identification and characterization of the Staphylococcus aureus gene cluster coding for staphyloferrin A. Biochemistry 48, 1025-1035
23. Beasley, F. C., Vinés, E. D., Grigg, J. C., Zheng, Q., Liu, S., Lajoie, G. A., Murphy, M. E., and Heinrichs, D. E. (2009) Characterization of staphyloferrin A biosynthetic and transport mutants in Staphylococcus aureus. Mol. Microbiol. 72, 947-963
24. Hannauer, M., Sheldon, J. R., and Heinrichs, D. E. (2015) Involvement of major facilitator superfamily proteins SfaA and SbnD in staphyloferrin secretion in Staphylococcus aureus. FEBS Lett. 589, 730-737
25. Dale, S. E., Doherty-Kirby, A., Lajoie, G., and Heinrichs, D. E. (2004) Role of siderophore biosynthesis in virulence of Staphylococcus aureus: identification and characterization of genes involved in production of a siderophore. Infect. Immun. 72, 29-37
26. Hanses, F., Roux, C., Dunman, P. M., Salzberger, B., and Lee, J. C. (2014) Staphylococcus aureus gene expression in a rat model of infective endocarditis. Genome Med. 6, 93
27. Cheung, J., Murphy, M. E., and Heinrichs, D. E. (2012) Discovery of an iron-regulated citrate synthase in Staphylococcus aureus. Chem. Biol. 19, 1568-1578
28. Sheldon, J. R., Marolda, C. L., and Heinrichs, D. E. (2014) TCA cycle activity in Staphylococcus aureus is essential for iron-regulated synthesis of staphyloferrin A, but not staphyloferrin B: the benefit of a second citrate synthase. Mol. Microbiol. 92, 824-839
29. Andrews, S. C., Robinson, A. K., and Rodríguez-Quiñones, F. (2003) Bacterial iron homeostasis. FEMS Microbiol. Rev. 27, 215-237
30. Fillat, M. F. (2014) The fur (ferric uptake regulator) superfamily: diversity and versatility of key transcriptional regulators. Arch. Biochem. Biophys. 546, 41-52
31. Bhatt, G., and Denny, T. P. (2004) Ralstonia solanacearum iron scavenging by the siderophore staphyloferrin B is controlled by PhcA, the global virulence regulator. J. Bacteriol. 186, 7896-7904
32. Flavier, A. B., Ganova-Raeva, L. M., Schell, M. A., and Denny, T. P. (1997) Hierarchical autoinduction in Ralstonia solanacearum: control of acylhomoserine lactone production by a novel autoregulatory system responsive to 3-hydroxypalmitic acid methyl ester. J. Bacteriol. 179, 7089-7097
33. Mesak, L. R., Yim, G., and Davies, J. (2009) Improved lux reporters for use in Staphylococcus aureus. Plasmid 61, 182-187
34. Cooper, J. D., Hannauer, M., Marolda, C. L., Briere, L. A., and Heinrichs, D. E. (2014) Identification of a positively charged platform in Staphylococcus aureus HtsA that is essential for ferric staphyloferrin A transport. Biochemistry 53, 5060-5069
35. Dumont, M. E., Corin, A. F., and Campbell, G. A. (1994) Noncovalent binding of heme induces a compact apocytochrome c structure. Biochemistry 33, 7368-7378
36. Hamza, I., Chauhan, S., Hassett, R., and O'Brian, M. R. (1998) The bacterial Irr protein is required for coordination of heme biosynthesis with iron availability. J. Biol. Chem. 273, 21669-21674
37. Singleton, C., White, G. F., Todd, J. D., Marritt, S. J., Cheesman, M. R., Johnston, A. W., and Le Brun, N. E. (2010) Heme-responsive DNA binding by the global iron regulator Irr from Rhizobium leguminosarum. J. Biol. Chem. 285, 16023-16031
38. Yang, J., Ishimori, K., and O'Brian, M. R. (2005) Two heme binding sites are involved in the regulated degradation of the bacterial iron response regulator (Irr) protein. J. Biol. Chem. 280, 7671-7676
39. Cassat, J. E., and Skaar, E. P. (2013) Iron in infection and immunity. Cell Host Microbe 13, 509-519
40. Nairz, M., Haschka, D., Demetz, E., and Weiss, G. (2014) Iron at the interface of immunity and infection. Front. Pharmacol. 5, 1-10
41. Tahlan, K., Ahn, S. K., Sing, A., Bodnaruk, T. D., Willems, A. R., Davidson, A. R., and Nodwell, J. R. (2007) Initiation of actinorhodin export in Streptomyces coelicolor. Mol. Microbiol. 63, 951-961
42. Graham, T. G., Wang, X., Song, D., Etson, C. M., van Oijen, A. M., Rudner, D. Z., and Loparo, J. J. (2014) ParB spreading requires DNA bridging. Genes Dev. 28, 1228-1238
43. Reniere, M. L., and Skaar, E. P. (2008) Staphylococcus aureus haem oxygenases are differentially regulated by iron and haem. Mol. Microbiol. 69, 1304-1315
44. Visai, L., Yanagisawa, N., Josefsson, E., Tarkowski, A., Pezzali, I., Rooijakkers, S. H., Foster, T. J., and Speziale, P. (2009) Immune evasion by Staphylococcus aureus conferred by iron-regulated surface determinant protein IsdH. Microbiology. 155, 667-679
45. Torres, V. J., Pishchany, G., Humayun, M., Schneewind, O., and Skaar, E. P. (2006) Staphylococcus aureus IsdB is a hemoglobin receptor required for heme iron utilization. J. Bacteriol. 188, 8421-8429
46. Cheng, A. G., Kim, H. K., Burts, M. L., Krausz, T., Schneewind, O., and Missiakas, D. M. (2009) Genetic requirements for Staphylococcus aureus abscess formation and persistence in host tissues. FASEB J. 23, 3393-3404
47. Kreiswirth, B. N., Löfdahl, S., Betley, M. J., O'Reilly, M., Schlievert, P. M., Bergdoll, M. S., and Novick, R. P. (1983) The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305, 709-712
48. Peng, H. L., Novick, R. P., Kreiswirth, B., Kornblum, J., and Schlievert, P. (1988) Cloning, characterization and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus. J. Bacteriol. 170, 4365-4372
49. Charpentier, E., Anton, A. I., Barry, P., Alfonso, B., Fang, Y., and Novick, R. P. (2004) Novel cassette-based shuttle vector system for Gram-positive bacteria. Appl. Environ. Microbiol. 70, 6076-6085