PNAS-4, an early DNA damage response gene, induces S phase arrest and apoptosis by activating checkpoint kinases in lung cancer cells

Journal of Biological Chemistry

Volumn 290, Issue 24, 2015, Pages 14927-14944

  Yuan, Zhu ^a   Guo, Wenhao ^b   Yang, Jun ^a   Li, Lei ^a   Wang, Meiliang ^a   Lei, Yi ^a   Wan, Yang ^a   Zhao, Xinyu ^a   Luo, Na ^c   Cheng, Ping ^a   Liu, Xinyu ^a   Nie, Chunlai ^a   Peng, Yong ^a   Tong, Aiping ^a   Wei, Yuquan ^a  

^a SICHUAN UNIVERSITY   (China)

^b SICHUAN UNIVERSITY   (China)

^c NANKAI UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL ORGANS; CELL DEATH; CHEMICAL ACTIVATION; CYTOLOGY; DISEASES; DNA; ENZYMES; GENES; HISTOLOGY; METHANE; PLATINUM COMPOUNDS; PROTEINS; TISSUE;

ACTION MECHANISMS; DNA DAMAGE RESPONSE; DNA-DEPENDENT PROTEIN KINASE; GENE SILENCING; LUNG CANCER CELLS; OVER-EXPRESSION; PRO-APOPTOTIC GENES; PROLIFERATION INHIBITION;

CELLS;

ATM PROTEIN; ATR PROTEIN; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; CYCLIN A; CYCLIN E; HISTONE H2AX; MITOGEN ACTIVATED PROTEIN KINASE P38; APOPTOSIS REGULATORY PROTEIN; ATM PROTEIN, HUMAN; ATR PROTEIN, HUMAN; PNAS4 PROTEIN, HUMAN; PRIMER DNA; PROTEIN KINASE; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; DNA STRAND BREAKAGE; DNA SYNTHESIS; DOWN REGULATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FEMALE; GENE; GENE OVEREXPRESSION; GENE SILENCING; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG CANCER CELL LINE; MALE; PNAS 4 GENE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; S PHASE CELL CYCLE CHECKPOINT; SIGNAL TRANSDUCTION; UPREGULATION; CELL CYCLE S PHASE; DNA DAMAGE; ENZYMOLOGY; GENETICS; LUNG TUMOR; METABOLISM; NUCLEOTIDE SEQUENCE; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; BASE SEQUENCE; CELL LINE, TUMOR; CHECKPOINT KINASE 2; DNA DAMAGE; DNA PRIMERS; ENZYME ACTIVATION; HUMANS; LUNG NEOPLASMS; PROTEIN KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; S PHASE;

EID: 84931274481     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.658419     Document Type: Article

References (64)

1. Han, S. W., and Roman, J. (2010) Targeting apoptotic signaling pathways in human lung cancer. Curr. Cancer Drug. Targets 10, 566-574
2. Johnstone, R. W., Ruefli, A. A., and Lowe, S. W. (2002) Apoptosis: a link between cancer genetics and chemotherapy. Cell 108, 153-164
3. Yu, J., and Zhang, L. (2004) Apoptosis in human cancer cells. Curr. Opin. Oncol. 16, 19-24
4. Choy, A., Severo, M. S., Sun, R., Girke, T., Gillespie, J. J., and Pedra, J. H. (2013) Decoding the ubiquitin-mediated pathway of arthropod disease vectors. PLoS One 8, e78077
5. Shin, E. J., Shin, H. M., Nam, E., Kim, W. S., Kim, J. H., Oh, B. H., and Yun, Y. (2012) DeSUMOylating isopeptidase: a second class of SUMO protease. EMBO Rep. 13, 339-346
6. Forrest, M. S., Lan, Q., Hubbard, A. E., Zhang, L., Vermeulen, R., Zhao, X., Li, G., Wu, Y. Y., Shen, M., Yin, S., Chanock, S. J., Rothman, N., and Smith, M. T. (2005) Discovery of novel biomarkers by microarray analysis of peripheral blood mononuclear cell gene expression in benzene-exposed workers. Environ. Health Perspect. 113, 801-807
7. Santin, A. D., Zhan, F., Bignotti, E., Siegel, E. R., Cané, S., Bellone, S., Palmieri, M., Anfossi, S., Thomas, M., Burnett, A., Kay, H. H., Roman, J. J., O'Brien, T. J., Tian, E., Cannon, M. J., Shaughnessy, J., Jr., and Pecorelli, S. (2005) Gene expression profiles of primary HPV16- and HPV18-infected early stage cervical cancers and normal cervical epithelium: identification of novel candidate molecular markers for cervical cancer diagnosis and therapy. Virology 331, 269-291
8. Best, C. J., Gillespie, J. W., Yi, Y., Chandramouli, G. V., Perlmutter, M. A., Gathright, Y., Erickson, H. S., Georgevich, L., Tangrea, M. A., Duray, P. H., González, S., Velasco, A., Linehan, W. M., Matusik, R. J., Price, D. K., Figg, W. D., Emmert-Buck, M. R., and Chuaqui, R. F. (2005) Molecular alterations in primary prostate cancer after androgen ablation therapy. Clin. Cancer Res. 11, 6823-6834
9. Filippov, V., Filippova, M., and Duerksen-Hughes, P. J. (2007) The early response to DNA damage can lead to activation of alternative splicing activity resulting in CD44 splice pattern changes. Cancer Res. 67, 7621-7630
10. Hou, S., Zhao, Z., Yan, F., Chen, X., Deng, H., Chen, X., Wang, Y., and Wei, Y. (2009) Genetic transfer of PNAS-4 induces apoptosis and enhances sensitivity to gemcitabine in lung cancer. Cell Biol. Int. 33, 276-282
11. Yan, F., Gou, L., Yang, J., Chen, L., Tong, A., Tang, M., Yuan, Z., Yao, S., Zhang, P., and Wei, Y. (2009) A novel pro-apoptosis gene PNAS4 that induces apoptosis in A549 human lung adenocarcinoma cells and inhibits tumor growth in mice. Biochimie 91, 502-507
12. Yuan, Z., Liu, H., Yan, F., Wang, Y., Gou, L., Nie, C., Ding, Z., Lai, S., Zhao, Y., Zhao, X., Li, J., Deng, H., Mao, Y., Chen, L., and Wei, Y. (2009) Improved therapeutic efficacy against murine carcinoma by combining honokiol with gene therapy of PNAS-4, a novel pro-apoptotic gene. Cancer Sci. 100, 1757-1766
13. Yuan, Z., Yan, F., Wang, Y. S., Liu, H. Y., Gou, L. T., Zhao, X. Y., Lai, S. T., Deng, H. X., Li, J., Ding, Z. Y., Xiong, S. Q., Kan, B., Mao, Y. Q., Chen, L. J., Wei, Y. Q., and Zhao, X. (2009) PNAS-4, a novel pro-apoptotic gene, can potentiate antineoplastic effects of cisplatin. Cancer Chemother. Pharmacol. 65, 13-25
14. Zeng, H., Yuan, Z., Zhu, H., Li, L., Shi, H., Wang, Z., Fan, Y., Deng, Q., Zeng, J., He, Y., Xiao, J., and Li, Z. (2012) Expression of hPNAS-4 radiosensitizes Lewis lung cancer. Int. J. Radiat. Oncol. Biol. Phys. 84, e533-e540
15. Li, L., Chen, D. B., Lin, C., Cao, K., Wan, Y., Zhao, X. Y., Nie, C. L., Yuan, Z., and Wei, Y. Q. (2013) hPNAS-4 inhibits proliferation through S phase arrest and apoptosis: underlying action mechanism inovarian cancer cells. Apoptosis 18, 467-479
16. Xu, X., Hamhouyia, F., Thomas, S. D., Burke, T. J., Girvan, A. C., McGregor, W. G., Trent, J. O., Miller, D. M., and Bates, P. J. (2001) Inhibition of DNA replication and induction of S phase cell cycle arrest by G-rich oligonucleotides. J. Biol. Chem. 276, 43221-43230
17. Baluchamy, S., Ravichandran, P., Periyakaruppan, A., Ramesh, V., Hall, J. C., Zhang, Y., Jejelowo, O., Gridley, D. S., Wu, H., and Ramesh, G. T. (2010) Induction of cell death through alteration of oxidants and antioxidants in lung epithelial cells exposed to high energy protons. J. Biol. Chem. 285, 24769-24774
18. Wei, Y. Q., Zhao, X., Kariya, Y., Fukata, H., Teshigawara, K., and Uchida, A. (1994) Induction of apoptosis by quercetin: involvement of heat shock protein. Cancer Res. 54, 4952-4957
19. Zhang, N., Yang, Y., Cheng, L., Zhang, X. M., Zhang, S., Wang, W., Liu, S. Y., Wang, S. Y., Wang, R. B., Xu, W. J., Dai, L., Yan, N., Fan, P., Dai, L. X., Tian, H. W., Liu, L., and Deng, H. X. (2012) Combination of Caspy2 and IP-10 gene therapy significantly improves therapeutic efficacy against murine malignant neoplasm growth and metastasis. Hum. Gene Ther. 23, 837-846
20. Salic, A., and Mitchison, T. J. (2008) A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc. Natl. Acad. Sci. U. S. A. 105, 2415-2420
21. Sinkkonen, S. T., Chai, R., Jan, T. A., Hartman, B. H., Laske, R. D., Gahlen, F., Sinkkonen, W., Cheng, A. G., Oshima, K., and Heller, S. (2011) Intrinsic regenerative potential of murine cochlear supporting cells. Sci. Rep. 1, 26
22. Kang, K., Oh, S. H., Yun, J. H., Jho, E. H., Kang, J. H., Batsuren, D., Tunsag, J., Park, K. H., Kim, M., and Nho, C. W. (2011) A novel topoisomerase inhibitor, daurinol, suppresses growth of HCT116 cells with low hematological toxicity compared to etoposide. Neoplasia 13, 1043-1057
23. Yang, D., Li, L., Liu, H., Wu, L., Luo, Z., Li, H., Zheng, S., Gao, H., Chu, Y., Sun, Y., Liu, J., and Jia, L. (2013) Inductionof autophagy and senescence by knockdown of ROC1 E3 ubiquitin ligase to suppress the growth of liver cancer cells. Cell Death Differ. 20, 235-247
24. Zhou, B., Yan, H., Li, Y., Wang, R., Chen, K., Zhou, Z., and Sun, X. (2012) PNAS-4 expression and its relationship to p53 in colorectal cancer. Mol. Biol. Rep. 39, 243-249
25. Harper, J. W., Adami, G. R., Wei, N., Keyomarsi, K., and Elledge, S. J. (1993) The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75, 805-816
26. Ashton, A. W., Watanabe, G., Albanese, C., Harrington, E. O., Ware, J. A., and Pestell, R. G. (1999) Protein kinase CS inhibition of S-phase transition in capillary endothelial cells involves the cyclin-dependent kinase inhibitor p27Kip1. J. Biol. Chem. 274, 20805-20811
27. Gartel, A. L., and Tyner, A. L. (2002) The role of the cyclin-dependent kinase inhibitor p21 in apoptosis. Mol. Cancer Ther. 1, 639-649
28. Beier, F., Taylor, A. C., and LuValle, P. (1999) The Raf-1/MEK/ERK pathway regulates the expression of the p21Cip1/Waf1 gene in chondrocytes. J. Biol. Chem. 274, 30273-30279
29. Kim, G. Y., Mercer, S. E., Ewton, D. Z., Yan, Z., Jin, K., and Friedman, E. (2002) The stress-activated protein kinases p38 α and JNK1 stabilize p21Cip1 by phosphorylation. J. Biol. Chem. 277, 29792-29802
30. Park, K. S., Ahn, Y., Kim, J. A., Yun, M. S., Seong, B. L., and Choi, K. Y. (2002) Extracellular zinc stimulates ERK-dependent activation of p21Cip/WAF1 and inhibits proliferation of colorectal cancer cells. Br. J. Pharmacol. 137, 597-607
31. Favata, M. F., Horiuchi, K. Y., Manos, E. J., Daulerio, A. J., Stradley, D. A., Feeser, W. S., Van Dyk, D. E., Pitts, W. J., Earl, R. A., Hobbs, F., Copeland, R. A., Magolda, R. L., Scherle, P. A., and Trzaskos, J. M. (1998) Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem. 273, 18623-18632
32. Dudley, D. T., Pang, L., Decker, S. J., Bridges, A. J., and Saltiel, A. R. (1995) A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. U. S. A. 92, 7686-7689
33. Yeo, E. J., Ryu, J. H., Chun, Y. S., Cho, Y. S., Jang, I. J., Cho, H., Kim, J., Kim, M. S., and Park, J. W. (2006) YC-1 induces S cell cycle arrest and apoptosis by activating checkpoint kinases. Cancer Res. 66, 6345-6352
34. Hassepass, I., Voit, R., and Hoffmann, I. (2003) Phosphorylation at serine 75 is required for UV-mediated degradation of human Cdc25A phosphatase at the S-phase checkpoint. J. Biol. Chem. 278, 29824-29829
35. Bartek, J., Lukas, C, and Lukas, J. (2004) Checking on DNA damage in S phase. Nat Rev. Mol. Cell Biol. 5, 792-804
36. Bartek, J., and Lukas, J. (2003) Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell 3, 421-429
37. Li, J., and Stern, D. F. (2005) Regulation of CHK2 by DNA-dependent protein kinase. J. Biol. Chem. 280, 12041-12050
38. Gewandter, J. S., Bambara, R. A., and O'Reilly, M. A. (2011) The RNA surveillance protein SMG1 activates p53 in response to DNA doublestrand breaks but not exogenously oxidized mRNA. Cell Cycle 10, 2561-2567
39. Gehen, S. C., Staversky, R. J., Bambara, R. A., Keng, P. C, and O'Reilly, M. A. (2008) hSMG-1 and ATM sequentially and independently regulate the G1 checkpoint during oxidative stress. Oncogene 27, 4065-4074
40. Brumbaugh, K. M., Otterness, D. M., Geisen, C., Oliveira, V., Brognard, J., Li, X., Lejeune, F., Tibbetts, R. S., Maquat, L. E., and Abraham, R. T. (2004) The mRNA surveillance protein hSMG-1 functions in genotoxic stress response pathways in mammalian cells. Mol. Cell 14, 585-598
41. Clarke, C. A., Bennett, L. N., and Clarke, P. R. (2005) Cleavage of claspin by caspase-7 during apoptosis inhibits the Chk1 pathway. J. Biol. Chem. 280, 35337-35345
42. Germain, M., Affar, E. B., D'Amours, D., Dixit, V. M., Salvesen, G. S., and Poirier, G. G. (1999) Cleavage of automodified poly (ADP-ribose) polymerase during apoptosis: evidence for involvement of caspase-7. J. Biol. Chem. 274, 28379-28384
43. Okita, N., Yoshimura, M., Watanabe, K., Minato, S., Kudo, Y., Higami, Y., and Tanuma, S. (2013) CHK1 cleavage in programmed cell death is intricately regulated by both caspase and non-caspase family proteases. Biochim. Biophys. Acta 1830, 2204-2213
44. Matsuura, K., Wakasugi, M., Yamashita, K., and Matsunaga, T. (2008) Cleavage-mediated activation of Chk1 during apoptosis. J. Biol. Chem. 283, 25485-25491
45. Bonner, W. M., Redon, C. E., Dickey, J. S., Nakamura, A. J., Sedelnikova, O. A., Solier, S., and Pommier, Y. (2008) 7H2AX and cancer. Nat. Rev. Cancer 8, 957-967
46. Solier, S., and Pommier, Y. (2014) The nuclear 7-H2AX apoptotic ring: implications for cancers and autoimmune diseases. Cell Mol. Life Sci. 71, 2289-2297
47. Foster, S. S., De, S., Johnson, L. K., Petrini, J. H., and Stracker, T. H. (2012) Cell cycle- and DNA repair pathway-specific effects of apoptosis on tumor suppression. Proc. Natl. Acad. Sci. U. S. A. 109, 9953-9958
48. Pabla, N., Huang, S., Mi, Q. S., Daniel, R., and Dong, Z. (2008) ATR-Chk2 signaling in p53 activation and DNA damage response during cisplatininduced apoptosis. J. Biol. Chem. 283, 6572-6583
49. Cai, P., Xia, X., Li, F., Cui, Y., Yang, Q., and Chen, M. (2012) PNAS4 knockout does not induce obviously neurocytes apoptosis and abnormal development in mice brain. Mol. Biol. Rep. 39, 621-628
50. Hunter, T., and Pines, J. (1994) Cyclins and cancer. II. Cyclin D and CDK inhibitors come of age. Cell 79, 573-582
51. Eastman, A. (2004) Cell cycle checkpoints and their impact on anticancer therapeutic strategies. J. CellBiochem. 91, 223-231
52. Masai, H., Matsumoto, S., You, Z., Yoshizawa-Sugata, N, and Oda, M. (2010) Eukaryotic chromosome DNA replication: where, when, and how? Annu. Rev. Biochem. 79, 89-130
53. Ray, D., and Kiyokawa, H. (2007) CDC25A levels determine the balance of proliferation and checkpoint response. Cell Cycle 6, 3039-3042
54. Mailand, N., Falck, J., Lukas, C., Syljuasen, R. G., Welcker, M., Bartek, J., and Lukas, J. (2000) Rapid destruction of human Cdc25A in response to DNA damage. Science 288, 1425-1429
55. Xiao, Z., Chen, Z., Gunasekera, A. H., Sowin, T. J., Rosenberg, S. H., Fesik, S., and Zhang, H. (2003) Chk1 mediates S and G2 arrests through Cdc25A degradation in response to DNA-damaging agents. J. Biol. Chem. 278, 21767-21773
56. Sørensen, C. S., Syljuåsen, R. G., Falck, J., Schroeder, T., Rönnstrand, L., Khanna, K. K., Zhou, B. B., Bartek, J., and Lukas, J. (2003) Chk1 regulates the S phase checkpoint by coupling the physiological turnover and ionizing radiation-induced accelerated proteolysis of Cdc25A. Cancer Cell 3, 247-258
57. Sancar, A., Lindsey-Boltz, L. A., Unsal-Kaçmaz, K., and Linn, S. (2004) Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73, 39-85
58. Cimprich, K. A., and Cortez, D. (2008) ATR: an essential regulator of genome integrity. Nat. Rev. Mol. Cell Biol. 9, 616-627
59. Lee, A. Y., Chiba, T., Truong, L. N., Cheng, A. N., Do, J., Cho, M. J., Chen, L., and Wu, X. (2012) Dbf4 is direct downstream target of ataxia telangiectasia mutated (ATM) and ataxia telangiectasia and Rad3-related (ATR) protein to regulate intra-S-phase checkpoint. J. Biol. Chem. 287, 2531-2543
60. Lee, J. H., and Paull, T. T. (2007) Activation and regulation of ATM kinase activity in response to DNA double-strand breaks. Oncogene 26, 7741-7748
61. Abraham, R. T. (2001) Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15, 2177-2196
62. Yamashita, A., Ohnishi, T., Kashima, I., Taya, Y., and Ohno, S. (2001) Human SMG-1, a novel phosphatidylinositol 3-kinase-related protein kinase, associates with components of the mRNA surveillance complex and is involved in the regulation of nonsense-mediated mRNA decay. Genes Dev. 15, 2215-2228
63. Zhang, Y. W., Otterness, D. M., Chiang, G. G., Xie, W., Liu, Y. C., Mercurio, F., and Abraham, R. T. (2005) Genotoxic stress targets human Chk1 for degradation by the ubiquitin-proteasome pathway. Mol. Cell 19, 607-618
64. Solier, S., and Pommier, Y. (2009) The apoptotic ring: a novel entity with phosphorylated histones H2AX and H2B and activated DNA damage response kinases. Cell Cycle 8, 1853-1859