Lamin A/C facilitates DNA damage response by modulating ATM signaling and homologous recombination pathways

Lamin A/C, a core component of the nuclear lamina, forms a mesh-like structure beneath the inner nuclear membrane. While its structural role is well-studied, its involvement in DNA metabolism remains unclear. We conducted sequential protein fractionation to determine the subcellular localization of...

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Main Authors: Seong-jung Kim, Su Hyung Park, Kyungjae Myung, Kyoo-young Lee
Format: Article
Language:English
Published: Taylor & Francis Group 2024-12-01
Series:Animal Cells and Systems
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Online Access:https://www.tandfonline.com/doi/10.1080/19768354.2024.2393820
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author Seong-jung Kim
Su Hyung Park
Kyungjae Myung
Kyoo-young Lee
author_facet Seong-jung Kim
Su Hyung Park
Kyungjae Myung
Kyoo-young Lee
author_sort Seong-jung Kim
collection DOAJ
description Lamin A/C, a core component of the nuclear lamina, forms a mesh-like structure beneath the inner nuclear membrane. While its structural role is well-studied, its involvement in DNA metabolism remains unclear. We conducted sequential protein fractionation to determine the subcellular localization of early DNA damage response (DDR) proteins. Our findings indicate that most DDR proteins, including ATM and the MRE11-RAD50-NBS1 (MRN) complex, are present in the nuclease – and high salt-resistant pellet fraction. Notably, ATM and MRN remain stably associated with these structures throughout the cell cycle, independent of ionizing radiation (IR)-induced DNA damage. Although Lamin A/C interacts with ATM and MRN, its depletion does not disrupt their association with nuclease-resistant structures. However, it impairs the IR-enhanced association of ATM with the nuclear matrix and ATM-mediated DDR signaling, as well as the interaction between ATM and MRN. This disruption impedes the recruitment of MRE11 to damaged DNA and the association of damaged DNA with the nuclear matrix. Additionally, Lamin A/C depletion results in reduced protein levels of CtIP and RAD51, which is mediated by transcriptional regulation. This, in turn, impairs the efficiency of homologous recombination (HR). Our findings indicate that Lamin A/C plays a pivotal role in DNA damage repair (DDR) by orchestrating ATM-mediated signaling, maintaining HR protein levels, and ensuring efficient DNA repair processes.
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spelling doaj-art-252959cfcbaf45b6943abeaefa027f3e2025-08-20T03:08:36ZengTaylor & Francis GroupAnimal Cells and Systems1976-83542151-24852024-12-0128140141610.1080/19768354.2024.2393820Lamin A/C facilitates DNA damage response by modulating ATM signaling and homologous recombination pathwaysSeong-jung Kim0Su Hyung Park1Kyungjae Myung2Kyoo-young Lee3Center for Genomic Integrity, Institute for Basic Science, Ulsan, KoreaCenter for Genomic Integrity, Institute for Basic Science, Ulsan, KoreaCenter for Genomic Integrity, Institute for Basic Science, Ulsan, KoreaCenter for Genomic Integrity, Institute for Basic Science, Ulsan, KoreaLamin A/C, a core component of the nuclear lamina, forms a mesh-like structure beneath the inner nuclear membrane. While its structural role is well-studied, its involvement in DNA metabolism remains unclear. We conducted sequential protein fractionation to determine the subcellular localization of early DNA damage response (DDR) proteins. Our findings indicate that most DDR proteins, including ATM and the MRE11-RAD50-NBS1 (MRN) complex, are present in the nuclease – and high salt-resistant pellet fraction. Notably, ATM and MRN remain stably associated with these structures throughout the cell cycle, independent of ionizing radiation (IR)-induced DNA damage. Although Lamin A/C interacts with ATM and MRN, its depletion does not disrupt their association with nuclease-resistant structures. However, it impairs the IR-enhanced association of ATM with the nuclear matrix and ATM-mediated DDR signaling, as well as the interaction between ATM and MRN. This disruption impedes the recruitment of MRE11 to damaged DNA and the association of damaged DNA with the nuclear matrix. Additionally, Lamin A/C depletion results in reduced protein levels of CtIP and RAD51, which is mediated by transcriptional regulation. This, in turn, impairs the efficiency of homologous recombination (HR). Our findings indicate that Lamin A/C plays a pivotal role in DNA damage repair (DDR) by orchestrating ATM-mediated signaling, maintaining HR protein levels, and ensuring efficient DNA repair processes.https://www.tandfonline.com/doi/10.1080/19768354.2024.2393820DNA damage response (DDR)Lamin A/CATMMRN complex
spellingShingle Seong-jung Kim
Su Hyung Park
Kyungjae Myung
Kyoo-young Lee
Lamin A/C facilitates DNA damage response by modulating ATM signaling and homologous recombination pathways
Animal Cells and Systems
DNA damage response (DDR)
Lamin A/C
ATM
MRN complex
title Lamin A/C facilitates DNA damage response by modulating ATM signaling and homologous recombination pathways
title_full Lamin A/C facilitates DNA damage response by modulating ATM signaling and homologous recombination pathways
title_fullStr Lamin A/C facilitates DNA damage response by modulating ATM signaling and homologous recombination pathways
title_full_unstemmed Lamin A/C facilitates DNA damage response by modulating ATM signaling and homologous recombination pathways
title_short Lamin A/C facilitates DNA damage response by modulating ATM signaling and homologous recombination pathways
title_sort lamin a c facilitates dna damage response by modulating atm signaling and homologous recombination pathways
topic DNA damage response (DDR)
Lamin A/C
ATM
MRN complex
url https://www.tandfonline.com/doi/10.1080/19768354.2024.2393820
work_keys_str_mv AT seongjungkim laminacfacilitatesdnadamageresponsebymodulatingatmsignalingandhomologousrecombinationpathways
AT suhyungpark laminacfacilitatesdnadamageresponsebymodulatingatmsignalingandhomologousrecombinationpathways
AT kyungjaemyung laminacfacilitatesdnadamageresponsebymodulatingatmsignalingandhomologousrecombinationpathways
AT kyooyounglee laminacfacilitatesdnadamageresponsebymodulatingatmsignalingandhomologousrecombinationpathways