Shr of group A streptococcus is a new type of composite NEAT protein involved in sequestering haem from methaemoglobin

Molecular Microbiology

Volumn 78, Issue 3, 2010, Pages 739-756

  Ouattara, Mahamoudou ^a   Bentley Cunha, Elizabeth ^a   Li, Xueru ^b   Huang, Ya Shu ^a   Dixon, Dabney ^a   Eichenbaum, Zehava ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

^b SOUTHWEST JIAOTONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FIBRONECTIN; HEME; IRON; LAMININ; LIGAND; METHEMOGLOBIN; PROTEIN NEAT; PROTEIN SHR; TYROSINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GROWTH; BINDING SITE; CLOSTRIDIUM; CLOSTRIDIUM NOVYI; EXTRACELLULAR MATRIX; IN VITRO STUDY; IN VIVO STUDY; IRON TRANSPORT; LIGAND BINDING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PYOGENIC BACTERIUM; STREPTOCOCCUS GROUP A;

BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CLOSTRIDIUM; HEME; HUMANS; METHEMOGLOBIN; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS PYOGENES;

CLOSTRIDIUM NOVYI; POSIBACTERIA; STREPTOCOCCUS PYOGENES; STREPTOCOCCUS SP. 'GROUP A';

EID: 77958592013     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07367.x     Document Type: Article

References (61)

1. Allen, C.E., and Schmitt, M.P. (2009) HtaA is an iron-regulated hemin binding protein involved in the utilization of heme iron in Corynebacterium diphtheriae. J Bacteriol 191: 2638-2648.
2. 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.
3. Aranda, R. t., Worley, C.E., Liu, M., Bitto, E., Cates, M.S., Olson, J.S., et al. (2007) Bis-methionyl coordination in the crystal structure of the heme-binding domain of the streptococcal cell surface protein Shp. J Mol Biol 374: 374-383.
4. Asakura, T., Minakami, S., Yoneyama, Y., and Yoshikawa, H. (1964) Combination of globin and its derivatives with hemins and porphyrins. J Biochem 56: 594-600.
5. Ascenzi, P., Bocedi, A., Visca, P., Altruda, F., Tolosano, E., Beringhelli, T., and Fasano, M. (2005) Hemoglobin and heme scavenging. IUBMB Life 57: 749-759.
6. Bates, C.S., Montañez, G.E., Woods, C.R., Vincent, R.M., and Eichenbaum, Z. (2003) Identification and characterization of a Streptococcus pyogenes operon involved in binding of hemoproteins and acquisition of iron. Infect Immun 71: 1042-1055.
7. Brown, S.B., and Lantzke, I.R. (1969) Solution structures of ferrihaem in some dipolar aprotic solvents and their binary aqueous mixtures. Biochem J 115: 279-285.
8. Bullen, J.J. (1981) The significance of iron in infection. Rev Infect Dis 3: 1127-1138.
9. 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.
10. Collier, G.S., Pratt, J.M., De Wet, C.R., and Tshabalala, C.F. (1979) Studies on haemin in dimethyl sulphoxide/water mixtures. Biochem J 179: 281-289.
11. Daou, N., Buisson, C., Gohar, M., Vidic, J., Bierne, H., Kallassy, M., et al. (2009) IlsA, a unique surface protein of Bacillus cereus required for iron acquisition from heme, hemoglobin and ferritin. PLoS Pathog 5: e1000675.
12. Drazek, E.S., Hammack, C.A., and Schmitt, M.P. (2000) Corynebacterium diphtheriae genes required for acquisition of iron from haemin and haemoglobin are homologous to ABC haemin transporters. Mol Microbiol 36: 68-84.
13. 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.
14. Dryla, A., Hoffmann, B., Gelbmann, D., Giefing, C., Hanner, M., Meinke, A., et al. (2007) High-affinity binding of the staphylococcal HarA protein to haptoglobin and hemoglobin involves a domain with an antiparallel eight-stranded beta-barrel fold. J Bacteriol 189: 254-264.
15. Eichenbaum, Z., Muller, E., Morse, S.A., and Scott, J.R. (1996) Acquisition of iron from host proteins by the group A streptococcus. Infect Immun 64: 5428-5429.
16. Eichenbaum, Z., Federle, M.J., Marra, D., De Vos, W.M., Kuipers, O.P., Kleerebezem, M., and Scott, J.R. (1998) Use of the lactococcal nisA promoter to regulate gene expression in gram-positive bacteria: comparison of induction level and promoter strength. Appl Environ Microbiol 64: 2763-2769.
17. Fisher, M., Huang, Y.S., Li, X., McIver, K.S., Toukoki, C., and Eichenbaum, Z. (2008) Shr is a broad-spectrum surface receptor that contributes to adherence and virulence in group A streptococcus. Infect Immun 76: 5006-5015.
18. Francis, R.T., Jr, Booth, J.W., and Becker, R.R. (1985) Uptake of iron from hemoglobin and the haptoglobin-hemoglobin complex by hemolytic bacteria. Int J Biochem 17: 767-773.
19. Gat, O., Zaide, G., Inbar, I., Grosfeld, H., Chitlaru, T., Levy, H., and Shafferman, A. (2008) Characterization of Bacillus anthracis iron-regulated surface determinant (Isd) proteins containing NEAT domains. Mol Microbiol 70: 983-999.
20. Genco, C.A., and Dixon, D.W. (2001) Emerging strategies in microbial haem capture. Mol Microbiol 39: 1-11.
21. 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.
22. 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.
23. Holden, M.T., Heather, Z., Paillot, R., Steward, K.F., Webb, K., Ainslie, F., et al. (2009) Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens. PLoS Pathog 5: e1000346.
24. 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.
25. Jin, B., Newton, S.M., Shao, Y., Jiang, X., Charbit, A., and Klebba, P.E. (2006) Iron acquisition systems for ferric hydroxamates, haemin and haemoglobin in Listeria monocytogenes. Mol Microbiol 59: 1185-1198.
26. Kobe, B., and Kajava, A.V. (2001) The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 11: 725-732.
27. Kunkle, C.A., and Schmitt, M.P. (2007) Comparative analysis of hmuO function and expression in Corynebacterium species. J Bacteriol 189: 3650-3654.
28. Lei, B., Liu, M., Voyich, J.M., Prater, C.I., Kala, S.V., DeLeo, F.R., and Musser, J.M. (2003) Identification and characterization of HtsA, a second heme-binding protein made by Streptococcus pyogenes. Infect Immun 71: 5962-5969.
29. Letunic, I., Doerks, T., and Bork, P. (2009) SMART 6: recent updates and new developments. Nucleic Acids Res 37: D229-D232.
30. Makinen, M.W.a.C..A.K. (1983) Structural and analytical aspects of the electronic spectra of hemproteins. In Iron Porphyrins. Gray, A.B.P.L.a.H.B. (ed.). Reading, MA: Addison-Wesley Publishing Company, pp. 141-236.
31. Maresso, A.W., Chapa, T.J., and Schneewind, O. (2006) Surface protein IsdC and Sortase B are required for heme-iron scavenging of Bacillus anthracis. J Bacteriol 188: 8145-8152.
32. Marraffini, L.A., and Schneewind, O. (2005) Anchor structure of staphylococcal surface proteins. V. Anchor structure of the sortase B substrate IsdC. J Biol Chem 280: 16263-16271.
33. 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 USA 99: 2293-2298.
34. Mazmanian, S.K., Skaar, E.P., Gaspar, A.H., Humayun, M., Gornicki, P., Jelenska, J., et al. (2003) Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299: 906-909.
35. Meehan, M., Burke, F.M., Macken, S., and Owen, P. (2010) Characterization of the haem-uptake system of the equine pathogen Streptococcus equi subsp. equi. Microbiology 156: 1824-1835.
36. Michiels, J., Xi, C., Verhaert, J., and Vanderleyden, J. (2002) The functions of Ca(2+) in bacteria: a role for EF-hand proteins? Trends Microbiol 10: 87-93.
37. Montañez, G.E., Neely, M.N., and Eichenbaum, Z. (2005) The streptococcal iron uptake (Siu) transporter is required for iron uptake and virulence in a zebrafish infection model. Microbiology 151: 3749-3757.
38. 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.
39. 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.
40. 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.
41. Rigden, D.J., Jedrzejas, M.J., and Galperin, M.Y. (2003) An extracellular calcium-binding domain in bacteria with a distant relationship to EF-hands. FEMS Microbiol Lett 221: 103-110.
42. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
43. Schultz, J., Milpetz, F., Bork, P., and Ponting, C.P. (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 95: 5857-5864.
44. 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.
45. Skaar, E.P., and Schneewind, O. (2004) Iron-regulated surface determinants (Isd) of Staphylococcus aureus: stealing iron from heme. Microbes Infect 6: 390-397.
46. 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.
47. Sook, B.R., Block, D.R., Sumithran, S., Montanez, G.E., Rodgers, K.R., Dawson, J.H., et al. (2008) Characterization of SiaA, a streptococcal heme-binding protein associated with a heme ABC transport system. Biochemistry 47: 2678-2688.
48. Stojiljkovic, I., and Perkins-Balding, D. (2002) Processing of heme and heme-containing proteins by bacteria. DNA Cell Biol 21: 281-295.
49. Thompson, J.M., Jones, H.A., and Perry, R.D. (1999) Molecular characterization of the hemin uptake locus (hmu) from Yersinia pestis and analysis of hmu mutants for hemin and hemoprotein utilization. Infect Immun 67: 3879-3892.
50. 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.
51. Tong, Y., and Guo, M. (2009) Bacterial heme-transport proteins and their heme-coordination modes. Arch Biochem Biophys 481: 1-15.
52. 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.
53. Umbreit, J. (2007) Methemoglobin - it's not just blue: a concise review. Am J Hematol 82: 134-144.
54. 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.
55. 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.
56. Wandersman, C., and Delepelaire, P. (2004) Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58: 611-647.
57. Watanabe, M., Tanaka, Y., Suenaga, A., Kuroda, M., Yao, M., Watanabe, N., et al. (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.
58. Wilks, A., and Schmitt, M.P. (1998) Expression and characterization of a heme oxygenase (Hmu O) from Corynebacterium diphtheriae. Iron acquisition requires oxidative cleavage of the heme macrocycle. J Biol Chem 273: 837-841.
59. Wu, R., Skaar, E.P., Zhang, R., Joachimiak, G., Gornicki, P., Schneewind, O., and Joachimiak, A. (2005) Staphylococcus aureus IsdG and IsdI, heme-degrading enzymes with structural similarity to monooxygenases. J Biol Chem 280: 2840-2846.
60. Zhou, Y., Yang, W., Kirberger, M., Lee, H.W., Ayalasomayajula, G., and Yang, J.J. (2006) Prediction of EF-hand calcium-binding proteins and analysis of bacterial EF-hand proteins. Proteins 65: 643-655.
61. 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.