Microtubule Assists Actomyosin to Regulate Cell Nuclear Mechanics and Chromatin Accessibility

Cellular behaviors and functions can be regulated by mechanical cues from microenvironments, which are transmitted to nucleus through the physical connections of cytoskeletons in the cells. How these physical connections determine transcriptional activity were not clearly known. The actomyosin, whic...

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Main Authors: Jiwen Geng, Zhefeng Kang, Qian Sun, Man Zhang, Peng Wang, Yupei Li, Jiameng Li, Baihai Su, Qiang Wei
Format: Article
Language:English
Published: American Association for the Advancement of Science (AAAS) 2023-01-01
Series:Research
Online Access:https://spj.science.org/doi/10.34133/research.0054
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author Jiwen Geng
Zhefeng Kang
Qian Sun
Man Zhang
Peng Wang
Yupei Li
Jiameng Li
Baihai Su
Qiang Wei
author_facet Jiwen Geng
Zhefeng Kang
Qian Sun
Man Zhang
Peng Wang
Yupei Li
Jiameng Li
Baihai Su
Qiang Wei
author_sort Jiwen Geng
collection DOAJ
description Cellular behaviors and functions can be regulated by mechanical cues from microenvironments, which are transmitted to nucleus through the physical connections of cytoskeletons in the cells. How these physical connections determine transcriptional activity were not clearly known. The actomyosin, which generates intracellular traction force, has been recognized to control the nuclear morphology. Here, we have revealed that microtubule, the stiffest cytoskeleton, is also involved in the process of nuclear morphology alteration. The microtubule negatively regulates the actomyosin-induced nuclear invaginations but not the nuclear wrinkles. Moreover, these nuclear shape changes are proven to mediate the chromatin remodeling, which essentially mediates cell gene expression and phenotype determination. The actomyosin disruption leads to the loss of chromatin accessibility, which can be partly recovered by microtubule interference through nuclear shape control. This finding answers the question of how mechanical cues regulate chromatin accessibility and cell behaviors. It also provides new insights into cell mechanotransduction and nuclear mechanics.
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spelling doaj.art-27a725c0c61e4a2cab1fe1717294151f2024-04-02T21:01:31ZengAmerican Association for the Advancement of Science (AAAS)Research2639-52742023-01-01610.34133/research.0054Microtubule Assists Actomyosin to Regulate Cell Nuclear Mechanics and Chromatin AccessibilityJiwen Geng0Zhefeng Kang1Qian Sun2Man Zhang3Peng Wang4Yupei Li5Jiameng Li6Baihai Su7Qiang Wei8Department of Nephrology, West China Hospital, Sichuan University, Chengdu, 610041, China.Department of Cardiovascular Surgery, West China Hospital, Sichuan University, Chengdu, 610041, China.College of Polymer Science and Engineering, College of Biomedical Engineering, State Key Laboratory of Polymer Materials and Engineering Sichuan University, Chengdu, 610065, China.College of Polymer Science and Engineering, College of Biomedical Engineering, State Key Laboratory of Polymer Materials and Engineering Sichuan University, Chengdu, 610065, China.College of Polymer Science and Engineering, College of Biomedical Engineering, State Key Laboratory of Polymer Materials and Engineering Sichuan University, Chengdu, 610065, China.Department of Nephrology, West China Hospital, Sichuan University, Chengdu, 610041, China.Department of Nephrology, West China Hospital, Sichuan University, Chengdu, 610041, China.Department of Nephrology, West China Hospital, Sichuan University, Chengdu, 610041, China.College of Polymer Science and Engineering, College of Biomedical Engineering, State Key Laboratory of Polymer Materials and Engineering Sichuan University, Chengdu, 610065, China.Cellular behaviors and functions can be regulated by mechanical cues from microenvironments, which are transmitted to nucleus through the physical connections of cytoskeletons in the cells. How these physical connections determine transcriptional activity were not clearly known. The actomyosin, which generates intracellular traction force, has been recognized to control the nuclear morphology. Here, we have revealed that microtubule, the stiffest cytoskeleton, is also involved in the process of nuclear morphology alteration. The microtubule negatively regulates the actomyosin-induced nuclear invaginations but not the nuclear wrinkles. Moreover, these nuclear shape changes are proven to mediate the chromatin remodeling, which essentially mediates cell gene expression and phenotype determination. The actomyosin disruption leads to the loss of chromatin accessibility, which can be partly recovered by microtubule interference through nuclear shape control. This finding answers the question of how mechanical cues regulate chromatin accessibility and cell behaviors. It also provides new insights into cell mechanotransduction and nuclear mechanics.https://spj.science.org/doi/10.34133/research.0054
spellingShingle Jiwen Geng
Zhefeng Kang
Qian Sun
Man Zhang
Peng Wang
Yupei Li
Jiameng Li
Baihai Su
Qiang Wei
Microtubule Assists Actomyosin to Regulate Cell Nuclear Mechanics and Chromatin Accessibility
Research
title Microtubule Assists Actomyosin to Regulate Cell Nuclear Mechanics and Chromatin Accessibility
title_full Microtubule Assists Actomyosin to Regulate Cell Nuclear Mechanics and Chromatin Accessibility
title_fullStr Microtubule Assists Actomyosin to Regulate Cell Nuclear Mechanics and Chromatin Accessibility
title_full_unstemmed Microtubule Assists Actomyosin to Regulate Cell Nuclear Mechanics and Chromatin Accessibility
title_short Microtubule Assists Actomyosin to Regulate Cell Nuclear Mechanics and Chromatin Accessibility
title_sort microtubule assists actomyosin to regulate cell nuclear mechanics and chromatin accessibility
url https://spj.science.org/doi/10.34133/research.0054
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