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Identification of differences between the surface proteins and glycoproteins of normal mouse (Balb/c) and human erythrocytes

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Summary

The topography of the external surface of the Balb/c mouse erythrocyte has been investigated and compared to the human erythrocyte by using a series of protein radiolabeling probes. After sodium dodecyl sulfate-polyacrylamide gel electrophoresis, the pattern of Coomassie Blue stained proteins was very similar for mouse and human erythrocyte ghosts, as was the distribution of radioactivity in protein bands after lactoperoxidase catalyzed radioiodination. The mouse erythrocyte glycoproteins identified by periodic-acid-Schiff and ‘Stains-All’ reagents, sialic acid analysis of gel slices, binding of125I-wheat germ agglutinin and125I-concanavalin A to the gels, and glycoprotein radiolabeling techniques, differed markedly from the sets of proteins labeled by radioiodination, and also differed from the human erythrocyte glycoproteins. Instead of the PAS I to PAS IV series of sialoglycoproteins characteristic of human erythrocytes, the mouse erythrocyte possesses a broad band of sialoglycoproteins with several peaks ranging in mol wt from 65,000 to 32,000. The same group of sialoglycoproteins were labeled by the periodate/B3H4 − technique specific for terminal sialic acid, and the galactose oxidase/B3H4 − method (plus neuraminidase) specific for galactosyl/N-acetylgalactosaminyl residues penultimate to sialic acid. These results emphasize the necessity to employ a variety of protein radiolabeling probes based on different labeling specificities, to study the membrane topography of cells which are poorly understood compared to the human erythrocyte membrane.

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References

  1. Aminoff, D., Bell, W.C., Fulton, I., Ingerbrigtsen, N. 1977. Effect of sialidase on the viability of erythrocytes in circulation.Am. J. Hematol. 1:419

    Google Scholar 

  2. Bell, W.C., Levy, G.N., Williams, R., Aminoff, D. 1977. Effect of galactose oxidase, with and without prior sialidase treatment, of the viability of erythrocytes in circulation.Proc. Nat. Acad. Sci. USA 74:4205

    PubMed  Google Scholar 

  3. Bender, W.W., Garan, H., Berg, H.C. 1971. Proteins of the human erythrocyte membrane as modified by Pronase.J. Mol. Biol. 58:783

    PubMed  Google Scholar 

  4. Blumenfeld, O.O., Gallop, P.M., Liao, T.-H. 1972. Modification and introduction of a specific radioactive label into the erythrocyte membrane sialoglycoproteins.Biochem. Biophys. Res. Commun. 48:242

    PubMed  Google Scholar 

  5. Bonner, W.M., Laskey, R.A. 1974. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels.Eur. J. Biochem. 46:83

    PubMed  Google Scholar 

  6. Bosmann, H.B. 1971. Red cell hydrolases: Glycosidase activities in human erythrocyte plasma membranes.J. Membrane Biol. 4:113

    Google Scholar 

  7. Bosmann, H.B. 1974. Red cell hydrolases. 3. Neuraminidase activity in isolated human erythrocyte plasma membranes.Vox Sang. 26:497

    PubMed  Google Scholar 

  8. Boxer, D.H., Jenkins, R.E., Tanner, M.J.A. 1974. The organization of the major protein in the human erythrocyte membrane.Biochem. J. 137:531

    PubMed  Google Scholar 

  9. Bretscher, M.S. 1971. Major human erythrocyte glycoprotein spans the cell membrane.Nature New Biol. 231:229

    PubMed  Google Scholar 

  10. Bretscher, M.S. 1971. Human erythrocyte membranes: Specific labelling of surface proteins.J. Mol. Biol. 58:775

    PubMed  Google Scholar 

  11. Bretscher, M.S. 1973. Membrane structure: Some general principles.Science 181:622

    PubMed  Google Scholar 

  12. Brown, K.N., Brown, I.N., Trigg, P.I., Phillips, R.S., Hills, L.A. 1970. Immunity to malaria. II. Serological response of monkeys sensitized by drug-suppressed infection or by dead parasitized cells in Freund's complete adjuvant.Exp. Parasitol. 28:318

    PubMed  Google Scholar 

  13. Carraway, K.L., Colton, D.G., Shin, B.C., Triplett, R.B. 1975. Species variability in the modification of erythrocyte surface proteins by enzymatic probes.Biochim. Biophys. Acta 382:181

    PubMed  Google Scholar 

  14. Chang, H., Langer, P.J., Lodish, H.F. 1976. Asynchronous synthesis of erythrocyte membrane proteins.Proc. Nat. Acad. Sci. USA 73:3206

    PubMed  Google Scholar 

  15. Conrad, M.J., Penniston, J.T. 1974. Surface proteins of the erythrocyte membrane. Effect of ageing.Vox Sang. 26:1

    PubMed  Google Scholar 

  16. Cunliffe, D.A., Cox, K.O. 1978. Effects of bromelain and pronase on erythrocyte membranes.Immunochemistry (in press)

  17. Curnow, J.A. 1968.In vitro agglutination of bovine erythrocytes infected with.Babesia argentina. Nature (London) 217:267

    Google Scholar 

  18. Demus, H., Mehl, E. 1970. The protein components of the erythrocyte membrane and their molecular weights.Biochim. Biophys. Acta 203:291

    PubMed  Google Scholar 

  19. Dodge, J.T., Mitchell, C., Hanahan, D.J. 1963. The preparation and chemical characteristics of hemoglobin-free ghosts of human erythrocytes.Arch. Biochem. 100:119

    PubMed  Google Scholar 

  20. Durocher, J.R., Payne, R.C., Conrad, M.E. 1975. Role of sialic acid in erythrocyte survival.Blood 45:11

    PubMed  Google Scholar 

  21. Fairbanks, G., Steck, T.L., Wallach, D.F.H. 1971. Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane.Biochemistry 10:2606.

    PubMed  Google Scholar 

  22. Fehlman, M., Lafleur, L., Marceau, N. 1975. Major changes in surface membrane proteins during erythropoiesis.Biochem. Biophys. Res. Commun. 66:322

    PubMed  Google Scholar 

  23. Fehlman, M., Lafleur, L., Marceau, N. 1976. Surface membrane differentiation of hemopoietic cells as observed by radioactive labeling.J. Cell. Physiol. 90:455

    Google Scholar 

  24. Furthmayr, H., Marchesi, V. 1976. Subunit structure of human erythrocyte Glycophorin A.Biochemistry 15:1137

    PubMed  Google Scholar 

  25. Gahmberg, C.G. 1976. External labeling of human erythrocyte glycoproteins.J. Biol. Chem. 251:510

    PubMed  Google Scholar 

  26. Gahmberg, C.G., Andersson, L.C. 1977. Selective radioactive labeling of cell surface sialoglycoproteins by periodate-tritiated borohydride.J. Biol. Chem. 252:5888

    PubMed  Google Scholar 

  27. Gahmberg, C.G., Hakomori, S. 1973. External labeling of cell surface galactose and galactosamine in glycolipid and glycoprotein of human erythrocytes.J. Biol. Chem. 248:4311

    PubMed  Google Scholar 

  28. Gahmberg, C.G., Hayry, P., Andersson, L.C. 1976. Characterization of surface glycoproteins of mouse lymphoid cells.J. Cell Biol. 68:642

    PubMed  Google Scholar 

  29. Gahmberg, C.G., Myllyla, G., Leikola, J., Pirkola, A., Nordling, S. 1976. Absence of the major sialoglycoprotein in the membrane of human En(a-) erythrocytes and increased glycosylation of Band 3.J. Biol. Chem. 251:6108

    PubMed  Google Scholar 

  30. Gattegno, L., Bladier, D., Cornillot, P. 1974. The role of sialic acid in the determination of survival of tabbit erythrocytes in the circulation.Carbohydr. Res. 34:361

    PubMed  Google Scholar 

  31. Gattegno, L., Bladier, D., Cornillot, P. 1975. Ageingin vivo and neuraminidase treatment of rabbit erythrocytes: Influence on half-life as assessed by Cr labelling.Hoppe Seyler's Z. Physiol. Chem. 356:391

    PubMed  Google Scholar 

  32. Glass, J., Fischer, S., Lavidor, L.M., Nunez, T. 1975. External surface membrane proteins in developing murine erythroid cells.Clin. Res. 23:274A

    Google Scholar 

  33. Glossman, H., Neville, D.M., Jr. 1971. Glycoproteins of cell surfaces. A comparative study of three different cell surfaces of the rat.J. Biol. Chem. 246:6339

    PubMed  Google Scholar 

  34. Gregoriadis, G., Putman, D., Louis, L., Neerunjun, D. 1974. Comparative effect and fate of non-entrapped and liposome-entrapped neuraminidase injected into rats.Biochem. J. 140:323

    PubMed  Google Scholar 

  35. Gurd, J.W., Evans, W.H. 1976. Identification of liver plasma membrane glycoproteins which bind to125I-labelled concanavalin A following electrophoresis in sodium dodecyl sulfate.Can J. Biochem 54:477

    PubMed  Google Scholar 

  36. Hamaguchi, H., Cleve, H. 1972. Solubilization and comparative analysis of mammalian erythrocyte membrane glycoproteins.Biochem. Biophys. Res. Commun. 47:459

    PubMed  Google Scholar 

  37. Hammon, K.S., Papermaster, D.S. 1976. Fluorometric assay of sialic acid in the picomole range: A modification of the thiobarbituric acid assay.Anal. Biochem. 74:292

    PubMed  Google Scholar 

  38. Hartree, E.F. 1972. Determination of protein: A modification of the Lowry method that gives a linear photometric response.Anal. Biochem. 48:422

    PubMed  Google Scholar 

  39. Howard, R.J., Smith, P.M., Mitchell, G.F. 1978. Removal of leucocytes from red cells inPlasmodium berghei-infected mouse blood and purification of schizont-infected cells.Ann. Trop. Med. Parasit (in press)

  40. Hubbard, A.L., Cohn, Z.A. 1972. The enzymatic iodination of the red cell membrane.J. Cell Biol. 55:390

    PubMed  Google Scholar 

  41. Hunter, W.M., Greenwood, F.C. 1962. Preparation of iodine-131 labelled human growth hormone of high specific activity.Nature (London) 194:495

    Google Scholar 

  42. Jancik, J., Schauer, R., Streicher, H.J. 1975. Influence of membrane-bound N-acetylneuraminic acid on the survival of erythrocytes in man.Hoppe Seyler's Z. Physiol. Chem. 356:1329

    PubMed  Google Scholar 

  43. Juliano, R.L. 1973. The proteins of the erythrocyte membrane.Biochim. Biophys. Acta 300:341

    PubMed  Google Scholar 

  44. Kathan, R.H., Winzler, R.J., Johnson, C.A. 1961. Preparation of an inhibitor of viral hemagglutination from human erythrocytes.J. Exp. Med. 113:37

    PubMed  Google Scholar 

  45. King, L.E., Jr., Morrison, M. 1976. The visualization of human erythrocyte membrane proteins and glycoproteins in SDS polyacrylamide gels employing a single staining procedure.Anal. Biochem. 71:223

    PubMed  Google Scholar 

  46. Kobylka, D., Khettry, A., Shin, B.C., Carraway, B.C. 1972. Proteins and glycoproteins of the erythrocyte membrane.J. Arch. Biochem. Biophys. 148:475

    Google Scholar 

  47. Koch, P., Gardner, F.H., Carter, J.R. 1973. Red cell maturation: Loss of a reticulocyte-specific membrane protein.Biochem. Biophys. Res. Commun. 54:1296

    PubMed  Google Scholar 

  48. Laemmli, U.K., Favre, M. 1973. Maturation of the head of bacteriophage T4. I. DNA packaging events.J. Mol. Biol. 80:575

    PubMed  Google Scholar 

  49. Lenard, J. 1970. Protein components of erythrocyte membranes from different animal species.Biochemistry 9:5037

    PubMed  Google Scholar 

  50. Liao, T.-H., Gallop, P.M., Blumenfeld, O.O. 1973. Modification of the sialyl residues of sialoglycoprotein(s) of the human erythrocyte surface.J. Biol. Chem. 248:8247

    PubMed  Google Scholar 

  51. Lotan, R., Lis, H., Rosenwasser, A., Novogrodsky, A., Sharon, N. 1973. Enhancement of the biological activities of soybean agglutinin by cross-linking with glutaraldehyde.Biochem. Biophys. Res. Commun. 55:1347

    PubMed  Google Scholar 

  52. Maddy, A.H. 1966. The properties of the protein of the plasma membrane of ox erythrocytes.Biochim. Biophys. Acta 117:193

    PubMed  Google Scholar 

  53. Marchesi, V.T., Tillack, T.W., Jackson, R.L., Segrest, J.P., Scott, R.E. 1972. Chemical characterization and surface orientation of the major glycoprotein of the human erythrocyte membrane.Proc. Nat. Acad. Sci. USA 69:1445

    PubMed  Google Scholar 

  54. Marton, L., Garvin, J. 1973. Subunit structure of the major human erythrocyte glyco-protein: Depolymerization by heating ghosts with sodium dodecyl sulfate.Biochem. Biophys. Res. Commun. 52:1457

    PubMed  Google Scholar 

  55. Miller, L.H. 1977. Hypothesis on the mechanism of erythrocyte invasion by malaria merozoites.Bulletin of the World Health Organization 55:155

    PubMed  Google Scholar 

  56. Mitchell, G.F., Hogarth-Scott, R.S., Edwards, R.D., Lewers, H.M., Cousins, G., Moore, T. 1976. Studies on immune response to parasite antigens in mice. I.Ascaris Suum larvae numbers and antiphosphorylchaline responses in infected mice of various strains and in hypothymic (nu/nu) mice.Int. Arch. Allergy Appl. Immunol. 52:64

    PubMed  Google Scholar 

  57. Morrison, M., Michaels, A.W., Phillips, D.R., Choi, S.-I. 1974. Life span of erythrocyte membrane protein.Nature (London) 248:763

    Google Scholar 

  58. Morrison, M., Mueller, T.J., Huber, C.T. 1974. Transmembrane orientation of the glycoproteins in normal human erythrocytes.J. Biol. Chem. 249:2658

    PubMed  Google Scholar 

  59. Morton, J.A., Pickles, M.M., Sutton, L. 1969. The correlation of the Bga blood group with the HL-47 leucocyte group: Demonstration of antigenic sites on red cells and leucocytes.Vox. Sang. 17:536

    PubMed  Google Scholar 

  60. Morton, J.A., Pickles, M.M., Sutton, L., Skoy, F. 1971. Identification of further antigen on red cells and lymphocytes. Association of BgB with W17 (Te57) and Bge with W28 (Da 15, Ba).Vox Sang. 21:141

    PubMed  Google Scholar 

  61. Mueller, T.J., Dow, A.W., Morrison, M. 1976. Heterogeneity of the sialoglycoproteins of the normal human erythrocyte membrane.Biochem. Biophys. Res. Commun. 72:94

    PubMed  Google Scholar 

  62. Mueller, T.J., Morrison, M. 1974. The transmembrane proteins in the plasma membrane of normal human erythrocytes.J. Biol. Chem. 249:7568

    PubMed  Google Scholar 

  63. Niehaus, W.G., Jr., Wold, F. 1970. Cross-linking of erythrocyte membranes with dimethyl adipimidate.Biochim. Biophys. Acta 196:170

    PubMed  Google Scholar 

  64. Nordhagen, R., Orjasaeter, H. 1974. Assocation between HLA and red cell antigens. An autoanalyzer study.Vox Sang. 26:97

    PubMed  Google Scholar 

  65. Phillips, D.R., Morrison, M., 1970. The arrangement of proteins in the human erythrocyte membrane.Biochem. Biophys. Res. Commun. 40:284

    PubMed  Google Scholar 

  66. Phillips, D.R., Morrison, M. 1971. Exterior proteins on the human erythrocyte membrane.Biochem. Biophys. Res. Commun. 45:1103

    PubMed  Google Scholar 

  67. Potempa, L.A., Garvin, J.E. 1976. A third form of the major glycoprotein of the human erythrocyte membrane in sodium dodecyl sulfate: Electrophoresis as band PAS-4 at high ionic strength.Biochem. Biophys. Res. Commun. 72:1049

    PubMed  Google Scholar 

  68. Reichstein, E., Blostein, R. 1975. Arrangement of human erythrocyte membrane proteins.J. Biol. Chem. 250:6256

    PubMed  Google Scholar 

  69. Robinson, P.J., Bull, F.G., Anderton, B.H., Roitt, I.M. 1975. Direct autoradiographic visualization in SDS-gels of lectin-binding components of the human erythrocyte membrane.FEBS Lett. 58:330

    PubMed  Google Scholar 

  70. Rubin, R.W., Milikowski, C. 1978. Over two hundred polypeptides resolved from the human erythrocyte membrane.Biochim. Biophys. Acta 509:100

    PubMed  Google Scholar 

  71. Saslaw, L.D., Corwin, L.M., Waravdekar, U.S. 1966. Production of chromophoric substances in the thiobarbituric acid tests.Arch. Biochem. Biophys. 114:61

    PubMed  Google Scholar 

  72. Schauer, R. 1973. Chemistry and biology of the acylneuraminic acids.Angew. Chem. Int. Ed. Engl. 12:127

    PubMed  Google Scholar 

  73. Schauer, R., Buscher, H.P., Casals-Stenzel, J. 1974. Sialic acids: Their analysis and enzymic modification in relation to the synthesis of submandibular-gland glycoproteins.Biochem. Soc. Symp. 40:87

    PubMed  Google Scholar 

  74. Schauer, R., Faillard, H. 1968. Das Verhalten isomerer N.O.-Diacetyl-neuramin säureglykoside im Submaxillarismucin von Pferd und Rind bei Einwirkung bakterieller Neuraminidase.Hoppe Seyler's Z. Physiol. Chem. 349:961

    PubMed  Google Scholar 

  75. Schroeder, W.F., Cox, H.W., Ristic, M. 1966. Anaemia, parasitemia, erythrophagocytosis, and haemagglutinins inBabesia rodhaini infection.Ann. Trop. Med. Parasit. 60:31

    PubMed  Google Scholar 

  76. Schulte, T.H., Marchesi, V.T. 1978. Self association of human erythrocyte Glycophorin A. Appearance of low mobility bands on sodium dodecyl sulfate gels.Biochim. Biophys. Acta 508:425

    PubMed  Google Scholar 

  77. Sears, D.A., Friedman, J.M., George, N.N. 1977. Topography of the external surface of the human red blood cell membrane studied with a nonpenetrating label[125]I diazodiiodosulfanilic acid.J. Biol. Chem. 252:712

    PubMed  Google Scholar 

  78. Segrest, J.R., Jackson, R.L., Andrews, E.P., Marchesi, V.T. 1971. Human erythrocyte membrane glycoprotein: A re-evaluation of molecular weight as determined by SDS polyacrylamide gel electrophoresis.Biochem. Biophys. Res. Commun. 44:390

    PubMed  Google Scholar 

  79. Shin, B.C., Carraway, K.L. 1974. Lactoperoxidase labeling of erythrocyte membranes from the inside and outside.Biochim. Biophys. Acta. 345:141

    PubMed  Google Scholar 

  80. Silverberg, M., Furthmayr, H., Marchesi, V. 1976. The effect of carboxymethylating a single methionine residue on the subunit interactions of Glycophorin A.Biochemistry 15:1448

    PubMed  Google Scholar 

  81. Snell, G.D. 1968. The H-2 locus of the mouse: Observation and speculations concerning its comparative genetics and its polymorphism.Folia Biologica 14:335

    PubMed  Google Scholar 

  82. Steck, T.L. 1974. The organization of proteins in the human red blood cell membrane.J. Cell Biol. 62:1

    PubMed  Google Scholar 

  83. Steck, T.L., Dawson, G. 1974. Topographical distribution of complex carbohydrates in the erythrocyte membrane.J. Biol. Chem. 249:2135

    PubMed  Google Scholar 

  84. Swanstrom, R., Shank, P.R. 1978. X-ray intensifying screens greatly enhance the detection by autoradiography of the radioactive isotopes32P and125I.Anal. Biochem. 86:184

    PubMed  Google Scholar 

  85. Tanner, M.J.A., Anstee, D.J., Judson, P.A. 1977. A carbohydrate-deficient membrane glycoprotein in human erythrocytes of phenotype S-s-.Biochem. J. 165:157

    PubMed  Google Scholar 

  86. Trigg, P.I., Hirst, S.I., Shakespeare, P.G., Tappenden, L. 1977. Labelling of membrane glycoprotein in erythrocytes infected withPlasmodium knowlesi.Bull. World Health Org. 55:205

    PubMed  Google Scholar 

  87. Triplett, R.B., Carraway, K.L. 1972. Proteolytic digestion of erythrocytes, resealed ghosts, and isolated membranes.Biochemistry 11:2897

    PubMed  Google Scholar 

  88. Tsai, C.-M., Huang, C.-C., Canellakis, E.S. 1973. Iodination of cell membranes. I. Optimal conditions for the iodination of exposed membrane components.Biochim. Biophys. Acta 332:47

    Google Scholar 

  89. Wallach, D.F.H. 1972. The dispositions of proteins in the plasma membranes of animal cells: Analytical approaches using controlled peptidolysis and protein labels.Biochim. Biophys. Acta 265:61

    PubMed  Google Scholar 

  90. Wallach, D.F.H., Conley, M. 1977. Altered membrane proteins of monkey erythrocytes infected with simian malaria.J. Mol. Med. 2:119

    Google Scholar 

  91. Zwaal, R.F.A., Van Deenen, L.L.M. 1968. Protein patterns of red cell membranes from different mammalian species.Biochim. Biophys. Acta 163:44

    PubMed  Google Scholar 

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  1. Russell J. Howard

    Present address: Malaria Section, N.I.A.I.D., National Institutes of Health, 20014, Bethesda, MD

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  1. Immunoparasitology Laboratory, The Walter and Eliza Hall Institute of Medical Research, Parkville, 3050, Melbourne, Victoria, Australia

    Russell J. Howard, Patricia M. Smith & Graham F. Mitchell

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Howard, R.J., Smith, P.M. & Mitchell, G.F. Identification of differences between the surface proteins and glycoproteins of normal mouse (Balb/c) and human erythrocytes. J. Membrain Biol. 49, 171–198 (1979). https://doi.org/10.1007/BF01868724

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