Ethanol metabolism and oxidative stress are required for unfolded protein response activation and steatosis in zebrafish with alcoholic liver disease

DMM Disease Models and Mechanisms

Volumn 6, Issue 5, 2013, Pages 1213-1226

  Tsedensodnom, Orkhontuya ^a   Vacaru, Ana M ^a   Howarth, Deanna L ^a   Yin, Chunyue ^b   Sadler, Kirsten C ^a,c  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; ALCOHOL DEHYDROGENASE; ALCOHOL DEHYDROGENASE 1; CYTOCHROME P450 2E1; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ALCOHOL LIVER DISEASE; ALCOHOL METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; LARVA; LIVER; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; STEATOSIS; UNFOLDED PROTEIN RESPONSE; ZEBRA FISH;

ALCOHOL DEHYDROGENASE; ANIMALS; ANTIOXIDANTS; CYTOCHROME P-450 CYP2E1; ENDOPLASMIC RETICULUM STRESS; ETHANOL; FATTY LIVER; HEPATIC STELLATE CELLS; LARVA; LIVER; LIVER DISEASES, ALCOHOLIC; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SECRETORY PATHWAY; SURVIVAL ANALYSIS; UNFOLDED PROTEIN RESPONSE; ZEBRAFISH;

EID: 84883890350     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.012195     Document Type: Article

References (54)

1. Baraona, E. and Lieber, C. S. (1982). Effects of alcohol on hepatic transport of proteins. Annu. Rev. Med. 33, 281-292.
2. Beier, J. I., Arteel, G. E. and McClain, C. J. (2011). Advances in alcoholic liver disease. Curr. Gastroenterol. Rep. 13, 56-64.
3. Caro, A. A. and Cederbaum, A. I. (2004). Oxidative stress, toxicology, and pharmacology of CYP2E1. Annu. Rev. Pharmacol. Toxicol. 44, 27-42.
4. Carten, J. D., Bradford, M. K. and Farber, S. A. (2011). Visualizing digestive organ morphology and function using differential fatty acid metabolism in live zebrafish. Dev. Biol. 360, 276-285.
5. Chu, J. and Sadler, K. C. (2009). New school in liver development: lessons from zebrafish. Hepatology 50, 1656-1663.
6. Cinaroglu, A., Gao, C., Imrie, D. and Sadler, K. C. (2011). Activating transcription factor 6 plays protective and pathological roles in steatosis due to endoplasmic reticulum stress in zebrafish. Hepatology 54, 495-508.
7. Csordás, G., Renken, C., Várnai, P., Walter, L., Weaver, D., Buttle, K. F., Balla, T., Mannella, C. A. and Hajnóczky, G. (2006). Structural and functional features and significance of the physical linkage between ER and mitochondria. J. Cell Biol. 174, 915-921.
8. Dasmahapatra, A. K., Doucet, H. L., Bhattacharyya, C. and Carvan, M. J., 3rd (2001). Developmental expression of alcohol dehydrogenase (ADH3) in zebrafish (Danio rerio). Biochem. Biophys. Res. Commun. 286, 1082-1086.
9. Di Giulio, R. T. and Hinton, D. E. (2008). The Toxicology of Fishes. Boca Raton, FL: CRC Press.
10. Donohue, T. M., Osna, N. A. and Clemens, D. L. (2006). Recombinant Hep G2 cells that express alcohol dehydrogenase and cytochrome P450 2E1 as a model of ethanol-elicited cytotoxicity. Int. J. Biochem. Cell Biol. 38, 92-101.
11. Field, H. A., Ober, E. A., Roeser, T. and Stainier, D. Y. (2003). Formation of the digestive system in zebrafish. I. Liver morphogenesis. Dev. Biol. 253, 279-290.
12. Goldstone, J. V., McArthur, A. G., Kubota, A., Zanette, J., Parente, T., Jönsson, M. E., Nelson, D. R. and Stegeman, J. J. (2010). Identification and developmental expression of the full complement of Cytochrome P450 genes in Zebrafish. BMC Genomics 11, 643.
13. Henkel, A. S., Elias, M. S. and Green, R. M. (2009). Homocysteine supplementation attenuates the unfolded protein response in a murine nutritional model of steatohepatitis. J. Biol. Chem. 284, 31807-31816.
14. Howarth, D. L., Passeri, M. and Sadler, K. C. (2011). Drinks like a fish: using zebrafish to understand alcoholic liver disease. Alcohol. Clin. Exp. Res. 35, 826-829.
15. Howarth, D. L., Vacaru, A. M., Tsedensodnom, O., Mormone, E., Nieto, N., Costantini, L. M., Snapp, E. L. and Sadler, K. C. (2012). Alcohol disrupts endoplasmic reticulum function and protein secretion in hepatocytes. Alcohol. Clin. Exp. Res. 36, 14-23.
16. Howarth, D. L., Yin, C., Yeh, K. and Sadler, K. C. (2013). Defining hepatic dysfunction parameters in two models of Fatty liver disease in zebrafish larvae. Zebrafish 10, 199-210.
17. Howe, K., Clark, M. D., Torroja, C. F., Torrance, J., Berthelot, C., Muffato, M., Collins, J. E., Humphray, S., McLaren, K., Matthews, L. et al. (2013). The zebrafish reference genome sequence and its relationship to the human genome. Nature 496, 498-503.
18. Hu, M., Wang, F., Li, X., Rogers, C. Q., Liang, X., Finck, B. N., Mitra, M. S., Zhang, R., Mitchell, D. A. and You, M. (2012). Regulation of hepatic lipin-1 by ethanol: role of AMP-activated protein kinase/sterol regulatory element-binding protein 1 signaling in mice. Hepatology 55, 437-446.
19. Imrie, D. and Sadler, K. C. (2012). Stress management: How the unfolded protein response impacts fatty liver disease. J. Hepatol. 57, 1147-1151.
20. Jang, Z. H., Chung, H. C., Ahn, Y. G., Kwon, Y. K., Kim, J. S., Ryu, J. H., Ryu, H., Kim, C. H. and Hwang, G. S. (2012). Metabolic profiling of an alcoholic fatty liver in zebrafish (Danio rerio). Mol. Biosyst. 8, 2001-2009.
21. Ji, C. (2012). Mechanisms of alcohol-induced endoplasmic reticulum stress and organ injuries. Biochem. Res. Int. 2012, 216450.
22. Ji, C. and Kaplowitz, N. (2003). Betaine decreases hyperhomocysteinemia, endoplasmic reticulum stress, and liver injury in alcohol-fed mice. Gastroenterology 124, 1488-1499.
23. Kaplan, L. A., Schultz, M. E., Schultz, R. J. and Crivello, J. F. (1991). Nitrosodiethylamine metabolism in the viviparous fish Poeciliopsis: evidence for the existence of liver P450pj activity and expression. Carcinogenesis 12, 647-652.
24. Kaplan, L. A., Fielding, E. and Crivello, J. F. (2001). The genetic regulation of liver microsomal CYP2E1 activity among strains of the viviparous fish Poeciliopsis. Comp Biochem Physiol 128, 143-152.
25. Korzh, S., Pan, X., Garcia-Lecea, M., Winata, C. L., Pan, X., Wohland, T., Korzh, V. and Gong, Z. (2008). Requirement of vasculogenesis and blood circulation in late stages of liver growth in zebrafish. BMC Dev. Biol. 8, 84.
26. Lee, J. S., Zheng, Z., Mendez, R., Ha, S. W., Xie, Y. and Zhang, K. (2012). Pharmacologic ER stress induces non-alcoholic steatohepatitis in an animal model. Toxicol. Lett. 211, 29-38.
27. Lieber, C. S. (1997). Cytochrome P-4502E1: its physiological and pathological role. Physiol. Rev. 77, 517-544.
28. Lu, Y. and Cederbaum, A. I. (2006). Enhancement by pyrazole of lipopolysaccharideinduced liver injury in mice: role of cytochrome P450 2E1 and 2A5. Hepatology 44, 263-274.
29. Malhi, H. and Kaufman, R. J. (2011). Endoplasmic reticulum stress in liver disease. J. Hepatol. 54, 795-809.
30. Malhotra, J. D. and Kaufman, R. J. (2007). Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid. Redox Signal. 9, 2277-2293.
31. Malhotra, J. D., Miao, H., Zhang, K., Wolfson, A., Pennathur, S., Pipe, S. W. and Kaufman, R. J. (2008). Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proc. Natl. Acad. Sci. USA 105, 18525-18530.
32. Mantena, S. K., King, A. L., Andringa, K. K., Eccleston, H. B. and Bailey, S. M. (2008). Mitochondrial dysfunction and oxidative stress in the pathogenesis of alcohol-and obesity-induced fatty liver diseases. Free Radic. Biol. Med. 44, 1259-1272.
33. Nebert, D. W., Nelson, D. R. and Feyereisen, R. (1989). Evolution of the cytochrome P450 genes. Xenobiotica 19, 1149-1160.
34. Nelson, D. R. (1999). Cytochrome P450 and the individuality of species. Arch. Biochem. Biophys. 369, 1-10.
35. Passeri, M. J., Cinaroglu, A., Gao, C. and Sadler, K. C. (2009). Hepatic steatosis in response to acute alcohol exposure in zebrafish requires sterol regulatory element binding protein activation. Hepatology 49, 443-452.
36. Paula, H., Asrani, S. K., Boetticher, N. C., Pedersen, R., Shah, V. H. and Kim, W. R. (2010). Alcoholic liver disease-related mortality in the United States: 1980-2003. Am. J. Gastroenterol. 105, 1782-1787.
37. Puri, P., Mirshahi, F., Cheung, O., Natarajan, R., Maher, J. W., Kellum, J. M. and Sanyal, A. J. (2008). Activation and dysregulation of the unfolded protein response in nonalcoholic fatty liver disease. Gastroenterology 134, 568-576.
38. Reimers, M. J., Hahn, M. E. and Tanguay, R. L. (2004). Two zebrafish alcohol dehydrogenases share common ancestry with mammalian class I, II, IV, and V alcohol dehydrogenase genes but have distinct functional characteristics. J. Biol. Chem. 279, 38303-38312.
39. Rinella, M. E., Siddiqui, M. S., Gardikiotes, K., Gottstein, J., Elias, M. and Green, R. M. (2011). Dysregulation of the unfolded protein response in db/db mice with dietinduced steatohepatitis. Hepatology 54, 1600-1609.
40. Rubin, E. and Lieber, C. S. (1968). Alcohol-induced hepatic injury in nonalcoholic volunteers. N. Engl. J. Med. 278, 869-876.
41. Rutkowski, D. T. and Kaufman, R. J. (2007). That which does not kill me makes me stronger: adapting to chronic ER stress. Trends Biochem. Sci. 32, 469-476.
42. Rutkowski, D. T., Wu, J., Back, S. H., Callaghan, M. U., Ferris, S. P., Iqbal, J., Clark, R., Miao, H., Hassler, J. R., Fornek, J. et al. (2008). UPR pathways combine to prevent hepatic steatosis caused by ER stress-mediated suppression of transcriptional master regulators. Dev. Cell 15, 829-840.
43. Simi, A. and Ingelman-Sundberg, M. (1999). Post-translational inhibition of cytochrome P-450 2E1 expression by chlomethiazole in Fao hepatoma cells. J. Pharmacol. Exp. Ther. 289, 847-852.
44. Teske, B. F., Wek, S. A., Bunpo, P., Cundiff, J. K., McClintick, J. N., Anthony, T. G. and Wek, R. C. (2011). The eIF2 kinase PERK and the integrated stress response facilitate activation of ATF6 during endoplasmic reticulum stress. Mol. Biol. Cell 22, 4390-4405.
45. Thakur, P. C., Stuckenholz, C., Rivera, M. R., Davison, J. M., Yao, J. K., Amsterdam, A., Sadler, K. C. and Bahary, N. (2011). Lack of de novo phosphatidylinositol synthesis leads to endoplasmic reticulum stress and hepatic steatosis in cdiptdeficient zebrafish. Hepatology 54, 452-462.
46. Wall, K. L. and Crivello, J. (1998). Chlorzoxazone metabolism by winter flounder liver microsomes: evidence for existence of a CYP2E1-like isoform in teleosts. Toxicol. Appl. Pharmacol. 151, 98-104.
47. Walter, P. and Ron, D. (2011). The unfolded protein response: from stress pathway to homeostatic regulation. Science 334, 1081-1086.
48. Wu, D. and Cederbaum, A. I. (2009). Oxidative stress and alcoholic liver disease. Semin. Liver Dis. 29, 141-154.
49. Wu, D. F., Clejan, L., Potter, B. and Cederbaum, A. I. (1990). Rapid decrease of cytochrome P-450IIE1 in primary hepatocyte culture and its maintenance by added 4-methylpyrazole. Hepatology 12, 1379-1389.
50. Xie, J., Farage, E., Sugimoto, M. and Anand-Apte, B. (2010). A novel transgenic zebrafish model for blood-brain and blood-retinal barrier development. BMC Dev. Biol. 10, 76.
51. Yin, C., Kikuchi, K., Hochgreb, T., Poss, K. D. and Stainier, D. Y. (2010). Hand2 regulates extracellular matrix remodeling essential for gut-looping morphogenesis in zebrafish. Dev. Cell 18, 973-984.
52. Yin, C., Evason, K. J., Maher, J. J. and Stainier, D. Y. (2012). The basic helix-loop-helix transcription factor, heart and neural crest derivatives expressed transcript 2, marks hepatic stellate cells in zebrafish: analysis of stellate cell entry into the developing liver. Hepatology 56, 1958-1970.
53. You, M., Fischer, M., Deeg, M. A. and Crabb, D. W. (2002). Ethanol induces fatty acid synthesis pathways by activation of sterol regulatory element-binding protein (SREBP). J. Biol. Chem. 277, 29342-29347.
54. Zhang, K., Wang, S., Malhotra, J., Hassler, J. R., Back, S. H., Wang, G., Chang, L., Xu, W., Miao, H., Leonardi, R. et al. (2011). The unfolded protein response transducer IRE1α prevents ER stress-induced hepatic steatosis. EMBO J. 30, 1357-1375.