Inhibition of autophagy enhances DNA damage-induced apoptosis by disrupting CHK1-dependent S phase arrest

Toxicology and Applied Pharmacology

Volumn 278, Issue 3, 2014, Pages 249-258

  Liou, Jong Shian ^a   Wu, Yi Chen ^a   Yen, Wen Yen ^a   Tang, Yu Shuan ^a   Kakadiya, Rajesh B ^b   Su, Tsann Long ^b   Yih, Ling Huei ^a  

^a INSTITUTE OF CELLULAR AND ORGANISMIC BIOLOGY   (Taiwan)

^b INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

Author keywords

Apoptosis; Autophagy; CHK1; DNA alkylating agent; DNA damage; S phase arrest

Indexed keywords

3 METHYLADENINE; BAFILOMYCIN A1; CASPASE 9; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; HISTONE H2AX; MICROTUBULE ASSOCIATED PROTEIN 1; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL CULTURE; CELL CYCLE; CELL CYCLE PHASE; CELL CYCLE S PHASE; CELL DEATH; CELL FATE; CELL GROWTH; CELL SURVIVAL; CONTROLLED STUDY; DNA CONTENT; DNA DAMAGE; DNA DAMAGE CHECKPOINT; DNA SYNTHESIS; FEMALE; GROWTH INHIBITION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; PROTEIN PHOSPHORYLATION; S PHASE CELL CYCLE CHECKPOINT;

APOPTOSIS; AUTOPHAGY; CHK1; DNA ALKYLATING AGENT; DNA DAMAGE; S PHASE ARREST;

ANTINEOPLASTIC AGENTS, ALKYLATING; APOPTOSIS; AUTOPHAGY; CARBAMATES; CARCINOMA; CELL PROLIFERATION; CELL SURVIVAL; CLASS III PHOSPHATIDYLINOSITOL 3-KINASES; CROSS-LINKING REAGENTS; DRUG SYNERGISM; ENZYME INHIBITORS; FEMALE; GENE SILENCING; HELA CELLS; HETEROCYCLIC COMPOUNDS, 3-RING; HUMANS; INDENES; NEOPLASM PROTEINS; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; S PHASE; UBIQUITIN-ACTIVATING ENZYMES; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84902314983     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2014.04.028     Document Type: Article

References (55)

1. Abedin M.J., Wang D., McDonnell M.A., Lehmann U., Kelekar A. Autophagy delays apoptotic death in breast cancer cells following DNA damage. Cell Death Differ. 2007, 14:500-510.
2. Akkari Y.M., Bateman R.L., Reifsteck C.A., Olson S.B., Grompe M. DNA replication is required to elicit cellular responses to psoralen-induced DNA interstrand cross-links. Mol. Cell. Biol. 2000, 20:8283-8289.
3. Ashwell S., Zabludoff S. DNA damage detection and repair pathways-recent advances with inhibitors of checkpoint kinases in cancer therapy. Clin. Cancer Res. 2008, 14:4032-4037.
4. Bassing C.H., Chua K.F., Sekiguchi J., Suh H., Whitlow S.R., Fleming J.C., Monroe B.C., Ciccone D.N., Yan C., Vlasakova K., Livingston D.M., Ferguson D.O., Scully R., Alt F.W. Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:8173-8178.
5. Bonner W.M., Redon C.E., Dickey J.S., Nakamura A.J., Sedelnikova O.A., Solier S., Pommier Y. GammaH2AX and cancer. Nat. Rev. Cancer 2008, 8:957-967.
6. Bosco E.E., Mayhew C.N., Hennigan R.F., Sage J., Jacks T., Knudsen E.S. RB signaling prevents replication-dependent DNA double-strand breaks following genotoxic insult. Nucleic Acids Res. 2004, 32:25-34. (Print 2004).
7. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
8. Chen Q., Xie W., Kuhn D.J., Voorhees P.M., Lopez-Girona A., Mendy D., Corral L.G., Krenitsky V.P., Xu W., Moutouh-de Parseval L., Webb D.R., Mercurio F., Nakayama K.I., Nakayama K., Orlowski R.Z. Targeting the p27 E3 ligase SCF(Skp2) results in p27- and Skp2-mediated cell-cycle arrest and activation of autophagy. Blood 2008, 111:4690-4699.
9. Daido S., Kanzawa T., Yamamoto A., Takeuchi H., Kondo Y., Kondo S. Pivotal role of the cell death factor BNIP3 in ceramide-induced autophagic cell death in malignant glioma cells. Cancer Res. 2004, 64:4286-4293.
10. Deans A.J., West S.C. DNA interstrand crosslink repair and cancer. Nat. Rev. Cancer 2011, 11:467-480.
11. Dotiwala F., Eapen V.V., Harrison J.C., Arbel-Eden A., Ranade V., Yoshida S., Haber J.E. DNA damage checkpoint triggers autophagy to regulate the initiation of anaphase. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E41-E49.
12. Dronkert M.L., Kanaar R. Repair of DNA interstrand cross-links. Mutat. Res. 2001, 486:217-247.
13. Furuta T., Takemura H., Liao Z.Y., Aune G.J., Redon C., Sedelnikova O.A., Pilch D.R., Rogakou E.P., Celeste A., Chen H.T., Nussenzweig A., Aladjem M.I., Bonner W.M., Pommier Y. Phosphorylation of histone H2AX and activation of Mre11, Rad50, and Nbs1 in response to replication-dependent DNA double-strand breaks induced by mammalian DNA topoisomerase I cleavage complexes. J. Biol. Chem. 2003, 278:20303-20312.
14. Garrett M.D., Collins I. Anticancer therapy with checkpoint inhibitors: what, where and when?. Trends Pharmacol. Sci. 2011, 32:308-316.
15. Harper J.W., Elledge S.J. The DNA damage response: ten years after. Mol. Cell 2007, 28:739-745.
16. Kabeya Y., Mizushima N., Ueno T., Yamamoto A., Kirisako T., Noda T., Kominami E., Ohsumi Y., Yoshimori T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 2000, 19:5720-5728.
17. Kakadiya R., Dong H., Lee P.C., Kapuriya N., Zhang X., Chou T.C., Lee T.C., Kapuriya K., Shah A., Su T.L. Potent antitumor bifunctional DNA alkylating agents, synthesis and biological activities of 3a-aza-cyclopenta[a]indenes. Bioorg. Med. Chem. 2009, 17:5614-5626.
18. Katayama M., Kawaguchi T., Berger M.S., Pieper R.O. DNA damaging agent-induced autophagy produces a cytoprotective adenosine triphosphate surge in malignant glioma cells. Cell Death Differ. 2007, 14:548-558.
19. Klionsky D.J., Cuervo A.M., Seglen P.O. Methods for monitoring autophagy from yeast to human. Autophagy 2007, 3:181-206.
20. Klionsky D.J., Abdalla F.C., Abeliovich H., Abraham R.T., Acevedo-Arozena A., et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012, 8:445-544.
21. Knizhnik A.V., Roos W.P., Nikolova T., Quiros S., Tomaszowski K.H., Christmann M., Kaina B. Survival and death strategies in glioma cells: autophagy, senescence and apoptosis triggered by a single type of temozolomide-induced DNA damage. PLoS One 2013, 8:e55665.
22. Kroemer G., Marino G., Levine B. Autophagy and the integrated stress response. Mol. Cell 2010, 40:280-293.
23. Kuzminov A. Single-strand interruptions in replicating chromosomes cause double-strand breaks. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:8241-8246.
24. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
25. Lambert S., Watson A., Sheedy D.M., Martin B., Carr A.M. Gross chromosomal rearrangements and elevated recombination at an inducible site-specific replication fork barrier. Cell 2005, 121:689-702.
26. Lee P.C., Kakadiya R., Su T.L., Lee T.C. Combination of bifunctional alkylating agent and arsenic trioxide synergistically suppresses the growth of drug-resistant tumor cells. Neoplasia 2010, 12:376-387.
27. Lee P.C., Lee H.J., Kakadiya R., Sanjiv K., Su T.L., Lee T.C. Multidrug-resistant cells overexpressing P-glycoprotein are susceptible to DNA crosslinking agents due to attenuated Src/nuclear EGFR cascade-activated DNA repair activity. Oncogene 2012, 23:133.
28. Leonce S., Kraus-Berthier L., Golsteyn R.M., David-Cordonnier M.H., Tardy C., Lansiaux A., Poindessous V., Larsen A.K., Pierre A. Generation of replication-dependent double-strand breaks by the novel N2-G-alkylator S23906-1. Cancer Res. 2006, 66:7203-7210.
29. Liang C., Feng P., Ku B., Dotan I., Canaani D., Oh B.H., Jung J.U. Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat. Cell Biol. 2006, 8:688-699.
30. McHugh P.J., Spanswick V.J., Hartley J.A. Repair of DNA interstrand crosslinks: molecular mechanisms and clinical relevance. Lancet Oncol. 2001, 2:483-490.
31. Meador J.A., Zhao M., Su Y., Narayan G., Geard C.R., Balajee A.S. Histone H2AX is a critical factor for cellular protection against DNA alkylating agents. Oncogene 2008, 27:5662-5671.
32. Mizushima N., Komatsu M. Autophagy: renovation of cells and tissues. Cell 2011, 147:728-741.
33. Mizushima N., Levine B., Cuervo A.M., Klionsky D.J. Autophagy fights disease through cellular self-digestion. Nature 2008, 451:1069-1075.
34. Mladenov E., Tsaneva I., Anachkova B. Activation of the S phase DNA damage checkpoint by mitomycin C. J. Cell. Physiol. 2007, 211:468-476.
35. Modesti M., Kanaar R. DNA repair: spot(light)s on chromatin. Curr. Biol. 2001, 11:R229-R232.
36. Niedernhofer L.J., Odijk H., Budzowska M., van Drunen E., Maas A., Theil A.F., de Wit J., Jaspers N.G., Beverloo H.B., Hoeijmakers J.H., Kanaar R. The structure-specific endonuclease Ercc1-Xpf is required to resolve DNA interstrand cross-link-induced double-strand breaks. Mol. Cell. Biol. 2004, 24:5776-5787.
37. Niedernhofer L.J., Lalai A.S., Hoeijmakers J.H. Fanconi anemia (cross)linked to DNA repair. Cell 2005, 123:1191-1198.
38. Nojima K., Hochegger H., Saberi A., Fukushima T., Kikuchi K., Yoshimura M., Orelli B.J., Bishop D.K., Hirano S., Ohzeki M., Ishiai M., Yamamoto K., Takata M., Arakawa H., Buerstedde J.M., Yamazoe M., Kawamoto T., Araki K., Takahashi J.A., Hashimoto N., Takeda S., Sonoda E. Multiple repair pathways mediate tolerance to chemotherapeutic cross-linking agents in vertebrate cells. Cancer Res. 2005, 65:11704-11711.
39. Paglin S., Hollister T., Delohery T., Hackett N., McMahill M., Sphicas E., Domingo D., Yahalom J. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res. 2001, 61:439-444.
40. Pichierri P., Rosselli F. The DNA crosslink-induced S-phase checkpoint depends on ATR-CHK1 and ATR-NBS1-FANCD2 pathways. EMBO J. 2004, 23:1178-1187.
41. Redon C., Pilch D., Rogakou E., Sedelnikova O., Newrock K., Bonner W. Histone H2A variants H2AX and H2AZ. Curr. Opin. Genet. Dev. 2002, 12:162-169.
42. Robert T., Vanoli F., Chiolo I., Shubassi G., Bernstein K.A., Rothstein R., Botrugno O.A., Parazzoli D., Oldani A., Minucci S., Foiani M. HDACs link the DNA damage response, processing of double-strand breaks and autophagy. Nature 2011, 471:74-79.
43. Rubinsztein D.C., Gestwicki J.E., Murphy L.O., Klionsky D.J. Potential therapeutic applications of autophagy. Nat. Rev. Drug Discov. 2007, 6:304-312.
44. Simone C. Signal-dependent control of autophagy and cell death in colorectal cancer cell: the role of the p38 pathway. Autophagy 2007, 3:468-471.
45. Soares D.G., Escargueil A.E., Poindessous V., Sarasin A., de Gramont A., Bonatto D., Henriques J.A., Larsen A.K. Replication and homologous recombination repair regulate DNA double-strand break formation by the antitumor alkylator ecteinascidin 743. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:13062-13067.
46. Vazquez M.V., Rojas V., Tercero J.A. Multiple pathways cooperate to facilitate DNA replication fork progression through alkylated DNA. DNA Repair (Amst) 2008, 7:1693-1704.
47. Wang Z., Lin H., Hua F., Hu Z.W. Repairing DNA damage by XRCC6/KU70 reverses TLR4-deficiency-worsened HCC development via restoring senescence and autophagic flux. Autophagy 2013, 9:6.
48. Wu W.K., Wu Y.C., Yu L., Li Z.J., Sung J.J., Cho C.H. Induction of autophagy by proteasome inhibitor is associated with proliferative arrest in colon cancer cells. Biochem. Biophys. Res. Commun. 2008, 374:258-263.
49. Wu Y.C., Yen W.Y., Yih L.H. Requirement of a functional spindle checkpoint for arsenite-induced apoptosis. J. Cell. Biochem. 2008, 105:678-687.
50. Wu Y.C., Yen W.Y., Ho H.Y., Su T.L., Yih L.H. Glyfoline induces mitotic catastrophe and apoptosis in cancer cells. Int. J. Cancer 2010, 126:1017-1028.
51. Yih L.H., Hsu N.C., Kuo H.H., Wu Y.C. Inhibition of the heat shock response by PI103 enhances the cytotoxicity of arsenic trioxide. Toxicol. Sci. 2012, 128:126-136.
52. Zeng X., Kinsella T.J. Mammalian target of rapamycin and S6 kinase 1 positively regulate 6-thioguanine-induced autophagy. Cancer Res. 2008, 68:2384-2390.
53. Zhang Y.W., Otterness D.M., Chiang G.G., Xie W., Liu Y.C., Mercurio F., Abraham R.T. Genotoxic stress targets human Chk1 for degradation by the ubiquitin-proteasome pathway. Mol. Cell 2005, 19:607-618.
54. Zhao Z., Oh S., Li D., Ni D., Pirooz S.D., Lee J.H., Yang S., Lee J.Y., Ghozalli I., Costanzo V., Stark J.M., Liang C. A dual role for UVRAG in maintaining chromosomal stability independent of autophagy. Dev. Cell 2012, 22:1001-1016.
55. Zhou B.B., Bartek J. Targeting the checkpoint kinases: chemosensitization versus chemoprotection. Nat. Rev. Cancer 2004, 4:216-225.