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New functionally-enhanced soy proteins as food ingredients with anti-viral activity

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Abstract

Respiratory viruses are a major public health problem because of their prevalence and high morbidity rate leading to considerable social and economic implications. Cranberry has therapeutic potential attributed to a comprehensive list of phytochemicals including anthocyanins, flavonols, and unique A-type proanthocyanidins. Soy flavonoids, including isoflavones, have demonstrated anti-viral effects in vitro and in vivo. Recently, it was demonstrated that edible proteins can efficiently sorb and concentrate cranberry polyphenols, including anthocyanins and proanthocyanins, providing greatly stabilized matrices suitable for food products. The combination of cranberry and soy phytoactives may be an effective dietary anti-viral resource. Anti-viral properties of both cranberry juice-enriched and cranberry pomace polyphenol-enriched soy protein isolate (CB-SPI and CBP-SPI) were tested against influenza viruses (H7N1, H5N3, H3N2), Newcastle disease virus and Sendai virus in vitro and in ovo. In our experiments, preincubation with CB-SPI or CBP-SPI resulted in inhibition of virus adsorption to chicken red blood cells and reduction in virus nucleic acid content up to 16-fold, however, CB-SPI and CBP-SPI did not affect hemagglutination. Additionally, CB-SPI and CBP-SPI inhibited viral replication and infectivity more effectively than the commercially available anti-viral drug Amizon. Results suggest CB-SPI and CBP-SPI may have preventative and therapeutic potential against viral infections that cause diseases of the respiratory and gastro-intestinal tract.

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References

  1. Andres A, Donovan SM, Kuhlenschmidt MS. Soy isoflavones and virus infections. J Nutr Biochem. 2009;20:563–9.

    Article  CAS  PubMed  Google Scholar 

  2. Betoret E, Betoret N, Vidal D, Fito P. Functional foods development: trends and technologies. Trends Food Sci Technol. 2011;22:498–508.

    Article  CAS  Google Scholar 

  3. Bresee J, Hayden FG. Epidemic influenza—responding to the expected but unpredictable. N Engl J Med. 2013;368:589–92.

    Article  CAS  PubMed  Google Scholar 

  4. Bukhtiarova TA, Trinus FP, Danilenko VF, Danilenko GI, Ovrutskii VM, Sharykina NI. Structure and antiinflammatory activity of isonicotinic and nicotinic amides. Pharm Chem J. 1997;31:597–9.

    Article  Google Scholar 

  5. Chan C, Lin K, Chan Y, Wang Y, Chi Y, Tu H, Shieh H, Liu W. Amplification of the entire genome of influenza A virus H1N1 and H3N2 subtypes by reverse-transcription polymerase chain reaction. J Virol Methods. 2006;136:38–43.

    Article  CAS  PubMed  Google Scholar 

  6. Chang A, Dutch RE. Paramyxovirus fusion and entry: multiple paths to a common end. Viruses. 2012;4:613–36.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  7. De Bruyne T, Pieters L, Witvrouw M, De Clercq E, Berge V, Vlietinck A. Biological evaluation of proanthocyanidin dimers and related polyphenols. J Nat Prod. 1999;62(7):954–8.

    Article  PubMed  Google Scholar 

  8. Fang N, Yu S, Badger TM. Comprehensive phytochemical profile of soy protein isolate. J Agric Food Chem. 2004;52:4012–20.

    Article  CAS  PubMed  Google Scholar 

  9. Foo LY, Lu Y, Howell AB, Vorsa N. The structure of cranberry proanthocyanidins which inhibit adherence of uropathogenic P-fimbriated Escherichia coli in vitro. Phytochemistry. 2000;54:173.

    Article  CAS  PubMed  Google Scholar 

  10. Foo LY, Lu Y, Howell AB, Vorsa N. A-type proanthocyanidin trimers from cranberry that Inhibit adherence of uropathogenic P-fimbriated Escherichia coli. J Nat Prod. 2000;63:1225–8.

    Article  CAS  PubMed  Google Scholar 

  11. Francis T, Pearson HE, Salk JE, Brown PN. Immunity in human subjects artificially infected with influenza virus, Type B. Am J Public Health Nations Health. 1944;34:317–34.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Gamblin SJ, Skehel JJ. Influenza hemagglutinin and neuraminidase membrane glycoproteins. J Biol Chem. 2010;285:28403–9.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  13. Georgi L, Johnson-Cicalese J, Honig J, Das S, Rajah V, Bhattacharya D, Bassil N, Rowland L, Polashock J, Vorsa N. The first genetic map of the American cranberry: exploration of synteny conservation and quantitative trait loci. Theor Appl Genet. 2013;126:673–92.

    Article  CAS  PubMed  Google Scholar 

  14. Grace MH, Massey AR, Mbeunkui F, Yousef GG, Lila MA. Comparison of health-relevant flavonoids in commonly consumed cranberry products. J Food Sci. 2012;77:H176–83.

    Article  CAS  PubMed  Google Scholar 

  15. Grace M, Guzman I, Roopchand ED, Moskal K, Cheng MD, Pogrebnyak N, Raskin I, Howell A, Lila MA. Stable binding of alternative protein-enriched food matrices with concentrated cranberry bioflavonoids for functional food applications. J Agric Food Chem. 2013;61:6856–64.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. Howell AB. Cranberry proanthocyanidins and the maintenance of urinary tract health. Crit Rev Food Sci Nutr. 2002;42:273–8.

    Article  CAS  PubMed  Google Scholar 

  17. Kapczynski DR, Afonso CL, Miller PJ. Immune responses of poultry to newcastle disease virus. Dev Comp Immunol. 2013;. doi:10.1016/j.dci.2013.04.012.

    Google Scholar 

  18. Killian ML. Hemagglutination assay for the avian Influenza virus. Methods Mol Biol. 2008;436:47–52.

    CAS  PubMed  Google Scholar 

  19. Klimov A, Balish A, Veguilla V, Sun H, Schiffer J, Lu X, Katz JM, Hancock K. Influenza virus titration, antigenic characterization, and serological methods for antibody detection. Influenza Virus. 2012;865:25–51.

    Article  CAS  Google Scholar 

  20. Lipson S, Sethi L, Cohen P, Gordon R, Tan I, Burdowski A, Stotzky G. Antiviral effects on bacteriophages and rotavirus by cranberry juice. Phytomedicine. 2007;14:23–30.

    Article  CAS  PubMed  Google Scholar 

  21. Morodomi Y, Inoue M, Hasegawa M, Okamoto T, Maehara Y, Yonemitsu Y. Sendai virus-based oncolytic gene therapy. In: Wei M, Good D, editors. Novel gene therapy approaches. Rijeka: InTech Publisher; 2013. p. 183–94.

    Google Scholar 

  22. Nesterova N, Zagorodnya S, Danilenko V, Baranova G, Golovan A. Studying of anti-epstein–barr virus activity of amizon and their derivative. Antiviral Res. 2008;78:A61.

    Article  Google Scholar 

  23. Oiknine-Djian E, Houri-Haddad Y, Weiss EI, Ofek I, Greenbaum E, Hartshorn K, Zakay-Rones Z. High molecular weight constituents of cranberry interfere with influenza virus neuraminidase activity. Planta Med. 2012;78:962–7.

    Article  CAS  PubMed  Google Scholar 

  24. Pappas E, Schaich K. Phytochemicals of cranberries and cranberry products: characterization, potential health effects, and processing stability. Crit Rev Food Sci Nutr. 2009;49:741–81.

    Article  CAS  PubMed  Google Scholar 

  25. Pedersen J. Hemagglutination-Inhibition test for avian influenza virus subtype identification and the detection and quantitation of serum antibodies to the avian influenza virus. In: Spackman E, editor. avian influenza virus. Totowa: Humana Press; 2008. p. 53–66.

    Chapter  Google Scholar 

  26. Pica N, Palese P. Toward a universal influenza virus vaccine: prospects and challenges. Annu Rev Med. 2013;64:189–202.

    Article  CAS  PubMed  Google Scholar 

  27. Poehling KA, Edwards KM, Griffin MR, Szilagyi PG, Staat MA, Iwane MK, Snively BM, Suerken CK, Hall CB, Weinberg GA. The burden of influenza in young children, 2004–2009. Pediatrics. 2013;131:207–16.

    Article  PubMed Central  PubMed  Google Scholar 

  28. Poulakou G, Pérez M, Rello J. Severe acute respiratory infections in the postpandemic era of H1N1. Curr Opin Crit Care. 2012;18:441–50.

    Article  PubMed  Google Scholar 

  29. Radulovic NS, Blagojevic PD, Stojanovic-Radic ZZ, Stojanovic NM. Antimicrobial plant metabolites: structural diversity and mechanism of action. Curr Med Chem. 2013;20:932–52.

    CAS  PubMed  Google Scholar 

  30. Reed LJ, Muench H. A simple method of estimating fifty per cent endpoints. Am J Epidemiol. 1938;27:493–7.

    Google Scholar 

  31. Roopchand DE, Grace M, Kuhn P, Cheng DM, Plundrich N, Poulev A, Howell A, Fridlender B, Lila MA, Raskin I. Efficient sorption of polyphenols to soybean flour enables natural fortification of foods. Food Chem. 2012;131:1193–200.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Roopchand DE, Krueger CG, Moskal K, Fridlender B, Lila MA, Raskin I. Food-compatible method for the efficient extraction and stabilization of cranberry pomace polyphenols. Food Chem. 2013;141:3664–9.

    Article  CAS  PubMed  Google Scholar 

  33. Roy A, Saraf S. Limonoids: overview of significant bioactive triterpenes distributed in plants kingdom. Biol Pharm Bull. 2006;29:191–201.

    Article  CAS  PubMed  Google Scholar 

  34. Serkedjieva J, Toshkova R, Antonova-Nikolova S, Stefanova T, Teodosieva A, Ivanova I. Effect of a plant polyphenol-rich extract on the lung protease activities of influenza-virus-infected mice. Antiviral Chem Chemother. 2007;18:75–82.

    Article  CAS  Google Scholar 

  35. Shmuely H, Ofek I, Weiss EI, Rones Z, Houri-Haddad Y. Cranberry components for the therapy of infectious disease. Curr Opin Biotechnol. 2012;23:148–52.

    Article  CAS  PubMed  Google Scholar 

  36. Singleton VL, Orthofer R, Lamuela-Raventós RM. Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. In: Lester P, editor. Methods in enzymology. New York: Academic Press; 1999. p. 152–78.

    Google Scholar 

  37. Spalatin J, Hanson RP, Beard PD. The hemagglutination-elution pattern as a marker in characterizing newcastle disease virus. Avian Dis. 1970;14:542–9.

    Article  CAS  PubMed  Google Scholar 

  38. Su Z. Anthocyanins and flavonoids of Vaccinium L. Pharm Crops. 2012;3:7–37.

    Article  CAS  Google Scholar 

  39. Su X, Howell AB, D’Souza DH. The effect of cranberry juice and cranberry proanthocyanidins on the infectivity of human enteric viral surrogates. Food Microbiol. 2010;27:535–40.

    Article  CAS  PubMed  Google Scholar 

  40. Tao Y, Pinzón-Arango PA, Howell AB, Camesano TA. Oral consumption of cranberry juice cocktail inhibits molecular-scale adhesion of clinical uropathogenic Escherichia Coli. J Med Food. 2011;14:739–45.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  41. Vorsa N, Johnson-Cicalese J. American cranberry. In: Badenes ML, Byrne DH, editors. Fruit breeding. New York: Springer; 2012. p. 191–223.

    Chapter  Google Scholar 

  42. Weiss EI, Houri-Haddad Y, Greenbaum E, Hochman N, Ofek I, Zakay-Rones Z. Cranberry juice constituents affect influenza virus adhesion and infectivity. Antiviral Res. 2005;66:9–12.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Grants 0113PK00473 and 0114PK00303 from the Ministry of Education and Science of the Republic of Kazakhstan, Grant PSC-CUNY 66638-00 44 and an SBIR Phase 1 grant from the National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases, Grant 1R43DK092104-01A1. Diana M. Cheng was supported by NIH training grant T32: 5T32AT004094-04.

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Correspondence to Aizhan Sabirzhanovna Turmagambetova.

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Turmagambetova, A.S., Sokolova, N.S., Bogoyavlenskiy, A.P. et al. New functionally-enhanced soy proteins as food ingredients with anti-viral activity. VirusDis. 26, 123–132 (2015). https://doi.org/10.1007/s13337-015-0268-6

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  • DOI: https://doi.org/10.1007/s13337-015-0268-6

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