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The immune-genes regulation mediated mechanisms of probiotics to control salmonella infection in chicken

  • M. ROYAN (a1)

Probiotics are live microorganisms with confirmed beneficial effects on poultry health, growth performance, immune system and gut microbial population. A better perception of the mechanisms underlying the immunomodulatory effects of probiotic bacteria is usually needed to give a superior direction to the development and administration of probiotics. The oral administration of probiotic bacteria influence host cytokine levels and therefore, alters both innate and adaptive host immune responses. Selected probiotics, including some lactobacillus isolates and enterococcal strains, have been considered to prevent salmonella colonisation. Part of the effect of probiotic bacteria may be mediated through changes in the immune system related genes, including cytokine expression. Administration of probiotics in chickens could moderate salmonella mediated changes in genes, including encoding pro-inflammatory cytokines, T helper (Th) 1 cytokines, and Th2 cytokines. This review summarises the findings on the mechanisms of salmonella inhibition by using probiotic bacteria at the molecular level.

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M.R. AKBARI , H.R. HAGHIGHI , J.R. CHAMBERS , J. BRISBIN , L.R. READ and S. SHARIF (2008) Expression of antimicrobial peptides in cecal tonsils of chickens treated with probiotics and infected with Salmonella enterica Serovar Typhimurium . Clinical and Vaccine Immunology 15: 1689-1693.

P.A. BARROW , M.A. LOVELL and J.M. SIMPSON (1988) Intestinal colonisation in the chicken of food-poisoning salmonella serotypes; microbial characteristics associated with fecal excretion. Avian Pathology 17: 571-588.

P.A. BARROW , N. BUMSTEAD , K. MARSTON , M.A. LOVELL and P. WIGLEY (2004) Faecal shedding and intestinal colonisation of Salmonella enterica in in-bred chickens: the effect of host-genetic background. Epidemiology and Infection 132: 117-126.

P.A. BARROW and O.C. FREITAS NETO (2011) Pullorum disease and fowl typhoid - new thoughts on old diseases: a review. Avian Pathology 40: 1-13.

R.K. BEAL , C. POWERS , P. WIGLEY , P.A. BARROW and A.L. SMITH (2004) Temporal dynamics of the cellular, humoral and cytokine responses in chickens during primary and secondary infection with Salmonella enterica serovar Typhimurium . Avian Pathology 33: 25-33.

A. BERNDT and U. METHNER (2001) Gamma/delta T cell response of chickens after oral administration of attenuated and non-attenuated Salmonella typhimurium strains. Veterinary Immunology and Immunopathology 78: 143-161.

A. BERNDT , J. PIEPER and U. METHNER (2006) Circulating y delta T cells in response to Salmonella enterica serovar Enteritidis exposure in chickens. Infection and Immunity 74: 3967-3978.

A. BERNDT , A. WILHELM , CH. JUGERT , J. PIEPER , K. SACHSE and U. METHNER (2007) Chicken caecum immune response to Salmonella enterica serovars of different levels of invasiveness. Infection and Immunity 75: 5993-6007.

K. BOBÍKOVÁ V. REVAJOVA , V. KARAFFOVA , M. LEVKUTOVA and M. LEVKUT (2015) IgA gene expression and quantification of cecal IgA+, IgM+, and CD4+cells in chickens treated with EFAL41 and infected with Salmonella enteritidis . Acta Histochemica 117: 629-634.

N.A. CASTILLO , G. PERDIGON and A. DE MORENO DE LEBLANC (2011) Oral administration of a probiotic Lactobacillus modulates cytokine production and TLR expression improving the immune response against Salmonella enterica serovar Typhimurium infection in mice. BMC Microbiology 11: 177.

J.R. CHAMBERS and J. GONG (2011) The intestinal microbiota and its modulation for salmonella control in chickens. Food Research International 44: 3149-3159.

L. CHAPPELL , P. KAISER , P. BARROW , M.A. JONES , C. JOHNSTON and P. WIGLEY (2009) The immunobiology of avian systemic salmonellosis. Veterinary Immunology and Immunopathology 128: 53-59.

J.H. CHEESEMAN , M.G. KAISER , C. CIRACI , P. KAISER and S.J. LAMONT (2007) Breed effect on early cytokine mRNA expression in spleen and caecum of chickens with and without Salmonella enteritidis infection. Developmental and Comparative Immunology 31: 52-60.

H.I. CHIANG , C.L. SWAGGERTY , M.H. KOGUT , S.E. DOWD , X. LI , I.Y. PEVZNER and H. ZHOU (2008) Gene expression profiling in chicken heterophils with Salmonella enteritidis stimulation using a chicken 44k Agilent microarray. BMC Genomics 9: 526.

H.R. CHRISTENSEN , H. FROKIAER and J.J. PESTKA (2002) Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. Journal of Immunology 168: 171-178.

E. DERIU , J.Z. LIU , M. PEEZESHKI , R.A. EDWARDS , R.J. OCHOA , H. CONTRERAS , S.J. LIBBY , F.C. FANG and M. RAFFATELLU (2013) Probiotic bacteria reduce Salmonella Typhimurium intestinal colonisation by competing for iron. Cell Host Microbe 14: 26-37.

B. DUGAS , A. MERCENIER , I. LENOIR-WIJNKOOP , C. ARNAUD , N. DUGAS and E. POSTAIRE (1999) Immunity and probiotics. Immunology Today 20: 387-390.

L. ECKMANN and M.F. KAGNOFF (2001) Cytokines in host defense against salmonella. Microbes and Infection 3: 1191-1200.

T. GANZ (2003) Defensins: antimicrobial peptides of innate immunity. Nature Reviews Immunology 3: 710-720.

H. GILL and J. PRASAD (2008) Probiotics, immunomodulation, and health benefits. Advances in Experimental Medicine and Biology 606: 423-54.

H.R. HAGHIGHI , M.F. ABDUL-CAREEM , R.A. DARA , J.R. CHAMBERS and S. SHARIF (2008) Cytokine gene expression in chicken cecal tonsils following treatment with probiotics and salmonella infection. Veterinary Microbiology 126: 225-233.

S.E. HIGGINS , A.D. WOLFENDEN G. TELLEZ , B.M. HARGIS and T.E. PORTER (2011) Transcriptional profiling of cecal gene expression in probiotic- and salmonella-challenged neonatal chicks. Poultry Science 90: 901-913

J. HU , H. YU , R.R. KULKARNI , S. SHARIF , S.W. CUI , M.Y. XIE , S.P. NIE and J. GONG (2015) Modulation of cytokine gene expression by selected lactobacillus isolates in the ileum, cecal tonsils, and spleen of salmonella-challenged broilers. Avian Pathology 44: 463-469.

S.M.L. KABIR (2009) The role of probiotics in poultry industry. International Journal of Molecular Sciences 10: 3531-3546.

D.J. LYNN , R. HIGGS , A.T. LOYD , C. O'FARRELLY , V. HERVE-GREPINET , Y. NYS , F.S. BRINKMAN , P.L. YU , A. SOULIER , P. KAISER , G. ZHANG and R.I. LEHRER (2007) Avian beta-defensin nomenclature: a community proposed update. Immunology Letters 110: 86-89.

M. MAREKOVÁ , A. LAUKOVÁ , M. SKAUGEN and I. NES (2007) Isolation and characterisation of a new bacteriocin, termed enterocin M, produced by environmental isolate Enterococcus faecium AL41. Journal of Industrial Microbiology and Biotechnology 34: 533-537.

P. MARIANI , P.A. BARROW , H.H. CHENG , M.M. GROENEN , R. NEGRINI and N. BUMSTEAD (2001) Localisation to chicken chromosome 5 of a novel locus determining salmonellosis resistance. Immunogenetics 53: 786-791.

M. MATULOVA , K. VARMUZOVA , F. SISAK , H. HAVLICKOVA , V. BABAK , K. STEJSKAL , Z. ZDRAHAL and I. RYCHLIK (2013) Chicken innate immune response to oral infection with Salmonella enteric serovar Enteritidis. Veterinary Research 44: 37.

G.C. MEAD (2000) Prospects for ‘competitive exclusion’ treatment to control salmonellas and other foodborne pathogens in poultry. Veterinary Journal 159: 111-123.

A. MENENDEZ and B.B. FINLAY (2007) Defensins in the immunology of bacterial infections. Current Opinion in Immunology 19: 385-391.

G.M. NAVA , L.R. BIEIKE , T.R. CALLAWAY and M.P. CASTANEDA (2005) Probiotic alternatives to reduce gastrointestinal infection: the poultry experience. Animal Health Research Review 6: 105-118.

J.C. NOUJAIM , R.L. ANDREATTI FILHO , E.T. LIMA , A.S. OKAMOTO , R.L. AMORIM and R. TORRES NETO (2008) Detection of T lymphocytes in intestine of broiler chicks treated with Lactobacillus spp. and challenged with Salmonella enterica Serovar Enteritidis . Poultry Science 87: 927-933.

A.M. O'HARA , P. O'REGAN , A. FANNING , C. O'MAHONY , J. MADSHARRY , A. LYONS , J. BIENENSTOCK , L. O'MAHONY and F. SHANAHAN (2006) Functional modulation of human intestinal epithelial cell responses by Bifidobacterium infantis and Lactobacillus salivarius . Immunology 118: 202-215.

M. ROYAN , G.Y. MENG , F. OTHMAN , A.Q. SAZILI and B. NAVIDSHAD (2011) Effects of conjugated linoleic acid, fish oil and soybean oil on PPARs (α & γ) mRNA expression in broiler chickens and their relation to body fat deposits. International Journal of Molecular Sciences12: 8581-8595.

Y. SAKAI , T. TSUKAHARA , W. BUKAWA , N. MATSUBARA and K. USHIDA (2006) Cell preparation of Enterococcus faecalis strain EC-12 prevents vancomycin-resistant enterococci colonisation in the caecum of newly hatched chicks. Poultry Science 85: 273-277.

A.M. SETTA , P.A. BARROW , P. KAISER and M.A. JONES (2012) Early immune dynamics following infection with Salmonella enterica serovars Enteritidis, infantis, pullorum and gallinarum: cytokine and chemokine gene expression profile and cellular changes of chicken cecal tonsils. Comparative Immunology, Microbiology and Infectious Diseases 35: 397-410.

M. STOYCHEVA and M. MURDJEVA (2005) Serum levels of interferon-gamma, interleukin-12, tumour necrosis factor-alpha, and interleukin-10, and bacterial clearance in patients with gastroenteric salmonella infection. Scandinavian Journal of Infectious Diseases 37: 11-14.

H. SUGIARTO and P.L. YU (2004) Avian antimicrobial peptides: the defense role of beta-defensins. Biochemical and Biophysical Research Communications 323: 721-727.

K. VARMUZOVA , T. KUBASOVA , L. DAVIDOVA-GERZOVA , F. SISAK , H. HAVLICKOVA , A. SEBKOVA , M. FALDYNOVA and I. RYCHLIK (2016) Composition of gut microbiota influences resistance of newly hatched chickens to Salmonella enteritidis infection. Frontiers in Microbiology 7: 957.

A. WÄCHTERSHÄUSER , S.M. LOITSCH and J. STEIN (2000) PPAR-γ is selectively upregulated in Caco-2 cells by butyrate. Biochemical and Biophysical Research Communications272: 380-385.

P. WIGLEY , S.D. HULME , N. BUMSTEAD and P.A. BARROW (2002) In vivo and in vitro studies of genetic resistance to systemic salmonellosis in the chicken encoded by the SAL1 locus. Microbes and Infection 4: 1111-1120.

P. WIGLEY , S. HULME , C. POWERS , R. BEAL , A. SMITH and P. BARROW (2005) Oral infection with the Salmonella enterica serovar Gallinarum 9R attenuated live vaccine as a model to characterise immunity to fowl typhoid in the chicken. BMC Veterinary Research 1: 2.

P. WIGLEY , S. HULME , L. ROTHWELL , N. BUMSTEAD , P. KAISER and P. BARROW (2006) Macrophages isolated from chickens genetically resistant or susceptible to systemic salmonellosis show magnitudinal and temporal differential expression of cytokines and chemokines following Salmonella enterica challenge. Infection and Immunity 74: 1425-1430.

P. WIGLEY (2014) Salmonella enterica in the chicken: how it has helped our understanding of immunology in a non-biomedical model species. Frontiers in Immunology 5: 482.

G.S. WITHANAGE , P. KAISER , P. WIGLEY , C. POWERS , P. MASTROENI , H. BROOKS , P. BARROW , A. SMITH , D. MASKELL and I. McCONNELL (2004) Rapid expression of chemokines and proinflammatory cytokines in newly hatched chickens infected with Salmonella enterica serovar Typhimurium . Infection and Immunity 72: 2152-2159.

G.S. WITHANAGE , P. WIGLEY , P. KAISER , P. MASTROENI , H. BROOKS , C. POWERS , R. BEAL , P. BARROW , D. MASKELL and I. McCONNELL (2005) Cytokine and chemokine responses associated with clearance of a primary Salmonella enterica serovar Typhimurium infection in the chicken and in protective immunity to rechallenge. Infection and Immunity 73: 5173-5182.

D. YANG , A. BIRAGYN , L.W. KWAK and J.J. OPPENHEIM (2002) Mammalian defensins in immunity: more than just microbicidal. Trends in Immunology 23: 291-296.

Y. YOSHIMURA , H. OHASHI , K. SUBEDI , M. NISHIBORI and N. ISOBE (2006) Effects of age, egg-laying activity, and Salmonella-inoculation on the expressions of gallinacin mRNA in the vagina of the hen oviduct. Journal of Reproduction and Development 52: 211-218.

G. ZHANG , L. MA and M.P. DOYLE (2007) Potential competitive exclusion bacteria from poultry inhibitory to Campylobacter jejuni and salmonella. Journal of Food Protection 70: 867-873.

H. ZHOU and S.J. LAMONT (2007) Global gene expression profile after Salmonella enterica Serovar enteritidis challenge in two F8 advanced intercross chicken lines. Cytogenetic and Genome Research. 117: 131-138.

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World's Poultry Science Journal
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