Effect of cell geometry in the evaluation of erythrocyte viscoelastic properties

Fran Gómez, Leandro S. Silva, Glauber Ribeiro de Sousa Araújo, Susana Frases, Ana Acacia S. Pinheiro, Ubirajara Agero, Bruno Pontes, and Nathan Bessa Viana
Phys. Rev. E 101, 062403 – Published 2 June 2020

Abstract

The red blood cell membrane-cytoskeleton is a complex structure mainly responsible for giving the cell rigidity and shape. It also provides the erythrocyte with the ability to pass through narrow capillaries of the vertebrate blood circulatory system. Although the red blood cell viscoelastic properties have been extensively studied, reported experimental data differ by up to three orders of magnitude. This could be attributed to the natural cell variability, to the different techniques employed, and also to the models used for the cell response, which are highly dependent on cell geometry. Here, we use two methodologies based on optical tweezers to investigate the viscoelastic behavior of healthy human red blood cells, one applying small cell deformations (microrheology) and another imposing large deformations (tether extraction). We also establish a defocusing microscopy-based method to characterize the cell geometry and thus the erythrocyte form factor, an essential parameter that allows comparisons among the viscoelastic properties at different conditions. Moreover, for small deformations, a soft glassy rheology model is used to discuss the results, while for large deformations two surface shear moduli and one surface viscosity are determined, together with the surface tension and bending modulus of the erythrocyte membrane lipid component. We also show that F-actin is not detected in tethers, although the erythrocyte membrane has physical properties like those of other adherent cells, known to have tethers containing F-actin inside. Altogether, our results show good agreement with the reported literature and we argue that, to properly compare the viscoelastic properties of red blood cells in different situations, the task of cell geometry characterization must be accomplished. This may be especially important when the influence of agents, like the malaria parasite, induces changes in both the geometry and chemical constituents of the erythrocyte membrane. Together, the new methodologies and procedures used in this study would allow the erythrocyte community to better explore the mechanical behavior of red blood cells and may be useful to characterize erythrocyte viscoelasticity changes in several blood diseases.

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  • Received 18 September 2019
  • Revised 20 April 2020
  • Accepted 11 May 2020

DOI:https://doi.org/10.1103/PhysRevE.101.062403

©2020 American Physical Society

Physics Subject Headings (PhySH)

Physics of Living Systems

Authors & Affiliations

Fran Gómez1,2,5, Leandro S. Silva3, Glauber Ribeiro de Sousa Araújo3, Susana Frases3, Ana Acacia S. Pinheiro3, Ubirajara Agero4, Bruno Pontes1,2,5, and Nathan Bessa Viana1,2,5,*

  • 1Instituto de Física, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Rio de Janeiro, 21941-972, Brazil
  • 2LPO-COPEA, Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Rio de Janeiro, 21941-902, Brazil
  • 3Instituto de Biofísica Carlos Chagas Filho, Rio de Janeiro, Rio de Janeiro, 21941-901, Brazil
  • 4Instituto de Ciências Exatas, Departamento de Física, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, 31270-901, Brazil
  • 5CENABIO - Centro Nacional de Biologia Estrutural e Bioimagem, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Rio de Janeiro, 21941-902, Brazil

  • *Corresponding author: nathan@if.ufrj.br

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Vol. 101, Iss. 6 — June 2020

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