BSTA promotes mTORC2-mediated phosphorylation of Akt1 to suppress expression of FoxC2 and stimulate adipocyte differentiation

Science Signaling

Volumn 6, Issue 257, 2013, Pages

  Yao, Yixin ^a   Suraokar, Milind ^a   Darnay, Bryant G ^a   Hollier, Brett G ^a,c   Shaiken, Tattym E ^a   Asano, Takayuki ^a,d   Chen, Chien Hung ^a   Chang, Benny H J ^b   Lu, Yiling ^a   Mills, Gordon B ^a   Sarbassov, Dos ^a   Mani, Sendurai A ^a   Abbruzzese, James L ^a   Reddy, Shrikanth A G ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^d ST MARIANNA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AKT1 PROTEIN; BSD DOMAIN CONTAINING SIGNAL TRANSDUCER AND AKT INTERACTOR PROTEIN; GROWTH FACTOR; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; PROTEIN KINASE B; REGULATOR PROTEIN; SERINE; TRANSCRIPTION FACTOR FOXC2; UNCLASSIFIED DRUG;

ADIPOCYTE; ADIPOGENESIS; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE REPRESSION; GENE SWITCHING; GENETIC CODE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ADIPOCYTES; ADIPOGENESIS; ANIMALS; CARRIER PROTEINS; CELL DIFFERENTIATION; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNOPRECIPITATION; MICE; MULTIPROTEIN COMPLEXES; NERVE TISSUE PROTEINS; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TWO-HYBRID SYSTEM TECHNIQUES;

MAMMALIA; MURINAE;

EID: 84872574955     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2003295     Document Type: Article

References (60)

1. B. D. Manning, L. C. Cantley, Akt/PKB signaling: Navigating downstream. Cell 129, 1261-1274 (2007).
2. T. F. Franke, PI3K/Akt: Getting it right matters. Oncogene 27, 6473-6488 (2008).
3. D. P. Brazil, Z. Z. Yang, B. A. Hemmings, Advances in protein kinase B signaling: Aktion on multiple fronts. Trends Biochem. Sci. 29, 233-242 (2004).
4. A. J. Cameron, M. De Rycker, V. Calleja, D. Alcor, S. Kjaer, B. Kostelecky, A. Saurin, A. Faisal, M. Laguerre, B. A. Hemmings, N. McDonald, B. Larijani, P. J. Parker, Protein kinases, from B to C. Biochem. Soc. Trans. 35, 1013-1017 (2007).
5. D. R. Alessi, L. R. Pearce, J. M. Garcia-Martinez, New insights into mTOR signaling: mTORC2 and beyond. Sci. Signal. 2, pe27 (2009).
6. L. Bozulic, B. A. Hemmings, PIKKing on PKB: Regulation of PKB activity by phosphorylation. Curr. Opin. Cell Biol. 21, 256-261 (2009).
7. L. R. Pearce, D. Komander, D. R. Alessi, The nuts and bolts of AGC protein kinases. Nat. Rev. Mol. Cell Biol. 11, 9-22 (2010).
8. D. D. Sarbassov, D. A. Guertin, S. M. Ali, D. M. Sabatini, Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307, 1098-1101 (2005).
9. T. Ikenoue, K. Inoki, Q. Yang, X. Zhou, K. L. Guan, Essential function of TORC2 in PKC and Akt turn motif phosphorylation, maturation and signalling. EMBO J. 27, 1919-1931 (2008).
10. V. Facchinetti, W. Ouyang, H. Wei, N. Soto, A. Lazorchak, C. Gould, C. Lowry, A. C. Newton, Y. Mao, R. Q. Miao, W. C. Sessa, J. Qin, P. Zhang, B. Su, E. Jacinto, The mammalian target of rapamycin complex 2 controls folding and stability of Akt and protein kinase C. EMBO J. 27, 1932-1943 (2008).
11. D. R. Alessi, M. Andjelkovic, B. Caudwell, P. Cron, N. Morrice, P. Cohen, B. A. Hemmings, Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 15, 6541-6551 (1996).
12. V. Hietakangas, S. M. Cohen, Re-evaluating Akt regulation: Role of TOR complex 2 in tissue growth. Genes Dev. 21, 632-637 (2007).
13. D. A. Guertin, D. M. Stevens, C. C. Thoreen, A. A. Burds, N. Y. Kalaany, J. Moffat, M. Brown, K. J. Fitzgerald, D. M. Sabatini, Ablation in mice of the mTORC components raptor, rictor, or mlst8 reveals that mTORC2 is required for signaling to Akt-FOXO and PKCα, but not S6K1. Dev. Cell 11, 859-871 (2006).
14. C. Shiota, J. T. Woo, J. Lindner, K. D. Shelton, M. A. Magnuson, Multiallelic disruption of the rictor gene in mice reveals that mTOR complex 2 is essential for fetal growth and viability. Dev. Cell 11, 583-589 (2006).
15. E. Jacinto, V. Facchinetti, D. Liu, N. Soto, S. Wei, S. Y. Jung, Q. Huang, J. Qin, B. Su, Sin1/mip1 maintains rictor-mTOR complex integrity and regulates Akt phosphorylation and substrate specificity. Cell 127, 125-137 (2006).
16. Q. Yang, K. Inoki, T. Ikenoue, K. L. Guan, Identification of Sin1 as an essential TORC2 component required for complex formation and kinase activity. Genes Dev. 20, 2820-2832 (2006).
17. K. Du, P. N. Tsichlis, Regulation of the Akt kinase by interacting proteins. Oncogene 24, 7401-7409 (2005).
18. T. F. Franke, Intracellular signaling by Akt: Bound to be specific. Sci. Signal. 1, pe29 (2008).
19. X. D. Peng, P. Z. Xu, M. L. Chen, A. Hahn-Windgassen, J. Skeen, J. Jacobs, D. Sundararajan, W. S. Chen, S. E. Crawford, K. G. Coleman, N. Hay, Dwarfism, impaired skin development, skeletal muscle atrophy, delayed bone development, and impeded adipogenesis in mice lacking Akt1 and Akt2. Genes Dev. 17, 1352-1365 (2003).
20. A. Baudry, Z. Z. Yang, B. A. Hemmings, PKBα is required for adipose differentiation of mouse embryonic fibroblasts. J. Cell Sci. 119, 889-897 (2006).
21. Y. C. Broder, S. Katz, A. Aronheim, The Ras recruitment system, a novel approach to the study of protein-protein interactions. Curr. Biol. 8, 1121-1124 (1998).
22. T. Doerks, S. Huber, E. Buchner, P. Bork, BSD: A novel domain in transcription factors and synapse-associated proteins. Trends Biochem. Sci. 27, 168-170 (2002).
23. J. Yang, P. Cron, V. Thompson, V. M. Good, D. Hess, B. A. Hemmings, D. Barford, Molecular mechanism for the regulation of protein kinase B/Akt by hydrophobic motif phosphorylation. Mol. Cell 9, 1227-1240 (2002).
24. D. A. Guertin, D. M. Stevens, M. Saitoh, S. Kinkel, K. Crosby, J. H. Sheen, D. J. Mullholland, M. A. Magnuson, H. Wu, D. M. Sabatini, mTOR complex 2 is required for the development of prostate cancer induced by Pten loss in mice. Cancer Cell 15, 148-159 (2009).
25. J. Brognard, E. Sierecki, T. Gao, A. C. Newton, PHLPP and a second isoform, PHLPP2, differentially attenuate the amplitude of Akt signaling by regulating distinct Akt isoforms. Mol. Cell 25, 917-931 (2007).
26. T. F. Franke, D. R. Kaplan, L. C. Cantley, A. Toker, Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science 275, 665-668 (1997).
27. K. Datta, T. F. Franke, T. O. Chan, A. Makris, S. I. Yang, D. R. Kaplan, D. K. Morrison, E. A. Golemis, P. N. Tsichlis, AH/PH domain-mediated interaction between Akt molecules and its potential role in Akt regulation. Mol. Cell. Biol. 15, 2304-2310 (1995).
28. J. Laine, G. Kunstle, T. Obata, M. Sha, M. Noguchi, The protooncogene TCL1 is an Akt kinase coactivator. Mol. Cell 6, 395-407 (2000).
29. M. P. Keller, Y. Choi, P. Wang, D. B. Davis, M. E. Rabaglia, A. T. Oler, D. S. Stapleton, C. Argmann, K. L. Schueler, S. Edwards, H. A. Steinberg, E. Chaibub Neto, R. Kleinhanz, S. Turner, M. K. Hellerstein, E. E. Schadt, B. S. Yandell, C. Kendziorski, A. D. Attie, A gene expression network model of type 2 diabetes links cell cycle regulation in islets with diabetes susceptibility. Genome Res. 18, 706-716 (2008).
30. Y. Hayashi, S. Iida, Y. Sato, A. Nakaya, A. Sawada, N. Kaji, H. Kamiya, Y. Baba, H. Harashima, DNA microarray analysis of type 2 diabetes-related genes co-regulated between white blood cells and livers of diabetic Otsuka Long-Evans Tokushima fatty (OLETF) rats. Biol. Pharm. Bull. 30, 763-771 (2007).
31. P. Seale, S. Kajimura, B. M. Spiegelman, Transcriptional control of brown adipocyte development and physiological function - Of mice and men. Genes Dev. 23, 788-797 (2009).
32. E. D. Rosen, O. A. MacDougald, Adipocyte differentiation from the inside out. Nat. Rev. Mol. Cell Biol. 7, 885-896 (2006).
33. A. Cederberg, L. M. Grønning, B. Ahrén, K. Taskén, P. Carlsson, S. Enerbäck, FOXC2 is a winged helix gene that counteracts obesity, hypertriglyceridemia, and diet-induced insulin resistance. Cell 106, 563-573 (2001).
34. K. E. Davis, M. Moldes, S. R. Farmer, The forkhead transcription factor FoxC2 inhibits white adipocyte differentiation. J. Biol. Chem. 279, 42453-42461 (2004).
35. I. Gerin, G. T. Bommer, M. E. Lidell, A. Cederberg, S. Enerback, O. A. MacDougald, On the role of FOX transcription factors in adipocyte differentiation and insulin-stimulated glucose uptake. J. Biol. Chem. 284, 10755-10763 (2009).
36. L. M. Grønning, A. Cederberg, N. Miura, S. Enerbäck, K. Taskén, Insulin and TNFα induce expression of the forkhead transcription factor gene Foxc2 in 3T3-L1 adipocytes via PI3K and ERK1/2-dependent pathways. Mol. Endocrinol. 16, 873-883 (2002).
37. E. L. Huttlin, M. P. Jedrychowski, J. E. Elias, T. Goswami, R. Rad, S. A. Beausoleil, J. Villén, W. Haas, M. E. Sowa, S. P. Gygi, A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143, 1174-1189 (2010).
38. Y. Yu, S. O. Yoon, G. Poulogiannis, Q. Yang, X. M. Ma, J. Villén, N. Kubica, G. R. Hoffman, L. C. Cantley, S. P. Gygi, J. Blenis, Phosphoproteomic analysis identifies Grb10 as an mTORC1 substrate that negatively regulates insulin signaling. Science 332, 1322-1326 (2011).
39. N. Cybulski, P. Polak, J. Auwerx, M. A. Rüegg, M. N. Hall, mTOR complex 2 in adipose tissue negatively controls whole-body growth. Proc. Natl. Acad. Sci. U.S.A. 106, 9902-9907 (2009).
40. A. Kumar, J. C. Lawrence Jr., D. Y. Jung, H. J. Ko, S. R. Keller, J. K. Kim, M. A. Magnuson, T. E. Harris, Fat cell-specific ablation of rictor in mice impairs insulin-regulated fat cell and whole-body glucose and lipid metabolism. Diabetes 59, 1397-1406 (2010).
41. A. A. Soukas, E. A. Kane, C. E. Carr, J. A. Melo, G. Ruvkun, Rictor/TORC2 regulates fat metabolism, feeding, growth, and life span in Caenorhabditis elegans. Genes Dev. 23, 496-511 (2009).
42. K. T. Jones, E. R. Greer, D. Pearce, K. Ashrafi, Rictor/TORC2 regulates Caenorhabditis elegans fat storage, body size, and development through sgk-1. PLoS Biol. 7, e60 (2009).
43. J. Nakae, T. Kitamura, Y. Kitamura, W. H. Biggs III, K. C. Arden, D. Accili, The forkhead transcription factor Foxo1 regulates adipocyte differentiation. Dev. Cell 4, 119-129 (2003).
44. A. Brunet, J. Park, H. Tran, L. S. Hu, B. A. Hemmings, M. E. Greenberg, Protein kinase SGK mediates survival signals by phosphorylating the forkhead transcription factor FKHRL1 (FOXO3a). Mol. Cell. Biol. 21, 952-965 (2001).
45. N. Di Pietro, V. Panel, S. Hayes, A. Bagattin, S. Meruvu, A. Pandolfi, L. Hugendubler, G. Fejes-Tóth, A. Naray-Fejes-Tóth, E. Mueller, Serum- and glucocorticoid-inducible kinase 1 (SGK1) regulates adipocyte differentiation via forkhead box O1. Mol. Endocrinol. 24, 370-380 (2010).
46. H. H. Zhang, J. Huang, K. Duvel, B. Boback, S. Wu, R. M. Squillace, C. L. Wu, B. D. Manning, Insulin stimulates adipogenesis through the Akt-TSC2-mTORC1 pathway. PLoS One 4, e6189 (2009).
47. P. Polak, N. Cybulski, J. N. Feige, J. Auwerx, M. A. Rüegg, M. N. Hall, Adipose-specific knockout of raptor results in lean mice with enhanced mitochondrial respiration. Cell Metab. 8, 399-410 (2008).
48. J. M. García-Martinez, D. R. Alessi, mTOR complex 2 (mTORC2) controls hydrophobic motif phosphorylation and activation of serum- and glucocorticoid-induced protein kinase 1 (SGK1). Biochem. J. 416, 375-385 (2008).
49. B. Lamothe, A. Besse, A. D. Campos, W. K. Webster, H. Wu, B. G. Darnay, Site-specific Lys-63-linked tumor necrosis factor receptor-associated factor 6 auto-ubiquitination is a critical determinant of IκB kinase activation. J. Biol. Chem. 282, 4102-4112 (2007).
50. Ras protein requires PDK1. Cell. Signal. 21, 502-508 (2009).
51. A. C. Hsieh, R. Bo, J. Manola, F. Vazquez, O. Bare, A. Khvorova, S. Scaringe, W. R. Sellers, A library of siRNA duplexes targeting the phosphoinositide 3-kinase pathway: Determinants of gene silencing for use in cell-based screens. Nucleic Acids Res. 32, 893-901 (2004).
52. G. Sithanandam, L. W. Fornwald, J. R. Fields, N. L. Morris, L. M. Anderson, Anti-tumor efficacy of naked siRNAs for ERBB3 or AKT2 against lung adenocarcinoma cell xenografts. Int. J. Cancer 130, 251-258 (2012).
53. E. Kinoshita, E. Kinoshita-Kikuta, K. Takiyama, T. Koike, Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol. Cell. Proteomics 5, 749-757 (2006).
54. X. Sui, S. Shin, R. Zhang, P. F. Firozi, L. Yang, J. L. Abbruzzese, S. A. Reddy, Hdm2 is regulated by K-Ras and mediates p53-independent functions in pancreatic cancer cells. Oncogene 28, 709-720 (2009).
55. Z. Y. Jiang, Q. L. Zhou, K. A. Coleman, M. Chouinard, Q. Boese, M. P. Czech, Insulin signaling through Akt/protein kinase B analyzed by small interfering RNA-mediated gene silencing. Proc. Natl. Acad. Sci. U.S.A. 100, 7569-7574 (2003).
56. Y. Zhang, S. Goldman, R. Baerga, Y. Zhao, M. Komatsu, S. Jin, Adipose-specific deletion of autophagy-related gene 7 (atg7) in mice reveals a role in adipogenesis. Proc. Natl. Acad. Sci. U.S.A. 106, 19860-19865 (2009).
57. C. Dani, A. G. Smith, S. Dessolin, P. Leroy, L. Staccini, P. Villageois, C. Darimont, G. Ailhaud, Differentiation of embryonic stem cells into adipocytes in vitro. J. Cell Sci. 110 (Pt. 11), 1279-1285 (1997).
58. Y. Yin, H. Yuan, C. Wang, N. Pattabiraman, M. Rao, R. G. Pestell, R. I. Glazer, 3-Phosphoinositide-dependent protein kinase-1 activates the peroxisome proliferator-activated receptor-γ and promotes adipocyte differentiation. Mol. Endocrinol. 20, 268-278 (2006).
59. 2+ in insulin-stimulated glucose transport in 3T3-L1 cells. J. Biol. Chem. 276, 27816-27824 (2001).
60. S. A. Harrison, J. M. Buxton, B. M. Clancy, M. P. Czech, Insulin regulation of hexose transport in mouse 3T3-L1 cells expressing the human HepG2 glucose transporter. J. Biol. Chem. 265, 20106-20116 (1990).