Cited by 526Chromatin Remodeling and CancerPARP inhibition in cancer therapyDNA Repair Mechanisms

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ARID1A Deficiency Impairs the DNA Damage Checkpoint and Sensitizes Cells to PARP Inhibitors

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Shen, Jianfeng, Peng, Yang, Wei, Leizhen, Zhang, Wei, Yang, Lin, Lan, Li, Kapoor, Prabodh, Ju, Zhenlin, Mo, Qianxing, Shih, Ie-Ming, Uray, Ivan P., Wu, Xiangwei, Brown, Powel H., Shen, Xuetong, Mills, Gordon B., Peng, Guang·2015·Cancer Discovery

DOI 10.1158/2159-8290.cd-14-0849PMC PMC4497871

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Abstract

ARID1A, SWI/SNF chromatin remodeling complex subunit, is a recently identified tumor suppressor that is mutated in a broad spectrum of human cancers. Thus, it is of fundamental clinical importance to understand its molecular functions and determine whether ARID1A deficiency can be exploited therapeutically. In this article, we report a key function of ARID1A in regulating the DNA damage checkpoint. ARID1A is recruited to DNA double-strand breaks (DSB) via its interaction with the upstream DNA damage checkpoint kinase ATR. At the molecular level, ARID1A facilitates efficient processing of DSB to single-strand ends and sustains DNA damage signaling. Importantly, ARID1A deficiency sensitizes cancer cells to PARP inhibitors in vitro and in vivo, providing a potential therapeutic strategy for patients with ARID1A-mutant tumors. Significance: ARID1A has been identified as one of the most frequently mutated genes across human cancers. Our data suggest that clinical utility of PARP inhibitors might be extended beyond patients with BRCA mutations to a larger group of patients with ARID1A-mutant tumors, which may exhibit therapeutic vulnerability to PARP inhibitors. Cancer Discov; 5(7); 752–67. ©2015 AACR. This article is highlighted in the In This Issue feature, p. 681

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Additional file 2 of ARID1A deficiency promotes progression and potentiates therapeutic antitumour immunity in hepatitis B virus-related hepatocellular carcinoma
Xing, T., Li, L., Rao, X., Zhao, J., Chen, Y., Ju, G., Xu, Y., Gao, X., Dong, G., Xia, X., et al. (2024) · Figshare · doi:10.6084/m9.figshare.24934568
Additional file 3 of ARID1A loss promotes RNA editing of CDK13 in an ADAR1-dependent manner
Zhu, T., Li, Q., Zhang, Z., Shi, J., Li, Y., Zhang, F., Li, L., Song, X., Shen, J., & Jia, R. (2024) · Figshare · doi:10.6084/m9.figshare.26729755
Self-citation
Additional file 3 of Genetic alterations and their therapeutic implications in epithelial ovarian cancer
Lapke, N., Chen, C.-H., Chang, T.-C., Chao, A., Lu, Y.-J., Lai, C.-H., Tan, K. T., Chen, H.-C., Lu, H.-Y., & Chen, S.-J. (2021) · Figshare · doi:10.6084/m9.figshare.14538774
Additional file 2 of Genome-wide DNA methylation in relation to ARID1A deficiency in ovarian clear cell carcinoma
Li, S., Meersma, G. J., Kupryjańczyk, J., de Jong, S., & Wisman, G. B. A. (2024) · Figshare · doi:10.6084/m9.figshare.26731948
Additional file 1 of Treatment for ovarian clear cell carcinoma with combined inhibition of WEE1 and ATR
Chien, W., Tyner, J. W., Gery, S., Zheng, Y., Li, L.-Y., Gopinatha Pillai, M. S., Nam, C., Bhowmick, N. A., Lin, D.-C., & Koeffler, H. P. (2023) · Figshare · doi:10.6084/m9.figshare.22679565
Additional file 1 of Mutation landscape of germline and somatic BRCA1/2 in patients with high-grade serous ovarian cancer
Eoh, K. J., Kim, H. M., Lee, J.-Y., Kim, S., Kim, S. W., Kim, Y. T., & Nam, E. J. (2020) · Figshare · doi:10.6084/m9.figshare.11978706
Additional file 3 of Genome-wide DNA methylation in relation to ARID1A deficiency in ovarian clear cell carcinoma
Li, S., Meersma, G. J., Kupryjańczyk, J., de Jong, S., & Wisman, G. B. A. (2024) · Figshare · doi:10.6084/m9.figshare.26731951
Additional file 1 of A novel targeted NGS panel identifies numerous homologous recombination deficiency (HRD)-associated gene mutations in addition to known BRCA mutations
Vogel, A., Haupts, A., Kloth, M. T., Roth, W., & Hartmann, N. (2024) · Figshare · doi:10.6084/m9.figshare.24954492
Additional file 4 of Genetic alterations and their therapeutic implications in epithelial ovarian cancer
Lapke, N., Chen, C.-H., Chang, T.-C., Chao, A., Lu, Y.-J., Lai, C.-H., Tan, K. T., Chen, H.-C., Lu, H.-Y., & Chen, S.-J. (2021) · Figshare · doi:10.6084/m9.figshare.14538777
Additional file 4 of Genome-wide DNA methylation in relation to ARID1A deficiency in ovarian clear cell carcinoma
Li, S., Meersma, G. J., Kupryjańczyk, J., de Jong, S., & Wisman, G. B. A. (2024) · Figshare · doi:10.6084/m9.figshare.26731954
Additional file 3 of ARID1A deficiency promotes progression and potentiates therapeutic antitumour immunity in hepatitis B virus-related hepatocellular carcinoma
Xing, T., Li, L., Rao, X., Zhao, J., Chen, Y., Ju, G., Xu, Y., Gao, X., Dong, G., Xia, X., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26658412
Additional file 8 of Genetic alterations and their therapeutic implications in epithelial ovarian cancer
Lapke, N., Chen, C.-H., Chang, T.-C., Chao, A., Lu, Y.-J., Lai, C.-H., Tan, K. T., Chen, H.-C., Lu, H.-Y., & Chen, S.-J. (2021) · Figshare · doi:10.6084/m9.figshare.14538789
Additional file 1 of Genetic alterations and their therapeutic implications in epithelial ovarian cancer
Lapke, N., Chen, C.-H., Chang, T.-C., Chao, A., Lu, Y.-J., Lai, C.-H., Tan, K. T., Chen, H.-C., Lu, H.-Y., & Chen, S.-J. (2021) · Figshare · doi:10.6084/m9.figshare.14538765
Additional file 4 of ARID1A loss promotes RNA editing of CDK13 in an ADAR1-dependent manner
Zhu, T., Li, Q., Zhang, Z., Shi, J., Li, Y., Zhang, F., Li, L., Song, X., Shen, J., & Jia, R. (2024) · Figshare · doi:10.6084/m9.figshare.26729758
Self-citation
Additional file 6 of ARID1A loss promotes RNA editing of CDK13 in an ADAR1-dependent manner
Zhu, T., Li, Q., Zhang, Z., Shi, J., Li, Y., Zhang, F., Li, L., Song, X., Shen, J., & Jia, R. (2024) · Figshare · doi:10.6084/m9.figshare.26729764
Self-citation
Additional file 1 of Genome-wide DNA methylation in relation to ARID1A deficiency in ovarian clear cell carcinoma
Li, S., Meersma, G. J., Kupryjańczyk, J., de Jong, S., & Wisman, G. B. A. (2024) · Figshare · doi:10.6084/m9.figshare.26731945
Additional file 1 of A comprehensive molecular analysis of 113 primary ovarian clear cell carcinomas reveals common therapeutically significant aberrations
Stružinská, I., Hájková, N., Hojný, J., Krkavcová, E., Michálková, R., Dvořák, J., Němejcová, K., Matěj, R., Laco, J., Drozenová, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26596391
Additional file 5 of ARID1A loss promotes RNA editing of CDK13 in an ADAR1-dependent manner
Zhu, T., Li, Q., Zhang, Z., Shi, J., Li, Y., Zhang, F., Li, L., Song, X., Shen, J., & Jia, R. (2024) · Figshare · doi:10.6084/m9.figshare.26729761
Self-citation
Additional file 7 of Genetic alterations and their therapeutic implications in epithelial ovarian cancer
Lapke, N., Chen, C.-H., Chang, T.-C., Chao, A., Lu, Y.-J., Lai, C.-H., Tan, K. T., Chen, H.-C., Lu, H.-Y., & Chen, S.-J. (2021) · Figshare · doi:10.6084/m9.figshare.14538786
Additional file 3 of A comprehensive molecular analysis of 113 primary ovarian clear cell carcinomas reveals common therapeutically significant aberrations
Stružinská, I., Hájková, N., Hojný, J., Krkavcová, E., Michálková, R., Dvořák, J., Němejcová, K., Matěj, R., Laco, J., Drozenová, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26596397
Additional file 2 of A comprehensive molecular analysis of 113 primary ovarian clear cell carcinomas reveals common therapeutically significant aberrations
Stružinská, I., Hájková, N., Hojný, J., Krkavcová, E., Michálková, R., Dvořák, J., Němejcová, K., Matěj, R., Laco, J., Drozenová, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26596394
Additional file 1 of ARID1A loss promotes RNA editing of CDK13 in an ADAR1-dependent manner
Zhu, T., Li, Q., Zhang, Z., Shi, J., Li, Y., Zhang, F., Li, L., Song, X., Shen, J., & Jia, R. (2024) · Figshare · doi:10.6084/m9.figshare.25971709
Self-citation
Additional file 2 of ARID1A loss promotes RNA editing of CDK13 in an ADAR1-dependent manner
Zhu, T., Li, Q., Zhang, Z., Shi, J., Li, Y., Zhang, F., Li, L., Song, X., Shen, J., & Jia, R. (2024) · Figshare · doi:10.6084/m9.figshare.25971796
Self-citation
Additional file 4 of A comprehensive molecular analysis of 113 primary ovarian clear cell carcinomas reveals common therapeutically significant aberrations
Stružinská, I., Hájková, N., Hojný, J., Krkavcová, E., Michálková, R., Dvořák, J., Němejcová, K., Matěj, R., Laco, J., Drozenová, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26596400
Additional file 10 of Genetic alterations and their therapeutic implications in epithelial ovarian cancer
Lapke, N., Chen, C.-H., Chang, T.-C., Chao, A., Lu, Y.-J., Lai, C.-H., Tan, K. T., Chen, H.-C., Lu, H.-Y., & Chen, S.-J. (2021) · Figshare · doi:10.6084/m9.figshare.14538762
Additional file 4 of ARID1A deficiency promotes progression and potentiates therapeutic antitumour immunity in hepatitis B virus-related hepatocellular carcinoma
Xing, T., Li, L., Rao, X., Zhao, J., Chen, Y., Ju, G., Xu, Y., Gao, X., Dong, G., Xia, X., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26658415
Additional file 9 of Genetic alterations and their therapeutic implications in epithelial ovarian cancer
Lapke, N., Chen, C.-H., Chang, T.-C., Chao, A., Lu, Y.-J., Lai, C.-H., Tan, K. T., Chen, H.-C., Lu, H.-Y., & Chen, S.-J. (2021) · Figshare · doi:10.6084/m9.figshare.14538792

Authors: Shen, J., Peng, Y., Wei, L., Zhang, W., Yang, L., Lan, L., Kapoor, P., Ju, Z., Mo, Q., Shih, I.-M., Uray, I. P., Wu, X., Brown, P. H., Shen, X., Mills, G. B., & Peng, G.
Affiliations: The University of Texas MD Anderson Cancer Center (US)
University of Pittsburgh (US)
Baylor College of Medicine (US)
Johns Hopkins University (US)
1Department of Clinical Cancer Prevention, The University of Texas MD Anderson Cancer Center, Houston, Texas.
Corresponding author: Peng, Guang
ORCID: Shen, Jianfeng
Peng, Yang
Zhang, Wei
Yang, Lin
Lan, Li
Ju, Zhenlin
Mo, Qianxing
Shih, Ie-Ming
Wu, Xiangwei
Brown, Powel H.
Mills, Gordon B.
Peng, Guang
Venue: Cancer Discovery
Publisher: American Association for Cancer Research (AACR)
Published: 2015-07-01
Volume: 5
Issue: 7
Pages: 752-767
ISSN: 2159-8274 (ISSN-L)
2159-8290
DOI: 10.1158/2159-8290.cd-14-0849
PMC: PMC4497871
OpenAlex: W2123454509
Cited by: 522
References: 61
Citations by year: 2026: 33 · 2025: 53 · 2024: 59 · 2023: 56 · 2022: 53 · 2021: 71 · 2020: 62 · 2019: 43 · 2018: 36 · 2017: 28 · 2016: 24 · 2015: 3
FWCI: 13.16
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Cancer Discovery (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
University of Debrecen Electronic Archive (University of Debrecen) (submittedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: National Cancer Institute (CA 016672, P50CA098258, P50-CA83639, R00CA149186, K99CA149186, P50CA083639, P30CA016672, R01CA181663)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
Health Sciences › Medicine › Oncology › PARP inhibition in cancer therapy
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Keywords: ARID1A, SWI/SNF complex, DNA damage checkpoint, PARP inhibitors, ATR kinase, DNA double-strand breaks, tumor suppressor, drug sensitivity
MeSH terms: Poly(ADP-ribose) Polymerase Inhibitors, Animals, Breast Neoplasms, DNA Damage, DNA-Binding Proteins, Female, Humans, Lung Neoplasms, Male, Nuclear Proteins, Transcription Factors, Xenograft Model Antitumor Assays, HCT116 Cells, Cell Line, Tumor, Mice, DNA Breaks, Double-Stranded, Ataxia Telangiectasia Mutated Proteins

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ARID1A Deficiency Impairs the DNA Damage Checkpoint and Sensitizes Cells to PARP Inhibitors

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