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High Dietary Iron Differentially Influences the Iron Distribution in the Livers and the Spleens of Laying Hens After Salmonella Typhimurium Infection

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Abstract

Salmonella and the host battle for iron (Fe), due to its importance for fundamental cellular processes. To investigate Fe redistribution of Salmonella-infected hens and the effects of high dietary Fe on it, Salmonella-free hens were randomly assigned to 1 of 4 treatments in 2 (two dietary Fe level) × 2 (Salmonella-inoculation or -noninoculation) factorial assignment. After feeding a basal diet supplemented with 60 (adequate, control) or 300 mg Fe/kg (high-Fe) for 4 weeks, 59-week-old Salmonella-free hens were orally inoculated with 5 × 107 colony-forming units of Salmonella Typhimurium (infection) or PBS (vehicle). Blood, spleen, and liver samples (n = 8) were collected at 14 days post-inoculation to determine Fe concentration and Fe transporters expression. Salmonella infection decreased (P < 0.05) hematocrit, serum Fe concentration, and splenic Fe concentration regardless of high-Fe or control hens, whereas increased (P < 0.05) Fe centration in the livers of high-Fe-treated hens. High dietary Fe increased hematocrit and serum Fe concentration, but did not affect (P = 0.11) splenic Fe concentration in Salmonella-infected hens. Salmonella infection did not influence (P = 0.31) liver Fe centration in control hens, but increased (P = 0.04) it in high-Fe-treated hens. High dietary Fe decreased (P < 0.01) the mRNA abundance of divalent metal transporter 1 and transferrin receptor, but increased (P < 0.02) ferroportin-1 (FPN1) mRNA and protein in the spleens and the livers regardless of Salmonella-infected or vehicle hens. Salmonella infection increased (P < 0.02) FPN1 mRNA and protein expression in the spleens, but did not influence its expression in the livers. These results suggested Salmonella infection and high dietary Fe differently influence the Fe distribution in the spleen and the liver of Salmonella-infected hens.

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References

  1. Vahl HA, van ’T Klooster AT (1987) Dietary iron and broiler performance. Br Poult Sci 28:567–576

    Article  PubMed  CAS  Google Scholar 

  2. Dostal A, Gagnon M, Chassard C, Zimmermann MB, O’Mahony L, Lacroix C (2014) Salmonella adhesion, invasion and cellular immune responses are differentially affected by iron concentrations in a combined in vitro gut fermentation-cell model. PLoS One 9:e93549

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Kortman GA, Mulder ML, Richters TJ, Shanmugam NK, Trebicka E, Boekhorst J, Timmerman HM, Roelofs R, Wiegerinck ET, Laarakkers CM, Swinkels DW, Bolhuis A, Cherayil BJ, Tjalsma H (2015) Low dietary iron intake restrains the intestinal inflammatory response and pathology of enteric infection by food-borne bacterial pathogens. Eur J Immunol 45:2553–2567

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Kortman GA, Roelofs RW, Swinkels DW, de Jonge MI, Burt SA, Tjalsma H (2014) Iron-induced virulence of Salmonella enterica serovar typhimurium at the intestinal epithelial interface can be suppressed by carvacrol. Antimicrob Agents Chemother 58:1664–1670

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Kogut MH, Arsenault RJ (2017) Immunometabolic phenotype alterations associated with the induction of disease tolerance and persistent asymptomatic infection of Salmonella in the chicken intestine. Front Immunol 8:372

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. 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

    Article  PubMed  CAS  Google Scholar 

  7. Bai SP, Huang Y, Luo YH, Wang LL, Ding XM, Wang JP, Zeng QF, Zhang KY (2015) Effect of dietary nonphytate phosphorus content on ileal lymphocyte subpopulations and cytokine expression in the cecal tonsils and spleen of laying hens that were or were not orally inoculated with Salmonella Typhimurium. Am J Vet Res 76:710–718

    Article  PubMed  CAS  Google Scholar 

  8. Monack DM (2013) Helicobacter and Salmonella persistent infection strategies. Cold Spring Harb Perspect Med 3:a10348

    Article  CAS  Google Scholar 

  9. Byndioss MX, Tsolis RM (2016) Chronic bacterial pathogens: mechanisms of persistence. Microbiol Spectr 4:515–528

    Google Scholar 

  10. Willemetz A, Beatty S, Richer E, Rubio A, Auriac A, Milkereit RJ, Thibaudeau O, Vaulont S, Malo D, Canonne-Hergaux F (2017) Iron and hepcidin independent downregulation of the iron exporter ferroportin in macrophages during Salmonella infection. Front Immunol 8:498

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Skaar EP (2010) The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathog 6:e1000949

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Brown DE, Nick HJ, McCoy MW, Moreland SM, Stepanek AM, Benik R, O’Connell KE, Pilonieta MC, Nagy TA, Detweiler CS (2015) Increased ferroportin-1 expression and rapid splenic iron loss occur with anemia caused by Salmonella enterica serovar Typhimurium infection in mice. Infect Immun 83:2290–2299

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Donovan A, Andrews NC (2004) The molecular regulation of iron metabolism. Hematol J 5:373–380

    Article  PubMed  CAS  Google Scholar 

  14. Chlosta S, Fishman DS, Harrington L, Johnson EE, Knutson MD, Wessling-Resnick M, Cherayil BJ (2006) The iron efflux protein ferroportin regulates the intracellular growth of Salmonella enterica. Infect Immun 74:3065–3067

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Methner U, al-Shabibi S, Meyer H (1995) Experimental oral infection of specific pathogen-free laying hens and cocks with Salmonella enteritidis strains. Zentralbl Veterinarmed 42:459–469

    CAS  Google Scholar 

  16. 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

    Article  PubMed  CAS  Google Scholar 

  17. Wu B, Cui H, Peng X, Fang J, Zuo Z, Huang J, Luo Q, Deng Y, Wang H, Liu J (2013) Changes of the serum cytokines contents in broilers fed on diets supplemented with nickel chloride. Biol Trace Elem Res 151:234–239

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  19. Zhang H, Gilbert ER, Pan S, Zhang K, Ding X, Wang J, Zeng Q, Bai S (2016) Dietary iron concentration influences serum concentrations of manganese in rats consuming organic or inorganic sources of manganese. Br J Nutr 115:585–593

    Article  PubMed  CAS  Google Scholar 

  20. Kortman GA, Boleij A, Swinkels DW, Tjalsma H (2012) Iron availability increases the pathogenic potential of Salmonella Typhimurium and other enteric pathogens at the intestinal epithelial interface. PLoS One 7:e29968

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Moreira AC, Neves JV, Silva T, Oliveira P, Gomes MS, Rodrigues PN (2017) Hepcidin-(in)dependent mechanisms of iron metabolism regulation during infection by Listeria and Salmonella. Infect Immun 85:e00353–e00317

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Machado AC, Boiago MM, do Carmo GM, Bottari NB, Araujo DN, Giuriatti J, Morsch VM, Schetinger MR, Casaqrande RA, Wisser CS, Stefani LM, Alves MS, Da Silva AS (2016) Anaemia, serum iron concentrations and δ-aminolevulinate dehydratase activity in laying hens infected naturally by Salmonella Gallinarum. J Comp Pathol 155:1–4

    Article  PubMed  CAS  Google Scholar 

  23. Nairz M, Schroll A, Haschka D, Dichtl S, Tymoszuk P, Demetz E, Moser P, Haas H, Fang FC, Theurl I, Weiss G (2017) Genetic and dietary iron overload differentially affect the course of Salmonella Typhimurium infection. Front Cell Infect Microbiol 7:110

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Nemeth E, Tuttle MS, Powelson J, Vaughn MB, Donovan A, Ward DM, Ganz T, Kaplan J (2004) Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 306:2090–2093

    Article  PubMed  CAS  Google Scholar 

  25. Hilton KB, Lambert LA (2008) Molecular evolution and characterization of hepcidin gene products in vertebrates. Gene 415:40–48

    Article  PubMed  CAS  Google Scholar 

  26. Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, Boron WF, Nussberger S, Gollan JL, Hediger MA (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388:482–488

    Article  PubMed  CAS  Google Scholar 

  27. Gammella E, Buratti P, Cairo G, Recalcati S (2017) The transferrin receptor: the cellular iron gate. Metallomics 9:1367–1375

    Article  PubMed  CAS  Google Scholar 

  28. Nairz M, Fritsche G, Brunner P, Talasz H, Hantke K, Weiss G (2008) Interferon-gamma limits the availability of iron for intramacrophage Salmonella typhimurium. Eur J Immunol 38:1923–1936

    Article  PubMed  CAS  Google Scholar 

  29. Nairz M, Schleicher U, Schroll A, Sonnweber T, Theurl I, Ludwiczek S, Talasz H, Brandacher G, Moser PL, Muckenthaler MU, Fang FC, Bogdan C, Weiss G (2013) Nitric oxide-mediated regulation of ferroportin-1 controls macrophage iron homeostasis and immune function in Salmonella infection. J Exp Med 210:855–873

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Zoller H, Theurl I, Koch R, Kaser A, Weiss G (2002) Mechanisms of iron mediated regulation of the duodenal iron transporters divalent metal transporter 1 and ferroportin 1. Blood Cells Mol Dis 29:488–497

    Article  PubMed  CAS  Google Scholar 

  31. Liu XB, Nguyer NB, Marquess KD, Yang F, Haile DJ (2005) Regulation of hepcidin and ferroportin expression by lipopolysaccharide in splenic macrophages. Blood Cells Mol Dis 35:47–56

    Article  PubMed  CAS  Google Scholar 

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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), Da Bei Nong Group Research foundation (B2016015), and Chinese Chelota Group Research Project (2016LD0001).

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Correspondence to Shiping Bai.

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All animals used in this study were cared for strictly following the current regulations on the care, use, and handling of experimental animals that was approved by the Animal Health and Care Committee of Sichuan Agricultural University, in accordance with Chinese legislation on animal welfare.

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The authors declare that they have no conflict of interest.

Appendices

Appendix 1

Table 4 Composition and nutrient level of the basal diet (air-dry basis, %)

Appendix 2

Table 5 Influences of high dietary iron and Salmonella infection on the performance of laying hens

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Bai, S., Zhang, K., Ding, X. et al. High Dietary Iron Differentially Influences the Iron Distribution in the Livers and the Spleens of Laying Hens After Salmonella Typhimurium Infection. Biol Trace Elem Res 185, 497–508 (2018). https://doi.org/10.1007/s12011-018-1275-4

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  • DOI: https://doi.org/10.1007/s12011-018-1275-4

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