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.

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2016-01-01
2021-10-28
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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 Microbiol 41:120–125 [View Article][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 Chemother 44:1818–1824 [View Article][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 Microbiol 63:1167–1173 [View Article][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 Biol 2:0008 [View Article][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 Res 28:235–242 [View Article][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 Microbiol 6:17–27 [View Article][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 Chemother 67:1159–1162 [View Article][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 Chemother 68:126–130 [View Article][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 Sci 4:1088–1099 [View Article][PubMed]
    [Google Scholar]
  11. Costerton J. W., Lewandowski Z., Caldwell D. E., Korber D. R., Lappin-Scott H. M. 1995; Microbial biofilms. Annu Rev Microbiol 49:711–745 [View Article][PubMed]
    [Google Scholar]
  12. Costerton J. W., Stewart P. S., Greenberg E. P. 1999; Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322 [View Article][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 Med 340:1–8 [View Article][PubMed]
    [Google Scholar]
  14. Davies D. 2003; Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov 2:114–122 [View Article][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. Science 280:295–298 [View Article][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 Chemother 45:1417–1421 [View Article][PubMed]
    [Google Scholar]
  17. Donlan R. M., Costerton J. W. 2002; Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193 [View Article][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 Surg 203:481–489 [View Article][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 Immun 18:330–337[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 Chemother 25:585–591 [View Article][PubMed]
    [Google Scholar]
  21. Fleisch H. 2002; Development of bisphosphonates. Breast Cancer Res 4:30–34 [View Article][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. JAMA 261:878–883 [View Article][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 Chem 47:1739–1749 [View Article][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 Res 12:1358–1367 [View Article][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 Bacteriol 171:5654–5658[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 Biochem 137:395–400 [View Article][PubMed]
    [Google Scholar]
  27. Fux C. A., Costerton J. W., Stewart P. S., Stoodley P. 2005; Survival strategies of infectious biofilms. Trends Microbiol 13:34–40 [View Article][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 pp 571–607 Edited by Walker J. M. Totowa, NJ: Humana Press; [View Article]
    [Google Scholar]
  29. Goede A., Dunkel M., Mester N., Frommel C., Preissner R. 2005; SuperDrug: a conformational drug database. Bioinformatics 21:1751–1753 [View Article][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 Infect 54:82–88 [View Article][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 Chem 47:1750–1759 [View Article][PubMed]
    [Google Scholar]
  32. Hall B. G. 2004; Predicting the evolution of antibiotic resistance genes. Nat Rev Microbiol 2:430–435 [View Article][PubMed]
    [Google Scholar]
  33. Huang B., Schroeder M. 2006; ligsitecsc : predicting ligand binding sites using the Connolly surface and degree of conservation. BMC Struct Biol 6:19 [View Article][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 Bacteriol 184:290–301 [View Article][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 Immun 54:13–20[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 Chemother 43:2990–2995[PubMed]
    [Google Scholar]
  37. Kohler-Ockmore J., Feneley R. C. L. 1996; Long-term catheterization of the bladder: prevalence and morbidity. Br J Urol 77:347–351 [View Article][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 Chem 275:13683–13689 [View Article][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 Res 37:D205–D210 [View Article][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 Chem 30:2785–2791 [View Article][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 Proteomics 3:608–614 [View Article][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 Biol 270:496–510 [View Article][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 Chem 25:1605–1612 [View Article][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 Microbiol 16:1157–1169 [View Article][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 Microbiol 193:711–722 [View Article][PubMed]
    [Google Scholar]
  46. Reszka A. A., Rodan G. A. 2003; Mechanism of action of bisphosphonates. Curr Osteoporos Rep 1:45–52 [View Article][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 Bioeng 103:575–577 [View Article][PubMed]
    [Google Scholar]
  48. Schembri M. A., Kjaergaard K., Klemm P. 2003; Global gene expression in Escherichia coli biofilms. Mol Microbiol 48:253–267 [View Article][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 Spectrom 14:460–470 [View Article][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. Biochemistry 40:9460–9468 [View Article][PubMed]
    [Google Scholar]
  51. Stewart P. S. 1996; Theoretical aspects of antibiotic diffusion into microbial biofilms. Antimicrob Agents Chemother 40:2517–2522[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. Urology 61:1059–1062 [View Article][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 Epidemiol 28:92–94 [View Article][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 Res 14:722–729 [View Article][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. Bone 33:805–811 [View Article][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. Electrophoresis 18:403–408 [View Article][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 Microbiol 57:1135–1140 [View Article][PubMed]
    [Google Scholar]
  58. Wilson M. 1996; Susceptibility of oral bacterial biofilms to antimicrobial agents. J Med Microbiol 44:79–87 [View Article][PubMed]
    [Google Scholar]
  59. Yang L., Givskov M. 2015; Chemical biology strategies for biofilm control. Microbiol Spectr 3: MB-0019-2015. [View Article][PubMed]
    [Google Scholar]
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