1887

Abstract

null mutants have been reported in the literature to be impaired in biofilm formation. To develop biofilm-inhibiting agents for prevention and control of adherent behaviour, analogues of a natural Cra ligand, fructose-1,6-bisphosphate, were identified based on two-dimensional similarity to the natural ligand. Of the analogues identified, those belonging to the bisphosphonate class of drug molecules were selected for study, as these are approved for clinical use in humans and their safety has been established. Computational and studies with purified Cra protein showed that risedronate sodium interacted with residues in the fructose-1,6-bisphosphate-binding site. Using a quantitative biofilm assay, risedronate sodium, at a concentration of 300–400 μM, was found to decrease and biofilm formation by >60 %. Risedronate drastically reduced the adherence of cells to a rubber Foley urinary catheter, demonstrating its utility in preventing the formation of biofilm communities on medical implant surfaces. The use of risedronate, either alone or in combination with other agents, to prevent the formation of biofilms on surfaces is a novel finding that can easily be translated into practical applications.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000193
2016-01-01
2020-01-22
Loading full text...

Full text loading...

/deliver/fulltext/jmm/65/1/9.html?itemId=/content/journal/jmm/10.1099/jmm.0.000193&mimeType=html&fmt=ahah

References

  1. Ahearn D. G., Grace D. T., Jennings M. J., Borazjani R. N., Boles K. J., Rose L. J., Simmons R. B., Ahanotu E. N.. 2000; Effects of hydrogel/silver coatings on in vitro adhesion to catheters of bacteria associated with urinary tract infections. Curr Microbiol41:120–125 [CrossRef][PubMed]
    [Google Scholar]
  2. Anderl J. N., Franklin M. J., Stewart P. S.. 2000; Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother44:1818–1824 [CrossRef][PubMed]
    [Google Scholar]
  3. Azevedo M. M., Ramalho P., Silva A. P., Teixeira-Santos R., Pina-Vaz C., Rodrigues A. G.. 2014; Polyethyleneimine and polyethyleneimine-based nanoparticles: novel bacterial and yeast biofilm inhibitors. J Med Microbiol63:1167–1173 [CrossRef][PubMed]
    [Google Scholar]
  4. Baba T., Ara T., Hasegawa M., Takai Y., Okumura Y., Baba M., Datsenko K. A., Tomita M., Wanner B. L., Mori H.. 2006; Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol2:0008 [CrossRef][PubMed]
    [Google Scholar]
  5. Berman H. M., Westbrook J., Feng Z., Gilliland G., Bhat T. N., Weissig H., Shindyalov I. N., Bourne P. E.. 2000; The Protein Data Bank. Nucleic Acids Res28:235–242 [CrossRef][PubMed]
    [Google Scholar]
  6. Cegelski L., Marshall G. R., Eldridge G. R., Hultgren S. J.. 2008; The biology and future prospects of antivirulence therapies. Nat Rev Microbiol6:17–27 [CrossRef][PubMed]
    [Google Scholar]
  7. Chang C., Evdokimova E., Kagan O., Savchenko A., Edwards A. M., Joachimiak A.. 2006; Crystal structure of N-terminal truncated DNA-binding transcriptional dual regulator from Escherichia coli K12. RCSB Protein Data Bank. http://www.rcsb.org/pdb/explore.do?structureId = 2iks.
  8. Cobrado L., Azevedo M. M., Silva-Dias A., Ramos J. P., Pina-Vaz C., Rodrigues A. G.. 2012; Cerium, chitosan and hamamelitannin as novel biofilm inhibitors?. J Antimicrob Chemother67:1159–1162 [CrossRef][PubMed]
    [Google Scholar]
  9. Cobrado L., Silva-Dias A., Azevedo M. M., Pina-Vaz C., Rodrigues A. G.. 2013; In vivo antibiofilm effect of cerium, chitosan and hamamelitannin against usual agents of catheter-related bloodstream infections. J Antimicrob Chemother68:126–130 [CrossRef][PubMed]
    [Google Scholar]
  10. Cohen S. L., Chait B. T., Ferré-D'Amaré A. R., Burley S. K.. 1995; Probing the solution structure of the DNA-binding protein Max by a combination of proteolysis and mass spectrometry. Protein Sci4:1088–1099 [CrossRef][PubMed]
    [Google Scholar]
  11. Costerton J. W., Lewandowski Z., Caldwell D. E., Korber D. R., Lappin-Scott H. M.. 1995; Microbial biofilms. Annu Rev Microbiol49:711–745 [CrossRef][PubMed]
    [Google Scholar]
  12. Costerton J. W., Stewart P. S., Greenberg E. P.. 1999; Bacterial biofilms: a common cause of persistent infections. Science284:1318–1322 [CrossRef][PubMed]
    [Google Scholar]
  13. Darouiche R. O., Raad I. I., Heard S. O., Thornby J. I., Wenker O. C., Gabrielli A., Berg J., Khardori N., Hanna H., other authors. 1999; A comparison of two antimicrobial-impregnated central venous catheters. N Engl J Med340:1–8 [CrossRef][PubMed]
    [Google Scholar]
  14. Davies D.. 2003; Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov2:114–122 [CrossRef][PubMed]
    [Google Scholar]
  15. Davies D. G., Parsek M. R., Pearson J. P., Iglewski B. H., Costerton J. W., Greenberg E. P.. 1998; The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science280:295–298 [CrossRef][PubMed]
    [Google Scholar]
  16. Domenico P., Baldassarri L., Schoch P. E., Kaehler K., Sasatsu M., Cunha B. A.. 2001; Activities of bismuth thiols against staphylococci and staphylococcal biofilms. Antimicrob Agents Chemother45:1417–1421 [CrossRef][PubMed]
    [Google Scholar]
  17. Donlan R. M., Costerton J. W.. 2002; Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev15:167–193 [CrossRef][PubMed]
    [Google Scholar]
  18. Edmiston C. E., Seabrook G. R., Goheen M. P., Krepel C. J., Johnson C. P., Lewis B. D., Brown K. R., Towne J. B.. 2006; Bacterial adherence to surgical sutures: can antibacterial-coated sutures reduce the risk of microbial contamination?. J Am Coll Surg203:481–489 [CrossRef][PubMed]
    [Google Scholar]
  19. Evans D. G., Evans D. J. Jr, Tjoa W.. 1977; Hemagglutination of human group A erythrocytes by enterotoxigenic Escherichia coli isolated from adults with diarrhea: correlation with colonization factor. Infect Immun18:330–337[PubMed]
    [Google Scholar]
  20. Evans D. J., Brown M. R. W., Allison D. G., Gilbert P.. 1990; Susceptibility of bacterial biofilms to tobramycin: role of specific growth rate and phase in the division cycle. J Antimicrob Chemother25:585–591 [CrossRef][PubMed]
    [Google Scholar]
  21. Fleisch H.. 2002; Development of bisphosphonates. Breast Cancer Res4:30–34 [CrossRef][PubMed]
    [Google Scholar]
  22. Flowers R. H. III, Schwenzer K. J., Kopel R. F., Fisch M. J., Tucker S. I., Farr B. M.. 1989; Efficacy of an attachable subcutaneous cuff for the prevention of intravascular catheter-related infection. A randomized, controlled trial. JAMA261:878–883 [CrossRef][PubMed]
    [Google Scholar]
  23. Friesner R. A., Banks J. L., Murphy R. B., Halgren T. A., Klicic J. J., Mainz D. T., Repasky M. P., Knoll E. H., Shelley M., other authors. 2004; Glide: a new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. J Med Chem47:1739–1749 [CrossRef][PubMed]
    [Google Scholar]
  24. Frith J. C., Mönkkönen J., Blackburn G. M., Russell R. G., Rogers M. J.. 1997; Clodronate and liposome-encapsulated clodronate are metabolized to a toxic ATP analog, adenosine 5′-(β,γ-dichloromethylene) triphosphate, by mammalian cells in vitro. J Bone Miner Res12:1358–1367 [CrossRef][PubMed]
    [Google Scholar]
  25. Fujisaki S., Nishino T., Katsuki H., Hara H., Nishimura Y., Hirota Y.. 1989; Isolation and characterization of an Escherichia coli mutant having temperature-sensitive farnesyl diphosphate synthase. J Bacteriol171:5654–5658[PubMed]
    [Google Scholar]
  26. Fujisaki S., Takahashi I., Hara H., Horiuchi K., Nishino T., Nishimura Y.. 2005; Disruption of the structural gene for farnesyl diphosphate synthase in Escherichia coli. J Biochem137:395–400 [CrossRef][PubMed]
    [Google Scholar]
  27. Fux C. A., Costerton J. W., Stewart P. S., Stoodley P.. 2005; Survival strategies of infectious biofilms. Trends Microbiol13:34–40 [CrossRef][PubMed]
    [Google Scholar]
  28. Gasteiger E., Hoogland C., Gattiker A., Duvaud S., Wilkins M. R., Appel R. D., Bairoch A.. 2005; Protein identification and analysis tools on the ExPASy server. In The Proteomics Protocols Hand-book pp571–607 Edited by Walker J. M.. Totowa, NJ: Humana Press; [CrossRef]
    [Google Scholar]
  29. Goede A., Dunkel M., Mester N., Frommel C., Preissner R.. 2005; SuperDrug: a conformational drug database. Bioinformatics21:1751–1753 [CrossRef][PubMed]
    [Google Scholar]
  30. Gómez-Alonso A., García-Criado F. J., Parreño-Manchado F. C., García-Sánchez J. E., García-Sánchez E., Parreño-Manchado A., Zambrano-Cuadrado Y.. 2007; Study of the efficacy of Coated VICRYL Plus Antibacterial suture (coated Polyglactin 910 suture with Triclosan) in two animal models of general surgery. J Infect54:82–88 [CrossRef][PubMed]
    [Google Scholar]
  31. Halgren T. A., Murphy R. B., Friesner R. A., Beard H. S., Frye L. L., Pollard W. T., Banks J. L.. 2004; Glide: a new approach for rapid, accurate docking and scoring. 2.Enrichment factors in database screening. J Med Chem47:1750–1759 [CrossRef][PubMed]
    [Google Scholar]
  32. Hall B. G.. 2004; Predicting the evolution of antibiotic resistance genes. Nat Rev Microbiol2:430–435 [CrossRef][PubMed]
    [Google Scholar]
  33. Huang B., Schroeder M.. 2006; ligsitecsc : predicting ligand binding sites using the Connolly surface and degree of conservation. BMC Struct Biol6:19 [CrossRef][PubMed]
    [Google Scholar]
  34. Jackson D. W., Suzuki K., Oakford L., Simecka J. W., Hart M. E., Romeo T.. 2002; Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J Bacteriol184:290–301 [CrossRef][PubMed]
    [Google Scholar]
  35. Johnson G. M., Lee D. A., Regelmann W. E., Gray E. D., Peters G., Quie P. G.. 1986; Interference with granulocyte function by Staphylococcus epidermidis slime. Infect Immun54:13–20[PubMed]
    [Google Scholar]
  36. Johnson J. R., Delavari P., Azar M.. 1999; Activities of a nitrofurazone-containing urinary catheter and a silver hydrogel catheter against multidrug-resistant bacteria characteristic of catheter-associated urinary tract infection. Antimicrob Agents Chemother43:2990–2995[PubMed]
    [Google Scholar]
  37. Kohler-Ockmore J., Feneley R. C. L.. 1996; Long-term catheterization of the bladder: prevalence and morbidity. Br J Urol77:347–351 [CrossRef][PubMed]
    [Google Scholar]
  38. Leite J. F., Amoscato A. A., Cascio M.. 2000; Coupled proteolytic and mass spectrometry studies indicate a novel topology for the glycine receptor. J Biol Chem275:13683–13689 [CrossRef][PubMed]
    [Google Scholar]
  39. Marchler-Bauer A., Anderson J. B., Chitsaz F., Derbyshire M. K., DeWeese-Scott C., Fong J. H., Geer L. Y., Geer R. C., Gonzales N. R., other authors. 2009; CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res37:D205–D210 [CrossRef][PubMed]
    [Google Scholar]
  40. Morris G. M., Huey R., Lindstrom W., Sanner M. F., Belew R. K., Goodsell D. S., Olson A. J.. 2009; AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. J Comput Chem30:2785–2791 [CrossRef][PubMed]
    [Google Scholar]
  41. Olsen J. V., Ong S.-E., Mann M.. 2004; Trypsin cleaves exclusively C-terminal to arginine and lysine residues. Mol Cell Proteomics3:608–614 [CrossRef][PubMed]
    [Google Scholar]
  42. Penin F., Geourjon C., Montserret R., Böckmann A., Lesage A., Yang Y. S., Bonod-Bidaud C., Cortay J. C., Nègre D., other authors. 1997; Three-dimensional structure of the DNA-binding domain of the fructose repressor from Escherichia coli by 1H and 15N NMR. J Mol Biol270:496–510 [CrossRef][PubMed]
    [Google Scholar]
  43. Pettersen E. F., Goddard T. D., Huang C. C., Couch G. S., Greenblatt D. M., Meng E. C., Ferrin T. E.. 2004; UCSF Chimera – a visualization system for exploratory research and analysis. J Comput Chem25:1605–1612 [CrossRef][PubMed]
    [Google Scholar]
  44. Ramseier T. M., Bledig S., Michotey V., Feghali R., Saier M.H., Jr. 1995; The global regulatory protein FruR modulates the direction of carbon flow in Escherichia coli. Mol Microbiol16:1157–1169 [CrossRef][PubMed]
    [Google Scholar]
  45. Reshamwala S. M. S., Noronha S. B.. 2011; Biofilm formation in Escherichia coli cra mutants is impaired due to down-regulation of curli biosynthesis. Arch Microbiol193:711–722 [CrossRef][PubMed]
    [Google Scholar]
  46. Reszka A. A., Rodan G. A.. 2003; Mechanism of action of bisphosphonates. Curr Osteoporos Rep1:45–52 [CrossRef][PubMed]
    [Google Scholar]
  47. Saito K., Fujisaki S., Nishino T.. 2007; Short-chain prenyl diphosphate synthase that condenses isopentenyl diphosphate with dimethylallyl diphosphate in ispA null Escherichia coli strain lacking farnesyl diphosphate synthase. J Biosci Bioeng103:575–577 [CrossRef][PubMed]
    [Google Scholar]
  48. Schembri M. A., Kjaergaard K., Klemm P.. 2003; Global gene expression in Escherichia coli biofilms. Mol Microbiol48:253–267 [CrossRef][PubMed]
    [Google Scholar]
  49. Shields S. J., Oyeyemi O., Lightstone F. C., Balhorn R.. 2003; Mass spectrometry and non-covalent protein-ligand complexes: confirmation of binding sites and changes in tertiary structure. J Am Soc Mass Spectrom14:460–470 [CrossRef][PubMed]
    [Google Scholar]
  50. Spolaore B., Bermejo R., Zambonin M., Fontana A.. 2001; Protein interactions leading to conformational changes monitored by limited proteolysis: apo form and fragments of horse cytochrome c. Biochemistry40:9460–9468 [CrossRef][PubMed]
    [Google Scholar]
  51. Stewart P. S.. 1996; Theoretical aspects of antibiotic diffusion into microbial biofilms. Antimicrob Agents Chemother40:2517–2522[PubMed]
    [Google Scholar]
  52. Trautner B. W., Hull R. A., Darouiche R. O.. 2003; Escherichia coli 83972 inhibits catheter adherence by a broad spectrum of uropathogens. Urology61:1059–1062 [CrossRef][PubMed]
    [Google Scholar]
  53. Trautner B. W., Hull R. A., Thornby J. I., Darouiche R. O.. 2007; Coating urinary catheters with an avirulent strain of Escherichia coli as a means to establish asymptomatic colonization. Infect Control Hosp Epidemiol28:92–94 [CrossRef][PubMed]
    [Google Scholar]
  54. van Beek E., Löwik C., van der Pluijm G., Papapoulos S.. 1999; The role of geranylgeranylation in bone resorption and its suppression by bisphosphonates in fetal bone explants in vitro: a clue to the mechanism of action of nitrogen-containing bisphosphonates. J Bone Miner Res14:722–729 [CrossRef][PubMed]
    [Google Scholar]
  55. van Beek E. R., Cohen L. H., Leroy I. M., Ebetino F. H., Löwik C. W., Papapoulos S. E.. 2003; Differentiating the mechanisms of antiresorptive action of nitrogen containing bisphosphonates. Bone33:805–811 [CrossRef][PubMed]
    [Google Scholar]
  56. Wilkins M. R., Lindskog I., Gasteiger E., Bairoch A., Sanchez J.-C., Hochstrasser D. F., Appel R. D.. 1997; Detailed peptide characterization using peptidemass – a World-Wide-Web-accessible tool. Electrophoresis18:403–408 [CrossRef][PubMed]
    [Google Scholar]
  57. Williams G. J., Stickler D. J.. 2008; Effect of triclosan on the formation of crystalline biofilms by mixed communities of urinary tract pathogens on urinary catheters. J Med Microbiol57:1135–1140 [CrossRef][PubMed]
    [Google Scholar]
  58. Wilson M.. 1996; Susceptibility of oral bacterial biofilms to antimicrobial agents. J Med Microbiol44:79–87 [CrossRef][PubMed]
    [Google Scholar]
  59. Yang L., Givskov M.. 2015; Chemical biology strategies for biofilm control. Microbiol Spectr3: MB-0019-2015. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000193
Loading
/content/journal/jmm/10.1099/jmm.0.000193
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error