Loss of Rotational Mobility of Band 3 Proteins in Human Erythrocyte Membranes Induced by Antibodies to Glycophorin A

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 1995 May 1

PMID 7612830

Citations 11

Authors

A Che

R J Cherry

Affiliations

Soon will be listed here.

Abstract

The effect of antibodies to glycophorin A on the rotational diffusion of band 3 in human erythrocyte membranes was investigated by transient dichrosim. Three antibodies that recognize different epitopes on the exofacial domain of glycophorin A all strongly reduce the rotational mobility of band 3. The effect is at most only weakly dependent on the distance of the epitope from the membrane surface. The degree of immobilization obtained with two of the antibodies, BRIC14 and R18, is very similar to that produced by antibodies to band 3 itself. Similar results were obtained with membranes stripped of skeletal proteins. Fab fragments and an antibody to glycophorin C had no effect on band 3 rotational mobility. These results rule out a mechanism whereby band 3 rotational immobilization results from enhanced interactions with the membrane skeleton that are mediated by a conformational change in glycophorin A. Rather, they strongly indicate that the antibodies to glycophorin A cross-link existing band 3-glycophorin A complexes that have lifetimes that are long compared with the millisecond time scale of the transient dichroism measurements.

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References

Triche T, TILLACK T, Kornfeld S . Localization of the binding sites for the Ricinus communis, Agaricus bisporus and wheat germ lectins on human erythrocyte membranes. Biochim Biophys Acta. 1975; 394(4):540-9. DOI: 10.1016/0005-2736(75)90139-x. View

LOWRY O, ROSEBROUGH N, FARR A, RANDALL R . Protein measurement with the Folin phenol reagent. J Biol Chem. 1951; 193(1):265-75. View

Tomita M, Furthmayr H, Marchesi V . Primary structure of human erythrocyte glycophorin A. Isolation and characterization of peptides and complete amino acid sequence. Biochemistry. 1978; 17(22):4756-70. DOI: 10.1021/bi00615a025. View

Cherry R . Measurement of protein rotational diffusion in membranes by flash photolysis. Methods Enzymol. 1978; 54:47-61. DOI: 10.1016/s0076-6879(78)54007-x. View

Nigg E, Cherry R . Influence of temperature and cholesterol on the rotational diffusion of band 3 in the human erythrocyte membrane. Biochemistry. 1979; 18(16):3457-65. DOI: 10.1021/bi00583a004. View

Nigg E, Bron C, GIRARDET M, Cherry R . Band 3-glycophorin A association in erythrocyte membrane demonstrated by combining protein diffusion measurements with antibody-induced cross-linking. Biochemistry. 1980; 19(9):1887-93. DOI: 10.1021/bi00550a024. View

Nigg E, Cherry R . Anchorage of a band 3 population at the erythrocyte cytoplasmic membrane surface: protein rotational diffusion measurements. Proc Natl Acad Sci U S A. 1980; 77(8):4702-6. PMC: 349914. DOI: 10.1073/pnas.77.8.4702. View

Chasis J, Mohandas N, SHOHET S . Erythrocyte membrane rigidity induced by glycophorin A-ligand interaction. Evidence for a ligand-induced association between glycophorin A and skeletal proteins. J Clin Invest. 1985; 75(6):1919-26. PMC: 425549. DOI: 10.1172/JCI111907. View

Welsh E, Thom D, Morris E, Rees D . Molecular organization of glycophorin A: implications for membrane interactions. Biopolymers. 1985; 24(12):2301-32. DOI: 10.1002/bip.360241210. View

10.

Scheuring U, Kollewe K, Haase W, Schubert D . A new method for the reconstitution of the anion transport system of the human erythrocyte membrane. J Membr Biol. 1986; 90(2):123-35. DOI: 10.1007/BF01869930. View

11.

Hadley T, Erkmen Z, Kaufman B, Futrovsky S, McGuinnis M, Graves P . Factors influencing invasion of erythrocytes by Plasmodium falciparum parasites: the effects of an N-acetyl glucosamine neoglycoprotein and an anti-glycophorin A antibody. Am J Trop Med Hyg. 1986; 35(5):898-905. DOI: 10.4269/ajtmh.1986.35.898. View

12.

Chasis J, Reid M, Jensen R, Mohandas N . Signal transduction by glycophorin A: role of extracellular and cytoplasmic domains in a modulatable process. J Cell Biol. 1988; 107(4):1351-7. PMC: 2115236. DOI: 10.1083/jcb.107.4.1351. View

13.

Clague M, Harrison J, Cherry R . Cytoskeletal restraints of band 3 rotational mobility in human erythrocyte membranes. Biochim Biophys Acta. 1989; 981(1):43-50. DOI: 10.1016/0005-2736(89)90080-1. View

14.

Pasvol G, Chasis J, Mohandas N, Anstee D, Tanner M, Merry A . Inhibition of malarial parasite invasion by monoclonal antibodies against glycophorin A correlates with reduction in red cell membrane deformability. Blood. 1989; 74(5):1836-43. View

15.

Gardner B, Parsons S, Merry A, Anstee D . Epitopes on sialoglycoprotein alpha: evidence for heterogeneity in the molecule. Immunology. 1989; 68(2):283-9. PMC: 1385431. View

16.

Tilley L, Foley M, Anders R, Dluzewski A, Gratzer W, Jones G . Rotational dynamics of the integral membrane protein, band 3, as a probe of the membrane events associated with Plasmodium falciparum infections of human erythrocytes. Biochim Biophys Acta. 1990; 1025(2):135-42. DOI: 10.1016/0005-2736(90)90090-b. View

17.

Telen M, Chasis J . Relationship of the human erythrocyte Wrb antigen to an interaction between glycophorin A and band 3. Blood. 1990; 76(4):842-8. View

18.

Matayoshi E, Jovin T . Rotational diffusion of band 3 in erythrocyte membranes. 1. Comparison of ghosts and intact cells. Biochemistry. 1991; 30(14):3527-38. DOI: 10.1021/bi00228a025. View

19.

Mohandas N, Winardi R, Knowles D, Leung A, Parra M, George E . Molecular basis for membrane rigidity of hereditary ovalocytosis. A novel mechanism involving the cytoplasmic domain of band 3. J Clin Invest. 1992; 89(2):686-92. PMC: 442903. DOI: 10.1172/JCI115636. View

20.

Schofield A, Tanner M, Pinder J, Clough B, Bayley P, Nash G . Basis of unique red cell membrane properties in hereditary ovalocytosis. J Mol Biol. 1992; 223(4):949-58. DOI: 10.1016/0022-2836(92)90254-h. View