Oxidative stress and hepatic stellate cell activation are key events in arsenic induced liver fibrosis in mice

Toxicology and Applied Pharmacology

Volumn 251, Issue 1, 2011, Pages 59-69

  Ghatak, Subhadip ^a   Biswas, Ayan ^a   Dhali, Gopal Krishna ^a   Chowdhury, Abhijit ^a,b   Boyer, James L ^c   Santra, Amal ^a,b  

^a INSTITUTE OF POST GRADUATE MEDICAL EDUCATION AND RESEARCH   (India)

^b Liver Foundation   (India)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Arsenic; Liver; Oxidative stress; Reactive oxygen species

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ARSENIC; BIOLOGICAL MARKER; COLLAGEN TYPE 1; CYTOKINE; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN BAX; PROTEIN BCL 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARSENIC POISONING; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; FATTY LIVER; FIBROGENESIS; INFLAMMATION; INFLAMMATORY CELL; LIVER CELL; LIVER FIBROSIS; LIVER INJURY; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; STELLATE CELL;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; ARSENITES; CELLS, CULTURED; COCULTURE TECHNIQUES; CYTOKINES; DISEASE MODELS, ANIMAL; DRUG-INDUCED LIVER INJURY; FATTY LIVER; HEPATIC STELLATE CELLS; INFLAMMATION MEDIATORS; LIPID PEROXIDATION; LIVER CIRRHOSIS; MALE; MICE; MICE, INBRED BALB C; NADPH OXIDASE; OXIDATIVE STRESS; SODIUM COMPOUNDS; TIME FACTORS;

MURINAE; MUS;

EID: 78751638450     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2010.11.016     Document Type: Article

References (59)

1. Arthur M.J. Fibrogenesis II (Metalloproteinases and their inhibitors in liver fibrosis). Am. J. Physiol. Gastrointest. Liver Physiol. 2000, 279:245-249.
2. Bachem M.G., Shell K.M., Melchior R., Kroof J., Gressner A.M. TNF-alpha and TGF-beta1 stimulate fibronectin synthesis and the transdifferentiation of fat storing cells in the rat liver into myofibroblast. Virchows Arch. B Cell Pathol. 1993, 63:123-130.
3. Bagla P., Kaiser J. India's spreading health crisis draws global arsenic experts. Science 1996, 274:174-175.
4. Bansal M.B., Kovalovich K., Gupta R., Li W., Agarwal A., Radbill B., et al. Interleukin-6 protects hepatocytes from CCl4-mediated necrosis and apoptosis in mice by reducing MMP-2 expression. J. Hepatol. 2005, 42:548-556.
5. Bataller R., Schwabe R.F., Choi Y.H., Yang L., Paik Y.H., Lindquist J., et al. NADPH oxidase signal transduces angiotensin II in hepatic stellate cells and is critical in hepatic fibrosis. J. Clin. Invest. 2003, 112:1383-1394.
6. Bissell D.M., Roulot D., George J. Transforming growth factor beta and the liver. Hepatology 2001, 34:859-867.
7. Cao Q., Mak K.M., Lieber C.S. Dilinoleoylphosphatidylcholine prevents transforming growth factor-β1-mediated collagen accumulation in cultured rat hepatic stellate cells. J. Lab. Clin. Med. 2002, 139:202-210.
8. Chen C.J., Chen C.W., Wu M.M. Arsenic and cancer. Lancet 1988, 1:414-415.
9. Chi I.C., Blackwell R.Q. A controlled retrospective study of blackfoot disease, an endemic peripheral gangrene disease in Taiwan. Am. J. Epidemiol. 1968, 88:7-24.
10. Choi J., Ou J.H. Mechanisms of Liver Injury. III. Oxidative stress in the pathogenesis of hepatitis C virus. Am. J. Physiol. Gastrointest. Liver Physiol. 2006, 290:G847-G851.
11. Das S., Santra A., Lahiri S., Guha Mazumder D.N. Implications of oxidative stress and hepatic cytokine (TNF-α and IL-6) response in the pathogenesis of hepatic collagenesis in chronic arsenic toxicity. Toxicol. Appl. Pharmacol. 2005, 204:18-26.
12. Davis G., Bayless K.J., Davis M., Meininger GA J. Regulation of tissue injury responses by the exposure of matricryptic sites within extracellular matrix molecules. Am. J. Pathol. 2000, 156:1489-1498.
13. Day C.P., James O.F. Hepatic steatosis: innocent bystander or guilty party?. Hepatology 1998, 27:1463-1466.
14. Ding W.X., Ni H.M., Francesca D.D., Stolz D.B., Yin X.M. Bid-dependent generation of oxygen radicals promotes death receptor activation-induced apoptosis in murine hepatocytes. Hepatology 2004, 40:403-413.
15. Dutta D.V., Mitra S.K., Chhuttani P.N., Chakravarti R.N. Chronic oral arsenic intoxication as a possible etiological factor in idiopathic portal hypertension (non-cirrhotic portal fibrosis) in India. Gut 1979, 20:378-384.
16. Elsharkawy A.M., Oakley F., Mann D.A. The role and regulation of hepatic stellate cell apoptosis in reversal of liver fibrosis. Apoptosis 2005, 10:927-939.
17. Environmental Protection Agency National primary drinking water regulations; arsenic and clarifications to compliance and new source contaminants monitoring; final rule. Fed. Regist. 2001, 66:6976-7066.
18. Esterbauer H., Schaur R.J., Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 1991, 11:81-128.
19. Fendorf S., Michael H.A., Van Geen A. Spatial and temporal variations of groundwater arsenic in south and Southeast Asia. Science 2010, 328:1123-1127.
20. Fontana L., Jerez D., Rojas-Valencia L., Solís-Herruzo J.A., Greenwel P., Rojkind M. Ethanol induces the expression of alpha 1(I) procollagen mRNA in a co-culture system containing a liver stellate cell-line and freshly isolated hepatocytes. Biochim. Biophys. Acta 1997, 1362:135-144.
21. Friedman S.L. Cytokines and fibrogenesis. Semin. Liver Dis. 1999, 19:129-140.
22. Friedman S.L. Mechanism of hepatic fibrogenesis. Gastroenterology 2008, 134:1655-1669.
23. Friedman S.L., Roll F.J., Boyles J., Bissell D.M. Hepatic lipocytes: the principal collagen-producing cells of normal rat liver. Proc. Nat. Acad. Sci. U.S.A. 1985, 82:8681-8685.
24. Goddard M.J., Tanhehco J.L., Dau P.C. Chronic arsenic poisoning masquerading as Landry-Guillian-Barré syndrome. Electromyogr. Clin. Neurophysiol. 1992, 32:419-423.
25. Guha Mazumdar D.N., Haque R., Ghosh N., De B.K., Santra A., Chakraborty D., et al. Arsenic levels in drinking water and the prevalence of skin lesions in West Bengal, India. Int. J. Epidemiol. 1998, 27:871-877.
26. Guha Mazumder D.N. Effect of chronic intake of arsenic-contaminated water on liver. Toxicol. Appl. Pharmacol. 2005, 206:169-175.
27. Guha Mazumder D.N. Chronic Arsenic toxicity and human health. Indian J. Med. Res. 2008, 128:436-447.
28. Guha Mazumder D.N., Chakraborty A.K., Ghose A., Gupta J.D., Chakraborty D.P., Dey S.B., et al. Chronic arsenic toxicity from drinking tubewell water in rural West Bengal. Bull. World Health Organ. 1988, 66:499-506.
29. Guha Mazumder D.N., Haque R., Ghosh N., De B.K., Santra A., Chakraborty D., et al. Arsenic in drinking water and the prevalence of respiratory effects in West Bengal, India. Int. J. Epidemiol. 2000, 29:1047-1052.
30. Harvey C.F. Poisoned waters traced to source. Nature 2008, 454:415-416.
31. Huet P.M., Guillaime E., Cote J., Légaré A., Lavoie P., Viallet A. Non-cirrhotic perisinusoidal portal hypertension-association with chronic arsenical intoxication. Gastroenterology 1975, 68:1270-1277.
32. IARC Some drinking water disinfectants and contaminants, including arsenic. IARC Monographs 2004, vol 84. IARC, Lyon.
33. Kim Y.M., Talanian R.V., Billiar T.R. Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J. Biol. Chem. 1997, 272:31138-31148.
34. Mandal M., Mandal A., Das S., Chakraborti T., Sajal C. Clinical implications of matrix metalloproteinases. Mol. Cell. Biochem. 2003, 252:305-329.
35. Morris J.S., Schmid M., Newman S., Scheuer P.J., Sherlock S. Arsenic and noncirrhotic portal hypertension. Gastroenterology 1974, 66:86-94.
36. Nakamura T., Torimura T., Sakamoto M., Hashimoto O., Taniguchi E., Inoue K., et al. Significance and therapeutic potential of endothelial progenitor cell transplantation in a cirrhotic liver rat model. Gastroenterology 2007, 133:91-107.
37. National Research Council Arsenic in Drinking Water 1999, National Academy Press, Washington, D.C.
38. Navas-Acien A., Sharrett A.R., Silbergeld E.K., Schwartz B.S., Nachman K.E., Burke T.A., et al. Arsenic exposure and cardiovascular disease: a systematic review of the epidemiologic evidence. Am. J. Epidemiol. 2005, 162:1037-1049.
39. Navas-Aciens A., Silbergeld E.K., Pastor-Barriuso R., Guallar E. Arsenic exposure and prevalence of Type 2 diabetes in US adults. JAMA 2008, 300:814-822.
40. Nevens F., Fevery J., Van Steenbergen W., Sciot R., Desmet V., De Groote J. Arsenic and non-cirrhotic portal hypertension. A report of eight cases. J. Hepatol. 1990, 11:80-85.
41. Nieto N., Friedman S.L., Greenwel P., Cederbaum A.I. CYP2E1 mediated oxidative stress induces collagen type I expression in rat hepatic stellate cells. Hepatology 1999, 30:987-995.
42. Nieto N., Dominguez-Rosales J.A., Fontana L., Salazar A., Armendariz-Borunda J., Greenwel P., et al. Rat hepatic stellate cells contribute to the acute-phase response with increased expression of alpha1(I) and alpha1(IV) collagens, tissue inhibitor of metalloproteinase-1, and matrix-metalloproteinase-2 messenger RNAs. Hepatology 2001, 33:597-607.
43. Nieto N., Friedman S.L., Cederbaum A.I. Stimulation and proliferation of primary rat hepatic stellate cells by cytochrome p450 2e1-derived reactive oxygen species. Hepatology 2002, 35:62-73.
44. Oltvai Z.N., Milliman C.L., Korsmeyer S.J. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 1993, 74:609-619.
45. Peng Z., Peng L., Yunxia F., Zandi E., Shertzer H.G., Xia Y. A critical role of IΚB kinase β in Metallothionein-1 expression and protection against arsenic toxicity. J. Biol. Chem. 2007, 282:21487-21496.
46. Pertoft H., Smedsrød B. Cell Separation 1987, 1-24. Academic Press, New York, Vol. 4. T.G. Pretlow, T.B. Pretlow (Eds.).
47. Rahman M., Tondel M., Ahmad S.A., Axelson O. Diabetes mellitus associated with arsenic exposure in Bangladesh. Am. J. Epidemiol. 1998, 148:198-203.
48. Santra A., DasGupta J., De B.K., Guha Mazumder D.N. Hepatic manifestations in chronic arsenic toxicity. Indian J. Gastroenterol. 1999, 18:152-155.
49. Santra A., Maiti A., Chowdhury A., Guha Mazumder D.N. Oxidative stress in liver of mice exposed to arsenic contaminated water. Indian J. Gastroenterol. 2000, 19:112-115.
50. Santra A., Maiti A., Das S., Lahiri S., Charkaborty S.K., Guha Mazumder D.N. Hepatic damage caused by arsenic (As) toxicity in experimental animals. Clin. Toxicol. 2000, 38:395-405.
51. Santra A., Chowdhury A., Ghatak S., Biswas A., Dhali G.K. Arsenic induces apoptosis in mouse liver is mitochondria dependent and is abrogated by N-acetylcysteine. Toxicol. Appl. Pharmacol. 2007, 220:146-155.
52. Smith A.H., Lingas E.O., Rahman M. Contamination of drinking-water by arsenic in Bangladesh: a public health emergency. Bull. World Health Organ. 2000, 78:1093-1103.
53. Straub A.C., Stolz D.B., Ross M.A., Hernández-Zavala A., Soucy N.V., Klei L.R., et al. Arsenic Stimulates Sinusoidal Endothelial Cell Capillarization and Vessel Remodeling in Mouse Liver. Hepatology 2007, 45:205-212.
54. Straub A.C., Clark K.A., Ross M.A., Chandra A.G., Li S., Gao X., et al. Arsenic-stimulated liver sinusoidal capillarization in mice requires NADPH oxidase-generated superoxide. J. Clin. Invest. 2008, 118:3980-3989.
55. Su G.L. Lipopolysaccharides in liver injury: molecular mechanisms of Kupffer cell activation. Am. J. Physiol. Gastrointest. Liver Physiol. 2002, 283:256-265.
56. Taipale J., Keski-Oja J. Growth factors in the extracellular matrix. FASEB J. 1997, 11:51-59.
57. Uchinami H., Seki E., Brenner D.A., D'Armiento J. Loss of MMP 13 attenuates murine hepatic injury and fibrosis during cholestasis. Hepatology 2006, 44:420-429.
58. World Health Organization Arsenic in Drinking Water. Fact Sheet No. 210 1999, 1-6. WHO Press, Geneva.
59. Yamauchi H., Yamamura Y. Metabolism and excretion of orally administered dimethylarsinic acid in the hamster. Toxicol. Appl. Pharmacol. 1984, 74:134-140.