Function and Structure of the Red Blood Cell Cytoskeleton

  • Makoto Nakao
Part of the Blood Cell Biochemistry book series (BLBI, volume 1)

Abstract

Mature red blood cells of mammals consist only of cytoplasm and a cell membrane: they lack nucleus, mitochondria, and all other organelles. Cytoplasm contains all enzymes of glycolysis and the hexose monophosphate shunt, and some of those for nucleoside and nucleotide metabolism. These systems provide energy-rich phosphate as ATP and reducing power as NADH and NADPH, as in any other cell. Since most of the synthetic systems for biochemical compounds are lacking in red cells, ATP is mostly consumed on the cell membrane, except for priming to pump glycolysis. The erythrocyte membrane usually obtained by osmotic hemolysis is composed of a lipid bilayer and a fibrous undercoat structure; the latter is generally classified as a part of the cytoskeleton.

Keywords

Lipid Bilayer Erythrocyte Membrane Human Erythrocyte Erythrocyte Ghost Membrane Skeleton 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

ACD blood

blood preserved with acid—citrate—dextrose (NIH formula A)

PCD blood

blood preserved with phosphate—citrate—dextrose

Hb

hemoglobin

PC

phosphatidylcholine

PE

phosphatidylethanolamine

PS

phosphatidylserine

PI

phosphatidylinositol

WGA

wheat germ agglutinin.

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References

  1. Anderson, D. R., Davis, J. L., and Larraway, K. L., 1977, Calcium-promoted changes of the human erythrocyte membrane. Involvement of spectrin, transglutaminase and a membrane bound proteinase, J. Biol. Chem. 252: 6617–6623.PubMedGoogle Scholar
  2. Anderson, J. P., and Morrow, J. S., 1987, The interaction of calmodulin with human erythrocyte spectrin. Inhibition of protein 4.1-stimulated actin binding, J. Biol. Chem. 262: 6365–6372.PubMedGoogle Scholar
  3. Anderson, R. A., and Lovrien, R. E., 1981, Erythrocyte sidedness in lectin control of the Ca-A23187 mediated discocyte—echinocyte conversion, Nature 292: 158–161.PubMedCrossRefGoogle Scholar
  4. Anderson, R. A., and Lovrien, R. E., 1984, Glycophorin is linked by band 4.1 protein to the human erythrocyte membrane skeleton, Nature 307: 655–658.PubMedCrossRefGoogle Scholar
  5. Anderson, R. A., and Marchesi, V. T., 1985, Regulation of the association of membrane skeletal protein 4.1 with glycophorin by a polyphosphoinositide, Nature 318: 295–298.PubMedCrossRefGoogle Scholar
  6. Avissar, N., Inbal, A., Rabizadeh, E., Shaklai, M., and Shaklai, N., 1984, Interaction of spectrin with hemin disaggregates spectrin associations, Biochem. Mt. 8: 113–120.Google Scholar
  7. Baess, B. U., and Vincenzi, F. F., 1980, Calmodulin activation of red blood cell (Ca2± + Mg2±)-ATPase and its antagonism by phenothiazine, Mol. Pharmacol. 18: 253–258.Google Scholar
  8. Beaven, G. H., Jean-Baptiste, L., Ungewickell, E., Baines, A. J., Shahbakhti, F., Pinder, J. C., Lux, S. E., and Gratzer, W. B., 1985, An examination of the soluble oligomeric complexes extracted from the red cell membrane and their relation to the membrane cytoskeleton, Eur. J. Cell Biol. 36: 299–306.PubMedGoogle Scholar
  9. Bennett, V., 1978, Purification of an active proteolytic fragment of the membrane attachment site for human erythrocyte spectrin, J. Biol. Chem. 253: 2292–2299.PubMedGoogle Scholar
  10. Bennett, V., 1982, Isolation of an ankyrin—band 3 oligomer from human erythrocyte membranes, Biochim. Biophys. Acta 689: 475–484.PubMedCrossRefGoogle Scholar
  11. Bennett, V., 1985, The membrane skeleton of human erythrocytes and its implications for more complex cells, Annu. Rev. Biochem. 54: 273–304.PubMedCrossRefGoogle Scholar
  12. Bennett, V., 1989, The spectrin—actin junction of erythrocyte membrane skeleton, Biochim. Biophys. Acta 988: 107–121.PubMedCrossRefGoogle Scholar
  13. Bennett, V., and Branton, D., 1977, Selective association of spectrin with the cytoplasmic surface of human erythrocyte plasma membranes, J. Biol. Chem. 252: 2753–2763.PubMedGoogle Scholar
  14. Bennett, V., and Stenbuck, P. J., 1979, Identification and partial purification of ankyrin, the high affinity membrane attachment site for human erythrocyte spectrin, J. Biol. Chem. 254: 2533–2541.PubMedGoogle Scholar
  15. Bennett, V., and Stenbuck, P. J., 1980, Association between ankyrin and the cytoplasmic domain of band 3 isolated from the human erythrocyte membrane, J. Biol. Chem. 255: 6424–6432.Google Scholar
  16. Bennett, V., Gardner, K., and Steiner, J. P., 1988, Brain adducin: A protein kinase C substrate that may mediate site-directed assembly at the spectrin—actin junction, J. Biol. Chem. 263: 5860–5869.PubMedGoogle Scholar
  17. Birchmyer, W., and Singer, S. J., 1977, On the mechanism of ATP-induced shape changes in human erythrocyte membranes. II. The role of ATP, J. Cell Biol. 73: 647–659.CrossRefGoogle Scholar
  18. Brenner, S., and Korn, E., 1980, Spectrin/actin complex isolated from sheep erythrocytes: Actin polymerization by simple nucleation, J. Biol. Chem. 255: 1670–1676.PubMedGoogle Scholar
  19. Burns, N. R., and Gratzer, W. B., 1985, Interaction of calmodulin with the red cell and its membrane skeleton and with spectrin, Biochemistry 24: 3070–3074.PubMedCrossRefGoogle Scholar
  20. Byers, J.,and Branton, D., 1985, Visualization of the protein associations in the erythrocyte membrane skeleton, Proc. Natl. Acad. Sci. USA 82:6153–6157.Google Scholar
  21. Calvez, J. Y., Zachowski, A., Herrmann, A., Morrot, G., and Devaux, P. F., 1988, Asymmetric distribution of phospholipids in spectrin-poor erythrocyte vesicles, Biochemistry 27: 5666–5670.PubMedCrossRefGoogle Scholar
  22. Carter, D. P., and Fairbanks, G., 1984, Inhibition of erythrocyte membrane shape change by band 3 cytoplasmic fragment, J. Cellular Biochem. 24: 385–393.CrossRefGoogle Scholar
  23. Chasis, J. A., and 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.PubMedCrossRefGoogle Scholar
  24. Church, A., Fairbanks, G., and Palek, J., 1975, Role of calcium in spectrin retention by ghosts of fresh and ATP depleted erythrocytes, Blood 46: 1004.Google Scholar
  25. Cohen, A. M., Liu, S.-C., Derick, L. H., and Palek, J., 1986, Ultrastructural studies of the interaction of spectrin with phosphatidylserine liposomes, Blood 68: 920–926.PubMedGoogle Scholar
  26. Cohen, A. M., Liu, S.-C., Lawler, J., Derick, L., and Palek, J., 1988, Identification of the protein 4.1 binding site to phosphatidylserine vesicles, Biochemistry 27: 614–619.PubMedCrossRefGoogle Scholar
  27. Cohen, C. M., 1983, The molecular organization of the red cell membrane skeleton, Semin. Hematol. 20: 14 1158.Google Scholar
  28. Cohen, C. M., and Foley, S. F., 1982, The role of band 4.1 in the association of actin with erythrocyte membranes, Biochim. Biophys. Acta 688: 691–701.PubMedCrossRefGoogle Scholar
  29. Cohen, C. M., and Foley, S. F., 1984, Biochemical characterization of complex formation by human erythrocyte spectrin, protein 4.1, and actin, Biochemistry 23: 6091–6098.PubMedCrossRefGoogle Scholar
  30. Cohen, C. M., and Foley, S. F., 1986, Phorbol ester-and Cat+-dependent phosphorylation of human red cell membrane skeletal proteins, J. Biol. Chem. 261: 7701–7709.PubMedGoogle Scholar
  31. Cohen, C. M., and Langley, R. C., Jr., 1984, Functional characterization of human erythrocyte spectrin a and ß chains: Association with actin and erythrocyte protein 4.1, Biochemistry 23: 4488–4495.PubMedCrossRefGoogle Scholar
  32. Choen, C. M., 1983, The molecular organization of the red cell membrane skeleton, Semin. in Hematol. 20:141–158.Google Scholar
  33. Coleman, T. R., Harris, A. S., Mische, S. M., Mooseker, M. S., and Morrow, J. S., 1987, Beta spectrin bestows protein 4.1 sensitivity on spectrin—actin interactions, J. Cell Biol. 104: 519–526.PubMedCrossRefGoogle Scholar
  34. Conboy, J., Kan, Y., Mohandas, N., and Shohet, S., 1986, Molecular cloning of protein 4.1, a major structural element of the human erythrocyte membrane skeleton, Proc. Natl. Acad. Sci. USA 83: 9512–9516.PubMedCrossRefGoogle Scholar
  35. Connor, J. C., and Schroit, A. J., 1988, Transbilayer movement of phosphatidylserine in erythrocytes: Inhibition of transport and preferential labeling of a 31,000-dalton protein by sulfhydryl reactive reagents, Biochemistry 27: 848–851.PubMedCrossRefGoogle Scholar
  36. Daleke, D. L., and Huestis, W. H., 1985, Incorporation and translocation of aminophospholipids in human erythrocytes, Biochemistry 24: 5406–5416.PubMedCrossRefGoogle Scholar
  37. Elbaum, D., Mimms, L. T., and Branton, D., 1984, Modulation of actin polymerization by the spectrin—band 4.1 complex, Biochemistry 23: 4813–4816.PubMedCrossRefGoogle Scholar
  38. Elgsaeter, A., and Branton, D., 1974, Intramembrane particle aggregation in erythrocyte ghosts. 1. The effects of protein removal, J. Cell Biol. 63: 1018–1030.PubMedCrossRefGoogle Scholar
  39. Fairbanks, B., Steck, T. L., and Wallach, D. F. H., 1971, Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane, Biochemistry 10: 2607–2617.CrossRefGoogle Scholar
  40. Fowler, V. M., 1987, Identification and purification of a tropomyosin binding protein from human erythrocytes, J. Biol. Chem. 262: 12792–12800.PubMedGoogle Scholar
  41. Fowler, V., and Bennett, V., 1984, Erythrocyte membrane tropomyosin purification and properties, J. Biol. Chem. 259: 5978–5989.PubMedGoogle Scholar
  42. Fowler, V. M., and Bennett, V., 1978, Association of spectrin with its membrane attachment site restricts lateral mobility of human erythrocyte integral proteins, J. Supramol. Struct. 8: 215–221.CrossRefGoogle Scholar
  43. Fowler, V. M., Davis, V., and Benett, V., 1985, Human erythrocyte myosin: Identification and purification, J. Cell Biol 100: 47–55.PubMedCrossRefGoogle Scholar
  44. Gardner, K., and Bennett, V., 1986, A new erythrocyte membrane-associated protein with calmodulin binding activity. Identification and purification, J. Biol. Chem. 261: 1339–1348.PubMedGoogle Scholar
  45. Gardner, K., and Bennett, V., 1987, Modulation of spectrin—actin assembly by erythrocyte adducin, Nature 328: 359–362.PubMedCrossRefGoogle Scholar
  46. Hall, T. G., and Bennett, V., 1987, Regulatory domains of erythrocyte ankyrin, J. Biol. Chem. 262: 1053710545.Google Scholar
  47. Hargreaves, W., Giedd, K., Verkleij, A., and Branton, D., 1980, Reassociation of ankyrin with band 3 in erythrocyte membranes and in lipid vesicles, J. Biol. Chem. 255: 11965–11972.PubMedGoogle Scholar
  48. Heast, C. W. M., 1982, Interactions between membrane skeleton proteins and the intrinsic domain of the erythrocyte membrane, Biochim. Biophys. Acta 694: 331–352.CrossRefGoogle Scholar
  49. Heubusch, P., Jung, C. Y., and Green, F. A., 1985, The osmotic response of human erythrocyte and the membrane cytoskeleton, J. Cell. Physiol. 122: 266–272.PubMedCrossRefGoogle Scholar
  50. Holt, G. D., Haltiwanger, R. S., Torres, C.-R., and Hart, G. W., 1987, Erythrocytes contain cytoplasmic glycoprotin, J. Biol. Chem. 262: 14847–14850.PubMedGoogle Scholar
  51. Husain, A., Howlett, G., and Sawyer, W. H., 1985a, The interaction of calmodulin with erythrocyte membrane proteins, Biochem. Int. 10: 1–12.PubMedGoogle Scholar
  52. Husain, A., Howlett, G. J., and Sawyer, W. H., 1985b, Calmodulin activation of red blood cell (Ca2+ + Mgt+)-ATPase and its antagonism by phenothiazine, Mol. Pharmacol. 18: 253–258.Google Scholar
  53. Janmey, P. A., and Stossel, T. P., 1987, Modulation of gelsolin function by phosphatidylinositol 4,5-bisphosphate, Nature 325: 362–364.PubMedCrossRefGoogle Scholar
  54. Jarret, H. W., and Penniston, J. T., 1978, Purification of the Cat+-stimulated ATPase activator from human erythrocytes, J. Biol. Chem. 253: 4676–4682.Google Scholar
  55. Jinbu, Y., Sato, S., Nakao, T., and Nakao, M., 1982, Ankyrin is necessary for both drug-induced and ATP-induced shape change of human erythrocyte ghosts, Biochem. Biophys. Res. Commun. 104: 1087–1092.PubMedCrossRefGoogle Scholar
  56. Jinbu, Y., Nakao, M., Otsuka, M., and Sato, S., 1983, Two steps in ATP-dependent shape change of human erythrocyte ghosts, Biochem. Biophys. Res. Commun. 112: 384–390.PubMedCrossRefGoogle Scholar
  57. Jinbu, Y., Sato, S., Nakao, M., and Tsukita, S., 1984a, Cat+- and Mg-ATP-dependent shape change of human erythrocyte ghosts and Triton shells, Exp. Cell Res. 151: 160–170.PubMedCrossRefGoogle Scholar
  58. Jinbu, Y., Sato, S., Nakao, T., Nakao, M., Tsukita, S., Tsukita, S., and Ishikawa, H., 1984b, The role of ankyrin in shape and deformability change of human erythrocyte ghosts, Biochim. Biophys. Acta 773: 237–245.PubMedCrossRefGoogle Scholar
  59. Jinbu, Y., Sato, S., and Nakao, M., 1984c, Reversible shape change of Triton treated erythrocyte ghosts induced by Cat+ and Mg-ATP, Nature 307: 376–378.PubMedCrossRefGoogle Scholar
  60. Knowles, W., Marchesi, S. L., and Marchesi, V. T., 1983, Spectrin: Structure, function, and abnormalities, Semin. Hematol. 20: 159–174.PubMedGoogle Scholar
  61. Kojima, Y., Nakao, M., Sato, S., and Hara, Y., 1988, Role of spectrin in maintaining shape of red cells, Seikagaku 60: 789 (in Japanese).Google Scholar
  62. Lange, Y., Gouch, A., and Steck, T. L., 1982a, Role of the bilayer in the shape of the isolated erythrocyte membrane, J. Membr. Biol. 69: 113–124.PubMedCrossRefGoogle Scholar
  63. Lange, Y., Hadesman, R. A., and Steck, T. L., 1982b, Role of the reticulum in the stability and shape of the isolated human erythrocyte membrane, J. Cell Biol. 92: 714–721.PubMedCrossRefGoogle Scholar
  64. Lin, D. C., and Lin, S., 1978, Actin polymerization induced by a motility-related high-affinity cytochalasin binding complex from erythrocyte membrane, Proc. Natl. Acad. Sci. USA 75: 2345–2349.Google Scholar
  65. Ling, E., Danilov, Y. N., and Cohen, C. M., 1988, Modulation of red cell band 4.1 function by cAMP dependent kinase and protein kinase C phosphorylation, J. Biol. Chem. 263: 2209–2216.PubMedGoogle Scholar
  66. Litman, D., Hsu, D. J., and Marchesi, V. T., 1980, Evidence that spectrin binds to macromolecular complexes on the linear surface of the red cell membrane, J. Cell Sci. 42: 1–22.PubMedGoogle Scholar
  67. Liu, S.-C., and Palek, J., 1979, Metabolic dependence of protein arrangement in human erythrocyte membranes. 2. Cross linking of major proteins in ghosts from fresh and ATP depleted red cells, Blood 54: 1117 1130.Google Scholar
  68. Liu, S.-C., and Palek, J., 1980, Spectrin tetramer dimer equilibrium and the stability of erythrocyte membrane skeletons, Nature 285: 586–588.PubMedCrossRefGoogle Scholar
  69. Liu, S.-C., and Palek, J., 1984, Hemoglobin enhances the self-association of spectrin heterodimers in human erythrocytes, J. Biol. Chem. 259: 11556–11562.PubMedGoogle Scholar
  70. Liu, S.-C., Fairbanks, G., and Palek, J., 1977, Spontaneous reversible protein cross linking in the human erythrocyte membrane: Temperature and pH dependence, Biochemistry 16: 4066–4074.PubMedCrossRefGoogle Scholar
  71. Liu, S.-C., Palek, J., Prchal, J., and Castleberry, R. P., 1981, Altered spectrin dimer—dimer association and instability of erythrocyte membrane skeletons in hereditary pyropoikilocytosis, J. Clin. Invest. 68: 597605.Google Scholar
  72. Liu, S.-C., Windisch, P., Kim, S., and Palek, J., 1984, Oligomeric states of spectrin in normal erythrocyte membranes: Biochemical and electron microscopic studies, Cell 37: 587–594.PubMedCrossRefGoogle Scholar
  73. Liu, S.-C., Zhai, S., Lawler, J., and Palek, J., 1985, Hemin-mediated dissociation of erythrocyte membrane skeletal proteins, J. Biol. Chem. 260: 12234–12239.PubMedGoogle Scholar
  74. Liu, S.-C., Derick, L. H., and Palek, J., 1987, Visualization of the hexagonal lattice in the erythrocyte membrane skeleton, J. Cell Biol. 104: 527–536.PubMedCrossRefGoogle Scholar
  75. Lorand, L., Shishido, R., Parameswaran, K. N., and Steck, T. L., 1975, Modification of human erythrocyte ghosts with transglutaminase, Biochem. Biophys. Res. Commun. 67: 1158–1166.PubMedCrossRefGoogle Scholar
  76. Luna, E. J., Kidd, G. H., and Branton, D., 1979, Identification by peptide analysis of the spectrin-binding protein in human erythrocytes, J. Biol. Chem. 254: 2526–2532.PubMedGoogle Scholar
  77. Lutz, H. U., Liu, S.-C., and Palek, J., 1977, Release of spectrin-free vesicles from human erythrocytes during ATP depletion. Part 1. Characterization of spectrin-free vesicles, J. Cell Biol. 73: 548–560.PubMedCrossRefGoogle Scholar
  78. Lux, S. E., 1979, Dissecting the red cell membrane skeleton, Nature 281: 426–429.PubMedCrossRefGoogle Scholar
  79. Maruta, H., and Mizuno, D., 1971, Selective recognition of various erythrocytes in endocytosis by mouse peritoneal macrophages, Nature 234: 246–248.Google Scholar
  80. Matsuzaki, F., Sutoh, K., and Ikai, A., 1985, Structural unit of the erythrocyte cytoskeleton. Isolation and electron microscopic examination, Eur. J. Cell Biol. 39: 153–160.PubMedGoogle Scholar
  81. Middelkoop, E., Lubin, B. H., Bevers, E. M., Op den Kamp, J. A. F., Comfurius, P., Chiu, D. T.-Y., Zwaal, R. F. A., van Deenen, L. L. M., and Roelofsen, B., 1988, Studies on sickled erythrocytes provide evidence that the asymmetric distribution of phosphatidylserine in the red cell membrane is maintained by both ATP-dependent translocation and interaction with membrane skeletal proteins, Biochim. Biophys. Acta 937: 281–288.PubMedCrossRefGoogle Scholar
  82. Mische, S. M., Mooseker, M. S., and Morrow, J. S., 1987, Erythrocyte adducin: A calmodulin-regulated actin-bundling protein that stimulates spectrin—actin binding, J. Cell Biol. 105: 2837–2845.PubMedCrossRefGoogle Scholar
  83. Mohandas, N., Chasis, J. A., and Shohet, S. T., 1983, The influence of membrane skeleton on red cell deformability, membrane material properties, and shape, Semin. Hematol. 20: 225–242.PubMedGoogle Scholar
  84. Morrow, J. S., and Marchesi, V. T., 1981, Self assembly of spectrin oligomers in vitro: A basis for a dynamic cytoskeleton, J. Cell Biol. 88: 463–468.PubMedCrossRefGoogle Scholar
  85. Morrow, J., Haigh, W., and Marchesi, V. T., 1984, Spectrin oligomers in vitro: A structural feature of the erythrocyte cytoskeleton, J. Supramol. Cell Biochem. 1: 275–287.Google Scholar
  86. Nakao, K., Wada, T., Kamiyama, T., and Nakao, M., 1962a, Clinical and experimental studies on the post-transfusion viability of the long-term stored erythrocytes, J. Jpn. Int. Soc. 51: 211–219 (in Japanese).CrossRefGoogle Scholar
  87. Nakao, K., Wada, T., Kamiyama, T., Nakao, M., and Nagano, K., 1962b, A direct relationship between adenosine triphosphatase-level and in vivo viability of erythrocytes, Nature 194: 877–878.PubMedCrossRefGoogle Scholar
  88. Nako, M., Nakao, T., Tatibana, M., Yoshikawa, H., and Abe, T., 1959, Effect of inosine and adenine on adenosine triphosphate regeneration and shape transformation in long-stored erythrocyte, Biochim. Biophys. Acta 32: 564–565.CrossRefGoogle Scholar
  89. Nakao, M., Nakao, T., and Yamazoe, S., 1960a, Adenosine triphosphate and maintenance of shape of the human red cells, Nature 187: 945–946.PubMedCrossRefGoogle Scholar
  90. Nakao, M., Nakao, T., Tatibana, M., and Yoshikawa, H., 1960b, Phosphorus metabolism in human erythrocyte. III. Regeneration of adenosine triphosphate in long-stored erythrocyte by incubation with inosine and adenine, J. Biochem. 47: 661–671.Google Scholar
  91. Nakao, M., Nakao, T., Arimatsu, Y., and Yoshikawa, H., 1960c, A new preservative medium maintaining the level of adenosine triphosphate and the osmotic resistance of erythrocyte, Proc. Jpn. Acad. 36: 43–47.Google Scholar
  92. Nakao, M., Nakao, T., Tatibana, M., and Yoshikawa, H., 1960d, Shape transformation of erythrocyte ghosts on addition of adenosine triphosphate to the medium, J. Biochem. 47: 694–695.Google Scholar
  93. Nakao, M., Nakao, T., Tatibana, M., and Yoshikawa, H., 1960e, Phosphorus metabolism in human erythrocyte. IV. Destruction of adenine nucleotides in stored blood, J. Biochem. 48: 672–684.Google Scholar
  94. Nakao, M., Nakao, T., Yamazoe, S., and Yoshikawa, H., 1961, Adenosine triphosphate and shape of erythrocyte, J. Biochem. 49: 487–492.PubMedGoogle Scholar
  95. Nakao, M., Motegi, T., Nakao, T., Yamazoe, S., and Yoshikawa, H., 1962a, A positive feedback mechanism of adenosine triphosphate synthesis in erythrocytes, Nature 191: 283–284.CrossRefGoogle Scholar
  96. Nakao, M., Nakao, T., Yoshikawa, H., Wada, T., Takaku, H., and Nakao, K., 1962b, A new preservative medium containing adenine and inosine, Proc. 8th Congr. Int. Soc. Blood Transf. Tokyo pp. 455–461.Google Scholar
  97. Nakao, M., Hoshino, K., and Nakao, T., 1981, Constancy of cell volume during shape change of erythrocytes induced by the increasing ATP content, J. Bioenerg. Biomembr. 13: 307–316.PubMedCrossRefGoogle Scholar
  98. Nakao, M., Nakao, T., Komatsu, Y., Sano, K., and Sasakawa, S., 1983, Isoosmotic sucrose, adenine inosine media for preservation of blood, Biomed. Biochim. Acta 42: 527–535.PubMedGoogle Scholar
  99. Nakao, M., Jinbu, Y., Sato, S., Ishigami, Y., Nakao, T., Ito-Ueno, E., and Wake, K., 1987, Structure and function of red cell cytoskeleton, Biomed. Biochim. Acta 46: 5–9.Google Scholar
  100. Nakao, T., Nagano, K., Adachi, K., and Nakao, M., 1964, Separation of two adenosine triphosphatase from erythrocyte membranes, Biochem. Biophys. Res. Commun. 13: 444–448.CrossRefGoogle Scholar
  101. Nakao, T., Nagai, F., and Nakao, M., 1982, Posttransfusion viability of rabbit erythrocytes preserved in a medium containing inosine, adenine, and isoosmotic sucrose, Vox Sang. 42: 217–222.PubMedCrossRefGoogle Scholar
  102. Nakashima, K., and Beutler, E., 1979, Comparison of structure and function of human erythrocyte and human actin, Proc. Natl. Acad. Sci. USA 76: 935–938.PubMedCrossRefGoogle Scholar
  103. Nelson, W. J., and Veshnock, P. J., 1987, Ankyrin binding to (Na+ + K+)ATPase and implications for the organization of membrane domains in polarized cells, Nature 328: 533–536.PubMedCrossRefGoogle Scholar
  104. Ohanian, V., Wolfe, L. C., John, K. M., Pinder, J. C., Lux, S. E., and Gratzer, W. B., 1984, Analysis of the ternary interaction of the red cell membrane skeletal proteins spectrin, actin, and 4.1, Biochemistry 23: 4416–4420.PubMedCrossRefGoogle Scholar
  105. Ohnishi, T., 1962, Extraction of actin-and myosin-like proteins from erythrocyte membrane, J. Biochem. 52: 307–308.PubMedGoogle Scholar
  106. Palek, J., and Lux, S. E., 1983, Red cell membrane skeletal defects on the red cell deformability, membrane material properties and shape, Semin. Haematol. 189: 225–240.Google Scholar
  107. Palek, J., Curby, W. A., and Lionetti, F. J., 1971a, Effects of calcium and ATP on volume of human red cell ghosts, Am. J. Physiol. 220: 19–26.PubMedGoogle Scholar
  108. Palek, J., Curby, W. A., and Lionetti, F. J., 1971b, Relation of calcium ion activated ATPase to calcium ion linked shrinkage of human red cell ghosts, Am. J. Physiol. 220: 1028–1032.PubMedGoogle Scholar
  109. Palek, J., Curby, W. A., and Lionetti, F. J., 1972, Size dependence of ghosts from stored erythrocytes on calcium and ATP, Blood 40: 261–275.PubMedGoogle Scholar
  110. Palek, J., Stewart, G., and Lionetti, F. J., 1974, The dependence of shape of human erythrocyte ghosts on calcium, magnesium and ATP, Blood 44: 583–597.PubMedGoogle Scholar
  111. Palek, J., Liu, P. A., and Liu, S.-C., 1978a, Polymerization of red cell membrane protein contributes to spheroechinocyte shape irreversibility, Nature 274: 505–507.PubMedCrossRefGoogle Scholar
  112. Palek, J., Liu, S.-C., and Snyder, L. M., 1978b, Metabolic dependence of protein arrangement in human erythrocyte membranes. Part 1. Analysis of spectrin-rich complexes in ATP depleted red cells, Blood 51: 385–396.PubMedGoogle Scholar
  113. Pasternack, F. R., Anderson, R. A., Leto, T. L., and Marchesi, V. T., 1985, Interactions between protein 4.1 and band 3, J. Biol. Chem. 260: 3676–3683.PubMedGoogle Scholar
  114. Patel, V. P., and Fairbanks, G., 1981, Spectrin phosphorylation and shape changes of human erythrocyte ghosts, J. Cell Biol. 88: 430–440.PubMedCrossRefGoogle Scholar
  115. Patel, V. P., and Fairbanks, G., 1986, Relationship of major phosphorylation reactions and Mg-ATPase activities to ATP-dependent shape change of human erythrocyte membranes, J. Biol. Chem. 261: 3170–3177.PubMedGoogle Scholar
  116. Pinder, J. C., and Gratzer, W. B., 1983, Structural and dynamic states of actin in the erythrocyte, J. Cell Biol. 96: 768–775.PubMedCrossRefGoogle Scholar
  117. Pinder, J., Ungewickell, E., Bray, D., and Gratzer, W. B., 1978, The spectrin actin complex and erythrocyte shape, J. Supramol. Struct. 8: 435–445.CrossRefGoogle Scholar
  118. Quist, E. E., 1980, Regulation of erythrocyte membrane shape by Cat+, Biochem. Biophys. Res. Commun. 92: 631–637.PubMedCrossRefGoogle Scholar
  119. Quist, E. E., and Reece, K. L., 1980, The role of diphosphatidylinositol in erythrocyte membrane shape regulation, Biochem. Biophys. Res. Commun. 95: 1023–1030.PubMedCrossRefGoogle Scholar
  120. Sato, S., and Nakao, M., 1981, Cross-linking of intact erythrocyte membrane with a newly synthesized cleavable bifunctional reagent, J. Biochem. 90: 1177–1185.PubMedGoogle Scholar
  121. Sato, S., and Nakao, M., 1986, Characterization of human erythrocytes cytoskeletal ATPase, J. Biochem. 100: 643–649.PubMedGoogle Scholar
  122. Sato, S., and Ohnishi, S., 1983, Interaction of a peripheral protein of the erythrocyte membrane, band 4.1 with phosphatidylserine-containing liposome and erythrocyte inside-out vesicles, Eur. J. Biochem. 130: 19–25.PubMedCrossRefGoogle Scholar
  123. Seigneuret, M., and Devaux, P. F., 1984, ATP-dependent asymmetric distribution of spin-labeled phospholipids in the erythrocyte membrane: Relation to shape changes, J. Cell Biol. 81: 3751–3755.Google Scholar
  124. Shahbakhti, F., and Gratzer, W. B., 1986, Analysis of the self-association of human red cell spectrin, Biochemistry 25: 5969–5975.PubMedCrossRefGoogle Scholar
  125. Shapiro, A. L., Vinuera, E., and Maizel, J. V., 1967, Molecular weight estimation of polypeptide chains by electrophoresis in SDS-polycarbonate gels, Biochem. Biophys. Res. Comm. 28: 815–821.PubMedCrossRefGoogle Scholar
  126. Sheetz, M. P. 1983, Membrane skeletal dynamics: Role in modulation of red cell deformability, mobility of transmembrane proteins, and shape, Semin. Hematol. 20: 175–188.PubMedGoogle Scholar
  127. Sheetz, M. P., and Singer, S. J., 1974, Biological membranes as bilayer couples. A molecular mechanism of drug-induced interactions, Proc. Natl. Acad. Sci. USA 71: 4457–4461.PubMedCrossRefGoogle Scholar
  128. Sheetz, M. P., and Singer, S. J., 1977, On the mechanism of ATP-induced shape changes in human erythrocyte membranes. I. The role of the spectrin complex, J. Cell Biol. 73: 638–696.PubMedCrossRefGoogle Scholar
  129. Shen, B. W., Josephs, R., and Steck, T. L., 1984, Ultrastructure of unit fragments of the skeleton of the human erythrocyte membrane, J. Cell Biol. 99: 810–821.PubMedCrossRefGoogle Scholar
  130. Shen, B. W., Josephs, R., and Steck, T. L., 1986, Ultrastructure of the intact skeleton of the human erythrocyte membrane, J. Cell Biol. 102: 997–1006.PubMedCrossRefGoogle Scholar
  131. Shotton, D. M., Burke, B. E., and Branton, D., 1979, The molecular structure of human erythrocyte spectrin. Biophysical and electron microscopic studies, J. Mol. Biol. 131: 303–320.PubMedCrossRefGoogle Scholar
  132. Siegel, D. L., and Branton, D., 1985, Partial purification and characterization of an actin-bundling protein, band 4.9, from human erythrocytes, J. Cell Biol. 100: 775–785.PubMedCrossRefGoogle Scholar
  133. Singer, S. J., and Nicolson, G. L., 1972, The fluid mosaic model of the structure of cell membrane, Science 175: 720–731.PubMedCrossRefGoogle Scholar
  134. Smith, D. K., and Palek, J., 1982, Modulation of lateral mobility of band 3 in the red cell membrane by oxidative cross linking of spectrin, Nature 297: 424–425.PubMedCrossRefGoogle Scholar
  135. Smith, D. K., and Palek, J., 1983, Sulthydryl reagents induce altered spectrin self association skeletal instability and increased thermal sensitivity of red cells, Blood 62: 1190–1196.PubMedGoogle Scholar
  136. Sobue, K., Muramoto, Y., Fujita, M., and Kakiuchi, S., 1982, Calmodulin binding protein of erythrocyte cytoskeleton, Biochem. Biophys. Res. Commun. 100: 1063–1068.CrossRefGoogle Scholar
  137. Speicher, D. W., and Marchesi, V. T., 1984, Erythrocyte spectrin is composed of many homologous triple helical segments, Nature 311: 177–180.PubMedCrossRefGoogle Scholar
  138. Srinivasan, Y., Elmer, L., Davis, J., Bennett, V., and Angelides, K., 1988, Ankyrin and spectrin associate with voltage-dependent sodium channels in brain, Nature 333: 177–180.PubMedCrossRefGoogle Scholar
  139. Steck, T. L., Weinstein, R. S., Straus, J. H., and Wallach, D. F. H., 1970, Inside-out red cell membrane vesicles preparation and purification, Science 168: 255–257.PubMedCrossRefGoogle Scholar
  140. Steck, T. L., Rams, B., and Strapazon, E., 1976, Proteolytic dissection of band 3, predominant polypeptide of the human erythrocyte membrane, Biochemistry 15: 1154–1161.CrossRefGoogle Scholar
  141. Steiner, J. P., and Bennett, V., 1988, Ankyrin-independent membrane protein-binding sites for brain and erythrocyte spectrin, J. Biol. Chem. 263: 11417–11425.Google Scholar
  142. Stromqvist, M., Berglund, A., Shanbhag, V. P., and Backman, L., 1988, Influence of calmodulin on the human red cell membrane skeleton, Biochemistry 27: 1104–1110.PubMedCrossRefGoogle Scholar
  143. Takakuwa, Y., Tchemia, G., Rossi, M., Benabadji, M., and Mohandas, N., 1986, Restoration of normal membrane stability of unstable protein 4.1-deficient erythrocyte membranes by incorporation of purified protein 4.1, J. Clin. Invest. 78: 80–85.PubMedCrossRefGoogle Scholar
  144. Teitel, P., 1965, Disk—sphere transformation and plasticity alteration of red blood cells, Nature 26: 409–410.CrossRefGoogle Scholar
  145. Tsuji, A., Kawasaki, K., and Ohnishi, S., 1988, Regulation of band 3 mobilities in erythrocyte ghost membranes by protein association and cytoskeletal meshwork, Biochemistry 27: 7447–7452.PubMedCrossRefGoogle Scholar
  146. Tsukita, S., Tsukita, S., and Ishikawa, H., 1980, Cytoskeletal network underlying the human erythrocyte membrane: Thin-section electron microscopy, J. Cell Biol. 85: 567–576.PubMedCrossRefGoogle Scholar
  147. Tsukita, S., Tsukita, S., Ishikawa, H., Sato, S., and Nakao, M., 1981, Electron microscopic study of reassociation of spectrin and actin with the human erythrocyte membrane, J. Cell Biol. 90: 70–77.PubMedCrossRefGoogle Scholar
  148. Tyler, J. M., Hargreaves, W. R., and Branton, D., 1979, Purification of two spectrin-binding proteins: Biochemical and electron microscopic evidence for site-specific reassociation between spectrin and bands 2.1 and 4.1, Proc. Natl. Acad. Sci. USA 76: 5192–5196.PubMedCrossRefGoogle Scholar
  149. Tyler, J., Reinhardt, B., and Branton, D., 1980, Associations of erythrocyte membrane proteins binding of purified bands 2.1 and 4.1 to spectrin, J. Biol. Chem. 255: 7034–7039.PubMedGoogle Scholar
  150. Ueno, E., Sato, S., Jinbu, Y., and Nakao, M., 1987, Dynamic association of band 3 with Triton shells in human erythrocyte ghosts, Biochim. Biophys. Acta 915: 77–86.PubMedCrossRefGoogle Scholar
  151. Ungewickell, E., Bennett, P., Calvert, R., Ghanian, V., and Gratzer, W. B., 1979, In vitro formation of complex between cytoskeletal proteins of human erythrocytes, Nature 280: 811–814.PubMedCrossRefGoogle Scholar
  152. Wada, T., Takaku, F., Nakao, K., Nakao, M., Nakao, T., and Yoshikawa, H., 1960, Posttransfusion survival of the red blood cells stored in a medium containing adenine and inosine, Proc. Jpn. Acad. 36: 618–623.Google Scholar
  153. Weed, R. I., LaCelle, P. L., and Merrill, E. W., 1969, Metabolic dependence of red cell deformability, J. Clin. Invest. 48: 795–809.CrossRefGoogle Scholar
  154. White, J. G., 1974, Effects of an ionophore A23187 on the surface morphology of normal erythrocytes, Am. J. Pathol. 77: 507–514.PubMedGoogle Scholar
  155. Wolf, M., and Sahyoun, N., 1986, Protein kinase C and phosphatidylserine bind to MT110,000/115,000 polypeptides enriched in cytoskeletal and postsynaptic density preparations, J. Biol. Chem. 261: 13327-13332.Google Scholar
  156. Wong, A. J., Kiehart, D. P., and Pollard, T. D., 1985, Myosin from human erythrocytes, J. Biol. Chem. 260: 46–49.PubMedGoogle Scholar
  157. Yu, J., and Goodman, S. R., 1979, Syndeins: The spectrin-binding(s) of the human erythrocyte membrane, J. Proc. Natl. Acad. Sci. USA 76: 2340–2344.CrossRefGoogle Scholar
  158. Yu, J., Fishman, D. A., and Steck, T. L., 1973, Selective solubilization of proteins and phospholipids from red cell membranes by nonionic detergents, J. Supramol. Struct. 1: 233–248.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1990

Authors and Affiliations

  • Makoto Nakao
    • 1
  1. 1.Department of BiochemistryTokyo Medical and Dental University School of MedicineTokyoJapan

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