Menaquinone biosynthesis potentiates haem toxicity in Staphylococcus aureus

Molecular Microbiology

Volumn 86, Issue 6, 2012, Pages 1376-1392

  Wakeman, Catherine A ^a   Hammer, Neal D ^a   Stauff, Devin L ^a,b   Attia, Ahmed S ^a,c   Anzaldi, Laura L ^a   Dikalov, Sergey I ^d   Calcutt, M Wade ^a   Skaar, Eric P ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GROVE CITY COLLEGE   (United States)

^c CAIRO UNIVERSITY   (Egypt)

^d VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; HEME; MENAQUINONE; PROTEIN HRTAB; SUPEROXIDE; UNCLASSIFIED DRUG;

ARTICLE; BIOSYNTHESIS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; MUTANT; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; STAPHYLOCOCCUS AUREUS; TOXICITY; TRANSPOSON;

ADENOSINE TRIPHOSPHATASES; BIOSYNTHETIC PATHWAYS; DNA TRANSPOSABLE ELEMENTS; GENE DELETION; HEME; MUTAGENESIS, INSERTIONAL; OXIDATIVE STRESS; STAPHYLOCOCCUS AUREUS; SUPEROXIDES; VITAMIN K 2;

STAPHYLOCOCCUS AUREUS; VERTEBRATA;

EID: 84870983592     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12063     Document Type: Article

References (69)

1. Aft, R.L., and Mueller, G.C. (1983) Hemin-mediated DNA strand scission. J Biol Chem 258: 12069-12072.
2. Aft, R.L., and Mueller, G.C. (1984) Hemin-mediated oxidative degradation of proteins. J Biol Chem 259: 301-305.
3. Anzaldi, L.L., and Skaar, E.P. (2010) Overcoming the heme paradox: heme toxicity and tolerance in bacterial pathogens. Infect Immun 78: 4977-4989.
4. Attia, A.S., Benson, M.A., Stauff, D.L., Torres, V.J., and Skaar, E.P. (2010) Membrane damage elicits an immunomodulatory program in Staphylococcus aureus. PLoS Pathog 6: e1000802.
5. Bae, T., and Schneewind, O. (2006) Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid 55: 58-63.
6. Barja, G. (1999) Mitochondrial oxygen radical generation and leak: sites of production in states 4 and 3, organ specificity, and relation to aging and longevity. J Bioenerg Biomembr 31: 347-366.
7. Baumert, N., von Eiff, C., Schaaff, F., Peters, G., Proctor, R.A., and Sahl, H.G. (2002) Physiology and antibiotic susceptibility of Staphylococcus aureus small colony variants. Microb Drug Resist 8: 253-260.
8. Becker, K., Harmsen, D., Mellmann, A., Meier, C., Schumann, P., Peters, G., and von Eiff, C. (2004) Development and evaluation of a quality-controlled ribosomal sequence database for 16S ribosomal DNA-based identification of Staphylococcus species. J Clin Microbiol 42: 4988-4995.
9. Bentley, R., and Meganathan, R. (1982) Biosynthesis of vitamin K (menaquinone) in bacteria. Microbiol Rev 46: 241-280.
10. Bibb, L.A., and Schmitt, M. (2010) The ABC transporter HrtAB confers resistance to hemin toxicity and is regulated in a hemin-dependent manner by the ChrAS two-component system in Corynebacterium diphtheriae. J Bacteriol 192: 4606-4617.
11. Bullen, J.J., and Griffiths, E. (1999) Iron and infection. In Molecular, Physiological and Clinical Aspects, 2nd edn. Bullen, J.J., and Griffiths, E. (eds). New York, NY, USA: John Wiley & Sons, pp. 327-368.
12. Crichton, R. (2001) Inorganic biochemistry of iron metabolism. In Molecular Mechanisms to Clinical Consequences, 2nd edn. Crichton, R. (ed.). West Sussex, UK: John Wiley & Sons, pp. 107-234.
13. DeLeo, F.R., Otto, M., Kreiswirth, B.N., and Chambers, H.F. (2010) Community-associated meticillin-resistant Staphylococcus aureus. Lancet 375: 1557-1568.
14. Du, R., Ho, B., and Ding, J.L. (2010) Rapid reprogramming of haemoglobin structure-function exposes multiple dual-antimicrobial potencies. EMBO J 29: 632-642.
15. Duesterberg, C.K., and Waite, T.D. (2007) Kinetic modeling of the oxidation of p-hydroxybenzoic acid by Fenton's reagent: implications of the role of quinones in the redox cycling of iron. Environ Sci Technol 41: 4103-4110.
16. Duthie, E.S., and Lorenz, L. (1952) Staphylococcal coagulase: mode of action and antigenicity. J Gen Microbiol 6: 95-107.
17. von Eiff, C., Bettin, D., Proctor, R.A., Rolauffs, B., Lindner, N., Winkelmann, W., and Peters, G. (1997a) Recovery of small colony variants of Staphylococcus aureus following gentamicin bead placement for osteomyelitis. Clin Infect Dis 25: 1250-1251.
18. von Eiff, C., Heilmann, C., Proctor, R.A., Woltz, C., Peters, G., and Götz, F. (1997b) A site-directed Staphylococcus aureus hemB mutant is a small-colony variant which persists intracellularly. J Bacteriol 179: 4706-4712.
19. von Eiff, C., Peters, G., and Becker, K. (2006) The small colony variant (SCV) concept - the role of staphylococcal SCVs in persistent infections. Injury 37 (Suppl. 2): S26-S33.
20. Fernandez, A., Lechardeur, D., Derré-Bobillot, A., Couvé, E., Gaudu, P., and Gruss, A. (2010) Two coregulated efflux transporters modulate intracellular heme and protoporphyrin IX availability in Streptococcus agalactiae. PLoS Pathog 6: e1000860.
21. Friedman, D.B., Stauff, D.L., Pishchany, G., Whitwell, C.W., Torres, V.J., and Skaar, E.P. (2006) Staphylococcus aureus redirects central metabolism to increase iron availability. PLoS Pathog 2: e87.
22. Gaupp, R., Ledala, N., and Somerville, G.A. (2012) Staphylococcal response to oxidative stress. Front Cell Infect Microbiol 2: 33.
23. Geyer, R., Peacock, A.D., White, D.C., Lytle, C., and Van Berkel, G.J. (2004) Atmospheric pressure chemical ionization and atmospheric pressure photoionization for simultaneous mass spectrometric analysis of microbial respiratory ubiquinones and menaquinones. J Mass Spectrom 39: 922-929.
24. Gordon, R.J., and Lowy, F.D. (2008) Pathogenesis of methicillin-resistant Staphylococcus aureus infection. Clin Infect Dis 46: S350-S359.
25. Gutteridge, J.M., Quinlan, G.J., and Wilkins, S. (1984) Mitomycin C-induced deoxyribose degradation inhibited by superoxide dismutase. A reaction involving iron, hydroxyl and semiquinone radicals. FEBS Lett 167: 37-41.
26. Hammer, N.D., and Skaar, E. (2011) Molecular mechanisms of Staphylococcus aureus iron acquisition. Annu Rev Microbiol 65: 129-147.
27. 2 isoprenologues by Staphylococcus aureus. J Bacteriol 100: 573-578.
28. Holländer, R. (1976) Correlation of the function of demethylmenaquinone in bacterial electron transport with its redox potential. FEBS Lett 72: 98-100.
29. Huycke, M.M., Moore, D., Joyce, W., Wise, P., Shepard, L., Kotake, Y., and Gilmore, M.S. (2001) Extracellular superoxide production by Enterococcus faecalis requires demethylmenaquinone and is attenuated by functional terminal quinol oxidases. Mol Microbiol 42: 729-740.
30. Jeffries, L., Harris, M., and Price, S.A. (1967) Atypical menaquinone pattern in a strain of Staphylococcus aureus. Nature 216: 808-809.
31. Jiang, N., Tan, N.S., Ho, B., and Ding, J.L. (2007) Respiratory protein-generated reactive oxygen species as an antimicrobial strategy. Nat Immunol 8: 1114-1122.
32. Kehl-Fie, T.E., and Skaar, E.P. (2010) Nutritional immunity beyond iron: a role for manganese and zinc. Curr Opin Chem Biol 14: 218-224.
33. Klevens, R.M., Morrison, M.A., Nadle, J., Petit, S., Gershman, K., Ray, S., etal.; Active Bacterial Core surveillance (ABCs) MRSA Investigators (2007) Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298: 1763-1771.
34. Korshunov, S., and Imlay, J.A. (2006) Detection and quantification of superoxide formed within the periplasm of Escherichia coli. J Bacteriol 188: 6326-6334.
35. Ladan, H., Nitzan, Y., and Malik, Z. (1993) The antibacterial activity of haemin compared with cobalt, zinc and magnesium protoporphyrin and its effect on pottassium loss and ultrastructure of Staphylococcus aureus. FEMS Microbiol Lett 112: 173-177.
36. Lannergard, J., von Eiff, C., Sander, G., Cordes, T., Seggewiss, J., Peters, G., etal. (2008) Identification of the genetic basis for clinical menadione-auxotrophic small-colony variant isolates of Staphylococcus aureus. Antimicrob Agents Chemother 52: 4017-4022.
37. Leatherbarrow, A.J.H., Yazdi, M.A., Curson, J., and Moir, A. (1998) The gerC locus of Bacillus subtilis, required for menaquinone biosynthesis, is concerned only indirectly with spore germination. Microbiology 144: 2125-2130.
38. Lechardeur, D., Cesselin, B., Liebl, U., Vos, M.H., Fernandez, A., Brun, C., etal. (2012) Discovery of intracellular heme-binding protein HrtR, which controls heme efflux by the conserved HrtB-HrtA transporter in Lactococcus lactis. J Biol Chem 287: 4752-4758.
39. Locigno, E.J., Zweier, J.L., and Villamena, F.A. (2005) Nitric oxide release from the unimolecular decomposition of the superoxide radical anion adduct of cyclic nitrones in aqueous medium. Org Biomol Chem 3: 3220-3227.
40. Lombardo, M.E., Araujo, L.S., Ciccarelli, A.B., and Batlle, A. (2005) A spectrophotometric method for estimating hemin in biological systems. Anal Biochem 341: 199-203.
41. Lukomski, S., Hoe, N., Abdi, I., Rurangirwa, J., Kordari, P., Liu, M., etal. (2000) Nonpolar inactivation of the hypervariable streptococcal inhibitor of complement gene (sic) in serotype M1 Streptococcus pyogenes significantly decreases mouse mucosal colonization. Infect Immun 68: 535-542.
42. McMillan, D.G., Marritt, S.J., Butt, J.N., and Jeuken, L.J. (2012) Menaquinone-7 is specific cofactor in tetraheme quinol dehydrogenase CymA. J Biol Chem 287: 14215-14225.
43. Medina, L.F., Hertz, P.F., Stefani, V., Henriques, J.A., Zanotto-Filho, A., and Brandelli, A. (2006) Aminonaphthoquinone induces oxidative stress in Staphylococcus aureus. Biochem Cell Biol 84: 720-727.
44. Musher, D.M., Baughn, R.E., Templeton, G.B., and Minuth, J.N. (1977) Emergence of variant forms of Staphylococcus aureus after exposure to gentamicin and infectivity of the variants in experimental animals. J Infect Dis 136: 360-369.
45. Nir, U., Ladan, H., Malik, Z., and Nitzan, Y. (1991) In vivo effects of porphyrins on bacterial DNA. J Photochem Photobiol B 11: 295-306.
46. Nitzan, Y., Wexler, H.M., and Finegold, S.M. (1994) Inactivation of anaerobic bacteria by various photosensitized porphyrins or by hemin. Curr Microbiol 29: 125-131.
47. Novick, R.P. (1991) Genetic systems in staphylococci. Methods Enzymol 204: 587-636.
48. Osyczka, A., Moser, C.C., and Dutton, P.L. (2005) Fixing the Q cycle. Trends Biochem Sci 30: 176-182.
49. Pedersen, M.B., Garrigues, C., Tuphile, K., Brun, C., Vido, K., Bennedsen, M., etal. (2008) Impact of aeration and heme-activated respiration on Lactococcus lactis gene expression: identification of a heme-responsive operon. J Bacteriol 190: 4903-4911.
50. Proctor, R.A., von Eiff, C., Kahl, B.C., Becker, K., McNamara, P., Herrmann, M., and Peters, G. (2006) Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat Rev Microbiol 4: 295-305.
51. Reniere, M., Torres, V., and Skaar, E. (2007) Intracellular metalloporphyrin metabolism in Staphylococcus aureus. Biometals 20: 333-345.
52. Rezaïki, L., Lamberet, G., Derré, A., Gruss, A., and Gaudu, P. (2008) Lactococcus lactis produces short-chain quinones that cross-feed Group B Streptococcus to activate respiration growth. Mol Microbiol 67: 947-957.
53. Rifkind, J.M., Ramasamy, S., Manoharan, P.T., Nagababu, E., and Mohanty, J.G. (2004) Redox reactions of hemoglobin. Antioxid Redox Signal 6: 657-666.
54. Seifert, H., von Eiff, C., and Fatkenheuer, G. (1999) Fatal case due to methicillin-resistant Staphylococcus aureus small colony variants in an AIDS patient. Emerg Infect Dis 5: 450-453.
55. Simon, J., van Spanning, R.J.M., and Richardson, D.J. (2008) The organisation of proton motive and non-proton motive redox loops in prokaryotic respiratory systems. Biochim Biophys Acta 1777: 1480-1490.
56. Skaar, E.P., Humayun, M., Bae, T., DeBord, K.L., and Schneewind, O. (2004) Iron-source preference of Staphylococcus aureus infections. Science 305: 1626-1628.
57. Stauff, D.L., and Skaar, E.P. (2009) Bacillus anthracis HssRS signalling to HrtAB regulates haem resistance during infection. Mol Microbiol 72: 763-778.
58. Stauff, D.L., Torres, V.J., and Skaar, E.P. (2007) Signaling and DNA-binding activities of the Staphylococcus aureus HssR-HssS two-component system required for heme sensing. J Biol Chem 282: 26111-26121.
59. Stauff, D.L., Bagaley, D., Torres, V.J., Joyce, R., Anderson, K.L., Kuechenmeister, L., etal. (2008) Staphylococcus aureus HrtA is an ATPase required for protection against heme toxicity and prevention of a transcriptional heme stress response. J Bacteriol 190: 3588-3596.
60. Stohs, S.J., and Bagchi, D. (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18: 321-336.
61. Torres, V.J., Stauff, D.L., Pishchany, G., Bezbradica, J.S., Gordy, L.E., Iturregui, J., etal. (2007) A Staphylococcus aureus regulatory system that responds to host heme and modulates virulence. Cell Host Microbe 1: 109-119.
62. Wakeman, C.A., and Skaar, E.P. (2012) Metalloregulation of Gram-positive pathogen physiology. Curr Opin Microbiol 15: 169-174.
63. Wertheim, H.F.L., Vos, M.C., Ott, A., van Belkum, A., Voss, A., Kluytmans, J.A.J.W., etal. (2004) Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. Lancet 364: 703-705.
64. Wissenbach, U., Ternes, D., and Unden, G. (1992) An Escherichia coli mutant containing only demethylmenaquinone, but no menaquinone: effects on fumarate, dimethylsulfoxide, trimethylamine N-oxide and nitrate respiration. Arch Microbiol 158: 68-73.
65. Youngman, P.J., Perkins, J.B., and Losick, R. (1983) Genetic transposition and insertional mutagenesis in Bacillus subtilis with Streptococcus faecalis transposon Tn917. Proc Natl Acad Sci USA 80: 2305-2309.
66. Yu, T.W., and Anderson, D. (1997) Reactive oxygen species-induced DNA damage and its modification: a chemical investigation. Mutat Res 379: 201-210.
67. Zamboni, N., and Sauer, U. (2003) Knockout of the high-coupling cytochrome aa3 oxidase reduces TCA cycle fluxes in Bacillus subtilis. FEMS Microbiol Lett 226: 121-126.
68. Zhang, H., Joseph, J., Vasquez-Vivar, J., Karoui, H., Nsanzumuhire, C., Martasek, P., etal. (2000) Detection of superoxide anion using an isotopically labeled nitrone spin trap: potential biological applications. FEBS Lett 473: 58-62.
69. Zhang, Y.W., Koyama, T., and Ogura, K. (1997) Two cistrons of the gerC operon of Bacillus subtilis encode the two subunits of heptaprenyl diphosphate synthase. J Bacteriol 179: 1417-1419.