G0/G1 switch gene 2 regulates cardiac lipolysis

Journal of Biological Chemistry

Volumn 290, Issue 43, 2015, Pages 26141-26150

  Heier, Christoph ^a   Radner, Franz P W ^a   Moustafa, Tarek ^a,b   Schreiber, Renate ^a   Grond, Susanne ^a   Eichmann, Thomas O ^a   Schweiger, Martina ^a   Schmidt, Albrecht ^c   Cerk, Ines K ^a   Oberer, Monika ^a   Christian Theussl, H ^d,e   Wojciechowski, Jacek ^d,e   Penninger, Josef M ^d,e   Zimmermann, Robert ^a   Zechner, Rudolf ^a  

^a UNIVERSITY OF GRAZ   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c MEDICAL UNIVERSITY OF GRAZ   (Austria)

^d RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^e INSTITUTE OF MOLECULAR BIOTECHNOLOGY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES; FATTY ACIDS; MAMMALS; METABOLISM; PROTEINS; SUBSTRATES; SYNTHESIS (CHEMICAL);

CARDIAC FUNCTIONS; EXPRESSION LEVELS; OVER-EXPRESSION; PROTEIN-PROTEIN INTERACTIONS; SIGNALING MOLECULES; SUBSTRATE UTILIZATION; TRANSGENIC MICE; TRIACYLGLYCEROLS;

HEART;

BRAIN NATRIURETIC PEPTIDE; COLLAGEN TYPE 1; COLLAGEN TYPE 3; G0 G1 SWITCH 2 PROTEIN; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; MYOSIN HEAVY CHAIN BETA; NUCLEIC ACID BINDING PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRIACYLGLYCEROL; TRIACYLGLYCEROL LIPASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; G0S2 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIAC LIPOLYSIS; CARDIAC STEATOSIS; CELL VACUOLE; COL1A1 GENE; COL3A1 GENE; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME REGULATION; ENZYME SUBSTRATE COMPLEX; G0S2 GENE; GENE; GENE CONTROL; GENE OVEREXPRESSION; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; LIPID HYDROLYSIS; LIPOGENESIS; LIPOLYSIS; MALE; MOLECULAR PATHOLOGY; MOUSE; MOUSE MUTANT; MYH7 GENE; NONHUMAN; NPPB GENE; NUTRITIONAL STATUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REFEEDING; STEATOSIS; TGF BETA GENE; TISSUE DISTRIBUTION; TNF ALPHA GENE; WILD TYPE MOUSE; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL LINE; GENETICS; HEART FUNCTION TEST; METABOLISM; TRANSGENIC MOUSE;

ANIMALS; CELL CYCLE PROTEINS; CELL LINE; G1 PHASE; HEART FUNCTION TESTS; LIPOLYSIS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYOCARDIUM; RESTING PHASE, CELL CYCLE; TRIGLYCERIDES;

EID: 84944894356     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.671842     Document Type: Article

References (38)

1. Neely, J. R., and Morgan, H. E. (1974) Relationship between carbohydrate and lipid metabolism and the energy balance of heart muscle. Annu. Rev. Physiol. 36, 413-459
2. Lopaschuk, G. D., Ussher, J. R., Folmes, C. D., Jaswal, J. S., and Stanley, W. C. (2010) Myocardial fatty acid metabolism in health and disease. Physiol. Rev. 90, 207-258
3. Kienesberger, P. C., Pulinilkunnil, T., Nagendran, J., and Dyck, J. R. (2013) Myocardial triacylglycerol metabolism. J. Mol. Cell. Cardiol. 55, 101-110
4. Goldberg, I. J., Trent, C. M., and Schulze, P. C. (2012) Lipid metabolism and toxicity in the heart. Cell. Metab. 15, 805-812
5. Lewin, T. M., and Coleman, R. A. (2003) Regulation of myocardial triacylglycerol synthesis and metabolism. Biochim. Biophys. Acta 1634, 63-75
6. Ellis, J. M., Mentock, S. M., Depetrillo, M. A., Koves, T. R., Sen, S., Watkins, S. M., Muoio, D. M., Cline, G. W., Taegtmeyer, H., Shulman, G. I., Willis, M. S., and Coleman, R. A. (2011) Mouse cardiac acyl coenzyme a synthetase 1 deficiency impairs fatty acid oxidation and induces cardiac hypertrophy. Mol. Cell. Biol. 31, 1252-1262
7. Banke, N. H., Wende, A. R., Leone, T. C., O'Donnell, J. M., Abel, E. D., Kelly, D. P., and Lewandowski, E. D. (2010) Preferential oxidation of triacylglyceridederived fatty acids in heart is augmented by the nuclear receptor PPARα. Circ. Res. 107, 233-241
8. Saddik, M., and Lopaschuk, G. D. (1991) Myocardial triglyceride turnover and contribution to energy substrate utilization in isolated working rat hearts. J. Biol. Chem. 266, 8162-8170
9. Borradaile, N. M., and Schaffer, J. E. (2005) Lipotoxicity in the heart. Curr. Hypertens. Rep. 7, 412-417
10. Bosma, M., Dapito, D. H., Drosatos-Tampakaki, Z., Huiping-Son, N., Huang, L. S., Kersten, S., Drosatos, K., and Goldberg, I. J. (2014) Sequestration of fatty acids in triglycerides prevents endoplasmic reticulum stress in an in vitro model of cardiomyocyte lipotoxicity. Biochim. Biophys. Acta 1841, 1648-1655
11. 1H-magnetic resonance spectroscopy study. Circulation 116, 1170-1175
12. McGavock, J. M., Victor, R. G., Unger, R. H., Szczepaniak, L. S., and American College of Physicians and the American Physiological Society (2006) Adiposity of the heart, revisited. Ann. Intern. Med. 144, 517-524
13. Schweiger, M., Lass, A., Zimmermann, R., Eichmann, T. O., and Zechner, R. (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, E289-96
14. Zimmermann, R., Strauss, J. G., Haemmerle, G., Schoiswohl, G., Birner-Gruenberger, R., Riederer, M., Lass, A., Neuberger, G., Eisenhaber, F., Hermetter, A., and Zechner, R. (2004) Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science 306, 1383-1386
15. Haemmerle, G., Lass, A., Zimmermann, R., Gorkiewicz, G., Meyer, C., Rozman, J., Heldmaier, G., Maier, R., Theussl, C., Eder, S., Kratky, D., Wagner, E. F., Klingenspor, M., Hoefler, G., and Zechner, R. (2006) Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase. Science 312, 734-737
16. Fischer, J., Lefèvre, C., Morava, E., Mussini, J. M., Laforêt, P., Negre-Salvayre, A., Lathrop, M., and Salvayre, R. (2007) The gene encoding adipose triglyceride lipase (PNPLA2) is mutated in neutral lipid storage disease with myopathy. Nat. Genet. 39, 28-30
17. Hirano, K., Ikeda, Y., Zaima, N., Sakata, Y., and Matsumiya, G. (2008) Triglyceride deposit cardiomyovasculopathy. N. Engl. J. Med. 359, 2396-2398
18. Kaneko, K., Kuroda, H., Izumi, R., Tateyama, M., Kato, M., Sugimura, K., Sakata, Y., Ikeda, Y., Hirano, K., and Aoki, M. (2014) A novel mutation in PNPLA2 causes neutral lipid storage disease with myopathy and triglyceride deposit cardiomyovasculopathy: a case report and literature review. Neuromuscul. Disord. 24, 634-641
19. Haemmerle, G., Moustafa, T., Woelkart, G., Büttner, S., Schmidt, A., van de Weijer, T., Hesselink, M., Jaeger, D., Kienesberger, P. C., Zierler, K., Schreiber, R., Eichmann, T., Kolb, D., Kotzbeck, P., Schweiger, M., Kumari, M., Eder, S., Schoiswohl, G., Wongsiriroj, N., Pollak, N. M., Radner, F. P., Preiss-Landl, K., Kolbe, T., Rülicke, T., Pieske, B., Trauner, M., Lass, A., Zimmermann, R., Hoefler, G., Cinti, S., Kershaw, E. E., Schrauwen, P., Madeo, F., Mayer, B., and Zechner, R. (2011) ATGL-mediated fat catabolism regulates cardiac mitochondrial function via PPAR-α and PGC-1. Nat. Med. 17, 1076-1085
20. Kienesberger, P. C., Pulinilkunnil, T., Nagendran, J., Young, M. E., Bogner-Strauss, J. G., Hackl, H., Khadour, R., Heydari, E., Haemmerle, G., Zechner, R., Kershaw, E. E., and Dyck, J. R. (2013) Early structural and metabolic cardiac remodelling in response to inducible adipose triglyceride lipase ablation. Cardiovasc. Res. 99, 442-451
21. Lass, A., Zimmermann, R., Haemmerle, G., Riederer, M., Schoiswohl, G., Schweiger, M., Kienesberger, P., Strauss, J. G., Gorkiewicz, G., and Zechner, R. (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
22. Radner, F. P., Streith, I. E., Schoiswohl, G., Schweiger, M., Kumari, M., Eichmann, T. O., Rechberger, G., Koefeler, H. C., Eder, S., Schauer, S., Theussl, H. C., Preiss-Landl, K., Lass, A., Zimmermann, R., Hoefler, G., Zechner, R., and Haemmerle, G. (2010) Growth retardation, impaired triacylglycerol catabolism, hepatic steatosis, and lethal skin barrier defect in mice lacking comparative gene identification-58 (CGI-58). J. Biol. Chem. 285, 7300-7311
23. Zierler, K. A., Jaeger, D., Pollak, N. M., Eder, S., Rechberger, G. N., Radner, F. P., Woelkart, G., Kolb, D., Schmidt, A., Kumari, M., Preiss-Landl, K., Pieske, B., Mayer, B., Zimmermann, R., Lass, A., Zechner, R., and Haemmerle, G. (2013) Functional cardiac lipolysis in mice critically depends on comparative gene identification-58. J. Biol. Chem. 288, 9892-9904
24. Yang, X., Lu, X., Lombès, M., Rha, G. B., Chi, Y. I., Guerin, T. M., Smart, E. J., and Liu, J. (2010) The G0/G1 switch gene 2 regulates adipose lipolysis through association with adipose triglyceride lipase. Cell. Metab. 11, 194-205
25. Russell, L., and Forsdyke, D. R. (1991) A human putative lymphocyte G0/G1 switch gene containing a CpG-rich island encodes a small basic protein with the potential to be phosphorylated. DNA Cell Biol. 10, 581-591
26. Kioka, H., Kato, H., Fujikawa, M., Tsukamoto, O., Suzuki, T., Imamura, H., Nakano, A., Higo, S., Yamazaki, S., Matsuzaki, T., Takafuji, K., Asanuma, H., Asakura, M., Minamino, T., Shintani, Y., Yoshida, M., Noji, H., Kitakaze, M., Komuro, I., Asano, Y., and Takashima, S. (2014) Evaluation of intramitochondrial ATP levels identifies G0/G1 switch gene 2 as a positive regulator of oxidative phosphorylation. Proc. Natl. Acad. Sci. U. S. A. 111, 273-278
27. Yamada, T., Park, C. S., Shen, Y., Rabin, K. R., and Lacorazza, H. D. (2014) G0S2 inhibits the proliferation of K562 cells by interacting with nucleolin in the cytosol. Leuk. Res. 38, 210-217
28. Welch, C., Santra, M. K., El-Assaad, W., Zhu, X., Huber, W. E., Keys, R. A., Teodoro, J. G., and Green, M. R. (2009) Identification of a protein, G0S2, that lacks Bcl-2 homology domains and interacts with and antagonizes Bcl-2. Cancer Res. 69, 6782-6789
29. Zhang, X., Xie, X., Heckmann, B. L., Saarinen, A. M., Czyzyk, T. A., and Liu, J. (2014) Targeted disruption of G0/G1 switch gene 2 enhances adipose lipolysis, alters hepatic energy balance, and alleviates high-fat dietinduced liver steatosis. Diabetes 63, 934-946
30. Heckmann, B. L., Zhang, X., Xie, X., Saarinen, A., Lu, X., Yang, X., and Liu, J. (2014) Defective adipose lipolysis and altered global energy metabolism in mice with adipose overexpression of the lipolytic inhibitor G0/G1 switch gene 2 (G0S2). J. Biol. Chem. 289, 1905-1916
31. Kienesberger, P. C., Pulinilkunnil, T., Sung, M. M., Nagendran, J., Haemmerle, G., Kershaw, E. E., Young, M. E., Light, P. E., Oudit, G. Y., Zechner, R., and Dyck, J. R. (2012) Myocardial ATGL overexpression decreases the reliance on fatty acid oxidation and protects against pressure overloadinduced cardiac dysfunction. Mol. Cell. Biol. 32, 740-750
32. Folch, J., Lees, M., and Sloane Stanley, G. H. (1957) A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497-509
33. Gruber, A., Cornaciu, I., Lass, A., Schweiger, M., Poeschl, M., Eder, C., Kumari, M., Schoiswohl, G., Wolinski, H., Kohlwein, S. D., Zechner, R., Zimmermann, R., and Oberer, M. (2010) The N-terminal region of comparative gene identification-58 (CGI-58) is important for lipid droplet binding and activation of adipose triglyceride lipase. J. Biol. Chem. 285, 12289-12298
34. Schweiger, M., Paar, M., Eder, C., Brandis, J., Moser, E., Gorkiewicz, G., Grond, S., Radner, F. P., Cerk, I., Cornaciu, I., Oberer, M., Kersten, S., Zechner, R., Zimmermann, R., and Lass, A. (2012) G0/G1 switch gene-2 regulates human adipocyte lipolysis by affecting activity and localization of adipose triglyceride lipase. J. Lipid Res. 53, 2307-2317
35. Mayer, N., Schweiger, M., Romauch, M., Grabner, G. F., Eichmann, T. O., Fuchs, E., Ivkovic, J., Heier, C., Mrak, I., Lass, A., Höfler, G., Fledelius, C., Zechner, R., Zimmermann, R., and Breinbauer, R. (2013) Development of small-molecule inhibitors targeting adipose triglyceride lipase. Nat. Chem. Biol. 9, 785-787
36. Moustafa, T., Fickert, P., Magnes, C., Guelly, C., Thueringer, A., Frank, S., Kratky, D., Sattler, W., Reicher, H., Sinner, F., Gumhold, J., Silbert, D., Fauler, G., Höfler, G., Lass, A., Zechner, R., and Trauner, M. (2012) Alterations in lipid metabolism mediate inflammation, fibrosis, and proliferation in a mouse model of chronic cholestatic liver injury. Gastroenterology 142, 140-151.e12
37. Zandbergen, F., Mandard, S., Escher, P., Tan, N. S., Patsouris, D., Jatkoe, T., Rojas-Caro, S., Madore, S., Wahli, W., Tafuri, S., Müller, M., and Kersten, S. (2005) The G0/G1 switch gene 2 is a novel PPAR target gene. Biochem. J. 392, 313-324
38. Ma, L., Robinson, L. N., and Towle, H. C. (2006) ChREBP·Mlx is the principal mediator of glucose-induced gene expression in the liver. J. Biol. Chem. 281, 28721-28730