Browse > Article
http://dx.doi.org/10.4014/jmb.1804.04001

Effects of Lactobacillus plantarum and Leuconostoc mesenteroides Probiotics on Human Seasonal and Avian Influenza Viruses  

Bae, Joon-Yong (Department of Microbiology, Institute for Viral Diseases, College of Medicine, Korea University)
Kim, Jin Il (Department of Microbiology, Institute for Viral Diseases, College of Medicine, Korea University)
Park, Sehee (Department of Microbiology, Institute for Viral Diseases, College of Medicine, Korea University)
Yoo, Kirim (Department of Microbiology, Institute for Viral Diseases, College of Medicine, Korea University)
Kim, In-Ho (Korea Food Research Institute)
Joo, Wooha (Daesang Co., Ltd.)
Ryu, Byung Hee (Daesang Co., Ltd.)
Park, Mee Sook (Department of Microbiology, Institute for Viral Diseases, College of Medicine, Korea University)
Lee, Ilseob (Department of Microbiology, Institute for Viral Diseases, College of Medicine, Korea University)
Park, Man-Seong (Department of Microbiology, Institute for Viral Diseases, College of Medicine, Korea University)
Publication Information
Journal of Microbiology and Biotechnology / v.28, no.6, 2018 , pp. 893-901 More about this Journal
Abstract
Influenza viruses that cause recurrent seasonal epidemics to humans can be controlled with vaccine and antiviral therapy. However, the medical treatments often exhibit limited efficacy in the elderly or immunosuppressed individuals. In these cases, daily uptake of probiotics may be an option to bring in health benefits against influenza. Here, we demonstrate the effects of probiotics Lactobacillus plantarum (Lp) and Leuconostoc mesenteroides (Lm) against seasonal and avian influenza viruses. As assessed by the plaque size reduction of human H1N1 and avian influenza H7N9 viruses, including green fluorescent protein-tagged H1N1 strain in cells, the selected Lp and Lm strains restrained viral replication in mouse lungs with statistical significance. Against lethal viral challenge, the Lp and Lm strains exhibited their beneficial effects by increasing the mean days and rates of survival of the infected mice. These results suggest that, despite rather narrow ranges of protective efficacy, the dietary supplement of Lactobacillus and Leuconostoc probiotics may promote health benefits against influenza.
Keywords
Dietary supplement; influenza; Lactobacillus plantarum; Leuconostoc mesenteroides; probiotic;
Citations & Related Records
Times Cited By KSCI : 2  (Citation Analysis)
연도 인용수 순위
1 Demicheli V, Jefferson T, Di Pietrantonj C, Ferroni E, Thorning S, Thomas RE, et al. 2018. Vaccines for preventing influenza in the elderly. Cochrane Database Syst. Rev. 2: CD004876.
2 Manicassamy B, Manicassamy S, Belicha-Villanueva A, Pisanelli G, Pulendran B, Garcia-Sastre A. 2010. Analysis of in vivo dynamics of influenza virus infection in mice using a GFP reporter virus. Proc. Natl. Acad. Sci. USA 107: 11531-11536.   DOI
3 Kim JI, Park S, Lee I, Lee S, Shin S, Won Y, et al. 2012. GFPexpressing influenza A virus for evaluation of the efficacy of antiviral agents. J. Microbiol. 50: 359-362.   DOI
4 Lee I, Kim JI, Park S, Bae JY, Yoo K, Yun SH, et al. 2017. Single PA mutation as a high yield determinant of avian influenza vaccines. Sci. Rep. 7: 40675.   DOI
5 Park S, Kim JI, Lee I, Lee S, Hwang MW, Bae JY, et al. 2013. Aronia melanocarpa and its components demonstrate antiviral activity against influenza viruses. Biochem. Biophys. Res. Commun. 440: 14-19.   DOI
6 Centers for Disease Control and Prevention (CDC). 2018. Disease burden of influenza. Available at https://www.cdc.gov/flu/about/disease/burden.htm.Accessed March 16, 2018.
7 World Health Organization (WHO). 2018. Cumulative number of confirmed human cases of avian influenza A(H5N1) reported to WHO. Available at http://www.who.int/influenza/human_animal_interface/H5N1_cumulative_table_archives/en/. Accessed March 2, 2018.
8 Food and Agriculture Organization of the United Nations (FAO). 2018. H7N9 situation. Available at http://www.fao.org/ag/againfo/programmes/en/empres/H7N9/situation_ update.html). Accessed March 28, 2018.
9 Starosila D, Rybalko S, Varbanetz L, Ivanskaya N, Sorokulova I. 2017. Anti-influenza activity of a Bacillus subtilis probiotic strain. Antimicrob. Agents Chemother. 61: e00539-17.
10 Fiore AE, Fry A, Shay D, Gubareva L, Bresee JS, Uyeki TM, et al. 2011. Antiviral agents for the treatment and chemoprophylaxis of influenza - recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm. Rep. 60: 1-24.
11 Centers for Disease Control and Prevention (CDC). 2018. Seasonal influenza vaccine effectiveness, 2005-2018. Available at https://www.cdc.gov/flu/professionals/vaccination/ effectiveness-studies.htm). Accessed March 15, 2018.
12 Kwak MK, Liu R, Kwon JO, Kim MK, Kim AH, Kang SO. 2013. Cyclic dipeptides from lactic acid bacteria inhibit proliferation of the influenza A virus. J. Microbiol. 51: 836-843.   DOI
13 Maeda N, Nakamura R, Hirose Y, Murosaki S, Yamamoto Y, Kase T, et al. 2009. Oral administration of heat-killed Lactobacillus plantarum L-137 enhances protection against influenza virus infection by stimulation of type I interferon production in mice. Int. Immunopharmacol. 9: 1122-1125.   DOI
14 Kiso M, Takano R, Sakabe S, Katsura H, Shinya K, Uraki R, et al. 2013. Protective efficacy of orally administered, heatkilled Lactobacillus pentosus b240 against influenza A virus. Sci. Rep. 3: 1563.   DOI
15 Goto H, Sagitani A, Ashida N, Kato S, Hirota T, Shinoda T, et al. 2013. Anti-influenza virus effects of both live and nonlive Lactobacillus acidophilus L-92 accompanied by the activation of innate immunity. Br. J. Nutr. 110: 1810-1818.   DOI
16 Kim JI, Lee I, Park S, Park MS. 2012. Surface glycoproteins determine the feature of the 2009 pandemic H1N1 virus. BMB Rep. 45: 653-658.   DOI
17 Lee YD, Hong YF, Jeon B, Jung BJ, Chung DK, Kim H. 2016. Differential cytokine regulatory effect of three Lactobacillus strains isolated from fermented foods. J. Microbiol. Biotechnol. 26: 1517-1526.   DOI
18 Kim JI, Lee I, Park S, Hwang MW, Bae JY, Lee S, et al. 2013. Genetic requirement for hemagglutinin glycosylation and its implications for influenza A H1N1 virus evolution. J. Virol. 87: 7539-7549.   DOI
19 Park S, Kim JI, Lee I, Bae JY, Yoo K, Nam M, et al. 2017. Adaptive mutations of neuraminidase stalk truncation and deglycosylation confer enhanced pathogenicity of influenza A viruses. Sci. Rep. 7: 10928.   DOI
20 Park S, Kim JI, Bae JY, Yoo K, Kim H, Kim IH, et al. 2018. Effects of heat-killed Lactobacillus plantarum against influenza viruses in mice. J. Microbiol. 56: 145-149.   DOI
21 Guillemard E, Tondu F, Lacoin F, Schrezenmeir J. 2010. Consumption of a fermented dairy product containing the probiotic Lactobacillus casei DN-114001 reduces the duration of respiratory infections in the elderly in a randomised controlled trial. Br. J. Nutr. 103: 58-68.   DOI
22 Boge T, Remigy M, Vaudaine S, Tanguy J, Bourdet-Sicard R, van der Werf S. 2009. A probiotic fermented dairy drink improves antibody response to influenza vaccination in the elderly in two randomised controlled trials. Vaccine 27: 5677-5684.   DOI
23 Palese P. 2004. Influenza: old and new threats. Nat. Med. 10: S82-S87.   DOI
24 Neumann G, Kawaoka Y. 2011. The first influenza pandemic of the new millennium. Influenza Other Respir. Viruses 5: 157-166.   DOI
25 Jung JY, Lee SH, Jeon CO. 2014. Kimchi microflora: history, current status, and perspectives for industrial kimchi production. Appl. Microbiol. Biotechnol. 98: 2385-2393.   DOI
26 Bitterman R, Eliakim-Raz N, Vinograd I, Zalmanovici Trestioreanu A, Leibovici L, Paul M. 2018. Influenza vaccines in immunosuppressed adults with cancer. Cochrane Database Syst. Rev. 2: CD008983.
27 Yeh TL, Shih PC, Liu SJ, Lin CH, Liu JM, Lei WT, et al. 2018. The influence of prebiotic or probiotic supplementation on antibody titers after influenza vaccination: a systematic review and meta-analysis of randomized controlled trials. Drug Des Devel. Ther. 12: 217-230.   DOI
28 Van Puyenbroeck K, Hens N, Coenen S, Michiels B, Beunckens C, Molenberghs G, et al. 2012. Efficacy of daily intake of Lactobacillus casei Shirota on respiratory symptoms and influenza vaccination immune response: a randomized, double-blind, placebo-controlled trial in healthy elderly nursing home residents. Am. J. Clin. Nutr. 95: 1165-1171.   DOI
29 Pessione E, Cirrincione S. 2016. Bioactive molecules released in food by lactic acid bacteria: encrypted peptides and biogenic amines. Front. Microbiol. 7: 876.
30 Cho J, Lee D, Yang C, Jeon J, Kim J, Han H. 2006. Microbial population dynamics of kimchi, a fermented cabbage product. FEMS Microbiol. Lett. 257: 262-267.   DOI
31 Choi CY, Kim YH, Oh S, Lee HJ, Kim JH, Park SH, et al. 2017. Anti-inflammatory potential of a heat-killed Lactobacillus strain isolated from kimchi on house dust mite-induced atopic dermatitis in NC/Nga mice. J. Appl. Microbiol. 123: 535-543.   DOI
32 Webster RG, Govorkova EA. 2014. Continuing challenges in influenza. Ann. N. Y. Acad. Sci. 1323: 115-139.   DOI
33 Lam TT, Wang J, Shen Y, Zhou B, Duan L, Cheung CL, et al. 2013. The genesis and source of the H7N9 influenza viruses causing human infections in China. Nature 502: 241-244.   DOI
34 MacDonald TT, Bell I. 2010. Probiotics and the immune response to vaccines. Proc. Nutr. Soc. 69: 442-446.   DOI
35 Wright PF, Neumann G, Kawaoka Y. 2013. Orthomyxoviruses. In Knipe DM, Howley PM (eds.), Fields Virology, 6th Ed. Ch. 41. Lippincott Williams & Wilkins, Philadelphia, USA.
36 Krammer F, Garcia-Sastre A, Palese P. 2017. Is it possible to develop a "universal" influenza virus vaccine? Toward a universal influenza virus vaccine: potential target antigens and critical aspects for vaccine development. Cold Spring Harb. Perspect. Biol. 2017: a028845.
37 Hill D, Sugrue I, Arendt E, Hill C, Stanton C, Ross RP. 2017. Recent advances in microbial fermentation for dairy and health. F1000Res. 6: 751.   DOI
38 Palese P, Tobita K, Ueda M, Compans RW. 1974. Characterization of temperature sensitive influenza virus mutants defective in neuraminidase. Virology 61: 397-410.   DOI
39 Jung YJ, Lee YT, Ngo VL, Cho YH, Ko EJ, Hong SM, et al. 2017. Heat-killed Lactobacillus casei confers broad protection against influenza A virus primary infection and develops heterosubtypic immunity against future secondary infection. Sci. Rep. 7: 17360.   DOI
40 Lei WT, Shih PC, Liu SJ, Lin CY, Yeh TL. 2017. Effect of probiotics and prebiotics on immune response to influenza vaccination in adults: a systematic review and meta-analysis of randomized controlled trials. Nutrients 9: 1175.   DOI
41 Park S, Kim JI, Park MS. 2012. Antiviral agents against influenza viruses. J. Bacteriol. Virol. 42: 284-293.   DOI
42 Nachbagauer R, Krammer F. 2017. Universal influenza virus vaccines and therapeutic antibodies. Clin. Microbiol. Infect. 23: 222-228.   DOI
43 Harding AT, Heaton NS. 2018. Efforts to improve the seasonal influenza vaccine. Vaccines (Basel) 6: E19.   DOI
44 Naesens L, Stevaert A, Vanderlinden E. 2016. Antiviral therapies on the horizon for influenza. Curr. Opin. Pharmacol. 30: 106-115.   DOI
45 Zimmermann P, Curtis N. 2018. The influence of probiotics on vaccine responses - a systematic review. Vaccine 36: 207-213.   DOI
46 Vitetta L, Saltzman ET, Thomsen M, Nikov T, Hall S. 2017. Adjuvant probiotics and the intestinal microbiome: enhancing vaccines and immunotherapy outcomes. Vaccines (Basel) 5: 50.   DOI
47 Chen MF, Weng KF, Huang SY, Liu YC, Tseng SN, Ojcius DM, et al. 2017. Pretreatment with a heat-killed probiotic modulates monocyte chemoattractant protein-1 and reduces the pathogenicity of influenza and enterovirus 71 infections. Mucosal Immunol. 10: 215-227.   DOI
48 de Vrese M, Winkler P, Rautenberg P, Harder T, Noah C, Laue C, et al. 2006. Probiotic bacteria reduced duration and severity but not the incidence of common cold episodes in a double blind, randomized, controlled trial. Vaccine 24: 6670-6674.   DOI