Table of Contents Author Guidelines Submit a Manuscript
Journal of Nanomaterials
Volume 2016, Article ID 9605906, 11 pages
http://dx.doi.org/10.1155/2016/9605906
Research Article

Antibacterial Activity of Partially Oxidized Ag/Au Nanoparticles against the Oral Pathogen Porphyromonas gingivalis W83

1Division of Biochemistry, Loma Linda University School of Medicine, Loma Linda, CA 92350, USA
2Northern Caribbean University, Manchester, Jamaica
3Division of Microbiology and Molecular Genetics, Loma Linda University School of Medicine, Loma Linda, CA 92350, USA
4Department of Earth and Biological Sciences, Loma Linda University School of Medicine, Loma Linda, CA 92350, USA
5College of Arts and Sciences, Faulkner University, Montgomery, AL 36109, USA

Received 24 September 2015; Accepted 26 January 2016

Academic Editor: Nay Ming Huang

Copyright © 2016 Megan S. Holden 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. S. Srinivasan, P. T. Kumar, S. V. Nair, S. V. Nair, K. P. Chennazhi, and R. Jayakumar, “Antibacterial and bioactive α- and β-chitin hydrogel/nanobioactive glass ceramic/nano silver composite scaffolds for periodontal regeneration,” Journal of Biomedical Nanotechnology, vol. 9, no. 11, pp. 1803–1816, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Pal, Y. K. Tak, and J. M. Song, “Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the gram-negative bacterium Escherichia coli,” Applied and Environmental Microbiology, vol. 73, no. 6, pp. 1712–1720, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. E. Weir, A. Lawlor, A. Whelan, and F. Regan, “The use of nanoparticles in anti-microbial materials and their characterization,” Analyst, vol. 133, no. 7, pp. 835–845, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. E. Amato, Y. A. Diaz-Fernandez, A. Taglietti et al., “Synthesis, characterization and antibacterial activity against gram positive and gram negative bacteria of biomimetically coated silver nanoparticles,” Langmuir, vol. 27, no. 15, pp. 9165–9173, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. I. Sondi and B. Salopek-Sondi, “Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria,” Journal of Colloid and Interface Science, vol. 275, no. 1, pp. 177–182, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. F. Martínez-Gutierrez, E. P. Thi, J. M. Silverman et al., “Antibacterial activity, inflammatory response, coagulation and cytotoxicity effects of silver nanoparticles,” Nanomedicine: Nanotechnology, Biology, and Medicine, vol. 8, no. 3, pp. 328–336, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. Z. Lu, K. Rong, J. Li, H. Yang, and R. Chen, “Size-dependent antibacterial activities of silver nanoparticles against oral anaerobic pathogenic bacteria,” Journal of Materials Science: Materials in Medicine, vol. 24, no. 6, pp. 1465–1471, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. P. Spacciapoli, D. Buxton, D. Rothstein, and P. Friden, “Antimicrobial activity of silver nitrate against periodontal pathogens,” Journal of Periodontal Research, vol. 36, no. 2, pp. 108–113, 2001. View at Publisher · View at Google Scholar · View at Scopus
  9. O. Brandt, M. Mildner, A. E. Egger et al., “Nanoscalic silver possesses broad-spectrum antimicrobial activities and exhibits fewer toxicological side effects than silver sulfadiazine,” Nanomedicine: Nanotechnology, Biology, and Medicine, vol. 8, no. 4, pp. 478–488, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. Z.-M. Xiu, Q.-B. Zhang, H. L. Puppala, V. L. Colvin, and P. J. J. Alvarez, “Negligible particle-specific antibacterial activity of silver nanoparticles,” Nano Letters, vol. 12, no. 8, pp. 4271–4275, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. M. N. Martin, A. J. Allen, R. I. Maccuspie, and V. A. Hackley, “Dissolution, agglomerate morphology, and stability limits of protein-coated silver nanoparticles,” Langmuir, vol. 30, no. 38, pp. 11442–11452, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. T. S. Peretyazhko, Q. Zhang, and V. L. Colvin, “Size-controlled dissolution of silver nanoparticles at neutral and acidic pH conditions: kinetics and size changes,” Environmental Science and Technology, vol. 48, no. 20, pp. 11954–11961, 2014. View at Publisher · View at Google Scholar · View at Scopus
  13. B. L. Pihlstrom, B. S. Michalowicz, and N. W. Johnson, “Periodontal diseases,” The Lancet, vol. 366, no. 9499, pp. 1809–1820, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. P. I. Eke, B. A. Dye, L. Wei, G. O. Thornton-Evans, and R. J. Genco, “Prevalence of periodontitis in adults in the united states: 2009 and 2010,” Journal of Dental Research, vol. 91, no. 10, pp. 914–920, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. R. P. Darveau, “Periodontitis: a polymicrobial disruption of host homeostasis,” Nature Reviews Microbiology, vol. 8, no. 7, pp. 481–490, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. S. S. Socransky, A. D. Haffajee, M. A. Cugini, C. Smith, and R. L. Kent Jr., “Microbial complexes in subgingival plaque,” Journal of Clinical Periodontology, vol. 25, no. 2, pp. 134–144, 1998. View at Publisher · View at Google Scholar · View at Scopus
  17. G. Hajishengallis and R. J. Lamont, “Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology,” Molecular Oral Microbiology, vol. 27, no. 6, pp. 409–419, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. G. Hajishengallis, S. Liang, M. A. Payne et al., “Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement,” Cell Host & Microbe, vol. 10, no. 5, pp. 497–506, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. G. R. Mettraux, F. A. Gusberti, and H. Graf, “Oxygen tension (pO2) in untreated human periodontal pockets,” Journal of Periodontology, vol. 55, no. 9, pp. 516–521, 1984. View at Publisher · View at Google Scholar · View at Scopus
  20. R. P. Darveau, G. Hajishengallis, and M. A. Curtis, “Porphyromonas gingivalis as a potential community activist for disease,” Journal of Dental Research, vol. 91, no. 9, pp. 816–820, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. L. G. Henry, M.-C. Boutrin, A. W. Aruni, A. Robles, A. Ximinies, and H. M. Fletcher, “Life in a diverse oral community—strategies for oxidative stress survival,” Journal of Oral Biosciences, vol. 56, no. 2, pp. 63–71, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. L. G. Henry, R. M. E. McKenzie, A. Robles, and H. M. Fletcher, “Oxidative stress resistance in Porphyromonas gingivalis,” Future Microbiology, vol. 7, no. 4, pp. 497–512, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. R. J. Genco and T. E. Van Dyke, “Reducing the risk of CVD in patients with periodontitis,” Nature Reviews Cardiology, vol. 7, no. 9, pp. 479–480, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. E. Lalla and P. N. Papapanou, “Diabetes mellitus and periodontitis: a tale of two common interrelated diseases,” Nature Reviews Endocrinology, vol. 7, no. 12, pp. 738–748, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Kaur, S. White, and P. M. Bartold, “Periodontal disease and rheumatoid arthritis: a systematic review,” Journal of Dental Research, vol. 92, no. 5, pp. 399–408, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. C. O. Bingham III and M. Moni, “Periodontal disease and rheumatoid arthritis: the evidence accumulates for complex pathobiologic interactions,” Current Opinion in Rheumatology, vol. 25, no. 3, pp. 345–353, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Mombelli, B. Schmid, A. Rutar, and N. P. Lang, “Persistence patterns of Porphyromonas gingivalis, Prevotella intermedia/nigrescens, and Actinobacillus actinomycetemcomitans after mechanical therapy of periodontal disease,” Journal of Periodontology, vol. 71, no. 1, pp. 14–21, 2000. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Sandros, P. Papapanou, and G. Dahlén, “Porphyromonas gingivalis invades oral epithelial cells in vitro,” Journal of Periodontal Research, vol. 28, no. 3, pp. 219–226, 1993. View at Publisher · View at Google Scholar · View at Scopus
  29. American Academy of Pediatric Dentistry, “Treatment of plaque-induced gingivitis, chronic periodontitis, and other clinical conditions,” Pediatric Dentistry, vol. 27, no. 7, supplement, pp. 202–211, 2006. View at Google Scholar
  30. “Treatment of plaque-induced gingivitis, chronic periodontitis, and other clinical conditions,” Journal of Periodontology, vol. 72, no. 12, pp. 1790–1800, 2001. View at Publisher · View at Google Scholar
  31. L. Rizzello and P. P. Pompa, “Nanosilver-based antibacterial drugs and devices: mechanisms, methodological drawbacks, and guidelines,” Chemical Society Reviews, vol. 43, no. 5, pp. 1501–1518, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. B. Reidy, A. Haase, A. Luch, K. A. Dawson, and I. Lynch, “Mechanisms of silver nanoparticle release, transformation and toxicity: a critical review of current knowledge and recommendations for future studies and applications,” Materials, vol. 6, no. 6, pp. 2295–2350, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Eckhardt, P. S. Brunetto, J. Gagnon, M. Priebe, B. Giese, and K. M. Fromm, “Nanobio silver: its interactions with peptides and bacteria, and its uses in medicine,” Chemical Reviews, vol. 113, no. 7, pp. 4708–4754, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. C. Levard, E. M. Hotze, G. V. Lowry, and G. E. Brown, “Environmental transformations of silver nanoparticles: impact on stability and toxicity,” Environmental Science & Technology, vol. 46, no. 13, pp. 6900–6914, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. A. P. Gondikas, A. Morris, B. C. Reinsch, S. M. Marinakos, G. V. Lowry, and H. Hsu-Kim, “Cysteine-induced modifications of zero-valent silver nanomaterials: implications for particle surface chemistry, aggregation, dissolution, and silver speciation,” Environmental Science & Technology, vol. 46, no. 13, pp. 7037–7045, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Banerjee, S. Sharma, A. Chattopadhyay, and S. S. Ghosh, “Enhanced antibacterial activity of bimetallic gold-silver core-shell nanoparticles at low silver concentration,” Nanoscale, vol. 3, no. 12, pp. 5120–5125, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. C.-N. Lok, C.-M. Ho, R. Chen et al., “Silver nanoparticles: partial oxidation and antibacterial activities,” Journal of Biological Inorganic Chemistry, vol. 12, no. 4, pp. 527–534, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. Z.-M. Xiu, J. Ma, and P. J. J. Alvarez, “Differential effect of common ligands and molecular oxygen on antimicrobial activity of silver nanoparticles versus silver ions,” Environmental Science & Technology, vol. 45, no. 20, pp. 9003–9008, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. R. Y. Prasad, J. K. McGee, M. G. Killius et al., “Investigating oxidative stress and inflammatory responses elicited by silver nanoparticles using high-throughput reporter genes in HepG2 cells: effect of size, surface coating, and intracellular uptake,” Toxicology in Vitro, vol. 27, no. 6, pp. 2013–2021, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. N. Alissawi, V. Zaporojtchenko, T. Strunskus et al., “Effect of gold alloying on stability of silver nanoparticles and control of silver ion release from vapor-deposited Ag–Au/polytetrafluoroethylene nanocomposites,” Gold Bulletin, vol. 46, no. 1, pp. 3–11, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. T. Li, B. Albee, M. Alemayehu et al., “Comparative toxicity study of Ag, Au, and Ag–Au bimetallic nanoparticles on Daphnia magna,” Analytical and Bioanalytical Chemistry, vol. 398, no. 2, pp. 689–700, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Grade, J. Eberhard, J. Jakobi, A. Winkel, M. Stiesch, and S. Barcikowski, “Alloying colloidal silver nanoparticles with gold disproportionally controls antibacterial and toxic effects,” Gold Bulletin, vol. 47, no. 1-2, pp. 83–93, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. C. A. Simpson, K. J. Salleng, D. E. Cliffel, and D. L. Feldheim, “In vivo toxicity, biodistribution, and clearance of glutathione-coated gold nanoparticles,” Nanomedicine: Nanotechnology, Biology, and Medicine, vol. 9, no. 2, pp. 257–263, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. L. G. Henry, W. Aruni, L. Sandberg, and H. M. Fletcher, “Protective role of the PG1036-PG1037-PG1038 operon in oxidative stress in Porphyromonas gingivalis W83,” PLoS ONE, vol. 8, no. 8, Article ID e69645, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. Y. Dou, W. Aruni, A. Muthiah, F. Roy, C. Wang, and H. Fletcher, “Studies of the extracytoplasmic function sigma factor PG0162 in Porphyromonas gingivalis,” Molecular Oral Microbiology, 2015. View at Publisher · View at Google Scholar
  46. Y. Dou, D. Osbourne, R. McKenzie, and H. M. Fletcher, “Involvement of extracytoplasmic function sigma factors in virulence regulation in Porphyromonas gingivalis W83,” FEMS Microbiology Letters, vol. 312, no. 1, pp. 24–32, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. R. M. E. McKenzie, N. A. Johnson, W. Aruni, Y. Dou, G. Masinde, and H. M. Fletcher, “Differential response of Porphyromonas gingivalis to varying levels and duration of hydrogen peroxide-induced oxidative stress,” Microbiology, vol. 158, no. 10, pp. 2465–2479, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. R. M. E. McKenzie, W. Aruni, N. A. Johnson et al., “Metabolome variations in the Porphyromonas gingivalis vimA mutant during hydrogen peroxide-induced oxidative stress,” Molecular Oral Microbiology, vol. 30, no. 2, pp. 111–127, 2015. View at Publisher · View at Google Scholar
  49. L. Kvítek, R. Prucek, A. Panáček, R. Novotný, J. Hrbáč, and R. Zbořil, “The influence of complexing agent concentration on particle size in the process of SERS active silver colloid synthesis,” Journal of Materials Chemistry, vol. 15, no. 10, pp. 1099–1105, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. L. Kvítek, A. Panáček, J. Soukupová et al., “Effect of surfactants and polymers on stability and antibacterial activity of silver nanoparticles (NPs),” The Journal of Physical Chemistry C, vol. 112, no. 15, pp. 5825–5834, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. M. S. Holden, K. E. Nick, M. Hall, J. R. Milligan, Q. Chen, and C. C. Perry, “Synthesis and catalytic activity of pluronic stabilized silver-gold bimetallic nanoparticles,” RSC Advances, vol. 4, no. 94, pp. 52279–52288, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. D. Paramelle, A. Sadovoy, S. Gorelik, P. Free, J. Hobley, and D. G. Fernig, “A rapid method to estimate the concentration of citrate capped silver nanoparticles from UV-visible light spectra,” Analyst, vol. 139, no. 19, pp. 4855–4861, 2014. View at Publisher · View at Google Scholar · View at Scopus
  53. K. D. Gilroy, A. Sundar, P. Farzinpour, R. A. Hughes, and S. Neretina, “Mechanistic study of substrate-based galvanic replacement reactions,” Nano Research, vol. 7, no. 3, pp. 365–379, 2014. View at Publisher · View at Google Scholar · View at Scopus
  54. X. Xia, Y. Wang, A. Ruditskiy, and Y. Xia, “25th anniversary article: galvanic replacement: a simple and versatile route to hollow nanostructures with tunable and well-controlled properties,” Advanced Materials, vol. 25, no. 44, pp. 6313–6332, 2013. View at Publisher · View at Google Scholar · View at Scopus
  55. E. González, J. Arbiol, and V. F. Puntes, “Carving at the nanoscale: sequential galvanic exchange and Kirkendall growth at room temperature,” Science, vol. 334, no. 6061, pp. 1377–1380, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. P. Mulvaney, “Surface plasmon spectroscopy of nanosized metal particles,” Langmuir, vol. 12, no. 3, pp. 788–800, 1996. View at Publisher · View at Google Scholar · View at Scopus
  57. G. C. Papavassiliou, “Surface plasmons in small Au-Ag alloy particles,” Journal of Physics F: Metal Physics, vol. 6, no. 4, pp. L103–L105, 1976. View at Publisher · View at Google Scholar · View at Scopus
  58. J. Liu and R. H. Hurt, “Ion release kinetics and particle persistence in aqueous nano-silver colloids,” Environmental Science & Technology, vol. 44, no. 6, pp. 2169–2175, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. A. Henglein, “Physicochemical properties of small metal particles in solution: ‘microelectrode’ reactions, chemisorption, composite metal particles, and the atom-to-metal transition,” The Journal of Physical Chemistry, vol. 97, no. 21, pp. 5457–5471, 1993. View at Publisher · View at Google Scholar · View at Scopus
  60. J. C. Love, L. A. Estroff, J. K. Kriebel, R. G. Nuzzo, and G. M. Whitesides, “Self-assembled monolayers of thiolates on metals as a form of nanotechnology,” Chemical Reviews, vol. 105, no. 4, pp. 1103–1169, 2005. View at Publisher · View at Google Scholar · View at Scopus
  61. J. M. Slocik and D. W. Wright, “Biomimetic mineralization of noble metal nanoclusters,” Biomacromolecules, vol. 4, no. 5, pp. 1135–1141, 2003. View at Publisher · View at Google Scholar · View at Scopus
  62. Q. Wu, H. Cao, Q. Luan et al., “Biomolecule-assisted synthesis of water-soluble silver nanoparticles and their biomedical applications,” Inorganic Chemistry, vol. 47, no. 13, pp. 5882–5888, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. A. Taglietti, Y. A. Diaz Fernandez, E. Amato et al., “Antibacterial activity of glutathione-coated silver nanoparticles against gram positive and gram negative bacteria,” Langmuir, vol. 28, no. 21, pp. 8140–8148, 2012. View at Publisher · View at Google Scholar · View at Scopus
  64. M. Bieri and T. Bürgi, “l-glutathione chemisorption on gold and acid/base induced structural changes:  a PM-IRRAS and time-resolved in situ ATR-IR spectroscopic study,” Langmuir, vol. 21, no. 4, pp. 1354–1363, 2005. View at Publisher · View at Google Scholar · View at Scopus
  65. W. Qian and S. Krimm, “Vibrational analysis of glutathione,” Biopolymers, vol. 34, no. 10, pp. 1377–1394, 1994. View at Publisher · View at Google Scholar · View at Scopus
  66. H.-J. Park, J. Y. Kim, J. Kim et al., “Silver-ion-mediated reactive oxygen species generation affecting bactericidal activity,” Water Research, vol. 43, no. 4, pp. 1027–1032, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. M. A. Kemper, M. M. Urrutia, T. J. Beveridge, A. L. Koch, and R. J. Doyle, “Proton motive force may regulate cell wall-associated enzymes of Bacillus subtilis,” Journal of Bacteriology, vol. 175, no. 17, pp. 5690–5696, 1993. View at Google Scholar · View at Scopus
  68. P. Dibrov, J. Dzioba, K. K. Gosink, and C. C. Häse, “Chemiosmotic mechanism of antimicrobial activity of Ag+ in Vibrio cholerae,” Antimicrobial Agents and Chemotherapy, vol. 46, no. 8, pp. 2668–2670, 2002. View at Publisher · View at Google Scholar · View at Scopus
  69. J. S. Kim, E. Kuk, K. N. Yu et al., “Antimicrobial effects of silver nanoparticles,” Nanomedicine: Nanotechnology, Biology, and Medicine, vol. 3, no. 1, pp. 95–101, 2007. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Yoshimura, Y. Nakano, Y. Yamashita, T. Oho, T. Saito, and T. Koga, “Formation of methyl mercaptan from l-methionine by Porphyromonas gingivalis,” Infection and Immunity, vol. 68, no. 12, pp. 6912–6916, 2000. View at Publisher · View at Google Scholar · View at Scopus
  71. L. D. Freedman and A. H. Corwin, “Oxidation reduction potentials of thiol-disulfide systems,” The Journal of Biological Chemistry, vol. 181, no. 2, pp. 601–621, 1949. View at Google Scholar · View at Scopus