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Green tea cultivar ‘Benifuuki’ potentiates split vaccine-induced immunoglobulin A production

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Abstract

Influenza is a widespread disease caused by infection with the influenza virus. Vaccination is considered to be the main countermeasure against influenza. A split vaccine is widely used to avoid severe adverse events, and it induces strong humoral immunity. However, the split vaccine alone cannot elicit mucosal immunity, including IgA production, and its preventative effects are limited. Here, we show that the green tea cultivar ‘Benifuuki’ extract enhanced the effect of a split vaccine on mucosal immunity. The frequency of IgA+ cells was increased in lung and Peyer’s patch that received Benifuuki diet. Secretion of hemagglutinin-specific mucosal IgA, which is closely linked to the prevention of viral infection, was significantly increased in the bronchoalveolar lavage fluid of split vaccine-immunized BALB/c mice that were administered green tea Benifuuki extract. Our findings suggest that Benifuuki intake enhanced the effects of the split vaccine on mucosal immunity.

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References

  1. Centers for Disease Control and Prevention (CDC) (2010) Estimates of deaths associated with seasonal influenza—United States, 1976–2007. MMWR Morb Mortal Wkly Rep 59:1057–1062

    Google Scholar 

  2. Thompson WW, Shay DK, Weintraub E, Brammer L, Cox N, Anderson LJ, Fukuda K (2003) Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 289:179–186

    Article  PubMed  Google Scholar 

  3. Koyama S, Aoshi T, Tanimoto T, Kumagai Y, Kobiyama K, Tougan T, Sakurai K, Coban C, Horii T, Akira S, Ishii KJ (2010) Plasmacytoid dendritic cells delineate immunogenicity of influenza vaccine subtypes. Sci Transl Med 2:25ra24

    Article  PubMed  Google Scholar 

  4. Wong SS, Webby RJ (2013) Traditional and new influenza vaccines. Clin Microbiol Rev 26:476–492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Chen D, Periwal SB, Larrivee K, Zuleger C, Erickson CA, Endres RL, Payne LG (2001) Serum and mucosal immune responses to an inactivated influenza virus vaccine induced by epidermal powder immunization. J Virol 75:7956–7965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Mantis NJ, Rol N, Corthésy B (2011) Secretory IgA’s complex roles in immunity and mucosal homeostasis in the gut. Mucosal Immunol 4:603–611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Proudfoot O, Esparon S, Tang CK, Laurie K, Barr I, Pietersz G (2015) Mannan adjuvants intranasally administered inactivated influenza virus in mice rendering low doses inductive of strong serum IgG and IgA in the lung. BMC Infect Dis 15:101

    Article  PubMed  PubMed Central  Google Scholar 

  8. Le TV, Mironova E, Garcin D, Compans RW (2011) Induction of influenza-specific mucosal immunity by an attenuated recombinant Sendai virus. PLoS One 6:e18780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Fagarasan S, Honjo T (2003) Intestinal IgA synthesis: regulation of front-line body defences. Nat Rev Immunol 3:63–72

    Article  CAS  PubMed  Google Scholar 

  10. Dougan SK, Ashour J, Karssemeijer RA, Popp MW, Avalos AM, Barisa M, Altenburg AF, Ingram JR, Cragnolini JJ, Guo C, Alt FW, Jaenisch R, Ploegh HL (2013) Antigen-specific B-cell receptor sensitizes B cells to infection by influenza virus. Nature 503:406–409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Imai K, Suga K, Nakachi K (1997) Cancer-preventive effects of drinking green tea among a Japanese population. Prev Med 26:769–775

    Article  CAS  PubMed  Google Scholar 

  12. Baba Y, Sonoda JI, Hayashi S, Tosuji N, Sonoda S, Makisumi K, Nakajo M (2012) Reduction of oxidative stress in liver cancer patients by oral green tea polyphenol tablets during hepatic arterial infusion chemotherapy. Exp Ther Med 4:452–458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Stoicov C, Saffari R, Houghton J (2009) Green tea inhibits Helicobacter growth in vivo and in vitro. Int J Antimicrob Agents 33:473–478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Kim YJ, Houng SJ, Kim JH, Kim YR, Ji HG, Lee SJ (2012) Nanoemulsified green tea extract shows improved hypocholesterolemic effects in C57BL/6 mice. J Nutr Biochem 23:186–191

    Article  CAS  PubMed  Google Scholar 

  15. Yung LM, Leung FP, Wong WT, Tian XY, Yung LH, Chen ZY, Yao XQ, Huang Y (2008) Tea polyphenols benefit vascular function. Inflammopharmacology 16:230–234

    Article  CAS  PubMed  Google Scholar 

  16. Hotta Y, Huang L, Muto T, Yajima M, Miyazeki K, Ishikawa N, Fukuzawa Y, Wakida Y, Tushima H, Ando H, Nonogaki T (2006) Positive inotropic effect of purified green tea catechin derivative in guinea pig hearts: the measurements of cellular Ca2+ and nitric oxide release. Eur J Pharmacol 552:123–130

    Article  CAS  PubMed  Google Scholar 

  17. Marathe SA, Datey AA, Chakravortty D (2012) Herbal cocktail as anti-infective: promising therapeutic for the treatment of viral diseases. Recent Pat Antiinfect Drug Discov 7:123–132

    Article  CAS  PubMed  Google Scholar 

  18. Tsukamoto S, Huang Y, Umeda D, Yamada S, Yamashita S, Kumazoe M, Kim Y, Murata M, Yamada K, Tachibana H (2014) 67-kDa laminin receptor-dependent protein phosphatase 2A (PP2A) activation elicits melanoma-specific antitumor activity overcoming drug resistance. J Bio Chem 289:32671–32681

    Article  CAS  Google Scholar 

  19. Suzuki T, Kumazoe M, Kim Y, Yamashita S, Nakahara K, Tsukamoto S, Sasaki M, Hagihara T, Tsurudome Y, Huang Y, Maeda-Yamamoto M, Shinoda Y, Yamaguchi W, Yamada K, Tachibana H (2013) Green tea extract containing a highly absorbent catechin prevents diet-induced lipid metabolism disorder. Sci Rep 3:2749

    Article  PubMed  PubMed Central  Google Scholar 

  20. Yoshino K, Miyase T, Sano M (2010) Preventive effects of C-2 epimeric isomers of tea catechins on mouse type I allergy. J Nutr Sci Vitaminol (Tokyo) 56:211–215

    Article  CAS  Google Scholar 

  21. Persson IA, Josefsson M, Persson K, Andersson RG (2006) Tea flavanols inhibit angiotensin-converting enzyme activity and increase nitric oxide production in human endothelial cells. J Pharm Pharmacol 58:1139–1144

    Article  CAS  PubMed  Google Scholar 

  22. Maeda-Yamamoto M, Ema K, Tokuda Y, Monobe M, Tachibana H, Sameshima Y, Kuriyama S (2011) Effect of green tea powder (Camellia sinensis L. cv. Benifuuki) particle size on O-methylated EGCG absorption in rats; The Kakegawa Study. Cytotechnology 63:171–179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Maeda-Yamamoto M, Ema K, Monobe M, Tokuda Y, Tachibana H (2012) Epicatechin-3-O-(3″-O-methyl)-gallate content in various tea cultivars (Camellia sinensis L.) and its in vitro inhibitory effect on histamine release. J Agric Food Chem 60:2165–2170

    Article  CAS  PubMed  Google Scholar 

  24. Kurita I, Maeda-Yamamoto M, Tachibana H, Kamei M (2010) Antihypertensive effect of Benifuuki tea containing O-methylated EGCG. J Agric Food Chem 58:1903–1908

    Article  CAS  PubMed  Google Scholar 

  25. Maeda-Yamamoto M, Ema K, Shibuichi I (2007) In vitro and in vivo anti-allergic effects of ‘benifuuki’ green tea containing O-methylated catechin and ginger extract enhancement. Cytotechnology 55:135–142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Maeda-Yamamoto M, Ema K, Monobe M, Shibuichi I, Shinoda Y, Yamamoto T, Fujisawa T (2009) The efficacy of early treatment of seasonal allergic rhinitis with benifuuki green tea containing O-methylated catechin before pollen exposure: an open randomized study. Allergol Int 58:437–444

    Article  CAS  PubMed  Google Scholar 

  27. Albu DI, Jones-Trower A, Woron AM, Stellrecht K, Broder CC, Metzger DW (2003) Intranasal vaccination using interleukin-12 and cholera toxin subunit B as adjuvants to enhance mucosal and systemic immunity to human immunodeficiency virus type 1 glycoproteins. J Virol 77:5589–5597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. van Riet E, Ainai A, Suzuki T, Hasegawa H (2012) Mucosal IgA responses in influenza virus infections; thoughts for vaccine design. Vaccine 30:5893–5900

    Article  PubMed  Google Scholar 

  29. Cao W, Liu YJ (2007) Innate immune functions of plasmacytoid dendritic cells. Curr Opin Immunol 19:24–30

    Article  PubMed  Google Scholar 

  30. Stöhr K (2002) Influenza—WHO cares. Lancet Infect Dis 2:517

    Article  PubMed  Google Scholar 

  31. Nichol KL, Treanor JJ (2006) Vaccines for seasonal and pandemic influenza. J Infect Dis 194:S111–S118

    Article  PubMed  Google Scholar 

  32. Russell CA, Jones TC, Barr IG, Cox NJ, Garten RJ, Gregory V, Gust ID, Hampson AW, Hay AJ, Hurt AC, de Jong JC, Kelso A, Klimov AI, Kageyama T, Komadina N, Lapedes AS, Lin YP, Mosterin A, Obuchi M, Odagiri T, Osterhaus AD, Rimmelzwaan GF, Shaw MW, Skepner E, Stohr K, Tashiro M, Fouchier RA, Smith DJ (2008) The global circulation of seasonal influenza A (H3N2) viruses. Science 320:340–346

    Article  CAS  PubMed  Google Scholar 

  33. Durham MD, Buchacz K, Armon C, Patel P, Wood K, Brooks JT; HIV Outpatient Study (HOPS) Investigators (2015) Seasonal influenza vaccination rates in the HIV outpatient study—United States, 1999–2013. Clin Infect Dis 60:976–977

    Article  PubMed  Google Scholar 

  34. Weber C, Sliva K, von Rhein C, Kümmerer BM, Schnierle BS (2015) The green tea catechin, epigallocatechin gallate inhibits chikungunya virus infection. Antiviral Res 113:1–3

    Article  CAS  PubMed  Google Scholar 

  35. Huang HC, Tao MH, Hung TM, Chen JC, Lin ZJ, Huang C (2014) (−)-Epigallocatechin-3-gallate inhibits entry of hepatitis B virus into hepatocytes. Antiviral Res 111:100–111

    Article  CAS  PubMed  Google Scholar 

  36. Ahmed M, Henson DA, Sanderson MC, Nieman DC, Gillitt ND, Lila MA (2014) The protective effects of a polyphenol-enriched protein powder on exercise-induced susceptibility to virus infection. Phytother Res 28:1829–1836

    Article  CAS  PubMed  Google Scholar 

  37. Pang JY, Zhao KJ, Wang JB, Ma ZJ, Xiao XH (2014) Green tea polyphenol, epigallocatechin-3-gallate, possesses the antiviral activity necessary to fight against the hepatitis B virus replication in vitro. J Zhejiang Univ Sci B 15:533–539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Kim M, Kim SY, Lee HW, Shin JS, Kim P, Jung YS, Jeong HS, Hyun JK, Lee CK (2013) Inhibition of influenza virus internalization by (−)-epigallocatechin-3-gallate. Antiviral Res 100:460–472

    Article  CAS  PubMed  Google Scholar 

  39. Suzuki Y (2005) Sialobiology of influenza: molecular mechanism of host range variation of influenza viruses. Biol Pharm Bull 28:399–408

    Article  CAS  PubMed  Google Scholar 

  40. Kuno-Sakai H, Kimura M, Ohta K, Shimojima R, Oh Y, Fukumi H (1994) Developments in mucosal influenza virus vaccines. Vaccine 12:1303–1310

    Article  CAS  PubMed  Google Scholar 

  41. Sawaengsak C, Mori Y, Yamanishi K, Mitrevej A, Sinchaipanid N (2014) Chitosan nanoparticle encapsulated hemagglutinin-split influenza virus mucosal vaccine. AAPS PharmSciTech 15:317–325

    Article  CAS  PubMed  Google Scholar 

  42. de Haan A, Haijema BJ, Voorn P, Meijerhof T, van Roosmalen ML, Leenhouts K (2012) Bacterium-like particles supplemented with inactivated influenza antigen induce cross-protective influenza-specific antibody responses through intranasal administration. Vaccine 30:4884–4891

    Article  PubMed  Google Scholar 

  43. Ichinohe T, Lee HK, Ogura Y, Flavell R, Iwasaki A (2009) Inflammasome recognition of influenza virus is essential for adaptive immune responses. J Exp Med 206:79–87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was kindly supported in part by Grants-in-Aid for Scientific Research (KAKENHI) from the Japan Society for the Promotion of Science to H. Tachibana (Grant Numbers 22228002 and 15H02448).

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Authors and Affiliations

  1. Division of Applied Biological Chemistry, Department of Bioscience and Biotechnology, Faculty of Agriculture, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka, 812-8581, Japan

    Yeong-Seon Won, Motofumi Kumazoe, Kanako Takamatsu & Hirofumi Tachibana

  2. Products Research and Development Laboratory, Asahi Soft Drinks Co., Ltd., Ibaraki, 302-0106, Japan

    Yuki Shinoda, Saki Sonoda, Kenji Okada & Takehisa Okamoto

Authors
  1. Yeong-Seon Won
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  2. Motofumi Kumazoe
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Correspondence to Hirofumi Tachibana.

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Won, YS., Kumazoe, M., Takamatsu, K. et al. Green tea cultivar ‘Benifuuki’ potentiates split vaccine-induced immunoglobulin A production. J Nat Med 71, 68–75 (2017). https://doi.org/10.1007/s11418-016-1028-7

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  • DOI: https://doi.org/10.1007/s11418-016-1028-7

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