Endoplasmic reticulum stress sensitizes cells to DNA damage-induced apoptosis through p53-dependent suppression of p21 CDKN1A

Nature Communications

Volumn 5, Issue , 2014, Pages

  Mlynarczyk, Coraline ^a   Fåhraeus, Robin ^a,b  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b MASARYK MEMORIAL CANCER INSTITUTE   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; CASPASE 7; CYCLIN DEPENDENT KINASE INHIBITOR 1A; DNA; MESSENGER RNA; MICRORNA; POLY(ADENOSINE DIPHOSPHATE RIBOSE); PROTEIN P53; SMALL INTERFERING RNA; STRATIFIN; CDKN1A PROTEIN, HUMAN; EXORIBONUCLEASE; PROTEIN 14 3 3; RFWD2 PROTEIN, HUMAN; SFN PROTEIN, HUMAN; TP53 PROTEIN, HUMAN; TUMOR MARKER; UBIQUITIN PROTEIN LIGASE;

APOPTOSIS; CELL ORGANELLE; DAMAGE; DNA; DRUG; GENOTOXICITY;

A549 CELL LINE; APOPTOSIS; ARTICLE; CELL CYCLE PROGRESSION; CONTROLLED STUDY; DNA DAMAGE; ENDOPLASMIC RETICULUM STRESS; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; HCT116 CELL LINE; HUMAN; HUMAN CELL; PROTEIN DEGRADATION; PROTEIN GLYCOSYLATION; PROTEIN RNA BINDING; RNA TRANSLATION; TRANSACTIVATION; CELL CYCLE CHECKPOINT; GENETICS; MCF 7 CELL LINE; METABOLISM; TUMOR CELL LINE;

14-3-3 PROTEINS; APOPTOSIS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA DAMAGE; ENDOPLASMIC RETICULUM STRESS; EXORIBONUCLEASES; G2 PHASE CELL CYCLE CHECKPOINTS; HCT116 CELLS; HUMANS; MCF-7 CELLS; TUMOR MARKERS, BIOLOGICAL; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN-PROTEIN LIGASES;

EID: 84923279273     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6067     Document Type: Article

References (69)

1. Schroder, M. & Kaufman, R. J. The mammalian unfolded protein response. Annu. Rev. Biochem. 74, 739-789 (2005
2. Szegezdi, E., Logue, S., Gorman, A. & Samali, A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 7, 880-885 (2006
3. Ozcan, L. & Tabas, I. Role of endoplasmic reticulum stress in metabolic disease and other disorders. Annu. Rev. Med. 63, 317-328 (2012
4. Ma, Y. & Hendershot, L. The role of the unfolded protein response in tumour development: Friend or foe? Nat. Rev. Cancer 4, 966-977 (2004
5. Ranganathan, A., Ojha, S., Kourtidis, A., Conklin, D. & Aguirre-Ghiso, J. Dual function of pancreatic endoplasmic reticulum kinase in tumor cell growth arrest and survival. Cancer Res. 68, 3260-3268 (2008
6. Huber, A.-L. et al. p58(IPK)-mediated attenuation of the proapoptotic PERKCHOP pathway allows malignant progression upon low glucose. Mol. Cell. 49, 1049-1059 (2013
7. Chatterjee, S., Hirota, H., Belfi, C., Berger, S. & Berger, N. Hypersensitivity to DNA cross-linking agents associated with up-regulation of glucose-regulated stress protein GRP78. Cancer Res. 57, 5112-5116 (1997
8. Yamada, M. et al. Cellular sensitization to cisplatin and carboplatin with decreased removal of platinum-DNA adduct by glucose-regulated stress. Cancer Chemother. Pharmacol. 44, 59-64 (1999
9. Al-Rawashdeh, F., Scriven, P., Cameron, I., Vergani, P. & Wyld, L. Unfolded protein response activation contributes to chemoresistance in hepatocellular carcinoma. Eur. J. Gastroenterol. Hepatol. 22, 1099-1105 (2010
10. Feng, R., Zhai, W., Yang, H., Jin, H. & Zhang, Q. Induction of ER stress protects gastric cancer cells against apoptosis induced by cisplatin and doxorubicin through activation of p38 MAPK. Biochem. Biophys. Res. Commun. 406, 299-304 (2011
11. Bourdon, J. C. et al. p53 isoforms can regulate p53 transcriptional activity. Genes Dev. 19, 2122-2137 (2005
12. Olivares-Illana, V. & Fahraeus, R. p53 isoforms gain functions. Oncogene 29, 5113-5119 (2010
13. Avery-Kiejda, K. A. et al. Small molecular weight variants of p53 are expressed in human melanoma cells and are induced by the DNA-damaging agent cisplatin. Clin. Cancer Res. 14, 1659-1668 (2008
14. Fujita, K. et al. p53 isoforms Delta133p53 and p53beta are endogenous regulators of replicative cellular senescence. Nat. Cell Biol. 11, 1135-1142 (2009
15. Takahashi, R. et al. p53 isoform profiling in glioblastoma and injured brain. Oncogene 32, 3165-3174 (2012
16. Powell, D. J. et al. Stress-dependent changes in the properties of p53 complexes by the alternative translation product p53/47. Cell Cycle 7, 950-959 (2008
17. Melis, J. P. et al. Genotoxic exposure: Novel cause of selection for a functional DeltaN-p53 isoform. Oncogene 30, 1764-1772 (2011
18. Scrable, H., Sasaki, T. & Maier, B. DeltaNp53 or p44: Priming the p53 pump. Int. J. Biochem. Cell Biol. 37, 913-919 (2005
19. Yin, Y., Stephen, C. W., Luciani, M. G. & Fahraeus, R. p53 Stability and activity is regulated by Mdm2-mediated induction of alternative p53 translation products. Nat. Cell Biol. 4, 462-467 (2002
20. Harding, H., Zhang, Y. & Ron, D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271-274 (1999
21. Fernandez, J. et al. Translation mediated by the internal ribosome entry site of the cat-1 mRNA is regulated by glucose availability in a PERK kinasedependent manner. J. Biol. Chem. 277, 11780-11787 (2002
22. Vattem, K. & Wek, R. Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc. Natl Acad. Sci. USA 101, 11269-11274 (2004
23. Bourougaa, K. et al. Endoplasmic reticulum stress induces G2 cell-cycle arrest via mRNA translation of the p53 isoform p53/47. Mol. Cell 38, 78-88 (2010
24. Candeias, M. M. et al. Expression of p53 and p53/47 are controlled by alternative mechanisms of messenger RNA translation initiation. Oncogene 25, 6936-6947 (2006
25. Sivan, G. & Elroy-Stein, O. Regulation of mRNA translation during cellular division. Cell Cycle 7, 741-744 (2008
26. Lin, S. C., Karoly, E. D. & Taatjes, D. J. The human DeltaNp53 isoform triggers metabolic and gene expression changes that activate mTOR and alter mitochondrial function. Aging Cell 12, 863-872 (2013
27. Takahashi, R. et al. p53 isoform profiling in glioblastoma and injured brain. Oncogene 32, 3165-3174 (2013
28. Ungewitter, E. & Scrable, H. Delta40p53 controls the switch from pluripotency to differentiation by regulating IGF signaling in ESCs. Genes Dev. 24, 2408-2419 (2010
29. Thomas, E., Zeps, N., Cregan, M., Hartmann, P. & Martin, T. 14-3-3sigma (sigma) regulates proliferation and differentiation of multipotent p63-positive cells isolated from human breastmilk. Cell Cycle 10, 278-284 (2011
30. Laronga, C., Yang, H. Y., Neal, C. & Lee, M. H. Association of the cyclindependent kinases and 14-3-3 sigma negatively regulates cell cycle progression. J. Biol. Chem. 275, 23106-23112 (2000
31. Samuel, T. et al. The G2/M regulator 14-3-3sigma prevents apoptosis through sequestration of Bax. J. Biol. Chem. 276, 45201-45206 (2001
32. Hermeking, H. et al. 14-3-3 sigma is a p53-regulated inhibitor of G2/M progression. Mol. Cell 1, 3-11 (1997
33. Chan, T. A., Hermeking, H., Lengauer, C., Kinzler, K. W. & Vogelstein, B. 14-3-3Sigma is required to prevent mitotic catastrophe after DNA damage. Nature 401, 616-620 (1999
34. Urano, T. et al. Efp targets 14-3-3 sigma for proteolysis and promotes breast tumour growth. Nature 417, 871-875 (2002
35. Choi, H. H. et al. COP9 signalosome subunit 6 stabilizes COP1, which functions as an E3 ubiquitin ligase for 14-3-3sigma. Oncogene 30, 4791-4801 (2011
36. Migliorini, D. et al. Cop1 constitutively regulates c-Jun protein stability and functions as a tumor suppressor in mice. J. Clin. Invest. 121, 1329-1343 (2011
37. Vitari, A. C. et al. COP1 is a tumour suppressor that causes degradation of ETS transcription factors. Nature 474, 403-406 (2011
38. Dornan, D. et al. COP1, the negative regulator of p53, is overexpressed in breast and ovarian adenocarcinomas. Cancer Res. 64, 7226-7230 (2004
39. Lee, Y. H. et al. Definition of ubiquitination modulator COP1 as a novel therapeutic target in human hepatocellular carcinoma. Cancer Res. 70, 8264-8269 (2010
40. Dornan, D. et al. ATM engages autodegradation of the E3 ubiquitin ligase COP1 after DNA damage. Science 313, 1122-1126 (2006
41. Yoneda-Kato, N., Tomoda, K., Umehara, M., Arata, Y. & Kato, J. Y. Myeloid leukemia factor 1 regulates p53 by suppressing COP1 via COP9 signalosome subunit 3. EMBO J. 24, 1739-1749 (2005
42. Favory, J. J. et al. Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. EMBO J. 28, 591-601 (2009
43. Efeyan, A., Collado, M., Velasco-Miguel, S. & Serrano, M. Genetic dissection of the role of p21Cip1/Waf1 in p53-mediated tumour suppression. Oncogene 26, 1645-1649 (2007
44. Martin-Caballero, J., Flores, J. M., Garcia-Palencia, P. & Serrano, M. Tumor susceptibility of p21(Waf1/Cip1)-deficient mice. Cancer Res. 61, 6234-6238 (2001
45. Adnane, J. et al. Loss of p21WAF1/CIP1 accelerates Ras oncogenesis in a transgenic/knockout mammary cancer model. Oncogene 19, 5338-5347 (2000
46. Zirbes, T. K. et al. Prognostic impact of p21/waf1/cip1 in colorectal cancer. Int. J. Cancer 89, 14-18 (2000
47. Komiya, T. et al. p21 expression as a predictor for favorable prognosis in squamous cell carcinoma of the lung. Clin. Cancer Res. 3, 1831-1835 (1997
48. Jung, J. M. et al. Increased levels of p21WAF1/Cip1 in human brain tumors. Oncogene 11, 2021-2028 (1995
49. Ferrandina, G. et al. p21WAF1/CIP1 protein expression in primary ovarian cancer. Int. J. Oncol. 17, 1231-1235 (2000
50. De la Cueva, E. et al. Tumorigenic activity of p21Waf1/Cip1 in thymic lymphoma. Oncogene 25, 4128-4132 (2006
51. Wang, Y. A., Elson, A. & Leder, P. Loss of p21 increases sensitivity to ionizing radiation and delays the onset of lymphoma in atm-deficient mice. Proc. Natl Acad. Sci. USA 94, 14590-14595 (1997
52. Dash, B. C. & El-Deiry, W. S. Phosphorylation of p21 in G2/M promotes cyclin B-Cdc2 kinase activity. Mol. Cell Biol. 25, 3364-3387 (2005
53. Suzuki, A., Tsutomi, Y., Akahane, K., Araki, T. & Miura, M. Resistance to Fas-mediated apoptosis: Activation of caspase 3 is regulated by cell cycle regulator p21WAF1 and IAP gene family ILP. Oncogene 17, 931-939 (1998
54. Asada, M. et al. Apoptosis inhibitory activity of cytoplasmic p21(Cip1/WAF1) in monocytic differentiation. EMBO J. 18, 1223-1234 (1999
55. Singer, S. et al. Nuclear pore component Nup98 is a potential tumor suppressor and regulates posttranscriptional expression of select p53 target genes. Mol. Cell 48, 799-810 (2012
56. Miyamoto, S., Hidaka, K., Jin, D. & Morisaki, T. RNA-binding proteins Rbm38 and Rbm24 regulate myogenic differentiation via p21-dependent and-independent regulatory pathways. Genes Cells 14, 1241-1252 (2009
57. Bornstein, G. et al. Role of the SCFSkp2 ubiquitin ligase in the degradation of p21Cip1 in S phase. J. Biol. Chem. 278, 25752-25757 (2003
58. Yu, Z. K., Gervais, J. L. & Zhang, H. Human CUL-1 associates with the SKP1/SKP2 complex and regulates p21(CIP1/WAF1) and cyclin D proteins. Proc. Natl Acad. Sci. USA 95, 11324-11329 (1998
59. Chiba, T. & Tanaka, K. Cullin-based ubiquitin ligase and its control by NEDD8-conjugating system. Curr. Protein Pept. Sci. 5, 177-184 (2004
60. Hainaut, P. & Hollstein, M. p53 and human cancer: The first ten thousand mutations. Adv. Cancer Res. 77, 81-137 (2000
61. Hermeking, H. MicroRNAs in the p53 network: Micromanagement of tumour suppression. Nat. Rev. Cancer 12, 613-626 (2012
62. Innocente, S. A., Abrahamson, J. L., Cogswell, J. P. & Lee, J. M. p53 regulates a G2 checkpoint through cyclin B1. Proc. Natl Acad. Sci. USA 96, 2147-2152 (1999
63. Roninson, I. B. Oncogenic functions of tumour suppressor p21(Waf1/Cip1/Sdi1): Association with cell senescence and tumour-promoting activities of stromal fibroblasts. Cancer Lett. 179, 1-14 (2002
64. Chen, W. et al. Direct interaction between Nrf2 and p21(Cip1/WAF1) upregulates the Nrf2-mediated antioxidant response. Mol. Cell 34, 663-673 (2009
65. Zhao, P. et al. c-Jun inhibits thapsigargin-induced ER stress through up-regulation of DSCR1/Adapt78. Exp. Biol. Med 233, 1289-1300 (2008
66. Dornan, D. et al. The ubiquitin ligase COP1 is a critical negative regulator of p53. Nature 429, 86-92 (2004
67. Su, C.-H. et al. Nuclear export regulation of COP1 by 14-3-3s in response to DNA damage. Mol. Cancer 9, 243 (2010
68. Allan, L. A. & Fried, M. p53-dependent apoptosis or growth arrest induced by different forms of radiation in U2OS cells: P21WAF1/CIP1 repression in UV induced apoptosis. Oncogene 18, 5403-5412 (1999
69. Beuvink, I. et al. The mTOR inhibitor RAD001 sensitizes tumor cells to DNA-damaged induced apoptosis through inhibition of p21 translation. Cell 120, 747-759 (2005).