Mechanistic target of rapamycin controls homeostasis of adipogenesis

Journal of Lipid Research

Volumn 54, Issue 8, 2013, Pages 2166-2173

  Yoon, Mee Sup ^a   Zhang, Chongben ^b   Sun, Yuting ^a   Schoenherr, Christopher J ^c   Chen, Jie ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

Adipocytes; CCAAT enhancer binding protein ; Mechanistic target of rapamycin complex 1; Peroxisome proliferator activated receptor

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN ALPHA; INSULIN RECEPTOR SUBSTRATE 1; MAMMALIAN TARGET OF RAPAMYCIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN KINASE B; S6 KINASE;

ADIPOGENESIS; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; GENE SILENCING; HOMEOSTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROADIPOCYTE; PROTEIN BLOOD LEVEL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TISSUE DIFFERENTIATION;

EID: 84880906852     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M037705     Document Type: Article

References (47)

1. Darlington, G. J., S. E. Ross, and O. A. MacDougald.1998.The role of C/EBP genes in adipocyte differentiation. J. Biol. Chem. 273 : 30057-30060.
2. Morrison, R. F., and S. R. Farmer.2000.Hormonal signaling and transcriptional control of adipocyte differentiation. J. Nutr. 130 : 3116S-3121S.
3. Rosen, E. D., C. J. Walkey, P. Puigserver, and B. M. Spiegelman. 2000.Transcriptional regulation of adipogenesis. Genes Dev. 14 : 1293-1307.
4. Rosen, E. D., and O. A. MacDougald.2006.Adipocyte differentiation from the inside out. Nat. Rev. Mol. Cell Biol. 7 : 885-896.
5. Erbay, E., J. E. Kim, and J. Chen.2005.Amino acid-sensing mTOR signaling. In Nutrient and Cell Signaling. J. Zempleni and K. Dakshinamurti, editors. CRC Press. 353-380.
6. Fingar, D. C., and J. Blenis.2004.Target of rapamycin (TOR): An integrator of nutrient and growth factor signals and coordinator of cell growth and cell cycle progression. Oncogene.23 : 3151-3171.
7. Sarbassov, D. D., S. M. Ali, and D. M. Sabatini.2005.Growing roles for the mTOR pathway. Curr. Opin. Cell Biol. 17 : 596-603.
8. Wullschleger, S., R. Loewith, and M. N. Hall.2006.TOR signaling in growth and metabolism. Cell.124 : 471-484.
9. Foster, K. G., and D. C. Fingar.2010. Mammalian target of rapamycin (mTOR): Conducting the cellular signaling symphony. J. Biol. Chem. 285: 14071-14077.
10. Ma, X. M., and J. Blenis.2009.Molecular mechanisms of mTORmediated translational control. Nat. Rev. Mol. Cell Biol. 10 : 307-318.
11. Laplante, M., and D. M. Sabatini.2009.An emerging role of mTOR in lipid biosynthesis. Curr. Biol. 19 : R1046-R1052.
12. Yeh, W. C., B. E. Bierer, and S. L. McKnight.1995.Rapamycin inhibits clonal expansion and adipogenic differentiation of 3T3-L1 cells. Proc. Natl. Acad. Sci. USA.92 : 11086-11090.
13. Bell, A., L. Grunder, and A. Sorisky.2000.Rapamycin inhibits human adipocyte differentiation in primary culture. Obes. Res. 8 : 249-254.
14. Gagnon, A., S. Lau, and A. Sorisky.2001.Rapamycin-sensitive phase of 3T3-L1 preadipocyte differentiation after clonal expansion. J. Cell. Physiol. 189 : 14-22.
15. Kim, J. E., and J. Chen.2004.Regulation of peroxisome proliferator-activated receptor-gamma activity by mammalian target of rapamycin and amino acids in adipogenesis. Diabetes.53 : 2748-2756.
16. Zhang, H. H., J. Huang, K. Düvel, B. Boback, S. Wu, R. M. Squillace, C-L. Wu, and B. D. Manning.2009.Insulin stimulates adipogenesis through the Akt-TSC2-mTORC1 pathway. PLoS ONE.4 : E6189.
17. Um, S. H., F. Frigerio, M. Watanabe, F. Picard, M. Joaquin, M. Sticker, S. Fumagalli, P. R. Allegrini, S. C. Kozma, J. Auwerx, et al. 2004.Absence of S6K1 protects against age-and diet-induced obesity while enhancing insulin sensitivity. Nature.431 : 200-205.
18. Carnevalli, L. S., K. Masuda, F. Frigerio, O. Le Bacquer, S. H. Um, V. Gandin, I. Topisirovic, N. Sonenberg, G. Thomas, and S. C. Kozma.2010.S6K1 plays a critical role in early adipocyte differentiation. Dev. Cell.18 : 763-774.
19. Le Bacquer, O., E. Petroulakis, S. Paglialunga, F. Poulin, D. Richard, K. Cianflone, and N. Sonenberg.2007.Elevated sensitivity to dietinduced obesity and insulin resistance in mice lacking 4E-BP1 and 4E-BP2. J. Clin. Invest. 117 : 387-396.
20. Cota, D., K. Proulx, K. A. Smith, S. C. Kozma, G. Thomas, S. C. Woods, and R. J. Seeley.2006.Hypothalamic mTOR signaling regulates food intake. Science.312 : 927-930.
21. Mori, H., K. Inoki, H. Munzberg, D. Opland, M. Faouzi, E. C. Villanueva, T. Ikenoue, D. Kwiatkowski, O. A. MacDougald, M. G. Myers, Jr ., et al.2009.Critical role for hypothalamic mTOR activity in energy balance. Cell Metab. 9 : 362-374.
22. Yang, S. B., A. C. Tien, G. Boddupalli, A. W. Xu, Y. N. Jan, and L. Y. Jan.2012.Rapamycin ameliorates age-dependent obesity associated with increased mTOR signaling in hypothalamic POMC neurons. Neuron.75 : 425-436.
23. Polak, P., N. Cybulski, J. N. Feige, J. Auwerx, M. A. Ruegg, and M. N. Hall.2008.Adipose-specific knockout of raptor results in lean mice with enhanced mitochondrial respiration. Cell Metab. 8 : 399-410.
24. Ventura, A., A. Meissner, C. P. Dillon, M. McManus, P. A. Sharp, L. Van Parijs, R. Jaenisch, and T. Jacks.2004. Cre-lox-regulated conditional RNA interference from transgenes. Proc. Natl. Acad. Sci. U S A.101: 10380-10385.
25. Kim, J. H., J. E. Kim, H. Y. Liu, W. Cao, and J. Chen.2008.Regulation of interleukin-6-induced hepatic insulin resistance by mammalian target of rapamycin through the STAT3-SOCS3 pathway. J. Biol. Chem. 283 : 708-715.
26. Ramirez-Zacarias, J. L., F. Castro-Munozledo, and W. Kuri-Harcuch. 1992.Quantitation of adipose conversion and triglycerides by staining intracytoplasmic lipids with Oil red O. Histochemistry.97 : 493-497.
27. Pearce, L. R., G. R. Alton, D. T. Richter, J. C. Kath, L. Lingardo, J. Chapman, C. Hwang, and D. R. Alessi.2010.Characterization of PF-4708671, a novel and highly specific inhibitor of p70 ribosomal S6 kinase (S6K1). Biochem. J. 431: 245-255.
28. Liu, Q., J. W. Chang, J. Wang, S. A. Kang, C. C. Thoreen, A. Markhard, W. Hur, J. Zhang, T. Sim, D. M. Sabatini, et al.2010. Discovery of 1-(4-(4-propionylpiperazin-1-yl)-3-(trifluoromethyl) phenyl)-9-(quinolin-3-yl) benzo[h][1,6]naphthyridin-2(1H)-one as a highly potent, selective mammalian target of rapamycin (mTOR) inhibitor for the treatment of cancer. J. Med. Chem. 53 : 7146-7155.
29. Um, S. H., D. D'Alessio, and G. Thomas.2006.Nutrient overload, insulin resistance, and ribosomal protein S6 kinase 1, S6K1. Cell Metab. 3 : 393-402.
30. Tzatsos, A., and K. V. Kandror.2006.Nutrients suppress phosphatidylinositol 3-kinase/Akt signaling via raptor-dependent mTORmediated insulin receptor substrate 1 phosphorylation. Mol. Cell. Biol. 26 : 63-76.
31. Hsu, P. P., S. A. Kang, J. Rameseder, Y. Zhang, K. A. Ottina, D. Lim, T. R. Peterson, Y. Choi, N. S. Gray, M. B. Yaffe, et al.2011. The mTOR-regulated phosphoproteome reveals a mechanism of mTORC1-mediated inhibition of growth factor signaling. Science. 332 : 1317-1322.
32. Yu, Y., S-O. Yoon, G. Poulogiannis, Q. Yang, X. M. Ma, J. Villen, N. Kubica, G. R. Hoffman, L. C. Cantley, S. P.Gygi, et al. 2011. Phosphoproteomic analysis identifi es Grb10 as an mTORC1 substrate that negatively regulates insulin signaling. Science.332 : 1322-1326.
33. Barnett, S. F., D. Defeo-Jones, S. Fu, P. J. Hancock, K. M. Haskell, R. E. Jones, J. A. Kahana, A. M. Kral, K. Leander, L. L. Lee, et al. 2005.Identification and characterization of pleckstrin-homologydomain-dependent and isoenzyme-specific Akt inhibitors. Biochem. J. 385 : 399-408.
34. Hresko, R. C., and M. Mueckler.2005. mTOR.RICTOR is the Ser473 kinase for Akt/protein kinase B in 3T3-L1 adipocytes. J. Biol. Chem.280: 40406-40416.
35. Kumar, A., J. C. Lawrence, Jr ., D. Y. Jung, H. J. Ko, S. R. Keller, J. K. Kim, M. A. Magnuson, and T. E. Harris.2010. Fat cell-specific ablation of rictor in mice impairs insulin-regulated fat cell and whole-body glucose and lipid metabolism. Diabetes.59: 1397-1406.
36. Cybulski, N., P. Polak, J. Auwerx, M. A. Ruegg, and M. N. Hall. 2009. mTOR complex 2 in adipose tissue negatively controls wholebody growth. Proc. Natl. Acad. Sci. U S A.106: 9902-9907.
37. Sarbassov, D. D., D. A. Guertin, S. M. Ali, and D. M. Sabatini.2005. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science.307 : 1098-1101.
38. Lamming, D. W., L. Ye, P. Katajisto, M. D. Goncalves, M. Saitoh, D. M. Stevens, J. G. Davis, A. B. Salmon, A. Richardson, R. S. Ahima, et al.2012.Rapamycin-induced insulin resistance is mediated by mTORC2 loss and uncoupled from longevity. Science.335 : 1638-1643.
39. Mauvais-Jarvis, F., K. Ueki, D. A. Fruman, M. F. Hirshman, K. Sakamoto, L. J. Goodyear, M. Iannacone, D. Accili, L. C. Cantley, and C. R. Kahn.2002.Reduced expression of the murine p85alpha subunit of phosphoinositide 3-kinase improves insulin signaling and ameliorates diabetes. J. Clin. Invest. 109 : 141-149.
40. Fruman, D. A., S. B. Snapper, C. M. Yballe, L. Davidson, J. Y. Yu, F. W. Alt, and L. C. Cantley.1999.Impaired B cell development and proliferation in absence of phosphoinositide 3-kinase p85alpha. Science.283 : 393-397.
41. Fruman, D. A., F. Mauvais-Jarvis, D. A. Pollard, C. M. Yballe, D. Brazil, R. T. Bronson, C. R. Kahn, and L. C. Cantley.2000.Hypoglycaemia, liver necrosis and perinatal death in mice lacking all isoforms of phosphoinositide 3-kinase p85 alpha. Nat. Genet. 26 : 379-382.
42. Laplante, M., S. Horvat, W. T. Festuccia, K. Birsoy, Z. Prevorsek, A. Efeyan, and D. M. Sabatini.2012.DEPTOR cell-autonomously promotes adipogenesis, and its expression is associated with obesity. Cell Metab. 16 : 202-212.
43. Peterson, T. R., M. Laplante, C. C. Thoreen, Y. Sancak, S. A. Kang, W. M. Kuehl, N. S. Gray, and D. M. Sabatini.2009.DEPTOR is an mTOR inhibitor frequently overexpressed in multiple myeloma cells and required for their survival. Cell.137 : 873-886.
44. Zhang, Y., K. Guo, R. E. LeBlanc, D. Loh, G. J. Schwartz, and Y. H. Yu.2007.Increasing dietary leucine intake reduces diet-induced obesity and improves glucose and cholesterol metabolism in mice via multimechanisms. Diabetes.56 : 1647-1654.
45. Fox, H. L., P. T. Pham, S. R. Kimball, L. S. Jefferson, and C. J. Lynch.1998.Amino acid effects on translational repressor 4E-BP1 are mediated primarily by L-leucine in isolated adipocytes. Am. J. Physiol. 275 : C1232-C1238.
46. Patti, M. E., E. Brambilla, L. Luzi, E. J. Landaker, and C. R. Kahn. 1998.Bidirectional modulation of insulin action by amino acids. J. Clin. Invest. 101 : 1519-1529.
47. Xu, G., G. Kwon, C. A. Marshall, T. A. Lin, J. C. Lawrence, Jr ., and M. L. McDaniel.1998.Branched-chain amino acids are essential in the regulation of PHAS-I and p70 S6 kinase by pancreatic betacells. A possible role in protein translation and mitogenic signaling. J. Biol. Chem. 273 : 28178-28184.