Microhomology-mediated end joining is activated in irradiated human cells due to phosphorylation-dependent formation of the XRCC1 repair complex
Abstract
Microhomology-mediated end joining (MMEJ), an error-prone pathway for DNA double-strand break (DSB) repair, is implicated in genomic rearrangement and oncogenic transformation; however, its contribution to repair of radiation-induced DSBs has not been characterized. We used recircularization of a linearized plasmid with 3'-P-blocked termini, mimicking those at X-ray-induced strand breaks, to recapitulate DSB repair via MMEJ or nonhomologous end-joining (NHEJ). Sequence analysis of the circularized plasmids allowed measurement of relative activity of MMEJ versus NHEJ. While we predictably observed NHEJ to be the predominant pathway for DSB repair in our assay, MMEJ was significantly enhanced in preirradiated cells, independent of their radiation-induced arrest in the G2/M phase. MMEJ activation was dependent on XRCC1 phosphorylation by casein kinase 2 (CK2), enhancing XRCC1’s interaction with the end resection enzymes MRE11 and CtIP. Both endonuclease and exonuclease activities of MRE11 were required for MMEJ, as has been observed for homology-directed DSB repair (HDR). Furthermore, the XRCC1 co-immunoprecipitate complex (IP) displayed MMEJ activity in vitro, which was significantly elevated after irradiation. Our studies thus suggest that radiation-mediated enhancement of MMEJ in cells surviving radiation therapy may contribute to their radioresistance and could be therapeutically targeted.
- Authors:
-
[1];
- Houston Methodist Research Inst., TX (United States). Dept. of Radiation Oncology; Univ. of Texas Medical Branch (UTMB), Galveston, TX (United States). Dept. of Biochemistry and Molecular Biology
- Houston Methodist Research Inst., TX (United States). Dept. of Radiation Oncology; Texas A&M Health Science Center, Bryan, TX (United States). College of Medicine
- EntroGen, Inc., Woodland Hills, CA (United States)
- Houston Methodist Research Inst., TX (United States). Dept. of Radiation Oncology
- Houston Methodist Research Inst., TX (United States). Dept. of Radiation Oncology; Cornell Univ., Ithaca, NY (United States). Weill Medical College
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Dept. of Cell and Molecular Biology
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Dept. of Cell and Molecular Biology; Univ. of Texas MD Anderson Cancer Center, Houston, TX (United States). Dept. of Molecular and Cellular Oncology
- Univ. of Alberta, Edmonton, AB (Canada). Cross Cancer Inst., Dept. of Oncology
- Houston Methodist Research Inst., TX (United States). Dept. of Radiation Oncology; Cornell Univ., Ithaca, NY (United States). Weill Medical College; Houston Methodist Neurological Inst., TX (United States)
- Houston Methodist Research Inst., TX (United States). Dept. of Radiation Oncology; Univ. of Texas Medical Branch (UTMB), Galveston, TX (United States). Dept. of Biochemistry and Molecular Biology; Texas A&M Health Science Center, Bryan, TX (United States). College of Medicine; Cornell Univ., Ithaca, NY (United States). Weill Medical College
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); USPHS; Robert A Welch Chemistry Chair; Cancer Prevention and Research Institute of Texas (CPRIT); National Space Biomedical Research Institute
- OSTI Identifier:
- 1625550
- Grant/Contract Number:
- AC02-05CH11231; R01 CA158910; R01 GM105090; R01 NS088645; P01 CA92548; R01 CA117638
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nucleic Acids Research
- Additional Journal Information:
- Journal Volume: 45; Journal Issue: 5; Journal ID: ISSN 0305-1048
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Biochemistry & molecular biology; Genome integrity, repair and replication
Citation Formats
Dutta, Arijit, Eckelmann, Bradley, Adhikari, Sanjay, Ahmed, Kazi Mokim, Sengupta, Shiladitya, Pandey, Arvind, Hegde, Pavana M., Tsai, Miaw-Sheue, Tainer, John A., Weinfeld, Michael, Hegde, Muralidhar L., and Mitra, Sankar. Microhomology-mediated end joining is activated in irradiated human cells due to phosphorylation-dependent formation of the XRCC1 repair complex. United States: N. p., 2016.
Web. doi:10.1093/nar/gkw1262.
Dutta, Arijit, Eckelmann, Bradley, Adhikari, Sanjay, Ahmed, Kazi Mokim, Sengupta, Shiladitya, Pandey, Arvind, Hegde, Pavana M., Tsai, Miaw-Sheue, Tainer, John A., Weinfeld, Michael, Hegde, Muralidhar L., & Mitra, Sankar. Microhomology-mediated end joining is activated in irradiated human cells due to phosphorylation-dependent formation of the XRCC1 repair complex. United States. https://doi.org/10.1093/nar/gkw1262
Dutta, Arijit, Eckelmann, Bradley, Adhikari, Sanjay, Ahmed, Kazi Mokim, Sengupta, Shiladitya, Pandey, Arvind, Hegde, Pavana M., Tsai, Miaw-Sheue, Tainer, John A., Weinfeld, Michael, Hegde, Muralidhar L., and Mitra, Sankar. Mon .
"Microhomology-mediated end joining is activated in irradiated human cells due to phosphorylation-dependent formation of the XRCC1 repair complex". United States. https://doi.org/10.1093/nar/gkw1262. https://www.osti.gov/servlets/purl/1625550.
@article{osti_1625550,
title = {Microhomology-mediated end joining is activated in irradiated human cells due to phosphorylation-dependent formation of the XRCC1 repair complex},
author = {Dutta, Arijit and Eckelmann, Bradley and Adhikari, Sanjay and Ahmed, Kazi Mokim and Sengupta, Shiladitya and Pandey, Arvind and Hegde, Pavana M. and Tsai, Miaw-Sheue and Tainer, John A. and Weinfeld, Michael and Hegde, Muralidhar L. and Mitra, Sankar},
abstractNote = {Microhomology-mediated end joining (MMEJ), an error-prone pathway for DNA double-strand break (DSB) repair, is implicated in genomic rearrangement and oncogenic transformation; however, its contribution to repair of radiation-induced DSBs has not been characterized. We used recircularization of a linearized plasmid with 3'-P-blocked termini, mimicking those at X-ray-induced strand breaks, to recapitulate DSB repair via MMEJ or nonhomologous end-joining (NHEJ). Sequence analysis of the circularized plasmids allowed measurement of relative activity of MMEJ versus NHEJ. While we predictably observed NHEJ to be the predominant pathway for DSB repair in our assay, MMEJ was significantly enhanced in preirradiated cells, independent of their radiation-induced arrest in the G2/M phase. MMEJ activation was dependent on XRCC1 phosphorylation by casein kinase 2 (CK2), enhancing XRCC1’s interaction with the end resection enzymes MRE11 and CtIP. Both endonuclease and exonuclease activities of MRE11 were required for MMEJ, as has been observed for homology-directed DSB repair (HDR). Furthermore, the XRCC1 co-immunoprecipitate complex (IP) displayed MMEJ activity in vitro, which was significantly elevated after irradiation. Our studies thus suggest that radiation-mediated enhancement of MMEJ in cells surviving radiation therapy may contribute to their radioresistance and could be therapeutically targeted.},
doi = {10.1093/nar/gkw1262},
journal = {Nucleic Acids Research},
number = 5,
volume = 45,
place = {United States},
year = {Mon Dec 19 00:00:00 EST 2016},
month = {Mon Dec 19 00:00:00 EST 2016}
}
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