Regulation of mTOR and cell growth in response to energy stress by REDD1

Molecular and Cellular Biology

Volumn 25, Issue 14, 2005, Pages 5834-5845

  Sofer, Avi ^a   Lei, Kui ^a   Johannessen, Cory M ^a   Ellisen, Leif W ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; HAMARTIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MAMMALIAN TARGET OF RAPAMYCIN; SMALL INTERFERING RNA; TETRACYCLINE; TUBERIN;

ANIMAL CELL; ARTICLE; CELL GROWTH; CELL SIZE; CONTROLLED STUDY; DEPHOSPHORYLATION; EMBRYO; ENZYME PHOSPHORYLATION; ENZYME REGULATION; GENE IDENTIFICATION; HUMAN; HUMAN CELL; HYPOXIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; REDD1 GENE; REGULATOR GENE; STRESS;

ANIMALS; CELL SIZE; ENERGY METABOLISM; ENZYME ACTIVATION; HUMANS; MICE; MONOMERIC GTP-BINDING PROTEINS; NEUROPEPTIDES; PHOSPHORYLATION; PROTEIN KINASES; REPRESSOR PROTEINS; RNA INTERFERENCE; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 21744459535     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.14.5834-5845.2005     Document Type: Article

References (58)

1. Arsham, A. M., J. J. Howell, and M. C. Simon. 2003. A novel hypoxia-inducible factor-independent hypoxic response regulating mammalian target of rapamycin and its targets. J. Biol. Chem. 278:29655-29660.
2. Brafman, A., I. Mett, M. Shafir, H. Gottlieb, G. Damari, S. Gozlan-Kelner, V. Vishnevskia-Dai, R. Skaliter, P. Einat, A. Faerman, E. Feinstein, and T. Shoshani. 2004. Inhibition of oxygen-induced retinopathy in RTP801-deficient mice. Investig. Ophthalmol. Vis. Sci. 45:3796-3805.
3. Brugarolas, J., K. Lei, R. L. Hurley, B. D. Manning, J. H. Reiling, E. Hafen, L. A. Witters, L. W. Ellisen, and W. G. Kaelin, Jr. 2004. Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev. 18:2893-2904.
4. Burnett, P. E., R. K. Barrow, N. A. Cohen, S. H. Snyder, and D. M. Sabatini. 1998. RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. Proc. Natl. Acad. Sci. USA 95:1432-1437.
5. Cantley, L. C. 2002. The phosphoinositide 3-kinase pathway. Science 296:1655-1657.
6. Carling, D. 2004. The AMP-activated protein kinase cascade-a unifying system for energy control. Trends Biochem. Sci. 29:18-24.
7. Cheadle, J. P., M. P. Reeve, J. R. Sampson, and D. J. Kwiatkowski. 2000. Molecular genetic advances in tuberous sclerosis. Hum. Genet. 107:97-114.
8. Corradetti, M. N., K. Inoki, N. Bardeesy, R. A. DePinho, and K. L. Guan. 2004. Regulation of the TSC pathway by LKB1: evidence of a molecular link between tuberous sclerosis complex and Peutz-Jeghers syndrome. Genes Dev. 18:1533-1538.
9. Corradetti, M. N., K. Inoki, and K. L. Guan. 2005. The stress-inducted proteins RTP801 and RTP801L are negative regulators of the mammalian target of rapamycin pathway. J. Biol. Chem. 280:9769-9772.
10. Dan, H. C., M. Sun, L. Yang, R. I. Feldman, X. M. Sui, C. C. Ou, M. Nellist, R. S. Yeung, D. J. Halley, S. V. Nicosia, W. J. Pledger, and J. Q. Cheng. 2002. Phosphatidylinositol 3-kinase/Akt pathway regulates tuberous sclerosis tumor suppressor complex by phosphorylation of tuberin. J. Biol. Chem. 277:35364-35370.
11. Dufner, A., and G. Thomas. 1999. Ribosomal S6 kinase signaling and the control of translation. Exp. Cell Res. 253:100-109.
12. Ellisen, L. W., N. Carlesso, T. Cheng, D. T. Scadden, and D. A. Haber. 2001. The Wilms tumor suppressor WT1 directs stage-specific quiescence and differentiation of human hematopoietic progenitor cells. EMBO J. 20:1897-1909.
13. Ellisen, L. W., R. E. Palmer, R. G. Maki, V. B. Truong, P. Tamayo, J. D. Oliner, and D. A. Haber. 2001. Cascades of transcriptional induction during human lymphocyte activation. Eur. J. Cell Biol. 80:321-328.
14. Ellisen, L. W., K. D. Ramsayer, C. M. Johannessen, A. Yang, H. Beppu, K. Minda, J. D. Oliner, F. McKeon, and D. A. Haber. 2002. REDD1, a developmentally regulated transcriptional target of p63 and p53, links p63 to regulation of reactive oxygen species. Mol. Cell 10:995-1005.
15. 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.
16. Fingar, D. C., C. J. Richardson, A. R. Tee, L. Cheatham, C. Tsou, and J. Blenis. 2004. mTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E. Mol. Cell Biol. 24:200-216.
17. Fingar, D. C., S. Salama, C. Tsou, E. Harlow, and J. Blenis. 2002. Mammalian cell size is controlled by mTOR and its downstream targets S6K1 and 4EBP1/eIF4E. Genes Dev. 16:1472-1487.
18. Gao, X., and D. Pan. 2001. TSC1 and TSC2 tumor suppressors antagonize insulin signaling in cell growth. Genes Dev. 15:1383-1392.
19. Garami, A., F. J. Zwartkruis, T. Nobukuni, M. Joaquin, M. Roccio, H. Stocker, S. C. Kozma, E. Hafen, J. L. Bos, and G. Thomas. 2003. Insulin activation of Rheb, a mediator of mTOR/S6K/4E-BP signaling, is inhibited by TSC1 and 2. Mol. Cell 11:1457-1466.
20. Gingras, A. C., S. G. Kennedy, M. A. O'Leary, N. Sonenberg, and N. Hay. 1998. 4E-BP1, a repressor of mRNA translation, is phosphorylated and inactivated by the Akt(PKB) signaling pathway. Genes Dev. 12:502-513.
21. Gingras, A. C., B. Raught, S. P. Gygi, A. Niedzwiecka, M. Miron, S. K. Burley, R. D. Polakiewicz, A. Wyslouch-Cieszynska, R. Aebersold, and N. Sonenberg. 2001. Hierarchical phosphorylation of the translation inhibitor 4E-BP1. Genes Dev. 15:2852-2864.
22. Gingras, A. C., B. Raught, and N. Sonenberg. 2001. Regulation of translation initiation by FRAP/mTOR. Genes Dev. 15:807-826.
23. Ha, J., S. Daniel, S. S. Broyles, and K. H. Kim. 1994. Critical phosphorylation sites for acetyl-CoA carboxylase activity. J. Biol. Chem. 269:22162-22168.
24. Hardie, D. G. 2004. The AMP-activated protein kinase pathway-new players upstream and downstream. J. Cell Sci. 117:5479-5487.
25. Harrington, L. S., G. M. Findlay, A. Gray, T. Tolkacheva, S. Wigfield, H. Rebholz, J. Barnett, N. R. Leslie, S. Cheng, P. R. Shepherd, I. Gout, C. P. Downes, and R. F. Lamb. 2004. The TSC1-2 tumor suppressor controls insulin-PI3K signaling via regulation of IRS proteins. J. Cell Biol. 166:213-223.
26. Harvey, M., A. T. Sands, R. S. Weiss, M. E. Hegi, R. W. Wiseman, P. Pantazis, B. C. Giovanella, M. A. Tainsky, A. Bradley, and L. A. Donehower. 1993. In vitro growth characteristics of embryo fibroblasts isolated from p53-deficient mice. Oncogene 8:2457-2467.
27. Hay, N., and N. Sonenberg. 2004. Upstream and downstream of mTOR. Genes Dev. 18:1926-1945.
28. Hogan, G., R. Beddington, F. Costantini, and E. Lacy. 1994. Manipulating the mouse embryo, a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
29. Inoki, K., M. N. Corradetti, and K. L. Guan. 2005. Dysregulation of the TSC-mTOR pathway in human disease. Nat. Genet. 37:19-24.
30. Inoki, K., Y. Li, T. Xu, and K. L. Guan. 2003. Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev. 17:1829-1834.
31. Inoki, K., Y. Li, T. Zhu, J. Wu, and K. L. Guan. 2002. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat. Cell Biol. 4:648-657.
32. Inoki, K., T. Zhu, and K. L. Guan. 2003. TSC2 mediates cellular energy response to control cell growth and survival. Cell 115:577-590.
33. Kwiatkowski, D. J., H. Zhang, J. L. Bandura, K. M. Heiberger, M. Glogauer, N. el-Hashemite, and H. Onda. 2002. A mouse model of TSC1 reveals sex-dependent lethality from liver hemangiomas, and up-regulation of p70S6 kinase activity in Tscl null cells. Hum. Mol. Genet. 11:525-534.
34. Li, E., T. H. Bestor, and R. Jaenisch. 1992. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69:915-926.
35. Li, Y., M. N. Corradetti, K. Inoki, and K. L. Guan. 2004. TSC2: filling the GAP in the mTOR signaling pathway. Trends Biochem. Sci. 29:32-38.
36. Li, Y., K. Inoki, and K. L. Guan. 2004. Biochemical and functional characterizations of small GTPase Rheb and TSC2 GAP activity. Mol. Cell. Biol. 24:7965-7975.
37. Manning, B. D., A. R. Tee, M. N. Logsdon, J. Blenis, and L. C. Cantley. 2002. Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/akt pathway. Mol. Cell 10:151-162.
38. Minokoshi, Y., T. Alquier, N. Furukawa, Y. B. Kim, A. Lee, B. Xue, J. Mu, F. Foufelle, P. Ferre, M. J. Birnbaum, B. J. Stuck, and B. B. Kahn. 2004. AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature 428:569-574.
39. Pan, D., J. Dong, Y. Zhang, and X. Gao. 2004. Tuberous sclerosis complex: from Drosophila to human disease. Trends Cell Biol. 14:78-85.
40. Potter, C. J., H. Huang, and T. Xu. 2001. Drosophila Tsc1 functions with Tsc2 to antagonize insulin signaling in regulating cell growth, cell proliferation, and organ size. Cell 105:357-368.
41. Potter, C. J., L. G. Pedraza, and T. Xu. 2002. Akt regulates growth by directly phosphorylating Tsc2. Nat. Cell Biol. 4:658-665.
42. Reiling, J. H., and E. Hafen. 2004. The hypoxia-induced paralogs Scylla and Charybdis inhibit growth by down-regulating S6K activity upstream of TSC in Drosophila. Genes Dev. 18:2879-2892.
43. Saucedo, L. J., X. Gao, D. A. Chiarelli, L. Li, D. Pan, and B. A. Edgar. 2003. Rheb promotes cell growth as a component of the insulin/TOR signalling network. Nat. Cell Biol. 5:566-571.
44. Shah, O. J., Z. Wang, and T. Hunter. 2004. Inappropriate activation of the TSC/Rheb/mTOR/S6K cassette induces IRS1/2 depletion, insulin resistance, and cell survival deficiencies. Curr. Biol. 14:1650-1656.
45. Shaw, R. J., N. Bardeesy, B. D. Manning, L. Lopez, M. Kosmatka, R. A. DePinho, and L. C. Cantley. 2004. The LKB1 tumor suppressor negatively regulates mTOR signaling. Cancer Cell 6:91-99.
46. Shaw, R. J., M. Kosmatka, N. Bardeesy, R. L. Hurley, L. A. Witters, R. A. DePinho, and L. C. Cantley. 2004. The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proc. Natl. Acad. Sci. USA 101:3329-3335.
47. Shibata, R., N. Ouchi, M. Ito, S. Kihara, I. Shiojima, D. R. Pimentel, M. Kumada, K. Sato, S. Schiekofer, K. Ohashi, T. Funahashi, W. S. Colucci, and K. Walsh. 2004. Adiponectin-mediated modulation of hypertrophic signals in the heart. Nat. Med. 10:1384-1389.
48. Shoshani, T., A. Faerman, I. Mett, E. Zelin, T. Tenne, S. Gorodin, Y. Moshel, S. Elbaz, A. Budanov, A. Chajut, H. Kalinski, I. Kamer, A. Rozen, O. Mor, E. Keshet, D. Leshkowitz, P. Einat, R. Skaliter, and E. Feinstein. 2002. Identification of a novel hypoxia-inducible factor 1-responsive gene. RTP801, involved in apoptosis. Mol. Cell. Biol. 22:2283-2293.
49. Sonenberg, N., and A. C. Gingras. 1998. The mRNA 5′ cap-binding protein eIF4E and control of cell growth. Curr. Opin. Cell Biol. 10:268-275.
50. Stocker, H., T. Radimerski, B. Schindelholz, F. Wittwer, P. Belawat, P. Daram, S. Breuer, G. Thomas, and E. Hafen. 2003. Rheb is an essential regulator of S6K in controlling cell growth in Drosophila. Nat. Cell Biol. 5:559-565.
51. Stolovich, M., H. Tang, E. Hornstein, G. Levy, R. Cohen, S. S. Bae, M. J. Birnbaum, and O. Meyuhas. 2002. Transduction of growth or mitogenic signals into translational activation of TOP mRNAs is fully reliant on the phosphatidylinositol 3-kinase-mediated pathway but requires neither S6K1 nor rpS6 phosphorylation. Mol. Cell. Biol. 22:8101-8113.
52. Sui, G., C. Soohoo, E. B. Affar, F. Gay, Y. Shi, W. C. Forrester, and Y. Shi. 2002. A DNA-based RNAi technology to suppress gene expression in mammalian cells. Proc. Natl. Acad. Sci. USA 99:5515-5520.
53. Tang, H., E. Hornstein, M. Stolovich, G. Levy, M. Livingstone, D. Templeton, J. Avruch, and O. Meyuhas. 2001. Amino acid-induced translation of TOP mRNAs is fully dependent on phosphatidylinositol 3-kinase-mediated signaling, is partially inhibited by rapamycin, and is independent of S6K1 and rpS6 phosphorylation. Mol. Cell. Biol. 21:8671-8683.
54. Tapon, N., N. Ito, B. J. Dickson, J. E. Treisman, and I. K. Hariharan. 2001. The Drosophila tuberous sclerosis complex gene homologs restrict cell growth and cell proliferation. Cell 105:345-355.
55. Tee, A. R., B. D. Manning, P. P. Roux, L. C. Cantley, and J. Blenis. 2003. Tuberous sclerosis complex gene products, Tuberin and Hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb. Curr. Biol. 13:1259-1268.
56. Wang, Z., M. H. Malone, M. J. Thomenius, F. Zhong, F. Xu, and C. W. Distelhorst. 2003. Dexamethasone-induced gene 2 (dig2) is a novel prosurvival stress gene induced rapidly by diverse apoptotic signals. J. Biol. Chem. 278:27053-27058.
57. Wendel, H. G., E. De Stanchina, J. S. Fridman, A. Malina, S. Ray, S. Kogan, C. Cordon-Cardo, J. Pelletier, and S. W. Lowe. 2004. Survival signalling by Akt and eIF4E in oncogenesis and cancer therapy. Nature 428:332-337.
58. Zhang, H., G. Cicchetti, H. Onda, H. B. Koon, K. Asrican, N. Bajraszewski, F. Vazquez, C. L. Carpenter, and D. J. Kwiatkowski. 2003. Loss of Tsc1/Tsc2 activates mTOR and disrupts PI3K-Akt signaling through downregulation of PDGFR. J. Clin. Investig. 112:1223-1233.