Competition between deformation and free volume quantified by 3D image analysis of red blood cell

Mehrnaz Babaki; Dmitry A. Fedosov; Amirreza Gholivand; Joeri Opdam; Remco Tuinier; Minne Paul Lettinga

doi:10.1016/j.bpj.2023.03.030

Competition between deformation and free volume quantified by 3D image analysis of red blood cell

Mehrnaz Babaki
, Dmitry A. Fedosov
, Amirreza Gholivand
, Joeri Opdam
, Remco Tuinier
, Minne Paul Lettinga (Corresponding author)

Research output: Contribution to journal › Article › Academic › peer-review

5 Citations (Scopus)

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Abstract

Cells in living organisms are subjected to mechanical strains caused by external forces like overcrowding, resulting in strong deformations that affect cell function. We study the interplay between deformation and crowding of red blood cells (RBCs) in dispersions of nonabsorbing rod-like viruses. We identify a sequence of configurational transitions of RBC doublets, including configurations that can only be induced by long-ranged attraction: highly fluctuating T-shaped and face-to-face configurations at low, and doublets approaching a complete spherical configuration at high, rod concentrations. Complementary simulations are used to explore different energy contributions to deformation as well as the stability of RBC doublet configurations. Our advanced analysis of 3D reconstructed confocal images of RBC doublets quantifies the depletion interaction and the resulting deformation energy. Thus, we introduce a noninvasive, high-throughput platform that is generally applicable to investigate the mechanical response of biological cells to external forces and characterize their mechanical properties.

Original language	English
Pages (from-to)	1646-1658
Number of pages	13
Journal	Biophysical Journal
Volume	122
Issue number	9
DOIs	https://doi.org/10.1016/j.bpj.2023.03.030
Publication status	Published - 2 May 2023

Bibliographical note

Funding Information:
M.B. acknowledges support by the International Helmholtz Research School of Biophysics and Soft Matter (IHRS BioSoft). D.A.F. gratefully acknowledges the computing time granted through JARA on the supercomputer JURECA at Forschungszentrum Jülich. J.O. and R.T. acknowledge financial support from the Dutch Ministry of Economic Affairs of the Netherlands via the Top Consortium for Knowledge and Innovation ( TKI ) roadmap Chemistry of Advanced Materials (grant no. CHEMIE.PGT.2018.006 ). We thank Thomas Fischer for stimulating discussions.

Funding Information:
M.B. acknowledges support by the International Helmholtz Research School of Biophysics and Soft Matter (IHRS BioSoft). D.A.F. gratefully acknowledges the computing time granted through JARA on the supercomputer JURECA at Forschungszentrum Jülich. J.O. and R.T. acknowledge financial support from the Dutch Ministry of Economic Affairs of the Netherlands via the Top Consortium for Knowledge and Innovation (TKI) roadmap Chemistry of Advanced Materials (grant no. CHEMIE.PGT.2018.006). We thank Thomas Fischer for stimulating discussions. The authors declare no competing interests.

Funding

M.B. acknowledges support by the International Helmholtz Research School of Biophysics and Soft Matter (IHRS BioSoft). D.A.F. gratefully acknowledges the computing time granted through JARA on the supercomputer JURECA at Forschungszentrum Jülich. J.O. and R.T. acknowledge financial support from the Dutch Ministry of Economic Affairs of the Netherlands via the Top Consortium for Knowledge and Innovation ( TKI ) roadmap Chemistry of Advanced Materials (grant no. CHEMIE.PGT.2018.006 ). We thank Thomas Fischer for stimulating discussions. M.B. acknowledges support by the International Helmholtz Research School of Biophysics and Soft Matter (IHRS BioSoft). D.A.F. gratefully acknowledges the computing time granted through JARA on the supercomputer JURECA at Forschungszentrum Jülich. J.O. and R.T. acknowledge financial support from the Dutch Ministry of Economic Affairs of the Netherlands via the Top Consortium for Knowledge and Innovation (TKI) roadmap Chemistry of Advanced Materials (grant no. CHEMIE.PGT.2018.006). We thank Thomas Fischer for stimulating discussions. The authors declare no competing interests.

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Cite this

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title = "Competition between deformation and free volume quantified by 3D image analysis of red blood cell",

abstract = "Cells in living organisms are subjected to mechanical strains caused by external forces like overcrowding, resulting in strong deformations that affect cell function. We study the interplay between deformation and crowding of red blood cells (RBCs) in dispersions of nonabsorbing rod-like viruses. We identify a sequence of configurational transitions of RBC doublets, including configurations that can only be induced by long-ranged attraction: highly fluctuating T-shaped and face-to-face configurations at low, and doublets approaching a complete spherical configuration at high, rod concentrations. Complementary simulations are used to explore different energy contributions to deformation as well as the stability of RBC doublet configurations. Our advanced analysis of 3D reconstructed confocal images of RBC doublets quantifies the depletion interaction and the resulting deformation energy. Thus, we introduce a noninvasive, high-throughput platform that is generally applicable to investigate the mechanical response of biological cells to external forces and characterize their mechanical properties.",

author = "Mehrnaz Babaki and Fedosov, \{Dmitry A.\} and Amirreza Gholivand and Joeri Opdam and Remco Tuinier and Lettinga, \{Minne Paul\}",

note = "Funding Information: M.B. acknowledges support by the International Helmholtz Research School of Biophysics and Soft Matter (IHRS BioSoft). D.A.F. gratefully acknowledges the computing time granted through JARA on the supercomputer JURECA at Forschungszentrum J{\"u}lich. J.O. and R.T. acknowledge financial support from the Dutch Ministry of Economic Affairs of the Netherlands via the Top Consortium for Knowledge and Innovation ( TKI ) roadmap Chemistry of Advanced Materials (grant no. CHEMIE.PGT.2018.006 ). We thank Thomas Fischer for stimulating discussions. Funding Information: M.B. acknowledges support by the International Helmholtz Research School of Biophysics and Soft Matter (IHRS BioSoft). D.A.F. gratefully acknowledges the computing time granted through JARA on the supercomputer JURECA at Forschungszentrum J{\"u}lich. J.O. and R.T. acknowledge financial support from the Dutch Ministry of Economic Affairs of the Netherlands via the Top Consortium for Knowledge and Innovation (TKI) roadmap Chemistry of Advanced Materials (grant no. CHEMIE.PGT.2018.006). We thank Thomas Fischer for stimulating discussions. The authors declare no competing interests. ",

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AU - Fedosov, Dmitry A.

AU - Gholivand, Amirreza

AU - Opdam, Joeri

AU - Tuinier, Remco

AU - Lettinga, Minne Paul

N1 - Funding Information: M.B. acknowledges support by the International Helmholtz Research School of Biophysics and Soft Matter (IHRS BioSoft). D.A.F. gratefully acknowledges the computing time granted through JARA on the supercomputer JURECA at Forschungszentrum Jülich. J.O. and R.T. acknowledge financial support from the Dutch Ministry of Economic Affairs of the Netherlands via the Top Consortium for Knowledge and Innovation ( TKI ) roadmap Chemistry of Advanced Materials (grant no. CHEMIE.PGT.2018.006 ). We thank Thomas Fischer for stimulating discussions. Funding Information: M.B. acknowledges support by the International Helmholtz Research School of Biophysics and Soft Matter (IHRS BioSoft). D.A.F. gratefully acknowledges the computing time granted through JARA on the supercomputer JURECA at Forschungszentrum Jülich. J.O. and R.T. acknowledge financial support from the Dutch Ministry of Economic Affairs of the Netherlands via the Top Consortium for Knowledge and Innovation (TKI) roadmap Chemistry of Advanced Materials (grant no. CHEMIE.PGT.2018.006). We thank Thomas Fischer for stimulating discussions. The authors declare no competing interests.

PY - 2023/5/2

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N2 - Cells in living organisms are subjected to mechanical strains caused by external forces like overcrowding, resulting in strong deformations that affect cell function. We study the interplay between deformation and crowding of red blood cells (RBCs) in dispersions of nonabsorbing rod-like viruses. We identify a sequence of configurational transitions of RBC doublets, including configurations that can only be induced by long-ranged attraction: highly fluctuating T-shaped and face-to-face configurations at low, and doublets approaching a complete spherical configuration at high, rod concentrations. Complementary simulations are used to explore different energy contributions to deformation as well as the stability of RBC doublet configurations. Our advanced analysis of 3D reconstructed confocal images of RBC doublets quantifies the depletion interaction and the resulting deformation energy. Thus, we introduce a noninvasive, high-throughput platform that is generally applicable to investigate the mechanical response of biological cells to external forces and characterize their mechanical properties.

AB - Cells in living organisms are subjected to mechanical strains caused by external forces like overcrowding, resulting in strong deformations that affect cell function. We study the interplay between deformation and crowding of red blood cells (RBCs) in dispersions of nonabsorbing rod-like viruses. We identify a sequence of configurational transitions of RBC doublets, including configurations that can only be induced by long-ranged attraction: highly fluctuating T-shaped and face-to-face configurations at low, and doublets approaching a complete spherical configuration at high, rod concentrations. Complementary simulations are used to explore different energy contributions to deformation as well as the stability of RBC doublet configurations. Our advanced analysis of 3D reconstructed confocal images of RBC doublets quantifies the depletion interaction and the resulting deformation energy. Thus, we introduce a noninvasive, high-throughput platform that is generally applicable to investigate the mechanical response of biological cells to external forces and characterize their mechanical properties.

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EP - 1658

JO - Biophysical Journal

JF - Biophysical Journal

IS - 9

ER -

Competition between deformation and free volume quantified by 3D image analysis of red blood cell

Abstract

Bibliographical note

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