Flow-induced mechanical coupling between perinuclear actin cap and nucleus governs spatiotemporal regulation of YAP transport Article Swipe

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Tianxiang Ma , Xiao Liu , Haoran Su , Yuan He , Fan Wu , Chenxing Gao , Kexin Li , Zhuqing Liang , Dongrui Zhang , Xing Zhang , Ke Hu , Shangyu Li , Wang Li , Min Wang , Shuhua Yue , Weili Hong , Xun Chen , Jing Zhang , Xiaoyan Deng , Pu Wang , Yubo Fan ·

YOU? · · 2022 · Open Access · · DOI: https://doi.org/10.1101/2022.11.15.516697

Mechanical forces, including flow shear stress, regulate fundamental cellular process by modulating the nucleocytoplasmic transport of transcription factors, such as Yes-associated Protein (YAP). However, the mechanical mechanism how flow induces the nucleocytoplasmic transport remains largely unclear. Here we found that unidirectional flow applied to endothelial cells induces biphasic YAP nucleocytoplasmic transport with initial nuclear import, followed by nuclear export as perinuclear actin cap forms and nuclear stiffening in a dose and timing-dependent manner. In contrast, pathological oscillatory flow induces slight actin cap formation and nuclear softening, sustaining YAP nuclear localization. To explain the disparately spatiotemporal distribution of YAP, we developed a three-dimensional mechanochemical model considering coupling processes of flow sensing, cytoskeleton organization, nucleus mechanotransduction, and YAP spatiotemporal transport. We discovered that actin cap formation and nuclear stiffness alteration under flow synergically regulate nuclear deformation, hence governing YAP transport. Furthermore, we expanded our single cell model to a collective vertex framework and found that actin cap irregularities in individual cells under flow shear stress potentially induce topological defects and spatially heterogeneous YAP distribution in cellular monolayers. Our work unveils the unified mechanism of flow-induced nucleocytoplasmic transport, offering a universal linkage between transcriptional regulation and mechanical stimulation.

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Mechanotransduction Nuclear transport Cell biology Actin Cytoskeleton Cytoplasm Nucleus Actin cytoskeleton Cell nucleus Biophysics Biology Chemistry Cell Genetics

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Type: preprint
Language: en
Landing Page: https://doi.org/10.1101/2022.11.15.516697
PDF: https://www.biorxiv.org/content/biorxiv/early/2023/05/03/2022.11.15.516697.full.pdf
OA Status: green
References: 52
Related Works: 10
OpenAlex ID: https://openalex.org/W4309263971

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DOI: https://doi.org/10.1101/2022.11.15.516697

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Title: Flow-induced mechanical coupling between perinuclear actin cap and nucleus governs spatiotemporal regulation of YAP transport

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Type: preprint

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Language: en

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Publication year: 2022

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Publication date: 2022-11-17

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Authors: Tianxiang Ma, Xiao Liu, Haoran Su, Yuan He, Fan Wu, Chenxing Gao, Kexin Li, Zhuqing Liang, Dongrui Zhang, Xing Zhang, Ke Hu, Shangyu Li, Wang Li, Min Wang, Shuhua Yue, Weili Hong, Xun Chen, Jing Zhang, Xiaoyan Deng, Pu Wang, Yubo Fan

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Landing page: https://doi.org/10.1101/2022.11.15.516697

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PDF URL: https://www.biorxiv.org/content/biorxiv/early/2023/05/03/2022.11.15.516697.full.pdf

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OA URL: https://www.biorxiv.org/content/biorxiv/early/2023/05/03/2022.11.15.516697.full.pdf

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Concepts: Mechanotransduction, Nuclear transport, Cell biology, Actin, Cytoskeleton, Cytoplasm, Nucleus, Actin cytoskeleton, Cell nucleus, Biophysics, Biology, Chemistry, Cell, Genetics

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Cited by: 0

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abstract_inverted_index.irregularities	156
abstract_inverted_index.spatiotemporal	95, 117
abstract_inverted_index.unidirectional	41
abstract_inverted_index.mechanochemical	103
abstract_inverted_index.transcriptional	191
abstract_inverted_index.timing-dependent	72
abstract_inverted_index.nucleocytoplasmic	14, 32, 50, 184
abstract_inverted_index.three-dimensional	102
abstract_inverted_index.mechanotransduction,	114
cited_by_percentile_year
corresponding_author_ids	https://openalex.org/A5066943052, https://openalex.org/A5100441036, https://openalex.org/A5100383529
countries_distinct_count	1
institutions_distinct_count	21
corresponding_institution_ids	https://openalex.org/I82880672
citation_normalized_percentile.value	0.16557119
citation_normalized_percentile.is_in_top_1_percent	False
citation_normalized_percentile.is_in_top_10_percent	False