The p97–Ataxin 3 complex regulates homeostasis of the DNA damage response E3 ubiquitin ligase RNF8
The E3 ubiquitin ligase RNF8 (RING finger protein 8) is a pivotal enzyme for DNA repair. However, RNF8 hyper‐accumulation is tumour‐promoting and positively correlates with genome instability, cancer cell invasion, metastasis and poor patient prognosis. Very little is known about the mechanisms regu...
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| Vydané v: | The EMBO journal Ročník 38; číslo 21; s. e102361 - n/a |
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| Médium: | Journal Article |
| Jazyk: | English |
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London
Nature Publishing Group UK
04.10.2019
Springer Nature B.V John Wiley and Sons Inc |
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| ISSN: | 0261-4189, 1460-2075, 1460-2075 |
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| Abstract | The E3 ubiquitin ligase RNF8 (RING finger protein 8) is a pivotal enzyme for DNA repair. However, RNF8 hyper‐accumulation is tumour‐promoting and positively correlates with genome instability, cancer cell invasion, metastasis and poor patient prognosis. Very little is known about the mechanisms regulating RNF8 homeostasis to preserve genome stability. Here, we identify the cellular machinery, composed of the p97/VCP ubiquitin‐dependent unfoldase/segregase and the Ataxin 3 (ATX3) deubiquitinase, which together form a physical and functional complex with RNF8 to regulate its proteasome‐dependent homeostasis under physiological conditions. Under genotoxic stress, when RNF8 is rapidly recruited to sites of DNA lesions, the p97–ATX3 machinery stimulates the extraction of RNF8 from chromatin to balance DNA repair pathway choice and promote cell survival after ionising radiation (IR). Inactivation of the p97–ATX3 complex affects the non‐homologous end joining DNA repair pathway and hypersensitises human cancer cells to IR. We propose that the p97–ATX3 complex is the essential machinery for regulation of RNF8 homeostasis under both physiological and genotoxic conditions and that targeting ATX3 may be a promising strategy to radio‐sensitise BRCA‐deficient cancers.
Synopsis
The RNF8 ubiquitin ligase is a key mediator of the ubiquitin‐mediated DNA damage response and regulator of double strand break repair pathway choice. Here, these roles are shown to depend on homeostatic regulation of RNF8 by the ubiquitin‐dependent segregase p97/VCP and the deubiquitinase Ataxin 3 (ATX3).
A p97‐ATX3 complex maintains proteasome‐dependent RNF8 homeostasis under physiological condition.
The p97‐ATX3 complex extracts RNF8 from chromatin after its recruitment to DNA damage sites.
p97‐ATX3‐mediated RNF8 extraction promotes timely RNF168 recruitment and utilization of non‐homologous end joining (NHEJ) repair.
Inactivation of the p97‐ATX3 complex hyper‐sensitizes BRCA2/homologous recombination‐deficient cells to ionizing radiation.
Graphical Abstract
Chromatin extraction of RNF8 by the ubiquitin‐dependent segregase p97/VCP and the deubiquitinase ATX3 emerges as a key mechanism for balancing DNA repair pathway choice. |
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| AbstractList | The E3 ubiquitin ligase RNF8 (RING finger protein 8) is a pivotal enzyme for DNA repair. However, RNF8 hyper‐accumulation is tumour‐promoting and positively correlates with genome instability, cancer cell invasion, metastasis and poor patient prognosis. Very little is known about the mechanisms regulating RNF8 homeostasis to preserve genome stability. Here, we identify the cellular machinery, composed of the p97/VCP ubiquitin‐dependent unfoldase/segregase and the Ataxin 3 (ATX3) deubiquitinase, which together form a physical and functional complex with RNF8 to regulate its proteasome‐dependent homeostasis under physiological conditions. Under genotoxic stress, when RNF8 is rapidly recruited to sites of DNA lesions, the p97–ATX3 machinery stimulates the extraction of RNF8 from chromatin to balance DNA repair pathway choice and promote cell survival after ionising radiation (IR). Inactivation of the p97–ATX3 complex affects the non‐homologous end joining DNA repair pathway and hypersensitises human cancer cells to IR. We propose that the p97–ATX3 complex is the essential machinery for regulation of RNF8 homeostasis under both physiological and genotoxic conditions and that targeting ATX3 may be a promising strategy to radio‐sensitise BRCA‐deficient cancers. The E3 ubiquitin ligase RNF8 (RING finger protein 8) is a pivotal enzyme for DNA repair. However, RNF8 hyper‐accumulation is tumour‐promoting and positively correlates with genome instability, cancer cell invasion, metastasis and poor patient prognosis. Very little is known about the mechanisms regulating RNF8 homeostasis to preserve genome stability. Here, we identify the cellular machinery, composed of the p97/VCP ubiquitin‐dependent unfoldase/segregase and the Ataxin 3 (ATX3) deubiquitinase, which together form a physical and functional complex with RNF8 to regulate its proteasome‐dependent homeostasis under physiological conditions. Under genotoxic stress, when RNF8 is rapidly recruited to sites of DNA lesions, the p97–ATX3 machinery stimulates the extraction of RNF8 from chromatin to balance DNA repair pathway choice and promote cell survival after ionising radiation (IR). Inactivation of the p97–ATX3 complex affects the non‐homologous end joining DNA repair pathway and hypersensitises human cancer cells to IR. We propose that the p97–ATX3 complex is the essential machinery for regulation of RNF8 homeostasis under both physiological and genotoxic conditions and that targeting ATX3 may be a promising strategy to radio‐sensitise BRCA‐deficient cancers. Synopsis The RNF8 ubiquitin ligase is a key mediator of the ubiquitin‐mediated DNA damage response and regulator of double strand break repair pathway choice. Here, these roles are shown to depend on homeostatic regulation of RNF8 by the ubiquitin‐dependent segregase p97/VCP and the deubiquitinase Ataxin 3 (ATX3). A p97‐ATX3 complex maintains proteasome‐dependent RNF8 homeostasis under physiological condition. The p97‐ATX3 complex extracts RNF8 from chromatin after its recruitment to DNA damage sites. p97‐ATX3‐mediated RNF8 extraction promotes timely RNF168 recruitment and utilization of non‐homologous end joining (NHEJ) repair. Inactivation of the p97‐ATX3 complex hyper‐sensitizes BRCA2/homologous recombination‐deficient cells to ionizing radiation. Graphical Abstract Chromatin extraction of RNF8 by the ubiquitin‐dependent segregase p97/VCP and the deubiquitinase ATX3 emerges as a key mechanism for balancing DNA repair pathway choice. The E3 ubiquitin ligase RNF8 (RING finger protein 8) is a pivotal enzyme for DNA repair. However, RNF8 hyper-accumulation is tumour-promoting and positively correlates with genome instability, cancer cell invasion, metastasis and poor patient prognosis. Very little is known about the mechanisms regulating RNF8 homeostasis to preserve genome stability. Here, we identify the cellular machinery, composed of the p97/VCP ubiquitin-dependent unfoldase/segregase and the Ataxin 3 (ATX3) deubiquitinase, which together form a physical and functional complex with RNF8 to regulate its proteasome-dependent homeostasis under physiological conditions. Under genotoxic stress, when RNF8 is rapidly recruited to sites of DNA lesions, the p97-ATX3 machinery stimulates the extraction of RNF8 from chromatin to balance DNA repair pathway choice and promote cell survival after ionising radiation (IR). Inactivation of the p97-ATX3 complex affects the non-homologous end joining DNA repair pathway and hypersensitises human cancer cells to IR. We propose that the p97-ATX3 complex is the essential machinery for regulation of RNF8 homeostasis under both physiological and genotoxic conditions and that targeting ATX3 may be a promising strategy to radio-sensitise BRCA-deficient cancers.The E3 ubiquitin ligase RNF8 (RING finger protein 8) is a pivotal enzyme for DNA repair. However, RNF8 hyper-accumulation is tumour-promoting and positively correlates with genome instability, cancer cell invasion, metastasis and poor patient prognosis. Very little is known about the mechanisms regulating RNF8 homeostasis to preserve genome stability. Here, we identify the cellular machinery, composed of the p97/VCP ubiquitin-dependent unfoldase/segregase and the Ataxin 3 (ATX3) deubiquitinase, which together form a physical and functional complex with RNF8 to regulate its proteasome-dependent homeostasis under physiological conditions. Under genotoxic stress, when RNF8 is rapidly recruited to sites of DNA lesions, the p97-ATX3 machinery stimulates the extraction of RNF8 from chromatin to balance DNA repair pathway choice and promote cell survival after ionising radiation (IR). Inactivation of the p97-ATX3 complex affects the non-homologous end joining DNA repair pathway and hypersensitises human cancer cells to IR. We propose that the p97-ATX3 complex is the essential machinery for regulation of RNF8 homeostasis under both physiological and genotoxic conditions and that targeting ATX3 may be a promising strategy to radio-sensitise BRCA-deficient cancers. The E3 ubiquitin ligase RNF8 (RING finger protein 8) is a pivotal enzyme for DNA repair. However, RNF8 hyper‐accumulation is tumour‐promoting and positively correlates with genome instability, cancer cell invasion, metastasis and poor patient prognosis. Very little is known about the mechanisms regulating RNF8 homeostasis to preserve genome stability. Here, we identify the cellular machinery, composed of the p97/VCP ubiquitin‐dependent unfoldase/segregase and the Ataxin 3 (ATX3) deubiquitinase, which together form a physical and functional complex with RNF8 to regulate its proteasome‐dependent homeostasis under physiological conditions. Under genotoxic stress, when RNF8 is rapidly recruited to sites of DNA lesions, the p97–ATX3 machinery stimulates the extraction of RNF8 from chromatin to balance DNA repair pathway choice and promote cell survival after ionising radiation (IR). Inactivation of the p97–ATX3 complex affects the non‐homologous end joining DNA repair pathway and hypersensitises human cancer cells to IR. We propose that the p97–ATX3 complex is the essential machinery for regulation of RNF8 homeostasis under both physiological and genotoxic conditions and that targeting ATX3 may be a promising strategy to radio‐sensitise BRCA‐deficient cancers. Synopsis The RNF8 ubiquitin ligase is a key mediator of the ubiquitin‐mediated DNA damage response and regulator of double strand break repair pathway choice. Here, these roles are shown to depend on homeostatic regulation of RNF8 by the ubiquitin‐dependent segregase p97/VCP and the deubiquitinase Ataxin 3 (ATX3). A p97‐ATX3 complex maintains proteasome‐dependent RNF8 homeostasis under physiological condition. The p97‐ATX3 complex extracts RNF8 from chromatin after its recruitment to DNA damage sites. p97‐ATX3‐mediated RNF8 extraction promotes timely RNF168 recruitment and utilization of non‐homologous end joining (NHEJ) repair. Inactivation of the p97‐ATX3 complex hyper‐sensitizes BRCA2/homologous recombination‐deficient cells to ionizing radiation. Chromatin extraction of RNF8 by the ubiquitin‐dependent segregase p97/VCP and the deubiquitinase ATX3 emerges as a key mechanism for balancing DNA repair pathway choice. |
| Author | Singh, Abhay Narayan Oehler, Judith Fielden, John Parsons, Jason Hernandez‐Carralero, Esperanza Tullis, Iain DC Kilgas, Susan Vaz, Bruno Cabrera, Elisa Ramadan, Kristijan Kiltie, Anne E Guérillon, Claire Barber, Paul R Meerang, Mayura Mailand, Niels Freire, Raimundo Torrecilla, Ignacio Li, Shudong Vojnovic, Borivoj |
| AuthorAffiliation | 6 Universidad Fernando Pessoa Canarias Santa Maria de Guia Spain 8 Present address: Department of Biochemistry University of Oxford Oxford UK 5 Institute of Pharmacology and Toxicology‐Vetsuisse Faculty University of Zurich Zurich Switzerland 3 Unidad de Investigación Hospital Universitario de Canarias La Laguna Spain 2 Novo Nordisk Foundation Center for Protein Research University of Copenhagen Copenhagen Denmark 1 Department of Oncology Cancer Research UK/Medical Research Council Oxford Institute for Radiation Oncology University of Oxford Oxford UK 4 Instituto de Tecnologías Biomédicas Universidad de La Laguna La Laguna Spain 7 Department of Molecular and Clinical Cancer Medicine Cancer Research Centre University of Liverpool Liverpool UK 9 Present address: Department of Thoracic Surgery University Hospital Zurich Zurich Switzerland |
| AuthorAffiliation_xml | – name: 6 Universidad Fernando Pessoa Canarias Santa Maria de Guia Spain – name: 3 Unidad de Investigación Hospital Universitario de Canarias La Laguna Spain – name: 8 Present address: Department of Biochemistry University of Oxford Oxford UK – name: 7 Department of Molecular and Clinical Cancer Medicine Cancer Research Centre University of Liverpool Liverpool UK – name: 9 Present address: Department of Thoracic Surgery University Hospital Zurich Zurich Switzerland – name: 4 Instituto de Tecnologías Biomédicas Universidad de La Laguna La Laguna Spain – name: 5 Institute of Pharmacology and Toxicology‐Vetsuisse Faculty University of Zurich Zurich Switzerland – name: 2 Novo Nordisk Foundation Center for Protein Research University of Copenhagen Copenhagen Denmark – name: 1 Department of Oncology Cancer Research UK/Medical Research Council Oxford Institute for Radiation Oncology University of Oxford Oxford UK |
| Author_xml | – sequence: 1 givenname: Abhay Narayan surname: Singh fullname: Singh, Abhay Narayan organization: Department of Oncology, Cancer Research UK/Medical Research Council Oxford Institute for Radiation Oncology, University of Oxford – sequence: 2 givenname: Judith surname: Oehler fullname: Oehler, Judith organization: Department of Oncology, Cancer Research UK/Medical Research Council Oxford Institute for Radiation Oncology, University of Oxford, Department of Biochemistry, University of Oxford – sequence: 3 givenname: Ignacio surname: Torrecilla fullname: Torrecilla, Ignacio organization: Department of Oncology, Cancer Research UK/Medical Research Council Oxford Institute for Radiation Oncology, University of Oxford – sequence: 4 givenname: Susan surname: Kilgas fullname: Kilgas, Susan organization: Department of Oncology, Cancer Research UK/Medical Research Council Oxford Institute for Radiation Oncology, University of Oxford – sequence: 5 givenname: Shudong surname: Li fullname: Li, Shudong organization: Department of Oncology, Cancer Research UK/Medical Research Council Oxford Institute for Radiation Oncology, University of Oxford – sequence: 6 givenname: Bruno surname: Vaz fullname: Vaz, Bruno organization: Department of Oncology, Cancer Research UK/Medical Research Council Oxford Institute for Radiation Oncology, University of Oxford – sequence: 7 givenname: Claire surname: Guérillon fullname: Guérillon, Claire organization: Novo Nordisk Foundation Center for Protein Research, University of Copenhagen – sequence: 8 givenname: John surname: Fielden fullname: Fielden, John organization: Department of Oncology, Cancer Research UK/Medical Research Council Oxford Institute for Radiation Oncology, University of Oxford – sequence: 9 givenname: Esperanza surname: Hernandez‐Carralero fullname: Hernandez‐Carralero, Esperanza organization: Unidad de Investigación, Hospital Universitario de Canarias, Instituto de Tecnologías Biomédicas, Universidad de La Laguna – sequence: 10 givenname: Elisa surname: Cabrera fullname: Cabrera, Elisa organization: Unidad de Investigación, Hospital Universitario de Canarias, Instituto de Tecnologías Biomédicas, Universidad de La Laguna – sequence: 11 givenname: Iain DC surname: Tullis fullname: Tullis, Iain DC organization: Department of Oncology, Cancer Research UK/Medical Research Council Oxford Institute for Radiation Oncology, University of Oxford – sequence: 12 givenname: Mayura surname: Meerang fullname: Meerang, Mayura organization: Institute of Pharmacology and Toxicology‐Vetsuisse Faculty, University of Zurich, Department of Thoracic Surgery, University Hospital Zurich – sequence: 13 givenname: Paul R surname: Barber fullname: Barber, Paul R organization: Department of Oncology, Cancer Research UK/Medical Research Council Oxford Institute for Radiation Oncology, University of Oxford – sequence: 14 givenname: Raimundo surname: Freire fullname: Freire, Raimundo organization: Unidad de Investigación, Hospital Universitario de Canarias, Instituto de Tecnologías Biomédicas, Universidad de La Laguna, Universidad Fernando Pessoa Canarias – sequence: 15 givenname: Jason surname: Parsons fullname: Parsons, Jason organization: Department of Molecular and Clinical Cancer Medicine, Cancer Research Centre, University of Liverpool – sequence: 16 givenname: Borivoj surname: Vojnovic fullname: Vojnovic, Borivoj organization: Department of Oncology, Cancer Research UK/Medical Research Council Oxford Institute for Radiation Oncology, University of Oxford – sequence: 17 givenname: Anne E orcidid: 0000-0001-7208-2912 surname: Kiltie fullname: Kiltie, Anne E organization: Department of Oncology, Cancer Research UK/Medical Research Council Oxford Institute for Radiation Oncology, University of Oxford – sequence: 18 givenname: Niels orcidid: 0000-0002-6623-709X surname: Mailand fullname: Mailand, Niels organization: Novo Nordisk Foundation Center for Protein Research, University of Copenhagen – sequence: 19 givenname: Kristijan orcidid: 0000-0001-5522-021X surname: Ramadan fullname: Ramadan, Kristijan email: kristijan.ramadan@oncology.ox.ac.uk organization: Department of Oncology, Cancer Research UK/Medical Research Council Oxford Institute for Radiation Oncology, University of Oxford |
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| Keywords | genome stability DNA double‐strand break repair Ataxin 3 p97/VCP ATPase E3 ubiquitin ligase RNF8 DNA double-strand break repair |
| Language | English |
| License | Attribution 2019 The Authors. Published under the terms of the CC BY 4.0 license. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
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| Snippet | The E3 ubiquitin ligase RNF8 (RING finger protein 8) is a pivotal enzyme for DNA repair. However, RNF8 hyper‐accumulation is tumour‐promoting and positively... The E3 ubiquitin ligase RNF8 (RING finger protein 8) is a pivotal enzyme for DNA repair. However, RNF8 hyper-accumulation is tumour-promoting and positively... |
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| SubjectTerms | Adenosine Triphosphatases - genetics Adenosine Triphosphatases - metabolism Ataxin Ataxin 3 Ataxin-3 - genetics Ataxin-3 - metabolism BRCA2 protein Breast cancer Cancer Cell Survival Chromatin Chromatin - genetics Damage Deactivation Deoxyribonucleic acid DNA DNA Breaks, Double-Stranded DNA damage DNA double‐strand break repair DNA Repair DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism E3 ubiquitin ligase RNF8 EMBO13 EMBO31 genome stability Genomes Genomic Instability Genotoxicity HEK293 Cells HeLa Cells Homeostasis Homologous recombination Homology Humans Inactivation Ionizing radiation Medical prognosis Metastases Non-homologous end joining Nuclear Proteins - genetics Nuclear Proteins - metabolism p97/VCP ATPase Physiology Proteasome Endopeptidase Complex - metabolism Proteasomes Proteolysis Recruitment Repair Signal Transduction Tumors Ubiquitin Ubiquitin - metabolism Ubiquitin-protein ligase Ubiquitin-Protein Ligases - genetics Ubiquitin-Protein Ligases - metabolism Ubiquitination |
| Title | The p97–Ataxin 3 complex regulates homeostasis of the DNA damage response E3 ubiquitin ligase RNF8 |
| URI | https://link.springer.com/article/10.15252/embj.2019102361 https://onlinelibrary.wiley.com/doi/abs/10.15252%2Fembj.2019102361 https://www.ncbi.nlm.nih.gov/pubmed/31613024 https://www.proquest.com/docview/2311474055 https://www.proquest.com/docview/2305799693 https://pubmed.ncbi.nlm.nih.gov/PMC6826192 |
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