Cingulin and paracingulin tether myosins-2 to junctions to mechanoregulate the plasma membrane

The mechanisms that regulate the spatial sorting of nonmuscle myosins-2 (NM2) isoforms and couple them mechanically to the plasma membrane are unclear. Here we show that the cytoplasmic junctional proteins cingulin (CGN) and paracingulin (CGNL1) interact directly with NM2s through their C-terminal c...

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Published inThe Journal of cell biology Vol. 222; no. 7; p. 1
Main Authors Rouaud, Florian, Huang, Wenmao, Flinois, Arielle, Jain, Kunalika, Vasileva, Ekaterina, Di Mattia, Thomas, Mauperin, Marine, Parry, David A D, Dugina, Vera, Chaponnier, Christine, Méan, Isabelle, Montessuit, Sylvie, Mutero-Maeda, Annick, Yan, Jie, Citi, Sandra
Format Journal Article
LanguageEnglish
Published United States Rockefeller University Press 03.07.2023
Subjects
Accumulation
Actin
Actomyosin
Adherens Junctions - metabolism
Binding
Biophysics
Cell Membrane - metabolism
Cytoskeletal Proteins - metabolism
Cytoskeleton
Cytoskeleton - metabolism
Filaments
Isoforms
Localization
Membranes
Myosin
Myosins - metabolism
Phalloidin
Proteins
Stiffness
Tight Junctions - metabolism
Tortuosity
Zonula occludens-1 protein
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Abstract The mechanisms that regulate the spatial sorting of nonmuscle myosins-2 (NM2) isoforms and couple them mechanically to the plasma membrane are unclear. Here we show that the cytoplasmic junctional proteins cingulin (CGN) and paracingulin (CGNL1) interact directly with NM2s through their C-terminal coiled-coil sequences. CGN binds strongly to NM2B, and CGNL1 to NM2A and NM2B. Knockout (KO), exogenous expression, and rescue experiments with WT and mutant proteins show that the NM2-binding region of CGN is required for the junctional accumulation of NM2B, ZO-1, ZO-3, and phalloidin-labeled actin filaments, and for the maintenance of tight junction membrane tortuosity and apical membrane stiffness. CGNL1 expression promotes the junctional accumulation of both NM2A and NM2B and its KO results in myosin-dependent fragmentation of adherens junction complexes. These results reveal a mechanism for the junctional localization of NM2A and NM2B and indicate that, by binding to NM2s, CGN and CGNL1 mechanically couple the actomyosin cytoskeleton to junctional protein complexes to mechanoregulate the plasma membrane.
AbstractList The mechanisms that regulate the spatial sorting of nonmuscle myosins-2 (NM2) isoforms and couple them mechanically to the plasma membrane are unclear. Here we show that the cytoplasmic junctional proteins cingulin (CGN) and paracingulin (CGNL1) interact directly with NM2s through their C-terminal coiled-coil sequences. CGN binds strongly to NM2B, and CGNL1 to NM2A and NM2B. Knockout (KO), exogenous expression, and rescue experiments with WT and mutant proteins show that the NM2-binding region of CGN is required for the junctional accumulation of NM2B, ZO-1, ZO-3, and phalloidin-labeled actin filaments, and for the maintenance of tight junction membrane tortuosity and apical membrane stiffness. CGNL1 expression promotes the junctional accumulation of both NM2A and NM2B and its KO results in myosin-dependent fragmentation of adherens junction complexes. These results reveal a mechanism for the junctional localization of NM2A and NM2B and indicate that, by binding to NM2s, CGN and CGNL1 mechanically couple the actomyosin cytoskeleton to junctional protein complexes to mechanoregulate the plasma membrane.
Rouaud et al. show that cingulin and paracingulin bind to specific myosin-2 isoforms through coiled-coil rod-mediated interactions and tether them to junctions to transmit force and modulate ZO-1 junctional accumulation, tight junction membrane tortuosity, apical membrane stiffness, and junctional architecture. The mechanisms that regulate the spatial sorting of nonmuscle myosins-2 (NM2) isoforms and couple them mechanically to the plasma membrane are unclear. Here we show that the cytoplasmic junctional proteins cingulin (CGN) and paracingulin (CGNL1) interact directly with NM2s through their C-terminal coiled-coil sequences. CGN binds strongly to NM2B, and CGNL1 to NM2A and NM2B. Knockout (KO), exogenous expression, and rescue experiments with WT and mutant proteins show that the NM2-binding region of CGN is required for the junctional accumulation of NM2B, ZO-1, ZO-3, and phalloidin-labeled actin filaments, and for the maintenance of tight junction membrane tortuosity and apical membrane stiffness. CGNL1 expression promotes the junctional accumulation of both NM2A and NM2B and its KO results in myosin-dependent fragmentation of adherens junction complexes. These results reveal a mechanism for the junctional localization of NM2A and NM2B and indicate that, by binding to NM2s, CGN and CGNL1 mechanically couple the actomyosin cytoskeleton to junctional protein complexes to mechanoregulate the plasma membrane.
Author Jain, Kunalika
Huang, Wenmao
Mauperin, Marine
Mutero-Maeda, Annick
Dugina, Vera
Citi, Sandra
Montessuit, Sylvie
Flinois, Arielle
Vasileva, Ekaterina
Rouaud, Florian
Di Mattia, Thomas
Parry, David A D
Yan, Jie
Chaponnier, Christine
Méan, Isabelle
AuthorAffiliation 2 Department of Physics, https://ror.org/01tgyzw49 National University of Singapore , Singapore, Singapore
5 Belozersky Institute of Physico-Chemical Biology, Moscow State University , Moscow, Russia
1 Department of Molecular and Cellular Biology, https://ror.org/01swzsf04 Faculty of Sciences, University of Geneva , Geneva, Switzerland
4 https://ror.org/052czxv31 School of Natural Sciences, Massey University , Palmerston North, New Zealand
3 https://ror.org/01tgyzw49 Mechanobiology Institute, National University of Singapore , Singapore, Singapore
6 Department of Pathology and Immunology, https://ror.org/01swzsf04 Faculty of Medicine, University of Geneva , Geneva, Switzerland
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Snippet The mechanisms that regulate the spatial sorting of nonmuscle myosins-2 (NM2) isoforms and couple them mechanically to the plasma membrane are unclear. Here we...
Rouaud et al. show that cingulin and paracingulin bind to specific myosin-2 isoforms through coiled-coil rod-mediated interactions and tether them to junctions...
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SubjectTerms Accumulation
Actin
Actomyosin
Adherens Junctions - metabolism
Binding
Biophysics
Cell Membrane - metabolism
Cytoskeletal Proteins - metabolism
Cytoskeleton
Cytoskeleton - metabolism
Filaments
Isoforms
Localization
Membranes
Myosin
Myosins - metabolism
Phalloidin
Proteins
Stiffness
Tight Junctions - metabolism
Tortuosity
Zonula occludens-1 protein
Title Cingulin and paracingulin tether myosins-2 to junctions to mechanoregulate the plasma membrane
URI https://www.ncbi.nlm.nih.gov/pubmed/37204781
https://www.proquest.com/docview/2834276275
https://search.proquest.com/docview/2816762642
https://pubmed.ncbi.nlm.nih.gov/PMC10202830
Volume 222
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