Sestrin regulation of TORC1: Is sestrin a leucine sensor?

Science Signaling

Volumn 9, Issue 431, 2016, Pages

  Lee, Jun Hee ^a   Cho, Uhn Soo ^a   Karin, Michael ^b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE KINASE; LEUCINE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; SESTRIN; TUBERIN; UNCLASSIFIED DRUG; HEAT SHOCK PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LIPID; NUCLEAR PROTEIN; SESN1 PROTEIN, HUMAN;

BINDING AFFINITY; CONFORMATIONAL TRANSITION; DROSOPHILA; HUMAN; MAMMAL; MUSCLE ATROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REVIEW; SENSOR; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; DRUG EFFECTS; INSULIN RESISTANCE; LIPID METABOLISM; LYSOSOME; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; HEAT-SHOCK PROTEINS; HUMANS; INSULIN RESISTANCE; LEUCINE; LIPID METABOLISM; LIPIDS; LYSOSOMES; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MODELS, BIOLOGICAL; MODELS, MOLECULAR; NUCLEAR PROTEINS; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION;

EID: 84973480905     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aaf2885     Document Type: Review

References (44)

1. S. Velasco-Miguel, L. Buckbinder, P. Jean, L. Gelbert, R. Talbott, J. Laidlaw, B. Seizinger, N. Kley, PA26, a novel target of the p53 tumor suppressor and member of the GADD family of DNA damage and growth arrest inducible genes. Oncogene 18, 127-137 (1999).
2. A. V. Budanov, T. Shoshani, A. Faerman, E. Zelin, I. Kamer, H. Kalinski, S. Gorodin, A. Fishman, A. Chajut, P. Einat, R. Skaliter, A. V. Gudkov, P. M. Chumakov, E. Feinstein, Identification of a novel stress-responsive gene Hi95 involved in regulation of cell viability. Oncogene 21, 6017-6031 (2002).
3. J. H. Lee, A. V. Budanov, M. Karin, Sestrins orchestrate cellular metabolism to attenuate aging. Cell Metab. 18, 792-801 (2013).
4. A. V. Budanov, M. Karin, p53 target genes sestrin1 and sestrin2 connect genotoxic stress and mTOR signaling. Cell 134, 451-460 (2008).
5. T. Sanli, K. Linher-Melville, T. Tsakiridis, G. Singh, Sestrin2 modulates AMPK subunit expression and its response to ionizing radiation in breast cancer cells. PLOS One 7, e32035 (2012).
6. A. Morrison, L. Chen, J. Wang, M. Zhang, H. Yang, Y. Ma, A. Budanov, J. H. Lee, M. Karin, J. Li, Sestrin2 promotes LKB1-mediated AMPK activation in the ischemic heart. FASEB J. 29, 408-417 (2015).
7. J. H. Lee, A. V. Budanov, E. J. Park, R. Birse, T. E. Kim, G. A. Perkins, K. Ocorr, M. H. Ellisman, R. Bodmer, E. Bier, M. Karin, Sestrin as a feedback inhibitor of TOR that prevents age related pathologies. Science 327, 1223-1228 (2010).
8. J. H. Lee, A. V. Budanov, S. Talukdar, E. J. Park, H. Park, H.-W. Park, G. Bandyopadhyay, N. Li, M. Aghajan, I. Jang, A. M. Wolfe, G. A. Perkins, M. H. Ellisman, E. Bier, M. Scadeng, M. Foretz, B. Viollet, J. Olefsky, M. Karin, Maintenance of metabolic homeostasis by Sestrin2 and Sestrin3. Cell Metab. 16, 311-321 (2012).
9. H.-W. Park, H. Park, S.-H. Ro, I. Jang, I. A. Semple, D. N. Kim, M. Kim, M. Nam, D. Zhang, L. Yin, J. H. Lee, Hepatoprotective role of Sestrin2 against chronic ER stress. Nat. Commun. 5, 4233 (2014).
10. S. G. Rhee, S. H. Bae, The antioxidant function of sestrins is mediated by promotion of autophagic degradation of Keap1 and Nrf2 activation and by inhibition of mTORC1. Free Radic. Biol. Med. 88, 205-211 (2015).
11. A. V. Budanov, A. A. Sablina, E. Feinstein, E. V. Koonin, P. M. Chumakov, Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpD. Science 304, 596-600 (2004).
12. H. Kim, S. An, S.-H. Ro, F. Teixeira, G. J. Park, C. Kim, C.-S. Cho, J.-S. Kim, U. Jakob, J. H. Lee, U.-S. Cho, Janus-faced Sestrin2 controls ROS and mTOR signalling through two separate functional domains. Nat. Commun. 6, 10025 (2015).
13. R. Tao, X. Xiong, S. Liangpunsakul, X. C. Dong, Sestrin 3 protein enhances hepatic insulin sensitivity by direct activation of the mTORC2-Akt signaling. Diabetes 64, 1211-1223 (2015).
14. B. Ding, A. Parmigiani, C. Yang, A. V. Budanov, Sestrin2 facilitates death receptor induced apoptosis in lung adenocarcinoma cells through regulation of XIAP degradation. Cell Cycle 14, 3231-3241 (2015).
15. M. Peng, N. Yin, M. O. Li, Sestrins function as guanine nucleotide dissociation inhibitors for Rag GTPases to control mTORC1 signaling. Cell 159, 122-133 (2014).
16. A. Parmigiani, A. Nourbakhsh, B. Ding, W. Wang, Y. C. Kim, K. Akopiants, K.-L. Guan, M. Karin, A. V. Budanov, Sestrins inhibit mTORC1 kinase activation through the GATOR complex. Cell Rep. 9, 1281-1291 (2014).
17. J. S. Kim, S.-H. Ro, M. Kim, H.-W. Park, I. A. Semple, H. L. Park, U.-S. Cho, W. Wang, K.-L. Guan, M. Karin, J. H. Lee, Sestrin2 inhibits mTOR through modulation of GATOR complexes. Sci. Rep. 5, 9502 (2015).
18. Y. Li, M. N. Corradetti, K. Inoki, K.-L. Guan, TSC2: Filling the GAP in the mTOR signaling pathway. Trends Biochem. Sci. 29, 32-38 (2004).
19. J. Kim, K.-L. Guan, Amino acid signaling in TOR activation. Annu. Rev. Biochem. 80, 1001-1032 (2011).
20. J. L. Jewell, K.-L. Guan, Nutrient signaling to mTOR and cell growth. Trends Biochem. Sci. 38, 233-242 (2013).
21. L. Chantranupong, R. L. Wolfson, D. M. Sabatini, Nutrient-sensing mechanisms across evolution. Cell 161, 67-83 (2015).
22. J. L. Jewell, Y. C. Kim, R. C. Russell, F.-X. Yu, H. W. Park, S. W. Plouffe, V. S. Tagliabracci, K.-L. Guan, Differential regulation of mTORC1 by leucine and glutamine. Science 347, 194-198 (2015).
23. J. D. Thomas, Y.-J. Zhang, Y.-H. Wei, J.-H. Cho, L. E. Morris, H.-Y. Wang, X. F. Zheng, Rab1A is an mTORC1 activator and a colorectal oncogene. Cancer Cell 26, 754-769 (2014).
24. A. Efeyan, L. D. Schweitzer, A. M. Bilate, S. Chang, O. Kirak, D. W. Lamming, D. M. Sabatini, RagA, but Not RagB, is essential for embryonic development and adult mice. Dev. Cell 29, 321-329 (2014).
25. Y. C. Kim, H. W. Park, S. Sciarretta, J.-S. Mo, J. L. Jewell, R. C. Russell, X. Wu, J. Sadoshima, K.-L. Guan, Rag GTPases are cardioprotective by regulating lysosomal function. Nat. Commun. 5, 4241 (2014).
26. N. Oshiro, J. Rapley, J. Avruch, Amino acids activate mammalian target of rapamycin (mTOR) complex 1 without changing Rag GTPase guanyl nucleotide charging. J. Biol. Chem. 289, 2658-2674 (2014).
27. K. Shen, H. Sidik, W. Talbot, The Rag-Ragulator complex regulates lysosome function and phagocytic flux in microglia. Cell Rep. 14, 547-559 (2016).
28. J. Jung, H. M. Genau, C. Behrends, Amino acid-dependent mTORC1 regulation by the lysosomal membrane protein SLC38A9. Mol. Cell Biol. 35, 2479-2494 (2015).
29. M. Rebsamen, L. Pochini, T. Stasyk, M. E. G. de Araújo, M. Galluccio, R. K. Kandasamy, B. Snijder, A. Fauster, E. L. Rudashevskaya, M. Bruckner, S. Scorzoni, P. A. Filipek, K. V. M. Huber, J. W. Bigenzahn, L. X. Heinz, C. Kraft, K. L. Bennett, C. Indiveri, L. A. Huber, G. Superti-Furga, SLC38A9 is a component of the lysosomal amino acid sensing machinery that controls mTORC1. Nature 519, 477-481 (2015).
30. S. Wang, Z.-Y. Tsun, R. L. Wolfson, K. Shen, G. A. Wyant, M. E. Plovanich, E. D. Yuan, T. D. Jones, L. Chantranupong, W. Comb, T. Wang, L. Bar-Peled, R. Zoncu, C. Straub, C. Kim, J. Park, B. L. Sabatini, D. M. Sabatini, Lysosomal amino acid transporter SLC38A9 signals arginine sufficiency to mTORC1. Science 347, 188-194 (2015).
31. J. M. Han, S. J. Jeong, M. C. Park, G. Kim, N. H. Kwon, H. K. Kim, S. H. Ha, S. H. Ryu, S. Kim, Leucyl-tRNA synthetase is an intracellular leucine sensor for the mTORC1 signaling pathway. Cell 149, 410-424 (2012).
32. Z.-Y. Tsun, L. Bar-Peled, L. Chantranupong, R. Zoncu, T. Wang, C. Kim, E. Spooner, D. M. Sabatini, The folliculin tumor suppressor is a GAP for the RagC/D GTPases that signal amino acid levels to mTORC1. Mol. Cell 52, 495-505 (2013).
33. G. Bonfils, M. Jaquenoud, S. Bontron, C. Ostrowicz, C. Ungermann, C. De Virgilio, Leucyl-tRNA synthetase controls TORC1 via the EGO complex. Mol. Cell 46, 105-110 (2012).
34. S. Dokudovskaya, M. P. Rout, SEA you later alli-GATOR-a dynamic regulator of the TORC1 stress response pathway. J. Cell Sci. 128, 2219-2228 (2015).
35. L. Bar-Peled, L. Chantranupong, A. D. Cherniack, W. W. Chen, K. A. Ottina, B. C. Grabiner, E. D. Spear, S. L. Carter, M. Meyerson, D. M. Sabatini, A tumor suppressor complex with GAP activity for the Rag GTPases that signal amino acid sufficiency to mTORC1. Science 340, 1100-1106 (2013).
36. L. Chantranupong, R. L. Wolfson, J. M. Orozco, R. A. Saxton, S. M. Scaria, L. Bar-Peled, E. Spooner, M. Isasa, S. P. Gygi, D. M. Sabatini, The Sestrins interact with GATOR2 to negatively regulate the amino-acid-sensing pathway upstream of mTORC1. Cell Rep. 9, 1-8 (2014).
37. R. A. Saxton, K. E. Knockenhauer, R. L. Wolfson, L. Chantranupong, M. E. Pacold, T. Wang, T. U. Schwartz, D. M. Sabatini, Structural basis for leucine sensing by the Sestrin2-mTORC1 pathway. Science 351, 53-58 (2016).
38. R. L. Wolfson, L. Chantranupong, R. A. Saxton, K. Shen, S. M. Scaria, J. R. Cantor, D. M. Sabatini, Sestrin2 is a leucine sensor for the mTORC1 pathway. Science 351, 43-48 (2016).
39. X. Chen, J.-J. Ma, M. Tan, P. Yao, Q.-H. Hu, G. Eriani, E.-D. Wang, Modular pathways for editing non-cognate amino acids by human cytoplasmic leucyl-tRNA synthetase. Nucleic Acids Res. 39, 235-247 (2011).
40. C.-C. Chen, S.-M. Jeon, P. T. Bhaskar, V. Nogueira, D. Sundararajan, I. Tonic, Y. Park, N. Hay, FoxOs inhibit mTORC1 and activate Akt by inducing the expression of Sestrin3 and Rictor. Dev. Cell 18, 592-604 (2010).
41. J. Ye, W. Palm, M. Peng, B. King, T. Lindsten, M. O. Li, C. Koumenis, C. B. Thompson, GCN2 sustains mTORC1 suppression upon amino acid deprivation by inducing Sestrin2. Genes Dev. 29, 2331-2336 (2015).
42. J. Gallinetti, E. Harputlugil, J. R. Mitchell, Amino acid sensing in dietary-restriction-mediated longevity: Roles of signal-transducing kinases GCN2 and TOR. Biochem. J. 449, 1-10 (2013).
43. F. Guo, D. R. Cavener, The GCN2 eIF2α kinase regulates fatty-acid homeostasis in the liver during deprivation of an essential amino acid. Cell Metab. 5, 103-114 (2007).
44. Y.-L. Yang, K.-S. Loh, B.-Y. Liou, I.-H. Chu, C.-J. Kuo, H.-D. Chen, C.-S. Chen, SESN-1 is a positive regulator of lifespan in Caenorhabditis elegans. Exp. Gerontol. 48, 371-379 (2013).