Table of Contents Author Guidelines Submit a Manuscript
Infectious Diseases in Obstetrics and Gynecology
Volume 2018, Article ID 1426109, 9 pages
https://doi.org/10.1155/2018/1426109
Research Article

Benzoyl Peroxide Inhibits Quorum Sensing and Biofilm Formation by Gardnerella vaginalis 14018

1Department of Biochemistry and Microbiology, Rutgers State University, New Brunswick, NJ, USA
2Department of Biology and Biotechnology, College of Sciences, Diyala University, Baqubah, Iraq
3Department of Life Sciences and Technology, Beuth University of Applied Sciences, Berlin, Germany
4Health Promoting Natural Laboratory, School of Environmental and Biological Sciences, Rutgers State University, New Brunswick, NJ, USA
5Scientelle, LLC, Morristown, NJ 07960, USA

Correspondence should be addressed to Michael L. Chikindas; ude.sregtur.posea@sadnikihct

Received 5 December 2017; Revised 12 March 2018; Accepted 23 May 2018; Published 2 July 2018

Academic Editor: Bryan Larsen

Copyright © 2018 Ammar Algburi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Centers for Disease Control and Prevention (CDC), “Sexually Transmitted Diseases Treatment Guidelines,” MMWR, 64(RR-3), 2015.
  2. R. H. Beigi, M. N. Austin, L. A. Meyn, M. A. Krohn, and S. L. Hillier, “Antimicrobial resistance associated with the treatment of bacterial vaginosis,” American Journal of Obstetrics & Gynecology, vol. 191, no. 4, pp. 1124–1129, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. D. Machado, J. Castro, A. Palmeira-de-Oliveira, J. Martinez-de-Oliveira, and N. Cerca, “Bacterial vaginosis biofilms: Challenges to current therapies and emerging solutions,” Frontiers in Microbiology, vol. 6, article 1528, 2016. View at Google Scholar · View at Scopus
  4. J. J. Schellenberg, M. H. Patterson, and J. E. Hill, “Gardnerella vaginalis diversity and ecology in relation to vaginal symptoms,” Research in Microbiology, vol. 168, no. 9-10, pp. 837–844, 2017. View at Publisher · View at Google Scholar · View at Scopus
  5. C. A. Muzny and J. R. Schwebke, “Biofilms: an underappreciated mechanism of treatment failure and recurrence in vaginal infections,” Clinical Infectious Diseases, vol. 61, no. 4, pp. 601–606, 2015. View at Publisher · View at Google Scholar · View at Scopus
  6. L. Hardy, N. Cerca, V. Jespers, M. Vaneechoutte, and T. Crucitti, “Bacterial biofilms in the vagina,” Research in Microbiology, vol. 168, pp. 859–864, 2017. View at Google Scholar · View at Scopus
  7. A. Algburi, N. Comito, D. Kashtanov, L. M. T. Dicks, and M. L. Chikindas, “Control of biofilm formation: Antibiotics and beyond,” Applied and Environmental Microbiology, vol. 83, no. 3, Article ID e02508-16, 2017. View at Publisher · View at Google Scholar · View at Scopus
  8. V. Monnet and R. Gardan, “Quorum-sensing regulators in Gram-positive bacteria: 'cherchez le peptide',” Molecular Microbiology, vol. 97, no. 2, pp. 181–184, 2015. View at Publisher · View at Google Scholar · View at Scopus
  9. K. Papenfort and B. L. Bassler, “Quorum sensing signal-response systems in Gram-negative bacteria,” Nature Reviews Microbiology, vol. 14, no. 9, pp. 576–588, 2016. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Swidsinski, W. Mendling, V. Loening-Baucke et al., “An adherent Gardnerella vaginalis biofilm persists on the vaginal epithelium after standard therapy with oral metronidazole,” American Journal of Obstetrics & Gynecology, vol. 198, no. 1, pp. 97.e1–97.e6, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. G. F. Kaufmann, J. Park, and K. D. Janda, “Bacterial quorum sensing: a new target for anti-infective immunotherapy,” Expert Opinion on Biological Therapy, vol. 8, no. 6, pp. 719–724, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Algburi, S. Zehm, V. Netrebov, A. B. Bren, V. Chistyakov, and M. L. Chikindas, “Subtilosin Prevents Biofilm Formation by Inhibiting Bacterial Quorum Sensing,” Probiotics and Antimicrobial Proteins, vol. 9, no. 1, pp. 81–90, 2017. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Whiteley, S. P. Diggle, and E. P. Greenberg, “Progress in and promise of bacterial quorum sensing research,” Nature, vol. 551, no. 7680, pp. 313–320, 2017. View at Publisher · View at Google Scholar · View at Scopus
  14. “WHO Model List of Essential Medicines,” World Health Organization, October 2013.
  15. L. Hegemann, S. M. Toso, K. Kitay, and C. F. Webster, “Anti‐inflammatory actions of benzoyl peroxide: effects on the generation of reactive oxygen species by leucocytes and the activity of protein kinase C and calmodulin,” British Journal of Dermatology, vol. 130, no. 5, pp. 569–575, 1994. View at Publisher · View at Google Scholar · View at Scopus
  16. E. Muller, J. Al-Attar, A. G. Wolff, and B. F. Farber, “Mechanism of salicylate-mediated inhibition of biofilm in Staphylococcus epidermidis,” The Journal of Infectious Diseases, vol. 177, no. 2, pp. 501–503, 1998. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Yang, M. T. Rybtke, T. H. Jakobsen et al., “Computer-aided identification of recognized drugs as Pseudomonas aeruginosa quorum-sensing inhibitors,” Antimicrobial Agents and Chemotherapy, vol. 53, no. 6, pp. 2432–2443, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. P. J. Nowatzki, R. R. Koepsel, P. Stoodley et al., “Salicylic acid-releasing polyurethane acrylate polymers as anti-biofilm urological catheter coatings,” Acta Biomaterialia, vol. 8, no. 5, pp. 1869–1880, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. M. B. K. Bandara, H. Zhu, P. R. Sankaridurg, and M. D. P. Willcox, “Salicylic acid reduces the production of several potential virulence factors of Pseudomonas aeruginosa associated with microbial keratitis,” Investigative Ophthalmology & Visual Science, vol. 47, no. 10, pp. 4453–4460, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. B. Prithiviraj, H. P. Bais, T. Weir et al., “Down regulation of virulence factors of Pseudomonas aeruginosa by salicylic acid attenuates its virulence on Arabidopsis thaliana and Caenorhabditis elegans,” Infection and Immunity, vol. 73, no. 9, pp. 5319–5328, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Chow, K. Gu, L. Jiang, and A. Nassour, “Salicylic acid affects swimming, twitching and swarming motility in Pseudomonas aeruginosa, resulting in decreased biofilm formation,” Journal of Experimental Microbiology and Immunology, vol. 15, pp. 22–29, 2011. View at Google Scholar
  22. S. Wattanavanitchakorn, C. Prakitchaiwattana, and P. Thamyongkit, “Rapid and simple colorimetric method for the quantification of AI-2 produced from Salmonella Typhimurium,” Journal of Microbiological Methods, vol. 99, no. 1, pp. 15–21, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Algburi, A. Volski, and M. L. Chikindas, “Natural antimicrobials subtilosin and lauramide arginine ethyl ester synergize with conventional antibiotics clindamycin and metronidazole against biofilms of Gardnerella vaginalis but not against biofilms of healthy vaginal lactobacilli,” Pathogens and Disease, vol. 73, no. 5, Article ID ftv018, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. G. A. O'Toole, “Microtiter dish Biofilm formation assay,” Journal of Visualized Experiments, vol. 47, article 2437, 2011. View at Google Scholar · View at Scopus
  25. M. K. Borucki, J. D. Peppin, D. White, F. Loge, and D. R. Call, “Variation in biofilm formation among strains of Listeria monocytogenes,” Applied and Environmental Microbiology, vol. 69, no. 12, pp. 7336–7342, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. Y. Kim, J. W. Lee, S.-G. Kang, S. Oh, and M. W. Griffiths, “Bifidobacterium spp. Influences the production of autoinducer-2 and biofilm formation by Escherichia coli O157: H7,” Anaerobe, vol. 18, no. 5, pp. 539–545, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. J. L. Patterson, A. Stull-Lane, P. H. Girerd, and K. K. Jefferson, “Analysis of adherence, biofilm formation and cytotoxicity suggests a greater virulence potential of Gardnerella vaginalis relative to other bacterial-vaginosis-associated anaerobes,” Microbiology, vol. 156, no. 2, pp. 392–399, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Machado and N. Cerca, “Influence of biofilm formation by gardnerella vaginalis and other anaerobes on bacterial vaginosis,” The Journal of Infectious Diseases, vol. 212, no. 12, pp. 1856–1861, 2015. View at Publisher · View at Google Scholar · View at Scopus
  29. P. Alves, J. Castro, C. Sousa, T. B. Cereija, and N. Cerca, “Gardnerella vaginalis Outcompetes 29 other bacterial species isolated from patients with bacterial vaginosis, using in an in vitro biofilm formation model,” The Journal of Infectious Diseases, vol. 210, no. 4, pp. 593–596, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. J. L. Patterson, P. H. Girerd, N. W. Karjane, and K. K. Jefferson, “Effect of biofilm phenotype on resistance of Gardnerella vaginalis to hydrogen peroxide and lactic acid,” American Journal of Obstetrics & Gynecology, vol. 197, no. 2, pp. 170–e7, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. L. Rosenberg, A. Carbone, U. Römling, K. Uhrich, and M. Chikindas, “Salicylic acid-based poly(anhydride esters) for control of biofilm formation in Salmonella enterica serovar Typhimurium,” Letters in Applied Microbiology, vol. 46, no. 5, pp. 593–599, 2008. View at Publisher · View at Google Scholar
  32. J. D. Bryers, R. A. Jarvis, J. Lebo, A. Prudencio, T. R. Kyriakides, and K. Uhrich, “Biodegradation of poly(anhydride-esters) into non-steroidal anti-inflammatory drugs and their effect on Pseudomonas aeruginosa biofilms in vitro and on the foreign-body response in vivo,” Biomaterials, vol. 27, no. 29, pp. 5039–5048, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. S. J. Pamp and T. Tolker-Nielsen, “Multiple roles of biosurfactants in structural biofilm development by Pseudomonas aeruginosa,” Journal of Bacteriology, vol. 189, no. 6, pp. 2531–2539, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. C.-Y. Chang, T. Krishnan, H. Wang et al., “Non-antibiotic quorum sensing inhibitors acting against N-acyl homoserine lactone synthase as druggable target,” Scientific Reports, vol. 4, article no. 7245, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. T. Coenye, E. Peeters, and H. J. Nelis, “Biofilm formation by Propionibacterium acnes is associated with increased resistance to antimicrobial agents and increased production of putative virulence factors,” Research in Microbiology, vol. 158, no. 4, pp. 386–392, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. A. G. Nusbaum, R. S. Kirsner, and C. A. Charles, “Biofilms in dermatology.,” Skin Therapy Letter, vol. 17, no. 7, pp. 1–5, 2012. View at Google Scholar · View at Scopus
  37. A. M. Layton, “Disorders of the sebaceous glands,” in Rook's Textbook of Dermatology. Thorough overview of acne pathogenesis, epidemiology and management, D. A. Burns, S. M. Breathnach, N. H. Cox, and C. Griffiths, Eds., pp. 42.1–42.89, Wiley, Oxford, UK, 2010. View at Google Scholar
  38. M. Ozolins, E. A. Eady, A. Avery et al., “Randomised controlled multiple treatment comparison to provide a cost-effectiveness rationale for the selection of antimicrobial therapy in acne,” Health Technology Assessment, vol. 9, no. 1, 2005. View at Google Scholar · View at Scopus
  39. S. Xu, V. L. Cavera, M. A. Rogers, Q. Huang, K. Zubovskiy, and M. L. Chikindas, “Benzoyl peroxide formulated polycarbophil/carbopol 934P hydrogel with selective antimicrobial activity, potentially beneficial for treatment and prevention of bacterial vaginosis,” Infectious Diseases in Obstetrics and Gynecology, vol. 2013, Article ID 909354, 10 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. R. A. Bojar, W. J. Cunliffe, and K. T. Holland, “The short‐term treatment of acne vulgaris with benzoyl peroxide: effects on the surface and follicular cutaneous microflora,” British Journal of Dermatology, vol. 132, no. 2, pp. 204–208, 1995. View at Publisher · View at Google Scholar · View at Scopus
  41. J. H. Cove and K. T. Holland, “The effect of benzoyl peroxide on cutaneous micro‐organisms in vitro,” Journal of Applied Bacteriology, vol. 54, no. 3, pp. 379–382, 1983. View at Publisher · View at Google Scholar · View at Scopus
  42. L. Nachin, L. Loiseau, D. Expert, and F. Barras, “SufC: An unorthodox cytoplasmic ABC/ATPase required for [Fe-S] biogenesis under oxidative stress,” EMBO Journal, vol. 22, no. 3, pp. 427–437, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. Z. Lou, Y. Tang, X. Song, and H. Wang, “Metabolomics-based screening of biofilm-inhibitory compounds against pseudomonas aeruginosa from burdock leaf,” Molecules, vol. 20, no. 9, pp. 16266–16277, 2015. View at Publisher · View at Google Scholar · View at Scopus
  44. D. Kuczyńska-Wiśnik, E. Matuszewska, B. Furmanek-Blaszk et al., “Antibiotics promoting oxidative stress inhibit formation of Escherichia coli biofilm via indole signalling,” Research in Microbiology, vol. 161, no. 10, pp. 847–853, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. J. M. Rothfork, G. S. Timmins, M. N. Harris et al., “Inactivation of a bacterial virulence pheromone by phagocyte-derived oxidants: New role for the NADPH oxidase in host defense,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 101, no. 38, pp. 13867–13872, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Zhu, E. Dizin, X. Hu, A.-S. Wavreille, J. Park, and D. Pei, “S-ribosylhomocysteinase (LuxS) is a mononuclear iron protein,” Biochemistry, vol. 42, no. 16, pp. 4717–4726, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. J. A. Imlay, “The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium,” Nature Reviews Microbiology, vol. 11, no. 7, pp. 443–454, 2013. View at Publisher · View at Google Scholar · View at Scopus