Effects of carbon tetrachloride on oxidative stress, inflammatory response and hepatocyte apoptosis in common carp (Cyprinus carpio)

Aquatic Toxicology

Volumn 152, Issue , 2014, Pages 11-19

  Jia, Rui ^a,b   Cao, Li Ping ^b   Du, Jin Liang ^b   Wang, Jia Hao ^a   Liu, Ying Juan ^a   Jeney, Galina ^c   Xu, Pao ^a,b   Yin, Guo Jun ^a,b  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b SOUTH CHINA SEA FISHERIES RESEARCH INSTITUTE   (China)

^c National Agricultural Research Center Research Institute for Fisherie and Aquaculture   (Hungary)

Author keywords

Apoptosis; Carbon tetrachloride; Cyprinus carpio; Inflammatory cytokines; Nuclear translocation factor

Indexed keywords

ALANINE AMINOTRANSFERASE; ARACHIS OIL; ASPARTATE AMINOTRANSFERASE; CARBON TETRACHLORIDE; CATALASE; CYTOCHROME P450 2E1; GLUTATHIONE; GLUTATHIONE PEROXIDASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; MALONALDEHYDE; SUPEROXIDE DISMUTASE; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

EXPERIMENTAL STUDY; FISH; GENE EXPRESSION; INORGANIC CARBON; INORGANIC COMPOUND; LABORATORY METHOD; TOXICITY TEST;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIOXIDANT ASSAY; APOPTOSIS; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BLOOD SAMPLING; CARP; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME BLOOD LEVEL; GENE EXPRESSION; HISTOPATHOLOGY; IN VITRO STUDY; INFLAMMATION; LIPID PEROXIDATION; LIVER; LIVER CELL; LIVER TOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UPREGULATION;

APOPTOSIS; CARBON TETRACHLORIDE; CYPRINUS CARPIO; INFLAMMATORY CYTOKINES; NUCLEAR TRANSLOCATION FACTOR;

ANIMALS; APOPTOSIS; CARBON TETRACHLORIDE; CARPS; CELL SURVIVAL; CYTOKINES; GENE EXPRESSION REGULATION; HEPATOCYTES; LIPID PEROXIDATION; NECROSIS; NF-KAPPA B; OXIDATIVE STRESS; OXIDOREDUCTASES; SIGNAL TRANSDUCTION; WATER POLLUTANTS, CHEMICAL;

EID: 84897936960     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2014.02.014     Document Type: Article

References (62)

1. Aldridge J.R., Moseley C.E., Boltz D.A., Negovetich N.J., Reynolds C., Franks J., Brown S.A., Doherty P.C., Webster R.G., Thomas P.G. TNF/iNOS-producing dendritic cells are the necessary evil of lethal influenza virus infection. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:5306-5311.
2. Allis J.W., Brown B.L., Simmons J.E., Hatch G.E., McDonald A., House D.E. Methanol potentiation of carbon tetrachloride hepatotoxicity: the central role of cytochrome P450. Toxicology 1996, 112:131-140.
3. 4)-induced tissue injury in male Wistar rats. Toxicol. Ind. Health 2011, 27:923-933.
4. 4 on rosy barb (Puntius conchonius) and amphioxus (Branchiostoma belcheri) with implications of liver ontogeny. Toxicol. Mech. Methods 2008, 18:627-633.
5. Cakmak I., Horst W.J. Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol. Plantarum 1991, 83:463-468.
6. Casillas E., Myers M., Ames W.E. Relationship of serum chemistry values to liver and kidney histopathology in English sole (Parophrys vetulus) after acute exposure to carbon tetrachloride. Aquat. Toxicol. 1983, 3:61-78.
7. Chen C.-Y., Wooster G.A., Bowser P.R. Comparative blood chemistry and histopathology of tilapia infected with Vibrio vulnificus or Streptococcus iniae or exposed to carbon tetrachloride, gentamicin, or copper sulfate. Aquaculture 2004, 239:421-443.
8. Chen H., Xing B., Liu X., Zhan B., Zhou J., Zhu H., Chen Z. Ozone oxidative preconditioning inhibits inflammation and apoptosis in a rat model of renal ischemia/reperfusion injury. Eur. J. Pharmacol. 2008, 581:306-314.
9. Cheshchevik V., Lapshina E., Dremza I., Zabrodskaya S., Reiter R., Prokopchik N., Zavodnik I. Rat liver mitochondrial damage under acute or chronic carbon tetrachloride-induced intoxication: protection by melatonin and cranberry flavonoids. Toxicol. Appl. Pharmacol. 2012, 261:271-279.
10. Clawson G. Mechanisms of carbon tetrachloride hepatotoxicity. Pathol. Immunopath. Res. 1989, 8:104-112.
11. 4 -intoxicated mice. Toxicology 2011, 280:33-43.
12. Forni L., Packer J., Slater T., Willson R. Reaction of the trichloromethyl and halothane-derived peroxy radicals with unsaturated fatty acids: a pulse radiolysis study. Chem. Biol. Interact. 1983, 45:171-177.
13. Ghosh S., May M.J., Kopp E.B. NF-{kappa} B and Rel proteins: evolutionarily conserved mediators of immune responses. Sci. Signal. 1998, 16:225.
14. Guicciardi M., Gores G. Apoptosis: a mechanism of acute and chronic liver injury. Gut 2005, 54:1024-1033.
15. 4-induced hepatocyte apoptosis in rats via a p53-mediated pathway. World J. Gastroenterol. 2013, 19:3781.
16. 4-induced hepatic fibrosis in mice. J. Pharmacol. Exp. Ther. 2012, 342:835-842.
17. Hua J., Qiu D.K., Li J.Q., Li E.L., Chen X.Y., Peng Y.S. Expression of Toll-like receptor 4 in rat liver during the course of carbon tetrachloride-induced liver injury. J. Gastroenterol. Hepatol. 2007, 22:862-869.
18. Ikatsu H., Shinoda S., Nakajima T. CYP2E1 level in rat liver injured by the interaction between carbon tetrachloride and chloroform. J. Occup. Health 1998, 40:223-229.
19. Jia R., Cao L., Xu P., Jeney G., Yin G. In vitro and in vivo hepatoprotective and antioxidant effects of Astragalus polysaccharides against carbon tetrachloride-induced hepatocyte damage in common carp (Cyprinus carpio). Fish Physiol. Biochem. 2012, 38:871-881.
20. Jiang W., Gao M., Sun S., Bi A., Xin Y., Han X., Wang L., Yin Z., Luo L. Protective effect of l-theanine on carbon tetrachloride-induced acute liver injury in mice. Biochem. Biophys. Res. Commun. 2012, 422:344-350.
21. Kavitha P., Ramesh R., Bupesh G., Stalin A., Subramanian P. Hepatoprotective activity of Tribulus terrestris extract against acetaminophen-induced toxicity in a freshwater fish (Oreochromis mossambicus). In Vitro Cell. Dev. Biol. Anim. 2011, 47:698-706.
22. Kim H.-Y., Park J., Lee K.-H., Lee D.-U., Kwak J.-H., Kim Y.S., Lee S.-M. Ferulic acid protects against carbon tetrachloride-induced liver injury in mice. Toxicology 2011, 282:104-111.
23. Kotsanis N., Metcalfe C. Enhancement of hepatocarcinogenesis in rainbow trout with carbon tetrachloride. Bull. Environ. Contam. Toxicol. 1991, 46:879-886.
24. Kumar S. Caspase function in programmed cell death. Cell Death Differ. 2006, 14:32-43.
25. Krasnov A., Afanasyev S., Oikari A. Hepatic responses of gene expression in juvenile brown trout (Salmo trutta lacustris) exposed to three model contaminants applied singly and in combination. Environ. Toxicol. Chem. 2007, 26:100-109.
26. Krasnov A., Koskinen H., Rexroad C., Afanasyev S., Mölsä H., Oikari A. Transcriptome responses to carbon tetrachloride and pyrene in the kidney and liver of juvenile rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 2005, 74:70-81.
27. Larsen B.D., Rampalli S., Burns L.E., Brunette S., Dilworth F.J., Megeney L.A. Caspase 3/caspase-activated DNase promote cell differentiation by inducing DNA strand breaks. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:4230-4235.
28. Li J., Yuan J. Caspases in apoptosis and beyond. Oncogene 2008, 27:6194-6206.
29. Lin X., Huang R., Zhang S., Zheng L., Wei L., He M., Zhou Y., Zhuo L., Huang Q. Methyl helicterate protects against CCl4-induced liver injury in rats by inhibiting oxidative stress, NF-κB activation, Fas/FasL pathway and cytochrome P4502E1 level. Food Chem. Toxicol. 2012, 50:3413-3420.
30. Liu J., Chen I., Kwang J. Characterization of a previously unidentified viral protein in porcine circovirus type 2-infected cells and its role in virus-induced apoptosis. J. virol. 2005, 79:8262-8274.
31. 4-induced hepatic injury in mice is associated with inhibition of nuclear factor kappa B binding. Hepatology 1995, 22:1474-1481.
32. -δδCT method. Methods 2001, 25:402-408.
33. Lora J., Alonso F.J., Segura J.A., Lobo C., Marquez J., Mates J.M. Antisense glutaminase inhibition decreases glutathione antioxidant capacity and increases apoptosis in Ehrlich ascitic tumour cells. Eur. J. Biochem. 2004, 271:4298-4306.
34. Malhi H., Gores G.J. Cellular and molecular mechanisms of liver injury. Gastroenterology 2008, 134:1641-1654.
35. Manuelpillai U., Tchongue J., Lourensz D., Vaghjiani V., Samuel C.S., Liu A., Williams E.D., Sievert W. Transplantation of human amnion epithelial cells reduces hepatic fibrosis in immunocompetent CCl4-treated mice. Cell Transplant. 2010, 19:1157-1168.
36. Marucci L., Alpini G., Glaser S.S., Alvaro D., Benedetti A., Francis H., Phinizy J.L., Marzioni M., Mauldin J., Venter J. Taurocholate feeding prevents CCl4-induced damage of large cholangiocytes through PI3-kinase-dependent mechanism. Am. J. Physiol. Gastrointest. Liver Physiol. 2003, 284:G290-G301.
37. Miller A.H., Maletic V., Raison C.L. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol. Psychiatry 2009, 65:732-741.
38. Muller D.N., Dechend R., Mervaala E.M., Park J.-K., Schmidt F., Fiebeler A., Theuer J., Breu V., Ganten D., Haller H. NF-κB inhibition ameliorates angiotensin II-induced inflammatory damage in rats. Hypertension 2000, 35:193-201.
39. OECD OECD Guidelines for the Testing of Chemicals 1994, Organization for Economic.
40. Ohkawa H., Ohishi N., Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 1979, 95:351-358.
41. Parajuli D.R., Park E.-J., Che X.-H., Jiang W.-Y., Kim Y.-C., Sohn D.H., Lee S.H. PF2401-SF, standardized fraction of Salvia miltiorrhiza, induces apoptosis of activated hepatic stellate cells in vitro and in vivo. Molecules 2013, 18:2122-2134.
42. Peskin A.V., Winterbourn C.C. A microtiter plate assay for superoxide dismutase using a water-soluble tetrazolium salt (WST-1). Clin. Chim. Acta 2000, 293:157-166.
43. Pesonen M., Andersson T.B. Fish primary hepatocyte culture; an important model for xenobiotic metabolism and toxicity studies. Aquat. Toxicol. 1997, 37:253-267.
44. Råbergh C.M., Lipsky M.M. Toxicity of chloroform and carbon tetrachloride in primary cultures of rainbow trout hepatocytes. Aquat. Toxicol. 1997, 37:169-182.
45. Recknagel R.O., Glende E.A., Dolak J.A., Waller R.L. Mechanisms of carbon tetrachloride toxicity. Pharmacol. Ther. 1989, 43:139-154.
46. Rotruck J., Pope A., Ganther H., Swanson A., Hafeman D., Hoekstra W.S. Biochemical role as a component of glutathione peroxidase. Science 1973, 179:588-590.
47. Reyes-Gordillo K., Segovia J., Shibayama M., Vergara P., Moreno M.G., Muriel P. Curcumin protects against acute liver damage in the rat by inhibiting NF-κB, proinflammatory cytokines production and oxidative stress. Biochim. Biophys. Acta 2007, 1770:989-996.
48. 4-induced fibrosis but not steatosis or inflammation. Alcohol. Clin. Exp. Res. 2012, 36:1139-1147.
49. Schwabe R.F., Seki E., Brenner D.A. Toll-like receptor signaling in the liver. Gastroenterology 2006, 130:1886-1900.
50. Shi H., Dong L., Jiang J., Zhao J., Zhao G., Dang X., Lu X., Jia M. Chlorogenic acid reduces liver inflammation and fibrosis through inhibition of toll-like receptor 4 signaling pathway. Toxicology 2013, 303:107-114.
51. Shim J.-Y., Kim M.-H., Kim H.-D., Ahn J.-Y., Yun Y.-S., Song J.-Y. Protective action of the immunomodulator ginsan against carbon tetrachloride-induced liver injury via control of oxidative stress and the inflammatory response. Toxicol. Appl. Pharmacol. 2010, 242:318-325.
52. Son G., Iimuro Y., Seki E., Hirano T., Kaneda Y., Fujimoto J. Selective inactivation of NF-κB in the liver using NF-κB decoy suppresses CCl4-induced liver injury and fibrosis. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 293:G631-G639.
53. Statham C.N., Croft W.A., Lech J.J. Uptake, distribution, and effects of carbon tetrachloride in rainbow trout (Salmo gairdneri). Toxicol. Appl. Pharmacol. 1978, 45:131-140.
54. 4-intoxicated mice. Fish. Sci. 2012, 78:911-921.
55. Tao L.-L., Cheng Y.-Y., Ding D., Mei S., Xu J.-W., Yu J., Ou-Yang Q., Deng L., Chen Q., Li Q.-Q. C/EBP-α ameliorates CCl4-induced liver fibrosis in mice through promoting apoptosis of hepatic stellate cells with little apoptotic effect on hepatocytes in vitro and in vivo. Apoptosis 2012, 17:492-502.
56. Vajdovich P., Szilagyi A., Gaál T. Evaluation of blood lipid peroxidation parameters in carbon tetrachloride (CCl4) toxicity in sheep. Acta Vet. Hung. 1995, 43:423.
57. Wang L.-L., Liu T., Wang C., Zhao F.-Q., Zhang Z.-W., Yao H.-D., Xing H.-J., Xu S.-W. Effects of atrazine and chlorpyrifos on the production of nitric oxide and expression of inducible nitric oxide synthase in the brain of common carp (Cyprinus carpio L.). Ecotoxicol. Environ. Saf. 2013, 43:239-324.
58. Weber L.W., Boll M., Stampfl A. Hepatotoxicity and mechanism of action of haloalkanes: carbon tetrachloride as a toxicological model. CRC Crit. Rev. Toxicol. 2003, 33:105-136.
59. Wieckowska A., Zein N.N., Yerian L.M., Lopez A.R., McCullough A.J., Feldstein A.E. In vivo assessment of liver cell apoptosis as a novel biomarker of disease severity in nonalcoholic fatty liver disease. Hepatology 2006, 44:27-33.
60. Yan F., Zhang Q.Y., Jiao L., Han T., Zhang H., Qin L.P., Khalid R. Synergistic hepatoprotective effect of Schisandrae lignans with Astragalus polysaccharides on chronic liver injury in rats. Phytomedicine 2009, 16:805-813.
61. Yen F.-L., Wu T.-H., Lin L.-T., Cham T.-M., Lin C.-C. Naringenin-loaded nanoparticles improve the physicochemical properties and the hepatoprotective effects of naringenin in orally-administered rats with CCl4-induced acute liver failure. Pharm. Res. 2009, 26:893-902.
62. Yin G.J., Cao L.P., Xu P., Jeney G., Nakao M., Lu C.P. Hepatoprotective and antioxidant effects of Glycyrrhiza glabra extract against carbon tetrachloride (CCl4)-induced hepatocyte damage in common carp (Cyprinus carpio). Fish Physiol. Biochem. 2011, 37:209-216.