Transcriptional up-regulation of ULK1 by ATF4 contributes to cancer cell survival

Biochemical Journal

Volumn 449, Issue 2, 2013, Pages 389-400

  Pike, Luke R G ^a   Singleton, Dean C ^a   Buffa, Francesca ^a   Abramczyk, Olga ^b   Phadwal, Kanchan ^c   Li, Ji Liang ^a   Simon, Anna Katharina ^c   Murray, James T ^d   Harris, Adrian L ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^c JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^d TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Autophagy; Endoplasmic reticulum stress; Hypoxia; Integrated stress response; UNC51 like kinase 1 (ULK1); Unfolded protein response (UPR)

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; BEVACIZUMAB; CASPASE 3; CASPASE 7; MESSENGER RNA; PROTEIN; PROTEIN P62; ULK1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIANGIOGENIC THERAPY; ARTICLE; AUTOPHAGY; BREAST CANCER; CANCER CELL; CELL SURVIVAL; CONTROLLED STUDY; DISEASE SEVERITY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; HUMAN; HUMAN TISSUE; HYPOXIA; LONG TERM EXPOSURE; MITOPHAGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN INDUCTION; TRANSCRIPTION INITIATION SITE; UPREGULATION;

ACTIVATING TRANSCRIPTION FACTOR 4; ANIMALS; AUTOPHAGY; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL HYPOXIA; CELL LINE, TUMOR; CELL SURVIVAL; ENDOPLASMIC RETICULUM STRESS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HT29 CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MCF-7 CELLS; MICE; MULTIVARIATE ANALYSIS; NEOPLASMS; PROGNOSIS; PROTEIN-SERINE-THREONINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SURVIVAL ANALYSIS; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 84871429513     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20120972     Document Type: Article

References (58)

1. Thomlinson, R. H. and Gray, L. H. (1955) The histological structure of some human lung cancers and the possible implications for radiotherapy. Br. J. Cancer 9, 539-549
2. 2 availability on human cancer. Nat. Rev. Cancer 8, 967-975
3. Olive, P. L., Banath, J. P. and Durand, R. E. (2002) The range of oxygenation in SiHa tumor xenografts. Radiat. Res. 158, 159-166 (Pubitemid 34851810)
4. Hockel, M., Schlenger, K., Aral, B., Mitze, M., Schaffer, U. and Vaupel, P. (1996) Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix. Cancer Res. 56, 4509-4515 (Pubitemid 26330463)
5. Hockel, M., Vorndran, B., Schlenger, K., Baussmann, E. and Knapstein, P. G. (1993) Tumor oxygenation: a new predictive parameter in locally advanced cancer of the uterine cervix. Gynecol. Oncol. 51, 141-149 (Pubitemid 24020354)
6. Milani, M. and Harris, A. L. (2008) Targeting tumour hypoxia in breast cancer. Eur. J. Cancer 44, 2766-2773
7. Harris, A. L. (2002) Hypoxia: a key regulatory factor in tumour growth. Nat. Rev. Cancer 2, 38-47
8. 2-dependent reaction cycle of Ero1-mediated oxidative protein folding in the endoplasmic reticulum. Mol. Cell 10, 983-994
9. Harding, H. P., Zhang, Y., Zeng, H., Novoa, I., Lu, P. D., Calfon, M., Sadri, N., Yun, C., Popko, B., Paules, R. et al. (2003) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11, 619-633 (Pubitemid 36385118)
10. Bernales, S., Papa, F. R. and Walter, P. (2006) Intracellular signaling by the unfolded protein response. Annu. Rev. Cell Dev. Biol. 22, 487-508
11. Harding, H. P., Novoa, I., Zhang, Y., Zeng, H., Wek, R., Schapira, M. and Ron, D. (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6, 1099-1108
12. Harding, H. P., Zhang, Y. and Ron, D. (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271-274 (Pubitemid 29051178)
13. Liang, G. and Hai, T. (1997) Characterization of human activating transcription factor 4, a transcriptional activator that interacts with multiple domains of cAMP-responsive element-binding protein (CREB)-binding protein. J. Biol. Chem. 272, 24088-24095 (Pubitemid 27410995)
14. Blais, J. D., Filipenko, V., Bi, M., Harding, H. P., Ron, D., Koumenis, C., Wouters, B. G. and Bell, J. C. (2004) Activating transcription factor 4 is translationally regulated by hypoxic stress. Mol. Cell. Biol. 24, 7469-7482 (Pubitemid 39121475)
15. Bobrovnikova-Marjon, E., Grigoriadou, C., Pytel, D., Zhang, F., Ye, J., Koumenis, C., Cavener, D. and Diehl, J. A. (2010) PERK promotes cancer cell proliferation and tumor growth by limiting oxidative DNA damage. Oncogene 29, 3881-3895
16. Bobrovnikova-Marjon, E., Hatzivassiliou, G., Grigoriadou, C., Romero, M., Cavener, D. R., Thompson, C. B. and Diehl, J. A. (2008) PERK-dependent regulation of lipogenesis during mouse mammary gland development and adipocyte differentiation. Proc. Natl. Acad. Sci. U.S.A. 105, 16314-16319
17. Yoshizawa, T., Hinoi, E., Jung, D. Y., Kajimura, D., Ferron, M., Seo, J., Graff, J. M., Kim, J. K. and Karsenty, G. (2009) The transcription factor ATF4 regulates glucose metabolism in mice through its expression in osteoblasts. J. Clin. Invest. 119, 2807-2817
18. Ghosh, R., Lipson, K. L., Sargent, K. E., Mercurio, A. M., Hunt, J. S., Ron, D. and Urano, F. (2010) Transcriptional regulation of VEGF-A by the unfolded protein response pathway. PLoS ONE 5, e9575
19. Rouschop, K. M., van den Beucken, T., Dubois, L., Niessen, H., Bussink, J., Savelkouls, K., Keulers, T., Mujcic, H., Landuyt, W., Voncken, J. W. et al. (2009) The unfolded protein response protects human tumor cells during hypoxia through regulation of the autophagy genes MAP1LC3B and ATG5. J. Clin. Invest. 120, 127-141
20. Rzymski, T. and Harris, A. L. (2007) The unfolded protein response and integrated stress response to anoxia. Clin. Cancer Res. 13, 2537-2540 (Pubitemid 46788018)
21. Rzymski, T., Milani, M., Pike, L., Buffa, F., Mellor, H. R., Winchester, L., Pires, I., Hammond, E., Ragoussis, I. and Harris, A. L. (2010) Regulation of autophagy by ATF4 in response to severe hypoxia. Oncogene 29, 4424-4435
22. Rouschop, K. M., Ramaekers, C. H., Schaaf, M. B., Keulers, T. G., Savelkouls, K. G., Lambin, P., Koritzinsky, M. and Wouters, B. G. (2009) Autophagy is required during cycling hypoxia to lower production of reactive oxygen species. Radiother. Oncol. 92, 411-416
23. Bi, M., Naczki, C., Koritzinsky, M., Fels, D., Blais, J., Hu, N., Harding, H., Novoa, I., Varia, M., Raleigh, J. et al. (2005) ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J. 24, 3470-3481 (Pubitemid 41486784)
24. Ye, J., Kumanova, M., Hart, L. S., Sloane, K., Zhang, H., De Panis, D. N., Bobrovnikova-Marjon, E., Diehl, J. A., Ron, D. and Koumenis, C. (2010) The GCN2-ATF4 pathway is critical for tumour cell survival and proliferation in response to nutrient deprivation. EMBO J. 29, 2082-2096
25. Degenhardt, K., Mathew, R., Beaudoin, B., Bray, K., Anderson, D., Chen, G., Mukherjee, C., Shi, Y., Gelinas, C., Fan, Y. et al. (2006) Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 10, 51-64
26. Yang, S., Wang, X., Contino, G., Liesa, M., Sahin, E., Ying, H., Bause, A., Li, Y., Stommel, J. M., Dell'antonio, G. et al. (2011) Pancreatic cancers require autophagy for tumor growth. Genes Dev. 25, 717-729
27. Guo, J. Y., Chen, H. Y., Mathew, R., Fan, J., Strohecker, A. M., Karsli-Uzunbas, G., Kamphorst, J. J., Chen, G., Lemons, J. M., Karantza, V. et al. (2011) Activated Ras requires autophagy to maintain oxidative metabolism and tumorigenesis. Genes Dev. 25, 460-470
28. Elgendy, M., Sheridan, C., Brumatti, G. and Martin, S. J. (2011) Oncogenic Ras-induced expression of Noxa and Beclin-1 promotes autophagic cell death and limits clonogenic survival. Mol. Cell 42, 23-35
29. Milani, M., Rzymski, T., Mellor, H. R., Pike, L., Bottini, A., Generali, D. and Harris, A. L. (2009) The role of ATF4 stabilization and autophagy in resistance of breast cancer cells treated with Bortezomib. Cancer Res. 69, 4415-4423
30. Rzymski, T., Paantjens, A., Bod, J. and Harris, A. L. (2008) Multiple pathways are involved in the anoxia response of SKIP3 including HuR-regulated RNA stability, NF-κB and ATF4. Oncogene 27, 4532-4543
31. Phadwal, K., Alegre-Abarrategui, J., Watson, A. S., Pike, L., Anbalagan, S., Hammond, E. M., Wade-Martins, R., McMichael, A., Klenerman, P. and Simon, A. K. (2012) A novel method for autophagy detection in primary cells: impaired levels of macroautophagy in immunosenescent T cells. Autophagy 8, 677-689
32. Otsuki, Y., Li, Z. and Shibata, M. A. (2003) Apoptotic detection methods: from morphology to gene. Prog. Histochem. Cytochem. 38, 275-339 (Pubitemid 36538343)
33. Kundu, M., Lindsten, T., Yang, C. Y., Wu, J., Zhao, F., Zhang, J., Selak, M. A., Ney, P. A. and Thompson, C. B. (2008) Ulk1 plays a critical role in the autophagic clearance of mitochondria and ribosomes during reticulocyte maturation. Blood 112, 1493-1502
34. Ivascu, A. and Kubbies, M. (2006) Rapid generation of single-tumor spheroids for high-throughput cell function and toxicity analysis. J. Biomol. Screening 11, 922-932 (Pubitemid 44847146)
35. Higgins, G. S., Harris, A. L., Prevo, R., Helleday, T., McKenna, W. G. and Buffa, F. M. (2010) Overexpression of POLQ confers a poor prognosis in early breast cancer patients. Oncotarget 1, 175-184
36. Koumenis, C., Naczki, C., Koritzinsky, M., Rastani, S., Diehl, A., Sonenberg, N., Koromilas, A. and Wouters, B. G. (2002) Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2α. Mol. Cell. Biol. 22, 7405-7416
37. Paez-Ribes, M., Allen, E., Hudock, J., Takeda, T., Okuyama, H., Vinals, F., Inoue, M., Bergers, G., Hanahan, D. and Casanovas, O. (2009) Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 15, 220-231
38. Casanovas, O., Hicklin, D. J., Bergers, G. and Hanahan, D. (2005) Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell 8, 299-309 (Pubitemid 41443415)
39. Ganley, I. G., Lam du, H., Wang, J., Ding, X., Chen, S. and Jiang, X. (2009) ULK1.ATG13.FIP200 complex mediates mTOR signaling and is essential for autophagy. J. Biol. Chem. 284, 12297-12305
40. Shang, L., Chen, S., Du, F., Li, S., Zhao, L. and Wang, X. (2011) Nutrient starvation elicits an acute autophagic response mediated by Ulk1 dephosphorylation and its subsequent dissociation from AMPK. Proc. Natl. Acad. Sci. U.S.A. 108, 4788-4793
41. Lee, J. W., Park, S., Takahashi, Y. and Wang, H. G. (2010) The association of AMPK with ULK1 regulates autophagy. PLoS ONE 5, e15394
42. Kim, J., Kundu, M., Viollet, B. and Guan, K. L. (2011) AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 13, 132-141
43. Egan, D. F., Shackelford, D. B., Mihaylova, M. M., Gelino, S., Kohnz, R. A., Mair, W., Vasquez, D. S., Joshi, A., Gwinn, D. M., Taylor, R. et al. (2011) Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331, 456-461
44. Scaffidi, P., Misteli, T. and Bianchi, M. E. (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418, 191-195 (Pubitemid 34773774)
45. Muller, S., Scaffidi, P., Degryse, B., Bonaldi, T., Ronfani, L., Agresti, A., Beltrame, M. and Bianchi, M. E. (2001) The double life of HMGB1 chromatin protein: architectural factor and extracellular signal. EMBO J. 20, 4337-4340 (Pubitemid 32772027)
46. Bustin, M. (1999) Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol. Cell. Biol. 19, 5237-5246
47. Mizushima, N. (2010) The role of the Atg1/ULK1 complex in autophagy regulation. Curr. Opin. Cell Biol. 22, 132-139
48. Gao, W., Shen, Z., Shang, L. and Wang, X. (2011) Upregulation of human autophagy-initiation kinase ULK1 by tumor suppressor p53 contributes to DNA-damage-induced cell death. Cell Death Differ. 18, 1598-1607
49. Mancias, J. D. and Kimmelman, A. C. (2011) Targeting autophagy addiction in cancer. Oncotarget 2, 1302-1306
50. Rabinowitz, J. D. and White, E. (2011) Autophagy and metabolism. Science 330, 1344-1348
51. Zhu, J. H., Horbinski, C., Guo, F., Watkins, S., Uchiyama, Y. and Chu, C. T. (2007) Regulation of autophagy by extracellular signal-regulated protein kinases during 1-methyl-4-phenylpyridinium-induced cell death. Am. J. Pathol. 170, 75-86 (Pubitemid 47339191)
52. Yee, K. S., Wilkinson, S., James, J., Ryan, K. M. and Vousden, K. H. (2009) PUMA- and Bax-induced autophagy contributes to apoptosis. Cell Death Differ. 16, 1135-1145
53. Xue, L., Fletcher, G. C. and Tolkovsky, A. M. (1999) Autophagy is activated by apoptotic signalling in sympathetic neurons: an alternative mechanism of death execution. Mol. Cell. Neurosci. 14, 180-198 (Pubitemid 29449222)
54. Crighton, D., Wilkinson, S., O'Prey, J., Syed, N., Smith, P., Harrison, P. R., Gasco, M., Garrone, O., Crook, T. and Ryan, K. M. (2006) DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 126, 121-134 (Pubitemid 44040988)
55. Berry, D. L. and Baehrecke, E. H. (2007) Growth arrest and autophagy are required for salivary gland cell degradation in Drosophila. Cell 131, 1137-1148 (Pubitemid 350235023)
56. Vandenabeele, P., Galluzzi, L., Vanden Berghe, T. and Kroemer, G. (2010) Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat. Rev. Mol. Cell Biol. 11, 700-714
57. Zhang, N., Chen, Y., Jiang, R., Li, E., Chen, X., Xi, Z., Guo, Y., Liu, X., Zhou, Y., Che, Y. and Yue, X. (2011) PARP and RIP 1 are required for autophagy induced by 11′-deoxyverticillin A, which precedes caspase-dependent apoptosis. Autophagy 7, 598-612
58. Bonapace, L., Bornhauser, B. C., Schmitz, M., Cario, G., Ziegler, U., Niggli, F. K., Schafer, B. W., Schrappe, M., Stanulla, M. and Bourquin, J. P. (2010) Induction of autophagy-dependent necroptosis is required for childhood acute lymphoblastic leukemia cells to overcome glucocorticoid resistance. J. Clin. Invest. 120, 1310-1323