Sestrin2 is induced by glucose starvation via the unfolded protein response and protects cells from non-canonical necroptotic cell death

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Ding, Boxiao ^a   Parmigiani, Anita ^a   Divakaruni, Ajit S ^b   Archer, Kellie ^a   Murphy, Anne N ^b   Budanov, Andrei V ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b San Diego   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ATF4 PROTEIN, MOUSE; GLUCOSE; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; NFE2L2 PROTEIN, MOUSE; NUCLEAR PROTEIN; REACTIVE OXYGEN METABOLITE; SESTRIN 2 PROTEIN, MOUSE; TARGET OF RAPAMYCIN KINASE; TRANSCRIPTION FACTOR NRF2;

ANIMAL; APOPTOSIS; BIOSYNTHESIS; ENDOPLASMIC RETICULUM STRESS; KNOCKOUT MOUSE; METABOLISM; MOUSE; PHYSIOLOGY; UNFOLDED PROTEIN RESPONSE;

ACTIVATING TRANSCRIPTION FACTOR 4; ANIMALS; APOPTOSIS; ENDOPLASMIC RETICULUM STRESS; GLUCOSE; MICE; MICE, KNOCKOUT; MULTIPROTEIN COMPLEXES; NF-E2-RELATED FACTOR 2; NUCLEAR PROTEINS; REACTIVE OXYGEN SPECIES; TOR SERINE-THREONINE KINASES; UNFOLDED PROTEIN RESPONSE;

EID: 84959467705     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep22538     Document Type: Article

References (59)

1. Lee, A. S. The glucose-regulated proteins: stress induction and clinical applications. Trends in biochemical sciences 26, 504-510 (2001).
2. Mihaylova, M. M. & Shaw, R. J. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat. Cell Biol. 13, 1016-1023 (2011).
3. Senft, D. & Ronai, Z. A. UPR, autophagy, and mitochondria crosstalk underlies the ER stress response. Trends in biochemical sciences 40, 141-148 (2015).
4. Walter, P. & Ron, D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 334, 1081-1086 (2011).
5. Rutkowski, D. T. & Kaufman, R. J. That which does not kill me makes me stronger: adapting to chronic ER stress. Trends in biochemical sciences 32, 469-476 (2007).
6. Rutkowski, D. T. & Kaufman, R. J. All roads lead to ATF4. Developmental cell 4, 442-444 (2003).
7. Cullinan, S. B. & Diehl, J. A. Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. The international journal of biochemistry & cell biology 38, 317-332 (2006).
8. Cullinan, S. B. et al. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Molecular and cellular biology 23, 7198-7209 (2003).
9. Budanov, A. V. et al. Identification of a novel stress-responsive gene Hi95 involved in regulation of cell viability. Oncogene 21, 6017-6031 (2002).
10. Budanov, A. V., Lee, J. H. & Karin, M. Stressin' Sestrins take an aging fight. Embo Mol. Med. 2, 388-400 (2010).
11. Lee, J. H. et al. Maintenance of metabolic homeostasis by sestrin2 and sestrin3. Cell Metab. 16, 311-321 (2012).
12. Budanov, A. V., Sablina, A. A., Feinstein, E., Koonin, E. V. & Chumakov, P. M. Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpD. Science 304, 596-600 (2004).
13. Sablina, A. A. et al. The antioxidant function of the p53 tumor suppressor. Nature medicine 11, 1306-1313 (2005).
14. Budanov, A. V. & Karin, M. p53 target genes sestrin1 and sestrin2 connect genotoxic stress and mTOR signaling. Cell 134, 451-460 (2008).
15. Wullschleger, S., Loewith, R. & Hall, M. N. TOR signaling in growth and metabolism. Cell 124, 471-484 (2006).
16. Laplante, M. & Sabatini, D. M. mTOR signaling in growth control and disease. Cell 149, 274-293 (2012).
17. Lee, J. H. et al. Sestrin as a feedback inhibitor of TOR that prevents age-related pathologies. Science 327, 1223-1228 (2010).
18. Hay, N. & Sonenberg, N. Upstream and downstream of mTOR. Genes & development 18, 1926-1945 (2004).
19. Dann, S. G., Selvaraj, A. & Thomas, G. mTOR Complex1-S6K1 signaling: at the crossroads of obesity, diabetes and cancer. Trends Mol. Med. 13, 252-259 (2007).
20. Parmigiani, A. et al. Sestrins Inhibit mTORC1 Kinase Activation through the GATOR Complex. Cell reports 9, 1281-1291 (2014).
21. Chantranupong, L. et al. The Sestrins Interact with GATOR2 to Negatively Regulate the Amino-Acid-Sensing Pathway Upstream of mTORC1. Cell reports 9, 1-8 (2014).
22. Peng, M., Yin, N. & Li, M. O. Sestrins Function as Guanine Nucleotide Dissociation Inhibitors for Rag GTPases to Control mTORC1 Signaling. Cell 159, 122-133 (2014).
23. Sancak, Y. et al. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141, 290-303 (2010).
24. Ben-Sahra, I. et al. Sestrin2 integrates Akt and mTOR signaling to protect cells against energetic stress-induced death. Cell death and differentiation 20, 611-619 (2013).
25. Shin, B. Y., Jin, S. H., Cho, I. J. & Ki, S. H. Nrf2-ARE pathway regulates induction of Sestrin-2 expression. Free radical biology & medicine 53, 834-841 (2012).
26. Wang, S. et al. ATF4 Gene Network Mediates Cellular Response to the Anticancer PAD Inhibitor YW3-56 in Triple-Negative Breast Cancer Cells. Molecular cancer therapeutics 14, 877-888 (2015).
27. Jones, R. G. et al. AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Molecular cell 18, 283-293 (2005).
28. Bae, S. H. et al. Sestrins activate Nrf2 by promoting p62-dependent autophagic degradation of Keap1 and prevent oxidative liver damage. Cell Metab. 17, 73-84 (2013).
29. Park, H. W. et al. Hepatoprotective role of Sestrin2 against chronic ER stress. Nature communications 5, 4233, doi: 10.1038/ncomms5233 (2014).
30. Ramirez-Peinado, S. et al. Glucose-starved cells do not engage in prosurvival autophagy. The Journal of biological chemistry 288, 30387-30398 (2013).
31. Zinszner, H. et al. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes & development 12, 982-995 (1998).
32. Lee, J. H., Budanov, A. V. & Karin, M. Sestrins orchestrate cellular metabolism to attenuate aging. Cell Metab 18, 792-801 (2013).
33. Vanden Berghe, T., Linkermann, A., Jouan-Lanhouet, S., Walczak, H. & Vandenabeele, P. Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nature reviews. Molecular cell biology 15, 135-147 (2014).
34. Green, D. R., Galluzzi, L. & Kroemer, G. Cell biology. Metabolic control of cell death. Science 345, 1250256, doi: 10.1126/science1250256 (2014).
35. Degterev, A. et al. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nature chemical biology 4, 313-321 (2008).
36. Dixon, S. J. et al. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149, 1060-1072 (2012).
37. Ozcan, U. et al. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313, 1137-1140 (2006).
38. Zheng, W., Degterev, A., Hsu, E., Yuan, J. & Yuan, C. Structure-activity relationship study of a novel necroptosis inhibitor, necrostatin-7. Bioorganic & medicinal chemistry letters 18, 4932-4935 (2008).
39. Divakaruni, A. S., Paradyse, A., Ferrick, D. A., Murphy, A. N. & Jastroch, M. Analysis and interpretation of microplate-based oxygen consumption and pH data. Methods in enzymology 547, 309-354 (2014).
40. Bruning, A., Rahmeh, M. & Friese, K. Nelfinavir and bortezomib inhibit mTOR activity via ATF4-mediated sestrin-2 regulation. Mol. Oncol. 7, 1012-1018 (2013).
41. Yang, J. H. et al. Isorhamnetin protects against oxidative stress by activating Nrf2 and inducing the expression of its target genes. Toxicology and applied pharmacology 274, 293-301 (2014).
42. He, C. H. et al. Identification of activating transcription factor 4 (ATF4) as an Nrf2-interacting protein. Implication for heme oxygenase-1 gene regulation. The Journal of biological chemistry 276, 20858-20865 (2001).
43. Ye, P. et al. Nrf2-and ATF4-dependent upregulation of xCT modulates the sensitivity of T24 bladder carcinoma cells to proteasome inhibition. Molecular and cellular biology 34, 3421-3434 (2014).
44. Budanov, A. V. Stress-responsive sestrins link p53 with redox regulation and mammalian target of rapamycin signaling. Antioxid. Redox. Signal. 15, 1679-1690 (2011).
45. Seo, K., Ki, S. H. & Shin, S. M. Sestrin2-AMPK activation protects mitochondrial function against glucose deprivation-induced cytotoxicity. Cellular signalling 27, 1533-1543 (2015).
46. Zamaraeva, M. V. et al. Cells die with increased cytosolic ATP during apoptosis: a bioluminescence study with intracellular luciferase. Cell death and differentiation 12, 1390-1397 (2005).
47. Morrison, A. et al. Sestrin2 promotes LKB1-mediated AMPK activation in the ischemic heart. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 29, 408-417 (2014).
48. Bonora, M. et al. Molecular mechanisms of cell death: central implication of ATP synthase in mitochondrial permeability transition. Oncogene 34, 1475-1486 (2015).
49. Leist, M., Single, B., Castoldi, A. F., Kuhnle, S. & Nicotera, P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. The Journal of experimental medicine 185, 1481-1486 (1997).
50. Kim, J. S. et al. Sestrin2 inhibits mTORC1 through modulation of GATOR complexes. Scientific reports 5, 9502, doi: 10.1038/srep02696 (2015).
51. Algret, R. et al. Molecular architecture and function of the SEA complex, a modulator of the TORC1 pathway. Mol. Cell Proteomics 13, 2855-2870 (2014).
52. Dokudovskaya, S. & Rout, M. P. SEA you later alli-GATOR - a dynamic regulator of the TORC1 stress response pathway. Journal of cell science 128, 2219-2228 (2015).
53. Liu, S. Y., Lee, Y. J. & Lee, T. C. Association of platelet-derived growth factor receptor beta accumulation with increased oxidative stress and cellular injury in sestrin 2 silenced human glioblastoma cells. FEBS Lett. 585, 1853-1858 (2011).
54. Ding, B., Parmigiani, A., Yang, C. & Budanov, A. V. Sestrin2 facilitates death receptor-induced apoptosis in lung adenocarcinoma cells through regulation of XIAP degradation. Cell cycle, 14, 3231-3241 (2015).
55. Fayaz, S. M., Suvanish Kumar, V. S. & Rajanikant, G. K. Necroptosis: who knew there were so many interesting ways to die? CNS & neurological disorders drug targets 13, 42-51 (2014).
56. Cazanave, S. C. et al. Degradation of Keap1 activates BH3-only proteins Bim and PUMA during hepatocyte lipoapoptosis. Cell death and differentiation 21, 1303-1312 (2014).
57. Mookerjee, S. A., Goncalves, R. L., Gerencser, A. A., Nicholls, D. G. & Brand, M. D. The contributions of respiration and glycolysis to extracellular acid production. Biochimica et biophysica acta 1847, 171-181 (2015).
58. Divakaruni, A. S. et al. Thiazolidinediones are acute, specific inhibitors of the mitochondrial pyruvate carrier. Proceedings of the National Academy of Sciences of the United States of America 110, 5422-5427 (2013).
59. Divakaruni, A. S., Rogers, G. W. & Murphy, A. N. Measuring Mitochondrial Function in Permeabilized Cells Using the Seahorse XF Analyzer or a Clark-Type Oxygen Electrode. Current protocols in toxicology/editorial board, Mahin D. Maines 60, 25.2.1-25.2.16 (2014).