Adipose triglyceride lipase is involved in the mobilization of triglyceride and retinoid stores of hepatic stellate cells

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1851, Issue 7, 2015, Pages 937-945

  Taschler, Ulrike ^a   Schreiber, Renate ^a   Chitraju, Chandramohan ^a   Grabner, Gernot F ^a   Romauch, Matthias ^a   Wolinski, Heimo ^a   Haemmerle, Guenter ^a   Breinbauer, Rolf ^b   Zechner, Rudolf ^a   Lass, Achim ^a   Zimmermann, Robert ^a  

^a UNIVERSITY OF GRAZ   (Austria)

^b GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

Adipose triglyceride lipase; Hepatic stellate cells; Retinoids; Retinyl ester

Indexed keywords

ADIPOSE TRIGLYCERIDE LIPASE; HORMONE SENSITIVE LIPASE; RETINYL PALMITATE ESTERASE; TRIACYLGLYCEROL; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG; CARBOXYLESTERASE; CHOLESTEROL ESTERASE; DESNUTRIN PROTEIN, MOUSE; RETINOID;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; COMPARATIVE GENE IDENTIFICATION 58; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BINDING; ENZYME DEGRADATION; G0 G1 SWITCH GENE 2; GENE IDENTIFICATION; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATOR GENE; STELLATE CELL; WHITE ADIPOSE TISSUE; ADIPOCYTE; ANIMAL; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; ENZYMOLOGY; FEMALE; GENETICS; KNOCKOUT MOUSE; LIPID METABOLISM; METABOLISM; PHYSIOLOGY;

MURINAE; MUS;

ADIPOCYTES; ANIMALS; CARBOXYLIC ESTER HYDROLASES; CERCOPITHECUS AETHIOPS; COS CELLS; FEMALE; HEPATIC STELLATE CELLS; LIPASE; LIPID METABOLISM; MICE; MICE, KNOCKOUT; RETINOIDS; STEROL ESTERASE; TRIGLYCERIDES;

EID: 84925746640     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2015.02.017     Document Type: Article

References (56)

1. D.N. D'Ambrosio, R.D. Clugston, and W.S. Blaner Vitamin A metabolism: an update Nutrients 3 2011 63 103
2. W.S. Blaner, S.M. O'Byrne, N. Wongsiriroj, J. Kluwe, D.M. D'Ambrosio, H. Jiang, R.F. Schwabe, E.M. Hillman, R. Piantedosi, and J. Libien Hepatic stellate cell lipid droplets: a specialized lipid droplet for retinoid storage Biochim. Biophys. Acta 1791 2009 467 473
3. R. Blomhoff, and H.K. Blomhoff Overview of retinoid metabolism and function J. Neurobiol. 66 2006 606 630
4. O. Ziouzenkova, and J. Plutzky Retinoid metabolism and nuclear receptor responses: New insights into coordinated regulation of the PPAR-RXR complex FEBS Lett. 582 2008 32 38
5. P.M. Amann, S.B. Eichmuller, J. Schmidt, and A.V. Bazhin Regulation of gene expression by retinoids Curr. Med. Chem. 18 2011 1405 1412
6. S.M. O'Byrne, N. Wongsiriroj, J. Libien, S. Vogel, I.J. Goldberg, W. Baehr, K. Palczewski, and W.S. Blaner Retinoid absorption and storage is impaired in mice lacking lecithin:retinol acyltransferase (LRAT) J. Biol. Chem. 280 2005 35647 35657
7. R. Schreiber, U. Taschler, K. Preiss-Landl, N. Wongsiriroj, R. Zimmermann, and A. Lass Retinyl ester hydrolases and their roles in vitamin A homeostasis Biochim. Biophys. Acta 1821 2012 113 123
8. E.H. Harrison Lipases and carboxylesterases: possible roles in the hepatic utilization of vitamin A J. Nutr. 130 2000 340S 344S
9. K. Strom, T.E. Gundersen, O. Hansson, S. Lucas, C. Fernandez, R. Blomhoff, and C. Holm Hormone-sensitive lipase (HSL) is also a retinyl ester hydrolase: evidence from mice lacking HSL FASEB J. 23 2009 2307 2316
10. G. Moiseyev, Y. Takahashi, Y. Chen, S. Gentleman, T.M. Redmond, R.K. Crouch, and J.X. Ma RPE65 is an iron(II)-dependent isomerohydrolase in the retinoid visual cycle J. Biol. Chem. 281 2006 2835 2840
11. T. Mello, A. Nakatsuka, S. Fears, W. Davis, H. Tsukamoto, W.F. Bosron, and S.P. Sanghani Expression of carboxylesterase and lipase genes in rat liver cell-types Biochem. Biophys. Res. Commun. 374 2008 460 464
12. G. Wolf Function of the protein RPE65 in the visual cycle Nutr. Rev. 63 2005 97 100
13. R. Zimmermann, J.G. Strauss, G. Haemmerle, G. Schoiswohl, R. Birner-Gruenberger, M. Riederer, A. Lass, G. Neuberger, F. Eisenhaber, A. Hermetter, and R. Zechner Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase Science 306 2004 1383 1386
14. A. Lass, R. Zimmermann, G. Haemmerle, M. Riederer, G. Schoiswohl, M. Schweiger, P. Kienesberger, J.G. Strauss, G. Gorkiewicz, and R. Zechner Adipose triglyceride lipase-mediated lipolysis of cellular fat stores is activated by CGI-58 and defective in Chanarin-Dorfman Syndrome Cell Metab. 3 2006 309 319
15. G. Haemmerle, R. Zimmermann, M. Hayn, C. Theussl, G. Waeg, E. Wagner, W. Sattler, T.M. Magin, E.F. Wagner, and R. Zechner Hormone-sensitive lipase deficiency in mice causes diglyceride accumulation in adipose tissue, muscle, and testis J. Biol. Chem. 277 2002 4806 4815
16. G. Haemmerle, A. Lass, R. Zimmermann, G. Gorkiewicz, C. Meyer, J. Rozman, G. Heldmaier, R. Maier, C. Theussl, S. Eder, D. Kratky, E.F. Wagner, M. Klingenspor, G. Hoefler, and R. Zechner Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase Science 312 2006 734 737
17. H.M. Nagy, M. Paar, C. Heier, T. Moustafa, P. Hofer, G. Haemmerle, A. Lass, R. Zechner, M. Oberer, and R. Zimmermann Adipose triglyceride lipase activity is inhibited by long-chain acyl-coenzyme A Biochim. Biophys. Acta 1841 2014 588 594
18. M. Kumari, G. Schoiswohl, C. Chitraju, M. Paar, I. Cornaciu, A.Y. Rangrez, N. Wongsiriroj, H.M. Nagy, P.T. Ivanova, S.A. Scott, O. Knittelfelder, G.N. Rechberger, R. Birner-Gruenberger, S. Eder, H.A. Brown, G. Haemmerle, M. Oberer, A. Lass, E.E. Kershaw, R. Zimmermann, and R. Zechner Adiponutrin functions as a nutritionally regulated lysophosphatidic acid acyltransferase Cell Metab. 15 2012 691 702
19. R. Blomhoff, and T. Berg Isolation and cultivation of rat liver stellate cells Methods Enzymol. 190 1990 58 71
20. R. Schreiber, U. Taschler, H. Wolinski, A. Seper, S.N. Tamegger, M. Graf, S.D. Kohlwein, G. Haemmerle, R. Zimmermann, R. Zechner, and A. Lass Esterase 22 and beta-glucuronidase hydrolyze retinoids in mouse liver J. Lipid Res. 50 2009 2514 2523
21. G. Troen, A. Nilsson, K.R. Norum, and R. Blomhoff Characterization of liver stellate cell retinyl ester storage Biochem. J. 300 Pt 3 1994 793 798
22. M. Schweiger, T.O. Eichmann, U. Taschler, R. Zimmermann, R. Zechner, and A. Lass Measurement of Lipolysis Methods Enzymol. 538C 2014 171 193
23. M. Schweiger, M. Paar, C. Eder, J. Brandis, E. Moser, G. Gorkiewicz, S. Grond, F.P. Radner, I. Cerk, I. Cornaciu, M. Oberer, S. Kersten, R. Zechner, R. Zimmermann, and A. Lass G0/G1 switch gene-2 regulates human adipocyte lipolysis by affecting activity and localization of adipose triglyceride lipase J. Lipid Res. 53 2012 2307 2317
24. C. Pirazzi, L. Valenti, B.M. Motta, P. Pingitore, K. Hedfalk, R.M. Mancina, M.A. Burza, C. Indiveri, Y. Ferro, T. Montalcini, C. Maglio, P. Dongiovanni, S. Fargion, R. Rametta, A. Pujia, L. Andersson, S. Ghosal, M. Levin, O. Wiklund, M. Iacovino, J. Boren, and S. Romeo PNPLA3 has retinyl-palmitate lipase activity in human hepatic stellate cells Hum. Mol. Genet. 23 2014 4077 4085
25. X. Yang, X. Lu, M. Lombes, G.B. Rha, Y.I. Chi, T.M. Guerin, E.J. Smart, and J. Liu The G(0)/G(1) switch gene 2 regulates adipose lipolysis through association with adipose triglyceride lipase Cell Metab. 11 2010 194 205
26. M. Yamada, W.S. Blaner, D.R. Soprano, J.L. Dixon, H.M. Kjeldbye, and D.S. Goodman Biochemical characteristics of isolated rat liver stellate cells Hepatology 7 1987 1224 1229
27. H.F. Hendriks, P.J. Brekelmans, R. Buytenhek, A. Brouwer, A.M. de Leeuw, and D.L. Knook Liver parenchymal cells differ from the fat-storing cells in their lipid composition Lipids 22 1987 266 273
28. H. Moriwaki, W.S. Blaner, R. Piantedosi, and D.S. Goodman Effects of dietary retinoid and triglyceride on the lipid composition of rat liver stellate cells and stellate cell lipid droplets J. Lipid Res. 29 1988 1523 1534
29. N. Mayer, M. Schweiger, M. Romauch, G.F. Grabner, T.O. Eichmann, E. Fuchs, J. Ivkovic, C. Heier, I. Mrak, A. Lass, G. Hofler, C. Fledelius, R. Zechner, R. Zimmermann, and R. Breinbauer Development of small-molecule inhibitors targeting adipose triglyceride lipase Nat. Chem. Biol. 9 2013 785 787
30. M. Schweiger, R. Schreiber, G. Haemmerle, A. Lass, C. Fledelius, P. Jacobsen, H. Tornqvist, R. Zechner, and R. Zimmermann Adipose triglyceride lipase and hormone-sensitive lipase are the major enzymes in adipose tissue triacylglycerol catabolism J. Biol. Chem. 281 2006 40236 40241
31. R. Bartz, J.K. Zehmer, M. Zhu, Y. Chen, G. Serrero, Y. Zhao, and P. Liu Dynamic activity of lipid droplets: protein phosphorylation and GTP-mediated protein translocation J. Proteome Res. 6 2007 3256 3265
32. M. Schweiger, A. Lass, R. Zimmermann, T.O. Eichmann, and R. Zechner Neutral lipid storage disease: genetic disorders caused by mutations in adipose triglyceride lipase/PNPLA2 or CGI-58/ABHD5 Am. J. Physiol. Endocrinol. Metab. 297 2009 E289 E296
33. K.T. Ong, M.T. Mashek, S.Y. Bu, A.S. Greenberg, and D.G. Mashek Adipose triglyceride lipase is a major hepatic lipase that regulates triacylglycerol turnover and fatty acid signaling and partitioning Hepatology 53 2011 116 126
34. J.W. Wu, S.P. Wang, F. Alvarez, S. Casavant, N. Gauthier, L. Abed, K.G. Soni, G. Yang, and G.A. Mitchell Deficiency of liver adipose triglyceride lipase in mice causes progressive hepatic steatosis Hepatology 54 2011 122 132
35. P.G. Chandak, B. Radovic, E. Aflaki, D. Kolb, M. Buchebner, E. Frohlich, C. Magnes, F. Sinner, G. Haemmerle, R. Zechner, I. Tabas, S. Levak-Frank, and D. Kratky Efficient phagocytosis requires triacylglycerol hydrolysis by adipose triglyceride lipase J. Biol. Chem. 285 2010 20192 20201
36. R. Zechner, R. Zimmermann, T.O. Eichmann, S.D. Kohlwein, G. Haemmerle, A. Lass, and F. Madeo FAT SIGNALS-lipases and lipolysis in lipid metabolism and signaling Cell Metab. 15 2012 279 291
37. J. Gao, and M. Simon Identification of a novel keratinocyte retinyl ester hydrolase as a transacylase and lipase J. Investig. Dermatol. 124 2005 1259 1266
38. J.G. Gao, and M. Simon A comparative study of human GS2, its paralogues, and its rat orthologue Biochem. Biophys. Res. Commun. 360 2007 501 506
39. J. Kluwe, N. Wongsiriroj, J.S. Troeger, G.Y. Gwak, D.H. Dapito, J.P. Pradere, H. Jiang, M. Siddiqi, R. Piantedosi, S.M. O'Byrne, W.S. Blaner, and R.F. Schwabe Absence of hepatic stellate cell retinoid lipid droplets does not enhance hepatic fibrosis but decreases hepatic carcinogenesis Gut 60 2011 1260 1268
40. C. Tsutsumi, M. Okuno, L. Tannous, R. Piantedosi, M. Allan, D.S. Goodman, and W.S. Blaner Retinoids and retinoid-binding protein expression in rat adipocytes J. Biol. Chem. 267 1992 1805 1810
41. J. Osuga, S. Ishibashi, T. Oka, H. Yagyu, R. Tozawa, A. Fujimoto, F. Shionoiri, N. Yahagi, F.B. Kraemer, O. Tsutsumi, and N. Yamada Targeted disruption of hormone-sensitive lipase results in male sterility and adipocyte hypertrophy, but not in obesity Proc. Natl. Acad. Sci. U. S. A. 97 2000 787 792
42. R. Zimmermann, G. Haemmerle, E.M. Wagner, J.G. Strauss, D. Kratky, and R. Zechner Decreased fatty acid esterification compensates for the reduced lipolytic activity in hormone-sensitive lipase-deficient white adipose tissue J. Lipid Res. 44 2003 2089 2099
43. K. Strom, O. Hansson, S. Lucas, P. Nevsten, C. Fernandez, C. Klint, S. Moverare-Skrtic, F. Sundler, C. Ohlsson, and C. Holm Attainment of brown adipocyte features in white adipocytes of hormone-sensitive lipase null mice PLoS One 3 2008 e1793
44. W.J. Shen, Z. Yu, S. Patel, D. Jue, L.F. Liu, and F.B. Kraemer Hormone-sensitive lipase modulates adipose metabolism through PPARgamma Biochim. Biophys. Acta 1811 2011 9 16
45. G. Haemmerle, T. Moustafa, G. Woelkart, S. Buttner, A. Schmidt, T. van de Weijer, M. Hesselink, D. Jaeger, P.C. Kienesberger, K. Zierler, R. Schreiber, T. Eichmann, D. Kolb, P. Kotzbeck, M. Schweiger, M. Kumari, S. Eder, G. Schoiswohl, N. Wongsiriroj, N.M. Pollak, F.P. Radner, K. Preiss-Landl, T. Kolbe, T. Rulicke, B. Pieske, M. Trauner, A. Lass, R. Zimmermann, G. Hoefler, S. Cinti, E.E. Kershaw, P. Schrauwen, F. Madeo, B. Mayer, and R. Zechner ATGL-mediated fat catabolism regulates cardiac mitochondrial function via PPAR-alpha and PGC-1 Nat. Med. 17 2011 1076 1085
46. M. Ahmadian, M.J. Abbott, T. Tang, C.S. Hudak, Y. Kim, M. Bruss, M.K. Hellerstein, H.Y. Lee, V.T. Samuel, G.I. Shulman, Y. Wang, R.E. Duncan, C. Kang, and H.S. Sul Desnutrin/ATGL Is Regulated by AMPK and Is Required for a Brown Adipose Phenotype Cell Metab. 13 2011 739 748
47. U.E. Lee, and S.L. Friedman Mechanisms of hepatic fibrogenesis Best Pract. Res. Clin. Gastroenterol. 25 2011 195 206
48. E. Mormone, J. George, and N. Nieto Molecular pathogenesis of hepatic fibrosis and current therapeutic approaches Chem. Biol. Interact. 193 2011 225 231
49. Y. Shirakami, S.A. Lee, R.D. Clugston, and W.S. Blaner Hepatic metabolism of retinoids and disease associations Biochim. Biophys. Acta 1821 2012 124 136
50. B.H. Davis, D. Coll, and D.W. Beno Retinoic acid suppresses the response to platelet-derived growth factor in human hepatic Ito-cell-like myofibroblasts: a post-receptor mechanism independent of raf/fos/jun/egr activation Biochem. J. 294 Pt 3 1993 785 791
51. K. Hellemans, P. Verbuyst, E. Quartier, F. Schuit, K. Rombouts, R.A. Chandraratna, D. Schuppan, and A. Geerts Differential modulation of rat hepatic stellate phenotype by natural and synthetic retinoids Hepatology 39 2004 97 108
52. Y. Mizobuchi, I. Shimizu, M. Yasuda, H. Hori, M. Shono, and S. Ito Retinyl palmitate reduces hepatic fibrosis in rats induced by dimethylnitrosamine or pig serum J. Hepatol. 29 1998 933 943
53. W.F. Seifert, A. Bosma, A. Brouwer, H.F. Hendriks, P.J. Roholl, R.E. van Leeuwen, G.C. van Thiel-de Ruiter, I. Seifert-Bock, and D.L. Knook Vitamin A deficiency potentiates carbon tetrachloride-induced liver fibrosis in rats Hepatology 19 1994 193 201
54. A.P. Geubel, C. De Galocsy, N. Alves, J. Rahier, and C. Dive Liver damage caused by therapeutic vitamin A administration: estimate of dose-related toxicity in 41 cases Gastroenterology 100 1991 1701 1709
55. Z. Dan, Y. Popov, E. Patsenker, D. Preimel, C. Liu, X.D. Wang, H.K. Seitz, D. Schuppan, and F. Stickel Hepatotoxicity of alcohol-induced polar retinol metabolites involves apoptosis via loss of mitochondrial membrane potential FASEB J. 19 2005 845 847
56. P. Jha, T. Claudel, A. Baghdasaryan, M. Mueller, E. Halilbasic, S.K. Das, A. Lass, R. Zimmermann, R. Zechner, G. Hoefler, and M. Trauner Role of adipose triglyceride lipase (PNPLA2) in protection from hepatic inflammation in mouse models of steatohepatitis and endotoxemia Hepatology 59 2014 858 869