Ultrastructural Aspects of Photodynamic Inactivation of Highly Pathogenic Avian H5N8 Influenza Virus
Abstract
:1. Introduction
2. Materials and Methods
2.1. Virus Production and Purification
2.2. Cell Culture and Virus Titration
2.3. Photodynamic Inactivation
2.4. Electron Microscopy
3. Results
3.1. Purified and Non-Purified Allantoic Fluid Comparison
3.2. H5N8 Photodynamic Inactivation and Infectivity
4. Discussion
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Jori, G.; Brown, S.B. Photosensitized inactivation of microorganisms. Photochem. Photobiol. Sci. 2004, 3, 403–405. [Google Scholar] [CrossRef] [PubMed]
- Kharkwal, G.B.; Sharma, S.K.; Huang, Y.Y.; Dai, T.; Hamblin, M.R. Photodynamic therapy for infections: Clinical applications. Lasers Surg. Med. 2011, 43, 755–767. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wainwright, M. Photoinactivation of viruses. Photochem. Photobiol. Sci. 2004, 3, 406–411. [Google Scholar] [CrossRef] [PubMed]
- Marotti, J.; Aranha, A.C.; Eduardo, C.P.; Ribeiro, M.S. Photodynamic therapy can be effective as a treatment for herpes simplex labialis. Photomed. Laser Surg. 2009, 27, 357–363. [Google Scholar] [CrossRef] [PubMed]
- Ryberg, E.C.; Chu, C.; Kim, J.H. Edible Dye-Enhanced Solar Disinfection with Safety Indication. Environ. Sci. Technol. 2018, 52, 13361–13369. [Google Scholar] [CrossRef]
- Trannoy, L.L.; Lagerberg, J.W.; Dubbelman, T.M.; Schuitmaker, H.J.; Brand, A. Positively charged porphyrins: A new series of photosensitizers for sterilization of RBCs. Transfusion 2004, 44, 1186–1196. [Google Scholar] [CrossRef]
- Wagner, S.J.; Robinette, D.; Storry, J.; Chen, X.Y.; Shumaker, J.; Benade, L. Differential sensitivities of viruses in red cell suspensions to methylene blue photosensitization. Transfusion 1994, 34, 521–526. [Google Scholar] [CrossRef]
- O’Brien, J.M.; Gaffney, D.K.; Wang, T.P.; Sieber, F. Merocyanine 540-sensitized photoinactivation of enveloped viruses in blood products: Site and mechanism of phototoxicity. Blood 1992, 80, 277–285. [Google Scholar]
- Lenard, J.; Rabson, A.; Vanderoef, R. Photodynamic inactivation of infectivity of human immunodeficiency virus and other enveloped viruses using hypericin and rose bengal: Inhibition of fusion and syncytia formation. Proc. Natl. Acad. Sci. USA 1993, 90, 158–162. [Google Scholar] [CrossRef]
- Vzorov, A.N.; Dixon, D.W.; Trommel, J.S.; Marzilli, L.G.; Compans, R.W. Inactivation of human immunodeficiency virus type 1 by porphyrins. Antimicrob. Agents Chemother. 2002, 46, 3917–3925. [Google Scholar] [CrossRef]
- Smetana, Z.; Ben-Hur, E.; Mendelson, E.; Salzberg, S.; Wagner, P.; Malik, Z. Herpes simplex virus proteins are damaged following photodynamic inactivation with phthalocyanines. J. Photochem. Photobiol. B Biol. 1998, 44, 77–83. [Google Scholar] [CrossRef]
- Sobotta, L.; Wierzchowski, M.; Mierzwicki, M.; Gdaniec, Z.; Mielcarek, J.; Persoons, L.; Goslinski, T.; Balzarini, J. Photochemical studies and nanomolar photodynamic activities of phthalocyanines functionalized with 1,4,7-trioxanonyl moieties at their non-peripheral positions. J. Inorg. Biochem. 2016, 155, 76–81. [Google Scholar] [CrossRef] [PubMed]
- Davies, M.J. Reactive species formed on proteins exposed to singlet oxygen. Photochem. Photobiol. Sci. 2004, 3, 17–25. [Google Scholar] [CrossRef] [PubMed]
- Costa, L.; Faustino, M.A.F.; Neves, M.G.P.M.S.; Cunha, A.; Almeida, A. Photodynamic Inactivation of Mammalian Viruses and Bacteriophages. Viruses 2012, 4, 1034–1074. [Google Scholar] [CrossRef] [Green Version]
- Spikes, J.D. Phthalocyanines as photosensitizers in biological systems and for the photodynamic therapy of tumors. Photochem. Photobiol. 1986, 43, 691–699. [Google Scholar] [CrossRef]
- Makarov, D.A.; Kuznetsova, N.A.; Yuzhakova, O.A.; Savvina, L.P.; Kaliya, O.L.; Lukyanets, E.A.; Negrimovskii, V.M.; Strakhovskaya, M.G. Effects of the degree of substitution on the physicochemical properties and photodynamic activity of zinc and aluminum phthalocyanine polycations. Russ. J. Phys. Chem. A 2009, 83, 1044–1050. [Google Scholar] [CrossRef]
- Minnock, A.; Vernon, D.I.; Schofield, J.; Griffiths, J.; Parish, J.H.; Brown, S.T. Photoinactivation of bacteria. Use of a cationic water-soluble zinc phthalocyanine to photoinactivate both gram-negative and gram-positive bacteria. J. Photochem. Photobiol. B 1996, 32, 159–164. [Google Scholar] [CrossRef]
- Ke, M.R.; Eastel, J.M.; Ngai, K.L.; Cheung, Y.Y.; Chan, P.K.; Hui, M.; Ng, D.K.; Lo, P.C. Photodynamic inactivation of bacteria and viruses using two monosubstituted zinc(II) phthalocyanines. Eur. J. Med. Chem. 2014, 84, 278–283. [Google Scholar] [CrossRef]
- Li, X.S.; Guo, J.; Zhuang, J.J.; Zheng, B.Y.; Ke, M.R.; Huang, J.D. Highly positive-charged zinc(II) phthalocyanine as non-aggregated and efficient antifungal photosensitizer. Bioorg. Med. Chem. Lett. 2015, 25, 2386–2389. [Google Scholar] [CrossRef]
- Kuznetsova, N.; Kaliya, O.; Strakhovskaya, M.; Zubairov, M. Photodynamic inactivation of avian influenza virus in aqueous media. In Proceedings of the First International Workshop on Application of Redox Technologies in the Environment 2009, Istanbul, Turkey, 14–15 September 2009; pp. 145–147. [Google Scholar]
- Zarubaev, V.V.; Belousova, I.M.; Kiselev, O.I.; Piotrovsky, L.B.; Anfimov, P.M.; Krisko, T.C.; Muraviova, T.D.; Rylkov, V.V.; Starodubzev, A.M.; Sirotkin, A.C. Photodynamic inactivation of influenza virus with fullerene C60 suspension in allantoic fluid. Photodiagnosis Photodyn Ther. 2007, 4, 31–35. [Google Scholar] [CrossRef]
- Stear, M.J. OIE Manual of Diagnostic Tests and Vaccines for Terrestrial Animals (Mammals, Birds and Bees), 5th ed.; Cambridge University Press: Cambridge, UK, 2004; 588p, ISBN 92-9044-622-6. [Google Scholar]
- Bonilla, N.; Rojas, M.I.; Cruz, G.N.F.; Hung, S.-H.; Rohwer, F.; Barr, J.J. Phage on tap—A quick and efficient protocol for the preparation of bacteriophage laboratory stocks. PeerJ 2016, 4, e2261. [Google Scholar] [CrossRef] [PubMed]
- Zaitsev, B.N.; Taranov, O.S.; Rudometova, N.B.; Shcherbakova, N.S.; Ilyichev, A.A.; Karpenko, L.I. An optimized method for counting viral particles using electron microscopy. Vavilov J. Genet. Breed. 2019, 23, 337–342. [Google Scholar] [CrossRef] [Green Version]
- Reed, L.J.; Muench, H. A simple method of estimating fifty per cent endpoints. Am. J. Epidemiol. 1938, 27, 493–497. [Google Scholar] [CrossRef]
- Li, B.; Lin, L.; Lin, H.; Wilson, B.C. Photosensitized singlet oxygen generation and detection: Recent advances and future perspectives in cancer photodynamic therapy. J. Biophotonics 2016, 11–12, 1314–1325. [Google Scholar] [CrossRef] [PubMed]
- Davison, E.; Colquhoun, W.J. Ultrathin Formvar Support Films for Transmission Electron Microscopy. Electron Microsc. Tech. 1985, 2, 35–43. [Google Scholar] [CrossRef]
- Scarff, C.A.; Fuller, M.J.G.; Thompson, R.F.; Iadaza, M.G. Variations on Negative Stain Electron Microscopy Methods: Tools for Tackling Challenging Systems. J. Vis. Exp. 2018, 132, e57199. [Google Scholar] [CrossRef] [PubMed]
- Brand, C.M.; Skehel, J.J. Crystalline antigen from the influenza virus envelope. Nat. New Biol. 1972, 238, 145–147. [Google Scholar] [CrossRef]
- Schaap, I.A.; Eghiaian, F.; des Georges, A.; Veigel, C. Effect of envelope proteins on the mechanical properties of influenza virus. J. Biol. Chem. 2012, 287, 41078–41088. [Google Scholar] [CrossRef]
- Zhirnov, O.P.; Manykin, A.A. Abnormal Morphological Vesicles in Influenza A Virus Exposed to Acid pH. Bull. Exp. Biol. Med. 2015, 158, 776–780. [Google Scholar] [CrossRef]
- Girotti, A.W.; Korytowski, W. Cholesterol Peroxidation as a Special Type of Lipid Oxidation in Photodynamic Systems. Photochem. Photobiol. 2019, 95, 73–82. [Google Scholar] [CrossRef]
- Müller-Breitkreutz, K.; Mohr, H.; Briviba, K.; Sies, H. Inactivation of viruses by chemically and photochemically generated singlet molecular oxygen. J. Photochem. Photobiol. B 1995, 30, 63–70. [Google Scholar] [CrossRef]
- Stief, T.W. The physiology and pharmacology of singlet oxygen. Med. Hypotheses 2003, 60, 567–572. [Google Scholar] [CrossRef]
Titer of Virus | Allantoic Fluid | Purified Suspension | Stored in Dark with PS (4 µM) | Irradiated for 20 Min without PS | Irradiated for 20 Min with PS (2 µM) | Irradiated for 20 Min with PS (4 µM) |
---|---|---|---|---|---|---|
lgTCID50/mL ± 2Ϭ | 8.375 ± 0.42 | 7.125 ± 0.34 | 7.25 ± 0.30 | 7.0 ± 0.42 | 0 | 0 |
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Korneev, D.; Kurskaya, O.; Sharshov, K.; Eastwood, J.; Strakhovskaya, M. Ultrastructural Aspects of Photodynamic Inactivation of Highly Pathogenic Avian H5N8 Influenza Virus. Viruses 2019, 11, 955. https://doi.org/10.3390/v11100955
Korneev D, Kurskaya O, Sharshov K, Eastwood J, Strakhovskaya M. Ultrastructural Aspects of Photodynamic Inactivation of Highly Pathogenic Avian H5N8 Influenza Virus. Viruses. 2019; 11(10):955. https://doi.org/10.3390/v11100955
Chicago/Turabian StyleKorneev, Denis, Olga Kurskaya, Kirill Sharshov, Justin Eastwood, and Marina Strakhovskaya. 2019. "Ultrastructural Aspects of Photodynamic Inactivation of Highly Pathogenic Avian H5N8 Influenza Virus" Viruses 11, no. 10: 955. https://doi.org/10.3390/v11100955