PARP1-mediated PPARα poly(ADP-ribosyl)ation suppresses fatty acid oxidation in non-alcoholic fatty liver disease

Journal of Hepatology

Volumn 66, Issue 5, 2017, Pages 962-977

  Huang, Kun ^a   Du, Meng ^a   Tan, Xin ^a   Yang, Ling ^a   Li, Xiangrao ^a   Jiang, Yuhan ^a   Wang, Cheng ^a   Zhang, Fengxiao ^a   Zhu, Feng ^a   Cheng, Min ^a   Yang, Qinglin ^b   Yu, Liqing ^c   Wang, Lin ^a   Huang, Dan ^a   Huang, Kai ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

High fat diet; Non alcoholic fatty liver disease; Poly(ADP ribose) polymerase 1; PPAR ; Transcriptional regulation

Indexed keywords

NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; POLY(ADENOSINE DIPHOSPHATE RIBOSE); SIRTUIN 1; FATTY ACID; PARP1 PROTEIN, HUMAN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PPARGC1A PROTEIN, HUMAN; SIRT1 PROTEIN, HUMAN;

ARTICLE; CELL STRESS; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DEACETYLATION; DIET RESTRICTION; DNA BINDING; FATTY ACID OXIDATION; GAIN OF FUNCTION MUTATION; GEL MOBILITY SHIFT ASSAY; GENE INTERACTION; GENE TARGETING; GENETIC MANIPULATION; GENETIC TRANSCRIPTION; GLUCOSE TOLERANCE TEST; HEP-G2 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; INSULIN TOLERANCE TEST; LABORATORY TEST; LIPID DIET; LIPID STORAGE; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; LIVER BIOPSY; LIVER CELL; LIVER CELL CARCINOMA; LOSS OF FUNCTION MUTATION; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY;

ANIMALS; DIET, HIGH-FAT; FATTY ACIDS; HEP G2 CELLS; HEPATOCYTES; HUMANS; MALE; MICE; MICE, INBRED C57BL; NON-ALCOHOLIC FATTY LIVER DISEASE; OXIDATION-REDUCTION; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR GAMMA COACTIVATOR 1-ALPHA; POLY (ADP-RIBOSE) POLYMERASE-1; POLY ADENOSINE DIPHOSPHATE RIBOSE; PPAR ALPHA; SIRTUIN 1;

EID: 85010199505     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2016.11.020     Document Type: Article

References (43)

1. [1] Anstee, Q.M., Day, C.P., The genetics of NAFLD. Nat Rev Gastroenterol Hepatol 10 (2013), 645–655.
2. [2] Loomba, R., Sanyal, A.J., The global NAFLD epidemic. Nat Rev Gastroenterol Hepatol 10 (2013), 686–690.
3. [3] Neuschwander-Tetri, B.A., Hepatic lipotoxicity and the pathogenesis of nonalcoholic steatohepatitis: the central role of nontriglyceride fatty acid metabolites. Hepatology 52 (2010), 774–788.
4. [4] Tilg, H., Moschen, A.R., Evolution of inflammation in nonalcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology 52 (2010), 1836–1846.
5. [5] Boursier, J., Diehl, A.M., Implication of gut microbiota in nonalcoholic fatty liver disease. PLoS Pathog, 11, 2015, e1004559.
6. [6] Fukunishi, S., Sujishi, T., Takeshita, A., Ohama, H., Tsuchimoto, Y., Asai, A., et al. Lipopolysaccharides accelerate hepatic steatosis in the development of nonalcoholic fatty liver disease in Zucker rats. J Clin Biochem Nutr 54 (2014), 39–44.
7. [7] Boutagy, N.E., McMillan, R.P., Frisard, M.I., Hulver, M.W., Metabolic endotoxemia with obesity: Is it real and is it relevant?. Biochimie 124 (2015), 11–20.
8. [8] Kohli, R., Pan, X., Malladi, P., Wainwright, M.S., Whitington, P.F., Mitochondrial reactive oxygen species signal hepatocyte steatosis by regulating the phosphatidylinositol 3-kinase cell survival pathway. J Biol Chem 282 (2007), 21327–21336.
9. [9] Lanaspa, M.A., Sanchez-Lozada, L.G., Choi, Y.J., Cicerchi, C., Kanbay, M., Roncal-Jimenez, C.A., et al. Uric acid induces hepatic steatosis by generation of mitochondrial oxidative stress: potential role in fructose-dependent and -independent fatty liver. J Biol Chem 287 (2012), 40732–40744.
10. [10] Pawlak, M., Lefebvre, P., Staels, B., Molecular mechanism of PPARalpha action and its impact on lipid metabolism, inflammation and fibrosis in non-alcoholic fatty liver disease. J Hepatol 62 (2015), 720–733.
11. [11] Fernandez-Miranda, C., Perez-Carreras, M., Colina, F., Lopez-Alonso, G., Vargas, C., Solis-Herruzo, J.A., A pilot trial of fenofibrate for the treatment of non-alcoholic fatty liver disease. Dig Liver Dis 40 (2008), 200–205.
12. [12] Keating, G.M., Fenofibrate: a review of its lipid-modifying effects in dyslipidemia and its vascular effects in type 2 diabetes mellitus. Am J Cardiovasc Drugs 11 (2011), 227–247.
13. [13] Zambon, A., Cusi, K., The role of fenofibrate in clinical practice. Diab Vasc Dis Res 4 (2007), S15–S20.
14. [14] Bajaj, M., Suraamornkul, S., Hardies, L.J., Glass, L., Musi, N., DeFronzo, R.A., Effects of peroxisome proliferator-activated receptor (PPAR)-alpha and PPAR-gamma agonists on glucose and lipid metabolism in patients with type 2 diabetes mellitus. Diabetologia 50 (2007), 1723–1731.
15. [15] Laurin, J., Lindor, K.D., Crippin, J.S., Gossard, A., Gores, G.J., Ludwig, J., et al. Ursodeoxycholic acid or clofibrate in the treatment of non-alcohol-induced steatohepatitis: a pilot study. Hepatology 23 (1996), 1464–1467.
16. [16] Luo, X., Kraus, W.L., On PAR with PARP: cellular stress signaling through poly(ADP-ribose) and PARP-1. Genes Dev 26 (2012), 417–432.
17. [17] Wang, C., Zhang, F., Wang, L., Zhang, Y., Li, X., Huang, K., et al. Poly(ADP-ribose) polymerase 1 promotes oxidative-stress-induced liver cell death via suppressing farnesoid X receptor alpha. Mol Cell Biol 33 (2013), 4492–4503.
18. [18] Mukhopadhyay, P., Rajesh, M., Cao, Z., Horvath, B., Park, O., Wang, H., et al. Poly (ADP-ribose) polymerase-1 is a key mediator of liver inflammation and fibrosis. Hepatology 59 (2014), 1998–2009.
19. [19] Bai, P., Canto, C., Oudart, H., Brunyanszki, A., Cen, Y., Thomas, C., et al. PARP-1 inhibition increases mitochondrial metabolism through SIRT1 activation. Cell Metab 13 (2011), 461–468.
20. [20] Devalaraja-Narashimha, K., Padanilam, B.J., PARP1 deficiency exacerbates diet-induced obesity in mice. J Endocrinol 205 (2010), 243–252.
21. [21] Erener, S., Mirsaidi, A., Hesse, M., Tiaden, A.N., Ellingsgaard, H., Kostadinova, R., et al. ARTD1 deletion causes increased hepatic lipid accumulation in mice fed a high-fat diet and impairs adipocyte function and differentiation. FASEB J 26 (2012), 2631–2638.
22. [22] Huang, D., Yang, C., Wang, Y., Liao, Y., Huang, K., PARP-1 suppresses adiponectin expression through poly(ADP-ribosyl)ation of PPAR gamma in cardiac fibroblasts. Cardiovasc Res 81 (2009), 98–107.
23. [23] Kersten, S., Peroxisome proliferator activated receptors and lipoprotein metabolism. PPAR Res, 2008, 2008, 132960.
24. [24] Pineda Torra, I., Jamshidi, Y., Flavell, D.M., Fruchart, J.C., Staels, B., Characterization of the human PPARalpha promoter: identification of a functional nuclear receptor response element. Mol Endocrinol 16 (2002), 1013–1028.
25. [25] Purushotham, A., Schug, T.T., Xu, Q., Surapureddi, S., Guo, X., Li, X., Hepatocyte-specific deletion of SIRT1 alters fatty acid metabolism and results in hepatic steatosis and inflammation. Cell Metab 9 (2009), 327–338.
26. [26] Weston, C.J., Shepherd, E.L., Claridge, L.C., Rantakari, P., Curbishley, S.M., Tomlinson, J.W., et al. Vascular adhesion protein-1 promotes liver inflammation and drives hepatic fibrosis. J Clin Invest 125 (2015), 501–520.
27. [27] Kleiner, D.E., Brunt, E.M., Van Natta, M., Behling, C., Contos, M.J., Cummings, O.W., et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41 (2005), 1313–1321.
28. [28] Li, J.Z., Huang, Y., Karaman, R., Ivanova, P.T., Brown, H.A., Roddy, T., et al. Chronic overexpression of PNPLA3I148M in mouse liver causes hepatic steatosis. J Clin Invest 122 (2012), 4130–4144.
29. [29] Rakhshandehroo, M., Hooiveld, G., Muller, M., Kersten, S., Comparative analysis of gene regulation by the transcription factor PPARalpha between mouse and human. PLoS One, 4, 2009, e6796.
30. [30] Nguyen, D., Samson, S.L., Reddy, V.T., Gonzalez, E.V., Sekhar, R.V., Impaired mitochondrial fatty acid oxidation and insulin resistance in aging: novel protective role of glutathione. Aging Cell 12 (2013), 415–425.
31. [31] Wei, Y., Clark, S.E., Thyfault, J.P., Uptergrove, G.M., Li, W., Whaley-Connell, A.T., et al. Oxidative stress-mediated mitochondrial dysfunction contributes to angiotensin II-induced nonalcoholic fatty liver disease in transgenic Ren2 rats. Am J Pathol 174 (2009), 1329–1337.
32. [32] Abdelmegeed, M.A., Yoo, S.H., Henderson, L.E., Gonzalez, F.J., Woodcroft, K.J., Song, B.J., PPARalpha expression protects male mice from high fat-induced nonalcoholic fatty liver. J Nutr 141 (2011), 603–610.
33. [33] Haigis, M.C., Guarente, L.P., Mammalian sirtuins–emerging roles in physiology, aging, and calorie restriction. Genes Dev 20 (2006), 2913–2921.
34. [34] Carmona, M.C., Louche, K., Nibbelink, M., Prunet, B., Bross, A., Desbazeille, M., et al. Fenofibrate prevents Rosiglitazone-induced body weight gain in ob/ob mice. Int J Obes (Lond) 29 (2005), 864–871.
35. [35] Rakhshandehroo, M., Knoch, B., Muller, M., Kersten, S., Peroxisome proliferator-activated receptor alpha target genes. PPAR Res, 2010, 2010, 612089.
36. [36] Reddy, J.K., Azarnoff, D.L., Hignite, C.E., Hypolipidaemic hepatic peroxisome proliferators form a novel class of chemical carcinogens. Nature 283 (1980), 397–398.
37. [37] Morimura, K., Cheung, C., Ward, J.M., Reddy, J.K., Gonzalez, F.J., Differential susceptibility of mice humanized for peroxisome proliferator-activated receptor alpha to Wy-14,643-induced liver tumorigenesis. Carcinogenesis 27 (2006), 1074–1080.
38. [38] Browning, J.D., Horton, J.D., Molecular mediators of hepatic steatosis and liver injury. J Clin Invest 114 (2004), 147–152.
39. [39] Ba, X., Garg, N.J., Signaling mechanism of poly(ADP-ribose) polymerase-1 (PARP-1) in inflammatory diseases. Am J Pathol 178 (2011), 946–955.
40. [40] Seki, E., Schwabe, R.F., Hepatic inflammation and fibrosis: functional links and key pathways. Hepatology 61 (2015), 1066–1079.
41. [41] Pawlak, M., Bauge, E., Bourguet, W., De Bosscher, K., Lalloyer, F., Tailleux, A., et al. The transrepressive activity of peroxisome proliferator-activated receptor alpha is necessary and sufficient to prevent liver fibrosis in mice. Hepatology 60 (2014), 1593–1606.
42. [42] Loyer, X., Paradis, V., Henique, C., Vion, A.C., Colnot, N., Guerin, C.L., et al. Liver microRNA-21 is overexpressed in non-alcoholic steatohepatitis and contributes to the disease in experimental models by inhibiting PPARalpha expression. Gut 65 (2015), 1882–1894.
43. [43] Szalowska, E., Tesfay, H.A., van Hijum, S.A., Kersten, S., Transcriptomic signatures of peroxisome proliferator-activated receptor alpha (PPARalpha) in different mouse liver models identify novel aspects of its biology. BMC Genomics, 15, 2014, 1106.