Metabolic Remodeling of the Human Red Blood Cell Membrane

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2010 Jan 19

PMID 20080583

Citations 136

Authors

YongKeun Park

Catherine A Best

Thorsten Auth

Nir S Gov

Samuel A Safran

Gabriel Popescu

Subra Suresh

Michael S Feld

Affiliations

Soon will be listed here.

Abstract

The remarkable deformability of the human red blood cell (RBC) results from the coupled dynamic response of the phospholipid bilayer and the spectrin molecular network. Here we present quantitative connections between spectrin morphology and membrane fluctuations of human RBCs by using dynamic full-field laser interferometry techniques. We present conclusive evidence that the presence of adenosine 5'-triphosphate (ATP) facilitates non-equilibrium dynamic fluctuations in the RBC membrane that are highly correlated with the biconcave shape of RBCs. Spatial analysis of the fluctuations reveals that these non-equilibrium membrane vibrations are enhanced at the scale of spectrin mesh size. Our results indicate that the dynamic remodeling of the coupled membranes powered by ATP results in non-equilibrium membrane fluctuations manifesting from both metabolic and thermal energies and also maintains the biconcave shape of RBCs.

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References

Mizuno D, Tardin C, Schmidt C, MacKintosh F . Nonequilibrium mechanics of active cytoskeletal networks. Science. 2007; 315(5810):370-3. DOI: 10.1126/science.1134404. View

Auth T, Safran S, Gov N . Fluctuations of coupled fluid and solid membranes with application to red blood cells. Phys Rev E Stat Nonlin Soft Matter Phys. 2008; 76(5 Pt 1):051910. DOI: 10.1103/PhysRevE.76.051910. View

Popescu G, Ikeda T, Dasari R, Feld M . Diffraction phase microscopy for quantifying cell structure and dynamics. Opt Lett. 2006; 31(6):775-7. DOI: 10.1364/ol.31.000775. View

Betz T, Lenz M, Joanny J, Sykes C . ATP-dependent mechanics of red blood cells. Proc Natl Acad Sci U S A. 2009; 106(36):15320-5. PMC: 2741249. DOI: 10.1073/pnas.0904614106. View

Muller E, HEGEWALD H, JAROSZEWICZ K, Cumme G, Hoppe H, FRUNDER H . Turnover of phosphomonoester groups and compartmentation of polyphosphoinositides in human erythrocytes. Biochem J. 1986; 235(3):775-83. PMC: 1146755. DOI: 10.1042/bj2350775. View

Park Y, Diez-Silva M, Popescu G, Lykotrafitis G, Choi W, Feld M . Refractive index maps and membrane dynamics of human red blood cells parasitized by Plasmodium falciparum. Proc Natl Acad Sci U S A. 2008; 105(37):13730-5. PMC: 2529332. DOI: 10.1073/pnas.0806100105. View

Gov N, Safran S . Red blood cell membrane fluctuations and shape controlled by ATP-induced cytoskeletal defects. Biophys J. 2004; 88(3):1859-74. PMC: 1305240. DOI: 10.1529/biophysj.104.045328. View

Lin L, Gov N, Brown F . Nonequilibrium membrane fluctuations driven by active proteins. J Chem Phys. 2006; 124(7):74903. DOI: 10.1063/1.2166383. View

Popescu G, Ikeda T, Goda K, Best-Popescu C, Laposata M, Manley S . Optical measurement of cell membrane tension. Phys Rev Lett. 2006; 97(21):218101. DOI: 10.1103/PhysRevLett.97.218101. View

10.

Manno S, Takakuwa Y, Mohandas N . Modulation of erythrocyte membrane mechanical function by protein 4.1 phosphorylation. J Biol Chem. 2004; 280(9):7581-7. DOI: 10.1074/jbc.M410650200. View

11.

Gov N . Active elastic network: cytoskeleton of the red blood cell. Phys Rev E Stat Nonlin Soft Matter Phys. 2007; 75(1 Pt 1):011921. DOI: 10.1103/PhysRevE.75.011921. View

12.

Sheetz M, Singer S . On the mechanism of ATP-induced shape changes in human erythrocyte membranes. I. The role of the spectrin complex. J Cell Biol. 1977; 73(3):638-46. PMC: 2111425. DOI: 10.1083/jcb.73.3.638. View

13.

PARPART A, Hoffman J . Flicker in erythrocytes; vibratory movements in the cytoplasm. J Cell Comp Physiol. 1956; 47(2):295-303. DOI: 10.1002/jcp.1030470208. View

14.

Li J, Lykotrafitis G, Dao M, Suresh S . Cytoskeletal dynamics of human erythrocyte. Proc Natl Acad Sci U S A. 2007; 104(12):4937-42. PMC: 1829243. DOI: 10.1073/pnas.0700257104. View

15.

Gov N, Zilman A, Safran S . Cytoskeleton confinement and tension of red blood cell membranes. Phys Rev Lett. 2003; 90(22):228101. DOI: 10.1103/PhysRevLett.90.228101. View

16.

Tchernia G, Mohandas N, SHOHET S . Deficiency of skeletal membrane protein band 4.1 in homozygous hereditary elliptocytosis. Implications for erythrocyte membrane stability. J Clin Invest. 1981; 68(2):454-60. PMC: 370818. DOI: 10.1172/jci110275. View

17.

Park Y, Popescu G, Badizadegan K, Dasari R, Feld M . Diffraction phase and fluorescence microscopy. Opt Express. 2009; 14(18):8263-8. DOI: 10.1364/oe.14.008263. View

18.

Tuvia S, Almagor A, Bitler A, Levin S, Korenstein R, Yedgar S . Cell membrane fluctuations are regulated by medium macroviscosity: evidence for a metabolic driving force. Proc Natl Acad Sci U S A. 1997; 94(10):5045-9. PMC: 24628. DOI: 10.1073/pnas.94.10.5045. View

19.

Patel V, Fairbanks G . Spectrin phosphorylation and shape change of human erythrocyte ghosts. J Cell Biol. 1981; 88(2):430-40. PMC: 2111749. DOI: 10.1083/jcb.88.2.430. View

20.

Mohandas N, Evans E . Mechanical properties of the red cell membrane in relation to molecular structure and genetic defects. Annu Rev Biophys Biomol Struct. 1994; 23:787-818. DOI: 10.1146/annurev.bb.23.060194.004035. View