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The Association Between Cytokines and Intestinal Mucosal Immunity Among Broilers Fed on Diets Supplemented with Fluorine

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Abstract

Fluorine (F) bioaccumulation has been reported in the organs and tissues of organisms, including intestine. The intestinal mucosa is very important to the immune development. Meanwhile, cytokines are present in the normal intestinal mucosal and play an important role in the immune function. Thus, changes of the cytokine contents are related to the state of intestinal mucosal immunity. In this study, we investigated the changes in contents of cytokines such as interleukin-2 (IL-2), interleukin-4 (IL-4), interleukin-6 (IL-6), interferon gamma (IFN-γ), and tumor necrosis factor-alpha (TNF-α) induced by dietary high F in the mucosa of different parts of intestines (duodenum, jejunum, and ileum) by enzyme-linked immunosorbent assay. A total of 280 one-day-old healthy avian broilers were randomly divided into four groups and fed on a corn–soybean basal diet as control diet (F 22.6 mg/kg) or the same basal diet supplemented with 400, 800, and 1,200 mg F/kg (high F groups I, II, and III) in the form of sodium fluoride for 42 days. The experimental data showed that the contents of IL-2, IL-4, IL-6, IFN-γ, and TNF-α in the intestinal mucosa were significantly decreased in the high F groups II and III when compared with those of the control group from 14 to 42 days of age. It was concluded that dietary F in the range of 800–1,200 mg/kg significantly reduced the contents of aforementioned cytokines in the intestinal mucosa of broilers, which could impact the function of intestinal mucosal immunity through the pathways that decreased the lymphocyte population and/or lymphocyte activation.

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Reference

  1. Fordyce FM, Vrana K, Zhovinsky E, Povorznuk V, Toth G, Hope BC, Iljinsky U, Baker J (2007) A health risk assessment for fluoride in Central Europe. Environ Geochem Health 29(2):83–102

    Article  PubMed  CAS  Google Scholar 

  2. Patra RC, Dwibedi SK, Bhardwaj B, Swarup D (2000) Industrial fluorosis in cattle and buffalo around Udaipur, India. Sci Total Environ 253(1–3):145–150

    Article  PubMed  CAS  Google Scholar 

  3. Blaszczyk L, Birkner E, Gutowska L, Romuk E, Chlubek D (2012) Influence of methionine and vitamin E on fluoride concentration in bones and teeth of rats exposed to sodium fluoride in drinking water. Biol Trace Elem Res 146(3):335–339

    Article  PubMed  CAS  Google Scholar 

  4. Ba Y, Zhang HZ, Wang G, Wen S, Yang Y, Zhu JY et al (2011) Association of dental fluorosis with polymorphisms of estrogen receptor gene in Chinese children. Biol Trace Elem Res 143(1):87–96

    Article  PubMed  CAS  Google Scholar 

  5. Liu H, Sun JC, Zhao ZT, Zhang JM, Xu H, Li GS (2011) Fluoride-induced oxidative stress in three-dimensional culture of OS732 cells and rats. Biol Trace Elem Res 143(1):446–456

    Article  PubMed  CAS  Google Scholar 

  6. Panneerselvam L, Subbiah K, Arumugam A, Senapathy JG (2012) Ferulic acid modulates fluoride-induced oxidative hepatotoxicity in male Wistar rats. Biol Trace Elem Res. doi:10.1007/s12011-012-9534-2

  7. Niu Q, Liu HL, Guan ZZ, Zeng Q, Guo S, He P et al (2012) The effect of c-Fos demethylation on sodium fluoride-induced apoptosis in L-02 cells. Biol Trace Elem Res 149(1):102–109

    Article  PubMed  CAS  Google Scholar 

  8. Basha PM, Sujitha NS (2012) Combined influence of intermittent exercise and temperature stress on the modulation of fluoride toxicity. Biol Trace Elem Res 148(1):69–75

    Article  PubMed  CAS  Google Scholar 

  9. Basha PM, Rai P, Begum S (2011) Evaluation of fluoride-induced oxidative stress in rat brain: a multigeneration study. Biol Trace Elem Res 142(3):623–637

    Article  PubMed  CAS  Google Scholar 

  10. Bai CM, Chen T, Cui Y, Gong T, Peng X, Cui HM (2010) Effect of high fluorine on the cell cycle and apoptosis of renal cells in chickens. Biol Trace Elem Res 138(1–3):173–180

    Article  PubMed  CAS  Google Scholar 

  11. Varol E, Varol S (2012) Does fluoride toxicity cause hypertension in patients with endemic fluorosis? Biol Trace Elem Res 150(1–3):1–2

    Article  PubMed  Google Scholar 

  12. Basha PM, Rai P, Begum S (2011) Fluoride toxicity and status of serum thyroid hormones, brain histopathology, and learning memory in rats: a multigenerational assessment. Biol Trace Elem Res 144(1–3):1083–1094

    Article  PubMed  CAS  Google Scholar 

  13. Dede O, Varol E, Altinbas A, Varol S (2011) Chronic fluoride exposure has a role in etiology of coronary artery ectasia: sialic acid/glycosaminoglycan ratio. Biol Trace Elem Res 143(2):695–701

    Article  PubMed  CAS  Google Scholar 

  14. Ciftic G, Cenesiz S, Yarim GF, Nisbet O, Nisbet C, Cenesiz M et al (2010) Effect of fluoride exposure on serum glycoprotein pattern and sialic acid level in rabbits. Biol Trace Elem Res 133(1):51–59

    Article  Google Scholar 

  15. Wang ZH, Li XL, Yang ZQ, Xu M (2010) Fluorine-induced apoptosis and lipid peroxidation in human hair follicles in vitro. Biol Trace Elem Res 137(3):280–288

    Article  PubMed  CAS  Google Scholar 

  16. Ersoy IH, Alanoglu EG, Koroglu BK, Varol S, Akcay S, Ugan Y et al (2010) Effect of endemic fluorosis on hematological parameters. Biol Trace Elem Res 138(1–3):22–27

    Article  PubMed  CAS  Google Scholar 

  17. Lohakare J, Pattanaik A, Khan SA (2010) Effect of long-term fluoride exposure on growth, nutrient utilization and fluoride kinetics of calves fed graded levels of dietary protein. Biol Trace Elem Res 138(1–3):148–162

    Article  PubMed  CAS  Google Scholar 

  18. Zhou BH, Wang HW, Wang JM, Zhang JH, Yan XY, Wang JD (2007) Effects of malnutrition and supplemented nutrition on nonspecific immune function changes induced by fluoride in rabbits. Fluoride 40(3):169–177

    CAS  Google Scholar 

  19. Loftenius A, Andersson B, Butler J, Ekstrand J (1999) Fluoride augments the mitogenic and antigenic response of human blood lymphocytes in vitro. Caries Res 33(2):148–155

    Article  PubMed  CAS  Google Scholar 

  20. Chen T, Cui Y, Gong T, Bai CM, Peng X, Cui HM (2009) Inhibition of splenocyte proliferation and spleen growth in young chickens fed high fluoride diets. Fluoride 42(3):203–209

    Google Scholar 

  21. Liu J, Cui HM, Peng X, Fang J, Zuo ZC, Wang HS et al (2012) High dietary fluorine induction of oxidative damage in the cecal tonsil of broilers. Fluoride 45(1):47–52

    Google Scholar 

  22. Chen T, Cui Y, Bai CM, Gong T, Peng X, Cui HM (2009) Decreased percentages of the peripheral blood T-cell subsets and the serum IL-2 contents in chickens fed on diets excess in fluorine. Biol Trace Elem Res 132(1–3):122–128

    Article  PubMed  CAS  Google Scholar 

  23. Chen T, Cui Y, Bai CM, Gong T, Peng X, Cui HM (2009) Increased apoptotic lymphocyte population in the spleen of young chickens fed diets high in fluorine. Fluoride 42(2):94–100

    CAS  Google Scholar 

  24. Liu J, Cui HM, Peng X, Fang J, Zuo ZC, Wang HS et al (2012) Decreased percentages of T-cell subsets and IL-2 contents in the cecal tonsil of broilers fed diets high in fluorine. Fluoride 45(1):53–57

    CAS  Google Scholar 

  25. Liu J, Cui HM, Peng X, Fang J, Zuo ZC, Wang HS et al (2012) Changes induced by dietary fluorine in the cecal tonsil cytokine content of broilers. Fluoride 45(2):101–106

    Google Scholar 

  26. Nochi T, Kiyono H (2006) Innate immunity in the mucosal immune system. Curr Pharm Des 12(32):4203–4213

    Article  PubMed  CAS  Google Scholar 

  27. Shang HF, Wang YY, Lai YN, Chiu WC, Yeh SL (2004) Effects of arginine supplementation on mucosal immunity in rats with septic peritonitis. Clin Nutr 23(4):561–569

    Article  PubMed  CAS  Google Scholar 

  28. Kudsk KA (2001) Importance of enteral feeding in maintaining gut integrity. Tech Gastrointest Endosc 3(1):2–8

    Article  Google Scholar 

  29. Chabalgoity JA, Baz A, Rial A, Grille S (2007) The relevance of cytokines for development of protective immunity and rational design of vaccines. Cytokine Growth Factor Rev 18(1–2):195–207

    Article  PubMed  CAS  Google Scholar 

  30. NRC (1994) Nutrient requirements of domestic animals. Nutrient requirements of poultry, 9th edn. National Academy of Science, Washington

    Google Scholar 

  31. Gaca MD, Pickering JA, Arthur MJ, Benyon RC (1999) Human and rat hepatic stellate cells produce stem cell factor: a possible mechanism for mast cell recruitment in liver fibrosis. J Hepatol 30(5):850–858

    Article  PubMed  CAS  Google Scholar 

  32. Ogra PL, Faden H, Welliver RC (2001) Vaccination strategies for mucosal immune responses. Clin Microbiol Rev 14(2):430–445

    Article  PubMed  CAS  Google Scholar 

  33. Rosenthal KL, Gallichan WS (1997) Challenges for vaccination against sexually-transmitted diseases: induction and long-term maintenance of mucosal immune responses in the female genital tract. Semin Immunol 9(5):303–314

    Article  PubMed  CAS  Google Scholar 

  34. Holmgren J, Czerkinsky C (2005) Mucosal immunity and vaccines. Nat Med 11(4 Suppl):S45–S53

    Article  PubMed  CAS  Google Scholar 

  35. Jeurlssen SH, Lewls F, van der Klis JD, Mroz Z, Rebel JM, ter Huurne AA (2002) Parameters and techniques to determine intestinal health of poultry as constituted by immunity, integrity, and functionality. Curr Issues Intest Microbiol 3(1):1–14

    Google Scholar 

  36. Fleisher TA, Oliveira JB (2004) Functional and molecular evaluation of lymphocytes. J Allergy Clin Immunol 114(2):227–234

    Article  PubMed  CAS  Google Scholar 

  37. Gallego M, Cacho ED, Bascuas JA (1995) Antigen-binding cells in the cecal tonsils and Peyer’s patches of the chicken after bovine serum albumin administration. Poult Sci 74:472–479

    Article  PubMed  CAS  Google Scholar 

  38. Perdigon G, Alvarez S, Rachid M, Aguero G, Gobbato N (1995) Immune system stimulation by probiotics. J Dairy Sci 78(7):1597–1606

    Article  PubMed  CAS  Google Scholar 

  39. Takahashi I, Kiyono H (1999) Gut as the largest immunologic tissue. J Parenter Enteral Nutr 23(5 Suppl):S7–S12

    Article  CAS  Google Scholar 

  40. Such J, Hillebrand DJ, Guarner C, Berk L, Zapater P, Westengard J et al (2001) Tumor necrosis factor-alpha, interleukin-6, and nitric oxide in sterile ascitic fluid and serum from patients with cirrhosis who subsequently develop ascitic fluid infection. Dig Dis Sci 46(11):2360–2366

    Article  PubMed  CAS  Google Scholar 

  41. Navasa M, Follo A, Filella X, Jimenez W, Francitorra A, Planas R et al (1998) Tumor necrosis factor and interleukin-6 in spontaneous bacterial peritonitis in cirrhosis: relationship with the development of renal impairment and mortality. Hepatology 27(5):12–27

    Article  Google Scholar 

  42. Starr R, Willson TA, Viney EM, Murray LJ, Rayner JR, Jenkins BJ et al (1997) A family of cytokine-inducible inhibitors of signalling. Nature 387(6636):917–921

    Article  PubMed  CAS  Google Scholar 

  43. Iijima H, Takahashi I, Kiyono H (2001) Mucosal immune network in the gut for the control of infectious diseases. Rev Med Virol 11(2):117–133

    Article  PubMed  CAS  Google Scholar 

  44. Deng YX, Cui HM, Peng X, Fang J, Wang KP, Cui W et al (2011) Effect of dietary vanadium on cecal tonsil T cell subsets and IL-2 contents in broilers. Biol Trace Elem Res 144(1–3):647–656

    Article  PubMed  CAS  Google Scholar 

  45. Zou J, Carrington A, Collet B, Dijkstra JM, Yoshiura Y, Bols N et al (2005) Identification and bioactivities of IFN-gamma in rainbow trout Oncorhynchus mykiss: the first Th1-type cytokine characterized functionally in fish. J Immunol 175(4):2484–2494

    PubMed  CAS  Google Scholar 

  46. Robertsen B, Zou J, Secombes C, Leong JA (2006) Molecular and expression analysis of an interferon-gamma-inducible guanylate-binding protein from rainbow trout (Oncorhynchus mykiss). Dev Comp Immunol 30(11):1023–1033

    Article  PubMed  CAS  Google Scholar 

  47. Laing KJ, Wang T, Zou J, Holland J, Hong S, Bols N et al (2001) Cloning and expression analysis of rainbow trout Oncorhynchus mykiss tumour necrosis factor-a. Eur J Biochem 268(5):1315–1322

    Article  PubMed  CAS  Google Scholar 

  48. Zou J, Peddie S, Scapigliati G, Zhang Y, Bols NC, Ellis AE et al (2003) Functional characterisation of the recombinant tumor necrosis factors in rainbow trout, Oncorhynchus mykiss. Dev Comp Immunol 27(9):813–822

    Article  PubMed  CAS  Google Scholar 

  49. Vassalli P (1992) The pathophysiology of tumor necrosis factors. Annu Rev Immunol 10:411–452

    Article  PubMed  CAS  Google Scholar 

  50. Sawai T, Goldstone N, Drongowski RA, Coran AG, Harmon CM (2001) Effect of secretory immunoglobulin A on bacterial translocation in an enterocyte–lymphocyte co-culture model. Pediatr Surg Int 17(4):275–279

    Article  PubMed  CAS  Google Scholar 

  51. Akira S, Hirano T, Taga T, Kishimoto T (1990) Biology of multifunctional cytokines: IL-6 and related molecules (IL 1 and TNF). FASEB J 4(11):2860–2867

    PubMed  CAS  Google Scholar 

  52. DiPiro JT (1997) Cytokine networks with infection: mycobacterial infections, leishmaniasis, human immunodeficiency virus infection, and sepsis. Pharmacotherapy 17(2):205–223

    PubMed  CAS  Google Scholar 

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Acknowledgments

This research was supported by the program for Changjiang scholars and the university innovative research team (IRT 0848), and the Education Department of Sichuan Province (09ZZ017).

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  1. Key Laboratory of Animal Diseases and Environmental Hazards of Sichuan Province, College of Veterinary Medicine, Sichuan Agricultural University, Yaan, Sichuan, 625014, China

    Qin Luo, Hengmin Cui, Xi Peng, Jing Fang, Zhicai Zuo, Juan Liu, Bangyuan Wu & Yubing Deng

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  1. Qin Luo
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Correspondence to Hengmin Cui.

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Luo, Q., Cui, H., Peng, X. et al. The Association Between Cytokines and Intestinal Mucosal Immunity Among Broilers Fed on Diets Supplemented with Fluorine. Biol Trace Elem Res 152, 212–218 (2013). https://doi.org/10.1007/s12011-013-9612-0

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