SpringerLink
Log in

Effect of High Dietary Manganese on the Immune Responses of Broilers Following Oral Salmonella typhimurium Inoculation

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Manganese (Mn) is an essential nutrient for both host and pathogen. Recent studies have demonstrated the nutritional immunity of Mn against Salmonella infection in mammals. To investigate the effect of high dietary Mn on immune responses of broilers following Salmonella challenge, 144 1-day-old male broilers were fed a basal diet (containing 20.04 mg Mn/kg) plus an additional 40 (the control group) or 400 mg Mn/kg (the H-Mn group) for 7 days. The 72 broilers in each group were then orally inoculated with 5 × 107 CFUs of Salmonella typhimurium (ATCC#14028) or phosphate-buffered saline. Peripheral blood, spleens, cecal tonsils, and bursa of Fabricius were collected from Salmonella-inoculated and Salmonella-noninoculated broilers (n = 6) at 2 days post inoculation (2 DPI) and 7 days post inoculation (7 DPI). Peripheral blood lymphocyte subpopulations were determined by flow cytometry. The messenger RNA (mRNA) abundance of genes was determined by quantitative real-time polymerase chain reaction. Salmonella counts were higher (P < 0.05) in the H-Mn group than that in the control group at 2 DPI in the cecal contents of Salmonella-inoculated broilers. High dietary Mn increased CD3+CD4+ and CD3+CD8+ percentages in the peripheral blood of Salmonella-inoculated broilers at 2 DPI. Salmonella inoculation increased interleukin (IL)-6 mRNA expression in spleens and bursa of Fabricius at 2 DPI and increased IL-1β and IL-6 mRNA expression in cecal tonsils at 7 DPI in the H-Mn group. These changes were not observed in the control group. High dietary Mn increased interferon-γ (IFN-γ) in spleens and decreased IFN-γ and IL-12 mRNA expression in cecal tonsils of Salmonella-inoculated broilers at 2 DPI. High dietary Mn decreased IL-17 mRNA expression in the bursa of Fabricius at 7 DPI, but increased this expression in cecal tonsils at 2 and 7 DPI in Salmonella-inoculated broilers. These results suggested that dietary Mn level affected T helper (Th) 1-cytokine reaction in spleens and cecal tonsils, and Th17-mediated immunity in cecal tonsils and the bursa of Fabricius of broilers when challenged with Salmonella.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Cox JM (1995) Salmonella enteritidis: the egg and I. Aust Vet J 72:108–115

    CAS  PubMed  Google Scholar 

  2. Humphrey TJ (1999) Contamination of eggs and poultry meat with Salmonella enterica serovar Enteritidis. In: Saeed AM (ed) Salmonella enterica serovar Enteritidis in humans and animals: epidemiology, pathogenesis and control. Iowa University State Press, Ames, pp 183–192

    Google Scholar 

  3. Chang EB (1989) Salmonella bacterial adherence and penetration of mucosal cells: inducing role of the epithelium. Gastroenterology 97:1055–1056

    CAS  PubMed  Google Scholar 

  4. Sheela RR, Babu U, Mu J, Elankumaran S, Bautista DA, Raybourne RB, Heckert RA, Song W (2003) Immune responses against Salmonella entrica serovar enteritidis infection in virally immunosuppressed chickens. Clin Diagn Lab Immunol 10:670–679

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Bai SP, Huang Y, Luo YH, Wang LL, Ding XM, Wang JP, Zeng QF, Zhang KY (2014) Alteration in lymphocytes responses, cytokine and chemokine profiles in laying hens infected with Salmonella typhimurium. Vet Immunol Immunopathol 160:235–243

    CAS  PubMed  Google Scholar 

  6. Brownell JR, Sadler WW, Fanelli MJ (1970) Role of bursal of Fabricius in chicken resistance to Salmonella typhimurium. Avian Dis 14:142–152

    CAS  PubMed  Google Scholar 

  7. Eckmann L, Kagnoff MF (2001) Cytokines in host defense against Salmonella. Microbes Infect 3:1191–1200

    CAS  PubMed  Google Scholar 

  8. Coburn B, Grassl GA, Finlay BB (2007) Salmonella, the host and disease: a brief review. Immunol Cell Biol 85:112–118

    PubMed  Google Scholar 

  9. Wilson A, Reyes E, Ofman J (2008) Prevalence and outcomes of anemia in inflammatory bowel disease: a systematic review of the literature. Am J Med 116:44S–49S

    Google Scholar 

  10. Matulova M, Stepanova H, Sisak F, Havlickova H, Faldynov M, Kyrova K, Volf J, Rychik I (2012) Cytokine signaling in splenic leukocytes from vaccinated and non-vaccinated chickens after intravenous infection with Salmonella Enteritidis. PLoS One 7:e32346

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Rychlik I, Matulova ME, Kyrova K (2014) Gene expression in the chicken caecum in response to infections with non-typhoid Salmonella. Vet Res 45:119

    PubMed  PubMed Central  Google Scholar 

  12. Elewaut D, DiDonato JA, Kim JM, Truong F, Eckmann L, Kagnoff MF (1999) NF-κB is a central regulator of intestinal epithelial cell innate immune response induced by infection with enteroinvasive bacteria. J Immunol 163:1457–1466

    CAS  PubMed  Google Scholar 

  13. Keen CL, Ensunsa JL, Watson MH, Baly DL, Donovan SM, Monaco MH, Clegg MS (1999) Nutritional aspects of manganese from experimental studies. Neurotoxicology 20:213–224

    CAS  PubMed  Google Scholar 

  14. Mokgobu MI, Anderson R, Steel HC, Cholo MC, Tintinger GR, Theron AJ (2012) Manganese promotes increased formation of hydrogen peroxide by activated human macrophages and neutrophils in vitro. Inhal Toxicol 24:634–644

    CAS  PubMed  Google Scholar 

  15. Rogers RR, Garner RJ, Riddle MM, Luebke RW, Smialowicz J (1983) Augmentation of murine natural killer cell activity by manganese chloride. Toxicol Appl Pharmacol 70:7–17

    CAS  PubMed  Google Scholar 

  16. Smialowicz RJ, Rogers RR, Riddle MM, Leubke RW, Rowe DG, Garner RJ (1984) Manganese chloride enhances murine cell-mediated cytotoxicity: effects on natural killer cells. J Immunopharmacol 6:1–23

    CAS  PubMed  Google Scholar 

  17. Zhu Y, Lu X, Wu D, Cai S, Li S, Teng X (2013) The effect of manganese-induced cytotoxicity on mRNA expressions of HSP27, HSP40, HSP70 and HSP90 in chicken spleen lymphocytes in vitro. Bio Trace Elem Res 156:144–152

    CAS  Google Scholar 

  18. Zhang P, Lokuta KM, Turner DE, Liu B (2010) Synergistic dopaminergic neurotoxicity of manganese and lipopolysaccharide: differential involvement of microglia and astroglia. J Neurochem 112:434–443

    CAS  PubMed  Google Scholar 

  19. Dodd CA, Filipov NM (2011) Manganese potentiates LPS-induced heme-oxygenase 1 in microglia but not dopaminergic cells: role in controlling microglial hydrogen peroxide and inflammatory cytokine output. Neurotoxicology 32:683–692

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Mokgobu MI, Cholo MC, Anderson R, Steel HC, Motheo MP, Hlatshwayo TN, Tintinger GR, Theron AJ (2015) Oxidative induction of pro-inflammatory cytokine formation by human monocyte-derived macrophages following exposure to manganese in vitro. J Immunotoxicol 12:98–103

    CAS  PubMed  Google Scholar 

  21. Gajula SS, Chelasani VK, Panda AK, Mantena VL, Savaram RR (2011) Effect of supplemental inorganic Zn and Mn and their interactions on the performance of broiler chicken, mineral bioavailability, and immune response. Biol Trace Elem Res 139:177–187

    CAS  PubMed  Google Scholar 

  22. Hart DA (1978) Evidence that manganese inhibits an early event during stimulation of lymphocytes by mitogens. Exp Cell Res 113:139–150

    CAS  PubMed  Google Scholar 

  23. Hahon N, Booth JA (1984) Effect of chromium and manganese particles on the interferon system. J Interf Res 4:17–27

    CAS  Google Scholar 

  24. Black JR, Ammerman CB, Henry RP, Miles RD (1984) Biological availability of manganese sources and effects of high dietary manganese on tissue mineral composition of broiler-type chicks. Poult Sci 63:1999–2006

    CAS  PubMed  Google Scholar 

  25. Conly AK, Poureslami R, Koutsos EA, Batal AB, Jung B, Beckstead R, Peterson DG (2012) Tolerance and efficacy of tribasic manganese chloride in growing broiler chickens. Poult Sci 91:1633–1640

    CAS  PubMed  Google Scholar 

  26. Chappell L, Kaiser P, Barrow P, Jones MA, Johnston C, Wigley P (2009) The immunobiology of avian systemic salmonellosis. Vet Immunol Immunopathol 128:53–59

    CAS  PubMed  Google Scholar 

  27. Methner U, Barrow PA, Berndt A (2010) Induction of a homologous and heterologous invasion-inhibition effect after administration of Salmonella strains to newly hatched chicks. Vaccine 28:6958–6963

    CAS  PubMed  Google Scholar 

  28. Erf GF, Bottje WG, Bersi TK (1998) CD4, CD8 and TCR defined T-cell subsets in thymus and spleen of 2- and 7-week old commercial broiler chickens. Vet Immunol Immunopathol 62:339–348

    CAS  PubMed  Google Scholar 

  29. Clark HL, Jhingran A, Sun Y, Vareechon C, de JesuS CS, Skaar EP, Chazin WJ, Calera JA, Hohl TM, Pearlman E (2016) Zinc and manganese chelation by neutrophil S100A8/A9 (calprotectin) limits extracellular Aspergillus fumigatus hyphal growth and corneal infection[J]. J Immunol 196:336

    CAS  PubMed  Google Scholar 

  30. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408

    CAS  Google Scholar 

  31. Lisher JP, Giedroc DP (2013) Manganese acquisition and homeostasis at the host-pathogen interface. Front Cell Infect Microbiol 3:91

    PubMed  PubMed Central  Google Scholar 

  32. Cheung HY, Vitkovic L, Brown MRW (1982) Toxic effect of manganese on growth and sporulation of Bacillus stearothermophilus. J Gen Microbiol 128:2395–2402

    CAS  Google Scholar 

  33. Li S, Lu L, Hao S, Wang Y, Zhang L, Liu S, Liu B, Li K, Luo X (2011) Dietary manganese modulates expression of the manganese-containing superoxide dismutase gene in chickens. J Nutr 141:189–194

    CAS  PubMed  Google Scholar 

  34. Sasai K, Yoshimura K, Lillehoj HS, Withanage GS, Fukata T, Baba E, Arakawa A (1997) Analysis of splenic and thymic lymphocyte subpopulations in chickens infected with Salmonella enteritidis. Vet Immunol Immunopathol 59:359

    CAS  PubMed  Google Scholar 

  35. Berndt A, Methner U (2001) Gamma/delta T cell response of chickens after oral administration of attenuated and non-attenuated Salmonella typhimurium strains. Vet Immunol Immunopathol 78:143

    CAS  PubMed  Google Scholar 

  36. Nakata A, Araki S, Park SH, Park JT, Kim DS, Park HC, Yokoyama K (2006) Decreases in CD8+ T, naive (CD4+CD45RA+) T, and B (CD19+) lymphocytes by exposure to manganese fume. Ind Health 44(4):592–597

    CAS  PubMed  Google Scholar 

  37. Hughes EA, Galán JE (2002) Immune responses to Salmonella: location, location, location? Immunity 16:325–328

    CAS  PubMed  Google Scholar 

  38. Diaz-Ochoa VE, Lam D, Lee CS, Klaus S, Behnsen J, Liu JZ, Chim N, Nuccio SP, Rathi SG, Mastroianni JR, Edwards RA, Jacobo CM, Cerasi M, Battistoni A, Ouellette AJ, Goulding CW, Chazin WJ, Skaar EP, Raffatellu M (2016) Salmonella mitigates oxidative stress and thrives in the inflamed gut by evading calprotectin-mediated manganese sequestration. Cell Host Microbe 19:814–825

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Liu XF, Li ZP, Tie F, Liu N, Zhang ZW, Xu SW (2013) Effects of manganese-toxicity on immune-related organs of cocks. Chemosphere 90:2085–2100

    CAS  PubMed  Google Scholar 

  40. Nauciel C, Espinasse-Maes F (1992) Role of gamma interferon and tumor necrosis factor alpha in resistance to Salmonella typhimurium infection. Infect Immun 60:450–454

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Gulig PA, Doyle TJ, Clare-Salzler MJ, Maiese RL, Matsui H (1997) Systemic infection of mice by wild-type but not Spv-Salmonella typhimurium is enhanced by neutralization of gamma interferon and tumor necrosis factor alpha. Infect Immun 65:5191–5197

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Bao S, Beagley KW, France MP, Shen J, Husband AJ (2000) Interferon-gamma plays a critical role in intestinal immunity against Salmonella typhimurium infection. Immunology 99:464–472

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Mastroeni P, Clare S, Khan S, Harrison JA, Hormaeche CE, Okamura H, Kurimoto M, Dougan G (1999) Interleukin 18 contributes to host resistance and gamma interferon production in mice infected with virulent Salmonella typhimurium. Infect Immun 67:478–483

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Mastroeni P, Harrison JA, Robinson JH, Clare S, Khan S, Maskell DJ, Dougan G, Hormaeche CE (1998) Interleukin-12 is required for control of the growth of attenuated aromatic-compound-dependent Salmonellae in BALB/c mice: role of gamma interferon and macrophage activation. Infect Immun 66:4767–4776

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Dybing JK, Walters N, Pascual DW (1999) Role of endogenous interleukin-18 in resolving wild-type and attenuated Salmonella typhimurium infections. Infect Immun 67:6242–6248

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Smialowicz RJ, Luebke RW, Rogers RR, Riddle MM, Rowe DG (1985) Manganese chloride enhances natural cell-mediated immune effector cell function: effects on macrophages. Immunopharmacology 9:1–11

    CAS  PubMed  Google Scholar 

  47. Kelchtermans H, Schurgers E, Geboes L, Miltera T, Van Damme J, Van Snick J, Uyttenhove C, Matthys P (2009) Effector mechanisms of interleukin-17 in collagen-induced arthritis in the absence of interferon-gamma and counteraction by interferon-gamma. Arthritis Res Ther 11:R122

    PubMed  PubMed Central  Google Scholar 

  48. O’Connor W Jr, Kamanaka M, Booth CJ, Town T, Nakae S, Iwakura Y, Kolls JK, Flavell RA (2009) A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat Immunol 10:603

    PubMed  PubMed Central  Google Scholar 

  49. Zheng Y, Valdez PA, Danilenko DM, Hu Y, Sa SM, Gong Q, Abbas AR, Modrusan Z, Ghilardi N, de Sauvage FJ, Ouyang W (2008) Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med 14:282–289

    CAS  PubMed  Google Scholar 

  50. Liu JZ, Pezeshki M, Raffatellu M (2009) Th17 cytokines and host-pathogen interactions at the mucosa: dichotomies of help and harm. Cytokine 48:156–160

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Geddes K, Rubino SJ, Magalhaes JG, Streutker C, Le Bourhis L, Cho JH, Robertson SJ, Kim CJ, Kaul R, Philpott DJ, Girardin SE (2011) Identification of an innate T helper type 17 response to intestinal bacterial pathogens. Nat Med 17:837–844

    CAS  PubMed  Google Scholar 

  52. Lu X, Zhu Y, Bai R, Li S, Teng X (2015) The effect of manganese-induced toxicity on the cytokine mRNA expression of chicken spleen lymphocytes in vitro. Res Vet Sci 101:165–167

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge the financial support provided by the Natural Science Foundation in Education Department of Sichuan (035Z1017), Sichuan International Cooperation Project (2017HH0051), Meat-Chicken Industry Chain Program of Sichuan Province (2016NZ0003-02), and Chinese Chelota Group Research Project (2016LD0001).

Author information

Authors and Affiliations

  1. Institute of Animal Nutrition, Feed Engineering Research Centre of Sichuan Province, Sichuan Agricultural University, Huimin Road 211#, Wenjiang District, Chengdu, Sichuan, 611130, China

    Shuqin Pan, Keying Zhang, Xuemei Ding, Jian** Wang, Huanwei Peng, Qiufeng Zeng, Yue Xuan, Zuowei Su & Shi** Bai

  2. Chinese Chelota Group, Liangshui Industrial Estate, **yu District, Guanghan, Sihuan, 618300, China

    Bing Wu

Authors
  1. Shuqin Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Keying Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xuemei Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jian** Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Huanwei Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qiufeng Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yue Xuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Zuowei Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Bing Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Shi** Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shi** Bai.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pan, S., Zhang, K., Ding, X. et al. Effect of High Dietary Manganese on the Immune Responses of Broilers Following Oral Salmonella typhimurium Inoculation. Biol Trace Elem Res 181, 347–360 (2018). https://doi.org/10.1007/s12011-017-1060-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-017-1060-9

Keywords

Search

Navigation