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Zeta Potential and Aggregation of Virus-Like Particle of Human Norovirus and Feline Calicivirus Under Different Physicochemical Conditions

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Abstract

Although the spread of human norovirus reportedly depends on its ability to bind to food materials, the mechanism of the phenomenon remains unknown. Since protein size and electrical charge are reportedly important parameters in their adsorption, the current work is focused on determining human noroviruses isoelectric point (IEP), electrical charge and aggregate size at different pH, ionic strength (IS), and temperature. Using the baculovirus expression vector system, we produced and purified virus-like particles (VLPs) of GI.1 and GII.4 noroviruses and feline calicivirus, determined their IEP, and examined their size and electrical charge using a Zetasizer Nano ZS apparatus. Shape and size were also visualized using transmission electron microscopy. IEPs were found close to pH 4. Net charge increased as the pH deviated from the IEP. VLPs were negatively charged at all IS tested and showed a gradual decrease in charge with increasing IS. At low temperature, VLPs were 20–45 nm in diameter at pH far from their IEP and under almost all IS conditions, while aggregates appeared at or near the IEP. At increased temperatures, aggregates appeared at or near the IEP and at high IS. Aggregation at the IEP was also confirmed by microscopy. This suggests that electrostatic interactions would be the predominant factor in VLPs adhesion at pH far from 4 and at low ionic strength. In contrast, non-electrostatic interactions would prevail at around pH 4 and would be reinforced by aggregates, since size generally favors multiple bonding with sorbents.

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References

  • Atmar, R. L. (2010). Noroviruses: State of the art. Food and Environmental Virology, 2, 117–126.

    Article  PubMed Central  PubMed  Google Scholar 

  • Ausar, S. F., Foubert, T. R., Hudson, M. H., Vedvick, T. S., & Middaugh, C. R. (2006). Conformational stability and disassembly of Norwalk Virus-like particles effect of pH and temperature. Journal of Biological Chemistry, 281(28), 19478–19488.

    Article  CAS  PubMed  Google Scholar 

  • Baker, E. A. (1982). Chemistry and morphology of plant epicuticular waxes. In D. F. Cutler, K. L. Alvin, & C. E. Price (Eds.), The plant cuticle (pp. 139–165). London, NY: Academic Press.

  • Bolt, P. S., Goodwin, J. W., & Ottewill, R. H. (2005). Studies on the preparation and characterization of monodisperse polystyrene latices. VI. Preparation of zwitterionic latices. Langmuir, 21, 9911–9916.

    Article  CAS  PubMed  Google Scholar 

  • Boulangé-Petermann, L., Doren, A., Baroux, B., & Bellon-Fontaine, M.-N. (1995). Zeta potential measurement on passive metals. Journal of Colloid and Interface Science, 171, 179–186.

    Article  Google Scholar 

  • Chattopadhyay, S., & Puls, R. (1999). Adsorption of bacteriophages on clay minerals. Environmental Science and Technology, 33(20), 3609–3614.

    Article  CAS  Google Scholar 

  • Creighton, T. (2010). The Biophysique chemistry of nucleic acids & proteins. Eastbourne, East Sussex: HP Helvetian Press.

  • D’Souza, D. H., Sair, A., Williams, K., Papafragkou, E., Jean, J., Moore, C., & Jaykus, L.-A. (2006). Persistence of caliciviruses on environmental surfaces and their transfer to food. International Journal of Food Microbiololy, 108, 84–91.

    Article  Google Scholar 

  • da Silva, A. K., Kavanagh, O. V., Estes, M. K., & Elimelech, M. (2011). Adsorption and aggregation properties of Norovirus GI and GII Virus-Like particles demonstrate differing responses to solution chemistry. Environmental Science and Technology, 45(2), 520–526.

    Article  PubMed  Google Scholar 

  • Di Martino, B., Marsilio, F., & Roy, P. (2007). Assemly of feline calicivirus-like particle and its immunogenicity. Veterinary Microbiology, 120, 173–178.

    Article  PubMed  Google Scholar 

  • Dillman, W. J, Jr, & Miller, I. F. (1973). On the adsorption of serum proteins on polymer membrane surfaces. Journal of Colloid and Interface Science, 44, 221–241.

    Article  CAS  Google Scholar 

  • Dowd, S., Pillai, S. D., Wang, S., & Corapcioglu, M. Y. (1998). Delineating the specific influence of virus isoelectric point and size on virus adsorption and transport through sandy soils. Applied and Environmental Microbiology, 64(2), 405–410.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Farrah, S. R., Bitton, G., Hoffmann, E. M., Lanni, O., Pancorbo, O. C., Lutrick, M. C., et al. (1981). Survival of enteroviruses and coliform bacteria in a sludge lagoon. Applied and Environmental Microbiology, 41(2), 459–465.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gerba, C. (1984). Applied and theoretical aspects of virus adsorption to surfaces. Advances in Applied Microbiology, 30, 133–168.

    Article  CAS  PubMed  Google Scholar 

  • Girard, M., Ngazoa, S., Mattison, K., & Jean, J. (2010). Attachment of noroviruses to stainless steel and their inactivation, using household disinfectants. Journal of Food Protection, 73(2), 400–404.

    CAS  PubMed  Google Scholar 

  • Glass, R. I., & Estes, M. (2009). Norovirus gastroenteritis. New England Journal of Medecine, 361(18), 1776–1785.

    Article  CAS  Google Scholar 

  • Goodridge, L., Goodridge, C., Wu, J., Giffiths, M., & Pawliszyn, J. (2004). Isoelectric point determination of Norovirus Virus-like Particles by capillary isoelectric focusing with whole column imaging detection. Analytical Chemistry, 76(1), 48–52.

    Article  CAS  PubMed  Google Scholar 

  • Green, K. Y., Ando, T., Balayan, M. S., Berke, T., Clarke, N., Estes, M. K., et al. (2000). Taxonomy of the Caliciviruses. Journal of Infectious Diseases, 181(Suppl. 2), 322–330.

    Article  Google Scholar 

  • Greening, G. E. (2006). Chapitre 2: Human and animal viruses in food (including taxonomy of enteric viruses). In M. S. Goyal (Ed.), Viruses in foods. Food microbiology and food safety (pp. 5–42). New York: Springer.

  • Hall, A. J., Vinjé, J., Lopman, B., Park, G. W., Yen, C., Gregoricus, N., & Parashar, U. (2011). Updated Norovirus outbreak management and disease prevention guidelines. Centers for Disease Control and Prevention MMWR, Recommendations and Reports, 60, 1–15.

    Google Scholar 

  • Huhti, L., Blazevic, V., Nurminen, K., Koho, T., Hytönen, V. P., & Vesikari, T. (2010). A comparison of methods for purification and concentration of norovirus GII-4 capsid virus-like particles. Archive of Virology, 155, 1855–1858.

    Article  CAS  Google Scholar 

  • Institut National de Santé Publique du Québec. (2011). Cas d’infection à Caliciviridae incluant le norovirus. STATLABO-Statistique d’Analyse du Laboratoire Santé Publique du Québec, 10, 1–12.

    Google Scholar 

  • Jiang, X., Wang, M., Graham, D. Y., & Estes, M. K. (1992). Expression, self-assembly, and antigenicity of the Norwalk virus capsid protein. Journal of Virology, 66(11), 6527–6532.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Koopmans, M., & Duizer, E. (2004). Foodborne viruses: An emerging problem. International Journal of Food Microbiology, 90, 23–41.

    Article  PubMed  Google Scholar 

  • Kozlowski, L. P. (2007–2013). Isoelectric point calculator. http://isoelectric.ovh.org. 2014.

  • Kroneman, A., Verhoef, L., Harris, J., Vennema, H., Duizer, E., van Duynhoven, Y., et al. (2008). Analysis of integrated virological and epidemiological reports of norovirus outbreaks collected within the foodborne viruses in Europe network from 1 July 2001 to 30 June 2006. Journal of Clinical Microbiology, 46(9), 2959–2965.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lamhoujeb, S., Fliss, I., Ngazoa, S. E., & Jean, J. (2009). Molecular study of the persistence of infectious human norovirus on food-contact surfaces. Food and Environmental Virology, 1, 51–56.

    Article  CAS  Google Scholar 

  • Le Guyader, F. S., Loisy, F., Atmar, R. L., Hutson, A. M., Estes, M. K., Ruvoën-Clouet, N., et al. (2006). Norwalk Virus–specific binding to oyster digestive tissues. Emerging Infectious Diseases, 12(6), 931–936.

    Article  PubMed Central  PubMed  Google Scholar 

  • Lefèvre, G., Cerovic, L., Milonjic, S., Fédoroff, M., Finne, J., & Jaubertie, A. (2009). Determination of isoelectric points of metals and metallic alloys by adhesion of latex particles. Journal of Colloid Interface Science, 337, 449–455.

    Article  PubMed  Google Scholar 

  • Michels, D. A., Salas-Solano, O., & Felten, C. (2011). Analysys of biopharmaceuticals. Bioprocess International, 9, 48–54.

    CAS  Google Scholar 

  • Michen, B., & Graule, T. (2010). Isoelectric points of viruses. Journal of Applied Microbiology, 109, 388–397.

    CAS  PubMed  Google Scholar 

  • Molodkina, L. M., Chernoberezhskii, Y. M., & Golokova, E. V. (2005). Electrokinetic properties and aggregate stability of nanosized biocolloids—Influenza virus dispersions. Glass Physics and Chemistry, 31(3), 291–300.

    Article  CAS  Google Scholar 

  • Norde, W., & Lyklema, J. (1978). The adsorption of human plasma albumin and bovine pancreas ribonuclease at negatively charged polystyrene surfaces: I. Adsorption isotherms. Effects of charge, ionic strength, and temperature. Journal of Colloid and Interface Science, 66, 257–265.

    Article  CAS  Google Scholar 

  • Patel, M. M., Widdowson, M.-A., Glass, R. I., Akazawa, K., Vinjé, J., & Parashar, U. D. (2008). Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerging Infectious Diseases, 14(8), 1224–1231.

    Article  PubMed Central  PubMed  Google Scholar 

  • Redman, J. A., Grant, S. B., Olson, T. M., Hardy, M. E., & Estes, M. K. (1997). Filtration of recombinant Norwalk Virus particles and bacteriophage MS2 in quartz sand: Importance of electrostatic interactions. Environmental Science and Technology, 31(12), 3378–3383.

    Article  CAS  Google Scholar 

  • Righetti, P. G., & Caravaggio, T. (1976). Isoelectric points and molecular weight of proteins: A table. Journal of Chromatography, 127, 1–28.

    Article  CAS  PubMed  Google Scholar 

  • Scallan, E., Hoekstra, R. M., Angulo, F. J., Tauxe, R. V., Widdowson, M.-A., Roy, S. L., et al. (2011). Foodborne illness acquired in the United States-major pathogens. Emerging Infectious Diseases, 17(1), 7–15.

    Article  PubMed Central  PubMed  Google Scholar 

  • Schaldach, C. M., Bourcier, W. L., Shaw, H. F., Viani, B. E., & Wilson, W. D. (2006). The influence of ionic strength on the interaction of viruses with charged surfaces under environmental conditions. Journal of Colloid Interface Science, 294, 1–10.

    Article  CAS  PubMed  Google Scholar 

  • Schultz, N., Metreveli, G., Franzreb, M., Frimmel, F. H., & Syldatk, C. (2008). Zeta potential measurement as a diagnostic tool in enzyme immobilisation. Colloids and Surfaces B: Biointerfaces, 66, 39–44.

    Article  CAS  PubMed  Google Scholar 

  • Shoemakers, G., van Duijn, E., Crawford, S. E., Uetrech, C., Baclayon, M., Roos, W. H., et al. (2010). Norwalk virus assembly and stability monitored by mass spectrometry. Molecular and Cellular Proteomics, 9(8), 1742–1751.

    Article  Google Scholar 

  • Siebenga, J. J., Vennema, H., Zheng, D.-P., Vinje, J., Lee, B. E., Pang, X.-L., et al. (2009). Norovirus illness is a global problem: emergence and spread of Norovirus GII.4 variants, 2001–2007. Journal of Infectious Diseases, 200, 802–812.

    Article  PubMed  Google Scholar 

  • Stawski, D., & Bellmann, C. (2009). Electrokinetic properties of polypropylene textile fabrics containing deposited layers of polyelectrolytes. Colloids and Surfaces A: Physicochemical and Engineering Aspects, 345, 191–194.

    Article  CAS  Google Scholar 

  • Stuart, C. M. A. (1991). Adsorbed polymers in colloidal system from statics to dynamics. Polymer Journal, 23(5), 669–682.

    Article  CAS  Google Scholar 

  • Vega, E., Smith, J., Garlamd, J., Matos, A., & Pillai, S. D. (2005). Variability of virus attachment patterns to butterhead lettuce. Journal of Food Protection, 68(10), 2112–2117.

    PubMed  Google Scholar 

  • Zheng, D.-P., Ando, T., Fankhauser, R. L., Beard, R. S., Glass, R. I., & Monroe, S. S. (2006). Norovirus classification and proposed strain nomenclature. Virology, 346, 312–323.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors are grateful to the Natural Sciences and Engineering Research Council of Canada (NSERC, #262956) for research grant and to Programme Canadien de Bourses de la Francophonie (PCBF) for scholarship awarded to Idrissa Samandoulgou.

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Samandoulgou, I., Fliss, I. & Jean, J. Zeta Potential and Aggregation of Virus-Like Particle of Human Norovirus and Feline Calicivirus Under Different Physicochemical Conditions. Food Environ Virol 7, 249–260 (2015). https://doi.org/10.1007/s12560-015-9198-0

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