Effects of heat-killed Lactococcus lactis subsp. lactis JCM 5805 on mucosal and systemic immune parameters, and antiviral reactions to influenza virus in healthy adults; a randomized controlled double-blind study

Journal of Functional Foods

Volumn 35, Issue , 2017, Pages 513-521

  Fujii, Toshio ^a   Jounai, Kenta ^b   Horie, Akira ^a   Takahashi, Hitoshi ^c   Suzuki, Hiroaki ^a   Ohshio, Konomi ^a   Fujiwara, Daisuke ^a   Yamamoto, Norio ^c,d  

^a KIRIN HOLDINGS CO LTD   (Japan)

^b Shizukuishi Iwate Gun   (Japan)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^d JUNTENDO UNIVERSITY   (Japan)

Author keywords

Immunoglobulin A; Influenza virus; Lactococcus lactis subsp. lactis JCM 5805; Phagocytic activity of neutrophil; Plasmacytoid dendritic cell; Type I interferon

Indexed keywords

EID: 85020825115     PISSN: 17564646     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jff.2017.06.011     Document Type: Article

References (46)

1. Abdallah, F., Hassanin, O., Positive regulation of humoral and innate immune responses induced by inactivated Avian Influenza Virus vaccine in broiler chickens. Veterinary Research Communications 39:1573–7446 (Electronic) (2015), 211–216.
2. Dalpke, A.H., Zimmermann, S., Albrecht, I., Heeg, K., Phosphodiester CpG oligonucleotides as adjuvants: Polyguanosine runs enhance cellular uptake and improve immunostimulative activity of phosphodiester CpG oligonucleotides in vitro and in vivo. Immunology 106:1 (2002), 102–112.
3. de Almada, C.N., Almada, C.N., Martinez, R.C.R., Sant'Ana, A.S., Paraprobiotics: Evidences on their ability to modify biological responses, inactivation methods and perspectives on their application in foods. Trends in Food Science & Technology 58 (2016), 96–114.
4. Ericson, D., Hamberg, K., Bratthall, G., Sinkiewicz-Enggren, G., Ljunggren, L., Salivary IgA response to probiotic bacteria and mutans streptococci after the use of chewing gum containing Lactobacillus reuteri. Pathogens and Disease 68:3 (2013), 82–87.
5. Fujii, T., Tomita, Y., Ikushima, S., Horie, A., Fujiwara, D., Draft genome sequence of Lactococcus lactis subsp. lactis JCM 5805(T), a strain that induces plasmacytoid dendritic cell activation. Genome Announcements 3:2 (2015), e00113–e00115.
6. Fujiwara, D., Inoue, S., Wakabayashi, H., Fujii, T., The anti-allergic effects of lactic acid bacteria are strain dependent and mediated by effects on both Th1/Th2 cytokine expression and balance. International Archives of Allergy and Immunology 135:3 (2004), 205–215.
7. Fukushima, Y., Miyaguchi, S., Yamano, T., Kaburagi, T., Iino, H., Ushida, K., Sato, K., Improvement of nutritional status and incidence of infection in hospitalised, enterally fed elderly by feeding of fermented milk containing probiotic Lactobacillus johnsonii La1 (NCC533). British Journal of Nutrition 98:5 (2007), 969–977.
8. Goto, H., Sagitani, A., Ashida, N., Kato, S., Hirota, T., Shinoda, T., Yamamoto, N., Anti-influenza virus effects of both live and non-live Lactobacillus acidophilus L-92 accompanied by the activation of innate immunity. British Journal of Nutrition 110:10 (2013), 1810–1818.
9. Hefti, H.P., Frese, M., Landis, H., Di Paolo, C., Aguzzi, A., Haller, O., Pavlovic, J., Human MxA protein protects mice lacking a functional alpha/beta interferon system against La Crosse virus and other lethal viral infections. Journal of Virology 73:8 (1999), 6984–6991.
10. Hirose, Y., Murosaki, S., Yamamoto, Y., Yoshikai, Y., Tsuru, T., Daily intake of heat-killed Lactobacillus plantarum L-137 augments acquired immunity in healthy adults. The Journal of Nutrition 136:12 (2006), 3069–3073.
11. Honda, K., Ohba, Y., Yanai, H., Negishi, H., Mizutani, T., Takaoka, A., Taniguchi, T., Spatiotemporal regulation of MyD88-IRF-7 signalling for robust type-I interferon induction. Nature 434:7036 (2005), 1035–1040.
12. Horisberger, M.A., Hochkeppel, H.K., IFN-alpha induced human 78 kD protein: Purification and homologies with the mouse Mx protein, production of monoclonal antibodies, and potentiation effect of IFN-gamma. Journal of Interferon Research 7:4 (1987), 331–343.
13. Hovanessian, A.G., Interferon-induced and double-stranded RNA-activated enzymes: A specific protein kinase and 2',5'-oligoadenylate synthetases. Journal of Interferon Research 11:4 (1991), 199–205.
14. Izumo, T., Maekawa, T., Ida, M., Noguchi, A., Kitagawa, Y., Shibata, H., Kiso, Y., Effect of intranasal administration of Lactobacillus pentosus S-PT84 on influenza virus infection in mice. International Immunopharmacology 10:9 (2010), 1101–1106.
15. Jounai, K., Ikado, K., Sugimura, T., Ano, Y., Braun, J., Fujiwara, D., Spherical lactic acid bacteria activate plasmacytoid dendritic cells immunomodulatory function via TLR9-dependent crosstalk with myeloid dendritic cells. PLoS ONE, 7(4), 2012, e32588.
16. Jounai, K., Sugimura, T., Ohshio, K., Fujiwara, D., Oral administration of Lactococcus lactis subsp. lactis JCM5805 enhances lung immune response resulting in protection from murine parainfluenza virus infection. PLoS ONE, 10(3), 2015, e0119055.
17. Kalliomäki, M., Salminen, S., Arvilommi, H., Kero, P., Koskinen, P., Isolauri, E., Probiotics in primary prevention of atopic disease: A randomised placebo-controlled trial. The Lancet 357:9262 (2001), 1076–1079.
18. Kawase, M., He, F., Kubota, A., Yoda, K., Miyazawa, K., Hiramatsu, M., Heat-killed Lactobacillus gasseri TMC0356 protects mice against influenza virus infection by stimulating gut and respiratory immune responses. FEMS Immunology and Medical Microbiology 64:2 (2012), 280–288.
19. Kimoto-Nira, H., Aoki, R., Sasaki, K., Suzuki, C., Mizumachi, K., Oral intake of heat-killed cells of Lactococcus lactis strain H61 promotes skin health in women. Journal of Nutritional Science 1 (2012), 1–7.
20. Kimoto-Nira, H., Nagakura, Y., Kodama, C., Shimizu, T., Okuta, M., Sasaki, K., Suzuki, Y., Effects of ingesting milk fermented by Lactococcus lactis H61 on skin health in young women: A randomized double-blind study. Journal of Dairy Science 97:9 (2014), 5898–5903.
21. Klijn, N., Weerkamp, A.H., de Vos, W.M., Detection and characterization of lactose-utilizing Lactococcus spp. in natural ecosystems. Applied and Environmental Microbiology 61:2 (1995), 788–792.
22. Kotani, Y., Kunisawa, J., Suzuki, Y., Sato, I., Saito, T., Toba, M., Kiyono, H., Role of Lactobacillus pentosus strain b240 and the Toll-like receptor 2 axis in Peyer's patch dendritic cell-mediated immunoglobulin A enhancement. PLoS ONE, 9(3), 2014, e91857.
23. Kotani, Y., Shinkai, S., Okamatsu, H., Toba, M., Ogawa, K., Yoshida, H., Kohda, N., Oral intake of Lactobacillus pentosus strain b240 accelerates salivary immunoglobulin A secretion in the elderly: A randomized, placebo-controlled, double-blind trial. Immunity & Ageing, 7, 2010, 11.
24. Martin, L.B., Weil, Z.M., Nelson, R.J., Seasonal changes in vertebrate immune activity: Mediation by physiological trade-offs. Philosophical Transactions of the Royal Society of London B: Biological Sciences 363:1490 (2008), 321–339.
25. Mendonça, F.H., Santos, S.S., Faria, I.d.S., Gonçalves e Silva, C.R., Jorge, A.O., Leão, M.V., Effects of probiotic bacteria on Candida presence and IgA anti-Candida in the oral cavity of elderly. Brazilian Dental Journal 23 (2012), 534–538.
26. Miyazawa, K., Kawase, M., Kubota, A., Yoda, K., Harata, G., Hosoda, M., He, F., Heat-killed Lactobacillus gasseri can enhance immunity in the elderly in a double-blind, placebo-controlled clinical study. Beneficial Microbes 6:4 (2015), 441–449.
27. Obayashi, K., Salivary mental stress proteins. Clinica Chimica Acta 425 (2013), 196–201.
28. Parcina, M., Wendt, C., Goetz, F., Zawatzky, R., Zähringer, U., Heeg, K., Bekeredjian-Ding, I., Staphylococcus aureus-induced plasmacytoid dendritic cell activation is based on an IgG-mediated memory response. The Journal of Immunology 181:6 (2008), 3823–3833.
29. Ramirez-Ortiz, Z.G., Lee, C.K., Wang, J.P., Boon, L., Specht, C.A., Levitz, S.M., A nonredundant role for plasmacytoid dendritic cells in host defense against the human fungal pathogen Aspergillus fumigatus. Cell Host & Microbe 9:5 (2011), 415–424.
30. Roller, M., Clune, Y., Collins, K., Rechkemmer, G., Watzl, B., Consumption of prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis has minor effects on selected immune parameters in polypectomised and colon cancer patients. British Journal of Nutrition 97:4 (2007), 676–684.
31. Sadler, A.J., Williams, B.R.G., Interferon-inducible antiviral effectors. Nature Reviews. Immunology 8:7 (2008), 559–568.
32. Shibata, T., Kanayama, M., Haida, M., Fujimoto, S., Oroguchi, T., Sata, K., Ishii, N., Lactococcus lactis JCM5805 activates anti-viral immunity and reduces symptoms of common cold and influenza in healthy adults in a randomized controlled trial. Journal of Functional Foods 24 (2016), 492–500.
33. Siegal, F.P., Kadowaki, N., Shodell, M., Fitzgerald-Bocarsly, P.A., Shah, K., Ho, S., Liu, Y.-J., The nature of the principal type 1 interferon-producing cells in human blood. Science 284:5421 (1999), 1835–1837.
34. Spanhaak, S., Havenaar, R., Schaafsma, G., The effect of consumption of milk fermented by Lactobacillus casei strain Shirota on the intestinal microflora and immune parameters in humans. European Journal of Clinical Nutrition 52:12 (1998), 899–907.
35. Stockinger, S., Kastner, R., Kernbauer, E., Pilz, A., Westermayer, S., Reutterer, B., Decker, T., Characterization of the interferon-producing cell in mice infected with Listeria monocytogenes. PLoS Pathogens, 5(3), 2009, e1000355.
36. Sugimura, T., Jounai, K., Ohshio, K., Tanaka, T., Suwa, M., Fujiwara, D., Immunomodulatory effect of Lactococcus lactis JCM5805 on human plasmacytoid dendritic cells. Clinical Immunology 149:3 (2013), 509–518.
37. Sugimura, T., Takahashi, H., Jounai, K., Ohshio, K., Kanayama, M., Tazumi, K., Yamamoto, N., Effects of oral intake of plasmacytoid dendritic cells-stimulative lactic acid bacterial strain on pathogenesis of influenza-like illness and immunological response to influenza virus. British Journal of Nutrition 114:5 (2015), 727–733.
38. Surono, I.S., Koestomo, F.P., Novitasari, N., Zakaria, F.R., Yulianasari, Koesnandar, Novel probiotic Enterococcus faecium IS-27526 supplementation increased total salivary sIgA level and bodyweight of pre-school children: A pilot study. Anaerobe 17:6 (2011), 496–500.
39. Suzuki, H., Ohshio, K., Fujiwara, D., Lactococcus lactis subsp. lactis JCM 5805 activates natural killer cells via dendritic cells. Bioscience, Biotechnology, and Biochemistry 80:4 (2015), 798–800.
40. Swiecki, M., Colonna, M., Unraveling the functions of plasmacytoid dendritic cells during viral infections, autoimmunity, and tolerance. Immunological Reviews 234:1 (2010), 142–162.
41. Szatraj, K., Szczepankowska, A.K., Saczynska, V., Florys, K., Gromadzka, B., Lepek, K., Bardowski, J., Expression of avian influenza haemagglutinin (H5) and chicken interleukin 2 (chIL-2) under control of the ptcB promoter in Lactococcus lactis. Acta Biochimica Polonica 61:3 (2014), 609–614.
42. Tailor, P., Tamura, T., Ozato, K., IRF family proteins and type I interferon induction in dendritic cells. Cell Research 16:2 (2006), 134–140.
43. Tezuka, H., Abe, Y., Asano, J., Sato, T., Liu, J., Iwata, M., Ohteki, T., Prominent role for plasmacytoid dendritic cells in mucosal T cell-independent IgA induction. Immunity 34:2 (2011), 247–257.
44. Trinchieri, G., Santoli, D., Anti-viral activity induced by culturing lymphocytes with tumor-derived or virus-transformed cells. Enhancement of human natural killer cell activity by interferon and antagonistic inhibition of susceptibility of target cells to lysis. The Journal of Experimental Medicine 147:5 (1978), 1314–1333.
45. Turan, K., Mibayashi, M., Sugiyama, K., Saito, S., Numajiri, A., Nagata, K., Nuclear MxA proteins form a complex with influenza virus NP and inhibit the transcription of the engineered influenza virus genome. Nucleic Acids Research 32:2 (2004), 643–652.
46. van Hylckama Vlieg, J.E.T., Rademaker, J.L.W., Bachmann, H., Molenaar, D., Kelly, W.J., Siezen, R.J., Natural diversity and adaptive responses of Lactococcus lactis. Current Opinion in Biotechnology 17:2 (2006), 183–190.