The lipoprotein components of the Isd and Hts transport systems are dispensable for acquisition of heme by Staphylococcus aureus

FEMS Microbiology Letters

Volumn 329, Issue 2, 2012, Pages 177-185

  Wright, John A ^a,b   Nair, Sean P ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Heme transport; Hemoglobin; Iron acquisition; Small colony variant

Indexed keywords

HEME; HEMOGLOBIN; IRON; LIPOPROTEIN; PERMEASE;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; CONTROLLED STUDY; ENZYME ACTIVITY; GENE DELETION; GENETIC VARIABILITY; HEMB GENE; HEME SYNTHESIS; HEME TRANSPORT SYSTEM; HTSA GENE; IRON REGULATED SURFACE DETERMINANT SYSTEM; ISDE GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; STAPHYLOCOCCUS AUREUS;

BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT, ACTIVE; CARRIER PROTEINS; CULTURE MEDIA; ESCHERICHIA COLI; GENE DELETION; HEME; HUMANS; LIPOPROTEINS; MUTATION; PHENOTYPE; PORPHOBILINOGEN SYNTHASE; STAPHYLOCOCCUS AUREUS;

STAPHYLOCOCCUS AUREUS; STRAWBERRY CRINKLE VIRUS;

EID: 84858699069     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/j.1574-6968.2012.02519.x     Document Type: Article

References (49)

1. Bae T & Schneewind O (2006) Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid 55: 58-63.
2. Bates DM, von Eiff C, McNamara PJ, Peters G, Yeaman MR, Bayer AS & Proctor RA (2003) Staphylococcus aureus menD and hemB mutants are as infective as the parent strains, but the menadione biosynthetic mutant persists within the kidney. J Infect Dis 187: 1654-1661.
3. Baumert N, von Eiff C, Schaaff F, Peters G, Proctor RA & Sahl HG (2002) Physiology and antibiotic susceptibility of Staphylococcus aureus small colony variants. Microb Drug Resist 8: 253-260.
4. Beasley FC, Vines ED, Grigg JC, Zheng Q, Liu S, Lajoie GA, Murphy ME & Heinrichs DE (2009) Characterization of staphyloferrin A biosynthetic and transport mutants in Staphylococcus aureus. Mol Microbiol 72: 947-963.
5. Beutler E & Waalen J (2006) The definition of anemia: what is the lower limit of normal of the blood hemoglobin concentration? Blood 107: 1747-1750.
6. Clarke SR & Foster SJ (2008) IsdA protects Staphylococcus aureus against the bactericidal protease activity of apolactoferrin. Infect Immun 76: 1518-1526.
7. Clarke SR, Wiltshire MD & Foster SJ (2004) IsdA of Staphylococcus aureus is a broad spectrum, iron-regulated adhesin. Mol Microbiol 51: 1509-1519.
8. Clarke SR, Mohamed R, Bian L, Routh AF, Kokai-Kun JF, Mond JJ, Tarkowski A & Foster SJ (2007) The Staphylococcus aureus surface protein IsdA mediates resistance to innate defenses of human skin. Cell Host Microbe 1: 199-212.
9. Clarke SR, Andre G, Walsh EJ, Dufrene YF, Foster TJ & Foster SJ (2009) Iron-regulated surface determinant protein A mediates adhesion of Staphylococcus aureus to human corneocyte envelope proteins. Infect Immun 77: 2408-2416.
10. Dinges MM, Orwin PM & Schlievert PM (2000) Exotoxins of Staphylococcus aureus. Clin Microbiol Rev 13: 16-34, table.
11. Dryla A, Gelbmann D, von Gabain A & Nagy E (2003) Identification of a novel iron regulated staphylococcal surface protein with haptoglobin-haemoglobin binding activity. Mol Microbiol 49: 37-53.
12. Gaskill ME & Khan SA (1988) Regulation of the enterotoxin B gene in Staphylococcus aureus. J Biol Chem 263: 6276-6280.
13. Gao W, Chua K, Davies JK et al. (2010) Two novel point mutations in clinical Staphylococcus aureus reduce linezolid susceptibility and switch on the stringent response to promote persistent infection. PLoS Pathog 6: e1000944.
14. Gomez-Gonzalez C, Acosta J, Villa J, Barrado L, Sanz F, Orellana MA, Otero JR & Chaves F (2010) Clinical and molecular characteristics of infections with CO2-dependent small-colony variants of Staphylococcus aureus. J Clin Microbiol 48: 2878-2884.
15. Grigg JC, Vermeiren CL, Heinrichs DE & Murphy ME (2007) Heme coordination by Staphylococcus aureus IsdE. J Biol Chem 282: 28815-28822.
16. Grigg JC, Cooper JD, Cheung J, Heinrichs DE & Murphy ME (2010) The Staphylococcus aureus siderophore receptor HtsA undergoes localized conformational changes to enclose staphyloferrin A in an arginine-rich binding pocket. J Biol Chem 285: 11162-11171.
17. Hammer ND & Skaar EP (2011) Molecular mechanisms of Staphylococcus aureus iron acquisition. Annu Rev Microbiol 65: 129-147.
18. Hartley JL, Temple GF & Brasch MA (2000) DNA cloning using in vitro site-specific recombination. Genome Res 10: 1788-1795.
19. Jonsson IM, von Eiff C, Proctor RA, Peters G, Ryden C & Tarkowski A (2003) Virulence of a hemB mutant displaying the phenotype of a Staphylococcus aureus small colony variant in a murine model of septic arthritis. Microb Pathog 34: 73-79.
20. Kafala B & Sasarman A (1994) Cloning and sequence analysis of the hemB gene of Staphylococcus aureus. Can J Microbiol 40: 651-657.
21. Kahl BC, Duebbers A, Lubritz G et al. (2003) Population dynamics of persistent Staphylococcus aureus isolated from the airways of cystic fibrosis patients during a 6-year prospective study. J Clin Microbiol 41: 4424-4427.
22. Kohler C, von Eiff C, Peters G, Proctor RA, Hecker M & Engelmann S (2003) Physiological characterization of a heme-deficient mutant of Staphylococcus aureus by a proteomic approach. J Bacteriol 185: 6928-6937.
23. Kreiswirth BN, Lofdahl S, Betley MJ, O'Reilly M, Schlievert PM, Bergdoll MS & Novick RP (1983) The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305: 709-712.
24. Krishna KK, Jacques DA, Pishchany G et al. (2011) The structural basis for hemoglobin capture by the Staphylococcus aureus cell-surface protein, IsdH. J Biol Chem 286: 38439-38447.
25. Mason WJ & Skaar EP (2009) Assessing the contribution of heme-iron acquisition to Staphylococcus aureus pneumonia using computed tomography. PLoS ONE 4: e6668.
26. Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P, Jelenska J, Joachmiak A, Missiakas DM & Schneewind O (2003) Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299: 906-909.
27. Miajlovic H, Zapotoczna M, Geoghegan JA, Kerrigan SW, Speziale P & Foster TJ (2010) Direct interaction of iron-regulated surface determinant IsdB of Staphylococcus aureus with the GPIIb/IIIa receptor on platelets. Microbiology 156: 920-928.
28. Muryoi N, Tiedemann MT, Pluym M, Cheung J, Heinrichs DE & Stillman MJ (2008) Demonstration of the iron-regulated surface determinant (Isd) heme transfer pathway in Staphylococcus aureus. J Biol Chem 283: 28125-28136.
29. Nguyen HD, Nguyen QA, Ferreira RC, Ferreira LC, Tran LT & Schumann W (2005) Construction of plasmid-based expression vectors for Bacillus subtilis exhibiting full structural stability. Plasmid 54: 241-248.
30. Oskouian B & Stewart GC (1990) Repression and catabolite repression of the lactose operon of Staphylococcus aureus. J Bacteriol 172: 3804-3812.
31. Proctor RA, van LP, Kristjansson M, Maslow JN & Arbeit RD (1995) Persistent and relapsing infections associated with small-colony variants of Staphylococcus aureus. Clin Infect Dis 20: 95-102.
32. Proctor RA, von Eiff C, Kahl BC, Becker K, McNamara P, Herrmann M & Peters G (2006) Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat Rev Microbiol 4: 295-305.
33. Raleigh EA, Murray NE, Revel H, Blumenthal RM, Westaway D, Reith AD, Rigby PW, Elhai J & Hanahan D (1988) McrA and McrB restriction phenotypes of some E. coli strains and implications for gene cloning. Nucleic Acids Res 16: 1563-1575.
34. Rouault TA (2004) Microbiology Pathogenic bacteria prefer heme. Science 305: 1577-1578.
35. Sassa S (2004) Why heme needs to be degraded to iron, biliverdin IXalpha, and carbon monoxide? Antioxid Redox Signal 6: 819-824.
36. Seggewiss J, Becker K, Kotte O et al. (2006) Reporter metabolite analysis of transcriptional profiles of a Staphylococcus aureus strain with normal phenotype and its isogenic hemB mutant displaying the small-colony-variant phenotype. J Bacteriol 188: 7765-7777.
37. Seifert H, Wisplinghoff H, Schnabel P & von Eiff C (2003) Small colony variants of Staphylococcus aureus and pacemaker-related infection. Emerg Infect Dis 9: 1316-1318.
38. Sendi P & Proctor RA (2009) Staphylococcus aureus as an intracellular pathogen: the role of small colony variants. Trends Microbiol 17: 54-58.
39. Skaar EP, Humayun M, Bae T, DeBord KL & Schneewind O (2004) Iron-source preference of Staphylococcus aureus infections. Science 305: 1626-1628.
40. Spanu T, Romano L, D'Inzeo T, Masucci L, Albanese A, Papacci F, Marchese E, Sanguinetti M & Fadda G (2005) Recurrent ventriculoperitoneal shunt infection caused by small-colony variants of Staphylococcus aureus. Clin Infect Dis 41: e48-e52.
41. 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.
42. Tsuji BT, von Eiff C, Kelchlin PA, Forrest A & Smith PF (2008) Attenuated vancomycin bactericidal activity against Staphylococcus aureus hemB mutants expressing the small-colony-variant phenotype. Antimicrob Agents Chemother 52: 1533-1537.
43. Vaudaux P, Francois P, Bisognano C, Kelley WL, Lew DP, Schrenzel J, Proctor RA, McNamara PJ, Peters G & von Eiff C (2002) Increased expression of clumping factor and fibronectin-binding proteins by hemB mutants of Staphylococcus aureus expressing small colony variant phenotypes. Infect Immun 70: 5428-5437.
44. von Eiff C, Bettin D, Proctor RA, Rolauffs B, Lindner N, Winkelmann W & Peters G (1997a) Recovery of small colony variants of Staphylococcus aureus following gentamicin bead placement for osteomyelitis. Clin Infect Dis 25: 1250-1251.
45. von Eiff C, Heilmann C, Proctor RA, Woltz C, Peters G & Gotz F (1997b) A site-directed Staphylococcus aureus hemB mutant is a small-colony variant which persists intracellularly. J Bacteriol 179: 4706-4712.
46. von Eiff C, McNamara P, Becker K, Bates D, Lei XH, Ziman M, Bochner BR, Peters G & Proctor RA (2006a) Phenotype microarray profiling of Staphylococcus aureus menD and hemB mutants with the small-colony-variant phenotype. J Bacteriol 188: 687-693.
47. von Eiff C, Peters G & Becker K (2006b) The small colony variant (SCV) concept - the role of staphylococcal SCVs in persistent infections. Injury 37(Suppl 2): S26-S33.
48. Waldron DE & Lindsay JA (2006) Sau1: a novel lineage-specific type I restriction-modification system that blocks horizontal gene transfer into Staphylococcus aureus and between S. aureus isolates of different lineages. J Bacteriol 188: 5578-5585.
49. Zhu H, Xie G, Liu M, Olson JS, Fabian M, Dooley DM & 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.