Skip to main content
SpringerLink
Log in

Decreased rotational diffusion of band 3 in melanesian ovalocytes from Papua, New Guinea

  • Articles
  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Summary

Melanesian ovalocytes from Papua New Guinea have an N-terminal extension of the band 3 polypeptide (Jones, G.L., Edmunson. H.M., Wesche, D., Saul, A. 1990.Biochim. Biophys. Acta 1096:33–40). The ovalocytes showed a threefold increase in shear elastic modulus as determined by micropipette aspiration measurements of membrane rigidity. Time-resolved phosphorescence anisotropy has been used to study the rotational freedom of band 3 in membranes prepared from ovalocytes. The ovalocytic polymorphism was found to be associated with a marked decrease in the rotational mobility of band 3. This may indicate participation of band 3 in large homoaggregates or in complexes with other proteins at the cytoplasmic surface. There was no morphological clustering of band 3 detectable by immunofluorescence microscopy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Becker, P.S., Lux, S.E. 1985. Hereditary spherocytosis and related disorders.Clin. Haematol. 14:15–19

    PubMed  Google Scholar 

  • Booth, P.B., Serjeantson, S., Woodfield, D.G., Amato, D. 1977. Selective depression of blood group antigens associated with hereditary ovalocytosis among Melanesians.Vox Sang. 32:99–110

    PubMed  Google Scholar 

  • Castelino, D., Saul, A., Myler, P., Kidson, C., Thomas, H., Cooke, R. 1981. Ovalocytosis in Papua New Guinea—dominantly inherited resistance to malaria.Southeast Asian J. Trop. Med. Public Health 12:549–555

    PubMed  Google Scholar 

  • Chasis, J.A., Mohandas, N. 1986. Erythrocyte membrane deformability and stability: Two distinct membrane properties that are independently regulated by skeletal protein associations.J. Cell Biol. 103:343–350

    PubMed  Google Scholar 

  • Cherry, R.J. 1978. Measurement of protein rotational diffusion in membranes by flash photolysis.Methods Enzymol. 54:47–61

    PubMed  Google Scholar 

  • Clague, M.J., Harrison, J.P., Cherry, R.J. 1989. Cytoskeletal restraints of band 3 rotational mobility in human erythrocyte membranes.Biochim. Biophys. Acta 981:43–50

    PubMed  Google Scholar 

  • Cooper, R.A. 1978. Influence of increased membrane cholesterol on membrane fluidity and cell function in human red blood cells.J. Supranol. Struct. 8:413–430

    Google Scholar 

  • Dluzewski, A.R., Rangahrachi, K., Wilson, R.J.M., Gratzer, W.B. 1983. A cytoplasmic requirement of red cells for invasion by malarial parasites.Mol. Biochem. Parasitol. 9:145–160

    PubMed  Google Scholar 

  • Dormandy, J., Flute, P., Matrai, A., Bogar, L., Mikita, J., Lowe, G.D.O., Anderson, J., Chien, S., Schmalzer, E., Herschenfeld, A. 1985. The new St. George's filtrometer.Clin. Haemorheol. 5:975–983

    Google Scholar 

  • Evans, E.A. 1983. Bending elastic modulus of red blood cell membrane derived from buckling instability in micropipette aspiration tests.Biophys. J. 43:27–30

    PubMed  Google Scholar 

  • Evans, E.A., La Celle, P. 1975. Intrinsic material properties of the erythrocyte membrane indicated by mechanical analysis of deformation.Blood 45:29–43

    PubMed  Google Scholar 

  • Hadley, T., Saul, A., Lamont, G., Hudson, D.E., Miller, L.H., Kidson, C. 1983. Resistance of Melanesian elliptocytes (ovalocytes) to invasion byPlasmodium falciparum andPlasmodium knowlesi malaria parasites in vitro.J. Clin. Invest. 71:780–782

    PubMed  Google Scholar 

  • Higashi, T., Richards, C.S., Uyeda, K. 1979. The interaction of phosphofructokinase with erythrocyte membranes.J. Biol. Chem. 254:9542–9550

    PubMed  Google Scholar 

  • Holt, M., Hogan, P.F., Nurse, G.T. 1981. The ovalocytosis polymorphism on the western border of Papua New Guinea.Hum. Biol. 53:22–34

    Google Scholar 

  • Jones, G.L. 1984. Red cell membrane proteins in Melanesian ovalocytosis-autophosphorylation and proteolysis.Proc. Aust. Biochem. Soc. 17:34

    Google Scholar 

  • Jones, G.L., Edmunson, H.M., Wesche, D., Saul, A. 1990. Human erythrocyte band 3 has an altered N-terminus in malaria resistant Melanesian ovalocytosis,Biochim. Biophys. Acta (in press)

  • Jovin, T.M., Bartholdi, M., Vaz, W.L.C., Austin, R.H. 1981. Rotational diffusion of biological macromolecules by timeresolved delayed luminescence (phosphorescence, fluorescence) anisotropy.Ann. N.Y. Acad. Sci. 366:176–196

    PubMed  Google Scholar 

  • Kay, M.M.B., Flowers, N., Goodman, J., Bosman, G. 1989. Alteration in membrane protein band 3 associated with accelerated erythrocyte aging.Proc. Natl. Acad. Sci. USA 86:5834–5838

    PubMed  Google Scholar 

  • Kidson, C., Lamont, G., Saul, A., Nurse, G. 1981. Ovalocytic erythrocytes from Melanesians are resistant to invasion by malaria parasites in culture.Proc. Natl. Acad. Sci. USA 78:5829–5832

    PubMed  Google Scholar 

  • Low, P.S. 1986. Structure and function of the cytoplasmic domain of band 3: Center of erythrocyte membrane-peripheral protein interactions.Biochim. Biophys. Acta 864:145–167

    PubMed  Google Scholar 

  • Low, P.S., Waugh, S.M., Zinke, K., Drenkhahn, D. 1985. The role of haemoglobin denaturation and band 3 clustering in red blood cell aging.Science 227:531–533

    PubMed  Google Scholar 

  • Lux, S.E., John, K.M., Kopito, R.R., Lodish, H.F. 1989. Cloning and characterization of band 3, the human erythrocyte anionexchange protein (AE1).Proc. Natl. Acad. Sci. USA 86:9089–9093

    PubMed  Google Scholar 

  • Marchesi, V.T. 1985. Stabilizing infrastructure of cell membranes.Annu. Rev. Cell Biol. 1:531–561

    PubMed  Google Scholar 

  • Matayoshi, E.D., Corin, A.F., Zidovetski, R., Sawyer, W.H., Jovin, T.M. 1983. Rotational dynamics of cell surface proteins by time-resolved phosphorescence anisotropy.In: Mobility and Recognition in Cell Biology. H. Sund and C. Veeger, editors. pp. 119–125. De Gruyter, Berlin

    Google Scholar 

  • Miller, L.H., Haynes, J.D., McAuliffe, F.M., Shiroish, T., Durocher, J.R., McGuinniss, M.H. 1977. Evidence for differences in erythrocyte surface receptors for the malarial parasites,Plasmodium falciparum andPlasmodium knowlesi.J. Exp. Med. 146:277–281

    PubMed  Google Scholar 

  • Mueller, T.J., Morrison, M. 1977. Detection of a variant protein 3, the major transmembrane protein of the human erythrocyte.J. Biol. Chem. 252:6573–6576

    PubMed  Google Scholar 

  • Nash, G.B., Johnson, C.S., Meiselman, H.J. 1986. Influence of oxygen tension on the viscoelastic behavior of red blood cells in sickle cell disease.Blood 67:110–118

    PubMed  Google Scholar 

  • Nigg, E.A., Cherry, R.J. 1979. Influence of temperature and cholesterol on the rotational diffusion of band 3 in the human erythrocyte membrane.Biochemistry 18:3457–3465

    PubMed  Google Scholar 

  • Pasternak, G.R., Anderson, R.A., Leto, T.L., Marchesi, V.T. 1985. Interactions between protein 4.1 and band 3.J. Biol. Chem. 260:3676–3683

    PubMed  Google Scholar 

  • Ranney, H.M., Rosenberg, G.H., Morrison, M., Mueller, T.J. 1990. Frequencies of band 3 variants of human red cell membranes in some different populations.Br. J. Haematol. 76:262–267

    Google Scholar 

  • Restall, C.J., Dale, R.E., Murray, E.K., Gilbert, C.W., Chapman, D. 1984. Rotational diffusion of calcium-dependent adenosine-5′-triphosphatase in sarcoplasmic reticulum: A detailed study.Biochemistry 23:6765–6776

    PubMed  Google Scholar 

  • Saul, A., Lamont, G., Sawyer, W.H., Kidson, C. 1984. Decreased membrane deformability in Melanesian ovalocytes from Papua New Guinea.J. Cell Biol. 98:1348–1354

    PubMed  Google Scholar 

  • Schlüter, K., Drenckhahn, D. 1986. Co-clustering of denatured haemoglobin with band 3: Its role in binding of autoantibodies against band 3 to abnormal and aged erythrocytes.Proc. Natl. Acad. Sci. USA 83:6137–6141

    PubMed  Google Scholar 

  • Serjeantson, S., Bryson, K., Amato, D., Babona, D. 1977. Malaria and hereditary ovalocytosis.Hum. Genet. 37:161–167

    PubMed  Google Scholar 

  • Tilley, L., Foley, M., Anders, R.F., Dluzewski, A.R., Gratzer, W.B., Jones, G.L., Sawyer, W.H. 1990. Rotational dynamics of the integral membrane protein, band 3, as a probe of the membrane events associated withPlasmodium falciparum infections of human erythrocytes.Biochim. Biophys. Acta 1025:135–142

    PubMed  Google Scholar 

  • Tilley, L., Sawyer, W.H., Morrison, J.R., Fidge, N.H. 1988. Rotational diffusion of human lipoproteins by time-resolved phosphorescence anisotropy.J. Biol. Chem. 263:17541–17547

    PubMed  Google Scholar 

  • Tsai, I.-H., Prasanna-Murthy, S.N., Steck, T.L. 1982. Effect of red cell membrane binding on the catalytic activity of glyceraldehyde-3-phosphate dehydrogenase.J. Biol. Chem. 257:1438–1442

    PubMed  Google Scholar 

  • Tsuji, A., Kawasaki, K., Ohnishi, S.-I., Merkle, H., Kusumi, A. 1988. Regulation of band 3 mobilities in erythrocyte ghost membranes by protein association and cytoskeletal meshwork.Biochemistry 27:7447–7452

    PubMed  Google Scholar 

  • Walder, J.A., Chatterjee, R., Steck, T.L., Low, P.S., Musso, G.F., Kaiser, E.T., Rogers, P.H., Arnone, A. 1984. The interaction of haemoglobin with the cytoplasmic domain of band 3 of the human erythrocyte membrane.J. Biol. Chem. 259:10238–10246

    PubMed  Google Scholar 

  • Waugh, R.E., Agre, P. 1988. Reduction of erythrocyte membrane viscoelastic coefficients reflect deficiencies in hereditary spherocytosis.J. Clin. Invest. 81:133–141

    PubMed  Google Scholar 

  • Willardson, B.M., Thevenin, B.J.-M., Harrison, M.L., Kuster, W.M., Benson, M.D., Low, P.S. 1989. Localisation of the ankyrin-binding site on erythrocyte membrane protein. band 3.J. Biol. Chem. 264:15893–15999

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry, La Trobe University, 3083, Bundoora, Victoria, Australia

    Leann Tilley

  2. Department of Haematology, The Medical School, University of Birmingham, Birmingham, United Kingdom

    Gerard B. Nash

  3. Queensland Institute of Medical Research, 4006, Herston, Queensland, Australia

    Graham L. Jones

  4. Department of Biochemistry, University of Melbourne, 3052, Parkville, Victoria, Australia

    William H. Sawyer

Authors
  1. Leann Tilley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gerard B. Nash
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Graham L. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. William H. Sawyer
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tilley, L., Nash, G.B., Jones, G.L. et al. Decreased rotational diffusion of band 3 in melanesian ovalocytes from Papua, New Guinea. J. Membrain Biol. 121, 59–66 (1991). https://doi.org/10.1007/BF01870651

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01870651

Key Words

Search

Navigation