Mechanism of the cadherin–catenin F-actin catch bond interaction

Wang, Amy; Dunn, Alexander R.; Weis, William I.

doi:10.7554/elife.80130

Mechanism of the cadherin–catenin F-actin catch bond interaction

Journal Article · Mon Aug 01 00:00:00 EDT 2022 · eLife

DOI:https://doi.org/10.7554/elife.80130· OSTI ID:1983349

^[1]; ^[1]; ^[1]

Stanford Univ., CA (United States)

Mechanotransduction at cell–cell adhesions is crucial for the structural integrity, organization, and morphogenesis of epithelia. At cell–cell junctions, ternary E-cadherin/β-catenin/αE-catenin complexes sense and transmit mechanical load by binding to F-actin. The interaction with F-actin, described as a two-state catch bond, is weak in solution but is strengthened by applied force due to force-dependent transitions between weak and strong actin-binding states. Here, we provide direct evidence from optical trapping experiments that the catch bond property principally resides in the αE-catenin actin-binding domain (ABD). Consistent with our previously proposed model, the deletion of the first helix of the five-helix ABD bundle enables stable interactions with F-actin under minimal load that are well described by a single-state slip bond, even when αE-catenin is complexed with β-catenin and E-cadherin. Our data argue for a conserved catch bond mechanism for adhesion proteins with structurally similar ABDs. We also demonstrate that a stably bound ABD strengthens load-dependent binding interactions between a neighboring complex and F-actin, but the presence of the other αE-catenin domains weakens this effect. These results provide mechanistic insight to the cooperative binding of the cadherin–catenin complex to F-actin, which regulate dynamic cytoskeletal linkages in epithelial tissues.

View Accepted Manuscript (DOE)

Research Organization:: SLAC National Accelerator Laboratory, Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)

Sponsoring Organization:: National Institutes of Health (NIH); National Science Foundation (NSF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1983349

Journal Information:: eLife, Journal Name: eLife Vol. 11; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

References (49)

UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
Adherens Junctions and Cancer Vasioukhin, Valeri Subcellular Biochemistry https://doi.org/10.1007/978-94-007-4186-7_16	book	January 2012
Dynamic strength of molecular adhesion bonds Evans, E.; Ritchie, K. Biophysical Journal, Vol. 72, Issue 4 https://doi.org/10.1016/S0006-3495(97)78802-7	journal	April 1997
α-Catenin Structure and Nanoscale Dynamics in Solution and in Complex with F-Actin Nicholl, Iain D.; Matsui, Tsutomu; Weiss, Thomas M. Biophysical Journal, Vol. 115, Issue 4 https://doi.org/10.1016/j.bpj.2018.07.005	journal	August 2018
Deconstructing the Cadherin-Catenin-Actin Complex Yamada, Soichiro; Pokutta, Sabine; Drees, Frauke Cell, Vol. 123, Issue 5 https://doi.org/10.1016/j.cell.2005.09.020	journal	December 2005
α-Catenin Is a Molecular Switch that Binds E-Cadherin-β-Catenin and Regulates Actin-Filament Assembly Drees, Frauke; Pokutta, Sabine; Yamada, Soichiro Cell, Vol. 123, Issue 5 https://doi.org/10.1016/j.cell.2005.09.021	journal	December 2005
Mechanical regulation of tension-transmission supramolecular linkages Le, Shimin; Yu, Miao; Yan, Jie Current Opinion in Solid State and Materials Science, Vol. 25, Issue 1 https://doi.org/10.1016/j.cossms.2020.100895	journal	February 2021
tweezercalib 2.1: Faster version of MatLab package for precise calibration of optical tweezers Hansen, Poul Martin; Tolic-Nørrelykke, Iva Marija; Flyvbjerg, Henrik Computer Physics Communications, Vol. 175, Issue 8 https://doi.org/10.1016/j.cpc.2006.07.009	journal	October 2006
Tensile Forces and Mechanotransduction at Cell–Cell Junctions Charras, Guillaume; Yap, Alpha S. Current Biology, Vol. 28, Issue 8 https://doi.org/10.1016/j.cub.2018.02.003	journal	April 2018
Actin-based force generation and cell adhesion in tissue morphogenesis Clarke, D. Nathaniel; Martin, Adam C. Current Biology, Vol. 31, Issue 10 https://doi.org/10.1016/j.cub.2021.03.031	journal	May 2021
The Structural Basis of Actin Organization by Vinculin and Metavinculin Kim, Laura Y.; Thompson, Peter M.; Lee, Hyunna T. Journal of Molecular Biology, Vol. 428, Issue 1 https://doi.org/10.1016/j.jmb.2015.09.031	journal	January 2016
Phenomenological and microscopic theories for catch bonds Chakrabarti, Shaon; Hinczewski, Michael; Thirumalai, D. Journal of Structural Biology, Vol. 197, Issue 1 https://doi.org/10.1016/j.jsb.2016.03.022	journal	January 2017
Structure of the Dimerization and β-Catenin- Binding Region of α-Catenin Pokutta, Sabine; Weis, William I. Molecular Cell, Vol. 5, Issue 3 https://doi.org/10.1016/s1097-2765(00)80447-5	journal	March 2000
Intrasteric Inhibition Mediates the Interaction of the I/LWEQ Module Proteins Talin1, Talin2, Hip1, and Hip12 with Actin Senetar, Melissa A.; Foster, Stanley J.; McCann, Richard O. Biochemistry, Vol. 43, Issue 49 https://doi.org/10.1021/bi0487239	journal	November 2004
Genome remodelling in a basal-like breast cancer metastasis and xenograft Ding, Li; Ellis, Matthew J.; Li, Shunqiang Nature, Vol. 464, Issue 7291 https://doi.org/10.1038/nature08989	journal	April 2010
α-Catenin as a tension transducer that induces adherens junction development Yonemura, Shigenobu; Wada, Yuko; Watanabe, Toshiyuki Nature Cell Biology, Vol. 12, Issue 6 https://doi.org/10.1038/ncb2055	journal	May 2010
Monomeric α-catenin links cadherin to the actin cytoskeleton Desai, Ridhdhi; Sarpal, Ritu; Ishiyama, Noboru Nature Cell Biology, Vol. 15, Issue 3 https://doi.org/10.1038/ncb2685	journal	February 2013
Force-dependent conformational switch of α-catenin controls vinculin binding Yao, Mingxi; Qiu, Wu; Liu, Ruchuan Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5525	journal	July 2014
Mechanobiology of collective cell behaviours Ladoux, Benoit; Mège, René-Marc Nature Reviews Molecular Cell Biology, Vol. 18, Issue 12 https://doi.org/10.1038/nrm.2017.98	journal	November 2017
Dimer asymmetry defines α-catenin interactions Rangarajan, Erumbi S.; Izard, Tina Nature Structural & Molecular Biology, Vol. 20, Issue 2 https://doi.org/10.1038/nsmb.2479	journal	January 2013
Structural definition of the F-actin–binding THATCH domain from HIP1R Brett, Tom J.; Legendre-Guillemin, Valerie; McPherson, Peter S. Nature Structural & Molecular Biology, Vol. 13, Issue 2 https://doi.org/10.1038/nsmb1043	journal	January 2006
Force-dependent allostery of the α-catenin actin-binding domain controls adherens junction dynamics and functions Ishiyama, Noboru; Sarpal, Ritu; Wood, Megan N. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07481-7	journal	November 2018
α-catenin switches between a slip and an asymmetric catch bond with F-actin to cooperatively regulate cell junction fluidity Arbore, C.; Sergides, M.; Gardini, L. Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-28779-7	journal	March 2022
Binding partner- and force-promoted changes in αE-catenin conformation probed by native cysteine labeling Terekhova, Ksenia; Pokutta, Sabine; Kee, Yee S. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-51816-3	journal	October 2019
The structure of the C-terminal actin-binding domain of talin Gingras, Alexandre R.; Bate, Neil; Goult, Benjamin T. The EMBO Journal, Vol. 27, Issue 2 https://doi.org/10.1038/sj.emboj.7601965	journal	December 2007
Mechano-adaptive sensory mechanism of α-catenin under tension Maki, Koichiro; Han, Sung-Woong; Hirano, Yoshinori Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep24878	journal	April 2016
Power spectrum analysis for optical tweezers Berg-Sørensen, Kirstine; Flyvbjerg, Henrik Review of Scientific Instruments, Vol. 75, Issue 3 https://doi.org/10.1063/1.1645654	journal	March 2004
Dynamics of unbinding of cell adhesion molecules: Transition from catch to slip bonds Barsegov, V.; Thirumalai, D. Proceedings of the National Academy of Sciences, Vol. 102, Issue 6 https://doi.org/10.1073/pnas.0406938102	journal	February 2005
E-catenin is an autoinhibited molecule that coactivates vinculin Choi, H. -J.; Pokutta, S.; Cadwell, G. W. Proceedings of the National Academy of Sciences, Vol. 109, Issue 22 https://doi.org/10.1073/pnas.1203906109	journal	May 2012
The C-terminal actin-binding domain of talin forms an asymmetric catch bond with F-actin Owen, Leanna M.; Bax, Nicolas A.; Weis, William I. Proceedings of the National Academy of Sciences, Vol. 119, Issue 10 https://doi.org/10.1073/pnas.2109329119	journal	March 2022
Alpha 1(E)-catenin is an actin-binding and -bundling protein mediating the attachment of F-actin to the membrane adhesion complex. Rimm, D. L.; Koslov, E. R.; Kebriaei, P. Proceedings of the National Academy of Sciences, Vol. 92, Issue 19 https://doi.org/10.1073/pnas.92.19.8813	journal	September 1995
An Autoinhibited Structure of α-Catenin and Its Implications for Vinculin Recruitment to Adherens Junctions Ishiyama, Noboru; Tanaka, Nobutoshi; Abe, Kentaro Journal of Biological Chemistry, Vol. 288, Issue 22 https://doi.org/10.1074/jbc.M113.453928	journal	April 2013
Danio rerio αE-catenin Is a Monomeric F-actin Binding Protein with Distinct Properties from Mus musculus αE-catenin Miller, Phillip W.; Pokutta, Sabine; Ghosh, Agnidipta Journal of Biological Chemistry, Vol. 288, Issue 31 https://doi.org/10.1074/jbc.M113.458406	journal	June 2013
Structural and Thermodynamic Characterization of Cadherin·β-Catenin·α-Catenin Complex Formation Pokutta, Sabine; Choi, Hee-Jung; Ahlsen, Goran Journal of Biological Chemistry, Vol. 289, Issue 19 https://doi.org/10.1074/jbc.M114.554709	journal	April 2014
Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II–dependent manner le Duc, Quint; Shi, Quanming; Blonk, Iris The Journal of Cell Biology, Vol. 189, Issue 7 https://doi.org/10.1083/jcb.201001149	journal	June 2010
αE-catenin actin-binding domain alters actin filament conformation and regulates binding of nucleation and disassembly factors Hansen, Scott D.; Kwiatkowski, Adam V.; Ouyang, Chung-Yueh Molecular Biology of the Cell, Vol. 24, Issue 23 https://doi.org/10.1091/mbc.E13-07-0388	journal	December 2013
Vinculin regulates directionality and cell polarity in two- and three-dimensional matrix and three-dimensional microtrack migration Rahman, Aniqua; Carey, Shawn P.; Kraning-Rush, Casey M. Molecular Biology of the Cell, Vol. 27, Issue 9 https://doi.org/10.1091/mbc.E15-06-0432	journal	May 2016
Adherens Junction: Molecular Architecture and Regulation Meng, W.; Takeichi, M. Cold Spring Harbor Perspectives in Biology, Vol. 1, Issue 6 https://doi.org/10.1101/cshperspect.a002899	journal	August 2009
Structure and Biochemistry of Cadherins and Catenins Shapiro, L.; Weis, W. I. Cold Spring Harbor Perspectives in Biology, Vol. 1, Issue 3 https://doi.org/10.1101/cshperspect.a003053	journal	August 2009
Actin and Actin-Binding Proteins Pollard, Thomas D. Cold Spring Harbor Perspectives in Biology, Vol. 8, Issue 8 https://doi.org/10.1101/cshperspect.a018226	journal	March 2016
The Actin Cytoskeleton and Actin-Based Motility Svitkina, Tatyana Cold Spring Harbor Perspectives in Biology, Vol. 10, Issue 1 https://doi.org/10.1101/cshperspect.a018267	journal	January 2018
A new look at the statistical model identification Akaike, H. IEEE Transactions on Automatic Control, Vol. 19, Issue 6 https://doi.org/10.1109/TAC.1974.1100705	journal	December 1974
The minimal cadherin-catenin complex binds to actin filaments under force Buckley, C. D.; Tan, J.; Anderson, K. L. Science, Vol. 346, Issue 6209 https://doi.org/10.1126/science.1254211	journal	October 2014
Models for the specific adhesion of cells to cells Bell, G. Science, Vol. 200, Issue 4342 https://doi.org/10.1126/science.347575	journal	May 1978
Vinculin forms a directionally asymmetric catch bond with F-actin Huang, Derek L.; Bax, Nicolas A.; Buckley, Craig D. Science, Vol. 357, Issue 6352 https://doi.org/10.1126/science.aan2556	journal	August 2017
Estimating the Dimension of a Model Schwarz, Gideon The Annals of Statistics, Vol. 6, Issue 2 https://doi.org/10.1214/aos/1176344136	journal	March 1978
Catch-Bond Model Derived from Allostery Explains Force-Activated Bacterial Adhesion Thomas, Wendy; Forero, Manu; Yakovenko, Olga Biophysical Journal, Vol. 90, Issue 3 https://doi.org/10.1529/biophysj.105.066548	journal	February 2006
Structural basis of αE-catenin–F-actin catch bond behavior Xu, Xiao-Ping; Pokutta, Sabine; Torres, Megan eLife, Vol. 9 https://doi.org/10.7554/eLife.60878	journal	September 2020
Molecular mechanism for direct actin force-sensing by α-catenin Mei, Lin; Espinosa de los Reyes, Santiago; Reynolds, Matthew J. eLife, Vol. 9 https://doi.org/10.7554/eLife.62514	journal	September 2020

Similar Records

αE-catenin actin-binding domain alters actin filament conformation and regulates binding of nucleation and disassembly factors

Journal Article · Tue Sep 24 20:00:00 EDT 2013 · Molecular Biology of the Cell · OSTI ID:1625233

Multi-level Force-dependent Allosteric Enhancement of αE-catenin Binding to F-actin by Vinculin

Journal Article · Thu Jan 19 19:00:00 EST 2023 · Journal of Molecular Biology · OSTI ID:1989198

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
actin
cadherin
cell adhesion
molecular biophysics
optical trap
structural biology
α-catenin
β-catenin

Mechanism of the cadherin–catenin F-actin catch bond interaction

Citation Formats

References (49)

Similar Records

Related Subjects