Sub-lethal concentration of arsenic interferes with the proliferation of hepatocytes and induces in vivo apoptosis in Clarias batrachus L.

Comparative Biochemistry and Physiology - C Toxicology and Pharmacology

Volumn 145, Issue 3, 2007, Pages 339-349

  Datta, Soma ^a   Saha, Dhira Rani ^b   Ghosh, Debabrata ^a   Majumdar, Tanmay ^a   Bhattacharya, Shelley ^a   Mazumder, Shibnath ^a  

^a VISVA BHARATI UNIVERSITY   (India)

^b NATIONAL INSTITUTE OF CHOLERA AND ENTERIC DISEASES   (India)

Author keywords

Apoptosis; Arsenic; Clarias batrachus; Liver; Toxicity

Indexed keywords

ALKALINE PHOSPHATASE; ARSENIC; ASPARTATE AMINOTRANSFERASE; CASPASE 3; DNA; LIPOCORTIN 5;

ALKALINE PHOSPHATASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BLOOD CHEMISTRY; CATFISH; CELL DAMAGE; CELL HYPERPLASIA; CELL ISOLATION; CELL NUCLEUS; CELL PROLIFERATION; CELL SIZE; CELL VACUOLE; CHROMATIN CONDENSATION; CLARIUS BATRACHUS; COMET ASSAY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENVIRONMENTAL EXPLOITATION; ENZYME ACTIVITY; HISTOLOGY; IN VIVO STUDY; INTRACELLULAR SPACE; LIVER CELL; LIVER SINUSOID; LIVER TOXICITY; MEGALOCYTOSIS; MITOCHONDRION; MITOCHONDRION SWELLING; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; ROUGH ENDOPLASMIC RETICULUM; SIGNAL TRANSDUCTION; STAINING; TRANSMISSION ELECTRON MICROSCOPY;

CLARIAS BATRACHUS;

EID: 33947720156     PISSN: 15320456     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpc.2007.01.005     Document Type: Article

References (68)

1. Allen T., and Rana S.V.S. Effect of arsenic (AsIII) on glutathione-dependent enzymes in liver and kidney of the fresh water fish Channa punctatus. Biol. Trace Elem. Res. 100 (2004) 39-48
2. Alnemri E.S., Livingston D.J., Nicholson D.W., Salvesen G., Thomberry N.A., and Wong W.W. Human ICE/CED-3 protease nomenclature. Cell 87 (1996) 171
3. Andrew A.S., Warren A.J., Brachowsky A., Temple K.A., Klei L., Soucy N.V., O'ara K.A., and Hamilton J.W. Genomic and proteomic profiling of responses to toxic metals in human lung cells. Environ. Health Perspect. 111 (2003) 825-835
4. ATSDR, 2002. Toxicological Profile for Arsenic. Agency for Toxic Substances and Disease Registry. SUDHHS, PHS, Washington, DC.
5. Au D.W.T., Wu R.S.S., Zhou B.S., and Lam P.K.S. Relationship between ultra structural changes and EROD activities in liver of fish exposed to benzo[a]pyrene. Environ. Pollut. 104 (1999) 235-247
6. Barchowsky A., Roussel R.R., Klei L.R., James P.E., Ganju N., Smith K.R., and Dudek E.J. Low levels of arsenic trioxide stimulate proliferative signals in primary vascular cells without activating stress effector pathways. Toxicol. Appl. Pharmacol. 159 (1999) 65-75
7. Bears H., Richards J.G., and Schulte P.M. Arsenic exposure alters hepatic arsenic species composition and stress mediated-gene expression in the common Killifish (Fundulus heteroclitus). Aquat. Toxicol. 77 (2006) 257-266
8. Bell J.G., McEvoy J., Tocher D.R., McGhee F., Campbell P.J., and Sargent J.R. Replacement of fish oil with rapeseed oil in diets of Atlantic salmon (Salmo salar) affects tissue lipid compositions and hepatocytes fatty acid metabolism. J. Nutr. 131 (2001) 1535-1543
9. Bernstam L., and Nriagu J. Molecular aspects of arsenic stress. J. Toxicol. Environ. Health, Part B. Crit. Rev. 3 (2000) 293-322
10. Bhattacharya A., and Bhattacharya S. Induction of oxidative stress by arsenic in Clarias batrachus: involvement of peroxisomes. Ecotoxicol. Environ. Saf. (2006) 10.1016/j.ecoenv.2005.11.002
11. Bolger T., and Connolly P.L. The selection of suitable indices for the measurement and analysis of fish condition. J. Fish Biol. 34 (1989) 171-182
12. Cantrell S.M., Joy-Schlezinger J., Stegeman J.J., Tillitt D.E., and Hannink M. Correlation of 2,3,7,8-t etrachlorodibenzo-p-dioxin-induced apoptotic cell death in the embryonic vasculature with embryotoxicity. Toxicol. Appl. Pharmacol. 148 (1998) 24-34
13. Cervantes C., Ji G., Ramirez J.L., and Silver S. Resistance to arsenic compounds in microorganisms. FEMS Microbiol. Rev. 15 (1994) 355-367
14. Chen H., Li S.F., Liu J., Diwan B.A., Barrett J.C., and Waalkes M.P. Chronic inorganic arsenic exposure induces hepatic global and individual gene hypomethylation: implications for arsenic hepatocarcinogenesis. Carcinogenesis 25 (2004) 1779-1786
15. Cheng H.Y., Li P., David M., Smithgall T.E., Feng L., and Lieberman M.W. Arsenic inhibition of the JAKSTAT pathway. Oncogene 23 (2004) 3603-3612
16. Chinnaiyan A.M., and Dixit V.M. The cell-death machine. Curr. Biol. 6 (1996) 555-562
17. Crunkhorn S.E., Plant K.E., Gibson G.G., Kramer K., Lyon J., Lord P.G., and Plant N.J. Gene expression changes in rat liver following exposure to liver growth agents: role of Kupffer cells in xenobiotic-mediated liver growth. Biochem. Pharmacol. 67 (2004) 107-118
18. Dutta S., Sinha B., Bhattacharya B., Chatterjee B., and Mazumder S. Characterization of galactose binding serum lectin from the Indian catfish, Clarias batrachus: possible involvement of fish lectin in differential recognition of pathogens. Comp. Biochem. Physiol. C, Comp. Pharmacol. Toxicol. 141 (2005) 76-84
19. Earnshaw W.C., Martins L.M., and Kaufmann S.H. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Ann. Rev. Biochem. 68 (1999) 383-424
20. Ercal N., Gurer-Orhan H., and Aykin-Burns N. Toxic metals and oxidative stress: Part I. Mechanisms involved in metal induced oxidative damage. Curr. Top. Med. Chem. 1 (2001) 529-539
21. Fu T., Guo D., Huang X., O'Gorman M.R.G., Huang L., Crawford S.E., and Soriano H.E. Apoptosis occurs in isolated and banked primary mouse hepatocytes. Cell Transplant 10 (2001) 59-66
22. Galicia G., Leyva R., Tenorio E.P., Ostrosky-Wegman P., and Saavedra R. Sodium arsenite retards proliferation of PHA-activated T cells by delaying the production and secretion of IL-2. Int. Immunopharmacol. 3 (2003) 671-682
23. Gernhöfer M., Pawert M., Schramm M., Müller E., and Triebskorn R. Ultra structural biomarkers as tools to characterize the health status of fish in contaminated streams. J. Aquat. Ecosyst. Stress Recovery 8 (2001) 241-260
24. Ghadially F.N. Ultra Structural Pathology of the Cell and Matrix: Vol. I + I (1988), Butterworths, London 1340
25. Ghosh D., Bhattacharya S., and Mazumder S. Perturbations in the catfish immune responses by arsenic: organ and cell specific effects. Comp. Biochem. Physiol. C, Comp. Pharmacol. Toxicol. 143 (2006) 455-463
26. Ghosh D., Datta S., Bhattacharya S., and Mazumder S. Long-term exposure to arsenic affects head kidney and impairs humoral immune responses of Clarias batrachus. Aquat. Toxicol. 81 (2007) 79-89
27. Gupta S., Yel L., Kim D., Kim C., Chiplunkar S., and Gollapudi S. Arsenic trioxide induces apoptosis in peripheral blood T lymphocyte subsets by inducing oxidative stress: a role of Bcl-2. Mol. Cancer Ther. 2 (2003) 711-719
28. Huang C., Ke Q., Costa M., and Shi X. Molecular mechanisms of arsenic carcinogenesis. Mol. Cell. Biochem. 255 (2004) 57-66
29. Hughes M.F. Arsenic toxicity and potential mechanisms of action. Toxicol. Lett. 133 (2002) 1-16
30. Janicke R.U., Sprengart M.L., Wati M.R., and Porter A.G. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J. Biol. Chem. 273 (1998) 9357-9360
31. Jimi S., Uchiyama M., Tataki A., Suzumiya J., and Hara S. Mechanisms of cell death induced by cadmium and arsenic. Ann. N.Y. Acad. Sci. 1011 (2004) 325-331
32. Johnson G.L., and Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 298 (2002) 1911-1912
33. Larochette N., Decaudin D., Jacotot E., Brenner C., Marzo I., Susin S.A., Zamzami N., Xie Z., Reed J., and Kroemer G. Arsenite induces apoptosis via a direct effect on the mitochondrial permeability transition pore. Exp. Cell Res. 249 (1999) 413-421
34. Larsen E.H., and Francesconi K.A. Arsenic concentrations correlate with salinity for fish taken from the North Sea and Baltic Waters. J. Mar. Biol. 83 (2003) 283-284
35. Lawrence J.W., and Eacho P.I. An overview of peroxisome proliferation. In: Plaa G.L., and Hewitt W.R. (Eds). Toxicology of the Liver (1998), Taylor and Francis 125-158
36. Liao C.M., Tsai J.W., Ling M.P., Lain H.M., Chou Y.H., and Yang P.T. Organ-specific toxicokinetics and dose-response of arsenic in tilapia Oreochromis mossambicus. Arch. Environ. Contam. Toxicol. 47 (2004) 502-510
37. Limuro Y., Nishiura T., Hellerbrand C., Behrns K.E., Schoonhoven R., Grisham J.W., and Brenner D.A. NFκB prevents apoptosis and liver dysfunction during liver regeneration. J. Clin. Invest. 101 (1998) 802-811
38. Liu J., Liu Y., Goyer R.A., Achanzar W., and Waalker M.P. Metallothionein-I/II null mice are more sensitive than wild-type mice to the hepatotoxic and nephrotoxic effects of chronic oral or injected arsenicals. Toxicol. Sci. 55 (2000) 460-467
39. Liu J., Kadiiska M.B., Liu Y., Lu T., Qu W., and Waalkes M.P. Stress related-gene expression in mice treated with inorganic arsenicals. Toxicol. Sci. 61 (2001) 314-320
40. Lowry O.H., Rosebrough N.J., Farr L., and Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193 (1951) 265-275
41. Lu M., Levin J., Sulpice E., Sequeira-Le Grand A., Alemany M., Caen J.P., and Han Z.C. Effect of arsenic trioxide on viability, proliferation, and apoptosis in human megakaryocytic leukemia cell lines. Exp. Hematol. 27 (1999) 845-852
42. Lu T., Liu J., LeCluyse E.L., Zhou Y.S., Ming-Liang Cheng M.L., and Waalkes M.P. Application of cDNA microarray to the study of arsenic-induced liver diseases in the population of Guizhou, China. Toxicol. Sci. 59 (2001) 185-192
43. McCafferty-Grad J., Bahlis N.J., Krett N., Aguilar T.M., Reis I., Lee K.P., and Boise L.H. Arsenic trioxide uses caspase-dependent and caspase independent death pathways in myeloma cells. Mol. Cancer Ther. 2 (2003) 1155-1164
44. Mitchelmore C.L., and Chipman J.K. DNA strand breakage in aquatic organisms and the potential value of the Comet assay in environmental monitoring. Mutat. Res. 399 (1998) 135-147
45. Miller Jr. W.H., Schipper H.M., Lee J.S., Singer J., and Waxman S. Mechanisms of action of arsenic trioxide. Cancer Res. 62 (2002) 3893-3903
46. Nagy P., Teramoto T., Factor V., Sanchez A., Schnur J., Paku S., and Thorgeirsson S. Reconstitution of liver mass via cellular hypertrophy in the rat. Hepatology 33 (2001) 339-345
47. Noreault T.L., Jacobs J.M., Nichols R.C., Trask H.W., Wrighton S.A., Sinclair P.R., Evans R.M., and Sinclair J.F. Arsenite decreases CYP3A23 induction in cultured rat hepatocytes by transcriptional and translational mechanisms. Toxicol. Appl. Pharmacol. 209 (2005) 174-182
48. Pedlar R.M., and Klaverkamp J.F. Accumulation and distribution of dietary arsenic in lake whitefish (Coregonus clupeaformis). Aquat. Toxicol. 57 (2002) 153-166
49. Pedlar R.M., Ptashynski M.D., Wautier K.G., Evans R.E., Baron C.L., and Klaverkamp J.F. The accumulation, distribution, and toxicological effects of dietary arsenic exposure in lake whitefish (Coregonus clupeaformis) and lake trout (Salvelinus namaycush). Comp. Biochem. Physiol. C, Comp. Pharmacol. Toxicol. 131 (2002) 73-91
50. Raisuddin S., and Jha A.N. Relative sensitivity of fish and mammalian cells to sodium arsenate and arsenite as determined by alkaline single-cell gel electrophoresis and cytokinesis-block micronucleus assay. Environ. Mol. Mutagen. 44 (2004) 83-89
51. Reimer K.J., Koch I., Ollson C.A., Cullen W.R., Granchinho S., Andrews P., Jamieson H., and Walker S.R. Arsenic Report vol. 72 (2002), Environmental Science Group, Royal Military College, Kingston, Ontario, Kingston
52. Roy S., and Bhattacharya S. Arsenic-induced histopathology and synthesis of stress proteins in liver and kidney of Channa punctatus. Ecotoxicol. Environ. Saf. 65 (2005) 218-229
53. Roy P., and Saha A. Metabolism and toxicity of arsenic: a human carcinogen. Curr. Sci. 82 (2002) 38-45
54. Roy S., Chattoraj A., and Bhattacharya S. Arsenic-induced changes in optic tectal histoarchitecture and acetylcholinesterase-acetylcholine profile in Channa punctatus: amelioration by selenium. Comp. Biochem. Physiol. C, Comp. Pharmacol. Toxicol. 144 (2006) 16-24
55. Schlegel R.A., and Williamson P. Phosphatidylserine, a death knell. Cell Death Differ. 8 (2001) 551-563
56. Schramm M., Müller E., and Triebskorn R. Brown trout (Salmo trutta f. Fario) liver ultra structure as a biomarker for assessment of small stream pollution. Biomarkers 3 (1998) 93-108
57. Sorenson E.M.B. Arsenic. In: Sorenson E.M.B. (Ed). Metal Poisoning in Fish (1991), CRC Press 61-99
58. Sweet L.I., Passino-Reader D.R., Meier P.G., and Omann G.M. Xenobiotic-induced apoptosis: significance and potential application as a general biomarker of response. Biomarkers 4 (1999) 237-253
59. Takatsu A., Kuroiwa T., and Uchiumi A. Arsenic accumulation in organs of the fresh water fish Tribolodon hakonensis. J. Trace Elem. Med. Biol. 13 (1999) 176-179
60. Vahter M. Mechanisms of arsenic biotransformation. Toxicology 181-182 (2002) 211-217
61. van Heerde W.L., Robert-Offerman S., Dumont E., Hofstra L., Doevendans P.A., Smiths J.F., Daemen M.J., and Reutelingsperger C.P. Markers of apoptosis in cardiovascular tissues: focus on annexin V. Cardiovasc. Res. 45 (2000) 549-559
62. Vermes I., Haanen C., Stefffens-Nakken H., and Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labeled annexin V. J. Immunol. Methods 184 (1995) 39-51
63. Waalkes M.P., Keefer L.K., and Diwan B.A. Induction of proliferative lesions of the uterus, testes, and liver in Swiss mice given repeated injections of sodium arsenate: possible estrogenic mode of action. Toxicol. Appl. Pharmacol. 166 (2000) 24-35
64. Wang Y.C., Chaung R.H., and Tung L.C. Comparison of the cytotoxicity induced by different exposure to sodium arsenite in two fish cell lines. Aquat. Toxicol. 69 (2004) 67-79
65. Wrobel K., Wrobel K., Parker B., Kannamkumarath S.S., and Caruso J.A. Determination of As(III), As(IV), monomethylarsonic acid, dimethylarsenic acid and arsenobetaine by HPLC-ICP-MS: analysis of reference material, fish tissue and urine. Talanta 58 (2002) 899-907
66. Wu W.Z., Zhou B.S., Xu Y., Schramm K.W., and Kettrup A. Cytological and biochemical alterations in Carassius auratus hepatocytes from exposure to sediment containing dioxins and related compounds. Arch. Environ. Contam. Toxicol. 37 (1999) 358-363
67. Yang J.L., and Chen H.C. Serum metabolic enzyme activities and hepatocyte ultrastructure of common carp after gallium exposure. Zool. Stud. 42 (2003) 455-461
68. Zhang T., Wang S.-S., Hong L., Wang X.-L., and Qi Q.-H. Arsenic trioxide induces apoptosis of rat hepatocellular carcinoma cells in vivo. J. Exp. Clin. Cancer Res. 22 (2003) 1-8