Role of the intestinal microbiota in the immunomodulation of influenza virus infection

Microbes and Infection

Volumn 19, Issue 12, 2017, Pages 570-579

  Chen, Chi Jene ^a,b   Wu, Guan Hong ^c   Kuo, Rei Lin ^c,d   Shih, Shin Ru ^c,d  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^d CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

Author keywords

Gut lung axis; Immunomodulation; Influenza virus; Intestinal microbiota; Vaccination

Indexed keywords

INFLUENZA VACCINE; PROBIOTIC AGENT;

ADAPTIVE IMMUNITY; ARTICLE; DRUG EFFICACY; GASTROENTERITIS; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOREGULATION; INFLUENZA; INNATE IMMUNITY; INTESTINE FLORA; NONHUMAN; PRIORITY JOURNAL; IMMUNOLOGY; INTESTINE; MICROBIOLOGY; VIROLOGY;

GASTROINTESTINAL MICROBIOME; HUMANS; IMMUNOMODULATION; INFLUENZA, HUMAN; INTESTINES;

EID: 85035776722     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2017.09.002     Document Type: Article

References (70)

1. Ley, R.E., Peterson, D.A., Gordon, J.I., Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124 (2006), 837–848.
2. Dethlefsen, L., McFall-Ngai, M., Relman, D.A., An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449 (2007), 811–818.
3. Round, J.L., Mazmanian, S.K., The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9 (2009), 313–323.
4. Kamada, N., Seo, S.U., Chen, G.Y., Nunez, G., Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol 13 (2013), 321–335.
5. Hooper, L.V., Gordon, J.I., Commensal host-bacterial relationships in the gut. Science 292 (2001), 1115–1118.
6. Macpherson, A.J., Harris, N.L., Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 4 (2004), 478–485.
7. Jakobsson, H.E., Abrahamsson, T.R., Jenmalm, M.C., Harris, K., Quince, C., Jernberg, C., et al. Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut 63 (2014), 559–566.
8. Thavagnanam, S., Fleming, J., Bromley, A., Shields, M.D., Cardwell, C.R., A meta-analysis of the association between caesarean section and childhood asthma. Clin Exp Allergy 38 (2008), 629–633.
9. Marsland, B.J., Trompette, A., Gollwitzer, E.S., The gut-lung axis in respiratory disease. Ann Am Thorac Soc 12:Suppl. 2 (2015), S150–S156.
10. Kristensen, K., Fisker, N., Haerskjold, A., Ravn, H., Simoes, E.A., Stensballe, L., Caesarean section and hospitalization for respiratory syncytial virus infection: a population-based study. Pediatr Infect Dis J 34 (2015), 145–148.
11. Fouhy, F., Guinane, C.M., Hussey, S., Wall, R., Ryan, C.A., Dempsey, E.M., et al. High-throughput sequencing reveals the incomplete, short-term recovery of infant gut microbiota following parenteral antibiotic treatment with ampicillin and gentamicin. Antimicrob Agents Chemother 56 (2012), 5811–5820.
12. Fanaro, S., Chierici, R., Guerrini, P., Vigi, V., Intestinal microflora in early infancy: composition and development. Acta Paediatr Suppl 91 (2003), 48–55.
13. Budden, K.F., Gellatly, S.L., Wood, D.L., Cooper, M.A., Morrison, M., Hugenholtz, P., et al. Emerging pathogenic links between microbiota and the gut-lung axis. Nat Rev Microbiol 15 (2017), 55–63.
14. Thorburn, A.N., McKenzie, C.I., Shen, S., Stanley, D., Macia, L., Mason, L.J., et al. Evidence that asthma is a developmental origin disease influenced by maternal diet and bacterial metabolites. Nat Commun, 6, 2015, 7320.
15. Ichinohe, T., Pang, I.K., Kumamoto, Y., Peaper, D.R., Ho, J.H., Murray, T.S., et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci U S A 108 (2011), 5354–5359.
16. Wang, J., Li, F., Wei, H., Lian, Z.X., Sun, R., Tian, Z., Respiratory influenza virus infection induces intestinal immune injury via microbiota-mediated Th17 cell-dependent inflammation. J Exp Med 211 (2014), 2397–2410.
17. Deriu, E., Boxx, G.M., He, X., Pan, C., Benavidez, S.D., Cen, L., et al. Influenza virus affects intestinal microbiota and secondary Salmonella infection in the gut through type I interferons. PLoS Pathog, 12, 2016, e1005572.
18. Qin, N., Zheng, B., Yao, J., Guo, L., Zuo, J., Wu, L., et al. Influence of H7N9 virus infection and associated treatment on human gut microbiota. Sci Rep, 5, 2015, 14771.
19. Abt, M.C., Osborne, L.C., Monticelli, L.A., Doering, T.A., Alenghat, T., Sonnenberg, G.F., et al. Commensal bacteria calibrate the activation threshold of innate antiviral immunity. Immunity 37 (2012), 158–170.
20. Food and Agriculture Organization (FAO), World Health Organization (WHO), Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. October 1-4, 2001, Joint FAO WHO Expert Consultation, Córdoba, Argentina.
21. Yasui, H., Kiyoshima, J., Hori, T., Shida, K., Protection against influenza virus infection of mice fed Bifidobacterium breve YIT4064. Clin Diagn Lab Immunol 6 (1999), 186–192.
22. Zelaya, H., Alvarez, S., Kitazawa, H., Villena, J., Respiratory antiviral immunity and immunobiotics: beneficial effects on inflammation-coagulation interaction during influenza virus infection. Front Immunol, 7, 2016, 633.
23. Kawahara, T., Takahashi, T., Oishi, K., Tanaka, H., Masuda, M., Takahashi, S., et al. Consecutive oral administration of Bifidobacterium longum MM-2 improves the defense system against influenza virus infection by enhancing natural killer cell activity in a murine model. Microbiol Immunol 59 (2015), 1–12.
24. Yasui, H., Kiyoshima, J., Hori, T., Reduction of influenza virus titer and protection against influenza virus infection in infant mice fed Lactobacillus casei Shirota. Clin Diagn Lab Immunol 11 (2004), 675–679.
25. Izumo, T., Maekawa, T., Ida, M., Noguchi, A., Kitagawa, Y., Shibata, H., et al. Effect of intranasal administration of Lactobacillus pentosus S-PT84 on influenza virus infection in mice. Int Immunopharmacol 10 (2010), 1101–1106.
26. Takeda, S., Takeshita, M., Kikuchi, Y., Dashnyam, B., Kawahara, S., Yoshida, H., et al. Efficacy of oral administration of heat-killed probiotics from Mongolian dairy products against influenza infection in mice: alleviation of influenza infection by its immunomodulatory activity through intestinal immunity. Int Immunopharmacol 11 (2011), 1976–1983.
27. Youn, H.N., Lee, D.H., Lee, Y.N., Park, J.K., Yuk, S.S., Yang, S.Y., et al. Intranasal administration of live Lactobacillus species facilitates protection against influenza virus infection in mice. Antivir Res 93 (2012), 138–143.
28. Song, J.A., Kim, H.J., Hong, S.K., Lee, D.H., Lee, S.W., Song, C.S., et al. Oral intake of Lactobacillus rhamnosus M21 enhances the survival rate of mice lethally infected with influenza virus. J Microbiol Immunol Infect 49 (2016), 16–23.
29. Iwabuchi, N., Yonezawa, S., Odamaki, T., Yaeshima, T., Iwatsuki, K., Xiao, J.Z., Immunomodulating and anti-infective effects of a novel strain of Lactobacillus paracasei that strongly induces interleukin-12. FEMS Immunol Med Microbiol 66 (2012), 230–239.
30. 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 Immunol Med Microbiol 64 (2012), 280–288.
31. Waki, N., Yajima, N., Suganuma, H., Buddle, B.M., Luo, D., Heiser, A., et al. Oral administration of Lactobacillus brevis KB290 to mice alleviates clinical symptoms following influenza virus infection. Lett Appl Microbiol 58 (2014), 87–93.
32. Goto, H., Sagitani, A., Ashida, N., Kato, S., Hirota, T., Shinoda, T., et al. Anti-influenza virus effects of both live and non-live Lactobacillus acidophilus L-92 accompanied by the activation of innate immunity. Br J Nutr 110 (2013), 1810–1818.
33. Park, M.K., Ngo, V., Kwon, Y.M., Lee, Y.T., Yoo, S., Cho, Y.H., et al. Lactobacillus plantarum DK119 as a probiotic confers protection against influenza virus by modulating innate immunity. PLoS One, 8, 2013, e75368.
34. Yeo, J.M., Lee, H.J., Kim, J.W., Lee, J.B., Park, S.Y., Choi, I.S., et al. Lactobacillus fermentum CJL-112 protects mice against influenza virus infection by activating T-helper 1 and eliciting a protective immune response. Int Immunopharmacol 18 (2014), 50–54.
35. Iwabuchi, N., Xiao, J.Z., Yaeshima, T., Iwatsuki, K., Oral administration of Bifidobacterium longum ameliorates influenza virus infection in mice. Biol Pharm Bull 34 (2011), 1352–1355.
36. Asama, T., Uematsu, T., Kobayashi, N., Tatefuji, T., Hashimoto, K., Oral administration of heat-killed Lactobacillus kunkeei YB38 improves murine influenza pneumonia by enhancing IgA production. Biosci Microbiota Food Health 36 (2017), 1–9.
37. Hori, T., Kiyoshima, J., Shida, K., Yasui, H., Effect of intranasal administration of Lactobacillus casei Shirota on influenza virus infection of upper respiratory tract in mice. Clin Diagn Lab Immunol 8 (2001), 593–597.
38. Hori, T., Kiyoshima, J., Shida, K., Yasui, H., Augmentation of cellular immunity and reduction of influenza virus titer in aged mice fed Lactobacillus casei strain Shirota. Clin Diagn Lab Immunol 9 (2002), 105–108.
39. Harata, G., He, F., Hiruta, N., Kawase, M., Kubota, A., Hiramatsu, M., et al. Intranasal administration of Lactobacillus rhamnosus GG protects mice from H1N1 influenza virus infection by regulating respiratory immune responses. Lett Appl Microbiol 50 (2010), 597–602.
40. Chen, M.F., Weng, K.F., Huang, S.Y., Liu, Y.C., Tseng, S.N., Ojcius, D.M., et al. Pretreatment with a heat-killed probiotic modulates monocyte chemoattractant protein-1 and reduces the pathogenicity of influenza and enterovirus 71 infections. Mucosal Immunol 10 (2017), 215–227.
41. Lebeer, S., Vanderleyden, J., De Keersmaecker, S.C., Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat Rev Microbiol 8 (2010), 171–184.
42. Rooks, M.G., Garrett, W.S., Gut microbiota, metabolites and host immunity. Nat Rev Immunol 16 (2016), 341–352.
43. Ichinohe, T., Lee, H.K., Ogura, Y., Flavell, R., Iwasaki, A., Inflammasome recognition of influenza virus is essential for adaptive immune responses. J Exp Med 206 (2009), 79–87.
44. Grangette, C., Nutten, S., Palumbo, E., Morath, S., Hermann, C., Dewulf, J., et al. Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids. Proc Natl Acad Sci U S A 102 (2005), 10321–10326.
45. Asong, J., Wolfert, M.A., Maiti, K.K., Miller, D., Boons, G.J., Binding and cellular activation studies reveal that Toll-like receptor 2 can differentially recognize peptidoglycan from gram-positive and gram-negative bacteria. J Biol Chem 284 (2009), 8643–8653.
46. Andersen-Nissen, E., Smith, K.D., Strobe, K.L., Barrett, S.L., Cookson, B.T., Logan, S.M., et al. Evasion of Toll-like receptor 5 by flagellated bacteria. Proc Natl Acad Sci U S A 102 (2005), 9247–9252.
47. Andersen-Nissen, E., Smith, K.D., Bonneau, R., Strong, R.K., Aderem, A., A conserved surface on Toll-like receptor 5 recognizes bacterial flagellin. J Exp Med 204 (2007), 393–403.
48. Schlee, M., Wehkamp, J., Altenhoefer, A., Oelschlaeger, T.A., Stange, E.F., Fellermann, K., Induction of human beta-defensin 2 by the probiotic Escherichia coli Nissle 1917 is mediated through flagellin. Infect Immun 75 (2007), 2399–2407.
49. Oh, J.Z., Ravindran, R., Chassaing, B., Carvalho, F.A., Maddur, M.S., Bower, M., et al. TLR5-mediated sensing of gut microbiota is necessary for antibody responses to seasonal influenza vaccination. Immunity 41 (2014), 478–492.
50. Goraya, M.U., Wang, S., Munir, M., Chen, J.L., Induction of innate immunity and its perturbation by influenza viruses. Protein Cell 6 (2015), 712–721.
51. Shaw, M.H., Kamada, N., Kim, Y.G., Nunez, G., Microbiota-induced IL-1beta, but not IL-6, is critical for the development of steady-state TH17 cells in the intestine. J Exp Med 209 (2012), 251–258.
52. Pociask, D.A., Scheller, E.V., Mandalapu, S., McHugh, K.J., Enelow, R.I., Fattman, C.L., et al. IL-22 is essential for lung epithelial repair following influenza infection. Am J Pathol 182 (2013), 1286–1296.
53. Gimeno Brias, S., Stack, G., Stacey, M.A., Redwood, A.J., Humphreys, I.R., The role of IL-22 in viral infections: paradigms and paradoxes. Front Immunol, 7, 2016, 211.
54. Kumar, P., Thakar, M.S., Ouyang, W., Malarkannan, S., IL-22 from conventional NK cells is epithelial regenerative and inflammation protective during influenza infection. Mucosal Immunol 6 (2013), 69–82.
55. Ivanov, S., Renneson, J., Fontaine, J., Barthelemy, A., Paget, C., Fernandez, E.M., et al. Interleukin-22 reduces lung inflammation during influenza A virus infection and protects against secondary bacterial infection. J Virol 87 (2013), 6911–6924.
56. Kobayashi, N., Saito, T., Uematsu, T., Kishi, K., Toba, M., Kohda, N., et al. Oral administration of heat-killed Lactobacillus pentosus strain b240 augments protection against influenza virus infection in mice. Int Immunopharmacol 11 (2011), 199–203.
57. Strugnell, R.A., Wijburg, O.L., The role of secretory antibodies in infection immunity. Nat Rev Microbiol 8 (2010), 656–667.
58. Suzuki, K., Maruya, M., Kawamoto, S., Sitnik, K., Kitamura, H., Agace, W.W., et al. The sensing of environmental stimuli by follicular dendritic cells promotes immunoglobulin A generation in the gut. Immunity 33 (2010), 71–83.
59. Tezuka, H., Abe, Y., Iwata, M., Takeuchi, H., Ishikawa, H., Matsushita, M., et al. Regulation of IgA production by naturally occurring TNF/iNOS-producing dendritic cells. Nature 448 (2007), 929–933.
60. Tezuka, H., Abe, Y., Asano, J., Sato, T., Liu, J., Iwata, M., et al. Prominent role for plasmacytoid dendritic cells in mucosal T cell-independent IgA induction. Immunity 34 (2011), 247–257.
61. Mohamadzadeh, M., Duong, T., Sandwick, S.J., Hoover, T., Klaenhammer, T.R., Dendritic cell targeting of Bacillus anthracis protective antigen expressed by Lactobacillus acidophilus protects mice from lethal challenge. Proc Natl Acad Sci U S A 106 (2009), 4331–4336.
62. Huyghebaert, N., Vermeire, A., Neirynck, S., Steidler, L., Remaut, E., Remon, J.P., Development of an enteric-coated formulation containing freeze-dried, viable recombinant Lactococcus lactis for the ileal mucosal delivery of human interleukin-10. Eur J Pharm Biopharm 60 (2005), 349–359.
63. Vandenbroucke, K., de Haard, H., Beirnaert, E., Dreier, T., Lauwereys, M., Huyck, L., et al. Orally administered L. lactis secreting an anti-TNF Nanobody demonstrate efficacy in chronic colitis. Mucosal Immunol 3 (2010), 49–56.
64. Shi, S.H., Yang, W.T., Yang, G.L., Cong, Y.L., Huang, H.B., Wang, Q., et al. Immunoprotection against influenza virus H9N2 by the oral administration of recombinant Lactobacillus plantarumNC8 expressing hemagglutinin in BALB/c mice. Virology 464–465 (2014), 166–176.
65. Shi, S.H., Yang, W.T., Yang, G.L., Zhang, X.K., Liu, Y.Y., Zhang, L.J., et al. Lactobacillus plantarum vaccine vector expressing hemagglutinin provides protection against H9N2 challenge infection. Virus Res 211 (2016), 46–57.
66. Yang, W.T., Yang, G.L., Wang, Q., Huang, H.B., Jiang, Y.L., Shi, C.W., et al. Protective efficacy of Fc targeting conserved influenza virus M2e antigen expressed by Lactobacillus plantarum. Antivir Res 138 (2017), 9–21.
67. Lei, H., Xu, Y., Chen, J., Wei, X., Lam, D.M., Immunoprotection against influenza H5N1 virus by oral administration of enteric-coated recombinant Lactococcus lactis mini-capsules. Virology 407 (2010), 319–324.
68. Davidson, L.E., Fiorino, A.M., Snydman, D.R., Hibberd, P.L., Lactobacillus GG as an immune adjuvant for live-attenuated influenza vaccine in healthy adults: a randomized double-blind placebo-controlled trial. Eur J Clin Nutr 65 (2011), 501–507.
69. Rizzardini, G., Eskesen, D., Calder, P.C., Capetti, A., Jespersen, L., Clerici, M., Evaluation of the immune benefits of two probiotic strains Bifidobacterium animalis ssp. lactis, BB-12(R) and Lactobacillus paracasei ssp. paracasei, L. casei 431(R) in an influenza vaccination model: a randomised, double-blind, placebo-controlled study. Br J Nutr 107 (2012), 876–884.
70. Kiso, M., Takano, R., Sakabe, S., Katsura, H., Shinya, K., Uraki, R., et al. Protective efficacy of orally administered, heat-killed Lactobacillus pentosus b240 against influenza A virus. Sci Rep, 3, 2013, 1563.