Inhibition of snail1-DNA-PKcs protein-protein interface sensitizes cancer cells and inhibits tumor metastasis

Journal of Biological Chemistry

Volumn 288, Issue 45, 2013, Pages 32506-32516

  Kang, Ga Young ^a   Pyun, Bo Jeong ^a,d   Seo, Haeng Ran ^b,e   Jin, Yeung Bae ^c   Lee, Hae June ^b   Lee, Yoon Jin ^b   Lee, Yun Sil ^a  

^a Ewha Womans University   (South Korea)

^b Korea Institute of Radiation and Medical Science   (South Korea)

^c Korea Atomic Energy Research Institute   (South Korea)

^d Korea Institute of Oriental Medicine (KIOM)   (South Korea)

^e Institute Pasteur Korea   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYTIC SUBUNITS; DNA DAMAGING AGENTS; DNA-DEPENDENT PROTEIN KINASE; GENOMIC INSTABILITY; PROTEIN INTERACTION; PROTEIN-PROTEIN INTERFACE; RECIPROCAL REGULATION; TUMOR METASTASIS;

AMINO ACIDS; ANIMALS; CELLS; DNA; MOLLUSCS; PROTEINS; REPAIR; TUMORS;

DNA SEQUENCES;

BETA GALACTOSIDASE; DNA DEPENDENT PROTEIN KINASE; LUCIFERASE; PROTEIN P53; TRANSCRIPTION FACTOR SNAIL; UVOMORULIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; BINDING SITE; CANCER CELL; CELL DEATH; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; METASTASIS; METASTASIS INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN SYNTHESIS; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; UBIQUITINATION;

DNA REPAIR; DNA-PKCS; MIGRATION; P53; PEPTIDES; PHOSPHORYLATION; SENSITIZATION; SNAIL1; SNAIL1 PHOSPHORYLATION;

ANIMALS; CELL LINE, TUMOR; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; NEOPLASM METASTASIS; NEOPLASM PROTEINS; NEOPLASMS; NUCLEAR PROTEINS; PEPTIDES; PROTEIN STABILITY; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84887502836     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.479840     Document Type: Article

References (43)

1. Barrallo-Gimeno, A., and Nieto, M. A. (2005) The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 132, 3151-3161
2. Huber, M. A., Kraut, N., and Beug, H. (2005) Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr. Opin. Cell Biol. 17, 548-558
3. Peinado, H., Olmeda, D., and Cano, A. (2007) Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat. Rev. Cancer 7, 415-428
4. Moreno-Bueno, G., Peinado, H., Molina, P., Olmeda, D., Cubillo, E., Santos, V., Palacios, J., Portillo, F., and Cano, A. (2009) The morphological and molecular features of the epithelial-to-mesenchymal transition. Nat. Protoc. 4, 1591-1613
5. Thiery, J. P., Acloque, H., Huang, R. Y., and Nieto, M. A. (2009) Epithelialmesenchymal transitions in development and disease. Cell 139, 871-890
6. Yang, A. D., Fan, F., Camp, E. R., van Buren, G., Liu, W., Somcio, R., Gray, M. J., Cheng, H., Hoff, P. M., and Ellis, L. M. (2006) Chronic oxaliplatin resistance induces epithelial-to-mesenchymal transition in colorectal cancer cell lines. Clin. Cancer Res. 12, 4147-4153
7. Kajiyama, H., Shibata, K., Terauchi, M., Yamashita, M., Ino, K., Nawa, A., and Kikkawa, F. (2007) Chemoresistance to paclitaxel induces epithelialmesenchymal transition and enhances metastatic potential for epithelial ovarian carcinoma cells. Int. J. Oncol. 31, 277-283
8. Cheng, G. Z., Chan, J., Wang, Q., Zhang, W., Sun, C. D., and Wang, L. H. (2007) Twist transcriptionally up-regulates AKT2 in breast cancer cells leading to increased migration, invasion, and resistance to paclitaxel. Cancer Res. 67, 1979-1987
9. Li, Q. Q., Xu, J. D., Wang, W. J., Cao, X. X., Chen, Q., Tang, F., Chen, Z. Q., Liu, X. P., and Xu, Z. D. (2009) Twist1-mediated adriamycin-induced epithelial-mesenchymal transition relates to multidrug resistance and invasive potential in breast cancer cells. Clin. Cancer Res. 15, 2657-2665
10. Kajita, M., McClinic, K. N., and Wade, P. A. (2004) Aberrant expression of the transcription factors Snail and Slug alters the response to genotoxic stress. Mol. Cell. Biol. 24, 7559-7566
11. Kurrey, N. K., Jalgaonkar, S. P., Joglekar, A. V., Ghanate, A. D., Chaskar, P. D., Doiphode, R. Y., and Bapat, S. A. (2009) Snail and Slug mediate radioresistance and chemoresistance by antagonizing p53-mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells. Stem Cells 27, 2059-2068
12. Mukherjee, B., Kessinger, C., Kobayashi, J., Chen, B. P., Chen, D. J., Chatterjee, A., and Burma, S. (2006) DNA-PK phosphorylates histone H2AX during apoptotic DNA fragmentation in mammalian cells. DNA Repair 5, 575-590
13. Solier, S., Sordet, O., Kohn, K. W., and Pommier, Y. (2009) Death receptorinduced activation of the Chk2- and histone H2AX-associatedDNAdamage response pathways. Mol. Cell. Biol. 29, 68-82
14. Shieh, S. Y., Ikeda, M., Taya, Y., and Prives, C. (1997) DNA damageinduced phosphorylation of p53 alleviates inhibition by MDM2. Cell 91, 325-334
15. Reitsema, T., Klokov, D., Banáth, J. P., and Olive, P. L. (2005) DNA-PK is responsible for enhanced phosphorylation of histone H2AX under hypertonic conditions. DNA Repair 4, 1172-1181
16. Kirchgessner, C. U., Patil, C. K., Evans, J. W., Cuomo, C. A., Fried, L. M., Carter, T., Oettinger, M. A., and Brown, J. M. (1995) DNA-dependent kinase (p350) as a candidate gene for the murine SCID defect. Science 267, 1178-1183
17. García-Barros, M., Thin, T. H., Maj, J., Cordon-Cardo, C., Haimovitz- Friedman, A., Fuks, Z., and Kolesnick, R. (2010) Impact of stromal sensitivity on radiation response of tumors implanted in SCID hosts revisited. Cancer Res. 70, 8179-8186
18. Zhang, S., Yajima, H., Huynh, H., Zheng, J., Callen, E., Chen, H. T., Wong, N., Bunting, S., Lin, Y. F., Li, M., Lee, K. J., Story, M., Gapud, E., Sleckman, B. P., Nussenzweig, A., Zhang, C. C., Chen, D. J., and Chen, B. P. (2011) Congenital bone marrow failure in DNA-PKcs mutant mice associated with deficiencies in DNA repair. J. Cell Biol. 193, 295-305
19. Lee, K. B., Parker, R. J., Bohr, V., Cornelison, T., and Reed, E. (1993) Cisplatin sensitivity/resistance in UV repair-deficient Chinese hamster ovary cells of complementation groups 1 and 3. Carcinogenesis 14, 2177-2180
20. Youn, C. K., Kim, M. H., Cho, H. J., Kim, H. B., Chang, I. Y., Chung, M. H., and You, H. J. (2004) Oncogenic H-Ras up-regulates expression of ERCC1 to protect cells from platinum-based anticancer agents. Cancer Res. 64, 4849-4857
21. Allalunis-Turner, M. J., Lintott, L. G., Barron, G. M., Day, R. S., 3rd, and Lees-Miller, S. P. (1995) Lack of correlation between DNA-dependent protein kinase activity and tumor cell radiosensitivity. Cancer Res. 55, 5200-5202
22. Gilley, D., Tanaka, H., Hande, M. P., Kurimasa, A., Li, G. C., Oshimura, M., and Chen, D. J. (2001) DNA-PKcs is critical for telomere capping. Proc. Natl. Acad. Sci. U.S.A. 98, 15084-15088
23. d'Adda di Fagagna, F., Hande, M. P., Tong, W. M., Roth, D., Lansdorp, P. M., Wang, Z. Q., and Jackson, S. P. (2001) Effects of DNA nonhomologous mammalian cells. Curr. Biol. 11, 1192-1196
24. Bailey, S. M., Meyne, J., Chen, D. J., Kurimasa, A., Li, G. C., Lehnert, B. E., and Goodwin, E. H. (1999) DNA double-strand break repair proteins are required to cap the ends of mammalian chromosomes. Proc. Natl. Acad. Sci. U.S.A. 96, 14899-14904
25. Espejel, S., Franco, S., Sgura, A., Gae, D., Bailey, S. M., Taccioli, G. E., and Blasco, M. A. (2002) Functional interaction between DNA-PKcs and telomerase in telomere length maintenance. EMBO J. 21, 6275-6287
26. Goytisolo, F. A., Samper, E., Edmonson, S., Taccioli, G. E., and Blasco, M. A. (2001) The absence of the DNA-dependent protein kinase catalytic subunit in mice results in anaphase bridges and in increased telomeric fusions with normal telomere length and G-strand overhang. Mol. Cell. Biol. 21, 3642-3651
27. Wong, R. H., Chang, I., Hudak, C. S., Hyun, S., Kwan, H. Y., and Sul, H. S. (2009) A role of DNA-PK for the metabolic gene regulation in response to insulin. Cell 136, 1056-1072
28. Kong, X., Shen, Y., Jiang, N., Fei, X., and Mi, J. (2011) Emerging roles of DNA-PK besides DNA repair. Cell Signal 23, 1273-1280
29. Wong, R. H., and Sul, H. S. (2009) DNA-PK: relaying the insulin signal to USF in lipogenesis. Cell cycle 8, 1977-1978
30. Pyun, B. J., Seo, H. R., Lee, H. J., Jin, Y. B., Kim, E. J., Kim, N. H., Kim, H. S., Nam, H. W., Yook, J. I., and Lee, Y. S. (2013) Mutual regulation between DNA-PKcs and snail1 leads to increased genomic instability and aggressive tumor characteristics. Cell Death Dis. 4, e517
31. Andersson, S., Davis, D. L., Dahlbäck, H., Jörnvall, H., and Russell, D. W. (1989) Cloning, structure, and expression of the mitochondrial cytochrome P-450 sterol 26-hydroxylase, a bile acid biosynthetic enzyme. J. Biol. Chem. 264, 8222-8229
32. Yook, J. I., Li, X. Y., Ota, I., Hu, C., Kim, H. S., Kim, N. H., Cha, S. Y., Ryu, J. K., Choi, Y. J., Kim, J., Fearon, E. R., and Weiss, S. J. (2006)AWnt-Axin2- GSK3β cascade regulates Snail1 activity in breast cancer cells. Nat. Cell Biol. 8, 1398-1406
33. Zhang, M. Z., Xu, J., Yao, B., Yin, H., Cai, Q., Shrubsole, M. J., Chen, X., Kon, V., Zheng, W., Pozzi, A., and Harris, R. C. (2009) Inhibition of 11β- hydroxysteroid dehydrogenase type II selectively blocks the tumor COX-2 pathway and suppresses colon carcinogenesis in mice and humans. J. Clin. Invest. 119, 876-885
34. Christie, D. R., Shaikh, F. M., Lucas, J. A., 4th, Lucas, J. A., 3rd, and Bellis, S. L. (2008) ST6Gal-I expression in ovarian cancer cells promotes an invasive phenotype by altering integrin glycosylation and function. J. Ovarian Res. 1, 3
35. Chiang, C., and Ayyanathan, K. (2013) Snail/Gfi-1 (SNAG) family zinc finger proteins in transcription regulation, chromatin dynamics, cell signaling, development, and disease. Cytokine Growth Factor Rev. 24, 123-131
36. Nieto, M. A. (2002) The Snail superfamily of zinc-finger transcription factors. Nat. Rev. Mol. Cell Biol. 3, 155-166
37. Collins, T., Stone, J. R., and Williams, A. J. (2001) All in the family: the BTB/POZ, KRAB, and SCAN domains. Mol. Cell. Biol. 21, 3609-3615
38. Carver, E. A., Jiang, R., Lan, Y., Oram, K. F., and Gridley, T. (2001) The mouse Snail gene encodes a key regulator of the epithelial-mesenchymal transition. Mol. Cell. Biol. 21, 8184-8188
39. Vincent, T., Neve, E. P., Johnson, J. R., Kukalev, A., Rojo, F., Albanell, J., Pietras, K., Virtanen, I., Philipson, L., Leopold, P. L., Crystal, R. G., de Herreros, A. G., Moustakas, A., Pettersson, R. F., and Fuxe, J. (2009) A SNAIL1-SMAD3/4 transcriptional repressor complex promotes TGF-β mediated epithelial-mesenchymal transition. Nat. Cell Biol. 11, 943-950
40. Ding, X., Park, S. I., McCauley, L. K., and Wang, C. Y. (2013) Signaling between transforming growth factor β (TGF-β) and transcription factor SNAI2 represses expression of microRNA miR-203 to promote epithelialmesenchymal transition and tumor metastasis. J. Biol. Chem. 288, 10241-10253
41. Dhasarathy, A., Phadke, D., Mav, D., Shah, R. R., and Wade, P. A. (2011) The transcription factors Snail and Slug activate the transforming growth factor-β signaling pathway in breast cancer. PLoS One 6, e26514
42. Wang, S., Guo, M., Ouyang, H., Li, X., Cordon-Cardo, C., Kurimasa, A., Chen, D. J., Fuks, Z., Ling, C. C., and Li, G. C. (2000) The catalytic subunit of DNA-dependent protein kinase selectively regulates p53-dependent apoptosis but not cell-cycle arrest. Proc. Natl. Acad. Sci. U.S.A. 97, 1584-1588
43. Surade, S., and Blundell, T. L. (2012) Structural biology and drug discovery of difficult targets: the limits of ligandability. Chem. Biol. 19, 42-50