Advertisement

Archives of Virology

, 153:1467 | Cite as

Inactivation and morphological changes of avian influenza virus by copper ions

  • M. Horie
  • H. OgawaEmail author
  • Y. Yoshida
  • K. Yamada
  • A. Hara
  • K. Ozawa
  • S. Matsuda
  • C. Mizota
  • M. Tani
  • Y. Yamamoto
  • M. Yamada
  • K. Nakamura
  • K. Imai
Original Article

Abstract

The infectivity of the H9N2 virus to MDCK cells was time-dependently inhibited by Cu2+ at concentrations of 2.5–250 μM. In 25 μM Cu2+ solution, the virus titer decreased by approximately 3 and 4 log within 3 and 6 h, respectively. Compared to Cu2+, Zn2+ was much less effective in virus inactivation. The H9N2 virus hemagglutinin activity was not affected by 2.5–250 μM Cu2+. The H9N2 virus neuraminidase (NA) activity was drastically reduced by 25 mM Cu2+, marginally reduced by 250 μM Cu2+, and not affected by 25 μM Cu2+. Thus, we found that copper ions suppress the infectivity of influenza virus at lower concentrations at which neither NA nor hemagglutination inhibition occurs. Electron microscopic analysis revealed morphological abnormalities of the Cu2+-treated H9N2 virus. Additional studies should be undertaken to clarify the mechanism underlying the antiviral effect of copper ions on influenza virus.

Keywords

Influenza Influenza Virus CuCl2 CuSO4 Virus Titer 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This work was partially supported by grants from the Program of Founding Research Centers for Emerging and Reemerging Infectious Diseases, and by grant-in aid for Exploratory Research (19659115), MEXT Japan.

References

  1. 1.
    Aruoma OI, Halliwell B, Gajewski E, Dizdaroglu M (1991) Copper-ion-dependent damage to the bases in DNA in the presence of hydrogen peroxide. Biochem J 273:601–604PubMedGoogle Scholar
  2. 2.
    Borkow G, Gabbay J (2005) Copper as a biocidal tool. Curr Med Chem 12:2163–2175PubMedCrossRefGoogle Scholar
  3. 3.
    Dizdaroglu M, Rao G, Halliwell B, Gajewski E (1991) Damage to the DNA bases in mammalian chromatin by hydrogen peroxide in the presence of ferric and cupric ions. Arch Biochem Biophys 285:317–324PubMedCrossRefGoogle Scholar
  4. 4.
    Evans GW (1973) Copper homeostasis in the mammalian system. Physiol Rev 53:535–570PubMedGoogle Scholar
  5. 5.
    Ewing HP, Pesti GM, Bakalli RI, Menten JFM (1998) Studies on the feeding of cupric sulfate pentahydrate, cupric citrate, and copper oxychloride to broiler chickens. Poult Sci 77:445–448PubMedGoogle Scholar
  6. 6.
    Howe C, Morgan C (1969) Interactions between Sendai virus and human erythrocytes. J Virol 3:70–81PubMedGoogle Scholar
  7. 7.
    Karlström AR, Levine RL (1991) Copper inhibits the protease from human immunodeficiency virus 1 by both cysteine-dependent and cysteine-independent mechanisms. Proc Natl Acad Sci USA 88:5552–5556PubMedCrossRefGoogle Scholar
  8. 8.
    Kopitz J, von Reitzenstein C, Mühl C, Cantz M (1994) Role of plasma membrane ganglioside sialidase of human neuroblastoma cells in growth control and differentiation. Biochem Biophys Res Commun 30:1188–1193CrossRefGoogle Scholar
  9. 9.
    Levinson W, Faras A, Woodson B, Jackson J, Bishop JM (1973) Inhibition of RNA-dependent DNA polymerase of Rous sarcoma virus by thiosemicarbazones and several cations. Proc Natl Acad Sci USA 70:164–168PubMedCrossRefGoogle Scholar
  10. 10.
    Miles RD, O’Keefe SF, Henry PR, Ammerman CB, Luo XG (1998) The effect of dietary supplementation with copper sulfate or tribasic copper chloride on broiler performance, relative copper bioavailability, and dietary prooxidant activity. Poult Sci 77:416–425PubMedGoogle Scholar
  11. 11.
    Miyagi T, Hata K, Hasegawa A, Aoyagi T (1993) Differential effect of various inhibitors on four types of rat sialidase. Glycoconj J 10:45–49PubMedCrossRefGoogle Scholar
  12. 12.
    Nackerdien Z, Rao G, Cacciuttolo MA, Gajewski E, Dizdaroglu M (1991) Chemical nature of DNA-protein cross-links produced in mammalian chromatin by hydrogen peroxide in the presence of iron or copper ions. Biochemistry 30:4873–4879PubMedCrossRefGoogle Scholar
  13. 13.
    Noyce JO, Michels H, Keevil CW (2007) Inactivation of influenza A virus on copper versus stainless steel surfaces. Appl Environ Microbiol 73:2748–2750PubMedCrossRefGoogle Scholar
  14. 14.
    Rafelson ME, Schneir M, Wilson VW (1963) Studies on the neuraminidase of influenza virus. II. Additional properties of the enzymes from the Asian and PR 8 strains. Arch Biochem Biophys 103:424–430PubMedCrossRefGoogle Scholar
  15. 15.
    Rifkind JM, Shin YA, Heim JM, Eichhorn GL (1976) Cooperative disordering of single-stranded polynucleotides thorough copper crosslinking. Biopolymers 15:1879–1902PubMedCrossRefGoogle Scholar
  16. 16.
    Sagripanti JL, Goering PL, Lamanna A (1991) Interaction of copper with DNA and antagonism by other metals. Toxicol Appl Pharamcol 110:477–485CrossRefGoogle Scholar
  17. 17.
    Sagripanti JL, Kraemer KH (1989) Site-specific oxidative DNA damage at polyguanosines produced by copper plus hydrogen peroxide. J Biol Chem 264:1729–1734Google Scholar
  18. 18.
    Sagripanti JL, Lightfoote MM (1996) Cupric and ferric ions inactivate HIV. AIDS Res Hum Retroviruses 12:333–337PubMedCrossRefGoogle Scholar
  19. 19.
    Sagripanti JL, Routson LB, Bonifacino AC, Lytle CD (1997) Mechanism of copper-mediated inactivation of herpes simplex virus. Antimicrob Agents Chemother 41:812–817PubMedGoogle Scholar
  20. 20.
    Sagripanti JL, Routson LB, Lytle CD (1993) Virus inactivation by copper or iron ions alone and in the presence of peroxide. Appl Environ Microbiol 59:4374–4376PubMedGoogle Scholar
  21. 21.
    Toyokuni S, Sagripanti JL (1996) Association between 8-hydroxy-2′-deoxyguanosine formation and DNA strand breaks mediated by copper and iron. Free Radic Biol Med 20:859–864PubMedCrossRefGoogle Scholar
  22. 22.
    Tulsiani DRP, Carubelli R (1970) Studies on the soluble and lysosomal neuraminidases of rat liver. J Biol Chem 245:1821–1827PubMedGoogle Scholar
  23. 23.
    United States Environmental Protection Agency. Public drinking water system. Available from http://www.epa.gov. Accessed 5 April 2008
  24. 24.
    Yohe HC, Rosenberg A (1978) Effect of neurotoxic divalent cations on the activity of the intrinsic nerve ending membrane-associated sialidase of bovine brain. Neurochem Res 3:101–113PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • M. Horie
    • 1
  • H. Ogawa
    • 2
    Email author
  • Y. Yoshida
    • 2
  • K. Yamada
    • 2
  • A. Hara
    • 2
  • K. Ozawa
    • 2
  • S. Matsuda
    • 2
  • C. Mizota
    • 3
  • M. Tani
    • 3
  • Y. Yamamoto
    • 4
  • M. Yamada
    • 4
  • K. Nakamura
    • 4
  • K. Imai
    • 2
  1. 1.Department of Virology, Research Institute for Microbial DiseasesOsaka UniversityOsakaJapan
  2. 2.Research Center for Animal Hygiene and Food SafetyObihiro University of Agriculture and Veterinary MedicineObihiroJapan
  3. 3.Department of Agro-Environmental ScienceObihiro University of Agriculture and Veterinary MedicineObihiroJapan
  4. 4.Research Team of Viral DiseasesNational Institute of Animal HealthTsukubaJapan

Personalised recommendations