IruO is a reductase for heme degradation by IsdI and IsdG proteins in staphylococcus aureus

Journal of Biological Chemistry

Volumn 288, Issue 36, 2013, Pages 25749-25759

  Loutet, Slade A ^a   Kobylarz, Marek J ^a   Chau, Crystal H T ^a   Murphy, Michael E P ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HEME DEGRADATION; IN-VIVO; IRON EXTRACTION; IRON SOURCES; OXIDOREDUCTASES; POTENTIAL TARGETS; REDUCTANTS; STAPHYLOCOCCUS AUREUS;

BACTERIA;

PORPHYRINS;

15 OXO BETA BILIRUBIN; 5 OXO DELTA BILIRUBIN; ASCORBIC ACID; BACTERIAL PROTEIN; BILIRUBIN DERIVATIVE; CATALASE; HEME; HYDROGEN PEROXIDE; IRON; IRON REGULATED SURFACE DETERMINANT G PROTEIN; IRON REGULATED SURFACE DETERMINANT I PROTEIN; OXIDOREDUCTASE; PROTEIN IRUO; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CHEMICAL REACTION; CLADISTICS; CONTROLLED STUDY; DEGRADATION; IRON TRANSPORT; PHYLOGENY; PRIORITY JOURNAL; PROTEIN FUNCTION; SEQUENCE HOMOLOGY; STAPHYLOCOCCUS AUREUS;

FAD; HEME; IRON; REDUCTASE; STAPHYLOBILINS; STAPHYLOCOCCUS AUREUS;

BACTERIAL PROTEINS; FLAVOPROTEINS; HEME; HYDROGEN PEROXIDE; IRON; MIXED FUNCTION OXYGENASES; NADP; OXIDANTS; OXYGENASES; STAPHYLOCOCCUS AUREUS;

EID: 84883721548     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.470518     Document Type: Article

References (80)

1. Gordon, R. J., and Lowy, F. D. (2008) Pathogenesis of methicillin-resistant Staphylococcus aureus infection. Clin. Infect. Dis. 46, S350-S359
2. Lowy, F. D. (1998) Staphylococcus aureus infections. N. Engl. J. Med. 339, 520-532
3. Thurlow, L. R., Joshi, G. S., and Richardson, A. R. (2012) Virulence strategies of the dominant USA300 lineage of community-associated methicillin- resistant Staphylococcus aureus (CA-MRSA). FEMS Immunol. Med. Microbiol. 65, 5-22
4. Nimmo, G. R. (2012) USA300 abroad. Global spread of a virulent strain of community-associated methicillin-resistant Staphylococcus aureus. Clin. Microbiol. Infect. 18, 725-734
5. Bullen, J. J., Rogers, H. J., Spalding, P. B., and Ward, C. G. (2005) Iron and infection. The heart of the matter. FEMS Immunol. Med. Microbiol. 43, 325-330
6. Weinberg, E. D. (1977) Infection and iron metabolism. Am. J. Clin. Nutr. 30, 1485-1490
7. Hammer, N. D., and Skaar, E. P. (2011) Molecular mechanisms of Staphylococcus aureus iron acquisition. Annu. Rev. Microbiol. 65, 129-147
8. 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
9. 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
10. 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
11. Sebulsky, M. T., Hohnstein, D., Hunter, M. D., and Heinrichs, D. E. (2000) Identification and characterization of a membrane permease involved in iron-hydroxamate transport in Staphylococcus aureus. J. Bacteriol. 182, 4394-4400
12. 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
13. 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
14. 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
15. 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
16. Vermeiren, C. L., Pluym, M., Mack, J., Heinrichs, D. E., and Stillman, M. J. (2006) Characterization of the heme binding properties of Staphylococcus aureus IsdA. Biochemistry 45, 12867-12875
17. Pishchany, G., Dickey, S. E., and Skaar, E. P. (2009) Subcellular localization of the Staphylococcus aureus heme iron transport components IsdA and IsdB. Infect. Immun. 77, 2624-2634
18. Tiedemann, M. T., Heinrichs, D. E., and Stillman, M. J. (2012) The multiprotein heme shuttle pathway in Staphylococcus aureus. Isd cog-wheel kinetics. J. Am. Chem. Soc. 134, 16578-16585
19. Dryla, A., Gelbmann, D., von Gabain, A., and Nagy, E. (2003) Identification of a novel iron regulated staphylococcal surface protein with haptoglobin- haemoglobin binding activity. Mol. Microbiol. 49, 37-53
20. Grigg, J. C., Vermeiren, C. L., Heinrichs, D. E., and Murphy, M. E. (2007) Heme coordination by Staphylococcus aureus IsdE. J. Biol. Chem. 282, 28815-28822
21. Pluym, M., Vermeiren, C. L., Mack, J., Heinrichs, D. E., and Stillman, M. J. (2007) Heme binding properties of Staphylococcus aureus IsdE. Biochemistry 46, 12777-12787
22. Skaar, E. P., Gaspar, A. H., and Schneewind, O. (2004) IsdG and IsdI, heme-degrading enzymes in the cytoplasm of Staphylococcus aureus. J. Biol. Chem. 279, 436-443
23. Wu, R., Skaar, E. P., Zhang, R., Joachimiak, G., Gornicki, P., Schneewind, O., and Joachimiak, A. (2005) Staphylococcus aureus IsdG and IsdI, hemedegrading enzymes with structural similarity to monooxygenases. J. Biol. Chem. 280, 2840-2846
24. Reniere, M. L., and Skaar, E. P. (2008) Staphylococcus aureus haem oxygenases are differentially regulated by iron and haem. Mol. Microbiol. 69, 1304-1315
25. 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
26. Mason, W. J., and Skaar, E. P. (2009) Assessing the contribution of hemeiron acquisition to Staphylococcus aureus pneumonia using computed tomography. PLoS ONE 4, e6668
27. Reniere, M. L., Ukpabi, G. N., Harry, S. R., Stec, D. F., Krull, R., Wright, D. W., Bachmann, B. O., Murphy, M. E., and Skaar, E. P. (2010) The IsdG-family of haem oxygenases degrades haem to a novel chromophore. Mol. Microbiol. 75, 1529-1538
28. Matsui, T., Nambu, S., Ono, Y., Goulding, C. W., Tsumoto, K., and Ikeda- Saito, M. (2013) Heme degradation by Staphylococcus aureus IsdG and IsdI liberates formaldehyde rather than carbon monoxide. Biochemistry 52, 3025-3027
29. Lee, W. C., Reniere, M. L., Skaar, E. P., and Murphy, M. E. (2008) Ruffling of metalloporphyrins bound to IsdG and IsdI, two heme-degrading enzymes in Staphylococcus aureus. J. Biol. Chem. 283, 30957-30963
30. Takayama, S.-i. J., Ukpabi, G., Murphy, M. E., and Mauk, A. G. (2011) Electronic properties of the highly ruffled heme bound to the heme degrading enzyme IsdI. Proc. Natl. Acad. Sci. 108, 13071-13076
31. Ukpabi, G., Takayama, S.-i. J., Mauk, A. G., and Murphy, M. E. (2012) Inactivation of IsdI heme oxidation by an active site substitution that diminishes heme ruffling. J. Biol. Chem. 287, 34179-88179
32. MacPherson, I. S., Rosell, F. I., Scofield, M., Mauk, A. G., and Murphy, M. E. (2010) Directed evolution of copper nitrite reductase to a chromogenic reductant. Protein Eng. Des. Sel. 23, 137-145
33. Tropea, J. E., Cherry, S., and Waugh, D. S. (2009) Expression and purification of soluble His6-tagged TEV protease. Methods Mol. Biol. 498, 297-307
34. Aliverti, A., Curti, B., and Vanoni, M. A. (1999) Identifying and quantitating FAD and FMN in simple and in iron-sulfur-containing flavoproteins. Methods Mol. Biol. 131, 9-23
35. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410
36. Di Tommaso, P., Moretti, S., Xenarios, I., Orobitg, M., Montanyola, A., Chang, J.-M., Taly, J.-F., and Notredame, C. (2011) T-Coffee.Aweb server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res. 39, W13-W17
37. Notredame, C., Higgins, D. G., and Heringa, J. (2000) T-coffee. A novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205-217
38. Gouy, M., Guindon, S., and Gascuel, O. (2010) SeaView version A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 27, 221-224
39. Allard, M., Moisan, H., Brouillette, E., Gervais, A. L., Jacques, M., Lacasse, P., Diarra, M. S., and Malouin, F. (2006) Transcriptional modulation of some Staphylococcus aureus iron-regulated genes during growth in vitro and in a tissue cage model in vivo. Microbes Infect. 8, 1679-1690
40. Jang, H. J., Nde, C., Toghrol, F., and Bentley, W. E. (2008) Microarray analysis of toxicogenomic effects of ortho-phenylphenol in Staphylococcus aureus. BMC genomics 9, 411
41. Palazzolo-Ballance, A. M., Reniere, M. L., Braughton, K. R., Sturdevant, D. E., Otto, M., Kreiswirth, B. N., Skaar, E. P., and DeLeo, F. R. (2008) Neutrophil microbicides induce a pathogen survival response in community- associated methicillin-resistant Staphylococcus aureus. J. Immunol. 180, 500-509
42. Malachowa, N., Whitney, A. R., Kobayashi, S. D., Sturdevant, D. E., Kennedy, A. D., Braughton, K. R., Shabb, D. W., Diep, B. A., Chambers, H. F., Otto, M., and DeLeo, F. R. (2011) Global changes in Staphylococcus aureus gene expression in human blood. PLoS One 6, e18617
43. Chang, W., Toghrol, F., and Bentley, W. E. (2006) Toxicogenomic response of Staphylococcus aureus to peracetic acid. Environ. Sci. Technol. 40, 5124-5131
44. Michel, A., Agerer, F., Hauck, C. R., Herrmann, M., Ullrich, J., Hacker, J., and Ohlsen, K. (2006) Global regulatory impact of ClpP protease of Staphylococcus aureus on regulons involved in virulence, oxidative stress response, autolysis, and DNA repair. J. Bacteriol. 188, 5783-5796
45. Richardson, A. R., Dunman, P. M., and Fang, F. C. (2006) The nitrosative stress response of Staphylococcus aureus is required for resistance to innate immunity. Mol. Microbiol. 61, 927-939
46. Sobral, R. G., Jones, A. E., Des Etages, S. G., Dougherty, T. J., Peitzsch, R. M., Gaasterland, T., Ludovice, A. M., de Lencastre, H., and Tomasz, A. (2007) Extensive and genome-wide changes in the transcription profile of Staphylococcus aureus induced by modulating the transcription of the cell wall synthesis gene murF. J. Bacteriol. 189, 2376-2391
47. Heinrichs, J. H., Gatlin, L. E., Kunsch, C., Choi, G. H., and Hanson, M. S. (1999) Identification and characterization of SirA, an iron-regulated protein from Staphylococcus aureus. J. Bacteriol. 181, 1436-1443
48. Xiong, A., Singh, V. K., Cabrera, G., and Jayaswal, R. K. (2000) Molecular characterization of the ferric-uptake regulator, Fur, from Staphylococcus aureus. Microbiology 146, 659-668
49. Baba, T., Bae, T., Schneewind, O., Takeuchi, F., and Hiramatsu, K. (2008) Genome sequence of Staphylococcus aureus strain Newman and comparative analysis of staphylococcal genomes. Polymorphism and evolution of two major pathogenicity islands. J. Bacteriol. 190, 300-310
50. Gill, S. R., Fouts, D. E., Archer, G. L., Mongodin, E. F., Deboy, R. T., Ravel, J., Paulsen, I. T., Kolonay, J. F., Brinkac, L., Beanan, M., Dodson, R. J., Daugherty, S. C., Madupu, R., Angiuoli, S. V., Durkin, A. S., Haft, D. H., Vamathevan, J., Khouri, H., Utterback, T., Lee, C., Dimitrov, G., Jiang, L., Qin, H., Weidman, J., Tran, K., Kang, K., Hance, I. R., Nelson, K. E., and Fraser, C. M. (2005) Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J. Bacteriol. 187, 2426-2438
51. Diep, B. A., Gill, S. R., Chang, R. F., Phan, T. H., Chen, J. H., Davidson, M. G., Lin, F., Lin, J., Carleton, H. A., Mongodin, E. F., Sensabaugh, G. F., and Perdreau-Remington, F. (2006) Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367, 731-739
52. Komori, H., Seo, D., Sakurai, T., and Higuchi, Y. (2010) Crystal structure analysis of Bacillus subtilis ferredoxin-NADP oxidoreductase and the structural basis for its substrate selectivity. Protein Sci. 19, 2279-2290
53. Kuriyan, J., Krishna, T. S., Wong, L., Guenther, B., Pahler, A., Williams, C. H., Jr., and Model, P. (1991) Convergent evolution of similar function in two structurally divergent enzymes. Nature 352, 172-174
54. Oliveira, M. A., Discola, K. F., Alves, S. V., Medrano, F. J., Guimarães, B. G., and Netto, L. E. (2010) Insights into the specificity of thioredoxin reductase- thioredoxin interactions. A structural and functional investigation of the yeastthioredoxin system. Biochemistry 49, 3317-3326
55. Kirkensgaard, K. G., Hägglund, P., Finnie, C., Svensson, B., and Henriksen, A. (2009) Structure of Hordeum vulgare NADPH-dependent thioredoxin reductase Unwinding the reaction mechanism. Acta Crystallogr. D. Biol. Crystallogr. 65, 932-941
56. Bieger, B., and Essen, L.-O. (2001) Crystal structure of the catalytic core component of the alkylhydroperoxide reductase AhpF from Escherichia coli. J. Mol. Biol. 307, 1-8
57. Finn, R. D., Mistry, J., Tate, J., Coggill, P., Heger, A., Pollington, J. E., Gavin, O. L., Gunasekaran, P., Ceric, G., Forslund, K., Holm, L., Sonnhammer, E. L., Eddy, S. R., and Bateman, A. (2010) The Pfam protein families database. Nucleic Acids Res. 38, D211-D222
58. Lennon, B. W., Williams, C. H., Jr., and Ludwig, M. L. (2000) Twists in catalysis. Alternating conformations of Escherichia coli thioredoxin reductase. Science 289, 1190-1194
59. Kunst, F., Ogasawara, N., Moszer, I., Albertini, A. M., Alloni, G., Azevedo, V., Bertero, M. G., Bessières, P., Bolotin, A., Borchert, S., Borriss, R., Boursier, L., Brans, A., Braun, M., Brignell, S. C., Bron, S., Brouillet, S., Bruschi, C.V., Caldwell, B., Capuano, V., Carter, N. M., Choi, S. K., Codani, J. J., Connerton, I. F., and Danchin, A. (1997) The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 390, 249-256
60. Ravel, J., Jiang, L., Stanley, S. T., Wilson, M. R., Decker, R. S., Read, T. D., Worsham, P., Keim, P. S., Salzberg, S. L., Fraser-Liggett, C. M., and Rasko, D. A. (2009) The complete genome sequence of Bacillus anthracis Ames "Ancestor." J. Bacteriol. 191, 445-446
61. Glaser, P., Frangeul, L., Buchrieser, C., Rusniok, C., Amend, A., Baquero, F., Berche, P., Bloecker, H., Brandt, P., Chakraborty, T., Charbit, A., Chetouani, F., Couvé, E., de Daruvar, A., Dehoux, P., Domann, E., Domínguez- Bernal, G., Duchaud, E., Durant, L., Dussurget, O., Entian, K. D., Fsihi, H., García-del Portillo, F., Garrido, P., Gautier, L., Goebel, W., Gómez-López, N., Hain, T., Hauf, J., Jackson, D., Jones, L. M., Kaerst, U., Kreft, J., Kuhn, M., Kunst, F., Kurapkat, G., Madueno, E., Maitournam, A., Vicente, J. M., Ng, E., Nedjari, H., Nordsiek, G., Novella, S., de Pablos, B., Pérez-Diaz, J. C., Purcell, R., Remmel, B., Rose, M., Schlueter, T., Simoes, N., Tierrez, A. (2001) Comparative genomics of Listeria species. Science 294, 849-852
62. Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S., Barry, C. E., 3rd, Tekaia, F., Badcock, K., Basham, D., Brown, D., Chillingworth, T., Connor, R., Davies, R., Devlin, K., Feltwell, T., Gentles, S., Hamlin, N., Holroyd, S., Hornsby, T., Jagels, K., Krogh, A., McLean, J., Moule, S., Murphy, L., Oliver, K., Osborne, J., Quail, M. A., Rajandream, M. A., Rogers, J., Rutter, S., Seeger, K., Skelton, J., Squares, R., Squares, S., Sulston, J. E., Taylor, K., Whitehead, S., and Barrell, B. G. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544
63. Ollinger, J., Song, K. B., Antelmann, H., Hecker, M., and Helmann, J. D. (2006) Role of the Fur regulon in iron transport in Bacillus subtilis. J. Bacteriol. 188, 3664-3673
64. Ledala, N., Sengupta, M., Muthaiyan, A., Wilkinson, B. J., and Jayaswal, R. K. (2010) Transcriptomic response of Listeria monocytogenes to iron limitation and Fur mutation. Appl. Environ. Microbiol. 76, 406-416
65. Carlson, P. E., Jr., Carr, K. A., Janes, B. K., Anderson, E. C., and Hanna, P. C. (2009) Transcriptional profiling of Bacillus anthracis Sterne (34F2) during iron starvation. PLoS ONE 4, e6988
66. Bergman, N. H., Anderson, E. C., Swenson, E. E., Janes, B. K., Fisher, N., Niemeyer, M. M., Miyoshi, A. D., and Hanna, P. C. (2007) Transcriptional profiling of Bacillus anthracis during infection of host macrophages. Infect. Immun. 75, 3434-3444
67. Zapotoczna, M., Heilbronner, S., Speziale, P., and Foster, T. J. (2012) Ironregulated surface determinant (Isd) proteins of Staphylococcus lugdunensis. J. Bacteriol. 194, 6453-6467
68. Haley, K. P., Janson, E. M., Heilbronner, S., Foster, T. J., and Skaar, E. P. (2011) Staphylococcus lugdunensis IsdG liberates iron from host heme. J. Bacteriol. 193, 4749-4757
69. Heilbronner, S., Holden, M. T., van Tonder, A., Geoghegan, J. A., Foster, T. J., Parkhill, J., and Bentley, S. D. (2011) Genome sequence of Staphylococcus lugdunensis N920143 allows identification of putative colonization and virulence factors. FEMS Microbiol. Lett. 322, 60-67
70. Seo, D., Kamino, K., Inoue, K., and Sakurai, H. (2004) Purification and characterization of ferredoxin-NADP reductase encoded by Bacillus subtilis yumC. Arch. Microbiol. 182, 80-89
71. Laurent, T. C., Moore, E. C., and Reichard, P. (1964) Enzymatic synthesis of deoxyribonucleotides. IV. Isolation and characterization of thioredoxin, the hydrogen donor from Escherichia coli B. J. Biol. Chem. 239, 3436-3444
72. Moore, E. C., Reichard, P., and Thelander, L. (1964) Enzymatic synthesis of deoxyribonucleotides. V. Purification and properties of thioredoxin reductase from Escherichia coli B. J. Biol. Chem. 239, 3445-3452
73. Russel, M., and Model, P. (1985) Direct cloning of the trxB gene that encodes thioredoxin reductase. J. Bacteriol. 163, 238-242
74. Navarro, J. A., Gleason, F. K., Cusanovich, M. A., Fuchs, J. A., Meyer, T. E., and Tollin, G. (1991) Kinetics of electron transfer from thioredoxin reductase to thioredoxin. Biochemistry 30, 2192-2195
75. Williams, C. H., Arscott, L. D., Müller, S., Lennon, B. W., Ludwig, M. L., Wang, P.-F., Veine, D. M., Becker, K., and Schirmer, R. H. (2000) Thioredoxin reductase. Eur. J. Biochem. 267, 6110-6117
76. Yoshinaga, T., Sassa, S., and Kappas, A. (1982) Purification and properties of bovine spleen heme oxygenase. Amino acid composition and sites of action of inhibitors of heme oxidation. J. Biol. Chem. 257, 7778-7785
77. Bonkovsky, H. L., Healey, J. F., and Pohl, J. (1990) Purification and characterization of heme oxygenase from chick liver. Eur. J. Biochem. 189, 155-166
78. Valton, J., Mathevon, C., Fontecave, M., Nivière, V., and Ballou, D. P. (2008) Mechanism and regulation of the two-component FMN-dependent monooxygenase ActVA-ActVB from Streptomyces coelicolor. J. Biol. Chem. 283, 10287-10296
79. Chim, N., Iniguez, A., Nguyen, T. Q., and Goulding, C. W. (2010) Unusual diheme conformation of the heme-degrading protein from Mycobacterium tuberculosis. J. Mol. Biol. 395, 595-608
80. Nambu, S., Matsui, T., Goulding, C. W., Takahashi, S., and Ikeda-Saito, M. (2013) A new way to degrade heme. The Mycobacterium tuberculosis enzymeMhuDcatalyzes heme degradation without generating CO. J. Biol. Chem. 288, 10101-10109