Toxicological effects of nickel chloride on IgA+B cells and sIgA, IgA, IgG, IgM in the intestinal mucosal immunity in Broilers

International Journal of Environmental Research and Public Health

Volumn 11, Issue 8, 2014, Pages 8175-8192

  Wu, Bangyuan ^a   Cui, Hengmin ^a   Peng, Xi ^a   Fang, Jing ^a   Zuo, Zhicai ^a   Deng, Junliang ^a   Huang, Jianying ^a  

^a SICHUAN AGRICULTURAL UNIVERSITY   (China)

Author keywords

Broiler; Cecal tonsil; Immunoglobulins; Nickel chloride; Small intestine

Indexed keywords

IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; NICKEL CHLORIDE; SECRETORY IMMUNOGLOBULIN; IMMUNOGLOBULIN CLASS; NICKEL; POLLUTANT;

ANTIBODY; BIRD; CHLORIDE; DIET; IMMUNITY; TOXICITY; TOXICOLOGY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; BROILER; CECAL TONSIL; CECUM; CONTROLLED STUDY; DIET SUPPLEMENTATION; DUODENUM; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMORAL IMMUNITY; ILEUM; IMMUNOGLOBULIN PRODUCTION; IMMUNOHISTOCHEMISTRY; IMMUNOTOXICITY; INFANT; INTESTINE MUCOSA; JEJUNUM; LYMPHOCYTE COUNT; LYMPHOCYTE SUBPOPULATION; NONHUMAN; PROTEIN CONTENT; ANALYSIS; ANIMAL; ANIMAL FOOD; CHICKEN; DIET; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; MUCOSAL IMMUNITY; POLLUTANT; RANDOMIZATION; SMALL INTESTINE; TOXICITY;

ANIMAL FEED; ANIMALS; CECUM; CHICKENS; DIET; DIETARY SUPPLEMENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENTAL POLLUTANTS; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN ISOTYPES; IMMUNOHISTOCHEMISTRY; INTESTINAL MUCOSA; INTESTINE, SMALL; NICKEL; RANDOM ALLOCATION;

EID: 84926119417     PISSN: 16617827     EISSN: 16604601     Source Type: Journal    
DOI: 10.3390/ijerph110808175     Document Type: Article

References (52)

1. World Health Organization (WHO). GEMS-Global Fresh Water Quality. Blackwell Reference: Oxford, UK, 1991.
2. Ayvaz, Z. Cevre Kirliligi ve Kontrolü. Paper presented at the meeting of E. ü. Uluslararas cevre koruma sempozyumu, Izmir, Turkey, 8, June, 1992; Vol.1.
3. Wu, B.Y.; Cui, H.M.; Peng, X.; Fang, J.; Zuo, Z.; Deng, J.; Huang, J. Investigation of the serum oxidative stress in broilers fed on diets supplemented with nickel chloride. Health 2013a, 5, 454-459.
4. World Health Organization (WHO). Environmental Health Criteria for Lindane 124. The International Programme on Chemical Safety (IPCS). Environmental Health Criteria: Geneva, Switzerland, 1991.
5. Kasprzak, K.S.; Sunderman, F.W., Jr.; Salnikow, K. Nickel carcinogenesis. Mutat. Res. 2003, 533, 67-97.
6. Hoang, T.C.; Tomasso, J.; Klaine, S. Influence of water quality and age on nickel toxicity to fathead minnows (Pimephales promelas). Environ. Toxicol. Chem. 2004, 23, 86-92.
7. Pandey, R.; Srivastava, S.P. Spermatotoxic effects of nickel in mice. B Environ. Contam. Tox. 2000, 64, 161-167.
8. Anke, M.; Groppel, B.; Krause, U.; Langer, M. Further data on the biological essentiality of nickel. In Trace Elements in Man and Animals 6; Hurley, L.S., Keen, C.L., Lonnerdal, B., Rucker, R.B., Eds.; Plenum: New York, NY, USA, 1988; pp. 467-469.
9. Ling, J.R.; Leach, M., Jr. Studies on nickel metabolism: interaction with other elements. Poult. Sci. 1979, 58, 591-596.
10. Vijayavela, K.; Gopalakrishnana, S.; Thiagarajanb, R.; Thilagam, H. Immunotoxic effects of nickel in the mud crab. Scylla serrata. Fish. Shellfish Immun. 2009, 26, 133-139.
11. Salsano, F.; Francia, C.; Roumpedaki, I.; Proietti, M.; Pisarri, S.; Verna, N.; Gabriele, E.; Di Gioacchino, G.; Di Gioacchino, M. Immune effects of nickel. Int. J. Immunopathol. Pharmacol. 2004, 17, 63-69.
12. Wu, B.Y.; Cui, H.M.; Peng, X.; Fang, J.; Zuo, Z.; Deng, J.; Huang, J. Changes in the serum cytokine contents in broilers fed on diets supplemented with nickel chloride. Biol. Trace Elem. Res. 2013b, 151, 234-239.
13. Wu, B.Y.; Cui, H.M.; Peng, X.; Fang, J.; Zuo, Z.; Deng, J.; Huang, J. Dietary nickel chloride induces oxidative stress, apoptosis and alters Bax/Bcl-2 and caspase-3 mRNA expression in the cecal tonsil of broilers. Food Chem. Toxicol. 2014, 63, 18-29.
14. Lillehoj, H.S.; Trout, J.M. Avian gut-associated lymphoid tissues and intestinal immune responses to Eimeria parasites. Clin. Microbiol. Rev. 1996, 9, 349-360.
15. Liu, J.; Cui, H.M.; Peng, X.; Fang, J.; Zuo, Z.C.; Deng, J.; Wang, H.; Wu, B.Y.; Deng, Y.X.; Wang, K. Decreased IgA+ B cells population and IgA, IgG, IgM contents of the cecal tonsil induced by dietary high fluorine in broilers. Int. J. Env. Res. Pub. Health 2013, 10, 1775-1785.
16. Akter, S.; Khan, M.Z.I.; Jahan, M.R.; Karim, M.R.; Islam, M.R. Histomorphological study of the lymphoid tissues of broiler chickens. Bangl. J. Vet. Med. 2006, 4, 87-92.
17. National Research Council (NRC). Nutrient Requirements of Poultry, 9th ed.; National Academy Press: Washington, DC, USA, 1994.
18. Clem, A.S. Fundamentals of vaccine immunology. J. Global Infect. Dis. 2011, 3, 73-78.
19. Parkin, J.; Cohen, B. An overview of the immune system. Lancet 2001, 357, 1777-1789.
20. Hecht, G.A. Microbial Pathogenesis and the Intestinal Epithelial Cell; ASM American Society for Microbiology: Washington, DC, USA, 2003; pp. 61-72.
21. Jolles, S.; Kaveri, S.V.; Orange, J. Current understanding and future directions. Clin. Exp. Immunol. 2009, 158, 68-70.
22. Perdigon, G.; Alvarez, S.; Rachid, M.; Agüero, G.; Gobbato, N. Immune system stimulation by probiotics. J. Dairy Sci. 1995, 78, 1597-1606.
23. Neutra, M.R.; Mantis, N.J.; Kraehenbuhl, J.P. Collaboration of epithelial cells with organized mucosal lymphoid tissues. Nat. Immunol. 2001, 2, 1004-1009.
24. Fagarasan, S.; Kinoshita, K.; Muramatsu, M.; Ikuta, K.; Honjo, T. In situ class switching and differentiation to IgA-producing cells in the gut lamina propria. Nature 2001, 413, 639-643.
25. Treagan, L. A survey of the effect of metals on the immune response. Biol. Trace Elem. Res. 1979, 1, 141-148.
26. Diagomanolin, V.; Farhang, M.; Ghazi-Khansari, M.; Jafarzadeh, N. Heavy metals (Ni, Cr, Cu) in the Karoon waterway river, Iran. Toxicol. Lett. 2004, 151, 63-67.
27. Bencko, V.; Wagner, V.; Wagnerova, M.; Zavázal, V. Human exposure to nickel and cobalt: Biological monitoring and immunobiochemical response. Environ. Res. 1986, 40, 399-410.
28. Figoni, R.A.; Treagan, L. Inhibitory effect of nickel and chromium upon antibody response of rats to immunization with T-1 phage. Res. Commun. Chem. Path Pharmacol. 1975, 11, 335-338.
29. Al-Tawil, N.G.; Marcusson, J.A.; Möller, E. T and B lymphocytes in patients with nickel sensitivity. Scand. J. Immunol. 1985, 22, 495-502.
30. Graham, J.A.; Gardner, D.E.; Miller, F.J.; Daniels, M.J.; Coffin, D.L. Effect of nickel chloride on primary antibody production in the spleen. Environ. Health Persp. 1975, 12, 109-113.
31. Graham, J.A.; Miller, F.J.; Daniels, M.J.; Payne, E.A.; Gardner, D.E. Influence of cadmium, nickel, and chromium on primary immunity in mice. Environ. Res. 1978, 16, 77-87.
32. Reynaud, C.A.; Imhof, B.A.; Anquez, V.; Weill, J.C. Emergence of committed B lymphoid progenitors in the developing chicken embryo. EMBO J. 1992, 11, 4349-4358.
33. Benatar, T.; Tkalec, L.; Ratcliffe, M.J.H. Stochastic rearrangement of immunoglobulin variable-region genes in chicken B-cell development. Proc. Natl. Acad. Sci. USA 1992, 89, 7615-7619.
34. Ratcliffe, M.J.H.; Ivanyi, J. Allotype suppression in the chicken. IV. Deletion of B cells and lack of suppressor cells during chronic suppression. Eur. J. Immunol. 1981, 11, 306-310.
35. Mockett, A.P.A. Monoclonal antibodies used to isolate IgM from chicken bile and avian sera and to detect specific IgM in chicken sera. Avian Pathol. 1986, 15, 337-348.
36. Lindner, C.; Wahl, B.; Föhse, L.; Suerbaum, S.; Macpherson, A.J.; Prinz, I.; Pabst, O. Age, microbiota, and T cells shape diverse individual IgA repertoires in the intestine. J. Exp. Med. 2012, 209, 365-377.
37. Brandtzaeg, P.; Baekkevold, E.S.; Morton, H.C. From B to A the mucosal way. Nat. Immunol. 2001, 2, 1093-1094.
38. Schroeder, H.W., Jr.; Cavacini, L. Structure and function of immunoglobulins. J. Allergy Clin. Immun. 2010, 125, S41-S52.
39. Wieland, W.H.; Orzaez, D.; Lammers, A.; Parmentier, H.; Verstegen, M.; Schots, A. A functional polymeric immunoglobulin receptor in chicken (Gallus gallus) indicates ancient role of secretory IgA in mucosal immunity. Biochem. J. 2004, 380, 669-676.
40. Lamm, M.E. Interaction of antigens and antibodies at mucosal surfaces. Annu. Rev. Microbiol. 1997, 51, 311-340.
41. Lammers, A.; Wieland, W.H.; Kruijt, L.; Jansma, A.; Straetemans, T.; Schots, A.; Hartoga, G.D.; Parmentier, H.K. Successive immunoglobulin and cytokine expression in the small intestine of juvenile chicken. Dev. Comp. Immunol. 2010, 34, 1254-1262.
42. Santos, R.R.; Sartori, A.; Lima, D.S.; Souza, P.R.; Coelho-Castelo, A.A.; Bonato, V.L.; Silva, C.L. DNA vaccine containing the mycobacterial hsp65 gene prevented insulitis in MLD-STZ diabetes. J. Immun. Based Ther. Vaccines 2009, 7, 4-15.
43. Mowat, A.M. Anatomical basis of tolerance and immunity to intestinal antigens. Nat. Rev. Immunol. 2003, 3, 331-341.
44. Zimmermann, K.; Haas, A.; Oxenius, A. Systemic antibody responses to gut microbes in health and disease. Gut Microbes 2012, 3, 42-47.
45. Fan, J.; Meng, Q.; Guo, G.; Xie, Y.; Li, X.; Xiu, Y.; Li, T.; Ma, L. Effects of early enteral nutrition supplemented with arginine on intestinal mucosal immunity in severely burned mice. Clin. Nutr. 2010, 29, 124-130.
46. Wu, B.Y.; Cui, H.M.; Peng, X.; Fang, J.; Zuo, Z.; Deng, J.; Huang, J. Toxicological effects of nickel chloride on the cytokine mRNA expression and protein levels in intestinal mucosal immunity of broilers. Environ. Toxicol. DOI: 10.1002/tox.22001.
47. Amin, P.B.; Diebel, L.N.; Liberati, D.M. T-cell cytokines affect mucosal immunoglobulin A transport. Am. J. Surg. 2007, 194, 128-133.
48. Perez-Carbajal, C.; Caldwell, D.; Farnell, M.; Stringfellow, K.; Pohl, S.; Casco, G.; Pro-Martinez, A.; Ruiz-Feria, C.A. Immune response of broiler chickens fed different levels of arginine and vitamin E to a coccidiosis vaccine and Eimeria challenge. Poultry Sci. 2010, 89, 1870-1877.
49. Boes, M. Role of natural and immune IgM antibodies in immune responses. Mol. Immunol. 2000, 37, 1141-1149.
50. Hirano, T.; Yasukawa, K.; Harada, H.; Taga, T.; Watanabe, Y.; Matsuda, T.; Kashiwamura, S.; Iwamatsu, A.; Tsunasawa, S.; Sakiyama, F.; et al. Complementary DNA for a novel human interleukin (BSF-2) that induces B lymphocytes to produce immunoglobulin. Nature 1986, 324, 73-76.
51. Shimizu, M.; Nagashima, H.; Sano, K.; Hashimoto, K.; Ozeki, M.; Tsuda, K.; Hatta, H. Molecular stability of chicken and rabbit immunoglobulin G. Biosci. Biotech. Bioch. 1992, 56, 270-274.
52. Koller, L.D.; Exon, J.H.; Roan, J.G. Humoral antibody response in mice after single dose exposure to lead or cadmium. Exp. Biol. Med. 1976, 151, 339-342.