Molecular basis of recognition of antibacterial porphyrins by heme-transporter IsdH-NEAT3 of Staphylococcus aureus

Biochemistry

Volumn 50, Issue 34, 2011, Pages 7311-7320

  Moriwaki, Yoshitaka ^a   Caaveiro, Jose M M ^a   Tanaka, Yoshikazu ^b   Tsutsumi, Hiroshi ^c   Hamachi, Itaru ^c   Tsumoto, Kouhei ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBACTERIAL COMPOUNDS; ANTIBACTERIAL PROPERTIES; ANTIBACTERIAL TREATMENT; ANTIBIOTIC RESISTANCE; ANTIMICROBIAL POTENCY; BACTERIAL CELLS; BINDING AFFINITIES; DITHIONITE; EXPERIMENTAL CONDITIONS; EXTRACELLULAR; METALLOPORPHYRINS; MOLECULAR BASIS; MOLECULAR MECHANISM; NATURAL LIGANDS; OXIDATION STATE; PATHOGENIC BACTERIUM; PROTOPORPHYRIN IX; PUBLIC HEALTH; S. AUREUS; STAPHYLOCOCCUS AUREUS; STRONG CORRELATION; THREE-DIMENSIONAL STRUCTURE; TRANSFER PROPERTIES; TRANSPORT SYSTEMS; TROJAN HORSE;

BACTERIA; BACTERIOLOGY; BINDING ENERGY; IRON; IRON COMPOUNDS; MANGANESE; ZINC COMPOUNDS;

PORPHYRINS;

CARRIER PROTEIN; COPPER; HEME; IRON; MANGANESE; METALLOPORPHYRIN; PORPHYRIN DERIVATIVE; PROTEIN ISDH NEAT3; PROTOPORPHYRIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BINDING AFFINITY; MOLECULAR RECOGNITION; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEIN TRANSPORT; RECEPTOR BINDING; REGULATORY MECHANISM; STAPHYLOCOCCUS AUREUS; SURFACE PROPERTY; THREE DIMENSIONAL IMAGING;

ANTI-BACTERIAL AGENTS; ANTIGENS, BACTERIAL; BIOLOGICAL TRANSPORT; CELL MEMBRANE; HEME; LIGANDS; METALLOPORPHYRINS; MODELS, MOLECULAR; OXIDATION-REDUCTION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; STAPHYLOCOCCUS AUREUS; STATIC ELECTRICITY;

BACTERIA (MICROORGANISMS); EQUIDAE; STAPHYLOCOCCUS AUREUS;

EID: 80051986335     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200493h     Document Type: Article

References (43)

1. Kuehnert, M. J., Kruszon-Moran, D., Hill, H. A., McQuillan, G., McAllister, S. K., Fosheim, G., McDougal, L. K., Chaitram, J., Jensen, B., Fridkin, S. K., Killgore, G., and Tenover, F. C. (2006) Prevalence of Staphylococcus aureus nasal colonization in the United States, 2001-2002 J. Infect. Dis. 193, 172-179 (Pubitemid 43113478)
2. Peacock, S. J., de Silva, I., and Lowy, F. D. (2001) What determines nasal carriage of Staphylococcus aureus? Trends Microbiol. 9, 605-610 (Pubitemid 33135417)
3. Wertheim, H. F., Vos, M. C., Ott, A., van Belkum, A., Voss, A., Kluytmans, J. A., van Keulen, P. H., Vandenbroucke-Grauls, C. M., Meester, M. H., and Verbrugh, H. A. (2004) Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers Lancet 364, 703-705 (Pubitemid 39140626)
4. Lowy, F. D. (1998) Staphylococcus aureus infections N. Engl. J. Med. 339, 520-532
5. Streit, J. M., Jones, R. N., Sader, H. S., and Fritsche, T. R. (2004) Assessment of pathogen occurrences and resistance profiles among infected patients in the intensive care unit: report from the SENTRY Antimicrobial Surveillance Program (North America, 2001) Int. J. Antimicrob. Agents 24, 111-118 (Pubitemid 38993688)
6. Kollef, M. H. and Micek, S. T. (2006) Methicillin-resistant Staphylococcus aureus: a new community-acquired pathogen? Curr. Opin. Infect. Dis. 19, 161-168 (Pubitemid 44139146)
7. Smith, T. L., Pearson, M. L., Wilcox, K. R., Cruz, C., Lancaster, M. V., Robinson-Dunn, B., Tenover, F. C., Zervos, M. J., Band, J. D., White, E., and Jarvis, W. R. (1999) Emergence of vancomycin resistance in Staphylococcus aureus. Glycopeptide-Intermediate Staphylococcus aureus Working Group N. Engl. J. Med. 340, 493-501
8. Rybak, M. J. and Akins, R. L. (2001) Emergence of methicillin-resistant Staphylococcus aureus with intermediate glycopeptide resistance: clinical significance and treatment options Drugs 61, 1-7 (Pubitemid 32108318)
9. Kuklin, N. A., Clark, D. J., Secore, S., Cook, J., Cope, L. D., McNeely, T., Noble, L., Brown, M. J., Zorman, J. K., Wang, X. M., Pancari, G., Fan, H., Isett, K., Burgess, B., Bryan, J., Brownlow, M., George, H., Meinz, M., Liddell, M. E., Kelly, R., Schultz, L., Montgomery, D., Onishi, J., Losada, M., Martin, M., Ebert, T., Tan, C. Y., Schofield, T. L., Nagy, E., Meineke, A., Joyce, J. G., Kurtz, M. B., Caulfield, M. J., Jansen, K. U., McClements, W., and Anderson, A. S. (2006) A novel Staphylococcus aureus vaccine: iron surface determinant B induces rapid antibody responses in rhesus macaques and specific increased survival in a murine S. aureus sepsis model Infect. Immun. 74, 2215-2223
10. Stranger-Jones, Y. K., Bae, T., and Schneewind, O. (2006) Vaccine assembly from surface proteins of Staphylococcus aureus Proc. Natl. Acad. Sci. U. S. A. 103, 16942-16947 (Pubitemid 44737357)
11. Kim, H. K., DeDent, A., Cheng, A. G., McAdow, M., Bagnoli, F., Missiakas, D. M., and Schneewind, O. (2010) IsdA and IsdB antibodies protect mice against Staphylococcus aureus abscess formation and lethal challenge Vaccine 28, 6382-6392
12. 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 (Pubitemid 36182452)
13. 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
14. Skaar, E. P. and Schneewind, O. (2004) Iron-regulated surface determinants (Isd) of Staphylococcus aureus: stealing iron from heme Microbes Infect. 6, 390-397 (Pubitemid 38393820)
15. Pilpa, R. M., Robson, S. A., Villareal, V. A., Wong, M. L., Phillips, M., and Clubb, R. T. (2009) Functionally distinct NEAT (NEAr Transporter) domains within the Staphylococcus aureus IsdH/HarA protein extract heme from methemoglobin J. Biol. Chem. 284, 1166-1176
16. Watanabe, M., Tanaka, Y., Suenaga, A., Kuroda, M., Yao, M., Watanabe, N., Arisaka, F., Ohta, T., Tanaka, I., and Tsumoto, K. (2008) Structural basis for multimeric heme complexation through a specific protein-heme interaction: the case of the third neat domain of IsdH from Staphylococcus aureus J. Biol. Chem. 283, 28649-28659
17. Tiedemann, M. T., Muryoi, N., Heinrichs, D. E., and Stillman, M. J. (2008) Iron acquisition by the haem-binding Isd proteins in Staphylococcus aureus: studies of the mechanism using magnetic circular dichroism Biochem. Soc. Trans. 36, 1138-1143
18. Clarke, S. R. and Foster, S. J. (2008) IsdA protects Staphylococcus aureus against the bactericidal protease activity of apolactoferrin Infect. Immun. 76, 1518-1526 (Pubitemid 351561995)
19. 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
20. Ster, C., Beaudoin, F., Diarra, M. S., Jacques, M., Malouin, F., and Lacasse, P. (2010) Evaluation of some Staphylococcus aureus iron-regulated proteins as vaccine targets Vet. Immunol. Immunopathol. 136, 311-318
21. Stojiljkovic, I., Kumar, V., and Srinivasan, N. (1999) Non-iron metalloporphyrins: potent antibacterial compounds that exploit haem/Hb uptake systems of pathogenic bacteria Mol. Microbiol. 31, 429-442 (Pubitemid 29046086)
22. Begum, K., Kim, H. S., Kumar, V., Stojiljkovic, I., and Wataya, Y. (2003) In vitro antimalarial activity of metalloporphyrins against Plasmodium falciparum Parasitol. Res. 90, 221-224 (Pubitemid 36819142)
23. Yukitake, H., Naito, M., Sato, K., Shoji, M., Ohara, N., Yoshimura, M., Sakai, E., and Nakayama, K. (2011) Effects of non-iron metalloporphyrins on growth and gene expression of Porphyromonas gingivalis Microbiol. Immunol. 55, 141-153
24. Nakae, Y., Fukusaki, E. I., Kajiyama, S., Kobayashi, A., Nakajima, S., and Sakata, I. (2005) The convenient screening method using albumin for the tumor localizing property of Ga-porphyrin complexes J. Photochem. Photobiol., A 172, 55-61 (Pubitemid 40549553)
25. Tanaka, Y., Morikawa, K., Ohki, Y., Yao, M., Tsumoto, K., Watanabe, N., Ohta, T., and Tanaka, I. (2007) Structural and mutational analyses of Drp35 from Staphylococcus aureus: a possible mechanism for its lactonase activity J. Biol. Chem. 282, 5770-5780 (Pubitemid 47093737)
26. Li, J. M., Umanoff, H., Proenca, R., Russell, C. S., and Cosloy, S. D. (1988) Cloning of the Escherichia coli K-12 hemB gene J. Bacteriol. 170, 1021-1025
27. Woodward, J. J., Martin, N. I., and Marletta, M. A. (2007) An Escherichia coli expression-based method for heme substitution Nature Methods 4, 43-45 (Pubitemid 46029474)
28. Leslie, A. G. (2006) The integration of macromolecular diffraction data Acta Crystallogr., Sect. D: Biol. Crystallogr. 62, 48-57
29. Evans, P. (2006) Scaling and assessment of data quality Acta Crystallogr., Sect. D: Biol. Crystallogr. 62, 72-82
30. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674 (Pubitemid 47080256)
31. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr., Sect. D: Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
32. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 486-501
33. 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
34. Liu, M., Tanaka, W. N., Zhu, H., Xie, G., Dooley, D. M., and Lei, B. (2008) Direct hemin transfer from IsdA to IsdC in the iron-regulated surface determinant (Isd) heme acquisition system of Staphylococcus aureus J. Biol. Chem. 283, 6668-6676
35. 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
36. Pluym, M., Muryoi, N., Heinrichs, D. E., and Stillman, M. J. (2008) Heme binding in the NEAT domains of IsdA and IsdC of Staphylococcus aureus J. Inorg. Biochem. 102, 480-488
37. Tiedemann, M. T., Muryoi, N., Heinrichs, D. E., and Stillman, M. J. (2009) Characterization of IsdH (NEAT domain 3) and IsdB (NEAT domain 2) in Staphylococcus aureus by magnetic circular dichroism spectroscopy and electrospray ionization mass spectrometry J. Porphyrins Phthalocyanines 13, 1006-1016
38. Cruickshank, D. W. (1999) Remarks about protein structure precision Acta Crystallogr., Sect. D: Biol. Crystallogr. 55, 583-601 (Pubitemid 29139232)
39. Reniere, M. L., Torres, V. J., and Skaar, E. P. (2007) Intracellular metalloporphyrin metabolism in Staphylococcus aureus Biometals 20, 333-345 (Pubitemid 46776560)
40. Sharp, K. H., Schneider, S., Cockayne, A., and Paoli, M. (2007) Crystal structure of the heme-IsdC complex, the central conduit of the Isd iron/heme uptake system in Staphylococcus aureus J. Biol. Chem. 282, 10625-10631 (Pubitemid 47093412)
41. Villareal, V. A., Pilpa, R. M., Robson, S. A., Fadeev, E. A., and Clubb, R. T. (2008) The IsdC protein from Staphylococcus aureus uses a flexible binding pocket to capture heme J. Biol. Chem. 283, 31591-31600
42. Gaudin, C. F., Grigg, J. C., Arrieta, A. L., and Murphy, M. E. (2011) Unique Heme-Iron Coordination by the Hemoglobin Receptor IsdB of Staphylococcus aureus Biochemistry 50, 5443-5452
43. Smith, L. J., Kahraman, A., and Thornton, J. M. (2010) Heme proteins - diversity in structural characteristics, function, and folding Proteins 78, 2349-2368