{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,10]],"date-time":"2026-10-10T15:01:52Z","timestamp":1791644512522,"version":"4.3.4"},"reference-count":48,"publisher":"Springer Science and Business Media LLC","issue":"5","license":[{"start":{"date-parts":[[2018,5,11]],"date-time":"2018-05-11T00:00:00Z","timestamp":1525996800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2018,5,11]],"date-time":"2018-05-11T00:00:00Z","timestamp":1525996800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Cell Death Dis"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Cancer stem cells (CSCs), representing the root of many solid tumors including ovarian cancer, have been implicated in disease recurrence, metastasis, and therapeutic resistance. Our previous study has demonstrated that the CSC subpopulation in ovarian cancer can be limited by DNA damage-binding protein 2 (DDB2). Here, we demonstrated that the ovarian CSC subpopulation can be maintained via cancer cell dedifferentiation, and DDB2 is able to suppress this non-CSC-to-CSC conversion by repression of<jats:italic>ALDH1A1<\/jats:italic>transcription. Mechanistically, DDB2 binds to the<jats:italic>ALDH1A1<\/jats:italic>gene promoter, facilitating the enrichment of histone H3K27me3, and competing with the transcription factor C\/EBP\u03b2 for binding to this region, eventually inhibiting the promoter activity of the<jats:italic>ALDH1A1<\/jats:italic>gene. The de-repression of ALDH1A1 expression contributes to DDB2 silencing-augmented non-CSC-to-CSC conversion and expansion of the CSC subpopulation. We further showed that treatment with a selective ALDH1A1 inhibitor blocked DDB2 silencing-induced expansion of CSCs, and halted orthotopic xenograft tumor growth. Together, our data demonstrate that DDB2, functioning as a transcription repressor, can abrogate ovarian CSC properties by downregulating ALDH1A1 expression.<\/jats:p>","DOI":"10.1038\/s41419-018-0585-y","type":"journal-article","created":{"date-parts":[[2018,5,11]],"date-time":"2018-05-11T12:35:24Z","timestamp":1526042124000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":38,"title":["DDB2 represses ovarian cancer cell dedifferentiation by suppressing ALDH1A1"],"prefix":"10.1038","volume":"9","author":[{"given":"Tiantian","family":"Cui","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amit Kumar","family":"Srivastava","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunhua","family":"Han","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dayong","family":"Wu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nissar","family":"Wani","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lu","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhiqin","family":"Gao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Meihua","family":"Qu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ning","family":"Zou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoli","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ping","family":"Yi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jianhua","family":"Yu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Erica H.","family":"Bell","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shyh-Ming","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David J.","family":"Maloney","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yanfang","family":"Zheng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Altaf A.","family":"Wani","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qi-En","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2018,5,11]]},"reference":[{"key":"585_CR1","doi-asserted-by":"publisher","first-page":"7","DOI":"10.3322\/caac.21332","volume":"66","author":"RL Siegel","year":"2016","unstructured":"Siegel, R. L., Miller, K. D. & Jemal, A. Cancer statistics, 2016. CA Cancer J. Clin. 66, 7\u201330 (2016).","journal-title":"CA Cancer J. Clin."},{"key":"585_CR2","doi-asserted-by":"publisher","first-page":"1371","DOI":"10.1016\/S0140-6736(09)61338-6","volume":"374","author":"BT Hennessy","year":"2009","unstructured":"Hennessy, B. T., Coleman, R. L. & Markman, M. Ovarian cancer. Lancet 374, 1371\u20131382 (2009).","journal-title":"Lancet"},{"key":"585_CR3","doi-asserted-by":"publisher","first-page":"188","DOI":"10.4161\/cc.7.2.5326","volume":"7","author":"PC Hermann","year":"2008","unstructured":"Hermann, P. C., Huber, S. L. & Heeschen, C. Metastatic cancer stem cells: a new target for anti-cancer therapy? Cell Cycle 7, 188\u2013193 (2008).","journal-title":"Cell Cycle"},{"key":"585_CR4","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1038\/nrc1590","volume":"5","author":"M Dean","year":"2005","unstructured":"Dean, M., Fojo, T. & Bates, S. Tumour stem cells and drug resistance. Nat. Rev. Cancer 5, 275\u2013284 (2005).","journal-title":"Nat. Rev. Cancer"},{"key":"585_CR5","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1038\/nrc3184","volume":"12","author":"LV Nguyen","year":"2012","unstructured":"Nguyen, L. V., Vanner, R., Dirks, P. & Eaves, C. J. Cancer stem cells: an evolving concept. Nat. Rev. Cancer 12, 133\u2013143 (2012).","journal-title":"Nat. Rev. Cancer"},{"key":"585_CR6","doi-asserted-by":"publisher","first-page":"4311","DOI":"10.1158\/0008-5472.CAN-08-0364","volume":"68","author":"S Zhang","year":"2008","unstructured":"Zhang, S. et al. Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res. 68, 4311\u20134320 (2008).","journal-title":"Cancer Res."},{"key":"585_CR7","doi-asserted-by":"publisher","first-page":"209","DOI":"10.1038\/onc.2008.374","volume":"28","author":"T Baba","year":"2009","unstructured":"Baba, T. et al. Epigenetic regulation of CD133 and tumorigenicity of CD133+ovarian cancer cells. Oncogene 28, 209\u2013218 (2009).","journal-title":"Oncogene"},{"key":"585_CR8","doi-asserted-by":"crossref","first-page":"2875","DOI":"10.1002\/stem.236","volume":"27","author":"MD Curley","year":"2009","unstructured":"Curley, M. D. et al. CD133 expression defines a tumor initiating cell population in primary human ovarian cancer. Stem Cells 27, 2875\u20132883 (2009).","journal-title":"Stem Cells"},{"key":"585_CR9","doi-asserted-by":"publisher","first-page":"3025","DOI":"10.1158\/0008-5472.CAN-04-3931","volume":"65","author":"SA Bapat","year":"2005","unstructured":"Bapat, S. A., Mali, A. M., Koppikar, C. B. & Kurrey, N. K. Stem and progenitor-like cells contribute to the aggressive behavior of human epithelial ovarian cancer. Cancer Res. 65, 3025\u20133029 (2005).","journal-title":"Cancer Res."},{"key":"585_CR10","doi-asserted-by":"publisher","first-page":"469","DOI":"10.1038\/sj.onc.1208211","volume":"24","author":"T Yoon","year":"2005","unstructured":"Yoon, T. et al. Tumor-prone phenotype of the DDB2-deficient mice. Oncogene 24, 469\u2013478 (2005).","journal-title":"Oncogene"},{"key":"585_CR11","doi-asserted-by":"publisher","first-page":"1578","DOI":"10.1093\/hmg\/ddm107","volume":"16","author":"T Itoh","year":"2007","unstructured":"Itoh, T., Iwashita, S., Cohen, M. B., Meyerholz, D. K. & Linn, S. Ddb2 is a haploinsufficient tumor suppressor and controls spontaneous germ cell apoptosis. Hum. Mol. Genet. 16, 1578\u20131586 (2007).","journal-title":"Hum. Mol. Genet."},{"key":"585_CR12","doi-asserted-by":"crossref","first-page":"977","DOI":"10.1002\/ijc.25112","volume":"127","author":"BM Barakat","year":"2009","unstructured":"Barakat, B. M. et al. Overexpression of DDB2 enhances the sensitivity of human ovarian cancer cells to cisplatin by augmenting cellular apoptosis. Int. J. Cancer 127, 977\u2013988 (2009).","journal-title":"Int. J. Cancer"},{"key":"585_CR13","doi-asserted-by":"publisher","first-page":"370","DOI":"10.1158\/1541-7786.MCR-13-0281","volume":"12","author":"R Zhao","year":"2014","unstructured":"Zhao, R. et al. DNA damage-binding complex recruits HDAC1 to repress Bcl-2 transcription in human ovarian cancer cells. Mol. Cancer Res. 12, 370\u2013380 (2014).","journal-title":"Mol. Cancer Res."},{"key":"585_CR14","doi-asserted-by":"publisher","first-page":"10690","DOI":"10.1073\/pnas.0812254106","volume":"106","author":"T Stoyanova","year":"2009","unstructured":"Stoyanova, T., Roy, N., Kopanja, D., Bagchi, S. & Raychaudhuri, P. DDB2 decides cell fate following DNA damage. Proc. Natl Acad. Sci. USA 106, 10690\u201310695 (2009).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"585_CR15","doi-asserted-by":"publisher","first-page":"3771","DOI":"10.1158\/0008-5472.CAN-12-4069","volume":"73","author":"N Roy","year":"2013","unstructured":"Roy, N. et al. DDB2 suppresses epithelial-to-mesenchymal transition in colon cancer. Cancer Res. 73, 3771\u20133782 (2013).","journal-title":"Cancer Res."},{"key":"585_CR16","doi-asserted-by":"publisher","first-page":"5040","DOI":"10.1158\/0008-5472.CAN-12-3655","volume":"73","author":"M Ennen","year":"2013","unstructured":"Ennen, M. et al. DDB2: a novel regulator of NF-kappaB and breast tumor invasion. Cancer Res. 73, 5040\u20135052 (2013).","journal-title":"Cancer Res."},{"key":"585_CR17","doi-asserted-by":"publisher","first-page":"2681","DOI":"10.1128\/MCB.01480-09","volume":"30","author":"N Roy","year":"2010","unstructured":"Roy, N. et al. DDB2, an essential mediator of premature senescence. Mol. Cell. Biol. 30, 2681\u20132692 (2010).","journal-title":"Mol. Cell. Biol."},{"key":"585_CR18","doi-asserted-by":"publisher","first-page":"784","DOI":"10.1158\/1541-7786.MCR-13-0638","volume":"12","author":"C Han","year":"2014","unstructured":"Han, C. et al. DDB2 suppresses tumorigenicity by limiting the cancer stem cell population in ovarian cancer. Mol. Cancer Res. 12, 784\u2013794 (2014).","journal-title":"Mol. Cancer Res."},{"key":"585_CR19","doi-asserted-by":"publisher","first-page":"1378","DOI":"10.4161\/cc.10.9.15486","volume":"10","author":"P Marcato","year":"2011","unstructured":"Marcato, P., Dean, C. A., Giacomantonio, C. A. & Lee, P. W. Aldehyde dehydrogenase: its role as a cancer stem cell marker comes down to the specific isoform. Cell Cycle 10, 1378\u20131384 (2011).","journal-title":"Cell Cycle"},{"key":"585_CR20","doi-asserted-by":"publisher","first-page":"3991","DOI":"10.1158\/0008-5472.CAN-10-3175","volume":"71","author":"IA Silva","year":"2011","unstructured":"Silva, I. A. et al. Aldehyde dehydrogenase in combination with CD133 defines angiogenic ovarian cancer stem cells that portend poor patient survival. Cancer Res. 71, 3991\u20134001 (2011).","journal-title":"Cancer Res."},{"key":"585_CR21","doi-asserted-by":"publisher","first-page":"e68187","DOI":"10.1371\/journal.pone.0068187","volume":"8","author":"K Yasuda","year":"2013","unstructured":"Yasuda, K. et al. Ovarian cancer stem cells are enriched in side population and aldehyde dehydrogenase bright overlapping population. PLoS ONE 8, e68187 (2013).","journal-title":"PLoS ONE"},{"key":"585_CR22","doi-asserted-by":"publisher","first-page":"1953","DOI":"10.1016\/j.drudis.2014.09.009","volume":"19","author":"K Pors","year":"2014","unstructured":"Pors, K. & Moreb, J. S. Aldehyde dehydrogenases in cancer: an opportunity for biomarker and drug development? Drug Discov. Today 19, 1953\u20131963 (2014).","journal-title":"Drug Discov. Today"},{"key":"585_CR23","doi-asserted-by":"publisher","first-page":"2297","DOI":"10.1038\/onc.2014.178","volume":"34","author":"S Condello","year":"2015","unstructured":"Condello, S. et al. beta-Catenin-regulated ALDH1A1 is a target in ovarian cancer spheroids. Oncogene 34, 2297\u20132308 (2015).","journal-title":"Oncogene"},{"key":"585_CR24","doi-asserted-by":"publisher","first-page":"11018","DOI":"10.18632\/oncotarget.6920","volume":"7","author":"H Tomita","year":"2016","unstructured":"Tomita, H., Tanaka, K., Tanaka, T. & Hara, A. Aldehyde dehydrogenase 1A1 in stem cells and cancer. Oncotarget 7, 11018\u201311032 (2016).","journal-title":"Oncotarget"},{"key":"585_CR25","doi-asserted-by":"publisher","first-page":"5453","DOI":"10.1172\/JCI76611","volume":"124","author":"D Zhao","year":"2014","unstructured":"Zhao, D. et al. NOTCH-induced aldehyde dehydrogenase 1A1 deacetylation promotes breast cancer stem cells. J. Clin. Invest. 124, 5453\u20135465 (2014).","journal-title":"J. Clin. Invest."},{"key":"585_CR26","doi-asserted-by":"publisher","first-page":"484","DOI":"10.1158\/1940-6207.CAPR-11-0414","volume":"5","author":"H Li","year":"2012","unstructured":"Li, H. et al. ALDH1A1 is a novel EZH2 target gene in epithelial ovarian cancer identified by genome-wide approaches. Cancer Prev. Res. 5, 484\u2013491 (2012).","journal-title":"Cancer Prev. Res."},{"key":"585_CR27","doi-asserted-by":"publisher","first-page":"6320","DOI":"10.1158\/0008-5472.CAN-16-0854","volume":"76","author":"Y Yokoyama","year":"2016","unstructured":"Yokoyama, Y. et al. BET inhibitors suppress ALDH activity by targeting ALDH1A1 super-enhancer in ovarian cancer. Cancer Res. 76, 6320\u20136330 (2016).","journal-title":"Cancer Res."},{"key":"585_CR28","doi-asserted-by":"publisher","first-page":"7838","DOI":"10.1093\/nar\/gkv667","volume":"43","author":"R Zhao","year":"2015","unstructured":"Zhao, R. et al. DDB2 modulates TGF-beta signal transduction in human ovarian cancer cells by downregulating NEDD4L. Nucleic Acids Res. 43, 7838\u20137849 (2015).","journal-title":"Nucleic Acids Res."},{"key":"585_CR29","doi-asserted-by":"publisher","first-page":"314","DOI":"10.1038\/nature09781","volume":"469","author":"JE Visvader","year":"2011","unstructured":"Visvader, J. E. Cells of origin in cancer. Nature 469, 314\u2013322 (2011).","journal-title":"Nature"},{"key":"585_CR30","doi-asserted-by":"publisher","first-page":"7950","DOI":"10.1073\/pnas.1102454108","volume":"108","author":"CL Chaffer","year":"2011","unstructured":"Chaffer, C. L. et al. Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state. Proc. Natl Acad. Sci. USA 108, 7950\u20137955 (2011).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"585_CR31","doi-asserted-by":"publisher","first-page":"244","DOI":"10.1002\/embr.201338254","volume":"15","author":"D Friedmann-Morvinski","year":"2014","unstructured":"Friedmann-Morvinski, D. & Verma, I. M. Dedifferentiation and reprogramming: origins of cancer stem cells. EMBO Rep. 15, 244\u2013253 (2014).","journal-title":"EMBO Rep."},{"key":"585_CR32","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms3126","volume":"4","author":"S Domcke","year":"2013","unstructured":"Domcke, S., Sinha, R., Levine, D. A., Sander, C. & Schultz, N. Evaluating cell lines as tumour models by comparison of genomic profiles. Nat. Commun. 4, 2126 (2013).","journal-title":"Nat. Commun."},{"key":"585_CR33","doi-asserted-by":"publisher","first-page":"1670","DOI":"10.1182\/blood-2008-05-156752","volume":"113","author":"BP Levi","year":"2009","unstructured":"Levi, B. P., Yilmaz, O. H., Duester, G. & Morrison, S. J. Aldehyde dehydrogenase 1a1 is dispensable for stem cell function in the mouse hematopoietic and nervous systems. Blood 113, 1670\u20131680 (2009).","journal-title":"Blood"},{"key":"585_CR34","doi-asserted-by":"publisher","first-page":"14165","DOI":"10.1074\/jbc.M808208200","volume":"284","author":"V Minig","year":"2009","unstructured":"Minig, V., Kattan, Z., van, B. J., Brunner, E. & Becuwe, P. Identification of DDB2 protein as a transcriptional regulator of constitutive SOD2 gene expression in human breast cancer cells. J. Biol. Chem. 284, 14165\u201314176 (2009).","journal-title":"J. Biol. Chem."},{"key":"585_CR35","doi-asserted-by":"publisher","first-page":"17521","DOI":"10.1074\/jbc.270.29.17521","volume":"270","author":"Y Yanagawa","year":"1995","unstructured":"Yanagawa, Y., Chen, J. C., Hsu, L. C. & Yoshida, A. The transcriptional regulation of human aldehyde dehydrogenase I gene. The structural and functional analysis of the promoter. J. Biol. Chem. 270, 17521\u201317527 (1995).","journal-title":"J. Biol. Chem."},{"key":"585_CR36","doi-asserted-by":"publisher","first-page":"30892","DOI":"10.1074\/jbc.M113.477158","volume":"288","author":"M Alam","year":"2013","unstructured":"Alam, M., Ahmad, R., Rajabi, H., Kharbanda, A. & Kufe, D. MUC1-C oncoprotein activates ERK--C\/EBPbeta signaling and induction of aldehyde dehydrogenase 1A1 in breast cancer cells. J. Biol. Chem. 288, 30892\u201330903 (2013).","journal-title":"J. Biol. Chem."},{"key":"585_CR37","doi-asserted-by":"publisher","first-page":"1039","DOI":"10.1126\/science.1076997","volume":"298","author":"R Cao","year":"2002","unstructured":"Cao, R. et al. Role of histone H3 lysine 27 methylation in polycomb-group silencing. Science 298, 1039\u20131043 (2002).","journal-title":"Science"},{"key":"585_CR38","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1016\/j.gde.2004.02.001","volume":"14","author":"R Cao","year":"2004","unstructured":"Cao, R. & Zhang, Y. The functions of E(Z)\/EZH2-mediated methylation of lysine 27 in histone H3. Curr. Opin. Genet. Dev. 14, 155\u2013164 (2004).","journal-title":"Curr. Opin. Genet. Dev."},{"key":"585_CR39","doi-asserted-by":"publisher","first-page":"5967","DOI":"10.1021\/acs.jmedchem.5b00577","volume":"58","author":"SM Yang","year":"2015","unstructured":"Yang, S. M. et al. Discovery of NCT-501, a potent and selective theophylline-based inhibitor of aldehyde dehydrogenase 1A1 (ALDH1A1). J. Med. Chem. 58, 5967\u20135978 (2015).","journal-title":"J. Med. Chem."},{"key":"585_CR40","doi-asserted-by":"publisher","first-page":"192","DOI":"10.1091\/mbc.e16-08-0573","volume":"28","author":"D Fantini","year":"2017","unstructured":"Fantini, D., Huang, S., Asara, J. M., Bagchi, S. & Raychaudhuri, P. Chromatin association of XRCC5\/6 in the absence of DNA damage depends on the XPE gene product DDB2. Mol. Biol. Cell 28, 192\u2013200 (2017).","journal-title":"Mol. Biol. Cell"},{"key":"585_CR41","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1186\/1479-7364-5-4-283","volume":"5","author":"B Jackson","year":"2011","unstructured":"Jackson, B. et al. Update on the aldehyde dehydrogenase gene (ALDH) superfamily. Hum. Genom. 5, 283\u2013303 (2011).","journal-title":"Hum. Genom."},{"key":"585_CR42","doi-asserted-by":"publisher","first-page":"3579","DOI":"10.1158\/0008-5472.CAN-13-3456","volume":"74","author":"D Raha","year":"2014","unstructured":"Raha, D. et al. The cancer stem cell marker aldehyde dehydrogenase is required to maintain a drug-tolerant tumor cell subpopulation. Cancer Res. 74, 3579\u20133590 (2014).","journal-title":"Cancer Res."},{"key":"585_CR43","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1186\/1479-7364-2-2-138","volume":"2","author":"V Vasiliou","year":"2005","unstructured":"Vasiliou, V. & Nebert, D. W. Analysis and update of the human aldehyde dehydrogenase (ALDH) gene family. Hum. Genom. 2, 138\u2013143 (2005).","journal-title":"Hum. Genom."},{"key":"585_CR44","doi-asserted-by":"publisher","first-page":"11707","DOI":"10.1073\/pnas.0603806103","volume":"103","author":"JP Chute","year":"2006","unstructured":"Chute, J. P. et al. Inhibition of aldehyde dehydrogenase and retinoid signaling induces the expansion of human hematopoietic stem cells. Proc. Natl Acad. Sci. USA 103, 11707\u201311712 (2006).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"585_CR45","doi-asserted-by":"publisher","first-page":"979","DOI":"10.1016\/0002-9378(72)90109-3","volume":"114","author":"PJ DiSaia","year":"1972","unstructured":"DiSaia, P. J., Sinkovics, J. G., Rutledge, F. N. & Smith, J. P. Cell-mediated immunity to human malignant cells. A brief review and further studies with two gynecologic tumors. Am. J. Obstet. Gynecol. 114, 979\u2013989 (1972).","journal-title":"Am. J. Obstet. Gynecol."},{"key":"585_CR46","first-page":"6250","volume":"45","author":"PA Andrews","year":"1985","unstructured":"Andrews, P. A., Murphy, M. P. & Howell, S. B. Differential potentiation of alkylating and platinating agent cytotoxicity in human ovarian carcinoma cells by glutathione depletion. Cancer Res. 45, 6250\u20136253 (1985).","journal-title":"Cancer Res."},{"key":"585_CR47","doi-asserted-by":"publisher","first-page":"8590","DOI":"10.1158\/0008-5472.CAN-06-1115","volume":"66","author":"J Li","year":"2006","unstructured":"Li, J. et al. DNA damage binding protein component DDB1 participates in nucleotide excision repair through DDB2 DNA-binding and cullin 4A ubiquitin ligase activity. Cancer Res. 66, 8590\u20138597 (2006).","journal-title":"Cancer Res."},{"key":"585_CR48","doi-asserted-by":"crossref","unstructured":"Hu, Y. & Smyth, G. K. ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J. Immunol. Methods 347, 70\u201378 (2009).","DOI":"10.1016\/j.jim.2009.06.008"}],"container-title":["Cell Death &amp; Disease"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41419-018-0585-y","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41419-018-0585-y.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41419-018-0585-y.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,7,6]],"date-time":"2024-07-06T18:12:44Z","timestamp":1720289564000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41419-018-0585-y"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,5,11]]},"references-count":48,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2018,5]]}},"alternative-id":["585"],"URL":"https:\/\/doi.org\/10.1038\/s41419-018-0585-y","relation":{},"ISSN":["2041-4889"],"issn-type":[{"value":"2041-4889","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,5,11]]},"assertion":[{"value":"15 January 2018","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"5 April 2018","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"10 April 2018","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"11 May 2018","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare that they have no conflict of interest.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}}],"article-number":"561"}}