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

Authors:
; ORCiD logo; ; ORCiD logo; ORCiD logo;
Publication Date:
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA), Office of Naval Reactors
OSTI Identifier:
1632048
Alternate Identifier(s):
OSTI ID: 1630784
Grant/Contract Number:  
ONR N00014-17-1-2628
Resource Type:
Published Article
Journal Name:
PLoS Computational Biology (Online)
Additional Journal Information:
Journal Name: PLoS Computational Biology (Online) Journal Volume: 16 Journal Issue: 5; Journal ID: ISSN 1553-7358
Publisher:
Public Library of Science (PLoS)
Country of Publication:
United States
Language:
English

Citation Formats

Alimohamadi, Haleh, Smith, Alyson S., Nowak, Roberta B., Fowler, Velia M., Rangamani, Padmini, and Elofsson, ed., Arne. Non-uniform distribution of myosin-mediated forces governs red blood cell membrane curvature through tension modulation. United States: N. p., 2020. Web. doi:10.1371/journal.pcbi.1007890.
Alimohamadi, Haleh, Smith, Alyson S., Nowak, Roberta B., Fowler, Velia M., Rangamani, Padmini, & Elofsson, ed., Arne. Non-uniform distribution of myosin-mediated forces governs red blood cell membrane curvature through tension modulation. United States. doi:https://doi.org/10.1371/journal.pcbi.1007890
Alimohamadi, Haleh, Smith, Alyson S., Nowak, Roberta B., Fowler, Velia M., Rangamani, Padmini, and Elofsson, ed., Arne. Tue . "Non-uniform distribution of myosin-mediated forces governs red blood cell membrane curvature through tension modulation". United States. doi:https://doi.org/10.1371/journal.pcbi.1007890.
@article{osti_1632048,
title = {Non-uniform distribution of myosin-mediated forces governs red blood cell membrane curvature through tension modulation},
author = {Alimohamadi, Haleh and Smith, Alyson S. and Nowak, Roberta B. and Fowler, Velia M. and Rangamani, Padmini and Elofsson, ed., Arne},
abstractNote = {},
doi = {10.1371/journal.pcbi.1007890},
journal = {PLoS Computational Biology (Online)},
number = 5,
volume = 16,
place = {United States},
year = {2020},
month = {5}
}

Journal Article:
Free Publicly Available Full Text
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DOI: https://doi.org/10.1371/journal.pcbi.1007890

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Works referenced in this record:

Mechanical and Geometrical Properties of Density-Separated Neonatal and Adult Erythrocytes
journal, November 1993


Mechanical Properties of the Red Cell Membrane in Relation to Molecular Structure and Genetic Defects
journal, June 1994


Erythrocyte responses in low-shear-rate flows: effects of non-biconcave stress-free state in the cytoskeleton
journal, February 2014

  • Peng, Zhangli; Mashayekh, Adel; Zhu, Qiang
  • Journal of Fluid Mechanics, Vol. 742
  • DOI: 10.1017/jfm.2014.14

Force Generation, Transmission, and Integration during Cell and Tissue Morphogenesis
journal, November 2011


Protein-Induced Membrane Curvature Alters Local Membrane Tension
journal, August 2014

  • Rangamani, Padmini; Mandadap, Kranthi K.; Oster, George
  • Biophysical Journal, Vol. 107, Issue 3
  • DOI: 10.1016/j.bpj.2014.06.010

Effect of Chain Length and Unsaturation on Elasticity of Lipid Bilayers
journal, July 2000


High-resolution data on the geometry of red blood cells
journal, December 1981


Interaction between surface shape and intra-surface viscous flow on lipid membranes
journal, October 2012

  • Rangamani, Padmini; Agrawal, Ashutosh; Mandadapu, Kranthi K.
  • Biomechanics and Modeling in Mechanobiology, Vol. 12, Issue 4
  • DOI: 10.1007/s10237-012-0447-y

Computer simulation of cytoskeleton-induced blebbing in lipid membranes
journal, November 2011


Red Blood Cell Membrane Fluctuations and Shape Controlled by ATP-Induced Cytoskeletal Defects
journal, March 2005


A Method for the Calculation of Vesicle Shapes
journal, April 1982

  • Luke, Jon C.
  • SIAM Journal on Applied Mathematics, Vol. 42, Issue 2
  • DOI: 10.1137/0142026

The Equations of Mechanical Equilibrium of a Model Membrane
journal, June 1977

  • Jenkins, James T.
  • SIAM Journal on Applied Mathematics, Vol. 32, Issue 4
  • DOI: 10.1137/0132063

The role of traction in membrane curvature generation
journal, August 2018

  • Alimohamadi, H.; Vasan, R.; Hassinger, J. E.
  • Molecular Biology of the Cell, Vol. 29, Issue 16
  • DOI: 10.1091/mbc.E18-02-0087

Curvature instability in membranes
journal, January 1986


ARP3 Controls the Podocyte Architecture at the Kidney Filtration Barrier
journal, December 2018


Theory of the Sphering of Red Blood Cells
journal, February 1968


Metabolic remodeling of the human red blood cell membrane
journal, January 2010

  • Park, Y.; Best, C. A.; Auth, T.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 4
  • DOI: 10.1073/pnas.0910785107

Echinocyte Shapes: Bending, Stretching, and Shear Determine Spicule Shape and Spacing
journal, April 2002


Shapes of bilayer vesicles with membrane embedded molecules
journal, September 1996

  • Kralj-Iglič, V.; Svetina, S.; Žekž, B.
  • European Biophysics Journal, Vol. 24, Issue 5
  • DOI: 10.1007/BF00180372

Dynamics of Myosin-Driven Skeletal Muscle Contraction: I. Steady-State Force Generation
journal, June 2005


Measuring cell surface area and deformability of individual human red blood cells over blood storage using quantitative phase imaging
journal, October 2016

  • Park, HyunJoo; Lee, SangYun; Ji, Misuk
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep34257

Lateral organization of membranes and cell shapes
journal, October 1981


Endocytic proteins drive vesicle growth via instability in high membrane tension environment
journal, March 2015

  • Walani, Nikhil; Torres, Jennifer; Agrawal, Ashutosh
  • Proceedings of the National Academy of Sciences
  • DOI: 10.1073/pnas.1418491112

Golgi apparatus self-organizes into the characteristic shape via postmitotic reassembly dynamics
journal, May 2017

  • Tachikawa, Masashi; Mochizuki, Atsushi
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 20
  • DOI: 10.1073/pnas.1619264114

Improved measurements of the erythrocyte geometry
journal, October 1972


Fluctuations of the Red Blood Cell Membrane: Relation to Mechanical Properties and Lack of ATP Dependence
journal, May 2008


Modeling Membrane Curvature Generation due to Membrane–Protein Interactions
journal, October 2018

  • Alimohamadi, Haleh; Rangamani, Padmini
  • Biomolecules, Vol. 8, Issue 4
  • DOI: 10.3390/biom8040120

Cytoskeletal dynamics of human erythrocyte
journal, March 2007

  • Li, J.; Lykotrafitis, G.; Dao, M.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 12
  • DOI: 10.1073/pnas.0700257104

Engineering cell shape and function
journal, April 1994


Dynamic modes of the cortical actomyosin gel during cell locomotion and division
journal, January 2006


Modeling of light scattering by biconcave and deformed red blood cells with the invariant imbedding T-matrix method
journal, May 2013


Static equilibrium configurations of a model red blood cell
journal, June 1977


Movement and force produced by a single myosin head
journal, November 1995

  • Molloy, J. E.; Burns, J. E.; Kendrick-Jones, J.
  • Nature, Vol. 378, Issue 6553
  • DOI: 10.1038/378209a0

Actin cortex mechanics and cellular morphogenesis
journal, October 2012

  • Salbreux, Guillaume; Charras, Guillaume; Paluch, Ewa
  • Trends in Cell Biology, Vol. 22, Issue 10
  • DOI: 10.1016/j.tcb.2012.07.001

Optical and mathematical corrections of micropipette measurements of red blood cell geometry during anisotonic perifusion
journal, December 1994


Myosin from human erythrocytes.
journal, January 1985


Mechanosensitive Fluorescent Probes to Image Membrane Tension in Mitochondria, Endoplasmic Reticulum, and Lysosomes
journal, February 2019

  • Goujon, Antoine; Colom, Adai; Straková, Karolína
  • Journal of the American Chemical Society, Vol. 141, Issue 8
  • DOI: 10.1021/jacs.8b13189

Formation and Interaction of Membrane Tubes
journal, May 2002


Changes in cell shape are correlated with metastatic potential in murine and human osteosarcomas
journal, February 2016

  • Lyons, Samanthe M.; Alizadeh, Elaheh; Mannheimer, Joshua
  • Biology Open, Vol. 5, Issue 3
  • DOI: 10.1242/bio.013409

Load-dependent modulation of non-muscle myosin-2A function by tropomyosin 4.2
journal, February 2016

  • Hundt, Nikolas; Steffen, Walter; Pathan-Chhatbar, Salma
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep20554

Forcing cells into shape: the mechanics of actomyosin contractility
journal, July 2015

  • Murrell, Michael; Oakes, Patrick W.; Lenz, Martin
  • Nature Reviews Molecular Cell Biology, Vol. 16, Issue 8
  • DOI: 10.1038/nrm4012

DLITE Uses Cell-Cell Interface Movement to Better Infer Cell-Cell Tensions
journal, November 2019


Connections between single-cell biomechanics and human disease states: gastrointestinal cancer and malaria
journal, January 2005


Depletion of membrane skeleton in red blood cell vesicles
journal, July 1995


Comparative hemorheology—Hematological implications of species differences in blood viscosity
journal, July 1971

  • Chien, Shu; Usami, Shunichi; Dellenback, Robert J.
  • Biorheology, Vol. 8, Issue 1
  • DOI: 10.3233/BIR-1971-8106

A mechanical model reveals that non-axisymmetric buckling lowers the energy barrier associated with membrane neck constriction
journal, January 2020

  • Vasan, R.; Rudraraju, S.; Akamatsu, M.
  • Soft Matter, Vol. 16, Issue 3
  • DOI: 10.1039/C9SM01494B

Contributions on the Shapes of red Blood Corpuscles
journal, January 1955


Use the force: membrane tension as an organizer of cell shape and motility
journal, February 2013

  • Diz-Muñoz, Alba; Fletcher, Daniel A.; Weiner, Orion D.
  • Trends in Cell Biology, Vol. 23, Issue 2
  • DOI: 10.1016/j.tcb.2012.09.006

Red blood cell shapes as explained on the basis of curvature elasticity
journal, August 1976


A novel strain energy relationship for red blood cell membrane skeleton based on spectrin stiffness and its application to micropipette deformation
journal, September 2015

  • Svetina, Saša; Kokot, Gašper; Kebe, Tjaša Švelc
  • Biomechanics and Modeling in Mechanobiology, Vol. 15, Issue 3
  • DOI: 10.1007/s10237-015-0721-x

Cell Membranes Resist Flow
journal, December 2018


Multiscale simulation of erythrocyte membranes
journal, March 2010


Amphiphile induced echinocyte-spheroechinocyte transformation of red blood cell shape
journal, June 1998

  • Iglič, A.; Kralj-Iglič, Veronika; Hägerstrand, Henry
  • European Biophysics Journal, Vol. 27, Issue 4
  • DOI: 10.1007/s002490050140

The curvature elasticity of fluid membranes : A catalogue of vesicle shapes
journal, January 1976


Dynamics and regulation of contractile actin–myosin networks in morphogenesis
journal, February 2011


Nonmuscle myosin-2: mix and match
journal, May 2012

  • Heissler, Sarah M.; Manstein, Dietmar J.
  • Cellular and Molecular Life Sciences, Vol. 70, Issue 1
  • DOI: 10.1007/s00018-012-1002-9

Anisotropic spontaneous curvatures in lipid membranes
journal, June 2014


Parametric-Equation Representation of Biconcave Erythrocytes
journal, March 1999


Why Do Red Blood Cells Have Asymmetric Shapes Even in a Symmetric Flow?
journal, October 2009


Coupling between vesicle shape and the non-homogeneous lateral distribution of membrane constituents in Golgi bodies
journal, August 2004


Shape and Biomechanical Characteristics of Human Red Blood Cells in Health and Disease
journal, May 2010

  • Diez-Silva, Monica; Dao, Ming; Han, Jongyoon
  • MRS Bulletin, Vol. 35, Issue 5
  • DOI: 10.1557/mrs2010.571

A Model of Piezo1-Based Regulation of Red Blood Cell Volume
journal, January 2019


Modeling protein-mediated morphology in biomembranes
journal, November 2008

  • Agrawal, Ashutosh; Steigmann, David J.
  • Biomechanics and Modeling in Mechanobiology, Vol. 8, Issue 5
  • DOI: 10.1007/s10237-008-0143-0

Experimental and theoretical study of light scattering by individual mature red blood cells by use of scanning flow cytometry and a discrete dipole approximation
journal, January 2005

  • Yurkin, Maxim A.; Semyanov, Konstantin A.; Tarasov, Peter A.
  • Applied Optics, Vol. 44, Issue 25, p. 5249-5256
  • DOI: 10.1364/AO.44.005249

Red Cell Deformability and its Relevance to Blood Flow
journal, March 1987


MYH9: Structure, functions and role of non-muscle myosin IIA in human disease
journal, July 2018


Myosin IIA interacts with the spectrin-actin membrane skeleton to control red blood cell membrane curvature and deformability
journal, April 2018

  • Smith, Alyson S.; Nowak, Roberta B.; Zhou, Sitong
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 19
  • DOI: 10.1073/pnas.1718285115

Evidence that asymmetry of the membrane/cytoskeletal complex in human red blood cell ghosts is responsible for their biconcave shape
journal, January 2018

  • Hoffman, Joseph F.
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 7
  • DOI: 10.1073/pnas.1721463115

Scattering of Light by a Red Blood Cell
journal, July 1998

  • Borovoi, A. G.
  • Journal of Biomedical Optics, Vol. 3, Issue 3
  • DOI: 10.1117/1.429883

The minimum energy of bending as a possible explanation of the biconcave shape of the human red blood cell
journal, January 1970


Feisty filaments: actin dynamics in the red blood cell membrane skeleton
journal, January 2016


New insights into erythrocyte membrane organization and microelasticity
journal, January 2000


Membrane bending energy and shape determination of phospholipid vesicles and red blood cells
journal, June 1989

  • Svetina, S.; Žekš, B.
  • European Biophysics Journal, Vol. 17, Issue 2
  • DOI: 10.1007/BF00257107

Flow-cytometric light scattering measurement of red blood cell volume and hemoglobin concentration
journal, January 1985

  • Tycko, D. H.; Metz, M. H.; Epstein, E. A.
  • Applied Optics, Vol. 24, Issue 9
  • DOI: 10.1364/AO.24.001355

Theoretical study of vesicle shapes driven by coupling curved proteins and active cytoskeletal forces
journal, January 2019

  • Fošnarič, Miha; Penič, Samo; Iglič, Aleš
  • Soft Matter, Vol. 15, Issue 26
  • DOI: 10.1039/C8SM02356E

Equilibrium Shape of Two-Component Unilamellar Membranes and Vesicles
journal, May 1992


What is the surface tension of a lipid bilayer membrane?
journal, September 1996


Elastic Properties of Lipid Bilayers: Theory and Possible Experiments
journal, December 1973


The red cell membrane and its cytoskeleton
journal, July 1981


Nonmuscle myosin II moves in new directions
journal, January 2008

  • Conti, M. A.; Adelstein, R. S.
  • Journal of Cell Science, Vol. 121, Issue 1
  • DOI: 10.1242/jcs.007112

Mechanical sensitivity of Piezo1 ion channels can be tuned by cellular membrane tension
journal, December 2015


Biological Membranes as Bilayer Couples. A Molecular Mechanism of Drug-Erythrocyte Interactions
journal, November 1974

  • Sheetz, M. P.; Singer, S. J.
  • Proceedings of the National Academy of Sciences, Vol. 71, Issue 11, p. 4457-4461
  • DOI: 10.1073/pnas.71.11.4457

Elastic properties of the red blood cell membrane that determine echinocyte deformability
journal, September 2003


Membrane Skeleton Detachment in Spherical and Cylindrical Microexovesicles
journal, October 1999


Lipid bilayer and cytoskeletal interactions in a red blood cell
journal, July 2013

  • Peng, Z.; Li, X.; Pivkin, I. V.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 33
  • DOI: 10.1073/pnas.1311827110

Correlation of enzymic properties and conformation of bovine erythrocyte myosin
journal, February 1989

  • Higashihara, Masaaki; Hartshorne, David J.; Craig, Roger
  • Biochemistry, Vol. 28, Issue 4
  • DOI: 10.1021/bi00430a032

The basics of epithelial-mesenchymal transition
journal, June 2009

  • Kalluri, Raghu; Weinberg, Robert A.
  • Journal of Clinical Investigation, Vol. 119, Issue 6
  • DOI: 10.1172/JCI39104

Decoding Information in Cell Shape
journal, September 2013


Myosin II controls cellular branching morphogenesis and migration in three dimensions by minimizing cell-surface curvature
journal, January 2015

  • Elliott, Hunter; Fischer, Robert S.; Myers, Kenneth A.
  • Nature Cell Biology, Vol. 17, Issue 2
  • DOI: 10.1038/ncb3092

Human erythrocyte myosin: identification and purification.
journal, January 1985

  • Fowler, V. M.; Davis, J. Q.; Bennett, V.
  • The Journal of Cell Biology, Vol. 100, Issue 1
  • DOI: 10.1083/jcb.100.1.47

Equilibrium shapes of red blood cells in osmotic swelling
journal, January 1980


Mechanical Properties of the Red Cell Membrane
journal, March 1964


Dynamics of actomyosin contractile activity during epithelial morphogenesis
journal, October 2011


Rac1 Activity Is Modulated by Huntingtin and Dysregulated in Models of Huntington’s Disease
journal, February 2019

  • Tousley, Adelaide; Iuliano, Maria; Weisman, Elizabeth
  • Journal of Huntington's Disease, Vol. 8, Issue 1
  • DOI: 10.3233/JHD-180311

A possible mechanism determining the stability of spiculated red blood cells
journal, January 1997


Normal red blood cells’ shape stabilized by membrane’s in-plane ordering
journal, December 2019


Fluid Films with Curvature Elasticity
journal, December 1999

  • Steigmann, D. J.
  • Archive for Rational Mechanics and Analysis, Vol. 150, Issue 2
  • DOI: 10.1007/s002050050183

Distribution of Size and Shape in Populations of Normal Human Red Cells
journal, March 1968


Red cell membrane: past, present, and future
journal, November 2008


Biomechanics of red blood cells in human spleen and consequences for physiology and disease
journal, June 2016

  • Pivkin, Igor V.; Peng, Zhangli; Karniadakis, George E.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 28
  • DOI: 10.1073/pnas.1606751113

Hybrid continuum–coarse-grained modeling of erythrocytes
journal, June 2018


Biconcave shape of human red-blood-cell ghosts relies on density differences between the rim and dimple of the ghost's plasma membrane
journal, December 2016

  • Hoffman, Joseph F.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 51
  • DOI: 10.1073/pnas.1615452113

Measurement of biophysical properties of red blood cells by resistance pulse spectroscopy: volume, shape, surface area, and deformability
journal, August 1985

  • Richieri, Gary V.; Akeson, Stephen P.; Mel, Howard C.
  • Journal of Biochemical and Biophysical Methods, Vol. 11, Issue 2-3
  • DOI: 10.1016/0165-022X(85)90047-8

Principles of Actomyosin Regulation In Vivo
journal, February 2019


Unconventional Processive Mechanics of Non-muscle Myosin IIB
journal, May 2010

  • Norstrom, Melanie F.; Smithback, Philip A.; Rock, Ronald S.
  • Journal of Biological Chemistry, Vol. 285, Issue 34
  • DOI: 10.1074/jbc.M110.123851

A fluorescent membrane tension probe
journal, August 2018


Optical Measurement of Cell Membrane Tension
journal, November 2006


Non-muscle myosin II takes centre stage in cell adhesion and migration
journal, November 2009

  • Vicente-Manzanares, Miguel; Ma, Xuefei; Adelstein, Robert S.
  • Nature Reviews Molecular Cell Biology, Vol. 10, Issue 11
  • DOI: 10.1038/nrm2786