The molecular pathobiology of cell membrane iron: The sickle red cell as a model

Free Radical Biology and Medicine

Volumn 24, Issue 6, 1998, Pages 1040-1048

  Browne, Paul ^a   Shalev, Oded ^b   Hebbel, Robert P ^c  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

Free radical; Hemoglobin; Iron; Membrane; Oxidation; Sickle

Indexed keywords

AMINOPHOSPHOLIPID; FERRITIN; GLOBIN; HEME; HEMOGLOBIN; HYDROXYL RADICAL; IRON;

CATALYST; CELL MEMBRANE; CYTOSOL; HEMOCHROMATOSIS; HEMOGLOBINOPATHY; HUMAN; IRON OVERLOAD; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; SICKLE CELL; THALASSEMIA;

ANEMIA, SICKLE CELL; ERYTHROCYTE MEMBRANE; ERYTHROCYTES, ABNORMAL; HUMANS; IRON; MODELS, BIOLOGICAL;

EID: 0032054340     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-5849(97)00391-2     Document Type: Review

References (69)

1. Asakura T., Minakata K., Adachi K., Russell M. O., Schwartz E. Denatured hemoglobin in sickle erythrocytes. J. Clin. Invest. 59:1977;633-640.
2. Kim H. C., Friedman S., Asakura T., Schwartz E. Inclusions in red blood cells containing Hb S or Hb C. Br. J. Haematol. 44:1980;547-554.
3. Kuross S. A., Rank B. H., Hebbel R. P. Excess heme in sickle erythrocyte inside-out membranes Possible role in thiol oxidation . Blood. 71:1988;876-882.
4. Rachmilewitz E. A. Denaturation of the normal and abnormal hemoglobin molecule. Review. Semin. Hematol. 11:1974;441-462.
5. Repka T., Shalev O., Reddy R., Yuan J., Abrahamov A., Rachmilewitz E. A., Low P. S., Hebbel R. P. Nonrandom association of free iron with membranes of sickle and b-thalassemic erythrocytes. Blood. 82:1993;3204-3210.
6. Waugh S. M., Walder J. A., Low P. S. Partial characterization of the copolymerization reaction of erythrocyte membrane band 3 with hemichromes. Biochem. 26:1987;1777-1783.
7. Waugh S. M., Willardson B. M., Kannan R., Labotka R. J., Low P. S. Heinz bodies induce clustering of band 3, glycophorin, and ankyrin in sickle cell erythrocytes. J. Clin. Invest. 78:1986;1155-1160.
8. Kannan R., Labotka R., Low P. S. Isolation and characterization of the hemichrome-stabilized membrane protein aggregates from sickle erythrocytes. Major site of autologous antibody binding. J. Biol. Chem. 263:1988;13766-13773.
9. Low P. S., Waugh S. M., Zinke K., Drenckhahn D. The role of hemoglobin denaturation and band 3 clustering in red blood cell aging. Science. 227:1985;531-533.
10. Kuross S. A., Hebbel R. P. Nonheme iron in sickle erythrocyte membranes Association with phospholipids and potential role in lipid peroxidation . Blood. 72:1988;1278-1285.
11. Hartley A., Rice-Evans C. Membrane-associated iron-species and membrane oxidation in sickle-cell disease. Biochem. Soc. Trans. 17:1989;116-118.
12. Shalev O., Hebbel R. P. Extremely high avidity association of Fe(III) with the sickle red cell membrane. Blood. 88:1996;349-352.
13. Shalev O., Repka T., Goldfarb A., Grinberg L., Abrahamov A., Olivieri N. F., Rachmilewitz E. A., Hebbel R. P. Deferiprone (L1) chelates pathologic iron deposits from membranes of intact thalassemic and sickle red blood cells both in vitro and in vivo. Blood. 86:1995;2008-2013.
14. Hendrickson H. S., Fullington J. G. Stabilities of metal complexes of phospholipids Ca(II), Mg (II), and Ni(II) complexes of phosphatidylserine and triphosphoinositide . Biochem. 4:1965;1599-1605.
15. Liu S.-C., Yi S. J., Mehta J. R., Nichols P. E., Ballas S. K., Yacono P. W., Golan D. E., Palek J. Red cell membrane remodeling in sickle cell anemia. Sequestration of membrane lipids and proteins in Heinz bodies. J. Clin. Invest. 97:1996;29-36.
16. Chétrite G., Cassoly R. Affinity of hemoglobin for the cytoplasmic fragment of human erythrocyte membrane band 3. Equilibrium measurements at physiological pH using matrix-bound proteins: The effects of ionic strength, deoxygenation and of 2,3-diphosphoglycerate. J. Mol. Biol. 185:1985;639-644.
17. Repka T., Hebbel R. P. Hydroxyl radical formation by sickle erythrocyte membranes Role of pathologic iron deposits and cytoplasmic reducing agents . Blood. 78:1991;2753-2758.
18. Hebbel R. P., Eaton J. W., Balasingam M., Steinberg M. H. Spontaneous oxygen radical generation by sickle erythrocytes. J. Clin. Invest. 70:1982;1253-1259.
19. Shalev O., Hebbel R. P. Catalysis of soluble hemoglobin oxidation by free iron on sickle red cell membranes. Blood. 87:1996;3948-3952.
20. Asakura T., Ohnishi T., Friedman S., Schwartz E. Abnormal precipitation of oxyhemoglobin S by mechanical shaking. Proc. Natl. Acad. Sci. U.S.A. 71:1974;1594-1598.
21. Adachi K., Kim J., Travitz R., Harano T., Asakura T. Effect of amino acid at the b6 position on surface hydrophobicity, stability, solubility, and the kinetics of polymerization of hemoglobin. J. Biol. Chem. 262:1987;12920-12925.
22. Marva E., Hebbel R. P. Denaturing interaction between sickle hemoglobin and phosphatidylserine liposomes. Blood. 83:1994;242-249.
23. LaBrake C. C., Fung L. Phospholipid vesicles promote human hemoglobin oxidation. J. Biol. Chem. 267:1992;16703-16711.
24. Hebbel R. P., Morgan W. T., Eaton J. W., Hedlund B. E. Accelerated autoxidation and heme loss due to instability of sickle hemoglobin. Proc. Natl. Acad. Sci. U.S.A. 85:1988;237-241.
25. MacDonald V. W., Charache S. Drug-induced oxidation and precipitation of hemoglobins A, S and C. Biochim. Biophys. Acta. 701:1982;39-44.
26. Watkins, J. A.; Claster, S.; Caughey, W. S. Enhanced production of oxy radicals and peroxide by hemoglobins S and F. Fed. Proc. Abstract 45:1640; 1986.
27. Shaklai N., Sharma V. S., Ranney H. M. Interaction of sickle cell hemoglobin with erythrocyte membranes. Proc. Natl. Acad. Sci. U.S.A. 78:1981;65-68.
28. Sugihara T., Hebbel R. P. Exaggerated cation leak from oxygenated sickle red blood cells during deformation Evidence for a unique leak pathway . Blood. 80:1992;2374-2378.
29. Beutler E. The effect of methemoglobin formation in sickle cell disease. J. Clin. Invest. 40:1961;1856-1871.
30. Shaklai N., Shviro Y., Rabizadeh E., Kirschner-Zilber E. Accumulation and drainage of hemin in the red cell membrane. Biochim. Biophys. Acta. 821:1985;355-366.
31. Liu S.-C., Zhai S., Palek J. Detection of hemin release during hemoglobin S denaturation. Blood. 71:1988;1755-1758.
32. Bauminger E. R., Cohen S. G., Ofer S., Rachmilewitz E. Quantitative studies of ferritin like iron in erythrocytes of thalassemia, sickle-cell anemia, and hemoglobin Hammersmith with Mossbauer spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 76:1979;939-943.
33. Theil, E. C. Regulation of ferritin and transferrin receptor mRNAs. J. Biol. Chem. Abstract 265:4771-4774; 1990.
34. Hebbel R. P. The sickle erythrocyte in double jeopardy Autoxidation and iron decompartmentalization . Semin. Hematol. 1:1990;51-69.
35. Hebbel R. P. Membrane-associated iron. Embury S. H., Hebbel R. P., Mohandas N., Steinberg M. H. Sickle cell disease Basic principles and clinical practice . 1994;163-172 Raven Press, New York.
36. Rank B. H., Carlsson J., Hebbel R. P. Abnormal redox status of membrane-protein thiols in sickle erythrocytes. J. Clin. Invest. 75:1985;1531-1537.
37. Rice-Evans C., Baysal E. Role of membrane-bound haemoglobin products in oxidative damage in sickle cell membranes. Acta Haemat. 78:1987;105-108.
38. Schwartz R. S., Rybicki A. C., Heath R. H., Lubin B. H. Protein 4. 1 in sickle erythrocytes. Evidence for oxidative damage. J. Biol. Chem. 262:1987;15666-15672.
39. Bencsath F. A., Shartava A., Monteiro C. A., Goodman S. R. Identification of the disulfide-linked peptide in irreversibly sickled cell beta-actin. Biochem. 35:1996;4403-4408.
40. Kuypers F. A., van den Berg J., Lubin B. H. Membrane lipids and vesiculation. Embury S. H., Hebbel R. P., Mohandas N., Steinberg M. H. Sickle cell disease Basic principles and clinical practice . 1994;139-152 Raven Press, New York.
41. Jain S. K., Shohet S. B. A novel phospholipid in irreversibly sickled cells Evidence for in vivo peroxidative membrane damage in sickle cell disease . Blood. 63:1984;362-367.
42. Hebbel R. P., Miller W. J. Phagocytosis of sickle erythrocytes Immunologic and oxidative determinants of hemolytic anemia . Blood. 64:1984;733-741.
43. Turrini F., Arese P., Yuan J., Low P. S. Clustering of integral membrane proteins of the human erythrocyte membrane stimulates autologous IgG binding, complement deposition, and phagocytosis. J. Biol. Chem. 266:1991;23611-23617.
44. Hebbel R. P., Miller W. J. Unique promotion of erythrophagocytosis by malondialdehyde. Am. J. Hematol. 29:1988;222-225.
45. Yla-Gerttuala S., Palinski W., Butler S. W., Picard S., Steinberg D., Witztum J. L. Rabbit and human atherosclerotic lesions contain IgG that recognizes epitopes of oxidized LEL. Atherosclerosis Thromb. 14:1994;32-40.
46. Brugnara C., Bunn H. F., Tosteson D. C. Regulation of erythrocyte cation and water content in sickle cell anemia. Science. 232:1986;388-390.
47. +-Cl_ cotransport in the transgenic SAD mouse. Am. J. Physiol. 269:1995;C899-C906.
48. Hebbel R. P., Leung A. N., Mohandas N. Oxidation-induced changes in microrheologic properties of the red blood cell membrane. Blood. 76:1990;1015-1020.
49. Sugihara T., Rawicz W., Evans E. A., Hebbel R. P. Lipid hydroperoxides permit deformation-dependent leak of monovalent cation from erythrocytes. Blood. 77:1991;2757-2763.
50. Rank B. H., Moyer N. L., Hebbel R. P. Vesiculation of sickle erythrocytes during thermal stress. Blood. 72:1988;1060-1063.
51. Hebbel R. P. Erythrocyte antioxidants and membrane vulnerability. J. Lab. Clin. Med. 107:1986;401-404.
52. Browne P. V., Shalev O., Kuypers F. A., Brugnara C., Solovey A., Mohandas N., Schrier S. L., Hebbel R. P. Removal of erythrocyte membrane iron in vivo ameliorates the pathobiology of murine thalassemia. J. Clin. Invest. 100:1997;1459-1464.
53. Shinar E., Rachmilewitz E. A. Oxidative denaturation of red blood cells in thalassemia. Semin. Hematol. 27:1990;70-82.
54. Scott M. D., van den Berg J. J. M., Repka T., Rouyer-Fessard P., Hebbel R. P., Beuzard Y., Lubin B. H. Effect of excess a-hemoglobin chains on cellular and membrane oxidation in model b-thalassemic erythrocytes. J. Clin. Invest. 91:1993;1706-1712.
55. Advani R., Rubin E., Mohandas N., Schrier S. L. Oxidative red blood cell membrane injury in the pathophysiology of severe mouse β-thalassemia. Blood. 79:1992;1064-1067.
56. Yuan J., Kannan R., Shinar E., Rachmilewitz E. A., Low P. S. Isolation, characterization, and immunoprecipitation studies of immune complexes from membranes of b-thalassemic erythrocytes. Blood. 79:1992;3007-3013.
57. Schrier S. L., Rachmilewitz E. A., Mohandas N. Cellular and membrane properties of alpha and beta thalassemic erythrocytes are different Implication for differences in clinical manifestations . Blood. 74:1989;2194-2202.
58. Shinar E., Rachmilewitz E. A., Lux S. E. Differing erythrocyte membrane skeletal protein defects in alpha and beta thalassemia. J. Clin. Invest. 83:1989;404-410.
59. Sorenson S., Rubin E., Polster H., Mohandas N., Schrier S. The role of membrane skeletal-associated α-globin in the pathophysiology of β-thalassemia. Blood. 75:1990;1333-1336.
60. Schrier S. L., Mohandas N. Globin-chain specificity of oxidation-induced changes in red blood cell membrane properties. Blood. 79:1992;1586-1592.
61. Advani R., Sorenson S., Shinar E., Lande W., Rachmilewitz E., Schrier S. L. Characterization and comparison of the red blood cell membrane damage in severe human α- and β-thalassemia. Blood. 79:1992;1058-1063.
62. Olivieri O., De Franceschi L., Capelini M. D., Girelli D., Corrocher R., Brugnara C. Oxidative damage and erythrocyte membrane transport abnormalities in thalassemias. Blood. 84:1994;315-320.
63. Bookchin R. M., Ortiz O. E., Shalev O., Tsurel S., Rachmilewitz E. A., Hockaday A., Lew V. L. Calcium transport and ultrastructure of red cells in beta-thalassemia intermedia. Blood. 72:1988;1602-1607.
64. Winterbourn C. C. Oxidative denaturation in congenital hemolytic anemias The unstable hemoglobins [Review] . Semin. Hematol. 27:1990;41-50.
65. Schlüter K., Drenckhahn D. Co-clustering of denatured hemoglobin with band 3 Its role in binding of autoantibodies against band 3 to abnormal and aged erythrocytes . Proc. Natl. Acad. Sci. U.S.A. 83:1986;6137-6141.
66. Halliday C. E. W., Halliday J. W., Powell L. W. The clinical manifestations of chronic iron overload [Review]. Baillére's Clin. Haematol. 2:1989;403-421.
67. Schafer A. I., Cheron R. G., Dluhy R., Cooper B., Gleason R. E., Soeldner J. S., Bunn H. F. Clinical consequences of acquired transfusional iron overload in adults. N. Engl. J. Med. 304:1981;319-324.
68. Minotti G., Di Gennaro M., D'Ugo D., Granone P. Possible sources of iron for lipid peroxidation. Free Rad. Res. Comms. 12:1991;99-106.
69. Voest E. E., Vreugdenhil G., Marx J. J. M. Iron-chelating agents in non-iron overload conditions. Ann. Intern. Med. 120:1994;490-499.