{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T13:24:39Z","timestamp":1790169879873,"version":"4.1.0"},"reference-count":35,"publisher":"Springer Science and Business Media LLC","issue":"9","license":[{"start":{"date-parts":[[2010,7,6]],"date-time":"2010-07-06T00:00:00Z","timestamp":1278374400000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cell Res"],"published-print":{"date-parts":[[2010,9]]},"DOI":"10.1038\/cr.2010.95","type":"journal-article","created":{"date-parts":[[2010,7,6]],"date-time":"2010-07-06T10:42:01Z","timestamp":1278412921000},"page":"1060-1075","source":"Crossref","is-referenced-by-count":24,"title":["Cellular processing determinants for the activation of damage signals in response to topoisomerase I-linked DNA breakage"],"prefix":"10.1038","volume":"20","author":[{"given":"Ting-Hsiang","family":"Huang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hsiang-Chin","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shang-Min","family":"Chou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu-Chen","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jia-Rong","family":"Fan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tsai-Kun","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2010,7,6]]},"reference":[{"key":"BFcr201095_CR1","doi-asserted-by":"publisher","first-page":"216","DOI":"10.1038\/nrc1296","volume":"4","author":"BB Zhou","year":"2004","unstructured":"Zhou BB, Bartek J . Targeting the checkpoint kinases: chemosensitization versus chemoprotection. Nat Rev Cancer 2004; 4:216\u2013225.","journal-title":"Nat Rev Cancer"},{"key":"BFcr201095_CR2","doi-asserted-by":"publisher","first-page":"605","DOI":"10.1038\/nature03442","volume":"434","author":"J Falck","year":"2005","unstructured":"Falck J, Coates J, Jackson SP . Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 2005; 434:605\u2013611.","journal-title":"Nature"},{"key":"BFcr201095_CR3","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1146\/annurev.biochem.73.011303.073723","volume":"73","author":"A Sancar","year":"2004","unstructured":"Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S . Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 2004; 73:39\u201385.","journal-title":"Annu Rev Biochem"},{"key":"BFcr201095_CR4","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1146\/annurev.pharmtox.41.1.53","volume":"41","author":"TK Li","year":"2001","unstructured":"Li TK, Liu LF . Tumor cell death induced by topoisomerase-targeting drugs. Annu Rev Pharmacol Toxicol 2001; 41:53\u201377.","journal-title":"Annu Rev Pharmacol Toxicol"},{"key":"BFcr201095_CR5","doi-asserted-by":"publisher","first-page":"789","DOI":"10.1038\/nrc1977","volume":"6","author":"Y Pommier","year":"2006","unstructured":"Pommier Y . Topoisomerase I inhibitors: camptothecins and beyond. Nat Rev Cancer 2006; 6:789\u2013802.","journal-title":"Nat Rev Cancer"},{"key":"BFcr201095_CR6","doi-asserted-by":"publisher","first-page":"338","DOI":"10.1038\/nrc2607","volume":"9","author":"JL Nitiss","year":"2009","unstructured":"Nitiss JL . Targeting DNA topoisomerase II in cancer chemotherapy. Nat Rev Cancer 2009; 9:338\u2013350.","journal-title":"Nat Rev Cancer"},{"key":"BFcr201095_CR7","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1016\/S1097-2765(04)00056-5","volume":"13","author":"JC Connelly","year":"2004","unstructured":"Connelly JC, Leach DR . Repair of DNA covalently linked to protein. Mol Cell 2004; 13:307\u2013316.","journal-title":"Mol Cell"},{"key":"BFcr201095_CR8","doi-asserted-by":"publisher","first-page":"15387","DOI":"10.1073\/pnas.242259599","volume":"99","author":"BL Staker","year":"2002","unstructured":"Staker BL, Hjerrild K, Feese MD, et al. The mechanism of topoisomerase I poisoning by a camptothecin analog. Proc Natl Acad Sci USA 2002; 99:15387\u201315392.","journal-title":"Proc Natl Acad Sci USA"},{"key":"BFcr201095_CR9","doi-asserted-by":"publisher","first-page":"1534","DOI":"10.1126\/science.279.5356.1534","volume":"279","author":"L Stewart","year":"1998","unstructured":"Stewart L, Redinbo MR, Qiu X, Hol WG, Champoux JJ . A model for the mechanism of human topoisomerase I. Science 1998; 279:1534\u20131541.","journal-title":"Science"},{"key":"BFcr201095_CR10","doi-asserted-by":"publisher","first-page":"1504","DOI":"10.1126\/science.279.5356.1504","volume":"279","author":"MR Redinbo","year":"1998","unstructured":"Redinbo MR, Stewart L, Kuhn P, Champoux JJ, Hol WG . Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 1998; 279:1504\u20131513.","journal-title":"Science"},{"key":"BFcr201095_CR11","doi-asserted-by":"publisher","first-page":"887","DOI":"10.1038\/embor.2009.97","volume":"10","author":"O Sordet","year":"2009","unstructured":"Sordet O, Redon CE, Guirouilh-Barbat J, et al. Ataxia telangiectasia mutated activation by transcription- and topoisomerase I-induced DNA double-strand breaks. EMBO Rep 2009; 10:887\u2013893.","journal-title":"EMBO Rep"},{"key":"BFcr201095_CR12","doi-asserted-by":"publisher","first-page":"28084","DOI":"10.1074\/jbc.M109.030601","volume":"284","author":"CP Lin","year":"2009","unstructured":"Lin CP, Ban Y, Lyu YL, Liu LF . Proteasome-dependent processing of topoisomerase I-DNA adducts into DNA double strand breaks at arrested replication forks. J Biol Chem 2009; 284:28084\u201328092.","journal-title":"J Biol Chem"},{"key":"BFcr201095_CR13","doi-asserted-by":"publisher","first-page":"21074","DOI":"10.1074\/jbc.M803493200","volume":"283","author":"CP Lin","year":"2008","unstructured":"Lin CP, Ban Y, Lyu YL, Desai SD, Liu LF . A ubiquitin-proteasome pathway for the repair of topoisomerase I-DNA covalent complexes. J Biol Chem 2008; 283:21074\u201321083.","journal-title":"J Biol Chem"},{"key":"BFcr201095_CR14","doi-asserted-by":"publisher","first-page":"452","DOI":"10.1016\/j.dnarep.2007.12.002","volume":"7","author":"JR Fan","year":"2008","unstructured":"Fan JR, Peng AL, Chen HC, et al. Cellular processing pathways contribute to the activation of etoposide-induced DNA damage responses. DNA Repair (Amst) 2008; 7:452\u2013463.","journal-title":"DNA Repair (Amst)"},{"key":"BFcr201095_CR15","doi-asserted-by":"publisher","first-page":"35997","DOI":"10.1074\/jbc.M604149200","volume":"281","author":"A Zhang","year":"2006","unstructured":"Zhang A, Lyu YL, Lin CP, et al. A protease pathway for the repair of topoisomerase II-DNA covalent complexes. J Biol Chem 2006; 281:35997\u201336003.","journal-title":"J Biol Chem"},{"key":"BFcr201095_CR16","doi-asserted-by":"publisher","first-page":"30814","DOI":"10.1074\/jbc.M603747200","volume":"281","author":"H Takemura","year":"2006","unstructured":"Takemura H, Rao VA, Sordet O, et al. Defective Mre11-dependent activation of Chk2 by ataxia telangiectasia mutated in colorectal carcinoma cells in response to replication-dependent DNA double strand breaks. J Biol Chem 2006; 281:30814\u201330823.","journal-title":"J Biol Chem"},{"key":"BFcr201095_CR17","doi-asserted-by":"publisher","first-page":"4181","DOI":"10.1093\/nar\/25.21.4181","volume":"25","author":"JX Wu","year":"1997","unstructured":"Wu JX, Liu LF . Processing of topoisomerase I cleavable complexes into DNA damage by transcription. Nucleic Acids Res 1997; 25:4181\u20134186.","journal-title":"Nucleic Acids Res"},{"key":"BFcr201095_CR18","first-page":"5908","volume":"53","author":"YP Tsao","year":"1993","unstructured":"Tsao YP, Russo A, Nyamuswa G, Silber R, Liu LF . Interaction between replication forks and topoisomerase-I-DNA cleavable complexes - studies in a cell-free Sv40 DNA-replication system. Cancer Res 1993; 53:5908\u20135914.","journal-title":"Cancer Res"},{"key":"BFcr201095_CR19","first-page":"5077","volume":"49","author":"YH Hsiang","year":"1989","unstructured":"Hsiang YH, Lihou MG, Liu LF . Arrest of replication forks by drug-stabilized topoisomerase i-dna cleavable complexes as a mechanism of cell killing by camptothecin. Cancer Res 1989; 49:5077\u20135082.","journal-title":"Cancer Res"},{"key":"BFcr201095_CR20","doi-asserted-by":"publisher","first-page":"757","DOI":"10.1083\/jcb.134.3.757","volume":"134","author":"EJ Morris","year":"1996","unstructured":"Morris EJ, Geller HM . Induction of neuronal apoptosis by camptothecin, an inhibitor of DNA topoisomerase-I: evidence for cell cycle-independent toxicity. J Cell Biol 1996; 134:757\u2013770.","journal-title":"J Cell Biol"},{"key":"BFcr201095_CR21","doi-asserted-by":"publisher","first-page":"1397","DOI":"10.1093\/emboj\/18.5.1397","volume":"18","author":"RG Shao","year":"1999","unstructured":"Shao RG, Cao CX, Zhang HL, et al. Replication-mediated DNA damage by camptothecin induces phosphorylation of RPA by DNA-dependent protein kinase and dissociates RPA: DNA-PK complexes. EMBO J 1999; 18:1397\u20131406.","journal-title":"EMBO J"},{"key":"BFcr201095_CR22","doi-asserted-by":"publisher","first-page":"2341","DOI":"10.1128\/MCB.23.7.2341-2350.2003","volume":"23","author":"SD Desai","year":"2003","unstructured":"Desai SD, Zhang H, Rodriguez-Bauman A, et al. Transcription-dependent degradation of topoisomerase I-DNA covalent complexes. Mol Cel Biol 2003; 23:2341\u20132350.","journal-title":"Mol Cel Biol"},{"key":"BFcr201095_CR23","first-page":"5926","volume":"61","author":"SD Desai","year":"2001","unstructured":"Desai SD, Li TK, Rodriguez-Bauman A, Rubin EH, Liu LF . Ubiquitin\/26S proteasome-mediated degradation of topoisomerase I as a resistance mechanism to camptothecin in tumor cells. Cancer Res 2001; 61:5926\u20135932.","journal-title":"Cancer Res"},{"key":"BFcr201095_CR24","doi-asserted-by":"publisher","first-page":"14587","DOI":"10.1074\/jbc.M311370200","volume":"279","author":"P Daroui","year":"2004","unstructured":"Daroui P, Desai SD, Li TK, Liu AA, Liu LF . Hydrogen peroxide induces topoisomerase I-mediated DNA damage and cell death. J Biol Chem 2004; 279:14587\u201314594.","journal-title":"J Biol Chem"},{"key":"BFcr201095_CR25","first-page":"2097","volume":"55","author":"D Subramanian","year":"1995","unstructured":"Subramanian D, Kraut E, Staubus A, Young DC, Muller MT . Analysis of topoisomerase I\/DNA complexes in patients administered topotecan. Cancer Res 1995; 55:2097\u20132103.","journal-title":"Cancer Res"},{"key":"BFcr201095_CR26","first-page":"2317","volume":"54","author":"CA Afshari","year":"1994","unstructured":"Afshari CA, Barrett JC . Disruption of G0-G1 arrest in quiescent and senescent cells treated with phosphatase inhibitors. Cancer Res 1994; 54:2317\u20132321.","journal-title":"Cancer Res"},{"key":"BFcr201095_CR27","first-page":"8400","volume":"63","author":"TK Li","year":"2003","unstructured":"Li TK, Houghton PJ, Desai SD, et al. Characterization of ARC-111 as a novel topoisomerase I-targeting anticancer drug. Cancer Res 2003; 63:8400\u20138407.","journal-title":"Cancer Res"},{"key":"BFcr201095_CR28","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1158\/1535-7163.621.3.5","volume":"3","author":"WY Siu","year":"2004","unstructured":"Siu WY, Lau A, Arooz T, et al. Topoisomerase poisons differentially activate DNA damage checkpoints through ataxia-telangiectasia mutated-dependent and -independent mechanisms. Mol Cancer Ther 2004; 3:621\u2013632.","journal-title":"Mol Cancer Ther"},{"key":"BFcr201095_CR29","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1038\/nature01368","volume":"421","author":"CJ Bakkenist","year":"2003","unstructured":"Bakkenist CJ, Kastan MB . DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003; 421:499\u2013506.","journal-title":"Nature"},{"key":"BFcr201095_CR30","first-page":"6919","volume":"50","author":"P D'Arpa","year":"1990","unstructured":"D'Arpa P, Beardmore C, Liu LF . Involvement of nucleic acid synthesis in cell killing mechanisms of topoisomerase poisons. Cancer Res 1990; 50:6919\u20136924.","journal-title":"Cancer Res"},{"key":"BFcr201095_CR31","doi-asserted-by":"publisher","first-page":"20303","DOI":"10.1074\/jbc.M300198200","volume":"278","author":"T Furuta","year":"2003","unstructured":"Furuta T, Takemura H, Liao ZY, et al. 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\u201320312.","journal-title":"J Biol Chem"},{"key":"BFcr201095_CR32","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1111\/j.1749-6632.2000.tb07020.x","volume":"922","author":"LF Liu","year":"2000","unstructured":"Liu LF, Desai SD, Li TK, Mao Y, Sun M, Sim SP . Mechanism of action of camptothecin. Ann N Y Acad Sci 2000; 922:1\u201310.","journal-title":"Ann N Y Acad Sci"},{"key":"BFcr201095_CR33","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1016\/S1535-6108(04)00120-5","volume":"5","author":"J Adams","year":"2004","unstructured":"Adams J . The development of proteasome inhibitors as anticancer drugs. Cancer Cell 2004; 5:417\u2013421.","journal-title":"Cancer Cell"},{"key":"BFcr201095_CR34","doi-asserted-by":"publisher","first-page":"1841","DOI":"10.1093\/annonc\/mdf337","volume":"13","author":"Y Xu","year":"2002","unstructured":"Xu Y, Villalona-Calero MA . Irinotecan: mechanisms of tumor resistance and novel strategies for modulating its activity. Ann Oncol 2002; 13:1841\u20131851.","journal-title":"Ann Oncol"},{"key":"BFcr201095_CR35","doi-asserted-by":"publisher","first-page":"1677","DOI":"10.1126\/science.281.5383.1677","volume":"281","author":"CE Canman","year":"1998","unstructured":"Canman CE, Lim DS, Cimprich KA, et al. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 1998; 281:1677\u20131679.","journal-title":"Science"}],"container-title":["Cell Research"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.nature.com\/articles\/cr201095.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/cr201095","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/cr201095.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,3,28]],"date-time":"2024-03-28T01:46:30Z","timestamp":1711590390000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/cr201095"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2010,7,6]]},"references-count":35,"journal-issue":{"issue":"9","published-print":{"date-parts":[[2010,9]]}},"alternative-id":["BFcr201095"],"URL":"https:\/\/doi.org\/10.1038\/cr.2010.95","relation":{},"ISSN":["1001-0602","1748-7838"],"issn-type":[{"value":"1001-0602","type":"print"},{"value":"1748-7838","type":"electronic"}],"subject":[],"published":{"date-parts":[[2010,7,6]]}}}