Deletion of CGI-58 or adipose triglyceride lipase differently affects macrophage function and atherosclerosis

Journal of Lipid Research

Volumn 55, Issue 12, 2015, Pages 2562-2575

  Goeritzer, Madeleine ^a   Schlager, Stefanie ^a   Radovic, Branislav ^a   Madreiter, Corina T ^a   Rainer, Silvia ^a   Thomas, Gwynneth ^b   Lord, Caleb C ^c   Sacks, Jessica ^d   Brown, Amanda L ^d   Vujic, Nemanja ^a   Obrowsky, Sascha ^a   Sachdev, Vinay ^a   Kolb, Dagmar ^a   Chandak, Prakash G ^a,e   Graier, Wolfgang F ^a   Sattler, Wolfgang ^a   Brown, J Mark ^d   Kratky, Dagmar ^a  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d LERNER RESEARCH INSTITUTE   (United States)

^e UNIVERSITY OF BERN   (Switzerland)

Author keywords

Comparative gene identification 58; Inflammation; Lipid droplets; Storage diseases

Indexed keywords

ADIPOSE TRIGLYCERIDE LIPASE; APOLIPOPROTEIN E; COMPARATIVE GENE IDENTIFICATION 58 PROTEIN; FAT DROPLET; HYDROLASE; LOW DENSITY LIPOPROTEIN RECEPTOR; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG; 1 ACYLGLYCEROPHOSPHATE ACYLTRANSFERASE; ABHD5 PROTEIN, MOUSE; ANTISENSE OLIGONUCLEOTIDE; DESNUTRIN PROTEIN, MOUSE; TRIACYLGLYCEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ATHEROSCLEROSIS; AORTA ROOT; APOPTOSIS; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; BONE MARROW CELL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; FEMALE; LIPID DIET; LIPID STORAGE; MACROPHAGE FUNCTION; MALE; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PHAGOCYTOSIS; ADVERSE EFFECTS; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL CULTURE; COMPARATIVE STUDY; CROSS BREEDING; GENE DELETION; GENE SILENCING; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MITOCHONDRION; PATHOLOGY; TRANSGENIC MOUSE; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

1-ACYLGLYCEROL-3-PHOSPHATE O-ACYLTRANSFERASE; ANIMALS; APOPTOSIS; ATHEROSCLEROSIS; CELLS, CULTURED; CROSSES, GENETIC; DIET, HIGH-FAT; FEMALE; GENE DELETION; GENE KNOCKDOWN TECHNIQUES; LIPASE; LIPID DROPLETS; MACROPHAGES, PERITONEAL; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; OLIGONUCLEOTIDES, ANTISENSE; PHAGOCYTOSIS; TRIGLYCERIDES;

EID: 84919725062     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M052613     Document Type: Article

References (32)

1. McLaren, J. E., D. R. Michael, T. G. Ashlin, and D. P. Ramji. 2011. Cytokines, macrophage lipid metabolism and foam cells: implications for cardiovascular disease therapy. Prog. Lipid Res. 50: 331-347.
2. Lass, A., R. Zimmermann, G. Haemmerle, M. Riederer, G. Schoiswohl, M. Schweiger, P. Kienesberger, J. G. Strauss, G. Gorkiewicz, and R. Zechner. 2006. Adipose triglyceride lipase-mediated lipolysis of cellular fat stores is activated by CGI-58 and defective in Chanarin-Dorfman syndrome. Cell Metab. 3: 309-319.
3. Zechner, R., R. Zimmermann, T. O. Eichmann, S. D. Kohlwein, G. Haemmerle, A. Lass, and F. Madeo. 2012. FAT SIGNALS-lipases and lipolysis in lipid metabolism and signaling. Cell Metab. 15: 279-291.
4. Schweiger, M., A. Lass, R. Zimmermann, T. O. Eichmann, and R. Zechner. 2009. Neutral lipid storage disease: genetic disorders caused by mutations in adipose triglyceride lipase/PNPLA2 or CGI-58/ABHD5. Am. J. Physiol. Endocrinol. Metab. 297: E289-E296.
5. Radner, F. P., I. E. Streith, G. Schoiswohl, M. Schweiger, M. Kumari, T. O. Eichmann, G. Rechberger, H. C. Koefeler, S. Eder, S. Schauer, et al. 2010. Growth retardation, impaired triacylglycerol catabolism, hepatic steatosis, and lethal skin barrier defect in mice lacking comparative gene identifi cation-58 (CGI-58). J. Biol. Chem. 285: 7300-7311.
6. Fischer, J., C. Lefevre, E. Morava, J. M. Mussini, P. Laforet, A. Negre-Salvayre, M. Lathrop, and R. Salvayre. 2007. The gene encoding adipose triglyceride lipase (PNPLA2) is mutated in neutral lipid storage disease with myopathy. Nat. Genet. 39: 28-30.
7. Haemmerle, G., A. Lass, R. Zimmermann, G. Gorkiewicz, C. Meyer, J. Rozman, G. Heldmaier, R. Maier, C. Theussl, S. Eder, et al. 2006. Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase. Science. 312: 734-737.
8. Lefèvre, C., F. Jobard, F. Caux, B. Bouadjar, A. Karaduman, R. Heilig, H. Lakhdar, A. Wollenberg, J. L. Verret, J. Weissenbach, et al. 2001. Mutations in CGI-58, the gene encoding a new protein of the esterase/lipase/thioesterase subfamily, in Chanarin-Dorfman syndrome. Am. J. Hum. Genet. 69: 1002-1012.
9. Brown, J. M., J. L. Betters, C. Lord, Y. Ma, X. Han, K. Yang, H. M. Alger, J. Melchior, J. Sawyer, R. Shah, et al. 2010. CGI-58 knockdown in mice causes hepatic steatosis, but prevents diet-induced obesity and glucose intolerance. J. Lipid Res. 51: 3306-3315.
10. Lord, C. C., and J. M. Brown. 2012. Distinct roles for alpha-beta hydrolase domain 5 (ABHD5/CGI-58) and adipose triglyceride lipase (ATGL/PNPLA2) in lipid metabolism and signaling. Adipocyte. 1: 123-131.
11. Zierler, K. A., R. Zechner, and G. Haemmerle. 2014. Comparative gene identification-58/alpha/beta hydrolase domain 5: more than just an adipose triglyceride lipase activator? Curr. Opin. Lipidol. 25: 102-109.
12. Aflaki, E., B. Radovic, P. G. Chandak, D. Kolb, T. Eisenberg, J. Ring, I. Fertschai, A. Uellen, H. Wolinski, S. D. Kohlwein, et al. 2011. Triacylglycerol accumulation activates the mitochondrial apoptosis pathway in macrophages. J. Biol. Chem. 286: 7418-7428.
13. Aflaki, E., P. Doddapattar, B. Radovic, S. Povoden, D. Kolb, N. Vujic, M. Wegscheider, H. Koefeler, T. Hornemann, W. F. Graier, et al. 2012. C16 ceramide is crucial for triacylglycerol-induced apoptosis in macrophages. Cell Death Dis. 3: e280.
14. Aflaki, E., N. A. Balenga, P. Luschnig-Schratl, H. Wolinski, S. Povoden, P. G. Chandak, J. G. Bogner-Strauss, S. Eder, V. Konya, S. D. Kohlwein, et al. 2011. Impaired Rho GTPase activation abrogates cell polarization and migration in macrophages with defective lipolysis. Cell. Mol. Life Sci. 68: 3933-3947.
15. Chandak, P. G., B. Radovic, E. Aflaki, D. Kolb, M. Buchebner, E. Frohlich, C. Magnes, F. Sinner, G. Haemmerle, R. Zechner, et al. 2010. Efficient phagocytosis requires triacylglycerol hydrolysis by adipose triglyceride lipase. J. Biol. Chem. 285: 20192-20201.
16. Lammers, B., P. G. Chandak, E. Aflaki, G. H. Van Puijvelde, B. Radovic, R. B. Hildebrand, I. Meurs, R. Out, J. Kuiper, T. J. Van Berkel, et al. 2011. Macrophage adipose triglyceride lipase deficiency attenuates atherosclerotic lesion development in low-density lipoprotein receptor knockout mice. Arterioscler. Thromb. Vasc. Biol. 31: 67-73.
17. Zierler, K. A., D. Jaeger, N. M. Pollak, S. Eder, G. N. Rechberger, F. P. Radner, G. Woelkart, D. Kolb, A. Schmidt, M. Kumari, et al. 2013. Functional cardiac lipolysis in mice critically depends on comparative gene identifi cation-58. J. Biol. Chem. 288: 9892-9904.
18. Clausen, B. E., C. Burkhardt, W. Reith, R. Renkawitz, and I. Forster. 1999. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8: 265-277.
19. Brown, J. M., S. Chung, J. K. Sawyer, C. Degirolamo, H. M. Alger, T. Nguyen, X. Zhu, M. N. Duong, A. L. Wibley, R. Shah, et al. 2008. Inhibition of stearoyl-coenzyme A desaturase 1 dissociates insulin resistance and obesity from atherosclerosis. Circulation. 118: 1467-1475.
20. Sattler, W., H. Puhl, M. Hayn, G. M. Kostner, and H. Esterbauer. 1991. Determination of fatty acids in the main lipoprotein classes by capillary gas chromatography: BF3/methanol transesterification of lyophilized samples instead of Folch extraction gives higher yields. Anal. Biochem. 198: 184-190.
21. Schweiger, M., T. O. Eichmann, U. Taschler, R. Zimmermann, R. Zechner, and A. Lass. 2014. Measurement of lipolysis. Methods Enzymol. 538: 171-193.
22. Pfaffl, M. W., G. W. Horgan, and L. Dempfle. 2002. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30: e36.
23. -/- mice without inducing liver steatosis and hypertriglyceridemia. J. Lipid Res. 50: 312-326.
24. Tischner, D., C. Manzl, C. Soratroi, A. Villunger, and G. Krumschnabel. 2012. Necrosis-like death can engage multiple proapoptotic Bcl-2 protein family members. Apoptosis. 17: 1197-1209.
25. Marciniak, S. J., C. Y. Yun, S. Oyadomari, I. Novoa, Y. Zhang, R. Jungreis, K. Nagata, H. P. Harding, and D. Ron. 2004. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 18: 3066-3077.
26. Martinez, F. O., A. Sica, A. Mantovani, and M. Locati. 2008. Macrophage activation and polarization. Front. Biosci. 13: 453-461.
27. Sharda, D. R., S. Yu, M. Ray, M. L. Squadrito, M. De Palma, T. A. Wynn, S. M. Morris, Jr., and P. A. Hankey. 2011. Regulation of macrophage arginase expression and tumor growth by the Ron receptor tyrosine kinase. J. Immunol. 187: 2181-2192.
28. Miao, H., J. Ou, Y. Ma, F. Guo, Z. Yang, M. Wiggins, C. Liu, W. Song, X. Han, M. Wang, et al. 2014. Macrophage CGI-58 deficiency activates ROS-inflammasome pathway to promote insulin resistance in mice. Cell Reports. 7: 223-235.
29. Eichmann, T. O., M. Kumari, J. T. Haas, R. V. Farese, Jr., R. Zimmermann, A. Lass, and R. Zechner. 2012. Studies on the substrate and stereo/regioselectivity of adipose triglyceride lipase, hormone-sensitive lipase, and diacylglycerol-O-acyltransferases. J. Biol. Chem. 287: 41446-41457.
30. Haemmerle, G., T. Moustafa, G. Woelkart, S. Büttner, A. Schmidt, T. van de Weijer, M. Hesselink, D. Jaeger, P. C. Kienesberger, K. Zierler, et al. 2011. ATGL-mediated fat catabolism regulates cardiac mitochondrial function via PPAR-alpha and PGC-1. Nat. Med. 17: 1076-1085.
31. Lord, C. C., J. L. Betters, P. T. Ivanova, S. B. Milne, D. S. Myers, J. Madenspacher, G. Thomas, S. Chung, M. Liu, M. A. Davis, et al. 2012. CGI-58/ABHD5-derived signaling lipids regulate systemic infl ammation and insulin action. Diabetes. 61: 355-363.
32. Baitsch, D., H. H. Bock, T. Engel, R. Telgmann, C. Muller-Tidow, G. Varga, M. Bot, J. Herz, H. Robenek, A. von Eckardstein, et al. 2011. Apolipoprotein E induces antiinfl ammatory phenotype in macrophages. Arterioscler. Thromb. Vasc. Biol. 31: 1160-1168.