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Immunomodulation of Antimicrobial Peptides Expression in the Gastrointestinal Tract by Probiotics in Response to Stimulation by Salmonella minnesota Lipopolysaccharides

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Abstract

The aim was to determine whether probiotics-feeding can affect the expression and localization of avian beta defensins (AvBDs) and proinflammatory cytokines in response to Salmonella minnesota lipopolysaccharide (LPS) in the gastrointestinal tract. One-day-old male Chunky broiler chicks were fed with or without 0.4% probiotics for 7 days (P-group and non-P-group, respectively). Then, they were orally challenged with no LPS (0-LPS), 1 µg LPS (1-LPS), or 100 µg LPS (100-LPS) (n = 5, each), in experiment 1, and with no LPS and 1 µg LPS (n = 6, each) in experiment 2. Five hours after LPS challenge, the proventriculi and ceca were collected. A total of seven and eight AvBDs were identified in proventriculus and cecum, respectively. The density of ir-AvBD12 in the surface epithelium of proventriculus increased in the P-group in response to 1-LPS and 100-LPS stimulation. In experiment 1, the expression of two AvBDs in the proventriculus and six AvBDs in the cecum of 1-LPS chicks was higher in P-group than in the non-P-group. Results of experiment 2 showed similar tendency to experiment 1. These results suggest that probiotics-feeding may enhance the immunodefense system mediated by AvBDs but not by cytokine, against infection by Gram-negative bacteria.

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References

  1. Walker WA, Goulet O, Morelli L, Antoine J (2006) Progress in the science of probiotics: from cellular microbiology and applied immunology to clinical nutrition. Eur J Nutr 45:1–18. https://doi.org/10.1007/s00394-006-1101-1

    Article  CAS  Google Scholar 

  2. Miyazaki Y, Takahashi K, Akiba Y (2007) Developmental changes in mRNA expression in immune-associated cells of intestinal tract of broiler chickens afterhatch and by dietary modification. Anim Sci J 78:527–534. https://doi.org/10.1111/j.1740-0929.2007.00472.x2007.00472.x

  3. Kaspers B, Schranner I, Lousch U (1991) Distribution of immunoglobulins during embryogenesis in the chicken. J Vet Med 38:73–79. https://doi.org/10.1111/j.1439-0442.1991.tb00986.x

  4. Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415:389–395. https://doi.org/10.1038/415389a

    Article  CAS  PubMed  Google Scholar 

  5. Zhao C, Nguyen T, Liu L, Sacco RE, Brogden KA, Lehrer RI (2001) Gallinacin-3, an inducible epithelial β-defensin in the chicken. Infect Immun 69(4):2684–2691. https://doi.org/10.1128/IAI.69.4.2684-2691.2001

  6. Xiao Y, Hughes AL, Ando J, Matsuda Y, Cheng JF, Skinner-Noble D, Zhang G (2004) A genome-wide screen identifies a single β-defensin gene cluster in the chicken: implications for the origin and evolution of mammalian defensins. BMC Genomics 5:56–66. https://doi.org/10.1186/1471-2164-5-56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Lynn DJ, Higgs R, Gaines S, Tierney J, James T, Lloyd AT, Fares MA, Mulcahy G, O’Farrelly C (2004) Bioinformatic discovery and initial characterization of nine novel antimicrobial peptide genes in the chicken. Immunogenetics 56:170–177. https://doi.org/10.1007/s00251-004-0675-0

    Article  CAS  PubMed  Google Scholar 

  8. Lynn DJ, Higgs R, Lloyd AT, O’Farrelly C, Hervé-Grépinet V, Nys Y, Brinkman FS, Yu PL, Soulier A, Kaiser P, Zhang G, Lehrer RI (2007) Avian beta-defensin nomenclature: a community proposed update. Immunol Lett 110:86–89. https://doi.org/10.1016/j.imlet.2007.03.007

  9. Sadeyen JR, Trotereau J, Protais J, Beaumont C, Sellier N, Salvat G, Velge P, Lalmanach AC (2006) Salmonella carrier-state in hens: study of host resistance by a gene expression approach. Microbes Infect 8:1308–1314. https://doi.org/10.1016/j.micinf.2005.12.0142005.12.014

  10. Werling D, Coffey TJ (2007) Pattern recognition receptors in companion and farm animals- the key to unlocking the door to animal disease. Vet J 174:240–251. https://doi.org/10.1016/j.tvjl.2006.10.010

    Article  CAS  PubMed  Google Scholar 

  11. Brownlie R, Allan B (2011) Avian toll-like receptors. Cell Tissue Res 343:121–130. https://doi.org/10.1007/s00441-010-1026-0

    Article  CAS  PubMed  Google Scholar 

  12. Nerren JR, He H, Genovese K, Kogut MH (2010) Expression of the avian-specific toll-like receptor 15 in chicken heterophils is mediated by Gram-negative and Gram-positive bacteria, but not TLR agonists. Vet Immunol Immunopath 136:151–156. https://doi.org/10.1016/j.vetimm.2010.02.017

    Article  CAS  Google Scholar 

  13. De Zoete MR, Bouwman LI, Keestra AM, Van Putten JPM (2011) Cleavage and activation of a toll-like receptor by microbial proteases. PNAS 108:4963–4973. https://doi.org/10.1073/pnas.1018135108

    Article  Google Scholar 

  14. Withanage GS, Kaiser P, Wigley P, Powers C, Mastroeni P, Brooks H, Barrow P, Smith A, Maskell D, McConnell I (2004) Rapid expression of chemokines and proinflammatory cytokines in newly hatched chickens infected with Salmonella enterica serovar Typhimurium. Infect Immun 72(4):2152–2159. https://doi.org/10.1128/IAI.72.4.2152-2159.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Withanage GS, Wigley P, Kaiser P, Mastroeni P, Brooks H, Powers C, Beal R, Barrow P, Maskell D, 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. Infect Immun 73:5173–5182. https://doi.org/10.1128/IAI.73.8.5173-5182.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Beal RK, Powers C, Wigley P, Barrow PA, Smith AL (2004) Temporal dynamics of the cellular, humoral and cytokine responses in chickens during primary and secondary infection with Salmonella enterica serovar Typhimurium. Avian Pathol 33:25–33. https://doi.org/10.1080/03079450310001636282

    Article  CAS  PubMed  Google Scholar 

  17. Brisbin JT, Gong J, Parvizi P, Sharif S (2010) Effects of Lactobacilli on cytokine expression by chicken spleen and cecal tonsil cells. Clin Vacc Immunol 17:1337–1343. https://doi.org/10.1128/CVI.00143-10

    Article  CAS  Google Scholar 

  18. Fasina YO, Holt PS, Moran ET, Moore RW, Conner DE, McKee SR (2008) Intestinal cytokine response of commercial source broiler chicks to Salmonella Typhimurium infection. Poult Sci 87(7):1335–1346. https://doi.org/10.3382/ps.2007-00526

    Article  CAS  PubMed  Google Scholar 

  19. Akbari MR, Haghighi HR, Chambers JR, Brisbin J, Read LR, Sharif S (2008) Expression of antimicrobial peptides in cecal tonsils of chickens treated with probiotics and infected with Salmonella enterica serovar typhimurium. Clin Vacc Immunol 15:1689–1693. https://doi.org/10.1128/CVI.00242-08

    Article  CAS  Google Scholar 

  20. Mohammed ESI, Igarashi Y, Isobe N, Yoshimura Y (2015) Effects of probiotics on the expression and localization of avian β-defensins in the proventriculus of broiler chicks. J Poult Sci 52:57–67. https://doi.org/10.2141/jpsa.0140114

    Article  CAS  Google Scholar 

  21. Mohammed ESI, Isobe N, Yoshimura Y (2016) Effects of probiotics on the expression of cathelicidins in response to stimulation by Salmonella Minnesota lipopolysaccharides in the proventriculus and cecum of broiler chicks. J Poult Sci 53:298–304. https://doi.org/10.2141/jpsa.0160064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real- time quantitative PCR and the 2-△△CT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262

    Article  CAS  Google Scholar 

  23. Ramasamy KT, Verma P, Reddy MR (2012) Differential gene expression of antimicrobial peptides β defensins in the gastrointestinal tract of Salmonella serovar Pullorum infected broiler chickens. Vet Res Comm 36:57–62. https://doi.org/10.1007/s11259-011-9512-8

    Article  Google Scholar 

  24. Hong YH, Song W, Lee SH, Lillehoj HS (2012) Differential gene expression profiles of β-defensins in the crop, intestine, and spleen using a necrotic enteritis model in 2 commercial broiler chicken lines. Poult Sci 91:1081–1088. https://doi.org/10.3382/ps.2011-01948

    Article  CAS  PubMed  Google Scholar 

  25. Derache C, Esnault E, Bonsergent C, Le Vern Y, Quere P, Lalmanach AC (2009) Differential modulation of β-defensin gene expression by Salmonella Enteritidis in intestinal epithelial cells from resistant and susceptible chicken inbred lines. Develop Comp Immunol 33:959–966. https://doi.org/10.1016/j.dci.2009.03.005

    Article  CAS  Google Scholar 

  26. Sonoda Y, Abdel Mageed AM, Isobe N, Yoshimura Y (2013) Induction of avian b-defensins by CpG oligodeoxynucleotides and proinflammatory cytokines in hen vaginal cells in vitro. Reproduction 145:621–631. https://doi.org/10.1530/REP-12-0518

    Article  CAS  PubMed  Google Scholar 

  27. Haghighi HR, Abdul-Careem MF, Dara RA, Chambers JR, Sharif S (2008) Cytokine gene expression in chicken cecal tonsils following treatment with probiotics and Salmonella infection. Vet Microbiol 126:225–233. https://doi.org/10.1016/j.vetmic.2007.06.026

    Article  CAS  PubMed  Google Scholar 

  28. Wu QJ, Zhou YM, Wu YN, Zhang LL, Wang T (2013) The effects of natural and modified clinoptilolite on intestinal barrier function and immune response to LPS in broiler chickens. Vet Immunol Immunopath 153:70–76. https://doi.org/10.1016/j.vetimm.2013.02.006

    Article  CAS  Google Scholar 

  29. Wang L, Chen J, Wang B, Wu D, Li H, Lu H, Wu H, Chai Y (2014) Protective effect of quercetin on lipopolysaccharide-induced acute lung injury in mice by inhibiting inflammatory cell influx. Exp Biol Med 239:1653–1662. https://doi.org/10.1177/1535370214537743

    Article  CAS  Google Scholar 

  30. Munyaka PM, Tactacan G, Jing MOK, House JD, Rodriguez-Lecompte JC (2012) Immunomodulation in young laying hens by dietary folic acid and acute immune responses after challenge with Escherichia coli lipopolysaccharide. Poult Sci 91:2454–2463. https://doi.org/10.3382/ps.2012-02381

    Article  CAS  PubMed  Google Scholar 

  31. Palazzo M, Balsari A, Rossini A, Selleri S, Calcaterra C, Gariboldi S, Zanobbio L, Arnaboldi F, Shirai YF, Serrao G, Rumio C (2007) Activation of enteroendocrine cells via TLRs induces hormone, chemokine, and defensin secretion. J Immunol 178:4296–4303. https://doi.org/10.4049/jimmunol.178.7.4296

    Article  CAS  PubMed  Google Scholar 

  32. Vora P, Youdim A, Thomas LS, Fukata M, Tesfay SY, Lukasek K, Michelsen KS, Wada A, Hirayama T, Arditi M, Abreu MT (2004) β- Defensin-2 expression is regulated by TLR signaling in intestinal epithelial cells. J Immunol 173:5398–5405. https://doi.org/10.4049/jimmunol.173.9.5398

    Article  CAS  PubMed  Google Scholar 

  33. Kogut MH, He H, Kaiser P (2005) Lipopolysaccharide binding protein/CD14/TLR4-dependent recognition of Salmonella LPS induces the functional activation of chicken heterophils and up-regulation of pro-inflammatory cytokine and chemokine gene expression in these cells. Anim Biotechnol 16:165–181. https://doi.org/10.1080/10495390500264896

    Article  CAS  PubMed  Google Scholar 

  34. Kogut MH, Iqbal M, He H, Philbin V, Kaiser P, Smith A (2005) Expression and function of toll-like receptors in chicken heterophils. Develop Comp Immunol 29:791–807. https://doi.org/10.1080/10495390500264896

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank Graduate school of Biosphere sciences, Hiroshima University, Japan where this work was done. The authors thank Toa Pharmaceutical Co., Ltd. (Tokyo) for kindly providing the probiotics (Toaraze for chickens) for this study.

Funding

This work was supported by a Ph.D. scholarship funded by South Valley University, Qena, Egypt and the Egyptian Ministry of Higher Education and Scientific Research, Mission Sector, Cairo, Egypt.

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Authors and Affiliations

  1. Department of Histology and Cytology, Faculty of Veterinary Medicine, South Valley University, Qena, 83523, Egypt

    Elsayed S. I. Mohammed

  2. Animal Health Research Institute, Qena Laboratory, Qena, Egypt

    Rasha Radey

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Correspondence to Elsayed S. I. Mohammed.

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Mohammed, E.S.I., Radey, R. Immunomodulation of Antimicrobial Peptides Expression in the Gastrointestinal Tract by Probiotics in Response to Stimulation by Salmonella minnesota Lipopolysaccharides. Probiotics & Antimicro. Prot. 13, 1157–1172 (2021). https://doi.org/10.1007/s12602-021-09746-y

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