• 1. Pond WG, Church DC, Pond KR, et al. Basic animal nutrition and feeding. 5th ed. Hoboken, NJ: Wiley, 2005; 125.

  • 2. National Research Council. Nutrient requirements of poultry. Washington, DC: National Academy Press, 1994; 19.

  • 3. Keshavarz K. Nonphytate phosphorus requirement of laying hens with and without phytase on a phase feeding program. Poult Sci 2000; 79: 748763.

    • Search Google Scholar
    • Export Citation
  • 4. Boling SD, Douglas MW, Johnson ML, et al. The effects of dietary available phosphorus levels and phytase on performance of young and older laying hens. Poult Sci 2000; 79: 224230.

    • Search Google Scholar
    • Export Citation
  • 5. Snow JL, Rafacz KA, Utterback PL, et al. Hy-Line W-36 and Hy-Line W-98 laying hens respond similarly to dietary phosphorus levels. Poult Sci 2005; 84: 757763.

    • Search Google Scholar
    • Export Citation
  • 6. Jokinen EI, Vielms J, Anltonen TM, et al. The effect of dietary phosphorus deficiency on the immune responses of European whitefish (Coregonus lavaretus L.). Fish Shellfish Immunol 2003; 15: 159168.

    • Search Google Scholar
    • Export Citation
  • 7. Kegley EB, Spears JW, Auman SK. Dietary phosphorus and an inflammatory challenge affect performance and immune function of weanling pigs. J Anim Sci 2001; 79: 413419.

    • Search Google Scholar
    • Export Citation
  • 8. Humphrey TJ. 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. Ames, Iowa: Iowa University State Press, 1999; 183192.

    • Search Google Scholar
    • Export Citation
  • 9. Nabb DP, O'Dell BL. Influence of dietary factors upon Salmonella typhimurium infection in the guinea pig. J Nutr 1964; 84: 191199.

  • 10. Doak RL, Garner GB, Huebner PF, et al. Effect of dietary phosphorus on blood phosphorus and leukocyte levels in experimental salmonellosis. Proc Soc Exp Biol Med 1972; 141: 953957.

    • Search Google Scholar
    • Export Citation
  • 11. Doak RL, Garner GB, O'Dell BL. Effect of dietary phosphorus on reticuloendothelial clearance of Salmonella organisms in endotoxin treated guinea pigs. Life Sci 1973; 13: 959968.

    • Search Google Scholar
    • Export Citation
  • 12. Swaggerty CL, Kaiser P, Rothwell L, et al. Heterophil cytokine mRNA profiles from genetically distinct lines of chickens with differential heterophil-mediated innate immune responses. Avian Pathol 2006; 35: 102108.

    • Search Google Scholar
    • Export Citation
  • 13. Kaiser P, Rothwell L, Galyov EE, et al. Differential cytokine expression in avian cells in response to invasion by Salmonella typhimurium, Salmonella enteritidis and Salmonella gallinarum. Microbiology 2000; 146: 32173226.

    • Search Google Scholar
    • Export Citation
  • 14. Kaiser MG, Cheeseman JH, Kaiser P, et al. Cytokine expression in chicken peripheral blood mononuclear cells after in vitro exposure to Salmonella enterica serovar Enteritidis. Poult Sci 2006; 85: 19071911.

    • Search Google Scholar
    • Export Citation
  • 15. Li S, Zhang MZ, Yan L, et al. Induction of CXC chemokine messenger-RNA expression in chicken oviduct epithelial cells by Salmonella enterica serovar Enteritidis via the type three secretion system-1. Avian Dis 2009; 53: 396404.

    • Search Google Scholar
    • Export Citation
  • 16. Withanage GS, Kaiser P, Wigley P, et al. Rapid expression of chemokines and proinflammatory cytokines in newly hatched chickens infected with Salmonella enterica serovar Typhimurium. Infect Immun 2004; 72: 21522159.

    • Search Google Scholar
    • Export Citation
  • 17. Withanage GS, Wigley P, Kaiser P, et al. 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 2005; 73: 51735182.

    • Search Google Scholar
    • Export Citation
  • 18. Berndt A, Wilhelm A, Jugert C, et al. Chicken cecum immune response to Salmonella enterica serovars of different levels of invasiveness. Infect Immun 2007; 75: 59936007.

    • Search Google Scholar
    • Export Citation
  • 19. Eckmann L, Kagnoff MF. Cytokines in host defense against Salmonella. Microbes Infect 2001; 3: 11911200.

  • 20. Methner U, Al-Shabibi S, Meyer H. Experimental oral infection of specific pathogen-free laying hens and cocks with Salmonella Enteritidis strains. Zentralbl Veterinarmed B 1995; 42: 459469.

    • Search Google Scholar
    • Export Citation
  • 21. Pan Z, Fang Q, Geng S, et al. Analysis of immune-related gene expression in chicken peripheral blood mononuclear cells following Salmonella enterica serovar Enteritidis infection in vitro. Res Vet Sci 2012; 93: 716720.

    • Search Google Scholar
    • Export Citation
  • 22. Hong YH, Lillehoj HS, Lillehoj EP, et al. Changes in immune-related gene expression and intestinal lymphocyte subpopulations following Eimeria maxima infection of chickens. Vet Immunol Immunopathol 2006; 114: 259272.

    • Search Google Scholar
    • Export Citation
  • 23. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001; 29: e45.

  • 24. SAS user's guide: statistics. Version 9.03. Cary, NC: SAS Institute Inc, 2003;2085–2220.

  • 25. Adi S, Pollock AS, Shigenage JK, et al. Role of monokines in the metabolic effects of endotoxin. J Clin Invest 1992; 89: 16031609.

    • Search Google Scholar
    • Export Citation
  • 26. Webel DM, Finck BN, Baker DH, et al. Time course of increased plasma cytokines, cortisol, and urea nitrogen in pigs following intraperitoneal injection of lipopolysaccharide. J Anim Sci 1997; 75: 15141520.

    • Search Google Scholar
    • Export Citation
  • 27. Wang JF, Wang M, Ma JL, et al. The influence of intramammary lipopolysaccharide infusion on serum Ca, P, vitamin D, cytokines and cortisol concentrations in lactating sows. J Vet Med A Physiol Pathol Clin Med 2006; 53: 113118.

    • Search Google Scholar
    • Export Citation
  • 28. Sandstedt H, Larsson L, Kvart C. Effect of E. coli ectotoxin on calcium and phosphate concentration in serum of dairy cows. Nord Vet Med 1984; 36: 406407.

    • Search Google Scholar
    • Export Citation
  • 29. Sasai K, Yoshimura K, Lillehoj HS, et al. Analysis of splenic and thymic lymphocyte subpopulations in chickens infected with Salmonella enteritidis. Vet Immunol Immunopathol 1997; 59: 359367.

    • Search Google Scholar
    • Export Citation
  • 30. Berndt A, Methner U. Gamma/delta T cell response of chickens after oral administration of attenuated and non-attenuated Salmonella typhimurium strains. Vet Immunol Immunopathol 2001; 78: 143161.

    • Search Google Scholar
    • Export Citation
  • 31. Noujaim JC, Andreatti Filho RL, Lima ET, et al. Detection of T lymphocytes in intestine of broiler chicks treated with Lactobacillus spp. and challenged with Salmonella enterica serovar Enteritidis. Poult Sci 2008; 87: 927933.

    • Search Google Scholar
    • Export Citation
  • 32. Briles DE, Benjamin W Jr, Posey B, et al. Independence of macrophage activation and expression of the alleles of the Ity (immunity to Typhimurium) locus. Microb Pathog 1986; 1: 3341.

    • Search Google Scholar
    • Export Citation
  • 33. Mastroeni P, Villarreal-Ramos B, Hormaeche CE. Effect of late administration of anti-TNF alpha antibodies on a Salmonella infection in the mouse model. Microb Pathog 1993; 14: 473480.

    • Search Google Scholar
    • Export Citation
  • 34. Liu N, Ru YJ, Cowieson AJ, et al. Effects of phytate and phytase on the performance and immune function of broilers fed nutritionally marginal diets. Poult Sci 2008; 87: 11051111.

    • Search Google Scholar
    • Export Citation
  • 35. Shasha SM, Kristal B, Barzilai M, et al. In vitro effect of PTH on normal T cell functions. Nephron 1988; 50: 212216.

  • 36. Klinger M, Alexiewicz JM, Linker-Israeli M, et al. Effect of parathyroid hormone on human T cell activation. Kidney Int 1990; 37: 15431551.

    • Search Google Scholar
    • Export Citation
  • 37. Lewin E, Ladefoged J, Brandi L, et al. Parathyroid hormone dependent T cell proliferation in uremic rats. Kidney Int 1993; 44: 379384.

    • Search Google Scholar
    • Export Citation
  • 38. Lemire JM, Adams JS, Sakai R, et al. 1α, 25-dihydroxyvitamin D3 suppresses proliferation and immunoglobulin production by normal human peripheral blood mononuclear cells. J Clin Invest 1984; 74: 657661.

    • Search Google Scholar
    • Export Citation
  • 39. Tsoukas CD, Provvedini DM. 1,25-dihydroxyvitamin D3: a novel immunoregulatory hormone. Science 1984; 224: 14381440.

  • 40. Hideshima T, Podar K, Chauhan D, et al. Cytokines and signal transduction. Best Pract Res Clin Haematol 2005; 18: 509524.

  • 41. Kogut MH, Rothwell L, Kaiser P. IFN-gamma priming of chicken heterophils upregulates the expression of proinflammatory and Th1 cytokine mRNA following receptor-mediated phagocytosis of Salmonella enterica serovar Enteritidis. J Interferon Cytokine Res 2005; 25: 7381.

    • Search Google Scholar
    • Export Citation
  • 42. Kano R, Konnai S, Onuma M, et al. Cytokines profiles in chickens infected with virulent and avirulent Marek's disease viruses: interferon-gamma is a key factor in the protection of Marek's disease by vaccination. Microbiol Immunol 2009; 53: 224232.

    • Search Google Scholar
    • Export Citation
  • 43. Schroder K, Hertzog PJ, Ravasi T, et al. Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 2004; 75: 163189.

    • Search Google Scholar
    • Export Citation
  • 44. Lee SM, Suen Y, Qian J, et al. The regulation and biological activity of interleukin 12. Leuk Lymphoma 1998; 29: 427438.

  • 45. Nakanishi K, Yoshimoto T, Tsutsui H, et al. Interleukin-18 regulates both Th1 and Th2 responses. Annu Rev Immunol 2001; 19: 423474.

    • Search Google Scholar
    • Export Citation
  • 46. Belardelli F. Role of interferons and other cytokines in the regulation of the immune response. APMIS 1995; 103: 161179.

  • 47. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 2003; 3: 2335.

  • 48. O'Garra A, Vieira PT. (H)1 cells control themselves by producing interleukin-10. Nat Rev Immunol 2007; 7: 425428.

  • 49. Penha Filho RA, Moura BS, de Almeida AM, et al. Humoral and cellular immune response generated by different vaccine programs before and after Salmonella Enteritidis challenge in chickens. Vaccine 2012; 30: 76377643.

    • Search Google Scholar
    • Export Citation
  • 50. Haghighi HR, Abdul-Careem MF, Dara RA, et al. Cytokine gene expression in chicken cecal tonsils following treatment with probiotics and Salmonella infection. Vet Microbiol 2008; 126: 225233.

    • Search Google Scholar
    • Export Citation
  • 51. Cheeseman JH, Kaiser MG, Ciraci C, et al. Breed effect on early cytokine mRNA expression in spleen and cecum of chickens with and without Salmonella Enteritidis infection. Dev Comp Immunol 2007; 31: 5260.

    • Search Google Scholar
    • Export Citation
  • 52. Boonstra A, Barrat FJ, Crain C, et al. 1alpha, 25-dihydroxyvitamin D3 has a direct effect on naive CD4(1) T cells to enhance the development of Th2 cells. J Immunol 2001; 167: 49744980.

    • Search Google Scholar
    • Export Citation
  • 53. Overbergh L, Decallonne B, Waer M, et al. 1alpha, 25-dihydroxyvitamin D3 induces an autoantigen-specific T-helper 1/T-helper 2 immune shift in NOD mice immunized with GAD65 (p524–543). Diabetes 2000; 49: 13011307.

    • Search Google Scholar
    • Export Citation
  • 54. Jiang Y, Yoshida A, Ishioka C, et al. Parathyroid hormone inhibits immunoglobulin production without affecting cell growth in human B cells. Clin Immunol Immunopathol 1992; 65: 286293.

    • Search Google Scholar
    • Export Citation

Advertisement

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

View More View Less
  • 1 Key Laboratory for Animal Disease-Resistance Nutrition of China's Ministry of Education, Institute of Animal Nutrition, Sichuan Agricultural University, Ya'an, Sichuan 625014, PR China.
  • | 2 College of Veterinary Medicine, Sichuan Agricultural University, Ya'an Sichuan 625014, PR, China.
  • | 3 Key Laboratory for Animal Disease-Resistance Nutrition of China's Ministry of Education, Institute of Animal Nutrition, Sichuan Agricultural University, Ya'an, Sichuan 625014, PR China.
  • | 4 Key Laboratory for Animal Disease-Resistance Nutrition of China's Ministry of Education, Institute of Animal Nutrition, Sichuan Agricultural University, Ya'an, Sichuan 625014, PR China.
  • | 5 Key Laboratory for Animal Disease-Resistance Nutrition of China's Ministry of Education, Institute of Animal Nutrition, Sichuan Agricultural University, Ya'an, Sichuan 625014, PR China.
  • | 6 Key Laboratory for Animal Disease-Resistance Nutrition of China's Ministry of Education, Institute of Animal Nutrition, Sichuan Agricultural University, Ya'an, Sichuan 625014, PR China.
  • | 7 Key Laboratory for Animal Disease-Resistance Nutrition of China's Ministry of Education, Institute of Animal Nutrition, Sichuan Agricultural University, Ya'an, Sichuan 625014, PR China.
  • | 8 Key Laboratory for Animal Disease-Resistance Nutrition of China's Ministry of Education, Institute of Animal Nutrition, Sichuan Agricultural University, Ya'an, Sichuan 625014, PR China.

Abstract

OBJECTIVE To evaluate the effects of dietary nonphytate phosphorus (NPP) content on ileal lymphocyte subpopulations and cytokine expression in the cecal tonsils and spleen of hens that were or were not inoculated with Salmonella Typhimurium.

ANIMALS 64 Salmonella-free hens.

PROCEDURES Hens were fed a diet with 0.22% (control; n = 32) or 0.42% (high-P; 32) NPP for 6 weeks and then orally inoculated with S Typhimurium (5 × 107 CFUs) or PBSS. Tissues were obtained from 8 S Typhimurium–inoculated and 8 PBSS-inoculated hens from each group at 2 and 7 days postinoculation (DPI). Percentages of ileal CD4+ and CD8+ lymphocytes were determined by flow cytometry. Cytokine mRNA expression was determined by quantitative real-time PCR assays.

RESULTS For S Typhimurium–inoculated hens, plasma parathyroid hormone concentration was significantly increased and 1,25-dihydroxyvitamin D3 concentration was decreased in hens fed the high-P diet, compared with values in hens fed the control diet. Salmonella Typhimurium inoculation caused an increase in the percentage of ileal CD8+ lymphocytes and the expression of interleukin (IL)-1β, IL-6, IL-8, interferon-γ, IL-12, and IL-18 in the cecal tonsils and spleen and a decrease in the expression of IL-4 and IL-10 in the cecal tonsils. Hens fed the high-P diet had significantly increased splenic expression of interferon-γ at 2 DPI and IL-1β, IL-6, IL-12, and IL-18 at 7 DPI, compared with hens fed the control diet.

CONCLUSIONS AND CLINICAL RELEVANCE Results suggested there was a T-helper 1 cytokine reaction in the cecal tonsils and spleen of S Typhimurium–inoculated hens, and dietary NPP content altered calcium regulation hormone concentrations and affected splenic cytokine expression.

Abstract

OBJECTIVE To evaluate the effects of dietary nonphytate phosphorus (NPP) content on ileal lymphocyte subpopulations and cytokine expression in the cecal tonsils and spleen of hens that were or were not inoculated with Salmonella Typhimurium.

ANIMALS 64 Salmonella-free hens.

PROCEDURES Hens were fed a diet with 0.22% (control; n = 32) or 0.42% (high-P; 32) NPP for 6 weeks and then orally inoculated with S Typhimurium (5 × 107 CFUs) or PBSS. Tissues were obtained from 8 S Typhimurium–inoculated and 8 PBSS-inoculated hens from each group at 2 and 7 days postinoculation (DPI). Percentages of ileal CD4+ and CD8+ lymphocytes were determined by flow cytometry. Cytokine mRNA expression was determined by quantitative real-time PCR assays.

RESULTS For S Typhimurium–inoculated hens, plasma parathyroid hormone concentration was significantly increased and 1,25-dihydroxyvitamin D3 concentration was decreased in hens fed the high-P diet, compared with values in hens fed the control diet. Salmonella Typhimurium inoculation caused an increase in the percentage of ileal CD8+ lymphocytes and the expression of interleukin (IL)-1β, IL-6, IL-8, interferon-γ, IL-12, and IL-18 in the cecal tonsils and spleen and a decrease in the expression of IL-4 and IL-10 in the cecal tonsils. Hens fed the high-P diet had significantly increased splenic expression of interferon-γ at 2 DPI and IL-1β, IL-6, IL-12, and IL-18 at 7 DPI, compared with hens fed the control diet.

CONCLUSIONS AND CLINICAL RELEVANCE Results suggested there was a T-helper 1 cytokine reaction in the cecal tonsils and spleen of S Typhimurium–inoculated hens, and dietary NPP content altered calcium regulation hormone concentrations and affected splenic cytokine expression.

Contributor Notes

Address correspondence to Dr. Zhang (zkeying@yahoo.com).