The interplay of protein kinase a and Perilipin 5 regulates cardiac lipolysis

Journal of Biological Chemistry

Volumn 290, Issue 3, 2015, Pages 1295-1306

  Pollak, Nina M ^a   Jaeger, Doris ^a   Kolleritsch, Stephanie ^a   Zimmermann, Robert ^a   Zechner, Rudolf ^a   Lass, Achim ^a   Haemmerle, Guenter ^a  

^a UNIVERSITY OF GRAZ   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ENZYMES; FATTY ACIDS; MAMMALS; METABOLISM; PHOSPHORYLATION; PROTEINS;

ADENYLYL CYCLASE; BARRIER FUNCTIONS; CARDIAC MUSCLES; ENERGY METABOLISM; HEART DYSFUNCTION; PHOSPHORYLATION SITES; PROTEIN KINASE A; TRANSFECTED CELLS;

HEART;

CYCLIC AMP DEPENDENT PROTEIN KINASE; PERILIPIN; PERILIPIN 5; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; INSULIN; LIPID; LIPID STORAGE DROPLET PROTEIN 5, MOUSE; MUSCLE PROTEIN; SIGNAL PEPTIDE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENERGY METABOLISM; ENZYME PHOSPHORYLATION; FATTY ACID OXIDATION; GLUCOSE HOMEOSTASIS; HEART MUSCLE METABOLISM; LIPOLYSIS; METABOLIC REGULATION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL; C57BL MOUSE; CHEMISTRY; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; GLUCOSE TOLERANCE TEST; HEART; HEART DISEASE; LIPID METABOLISM; METABOLISM; MITOCHONDRION; MUTATION; PHOSPHORYLATION; PHYSIOLOGY; TRANSGENIC MOUSE;

MUS; MUS MUSCULUS;

ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCOSE TOLERANCE TEST; HEART; HEART DISEASES; INSULIN; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPID METABOLISM; LIPIDS; LIPOLYSIS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOCHONDRIA; MUSCLE PROTEINS; MUTATION; PHOSPHORYLATION; TRANSFECTION;

EID: 84922269099     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.604744     Document Type: Article

References (39)

1. Bickel, P. E., Tansey, J. T., and Welte, M. A. (2009) PAT proteins, an ancient family of lipid droplet proteins that regulate cellular lipid stores. Biochim. Biophys. Acta 1791, 419-440
2. Kühnlein, R. P. (2012) Thematic review series: Lipid droplet synthesis and metabolism: from yeast to man. Lipid droplet-based storage fat metabolism in Drosophila. J. Lipid Res. 53, 1430-1436
3. Brasaemle, D. L. (2007) Thematic review series: adipocyte biology. The perilipin family of structural lipid droplet proteins: stabilization of lipid droplets and control of lipolysis. J. Lipid Res. 48, 2547-2559
4. Konige, M., Wang, H., and Sztalryd, C. (2014) Role of adipose-specific lipid droplet proteins in maintaining whole body energy homeostasis. Biochim. Biophys. Acta 1842, 393-401
5. Zechner, R., Zimmermann, R., Eichmann, T. O., Kohlwein, S. D., Haemmerle, G., Lass, A., and Madeo, F. (2012) Fat signals-lipases and lipolysis in lipid metabolism and signaling. Cell Metab. 15, 279-291
6. Schaffer, J. E. (2003) Lipotoxicity: when tissues overeat. Curr. Opin. Lipidol. 14, 281-287
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 triacylglyceride-derived fatty acids in heart is augmented by the nuclear receptor PPARα. Circ. Res. 107, 233-241
8. 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
9. Wang, C., Zhao, Y., Gao, X., Li, L., Yuan, Y., Liu, F., Zhang, L., Wu, J., Hu, P., Zhang, X., Gu, Y., Xu, Y., Li, Z., Zhang, H., and Ye, J. (2014) Perilipin 5 improves hepatic lipotoxicity by inhibiting lipolysis. Hepatology 10.1002/hep.27409
10. Egan, J. J., Greenberg, A. S., Chang, M. K., and Londos, C. (1990) Control of endogenous phosphorylation of the major cAMP-dependent protein kinase substrate in adipocytes by insulin and β-adrenergic stimulation. J. Biol. Chem. 265, 18769-18775
11. Miyoshi, H., Perfield, J. W., 2nd, Souza, S. C., Shen, W.-J., Zhang, H.-H., Stancheva, Z. S., Kraemer, F. B., Obin, M. S., and Greenberg, A. S. (2007) Control of adipose triglyceride lipase action by serine 517 of perilipin A globally regulates protein kinase A-stimulated lipolysis in adipocytes. J. Biol. Chem. 282, 996-1002
12. Granneman, J. G., Moore, H.-P., Krishnamoorthy, R., and Rathod, M. (2009) Perilipin controls lipolysis by regulating the interactions of ABhydrolase containing 5 (Abhd5) and adipose triglyceride lipase (Atgl). J. Biol. Chem. 284, 34538-34544
13. Subramanian, V., Rothenberg, A., Gomez, C., Cohen, A. W., Garcia, A., Bhattacharyya, S., Shapiro, L., Dolios, G., Wang, R., Lisanti, M. P., and Brasaemle, D. L. (2004) Perilipin A mediates the reversible binding of CGI-58 to lipid droplets in 3T3-L1 adipocytes. J. Biol. Chem. 279, 42062-42071
14. Yamaguchi, T., Omatsu, N., Matsushita, S., and Osumi, T. (2004) CGI-58 interacts with perilipin and is localized to lipid droplets. Possible involvement of CGI-58 mislocalization in Chanarin-Dorfman syndrome. J. Biol. Chem. 279, 30490-30497
15. Kimmel, A. R., and Sztalryd, C. (2014) Perilipin 5, a lipid droplet protein adapted to mitochondrial energy utilization. Curr. Opin. Lipidol. 25, 110-117
16. Wolins, N. E., Quaynor, B. K., Skinner, J. R., Tzekov, A., Croce, M. A., Gropler, M. C., Varma, V., Yao-Borengasser, A., Rasouli, N., Kern, P. A., Finck, B. N., and Bickel, P. E. (2006) OXPAT/PAT-1 is a PPAR-induced lipid droplet protein that promotes fatty acid utilization. Diabetes 55, 3418-3428
17. Yamaguchi, T., Matsushita, S., Motojima, K., Hirose, F., and Osumi, T. (2006) MLDP, a novel PAT family protein localized to lipid droplets and enriched in the heart, is regulated by peroxisome proliferator-activated receptor α. J. Biol. Chem. 281, 14232-14240
18. Dalen, K. T., Dahl, T., Holter, E., Arntsen, B., Londos, C., Sztalryd, C., and Nebb, H. I. (2007) LSDP5 is a PAT protein specifically expressed in fatty acid oxidizing tissues. Biochim. Biophys. Acta 1771, 210-227
19. Granneman, J. G., Moore, H.-P., Mottillo, E. P., and Zhu, Z. (2009) Functional interactions between Mldp (LSDP5) and Abhd5 in the control of intracellular lipid accumulation. J. Biol. Chem. 284, 3049-3057
20. Wang, H., Hu, L., Dalen, K., Dorward, H., Marcinkiewicz, A., Russell, D., Gong, D., Londos, C., Yamaguchi, T., Holm, C., Rizzo, M. A., Brasaemle, D., and Sztalryd, C. (2009) Activation of hormone-sensitive lipase requires two steps, protein phosphorylation and binding to the PAT-1 domain of lipid droplet coat proteins. J. Biol. Chem. 284, 32116-32125
21. Wang, H., Bell, M., Sreenivasan, U., Sreenevasan, U., Hu, H., Liu, J., Dalen, K., Londos, C., Yamaguchi, T., Rizzo, M. A., Coleman, R., Gong, D., Brasaemle, D., and Sztalryd, C. (2011) Unique regulation of adipose triglyceride lipase (ATGL) by perilipin 5, a lipid droplet-associated protein. J. Biol. Chem. 286, 15707-15715
22. Macpherson, R. E., Vandenboom, R., Roy, B. D., and Peters, S. J. (2013) Skeletal muscle PLIN3 and PLIN5 are serine phosphorylated at rest and following lipolysis during adrenergic or contractile stimulation. Physiol. Rep. 1, e00084
23. Mason, R. R., Mokhtar, R., Matzaris, M., Selathurai, A., Kowalski, G. M., Mokbel, N., Meikle, P. J., Bruce, C. R., and Watt, M. J. (2014) PLIN5 deletion remodels intracellular lipid composition and causes insulin resistance in muscle. Mol. Metab. 3, 652-663
24. Kuramoto, K., Okamura, T., Yamaguchi, T., Nakamura, T. Y., Wakabayashi, S., Morinaga, H., Nomura, M., Yanase, T., Otsu, K., Usuda, N., Matsumura, S., Inoue, K., Fushiki, T., Kojima, Y., Hashimoto, T., Sakai, F., Hirose, F., and Osumi, T. (2012) Perilipin 5, a lipid droplet-binding protein, protects heart from oxidative burden by sequestering fatty acid from excessive oxidation. J. Biol. Chem. 287, 23852-23863
25. Wang, H., Sreenivasan, U., Gong, D.-W., O'Connell, K. A., Dabkowski, E. R., Hecker, P. A., Ionica, N., Konig, M., Mahurkar, A., Sun, Y., Stanley, W. C., and Sztalryd, C. (2013) Cardiomyocyte-specific perilipin 5 overexpression leads to myocardial steatosis and modest cardiac dysfunction. J. Lipid Res. 54, 953-965
26. Pollak, N. M., Schweiger, M., Jaeger, D., Kolb, D., Kumari, M., Schreiber, R., Kolleritsch, S., Markolin, P., Grabner, G. F., Heier, C., Zierler, K. A., Rülicke, T., Zimmermann, R., Lass, A., Zechner, R., and Haemmerle, G. (2013) Cardiac-specific overexpression of perilipin 5 provokes severe cardiac steatosis via the formation of a lipolytic barrier. J. Lipid Res. 54, 1092-1102
27. 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
28. Folch, J., Lees, M., and Sloane Stanley, G. H. (1957) A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226, 497-509
29. 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
30. Hirschey, M. D., Shimazu, T., Goetzman, E., Jing, E., Schwer, B., Lombard, D. B., Grueter, C. A., Harris, C., Biddinger, S., Ilkayeva, O. R., Stevens, R. D., Li, Y., Saha, A. K., Ruderman, N. B., Bain, J. R., Newgard, C. B., Farese, R. V., Jr., Alt, F. W., Kahn, C. R., and Verdin, E. (2010) SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 464, 121-125
31. Amthor, H., Macharia, R., Navarrete, R., Schuelke, M., Brown, S. C., Otto, A., Voit, T., Muntoni, F., Vrbóva, G., Partridge, T., Zammit, P., Bunger, L., and Patel, K. (2007) Lack of myostatin results in excessive muscle growth but impaired force generation. Proc. Natl. Acad. Sci. U.S.A. 104, 1835-1840
32. 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
33. Yamaguchi, T., Omatsu, N., Omukae, A., and Osumi, T. (2006) Analysis of interaction partners for perilipin and ADRP on lipid droplets. Mol. Cell. Biochem. 284, 167-173
34. Chang, B. H., Li, L., Paul, A., Taniguchi, S., Nannegari, V., Heird, W. C., and Chan, L. (2006) Protection against fatty liver but normal adipogenesis in mice lacking adipose differentiation-related protein. Mol. Cell. Biol. 26, 1063-1076
35. Bosma, M., Hesselink, M. K., Sparks, L. M., Timmers, S., Ferraz, M. J., Mattijssen, F., van Beurden, D., Schaart, G., de Baets, M. H., Verheyen, F. K., Kersten, S., and Schrauwen, P. (2012) Perilipin 2 improves insulin sensitivity in skeletal muscle despite elevated intramuscular lipid levels. Diabetes 61, 2679-2690
36. McManaman, J. L., Bales, E. S., Orlicky, D. J., Jackman, M., MacLean, P. S., Cain, S., Crunk, A. E., Mansur, A., Graham, C. E., Bowman, T. A., and Greenberg, A. S. (2013) Perilipin-2-null mice are protected against dietinduced obesity, adipose inflammation, and fatty liver disease. J. Lipid Res. 54, 1346-1359
37. Wang, H., Sreenivasan, U., Sreenevasan, U., Hu, H., Saladino, A., Polster, B. M., Lund, L. M., Gong, D. W., Stanley, W. C., and Sztalryd, C. (2011) Perilipin 5, a lipid droplet-associated protein, provides physical and metabolic linkage to mitochondria. J. Lipid Res. 52, 2159-2168
38. Bosma, M., Minnaard, R., Sparks, L. M., Schaart, G., Losen, M., de Baets, M. H., Duimel, H., Kersten, S., Bickel, P. E., Schrauwen, P., and Hesselink, M. K. (2012) The lipid droplet coat protein perilipin 5 also localizes to muscle mitochondria. Histochem. Cell Biol. 137, 205-216
39. 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