Staphylococcus aureus uses a novel multidomain receptor to break apart human hemoglobin and steal its heme

Journal of Biological Chemistry

Volumn 288, Issue 2, 2013, Pages 1065-1078

  Spirig, Thomas ^a,e   Malmirchegini, G Reza ^a   Zhang, Jiang ^a   Robson, Scott A ^a,f   Sjodt, Megan ^a   Liu, Mengyao ^d   Kumar, Kaavya Krishna ^c   Dickson, Claire F ^c   Gell, David A ^c   Lei, Benfang ^d   Loo, Joseph A ^a,b   Clubb, Robert T ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF TASMANIA   (Australia)

^d MONTANA STATE UNIVERSITY   (United States)

^e ETH ZURICH   (Switzerland)

^f HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; ELECTROSPRAY IONIZATION; HEMOGLOBIN; IRON; MASS SPECTROMETRY; STAPHYLOCOCCUS AUREUS;

ELECTROSPRAY IONIZATION MASS SPECTROMETRY; GRAM-POSITIVE PATHOGENS; HEME TRANSFERS; IRON TRANSPORTER; LIFE-THREATENING INFECTIONS; SHAPED STRUCTURES; STERIC STRAINS; THREE-DIMENSIONAL STRUCTURE;

PORPHYRINS;

BACTERIAL PROTEIN; CARRIER PROTEIN; HEME; HEMOGLOBIN; ISDB RECEPTOR; ISDH RECEPTOR; NEAR IRON TRANSPORTER DOMAIN PROTEIN; TETRAMER; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL METABOLISM; BINDING AFFINITY; CONTROLLED STUDY; DNA SEQUENCE; ELECTROSPRAY MASS SPECTROMETRY; HOST PATHOGEN INTERACTION; HUMAN; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; STAPHYLOCOCCUS AUREUS; THREE DIMENSIONAL IMAGING; TRANSPORT KINETICS;

POSIBACTERIA; STAPHYLOCOCCUS AUREUS;

EID: 84872360057     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.419119     Document Type: Article

References (70)

1. Klevens, R. M., Morrison, M. A., Nadle, J., Petit, S., Gershman, K., Ray, S., Harrison, L. H., Lynfield, R., Dumyati, G., Townes, J. M., Craig, A. S., Zell, E. R., Fosheim, G. E., McDougal, L. K., Carey, R. B., Fridkin, S. K., and Active Bacterial Core surveillance (ABCs) MRSA Investigators (2007) Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298, 1763-1771 (Pubitemid 47598444)
2. Papanikolaou, G., and Pantopoulos, K. (2005) Iron metabolism and toxicity. Toxicol. Appl. Pharmacol. 202, 199-211 (Pubitemid 40040559)
3. Ward, P. P., and Conneely, O. M. (2004) Lactoferrin. Role in iron homeostasis and host defense against microbial infection. Biometals 17, 203-208 (Pubitemid 38987138)
4. 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
5. Reniere, M. L., Torres, V. J., and Skaar, E. P. (2007) Intracellular metalloporphyrin metabolism in Staphylococcus aureus. Biometals 20, 333-345 (Pubitemid 46776560)
6. 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)
7. Ton-That, H., Marraffini, L. A., and Schneewind, O. (2004) Protein sorting to the cell wall envelope of Gram-positive bacteria. Biochim. Biophys. Acta 1694, 269-278 (Pubitemid 39535074)
8. 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 (Pubitemid 36792002)
9. Taylor, J. M., and Heinrichs, D. E. (2002) Transferrin binding in Staphylococcus aureus. Involvement of a cell wall-anchored protein. Mol. Microbiol. 43, 1603-1614 (Pubitemid 34595550)
10. Clarke, S. R., Wiltshire, M. D., and Foster, S. J. (2004) IsdA of Staphylococcus aureus is a broad spectrum, iron-regulated adhesin. Mol. Microbiol. 51, 1509-1519 (Pubitemid 38338910)
11. 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)
12. Mazmanian, S. K., Ton-That, H., Su, K., and Schneewind, O. (2002) An iron-regulated sortase anchors a class of surface protein during Staphylococcus aureus pathogenesis. Proc. Natl. Acad. Sci. U.S.A. 99, 2293-2298 (Pubitemid 34169054)
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. Zhu, H., Xie, G., Liu, M., Olson, J. S., Fabian, M., Dooley, D. M., and Lei, B. (2008) Pathway for heme uptake from human methemoglobin by the iron-regulated surface determinants system of Staphylococcus aureus. J. Biol. Chem. 283, 18450-18460
15. 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 (Pubitemid 38044844)
16. 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
17. Pishchany, G., McCoy, A. L., Torres, V. J., Krause, J. C., Crowe, J. E., Jr., Fabry, M. E., and Skaar, E. P. (2010) Specificity for human hemoglobin enhances Staphylococcus aureus infection. Cell Host Microbe 8, 544-550
18. 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 (Pubitemid 47606047)
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. Newton, S. M., Klebba, P. E., Raynaud, C., Shao, Y., Jiang, X., Dubail, I., Archer, C., Frehel, C., and Charbit, A. (2005) The svpA-srtB locus of Listeria monocytogenes. Fur-mediated iron regulation and effect on virulence. Mol. Microbiol. 55, 927-940 (Pubitemid 40203704)
21. Xiao, Q., Jiang, X., Moore, K. J., Shao, Y., Pi, H., Dubail, I., Charbit, A., Newton, S. M., and Klebba, P. E. (2011) Sortase independent and dependent systems for acquisition of haem and haemoglobin in Listeria monocytogenes. Mol. Microbiol. 80, 1581-1597
22. Honsa, E. S., and Maresso, A. W. (2011) Mechanisms of iron import in anthrax. Biometals 24, 533-545
23. Liu, M., and Lei, B. (2005) Heme transfer from streptococcal cell surface protein Shp to HtsA of transporter HtsABC. Infect. Immun. 73, 5086-5092 (Pubitemid 41105667)
24. Nygaard, T. K., Blouin, G. C., Liu, M., Fukumura, M., Olson, J. S., Fabian, M., Dooley, D. M., and Lei, B. (2006) The mechanism of direct heme transfer from the streptococcal cell surface protein Shp to HtsA of the HtsABC transporter. J. Biol. Chem. 281, 20761-20771 (Pubitemid 44115417)
25. Zhu, H., Liu, M., and Lei, B. (2008) The surface protein Shr of Streptococcus pyogenes binds heme and transfers it to the streptococcal heme-binding protein Shp. BMC Microbiol. 8, 15
26. Andrade, M. A., Ciccarelli, F. D., Perez-Iratxeta, C., and Bork, P. (2002) NEAT: a domain duplicated in genes near the components of a putative Fe3+ siderophore transporter from Gram-positive pathogenic bacteria. Genome Biol. 3, RESEARCH0047
27. Grigg, J. C., Vermeiren, C. L., Heinrichs, D. E., and Murphy, M. E. (2007) Haem recognition by a Staphylococcus aureus NEAT domain. Mol. Microbiol. 63, 139-149 (Pubitemid 44968115)
28. 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
29. 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)
30. Villareal, V. A., Spirig, T., Robson, S. A., Liu, M., Lei, B., and Clubb, R. T. (2011) Transient weak protein-protein complexes transfer heme across the cell wall of Staphylococcus aureus. J. Am. Chem. Soc. 133, 14176-14179
31. Abe, R., Caaveiro, J. M., Kozuka-Hata, H., Oyama, M., and Tsumoto, K. (2012) Mapping ultra-weak protein-protein interactions between heme transporters of Staphylococcus aureus. J. Biol. Chem. 287, 16477-16487
32. 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 (Pubitemid 44894042)
33. 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
34. Hargrove, M. S., Whitaker, T., Olson, J. S., Vali, R. J., and Mathews, A. J. (1997) Quaternary structure regulates hemin dissociation from human hemoglobin. J. Biol. Chem. 272, 17385-17389 (Pubitemid 27311165)
35. Senturia, R., Faller, M., Yin, S., Loo, J. A., Cascio, D., Sawaya, M. R., Hwang, D., Clubb, R. T., and Guo, F. (2010) Structure of the dimerization domain of DiGeorge critical region 8. Protein Sci. 19, 1354-1365
36. Spirig, T., and Clubb, R. T. (2012) Backbone 1H, 13C, and 15N resonance assignments of the 39 kDa staphylococcal hemoglobin receptor IsdH. Biomol. NMR Assign. 6, 169-172
37. Ascoli, F., Fanelli, M. R., and Antonini, E. (1981) Preparation and properties of apohemoglobin and reconstituted hemoglobins. Methods Enzymol. 76, 72-87
38. 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
39. Cavanagh, J., Fairbrother, W. J., Palmer, A. G., and Skelton, N. J. (1996) Protein NMR Spectroscopy: Principles and Practice. Academic Press, San Diego, CA
40. Shen, Y., Delaglio, F., Cornilescu, G., and Bax, A. (2009) TALOS+. A hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR 44, 213-223
41. Vuister, G. W., and Bax, A. (1993) Quantitative J correlation. A new approach for measuring homonuclear three-bond J(HNH.α.) coupling constants in 15N-enriched proteins. J. Am. Chem. Soc. 115, 7772-7777
42. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe. A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
43. Garrett, D. S., Powers, R., Gronenborn, A. M., and Clore, G. M. (2011) A common sense approach to peak picking in two-, three-, and four-dimensional spectra using automatic computer analysis of contour diagrams. J. Magn. Reson. 213, 357-363
44. Herrmann, T., Güntert, P., and Wüthrich, K. (2002) Protein NMR structure determination with automated NOE-identification in the NOESY spectra using the new software ATNOS. J. Biomol. NMR 24, 171-189
45. Cornilescu, G., Delaglio, F., and Bax, A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13, 289-302 (Pubitemid 29143535)
46. Brünger, A. T., Clore, G. M., Gronenborn, A. M., Saffrich, R., and Nilges, M. (1993) Assessing the quality of solution nuclear magnetic resonance structures by complete cross-validation. Science 261, 328-331
47. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR. Programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486 (Pubitemid 126706801)
48. DeLano, W. L. (2006) The PyMOL Molecular Graphics System, version 0.99, DeLano Scientific, South San Francisco, CA
49. Goddard, T. D., and Kneller, D. G. (2001) Sparky NMR Analysis Software, University of California, San Francisco
50. Krishna Kumar, K., Jacques, D. A., Pishchany, G., Caradoc-Davies, T., Spirig, T., Malmirchegini, G. R., Langley, D. B., Dickson, C. F., Mackay, J. P., Clubb, R. T., Skaar, E. P., Guss, J. M., and Gell, D. A. (2011) Structural basis for hemoglobin capture by Staphylococcus aureus cell-surface protein, IsdH. J. Biol. Chem. 286, 38439-38447
51. Pilpa, R. M., Fadeev, E. A., Villareal, V. A., Wong, M. L., Phillips, M., and Clubb, R. T. (2006) Solution structure of the NEAT (NEAr Transporter) domain from IsdH/HarA. The human hemoglobin receptor in Staphylococcus aureus. J. Mol. Biol. 360, 435-447 (Pubitemid 44202313)
52. Dryla, A., Hoffmann, B., Gelbmann, D., Giefing, C., Hanner, M., Meinke, A., Anderson, A. S., Koppensteiner, W., Konrat, R., von Gabain, A., and Nagy, E. (2007) High-affinity binding of the staphylococcal HarA protein to haptoglobin and hemoglobin involves a domain with an antiparallel eight-stranded β-barrel fold. J. Bacteriol. 189, 254-264 (Pubitemid 46036241)
53. 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
54. 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
55. Loo, J. A. (2000) Electrospray ionization mass spectrometry. A technology for studying noncovalent macromolecular complexes. Int. J. Mass Spectrom. 200, 175-186
56. Sugita, Y. (1975) Differences in spectra of α and β chains of hemoglobin between isolated state and in tetramer. J. Biol. Chem. 250, 1251-1256
57. Liu, J., and Konermann, L. (2011) Protein-protein binding affinities in solution determined by electrospray mass spectrometry. J. Am. Soc. Mass Spectrom. 22, 408-417
58. Griffith, W. P., and Kaltashov, I. A. (2003) Highly asymmetric interactions between globin chains during hemoglobin assembly revealed by electrospray ionization mass spectrometry. Biochemistry 42, 10024-10033 (Pubitemid 37012878)
59. Benesch, R. E., and Kwong, S. (1995) Coupled reactions in hemoglobin. Heme-globin and dimer-dimer association. J. Biol. Chem. 270, 13785-13786
60. Moriwaki, Y., Caaveiro, J. M., Tanaka, Y., Tsutsumi, H., Hamachi, I., and Tsumoto, K. (2011) Molecular basis of recognition of antibacterial porphyrins by heme-transporter IsdH-NEAT3 of Staphylococcus aureus. Biochemistry 50, 7311-7320
61. Gouda, H., Torigoe, H., Saito, A., Sato, M., Arata, Y., and Shimada, I. (1992) Three-dimensional solution structure of the B domain of staphylococcal protein A. Comparisons of the solution and crystal structures. Biochemistry 31, 9665-9672
62. Schneider, J. P., Lombardi, A., and DeGrado, W. F. (1998) Analysis and design of three-stranded coiled coils and three-helix bundles. Fold. Des. 3, R29-R40 (Pubitemid 28166177)
63. Bunn, F. H., and Forger, B. G. (1986) Hemoglobin: Molecular, Genetic, and Clinical Aspects, pg. 21-27, W. B. Saunders Co., Philadelphia
64. Waks, M., Yip, Y. K., and Beychok, S. (1973) Influence of prosthetic groups on protein folding and subunit assembly. Recombination of separated human α- and β-globin chains with heme and alloplex interactions of globin chains with heme-containing subunits. J. Biol. Chem. 248, 6462-6470
65. Lu, C., Xie, G., Liu, M., Zhu, H., and Lei, B. (2012) Direct heme transfer reactions in the group a streptococcus heme acquisition pathway. PLoS One 7, e37556
66. Ouattara, M., Cunha, E. B., Li, X., Huang, Y. S., Dixon, D., and Eichenbaum, Z. (2010) Shr of group A streptococcus is a new type of composite NEAT protein involved in sequestering haem from methaemoglobin. Mol. Microbiol. 78, 739-756
67. Honsa, E. S., Fabian, M., Cardenas, A. M., Olson, J. S., and Maresso, A. W. (2011) The five near-iron transporter (NEAT) domain anthrax hemophore, IsdX2, scavenges heme from hemoglobin and transfers heme to the surface protein IsdC. J. Biol. Chem. 286, 33652-33660
68. Maresso, A. W., Garufi, G., and Schneewind, O. (2008) Bacillus anthracis secretes proteins that mediate heme acquisition from hemoglobin. PLoS Pathog. 4, e1000132
69. Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr. Protoc. Bioinformatics, Chapter 2, Unit 2.3
70. Wishart, D. S., Bigam, C. G., Holm, A., Hodges, R. S., and Sykes, B. D. (1995) 1H, 13C, and 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects. J. Biomol. NMR 5, 67-81