Nonlinear mechanics of lamin filaments and the meshwork topology build an emergent nuclear lamina

K. Tanuj Sapra (), Zhao Qin, Anna Dubrovsky-Gaupp, Ueli Aebi, Daniel J. Müller, Markus J. Buehler and Ohad Medalia ()
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K. Tanuj Sapra: University of Zurich
Zhao Qin: Massachusetts Institute of Technology
Anna Dubrovsky-Gaupp: University of Zurich
Ueli Aebi: University of Basel
Daniel J. Müller: ETH Zurich
Markus J. Buehler: Massachusetts Institute of Technology
Ohad Medalia: University of Zurich

Nature Communications, 2020, vol. 11, issue 1, 1-14

Abstract: Abstract The nuclear lamina—a meshwork of intermediate filaments termed lamins—is primarily responsible for the mechanical stability of the nucleus in multicellular organisms. However, structural-mechanical characterization of lamin filaments assembled in situ remains elusive. Here, we apply an integrative approach combining atomic force microscopy, cryo-electron tomography, network analysis, and molecular dynamics simulations to directly measure the mechanical response of single lamin filaments in three-dimensional meshwork. Endogenous lamin filaments portray non-Hookean behavior – they deform reversibly at a few hundred picoNewtons and stiffen at nanoNewton forces. The filaments are extensible, strong and tough similar to natural silk and superior to the synthetic polymer Kevlar®. Graph theory analysis shows that the lamin meshwork is not a random arrangement of filaments but exhibits small-world properties. Our results suggest that lamin filaments arrange to form an emergent meshwork whose topology dictates the mechanical properties of individual filaments. The quantitative insights imply a role of meshwork topology in laminopathies.

Date: 2020
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DOI: 10.1038/s41467-020-20049-8

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