BCL-3 loss sensitises colorectal cancer cells to DNA damage by targeting homologous recombination
The proto-oncogene BCL-3 is upregulated in a subset of colorectal cancers (CRC), where it has been shown to enhance tumour cell survival. However, although increased expression correlates with poor patient prognosis, the role of BCL-3 in determining therapeutic response remains largely unknown. In t...
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| Published in | DNA repair Vol. 115; p. 103331 |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Netherlands
Elsevier B.V
01.07.2022
Elsevier |
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| Abstract | The proto-oncogene BCL-3 is upregulated in a subset of colorectal cancers (CRC), where it has been shown to enhance tumour cell survival. However, although increased expression correlates with poor patient prognosis, the role of BCL-3 in determining therapeutic response remains largely unknown. In this study, we use combined approaches in multiple cell lines and pre-clinical mouse models to investigate the function of BCL-3 in the DNA damage response. We show that suppression of BCL-3 increases γH2AX foci formation and decreases homologous recombination in CRC cells, resulting in reduced RAD51 foci number and increased sensitivity to PARP inhibition. Importantly, a similar phenotype is seen in Bcl3-/- mice, where Bcl3-/- mouse crypts also exhibit sensitivity to DNA damage with increased γH2AX foci compared to wild type mice. Additionally, Apc.Kras-mutant x Bcl3-/- mice are more sensitive to cisplatin chemotherapy compared to wild type mice. Taken together, our results identify BCL-3 as a regulator of the cellular response to DNA damage and suggests that elevated BCL-3 expression, as observed in CRC, could increase resistance of tumour cells to DNA damaging agents including radiotherapy. These findings offer a rationale for targeting BCL-3 in CRC as an adjunct to conventional therapies and suggest that BCL-3 expression in tumours could be a useful biomarker in stratification of rectal cancer patients for neo-adjuvant chemoradiotherapy. |
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| AbstractList | The proto-oncogene BCL-3 is upregulated in a subset of colorectal cancers (CRC), where it has been shown to enhance tumour cell survival. However, although increased expression correlates with poor patient prognosis, the role of BCL-3 in determining therapeutic response remains largely unknown. In this study, we use combined approaches in multiple cell lines and pre-clinical mouse models to investigate the function of BCL-3 in the DNA damage response. We show that suppression of BCL-3 increases γH2AX foci formation and decreases homologous recombination in CRC cells, resulting in reduced RAD51 foci number and increased sensitivity to PARP inhibition. Importantly, a similar phenotype is seen in Bcl3
-/-
mice, where Bcl3
-/-
mouse crypts also exhibit sensitivity to DNA damage with increased γH2AX foci compared to wild type mice. Additionally, Apc.Kras-mutant x Bcl3
-/-
mice are more sensitive to cisplatin chemotherapy compared to wild type mice. Taken together, our results identify BCL-3 as a regulator of the cellular response to DNA damage and suggests that elevated BCL-3 expression, as observed in CRC, could increase resistance of tumour cells to DNA damaging agents including radiotherapy. These findings offer a rationale for targeting BCL-3 in CRC as an adjunct to conventional therapies and suggest that BCL-3 expression in tumours could be a useful biomarker in stratification of rectal cancer patients for neo-adjuvant chemoradiotherapy. The proto-oncogene BCL-3 is upregulated in a subset of colorectal cancers (CRC), where it has been shown to enhance tumour cell survival. However, although increased expression correlates with poor patient prognosis, the role of BCL-3 in determining therapeutic response remains largely unknown. In this study, we use combined approaches in multiple cell lines and pre-clinical mouse models to investigate the function of BCL-3 in the DNA damage response. We show that suppression of BCL-3 increases γH2AX foci formation and decreases homologous recombination in CRC cells, resulting in reduced RAD51 foci number and increased sensitivity to PARP inhibition. Importantly, a similar phenotype is seen in Bcl3 mice, where Bcl3 mouse crypts also exhibit sensitivity to DNA damage with increased γH2AX foci compared to wild type mice. Additionally, Apc.Kras-mutant x Bcl3 mice are more sensitive to cisplatin chemotherapy compared to wild type mice. Taken together, our results identify BCL-3 as a regulator of the cellular response to DNA damage and suggests that elevated BCL-3 expression, as observed in CRC, could increase resistance of tumour cells to DNA damaging agents including radiotherapy. These findings offer a rationale for targeting BCL-3 in CRC as an adjunct to conventional therapies and suggest that BCL-3 expression in tumours could be a useful biomarker in stratification of rectal cancer patients for neo-adjuvant chemoradiotherapy. The proto-oncogene BCL-3 is upregulated in a subset of colorectal cancers (CRC), where it has been shown to enhance tumour cell survival. However, although increased expression correlates with poor patient prognosis, the role of BCL-3 in determining therapeutic response remains largely unknown. In this study, we use combined approaches in multiple cell lines and pre-clinical mouse models to investigate the function of BCL-3 in the DNA damage response. We show that suppression of BCL-3 increases γH2AX foci formation and decreases homologous recombination in CRC cells, resulting in reduced RAD51 foci number and increased sensitivity to PARP inhibition. Importantly, a similar phenotype is seen in Bcl3-/- mice, where Bcl3-/- mouse crypts also exhibit sensitivity to DNA damage with increased γH2AX foci compared to wild type mice. Additionally, Apc.Kras-mutant x Bcl3-/- mice are more sensitive to cisplatin chemotherapy compared to wild type mice. Taken together, our results identify BCL-3 as a regulator of the cellular response to DNA damage and suggests that elevated BCL-3 expression, as observed in CRC, could increase resistance of tumour cells to DNA damaging agents including radiotherapy. These findings offer a rationale for targeting BCL-3 in CRC as an adjunct to conventional therapies and suggest that BCL-3 expression in tumours could be a useful biomarker in stratification of rectal cancer patients for neo-adjuvant chemoradiotherapy. The proto-oncogene BCL-3 is upregulated in a subset of colorectal cancers (CRC), where it has been shown to enhance tumour cell survival. However, although increased expression correlates with poor patient prognosis, the role of BCL-3 in determining therapeutic response remains largely unknown. In this study, we use combined approaches in multiple cell lines and pre-clinical mouse models to investigate the function of BCL-3 in the DNA damage response. We show that suppression of BCL-3 increases γH2AX foci formation and decreases homologous recombination in CRC cells, resulting in reduced RAD51 foci number and increased sensitivity to PARP inhibition. Importantly, a similar phenotype is seen in Bcl3-/- mice, where Bcl3-/- mouse crypts also exhibit sensitivity to DNA damage with increased γH2AX foci compared to wild type mice. Additionally, Apc.Kras-mutant x Bcl3-/- mice are more sensitive to cisplatin chemotherapy compared to wild type mice. Taken together, our results identify BCL-3 as a regulator of the cellular response to DNA damage and suggests that elevated BCL-3 expression, as observed in CRC, could increase resistance of tumour cells to DNA damaging agents including radiotherapy. These findings offer a rationale for targeting BCL-3 in CRC as an adjunct to conventional therapies and suggest that BCL-3 expression in tumours could be a useful biomarker in stratification of rectal cancer patients for neo-adjuvant chemoradiotherapy.The proto-oncogene BCL-3 is upregulated in a subset of colorectal cancers (CRC), where it has been shown to enhance tumour cell survival. However, although increased expression correlates with poor patient prognosis, the role of BCL-3 in determining therapeutic response remains largely unknown. In this study, we use combined approaches in multiple cell lines and pre-clinical mouse models to investigate the function of BCL-3 in the DNA damage response. We show that suppression of BCL-3 increases γH2AX foci formation and decreases homologous recombination in CRC cells, resulting in reduced RAD51 foci number and increased sensitivity to PARP inhibition. Importantly, a similar phenotype is seen in Bcl3-/- mice, where Bcl3-/- mouse crypts also exhibit sensitivity to DNA damage with increased γH2AX foci compared to wild type mice. Additionally, Apc.Kras-mutant x Bcl3-/- mice are more sensitive to cisplatin chemotherapy compared to wild type mice. Taken together, our results identify BCL-3 as a regulator of the cellular response to DNA damage and suggests that elevated BCL-3 expression, as observed in CRC, could increase resistance of tumour cells to DNA damaging agents including radiotherapy. These findings offer a rationale for targeting BCL-3 in CRC as an adjunct to conventional therapies and suggest that BCL-3 expression in tumours could be a useful biomarker in stratification of rectal cancer patients for neo-adjuvant chemoradiotherapy. |
| ArticleNumber | 103331 |
| Author | Flanagan, Dustin J. Baird, Duncan M. Morgan, Rhys G. Sansom, Owen J. Collard, Tracey J. Ngo, Greg Parker, Christopher Timms, Penny Williams, Ann C. Chambers, Adam C. Ho, Jasmine Wing Yu |
| Author_xml | – sequence: 1 givenname: Christopher surname: Parker fullname: Parker, Christopher organization: Colorectal Tumour Biology Group, School of Cellular and Molecular Medicine, Faculty of Life Sciences, Biomedical Sciences Building, University Walk, University of Bristol, Bristol BS8 1TD, UK – sequence: 2 givenname: Adam C. surname: Chambers fullname: Chambers, Adam C. email: adam.chambers@bristol.ac.uk organization: Colorectal Tumour Biology Group, School of Cellular and Molecular Medicine, Faculty of Life Sciences, Biomedical Sciences Building, University Walk, University of Bristol, Bristol BS8 1TD, UK – sequence: 3 givenname: Dustin J. surname: Flanagan fullname: Flanagan, Dustin J. organization: Cancer Research UK Beatson Institute, Garscube Estate, Switchback Road, Bearsden, Glasgow G61 1BD UK – sequence: 4 givenname: Jasmine Wing Yu surname: Ho fullname: Ho, Jasmine Wing Yu organization: Cancer Research UK Beatson Institute, Garscube Estate, Switchback Road, Bearsden, Glasgow G61 1BD UK – sequence: 5 givenname: Tracey J. surname: Collard fullname: Collard, Tracey J. organization: Colorectal Tumour Biology Group, School of Cellular and Molecular Medicine, Faculty of Life Sciences, Biomedical Sciences Building, University Walk, University of Bristol, Bristol BS8 1TD, UK – sequence: 6 givenname: Greg surname: Ngo fullname: Ngo, Greg organization: Division of Cancer and Genetics, School of Medicine, Cardiff University, Cardiff CF14 4XN UK – sequence: 7 givenname: Duncan M. surname: Baird fullname: Baird, Duncan M. organization: Division of Cancer and Genetics, School of Medicine, Cardiff University, Cardiff CF14 4XN UK – sequence: 8 givenname: Penny surname: Timms fullname: Timms, Penny organization: Colorectal Tumour Biology Group, School of Cellular and Molecular Medicine, Faculty of Life Sciences, Biomedical Sciences Building, University Walk, University of Bristol, Bristol BS8 1TD, UK – sequence: 9 givenname: Rhys G. surname: Morgan fullname: Morgan, Rhys G. organization: School of Life Sciences, University of Sussex, Sussex House, Falmer, Brighton BN1 9RH UK – sequence: 10 givenname: Owen J. surname: Sansom fullname: Sansom, Owen J. organization: Cancer Research UK Beatson Institute, Garscube Estate, Switchback Road, Bearsden, Glasgow G61 1BD UK – sequence: 11 givenname: Ann C. surname: Williams fullname: Williams, Ann C. email: Ann.C.Williams@bristol.ac.uk organization: Colorectal Tumour Biology Group, School of Cellular and Molecular Medicine, Faculty of Life Sciences, Biomedical Sciences Building, University Walk, University of Bristol, Bristol BS8 1TD, UK |
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| CitedBy_id | crossref_primary_10_1186_s12943_023_01922_8 crossref_primary_10_3390_biomedicines12010143 crossref_primary_10_1016_j_neuroscience_2023_11_025 crossref_primary_10_3390_cancers16152676 crossref_primary_10_1016_j_bbadis_2024_167438 |
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| Keywords | H2AX LCCRT CRISPR IR HR PARP siRNA Colorectal cancer/DNA Damage response/Therapy response/Chemoradiotherapy/Homologous recombination BCL-3 DSB DDR CRC NHEJ |
| Language | English |
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| SubjectTerms | Animals Cell Line, Tumor Cisplatin - therapeutic use Colorectal cancer/DNA Damage response/Therapy response/Chemoradiotherapy/Homologous recombination Colorectal Neoplasms - drug therapy Colorectal Neoplasms - genetics DNA Damage Homologous Recombination Humans Mice |
| Title | BCL-3 loss sensitises colorectal cancer cells to DNA damage by targeting homologous recombination |
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