IlsA, a unique surface protein of Bacillus cereus required for iron acquisition from heme, hemoglobin and ferritin

PLoS Pathogens

Volumn 5, Issue 11, 2009, Pages

  Daou, Nadine ^a,b   Buisson, Christophe ^a   Gohar, Michel ^a   Vidic, Jasmina ^c   Bierne, Hélène ^d   Kallassy, Mireille ^b   Lereclus, Didier ^a   Nielsen LeRoux, Christina ^a  

^a CEMAGREF   (France)

^b SAINT JOSEPH UNIVERSITY   (Lebanon)

^c INRA Institut National de la Recherche Agronomique   (France)

^d INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FERRITIN; HEME; HEMOGLOBIN; ILSA PROTEIN; IRON; LACTOFERRIN; MEMBRANE PROTEIN; TRANSFERRIN; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS CEREUS; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM CULTURE; CONTROLLED STUDY; HOST; IRON TRANSPORT; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; ANIMAL; CELL LINE; CHEMISTRY; GROWTH, DEVELOPMENT AND AGING; INSECT; METABOLISM; PATHOGENICITY;

BACILLUS CEREUS; HEXAPODA;

ANIMALS; BACILLUS CEREUS; BACTERIAL PROTEINS; CELL LINE; FERRITINS; HEME; HEMOGLOBINS; INSECTS; IRON; LACTOFERRIN; TRANSFERRIN;

EID: 73549101129     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000675     Document Type: Article

References (69)

1. Braun V (2001) Iron uptake mechanisms and their regulation in pathogenic bacteria. Int J Med Microbiol 291: 67-79.
2. Wandersman C, Delepelaire P (2004) Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58: 611-647.
3. Ratledge C, Dover LG (2000) Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54: 881-941.
4. Crosa JH, Walsh CT (2002) Genetics and assembly line enzymology of siderophore biosynthesis in bacteria. Microbiol Mol Biol Rev 66: 223-249.
5. Stojiljkovic I, Larson J, Hwa V, Anic S, So M (1996) HmbR outer membrane receptors of pathogenic Neisseria spp.: iron-regulated, hemoglobin-binding proteins with a high level of primary structure conservation. J Bacteriol 178: 4670-4678.
6. Lewis LA, Sung MH, Gipson M, Hartman K, Dyer DW (1998) Transport of intact porphyrin by HpuAB, the hemoglobin-haptoglobin utilization system of Neisseria meningitidis. J Bacteriol 180: 6043-6047.
7. Wandersman C, Stojiljkovic I (2000) Bacterial heme sources: the role of heme, hemoprotein receptors and hemophores. Curr Opin Microbiol 3: 215-220.
8. Genco CA, Dixon DW (2001) Emerging strategies in microbial haem capture. Mol Microbiol 39: 1-11.
9. Mazmanian SK, Ton-That H, Su K, 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.
10. Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P, et al. (2003) Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299: 906-909.
11. 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.
12. Grigg JC, Vermeiren CL, Heinrichs DE, Murphy ME (2007) Haem recognition by a Staphylococcus aureus NEAT domain. Mol Microbiol 63: 139-149.
13. Maresso AW, Garufi G, Schneewind O (2008) Bacillus anthracis secretes proteins that mediate heme acquisition from hemoglobin. PLoS Pathog 4: e1000132. doi:10.1371/journal.ppat.1000132.
14. Gat O, Zaide G, Inbar I, Grosfeld H, Chitlaru T, et al. (2008) Characterization of Bacillus anthracis iron-regulated surface determinant (Isd) proteins containing NEAT domains. Mol Microbiol 70: 983-999.
15. Helgason E, Okstad OA, Caugant DA, Johansen HA, Fouet A, et al. (2000) Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis-one species on the basis of genetic evidence. Appl Environ Microbiol 66: 2627-2630.
16. Kolsto AB, Lereclus D, Mock M (2002) Genome structure and evolution of the Bacillus cereus group. Curr Top Microbiol Immunol 264: 95-108.
17. Vilas-Boas GT, Peruca AP, Arantes OM (2007) Biology and taxonomy of Bacillus cereus, Bacillus anthracis, and Bacillus thuringiensis. Can J Microbiol 53: 673-687.
18. Stenfors Arnesen LP, Fagerlund A, Granum PE (2008) From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol Rev 32: 579-606.
19. Miller JM, Hair JG, Hebert M, Hebert L, Roberts FJ Jr, et al. (1997) Fulminating bacteremia and pneumonia due to Bacillus cereus. J Clin Microbiol 35: 504-507.
20. Callegan MC, Booth MC, Jett BD, Gilmore MS (1999) Pathogenesis of gram-positive bacterial endophthalmitis. Infect Immun 67: 3348-3356.
21. Hilliard NJ, Schelonka RL, Waites KB (2003) Bacillus cereus bacteremia in a preterm neonate. J Clin Microbiol 41: 3441-3444.
22. Hoffmaster AR, Ravel J, Rasko DA, Chapman GD, Chute MD, et al. (2004) Identification of anthrax toxin genes in a Bacillus cereus associated with an illness resembling inhalation anthrax. Proc Natl Acad Sci U S A 101: 8449-8454.
23. Slamti L, Lereclus D (2002) A cell-cell signaling peptide activates the PlcR virulence regulon in bacteria of the Bacillus cereus group. EMBO J 21: 4550-4559.
24. Gohar M, Faegri K, Perchat S, Ravnum S, Okstad OA, et al. (2008) The PlcR virulence regulon of Bacillus cereus. PLoS ONE 3: e2793. doi:10.1371/journal. pone.0002793.
25. Salamitou S, Ramisse F, Brehelin M, Bourguet D, Gilois N, et al. (2000) The plcR regulon is involved in the opportunistic properties of Bacillus thuringiensis and Bacillus cereus in mice and insects. Microbiology 146 (Pt 11): 2825-2832.
26. 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.
27. Zawadzka AM, Abergel RJ, Nichiporuk R, Andersen UN, Raymond KN (2009) Siderophore-mediated iron acquisition systems in Bacillus cereus: Identification of receptors for anthrax virulence-associated petrobactin. Biochemistry 48: 3645-3657.
28. Sato N, Kurotaki H, Watanabe T, Mikami T, Matsumoto T (1998) Use of hemoglobin as an iron source by Bacillus cereus. Biol Pharm Bull 21: 311-314.
29. Park RY, Choi MH, Sun HY, Shin SH (2005) Production of catecholsiderophore and utilization of transferrin-bound iron in Bacillus cereus. Biol Pharm Bull 28: 1132-1135.
30. Sato N, Ikeda S, Mikami T, Matsumoto T (1999) Bacillus cereus dissociates hemoglobin and uses released heme as an iron source. Biol Pharm Bull 22: 1118-1121.
31. Sato N, Kurotaki H, Ikeda S, Daio R, Nishinome N, et al. (1999) Lactoferrin inhibits Bacillus cereus growth and heme analogs recover its growth. Biol Pharm Bull 22: 197-199.
32. 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.
33. Dower WJ, Miller JF, Ragsdale CW (1988) High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res 16: 6127-6145.
34. Lereclus D, Arantes O, Chaufaux J, Lecadet M (1989) Transformation and expression of a cloned delta-endotoxin gene in Bacillus thuringiensis. FEMS Microbiol Lett 51: 211-217.
35. Arantes O, Lereclus D (1991) Construction of cloning vectors for Bacillus thuringiensis. Gene 108: 115-119.
36. Vargas C, McEwan AG, Downie JA (1993) Detection of c-type cytochromes using enhanced chemiluminescence. Anal Biochem 209: 323-326.
37. Fortinea N, Trieu-Cuot P, Gaillot O, Pellegrini E, Berche P, et al. (2000) Optimization of green fluorescent protein expression vectors for in vitro and in vivo detection of Listeria monocytogenes. Res Microbiol 151: 353-360.
38. Fedhila S, Nel P, Lereclus D (2002) The InhA2 metalloprotease of Bacillus thuringiensis strain 407 is required for pathogenicity in insects infected via the oral route. J Bacteriol 184: 3296-3304.
39. Guerout-Fleury AM, Shazand K, Frandsen N, Stragier P (1995) Antibioticresistance cassettes for Bacillus subtilis. Gene 167: 335-336.
40. Bouillaut L, Ramarao N, Buisson C, Gilois N, Gohar M, et al. (2005) FlhA influences Bacillus thuringiensis PlcR-regulated gene transcription, protein production, and virulence. Appl Environ Microbiol 71: 8903-8910.
41. Finney DJ (1971) Probit Analysis. London: Cambridge University Press.
42. Raymond M, Prato G, Ratsira D (1993) PROBIT analysis of mortality assays displaying quantal response. Saint Georges d'Orgue, France: PRAXEME.
43. Locke MN, H (1992) Iron economy in insects: transport, metabolism, and storage. Annu Rev Entomol 37: 195-215.
44. Yuk JE, Seo DH, Choi CW, HAN J, Choi HK, PARK JB, Hwang SY, Koh SK, Yun CY (2005) Characterization of Tissue-Ferritin Purified from Wax Moth. Entomol Reaserch 35: 227-234.
45. Dunphy GB, Niven DF, Chadwick JS (2002) Iron contributes to the antibacterial functions of the haemolymph of Galleria mellonella. J Insect Physiol 48: 903-914.
46. Bullen JJ, Rogers HJ, Spalding PB, Ward CG (2006) Natural resistance, iron and infection: a challenge for clinical medicine. J Med Microbiol 55: 251-258.
47. You SA, Wang Q (2005) Ferritin in atherosclerosis. Clin Chim Acta 357: 1-16.
48. Kim BS, Lee CS, Yun CY, Yeo SM, Park WM, et al. (2001) Characterization and immunological analysis of ferritin from the hemolymph of Galleria mellonella. Comp Biochem Physiol A Mol Integr Physiol 129: 501-509.
49. Valenti P, Antonini G (2005) Lactoferrin: an important host defence against microbial and viral attack. Cell Mol Life Sci 62: 2576-2587.
50. Lindback T, Okstad OA, Rishovd AL, Kolsto AB (1999) Insertional inactivation of hblC encoding the L2 component of Bacillus cereus ATCC 14579 haemolysin BL strongly reduces enterotoxigenic activity, but not the haemolytic activity against human erythrocytes. Microbiology 145 (Pt 11): 3139-3146.
51. Andreeva ZI, Nesterenko VF, Yurkov IS, Budarina ZI, Sineva EV, et al. (2006) Purification and cytotoxic properties of Bacillus cereus hemolysin II. Protein Expr Purif 47: 186-193.
52. Fagerlund A, Lindback T, Storset AK, Granum PE, Hardy SP (2008) Bacillus cereus Nhe is a pore-forming toxin with structural and functional properties similar to the ClyA (HlyE, SheA) family of haemolysins, able to induce osmotic lysis in epithelia. Microbiology 154: 693-704.
53. Agaisse H, Gominet M, Okstad OA, Kolsto AB, Lereclus D (1999) PlcR is a pleiotropic regulator of extracellular virulence factor gene expression in Bacillus thuringiensis. Mol Microbiol 32: 1043-1053.
54. Taylor JM, Heinrichs DE (2002) Transferrin binding in Staphylococcus aureus: involvement of a cell wall-anchored protein. Mol Microbiol 43: 1603-1614.
55. Clarke SR, Wiltshire MD, Foster SJ (2004) IsdA of Staphylococcus aureus is a broad spectrum, iron-regulated adhesin. Mol Microbiol 51: 1509-1519.
56. Kobe B, Kajava AV (2001) The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 11: 725-732.
57. Bierne H, Sabet C, Personnic N, Cossart P (2007) Internalins: a complex family of leucine-rich repeat-containing proteins in Listeria monocytogenes. Microbes Infect 9: 1156-1166.
58. Almeida RS, Brunke S, Albrecht A, Thewes S, Laue M, et al. (2008) the hyphal-associated adhesin and invasin Als3 of Candida albicans mediates iron acquisition from host ferritin. PLoS Pathog 4: e1000217. doi:10.1371/journal. ppat.1000217.
59. Navarre WW, Schneewind O (1999) Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63: 174-229.
60. Kern JW, Schneewind O (2008) BslA, a pXO1-encoded adhesin of Bacillus anthracis. Mol Microbiol 68: 504-515.
61. 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.
62. Maresso AW, Schneewind O (2006) Iron acquisition and transport in Staphylococcus aureus. Biometals 19: 193-203.
63. Muryoi N, Tiedemann MT, Pluym M, Cheung J, Heinrichs DE, et al. (2008) Demonstration of the iron-regulated surface determinant (Isd) heme transfer pathway in Staphylococcus aureus. J Biol Chem 283: 28125-28136.
64. Deneer HG, Healey V, Boychuk I (1995) Reduction of exogenous ferric iron by a surface-associated ferric reductase of Listeria spp. Microbiology 141 (Pt 8): 1985-1992.
65. Whitby PW, Vanwagoner TM, Springer JM, Morton DJ, Seale TW, et al. (2006) Burkholderia cenocepacia utilizes ferritin as an iron source. J Med Microbiol 55: 661-668.
66. Vierstraete E, Verleyen P, Baggerman G, D'Hertog W, Van den Bergh G, et al. (2004) A proteomic approach for the analysis of instantly released wound and immune proteins in Drosophila melanogaster hemolymph. Proc Natl Acad Sci U S A 101: 470-475.
67. Larson JA, Howie HL, So M (2004) Neisseria meningitidis accelerates ferritin degradation in host epithelial cells to yield an essential iron source. Mol Microbiol 53: 807-820.
68. Fouet A, Mesnage S (2002) Bacillus anthracis cell envelope components. Curr Top Microbiol Immunol 271: 87-113.
69. Jensen GB, Hansen BM, Eilenberg J, Mahillon J (2003) The hidden lifestyles of Bacillus cereus and relatives. Environ Microbiol 5: 631-640.