Sortase independent and dependent systems for acquisition of haem and haemoglobin in Listeria monocytogenes

Molecular Microbiology

Volumn 80, Issue 6, 2011, Pages 1581-1597

  Xiao, Qiaobin ^a   Jiang, Xiaoxu ^a,d   Moore, Kyle J ^a   Shao, Yi ^a   Pi, Hualiang ^a   Dubail, Iharilalao ^b,c   Charbit, Alain ^b,c   Newton, Salete M ^a,d   Klebba, Phillip E ^a,d  

^a UNIVERSITY OF OKLAHOMA   (United States)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c INSERM   (France)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; CELL MEMBRANE PROTEIN; FERRIC ION; FERRIOXAMINE; HEME; HEMOGLOBIN; IRON BINDING PROTEIN; LIPOPROTEIN; PEPTIDOGLYCAN; PERMEASE; PORPHYRIN; PROTEIN FHUD; PROTEIN HBP2; PROTEIN HUPD; PROTEIN HUPDGC; PROTEIN HUPG; SIDEROPHORE; SORTASE; SORTASE A; SORTASE B; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BINDING AFFINITY; CELL MEMBRANE TRANSPORT; CHROMOSOME DELETION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOPLASM; ENZYME PURIFICATION; FEMALE; GENETIC CODE; GENETIC COMPLEMENTATION; IRON TRANSPORT; LD 50; LISTERIA MONOCYTOGENES; LISTERIOSIS; MOUSE; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN FUNCTION; STAPHYLOCOCCUS AUREUS; WILD TYPE;

AMINOACYLTRANSFERASES; ANIMALS; BACTERIAL PROTEINS; CYSTEINE ENDOPEPTIDASES; FEMALE; HEME; HEMOGLOBINS; HUMANS; LISTERIA MONOCYTOGENES; LISTERIOSIS; MICE; OPERON; VIRULENCE;

LISTERIA MONOCYTOGENES; STAPHYLOCOCCUS AUREUS;

EID: 79958795022     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07667.x     Document Type: Article

References (83)

1. Annamalai, R., Jin, B., Cao, Z., Newton, S.M., and Klebba, P.E. (2004) Recognition of ferric catecholates by FepA. J Bacteriol 186: 3578-3589.
2. Arnoux, P., Haser, R., Izadi, N., Lecroisey, A., Delepierre, M., Wandersman, C., and Czjzek, M. (1999) The crystal structure of HasA, a hemophore secreted by Serratia marcescens. Nat Struct Biol 6: 516-520.
3. Arslan, S.Y., Leung, K.P., and Wu, C.D. (2009) The effect of lactoferrin on oral bacterial attachment. Oral Microbiol Immunol 24: 411-416.
4. Asher, C., de Villiers, K.A., and Egan, T.J. (2009) Speciation of ferriprotoporphyrin IX in aqueous and mixed aqueous solution is controlled by solvent identity, pH, and salt concentration. Inorg Chem 48: 7994-8003.
5. Babusiak, M., Man, P., Sutak, R., Petrak, J., and Vyoral, D. (2005) Identification of heme binding protein complexes in murine erythroleukemic cells: study by a novel two-dimensional native separation - liquid chromatography and electrophoresis. Proteomics 5: 340-350.
6. Baichoo, N., Wang, T., Ye, R., and Helmann, J.D. (2002) Global analysis of the Bacillus subtilis Fur regulon and the iron starvation stimulon. Mol Microbiol 45: 1613-1629.
7. Bierne, H., Mazmanian, S.K., Trost, M., Pucciarelli, M.G., Liu, G., Dehoux, P., etal. (2002) Inactivation of the srtA gene in Listeria monocytogenes inhibits anchoring of surface proteins and affects virulence. Mol Microbiol 43: 869-881.
8. Bierne, H., Garandeau, C., Pucciarelli, M.G., Sabet, C., Newton, S.M., del Portillo, F.G., etal. (2004) Sortase B, a new class of sortase in Listeria monocytogenes. J Bacteriol 186: 1972-1982.
9. Bigot, A., Pagniez, H., Botton, E., Frehel, C., Dubail, I., Jacquet, C., etal. (2005) Role of FliF and FliI of Listeria monocytogenes in flagellar assembly and pathogenicity. Infect Immun 73: 5530-5539.
10. Braun, V. (2005) Bacterial iron transport related to virulence. Contrib Microbiol 12: 210-233.
11. Burkhard, K.A., and Wilks, A. (2008) Functional characterization of the Shigella dysenteriae heme ABC transporter. Biochemistry 47: 7977-7979.
12. Cabrera, G., Xiong, A., Uebel, M., Singh, V.K., and Jayaswal, R.K. (2001) Molecular characterization of the iron-hydroxamate uptake system in Staphylococcus aureus. Appl Environ Microbiol 67: 1001-1003.
13. Camejo, A., Buchrieser, C., Couve, E., Carvalho, F., Reis, O., Ferreira, P., etal. (2009) In vivo transcriptional profiling of Listeria monocytogenes and mutagenesis identify new virulence factors involved in infection. PLoS Pathog 5: e1000449.
14. Carniel, E. (2001) The Yersinia high-pathogenicity island: an iron-uptake island. Microbes Infect 3: 561-569.
15. Chastanet, A., Derre, I., Nair, S., and Msadek, T. (2004) clpB, a novel member of the Listeria monocytogenes CtsR regulon, is involved in virulence but not in general stress tolerance. J Bacteriol 186: 1165-1174.
16. de Chastellier, C., and Berche, P. (1994) Fate of Listeria monocytogenes in murine macrophages: evidence for simultaneous killing and survival of intracellular bacteria. Infect Immun 62: 543-553.
17. Clarke, T.E., Braun, V., Winkelmann, G., Tari, L.W., and Vogel, H.J. (2002) X-ray crystallographic structures of the Escherichia coli periplasmic protein FhuD bound to hydroxamate-type siderophores and the antibiotic albomycin. J Biol Chem 277: 13966-13972.
18. 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.
19. Dale, S.E., Sebulsky, M.T., and Heinrichs, D.E. (2004) Involvement of SirABC in iron-siderophore import in Staphylococcus aureus. J Bacteriol 186: 8356-8362.
20. Demchick, P., and Koch, A.L. (1996) The permeability of the wall fabric of Escherichia coli and Bacillus subtilis. J Bacteriol 178: 768-773.
21. Dower, W.J., Miller, J.F., and Ragsdale, C.W. (1988) High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res 16: 6127-6145.
22. Drazek, E.S., Hammack, C.A., and Schmitt, M.P. (2000) Corynebacterium diphtheriae genes required for acquisition of iron from haemin and Hb are homologous to ABC haemin transporters. Mol Microbiol 36: 68-84.
23. Emery, T. (1971) Role of ferrichrome as a ferric ionophore in Ustilago sphaerogena. Biochemistry 10: 1483-1488.
24. Fabian, M., Solomaha, E., Olson, J.S., and Maresso, A.W. (2009) Heme transfer to the bacterial cell envelope occurs via a secreted hemophore in the Gram-positive pathogen Bacillus anthracis. J Biol Chem 284: 32138-32146.
25. Falk, J.E. (1964) Porphyrins and Metalloporphyrins. New York: American Elsevier Publishing Company.
26. Ginalski, K. (2006) Comparative modeling for protein structure prediction. Curr Opin Struct Biol 16: 172-177.
27. Glaser, P., Frangeul, L., Buchrieser, C., Rusniok, C., Amend, A., Baquero, F., etal. (2001) Comparative genomics of Listeria species. Science 294: 849-852.
28. 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.
29. Hanahan, D. (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166: 557-580.
30. Hanks, T.S., Liu, M., McClure, M.J., and Lei, B. (2005) ABC transporter FtsABCD of Streptococcus pyogenes mediates uptake of ferric ferrichrome. BMC Microbiol 5: 62.
31. Immenschuh, S., Baumgart-Vogt, E., and Mueller, S. (2010) Heme oxygenase-1 and iron in liver inflammation: a complex alliance. Curr Drug Targets 11: 1541-1550.
32. Jin, B., Newton, S.M., Shao, Y., Jiang, X., Charbit, A., and Klebba, P.E. (2005) Iron acquisition systems for ferric hydroxamates, haemin and haemoglobin in Listeria monocytogenes. Mol Microbiol 59: 1185-1198.
33. Konopka, K., Mareschal, J.C., and Crichton, R.R. (1981) Iron transfer form transferrin to ferritin mediated by polyphosphate compounds. Biochim Biophys Acta 677: 417-423.
34. Konopka, K., Bindereif, A., and Neilands, J.B. (1982) Aerobactin-mediated utilization of transferrin iron. Biochemistry 21: 6503-6508.
35. Kryshtafovych, A., Venclovas, C., Fidelis, K., and Moult, J. (2005) Progress over the first decade of CASP experiments. Proteins 61 (Suppl. 7): 225-236.
36. Lauer, P., Chow, M.Y., Loessner, M.J., Portnoy, D.A., and Calendar, R. (2002) Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors. J Bacteriol 184: 4177-4186.
37. 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.
38. Lei, B., Smoot, L.M., Menning, H.M., Voyich, J.M., Kala, S.V., Deleo, F.R., etal. (2002) Identification and characterization of a novel heme-associated cell surface protein made by Streptococcus pyogenes. Infect Immun 70: 4494-4500.
39. 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.
40. Li, X.L., Robbins, J.W., Jr., and Taylor, K.B. (1990) The production of recombinant beta- galactosidase in Escherichia coli in yeast extract enriched medium. J Ind Microbiol 5: 85-93.
41. Liu, M., and Lei, B. (2005) Heme transfer from streptococcal cell surface protein Shp to HtsA of transporter HtsABC. Infect Immun 73: 5086-5092.
42. 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.
43. Maresso, A.W., Garufi, G., and Schneewind, O. (2008) Bacillus anthracis secretes proteins that mediate heme acquisition from hemoglobin. PLoS Pathog 4: e1000132.
44. 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.
45. Mazmanian, S.K., Skaar, E.P., Gaspar, A.H., Humayun, M., Gornicki, P., Jelenska, J., etal. (2003) Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299: 906-909.
46. Meroueh, S.O., Bencze, K.Z., Hesek, D., Lee, M., Fisher, J.F., Stemmler, T.L., and Mobashery, S. (2006) Three-dimensional structure of the bacterial cell wall peptidoglycan. Proc Natl Acad Sci USA 103: 4404-4409.
47. Neidhardt, F.C., Bloch, P.L., and Smith, D.F. (1974) Culture medium for enterobacteria. J Bacteriol 119: 736-747.
48. Neilands, J.B. (1974) Iron and its role in microbial physiology. In Microbial Iron Metabolism - A Comprehensive Treatise. Neilands, J.B. (ed.). New York: Academic Press, pp. 4-34.
49. Newton, S.M., Igo, J.D., Scott, D.C., and Klebba, P.E. (1999) Effect of loop deletions on the binding and transport of ferric enterobactin by FepA. Mol Microbiol 32: 1153-1165.
50. Newton, S.M., Klebba, P.E., Raynaud, C., Shao, Y., Jiang, X., Dubail, I., etal. (2005) The svpA-srtB locus of Listeria monocytogenes: Fur-mediated iron regulation and effect on virulence. Mol Microbiol 55: 927-940.
51. Newton, S.M., Trinh, V., Pi, H., and Klebba, P.E. (2010) Direct measurements of the outer membrane stage of ferric enterobactin transport: postuptake binding. J Biol Chem 285: 17488-17497.
52. Nygaard, T.K., Blouin, G.C., Liu, M., Fukumura, M., Olson, J.S., Fabian, M., etal. (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.
53. Perry, R.D., Shah, J., Bearden, S.W., Thompson, J.M., and Fetherston, J.D. (2003) Yersinia pestis TonB: role in iron, heme, and hemoprotein utilization. Infect Immun 71: 4159-4162.
54. Premaratne, R.J., Lin, W.J., and Johnson, E.A. (1991) Development of an improved chemically defined minimal medium for Listeria monocytogenes. Appl Environ Microbiol 57: 3046-3048.
55. Ran, Y., Liu, M., Zhu, H., Nygaard, T.K., Brown, D.E., Fabian, M., etal. (2010) Spectroscopic identification of heme axial ligands in HtsA that are involved in heme acquisition by Streptococcus pyogenes. Biochemistry 49: 2834-2842.
56. Reeder, B.J. (2010) The redox activity of hemoglobins: from physiologic functions to pathologic mechanisms. Antioxid Redox Signal 13: 1087-1123.
57. Reniere, M.L., Torres, V.J., and Skaar, E.P. (2007) Intracellular metalloporphyrin metabolism in Staphylococcus aureus. Biometals 20: 333-345.
58. Robinson, S.R., Dang, T.N., Dringen, R., and Bishop, G.M. (2009) Hemin toxicity: a preventable source of brain damage following hemorrhagic stroke. Redox Rep 14: 228-235.
59. Roth, Z. (1961) [A graphic probit method for the calculation of LD50 and relative toxicity.] Cesk Fysiol 10: 408-422.
60. Schneider, R., and Hantke, K. (1993) Iron-hydroxamate uptake systems in Bacillus subtilis: identification of a lipoprotein as part of a binding protein-dependent transport system. Mol Microbiol 8: 111-121.
61. Schneider, S., and Paoli, M. (2005) Crystallization and preliminary X-ray diffraction analysis of the haem-binding protein HemS from Yersinia enterocolitica. Acta Crystallogr Sect F Struct Biol Cryst Commun 61: 802-805.
62. Scott, D.C., Cao, Z., Qi, Z., Bauler, M., Igo, J.D., Newton, S.M., and Klebba, P.E. (2001) Exchangeability of N termini in the ligand-gated porins of Escherichia coli. J Biol Chem 276: 13025-13033.
63. 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.
64. Sinclair, P.R., Gorman, N., and Jacobs, J.M. (1999) Current Protocols in Toxicology. San Francisco, CA: John Wiley and Sons.
65. Singh, A., Isaac, A.O., Luo, X., Mohan, M.L., Cohen, M.L., Chen, F., etal. (2009) Abnormal brain iron homeostasis in human and animal prion disorders. PLoS Pathog 5: e1000336.
66. Skaar, E.P., Humayun, M., Bae, T., DeBord, K.L., Schneewind, O., and Gaspar, A.H. (2004) Iron-source preference of Staphylococcus aureus infections. Science 305: 1626-1628.
67. Smith, K., and Youngman, P. (1992) Use of a new integrational vector to investigate compartment-specific expression of the Bacillus subtilis spoIIM gene. Biochimie 74: 705-711.
68. Stauff, D.L., and Skaar, E.P. (2009) The heme sensor system of Staphylococcus aureus. Contrib Microbiol 16: 120-135.
69. Stojiljkovic, I., and Hantke, K. (1994) Transport of haemin across the cytoplasmic membrane through a haemin-specific periplasmic binding-protein-dependent transport system in Yersinia enterocolitica. Mol Microbiol 13: 719-732.
70. Stork, M., Di Lorenzo, M., Mourino, S., Osorio, C.R., Lemos, M.L., and Crosa, J.H. (2004) Two tonB systems function in iron transport in Vibrio anguillarum, but only one is essential for virulence. Infect Immun 72: 7326-7329.
71. Tarlovsky, Y., Fabian, M., Solomaha, E., Honsa, E., Olson, J.S., and Maresso, A.W. (2010) A Bacillus anthracis S-layer homology protein that binds heme and mediates heme delivery to IsdC. J Bacteriol 192: 3503-3511.
72. 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.
73. Tidmarsh, G.F., Klebba, P.E., and Rosenberg, L.T. (1983) Rapid release of iron from ferritin by siderophores. J Inorg Biochem 18: 161-168.
74. Toledo-Arana, A., Dussurget, O., Nikitas, G., Sesto, N., Guet-Revillet, H., Balestrino, D., etal. (2009) The Listeria transcriptional landscape from saprophytism to virulence. Nature 459: 950-956.
75. Tong, Y., and Guo, M. (2007) Cloning and characterization of a novel periplasmic heme-transport protein from the human pathogen Pseudomonas aeruginosa. J Biol Inorg Chem 12: 735-750.
76. Touhami, A., Jericho, M.H., and Beveridge, T.J. (2004) Atomic force microscopy of cell growth and division in Staphylococcus aureus. J Bacteriol 186: 3286-3295.
77. Tsai, H.N., and Hodgson, D.A. (2003) Development of a synthetic minimal medium for Listeria monocytogenes. Appl Environ Microbiol 69: 6943-6945.
78. de Villiers, K.A., Kaschula, C.H., Egan, T.J., and Marques, H.M. (2007) Speciation and structure of ferriprotoporphyrin IX in aqueous solution: spectroscopic and diffusion measurements demonstrate dimerization, but not μ-oxo dimer formation. J Biol Inorg Chem 12: 101-117.
79. Wayne, R., Frick, K., and Neilands, J.B. (1976) Siderophore protection against colicins M, B, V, and Ia in Escherichia coli. J Bacteriol 126: 7-12.
80. Wyckoff, E.E., Schmitt, M., Wilks, A., and Payne, S.M. (2004) HutZ is required for efficient heme utilization in Vibrio cholerae. J Bacteriol 186: 4142-4151.
81. Zhao, S., Montanez, G.E., Kumar, P., Sannigrahi, S., and Tzeng, Y.L. (2010) Regulatory role of the MisR/S two-component system in hemoglobin utilization in Neisseria meningitidis. Infect Immun 78: 1109-1122.
82. Zhu, H., Xie, G., Liu, M., Olson, J.S., Fabian, M., Dooley, D.M., and Lei, B. (2008a) Pathway for heme uptake from human methemoglobin by the iron-regulated surface determinants system of Staphylococcus aureus. J Biol Chem 283: 18450-18460.
83. Zhu, H., Liu, M., and Lei, B. (2008b) The surface protein Shr of Streptococcus pyogenes binds heme and transfers it to the streptococcal heme-binding protein Shp. BMC Microbiol 8: 15.