ACSL3 and GSK-3β are essential for lipid upregulation induced by endoplasmic reticulum stress in liver cells

Journal of Cellular Biochemistry

Volumn 112, Issue 3, 2011, Pages 881-893

  Chang, Yung Sheng ^a   Tsai, Chien Ting ^a   Huangfu, Chien An ^a   Huang, Wen Ya ^a   Lei, Huan Yao ^a   Lin, Chiou Feng ^a   Su, Ih Jen ^b   Chang, Wen Tsan ^a   Wu, Pei Huan ^a   Chen, Ya Ting ^a   Hung, Jui Hsiang ^c   Young, Kung Chia ^a,d   Lai, Ming Derg ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^c CHIA NAN UNIVERSITY OF PHARMACY AND SCIENCE   (Taiwan)

^d NONE   (Taiwan)

Author keywords

ACSL3; Endoplasmic reticulum stress; GSK 3beta; Lipid dysregulation

Indexed keywords

ACYL COA SYNTHETASE 3; GLYCOGEN SYNTHASE KINASE 3BETA; LIGASE INHIBITOR; LONG CHAIN FATTY ACID COENZYME A LIGASE; SHORT HAIRPIN RNA; TRIACSIN C; TUNICAMYCIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME REGULATION; LIPID METABOLISM; LIPID STORAGE; LIPOGENESIS; LIVER CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

ANIMALS; CELL LINE, TUMOR; COENZYME A LIGASES; ENDOPLASMIC RETICULUM; ENZYME INHIBITORS; GLYCOGEN SYNTHASE KINASE 3; HEAT-SHOCK PROTEINS; HEPATOCYTES; HUMANS; LIPIDS; LIVER; MICE; MICE, INBRED C57BL; RNA INTERFERENCE; STRESS, PHYSIOLOGICAL; TRIAZENES; TUNICAMYCIN; UP-REGULATION;

HEPATITIS B VIRUS; MUS;

EID: 79951785549     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22996     Document Type: Article

References (46)

1. Baltzis D, Pluquet O, Papadakis AI, Kazemi S, Qu LK, Koromilas AE. 2007. The eIF2alpha kinases PERK and PKR activate glycogen synthase kinase 3 to promote the proteasomal degradation of p53. J Biol Chem 282:31675-31687. (Pubitemid 350044850)
2. Beurel E, Jope RS. 2008. Differential regulation of STAT family members by glycogen synthase kinase-3. J Biol Chem 283:21934-21944.
3. Bu SY, Mashek MT, Mashek DG. 2009. Suppression of long chain acyl-CoA synthetase 3 decreases hepatic de novo fatty acid synthesis through decreased transcriptional activity. J Biol Chem 284:30474-30483.
4. Coleman RA, Lewin TM, Muoio DM. 2000. Physiological and nutritional regulation of enzymes of triacylglycerol synthesis. Annu Rev Nutr 20:77-103.
5. Fiorentino L, Vivanti A, Cavalera M, Marzano V, Ronci M, Fabrizi M, Menini S, Pugliese G, Menghini R, Khokha R, Lauro R, Urbani A, Federici M. 2010. Increased tumor necrosis factor alpha-converting enzyme activity induces insulin resistance and hepatosteatosis in mice. Hepatology 51:103-110.
6. Fujimoto Y, Itabe H, Sakai J, Makita M, Noda J, Mori M, Higashi Y, Kojima S, Takano T. 2004. Identification of major proteins in the lipid droplet-enriched fraction isolated from the human hepatocyte cell line HuH7. Biochim Biophys Acta 1644:47-59. (Pubitemid 38117041)
7. Fujimoto Y, Itabe H, Kinoshita T, Homma KJ, Onoduka J, Mori M, Yamaguchi S, Makita M, Higashi Y, Yamashita A, Takano T. 2007. Involvement of ACSL in local synthesis of neutral lipids in cytoplasmic lipid droplets in human hepatocyte HuH7. J Lipid Res 48:1280-1292. (Pubitemid 47312030)
8. Gaspar ML, Jesch SA, Viswanatha R, Antosh AL, Brown WJ, Kohlwein SD, Henry SA. 2008. A block in ER-to-golgi trafficking inhibits phospholipid synthesis and induces neutral lipid accumulation. J Biol Chem 283:25735-25751.
9. Goodman JM. 2008. The gregarious lipid droplet. J Biol Chem 283:28005-28009.
10. Götschel F, Kern C, Lang S, Sparna T, Markmann C, Schwager J, McNelly S, von Weizsäcker F, Laufer S, Hecht A, Merfort I. 2008. Inhibition of GSK3 differentially modulates NF-kappaB, CREB, AP-1 and beta-catenin signaling in hepatocytes, but fails to promote TNF-alpha-induced apoptosis. Exp Cell Res 314:1351-1366.
11. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D. 2000. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6:1099-1108.
12. Hertz R, Magenheim J, Berman I, Bar-Tana J. 1998. Fatty acyl-CoA thioesters are ligands of hepatic nuclear factor-4alpha. Nature 392:512-516. (Pubitemid 28168984)
13. Hsu IR, Kim SP, Kabir M, Bergman RN. 2007. Metabolic syndrome, hyperinsulinemia, and cancer. Am J Clin Nutr 86:s867-s871.
14. Hu P, Han Z, Couvillon AD, Kaufman RJ, Exton JH. 2006. Autocrine tumor necrosis factor alpha links endoplasmic reticulum stress to the membrane death receptor pathway through IRE1alpha-mediated NF-kappaB activation and down-regulation of TRAF2 expression. Mol Cell Biol 26:3071-3084.
15. Huang WC, Lin YS, Chen CL, Wang CY, Chiu WH, Lin CF. 2009. Glycogen synthase kinase-3beta mediates endoplasmic reticulum stress-induced lysosomal apoptosis in leukemia. J Pharmacol Exp Ther 329:524-531.
16. Hung JH, Su IJ, Lei HY, Wang HC, Lin WC, Chang WT, Huang W, Chang WC, Chang YS, Chen CC, Lai MD. 2004. Endoplasmic reticulum stress stimulates the expression of cyclooxygenase-2 through activation of NF-kappaB and pp38 mitogen-activated protein kinase. J Biol Chem 279:46384-46392. (Pubitemid 39518279)
17. Jiang HY, Wek SA, McGrath BC, Scheuner D, Kaufman RJ, Cavener DR, Wek RC. 2003. Phosphorylation of the alpha subunit of eukaryotic initiation factor 2 is required for activation of NF-kappaB in response to diverse cellular stresses. Mol Cell Biol 23:5651-5663. (Pubitemid 36951330)
18. Kang H, Lee SK, Kim MH, Choi H, Lee SH, Kwack K. 2009. Acyl-CoA synthetase long-chain family member 6 is associated with premature ovarian failure. Fertil Steril 91:1339-1343.
19. Kotliarova S, Pastorino S, Kovell LC, Kotliarov Y, Song H, Zhang W, Bailey R, Maric D, Zenklusen JC, Lee J, Fine HA. 2008. Glycogen synthase kinase-3 inhibition induces glioma cell death through c-MYC, nuclear factor-kappaB, and glucose regulation. Cancer Res 68:6643-6651.
20. Lee AH, Scapa EF, Cohen DE, Glimcher LH. 2008. Regulation of hepatic lipogenesis by the transcription factor XBP1. Science 320:1492-1496. (Pubitemid 351929428)
21. Lewin TM, Kim JH, Granger DA, Vance JE, Coleman RA. 2001. Acyl-CoA synthetase isoforms 1, 4, and 5 are present in different subcellular membranes in rat liver and can be inhibited independently. J Biol Chem 276:24674-24679.
22. Li LO, Mashek DG, An J, Doughman SD, Newgard CB, Coleman RA. 2006. Overexpression of rat long chain acyl-coa synthetase 1 alters fatty acid metabolism in rat primary hepatocytes. J Biol Chem 281:37246-37255.
23. Li LO, Ellis JM, Paich HA, Wang S, Gong N, Altshuller G, Thresher RJ, Koves TR, Watkins SM, Muoio DM, Cline GW, Shulman GI, Coleman RA. 2009. Liver-specific loss of long chain acyl-CoA synthetase-1 decreases triacylglycerol synthesis and beta-oxidation and alters phospholipid fatty acid composition. J Biol Chem 284:27816-27826.
24. Lu TJ, Lai WY, Huang CY, Hsieh WJ, Yu JS, Hsieh YJ, Chang WT, Leu TH, Chang WC, Chuang WJ, Tang MJ, Chen TY, Lu TL, Lai MD. 2006. Inhibition of cell migration by autophosphorylated mammalian sterile 20-like kinase 3 (MST3) involves paxillin and protein-tyrosine phosphatase-PEST. J Biol Chem 281:38405-38417.
25. Mashek DG, McKenzie MA, Van Horn CG, Coleman RA. 2006. Rat long chain acyl-CoA synthetase 5 increases fatty acid uptake and partitioning to cellular triacylglycerol in McArdle-RH7777 cells. J Biol Chem 281:945-950.
26. Matsuda D, Namatame I, Ohshiro T, Ishibashi S, Omura S, Tomoda H. 2008. Anti-atherosclerotic activity of triacsin C, an acyl-CoA synthetase inhibitor. J Antibiot (Tokyo) 61:318-321.
27. Obata Y, Fukumoto Y, Nakayama Y, Kuga T, Dohmae N, Yamaguchi N. 2010. The Lyn kinase C-lobe mediates Golgi export of Lyn through conformation-dependent ACSL3 association. J Cell Sci 123:2649-2662.
28. Oyadomari S, Harding HP, Zhang Y, Oyadomari M, Ron D. 2008. Dephosphorylation of translation initiation factor 2alpha enhances glucose tolerance and attenuates hepatosteatosis in mice. Cell Metab 7:520-532. (Pubitemid 351729207)
29. Pahl HL, Baeuerle PA. 1996. Activation of NF-kappa B by ER stress requires both Ca2+ and reactive oxygen intermediates as messengers. FEBS Lett 392:129-136. (Pubitemid 26276734)
30. Parkes HA, Preston E, Wilks D, Ballesteros M, Carpenter L, Wood L, Kraegen EW, Furler SM, Cooney GJ. 2006. Overexpression of acyl-CoA synthetase-1 increases lipid deposition in hepatic (HepG2) cells and rodent liver in vivo. Am J Physiol Endocrinol Metab 291:E737-E744. (Pubitemid 44484915)
31. Pluquet O, Qu LK, Baltzis D, Koromilas AE. 2005. Endoplasmic reticulum stress accelerates p53 degradation by the cooperative actions of Hdm2 and glycogen synthase kinase 3beta. Mol Cell Biol 25:9392-9405. (Pubitemid 41507840)
32. Qu L, Huang S, Baltzis D, Rivas-Estilla AM, Pluquet O, Hatzoglou M, Koumenis C, Taya Y, Yoshimura A, Koromilas AE. 2004. Endoplasmic reticulum stress induces p53 cytoplasmic localization and prevents p53-dependent apoptosis by a pathway involving glycogen synthase kinase-3beta. Genes Dev 18:261-277. (Pubitemid 38199252)
33. Rajas F, Gautier A, Bady I, Montano S, Mithieux G. 2002. Polyunsaturated fatty acyl coenzyme A suppress the glucose-6-phosphatase promoter activity by modulating the DNA binding of hepatocyte nuclear factor 4 alpha. J Biol Chem 277:15736-15744. (Pubitemid 34967848)
34. Raven JF, Baltzis D, Wang S, Mounir Z, Papadakis AI, Gao HQ, Koromilas AE. 2008. PKR and PKR-like endoplasmic reticulum kinase induce the proteasome-dependent degradation of cyclin D1 via a mechanism requiring eukaryotic initiation factor 2alpha phosphorylation. J Biol Chem 283: 3097-3108.
35. Reddy JK, Rao MS. 2006. Lipid metabolism and liver inflammation. II. Fatty liver disease and fatty acid oxidation.AmJ Physiol Gastrointest Liver Physiol 290:G852-G858.
36. Rutkowski DT, Wu J, Back SH, Callaghan MU, Ferris SP, Iqbal J, Clark R, Miao H, Hassler JR, Fornek J, Katze MG, Hussain MM, Song B, Swathirajan J, Wang J, Yau GD, Kaufman RJ. 2008. UPR pathways combine to prevent hepatic steatosis caused by ER stress-mediated suppression of transcriptional master regulators. Dev Cell 15:829-840.
37. Soupene E, Kuypers FA. 2008. Mammalian long-chain acyl-CoA synthetases. Exp Biol Med (Maywood) 233:507-521. (Pubitemid 351657352)
38. Starley BQ, Calcagno CJ, Harrison SA. 2010. Nonalcoholic fatty liver disease and hepatocellular carcinoma: A weighty connection. Hepatology 51:1820-1832.
39. Steinbrecher KA, Wilson W III, Cogswell PC, Baldwin AS. 2005. Glycogen synthase kinase 3beta functions to specify gene-specific, NF-kappaB-dependent transcription. Mol Cell Biol 25:8444-8455. (Pubitemid 41369166)
40. Thiele C, Spandl J. 2008. Cell biology of lipid droplets. Curr Opin Cell Biol 20:378-385.
41. Wang HC, Chang WT, Chang WW, Wu HC, Huang W, Lei HY, Lai MD, Fausto N, Su IJ. 2005. Hepatitis B virus pre-S2 mutant upregulates cyclin A expression and induces nodular proliferation of hepatocytes. Hepatology 41:761-770. (Pubitemid 40462938)
42. Wang D, Wei Y, Pagliassotti MJ. 2006. Saturated fatty acids promote endoplasmic reticulum stress and liver injury in rats with hepatic steatosis. Endocrinology 147:943-951. (Pubitemid 43113013)
43. Xu J, Teran-Garcia M, Park JH, Nakamura MT, Clarke SD. 2001. Polyunsaturated fatty acids suppress hepatic sterol regulatory element-binding protein-1 expression by accelerating transcript decay. J Biol Chem 276:9800-9807.
44. Yang JC, Teng CF, Wu HC, Tsai HW, Chuang HC, Tsai TF, Hsu YH, Huang W, Wu LW, Su IJ. 2009. Enhanced expression of vascular endothelial growth factor-A in ground glass hepatocytes and its implication in hepatitis B virus hepatocarcinogenesis. Hepatology 49:1962-1971.
45. Yao H, Ye J. 2008. Long chain acyl-CoA synthetase 3-mediated phosphatidylcholine synthesis is required for assembly of very low density lipoproteins in human hepatoma Huh7 cells. J Biol Chem 283:849-854.
46. Ye J, Rawson RB, Komuro R, Chen X, Dave UP, Prywes R, Brown MS, Goldstein JL. 2000. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 6:1355-1364. (Pubitemid 32045928)