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PMID: 2393702 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

The membrane skeleton of erythrocytes. A percolation model.

Biophysical journal ·Vol. 57 ·No. 6 ·1990-06-00 ·Pages 1167-77

Saxton MJ

Abstract

The spectrin network on the cytoplasmic surface of the erythrocyte membrane is modeled as a triangular lattice of spectrin tetramers. This network obstructs lateral diffusion of proteins and provides mechanical reinforcement to the membrane. These effects are treated in a systematic and unified manner in terms of a percolation model. The diffusion coefficient is obtained as a function of the fraction of normal spectrin tetramers for both static and fluctuating barriers. The elasticity of the network is calculated as a function of the fraction of normal spectrin and the ratio of bending to stretching energies. For static barriers, elasticity and lateral diffusion are incompatible: if a network is connected enough to be elastic, it is connected enough to block long-range lateral diffusion. The elasticity and the force required for mechanical breakdown go to zero at the percolation threshold; experimental evidence suggests the existence of a stability threshold at or near the percolation threshold. The model is qualitatively applicable to other cells with membrane skeletons, such as epithelial cells, in which localization of membrane proteins is essential to differentiation.

MeSH Terms
Algorithms Diffusion Erythrocyte Membrane/metabolism,ultrastructure Humans Macromolecular Substances Mathematics Models, Structural Monte Carlo Method Spectrin/metabolism,ultrastructure
Chemicals
Macromolecular Substances Spectrin
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Saxton M J
Plant Growth Laboratory, University of California, Davis 95616.
References (51)
51 references, click to expand
  1. Partial deficiency of erythrocyte spectrin in hereditary spherocytosis.
    Nature. 1985 Mar 28-Apr 3;314(6009):380-3 PMID: 3982506
  2. Elastic properties of three-dimensional percolation networks with stretching and bond-bending forces.
    Phys Rev B Condens Matter. 1988 Oct 1;38(10):7173-7176 PMID: 9945432
  3. Colocalization and coprecipitation of ankyrin and Na+,K+-ATPase in kidney epithelial cells.
    Eur J Cell Biol. 1988 Feb;45(2):230-7 PMID: 2835237
  4. The lateral mobility of the (Na+,K+)-dependent ATPase in Madin-Darby canine kidney cells.
    J Cell Biol. 1986 Apr;102(4):1256-63 PMID: 3007531
  5. Effects of inherited membrane abnormalities on the viscoelastic properties of erythrocyte membrane.
    Biophys J. 1987 Mar;51(3):363-9 PMID: 2952176
  6. Protein 4.1 in sickle erythrocytes. Evidence for oxidative damage.
    J Biol Chem. 1987 Nov 15;262(32):15666-72 PMID: 3316203
  7. Inherited hemolytic disease in mice: a review and update.
    Lab Anim Sci. 1980 Apr;30(2 Pt 1):197-205 PMID: 6763106
  8. Distribution of transport proteins over animal cell membranes.
    J Membr Biol. 1984;77(3):169-86 PMID: 6321741
  9. Lipid diffusibility in the intact erythrocyte membrane.
    Biophys J. 1983 Jun;42(3):295-305 PMID: 6603237
  10. The polarized distribution of an apical cell surface glycoprotein is maintained by interactions with the cytoskeleton of Madin-Darby canine kidney cells.
    J Cell Biol. 1988 Dec;107(6 Pt 1):2377-87 PMID: 3198692
  11. Erythrocyte spectrin is comprised of many homologous triple helical segments.
    Nature. 1984 Sep 13-19;311(5982):177-80 PMID: 6472478
  12. A new mutation (sph) causing neonatal jaundice in the house mouse.
    Can J Genet Cytol. 1962 Jun;4:219-25 PMID: 14451913
  13. Lateral mobility of integral membrane proteins is increased in spherocytic erythrocytes.
    Nature. 1980 Jun 12;285(5765):510-1 PMID: 7402296
  14. Effective-medium theory of percolation on central-force elastic networks. II. Further results.
    Phys Rev B Condens Matter. 1985 Jun 1;31(11):7276-7281 PMID: 9935648
  15. The molecular basis of erythrocyte shape.
    Science. 1986 Dec 5;234(4781):1217-23 PMID: 3775380
  16. The spectrin-actin junction of erythrocyte membrane skeletons.
    Biochim Biophys Acta. 1989 Jan 18;988(1):107-21 PMID: 2642392
  17. 2,3-Diphosphoglycerate and ATP dissociate erythrocyte membrane skeletons.
    J Biol Chem. 1980 Oct 25;255(20):9955-60 PMID: 7430109
  18. Behavior of depleted elastic networks: Comparison of effective-medium and numerical calculations.
    Phys Rev B Condens Matter. 1985 Oct 1;32(7):4607-4617 PMID: 9937642
  19. Regulation of band 3 mobilities in erythrocyte ghost membranes by protein association and cytoskeletal meshwork.
    Biochemistry. 1988 Sep 20;27(19):7447-52 PMID: 2462903
  20. Colocalization of band 3 with ankyrin and spectrin at the basal membrane of intercalated cells in the rat kidney.
    Science. 1985 Dec 13;230(4731):1287-9 PMID: 2933809
  21. Unique alpha-spectrin mutant in a kindred with common hereditary elliptocytosis.
    J Clin Invest. 1987 Mar;79(3):989-96 PMID: 3818958
  22. Hereditary elliptocytosis, spherocytosis and related disorders: consequences of a deficiency or a mutation of membrane skeletal proteins.
    Blood Rev. 1987 Sep;1(3):147-68 PMID: 3332099
  23. The Wellcome lecture, 1988. Muscular dystrophy: a time of hope.
    Proc R Soc Lond B Biol Sci. 1989 Jun 22;237(1286):1-9 PMID: 2569197
  24. Visualization of the hexagonal lattice in the erythrocyte membrane skeleton.
    J Cell Biol. 1987 Mar;104(3):527-36 PMID: 2434513
  25. Molecular defect in the membrane skeleton of blood bank-stored red cells. Abnormal spectrin-protein 4.1-actin complex formation.
    J Clin Invest. 1986 Dec;78(6):1681-6 PMID: 3782475
  26. Erythrocyte membrane deformability and stability: two distinct membrane properties that are independently regulated by skeletal protein associations.
    J Cell Biol. 1986 Aug;103(2):343-50 PMID: 3733870
  27. Rotational diffusion of band 3 proteins in the human erythrocyte membrane.
    Nature. 1976 Sep 30;263(5576):389-93 PMID: 972675
  28. Red cell membrane skeletal defects in hereditary and acquired hemolytic anemias.
    Semin Hematol. 1983 Jul;20(3):189-224 PMID: 6353590
  29. Trapped by a skeleton--the maintenance of epithelial membrane domains.
    Bioessays. 1987 Oct;7(4):179-81 PMID: 2825661
  30. Elastic fracture in random materials.
    Phys Rev B Condens Matter. 1988 Apr 1;37(10):5500-5507 PMID: 9943739
  31. Lateral diffusion in an archipelago. Distance dependence of the diffusion coefficient.
    Biophys J. 1989 Sep;56(3):615-22 PMID: 2790141
  32. Effects of intracellular Ca2+ and proteolytic digestion of the membrane skeleton on the mechanical properties of the red blood cell membrane.
    Biochim Biophys Acta. 1987 Nov 27;905(1):181-94 PMID: 2445380
  33. A milling crowd model for local and long-range obstructed lateral diffusion. Mobility of excimeric probes in the membrane of intact erythrocytes.
    Biophys J. 1986 May;49(5):987-1001 PMID: 3778578
  34. Decreased membrane mechanical stability and in vivo loss of surface area reflect spectrin deficiencies in hereditary spherocytosis.
    J Clin Invest. 1988 Aug;82(2):617-23 PMID: 3403720
  35. Matrix control of protein diffusion in biological membranes.
    Proc Natl Acad Sci U S A. 1981 Jun;78(6):3576-80 PMID: 6943558
  36. Analysis of the self-association of human red cell spectrin.
    Biochemistry. 1986 Oct 7;25(20):5969-75 PMID: 3790499
  37. The spectrin network as a barrier to lateral diffusion in erythrocytes. A percolation analysis.
    Biophys J. 1989 Jan;55(1):21-8 PMID: 2930822
  38. Reductions of erythrocyte membrane viscoelastic coefficients reflect spectrin deficiencies in hereditary spherocytosis.
    J Clin Invest. 1988 Jan;81(1):133-41 PMID: 3335631
  39. Sulfhydryl reagents induce altered spectrin self-association, skeletal instability, and increased thermal sensitivity of red cells.
    Blood. 1983 Dec;62(6):1190-6 PMID: 6640108
  40. Effective-medium theory of percolation on central-force elastic networks.
    Phys Rev B Condens Matter. 1985 Jan 1;31(1):276-280 PMID: 9935421
  41. Viscoelastic properties of red cell membrane in hereditary elliptocytosis.
    Blood. 1989 Feb;73(2):592-5 PMID: 2917191
  42. Clinical disorders of the red cell membrane skeleton.
    Crit Rev Oncol Hematol. 1986;5(4):397-453 PMID: 2945665
  43. Dystrophin. The gene and its product.
    Nature. 1989 Jun 22;339(6226):584-6 PMID: 2660004
  44. Contributions of the beta-subunit to spectrin structure and function.
    Cell Motil Cytoskeleton. 1989;12(4):248-63 PMID: 2524283
  45. Defective spectrin dimer-dimer association in a family with transfusion dependent homozygous hereditary elliptocytosis.
    Br J Haematol. 1983 Jun;54(2):163-72 PMID: 6849840
  46. Membrane skeletal dynamics: role in modulation of red cell deformability, mobility of transmembrane proteins, and shape.
    Semin Hematol. 1983 Jul;20(3):175-88 PMID: 6353589
  47. Restriction of the lateral motion of band 3 in the erythrocyte membrane by the cytoskeletal network: dependence on spectrin association state.
    Biochemistry. 1986 Oct 7;25(20):6133-9 PMID: 3790510
  48. Human erythrocyte spectrin dimer intrinsic viscosity: temperature dependence and implications for the molecular basis of the erythrocyte membrane free energy.
    Biochim Biophys Acta. 1985 Jun 11;816(1):102-10 PMID: 4005229
  49. Clinical and laboratory study of two Caucasian families with hereditary pyropoikilocytosis and hereditary elliptocytosis.
    Am J Clin Pathol. 1987 Jul;88(1):58-65 PMID: 3604989
  50. The organization of proteins in the human red blood cell membrane. A review.
    J Cell Biol. 1974 Jul;62(1):1-19 PMID: 4600883
  51. Spectrin and related molecules.
    CRC Crit Rev Biochem. 1988;23(2):171-234 PMID: 3048888
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
1990-06-00
Pages
1167-77
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1280827
Subset
IM
Grants
NIGMS NIH HHS · GM38133 · United States
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