Antimicrobial Effects and Mechanism(s) of Silver Nanoparticle

은나노 입자의 항균작용과 작용기작

  • Hwang, In-Sok (School of Life Sciences and Biotechnology, College of Natural Sciences, Kyungpook National University) ;
  • Cho, Jae-Yong (School of Life Sciences and Biotechnology, College of Natural Sciences, Kyungpook National University) ;
  • Hwang, Ji-Hong (School of Life Sciences and Biotechnology, College of Natural Sciences, Kyungpook National University) ;
  • Hwang, Bo-Mi (School of Life Sciences and Biotechnology, College of Natural Sciences, Kyungpook National University) ;
  • Choi, Hye-Min (School of Life Sciences and Biotechnology, College of Natural Sciences, Kyungpook National University) ;
  • Lee, June-Young (School of Life Sciences and Biotechnology, College of Natural Sciences, Kyungpook National University) ;
  • Lee, Dong-Gun (School of Life Sciences and Biotechnology, College of Natural Sciences, Kyungpook National University)
  • 황인석 (경북대학교 자연과학대학 생명과학부) ;
  • 조재용 (경북대학교 자연과학대학 생명과학부) ;
  • 황지홍 (경북대학교 자연과학대학 생명과학부) ;
  • 황보미 (경북대학교 자연과학대학 생명과학부) ;
  • 최혜민 (경북대학교 자연과학대학 생명과학부) ;
  • 이준영 (경북대학교 자연과학대학 생명과학부) ;
  • 이동건 (경북대학교 자연과학대학 생명과학부)
  • Received : 2011.02.08
  • Accepted : 2011.03.03
  • Published : 2011.03.28

Abstract

The antimicrobial effects of silver (Ag) ion or salts are well known. Recently, silver nanoparticle is attracting an interest in a wide variety of fields since it has been known to be safe and effective as an antimicrobial agent against a broad spectrum of microorganisms. Although silver nanoparticle has been applied to various kinds of products owing to its potent antimicrobial activity, the effects of silver nanoparticle on microorganisms and antimicrobial mechanism have not been revealed clearly. In this paper, we summarized the characteristics, antimicrobial activities and mechanisms, cytotoxicity and applicability of silver nanoparticle.

Acknowledgement

Grant : Center for Food & Nutritional Genomics

Supported by : National Research Foundation (NRF)

References

  1. Alt, V., T. Bechert, P. Steinrucke, M. Wagener, P. Seidel, E. Dingeldein, D. Scheddin, E. Domann, and R. Schnettler. 2004. Nanoparticulate silver. A new antimicrobial substance for bone cement. Orthopade. 33: 885-892.
  2. Arakawa, H., J. F. Neault, and H. A. Tajmir-Riahi. 2001. Silver(I) complexes with DNA and RNA studied by Fourier transform infrared spectroscopy and capillary electrophoresis. Biophys. J. 81: 1580-1587. https://doi.org/10.1016/S0006-3495(01)75812-2
  3. Butkus, M. A., M. P. Labare, J. A. Starke, K. Moon, and M. Talbot. 2004. Use of aqueous silver to enhance inactivation of coliphage MS-2 by UV disinfection. Appl. Environ. Microbiol. 70: 2848-2853. https://doi.org/10.1128/AEM.70.5.2848-2853.2004
  4. Carlson, C. et al. 2008. Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. J. Phys. Chem. B 112: 13608-13619. https://doi.org/10.1021/jp712087m
  5. Cha, K., H. W. Hong, Y. G. Choi, M. J. Lee, J. H. Park, H. K. Chae, G. Ryu, and H. Myung. 2008. Comparison of acute responses of mice livers to short-term exposure to nanosized or micro-sized silver particles. Biotechnol. Lett. 30: 1893-1899. https://doi.org/10.1007/s10529-008-9786-2
  6. Chaloupka, K., Y. Malam, and A. M. Seifalian. 2010. Nanosilver as a new generation of nanoproduct in biomedical applications. Trends in Biotechnology. 28: 580- 588. https://doi.org/10.1016/j.tibtech.2010.07.006
  7. Chen, P. et al. 2007. Synthesis of silver nanoparticles by γ- ray irradiation in acetic water solution containing chitosan. Radiat. Phys. Chem. 76: 1165-1168. https://doi.org/10.1016/j.radphyschem.2006.11.012
  8. Choi, O. and Z. Hu. 2008. Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. Environ. Sci. Technol. 42: 4583-4588. https://doi.org/10.1021/es703238h
  9. Cohen, M. L. 1992. Epidemiology of drug resistance; implications for a post-antimicrobial era. Science 257: 1050- 1055. https://doi.org/10.1126/science.257.5073.1050
  10. Courrol, L. C., F. R. O. Silva, and L. Gomes. 2007. A simple method to synthesize silver nanoparticles by photoreduction. Colloids Surf. A 305: 54-57. https://doi.org/10.1016/j.colsurfa.2007.04.052
  11. Davis, R. L. and S. F. Etris. 1997. The development and functions of silver in water purification and disease control. Catalysis Today. 36: 107. https://doi.org/10.1016/S0920-5861(96)00203-9
  12. Fayaz, A. M., K. Balaji, M. Girilal, R. Yadav, P. T. Kalaichelvan, and R. Venketesan. 2010. Biogenic synthesis of silver nanoparticles and their synergistic effect with antibiotics: a study against gram-positive and gram-negative bacteria. Nanomedicine 6: 103-109. https://doi.org/10.1016/j.nano.2009.04.006
  13. Feng, Q. L, J. Wu, G. Q. Chen, F. Z. Cui, T. N. Kim, and J. O. Kim. 2000. A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. J. Biomed. Mater. Res. 52: 662-668. https://doi.org/10.1002/1097-4636(20001215)52:4<662::AID-JBM10>3.0.CO;2-3
  14. Gajbhiye, M., J. Kesharwani, A. Ingle, A. Gade, and M. Rai. 2009. Fungus-mediated synthesis of silver nanoparticles and their activity against pathogenic fungi in combination with fluconazole. Nanomedicine 5: 382-386. https://doi.org/10.1016/j.nano.2009.06.005
  15. Gogoi, S. K., P. Gopinath, A. Paul, A. Ramesh, S. S. Ghosh, and A. Chattopadhyay. 2006. Green fluorescent proteinexpressing Escherichia coli as a model system for investigating the antimicrobial activities of silver nano-particles. Langmuir 22: 9322-9328. https://doi.org/10.1021/la060661v
  16. Graf, P. et al. 2009. Peptide-coated silver nanoparticles: synthesis, surface chemistry, and pH-triggered, reversible assembly into particle assemblies. Chemistry 15: 5831-5844. https://doi.org/10.1002/chem.200802329
  17. Greenfeld, J. I., L. Sampath, S. J. Popilskis, S. R. Brunnert, S. Stylianos, and S. Modak. 1995. Decreased bacterial adherence and biofilm formation on chlorhexidine and silver sulfadiazine-impregnated central venous catheters implanted in swine. Crit. Care Med. 23: 894-900. https://doi.org/10.1097/00003246-199505000-00018
  18. Gutierrez, F. M., P. L. Olive, A. Banuelos, E. Orrantia, N. Nino, E. M. Sanchez, F. Ruiz, H. Bach, and Y. A. Gay. 2010. Synthesis, characterization, and evaluation of antimicrobial and cytotoxic effect of silver and titanium nanoparticles. Nanomedicine 6: 681-688. https://doi.org/10.1016/j.nano.2010.02.001
  19. Holt, K. B. and A. J. Bard. 2005. The Interaction of Silver (I) Ions with the Respiratory Chain of Escherichia coli: An Electrochemical and Scanning Electrochemical Microscopy Study of the Antimicrobial Mechanism of Micromolar $Ag^{+}$. Biochemistry 44: 13214-13223. https://doi.org/10.1021/bi0508542
  20. Imran, M., A. M. Revol-Junelles, A. Martyn, E. A. Tehrany, M. Jacquot, M. Linder, and S. Desobry. 2010. Active food packaging evolution: transformation from micro- to nanotechnology. Food. Science and Nutrition 50: 799-821.
  21. Izatt, R. M., J. J. Christensen, and J. H. Rytting. 1971. Sites and thermodynamic quantities associated with proton and metal ion interaction with ribonucleic acid, deoxyribonucleic acid, and their constituent bases, nucleosides, and nucleotides. Chem. Rev. 71: 439-481. https://doi.org/10.1021/cr60273a002
  22. Jain, P. and T. Pradeep. 2005. Potential of silver nanoparticle -coated polyurethane foam as an antibacterial water filter. Biotechnol. Bioeng. 90: 59-63. https://doi.org/10.1002/bit.20368
  23. Jung, W. K. et al. 2008. Antibacterial activity and mechanism of action of the silver ion in Staphylococcus aureus and Escherichia coli. Appl. Environ. Microbiol. 74: 2171?2178. https://doi.org/10.1128/AEM.02001-07
  24. Kalishwaralal, K., S. Barathmanikanth, S. R. K. Pandian, V. Deepak, and S. Gurunathan. 2010. Silver nanoparticles impede the biofilm formation by Pseudomonas aeruginosa and Staphylococcus epidermidis. Colloids and Surfaces B. 79: 340-344. https://doi.org/10.1016/j.colsurfb.2010.04.014
  25. Kim, J. S., E. Kuk, K. N. Yu, J. H. Kim, S. J. Park, H. J. Lee, S. H. Kim, Y. K. Park, Y. H. Park, C. Y. Hwang, Y. K. Kim, Y. S. Lee, D. H. Jeong, and M. H. Cho. 2007. Antimicrobial effects of silver nanoparticles. Nanomedicine 3: 95-101. https://doi.org/10.1016/j.nano.2006.12.001
  26. Kim, J. Y., C. Lee, M. Cho, and J. Yoon. 2008. Enhanced inactivation of E. coli and MS-2 phage by silver ions combined with UV-A and visible light irradiation. Water Res. 42: 356-362. https://doi.org/10.1016/j.watres.2007.07.024
  27. Kim, J. Y., T. Y. Kim, and J. Y. Yoon. 2009. Antimicrobial Activity and Mechanism of Silver. J. Korean Ind. Eng. Chem. 20: 251-257.
  28. Kim, K. J., W. S. Sung, B. K. Suh, S. K. Moon, J. S. Choi, J. G. Kim, and D. G. Lee. 2009. Antifungal activity and mode of action of silver nano-particles on Candida albicans. Biometals. 22: 235-242. https://doi.org/10.1007/s10534-008-9159-2
  29. Kim, K. J., W. S. Sung, S. K. Moon, J. S. Choi, J. G. Kim, and D. G. Lee. 2008. Antifungal effect of silver nanoparticles on dermatophytes. J. Microbiol. Biotechnol. 18: 1482-1484.
  30. Kokura, S., O. Handa, T. Takagi, T. Ishikawa, Y. Naito, and T. Yoshikawa. 2010. Silver nanoparticles as a safe preservative for use in cosmetics. Nanomedicine 6: 570-574. https://doi.org/10.1016/j.nano.2009.12.002
  31. Kora, A. J. et al. 2009. Superior bactericidal activity of SDS capped silver nanoparticles: synthesis and characterization. Mater. Sci. Eng. C. 29: 2104-2109. https://doi.org/10.1016/j.msec.2009.04.010
  32. Kumar, A., P. K. Vemula, P. M. Ajayan, and G. John. 2008. Silver-nanoparticle-embedded antimicrobial paints based on vegetable oil. Nat. Mater. 7: 236-241. https://doi.org/10.1038/nmat2099
  33. Landeen, L. K., M. T. Yahya, and C. P. Gerba. 1989. Efficacy of copper and silver ions and reduced levels of free chlorine in inactivation of Legionella pneumophila. Appl. Environ. Microbiol. 55: 3045-3050.
  34. Lara, H. H., N. V. Ayala-Nuñez, L. Ixtepan-Turrent, and C. Rodriguez-Padilla. 2010. Mode of antiviral action of silver nanoparticles against HIV-1. J. Nanobiotechnology 8: 1. https://doi.org/10.1186/1477-3155-8-1
  35. Liau, S. Y., D. C. Read, W. J. Pugh, J. R. Furr, and A. D. Russell. 1997. Interaction of silver-nitrate with readily identifiable groups: relationship to the antibacterial action of silver ions. Lett. Appl. Microbiol. 25: 279-283. https://doi.org/10.1046/j.1472-765X.1997.00219.x
  36. Li, P., J. Li, C. Wu, Q. Wu, and J. Li. 2005. Synergistic antibacterial effects of β-lactam antibiotic combined with silver nanoparticles. Nanotechnology 16: 1912-1917. https://doi.org/10.1088/0957-4484/16/9/082
  37. Lok, C. N. et al. 2007. Silver nanoparticles: partial oxidation and antibacterial activities. J. Biol. Inorg. Chem. 12: 527- 534. https://doi.org/10.1007/s00775-007-0208-z
  38. Lu, Y., G. L. Liu, and L. P. Lee. 2005. High-density silver nanoparticle film with temperature-controllable interparticle spacing for a tunable surface enhanced Raman scattering substrate. Nano. Lett. 5: 5-9. https://doi.org/10.1021/nl048965u
  39. Morones, J. R., J. L. Elechiguerra, A. Camacho, K. Holt, J. B. Kouri, J. T. Ramirez, and M. J. Yacaman. 2005. The bactericidal effect of silver nanoparticles. Nanotechnology 16: 2345-2353.
  40. Nanda, A. and M. Saravanan. 2009. Biosynthesis of silver nanoparticles from Staphylococcus aureus and its antimicrobial activity against MRSA and MRSE. Nanomedicine 5: 452-456. https://doi.org/10.1016/j.nano.2009.01.012
  41. Pal, S., Y. K. Tak, and J. M. Song. 2007. Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the Gram-negative bacterium Escherichia coli. Apple. Environ. Microbiol. 73: 1712-1720. https://doi.org/10.1128/AEM.02218-06
  42. Park, H. J., J. Y. Kim, J. Kim, J. H. Lee, J. S. Hahn, M. B. Gu, and J. Yoon. 2009. Silver-ion-mediated reactive oxygen species generation affecting bactericidal activity. Water Res. 43: 1027-1032. https://doi.org/10.1016/j.watres.2008.12.002
  43. Pedahzur, R., H. I. Shuval, and S. Ulitzur. 1997. Silver and hydrogen peroxide as potential drinking water disinfectants: Their bactericidal effects and possible modes of action. Water Sci. Technol. 35: 87-93.
  44. Pedahzur, R., O. Lev, B. Fattal, and H. I. Shuval. 1995. The interaction of silver ions and hydrogen peroxide in the inactivation of E. coli: a preliminary evaluation of a new long acting residual drinking water disinfectant. Water Sci. Technol. 31: 123-129.
  45. Ravelin, J. 1869. Chemistry of vegetation. Sci. Nat. 11: 93-102.
  46. Roh, J. Y. et al. 2009. Ecotoxicity of silver nanoparticles on the soil nematode Caenorhabditis elegans using functional ecotoxicogenomics. Environ. Sci. Technol. 43: 3933-3940. https://doi.org/10.1021/es803477u
  47. Sekhon, B. S. and S. R. Kamboj. 2010. Inorganic nanomedicine-part 2. Nanomedicine 6: 612-618. https://doi.org/10.1016/j.nano.2010.04.003
  48. Shahverdi, A. R. et al. 2007. Rapid synthesis of silver nanoparticles using culture supernatants of Enterobacteria: a novel biological approach. Process Biochem. 42: 919-923. https://doi.org/10.1016/j.procbio.2007.02.005
  49. Shahverdi, A. R., A. Fakhimi, H. R. Shahverdi, and S. Minaian. 2007. Synthesis and effect of silver nanoparticles on the antibacterial activity of different antibiotics against Staphylococcus aureus and Escherichia coli. Nanomedicine 3: 168-171. https://doi.org/10.1016/j.nano.2007.02.001
  50. Shaligram, N. S. et al. 2009. Biosynthesis of silver nanoparticles using aqueous extract from the compactin producing fungal strain. Process Biochem. 44: 939-943. https://doi.org/10.1016/j.procbio.2009.04.009
  51. Shrivastava, S. 2007. Characterization of enhanced antibacterial effects of novel silver nanoparticles. Nanotechnology 18: 225103-225112. https://doi.org/10.1088/0957-4484/18/22/225103
  52. Sondi, I. and B. S. Sondi. 2004. Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. J. Colloid Interface Sci. 275: 177-182. https://doi.org/10.1016/j.jcis.2004.02.012
  53. Tian, J., K. K. Wong, C. M. Ho, C. N. Lok, W. Y. Yu, C. M. Che, J. F. Chiu, and P. K. Tam. 2007. Topical delivery of silver nanoparticles promotes wound healing. Chem. Med. Chem. 2: 129-136. https://doi.org/10.1002/cmdc.200600171
  54. Tien, D. C. et al. 2008. Colloidal silver fabrication using the spark discharge system and its antimicrobial effect on Staphylococcus aureus. Med. Eng. Phys. 30: 948-952. https://doi.org/10.1016/j.medengphy.2007.10.007
  55. Vigneshwaran, N. et al. 2006. A novel one-pot 'green' synthesis of stable silver nanoparticles using soluble starch. Carbohydr. Res. 341: 2012-2018. https://doi.org/10.1016/j.carres.2006.04.042
  56. Xu, G-N. et al. 2008. Preparation and characterization of stable monodisperse silver nanoparticles via photoreduction. Colloids Surf. A. 320: 222-226. https://doi.org/10.1016/j.colsurfa.2008.01.056
  57. Yamanaka, M. et al. 2005. Bactericidal actions of a silver ion solution on Escherichia coli, studied by energy-filtering transmission electron microscopy and proteomic analysis. Appl. Environ. Microbiol. 71: 7589-7593. https://doi.org/10.1128/AEM.71.11.7589-7593.2005
  58. Yang, Q., F. Wang, K. Tang, C. Wang, Z. Chen, and Y. Qian. 2002. The formation of fractal Ag nanocrystallites via γ- irradiation route in isopropyl alcohol. Mater. Chem. Phys. 78: 495-500.
  59. Yang, W. J. et al. 2009. Food storage material silver nanoparticles interfere with DNA replication fidelity and bind with DNA. Nanotechnology. 20: 085102. https://doi.org/10.1088/0957-4484/20/8/085102
  60. Yeo, S. Y., H. J. Lee, and S. H. Jeong. 2003. Preparation of nanocomposite fibers for permanent antibacterial effect. J. Mater. Sci. 38: 2143-2147. https://doi.org/10.1023/A:1023767828656