VirusDisease

, Volume 26, Issue 3, pp 123–132 | Cite as

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

  • Aizhan Sabirzhanovna Turmagambetova
  • Nadezhda Sergeevna Sokolova
  • Andrey Pavlinovich Bogoyavlenskiy
  • Vladimir Eleazarovich Berezin
  • Mary Ann Lila
  • Diana M. Cheng
  • Vyacheslav Dushenkov
Original Article

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.

Keywords

Cranberry Polyphenols Flavonoids Anti-viral 

References

  1. 1.
    Andres A, Donovan SM, Kuhlenschmidt MS. Soy isoflavones and virus infections. J Nutr Biochem. 2009;20:563–9.CrossRefPubMedGoogle Scholar
  2. 2.
    Betoret E, Betoret N, Vidal D, Fito P. Functional foods development: trends and technologies. Trends Food Sci Technol. 2011;22:498–508.CrossRefGoogle Scholar
  3. 3.
    Bresee J, Hayden FG. Epidemic influenza—responding to the expected but unpredictable. N Engl J Med. 2013;368:589–92.CrossRefPubMedGoogle Scholar
  4. 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.CrossRefGoogle Scholar
  5. 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.CrossRefPubMedGoogle Scholar
  6. 6.
    Chang A, Dutch RE. Paramyxovirus fusion and entry: multiple paths to a common end. Viruses. 2012;4:613–36.PubMedCentralCrossRefPubMedGoogle Scholar
  7. 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.CrossRefPubMedGoogle Scholar
  8. 8.
    Fang N, Yu S, Badger TM. Comprehensive phytochemical profile of soy protein isolate. J Agric Food Chem. 2004;52:4012–20.CrossRefPubMedGoogle Scholar
  9. 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.CrossRefPubMedGoogle Scholar
  10. 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.CrossRefPubMedGoogle Scholar
  11. 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.PubMedCentralCrossRefPubMedGoogle Scholar
  12. 12.
    Gamblin SJ, Skehel JJ. Influenza hemagglutinin and neuraminidase membrane glycoproteins. J Biol Chem. 2010;285:28403–9.PubMedCentralCrossRefPubMedGoogle Scholar
  13. 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.CrossRefPubMedGoogle Scholar
  14. 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.CrossRefPubMedGoogle Scholar
  15. 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.PubMedCentralCrossRefPubMedGoogle Scholar
  16. 16.
    Howell AB. Cranberry proanthocyanidins and the maintenance of urinary tract health. Crit Rev Food Sci Nutr. 2002;42:273–8.CrossRefPubMedGoogle Scholar
  17. 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. 18.
    Killian ML. Hemagglutination assay for the avian Influenza virus. Methods Mol Biol. 2008;436:47–52.PubMedGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. 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.CrossRefPubMedGoogle Scholar
  21. 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. 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.CrossRefGoogle Scholar
  23. 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.CrossRefPubMedGoogle Scholar
  24. 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.CrossRefPubMedGoogle Scholar
  25. 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.CrossRefGoogle Scholar
  26. 26.
    Pica N, Palese P. Toward a universal influenza virus vaccine: prospects and challenges. Annu Rev Med. 2013;64:189–202.CrossRefPubMedGoogle Scholar
  27. 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.PubMedCentralCrossRefPubMedGoogle Scholar
  28. 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.CrossRefPubMedGoogle Scholar
  29. 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.PubMedGoogle Scholar
  30. 30.
    Reed LJ, Muench H. A simple method of estimating fifty per cent endpoints. Am J Epidemiol. 1938;27:493–7.Google Scholar
  31. 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.PubMedCentralCrossRefPubMedGoogle Scholar
  32. 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.CrossRefPubMedGoogle Scholar
  33. 33.
    Roy A, Saraf S. Limonoids: overview of significant bioactive triterpenes distributed in plants kingdom. Biol Pharm Bull. 2006;29:191–201.CrossRefPubMedGoogle Scholar
  34. 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.CrossRefGoogle Scholar
  35. 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.CrossRefPubMedGoogle Scholar
  36. 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. 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.CrossRefPubMedGoogle Scholar
  38. 38.
    Su Z. Anthocyanins and flavonoids of Vaccinium L. Pharm Crops. 2012;3:7–37.CrossRefGoogle Scholar
  39. 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.CrossRefPubMedGoogle Scholar
  40. 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.PubMedCentralCrossRefPubMedGoogle Scholar
  41. 41.
    Vorsa N, Johnson-Cicalese J. American cranberry. In: Badenes ML, Byrne DH, editors. Fruit breeding. New York: Springer; 2012. p. 191–223.CrossRefGoogle Scholar
  42. 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.CrossRefPubMedGoogle Scholar

Copyright information

© Indian Virological Society 2015

Authors and Affiliations

  • Aizhan Sabirzhanovna Turmagambetova
    • 1
  • Nadezhda Sergeevna Sokolova
    • 1
  • Andrey Pavlinovich Bogoyavlenskiy
    • 1
  • Vladimir Eleazarovich Berezin
    • 1
  • Mary Ann Lila
    • 2
  • Diana M. Cheng
    • 3
  • Vyacheslav Dushenkov
    • 4
  1. 1.Institute of Microbiology and VirologyAlmatyKazakhstan
  2. 2.Plants for Human Health InstituteNorth Carolina State UniversityKannapolisUSA
  3. 3.Department of Plant Biology and Pathology, RutgersThe State University of New JerseyNew BrunswickUSA
  4. 4.Hostos Community CollegeCity University of New YorkBronxUSA

Personalised recommendations