The transcription factor PREP1(PKNOX1) regulates nuclear stiffness, the expression of LINC complex proteins and mechanotransduction

Mechanosignaling, initiated by extracellular forces and propagated through the intracellular cytoskeletal network, triggers signaling cascades employed in processes as embryogenesis, tissue maintenance and disease development. While signal transduction by transcription factors occurs downstream of c...

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Published inCommunications biology Vol. 5; no. 1; pp. 456 - 14
Main Authors Purushothaman, Divya, Bianchi, Laura F., Penkov, Dmitry, Poli, Alessandro, Li, Qingsen, Vermezovic, Jelena, Pramotton, Francesca M., Choudhary, Ramveer, Pennacchio, Fabrizio A., Sommariva, Elena, Foiani, Marco, Gauthier, Nils, Maiuri, Paolo, Blasi, Francesco
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 12.05.2022
Nature Publishing Group
Nature Portfolio
Subjects
14
14/19
14/3
38
38/89
631/80/128/1276
631/80/386/1700
631/80/79/2027
631/80/79/2066
82
96
Actomyosin
Biology
Biomedical and Life Sciences
Cytoskeleton
Embryogenesis
Extracellular matrix
Homeostasis
Intracellular signalling
Life Sciences
Mechanotransduction
Membrane proteins
Nuclei
Signal transduction
Stoichiometry
Transcription factors
Yes-associated protein
Online AccessGet full text
ISSN2399-3642
2399-3642
DOI10.1038/s42003-022-03406-9

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Abstract Mechanosignaling, initiated by extracellular forces and propagated through the intracellular cytoskeletal network, triggers signaling cascades employed in processes as embryogenesis, tissue maintenance and disease development. While signal transduction by transcription factors occurs downstream of cellular mechanosensing, little is known about the cell intrinsic mechanisms that can regulate mechanosignaling. Here we show that transcription factor PREP1 (PKNOX1) regulates the stiffness of the nucleus, the expression of LINC complex proteins and mechanotransduction of YAP-TAZ. PREP1 depletion upsets the nuclear membrane protein stoichiometry and renders nuclei soft. Intriguingly, these cells display fortified actomyosin network with bigger focal adhesion complexes resulting in greater traction forces at the substratum. Despite the high traction, YAP-TAZ translocation is impaired indicating disrupted mechanotransduction. Our data demonstrate mechanosignaling upstream of YAP-TAZ and suggest the existence of a transcriptional mechanism actively regulating nuclear membrane homeostasis and signal transduction through the active engagement/disengagement of the cell from the extracellular matrix. The transcription factor PREP1 binds to promoter regions of SUN1, SUN2 and LAP2 genes and promotes nuclear stiffness, and its depletion results in impaired mechanotransduction.
AbstractList Mechanosignaling, initiated by extracellular forces and propagated through the intracellular cytoskeletal network, triggers signaling cascades employed in processes as embryogenesis, tissue maintenance and disease development. While signal transduction by transcription factors occurs downstream of cellular mechanosensing, little is known about the cell intrinsic mechanisms that can regulate mechanosignaling. Here we show that transcription factor PREP1 (PKNOX1) regulates the stiffness of the nucleus, the expression of LINC complex proteins and mechanotransduction of YAP-TAZ. PREP1 depletion upsets the nuclear membrane protein stoichiometry and renders nuclei soft. Intriguingly, these cells display fortified actomyosin network with bigger focal adhesion complexes resulting in greater traction forces at the substratum. Despite the high traction, YAP-TAZ translocation is impaired indicating disrupted mechanotransduction. Our data demonstrate mechanosignaling upstream of YAP-TAZ and suggest the existence of a transcriptional mechanism actively regulating nuclear membrane homeostasis and signal transduction through the active engagement/disengagement of the cell from the extracellular matrix.Mechanosignaling, initiated by extracellular forces and propagated through the intracellular cytoskeletal network, triggers signaling cascades employed in processes as embryogenesis, tissue maintenance and disease development. While signal transduction by transcription factors occurs downstream of cellular mechanosensing, little is known about the cell intrinsic mechanisms that can regulate mechanosignaling. Here we show that transcription factor PREP1 (PKNOX1) regulates the stiffness of the nucleus, the expression of LINC complex proteins and mechanotransduction of YAP-TAZ. PREP1 depletion upsets the nuclear membrane protein stoichiometry and renders nuclei soft. Intriguingly, these cells display fortified actomyosin network with bigger focal adhesion complexes resulting in greater traction forces at the substratum. Despite the high traction, YAP-TAZ translocation is impaired indicating disrupted mechanotransduction. Our data demonstrate mechanosignaling upstream of YAP-TAZ and suggest the existence of a transcriptional mechanism actively regulating nuclear membrane homeostasis and signal transduction through the active engagement/disengagement of the cell from the extracellular matrix.
Mechanosignaling, initiated by extracellular forces and propagated through the intracellular cytoskeletal network, triggers signaling cascades employed in processes as embryogenesis, tissue maintenance and disease development. While signal transduction by transcription factors occurs downstream of cellular mechanosensing, little is known about the cell intrinsic mechanisms that can regulate mechanosignaling. Here we show that transcription factor PREP1 (PKNOX1) regulates the stiffness of the nucleus, the expression of LINC complex proteins and mechanotransduction of YAP-TAZ. PREP1 depletion upsets the nuclear membrane protein stoichiometry and renders nuclei soft. Intriguingly, these cells display fortified actomyosin network with bigger focal adhesion complexes resulting in greater traction forces at the substratum. Despite the high traction, YAP-TAZ translocation is impaired indicating disrupted mechanotransduction. Our data demonstrate mechanosignaling upstream of YAP-TAZ and suggest the existence of a transcriptional mechanism actively regulating nuclear membrane homeostasis and signal transduction through the active engagement/disengagement of the cell from the extracellular matrix. The transcription factor PREP1 binds to promoter regions of SUN1, SUN2 and LAP2 genes and promotes nuclear stiffness, and its depletion results in impaired mechanotransduction.
Mechanosignaling, initiated by extracellular forces and propagated through the intracellular cytoskeletal network, triggers signaling cascades employed in processes as embryogenesis, tissue maintenance and disease development. While signal transduction by transcription factors occurs downstream of cellular mechanosensing, little is known about the cell intrinsic mechanisms that can regulate mechanosignaling. Here we show that transcription factor PREP1 (PKNOX1) regulates the stiffness of the nucleus, the expression of LINC complex proteins and mechanotransduction of YAP-TAZ. PREP1 depletion upsets the nuclear membrane protein stoichiometry and renders nuclei soft. Intriguingly, these cells display fortified actomyosin network with bigger focal adhesion complexes resulting in greater traction forces at the substratum. Despite the high traction, YAP-TAZ translocation is impaired indicating disrupted mechanotransduction. Our data demonstrate mechanosignaling upstream of YAP-TAZ and suggest the existence of a transcriptional mechanism actively regulating nuclear membrane homeostasis and signal transduction through the active engagement/disengagement of the cell from the extracellular matrix.The transcription factor PREP1 binds to promoter regions of SUN1, SUN2 and LAP2 genes and promotes nuclear stiffness, and its depletion results in impaired mechanotransduction.
Mechanosignaling, initiated by extracellular forces and propagated through the intracellular cytoskeletal network, triggers signaling cascades employed in processes as embryogenesis, tissue maintenance and disease development. While signal transduction by transcription factors occurs downstream of cellular mechanosensing, little is known about the cell intrinsic mechanisms that can regulate mechanosignaling. Here we show that transcription factor PREP1 (PKNOX1) regulates the stiffness of the nucleus, the expression of LINC complex proteins and mechanotransduction of YAP-TAZ. PREP1 depletion upsets the nuclear membrane protein stoichiometry and renders nuclei soft. Intriguingly, these cells display fortified actomyosin network with bigger focal adhesion complexes resulting in greater traction forces at the substratum. Despite the high traction, YAP-TAZ translocation is impaired indicating disrupted mechanotransduction. Our data demonstrate mechanosignaling upstream of YAP-TAZ and suggest the existence of a transcriptional mechanism actively regulating nuclear membrane homeostasis and signal transduction through the active engagement/disengagement of the cell from the extracellular matrix.
The transcription factor PREP1 binds to promoter regions of SUN1, SUN2 and LAP2 genes and promotes nuclear stiffness, and its depletion results in impaired mechanotransduction.
ArticleNumber 456
Author Sommariva, Elena
Purushothaman, Divya
Gauthier, Nils
Li, Qingsen
Foiani, Marco
Bianchi, Laura F.
Penkov, Dmitry
Pramotton, Francesca M.
Pennacchio, Fabrizio A.
Blasi, Francesco
Choudhary, Ramveer
Maiuri, Paolo
Poli, Alessandro
Vermezovic, Jelena
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CitedBy_id crossref_primary_10_1016_j_ceb_2023_102222
crossref_primary_10_1002_1873_3468_14757
crossref_primary_10_1016_j_ceb_2023_102208
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Snippet Mechanosignaling, initiated by extracellular forces and propagated through the intracellular cytoskeletal network, triggers signaling cascades employed in...
The transcription factor PREP1 binds to promoter regions of SUN1, SUN2 and LAP2 genes and promotes nuclear stiffness, and its depletion results in impaired...
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Actomyosin
Biology
Biomedical and Life Sciences
Cytoskeleton
Embryogenesis
Extracellular matrix
Homeostasis
Intracellular signalling
Life Sciences
Mechanotransduction
Membrane proteins
Nuclei
Signal transduction
Stoichiometry
Transcription factors
Yes-associated protein
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Title The transcription factor PREP1(PKNOX1) regulates nuclear stiffness, the expression of LINC complex proteins and mechanotransduction
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Volume 5
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