Susceptibility of L-FABP -/- mice to oxidative stress in early-stage alcoholic liver

Journal of Lipid Research

Volumn 54, Issue 5, 2013, Pages 1335-1345

  Smathers, Rebecca L ^a   Galligan, James J ^a,b   Shearn, Colin T ^a   Fritz, Kristofer S ^a   Mercer, Kelly ^c   Ronis, Martin ^c   Orlicky, David J ^d   Davidson, Nicholas O ^e   Petersen, Dennis R ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VANDERBILT INGRAM CANCER CENTER   (United States)

^d UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alcoholic liver disease; Lipid peroxidation; Liver fatty acid binding protein; Malondialdehyde

Indexed keywords

4 HYDROXYNONENAL; 8 ISOPROSTANE; CARNITINE PALMITOYLTRANSFERASE I; CHOLESTEROL; CYTOCHROME P450 2E1; FATTY ACID BINDING PROTEIN; GLUCOSE; GLUTATHIONE; INSULIN; LIPID; MALONALDEHYDE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; REACTIVE OXYGEN METABOLITE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; TRIACYLGLYCEROL;

ALCOHOL BLOOD LEVEL; ALCOHOL CONSUMPTION; ALCOHOL LIVER CIRRHOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL LIVER LEVEL; CONTROLLED STUDY; DISEASE PREDISPOSITION; FATTY ACID OXIDATION; FATTY ACID SYNTHESIS; FOOD INTAKE; GLUCOSE BLOOD LEVEL; INSULIN BLOOD LEVEL; INTRACELLULAR SIGNALING; LIPID LIVER LEVEL; LIPID PEROXIDATION; MALE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRIACYLGLYCEROL BLOOD LEVEL; WEIGHT REDUCTION;

EID: 84876792281     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M034892     Document Type: Article

References (53)

1. Lucey, M. R., P. Mathurin, and T. R. Morgan. 2009. Alcoholic hepatitis. N. Engl. J. Med. 360 : 2758-2769.
2. Beier, J. I., G. E. Arteel, and C. J. McClain. 2011. Advances in alcoholic liver disease. Curr. Gastroenterol. Rep. 13 : 56-64.
3. Sozio, M., and D. W. Crabb. 2008. Alcohol and lipid metab olism. Am. J. Physiol. Endocrinol. Metab. 295 : E10-E16.
4. Zakhari, S., and T. K. Li. 2007. Determinants of alcohol use and abuse: Impact of quantity and frequency patterns on liver disease. Hepatology. 46 : 2032-2039.
5. Nagy, L. E. 2004. Molecular aspects of alcohol metabolism: Transcription factors involved in early ethanol-induced liver injury. Annu. Rev. Nutr. 24 : 55-78.
6. Clugston, R. D., H. Jiang, M. X. Lee, R. Piantedosi, J. J. Yuen, R. Ramakrishnan, M. J. Lewis, M. E. Gottesman, L. S. Huang, I. J. Goldberg, et al. 2011. Altered hepatic lipid metabolism in C57BL/6 mice fed alcohol: A targeted lipidomic and gene expression study. J. Lipid Res. 52 : 2021-2031.
7. Smathers, R. L., K. S. Fritz, J. J. Galligan, C. T. Shearn, P. Reigan, M. J. Marks, and D. R. Petersen. 2012. Characterization of 4-HNE Modified L-FABP reveals alterations in structural and functional dynamics. PLoS ONE. 7 : E38459.
8. Smathers, R. L., J. J. Galligan, B. J. Stewart, and D. R. Petersen. 2011. Overview of lipid peroxidation products and hepatic protein modification in alcoholic liver disease. Chem. Biol. Interact. 192 : 107-112.
9. McIntosh, A. L., H. Huang, B. P. Atshaves, E. Wellberg, D. V. Kuklev, W. L. Smith, A. B. Kier, and F. Schroeder. 2010. Fluorescent n-3 and n-6 very long chain polyunsaturated fatty acids: Three-photon imaging in living cells expressing liver fatty acid-binding protein. J. Biol. Chem. 285 : 18693-18708.
10. Newberry, E. P., Y. Xie, S. Kennedy, X. Han, K. K. Buhman, J. Luo, R. W. Gross, and N. O. Davidson. 2003. Decreased hepatic triglyceride accumulation and altered fatty acid uptake in mice with deletion of the liver fatty acid-binding protein gene. J. Biol. Chem. 278 : 51664-51672.
11. Fritz, K. S., J. J. Galligan, M. D. Hirschey, E. Verdin, and D. R. Petersen. 2012. Mitochondrial acetylome analysis in a mouse model of alcohol-induced liver injury utilizing SIRT3 knockout mice. J. Proteome Res. 11 : 1633-1643.
12. Galligan, J. J., R. L. Smathers, C. T. Shearn, K. S. Fritz, D. S. Backos, H. Jiang, C. C. Franklin, D. J. Orlicky, K. N. Maclean, and D. R. Petersen. 2012. Oxidative stress and the ER stress response in a murine model for early-stage alcoholic liver disease. J. Toxicol. 2012 : 207594.
13. Roede, J. R., D. J. Orlicky, A. B. Fisher, and D. R. Petersen. 2009. Overexpression of peroxiredoxin 6 does not prevent ethanolmediated oxidative stress and may play a role in hepatic lipid accumulation. J. Pharmacol. Exp. Ther. 330 : 79-88.
14. Hartley, D. P., and D. R. Petersen. 1997. Co-metabolism of ethanol, ethanol-derived acetaldehyde, and 4-hydroxynonenal in isolated rat hepatocytes. Alcohol. Clin. Exp. Res. 21 : 298-304.
15. Hartley, D. P., K. L. Kolaja, J. Reichard, and D. R. Petersen. 1999. 4-Hydroxynonenal and malondialdehyde hepatic protein adducts in rats treated with carbon tetrachloride: Immunochemical detection and lobular localization. Toxicol. Appl. Pharmacol. 161 : 23-33.
16. Rinaldi, R., Y. Aniya, R. Svensson, E. Eliasson, S. Swedmark, M. Shimoji, and R. Morgenstern. 2004. NADPH dependent activation of microsomal glutathione transferase 1. Chem. Biol. Interact. 147 : 163-172.
17. Wu, X., Y. Tong, K. Shankar, J. N. Baumgardner, J. Kang, J. Badeaux, T. M. Badger, and M. J. Ronis. 2011. Lipid fatty acid profile analyses in liver and serum in rats with nonalcoholic steatohepatitis using improved gas chromatography-mass spectrometry methodology. J. Agric. Food Chem. 59 : 747-754.
18. Eder, K. 1995. Gas chromatographic analysis of fatty acid methyl esters. J. Chromatogr. B Biomed. Appl. 671 : 113-131.
19. Lambert, A. J., M. Portero-Otin, R. Pamplona, and B. J. Merry. 2004. Effect of ageing and caloric restriction on specific markers of protein oxidative damage and membrane peroxidizability in rat liver mitochondria. Mech. Ageing Dev. 125 : 529-538.
20. Galligan, J. J., R. L. Smathers, K. S. Fritz, L. E. Epperson, L. E. Hunter, and D. R. Petersen. 2012. Protein carbonylation in a murine model for early alcoholic liver disease. Chem. Res. Toxicol. 25 : 1012-1021.
21. Hostetler, H. A., A. L. McIntosh, B. P. Atshaves, S. M. Storey, H. R. Payne, A. B. Kier, and F. Schroeder. 2009. L-FABP directly interacts with PPARalpha in cultured primary hepatocytes. J. Lipid Res. 50 : 1663-1675.
22. McIntosh, A. L., B. P. Atshaves, H. A. Hostetler, H. Huang, J. Davis, O. I. Lyuksyutova, D. Landrock, A. B. Kier, and F. Schroeder. 2009. Liver type fatty acid binding protein (L-FABP) gene ablation reduces nuclear ligand distribution and peroxisome proliferator-activated receptor-alpha activity in cultured primary hepatocytes. Arch. Biochem. Biophys. 485 : 160-173.
23. Newberry, E. P., Y. Xie, S. M. Kennedy, J. Luo, and N. O. Davidson. 2006. Protection against Western diet-induced obesity and hepatic steatosis in liver fatty acid-binding protein knockout mice. Hepatology. 44 : 1191-1205.
24. Al Qatari, M., M. F. Shih, and P. V. Taberner. 1996. Chronic ethanol consumption ameliorates the maturity-onset diabetes-obesity syndrome in CBA mice. Alcohol Alcohol. 31 : 89-99.
25. Poli, G. 2000. Pathogenesis of liver fibrosis: Role of oxidative stress. Mol. Aspects Med. 21 : 49-98.
26. Sampey, B. P., S. Korourian, M. J. Ronis, T. M. Badger, and D. R. Petersen. 2003. Immunohistochemical characterization of hepatic malondialdehyde and 4-hydroxynonenal modified proteins during early stages of ethanol-induced liver injury. Alcohol. Clin. Exp. Res. 27 : 1015-1022.
27. Shaw, S., K. P. Rubin, and C. S. Lieber. 1983. Depressed hepatic glutathione and increased diene conjugates in alcoholic liver disease. Evidence of lipid peroxidation. Dig. Dis. Sci. 28 : 585-589.
28. Wu, D., and A. I. Cederbaum. 2003. Alcohol, oxidative stress, and free radical damage. Alcohol Res. Health. 27 : 277-284.
29. Hayes, J. D., and L. I. McLellan. 1999. Glutathione and glutathionedependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Radic. Res. 31 : 273-300.
30. Fritz, K. S., and D. R. Petersen. 2011. Exploring the biology of lipid peroxidation-derived protein carbonylation. Chem. Res. Toxicol. 24 : 1411-1419.
31. Martin, G. G., H. Huang, B. P. Atshaves, B. Binas, and F. Schroeder. 2003. Ablation of the liver fatty acid binding protein gene decreases fatty acyl CoA binding capacity and alters fatty acyl CoA pool distribution in mouse liver. Biochemistry. 42 : 11520-11532.
32. Alaynick, W. A. 2008. Nuclear receptors, mitochondria and lipid metabolism. Mitochondrion. 8 : 329-337.
33. Sugden, M. C., P. W. Caton, and M. J. Holness. 2010. PPAR control: It's SIRTainly as easy as PGC. J. Endocrinol. 204 : 93-104.
34. Reddy, J. K., and M. S. Rao. 2006. Lipid metabolism and liver inflammation. II. Fatty liver disease and fatty acid oxidation. Am. J. Physiol. Gastrointest. Liver Physiol. 290 : G852-G858.
35. Crabb, D. W. 2004. Alcohol deranges hepatic lipid metabolism via altered transcriptional regulation. Trans. Am. Clin. Climatol. Assoc. 115 : 273-287.
36. Schroeder, F., A. D. Petrescu, H. Huang, B. P. Atshaves, A. L. McIntosh, G. G. Martin, H. A. Hostetler, A. Vespa, D. Landrock, K. K. Landrock, et al. 2008. Role of fatty acid binding proteins and long chain fatty acids in modulating nuclear receptors and gene transcription. Lipids. 43 : 1-17.
37. Feldstein, A. E., and S. M. Bailey. 2011. Emerging role of redox dysregulation in alcoholic and nonalcoholic fatty liver disease. Antioxid. Redox Signal. 15 : 421-424.
38. Grattagliano, I., S. Russmann, C. Diogo, L. Bonfrate, P. J. Oliveira, D. Q. Wang, and P. Portincasa. 2011. Mitochondria in chronic liver disease. Curr. Drug Targets. 12 : 879-893.
39. Hirschey, M. D., and E. Verdin. 2010. Measuring fatty acid oxidation in tissue homogenates. In Protocol Exchange. Nature Publishing Group, London, UK. 1-10.
40. Arteel, G. E. 2010. Animal models of alcoholic liver disease. Dig. Dis. 28 : 729-736.
41. Ramaiah, S., C. Rivera, and G. Arteel. 2004. Early-phase alcoholic liver disease: An update on animal models, pathology, and pathogenesis. Int. J. Toxicol. 23 : 217-231.
42. Ronis, M. J., A. Butura, S. Korourian, K. Shankar, P. Simpson, J. Badeaux, E. Albano, M. Ingelman-Sundberg, and T. M. Badger. 2008. Cytokine and chemokine expression associated with steatohepatitis and hepatocyte proliferation in rats fed ethanol via total enteral nutrition. Exp. Biol. Med. (Maywood). 233 : 344-355.
43. Newberry, E. P., S. M. Kennedy, Y. Xie, B. T. Sternard, J. Luo, and N. O. Davidson. 2008. Diet-induced obesity and hepatic steatosis in L-Fabp α /α mice is abrogated with SF, but not PUFA, feeding and attenuated after cholesterol supplementation. Am. J. Physiol. Gastrointest. Liver Physiol. 294 : G307-G314.
44. De Minicis, S., and D. A. Brenner. 2008. Oxidative stress in alcoholic liver disease: Role of NADPH oxidase complex. J. Gastroenterol. Hepatol. 23 (Suppl. 1) : S98-S103.
45. Ronis, M. J., L. Hennings, B. Stewart, A. G. Basnakian, E. O. Apostolov, E. Albano, T. M. Badger, and D. R. Petersen. 2011. Effects of long-term ethanol administration in a rat total enteral nutrition model of alcoholic liver disease. Am. J. Physiol. Gastrointest. Liver Physiol. 300 : G109-G119.
46. Zhong, W., Y. Zhao, Y. Tang, X. Wei, X. Shi, W. Sun, X. Sun, X. Yin, S. Kim, C. J. McClain, et al. 2012. Chronic alcohol exposure stimulates adipose tissue lipolysis in mice: Role of reverse triglyceride transport in the pathogenesis of alcoholic steatosis. Am. J. Pathol. 180 : 998-1007.
47. Berger, J., and D. E. Moller. 2002. The mechanisms of action of PPARs. Annu. Rev. Med. 53 : 409-435.
48. Ronis, M. J., J. N. Baumgardner, J. C. Marecki, L. Hennings, X. Wu, K. Shankar, M. A. Cleves, H. Gomez-Acevedo, and T. M. Badger. 2012. Dietary fat source alters hepatic gene expression profile and determines the type of liver pathology in rats overfed via total enteral nutrition. Physiol. Genomics. 44 : 1073-1089.
49. Wu, D., and A. I. Cederbaum. 2009. Oxidative stress and alcoholic liver disease. Semin. Liver Dis. 29 : 141-154.
50. Hellberg, K., P. A. Grimsrud, A. C. Kruse, L. J. Banaszak, D. H. Ohlendorf, and D. A. Bernlohr. 2010. X-ray crystallographic analysis of adipocyte fatty acid binding protein (aP2) modified with 4-hydroxy-2-nonenal. Protein Sci. 19 : 1480-1489.
51. Wang, G., Y. Gong, J. Anderson, D. Sun, G. Minuk, M. S. Roberts, and F. J. Burczynski. 2005. Antioxidative function of L-FABP in L-FABP stably transfected Chang liver cells. Hepatology. 42 : 871-879.
52. Yan, J., Y. Gong, Y. M. She, G. Wang, M. S. Roberts, and F. J. Burczynski. 2009. Molecular mechanism of recombinant liver fatty acid binding protein's antioxidant activity. J. Lipid Res. 50 : 2445-2454.
53. Bennaars-Eiden, A., L. Higgins, A. V. Hertzel, R. J. Kapphahn, D. A. Ferrington, and D. A. Bernlohr. 2002. Covalent modification of epithelial fatty acid-binding protein by 4-hydroxynonenal in vitro and in vivo. Evidence for a role in antioxidant biology. J. Biol. Chem. 277 : 50693-50702.