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.
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References
Meenakshi, Maheshwari RC (2006) Fluoride in drinking water and its removal. J Hazard Mater 137(1):456–463
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
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
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
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
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
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
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
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
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
Zahvoronkov AA, Strochkova LS (1981) Fluorosis: geographical pathology and some experimental findings. Fluoride 14(4):182–191
Sharma JD, Jain P, Sohu D (2009) Gastric discomforts from fluoride in drinking water in Sanganer Tehsil, Rajasthan, India. Fluoride 42(4):286–291
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
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
Nochi T, Kiyono H (2006) Innate immunity in the mucosal immune system. Curr Pharm Des 12(32):4203–4213
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
Parkin J, Cohen B (2001) An overview of the immune system. Lancet 357(9270):1777–1789
Perdigon G, Alvarez S, Rachid M, Aguero G, Gobbato N (1995) Immune system stimulation by probiotics. J Dairy Sci 78(7):1597–1606
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
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
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
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
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
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
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
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
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
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
Elphick DA, Mahida YR (2005) Paneth cells: their role in innate immunity and inflammatory disease. Gut 54(12):1802–1809
Buer J, Balling R (2003) Mice, microbes and models of infection. Nat Rev Genet 4(3):195–205
Jolles S, Kaveri SV, Orange J (2009) Current understanding and future directions. Clin Exp Immunol 158(Suppl 1):68–70
Hanly WC, Artwohl JE, Bennett T (1995) Review of polyclonal antibody production procedures in mammals and poultry. ILAR J 37(3):93–118
Lamm ME, Nedrud JG, Kaetzel CS, Mazanec MB (1995) IgA and mucosal defense. APMIS 103(4):241–246
Amin PB, Diebel LN, Liberati DM (2007) T-cell cytokines affect mucosal immunoglobulin A transport. Am J Surg 194(1):128–133
Mazanec MB, Kaetzel CS, Lamm ME, Fletcher D, Nedrud JG (1992) Intracellular neutralization of virus by immunoglobulin A antibodies. PNAS 89(15):6901–6905
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
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
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
Parker DC (1993) T cell- dependent B cell activation. Annu Rev Immunol 11:331–360
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
Ratcliffe MJ (2006) Antibodies, immunoglobulin genes and the bursa of Fabricius in chicken B cell development. Dev Comp Immunol 30(1–2):101–118
Boes M (2000) Role of natural and immune IgM antibodies in immune responses. Mol Immunol 37(18):1141–1149
Casali P, Schettino EW (1996) Structure and function of natural antibodies. Curr Top Microbiol Immunol 210:167–179
Sharma JM (1999) Introduction to poultry vaccines and immunity. Adv Vet Med 41:481–494
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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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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
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DOI: https://doi.org/10.1007/s12011-013-9713-9