Genetic evidence for an alternative citrate-dependent biofilm formation pathway in Staphylococcus aureus that is dependent on fibronectin binding proteins and the grars two-component regulatory system

Infection and Immunity

Volumn 76, Issue 6, 2008, Pages 2469-2477

  Shanks, Robert M Q ^a,c   Meehl, Michael A ^a,d   Brothers, Kimberly M ^a   Martinez, Raquel M ^a   Donegan, Niles P ^a   Graber, Martha L ^b   Cheung, Ambrose L ^a   O'Toole, George A ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b DARTMOUTH HITCHCOCK MEDICAL CENTER   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d GlycoFi Incorporated   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACONITATE HYDRATASE; ADHESIN; ALPHA CRYSTALLIN; CITRIC ACID; FIBRONECTIN BINDING PROTEIN; FIBRONECTIN BINDING PROTEIN A; FIBRONECTIN BINDING PROTEIN B; POLYSACCHARIDE; UNCLASSIFIED DRUG; VANCOMYCIN; CITRATE SODIUM; FIBRONECTIN BINDING PROTEIN, BACTERIA; FIBRONECTIN-BINDING PROTEIN, BACTERIA; TRICARBOXYLIC ACID;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; BIOFILM; CATHETER INFECTION; CELL INTERACTION; CITRIC ACID CYCLE; GENE EXPRESSION; GENETIC ANALYSIS; IN VIVO STUDY; LABORATORY TEST; PRIORITY JOURNAL; PROTEIN BINDING; STAPHYLOCOCCUS AUREUS; VIRULENCE; BACTERIUM ADHERENCE; DOSE RESPONSE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY;

ADHESINS, BACTERIAL; BACTERIAL ADHESION; BIOFILMS; CITRATES; CITRIC ACID; CITRIC ACID CYCLE; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION, BACTERIAL; STAPHYLOCOCCUS AUREUS; TRICARBOXYLIC ACIDS;

EID: 46249123801     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01370-07     Document Type: Article

References (75)

1. Adler, R. H., and J. E. Snoke. 1962. Requirement of divalent metal ions for bacitracin activity. J. Bacteriol. 83:1315-1317.
2. Appelbaum, P. C. 2006. The emergence of vancomycin-intermediate and vancomycin-resistant Staphylococcus aureus. Clin. Microbiol. Infect. 12(Suppl. 1):16-23.
3. Arciola, C. R., Y. Bustanji, M. Conti, D. Campoccia, L. Baldassarri, B. Samori, and L. Montanaro. 2003. Staphylococcus epidermidis - fibronectin binding and its inhibition by heparin. Biomaterials 24:3013-3019.
4. Arciola, C. R., D. Campoccia, and L. Montanaro. 2002. Detection of biofilm-forming strains of Staphylococcus epidermidis and S. aureus. Expert Rev. Mol. Diagn. 2:478-484.
5. Beenken, K. E., P. M. Dunman, F. McAleese, D. Macapagal, E. Murphy, S. J. Projan, J. S. Blevins, and M. S. Smeltzer. 2004. Global gene expression in Staphylococcus aureus biofilms. J. Bacteriol. 186:4665-4684.
6. Begun, J., J. M. Gaiani, H. Rohde, D. Mack, S. B. Calderwood, F. M. Ausubel, and C. D. Sifri. 2007. Staphylococcal biofilm exopolysaccharide protects against Caenorhabditis elegans immune defenses. PLoS Pathog. 3:e57.
7. Best, G. K., and N. N. Durham. 1964. Effect of vancomycin on Bacillus subtilis. Arch. Biochem. Biophys. 105:120-125.
8. Best, G. K., and N. N. Durham. 1965. Vancomycin adsorption to Bacillus subtilis cell walls. Arch. Biochem. Biophys. 111:685-692.
9. Caiazza, N. C., and G. A. O'Toole. 2003. Alpha-toxin is required for biofilm formation by Staphylococcus aureus. J. Bacteriol. 185:3214-3217.
10. Chatterjee, I., P. Becker, M. Grundmeier, M. Bischoff, G. A. Somerville, G. Peters, B. Sinha, N. Harraghy, R. A. Proctor, and M. Herrmann. 2005. Staphylococcus aureus ClpC is required for stress resistance, aconitase activity, growth recovery, and death. J. Bacteriol. 187:4488-4496.
11. Cheung, A. L., M. G. Bayer, and J. H. Heinrichs. 1997. sar genetic determinants necessary for transcription of RNAII and RNAIII in the agr locus of Staphylococcus aureus. J. Bacteriol. 179:3963-3971.
12. Cheung, A. L., J. M. Koomey, C. A. Butler, S. J. Projan, and V. A. Fischetti. 1992. Regulation of exoprotein expression in Staphylococcus aureus by a locus (sar) distinct from agr. Proc. Natl. Acad. Sci. USA 89:6462-6466.
13. Cheung, A. L., and S. J. Projan. 1994. Cloning and sequencing of sarA of Staphylococcus aureus, a gene required for the expression of agr. J. Bacteriol. 176:4168-4172.
14. Cheung, A. L., and G. Zhang. 2002. Global regulation of virulence determinants in Staphylococcus aureus by the SarA protein family. Front. Biosci. 7:d1825-d1842.
15. Chien, Y., A. C. Manna, S. J. Projan, and A. L. Cheung. 1999. SarA, a global regulator of virulence determinants in Staphylococcus aureus, binds to a conserved motif essential for sar-dependent gene regulation. J. Biol. Chem. 274:37169-37176.
16. Chokr, A., D. Leterme, D. Watier, and S. Jabbouri. 2007. Neither the presence of ica locus, nor in vitro-biofilm formation ability is a crucial parameter for some Staphylococcus epidermidis strains to maintain an infection in a guinea pig tissue cage model. Microb. Pathog. 42:94-97.
17. Cramton, S. E., C. Gerke, N. F. Schnell, W. W. Nichols, and F. Gotz. 1999. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect. Immun. 67:5427-5433.
18. Cui, L., J. Lian, H. Neoh, E. Reyes, and K. Hiramatsu. 2005. DNA microarray-based identification of genes associated with glycopeptide resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 49:3404-3413.
19. del Pozo, J. L., and R. Patel. 2007. The challenge of treating biofilm-associated bacterial infections. Clin. Pharmacol. Ther. 82:204-209.
20. Dunman, P. M., E. Murphy, S. Haney, D. Palacios, G. Tucker-Kellogg, S. Wu, E. L. Brown, R. J. Zagursky, D. Shlaes, and S. J. Projan. 2001. Transcription profiling-based identification of Staphylococcus aureus genes regulated by the agr and/or sarA loci. J. Bacteriol. 183:7341-7353.
21. Fluckiger, U., M. Ulrich, A. Steinhuber, G. Doring, D. Mack, R. Landmann, C. Goerke, and C. Wolz. 2005. Biofilm formation, icaADBC transcription, and polysaccharide intercellular adhesin synthesis by staphylococci in a device-related infection model. Infect. Immun. 73:1811-1819.
22. Forsyth, R. A., R. J. Haselbeck, K. L. Ohlsen, R. Yamamoto, T. H. Xu, J. D. Trawick, D. Wall, L. Wang, V. Brown-Driver, J. M. Froelich, G. C. Kedar, P. King, M. McCartney, C. Malone, B. Misiner, D. Robbins, Z. Tan, Z. Zhu, G. Carr, D. A. Mosca, C. Zamudio, J. G. Foulkes, and J. W. Zyskind. 2002. A genome-wide strategy for the identification of essential genes in Staphylococcus aureus. Mol. Microbiol. 43:1387-1400.
23. Francois, P., P. H. T. Quoc, C. Bisognano, W. L. Kelley, D. P. Lew, J. Schrenzel, S. E. Cramton, F. Gotz, and P. Vaudaux. 2003. Lack of biofilm contribution to bacterial colonisation in an experimental model of foreign body infection by Staphylococcus aureus and Staphylococcus epidermidis. FEMS Immunol. Med. Microbiol. 35:135-140.
24. Frank, K. L., A. D. Hanssen, and R. Patel. 2004. icaA is not a useful diagnostic marker for prosthetic joint infection. J. Clin. Microbiol. 42:4846-4849.
25. Frees, D., A. Chastanet, S. Qazi, K. Sorensen, P. Hill, T. Msadek, and H. Ingmer. 2004. Clp ATPases are required for stress tolerance, intracellular replication and biofilm formation in Staphylococcus aureus. Mol. Microbiol. 54:1445-1462.
26. Gill, S. R., D. E. Fouts, G. L. Archer, E. F. Mongodin, R. T. Deboy, J. Ravel, I. T. Paulsen, J. F. Kolonay, L. Brinkac, M. Beanan, R. J. Dodson, S. C. Daugherty, R. Madupu, S. V. Angiuoli, A. S. Durkin, D. H. Haft, J. Vamathevan, H. Khouri, T. Utterback, C. Lee, G. Dimitrov, L. Jiang, H. Qin, J. Weidman, K. Tran, K. Kang, I. R. Hance, K. E. Nelson, and C. M. Fraser. 2005. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J. Bacteriol. 187:2426-2438.
27. Gotz, F. 2002. Staphylococcus and biofilms. Mol. Microbiol. 43:1367-1378.
28. Grundmeier, M., M. Hussain, P. Becker, C. Heilmann, G. Peters, and B. Sinha. 2004. Truncation of fibronectin-binding proteins in Staphylococcus aureus strain Newman leads to deficient adherence and host cell invasion due to loss of the cell wall anchor function. Infect. Immun. 72:7155-7163.
29. Hall-Stoodley, L., J. W. Costerton, and P. Stoodley. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2:95-108.
30. Hauck, C. R., and K. Ohlsen. 2006. Sticky connections: extracellular matrix protein recognition and integrin-mediated cellular invasion by Staphylococcus aureus. Curr. Opin. Microbiol. 9:5-11.
31. Helander, I. M., and T. Mattila-Sandholm. 2000. Fluorometric assessment of gram-negative bacterial permeabilization. J. Appl. Microbiol. 88:213-219.
32. Herbert, S., A. Bera, C. Nerz, D. Kraus, A. Peschel, C. Goerke, M. Meehl, A. Cheung, and F. Gotz. 2007. Molecular basis of resistance to muramidase and cationic antimicrobial peptide activity of lysozyme in staphylococci. PLoS Pathog. 3:e102.
33. B modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J. Bacteriol. 184:5457-5467.
34. Joh, H. J., K. House-Pompeo, J. M. Patti, S. Gurusiddappa, and M. Hook. 1994. Fibronectin receptors from gram-positive bacteria: comparison of active sites. Biochemistry 33:6086-6092.
35. Kornblum, J., B. Kreiswirth, S. J. Projan, H. Ross, and R. P. Novick. 1990. agr: a polycistronic locus regulating exoprotein synthesis in Staphylococcus aureus, p. 373-402. In R. P. Novick (ed.), Molecular biology of the staphylococci. VCH Publishers, New York, NY.
36. Kristian, S. A., T. Golda, F. Ferracin, S. E. Cramton, B. Neumeister, A. Peschel, F. Gotz, and R. Landmann. 2004. The ability of biofilm formation does not influence virulence of Staphylococcus aureus and host response in a mouse tissue cage infection model. Microb. Pathog. 36:237-245.
37. Kropec, A., T. Maira-Litran, K. K. Jefferson, M. Grout, S. E. Cramton, F. Gotz, D. A. Goldmann, and G. B. Pier. 2005. Poly-N-acetylglucosamine production in Staphylococcus aureus is essential for virulence in murine models of systemic infection. Infect. Immun. 73:6868-6876.
38. Kuchma, S. L., K. M. Brothers, J. H. Merritt, N. T. Liberati, F. M. Ausubel, and G. A. O'Toole. 2007. BifA, a cyclic-di-GMP phosphodiesterase, inversely regulates biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J. Bacteriol. 189:8165-8178.
39. Kuroda, M., T. Ohta, I. Uchiyama, T. Baba, H. Yuzawa, I. Kobayashi, L. Cui, A. Oguchi, K. Aoki, Y. Nagai, J. Lian, T. Ito, M. Kanamori, H. Matsumaru, A. Maruyama, H. Murakami, A. Hosoyama, Y. Mizutani-Ui, N. K. Takahashi, T. Sawano, R. Inoue, C. Kaito, K. Sekimizu, H. Hirakawa, S. Kuhara, S. Goto, J. Yabuzaki, M. Kanehisa, A. Yamashita, K. Oshima, K. Furuya, C. Yoshino, T. Shiba, M. Hattori, N. Osgasawara, H. Hayashi, and K. Hiramatsu. 2001. Whole genome sequencing of methicillin-resistant Staphylococcus aureus. Lancet 357:1225-1240.
40. Lee, Y.-L., T. Cesario, J. Owens, E. Shanbrom, and L. D. Thrupp. 2002. Antibacterial activity of citrate and acetate. Nutrition 18:665-666.
41. Lee, Y.-L., L. D. Thrupp, T. Owens, T. Cesario, and E. Shanbrom. 2001. Bactericidal activity of citrate against gram-positive cocci. Lett. Appl. Microbiol. 33:349-351.
42. Li, H., L. Xu, J. Wang, Y. Wen, C. Vuong, M. Otto, and Q. Gao. 2005. Conversion of Staphylococcus epidermidis strains from commensal to invasive by expression of the ica locus encoding production of biofilm exopolysaccharide. Infect. Immun. 73:3188-3191.
43. Lowy, F. D. 1998. Staphylococcus aureus infections. N. Engl. J. Med. 339:520-532.
44. Mack, D., W. Fischer, A. Krokotsch, K. Leopold, R. Hartmann, H. Egge, and R. Laufs. 1996. The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear β-1,6-linked glucosaminoglycan: purification and structural analysis. J. Bacteriol. 178:175-183.
45. Mack, D., M. Nedelmann, A. Krokotsch, A. Schwarzkopf, J. Heesemann, and R. Laufs. 1994. Characterization of transposon mutants of biofilm-producing Staphylococcus epidermidis impaired in the accumulative phase of biofilm production: genetic identification of a hexosamine-containing polysaccharide intercellular adhesin. Infect. Immun. 62:3244-3253.
46. Mack, D., J. Riedewald, H. Rohde, T. Magnus, H. H. Feucht, H. A. Elsner, R. Laufs, and M. E. Rupp. 1999. Essential functional role of the polysaccharide intercellular adhesin of Staphylococcus epidermidis in hemagglutination. Infect. Immun. 67:1004-1008.
47. Manna, A., and A. L. Cheung. 2001. Characterization of sarR, a modulator of sar expression in Staphylococcus aureus. Infect. Immun. 69:885-896.
48. Mascher, T., N. G. Margulis, T. Wang, R. W. Ye, and J. D. Helmann. 2003. Cell wall stress responses in Bacillus subtilis: the regulatory network of the bacitracin stimulon. Mol. Microbiol. 50:1591-1604.
49. McAleese, F., S. W. Wu, K. Sieradzki, P. Dunman, E. Murphy, S. Projan, and A. Tomasz. 2006. Overexpression of genes of the cell wall stimulon in clinical isolates of Staphylococcus aureus exhibiting vancomycin-intermediate-S. aureus-type resistance to vancomycin. J. Bacteriol. 188:1120-1133.
50. McKenney, D., J. Hubner, E. Muller, Y. Wang, D. A. Goldmann, and G. B. Pier. 1998. The ica locus of Staphylococcus epidermidis encodes production of the capsular polysaccharide/adhesin. Infect. Immun. 66:4711-4720.
51. Meehl, M., S. Herbert, F. Gotz, and A. Cheung. 2007. Interaction of the GraRS two-component system with the VraFG ABC transporter to support vancomycin-intermediate resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 51:2679-2689.
52. Ninin, E., N. Caroff, E. Espaze, J. Maraillac, D. Lepelletier, N. Milpied, and H. Richet. 2006. Assessment of ica operon carriage and biofilm production in Staphylococcus epidermidis isolates causing bacteraemia in bone marrow transplant recipients. Clin. Microbiol. Infect. 12:446-452.
53. O'Gara, J. P. 2007. ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol. Lett. 270:179-188.
54. O'Toole, G., H. B. Kaplan, and R. Kolter. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:49-79.
55. Pratten, J., S. J. Foster, P. F. Chan, M. Wilson, and S. P. Nair. 2001. Staphylococcus aureus accessory regulators: expression within biofilms and effect on adhesion. Microbes Infect. 3:633-637.
56. Raad, I. 1998. Intravascular-catheter-related infections. Lancet 351:893-898.
57. Raad, I. I., and H. A. Hanna. 2002. Intravascular catheter-related infections. Arch. Intern. Med. 162:871-878.
58. ++ on the activity of vancomycin against Escherichia coli. Appl. Microbiol. 14:902-904.
59. Satorres, S. E., and L. E. Alcaráz. 2007. Prevalence of icaA and icaD genes in Staphylococcus aureus and Staphylococcus epidermidis strains isolated from patients and hospital staff. Cent. Eur. J. Public Health 15:87-90.
60. Shah, C. B., M. W. Mittelman, J. W. Costerton, S. Parenteau, M. Pelak, R. Arsenault, and L. A. Mermel. 2002. Antimicrobial activity of a novel catheter lock solution. Antimicrob. Agents Chemother. 46:1674-1679.
61. Shanks, R. M., N. P. Donegan, M. L. Graber, S. E. Buckingham, M. E. Zegans, A. L. Cheung, and G. A. O'Toole. 2005. Heparin stimulates Staphylococcus aureus biofilm formation. Infect. Immun. 73:4596-4606.
62. Shanks, R. M., J. L. Sargent, R. M. Martinez, M. L. Graber, and G. A. O'Toole. 2006. Catheter lock solutions influence staphylococcal biofilm formation on abiotic surfaces. Nephrol. Dial. Transplant. 21:2247-2255.
63. Somerville, G. A., M. S. Chaussee, C. I. Morgan, J. R. Fitzgerald, D. W. Dorward, L. J. Reitzer, and J. M. Musser. 2002. Staphylococcus aureus aconitase inactivation unexpectedly inhibits post-exponential-phase growth and enhances stationary-phase survival. Infect. Immun. 70:6373-6382.
64. Somerville, G. A., B. Said-Salim, J. M. Wickman, S. J. Raffel, B. N. Kreiswirth, and J. M. Musser. 2003. Correlation of acetate catabolism and growth yield in Staphylococcus aureus: implications for host-pathogen interactions. Infect. Immun. 71:4724-4732.
65. Strasters, K. C., and K. C. Winkler. 1963. Carbohydrate metabolism of Staphylococcus aureus. J. Gen. Microbiol. 33:213-229.
66. Valle, J., A. Toledo-Arana, C. Berasain, J. M. Ghigo, B. Amorena, J. R. Penades, and I. Lasa. 2003. SarA and not sigmaB is essential for biofilm development by Staphylococcus aureus. Mol. Microbiol. 48:1075-1087.
67. Vaudaux, P., T. Avramoglou, D. Letourneur, D. P. Lew, and J. Jozefonvicz. 1992. Inhibition by heparin and derivatized dextrans of Staphylococcus aureus adhesion to fibronectin-coated biomaterials. J. Biomater. Sci. Polym. Ed. 4:89-97.
68. Vaudaux, P., P. Francois, C. Bisognano, W. L. Kelley, D. P. Lew, J. Schrenzel, R. A. Proctor, P. J. McNamara, G. Peters, and C. Von Eiff. 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.
69. Vuong, C., J. B. Kidder, E. R. Jacobson, M. Otto, R. A. Proctor, and G. A. Somerville. 2005. Staphylococcus epidermidis polysaccharide intercellular adhesin production significantly increases during tricarboxylic acid cycle stress. J. Bacteriol. 187:2967-2973.
70. Vuong, C., S. Kocianova, J. M. Voyich, Y. Yao, E. R. Fischer, F. R. Deleo, and M. Otto. 2004. A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J. Biol. Chem. 279:54881-54886.
71. Vuong, C., and M. Otto. 2002. Staphylococcus epidermidis infections. Microbes Infect. 4:481-489.
72. Vuong, C., H. L. Saenz, F. Gotz, and M. Otto. 2000. Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus. J. Infect. Dis. 182:1688-1693.
73. Wolz, C., P. Pohlmann-Dietze, A. Steinhuber, Y. T. Chien, A. Manna, W. van Wamel, and A. Cheung. 2000. Agr-independent regulation of fibronectin-binding protein(s) by the regulatory locus sar in Staphylococcus aureus. Mol. Microbiol. 36:230-243.
74. Yarwood, J. M., and P. M. Schlievert. 2003. Quorum sensing in Staphylococcus infections. J. Clin. Investig. 112:1620-1625.
75. Zegans, M. E., R. M. Q. Shanks, and G. A. O'Toole. 2005. Bacterial biofilms and ocular infections. Ocul. Surface 3:12-19.