Modality of bacterial growth presents unique targets: How do we treat biofilm-mediated infections?

Current Opinion in Microbiology

Volumn 13, Issue 5, 2010, Pages 610-615

  Fey, Paul D ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; AMIKACIN; BETA N ACETYLHEXOSAMINIDASE; CEFOTAXIME; CHLORHEXIDINE; CIPROFLOXACIN; COLISTIN; DALFOPRISTIN PLUS QUINUPRISTIN; DAPTOMYCIN; DEOXYRIBONUCLEASE I; DISPERSIN B; DORNASE ALFA; FIBRONECTIN BINDING PROTEIN; LINEZOLID; OXACILLIN; RIFAMPICIN; SULFADIAZINE SILVER; TIGECYCLINE; UNCLASSIFIED DRUG; VANCOMYCIN;

BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL METABOLISM; BIOFILM; CELL COMMUNICATION; DRUG SCREENING; HUMAN; NONHUMAN; PHENOTYPE; QUORUM SENSING; REVIEW; STAPHYLOCOCCUS; STAPHYLOCOCCUS INFECTION;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BIOFILMS; DEOXYRIBONUCLEASE I; QUORUM SENSING; STAPHYLOCOCCUS;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS;

EID: 77957760025     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2010.09.007     Document Type: Review

References (66)

1. Kohanski M.A., Dwyer D.J., Hayete B., Lawrence C.A., Collins J.J. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 2007, 130:797-810.
2. Harro J.M., Peters B.M., O'May G.A., Archer N., Kerns P., Prabhakara R., Shirtliff M.E. Vaccine development in Staphylococcus aureus: taking the biofilm phenotype into consideration. FEMS Immunol Med Microbiol 2010, 59:306-323.
3. Stewart P.S., Costerton J.W. Antibiotic resistance of bacteria in biofilms. Lancet 2001, 358:135-138.
4. Fux C.A., Stoodley P., Hall-Stoodley L., Costerton J.W. Bacterial biofilms: a diagnostic and therapeutic challenge. Expert Rev Anti Infect Ther 2003, 1:667-683.
5. Hall-Stoodley L., Stoodley P. Evolving concepts in biofilm infections. Cell Microbiol 2009, 11:1034-1043.
6. Parsek M.R., Singh P.K. Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol 2003, 57:677-701.
7. Lopez D., Vlamakis H., Kolter R. Biofilms. Cold Spring Harb Perspect Biol 2010, 2:a000398.
8. National Nosocomial Infections Surveillance System National Nosocomial Infections Surveillance (NNIS) System Report, data summary from January 1992 through June 2004, issued October 2004. Am J Infect Control 2004, 32:470-485.
9. Lowy F.D. Staphylococcus aureus infections. N Engl J Med 1998, 339:520-532.
10. Fey P.D., Olson M.E. Current concepts in biofilm formation of Staphylococcus epidermidis. Future Microbiol 2010, 5:917-933.
11. Otto M. Staphylococcus epidermidis-the 'accidental' pathogen. Nat Rev Microbiol 2009, 7:555-567.
12. O'Gara J.P. ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol Lett 2007, 270:179-188.
13. Heilmann C., Schweitzer O., Gerke C., Vanittanakom N., Mack D., Gotz F. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol 1996, 20:1083-1091.
14. Ganeshnarayan K., Shah S.M., Libera M.R., Santostefano A., Kaplan J.B. Poly-N-acetylglucosamine matrix polysaccharide impedes fluid convection and transport of the cationic surfactant cetylpyridinium chloride through bacterial biofilms. Appl Environ Microbiol 2009.
15. Vuong C., Voyich J.M., Fischer E.R., Braughton K.R., Whitney A.R., DeLeo F.R., Otto M. Polysaccharide intercellular adhesin (PIA) protects Staphylococcus epidermidis against major components of the human innate immune system. Cell Microbiol 2004, 6:269-275.
16. Rupp M.E., Ulphani J.S., Fey P.D., Bartscht K., Mack D. Characterization of the importance of polysaccharide intercellular adhesin/hemagglutinin of Staphylococcus epidermidis in the pathogenesis of biomaterial-based infection in a mouse foreign body infection model. Infect Immun 1999, 67:2627-2632.
17. Rupp M.E., Ulphani J.S., Fey P.D., Mack D. Characterization of Staphylococcus epidermidis polysaccharide intercellular adhesin/hemagglutinin in the pathogenesis of intravascular catheter-associated infection in a rat model. Infect Immun 1999, 67:2656-2659.
18. Galdbart J.O., Allignet J., Tung H.S., Ryden C., El Solh N. Screening for Staphylococcus epidermidis markers discriminating between skin-flora strains and those responsible for infections of joint prostheses. J Infect Dis 2000, 182:351-355.
19. Kozitskaya S., Olson M.E., Fey P.D., Witte W., Ohlsen K., Ziebuhr W. Clonal analysis of Staphylococcus epidermidis isolates carrying or lacking biofilm-mediating genes by multilocus sequence typing. J Clin Microbiol 2005, 43:4751-4757.
20. Beenken K.E., Dunman P.M., McAleese F., Macapagal D., Murphy E., Projan S.J., Blevins J.S., Smeltzer M.S. Global gene expression in Staphylococcus aureus biofilms. J Bacteriol 2004, 186:4665-4684.
21. Fitzpatrick F., Humphreys H., O'Gara J.P. Evidence for icaADBC-independent biofilm development mechanism in methicillin-resistant Staphylococcus aureus clinical isolates. J Clin Microbiol 2005, 43:1973-1976.
22. Valle J., Toledo-Arana A., Berasain C., Ghigo J.M., Amorena B., Penades J.R., Lasa I. SarA and not sigmaB is essential for biofilm development by Staphylococcus aureus. Mol Microbiol 2003, 48:1075-1087.
23. Banner M.A., Cunniffe J.G., Macintosh R.L., Foster T.J., Rohde H., Mack D., Hoyes E., Derrick J., Upton M., Handley P.S. Localized tufts of fibrils on Staphylococcus epidermidis NCTC 11047 are comprised of the accumulation-associated protein. J Bacteriol 2007, 189:2793-2804.
24. Clarke S.R., Harris L.G., Richards R.G., Foster S.J. Analysis of Ebh, a 1.1-megadalton cell wall-associated fibronectin-binding protein of Staphylococcus aureus. Infect Immun 2002, 70:6680-6687.
25. Rohde H., Burdelski C., Bartscht K., Hussain M., Buck F., Horstkotte M.A., Knobloch J.K., Heilmann C., Herrmann M., Mack D. Induction of Staphylococcus epidermidis biofilm formation via proteolytic processing of the accumulation-associated protein by staphylococcal and host proteases. Mol Microbiol 2005, 55:1883-1895.
26. Tormo M.A., Knecht E., Gotz F., Lasa I., Penades J.R. Bap-dependent biofilm formation by pathogenic species of Staphylococcus: evidence of horizontal gene transfer?. Microbiology 2005, 151:2465-2475.
27. Merino N., Toledo-Arana A., Vergara-Irigaray M., Valle J., Solano C., Calvo E., Lopez J.A., Foster T.J., Penades J.R., Lasa I. Protein A-mediated multicellular behavior in Staphylococcus aureus. J Bacteriol 2009, 191:832-843.
28. O'Neill E., Pozzi C., Houston P., Humphreys H., Robinson D.A., Loughman A., Foster T.J., O'Gara J.P. A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectin-binding proteins, FnBPA and FnBPB. J Bacteriol 2008, 190:3835-3850.
29. Corrigan R.M., Rigby D., Handley P., Foster T.J. The role of Staphylococcus aureus surface protein SasG in adherence and biofilm formation. Microbiology 2007, 153:2435-2446.
30. Rice K.C., Mann E.E., Endres J.L., Weiss E.C., Cassat J.E., Smeltzer M.S., Bayles K.W. The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc Natl Acad Sci U S A 2007, 104:8113-8118.
31. Rohde H., Burandt E.C., Siemssen N., Frommelt L., Burdelski C., Wurster S., Scherpe S., Davies A.P., Harris L.G., Horstkotte M.A., et al. Polysaccharide intercellular adhesin or protein factors in biofilm accumulation of Staphylococcus epidermidis and Staphylococcus aureus isolated from prosthetic hip and knee joint infections. Biomaterials 2007, 28:1711-1720.
32. Vergara-Irigaray M., Valle J., Merino N., Latasa C., Garcia B., Ruiz de Los Mozos I., Solano C., Toledo-Arana A., Penades J.R., Lasa I. Relevant role of fibronectin-binding proteins in Staphylococcus aureus biofilm-associated foreign-body infections. Infect Immun 2009, 77:3978-3991.
33. Stewart P.S., Franklin M.J. Physiological heterogeneity in biofilms. Nat Rev Microbiol 2008, 6:199-210.
34. Rani S.A., Pitts B., Beyenal H., Veluchamy R.A., Lewandowski Z., Davison W.M., Buckingham-Meyer K., Stewart P.S. Spatial patterns of DNA replication, protein synthesis, and oxygen concentration within bacterial biofilms reveal diverse physiological states. J Bacteriol 2007, 189:4223-4233.
35. Lewis K. Persister cells. Annu Rev Microbiol 2010.
36. Singh R., Ray P., Das A., Sharma M. Role of persisters and small-colony variants in antibiotic resistance of planktonic and biofilm-associated Staphylococcus aureus: an in vitro study. J Med Microbiol 2009, 58:1067-1073.
37. Dorr T., Vulic M., Lewis K. Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol 2010, 8:e1000317.
38. Resch A., Rosenstein R., Nerz C., Gotz F. Differential gene expression profiling of Staphylococcus aureus cultivated under biofilm and planktonic conditions. Appl Environ Microbiol 2005, 71:2663-2676.
39. Yao Y., Sturdevant D.E., Otto M. Genomewide analysis of gene expression in Staphylococcus epidermidis biofilms: insights into the pathophysiology of S. epidermidis biofilms and the role of phenol-soluble modulins in formation of biofilms. J Infect Dis 2005, 191:289-298.
40. Zhu Y., Weiss E.C., Otto M., Fey P.D., Smeltzer M.S., Somerville G.A. Staphylococcus aureus biofilm metabolism and the influence of arginine on polysaccharide intercellular adhesin synthesis, biofilm formation, and pathogenesis. Infect Immun 2007, 75:4219-4226.
41. Somerville G.A., Proctor R.A. At the crossroads of bacterial metabolism and virulence factor synthesis in Staphylococci. Microbiol Mol Biol Rev 2009, 73:233-248.
42. Rupp M.E., Archer G.L. Coagulase-negative staphylococci: pathogens associated with medical progress. Clin Infect Dis 1994, 19:231-243. quiz 244-235.
43. Rupp M.E., Lisco S.J., Lipsett P.A., Perl T.M., Keating K., Civetta J.M., Mermel L.A., Lee D., Dellinger E.P., Donahoe M., et al. Effect of a second-generation venous catheter impregnated with chlorhexidine and silver sulfadiazine on central catheter-related infections: a randomized, controlled trial. Ann Intern Med 2005, 143:570-580.
44. Ammons C.B. Anti-biofilm strategies and the need for innovations in wound care. Recent Pat Antiinfect Drug Discov 2010, 5:10-17.
45. Aslam S., Trautner B.W., Ramanathan V., Darouiche R.O. Combination of tigecycline and N-acetylcysteine reduces biofilm-embedded bacteria on vascular catheters. Antimicrob Agents Chemother 2007, 51:1556-1558.
46. Trampuz A., Zimmerli W. Antimicrobial agents in orthopaedic surgery: prophylaxis and treatment. Drugs 2006, 66:1089-1105.
47. Mogenet I., Raetz-Dillon S., Canonge J.M., Archambaud M., Bonnet E. Successful treatment of Staphylococcus epidermidis hip prosthesis infection with oral linezolid. Ann Pharmacother 2004, 38:986-988.
48. Raad I., Alrahwan A., Rolston K. Staphylococcus epidermidis: emerging resistance and need for alternative agents. Clin Infect Dis 1998, 26:1182-1187.
49. Saginur R., Stdenis M., Ferris W., Aaron S.D., Chan F., Lee C., Ramotar K. Multiple combination bactericidal testing of staphylococcal biofilms from implant-associated infections. Antimicrob Agents Chemother 2006, 50:55-61.
50. Saleh-Mghir A., Ameur N., Muller-Serieys C., Ismael F., Lemaitre F., Massias L., Feger C., Bleton R., Cremieux A.C. Combination of quinupristin-dalfopristin (Synercid) and rifampin is highly synergistic in experimental Staphylococcus aureus joint prosthesis infection. Antimicrob Agents Chemother 2002, 46:1122-1124.
51. Widmer A.F., Gaechter A., Ochsner P.E., Zimmerli W. Antimicrobial treatment of orthopedic implant-related infections with rifampin combinations. Clin Infect Dis 1992, 14:1251-1253.
52. Zimmerli W., Widmer A.F., Blatter M., Frei R., Ochsner P.E. Role of rifampin for treatment of orthopedic implant-related staphylococcal infections: a randomized controlled trial. JAMA 1998, 279:1537-1541. Foreign-Body Infection (FBI) Study Group.
53. Olson M.E., Slater S.R., Rupp M.E., Fey P.D. Rifampicin enhances activity of daptomycin and vancomycin against both a polysaccharide intercellular adhesin (PIA)-dependent and -independent Staphylococcus epidermidis biofilm. J. Infect. Dis. 2010, Epub ahead of print.
54. Pamp S.J., Gjermansen M., Johansen H.K., Tolker-Nielsen T. Tolerance to the antimicrobial peptide colistin in Pseudomonas aeruginosa biofilms is linked to metabolically active cells, and depends on the pmr and mexAB-oprM genes. Mol Microbiol 2008, 68:223-240.
55. Kaplan J.B. Therapeutic potential of biofilm-dispersing enzymes. Int J Artif Organs 2009, 32:545-554.
56. Qin Z., Ou Y., Yang L., Zhu Y., Tolker-Nielsen T., Molin S., Qu D. Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology 2007, 153:2083-2092.
57. Mann E.E., Rice K.C., Boles B.R., Endres J.L., Ranjit D., Chandramohan L., Tsang L.H., Smeltzer M.S., Horswill A.R., Bayles K.W. Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS One 2009, 4:e5822.
58. Shak S., Capon D.J., Hellmiss R., Marsters S.A., Baker C.L. Recombinant human DNase I reduces the viscosity of cystic fibrosis sputum. Proc Natl Acad Sci U S A 1990, 87:9188-9192.
59. Ramasubbu N., Thomas L.M., Ragunath C., Kaplan J.B. Structural analysis of dispersin B, a biofilm-releasing glycoside hydrolase from the periodontopathogen Actinobacillus actinomycetemcomitans. J Mol Biol 2005, 349:475-486.
60. Izano E.A., Amarante M.A., Kher W.B., Kaplan J.B. Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Appl Environ Microbiol 2008, 74:470-476.
61. Njoroge J., Sperandio V. Jamming bacterial communication: new approaches for the treatment of infectious diseases. EMBO Mol Med 2009, 1:201-210.
62. Novick R.P., Geisinger E. Quorum sensing in staphylococci. Annu Rev Genet 2008, 42:541-564.
63. Vuong C., Gerke C., Somerville G.A., Fischer E.R., Otto M. Quorum-sensing control of biofilm factors in Staphylococcus epidermidis. J Infect Dis 2003, 188:706-718.
64. Kong K.F., Vuong C., Otto M. Staphylococcus quorum sensing in biofilm formation and infection. Int J Med Microbiol 2006, 296:133-139.
65. Boles B.R., Horswill A.R. Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 2008, 4:e1000052.
66. Schaffer A.C., Lee J.C. Staphylococcal vaccines and immunotherapies. Infect Dis Clin North Am 2009, 23:153-171.