The biofilm matrix destabilizers, EDTA and DNaseI, enhance the susceptibility of nontypeable Hemophilus influenzae biofilms to treatment with ampicillin and ciprofloxacin

MicrobiologyOpen

Volumn 3, Issue 4, 2014, Pages 557-567

  Cavaliere, Rosalia ^a   Ball, Jessica L ^b   Turnbull, Lynne ^a   Whitchurch, Cynthia B ^a  

^a UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Antibiotic; Biofilm; Cations; eDNA; Matrix

Indexed keywords

AMPICILLIN; BARIUM; CALCIUM; CIPROFLOXACIN; DEOXYRIBONUCLEASE I; EDETIC ACID; IRON; MAGNESIUM; MANGANESE; ZINC; ANTIINFECTIVE AGENT;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL CELL; BIOFILM; BIOFILM DEVELOPMENT; BIOFILM FORMATION; BIOFILM STABILITY; CELL ADHESION; CHELATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; MATRIX ATTACHMENT REGION; MEMBRANE STABILIZATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; NONTYPEABLE HAEMOPHILUS INFLUENZAE; PRIORITY JOURNAL; TREATMENT RESPONSE; DRUG EFFECTS; HAEMOPHILUS INFECTION; HAEMOPHILUS INFLUENZAE; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; PHYSIOLOGY;

AMPICILLIN; ANTI-BACTERIAL AGENTS; BIOFILMS; CIPROFLOXACIN; DEOXYRIBONUCLEASE I; EDETIC ACID; HAEMOPHILUS INFECTIONS; HAEMOPHILUS INFLUENZAE; HUMANS; MICROBIAL SENSITIVITY TESTS;

EID: 84906084315     PISSN: None     EISSN: 20458827     Source Type: Journal    
DOI: 10.1002/mbo3.187     Document Type: Article

References (51)

1. Allesen-Holm, M., K. B. Barken, L. Yang, M. Klausen, J. S. Webb, S. Kjelleberg, et al. 2006. A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol. Microbiol. 59:1114-28.
2. Asbell, M. A., and R. G. Eagon. 1966. Role of multivalent cations in the organization, structure, and assembly of the cell wall of Pseudomonas aeruginosa. J. Bacteriol. 92:380-387.
3. Banin, E., K. M. Brady, and E. P. Greenberg. 2006. Chelator-induced dispersal and killing of Pseudomonas aeruginosa cells in a biofilm. Appl. Environ. Microbiol. 72:2064-2069.
4. de Beer, D., P. Stoodley, and Z. Lewandowski. 1997. Measurement of local diffusion coefficients in biofilms by microinjection and confocal microscopy. Biotechnol. Bioeng. 53:151-158.
5. Brown, M. R., D. G. Allison, and P. Gilbert. 1988. Resistance of bacterial biofilms to antibiotics: a growth-rate related effect? J. Antimicrob. Chemother. 22:777-780.
6. Chen, X., and P. S. Stewart. 2002. Role of electrostatic interactions in cohesion of bacterial biofilms. Appl. Microbiol. Biotechnol. 59:718-720.
7. Chiang, W. C., M. Nilsson, P. O. Jensen, N. Hoiby, T. E. Nielsen, M. Givskov, et al. 2013. Extracellular DNA shields against aminoglycosides in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 57:2352-2361.
8. Coleman, H. N., D. A. Daines, J. Jarisch, and A. L. Smith. 2003. Chemically defined media for growth of Haemophilus influenzae strains. J. Clin. Microbiol. 41:4408-4410.
9. Costerton, J. W., R. T. Irvin, and K. J. Cheng. 1981. The bacterial glycocalyx in nature and disease. Annu. Rev. Microbiol. 35:299-324.
10. Costerton, J. W., Z. Lewandowski, D. E. Caldwell, D. R. Korber, and H. M. Lappin-Scott. 1995. Microbial biofilms. Annu. Rev. Microbiol. 49:711-745.
11. Costerton, J. W., P. S. Stewart, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322.
12. Donlan, R. M., and J. W. Costerton. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15:167-193.
13. Ehrlich, G. D., R. Veeh, X. Wang, J. W. Costerton, J. D. Hayes, F. Z. Hu, et al. 2002. Mucosal biofilm formation on middle-ear mucosa in the chinchilla model of otitis media. JAMA 287:1710-1715.
14. Fux, C. A., J. W. Costerton, P. S. Stewart, and P. Stoodley. 2005. Survival strategies of infectious biofilms. Trends Microbiol. 13:34-40.
15. Geesey, G. G., B. Wigglesworth-Cooksey, and K. E. Cooksey. 2000. Influence of calcium and other cations on surface adhesion of bacteria and diatoms: a review. Biofouling 15:195-205.
16. Gray, G. W., and S. G. Wilkinson. 1965. The effect of ethylenediaminetetra-acetic acid on the cell walls of some gram-negative bacteria. J. Gen. Microbiol. 39:385-399.
17. Greiner, L. L., H. Watanabe, N. J. Phillips, J. Shao, A. Morgan, A. Zaleski, et al. 2004. Nontypeable Haemophilus influenzae strain 2019 produces a biofilm containing N-acetylneuraminic acid that may mimic sialylated O-linked glycans. Infect. Immun. 72:4249-4260.
18. Hall-Stoodley, L., F. Z. Hu, A. Gieseke, L. Nistico, D. Nguyen, J. Hayes, et al. 2006. Direct detection of bacterial biofilms on the middle-ear mucosa of children with chronic otitis media. JAMA 296:202-211.
19. Hancock, R. E. 1984. Alterations in outer membrane permeability. Annu. Rev. Microbiol. 38:237-264.
20. Hancock, R. E., and P. G. Wong. 1984. Compounds which increase the permeability of the Pseudomonas aeruginosa outer membrane. Antimicrob. Agents Chemother. 26:48-52.
21. Heydorn, A., A. T. Nielsen, M. Hentzer, C. Sternberg, M. Givskov, B. K. Ersboll, et al. 2000. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146(Pt 10):2395-2407.
22. Izano, E. A., S. M. Shah, and J. B. Kaplan. 2009. Intercellular adhesion and biocide resistance in nontypeable Haemophilus influenzae biofilms. Microb. Pathog. 46:207-213.
23. Jakubovics, N. S., R. C. Shields, N. Rajarajan, and J. G. Burgess. 2013. Life after death: the critical role of extracellular DNA in microbial biofilms. Lett. Appl. Microbiol. 57:467-475.
24. James, G. A., D. R. Korber, D. E. Caldwell, and J. W. Costerton. 1995. Digital image analysis of growth and starvation responses of a surface-colonizing Acinetobacter sp. J. Bacteriol. 177:907-915.
25. Jurcisek, J. A., and L. O. Bakaletz. 2007. Biofilms formed by nontypeable Haemophilus influenzae in vivo contain both double-stranded DNA and type IV pilin protein. J. Bacteriol. 189:3868-3875.
26. Leive, L. 1974. The barrier function of the gram-negative envelope. Ann. N. Y. Acad. Sci. 235:109-129.
27. Leive, L., and V. Kollin. 1967. Controlling EDTA treatment to produce permeable Escherichia coli with normal metabolic processes. Biochem. Biophys. Res. Commun. 28:229-236.
28. Lewenza, S. 2013. Extracellular DNA-induced antimicrobial peptide resistance mechanisms in Pseudomonas aeruginosa. Front. Microbiol. 4:21.
29. Lewis, R. E., D. J. Diekema, S. A. Messer, M. A. Pfaller, and M. E. Klepser. 2002. Comparison of Etest, chequerboard dilution and time-kill studies for the detection of synergy or antagonism between antifungal agents tested against Candida species. J. Antimicrob. Chemother. 49:345-351.
30. Marcus, H., A. Austria, and N. R. Baker. 1989. Adherence of Pseudomonas aeruginosa to tracheal epithelium. Infect. Immun. 57:1050-1053.
31. Matsukawa, M., and E. P. Greenberg. 2004. Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development. J. Bacteriol. 186:4449-4456.
32. Merino, S., R. Gavin, M. Altarriba, L. Izquierdo, M. E. Maguire, and J. M. Tomas. 2001. The MgtE Mg2 + transport protein is involved in Aeromonas hydrophila adherence. FEMS Microbiol. Lett. 198:189-195.
33. Messiaen, A. S., H. Nelis, and T. Coenye. 2014. Investigating the role of matrix components in protection of Burkholderia cepacia complex biofilms against tobramycin. J. Cyst. Fibros. 13:56-62.
34. Moriyama, S., M. Hotomi, J. Shimada, D. S. Billal, K. Fujihara, and N. Yamanaka. 2009. Formation of biofilm by Haemophilus influenzae isolated from pediatric intractable otitis media. Auris Nasus Larynx 36:525-531.
35. Mulcahy, H., L. Charron-Mazenod, and S. Lewenza. 2008. Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog. 4:e1000213.
36. Nemoto, K., K. Hirota, K. Murakami, K. Taniguti, H. Murata, D. Viducic, et al. 2003. Effect of Varidase (streptodornase) on biofilm formed by Pseudomonas aeruginosa. Chemotherapy 49:121-125.
37. Nikaido, H., and M. Vaara. 1985. Molecular basis of bacterial outer membrane permeability. Microbiol. Rev. 49:1-32.
38. Odds, F. C. 2003. Synergy, antagonism, and what the chequerboard puts between them. J. Antimicrob. Chemother. 52:1.
39. O'Toole, G., H. B. Kaplan, and R. Kolter. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:49-79.
40. Ozerdem Akpolat, N., S. Elci, S. Atmaca, H. Akbayin, and K. Gul. 2003. The effects of magnesium, calcium and EDTA on slime production by Staphylococcus epidermidis strains. Folia Microbiol. 48:649-53.
41. Raad, I., R. Hachem, R. K. Tcholakian, and R. Sherertz. 2002. Efficacy of minocycline and EDTA lock solution in preventing catheter-related bacteremia, septic phlebitis, and endocarditis in rabbits. Antimicrob. Agents Chemother. 46:327-332.
42. Slinger, R., F. Chan, W. Ferris, S. W. Yeung, M. St Denis, I. Gaboury, et al. 2006. Multiple combination antibiotic susceptibility testing of nontypeable Haemophilus influenzae biofilms. Diagn. Microbiol. Infect. Dis. 56:247-53.
43. Song, B., and L. G. Leff. 2006. Influence of magnesium ions on biofilm formation by Pseudomonas fluorescens. Microbiol. Res. 161:355-361.
44. Starner, T. D., N. Zhang, G. Kim, M. A. Apicella, P. B. McCray, Jr. 2006. Haemophilus influenzae forms biofilms on airway epithelia: implications in cystic fibrosis. Am. J. Respir. Crit. Care Med. 174:213-220.
45. Steinberger, R. E., A. R. Allen, H. G. Hansa, and P. A. Holden. 2002. Elongation correlates with nutrient deprivation in Pseudomonas aeruginosa-unsaturates biofilms. Microb. Ecol. 43:416-423.
46. Stewart, P. S. 2003. Diffusion in biofilms. J. Bacteriol. 185:1485-1491.
47. Sutherland, I. W. 2001. The biofilm matrix - an immobilized but dynamic microbial environment. Trends Microbiol. 9:222-227.
48. Swaminathan, R. 2003. Magnesium metabolism and its disorders. Clin. Biochem. Rev. 24:47-66.
49. Swords, W. E. 2012. Nontypeable Haemophilus influenzae biofilms: role in chronic airway infections. Front. Cell. Infect. Microbiol. 2:97.
50. Walters, M. C., III, F. Roe, A. Bugnicourt, M. J. Franklin, and P. S. Stewart. 2003. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob. Agents Chemother. 47:317-23.
51. Whitchurch, C. B., T. Tolker-Nielsen, P. C. Ragas, and J. S. Mattick. 2002. Extracellular DNA required for bacterial biofilm formation. Science 295:1487.