Skip to main content

Advertisement

Log in

Intestinal IgA+ Cell Numbers as well as IgA, IgG, and IgM Contents Correlate with Mucosal Humoral Immunity of Broilers During Supplementation with High Fluorine in the Diets

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

Abstract

Fluoride (F), a well-recognized harmful substance, is easily absorbed by the intestinal mucosa. The intestinal mucosal immune system is equipped with unique innate and adaptive defense mechanisms that provide a first line of protection against infectious agents. Meanwhile, immunoglobulins are the major secretory products of the adaptive immune system and their levels can be a strong indicator of a disease or condition. In this study, therefore, we investigated the effects of high dietary fluorine on the numbers of immunoglobulin A-positive (IgA+) cells in the lamina propria of intestines (duodenum, jejunum and ileum) by immunohistochemistry as well as on the contents of immunoglobulin A (IgA), immunoglobulin G (IgG), and immunoglobulin M (IgM) in the mucosa of intestines (duodenum, jejunum, and ileum) by enzyme-linked immunosorbent assay (ELISA). A total of 280 1-day-old healthy avian broilers were randomly divided into four groups and fed on a corn–soybean basal diet as control diet (fluorine 22.6 mg/kg) or the same basal diet supplemented with 400, 800, and 1,200 mg/kg fluorine (high fluorine groups I, II, and III) in the form of sodium fluoride (NaF) for 42 days. The experimental data showed that the numbers of IgA+ cells as well as the IgA, IgG, and IgM contents were significantly decreased (P < 0.01 or P < 0.05) in the high fluorine groups II and III when compared with those of the control group. It was concluded that dietary fluorine in the range of 800–1,200 mg/kg significantly reduced the numbers of the IgA+ cells and the contents of aforementioned immunoglobulins in the intestines (duodenum, jejunum, and ileum) of broilers, which could finally impact the mucosal humoral immune function in the intestines by a way that reduces the lymphocyte population and/or lymphocyte activation.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  1. Meenakshi, Maheshwari RC (2006) Fluoride in drinking water and its removal. J Hazard Mater 137(1):456–463

    Article  PubMed  CAS  Google Scholar 

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

    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. Gui CZ, Ran LY, Li JP, Guan ZZ (2010) Changes of learning and memory ability and brain nicotinic receptors of rat offspring with coal burning fluorosis. Neurotoxicol Teratol 32(5):536–541

    Article  PubMed  CAS  Google Scholar 

  5. 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 

  6. Chen T, Cui HM, Cui Y, Bai CM, Gong T, Peng X (2010) Cell-cycle blockage associated with increased apoptotic cells in the thymus of chickens fed on diets high in fluorine. Hum Exp Toxicol 30:685–692

    Article  PubMed  Google Scholar 

  7. Bouaziz H, Ketata S, Jammoussi K, Boudawara T, Ayedi F, Ellouze F, Zeghal N (2006) Effects of sodium fluoride on hepatic toxicity in adult mice and their suckling pups. Pestic Biochem Physiol 86(3):124–130

    Article  CAS  Google Scholar 

  8. Chen T, Cui HM, Cui Y, Bai CM, Gong T (2011) Decreased antioxidase activities and oxidative stress in the spleen of chickens fed on high-fluorine. Hum Exp Toxicol 30(9):1282–1286

    Article  PubMed  CAS  Google Scholar 

  9. 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 

  10. Liu J, Cui HM, Peng X, Fang J, Zuo ZC, Wang HS, Wu BY, Deng YX, Wang KP (2013) Dietary high fluorine induces apoptosis and alters Bcl-2, Bax and Caspase-3 protein expression in the cecal tonsil lymphocytes of broilers. Biol Trace Elem Res 152(1):25–30

    Article  PubMed  CAS  Google Scholar 

  11. Zahvoronkov AA, Strochkova LS (1981) Fluorosis: geographical pathology and some experimental findings. Fluoride 14(4):182–191

    Google Scholar 

  12. Sharma JD, Jain P, Sohu D (2009) Gastric discomforts from fluoride in drinking water in Sanganer Tehsil, Rajasthan, India. Fluoride 42(4):286–291

    CAS  Google Scholar 

  13. Chauhan SS, Ojha S, Mahmood A (2011) Modulation of lipid peroxidation and antioxidant defense systems in rat intestine by subchronic fluoride and ethanol administration. Alcohol 45(7):663–672

    Article  PubMed  CAS  Google Scholar 

  14. Islam M, Mishra PC, Patel R (2011) Fluoride adsorption from aqueous solution by a hybrid thorium phosphate composite. Chem Eng J 166(3):978–985

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  16. 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 

  17. Parkin J, Cohen B (2001) An overview of the immune system. Lancet 357(9270):1777–1789

    Article  PubMed  CAS  Google Scholar 

  18. 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 

  19. Amira S, Soufane S, Gharzouli K (2005) Effect of sodium fluoride on gastric emptying and intestinal transit in mice. Exp Toxicol Pathol 57(1):59–64

    Article  PubMed  CAS  Google Scholar 

  20. Liu J, Cui HM, Peng X, Fang J, Zuo ZC, Wang HS, Wu BY, Deng YX, Wang KP (2012) High dietary fluorine induction of oxidative damage in the cecal tonsil of broilers. Fluoride 45(1):47–52

    Google Scholar 

  21. Luo Q, Cui HM, Peng X, Fang J, Zuo ZC, Liu J, Wu BY, Wang HS, Deng YB, Huang JY (2012) Intestinal oxidative stress in broilers caused by high dietary fluorine. Fluoride 45(4):349–356

    CAS  Google Scholar 

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

    Google Scholar 

  23. Luo Q, Cui HM, Peng X, Fang J, Zuo ZC, Liu J, Wu BY, Wang HS, Deng YB (2013) The association between cytokines and intestinal mucosal immunity among broilers fed on diets supplemented with fluorine. Biol Trace Elem Res 152(2):212–218

    Article  PubMed  CAS  Google Scholar 

  24. Oliveira CA, Telles LF, Oliveira AG, Kalapothakis E, Goncalves-Dornelas H, Mahecha GA (2006) Expression of different classes of immunoglobulin in intraepithelial plasma cells of the Harderian gland of domestic ducks Anas platyrhynchos. Vet Immunol Immunopathol 113(3–4):257–266

    Article  PubMed  CAS  Google Scholar 

  25. Liu J, Cui HM, Peng X, Fang J, Zuo ZC, Deng JL, Wang HS, Wu BY, Deng YX, Wang KP (2013) Decreased IgA+ B cells population and IgA, IgG, IgM contents of the cecal tonsil induced by dietary high fluorine in broilers. Int J Environ Res Public Health 10(5):1775–1785

    Article  PubMed  CAS  Google Scholar 

  26. 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 

  27. Shanthakumari D, Srinivasalu S, Subramanian S (2007) Effect of fluoride intoxication on the levels of intestinal antioxidants studied in rats. Methods Find Exp Clin Pharmacol 29(2):93

    Article  PubMed  CAS  Google Scholar 

  28. Blaszczyk L, Birkner E, Gutowska I, Romuk E, Chlubek D (2012) Influence of metthionine 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 

  29. Elphick DA, Mahida YR (2005) Paneth cells: their role in innate immunity and inflammatory disease. Gut 54(12):1802–1809

    Article  PubMed  CAS  Google Scholar 

  30. Buer J, Balling R (2003) Mice, microbes and models of infection. Nat Rev Genet 4(3):195–205

    Article  PubMed  CAS  Google Scholar 

  31. Jolles S, Kaveri SV, Orange J (2009) Current understanding and future directions. Clin Exp Immunol 158(Suppl 1):68–70

    Article  PubMed  CAS  Google Scholar 

  32. Hanly WC, Artwohl JE, Bennett T (1995) Review of polyclonal antibody production procedures in mammals and poultry. ILAR J 37(3):93–118

    Article  PubMed  Google Scholar 

  33. Lamm ME, Nedrud JG, Kaetzel CS, Mazanec MB (1995) IgA and mucosal defense. APMIS 103(4):241–246

    Article  PubMed  CAS  Google Scholar 

  34. Amin PB, Diebel LN, Liberati DM (2007) T-cell cytokines affect mucosal immunoglobulin A transport. Am J Surg 194(1):128–133

    Article  PubMed  CAS  Google Scholar 

  35. Mazanec MB, Kaetzel CS, Lamm ME, Fletcher D, Nedrud JG (1992) Intracellular neutralization of virus by immunoglobulin A antibodies. PNAS 89(15):6901–6905

    Article  PubMed  CAS  Google Scholar 

  36. Albanese CT, Smith SD, Watkins S, Kurkchubasche A, Simmons RL, Rowe MI (1994) Effect of secretory IgA on transepithelial passage of bacteria across the intact ileum in vitro. J Am Coll Surg 179(6):679–688

    PubMed  CAS  Google Scholar 

  37. 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 

  38. Liu J, Cui HM, Peng X, Fang J, Zuo ZC, Wang HS, Wu BY, Deng YX, Wang KP (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 

  39. Parker DC (1993) T cell- dependent B cell activation. Annu Rev Immunol 11:331–360

    Article  PubMed  CAS  Google Scholar 

  40. 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 

  41. Ratcliffe MJ (2006) Antibodies, immunoglobulin genes and the bursa of Fabricius in chicken B cell development. Dev Comp Immunol 30(1–2):101–118

    Article  PubMed  CAS  Google Scholar 

  42. Boes M (2000) Role of natural and immune IgM antibodies in immune responses. Mol Immunol 37(18):1141–1149

    Article  PubMed  CAS  Google Scholar 

  43. Casali P, Schettino EW (1996) Structure and function of natural antibodies. Curr Top Microbiol Immunol 210:167–179

    Article  PubMed  CAS  Google Scholar 

  44. Sharma JM (1999) Introduction to poultry vaccines and immunity. Adv Vet Med 41:481–494

    Article  PubMed  CAS  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hengmin Cui.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Luo, Q., Cui, H., Peng, X. et al. Intestinal IgA+ Cell Numbers as well as IgA, IgG, and IgM Contents Correlate with Mucosal Humoral Immunity of Broilers During Supplementation with High Fluorine in the Diets. Biol Trace Elem Res 154, 62–72 (2013). https://doi.org/10.1007/s12011-013-9713-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-013-9713-9

Keywords

Navigation