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Publications

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Epublish 45 citations

PubMed: 32453720 DOI: 10.1371/journal.pcbi.1007890

Non-uniform distribution of myosin-mediated forces governs red blood cell membrane curvature through tension modulation.

PLoS Comput Biol 16(5):e1007890

Authors: Haleh Alimohamadi, Alyson S Smith, Roberta B Nowak, Velia M Fowler, Padmini Rangamani

Affiliations

  • Department of Mechanical and Aerospace Engineering, University of California San Diego, La Jolla, California, United States of America.
  • Department of Molecular Medicine, The Scripps Research Institute, La Jolla, California, United States of America.
  • Department of Biological Sciences, University of Delaware, Newark, Delaware, United States of America.

Abstract

The biconcave disk shape of the mammalian red blood cell (RBC) is unique to the RBC and is vital for its circulatory function. Due to the absence of a transcellular cytoskeleton, RBC shape is determined by the membrane skeleton, a network of actin filaments cross-linked by spectrin and attached to membrane proteins. While the physical properties of a uniformly distributed actin network interacting with the lipid bilayer membrane have been assumed to control RBC shape, recent experiments reveal that RBC biconcave shape also depends on the contractile activity of nonmuscle myosin IIA (NMIIA) motor proteins. Here, we use the classical Helfrich-Canham model for the RBC membrane to test the role of heterogeneous force distributions along the membrane and mimic the contractile activity of sparsely distributed NMIIA filaments. By incorporating this additional contribution to the Helfrich-Canham energy, we find that the RBC biconcave shape depends on the ratio of forces per unit volume in the dimple and rim regions of the RBC. Experimental measurements of NMIIA densities at the dimple and rim validate our prediction that (a) membrane forces must be non-uniform along the RBC membrane and (b) the force density must be larger in the dimple than the rim to produce the observed membrane curvatures. Furthermore, we predict that RBC membrane tension and the orientation of the applied forces play important roles in regulating this force-shape landscape. Our findings of heterogeneous force distributions on the plasma membrane for RBC shape maintenance may also have implications for shape maintenance in different cell types.

MeSH

Cells, Actins, Erythrocytes, Blood, Myosins, Cell Membrane, Maintenance, Blood Cells, Membranes, Computational Biology

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