Copper exposure induces oxidative injury, disturbs the antioxidant system and changes the Nrf2/ARE (CuZnSOD) signaling in the fish brain: Protective effects of myo-inositol

Aquatic Toxicology

Volumn 155, Issue , 2014, Pages 301-313

  Jiang, Wei Dan ^a   Liu, Yang ^a   Hu, Kai ^a   Jiang, Jun ^a   Li, Shu Hong ^a   Feng, Lin ^a   Zhou, Xiao Qiu ^a  

^a SICHUAN AGRICULTURAL UNIVERSITY   (China)

Author keywords

Antioxidant; Copper; Jian carp (Cyprinus carpio var. Jian); Myo inositol; Nrf2; Oxidative stress

Indexed keywords

ANTIOXIDANT; BRAIN; COPPER; CYPRINID; ENZYME ACTIVITY; GENE; NERVOUS SYSTEM; RNA; TOXICITY;

ANTIOXIDANT; COPPER; JIAN CARP (CYPRINUS CARPIO VAR. JIAN); MYO-INOSITOL; NRF2; OXIDATIVE STRESS;

ANIMALS; ANTIOXIDANTS; BRAIN; CARPS; COPPER; GENE EXPRESSION REGULATION, ENZYMOLOGIC; INOSITOL PHOSPHATES; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE; WATER POLLUTANTS, CHEMICAL;

EID: 84905164892     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2014.07.003     Document Type: Article

References (56)

1. Al-Bairuty G.A., Shaw B.J., Handy R.D., Henry T.B. Histopathological effects of waterborne copper nanoparticles and copper sulphate on the organs of rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 2013, 126:104-115.
2. Attia A.A., ElMazoudy R.H., El-Shenawy N.S. Antioxidant role of propolis extract against oxidative damage of testicular tissue induced by insecticide chlorpyrifos in rats. Pestic. Biochem. Physiol. 2012, 103:87-93.
3. Bae S.H., Sung S.H., Oh S.Y., Lim J.M., Lee S.K., Park Y.N., Lee H.E., Kang D., Rhee S.G. Sestrins activate Nrf2 by promoting p62-dependent autophagic degradation of Keap1 and prevent oxidative liver damage. Cell Metab. 2013, 17:73-84.
4. Baltacioǧlu E., Akalin F.A., Alver A., Deǧer O., Karabulut E. Protein carbonyl levels in serum and gingival crevicular fluid in patients with chronic periodontitis. Arch. Oral Biol. 2008, 53:716-722.
5. Boettler U., Sommerfeld K., Volz N., Pahlke G., Teller N., Somoza V., Lang R., Hofmann T., Marko D. Coffee constituents as modulators of Nrf2 nuclear translocation and ARE (EpRE)-dependent gene expression. J. Nutr. Biochem. 2011, 22:426-440.
6. 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.
7. Chang H., Guo M., Kasten F.H., Chang M., Huang G., Wang Y., Wang R., Jeng J. Stimulation of glutathione depletion, ROS production and cell cycle arrest of dental pulp cells and gingival epithelial cells by HEMA. Biomaterials 2005, 26:745-753.
8. El-Sayed T., Mota A., Fraternali F., Ortiz M. Biomechanics of traumatic brain injury. Comput. Meth. Appl. Mech. Eng. 2008, 197:4692-4701.
9. Gao D., Xu Z.E., Zhang X., Wang H., Wang Y., Min W. Molecular cloning, immunohistochemical localization, characterization and expression analysis of caspase-9 from the purse red common carp (Cyprinus carpio) exposed to cadmium. Aquat. Toxicol. 2013, 142:53-62.
10. Giuliani M.E., Regoli F. Identification of the Nrf2-Keap1 pathway in the European eel Anguilla anguilla: role for a transcriptional regulation of antioxidant genes in aquatic organisms. Aquat. Toxicol. 2014, 150:117-123.
11. Gornicka A., Fettig J., Eguchi A., Berk M.P., Thapaliya S., Dixon L.J., Feldstein A.E. Adipocyte hypertrophy is associated with lysosomal permeability both in vivo and in vitro: role in adipose tissue inflammation. Am. J. Physiol.-Endocrinol. Metab. 2012, 303:E597-E606.
12. Halliwell B. The role of oxygen radicals in human disease, with particular reference to the vascular system. Pathophysiol. Haemostasis Thromb. 1993, 23:118-126.
13. Haris M., Cai K., Singh A., Hariharan H., Reddy R. In vivo mapping of brain myo-inositol. NeuroImage 2011, 54:2079-2085.
14. He W., Zhou X.Q., Feng L., Jiang J., Liu Y. Dietary pyridoxine requirement of juvenile Jian carp (Cyprinus carpio var. Jian). Aquacult. Nutr. 2009, 15:402-408.
15. Itoh K., Wakabayashi N., Katoh Y., Ishii T., O'Connor T., Yamamoto M. Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles. Genes Cells 2003, 8:379-391.
16. Jia R., Cao L., Du J., Wang J., Liu Y., Jeney G., Xu P., Yin G. Effects of carbon tetrachloride on oxidative stress, inflammatory response and hepatocyte apoptosis in common carp (Cyprinus carpio). Aquat. Toxicol. 2014, 152:11-19.
17. Jiang W. Effects of myo-inositol on the antioxidant ability in the intestine of juveniles Jian carp (Cyprinus carpio var. Jian) and the mechanism studies. Dissertation 2012, Sichuan Agricultural University, Ya'an, China.
18. Jiang W., Wu P., Kuang S., Liu Y., Jiang J., Hu K., Li S., Tang L., Feng L., Zhou X. Myo-inositol prevents copper-induced oxidative damage and changes in antioxidant capacity in various organs and the enterocytes of juvenile Jian carp (Cyprinus carpio var. Jian). Aquat. Toxicol. 2011, 105:543-551.
19. Jiang W., Liu Y., Jiang J., Hu K., Li S., Feng L., Zhou X. In vitro interceptive and reparative effects of myo-inositol against copper-induced oxidative damage and antioxidant system disturbance in primary cultured fish enterocytes. Aquat. Toxicol. 2013, 132-133:100-110.
20. Jiang W., Feng L., Liu Y., Jiang J., Zhou X. Growth, digestive capacity and intestinal microflora of juvenile Jian carp (Cyprinus carpio var. Jian) fed graded levels of dietary inositol. Aquacult. Res. 2009, 40:955-962.
21. Jiang W., Feng L., Liu Y., Jiang J., Zhou X. Myo-inositol prevents oxidative damage, inhibits oxygen radical generation and increases antioxidant enzyme activities of juvenile Jian carp (Cyprinus carpio var. Jian). Aquacult. Res. 2009, 40:1770-1776.
22. Jiang W., Kuang S., Liu Y., Jiang J., Hu K., Li S., Tang L., Feng L., Zhou X. Effects of myo-inositol on proliferation, differentiation, oxidative status and antioxidant capacity of carp enterocytes in primary culture. Aquacult. Nutr. 2013, 19:45-53.
23. Jin Y., Tian L., Zeng S., Xie S., Yang H., Liang G., Liu Y. Dietary lipid requirement on non-specific immune responses in juvenile grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol. 2013, 34:1202-1208.
24. Kobayashi M., Itoh K., Suzuki T., Osanai H., Nishikawa K., Katoh Y., Takagi Y., Yamamoto M. Identification of the interactive interface and phylogenic conservation of the Nrf2-Keap1 system. Genes Cells 2002, 7:807-820.
25. Kobayashi M., Li L., Iwamoto N., Nakajima-Takagi Y., Kaneko H., Nakayama Y., Eguchi M., Wada Y., Kumagai Y., Yamamoto M. The antioxidant defense system Keap1-Nrf2 comprises a multiple sensing mechanism for responding to a wide range of chemical compounds. Mol. Cell. Biol. 2009, 29:493-502.
26. Kohen R., Nyska A. Invited review: oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol. Pathol. 2002, 30:620-650.
27. Li H., Feng L., Jiang W., Liu Y., Jiang J., Li S., Zhou X. Oxidative stress parameters and anti-apoptotic response to hydroxyl radicals in fish erythrocytes: Protective effects of glutamine, alanine, citrulline and proline. Aquat. Toxicol. 2013, 126:169-179.
28. Lushchak V.I., Lushchak L.P., Mota A.A., Hermes-Lima M. Oxidative stress and antioxidant defenses in goldfish Carassius auratus during anoxia and reoxygenation. Am. J. Physiol.-Regul. Integr. Comp. Physiol. 2001, 280:R100-R107.
29. Lyu K., Zhu X., Chen R., Chen Y., Yang Z. Molecular cloning of manganese superoxide dismutase gene in the cladoceran Daphnia magna: effects of microcystin, nitrite, and cadmium on gene expression profiles. Aquat. Toxicol. 2014, 148:55-64.
30. Lyu K., Zhu X., Wang Q., Chen Y., Yang Z. Copper/zinc superoxide dismutase from the Cladoceran Daphnia magna: molecular cloning and expression in response to different acute environmental stressors. Environ. Sci. Technol. 2013, 47:8887-8893.
31. Martinez-Alvarez R.M., Morales A.E., Sanz A. Antioxidant defenses in fish: biotic and abiotic factors. Rev. Fish Biol. Fish. 2005, 15:75-88.
32. Mieiro C.L., Pereira M.E., Duarte A.C., Pacheco M. Brain as a critical target of mercury in environmentally exposed fish (Dicentrarchus labrax)-bioaccumulation and oxidative stress profiles. Aquat. Toxicol. 2011, 103:233-240.
33. Mieiro C.L., Pacheco M., Pereira M.E., Duarte A.C. Mercury distribution in key tissues of fish (Liza aurata) inhabiting a contaminated estuary-implications for human and ecosystem health risk assessment. J. Environ. Monit. 2009, 11:1004-1012.
34. Mitsuishi Y., Taguchi K., Kawatani Y., Shibata T., Nukiwa T., Aburatani H., Yamamoto M., Motohashi H. Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming. Cancer Cell 2012, 22:66-79.
35. Monteiro S.M., Dos Santos N., Calejo M., Fontainhas-Fernandes A., Sousa M. Copper toxicity in gills of the teleost fish, Oreochromis niloticus: effects in apoptosis induction and cell proliferation. Aquat. Toxicol. 2009, 94:219-228.
36. Mustafa S.A., Davies S.J., Jha A.N. Determination of hypoxia and dietary copper mediated sub-lethal toxicity in carp, Cyprinus carpio, at different levels of biological organisation. Chemosphere 2012, 87:413-422.
37. Nakajima H., Nakajima-Takagi Y., Tsujita T., Akiyama S., Wakasa T., Mukaigasa K., Kaneko H., Tamaru Y., Yamamoto M., Kobayashi M. Tissue-restricted expression of Nrf2 and its target genes in zebrafish with gene-specific variations in the induction profiles. PLoS One 2011, 6(10):e26884. 10.1371/journal.pone.0026884.
38. Niture S.K., Jain A.K., Jaiswal A.K. Antioxidant-induced modification of INrf2 cysteine 151 and PKC-delta-mediated phosphorylation of Nrf2 serine 40 are both required for stabilization and nuclear translocation of Nrf2 and increased drug resistance. J. Cell Sci. 2009, 122:4452-4464.
39. Oliveira M., Pacheco M., Santos M.A. Organ specific antioxidant responses in golden grey mullet (Liza aurata) following a short-term exposure to phenanthrene. Sci. Total Environ. 2008, 396:70-78.
40. Rudneva I.I. Blood antioxidant system of Black Sea elasmobranch and teleosts. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 1997, 118:255-260.
41. Şahin E., Gümüşlü S. Alterations in brain antioxidant status, protein oxidation and lipid peroxidation in response to different stress models. Behav. Brain Res. 2004, 155:241-248.
42. Santoro M., Caffaratti E., Salas-Peregrin J.M., Korecz L., Rockenbauer A., Sala L.F., Signorella S. Kinetics and mechanism of the chromic oxidation of myo-inositol. Polyhedron 2007, 26:169-177.
43. Schmidt M.M., Dringen R. Glutathione (GSH) Synthesis and Metabolism Neural Metabolism In Vivo 2012, 1029-1050. Springer, US, (Reprinted).
44. Shaw B.J., Al-Bairuty G., Handy R.D. Effects of waterborne copper nanoparticles and copper sulphate on rainbow trout (Oncorhynchus mykiss): physiology and accumulation. Aquat. Toxicol. 2012, 116:90-101.
45. Shiau S., Su S. Juvenile tilapia (Oreochromis niloticus×Oreochromis aureus) requires dietary myo-inositol for maximal growth. Aquaculture 2005, 243:273-277.
46. Singh A., Misra V., Thimmulappa R.K., Lee H., Ames S., Hoque M.O., Herman J.G., Baylin S.B., Sidransky D., Gabrielson E. Dysfunctional KEAP1-NRF2 interaction in non-small-cell lung cancer. PLoS Med. 2006, 3:e420.
47. Skiba-Cassy S., Lansard M., Panserat S., Médale F. Rainbow trout genetically selected for greater muscle fat content display increased activation of liver TOR signaling and lipogenic gene expression. Am. J. Physiol.-Regul. Integr. Comp. Physiol. 2009, 297:R1421-R1429.
48. Takagi Y., Kobayashi M., Li L., Suzuki T., Nishikawa K., Yamamoto M. MafT, a new member of the small Maf protein family in zebrafish. Biochem. Biophys. Res. Commun. 2004, 320:62-69.
49. Upadhyay R., Panda S.K. Zinc reduces copper toxicity induced oxidative stress by promoting antioxidant defense in freshly grown aquatic duckweed Spirodela polyrhiza L. J. Hazard. Mater. 2010, 175:1081-1084.
50. US EPA EPA's 2007 Report on the Environment: Science Report (SAB Review Draft) 2007, US EPA, 〈http://cfpub.epa.gov/ncea/cfm/recordisplay.cfm?deid=140917〉.
51. Vardi N., Parlakpinar H., Ozturk F., Ates B., Gul M., Cetin A., Erdogan A., Otlu A. Potent protective effect of apricot and β-carotene on methotrexate-induced intestinal oxidative damage in rats. Food Chem. Toxicol. 2008, 46:3015-3022.
52. Wu G., Fang Y., Yang S., Lupton J.R., Turner N.D. Glutathione metabolism and its implications for health. J. Nutr. 2004, 134:489-492.
53. Xu S., Zhou Z., Zhang L., Yu Z., Zhang W., Wang Y., Wang X., Li M., Chen Y., Chen C. Exposure to 1800MHz radiofrequency radiation induces oxidative damage to mitochondrial DNA in primary cultured neurons. Brain Res. 2010, 1311:189-196.
54. Yao J., Liu J., Kong X., Zhang S., Wang X., Yu M., Zhan Y., Li W., Xu W., Tang L. Induction of activation of the antioxidant response element and stabilization of Nrf2 by 3-(3-pyridylmethylidene)-2-indolinone (PMID) confers protection against oxidative stress-induced cell death. Toxicol. Appl. Pharmacol. 2012, 259:227-235.
55. Zhang J., Guo L., Feng L., Jiang W., Kuang S., Liu Y., Hu K., Jiang J., Li S., Tang L., Zhou X. Soybean β-conglycinin induces inflammation and oxidation and causes dysfunction of intestinal digestion and absorption in fish. PLoS One 2013, 8(3). e58115, 1-12. 10.1371/journal.pone.0058115.
56. Zhang X., Zhu Y., Cai L., Wu T. Effects of fasting on the meat quality and antioxidant defenses of market-size farmed large yellow croaker (Pseudosciaena crocea). Aquaculture 2008, 280:136-139.