Bacillus anthracis secretes proteins that mediate heme acquisition from hemoglobin

PLoS Pathogens

Volumn 4, Issue 8, 2008, Pages

  Maresso, Anthony W ^a   Garufi, Gabriella ^a   Schneewind, Olaf ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HEME; HEMOGLOBIN; IRON; ISDX1 PROTEIN; ISDX2 PROTEIN; UNCLASSIFIED DRUG; IRON BINDING PROTEIN;

ARTICLE; BACILLUS ANTHRACIS; BACTERIAL GROWTH; BACTERIAL MEMBRANE; CELL WALL; CONTROLLED STUDY; GRAM POSITIVE BACTERIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN SECRETION; HUMAN; METABOLISM; MOLECULAR EVOLUTION; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SECRETION; TRANSPORT AT THE CELLULAR LEVEL;

BACILLUS ANTHRACIS; BACTERIA (MICROORGANISMS); POSIBACTERIA; VERTEBRATA;

BACILLUS ANTHRACIS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; EVOLUTION, MOLECULAR; HEMOGLOBINS; HUMANS; IRON; IRON-BINDING PROTEINS; PROTEIN STRUCTURE, TERTIARY;

EID: 50849124753     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000132     Document Type: Article

References (74)

1. Koch R (1876) Die Ätiologie der Milzbrand-Krankheit, begründet auf die Entwicklungsgeschichte des Bacillus anthracis. Beiträge zur Biologie der Pflanzen 2: 277-310.
2. Dixon TC, Meselson M, Guillemin J, Hanna PC (1999) Anthrax. N Engl J Med 341: 815-826.
3. Mock M, Fouet A (2001) Anthrax. Annu Rev Microbiol 55: 647-671.
4. Guidi-Rontani C, Levy M, Ohayon H, Mock M (2001) Fate of germinated Bacillus anthracis spores in primary murine macrophages. Mol Microbiol 42: 931-938.
5. Dixon TC, Fadl AA, Koehler TM, Swanson JA, Hanna PC (2000) Early Bacillus anthracis-macrophage interactions: intracellular survival survival and escape. Cell Microbiol 2: 453-463.
6. Candela T, Fouet A (2006) Poly-γ-glutamate in bacteria. Mol Microbiol 60: 1091-1098.
7. Friedlander AM (2001) Tackling anthrax. Nature 414: 160-161.
8. Collier RJ, Young JA (2003) Anthrax toxin. Annu Rev Cell Dev Biol 19: 45-70.
9. Drysdale M, Heninger S, Hutt J, Chen Y, Lyons CR, et al. (2005) Capsule synthesis by Bacillus anthracis is required for dissemination in murine inhalation anthrax. Embo J 24: 221-227.
10. Candela T, Fouet A (2005) Bacillus anthracis CapD, belonging to the γ-glutamyltranspeptidase family, is required for the covalent anchoring of capsule to peptidoglycan. Mol Microbiol 57: 717-726.
11. Mesnage S, Fontaine T, Mignot T, Delepierre M, Mock M, et al. (2000) Bacterial SLH domain proteins are non-covalently anchored to the cell surface via a conserved mechanism involving wall polysaccharide pyruvylation. Embo J 19: 4473-4484.
12. Fouet A, Mesnage S (2002) Bacillus anthracis cell envelope components. Curr Top Microbiol Immunol 271: 87-113.
13. Navarre WW, Schneewind O (1999) Surface proteins of Gram-positive bacteria and the mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63: 174-229.
14. Maresso AW, Schneewind O (2006) Iron acquisition and transport in Staphylococcus aureus. Biometals 19: 193-203.
15. Mazmanian SK, Skaar EP, Gasper AH, Humayun M, Gornicki P, et al. (2003) Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299: 906-909.
16. Torres VJ, Pishchany G, Humayun M, Schneewind O, Skaar EP (2006) Staphylococcus aureus IsdB is a hemoglobin receptor required for heme iron utilization. J Bacteriol 188: 8421-8429.
17. Skaar EP, Gaspar AH, Schneewind O (2004) IsdG and IsdI, heme degrading enzymes in the cytoplasm of Staphylococcus aureus. J Biol Chem 279: 436-443.
18. Skaar EP, Schneewind O (2004) Iron-regulated surface determinants (Isd) of Staphylococcus aureus: stealing iron from heme. Microbes Infect 6: 390-397.
19. 3+ siderophore transporter from Gram-positive pathogenic bacteria. Genome Biol 3: RESEARCH0047.
20. Grigg JC, Vermeiren CL, Heinrichs DE, Murphy ME (2007) Haem recognition by a Staphylococcus aureus NEAT domain. Mol Microbiol 63: 139-149.
21. Vermeiren CL, Pluym M, Mack J, Heinrichs DE, Stillman MJ (2006) Characterization of the heme binding properties of Staphylococcus aureus IsdA. Biochemistry 45: 12867-12875.
22. Mazmanian SK, Ton-That H, Su K, Schneewind O (2002) An iron-regulated sortase enzyme anchors a class of surface protein during Staphylococcus aureus pathogenesis. Proc Natl Acad Sci USA 99: 2293-2298.
23. Marraffini LA, Schneewind O (2005) Anchor structure of staphylococcal surface proteins. V. Anchor structure of the sortase B substrate IsdC. J Biol Chem 280: 16263-16271.
24. Skaar EP, Gaspar AH, Schneewind O (2006) Bacillus anthracis IsdG, a heme-degrading monooxygenase. J Bacteriol 188: 1071-1080.
25. Maresso AW, Chapa TJ, Schneewind O (2006) Surface protein IsdC and sortase B are required for heme-iron scavenging of Bacillus anthracis. J Bacteriol 188: 8145-8152.
26. Marraffini LA, Schneewind O (2006) Targeting proteins to the cell wall of sporulating Bacillus anthracis. Mol Microbiol 62: 1402-1417.
27. Izadi N, Henry Y, Haladjian J, Goldberg ME, Wandersman C, et al. (1997) Purification and characterization of an extracellular heme-binding protein, HasA, involved in heme iron acquisition. Biochemistry 36: 7050-7057.
28. Nienhaus K, Nienhaus GU (2005) Probing heme protein-ligand interactions by UV/visible absorption spectroscopy. Methods Mol Biol 305: 215-242.
29. Wandersman C, Stojiljkovic I (2000) Bacterial heme sources: the role of heme, hemoprotein receptors and hemophores. Curr Opin Microbiol 3: 215-220.
30. Wandersman C, Delepelaire P (2004) Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58: 611-647.
31. Cescau S, Cwerman H, Letoffe S, Delepelaire P, Wandersman C, et al. (2007) Heme acquisition by hemophores. Biometals 20: 603-613.
32. Letoffe S, Ghigo JM, Wandersman C (1994) Secretion of the Serratia marcescens HasA protein by an ABC transporter. J Bacteriol 176: 5372-5377.
33. Letoffe S, Ghigo JM, Wandersman C (1994) Iron acquisition from heme and hemoglobin by a Serratia marcescens extracellular protein. Proc Natl Acad Sci USA 91: 9876-9880.
34. Izadi-Pruneyre N, Huche F, Lukat-Rodgers GS, Lecroisey A, Gilli R, et al. (2006) The heme transfer from the soluble HasA hemophore to its membrane-bound receptor HasR is driven by protein-protein interaction from a high to a lower affinity binding site. J Biol Chem 281: 25541-25550.
35. Hargrove MS, Barrick D, Olson JS (1996) The association rate constant for heme binding to globin is independent of protein structure. Biochemistry 35: 11293-11299.
36. Genco CA, Dixon DW (2001) Emerging strategies in microbial haem capture. Mol Microbiol 39: 1-11.
37. Morton TA, Myszka DG (1998) Kinetic analysis of macromolecular interactions using surface plasmon resonance biosensors. Methods Enzymol 295: 268-294.
38. Myszka DG (2000) Kinetic, equilibrium, and thermodynamic analysis of macromolecular interactions with BIACORE. Methods Enzymol 323: 325-340.
39. Ordway GA, Garry DJ (2004) Myoglobin: an essential hemoprotein in striated muscle. J Exp Biol 207: 3441-3446.
40. Cendrowski S, MacArthur W, Hanna P (2004) Bacillus anthracis requires siderophore biosynthesis for growth in macrophages and mouse virulence. Mol Microbiol 51: 407-417.
41. Crosa JH, Mey AR, Payne SM (2004) Iron Transport in Bacteria. Washington, D.C.: American Society of Microbiology Press.
42. Wittenberg JB, Wittenberg BA (1990) Mechanisms of cytoplasmic hemoglobin and myoglobin function. Annu Rev Biophys Biophys Chem 19: 217-241.
43. Fischbach MA, Lin H, Liu DR, Walsh CT (2006) How pathogenic bacteria evade mammalian sabotage in the battle for iron. Nat Chem Biol 2: 132-138.
44. Goetz DH, Holmes MA, Borregaard N, Bluhm ME, Raymond KN, et al. (2002) The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol Cell 10: 1033-1043.
45. Koppisch AT, Browder CC, Moe AL, Shelley JT, Kinkel BA, et al. (2005) Petrobactin is the primary siderophore synthesized by Bacillus anthracis str. Sterne under conditions of iron starvation. Biometals 18: 577-585.
46. Wilson MK, Abergel RJ, Raymond KN, Arceneaux JE, Byers BR (2006) Siderophores of Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis. Biochem Biophys Res Commun 348: 320-325.
47. Lee JY, Janes BK, Passalacqua KD, Pfleger BF, Bergman NH, et al. (2007) Biosynthetic analysis of the petrobactin siderophore pathway from Bacillus anthracis. J Bacteriol 189: 1698-1710.
48. Pfleger BF, Lee JY, Somu RV, Aldrich CC, Hanna PC, et al. (2007) Characterization and analysis of early enzymes for petrobactin biosynthesis in Bacillus anthracis. Biochemistry 46: 4147-4157.
49. Abergel RJ, Wilson MK, Arceneaux JE, Hoette TM, Strong RK, et al. (2006) Anthrax pathogen evades the mammalian immune system through stealth siderophore production. Proc Natl Acad Sci USA 103: 18499-18503.
50. Mesnage S, Tosi-Couture E, Mock M, Gounon P, Fouet A (1997) Molecular characterization of the Bacillus anthracis main S-layer component: evidence that it is the major cell-assoiated antigen. Mol Microbiol 23: 1147-1155.
51. Mignot T, Mesnage S, Couture-Tosi E, Mock M, Fouet A (2002) Developmental switch of S-layer protein synthesis in Bacillus anthracis. Mol Microbiol 43: 1615-1627.
52. Pluym M, Muryoi N, Heinrichs DE, Stillman MJ (2008) Heme binding in the NEAT domains of IsdA and IsdC of Staphylococcus aureus. J Inorg Biochem 102: 480-488.
53. Sharp KH, Schneider S, Cockayne A, 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.
54. Gaspar AH, Marraffini LA, Glass EM, Debord KL, Ton-That H, et al. (2005) Bacillus anthracis Sortase A (SrtA) Anchors LPXTG Motif-Containing Surface Proteins to the Cell Wall Envelope. J Bacteriol 187: 4646-4655.
55. Fedhila S, Daou N, Lereclus D, Nielsen-LeRoux C (2006) Identification of Bacillus cereus internalin and other candidate virulence genes specifically induced during oral infection in insects. Mol Microbiol 62: 339-355.
56. Kern JW, Schneewind O (2008) BslA, a pXO1-encoded adhesin of Bacillus anthracis. Mol Microbiol 68: 504-515.
57. Delepelaire P (2004) Type I secretion in gram-negative bacteria. Biochim Biophys Acta 1694: 149-161.
58. Delepelaire P, Wandersman C (1998) The SecB chaperone is involved in the secretion of the Serratia marcescens HasA protein through an ABC transporter. Embo J 17: 936-944.
59. Deniau C, Gilli R, Izadi-Pruneyre N, Letoffe S, Delepierre M, et al. (2003) Thermodynamics of heme binding to the HasA(SM) hemophore: effect of mutations at three key residues for heme uptake. Biochemistry 42: 10627-10633.
60. Letoffe S, Nato F, Goldberg ME, Wandersman C (1999) Interactions of HasA, a bacterial haemophore, with haemoglobin and with its outer membrane receptor HasR. Mol Microbiol 33: 546-555.
61. Letoffe S, Deniau C, Wolff N, Dassa E, Delepelaire P, et al. (2001) Haemophore-mediated bacterial haem transport: evidence for a common or overlapping site for haem-free and haem-loaded haemophore on its specific outer membrane receptor. Mol Microbiol 41: 439-450.
62. Stojiljkovic I, 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.
63. Rossi MS, Paquelin A, Ghigo JM, Wandersman C (2003) Haemophore-mediated signal transduction across the bacterial cell envelope in Serratia marcescens: the inducer and the transported substrate are different molecules. Mol Microbiol 48: 1467-1480.
64. Biville F, Cwerman H, Letoffe S, Rossi MS, Drouet V, et al. (2004) Haemophore-mediated signalling in Serratia marcescens: a new mode of regulation for an extra cytoplasmic function (ECF) sigma factor involved in haem acquisition. Mol Microbiol 53: 1267-1277.
65. Hanson MS, Pelzel SE, Latimer J, Muller-Eberhard U, Hansen EJ (1992) Identification of a genetic locus of Haemophilus influenzae type b necessary for the binding and utilization of heme bound to human hemopexin. Proc Natl Acad Sci USA 89: 1973-1977.
66. Rossi MS, Fetherston JD, Letoffe S, Carniel E, Perry RD, et al. (2001) Identification and characterization of the hemophore-dependent heme acquisition system of Yersinia pestis. Infect Immun 69: 6707-6717.
67. Letoffe S, Redeker V, Wandersman C (1998) Isolation and characterization of an extracellular haem-binding protein from Pseudomonas aeruginosa that shares function and sequence similarities with the Serratia marcescens HasA haemophore. Mol Microbiol 28: 1223-1234.
68. Letoffe S, Omori K, Wandersman C (2000) Functional characterization of the HasA(PF) hemophore and its truncated and chimeric variants: determination of a region involved in binding to the hemophore receptor. J Bacteriol 182: 4401-4405.
69. Debarbieux L, Wandersman C (2004) Hemophore-dependent heme acquisition systems. In: Crosa JH, Mey AR, Payne SM, eds. Iron transport in bacteria. Washington, D.C.: ASM Press. pp 38-47.
70. Pilpa RM, Fadeev EA, Villareal VA, Wong ML, Phillips M, et al. (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.
71. Arnoux P, Haser R, Izadi N, Lecroisey A, Delepierre M, et al. (1999) The crystal structure of HasA, a hemophore secreted by Serratia marcescens. Nat Struct Biol 6: 516-520.
72. Sterne M (1937) Avirulent anthrax vaccine. Onderstepoort J Vet Sci Animal Ind 21: 41-43.
73. Schurter W, Geiser M, Mathe D (1989) Efficient transformation of Bacillus thuringiensis and B. cereus via electroporation: transformation of acrystalliferous strains with a cloned delta-endotoxin gene. Mol Gen Genet 218: 177-181.
74. Johnsson B, Lofas S, Lindquist G (1991) Immobilization of proteins to a carboxymethyldextran-modified gold surface for biospecific interaction analysis in surface plasmon resonance sensors. Anal Biochem 198: 268-277.