Endoplasmic reticulum (ER) stress induces sirtuin 1 (SIRT1) expression via the PI3K-Akt-GSK3β signaling pathway and promotes hepatocellular injury

Journal of Biological Chemistry

Volumn 290, Issue 51, 2015, Pages 30366-30374

  Koga, Tomoaki ^a,b   Suico, Mary Ann ^a   Shimasaki, Shogo ^a   Watanabe, Eriko ^a   Kai, Yukari ^a   Koyama, Kosuke ^a   Omachi, Kohei ^a   Morino Koga, Saori ^a   Sato, Takashi ^a   Shuto, Tsuyoshi ^a   Mori, Kazutoshi ^c   Hino, Shinjiro ^a   Nakao, Mitsuyoshi ^a   Kai, Hirofumi ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DIAGNOSIS; PULMONARY DISEASES;

BIOLOGICAL PROCESS; CHRONIC OBSTRUCTIVE PULMONARY DISEASE; ENDOPLASMIC RETICULUM STRESS; HISTONE DEACETYLASES; INHIBITOR SCREENINGS; MOLECULAR MECHANISM; PHARMACOLOGICAL INHIBITION; SIGNALING PATHWAYS;

CELL MEMBRANES;

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; GLYCOGEN SYNTHASE KINASE 3BETA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SELISISTAT; SIRTUIN 1; X BOX BINDING PROTEIN 1; 6-CHLORO-2,3,4,9-TETRAHYDRO-1H-CARBAZOLE-1-CARBOXAMIDE; CARBAZOLE DERIVATIVE; GLYCOGEN SYNTHASE KINASE 3; GSK3B PROTEIN, HUMAN; GSK3B PROTEIN, MOUSE; SIRT1 PROTEIN, HUMAN; SIRT1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; DISEASE SEVERITY; EMBRYO; ENDOPLASMIC RETICULUM STRESS; ENZYME INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL DAMAGE; LIVER INJURY; MALE; MOLECULAR MODEL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; LIVER CELL; METABOLISM; PATHOLOGY;

ANIMALS; CARBAZOLES; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; HEK293 CELLS; HEPATOCYTES; HUMANS; MICE; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SIRTUIN 1; TRANSCRIPTION FACTORS;

EID: 84950312175     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.664169     Document Type: Article

References (36)

1. Ellgaard, L., and Helenius, A. (2003) Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 4, 181-191
2. Hetz, C., and Mollereau, B. (2014) Disturbance of endoplasmic reticulum proteostasis in neurodegenerative diseases. Nat. Rev. Neurosci. 15, 233-249
3. Xu, C., Bailly-Maitre, B., and Reed, J. C. (2005) Endoplasmic reticulum stress: cell life and death decisions. J. Clin. Investig. 115, 2656-2664
4. Hetz, C. (2012) The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell Biol. 13, 89-102
5. Hetz, C., Chevet, E., and Harding, H. P. (2013) Targeting the unfolded protein response in disease. Nat. Rev. Drug. Discov. 12, 703-719
6. Jorgensen, E., Stinson, A., Shan, L., Yang, J., Gietl, D., and Albino, A. P. (2008) Cigarette smoke induces endoplasmic reticulum stress and the unfolded protein response in normal and malignant human lung cells. BMC Cancer 8, 229
7. Min, T., Bodas, M., Mazur, S., and Vij, N. (2011) Critical role of proteostasis-imbalance in pathogenesis of COPD and severe emphysema. J. Mol. Med. 89, 577-593
8. Deng, C. X. (2009) SIRT1, is it a tumor promoter or tumor suppressor? Int. J. Biol. Sci. 5, 147-152
9. Raynes, R., Brunquell, J., and Westerheide, S. D. (2013) Stress inducibility of SIRT1 and its role in cytoprotection and cancer. Genes Cancer 4, 172-182
10. Houtkooper, R. H., Pirinen, E., and Auwerx, J. (2012) Sirtuins as regulators of metabolism and healthspan. Nat. Rev. Mol. Cell Biol. 13, 225-238
11. Wang, C., Chen, L., Hou, X., Li, Z., Kabra, N., Ma, Y., Nemoto, S., Finkel, T., Gu, W., Cress, W. D., and Chen, J. (2006) Interactions between E2F1 and SirT1 regulate apoptotic response to DNA damage. Nat. Cell Biol. 8, 1025-1031
12. Ghosh, H. S., Reizis, B., and Robbins, P. D. (2011) SIRT1 associates with eIF2-α and regulates the cellular stress response. Sci. Rep. 1, 150
13. Wang, F. M., Chen, Y. J., and Ouyang, H. J. (2011) Regulation of unfolded protein response modulator XBP1s by acetylation and deacetylation. Biochem. J. 433, 245-252
14. Wang, F. M., Galson, D. L., Roodman, G. D., and Ouyang, H. (2011) Resveratrol triggers the pro-apoptotic endoplasmic reticulum stress response and represses pro-survival XBP1 signaling in human multiple myeloma cells. Exp. Hematol. 39, 999-1006
15. Herranz, D., and Serrano, M. (2010) SIRT1: recent lessons from mouse models. Nat. Rev. Cancer 10, 819-823
16. Chen, D., Bruno, J., Easlon, E., Lin, S. J., Cheng, H. L., Alt, F. W., and Guarente, L. (2008) Tissue-specific regulation of SIRT1 by calorie restriction. Genes Dev. 22, 1753-1757
17. Purushotham, A., Schug, T. T., Xu, Q., Surapureddi, S., Guo, X., and Li, X. (2009) Hepatocyte-specific deletion of SIRT1 alters fatty acid metabolism and results in hepatic steatosis and inflammation. Cell Metab. 9, 327-338
18. Li, Y., Xu, S., Giles, A., Nakamura, K., Lee, J. W., Hou, X., Donmez, G., Li, J., Luo, Z., Walsh, K., Guarente, L., and Zang, M. (2011) Hepatic overexpression of SIRT1 in mice attenuates endoplasmic reticulum stress and insulin resistance in the liver. FASEB J. 25, 1664-1679
19. Haze, K., Yoshida, H., Yanagi, H., Yura, T., and Mori, K. (1999) Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell 10, 3787-3799
20. Yoshida, H., Matsui, T., Yamamoto, A., Okada, T., and Mori, K. (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107, 881-891
21. Yoshida, H., Uemura, A., and Mori, K. (2009) pXBP1(U), a negative regulator of the unfolded protein response activator pXBP1(S), targets ATF6 but not ATF4 in proteasome-mediated degradation. Cell Struct. Funct. 34, 1-10
22. Shuto, T., Furuta, T., Oba, M., Xu, H., Li, J. D., Cheung, J., Gruenert, D. C., Uehara, A., Suico, M. A., Okiyoneda, T., and Kai, H. (2006) Promoter hypomethylation of Toll-like receptor-2 gene is associated with increased proinflammatory response toward bacterial peptidoglycan in cystic fibrosis bronchial epithelial cells. FASEB J. 20, 782-784
23. Koga, T., Lim, J. H., Jono, H., Ha, U. H., Xu, H., Ishinaga, H., Morino, S., Xu, X., Yan, C., Kai, H., and Li, J. D. (2008) Tumor suppressor cylindromatosis acts as a negative regulator for Streptococcus pneumoniae-induced NFAT signaling. J. Biol. Chem. 283, 12546-12554
24. Koga, T., Suico, M. A., Nakamura, H., Taura, M., Lu, Z., Shuto, T., Okiyoneda, T., and Kai, H. (2005) Sp1-dependent regulation of myeloid Elf-1 like factor in human epithelial cells. FEBS Lett. 579, 2811-2816
25. Taura, M., Fukuda, R., Suico, M. A., Eguma, A., Koga, T., Shuto, T., Sato, T., Morino-Koga, S., and Kai, H. (2010) TLR3 induction by anticancer drugs potentiates poly I:C-induced tumor cell apoptosis. Cancer Sci. 101, 1610-1617
26. Yamamoto, K., Takahara, K., Oyadomari, S., Okada, T., Sato, T., Harada, A., and Mori, K. (2010) Induction of liver steatosis and lipid droplet formation in ATF6α-knockout mice burdened with pharmacological endoplasmic reticulum stress. Mol. Biol. Cell 21, 2975-2986
27. Medina, M., and Wandosell, F. (2011) Deconstructing GSK-3: the fine regulation of its activity. Int. J. Alzheimers Dis. 2011, 479249
28. Cole, A. R., Knebel, A., Morrice, N. A., Robertson, L. A., Irving, A. J., Connolly, C. N., and Sutherland, C. (2004) GSK-3 phosphorylation of the Alzheimer epitope within collapsin response mediator proteins regulates axon elongation in primary neurons. J. Biol. Chem. 279, 50176-50180
29. Viswanathan, M., Kim, S. K., Berdichevsky, A., and Guarente, L. (2005) A role for SIR-2.1 regulation of ER stress response genes in determining C. elegans life span. Dev. Cell 9, 605-615
30. Jung, T. W., Lee, K. T., Lee, M. W., and Ka, K. H. (2012) SIRT1 attenuates palmitate-induced endoplasmic reticulum stress and insulin resistance in HepG2 cells via induction of oxygen-regulated protein 150. Biochem. Biophys. Res. Commun. 422, 229-232
31. Winnay, J. N., Boucher, J., Mori, M. A., Ueki, K., and Kahn, C. R. (2010) A regulatory subunit of phosphoinositide 3-kinase increases the nuclear accumulation of X-box-binding protein-1 to modulate the unfolded protein response. Nat. Med. 16, 438-445
32. Winnay, J. N., Dirice, E., Liew, C. W., Kulkarni, R. N., and Kahn, C. R. (2014) p85 deficiency protects β-cells from endoplasmic reticulum stress-induced apoptosis. Proc. Natl. Acad. Sci. U.S.A. 111, 1192-1197
33. Hosoi, T., Hyoda, K., Okuma, Y., Nomura, Y., and Ozawa, K. (2007) Akt up- and down-regulation in response to endoplasmic reticulum stress. Brain Res. 1152, 27-31
34. Qin, L., Wang, Z., Tao, L., and Wang, Y. (2010) ER stress negatively regulates AKT/TSC/mTOR pathway to enhance autophagy. Autophagy 6, 239-247
35. Zhang, W., Neo, S. P., Gunaratne, J., Poulsen, A., Boping, L., Ong, E. H., Sangthongpitag, K., Pendharkar, V., Hill, J., and Cohen, S. M. (2015) Feedback regulation on PTEN/AKT pathway by the ER stress kinase PERK mediated by interaction with the Vault complex. Cell Signal 27, 436-442
36. Yung, H. W., Charnock-Jones, D. S., and Burton, G. J. (2011) Regulation of AKT phosphorylation at Ser473 and Thr308 by endoplasmic reticulum stress modulates substrate specificity in a severity dependent manner. PLoS One 6, e17894