Dietary nickel chloride induces oxidative stress, apoptosis and alters Bax/Bcl-2 and caspase-3 mRNA expression in the cecal tonsil of broilers

Food and Chemical Toxicology

Volumn 63, Issue , 2014, Pages 18-29

  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

Apoptosis protein expression; Broilers; Cecal tonsil; MRNA expression; Oxidative stress

Indexed keywords

CASPASE 3; CATALASE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; HYDROXYL RADICAL; MALONALDEHYDE; MESSENGER RNA; NICKEL CHLORIDE; PROTEIN BAX; PROTEIN BCL 2; SUPEROXIDE DISMUTASE;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BROILER; CECAL TONSIL; CONTROLLED STUDY; DIET SUPPLEMENTATION; DIETARY INTAKE; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; INTESTINE MUCOSA; LYMPHOCYTE; MUCOSAL IMMUNITY; NONHUMAN; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; TONSIL;

AVES; GLYCINE MAX; ZEA MAYS;

APOPTOSIS PROTEIN EXPRESSION; BROILERS; CECAL TONSIL; MRNA EXPRESSION; OXIDATIVE STRESS;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CASPASE 3; CATALASE; CHICKENS; GLUTATHIONE PEROXIDASE; MALONDIALDEHYDE; NICKEL; OXIDATIVE STRESS; PALATINE TONSIL; RNA, MESSENGER; SUPEROXIDE DISMUTASE;

EID: 84887570366     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2013.10.033     Document Type: Article

References (76)

1. Adams J.M., Cory S. The Bcl-2 protein family: arbiters of cell survival. Science 1998, 281:1322-1326.
2. 1 and ethanol co-exposure induces hepatic oxidative damage in mice. Toxicol. Ind. Health 2010, 26:717-724.
3. Ahamed M., Akhtar M.J., Siddiqui M.A., Ahmad J., Musarratc J., Al-Khedhairyc A.A., AlSalhia M.S., Alrokayana S.A. Oxidative stress mediated apoptosis induced by nickel ferrite nanoparticles in cultured A549 cells. Toxicology 2011, 283:101-108.
4. Albini B., Wick G. Delineation of B and T lymphoid cells in the chicken. Immunology 1974, 112:444-461.
5. Alnemri E.S., Livingston D.J., Nicholson D.W., Salvesen G., Thornberry N.A., Wong W.W., Yuan J. Human ICE/CED-3 protease nomenclature. Cell 1996, 87:171.
6. Aspegren N., Rorsman H. Short-term culture of leucocytes in nickel hypersensitivity. Acta Dermatol. Vener. 1962, 42:412-417.
7. Athar M., Hasan S.K., Srivastava R.C. Evidence for the involvement of hydroxyl radicals in nickel mediated enhancement of lipid peroxidation: implications for nickel carcinogenesis. Biochem. Biophys. Res. Co. 1987, 147:1276-1281.
8. Agency for Toxic Substances and Disease Registry (ATSDR), 2005. Toxicological Profile for Nickel. Department of Health and Human Services, Public Health Service, Atlanta, GA, US, pp. 95-107.
9. Aw T.Y. Intestinal glutathione: determinant of mucosal peroxide transport, metabolism, and oxidative susceptibility. Toxicol. Appl. Pharm. 2005, 204:320-328.
10. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
11. Cempel M., Nikel G. Nickel: a review of its sources and environmental toxicology. Pol. J. Environ. Stud. 2006, 15:375-382.
12. Chen J.J., Yu B.P. Alteration in mitochondrial membrane fluidity by lipid peroxidation products. Free Radic. Biol. Med. 1994, 17:411-418.
13. Chen C.Y., Sheu J.Y., Lin T.H. Oxidative effects of nickel on bone marrow and blood of rats. J. Toxicol. Environ. Health A 1999, 58:475-483.
14. Chinnaiyan A.M., Orth K., O'Rourke K., Duan H., Poirier G.G., Dixit V.M. Molecular ordering of the cell death pathway: bcl-2 and bcl-xL function upstream of the ced-3-like apoptotic proteases. J. Biol. Chem. 1996, 271:4573-4576.
15. Chowdhury M.J., Bucking C., Wood C.M. Is nickel an essential metal for aquatic animals. Integr. Environ. Assess. Manage. 2008, 4:266-267.
16. Clayton G.D., Clayton F.E. Patty's Industrial Hygiene Toxicology 1994, A Wiley-Interscience Publication, New York, pp. 2157-2173. fourth ed.
17. Coogan T.P., Latta D.M., Snow E.T., Costa M., Lawrence A. Toxicity and carcinogenicity of nickel compounds. Crit. Rev. Toxicol. 1989, 19:341-384.
18. Costa M., Klein C.B. Nickel carcinogenesis, mutation, epigenetics, or selection. Environ. Health Perspect. 1999, 107:A438-A439.
19. Cotran K., Kumar V. Robbins Pathologic Basis of Disease 1998, W.B. Saunders Company, Philadelphia.
20. Das K.K., Das S.N., Dhundasi S.A. Nickel, its adverse health effects & oxidative stress. Ind. J. Med. Res. 2008, 128:412-425.
21. 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.
22. Donskoy E., Donskoy M., Forouhar F., Gillies C.G., Marzouk A., Reid M.C., Zaharia O., Sunderman F.W. Hepatic toxicity of nickel chloride in rats. Ann. Clin. Lab. Sci. 1986, 16:108-117.
23. Dusanic D., Bencina D., Oven I. Mycoplasma synoviae induces upregulation of apoptotic genes, secretion of nitric oxide and appearance of an apoptotic phenotype in infected chicken chondrocytes. Vet. Res. 2012, 43:1-14.
24. Flohe L., Beckmann R., Giertz H., Loschen G. Oxygen-centered free radicals as mediators of inflammation. Oxidative Stress 1985, 405-437. Academic Press, New York. H. Sies (Ed.).
25. Freeman B.A., Crapo J.D. Biology of disease: free radicals and tissue injury. Lab. Invest. 1982, 47:412-426.
26. Gaca M.D.A., Pickering J.A., Arthur M.J.P., Benyon R.C. Human and rat hepatic stellate cells produce stem cell factor: a possible mechanism for mast cell recruitment in liver fibrosis. J. Hepatol. 1999, 30(5):850-858.
27. Gagliano N., Dalle D.I., Torri C., Migliori M., Grizzi F., Milzani A., Filippi C., Annoni G., Colombo P., Costa F., Cava G.G., Bertelli A.A.E., Giovannini L., Gioia M. Early cytotoxic effects of ochratoxin A in rat liver: a morphological, biochemical and molecular study. Toxicology 2006, 225:214-224.
28. Ghavami S., Hashemi M., Ande S.R., Yeganeh B., Xiao W., Eshraghi M., Bus C.J., Kadkhoda K., Wiechec E., Halayko A.J., Los M. Apoptosis and cancer: mutations within caspase genes. J. Med. Genet. 2009, 46:497-510.
29. Haber L.T., Erdreicht L., Diamond G.L., Maier A.M., Ratney R., Zhao Q., Dourson M.L. Hazard identification and dose response of inhaled nickel-soluble salts. Regul. Toxicol. Pharmacol. 2000, 31:210-230.
30. Halliwell B., Chirico S. Lipid peroxidation: its mechanism, measurement, and significance. Am. J. Clin. Nutr. 1993, 57:715S-725S.
31. Hamidu J.A., Uddin Z., Li M. Broiler egg storage induces cell death and influences embryo quality. Poult. Sci. 2011, 90:1749-1757.
32. Hockenbery D.M., Oltvai Z.N., Yin X.M., Milliman C.L., Korsmeyer S.J. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 1993, 75:241-251.
33. Hoshi H., Mori T. Identification of the bursa-dependent and Thymus-dependent areas in the tonsilla caecalis of chickens. Tohoku. Exp. Med. 1973, 111:309-322.
34. Howard S., Bottino C., Brooke S., Cheng E., Giffard R.G., Sapol-sky R. Neuroprotective effects of Bcl-2 overexpression in hippocampal cultures: interactions with pathways of oxidative damage. J. Neurochem. 2002, 83:914-923.
35. Humberd J., Boyd K., Webster R.G. Emergence of influenza A virus variants after prolonged shedding from pheasants. J. Virol. 2007, 81:4044-4051.
36. Iqbal M., Philbin V.J., Smith A.L. Expression patterns of chicken Toll-like receptor mRNA in tissues, immune cell subsets and cell lines. Vet. Immunol. Immunop. 2005, 104:17-127.
37. Janero D.R. Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radic. Biol. Med. 1990, 9:515-540.
38. Janicka K., Cempel M. Lipid peroxidation and selected antioxidants in rat liver after oral exposure to nickel (II) chloride. Bromatol. Chem. Toksykol. 2001, 34:291-295.
39. Kannana K., Jain S.K. Oxidative stress and apoptosis. Pathophysiology 2000, 7:153-163.
40. Kasprzak K.S. The role of oxidative damage in metal carcinogenicity. Chem. Res. Toxicol. 1991, 4:604-615.
41. Kasprzak K.S. Possible role of oxidative damage in metal-induced carcinogenesis. Cancer Invest. 1995, 13:411-430.
42. Koh J.K., Kim W.H., Lee C.H. Early gene expression in mouse spleen cells after exposure to nickel acetate. J. Toxicol. Publ. Health 2006, 22:95-102.
43. Kok P.L., Shan H.H., Ranil D.S., Benny H.T., Yi Z.Z. Oxidative stress: apoptosis in neuronal injury. Curr. Alzheimer Res. 2006, 3:327-337.
44. LaBella F.S., Dular R., Lemon P., Vivian S., Queen G. Prolactin secretion is specifically inhibited by nickel. Nature 1973, 245:330-332.
45. LaBella F.S., Dular R., Vivian S., Queen G. Pituitary hormone releasing or inhibiting activity of metal ions present in hypothalamic extracts. Biochem. Biophys. Res. Co. 1973, 52:786-791.
46. Lee K.H., Kim K.C., Jung Y.J., Ham Y.H., Jang J.J. Induction of apoptosis in p53-deficient human hepatoma cell line by wild-type p53 gene transduction: inhibition by antioxidant. Mol. Cell 2001, 12:17-24.
47. Lillehoj H.S., Lillehoj E.P. Avian coccidiosis. A review of acquired intestinal immunity and vaccination strategies. Avian Dis. 2000, 44:408-425.
48. 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.
49. Ling J.R., Leach R.M. Studies on nickel metabolism: interaction with other elements. Poult. Sci. 1979, 58:591-596.
50. Marnett L.J. Lipid peroxidation-DNA damage by malondialdehyde. Mutat. Res-Fund. Mol. Mech. 1999, 424:83-95.
51. Mates J.M., Sanchez-Jimenez F.M. Role of reactive oxygen species in apoptosis: implications for cancer therapy. Int. J. Biochem. Cell Biol. 2000, 32:157-170.
52. Muller F.L., Lustgarten M.S., Jang Y., Richardson A., Remmen H.V. Trends in oxidative aging theories. Free Radic. Biol. Med. 2007, 43:477-503.
53. Nielsen F.H. Nutrition requirement for boron, silicon vanadium, nickel and arsenic: current knowledge and speculations. FASEB J. 1991, 5:2661-2667.
54. Nielsen F.H., Uthus E.O., Poellot R.A., Shuler T.R. Dietary vitamin B12, sulfur amino acids, and oddchain fatty acids affect the responses of rats to nickel deprivation. Biol. Trace Elem. Res. 1993, 37:1-15.
55. NRC, 1994. Nutrient Requirements of Domestic Animals. Nutrient Requirements of Poultry, ninth ed. National Academy of Science, Washington, DC.
56. Petit A., Mwale F., Zukor D.J., Catelas I., Antoniou J., Huk O.L. Effect of cobalt and chromium ions on bcl-2, bax, caspase-3, and caspase-8 expression in human U937 macrophages. Biomaterials 2004, 25:2013-2018.
57. Phipps T., Tank S.L., Wirtz J., Brewer L., Coyner A., Ortego L.A., Fairbrother A. Essentiality of nickel and homeostatic mechanisms for its regulation in terrestrial organisms. Environ. Rev. 2002, 10:209-261.
58. Ragsdale S.W. Nickel enzymes and cofactors. Encyclopedia of Inorganic Chemistry 2006, 3378-3393. John Wiley & Sons Ltd., New York. R.B. King (Ed.).
59. Reiter R.J., Melchiorri D., Sewerynek E., Poeggeler B., Barlow-Walden L., Chuang J., Ortiz G.G. A review of the evidence supporting melatonin's role as an antioxidant. J. Pineal Res. 1995, 18:1-11.
60. 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.
61. Salvesen G.S. Caspases: opening the boxes and interpreting the arrows. Cell Death Differ. 2002, 9:3-5.
62. Scott-Fordsmand J.J. Toxicity of nickel to soil organisms in Denmark. Rev. Environ. Contam. Toxicol. 1997, 148:1-34.
63. 1. Free Radical Biol. Med. 1996, 21:139-146.
64. Shirkey R.J., Chakraborty J., Bridges J.W. An improved method for preparing rat small intestine microsomal fractions for studying drug metabolism. Anal. Biochem. 1979, 93:73-81.
65. Stangl G.I., Kirchgessner M. Nickel deficiency alters liver lipid metabolism in rats. J. Nutr. 1996, 126:2466-2473.
66. Starkov A.A., Polster B.M., Fiskum G. Regulation of hydrogen peroxide production by brain mitochondria by calcium and Bax. J. Neurochem. 2002, 83:220-228.
67. Streit W.J., Kincaid-Colton C.A. The brain's immune system. Sci. Am. 1995, 273:54-61.
68. Sunderman F.W., Marzouk A., Hopfer S.M., Zaharia O., Reid M.C. Increased lipid peroxidation in tissues of nickel chloride-treated rats. Ann. Clin. Lab. Sci. 1985, 15:229-236.
69. Thornberry N.A., Lazebnik Y. Caspases: enemies within. Science 1998, 281:1312-1316.
70. Uthus E.O., Poellot R.A. Dietary nickel and folic acid interact to affect folate and methionine metabolism in the rat. Biol. Trace Elem. Res. 1997, 58:25-33.
71. Vijayavel K., Gopalakrishnan S., Thiagarajan R., Thilagam H. Immunotoxic effects of nickel in the mud crab Scylla serrata. Fish. Shellfish. Immun. 2009, 26:133-139.
72. Walters J., Pop C., Scott F.L., Drag M., Swartz P., Mattos C., Salvesen G.S., Clark A.C. A constitutively active and uninhibitable caspase-3 zymogen efficiently induces apoptosis. Biochem. J. 2009, 424:335-345.
73. Wei Q., Kasprzak K.S., Kadiiska M., Liu J., Chen H., Maciag A., Mason R.P., Michael P. Mechanisms of arsenic-induced cross-tolerance to nickel cytotoxicity, genotoxicity, and apoptosis in rat liver epithelial cells. Toxicol. Sci. 2001, 63:189-195.
74. Yang J., Liu X.S., Bhalla K., Kim C.N., Ibrado A.M., Cai J.Y., Peng T., Jones D.P., Wang X.D. Prevention of apoptosis by bcl-2: release of cytochrome c from mitochondria blocked. Science 1997, 275:1129-1132.
75. 1. Pharm. Med. 2011, 3:205-210.
76. Yokoi K., Uthus E.O., Nielsen F.H. Nickel deficiency diminishes sperm quantity and movement in rats. Biol. Trace Elem. Res. 2003, 93:141-153.