Cargando…

Transgenic force sensors and software to measure force transmission across the mammalian nuclear envelope in vivo

Nuclear mechanotransduction is a growing field with exciting implications for the regulation of gene expression and cellular function. Mechanical signals may be transduced to the nuclear interior biochemically or physically through connections between the cell surface and chromatin. To define mechan...

Descripción completa

Detalles Bibliográficos
Autores principales: Fenelon, Kelli D., Thomas, Evan, Samani, Mohammad, Zhu, Min, Tao, Hirotaka, Sun, Yu, McNeill, Helen, Hopyan, Sevan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9672859/
https://www.ncbi.nlm.nih.gov/pubmed/36350289
http://dx.doi.org/10.1242/bio.059656
_version_ 1784832834278522880
author Fenelon, Kelli D.
Thomas, Evan
Samani, Mohammad
Zhu, Min
Tao, Hirotaka
Sun, Yu
McNeill, Helen
Hopyan, Sevan
author_facet Fenelon, Kelli D.
Thomas, Evan
Samani, Mohammad
Zhu, Min
Tao, Hirotaka
Sun, Yu
McNeill, Helen
Hopyan, Sevan
author_sort Fenelon, Kelli D.
collection PubMed
description Nuclear mechanotransduction is a growing field with exciting implications for the regulation of gene expression and cellular function. Mechanical signals may be transduced to the nuclear interior biochemically or physically through connections between the cell surface and chromatin. To define mechanical stresses upon the nucleus in physiological settings, we generated transgenic mouse strains that harbour FRET-based tension sensors or control constructs in the outer and inner aspects of the nuclear envelope. We knocked-in a published esprin-2G sensor to measure tensions across the LINC complex and generated a new sensor that links the inner nuclear membrane to chromatin. To mitigate challenges inherent to fluorescence lifetime analysis in vivo, we developed software (FLIMvivo) that markedly improves the fitting of fluorescence decay curves. In the mouse embryo, the sensors responded to cytoskeletal relaxation and stretch applied by micro-aspiration. They reported organ-specific differences and a spatiotemporal tension gradient along the proximodistal axis of the limb bud, raising the possibility that mechanical mechanisms coregulate pattern formation. These mouse strains and software are potentially valuable tools for testing and refining mechanotransduction hypotheses in vivo.
format Online
Article
Text
id pubmed-9672859
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher The Company of Biologists Ltd
record_format MEDLINE/PubMed
spelling pubmed-96728592022-11-18 Transgenic force sensors and software to measure force transmission across the mammalian nuclear envelope in vivo Fenelon, Kelli D. Thomas, Evan Samani, Mohammad Zhu, Min Tao, Hirotaka Sun, Yu McNeill, Helen Hopyan, Sevan Biol Open Methods & Techniques Nuclear mechanotransduction is a growing field with exciting implications for the regulation of gene expression and cellular function. Mechanical signals may be transduced to the nuclear interior biochemically or physically through connections between the cell surface and chromatin. To define mechanical stresses upon the nucleus in physiological settings, we generated transgenic mouse strains that harbour FRET-based tension sensors or control constructs in the outer and inner aspects of the nuclear envelope. We knocked-in a published esprin-2G sensor to measure tensions across the LINC complex and generated a new sensor that links the inner nuclear membrane to chromatin. To mitigate challenges inherent to fluorescence lifetime analysis in vivo, we developed software (FLIMvivo) that markedly improves the fitting of fluorescence decay curves. In the mouse embryo, the sensors responded to cytoskeletal relaxation and stretch applied by micro-aspiration. They reported organ-specific differences and a spatiotemporal tension gradient along the proximodistal axis of the limb bud, raising the possibility that mechanical mechanisms coregulate pattern formation. These mouse strains and software are potentially valuable tools for testing and refining mechanotransduction hypotheses in vivo. The Company of Biologists Ltd 2022-11-09 /pmc/articles/PMC9672859/ /pubmed/36350289 http://dx.doi.org/10.1242/bio.059656 Text en © 2022. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Methods & Techniques
Fenelon, Kelli D.
Thomas, Evan
Samani, Mohammad
Zhu, Min
Tao, Hirotaka
Sun, Yu
McNeill, Helen
Hopyan, Sevan
Transgenic force sensors and software to measure force transmission across the mammalian nuclear envelope in vivo
title Transgenic force sensors and software to measure force transmission across the mammalian nuclear envelope in vivo
title_full Transgenic force sensors and software to measure force transmission across the mammalian nuclear envelope in vivo
title_fullStr Transgenic force sensors and software to measure force transmission across the mammalian nuclear envelope in vivo
title_full_unstemmed Transgenic force sensors and software to measure force transmission across the mammalian nuclear envelope in vivo
title_short Transgenic force sensors and software to measure force transmission across the mammalian nuclear envelope in vivo
title_sort transgenic force sensors and software to measure force transmission across the mammalian nuclear envelope in vivo
topic Methods & Techniques
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9672859/
https://www.ncbi.nlm.nih.gov/pubmed/36350289
http://dx.doi.org/10.1242/bio.059656
work_keys_str_mv AT fenelonkellid transgenicforcesensorsandsoftwaretomeasureforcetransmissionacrossthemammaliannuclearenvelopeinvivo
AT thomasevan transgenicforcesensorsandsoftwaretomeasureforcetransmissionacrossthemammaliannuclearenvelopeinvivo
AT samanimohammad transgenicforcesensorsandsoftwaretomeasureforcetransmissionacrossthemammaliannuclearenvelopeinvivo
AT zhumin transgenicforcesensorsandsoftwaretomeasureforcetransmissionacrossthemammaliannuclearenvelopeinvivo
AT taohirotaka transgenicforcesensorsandsoftwaretomeasureforcetransmissionacrossthemammaliannuclearenvelopeinvivo
AT sunyu transgenicforcesensorsandsoftwaretomeasureforcetransmissionacrossthemammaliannuclearenvelopeinvivo
AT mcneillhelen transgenicforcesensorsandsoftwaretomeasureforcetransmissionacrossthemammaliannuclearenvelopeinvivo
AT hopyansevan transgenicforcesensorsandsoftwaretomeasureforcetransmissionacrossthemammaliannuclearenvelopeinvivo