Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-06T09:42:09.897Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  15 June 2017

M. ROYAN
M. ROYAN*
Affiliation:
North Region Branch, Agricultural Biotechnology Research Institute of Iran (ABRII), Agricultural Research, Education and Extension Organization (AREEO), Rasht, Iran
*
Corresponding author: [email protected]
Get access

Abstract

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.

Keywords

probioticssalmonellaimmune related geneschicken
Type
Reviews
Information
World's Poultry Science Journal , Volume 73 , Issue 3 , September 2017 , pp. 603 - 610
Copyright
Copyright © World's Poultry Science Association 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

AKBARI, M.R., HAGHIGHI, H.R., CHAMBERS, J.R., BRISBIN, J., READ, L.R. and SHARIF, S. (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.CrossRefGoogle ScholarPubMed
BARROW, P.A., LOVELL, M.A. and SIMPSON, J.M. (1988) Intestinal colonisation in the chicken of food-poisoning salmonella serotypes; microbial characteristics associated with fecal excretion. Avian Pathology 17: 571-588.CrossRefGoogle Scholar
BARROW, P.A., BUMSTEAD, N., MARSTON, K., LOVELL, M.A. and WIGLEY, P. (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.CrossRefGoogle ScholarPubMed
BARROW, P.A. and FREITAS NETO, O.C. (2011) Pullorum disease and fowl typhoid - new thoughts on old diseases: a review. Avian Pathology 40: 1-13.CrossRefGoogle ScholarPubMed
BEAL, R.K., POWERS, C., WIGLEY, P., BARROW, P.A. and SMITH, A.L. (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.CrossRefGoogle ScholarPubMed
BERNDT, A. and METHNER, U. (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.CrossRefGoogle ScholarPubMed
BERNDT, A., PIEPER, J. and METHNER, U. (2006) Circulating y delta T cells in response to Salmonella enterica serovar Enteritidis exposure in chickens. Infection and Immunity 74: 3967-3978.CrossRefGoogle Scholar
BERNDT, A., WILHELM, A., JUGERT, CH., PIEPER, J., SACHSE, K. and METHNER, U. (2007) Chicken caecum immune response to Salmonella enterica serovars of different levels of invasiveness. Infection and Immunity 75: 5993-6007.CrossRefGoogle ScholarPubMed
BOBÍKOVÁ, K. REVAJOVA, V., KARAFFOVA, V., LEVKUTOVA, M. and LEVKUT, M. (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.CrossRefGoogle ScholarPubMed
CASTILLO, N.A., PERDIGON, G. and DE MORENO DE LEBLANC, A. (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.CrossRefGoogle ScholarPubMed
CHAMBERS, J.R. and GONG, J. (2011) The intestinal microbiota and its modulation for salmonella control in chickens. Food Research International 44: 3149-3159.CrossRefGoogle Scholar
CHAPPELL, L., KAISER, P., BARROW, P., JONES, M.A., JOHNSTON, C. and WIGLEY, P. (2009) The immunobiology of avian systemic salmonellosis. Veterinary Immunology and Immunopathology 128: 53-59.CrossRefGoogle ScholarPubMed
CHEESEMAN, J.H., KAISER, M.G., CIRACI, C., KAISER, P. and LAMONT, S.J. (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.CrossRefGoogle ScholarPubMed
CHEN, C.C., LOUIE, S., SHI, H.N. and WALKER, W.A. (2005) Preinoculation with the probiotic Lactobacillus acidophilus early in life effectively inhibits murine Citrobacter rodentium colitis. Pediatric Research 58: 1185-1191.Google Scholar
CHIANG, H.I., SWAGGERTY, C.L., KOGUT, M.H., DOWD, S.E., LI, X., PEVZNER, I.Y. and ZHOU, H. (2008) Gene expression profiling in chicken heterophils with Salmonella enteritidis stimulation using a chicken 44k Agilent microarray. BMC Genomics 9: 526.CrossRefGoogle Scholar
CHRISTENSEN, H.R., FROKIAER, H. and PESTKA, J.J. (2002) Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. Journal of Immunology 168: 171-178.CrossRefGoogle ScholarPubMed
DERIU, E., LIU, J.Z., PEEZESHKI, M., EDWARDS, R.A., OCHOA, R.J., CONTRERAS, H., LIBBY, S.J., FANG, F.C. and RAFFATELLU, M. (2013) Probiotic bacteria reduce Salmonella Typhimurium intestinal colonisation by competing for iron. Cell Host Microbe 14: 26-37.CrossRefGoogle ScholarPubMed
DE SIMONE, C., VESELY, R., BIANCHI-SALVADORI, B. and JIRILLO, E. (1993) The role of probiotics in modulation of the immune system in man and animals. International Journal of Immunotherapy 9: 23-28.Google Scholar
DUGAS, B., MERCENIER, A., LENOIR-WIJNKOOP, I., ARNAUD, C., DUGAS, N. and POSTAIRE, E. (1999) Immunity and probiotics. Immunology Today 20: 387-390.CrossRefGoogle ScholarPubMed
ECKMANN, L. and KAGNOFF, M.F. (2001) Cytokines in host defense against salmonella. Microbes and Infection 3: 1191-1200.CrossRefGoogle ScholarPubMed
GANZ, T. (2003) Defensins: antimicrobial peptides of innate immunity. Nature Reviews Immunology 3: 710-720.CrossRefGoogle ScholarPubMed
GILL, H. and PRASAD, J. (2008) Probiotics, immunomodulation, and health benefits. Advances in Experimental Medicine and Biology 606: 423-54.CrossRefGoogle ScholarPubMed
HAGHIGHI, H.R., ABDUL-CAREEM, M.F., DARA, R.A., CHAMBERS, J.R. and SHARIF, S. (2008) Cytokine gene expression in chicken cecal tonsils following treatment with probiotics and salmonella infection. Veterinary Microbiology 126: 225-233.CrossRefGoogle ScholarPubMed
HENDERSON, S.C., BOUNOUS, D.I. and LEE, M.D. (1999) Early events in the pathogenesis of avian salmonellosis. Infection and Immunity 67: 3580-3586.CrossRefGoogle ScholarPubMed
HIGGINS, S.E., WOLFENDEN, A.D. TELLEZ, G., HARGIS, B.M. and PORTER, T.E. (2011) Transcriptional profiling of cecal gene expression in probiotic- and salmonella-challenged neonatal chicks. Poultry Science 90: 901-913 CrossRefGoogle ScholarPubMed
HU, J., YU, H., KULKARNI, R.R., SHARIF, S., CUI, S.W., XIE, M.Y., NIE, S.P. and GONG, J. (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.CrossRefGoogle ScholarPubMed
JIE-LUN, H., HAI, Y., RAVEENDRA, R.K., SHAYAN, S., STEVE, W.C, MING-YONG, X., SHAO-PING, N. and JOSHUA, G. (2015) Modulation of cytokine gene expression by selected Lactobacillus isolates in the ileum, caecal tonsils and spleen of Salmonella-challenged broilers. Avian Pathology 44: 463-469.Google Scholar
KABIR, S.M.L. (2009) The role of probiotics in poultry industry. International Journal of Molecular Sciences 10: 3531-3546.CrossRefGoogle Scholar
LAUKOVÁ, A., MAREK, I. and STYRIAK, I. (2003) Inhibitory effects of different enterocins again fecal bacterial isolates. Berliner und Münchener Tierärztliche Wochenschrift 116: 37-40.Google ScholarPubMed
LYNN, D.J., HIGGS, R., LOYD, A.T., O'FARRELLY, C., HERVE-GREPINET, V., NYS, Y., BRINKMAN, F.S., YU, P.L., SOULIER, A., KAISER, P., ZHANG, G. and LEHRER, R.I. (2007) Avian beta-defensin nomenclature: a community proposed update. Immunology Letters 110: 86-89.CrossRefGoogle ScholarPubMed
MAREKOVÁ, M., LAUKOVÁ, A., SKAUGEN, M. and NES, I. (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.CrossRefGoogle ScholarPubMed
MARIANI, P., BARROW, P.A., CHENG, H.H., GROENEN, M.M., NEGRINI, R. and BUMSTEAD, N. (2001) Localisation to chicken chromosome 5 of a novel locus determining salmonellosis resistance. Immunogenetics 53: 786-791.CrossRefGoogle ScholarPubMed
MATULOVA, M., VARMUZOVA, K., SISAK, F., HAVLICKOVA, H., BABAK, V., STEJSKAL, K., ZDRAHAL, Z. and RYCHLIK, I. (2013) Chicken innate immune response to oral infection with Salmonella enteric serovar Enteritidis. Veterinary Research 44: 37.CrossRefGoogle Scholar
MEAD, G.C. (2000) Prospects for ‘competitive exclusion’ treatment to control salmonellas and other foodborne pathogens in poultry. Veterinary Journal 159: 111-123.CrossRefGoogle ScholarPubMed
MENENDEZ, A. and FINLAY, B.B. (2007) Defensins in the immunology of bacterial infections. Current Opinion in Immunology 19: 385-391.CrossRefGoogle ScholarPubMed
NAVA, G.M., BIEIKE, L.R., CALLAWAY, T.R. and CASTANEDA, M.P. (2005) Probiotic alternatives to reduce gastrointestinal infection: the poultry experience. Animal Health Research Review 6: 105-118.CrossRefGoogle ScholarPubMed
NOUJAIM, J.C., ANDREATTI FILHO, R.L., LIMA, E.T., OKAMOTO, A.S., AMORIM, R.L. and TORRES NETO, R. (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.CrossRefGoogle ScholarPubMed
O'HARA, A.M., O'REGAN, P., FANNING, A., O'MAHONY, C., MADSHARRY, J., LYONS, A., BIENENSTOCK, J., O'MAHONY, L. and SHANAHAN, F. (2006) Functional modulation of human intestinal epithelial cell responses by Bifidobacterium infantis and Lactobacillus salivarius . Immunology 118: 202-215.CrossRefGoogle ScholarPubMed
OLIVARES, M., DIAZ-ROPERO, M.P., GOMEZ, N., LARA-VILLOSLADA, F., SIERRA, S., MALDONADO, J.A., MARTIN, R., RODRIGUEZ, J.M. and XAUS, J. (2006) The consumption of two new probiotic strains, Lactobacillus gasseri CECT 5714 and Lactobacillus coryniformis CECT 5711, boosts the immune system of healthy humans. International Microbiology 9: 47-52.Google ScholarPubMed
ROYAN, M., MENG, G.Y., OTHMAN, F., SAZILI, A.Q. and NAVIDSHAD, B. (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.CrossRefGoogle ScholarPubMed
SAKAI, Y., TSUKAHARA, T., BUKAWA, W., MATSUBARA, N. and USHIDA, K. (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.CrossRefGoogle ScholarPubMed
SCHLEE, M., HARDER, J., KOTEN, B., STANGE, E.F., WEHKAMP, J. and FELLER-MANN, K. (2008) Probiotic lactobacilli and VSL#3 induce enterocyte beta-de-fensin 2. Clinical and Experimental Immunology 151: 528-535.Google Scholar
SETTA, A.M., BARROW, P.A., KAISER, P. and JONES, M.A. (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.CrossRefGoogle ScholarPubMed
STOYCHEVA, M. and MURDJEVA, M. (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.CrossRefGoogle ScholarPubMed
SUGIARTO, H. and YU, P.L. (2004) Avian antimicrobial peptides: the defense role of beta-defensins. Biochemical and Biophysical Research Communications 323: 721-727.CrossRefGoogle ScholarPubMed
VARMUZOVA, K., KUBASOVA, T., DAVIDOVA-GERZOVA, L., SISAK, F., HAVLICKOVA, H., SEBKOVA, A., FALDYNOVA, M. and RYCHLIK, I. (2016) Composition of gut microbiota influences resistance of newly hatched chickens to Salmonella enteritidis infection. Frontiers in Microbiology 7: 957.CrossRefGoogle ScholarPubMed
WÄCHTERSHÄUSER, A., LOITSCH, S.M. and STEIN, J. (2000) PPAR-γ is selectively upregulated in Caco-2 cells by butyrate. Biochemical and Biophysical Research Communications272: 380-385.CrossRefGoogle ScholarPubMed
WIGLEY, P., HULME, S.D., BUMSTEAD, N. and BARROW, P.A. (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.CrossRefGoogle ScholarPubMed
WIGLEY, P., HULME, S., POWERS, C., BEAL, R., SMITH, A. and BARROW, P. (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.CrossRefGoogle Scholar
WIGLEY, P., HULME, S., ROTHWELL, L., BUMSTEAD, N., KAISER, P. and BARROW, P. (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.CrossRefGoogle ScholarPubMed
WIGLEY, P. (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.CrossRefGoogle Scholar
WITHANAGE, G.S., KAISER, P., WIGLEY, P., POWERS, C., MASTROENI, P., BROOKS, H., BARROW, P., SMITH, A., MASKELL, D. and McCONNELL, I. (2004) Rapid expression of chemokines and proinflammatory cytokines in newly hatched chickens infected with Salmonella enterica serovar Typhimurium . Infection and Immunity 72: 2152-2159.CrossRefGoogle ScholarPubMed
WITHANAGE, G.S., WIGLEY, P., KAISER, P., MASTROENI, P., BROOKS, H., POWERS, C., BEAL, R., BARROW, P., MASKELL, D. and McCONNELL, I. (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.CrossRefGoogle ScholarPubMed
YANG, D., BIRAGYN, A., KWAK, L.W. and OPPENHEIM, J.J. (2002) Mammalian defensins in immunity: more than just microbicidal. Trends in Immunology 23: 291-296.CrossRefGoogle ScholarPubMed
YANG, X.J., BRISBIN, J., YU, H., WANG, Q., YIN, F.G., ZHANG, Y.G., SABOUR, P., SHARIF, S. and GONG, J. (2014) Selected lactic acid-producing bacterial isolates with the capacity to reduce salmonella translocation and virulence gene expression in chickens. Plos One 9: e93022. doi:10.1371/journal.pone.0093022.CrossRefGoogle Scholar
YOSHIMURA, Y., OHASHI, H., SUBEDI, K., NISHIBORI, M. and ISOBE, N. (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.CrossRefGoogle ScholarPubMed
ZHANG, G., MA, L. and DOYLE, M.P. (2007) Potential competitive exclusion bacteria from poultry inhibitory to Campylobacter jejuni and salmonella. Journal of Food Protection 70: 867-873.CrossRefGoogle ScholarPubMed
ZHANG, S., LILLEHOJ, H.S.C., KIM, H., KEELER, C.L., BABU, U. and ZJANG, M.Z. (2008) Transcriptional response of chicken macrophages to Salmonella enterica serovar Enteritidis infection. Developmental Biology (Basel) 132: 141-151.Google ScholarPubMed
ZHOU, H. and LAMONT, S.J. (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.CrossRefGoogle ScholarPubMed