Fat-specific protein 27 (FSP27) interacts with adipose triglyceride lipase (ATGL) to regulate lipolysis and insulin sensitivity in human adipocytes

Journal of Biological Chemistry

Volumn 289, Issue 17, 2014, Pages 12029-12039

  Grahn, Tan Hooi Min ^a   Kaur, Rajween ^a   Yin, Jun ^a   Schweiger, Martina ^b   Sharma, Vishva Mitra ^a   Lee, Mi Jeong ^a   Ido, Yasuo ^a   Smas, Cynthia M ^c   Zechner, Rudolf ^b   Lass, Achim ^b   Puri, Vishwajeet ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF GRAZ   (Austria)

^c MEDICAL COLLEGE OF OHIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; INSULIN;

ADIPOCYTES; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN SIGNALING; LIPOLYTIC;

ENZYMES;

ADIPOSE TRIACYLGLYCEROL LIPASE; FAT SPECIFIC PROTEIN 27; PROTEIN KINASE B; REGULATOR PROTEIN; TRIACYLGLYCEROL; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; FIBROBLAST CULTURE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID STORAGE; LIPOLYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ADIPOCYTE; ADIPOSE TISSUE METABOLISM; ADIPOSE TRIGLYCERIDE LIPASE; DIABETES; DIACYLGLYCEROL; FATTY ACID; FATTY ACID METABOLISM; INSULIN RESISTANCE; OBESITY;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; HUMANS; INSULIN; INSULIN RESISTANCE; LIPASE; LIPOLYSIS; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; PROTEIN BINDING; PROTEINS; SIGNAL TRANSDUCTION; TRIGLYCERIDES;

EID: 84899428316     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.539890     Document Type: Article

References (62)

1. Unger, R. H., Clark, G. O., Scherer, P. E., and Orci, L. (2010) Lipid homeostasis, lipotoxicity and the metabolic syndrome. Biochim. Biophys. Acta 1801, 209-214
2. Boden, G. (1997) Role of fatty acids in the pathogenesis of insulin resistance and NIDDM. Diabetes 46, 3-10
3. Boden, G., Chen, X., Ruiz, J., White, J. V., and Rossetti, L. (1994) Mechanisms of fatty acid-induced inhibition of glucose uptake. J. Clin. Invest. 93, 2438-2446
4. Dresner, A., Laurent, D., Marcucci, M., Griffin, M. E., Dufour, S., Cline, G. W., Slezak, L. A., Andersen, D. K., Hundal, R. S., Rothman, D. L., Petersen, K. F., and Shulman, G. I. (1999) Effects of free fatty acids on glucose transport and IRS-1-associated phosphatidylinositol 3-kinase activity. J. Clin. Invest. 103, 253-259
5. Ferrannini, E., Barrett, E. J., Bevilacqua, S., and DeFronzo, R. A. (1983) Effect of fatty acids on glucose production and utilization in man. J. Clin. Invest. 72, 1737-1747
6. 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
7. Lass, A., Zimmermann, R., Oberer, M., and Zechner, R. (2011) Lipolysis: a highly regulated multi-enzyme complex mediates the catabolism of cellular fat stores. Prog. Lipid Res. 50, 14-27
8. Rajala, M. W., and Scherer, P. E. (2003) Minireview: the adipocyte: at the crossroads of energy homeostasis, inflammation, and atherosclerosis. Endocrinology 144, 3765-3773
9. Villena, J. A., Roy, S., Sarkadi-Nagy, E., Kim, K. H., and Sul, H. S. (2004) Desnutrin, an adipocyte gene encoding a novel patatin domain-containing protein, is induced by fasting and glucocorticoids: ectopic expression of desnutrin increases triglyceride hydrolysis. J. Biol. Chem. 279, 47066-47075
10. 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
11. Ahmadian, M., Wang, Y., and Sul, H. S. (2010) Lipolysis in adipocytes. Int. J. Biochem. Cell Biol. 42, 555-559
12. Jenkins, C. M., Mancuso, D. J., Yan, W., Sims, H. F., Gibson, B., and Gross, R. W. (2004) Identification, cloning, expression, and purification of three novel human calcium-independent phospholipase A2 family members possessing triacylglycerol lipase and acylglycerol transacylase activities. J. Biol. Chem. 279, 48968-48975
13. Soni, K. G., Mardones, G. A., Sougrat, R., Smirnova, E., Jackson, C. L., and Bonifacino, J. S. (2009) Coatomer-dependent protein delivery to lipid droplets. J. Cell Sci. 122, 1834-1841
14. 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
15. Granneman, J. G., Moore, H. P., Krishnamoorthy, R., and Rathod, M. (2009) Perilipin controls lipolysis by regulating the interactions of ABFSP27 hydrolase containing 5 (ABHD5) and adipose triglyceride lipase (ATGL). J. Biol. Chem. 284, 34538-34544
16. 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
17. 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
18. 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
19. Danesch, U., Hoeck, W., and Ringold, G. M. (1992) Cloning and transcriptional regulation of a novel adipocyte-specific gene, FSP27. CAAT-enhancer- binding protein (C/EBP) and C/EBP-like proteins interact with sequences required for differentiation-dependent expression. J. Biol. Chem. 267, 7185-7193
20. Su, A. I., Cooke, M. P., Ching, K. A., Hakak, Y., Walker, J. R., Wiltshire, T., Orth, A. P., Vega, R. G., Sapinoso, L. M., Moqrich, A., Patapoutian, A., Hampton, G. M., Schultz, P. G., and Hogenesch, J. B. (2002) Large-scale analysis of the human and mouse transcriptomes. Proc. Natl. Acad. Sci. U.S.A. 99, 4465-4470
21. Yu, S., Matsusue, K., Kashireddy, P., Cao, W. Q., Yeldandi, V., Yeldandi, A. V., Rao, M. S., Gonzalez, F. J., and Reddy, J. K. (2003) Adipocyte-specific gene expression and adipogenic steatosis in the mouse liver due to peroxisome proliferator-activated receptor gamma1 (PPAR γ 1) overexpression. J. Biol. Chem. 278, 498-505
22. Williams, P. M., Chang, D. J., Danesch, U., Ringold, G. M., and Heller, R. A. (1992) CCAAT/enhancer binding protein expression is rapidly extinguished in TA1 adipocyte cells treated with tumor necrosis factor. Mol. Endocrinol. 6, 1135-1141
23. Kim, J. Y., Liu, K., Zhou, S., Tillison, K., Wu, Y., and Smas, C. M. (2008) Assessment of fat-specific protein 27 in the adipocyte lineage suggests a dual role for FSP27 in adipocyte metabolism and cell death. Am. J. Physiol. Endocrinol. Metab. 294, E654-E667
24. Liu, K., Zhou, S., Kim, J. Y., Tillison, K., Majors, D., Rearick, D., Lee, J. H., Fernandez-Boyanapalli, R. F., Barricklow, K., Houston, M. S., and Smas, C. M. (2009) Functional analysis of FSP27 protein regions for lipid droplet localization, caspase-dependent apoptosis, and dimerization with CIDEA. Am. J. Physiol. Endocrinol. Metab. 297, E1395-E1413
25. 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
26. Puri, V., Ranjit, S., Konda, S., Nicoloro, S. M., Straubhaar, J., Chawla, A., Chouinard, M., Lin, C., Burkart, A., Corvera, S., Perugini, R. A., and Czech, M. P. (2008) Cidea is associated with lipid droplets and insulin sensitivity in humans. Proc. Natl. Acad. Sci. U.S.A. 105, 7833-7838
27. Puri, V., and Czech, M. P. (2008) Lipid droplets: FSP27 knockout enhances their sizzle. J. Clin. Invest. 118, 2693-2696
28. Puri, V., Konda, S., Ranjit, S., Aouadi, M., Chawla, A., Chouinard, M., Chakladar, A., and Czech, M. P. (2007) Fat-specific protein 27, a novel lipid droplet protein that enhances triglyceride storage. J. Biol. Chem. 282, 34213-34218
29. 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
30. Toh, S. Y., Gong, J., Du, G., Li, J. Z., Yang, S., Ye, J., Yao, H., Zhang, Y., Xue, B., Li, Q., Yang, H., Wen, Z., and Li, P. (2008) Up-regulation of mitochondrial activity and acquirement of brown adipose tissue-like property in the white adipose tissue of fsp27 deficient mice. PLoS ONE 3, e2890
31. Grahn, T. H., Zhang, Y., Lee, M. J., Sommer, A. G., Mostoslavsky, G., Fried, S. K., Greenberg, A. S., and Puri, V. (2013) FSP27 and PLIN1 interaction promotes the formation of large lipid droplets in human adipocytes. Biochem. Biophys. Res. Commun. 432, 296-301
32. Sun, Z., Gong, J., Wu, H., Xu, W., Wu, L., Xu, D., Gao, J., Wu, J. W., Yang, H., Yang, M., and Li, P. (2013) Perilipin1 promotes unilocular lipid droplet formation through the activation of Fsp27 in adipocytes. Nat. Commun. 4, 1594
33. Martinez-Botas, J., Anderson, J. B., Tessier, D., Lapillonne, A., Chang, B. H., Quast, M. J., Gorenstein, D., Chen, K. H., and Chan, L. (2000) Absence of perilipin results in leanness and reverses obesity in Lepr(db/db) mice. Nat. Genet. 26, 474-479
34. Tansey, J. T., Sztalryd, C., Gruia-Gray, J., Roush, D. L., Zee, J. V., Gavrilova, O., Reitman, M. L., Deng, C. X., Li, C., Kimmel, A. R., and Londos, C. (2001) Perilipin ablation results in a lean mouse with aberrant adipocyte lipolysis, enhanced leptin production, and resistance to diet-induced obesity. Proc. Natl. Acad. Sci. U.S.A. 98, 6494-6499
35. Zimmermann, R., Lass, A., Haemmerle, G., and Zechner, R. (2009) Fate of fat: the role of adipose triglyceride lipase in lipolysis. Biochim. Biophys. Acta 1791, 494-500
36. Castro-Chavez, F., Yechoor, V. K., Saha, P. K., Martinez-Botas, J., Wooten, E. C., Sharma, S., O'Connell, P., Taegtmeyer, H., and Chan, L. (2003) Coordinated upregulation of oxidative pathways and downregulation of lipid biosynthesis underlie obesity resistance in perilipin knockout mice: a microarray gene expression profile. Diabetes 52, 2666-2674
37. Zhou, Z., Yon Toh, S., Chen, Z., Guo, K., Ng, C. P., Ponniah, S., Lin, S. C., Hong, W., and Li, P. (2003) Cidea-deficient mice have lean phenotype and are resistant to obesity. Nat. Genet. 35, 49-56
38. Dobrzyn, P., Dobrzyn, A., Miyazaki, M., Cohen, P., Asilmaz, E., Hardie, D. G., Friedman, J. M., and Ntambi, J. M. (2004) Stearoyl-CoA desaturase 1 deficiency increases fatty acid oxidation by activating AMP-activated protein kinase in liver. Proc. Natl. Acad. Sci. U.S.A. 101, 6409-6414
39. Ntambi, J. M., Miyazaki, M., Stoehr, J. P., Lan, H., Kendziorski, C. M., Yandell, B. S., Song, Y., Cohen, P., Friedman, J. M., and Attie, A. D. (2002) Loss of stearoyl-CoA desaturase-1 function protects mice against adiposity. Proc. Natl. Acad. Sci. U.S.A. 99, 11482-11486
40. Rubio-Cabezas, O., Puri, V., Murano, I., Saudek, V., Semple, R. K., Dash, S., Hyden, C. S., Bottomley, W., Vigouroux, C., Magré, J., Raymond-Barker, P., Murgatroyd, P. R., Chawla, A., Skepper, J. N., Chatterjee, V. K., Suliman, S., Patch, A. M., Agarwal, A. K., Garg, A., Barroso, I., Cinti, S., Czech, M. P., Argente, J., O'Rahilly, S., Savage, D. B., and LD Screening Consortium (2009) Partial lipodystrophy and insulin resistant diabetes in a patient with a homozygous nonsense mutation in CIDEC. EMBO Mol. Med. 1, 280-287
41. Itani, S. I., Ruderman, N. B., Schmieder, F., and Boden, G. (2002) Lipidinduced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IκB-α
42. Nguyen, M. T., Satoh, H., Favelyukis, S., Babendure, J. L., Imamura, T., Sbodio, J. I., Zalevsky, J., Dahiyat, B. I., Chi, N. W., and Olefsky, J. M. (2005) JNK and tumor necrosis factor-α mediate free fatty acid-induced insulin resistance in 3T3-L1 adipocytes. J. Biol. Chem. 280, 35361-35371
43. Yu, C., Chen, Y., Cline, G. W., Zhang, D., Zong, H., Wang, Y., Bergeron, R., Kim, J. K., Cushman, S. W., Cooney, G. J., Atcheson, B., White, M. F., Kraegen, E. W., and Shulman, G. I. (2002) Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-1)-associated phosphatidylinositol 3-kinase activity in muscle. J. Biol. Chem. 277, 50230-50236
44. Guilherme, A., Virbasius, J. V., Puri, V., and Czech, M. P. (2008) Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat. Rev. Mol. Cell Biol. 9, 367-377
45. Lee, M. J., Wu, Y., and Fried, S. K. (2012) A modified protocol to maximize differentiation of human preadipocytes and improve metabolic phenotypes. Obesity 20, 2334-2340
46. Mostoslavsky, G., Kotton, D. N., Fabian, A. J., Gray, J. T., Lee, J. S., and Mulligan, R. C. (2005) Efficiency of transduction of highly purified murine hematopoietic stem cells by lentiviral and oncoretroviral vectors under conditions of minimal in vitro manipulation. Mol. Ther. 11, 932-940
47. Lee, M. J., Pickering, R. T., and Puri, V. (2013) Prolonged efficiency of siRNA-mediated gene silencing in primary cultures of human preadipocytes and adipocytes. Obesity, in press
48. Jambunathan, S., Yin, J., Khan, W., Tamori, Y., and Puri, V. (2011) FSP27 promotes lipid droplet clustering and then fusion to regulate triglyceride accumulation. PLoS ONE 6, e28614
49. Gong, J., Sun, Z., Wu, L., Xu, W., Schieber, N., Xu, D., Shui, G., Yang, H., Parton, R. G., and Li, P. (2011) Fsp27 promotes lipid droplet growth by lipid exchange and transfer at lipid droplet contact sites. J. Cell Biol. 195, 953-963
50. Yang, X., Heckmann, B. L., Zhang, X., Smas, C. M., and Liu, J. (2013) Distinct mechanisms regulate ATGL-mediated adipocyte lipolysis by lipid droplet coat proteins. Mol. Endocrinol. 27, 116-126
51. 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
52. Soukas, A., Socci, N. D., Saatkamp, B. D., Novelli, S., and Friedman, J. M. (2001) Distinct transcriptional profiles of adipogenesis in vivo and in vitro. J. Biol. Chem. 276, 34167-34174
53. Bays, H., Mandarino, L., and DeFronzo, R. A. (2004) Role of the adipocyte, free fatty acids, and ectopic fat in pathogenesis of type 2 diabetes mellitus: peroxisomal proliferator-activated receptor agonists provide a rational therapeutic approach. J. Clin. Endocrinol. Metab. 89, 463-478
54. Boden, G., and Shulman, G. I. (2002) Free fatty acids in obesity and type 2 diabetes: defining their role in the development of insulin resistance and β-cell dysfunction. Eur. J. Clin. Invest. 32, 14-23
55. Lewis, G. F., Carpentier, A., Adeli, K., and Giacca, A. (2002) Disordered fat storage and mobilization in the pathogenesis of insulin resistance and type 2 diabetes. Endocr. Rev. 23, 201-229
56. Van Epps-Fung, M., Williford, J., Wells, A., and Hardy, R. W. (1997) Fatty acid-induced insulin resistance in adipocytes. Endocrinology 138, 4338-4345
57. 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
58. Hoy, A. J., Bruce, C. R., Turpin, S. M., Morris, A. J., Febbraio, M. A., and Watt, M. J. (2011) Adipose triglyceride lipase-null mice are resistant to high-fat diet-induced insulin resistance despite reduced energy expenditure and ectopic lipid accumulation. Endocrinology 152, 48-58
59. 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
60. 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
61. Sztalryd, C., Xu, G., Dorward, H., Tansey, J. T., Contreras, J. A., Kimmel, A. R., and Londos, C. (2003) Perilipin A is essential for the translocation of hormone-sensitive lipase during lipolytic activation. J. Cell Biol. 161, 1093-1103
62. Tansey, J. T., Huml, A. M., Vogt, R., Davis, K. E., Jones, J. M., Fraser, K. A., Brasaemle, D. L., Kimmel, A. R., and Londos, C. (2003) Functional studies on native and mutated forms of perilipins: a role in protein kinase A-mediated lipolysis of triacylglycerols. J. Biol. Chem. 278, 8401-8406