Insulin inhibits lipolysis in adipocytes via the evolutionarily conserved mTORC1-Egr1-ATGL-mediated pathway

Molecular and Cellular Biology

Volumn 33, Issue 18, 2013, Pages 3659-3666

  Chakrabarti, Partha ^a,b   Kim, Ju Youn ^a,c   Singh, Maneet ^a   Shin, Yu Kyong ^a   Kim, Jessica ^a   Kumbrink, Joerg ^a   Wu, Yuanyuan ^a   Lee, Mi Jeong ^a   Kirsch, Kathrin H ^a   Fried, Susan K ^a   Kandror, Konstantin V ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOSE TRIGLYCERIDE LIPASE; EARLY GROWTH RESPONSE FACTOR 1; INSULIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EPIDIDYMIS FAT; GENE EXPRESSION; HUMAN; HUMAN CELL; LIPOLYSIS; MALE; MAMMAL CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; CELLS, CULTURED; DNA-BINDING PROTEINS; EARLY GROWTH RESPONSE PROTEIN 1; EVOLUTION, MOLECULAR; HEK293 CELLS; HUMANS; INSULIN; LIPASE; LIPOLYSIS; MALE; MICE; MICE, INBRED C57BL; MULTIPROTEIN COMPLEXES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS;

EID: 84883548896     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01584-12     Document Type: Article

References (54)

1. Guilherme A, Virbasius JV, Puri V, Czech MP. 2008. Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat. Rev. Mol. Cell. Biol. 9:367-377.
2. Savage DB, Petersen KF, Shulman GI. 2007. Disordered lipid metabolism and the pathogenesis of insulin resistance. Physiol. Rev. 87:507-520.
3. Stumvoll M, Goldstein BJ, van Haeften TW. 2008. Type 2 diabetes: pathogenesis and treatment. Lancet 371:2153-2156.
4. Qatanani M, Lazar MA. 2007. Mechanisms of obesity-associated insulin resistance: many choices on the menu. Genes Dev. 21:1443-1455.
5. Coen PM, Goodpaster BH. 2012. Role of intramyocellular lipids in human health. Trends Endocrinol. Metab. 23:391-398.
6. McGarry JD. 1992. What if Minkowski had been ageusic? An alternative angle on diabetes. Science 258:766-770.
7. McGarry JD. 2002. Banting lecture 2001: dysregulation of fatty acid metabolism in the etiology of type 2 diabetes. Diabetes 51:7-18.
8. Zechner R, Kienesberger PC, Haemmerle G, Zimmermann R, Lass A. 2009. Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores. J. Lipid Res. 50:3-21.
9. Duncan RE, Ahmadian M, Jaworski K, Sarkadi-Nagy E, Sul HS. 2007. Regulation of lipolysis in adipocytes. Annu. Rev. Nutr. 27:79-101.
10. Lafontan M, Langin D. 2009. Lipolysis and lipid mobilization in human adipose tissue. Prog. Lipid Res. 48:275-297.
11. Coleman RA, Mashek DG. 2011. Mammalian triacylglycerol metabolism: synthesis, lipolysis, and signaling. Chem. Rev. 111:6359-6386.
12. Zimmermann R, Strauss JG, Haemmerle G, Schoiswohl G, Birner-Gruenberger R, Riederer M, Lass A, Neuberger G, Eisenhaber F, Hermetter A, Zechner R. 2004. Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science 306:1383-1386.
13. Villena JA, Roy S, Sarkadi-Nagy E, Kim KH, Sul HS. 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.
14. Jenkins CM, Mancuso DJ, Yan W, Sims HF, Gibson B, Gross RW. 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.
15. Smirnova E, Goldberg EB, Makarova KS, Lin L, Brown WJ, Jackson CL. 2006. ATGL has a key role in lipid droplet/adiposome degradation in mammalian cells. EMBO Rep. 7:106-113.
16. Haemmerle G, Lass A, Zimmermann R, Gorkiewicz G, Meyer C, Rozman J, Heldmaier G, Maier R, Theussl C, Eder S, Kratky D, Wagner EF, Klingenspor M, Hoefler G, Zechner R. 2006. Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase. Science 312:734-737.
17. Bezaire V, Mairal A, Ribet C, Lefort C, Girousse A, Jocken J, Laurencikiene J, Anesia R, Rodriguez AM, Ryden M, Stenson BM, Dani C, Ailhaud G, Arner P, Langin D. 2009. Contribution of adipose triglyceride lipase and hormone-sensitive lipase to lipolysis in hMADS adipocytes. J. Biol. Chem. 284:18282-18291.
18. Miyoshi H, Perfield JW, 2nd, Obin MS, Greenberg AS. 2008. Adipose triglyceride lipase regulates basal lipolysis and lipid droplet size in adipocytes. J. Cell. Biochem. 105:1430-1436.
19. Kershaw EE, Hamm JK, Verhagen LA, Peroni O, Katic M, Flier JS. 2006. Adipose triglyceride lipase: function, regulation by insulin, and comparison with adiponutrin. Diabetes 55:148-157.
20. Gronke S, Mildner A, Fellert S, Tennagels N, Petry S, Muller G, Jackle H, Kuhnlein RP. 2005. Brummer lipase is an evolutionary conserved fat storage regulator in Drosophila. Cell Metab. 1:323-330.
21. Kurat CF, Natter K, Petschnigg J, Wolinski H, Scheuringer K, Scholz H, Zimmermann R, Leber R, Zechner R, Kohlwein SD. 2006. Obese yeast: triglyceride lipolysis is functionally conserved from mammals to yeast. J. Biol. Chem. 281:491-500.
22. Chakrabarti P, English T, Shi J, Smas CM, Kandror KV. 2010. The mTOR complex 1 suppresses lipolysis, stimulates lipogenesis and promotes fat storage. Diabetes 59:775-781.
23. Kitamura T, Kitamura Y, Kuroda S, Hino Y, Ando M, Kotani K, Konishi H, Matsuzaki H, Kikkawa U, Ogawa W, Kasuga M. 1999. Insulin-induced phosphorylation and activation of cyclic nucleotide phosphodiesterase 3B by the serine-threonine kinase Akt. Mol. Cell. Biol. 19:6286-6296.
24. Choi SM, Tucker DF, Gross DN, Easton RM, DiPilato LM, Dean AS, Monks BR, Birnbaum MJ. 2010. Insulin regulates adipocyte lipolysis via an Akt-independent signaling pathway. Mol. Cell. Biol. 30:5009-5020.
25. Kim JY, Tillison K, Lee JH, Rearick DA, Smas CM. 2006. The adipose tissue triglyceride lipase ATGL/PNPLA2 is downregulated by insulin and TNF-alpha in 3T3-L1 adipocytes and is a target for transactivation by PPAR . Am. J. Physiol. Endocrinol. Metab. 291:E115-E127.
26. Lake AC, Sun Y, Li JL, Kim JE, Johnson JW, Li D, Revett T, Shih HH, Liu W, Paulsen JE, Gimeno RE. 2005. Expression, regulation, and triglyceride hydrolase activity of adiponutrin family members. J. Lipid Res. 46:2477-2487.
27. Fortier M, Wang SP, Mauriege P, Semache M, Mfuma L, Li H, Levy E, Richard D, Mitchell GA. 2004. Hormone-sensitive lipase-independent adipocyte lipolysis during beta-adrenergic stimulation, fasting, and dietary fat loading. Am. J. Physiol. Endocrinol. Metab. 287:E282-E288.
28. Nielsen TS, Vendelbo MH, Jessen N, Pedersen SB, Jorgensen JO, Lund S, Moller N. 2011. Fasting, but not exercise, increases adipose triglyceride lipase (ATGL) protein and reduces G0/G1 switch gene 2 (G0S2) protein and mRNA content in human adipose tissue. J. Clin. Endocrinol. Metab. 96:E1293-E1297.
29. Alsted TJ, Nybo L, Schweiger M, Fledelius C, Jacobsen P, Zimmermann R, Zechner R, Kiens B. 2009. Adipose triglyceride lipase in human skeletal muscle is upregulated by exercise training. Am. J. Physiol. Endocrinol. Metab. 296:E445-E453.
30. Chakrabarti P, Kandror KV. 2009. FoxO1 control s insulin-dependent ATGL expression and lipolysis in adipocytes. J. Biol. Chem. 284:13296-13300.
31. Chakrabarti P, English T, Karki S, Qiang L, Tao R, Kim J, Luo Z, Farmer SR, Kandror KV. 2011. SIRT1 controls lipolysis in adipocytes via FOXO1-mediated expression of ATGL. J. Lipid Res. 52:1693-1701.
32. Luong N, Davies CR, Wessells RJ, Graham SM, King MT, Veech R, Bodmer R, Oldham SM. 2006. Activated FOXO-mediated insulin resistance is blocked by reduction of TOR activity. Cell Metab. 4:133-142.
33. Birse RT, Choi J, Reardon K, Rodriguez J, Graham S, Diop S, Ocorr K, Bodmer R, Oldham S. 2010. High-fat-diet-induced obesity and heart dysfunction are regulated by the TOR pathway in Drosophila. Cell Metab. 12:533-544.
34. Xu Z, Kandror KV. 2002. Translocation of small preformed vesicles is responsible for the insulin activation of glucose transport in adipose cells: evidence from the in vitro reconstitution assay. J. Biol. Chem. 277:47972-47975.
35. Kumbrink J, Kirsch KH, Johnson JP. 2010. EGR1, EGR2, and EGR3 activate the expression of their coregulator NAB2 establishing a negativefeedback loop in cells of neuroectodermal and epithelial origin. J. Cell. Biochem. 111:207-217.
36. Lucerna M, Pomyje J, Mechtcheriakova D, Kadl A, Gruber F, Bilban M, Sobanov Y, Schabbauer G, Breuss J, Wagner O, Bischoff M, Clauss M, Binder BR, Hofer E. 2006. Sustained expression of early growth response protein-1 blocks angiogenesis and tumor growth. Cancer Res. 66:6708-6713.
37. Huang J, Manning BD. 2008. The TSC1-TSC2 complex: a molecular switchboard controlling cell growth. Biochem. J. 412:179-190.
38. Festuccia WT, Laplante M, Berthiaume M, Gelinas Y, Deshaies Y. 2006. PPAR agonism increases rat adipose tissue lipolysis, expression of glyceride lipases, and the response of lipolysis to hormonal control. Diabetologia 49:2427-2436.
39. Kershaw EE, Schupp M, Guan HP, Gardner NP, Lazar MA, Flier JS. 2007. PPAR regulates adipose triglyceride lipase in adipocytes in vitro and in vivo. Am. J. Physiol. Endocrinol. Metab. 293:E1736-E1745.
40. Nielsen R, Pedersen TA, Hagenbeek D, Moulos P, Siersbaek R, Megens E, Denissov S, Borgesen M, Francoijs KJ, Mandrup S, Stunnenberg HG. 2008. Genome-wide profiling of PPAR :RXR and RNA polymerase II occupancy reveals temporal activation of distinct metabolic pathways and changes in RXR dimer composition during adipogenesis. Genes Dev. 22: 2953-2967.
41. Eguchi J, Wang X, Yu S, Kershaw EE, Chiu PC, Dushay J, Estall JL, Klein U, Maratos-Flier E, Rosen ED. 2011. Transcriptional control of adipose lipid handling by IRF4. Cell Metab. 13:249-259.
42. Estruch F, Carlson M. 1993. Two homologous zinc finger genes identified by multicopy suppression in a SNF1 protein kinase mutant of Saccharomyces cerevisiae. Mol. Cell. Biol. 13:3872-3881.
43. Boyle KB, Hadaschik D, Virtue S, Cawthorn WP, Ridley SH, O'Rahilly S, Siddle K. 2009. The transcription factors Egr1 and Egr2 have opposing influences on adipocyte differentiation. Cell Death Differ. 16:782-789.
44. Wang W, Huang L, Huang Y, Yin JW, Berk AJ, Friedman JM, Wang G. 2009. Mediator MED23 links insulin signaling to the adipogenesis transcription cascade. Dev. Cell 16:764-771.
45. Carnevalli LS, Masuda K, Frigerio F, Le Bacquer O, Um SH, Gandin V, Topisirovic I, Sonenberg N, Thomas G, Kozma SC. 2010. S6K1 plays a critical role in early adipocyte differentiation. Dev. Cell 18:763-774.
46. Shen N, Yu X, Pan FY, Gao X, Xue B, Li CJ. 2011. An early response transcription factor, egr-1, enhances insulin resistance in type 2 diabetes with chronic hyperinsulinism. J. Biol. Chem. 286:14508-14515.
47. Gokey NG, Lopez-Anido C, Gillian-Daniel AL, Svaren J. 2011. Early growth response 1 (egr1) regulates cholesterol biosynthetic gene expression. J. Biol. Chem. 286:29501-29510.
48. Brand E, Herrmann SM, Nicaud V, Evans A, Ruidavets JB, Arveiler D, Luc G, Cambien F, Soubrier F. 2000. Identification of two polymorphisms in the early growth response protein-1 gene: possible association with lipid variables. J. Mol. Med. (Berlin) 78:81-86.
49. Thiel G, Cibelli G. 2002. Regulation of life and death by the zinc finger transcription factor Egr-1. J. Cell Physiol. 193:287-292.
50. Sartipy P, Loskutoff DJ. 2003. Expression profiling identifies genes that continue to respond to insulin in adipocytes made insulin-resistant by treatment with tumor necrosis factor-alpha. J. Biol. Chem. 278:52298-52306.
51. Kralisch S, Klein J, Lossner U, Bluher M, Paschke R, Stumvoll M, Fasshauer M. 2005. Isoproterenol, TNFα, and insulin downregulate adipose triglyceride lipase in 3T3-L1 adipocytes. Mol. Cell. Endocrinol. 240: 43-49.
52. Um SH, Frigerio F, Watanabe M, Picard F, Joaquin M, Sticker M, Fumagalli S, Allegrini PR, Kozma SC, Auwerx J, Thomas G. 2004. Absence of S6K1 protects against age-and diet-induced obesity while enhancing insulin sensitivity. Nature 431:200-205.
53. Jocken JW, Langin D, Smit E, Saris WH, Valle C, Hul GB, Holm C, Arner P, Blaak EE. 2007. Adipose triglyceride lipase and hormonesensitive lipase protein expression is decreased in the obese insulinresistant state. J. Clin. Endocrinol. Metab. 92:2292-2299.
54. Karpe F, Dickmann JR, Frayn KN. 2011. Fatty acids, obesity, and insulin resistance: time for a reevaluation. Diabetes 60:2441-2449