Depletion of RAD17 sensitizes pancreatic cancer cells to gemcitabine

Journal of Cell Science

Volumn 126, Issue 15, 2013, Pages 3380-3389

  Fredebohm, Johannes ^a   Wolf, Jonas ^a   Hoheisel, Jörg D ^a   Boettcher, Michael ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

ATR CHK1 signalling pathway; Gemcitabine; Gemcitabine combination therapy; Pancreatic cancer; RAD17; shRNA screening

Indexed keywords

CELL DNA; CHECKPOINT KINASE 1; GEMCITABINE; RAD17 PROTEIN; REGULATOR PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ANAPHASE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELLULAR DISTRIBUTION; CHEMOSENSITIZATION; CONTROLLED STUDY; DNA DAMAGE; DNA FRAGMENTATION; DRUG CYTOTOXICITY; ENZYME INHIBITION; GENE SILENCING; GENE TARGETING; MITOSIS; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN DEPLETION; RNA INTERFERENCE; S PHASE CELL CYCLE CHECKPOINT;

ATR/CHK1 SIGNALLING PATHWAY; GEMCITABINE; GEMCITABINE-COMBINATION THERAPY; PANCREATIC CANCER; RAD17; SHRNA SCREENING;

ANTIMETABOLITES, ANTINEOPLASTIC; CELL CYCLE PROTEINS; CELL LINE, TUMOR; DEOXYCYTIDINE; HUMANS; PANCREATIC NEOPLASMS; PHOSPHORYLATION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84883325294     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.124768     Document Type: Article

References (51)

1. Aarts, M., Sharpe, R., Garcia-Murillas, I., Gevensleben, H., Hurd, M. S., Shumway, S. D., Toniatti, C., Ashworth, A. and Turner, N. C. (2012). Forced mitotic entry of S-phase cells as a therapeutic strategy induced by inhibition of WEE1. Cancer Discov. 2, 524-539.
2. Alberts, B. (2002). Molecular Biology of the Cell. New York, NY: Garland Science.
3. Azorsa, D. O., Gonzales, I. M., Basu, G. D., Choudhary, A., Arora, S., Bisanz, K. M., Kiefer, J. A., Henderson, M. C., Trent, J. M., Von Hoff, D. D. et al. (2009). Synthetic lethal RNAi screening identifies sensitizing targets for gemcitabine therapy in pancreatic cancer. J. Transl. Med. 7, 43.
4. Baptiste, N., Friedlander, P., Chen, X. and Prives, C. (2002). The proline-rich domain of p53 is required for cooperation with anti-neoplastic agents to promote apoptosis of tumor cells. Oncogene 21, 9-21.
5. Boutros, R., Lobjois, V. and Ducommun, B. (2007). CDC25 phosphatases in cancer cells: key players? Good targets? Nat. Rev. Cancer 7, 495-507.
6. Carrassa, L. and Damia, G. (2011). Unleashing Chk1 in cancer therapy. Cell Cycle 10, 2121-2128.
7. Castedo, M., Perfettini, J. L., Roumier, T., Valent, A., Raslova, H., Yakushijin, K., Horne, D., Feunteun, J., Lenoir, G., Medema, R. et al. (2004). Mitotic catastrophe constitutes a special case of apoptosis whose suppression entails aneuploidy. Oncogene 23, 4362-4370.
8. Chen, Z., Xiao, Z., Gu, W. Z., Xue, J., Bui, M. H., Kovar, P., Li, G., Wang, G., Tao, Z. F., Tong, Y. et al. (2006). Selective Chk1 inhibitors differentially sensitize p53-deficient cancer cells to cancer therapeutics. Int. J. Cancer 119, 2784-2794.
9. Cortez, D., Guntuku, S., Qin, J. and Elledge, S. J. (2001). ATR and ATRIP: partners in checkpoint signaling. Science 294, 1713-1716.
10. Crul, M., van Waardenburg, R. C., Bocxe, S., van Eijndhoven, M. A., Pluim, D., Beijnen, J. H. and Schellens, J. H. (2003). DNA repair mechanisms involved in gemcitabine cytotoxicity and in the interaction between gemcitabine and cisplatin. Biochem. Pharmacol. 65, 275-282.
11. Czekanska, E. M. (2011). Assessment of cell proliferation with resazurin-based fluorescent dye. Methods Mol. Biol. 740, 27-32.
12. Davies, K. D., Cable, P. L., Garrus, J. E., Sullivan, F. X., von Carlowitz, I., Huerou, Y. L., Wallace, E., Woessner, R. D. and Gross, S. (2011). Chk1 inhibition and Wee1 inhibition combine synergistically to impede cellular proliferation. Cancer Biol. Ther. 12, 788-796.
13. Echeverri, C. J., Beachy, P. A., Baum, B., Boutros, M., Buchholz, F., Chanda, S. K., Downward, J., Ellenberg, J., Fraser, A. G., Hacohen, N. et al. (2006). Minimizing the risk of reporting false positives in large-scale RNAi screens. Nat. Methods 3, 777-779.
14. Fredebohm, J., Boettcher, M., Eisen, C., Gaida, M. M., Heller, A., Keleg, S., Tost, J., Greulich-Bode, K. M., Hotz-Wagenblatt, A., Lathrop, M. et al. (2012). Establishment and characterization of a highly tumourigenic and cancer stem cell enriched pancreatic cancer cell line as a well defined model system. PLoS ONE 7, e48503.
15. Garrett, M. D. and Collins, I. (2011). Anticancer therapy with checkpoint inhibitors: what, where and when? Trends Pharmacol. Sci. 32, 308-316.
16. Glienke, W., Maute, L., Wicht, J. and Bergmann, L. (2012). The dual PI3K/mTOR inhibitor NVP-BGT226 induces cell cycle arrest and regulates Survivin gene expression in human pancreatic cancer cell lines. Tumour Biol. 33, 757-765.
17. Hackert, T., Büchler, M. W. and Werner, J. (2009). Surgical options in the management of pancreatic cancer. Minerva Chir. 64, 465-476.
18. Hans, F. and Dimitrov, S. (2001). Histone H3 phosphorylation and cell division. Oncogene 20, 3021-3027.
19. Heinemann, V., Boeck, S., Hinke, A., Labianca, R. and Louvet, C. (2008). Meta-analysis of randomized trials: evaluation of benefit from gemcitabine-based combination chemotherapy applied in advanced pancreatic cancer. BMC Cancer 8, 82.
20. Huang, P., Chubb, S., Hertel, L. W., Grindey, G. B. and Plunkett, W. (1991). Action of 29,29-difluorodeoxycytidine on DNA synthesis. Cancer Res. 51, 6110-6117.
21. Huang, D. W., Sherman, B. T. and Lempicki, R. A. (2009). Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1-13.
22. Hung, S. W., Mody, H. R. and Govindarajan, R. (2012). Overcoming nucleoside analog chemoresistance of pancreatic cancer: a therapeutic challenge. Cancer Lett. 320, 138-149.
23. Iorns, E., Lord, C. J., Turner, N. and Ashworth, A. (2007). Utilizing RNA interference to enhance cancer drug discovery. Nat. Rev. Drug Discov. 6, 556-568.
24. Kassner, P. D. (2008). Discovery of novel targets with high throughput RNA interference screening. Comb. Chem. High Throughput Screen. 11, 175-184.
25. Kern, S. E., Shi, C. and Hruban, R. H. (2011). The complexity of pancreatic ductal cancers and multidimensional strategies for therapeutic targeting. J. Pathol. 223, 295-306.
26. Ko, A. H., Youssoufian, H., Gurtler, J., Dicke, K., Kayaleh, O., Lenz, H. J., Keaton, M., Katz, T., Ballal, S. and Rowinsky, E. K. (2012). A phase II randomized study of cetuximab and bevacizumab alone or in combination with gemcitabine as first-line therapy for metastatic pancreatic adenocarcinoma. Invest. New Drugs 30, 1597-1606.
27. Landau, H. J., McNeely, S. C., Nair, J. S., Comenzo, R. L., Asai, T., Friedman, H., Jhanwar, S. C., Nimer, S. D. and Schwartz, G. K. (2012). The checkpoint kinase inhibitor AZD7762 potentiates chemotherapy-induced apoptosis of p53-mutated multiple myeloma cells. Mol. Cancer Ther. 11, 1781-1788.
28. Lee, J. and Dunphy, W. G. (2010). Rad17 plays a central role in establishment of the interaction between TopBP1 and the Rad9-Hus1-Rad1 complex at stalled replication forks. Mol. Biol. Cell 21, 926-935.
29. Ma, Z., Yao, G., Zhou, B., Fan, Y., Gao, S. and Feng, X. (2012). The Chk1 inhibitor AZD7762 sensitises p53 mutant breast cancer cells to radiation in vitro and in vivo. Mol. Med. Rep. 6, 897-903.
30. Majka, J., Binz, S. K., Wold, M. S. and Burgers, P. M. (2006). Replication protein A directs loading of the DNA damage checkpoint clamp to 59-DNA junctions. J. Biol. Chem. 281, 27855-27861.
31. Merl, M. Y., Abdelghany, O., Li, J. and Saif, M. W. (2010). First-line treatment of metastatic pancreatic adenocarcinoma: can we do better? Highlights from the "2010 ASCO Annual Meeting". Chicago, IL, USA. June 4-8, 2010. JOP 11, 317-320.
32. Moore, M. J., Goldstein, D., Hamm, J., Figer, A., Hecht, J. R., Gallinger, S., Au, H. J., Murawa, P., Walde, D., Wolff, R. A. et al.; National Cancer Institute of Canada Clinical Trials Group (2007). Erlotinib plus gemcitabine compared with gemcitabine alone in patients with advanced pancreatic cancer: a phase III trial of the National Cancer Institute of Canada Clinical Trials Group. J. Clin. Oncol. 25, 1960-1966.
33. O'Connell, M. J., Raleigh, J. M., Verkade, H. M. and Nurse, P. (1997). Chk1 is a wee1 kinase in the G2 DNA damage checkpoint inhibiting cdc2 by Y15 phosphorylation. EMBO J. 16, 545-554.
34. Ouyang, H., Mou, L., Luk, C., Liu, N., Karaskova, J., Squire, J. and Tsao, M. S. (2000). Immortal human pancreatic duct epithelial cell lines with near normal genotype and phenotype. Am. J. Pathol. 157, 1623-1631.
35. Petitjean, A., Mathe, E., Kato, S., Ishioka, C., Tavtigian, S. V., Hainaut, P. and Olivier, M. (2007). Impact of mutant p53 functional properties on TP53 mutation patterns and tumor phenotype: lessons from recent developments in the IARC TP53 database. Hum. Mutat. 28, 622-629.
36. Philip, P. A. (2008). Targeted therapies for pancreatic cancer. Gastrointest Cancer Res. 2 Suppl., S16-S19.
37. Ritchie, M. E., Dunning, M. J., Smith, M. L., Shi, W. and Lynch, A. G. (2011). BeadArray expression analysis using bioconductor. PLoS Comput. Biol. 7, e1002276.
38. Safran, H., Iannitti, D., Ramanathan, R., Schwartz, J. D., Steinhoff, M., Nauman, C., Hesketh, P., Rathore, R., Wolff, R., Tantravahi, U. et al. (2004). Herceptin and gemcitabine for metastatic pancreatic cancers that overexpress HER-2/neu. Cancer Invest. 22, 706-712.
39. Sambrook, J. and Russell, D. W. (2006). SDS-polyacrylamide gel electrophoresis of proteins. CSH Protoc 2006.
40. Schmitt, M. and Pawlita, M. (2009). High-throughput detection and multiplex identification of cell contaminations. Nucleic Acids Res. 37, e119.
41. Shiomi, Y., Shinozaki, A., Nakada, D., Sugimoto, K., Usukura, J., Obuse, C. and Tsurimoto, T. (2002). Clamp and clamp loader structures of the human checkpoint protein complexes, Rad9-1-1 and Rad17-RFC. Genes Cells 7, 861-868.
42. Siegel, R., Naishadham, D. and Jemal, A. (2013). Cancer statistics, 2013. CA Cancer J. Clin. 63, 11-30.
43. Stathis, A. and Moore, M. J. (2010). Advanced pancreatic carcinoma: current treatment and future challenges. Nat. Rev. Clin Oncol. 7, 163-172.
44. Takai, H., Tominaga, K., Motoyama, N., Minamishima, Y. A., Nagahama, H., Tsukiyama, T., Ikeda, K., Nakayama, K., Nakanishi, M. and Nakayama, K. (2000). Aberrant cell cycle checkpoint function and early embryonic death in Chk1(-/-) mice. Genes Dev. 14, 1439-1447.
45. Venkatesha, V. A., Parsels, L. A., Parsels, J. D., Zhao, L., Zabludoff, S. D., Simeone, D. M., Maybaum, J., Lawrence, T. S. and Morgan, M. A. (2012). Sensitization of pancreatic cancer stem cells to gemcitabine by Chk1 inhibition. Neoplasia 14, 519-525.
46. Walker, K. K. and Levine, A. J. (1996). Identification of a novel p53 functional domain that is necessary for efficient growth suppression. Proc. Natl. Acad. Sci. USA 93, 15335-15340.
47. Wang, Z., Li, Y., Ahmad, A., Banerjee, S., Azmi, A. S., Kong, D. and Sarkar, F. H. (2011). Pancreatic cancer: understanding and overcoming chemoresistance. Nat. Rev. Gastroenterol Hepatol. 8, 27-33.
48. Yan, S. and Michael, W. M. (2009). TopBP1 and DNA polymerase alpha-mediated recruitment of the 9-1-1 complex to stalled replication forks: implications for a replication restart-based mechanism for ATR checkpoint activation. Cell Cycle 8, 2877-2884.
49. Zhu, J., Jiang, J., Zhou, W., Zhu, K. and Chen, X. (1999). Differential regulation of cellular target genes by p53 devoid of the PXXP motifs with impaired apoptotic activity. Oncogene 18, 2149-2155.
50. Zou, L. and Elledge, S. J. (2003). Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300, 1542-1548.
51. Zufferey, R., Nagy, D., Mandel, R. J., Naldini, L. and Trono, D. (1997). Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat. Biotechnol. 15, 871-875.