Active involvement of micro-lipid droplets and lipiddroplet-associated proteins in hormone-stimulated lipolysis in adipocytes

Journal of Cell Science

Volumn 125, Issue 24, 2012, Pages 6127-6136

  Hashimoto, Takeshi ^a,b   Segawa, Hiroki ^c   Okuno, Masanari ^c   Kano, Hideaki ^c,d   Hamaguchi, Hiro o ^c   Haraguchi, Tokuko ^e,f   Hiraoka, Yasushi ^e,f   Hasui, Shiho ^b   Yamaguchi, Tomohiro ^b,g   Hirose, Fumiko ^b   Osumi, Takashi ^b  

^a RITSUMEIKAN UNIVERSITY   (Japan)

^b UNIVERSITY OF HYOGO   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d UNIVERSITY OF TSUKUBA   (Japan)

^e OSAKA UNIVERSITY   (Japan)

^f NATIONAL INSTITUTE OF INFORMATION AND COMMUNICATIONS TECHNOLOGY   (Japan)

^g SHOWA UNIVERSITY   (Japan)

Author keywords

CARS microscopy; Fatty acid; Lipid droplet; Lipid metabolism; Lipolysis

Indexed keywords

ADIPOSE TRIGLYCERIDE LIPASE; BROMOENOL LACTONE; CGI 58; FAT DROPLET; FATTY ACID; GLYCEROL; GLYCEROL KINASE; GLYCEROPHOSPHATE; GREEN FLUORESCENT PROTEIN; HORMONE SENSITIVE LIPASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PERILIPIN; PROTEIN; UNCLASSIFIED DRUG; CHOLESTEROL ESTERASE; TRIACYLGLYCEROL LIPASE;

ADIPOCYTE; ARTICLE; CONTROLLED STUDY; COVALENT BOND; CYTOPLASM; ENZYME ACTIVITY; ESTERIFICATION; IN VIVO STUDY; LIPOGENESIS; LIPOLYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAMAN SPECTROMETRY; 3T3 CELL LINE; ANIMAL; CULTURE TECHNIQUE; CYTOLOGY; FLUORESCENCE MICROSCOPY; LIPID METABOLISM; LIQUID PHASE MICROEXTRACTION; METABOLISM; MOUSE;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; CELL CULTURE TECHNIQUES; LIPASE; LIPID METABOLISM; LIPOLYSIS; LIQUID PHASE MICROEXTRACTION; MICE; MICROSCOPY, FLUORESCENCE; STEROL ESTERASE;

EID: 84875597610     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.113084     Document Type: Article

References (40)

1. Ariotti, N., Murphy, S., Hamilton, N. A., Wu, L., Green, K., Schieber, N. L., Li, P., Martin, S. and Parton, R. G. (2012). Postlipolytic insulin-dependent remodeling of micro lipid droplets in adipocytes. Mol. Biol. Cell 23, 1826-1837.
2. Blanchette-Mackie, E. J., Dwyer, N. K., Barber, T., Coxey, R. A., Takeda, T., Rondinone, C. M., Theodorakis, J. L., Greenberg, A. S. and Londos, C. (1995). Perilipin is located on the surface layer of intracellular lipid droplets in adipocytes. J. Lipid Res. 36, 1211-1226.
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. Brasaemle, D. L. (2011). DisseCCTing phospholipid function in lipid droplet dynamics. Cell Metab. 14, 437-438.
5. Brasaemle, D. L. and Wolins, N. E. (2012). Packaging of fat: an evolving model of lipid droplet assembly and expansion. J. Biol. Chem. 287, 2273-2279.
6. Brasaemle, D. L., Dolios, G., Shapiro, L. and Wang, R. (2004). Proteomic analysis of proteins associated with lipid droplets of basal and lipolytically stimulated 3T3-L1 adipocytes. J. Biol. Chem. 279, 46835-46842.
7. Evans, C. L. and Xie, X. S. (2008). Coherent anti-stokes Raman scattering microscopy: chemical imaging for biology and medicine. Annu Rev. Anal. Chem (Palo Alto Calif) 1, 883-909.
8. Farese, R. V., Jr and Walther, T. C. (2009). Lipid droplets finally get a little R-E-S-P-E-C-T. Cell 139, 855-860.
9. Fumoto, T., Yamaguchi, T., Hirose, F. and Osumi, T. (2007). Orphan nuclear receptor Nur77 accelerates the initial phase of adipocyte differentiation in 3T3-L1 cells by promoting mitotic clonal expansion. J. Biochem. 141, 181-192.
10. Gaidhu, M. P., Fediuc, S., Anthony, N. M., So, M., Mirpourian, M., Perry, R. L. and Ceddia, R. B. (2009). Prolonged AICAR-induced AMP-kinase activation promotes energy dissipation in white adipocytes: novel mechanisms integrating HSL and ATGL. J. Lipid Res. 50, 704-715.
11. Ghosh, A. K., Ramakrishnan, G., Chandramohan, C. and Rajasekharan, R. (2008). CGI-58, the causative gene for Chanarin-Dorfman syndrome, mediates acylation of lysophosphatidic acid. J. Biol. Chem. 283, 24525-24533.
12. Granneman, J. G. and Moore, H. P. (2008). Location, location: protein trafficking and lipolysis in adipocytes. Trends Endocrinol. Metab. 19, 3-9.
13. Granneman, J. G., Moore, H. P., Granneman, R. L., Greenberg, A. S., Obin, M. S. and Zhu, Z. (2007). Analysis of lipolytic protein trafficking and interactions in adipocytes. J. Biol. Chem. 282, 5726-5735.
14. Granneman, J. G., Moore, H. P., Krishnamoorthy, R. and Rathod, M. (2009). Perilipin controls lipolysis by regulating the interactions of AB-hydrolase containing 5 (Abhd5) and adipose triglyceride lipase (Atgl). J. Biol. Chem. 284, 34538-34544.
15. Guo, Y., Walther, T. C., Rao, M., Stuurman, N., Goshima, G., Terayama, K., Wong, J. S., Vale, R. D., Walter, P. and Farese, R. V. (2008). Functional genomic screen reveals genes involved in lipid-droplet formation and utilization. Nature 453, 657-661.
16. Haraguchi, T., Ding, D. Q., Yamamoto, A., Kaneda, T., Koujin, T. and Hiraoka, Y. (1999). Multiple-color fluorescence imaging of chromosomes and microtubules in living cells. Cell Struct. Funct. 24, 291-298.
17. Leroyer, S. N., Tordjman, J., Chauvet, G., Quette, J., Chapron, C., Forest, C. and Antoine, B. (2006). Rosiglitazone controls fatty acid cycling in human adipose tissue by means of glyceroneogenesis and glycerol phosphorylation. J. Biol. Chem. 281, 13141-13149.
18. Liu, P., Ying, Y., Zhao, Y., Mundy, D. I., Zhu, M. and Anderson, R. G. (2004). Chinese hamster ovary K2 cell lipid droplets appear to be metabolic organelles involved in membrane traffic. J. Biol. Chem. 279, 3787-3792.
19. Marcinkiewicz, A., Gauthier, D., Garcia, A. and Brasaemle, D. L. (2006). The phosphorylation of serine 492 of perilipin A directs lipid droplet fragmentation and dispersion. J. Biol. Chem. 281, 11901-11909.
20. Miyoshi, H., Souza, S. C., Zhang, H. H., Strissel, K. J., Christoffolete, M. A., Kovsan, J., Rudich, A., Kraemer, F. B., Bianco, A. C., Obin, M. S. et al. (2006). Perilipin promotes hormone-sensitive lipase-mediated adipocyte lipolysis via phosphorylation-dependent and -independent mechanisms. J. Biol. Chem. 281, 15837-15844.
21. 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.
22. Miyoshi, H., Perfield, J. W., 2nd, Obin, M. S. and Greenberg, A. S. (2008). Adipose triglyceride lipase regulates basal lipolysis and lipid droplet size in adipocytes. J. Cell. Biochem. 105, 1430-1436.
23. Montero-Moran, G., Caviglia, J. M., McMahon, D., Rothenberg, A., Subramanian, V., Xu, Z., Lara-Gonzalez, S., Storch, J., Carman, G. M. and Brasaemle, D. L. (2010). CGI-58/ABHD5 is a coenzyme A-dependent lysophosphatidic acid acyltransferase. J. Lipid Res. 51, 709-719.
24. Moore, H. P., Silver, R. B., Mottillo, E. P., Bernlohr, D. A. and Granneman, J. G. (2005). Perilipin targets a novel pool of lipid droplets for lipolytic attack by hormonesensitive lipase. J. Biol. Chem. 280, 43109-43120.
25. Ohsaki, Y., Cheng, J., Suzuki, M., Shinohara, Y., Fujita, A. and Fujimoto, T. (2009). Biogenesis of cytoplasmic lipid droplets: from the lipid ester globule in the membrane to the visible structure. Biochim. Biophys. Acta 1791, 399-407.
26. Okuno, M., Kano, H., Leproux, P., Couderc, V., Day, J. P., Bonn, M. and Hamaguchi, H. O. (2010). Quantitative CARS molecular fingerprinting of single living cells with the use of the maximum entropy method. Angew. Chem. Int. Ed. Engl. 49, 6773-6777.
27. Paar, M., Jüngst, C., Steiner, N. A., Magnes, C., Sinner, F., Kolb, D., Lass, A., Zimmermann, R., Zumbusch, A., Kohlwein, S. D. et al. (2012). Remodeling of lipid droplets during lipolysis and growth in adipocytes. J. Biol. Chem. 287, 11164-11173.
28. Reshef, L., Olswang, Y., Cassuto, H., Blum, B., Croniger, C. M., Kalhan, S. C., Tilghman, S. M. and Hanson, R. W. (2003). Glyceroneogenesis and the triglyceride/ fatty acid cycle. J. Biol. Chem. 278, 30413-30416.
29. Ruderman, N. B., Park, H., Kaushik, V. K., Dean, D., Constant, S., Prentki, M. and Saha, A. K. (2003a). AMPK as a metabolic switch in rat muscle, liver and adipose tissue after exercise. Acta Physiol. Scand. 178, 435-442.
30. Ruderman, N. B., Saha, A. K. and Kraegen, E. W. (2003b). Minireview: malonyl CoA, AMP-activated protein kinase, and adiposity. Endocrinology 144, 5166-5171.
31. Schmidt, J. A. and Brown, W. J. (2009). Lysophosphatidic acid acyltransferase 3 regulates Golgi complex structure and function. J. Cell Biol. 186, 211-218.
32. Shen, W. J., Patel, S., Miyoshi, H., Greenberg, A. S. and Kraemer, F. B. (2009). Functional interaction of hormone-sensitive lipase and perilipin in lipolysis. J. Lipid Res. 50, 2306-2313.
33. Wang, H., Bell, M., Sreenevasan, U., Hu, H., Liu, J., Dalen, K., Londos, C., Yamaguchi, T., Rizzo, M. A., Coleman, R. et al. (2011). Unique regulation of adipose triglyceride lipase (ATGL) by perilipin 5, a lipid droplet-associated protein. J. Biol. Chem. 286, 15707-15715.
34. Yamaguchi, T. (2010). Crucial role of CGI-58/a/b hydrolase domain-containing protein 5 in lipid metabolism. Biol. Pharm. Bull. 33, 342-345.
35. 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.
36. Yamaguchi, T., Omatsu, N., Morimoto, E., Nakashima, H., Ueno, K., Tanaka, T., Satouchi, K., Hirose, F. and Osumi, T. (2007). CGI-58 facilitates lipolysis on lipid droplets but is not involved in the vesiculation of lipid droplets caused by hormonal stimulation. J. Lipid Res. 48, 1078-1089.
37. Yamasaki, M., Hashiguchi, N., Fujiwara, C., Imanaka, T., Tsukamoto, T. and Osumi, T. (1999). Formation of peroxisomes from peroxisomal ghosts in a peroxisome-deficient mammalian cell mutant upon complementation by protein microinjection. J. Biol. Chem. 274, 35293-35296.
38. Yamashita, D., Yamaguchi, T., Shimizu, M., Nakata, N., Hirose, F. and Osumi, T. (2004). The transactivating function of peroxisome proliferator-activated receptor c is negatively regulated by SUMO conjugation in the amino-terminal domain. Genes Cells 9, 1017-1029.
39. Yamashita, D., Sano, Y., Adachi, Y., Okamoto, Y., Osada, H., Takahashi, T., Yamaguchi, T., Osumi, T. and Hirose, F. (2007). hDREF regulates cell proliferation and expression of ribosomal protein genes. Mol. Cell. Biol. 27, 2003-2013.
40. Zechner, R., Kienesberger, P. C., Haemmerle, G., Zimmermann, R. and Lass, A. (2009). Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores. J. Lipid Res. 50, 3-21.