Nuclear F-actin counteracts nuclear deformation and promotes fork repair during replication stress
Filamentous actin (F-actin) provides cells with mechanical support and promotes the mobility of intracellular structures. Although F-actin is traditionally considered to be cytoplasmic, here we reveal that nuclear F-actin participates in the replication stress response. Using live and super-resoluti...
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| Veröffentlicht in: | Nature cell biology Jg. 22; H. 12; S. 1460 - 1470 |
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| Sprache: | Englisch |
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01.12.2020
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| ISSN: | 1465-7392, 1476-4679, 1476-4679 |
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| Abstract | Filamentous actin (F-actin) provides cells with mechanical support and promotes the mobility of intracellular structures. Although F-actin is traditionally considered to be cytoplasmic, here we reveal that nuclear F-actin participates in the replication stress response. Using live and super-resolution imaging, we find that nuclear F-actin is polymerized in response to replication stress through a pathway regulated by ATR-dependent activation of mTORC1, and nucleation through IQGAP1, WASP and ARP2/3. During replication stress, nuclear F-actin increases the nuclear volume and sphericity to counteract nuclear deformation. Furthermore, F-actin and myosin II promote the mobility of stressed-replication foci to the nuclear periphery through increasingly diffusive motion and directed movements along the nuclear actin filaments. These actin functions promote replication stress repair and suppress chromosome and mitotic abnormalities. Moreover, we find that nuclear F-actin is polymerized in vivo in xenograft tumours after treatment with replication-stress-inducing chemotherapeutic agents, indicating that this pathway has a role in human disease. |
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| AbstractList | Filamentous actin (F-actin) provides cells with mechanical support and promotes the mobility of intracellular structures. Although F-actin is traditionally considered to be cytoplasmic, here we reveal that nuclear F-actin participates in the replication stress response. Using live and super-resolution imaging, we find that nuclear F-actin is polymerized in response to replication stress through a pathway regulated by ATR-dependent activation of mTORC1, and nucleation through IQGAP1, WASP and ARP2/3. During replication stress, nuclear F-actin increases the nuclear volume and sphericity to counteract nuclear deformation. Furthermore, F-actin and myosin II promote the mobility of stressed-replication foci to the nuclear periphery through increasingly diffusive motion and directed movements along the nuclear actin filaments. These actin functions promote replication stress repair and suppress chromosome and mitotic abnormalities. Moreover, we find that nuclear F-actin is polymerized in vivo in xenograft tumours after treatment with replication-stress-inducing chemotherapeutic agents, indicating that this pathway has a role in human disease. Filamentous actin (F-actin) provides cells with mechanical support and promotes the mobility of intracellular structures. Although F-actin is traditionally considered to be cytoplasmic, here we reveal that nuclear F-actin participates in the replication stress response. Using live and super-resolution imaging, we find that nuclear F-actin is polymerized in response to replication stress through a pathway regulated by ATR-dependent activation of mTORC1, and nucleation through IQGAP1, WASP and ARP2/3. During replication stress, nuclear F-actin increases the nuclear volume and sphericity to counteract nuclear deformation. Furthermore, F-actin and myosin II promote the mobility of stressed-replication foci to the nuclear periphery through increasingly diffusive motion and directed movements along the nuclear actin filaments. These actin functions promote replication stress repair and suppress chromosome and mitotic abnormalities. Moreover, we find that nuclear F-actin is polymerized in vivo in xenograft tumours after treatment with replication-stress-inducing chemotherapeutic agents, indicating that this pathway has a role in human disease.Filamentous actin (F-actin) provides cells with mechanical support and promotes the mobility of intracellular structures. Although F-actin is traditionally considered to be cytoplasmic, here we reveal that nuclear F-actin participates in the replication stress response. Using live and super-resolution imaging, we find that nuclear F-actin is polymerized in response to replication stress through a pathway regulated by ATR-dependent activation of mTORC1, and nucleation through IQGAP1, WASP and ARP2/3. During replication stress, nuclear F-actin increases the nuclear volume and sphericity to counteract nuclear deformation. Furthermore, F-actin and myosin II promote the mobility of stressed-replication foci to the nuclear periphery through increasingly diffusive motion and directed movements along the nuclear actin filaments. These actin functions promote replication stress repair and suppress chromosome and mitotic abnormalities. Moreover, we find that nuclear F-actin is polymerized in vivo in xenograft tumours after treatment with replication-stress-inducing chemotherapeutic agents, indicating that this pathway has a role in human disease. Filamentous actin (F-actin) provides cells with mechanical support and promotes the mobility of intracellular structures. Although F-actin is traditionally considered to be cytoplasmic, here we reveal that nuclear F-actin participates in the replication stress response. Using live and super-resolution imaging, we find that nuclear F-actin is polymerized in response to replication stress through a pathway regulated by ATR-dependent activation of mTORC1, and nucleation through IQGAP1, WASP and ARP2/3. During replication stress, nuclear F-actin increases the nuclear volume and sphericity to counteract nuclear deformation. Furthermore, F-actin and myosin II promote the mobility of stressed-replication foci to the nuclear periphery through increasingly diffusive motion and directed movements along the nuclear actin filaments. These actin functions promote replication stress repair and suppress chromosome and mitotic abnormalities. Moreover, we find that nuclear F-actin is polymerized in vivo in xenograft tumours after treatment with replication-stress-inducing chemotherapeutic agents, indicating that this pathway has a role in human disease.Lamm et al. report that replication stress activates mTOR through ATR to induce nuclear actin polymerization, facilitating the recovery from replication stress. |
| Author | Lamm, Noa Nobis, Max Biro, Maté Read, Mark N Masamsetti, V Pragathi Cesare, Anthony J Van Ly, David Page, Scott G Timpson, Paul |
| Author_xml | – sequence: 1 givenname: Noa surname: Lamm fullname: Lamm, Noa organization: Genome Integrity Unit, Children's Medical Research Institute, University of Sydney, Westmead, New South Wales, Australia – sequence: 2 givenname: Mark N orcidid: 0000-0002-1481-4780 surname: Read fullname: Read, Mark N organization: School of Computer Science, The Westmead Initiative and The Charles Perkins Centre, University of Sydney, Camperdown, New South Wales, Australia – sequence: 3 givenname: Max surname: Nobis fullname: Nobis, Max organization: The Garvan Institute of Medical Research, St Vincent's Clinical School, Faculty of Medicine, University of New South Wales, Sydney, New South Wales, Australia – sequence: 4 givenname: David surname: Van Ly fullname: Van Ly, David organization: School of Medicine, The University of Notre Dame Australia, Sydney, New South Wales, Australia – sequence: 5 givenname: Scott G surname: Page fullname: Page, Scott G organization: Genome Integrity Unit, Children's Medical Research Institute, University of Sydney, Westmead, New South Wales, Australia – sequence: 6 givenname: V Pragathi orcidid: 0000-0002-0251-1707 surname: Masamsetti fullname: Masamsetti, V Pragathi organization: Genome Integrity Unit, Children's Medical Research Institute, University of Sydney, Westmead, New South Wales, Australia – sequence: 7 givenname: Paul surname: Timpson fullname: Timpson, Paul organization: The Garvan Institute of Medical Research, St Vincent's Clinical School, Faculty of Medicine, University of New South Wales, Sydney, New South Wales, Australia – sequence: 8 givenname: Maté orcidid: 0000-0001-5852-3726 surname: Biro fullname: Biro, Maté organization: EMBL Australia, Single Molecule Science node, School of Medical Sciences, University of New South Wales, Sydney, New South Wales, Australia – sequence: 9 givenname: Anthony J orcidid: 0000-0002-0864-1254 surname: Cesare fullname: Cesare, Anthony J email: tcesare@cmri.org.au organization: Genome Integrity Unit, Children's Medical Research Institute, University of Sydney, Westmead, New South Wales, Australia. tcesare@cmri.org.au |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33257806$$D View this record in MEDLINE/PubMed |
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| Snippet | Filamentous actin (F-actin) provides cells with mechanical support and promotes the mobility of intracellular structures. Although F-actin is traditionally... |
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| SubjectTerms | Abnormalities Actin Actin Cytoskeleton - metabolism Actins - genetics Actins - metabolism Animals Antineoplastic Agents - pharmacology Carboplatin - pharmacology Cell Line Cell Line, Tumor Cell Nucleus - genetics Cell Nucleus - metabolism Chemotherapy Chromosomes DNA Repair - genetics DNA Replication - genetics Filaments Humans Image resolution IQGAP1 protein Mechanistic Target of Rapamycin Complex 1 - genetics Mechanistic Target of Rapamycin Complex 1 - metabolism Mice, Inbred NOD Mice, Knockout Mice, SCID Mobility Myosin Neoplasms - drug therapy Neoplasms - genetics Neoplasms - metabolism Nuclear deformation Nucleation Polymerization Repair Replication TOR protein Tumors Xenograft Model Antitumor Assays - methods Xenografts Xenotransplantation |
| Title | Nuclear F-actin counteracts nuclear deformation and promotes fork repair during replication stress |
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