ATM-mediated stabilization of ZEB1 promotes DNA damage response and radioresistance through CHK1

Nature Cell Biology

Volumn 16, Issue 9, 2014, Pages 864-875

  Zhang, Peijing ^a   Wei, Yongkun ^a   Wang, L i ^a   Debeb, Bisrat G ^a   Yuan, Yuan ^a   Zhang, Jinsong ^a   Yuan, Jingsong ^a   Wang, Min ^a   Chen, Dahu ^a   Sun, Yutong ^a   Woodward, Wendy A ^a   Liu, Yongqing ^b   Dean, Douglas C ^b   Liang, Han ^a   Hu, Ye ^c   Ang, K Kian ^a   Hung, Mien Chie ^a,d,e   Chen, Junjie ^a,e   Ma, Li ^a,e  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF LOUISVILLE SCHOOL OF MEDICINE   (United States)

^c HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^d CHINA MEDICAL UNIVERSITY   (Taiwan)

^e UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; CHECKPOINT KINASE 1; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; TRANSCRIPTION FACTOR ZEB1;

ARTICLE; BREAST CANCER CELL LINE; CANCER RESISTANCE; CELL INTERACTION; CELL STRUCTURE; CELL SUBPOPULATION; CONTROLLED STUDY; DNA DAMAGE RESPONSE; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; RADIOSENSITIVITY; UPREGULATION;

ANIMALS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; BREAST NEOPLASMS; DNA DAMAGE; DNA REPAIR; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HELA CELLS; HOMEODOMAIN PROTEINS; HUMANS; KAPLAN-MEIER ESTIMATE; MCF-7 CELLS; MICE; MICE, NUDE; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN STABILITY; RADIATION TOLERANCE; TRANSCRIPTION FACTORS; TWIST TRANSCRIPTION FACTOR; UBIQUITIN THIOLESTERASE; UBIQUITINATION; UP-REGULATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84908149021     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3013     Document Type: Article

References (66)

1. Bedford, J. S. Sublethal damage, potentially lethal damage, and chromosomal aberrations in mammalian cells exposed to ionizing radiations. Int. J. Radiat. Oncol. Biol. Phys. 21, 1457-1469 (1991).
2. Frankenberg-Schwager, M., Frankenberg, D., Blocher, D. & Adamczyk, C. Effect of dose rate on the induction of DNA double-strand breaks in eucaryotic cells. Radiat. Res. 87, 710-717 (1981).
3. Buchholz, T. A. Radiation therapy for early-stage breast cancer after breast-conserving surgery. N. Engl. J. Med. 360, 63-70 (2009).
4. Jameel, J. K., and Rao., V. S., Cawkwell, L. & Drew, P. J. Radioresistance in carcinoma of the breast. Breast 13, 452-460 (2004).
5. Zhou, B. B. & Elledge, S. J. The DNA damage response: putting checkpoints in perspective. Nature 408, 433-439 (2000).
6. Sancar, A., Lindsey-Boltz, L. A., Unsal-Kacmaz, K. & Linn, S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73, 39-85 (2004).
7. Parrilla-Castellar, E. R., Arlander, S. J. & Karnitz, L. Dial 9-1-1 for DNA damage: the Rad9-Hus1-Rad1 (9-1-1) clamp complex. DNA Repair (Amst) 3, 1009-1014 (2004).
8. Rogakou, E. P., and Pilch., D. R., Orr, A. H., Ivanova, V. S. & Bonner, W. M. DNA doublestranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273, 5858-5868 (1998).
9. Reinhardt, H. C. & Yaffe, M. B. Kinases that control the cell cycle in response to DNA damage: Chk1, Chk2, and MK2. Curr. Opin. Cell Biol. 21, 245-255 (2009).
10. Wang, B., Matsuoka, S., Carpenter, P. B. & Elledge, S. J. 53BP1, a mediator of the DNA damage checkpoint. Science 298, 1435-1438 (2002).
11. Stewart, G. S., Wang, B., Bignell, C. R., Taylor, A. M. & Elledge, S. J. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421, 961-966 (2003).
12. Stucki, M. et al. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123, 1213-1226 (2005).
13. Bao, S. et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444, 756-760 (2006).
14. Baumann, M., Krause, M. & Hill, R. Exploring the role of cancer stem cells in radioresistance. Nat. Rev. Cancer 8, 545-554 (2008).
15. Mani, S. A. et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133, 704-715 (2008).
16. Yang, J. & Weinberg, R. A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 14, 818-829 (2008).
17. Thiery, J. P., Acloque, H., Huang, R. Y. & Nieto, M. A. Epithelial-mesenchymal transitions in development and disease. Cell 139, 871-890 (2009).
18. Elenbaas, B. et al. Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells. Genes Dev. 15, 50-65 (2001).
19. Chang, C. J. et al. p53 regulates epithelial-mesenchymal transition and stem cell properties through modulating miRNAs. Nat. Cell Biol. 13, 317-323 (2011).
20. Kim, T. et al. p53 regulates epithelial-mesenchymal transition through microRNAs targeting ZEB1 and ZEB2. J. Exp. Med. 208, 875-883 (2011).
21. Banath, J. P., Macphail, S. H. & Olive, P. L. Radiation sensitivity, H2AX phosphorylation, and kinetics of repair of DNA strand breaks in irradiated cervical cancer cell lines. Cancer Res. 64, 7144-7149 (2004).
22. Olive, P. L. & Banath, J. P. Phosphorylation of histone H2AX as a measure of radiosensitivity. Int. J. Radiat. Oncol. Biol. Phys. 58, 331-335 (2004).
23. Taneja, N. et al. Histone H2AX phosphorylation as a predictor of radiosensitivity and target for radiotherapy. J. Biol. Chem. 279, 2273-2280 (2004).
24. 2) not a gaussian distribution. Mutat. Res. 398, 101-110 (1998).
25. Sung, P. & Klein, H. Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat. Rev. Mol. Cell Biol. 7, 739-750 (2006).
26. Pierce, A. J., and Johnson., R. D., Thompson, L. H. & Jasin, M. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev. 13, 2633-2638 (1999).
27. Weinstock, D. M., Nakanishi, K., Helgadottir, H. R. & Jasin, M. Assaying doublestrand break repair pathway choice in mammalian cells using a targeted endonuclease or the RAG recombinase. Methods Enzymol. 409, 524-540 (2006).
28. Smith, J., and Tho., L. M., Xu, N. & Gillespie, D. A. The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Adv. Cancer Res. 108, 73-112 (2010).
29. Bartek, J. & Lukas, J. Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell 3, 421-429 (2003).
30. Sorensen, C. S. et al. The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat. Cell Biol. 7, 195-201 (2005).
31. Ma, C. X., Janetka, J. W. & Piwnica-Worms, H. Death by releasing the breaks: CHK1 inhibitors as cancer therapeutics. Trends Mol. Med. 17, 88-96 (2011).
32. Lukas, C. et al. DNA damage-activated kinase Chk2 is independent of proliferation or differentiation yet correlates with tissue biology. Cancer Res. 61, 4990-4993 (2001).
33. Collis, S. J. et al. HCLK2 is essential for the mammalian S-phase checkpoint and impacts on Chk1 stability. Nat. Cell Biol. 9, 391-401 (2007).
34. Leung-Pineda, V., Huh, J. & Piwnica-Worms, H. DDB1 targets Chk1 to the Cul4 E3 ligase complex in normal cycling cells and in cells experiencing replication stress. Cancer Res. 69, 2630-2637 (2009).
35. Zhang, Y. W. et al. Genotoxic stress targets human Chk1 for degradation by the ubiquitin-proteasome pathway. Mol. Cell 19, 607-618 (2005).
36. Furusawa, T., Moribe, H., Kondoh, H. & Higashi, Y. Identification of CtBP1 and CtBP2 as corepressors of zinc finger-homeodomain factor deltaEF1. Mol. Cell Biol. 19, 8581-8590 (1999).
37. Postigo, A. A. & Dean, D. C. ZEB represses transcription through interaction with the corepressor CtBP. Proc. Natl Acad. Sci. USA 96, 6683-6688 (1999).
38. Byles, V. et al. SIRT1 induces EMT by cooperating with EMT transcription factors and enhances prostate cancer cell migration and metastasis. Oncogene 31, 4619-4629 (2012).
39. Li, M. et al. Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature 416, 648-653 (2002).
40. Cummins, J. M. et al. Tumour suppression: disruption of HAUSP gene stabilizes p53. Nature 428, 486 (2004).
41. Li, M., and Brooks., C. L., Kon, N. & Gu, W. A dynamic role of HAUSP in the p53-Mdm2 pathway. Mol. Cell 13, 879-886 (2004).
42. Qing, P., Han, L., Bin, L., Yan, L. & Ping, W. X. USP7 regulates the stability and function of HLTF through deubiquitination. J. Cell Biochem. 112, 3856-3862 (2011).
43. Song, M. S. et al. The deubiquitinylation and localization of PTEN are regulated by a HAUSP-PML network. Nature 455, 813-817 (2008).
44. Faustrup, H., Bekker-Jensen, S., Bartek, J., Lukas, J. & Mailand, N. USP7 counteracts SCFbetaTrCP-but not APCCdh1-mediated proteolysis of Claspin. J. Cell Biol. 184, 13-19 (2009).
45. Savitsky, K. et al. A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 268, 1749-1753 (1995).
46. Ahn, J. Y., and Schwarz., J. K., Piwnica-Worms, H. & Canman, C. E. Threonine 68 phosphorylation by ataxia telangiectasia mutated is required for efficient activation of Chk2 in response to ionizing radiation. Cancer Res. 60, 5934-5936 (2000).
47. Cortez, D., Wang, Y., Qin, J. & Elledge, S. J. Requirement of ATM-dependent phosphorylation of brca1 in the DNA damage response to double-strand breaks. Science 286, 1162-1166 (1999).
48. Canman, C. E. et al. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281, 1677-1679 (1998).
49. Banin, S. et al. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 281, 1674-1677 (1998).
50. Toledo, L. I. et al. A cell-based screen identifies ATR inhibitors with synthetic lethal properties for cancer-associated mutations. Nat. Struct. Mol. Biol. 18, 721-727 (2011).
51. Chen, D. et al. LIFR is a breast cancer metastasis suppressor upstream of the Hippo-YAP pathway and a prognostic marker. Nat. Med. 18, 1511-1517 (2012).
52. Brabletz, T., Lyden, D., Steeg, P. S. & Werb, Z. Roadblocks to translational advances on metastasis research. Nat. Med. 19, 1104-1109 (2013).
53. Wang, Y. et al. Gene-expression profiles to predict distant metastasis of lymph-nodenegative primary breast cancer. Lancet 365, 671-679 (2005).
54. Horsman, M. R. et al. Tumor radiosensitizers - current status of development of various approaches: report of an International Atomic Energy Agency meeting. Int. J. Radiat. Oncol. Biol. Phys. 64, 551-561 (2006).
55. Singh, A. & Settleman, J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene 29, 4741-4751 (2010).
56. Bartek, J. & Lukas, J. Mammalian G1- and S-phase checkpoints in response to DNA damage. Curr. Opin. Cell Biol. 13, 738-747 (2001).
57. Graham, T. R. et al. Reciprocal regulation of ZEB1 and AR in triple negative breast cancer cells. Breast Cancer Res. Treat. 123, 139-147 (2010).
58. Karihtala, P. et al. Vimentin, zeb1 and Sip1 are up-regulated in triple-negative and basal-like breast cancers: association with an aggressive tumour phenotype. Breast Cancer Res. Treat. 138, 81-90 (2013).
59. Kenney, P. A. et al. Novel ZEB1 expression in bladder tumorigenesis. BJU Int. 107, 656-663 (2011).
60. Spoelstra, N. S. et al. The transcription factor ZEB1 is aberrantly expressed in aggressive uterine cancers. Cancer Res. 66, 3893-3902 (2006).
61. Garrett, M. D. & Collins, I. Anticancer therapy with checkpoint inhibitors: what, where and when? Trends Pharmacol. Sci. 32, 308-316 (2011).
62. Liu, Y., El-Naggar, S., Darling, D. S., Higashi, Y. & Dean, D. C. Zeb1 links epithelial-mesenchymal transition and cellular senescence. Development 135, 579-588 (2008).
63. Stewart, S. A. et al. Lentivirus-delivered stable gene silencing by RNAi in primary cells. RNA 9, 493-501 (2003).
64. Yuan, J., Luo, K., Zhang, L., Cheville, J. C. & Lou, Z. USP10 regulates p53 localization and stability by deubiquitinating p53. Cell 140, 384-396 (2010).
65. Richardson, C., Moynahan, M. E. & Jasin, M. Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev. 12, 3831-3842 (1998).
66. Wang, L. et al. MK-4827, a PARP-1/-2 inhibitor, strongly enhances response of human lung and breast cancer xenografts to radiation. Invest. New Drugs 30, 2113-2120 (2012).