Distinct roles of the phosphatidate phosphatases lipin 1 and 2 during adipogenesis and lipid droplet biogenesis in 3T3-L1 cells

Journal of Biological Chemistry

Volumn 288, Issue 48, 2013, Pages 34502-34513

  Sembongi, Hiroshi ^a   Miranda, Merce ^b   Han, Gil Soo ^c   Fakas, Stylianos ^c   Grimsey, Neil ^a,d   Vendrell, Joan ^b   Carman, George M ^c   Siniossoglou, Symeon ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b INSTITUT D INVESTIGACIÓ SANITÀRIA PERE VIRGILI IISPV   (Spain)

^c RUTGERS UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVITY LEVELS; ADIPOCYTES; ADIPOGENESIS; LIPID BIOSYNTHESIS; LIPID DROPLETS; TRIACYLGLYCEROLS;

BIOCHEMISTRY; BIOSYNTHESIS; CELLS; CYTOLOGY; DROPS; GLYCEROL; LIPIDS; MAMMALS; PHOSPHATASES;

LOADING;

FAT DROPLET; LIPIN 1; LIPIN 2; PHOSPHATIDATE PHOSPHATASE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE; ANIMAL CELL; ARTICLE; BIOGENESIS; CELL DIFFERENTIATION; CELL FUNCTION; CELL STRAIN 3T3; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; FLOW CYTOMETRY; FRACTIONATION; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; WESTERN BLOTTING;

EID: 84889040528     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.488445     Document Type: Article

References (41)

1. Han, G.-S., Wu, W.-I., and Carman, G. M. (2006) The Saccharomyces cerevisiae Lipin homolog is a Mg2+-dependent phosphatidate phosphatase enzyme. J. Biol. Chem. 281, 9210-9218
2. Donkor, J., Sariahmetoglu, M., Dewald, J., Brindley, D. N., and Reue, K. (2007) Three mammalian lipins act as phosphatidate phosphatases with distinct tissue expression patterns. J. Biol. Chem. 282, 3450-3457
3. Walther, T. C., and Farese, R. V., Jr. (2012) Lipid droplets and cellular lipid metabolism. Annu. Rev. Biochem. 81, 687-714
4. Lykidis, A., and Jackowski, S. (2001) Regulation of mammalian cell membrane biosynthesis. Prog. Nucleic Acid Res. Mol. Biol. 65, 361-393
5. Nadra, K., de Preux Charles, A. S., Médard, J. J., Hendriks, W. T., Han, G.-S., Grès, S., Carman, G. M., Saulnier-Blache, J. S., Verheijen, M. H., and Chrast, R. (2008) Phosphatidic acid mediates demyelination in Lpin1 mutant mice. Genes Dev. 22, 1647-1661
6. Brindley, D. N., Pilquil, C., Sariahmetoglu, M., and Reue, K. (2009) Phosphatidate degradation. Phosphatidate phosphatases (lipins) and lipid phosphate phosphatases. Biochim. Biophys. Acta. 1791, 956-961
7. Finck, B. N., Gropler, M. C., Chen, Z., Leone, T. C., Croce, M. A., Harris, T. E., Lawrence, J. C., Jr., and Kelly, D. P. (2006) Lipin 1 is an inducible amplifier of the hepatic PGC-1α/PPARγ regulatory pathway. Cell. Metab. 4, 199-210
8. Koh, Y. K., Lee, M. Y., Kim, J. W., Kim, M., Moon, J. S., Lee, Y. J., Ahn, Y. H., and Kim, K. S. (2008) Lipin1 is a key factor for the maturation and maintenance of adipocytes in the regulatory network with CCAAT/enhancerbinding protein α and peroxisome proliferator-activated receptor γ2. J. Biol. Chem. 283, 34896-34906
9. Liu, G. H., and Gerace, L. (2009) Sumoylation regulates nuclear localization of lipin-1α in neuronal cells. PLoS One 4, e7031
10. Kim, H. B., Kumar, A., Wang, L., Liu, G. H., Keller, S. R., Lawrence, J. C., Jr., Finck, B. N., and Harris, T. E. (2010) Lipin 1 represses NFATc4 transcriptional activity in adipocytes to inhibit secretion of inflammatory factors. Mol. Cell. Biol. 30, 3126-3139
11. Peterson, T. R., Sengupta, S. S., Harris, T. E., Carmack, A. E., Kang, S. A., Balderas, E., Guertin, D. A., Madden, K. L., Carpenter, A. E., Finck, B. N., and Sabatini, D. M. (2011) mTOR complex 1 regulates lipin 1 localization to control the SREBP pathway. Cell 146, 408-420
12. Brindley, D. N. (2004) Lipid phosphate phosphatases and related proteins. Signaling functions in development, cell division, and cancer. J. Cell. Biochem. 92, 900-912
13. Péterfy, M., Phan, J., Xu, P., and Reue, K. (2001) Lipodystrophy in the fld mouse results from mutation of a new gene encoding a nuclear protein, lipin. Nat. Genet. 27, 121-124
14. Péterfy, M., Phan, J., and Reue, K. (2005) Alternatively spliced lipin isoforms exhibit distinct expression pattern, subcellular localization, and role in adipogenesis. J. Biol. Chem. 280, 32883-32889
15. Wang, H., Zhang, J., Qiu, W., Han, G.-H., Carman, G. M., and Adeli, K. (2011) Lipin-1Α isoform is a novel lipid droplet-associated protein highly expressed in the brain. FEBS Lett. 585, 1979-1984
16. Bou Khalil, M., Sundaram, M., Zhang, H. Y., Links, P. H., Raven, J. F., Manmontri, B., Sariahmetoglu, M., Tran, K., Reue, K., Brindley, D. N., and Yao, Z. (2009) The level and compartmentalization of phosphatidate phosphatase-1 (lipin-1) control the assembly and secretion of hepatic VLDL. J. Lipid Res. 50, 47-58
17. Liu, G. H., and Gerace, L. (2009) Sumoylation regulates nuclear localization of lipin-1α in neuronal cells. PLoS One 4, e7031
18. Haller, J. F., Krawczyk, S. A., Gostilovitch, L., Corkey, B. E., and Zoeller, R. A. (2011) Glucose-6-phosphate isomerase deficiency results in mTOR activation, failed translocation of lipin 1α to the nucleus and hypersensitivity to glucose. Implications for the inherited glycolytic disease. Biochim. Biophys. Acta 1812, 1393-1402
19. Han G.-S., and Carman G. M. (2010) Characterization of the human LPIN1-encoded phosphatidate phosphatase isoforms. J. Biol. Chem. 285, 14628-14638
20. Mul, J. D., Nadra, K., Jagalur, N. B., Nijman, I. J., Toonen, P. W., Médard, J. J., Grès, S., de Bruin, A., Han, G.-S., Brouwers, J. F., Carman, G. M., Saulnier-Blache, J. S., Meijer, D., Chrast, R., and Cuppen, E. (2011) A hypomorphic mutation in Lpin1 induces progressively improving neuropathy and lipodystrophy in the rat. J. Biol. Chem. 286, 26781-26793
21. Phan, J., Péterfy, M., and Reue, K. (2004) Lipin expression preceding peroxisome proliferator-activated receptor-gamma is critical for adipogenesis in vivo and in vitro. J. Biol. Chem. 279, 29558-29564
22. Zhang, P., Takeuchi, K., Csaki, L. S., and Reue, K. (2012) Lipin-1 phosphatidic phosphatase activity modulates phosphatidate levels to promote peroxisome proliferator-activated receptor γ (PPARγ) gene expression during adipogenesis. J. Biol. Chem. 287, 3485-3494
23. Rochford, J. J., Semple, R. K., Laudes, M., Boyle, K. B., Christodoulides, C., Mulligan, C., Lelliott, C. J., Schinner, S., Hadaschik, D., Mahadevan, M., Sethi, J. K., Vidal-Puig, A., and O'Rahilly, S. (2004) ETO/MTG8 is an inhibitor of C/EBPbeta activity and a regulator of early adipogenesis. Mol. Cell. Biol. 24, 9863-9872
24. Grimsey, N., Han, G.-S., O'Hara, L., Rochford, J. J., Carman, G. M., and Siniossoglou, S. (2008) Temporal and spatial regulation of the phosphatidate phosphatases lipin 1 and 2. J. Biol. Chem. 283, 29166-29174
25. Swift, S., Lorens, J. B., Achacoso, P., and Nolan, G. P. (1999) Rapid production of retroviruses for efficient gene delivery to mammalian cells using 293T cellbased systems. In Current Protocols in Immunology (Coligan, J. E., Kruisbeek, A. M., Margulies, D. H., Shevach, E. M., and Strober, W., eds) Suppl. 31, Unit 10.17C, John Wiley & Sons Inc.
26. Nishino, N., Tamori, Y., Tateya, S., Kawaguchi, T., Shibakusa, T., Mizunoya, W., Inoue, K., Kitazawa, R., Kitazawa, S., Matsuki, Y., Hiramatsu, R., Masubuchi, S., Omachi, A., Kimura, K., Saito, M., Amo, T., Ohta, S., Yamaguchi, T., Osumi, T., Cheng, J., Fujimoto, T., Nakao, H., Nakao, K., Aiba, A., Okamura, H., Fushiki, T., and Kasuga, M. (2008) FSP27 contributes to efficient energy storage in murine white adipocytes by promoting the formation of unilocular lipid droplets. J. Clin. Invest. 118, 2808-2821
27. Morita, S. Y., Ueda, K., and Kitagawa, S. (2009) Enzymatic measurement of phosphatidic acid in cultured cells. J. Lipid Res. 50, 1945-1952
28. Bligh, E. G., and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917
29. Fakas, S., Qiu, Y., Dixon, J. L., Han, G.-S., Ruggles K. V., Garbarino, J., Sturley, S. L., and Carman, G. M. (2011) Phosphatidate phosphatase activity plays key role in protection against fatty acid-induced toxicity in yeast. J. Biol. Chem. 286, 29074-29085
30. Carman, G. M., and Lin, Y.-P. (1991) Phosphatidate phosphatase from yeast. Methods Enzymol. 197, 548-553
31. Adeyo O., Horn, P. J., Lee, S., Binns, D. D., Chandrahas, A., Chapman, K. D., and Goodman, J. M. (2011) The yeast lipin orthologue Pah1p is important for biogenesis of lipid droplets. J. Cell Biol. 192, 1043-1055
32. Brasaemle, D. L. (2007) The perilipin family of structural lipid droplet proteins. Stabilization of lipid droplets and control of lipolysis. J. Lipid Res. 48, 2547-2559
33. Keller, P., Petrie, J. T., De Rose, P., Gerin, I., Wright, W. S., Chiang, S. H., Nielsen, A. R., Fischer, C. P., Pedersen, B. K., and MacDougald, O. A. (2008) Fat-specific protein 27 regulates storage of triacylglycerol. J. Biol. Chem. 283, 14355-14365
34. Gropler, M. C., Harris, T. E., Hall, A. M., Wolins, N. E., Gross, R. W., Han, X., Chen, Z., and Finck, B. N. (2009) Lipin 2 is a liver-enriched phosphatidate phosphohydrolase enzyme that is dynamically regulated by fasting and obesity in mice. J. Biol. Chem. 284, 6763-6772
35. Dwyer, J. R., Donkor, J., Zhang, P., Csaki, L. S., Vergnes, L., Lee, J. M., Dewald, J., Brindley, D. N., Atti, E., Tetradis, S., Yoshinaga, Y., De Jong, P. J., Fong, L. G., Young, S. G., and Reue, K. (2012) Mouse lipin-1 and lipin-2 cooperate to maintain glycerolipid homeostasis in liver and aging cerebellum. Proc. Natl. Acad. Sci. U.S.A. 109, E2486-E2495
36. Wilfling, F., Wang, H., Haas, J. T., Krahmer, N., Gould, T. J., Uchida, A., Cheng, J. X., Graham, M., Christiano, R., Fröhlich, F., Liu, X., Buhman, K. K., Coleman, R. A., Bewersdorf, J., Farese, R. V., Jr., and Walther, T. C. (2013) Triacylglycerol synthesis enzymes mediate lipid droplet growth by relocalizing from the ER to lipid droplets. Dev. Cell. 24, 384-399
37. Valdearcos M., Esquinas, E., Meana, C., Gil-de-Gómez, L., Guijas, C., Balsinde, J., and Balboa, M. A. (2011) Subcellular localization and role of lipin- 1 in human macrophages. J. Immunol. 186, 6004-6013
38. Mylonis, I., Sembongi, H., Befani, C., Liakos, P., Siniossoglou, S., and Simos, G. (2012) Hypoxia causes triglyceride accumulation by HIF-1-mediated stimulation of lipin 1 expression. J. Cell Sci. 125, 3485-3493
39. Nadra K., Médard, J. J., Mul, J. D., Han, G.-S., Grès, S., Pende, M., Metzger, D., Chambon, P., Cuppen, E., Saulnier-Blache, J. S., Carman, G. M., Desvergne, B., and Chrast, R. (2012) Cell autonomous lipin 1 function is essential for development and maintenance of white and brown adipose tissue. Mol. Cell. Biol. 32, 4794-4810
40. Yang, H., Galea, A., Sytnyk, V., and Crossley, M. (2012) Controlling the size of lipid droplets. Lipid and protein factors. Curr. Opin. Cell Biol. 24, 509-516
41. Stapleton, C. M., Mashek, D. G., Wang, S., Nagle, C. A., Cline, G. W., Thuillier, P., Leesnitzer, L. M., Li, L. O., Stimmel, J. B., Shulman, G. I., and Coleman, R. A. (2011) Lysophosphatidic acid activates peroxisome proliferator activated receptor-γ in CHO cells that overexpress glycerol-3- phosphate acyltransferase-1. PLoS One 6, e18932