Interactions between lactobacilli and chicken macrophages induce antiviral responses against avian influenza virus

Research in Veterinary Science

Volumn 125, Issue , 2019, Pages 441-450

  Shojadoost, Bahram ^a   Kulkarni, Raveendra R ^a   Brisbin, Jennifer T ^a,b   Quinteiro Filho, Wanderley ^a,c   Alkie, Tamiru N ^a   Sharif, Shayan ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b Ceva Animal Health Inc   (Canada)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Avian influenza virus; Innate immunity; Lactobacilli; Macrophages; Probiotics

Indexed keywords

2',5' OLIGOADENYLATE SYNTHETASE; ALPHA INTERFERON; B7 ANTIGEN; CD40 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; INTERFERON INDUCIBLE TRANSMEMBRANE PROTEIN M3; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 1BETA; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MEMBRANE PROTEIN; NITRIC OXIDE; PROBIOTIC AGENT; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN EXPRESSION; ANTIVIRAL ACTIVITY; ARTICLE; AVIAN INFLUENZA VIRUS; CELL INTERACTION; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFICACY; DRUG MECHANISM; GENE EXPRESSION; IMMUNOSTIMULATION; IN VITRO STUDY; INFLUENZA A VIRUS (H4N6); INNATE IMMUNITY; LACTOBACILLUS; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS REUTERI; LACTOBACILLUS SALIVARIUS; MACROPHAGE CELL LINE; MACROPHAGE FUNCTION; MQ NCSU CELL LINE; NONHUMAN; PROTEIN EXPRESSION; VIRUS CELL INTERACTION; VIRUS TITRATION; ANIMAL; AVIAN INFLUENZA; CHICKEN; IMMUNOLOGY; INFLUENZA A VIRUS; MACROPHAGE; PHYSIOLOGY;

ANIMALS; CHICKENS; INFLUENZA A VIRUS; INFLUENZA IN BIRDS; LACTOBACILLUS; MACROPHAGES; PROBIOTICS;

EID: 85033565787     PISSN: 00345288     EISSN: 15322661     Source Type: Journal    
DOI: 10.1016/j.rvsc.2017.10.007     Document Type: Article

References (47)

1. Barjesteh, N., Behboudi, S., Brisbin, J.T., Villanueva, A.I., Nagy, E., Sharif, S., TLR ligands induce antiviral responses in chicken macrophages. PLoS One, 9(8), 2014, e105713.
2. Borchers, A.T., Selmi, C., Meyers, F.J., Keen, C.L., Gershwin, M.E., Probiotics and immunity. J. Gastroenterol. 44 (2009), 26–46.
3. Boris, S., Barbés, C., Role played by lactobacilli in controlling the population of vaginal pathogens. Microbes Infect. 2 (2000), 543–546.
4. Brisbin, J.T., Zhou, H., Gong, J., Sabour, P., Akbari, M.R., Haghighi, H.R., Yu, H., Clarke, A., Sarson, A.J., Sharif, S., Gene expression profiling of chicken lymphoid cells after treatment with Lactobacillus acidophilus cellular components. Dev. Comp. Immunol. 32 (2008), 563–574.
5. Brisbin, J.T., Gong, J., Sharif, S., Interactions between commensal bacteria and the gut-associated immune system of the chicken. Anim. Health Res. Rev. 9 (2008), 101–110.
6. Brisbin, J.T., Gong, J., Parvizi, P., Sharif, S., Effects of lactobacilli on cytokine expression by chicken spleen and cecal tonsil cells. Clin. Vaccine Immunol. 17 (2010), 1337–1343.
7. Brisbin, J.T., Gong, J., Orouji, S., Esufali, J., Mallick, A.I., Parvizi, P., Shewen, P.E., Sharif, S., Oral treatment of chickens with lactobacilli influences elicitation of immune responses. Clin. Vaccine Immunol. 18 (2011), 1447–1455.
8. Brisbin, J.T., Davidge, L., Roshdieh, A., Sharif, S., Characterization of the effects of three Lactobacillus species on the function of chicken macrophages. Res. Vet. Sci. 100 (2015), 39–44.
9. Charteris, W.P., Kelly, P.M., Morelli, L., Collins, J.K., Development and application of an in vitro methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in the upper human gastrointestinal tract. J. Appl. Microbiol. 84 (1998), 759–768.
10. Cox, N., Webster, R.G., Krauss, S., Guan, Y., Hay, A., Yu, K., Shortridge, K., Peiris, M., Kida, H., Brown, I., Stöhr, K., WHO Manual on Animal Influenza Diagnosis and Surveillance. 2nd edition, 2002 WHO/CDS/CSR/NCS/2002.5 Rev 1 94 pages.
11. Cross, M.L., Mortensen, R.R., Kudsk, J., Gill, H.S., Dietary intake of Lactobacillus rhamnosus HNOO1 enhances production of both Th1 and Th2 cytokines in antigen-primed mice. Med. Microbiol. Immunol. 191 (2002), 49–53.
12. Dugas, B., Mercenier, A., Lenoir-Wijnkoop, I., Arnaud, C., Dugas, N., Postaire, E., Immunity and probiotics. Immunol. Today 20 (1999), 387–390.
13. Ellermann-Eriksen, S., Macrophages and cytokines in the early defence against herpes simplex virus. Virol. J., 2, 2005, 59.
14. Fong, F.L.Y., Shah, N.P., Kirjavainen, P., El-Nezami, H., Mechanism of action of probiotic bacteria on intestinal and systemic immunities and antigen-presenting cells. Int. Rev. Immunol. 185 (2015), 1–11.
15. Garcia-Crespo, K.E., Chan, C.C., Gabryszewski, S.J., Percopo, C.M., Rigaux, P., Dyer, K.D., Domachowske, J.B., Rosenberg, H.F., Lactobacillus priming of the respiratory tract: heterologous immunity and protection against lethal pneumovirus infection. Antivir. Res. 97 (2013), 270–279.
16. Haghighi, H.R., Gong, J., Gyles, C.L., Hayes, M.A., Zhou, H., Sanei, B., Chambers, J.R., Sharif, S., Probiotics stimulate production of natural antibodies in chickens. Clin. Vaccine Immunol. 13 (2006), 975–980.
17. Haghighi, H.R., Abdul-Careem, M.F., Dara, R.A., Chambers, J.R., Sharif, S., Cytokine gene expression in chicken cecal tonsils following treatment with probiotics and Salmonella infection. Vet. Microbiol. 126 (2008), 225–233.
18. Hibbs, J.B., Taintor, R.R., Vavrin, Z., Rachlin, E.M., Nitric oxide: a cytotoxic activated macrophage effector molecule. Biochem. Biophys. Res. Commun. 157 (1988), 87–94.
19. Hu, J., Yu, H., Kulkarni, R.R., Sharif, S., Cui, S.W., Xie, Y., Nie, S., Gong, J., Modulation of cytokine gene expression by selected Lactobacillus isolates in the ileum, caecal tonsils and spleen of Salmonella-challenged broilers. Avian. Pathol. 44 (2015), 463–469.
20. Isolauri, E., Sütas, Y., Kankaanpää, P., Arvilommi, H., Salminen, S., Probiotics: effects on immunity. Am. J. Clin. Nutr. 73 (2001), 444–450.
21. Ivec, M., Botić, T., Koren, S., Jakobsen, M., Weingartl, H., Cencic, A., Interactions of macrophages with probiotic bacteria lead to increased antiviral response against vesicular stomatitis virus. Antivir. Res. 75 (2007), 266–274.
22. József, L., Khreiss, T., Filep, J.G., CpG motifs in bacterial DNA delay apoptosis of neutrophil granulocytes. FASEB J. 18 (2004), 1776–1778.
23. Kaila, M., Isolauri, E., Saxelin, M., Arvilommi, H., Vesikari, T., Viable versus inactivated lactobacillus strain GG in acute rotavirus diarrhoea. Arch. Dis. Child. 72 (1995), 51–53.
24. 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.
25. Kengatharan, M., De Kimpe, S.J., Thiemermann, C., Analysis of the signal transduction in the induction of nitric oxide synthase by lipoteichoic acid in macrophages. Br. J. Pharmacol. 117 (1996), 1163–1170.
26. de Kivit, S., Tobin, M.C., Forsyth, C.B., Keshavarzian, A., Landay, A.L., Regulation of intestinal immune responses through TLR activation: implications for pro- and prebiotics. Front. Immunol., 5, 2014, 60.
27. Korhonen, R., Korpela, R., Saxelin, M., Mäki, M., Kankaanranta, H.M.E., Induction of nitric oxide synthesis by probiotic Lactobacillus rhamnosus GG in J774 macrophages and human T84 intestinal epithelial cells. Inflammation 25 (2001), 223–232.
28. Lammers, K.M., Brigidi, P., Vitali, B., Gionchetti, P., Rizzello, F., Caramelli, E., Matteuzzi, D., Campieri, M., Immunomodulatory effects of probiotic bacteria DNA: IL-1 and IL-10 response in human peripheral blood mononuclear cells. FEMS Immunol. Med. Microbiol. 38 (2003), 165–172.
29. Lee, Y.K., Lim, C.Y., Teng, W.L., Ouwehand, A.C., Tuomola, E.M., Salminen, S., Quantitative approach in the study of adhesion of lactic acid bacteria to intestinal cells and their competition with enterobacteria. Appl. Environ. Microbiol. 66 (2000), 3692–3697.
30. Majamaa, H., Isolauri, E., Saxelin, M.V.T., Lactic acid bacteria in the treatment of acute rotavirus gasteroenteritis. J. Pediatr. Gastroenterol. Nutr. 20 (1995), 333–338.
31. Mannik, J.B., The antiviral role of nitric oxide. J Immunol Res 146 (1995), 693–697.
32. Miettinen, M., Matikainen, S., Vuopio-Varkila, J., Pirhonen, J., Varkila, K., Kurimoto, M., Julkunen, I., Lactobacilli and streptococci induce interleukin-12 (IL-12), IL-18, and gamma interferon production in human peripheral blood mononuclear cells. Infect. Immun. 66 (1998), 6058–6062.
33. Miettinen, M., Pietilä, T.E., Kekkonen, R.A., Kankainen, M., Latvala, S., Pirhonen, J., Österlund, P., Korpela, R., Julkunen, I., Nonpathogenic Lactobacillus rhamnosus activates the inflammasome and antiviral responses in human macrophages. Gut Microbes 3 (2012), 510–522.
34. Morita, H., He, F., Fuse, T., Ouwehand, A.C., Hashimoto, H., Hosoda, M., Mizumachi, K., Kurisaki, J.-I., Cytokine production by the murine macrophage cell line J774.1 after exposure to lactobacilli. Biosci. Biotechnol. Biochem. 66 (2002), 1963–1966.
35. Pagnini, C., Saeed, R., Bamias, G., Arseneau, K.O., Pizarro, T.T., Cominelli, F., Probiotics promote gut health through stimulation of epithelial innate immunity. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 454–459.
36. Parvizi, P., Read, L., Abdul-Careem, M.F., Lusty, C., Sharif, S., Cytokine gene expression in splenic CD4(+) and CD8(+) T-cell subsets of chickens infected with Marek's disease virus. Viral Immunol. 22 (2009), 31–38.
37. Pfaffl, M.W., A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29 (2001), 2002–2007.
38. Quinteiro-Filho, W.M., Brisbin, J.T., Hodgins, D.C., Sharif, S., Lactobacillus and Lactobacillus cell-free culture supernatants modulate chicken macrophage activities. Res. Vet. Sci. 103 (2015), 170–175.
39. Qureshi, M.A., Miller, L., Lillehoj, H.S.F.M., Establishment and characterization of a chicken mononuclear cell line. Vet. Immunol. Immunopathol. 26 (1990), 237–250.
40. Reid, G., Bruce, a.W., McGroarty, J.a., Cheng, K.J., Costerton, J.W., Is there a role for lactobacilli in prevention of urogenital and intestinal infections?. Clin. Microbiol. Rev. 3 (1990), 335–344.
41. Seo, B.J., Rather, I.a., Kumar, V.J.R., Choi, U.H., Moon, M.R., Lim, J.H., Park, Y.H., Evaluation of Leuconostoc mesenteroides YML003 as a probiotic against low-pathogenic avian influenza (H9N2) virus in chickens. J. Appl. Microbiol. 113 (2012), 163–171.
42. Shojadoost, B., Behboudi, S., Villanueva, a.I., Brisbin, J.T., Ashkar, a.a., Sharif, S., Vitamin D3 modulates the function of chicken macrophages. Res. Vet. Sci. 100 (2015), 45–51.
43. Slover, C.M., Danziger, L., Lactobacillus : a review. Clin. Microbiol. Newsl. 30 (2008), 23–27.
44. St Paul, M., Mallick, A.I., Haq, K., Orouji, S., Abdul-Careem, M.F., Sharif, S., In vivo administration of ligands for chicken toll-like receptors 4 and 21 induces the expression of immune system genes in the spleen. Vet. Immunol. Immunopathol. 144:3–4 (2011), 228–237.
45. Villanueva, A.I., Kulkarni, R.R., Sharif, S., Synthetic double-stranded RNA oligonucleotides are immunostimulatory for chicken spleen cells. Dev. Comp. Immunol. 35:1 (2011), 28–34.
46. Weiss, G., Rasmussen, S., Zeuthen, L.H., Nielsen, B.N., Jarmer, H., Jespersen, L., Frøkiaer, H., Lactobacillus acidophilus induces virus immune defence genes in murine dendritic cells by a toll-like receptor-2-dependent mechanism. Immunology 131 (2010), 268–281.
47. Yurong, Y., Ruiping, S., Shimin, Z., Yibao, J., Effect of probiotics on intestinal mucosal immunity and ultrastructure of cecal tonsils of chickens. Arch. Anim. Nutr. 59 (2005), 237–246.