Reactive oxygen species and phosphatidylserine externalization in murine sickle red cells

British Journal of Haematology

Volumn 124, Issue 3, 2004, Pages 391-402

  Banerjee, Tinku ^a   Kuypers, Frans A ^a  

^a CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

Author keywords

Flipase; Phosphatidylserine; Reactive oxygen species; Reduced glutathione; Sickle cell

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMINOPHOSPHOLIPID; CARRIER PROTEIN; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUTATHIONE; GLUTATHIONE REDUCTASE; PHOSPHATIDYLSERINE; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; DATA ANALYSIS; ENERGY CONSUMPTION; ENZYME ACTIVITY; EXOCYTOSIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SICKLE CELL; STATISTICAL SIGNIFICANCE;

ADENOSINE TRIPHOSPHATE; ANEMIA, SICKLE CELL; ANIMALS; CARRIER PROTEINS; ERYTHROCYTES; FLOW CYTOMETRY; GLUCOSEPHOSPHATE DEHYDROGENASE; GLUTATHIONE; GLUTATHIONE REDUCTASE; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MODELS, ANIMAL; PHOSPHATIDYLSERINES; PHOSPHOLIPID TRANSFER PROTEINS; REACTIVE OXYGEN SPECIES;

EID: 0842287251     PISSN: 00071048     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2141.2003.04781.x     Document Type: Article

References (61)

1. al-Ali, A.K. (1994) Erythrocyte reduced glutathione level in sickle cell anaemia and glucose-6-phosphate dehydrogenase deficient Saudi subjects. Annals of Clinical Biochemistry, 31(Pt 3), 296-297.
2. Anderson, H.A., Maylock, C.A., Williams, J.A., Paweletz, C.P., Shu, H. & Shacter, E. (2003) Serum-derived protein S binds to phosphatidylserine and stimulates the phagocytosis of apoptotic cells. Nature Immunology, 4, 87-91.
3. Bass, D.A., Parce, J.W., Dechatelet, L.R., Szejda, P., Seeds, M.C. & Thomas, M. (1983) Flow cytometric studies of oxidative product formation by neutrophils: a graded response to membrane stimulation. Journal of Immunology, 130, 1910-1917.
4. Belcher, J.D., Bryant, C.J., Nguyen, J., Bowlin, P.R., Kielbik, M.C., Bischof, J.C., Hebbel, R.P. & Vercellotti, G.M. (2003) Transgenic sickle mice have vascular inflammation. Blood, 101, 3953-3959.
5. Bensinger, T.A. & Gillette, P.N. (1974) Hemolysis in sickle cell disease. Archives of Internal Medicine, 133, 624-631.
6. van den Berg, J.J.M., Kuypers, F.A., Lubin, B.H., Roelofsen, B. & Op den Kamp, J.A.F. (1991) Direct and continuous measurement of hydroperoxide-induced oxidative stress on the membrane of intact erythrocytes. Free Radical Biology and Medicine, 11, 255-261.
7. Blumenfeld, N., Zachowski, A., Galacteros, F., Beuzard, Y. & Devaux, P.F. (1991) Transmembrane mobility of phospholipids in sickle erythrocytes: effect of deoxygenation on diffusion and asymmetry. Blood, 77, 849-854.
8. Bonomini, M., Sirolli, V., Settefrati, N., Dottori, S., Di Liberato, L. & Arduini, A. (1999) Increased erythrocyte phosphatidylserine exposure in chronic renal failure. Journal of the American Society of Nephrology, 10, 1982-1990.
9. Borenstain-Ben Yashar, V., Barenholz, Y., Hy-Am, E., Rachmilewitz, E.A. & Eldor, A. (1993) Phosphatidylserine in the outer leaflet of red blood cells from beta-thalassemia patients may explain the chronic hypercoagulable state and thrombotic episodes. American Journal of Hematology, 44, 63-65.
10. Carrell, R.W., Winterbourn, C.C. & Rachmilewitz, E.A. (1975) Activated oxygen and haemolysis. British Journal of Haematology, 30, 259-264.
11. Chiu, D.T.-Y., van den Berg, J., Kuypers, F.A., Hung, I.-J., Wei, J.-S. & Liu, T.-Z. (1996) Correlation of membrane lipid peroxidation with oxidation of hemoglobin variants: Possibly related to the rates of hemin release. Free Radical Biology and Medicine, 21, 89-95.
12. Comfurius, P., Senden, J.M.G., Tilly, R.H.J., Schroit, A.J., Bevers, E.M. & Zwaal, R.F.A. (1990) Loss of membrane phospholipid asymmetry in platelets and red cells may be associated with calcium-induced shedding of plasma membrane and inhibition of aminophospholipid translocase. Biochimica et Biophysica Acta, 1026, 153-160.
13. Das, S.K. & Nair, R.C. (1980) Superoxide dismutase, glutathione peroxidase, catalase and lipid peroxidation of normal and sickled erythrocytes. British Journal of Haematology, 44, 87-92.
14. De Jong, K., Geldwerth, D. & Kuypers, F.A. (1997) Oxidative damage does not alter membrane phospholipid asymmetry in human erythrocytes. Biochemistry, 36, 6768-6776.
15. Devaux, P.F. (1988) Phospholipid flippases. FEBS Letters, 234, 8-12.
16. Dincer, Y., Akcay, T., Alademir, Z. & Ilkova, H. (2002) Effect of oxidative stress on glutathione pathway in red blood cells from patients with insulin-dependent diabetes mellitus. Metabolism: Clinical and Experimental, 51, 1360-1362.
17. Fadok, V.A., de Cathelineau, A., Daleke, D.L., Henson, P.M. & Bratton, D.L. (2001) Loss of phospholipid asymmetry and surface exposure of phosphatidylserine is required for phagocytosis of apoptotic cells by macrophages and fibroblasts. Journal of Biological Chemistry, 276, 1071-1077.
18. Gaetani, G.F., Galiano, S., Canepa, L., Ferraris, A.M. & Kirkman, H.N. (1989) Catalase and glutathione peroxidase are equally active in detoxification of hydrogen peroxide in human erythrocytes. Blood, 73, 334-339.
19. Glock, G. & McLean, P. (1953) Further studies on the properties and assay of glucose-6-phosphate-dehydrogenase and 6-phosphogluconate dehydroxygenase of rat liver. Biochemical Journal, 55, 400-408.
20. Harvey, J.W. (1996) Congenital erythrocyte enzyme deficiencies. Veterinarian Clinic North American Small Animal Practices, 26, 1003-1011.
21. el-Hazmi, M.A. & Warsy, A.S. (1989) Glutathione reductase in the south-western province of Saudi Arabia - genetic variation vs. acquired deficiency. Haematologia (Budapest), 22, 37-42.
22. Hebbel, R.P., Eaton, J.W., Balasingam, M. & Steinberg, M.H. (1982) Spontaneous oxygen radical generation by sickle erythrocytes. Journal of Clinical Investigation, 70, 1253-1259.
23. Hebbel, R.P., Morgan, W.T., Eaton, J.W. & Hedlund, B.E. (1988) Accelerated autoxidation and heme loss due to instability of sickle hemoglobin. Proceedings of the National Academy of Sciences of the United States of America, 85, 237-241.
24. Herrmann, A. & Devaux, P.F. (1990) Alteration of the aminophospholipid translocase activity during in vivo and artificial aging of human erythrocytes. Biochimica et Biophysica Acta, 1027, 41-46.
25. de Jong, K., Emerson, R., Butler, H., Narla, M. & Kuypers, F.A. (2001a) Short survival of PS exposing red blood cells in murine sickle cell anemia. Blood, 98, 1577-1584.
26. de Jong, K., Larkin, S.K., Styles, L.A., Bookchin, R.M. & Kuypers, F.A. (2001b) Characterization of the phosphatidylserine-exposing subpopulation of sickle cells. Blood, 98, 860-867.
27. Kattamis, C. & Kattamis, A.C. (2001) Oxidative stress disturbances in erythrocytes of beta-thalassemia. Journal of Pediatric Hematology/Oncology, 18, 85-88.
28. Khan, A.A., Schuler, M.M. & Coppock, R.W. (1987) Inhibitory effects of various sulfur compounds on the activity of bovine erythrocyte enzymes. Journal of Toxicology and Environmental Health, 22, 481-490.
29. Kim, D.K., Cho, E.S. & Um, H.D. (2000) Caspase-dependent and -independent events in apoptosis induced by hydrogen peroxide. Experimental Cell Research, 257, 82-88.
30. Kletzien, R.F., Harris, P.K. & Foellmi, L.A. (1994) Glucose-6-phosphate dehydrogenase: a "housekeeping" enzyme subject to tissue-specific regulation by hormones, nutrients, and oxidant stress. FASEB Journal, 8, 174-181.
31. Kojima, H., Newton-Nash, D., Weiss, H.J., Zhao, J., Sims, P.J. & Wiedmer, T. (1994) Production and characterization of transformed B-lymphocytes expressing the membrane defect of Scott syndrome. Journal of Clinical Investigation, 94, 2237-2244.
32. Kuypers, F.A. (1998) Phospholipid asymmetry in health and disease. Current Opinion in Hematology, 5, 122-131.
33. Kuypers, F.A., Lewis, R.A., Ernst, J.D., Discher, D. & Lubin, B.H. (1996) Detection of altered membrane phospholipid asymmetry in subpopulations of human red cells using fluorescently labeled annexin V. Blood, 87, 1179-1187.
34. Kuypers, F.A., Yuan, J., Lewis, R.A., Snyder, L.M., Kiefer, C.R., Bunyaratvej, A., Fucharoen, S., Ma, L., Styles, L., de Jong, K. & Schrier, S.L. (1998) Membrane phospholipid asymmetry in human thalassemia. Blood, 91, 3044-3051.
35. Lachant, N.A., Davidson, W.D. & Tanaka, K.R. (1983) Impaired pentose phosphate shunt function in sickle cell disease: a potential mechanism for increased Heinz body formation and membrane lipid peroxidation. American Journal of Hematology, 15, 1-13.
36. Mandal, D., Moitra, P.K., Saha, S. & Basu, J. (2002) Caspase 3 regulates phosphatidylserine externalization and phagocytosis of oxidatively stressed erythrocytes. FEBS Letters, 513, 184-188.
37. Manodori, A.B. & Kuypers, F.A. (2002) Altered red cell turnover in diabetic mice. Journal of Laboratory and Clinical Medicine, 140, 161-165.
38. Matsura, T., Serinkan, B.F., Jiang, J. & Kagan, V.E. (2002) Phosphatidylserine peroxidation/externalization during staurosporine-induced apoptosis in HL-60 cells. FEBS Letters, 524, 25-30.
39. Meister, A. (1988) Glutathione metabolism and its selective modification. Journal of Biological Chemistry, 263, 17205-17208.
40. Meister, A. & Anderson, M.E. (1983) Glutathione. Annual Review of Biochemistry, 52, 711-760.
41. Nagel, R.L. (1998) A knockout of a transgenic mouse - animal models of sickle cell anemia. New England Journal of Medicine, 339, 194-195.
42. Pandolfi, P.P., Sonati, F., Rivi, R., Mason, P., Grosveld, F. & Luzzatto, L. (1995) Targeted disruption of the housekeeping gene encoding glucose 6-phosphate dehydrogenase (G6PD): G6PD is dispensable for pentose synthesis but essential for defense against oxidative stress. EMBO Journal, 14, 5209-5215.
43. Paszty, C., Brion, C.M., Manci, E., Witkowska, H.E., Stevens, M.E., Mohandas, N. & Rubin, E.M. (1997) Transgenic knockout mice with exclusively human sickle hemoglobin and sickle cell disease. Science, 278, 876-878.
44. Rice-Evans, C., Omorphos, S.C. & Baysal, E. (1986) Sickle cell membranes and oxidative damage. Biochemical Journal, 237, 265-269.
45. Salh, B., Assi, K., Huang, S., O'Brien, L., Steinbrecher, U. & Gomez-Munoz, A. (2002) Dissociated ROS production and ceramide generation in sulfasalazine-induced cell death in Raw 264.7 cells. Journal of Leukocyte Biology, 72, 790-799.
46. Salvemini, F., Franze, A., Iervolino, A., Filosa, S., Salzano, S. & Ursini, M.V. (1999) Enhanced glutathione levels and oxidoresistance mediated by increased glucose-6-phosphate dehydrogenase expression. Journal of Biological Chemistry, 274, 2750-2757.
47. Setty, B.N., Kulkarni, S. & Stuart, M.J. (2002) Role of erythrocyte phosphatidylserine in sickle red cell-endothelial adhesion. Blood, 99, 1564-1571.
48. Shimizu, Y., Kawarada, S.Y., Suzuki, M. & Tanaka, T. (1991) Interstrain differences in red cell enzyme activities in mice and rats. Comparative Biology and Physiology - Part B: Biochemistry & Molecular Biology, 100, 687-690.
49. Sims, P.J. & Wiedmer, T. (2001) Unraveling the mysteries of phospholipid scrambling. Thrombosis and Haemostasis, 86, 266-275.
50. Srinivasan, P.T. & Basu, J. (1996) Altered membrane phospholipid organization and erythrophagocytosis in E beta-thalassemia. Biochimica et Biophysica Acta, 1285, 65-70.
51. Stocks, J., Offerman, E.L., Modell, C.B. & Dormandy, T.L. (1972) The susceptibility to autoxidation of human red cell lipids in health and disease. British Journal of Haematology, 23, 713-724.
52. Ursini, M.V., Parrella, A., Rosa, G., Salzano, S. & Martini, G. (1997) Enhanced expression of glucose-6-phosphate dehydrogenase in human cells sustaining oxidative stress. Biochemical Journal, 323(Pt 3), 801-806.
53. Vincent, A.M., Brownlee, M. & Russell, J.W. (2002) Oxidative stress and programmed cell death in diabetic neuropathy. Annals of the New York Academy of Sciences, 959, 368-383.
54. Wallace, W. & Caughey, W. (1979) Superoxide as a Participant in the Chemistry of Oxy-hemoglobin. Academic Press, New York.
55. Wenderoth, I., Scheibe, R. & von Schaewen, A. (1997) Identification of the cysteine residues involved in redox modification of plant plastidic glucose-6-phosphate dehydrogenase. Journal of Biological Chemistry, 272, 26985-26990.
56. Wetterstroem, N., Brewer, G.J., Warth, J.A., Mitchinson, A. & Near, K. (1984) Relationship of glutathione levels and Heinz body formation to irreversibly sickled cells in sickle cell anemia. Journal of Laboratory and Clinical Medicine, 103, 589-596.
57. Wilson, M.J., Richter-Lowney, K. & Daleke, D.L. (1993) Hyperglycemia induces a loss of phospholipid asymmetry in human erythrocytes. Biochemistry, 32, 11302-11310.
58. Wood, B.L., Gibson, D.F. & Tait, J.F. (1996) Increased erythrocyte phosphatidylserine exposure in sickle cell disease: flow-cytometric measurement and clinical associations. Blood, 88, 1873-1880.
59. Yasin, Z., Witting, S., Palascak, M.B., Joiner, C.H., Rucknagel, D.L. & Franco, R.S. (2003) Phosphatidylserine externalization in sickle red blood cells: associations with cell age, density, and hemoglobin F. Blood, 102, 365-370.
60. Zhao, J., Zhou, Q., Wiedmer, T. & Sims, P.J. (1998) Level of expression of phospholipid scramblase regulates induced movement of phosphatidylserine to the cell surface. Journal of Biological Chemistry, 273, 6603-6606.
61. Zhong, L., Arner, E.S. & Holmgren, A. (2000) Structure and mechanism of mammalian thioredoxin reductase: the active site is a redox-active selenolthiol/selenenylsulfide formed from the conserved cysteine-selenocysteine sequence. Proceedings of the National Academy of Sciences of the United States of America, 97, 5854-5859.