An ensemble of flexible conformations underlies mechanotransduction by the cadherin–catenin adhesion complex

Bush, Martin; Alhanshali, Bashir M.; Qian, Shuo; Stanley, Christopher B.; Heller, William T.; Matsui, Tsutomu; Weiss, Thomas M.; Nicholl, Iain D.; Walz, Thomas; Callaway, David J.  E.; Bu, Zimei

doi:10.1073/pnas.1911489116

An ensemble of flexible conformations underlies mechanotransduction by the cadherin–catenin adhesion complex

Journal Article · Mon Oct 07 00:00:00 EDT 2019 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1911489116· OSTI ID:1625048

Bush, Martin ^[1]; Alhanshali, Bashir M. ^[2]; ^[3]; Stanley, Christopher B. ^[3]; ^[3]; Matsui, Tsutomu ^[4]; Weiss, Thomas M. ^[4]; Nicholl, Iain D. ^[5]; Walz, Thomas ^[6]; Callaway, David J. E. ^[7]; Bu, Zimei ^[2]

Rockefeller Univ., New York, NY (United States). Lab. of Molecular Electron Microscopy; DOE/OSTI
City College of New York, NY (United States); City Univ. of New York (CUNY), NY (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
Univ. of Wolverhampton (United Kingdom)
Rockefeller Univ., New York, NY (United States). Lab. of Molecular Electron Microscopy
City College of New York, NY (United States)

The cadherin–catenin adhesion complex is the central component of the cell–cell adhesion adherens junctions that transmit mechanical stress from cell to cell. We have determined the nanoscale structure of the adherens junction complex formed by the α-catenin•β-catenin•epithelial cadherin cytoplasmic domain (ABE) using negative stain electron microscopy, small-angle X-ray scattering, and selective deuteration/small-angle neutron scattering. The ABE complex is highly pliable and displays a wide spectrum of flexible structures that are facilitated by protein-domain motions in α- and β-catenin. Moreover, the 107-residue intrinsically disordered N-terminal segment of β-catenin forms a flexible “tongue” that is inserted into α-catenin and participates in the assembly of the ABE complex. The unanticipated ensemble of flexible conformations of the ABE complex suggests a dynamic mechanism for sensitivity and reversibility when transducing mechanical signals, in addition to the catch/slip bond behavior displayed by the ABE complex under mechanical tension. Our results provide mechanistic insight into the structural dynamics for the cadherin–catenin adhesion complex in mechanotransduction.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)

Sponsoring Organization:: National Center for Research Resources; National Institutes of Health (NIH); National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1625048

Alternate ID(s):: OSTI ID: 1761767

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 43 Vol. 116; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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An ensemble of flexible conformations underlies mechanotransduction by the cadherin–catenin adhesion complex

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