Hemoglobin S polymerization and red cell membrane changes

Hematology/Oncology Clinics of North America

Volumn 28, Issue 2, 2014, Pages 155-179

  Kuypers, Frans A ^a  

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

Author keywords

Membrane lipids; Microparticles; Oxidative damage; Polymerization

Indexed keywords

HEMOGLOBIN S; MEMBRANE LIPID; MEMBRANE PHOSPHOLIPID; PHOSPHATIDYLSERINE; PHOSPHOLIPID; LIPID BILAYER;

ACUTE CHEST SYNDROME; ERYTHROCYTE MEMBRANE; ERYTHROPOIESIS; HUMAN; INTRAVASCULAR HEMOLYSIS; LIPID MEMBRANE; LIPID METABOLISM; MEMBRANE MICROPARTICLE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN POLYMERIZATION; PROTEIN PURIFICATION; REVIEW; SICKLE CELL ANEMIA; VASCULAR DISEASE; BIOLOGICAL MODEL; BLOOD; ERYTHROCYTE; LIPID BILAYER; METABOLISM; OXIDATION REDUCTION REACTION; POLYMERIZATION;

ANEMIA, SICKLE CELL; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; HEMOGLOBIN, SICKLE; HUMANS; LIPID BILAYERS; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; POLYMERIZATION;

EID: 84896719541     PISSN: 08898588     EISSN: 15581977     Source Type: Journal    
DOI: 10.1016/j.hoc.2013.12.002     Document Type: Review

References (170)

1. Herrick J.B. Peculiar elongated and sickle-shaped red blood corpuscles in a case of severe anemia. 1910. Yale J Biol Med 2001, 74(3):179-184.
2. Pauling L., Itano H.A., et al. Sickle cell anemia a molecular disease. Science 1949, 110(2865):543-548.
3. Hebbel R.P. The sickle erythrocyte in double jeopardy: autoxidation and iron decompartmentalization. Semin Hematol 1990, 27(1):51-69.
4. Mohandas N., An X. New insights into function of red cell membrane proteins and their interaction with spectrin-based membrane skeleton. Transfus Clin Biol 2006, 13(1-2):29-30. 10.1016/j.tracli.2006.02.017.
5. Tse W.T., Lux S.E. Red blood cell membrane disorders. Br J Haematol 1999, 104(1):2-13.
6. Martorana M.C., Mojoli G., Cianciulli P., et al. Sickle cell anaemia: haemorheological aspects. Ann Ist Super Sanita 2007, 43(2):164-170.
7. Athanassiou G., Moutzouri A., Kourakli A., et al. Effect of hydroxyurea on the deformability of the red blood cell membrane in patients with sickle cell anemia. Clin Hemorheol Microcirc 2006, 35(1-2):291-295.
8. Vekilov P.G. Sickle-cell haemoglobin polymerization: is it the primary pathogenic event of sickle-cell anaemia?. Br J Haematol 2007, 139(2):173-184. 10.1111/j.1365-2141.2007.06794.
9. Knee K.M., Roden C.K., Flory M.R., et al. The role of beta93 Cys in the inhibition of Hb S fiber formation. Biophys Chem 2007, 127(3):181-193. 10.1016/j.bpc.2007.02.002.
10. Aprelev A., Weng W., Zakharov M., et al. Metastable polymerization of sickle hemoglobin in droplets. JMol Biol 2007, 369(5):1170-1174. 10.1016/j.jmb.2007.04.030.
11. Srinivasulu S., Perumalsamy K., Upadhya R., et al. Pair-wise interactions of polymerization inhibitory contact site mutations of hemoglobin-S. Protein J 2006, 25(7-8):503-516. 10.1007/s10930-006-9034-3.
12. Rotter M., Yosmanovich D., Briehl R.W., et al. Nucleation of sickle hemoglobin mixed with hemoglobin A: experimental and theoretical studies of hybrid-forming mixtures. Biophys J 2011, 101(11):2790-2797. 10.1016/j.bpj.2011.10.027.
13. Wang W.C. The pharmacotherapy of sickle cell disease. Expert Opin Pharmacother 2008, 9(17):3069-3082. 10.1517/14656560802519878.
14. Coleman E., Inusa B. Sickle cell anemia: targeting the role of fetal hemoglobinintherapy. Clin Pediatr 2007, 46(5):386-391. 10.1177/0009922806297751.
15. Moreira L.S., de Andrade T.G., Albuquerque D.M., et al. Identification of differentially expressed genes induced by hydroxyurea in reticulocytes from sickle cell anaemia patients. Clin Exp Pharmacol Physiol 2008, 35(5-6):651-655. 10.1111/j.1440-1681.2007.04861.
16. Ghatpande S.S., Choudhary P.K., Quinn C.T., et al. Pharmaco-proteomic study of hydroxyurea-induced modifications in the sickle red blood cell membrane proteome. Exp Biol Med 2008, 233(12):1510-1517. 10.3181/0805-S-149.
17. Johnson C., Telen M.J. Adhesion molecules and hydroxyurea in the pathophysiology of sickle cell disease. Haematologica 2008, 93(4):481-485. 10.3324/haematol.12734.
18. Cartron J.P., Elion J. Erythroid adhesion molecules in sickle cell disease: effect of hydroxyurea. Transfus Clin Biol 2008, 15(1-2):39-50. 10.1016/j.tracli.2008.05.001.
19. Styles L.A., Lubin B., Vichinsky E., et al. Decrease of very late activation antigen-4 and CD36 on reticulocytes in sickle cell patients treated with hydroxyurea. Blood 1997, 89(7):2554-2559.
20. Haynes J., Obiako B., Hester R.B., et al. Hydroxyurea attenuates activated neutrophil-mediated sickle erythrocyte membrane phosphatidylserine exposure and adhesion to pulmonary vascular endothelium. Am J Physiol Heart Circ Physiol 2008, 294(1):H379-H385. 10.1152/ajpheart.01068.2007.
21. Daak A.A., Ghebremeskel K., Elbashir M.I., et al. Hydroxyurea therapy mobilises arachidonic acid from inner cell membrane aminophospholipids in patients with homozygous sickle cell disease. JLipids 2011, 2011:718014. 10.1155/2011/718014.
22. van Dijk T.B., Gillemans N., Pourfarzad F., et al. Fetal globin expression is regulated by Friend of Prmt1. Blood 2010, 116(20):4349-4352. 10.1182/blood-2010-03-274399.
23. Chen Z., Luo H.Y., Basran R.K., et al. AT-to-G transversion at nucleotide -567 upstream of HBG2 in a GATA-1 binding motif is associated with elevated hemoglobin F. Mol Cell Biol 2008, 28(13):4386-4393.
24. Lettre G., Sankaran V.G., Bezerra M.A., et al. DNA polymorphisms at the BCL11A, HBS1L-MYB, and beta-globin loci associate with fetal hemoglobin levels and pain crises in sickle cell disease. Proc Natl Acad Sci USA 2008, 105(33):11869-11874.
25. Sebastiani P., Wang L., Nolan V.G., et al. Fetal hemoglobin in sickle cell anemia: Bayesian modeling of genetic associations. Am J Hematol 2008, 83(3):189-195. 10.1002/ajh.21048.
26. Uda M., Galanello R., Sanna S., et al. Genome-wide association study shows BCL11A associated with persistent fetal hemoglobin and amelioration of the phenotype of beta-thalassemia. Proc Natl Acad Sci USA 2008, 105(5):1620-1625.
27. Menzel S., Garner C., Gut I., et al. AQTL influencing F cell production maps to a gene encoding a zinc-finger protein on chromosome 2p15. Nat Genet 2007, 39(10):1197-1199.
28. Saiki Y., Yamazaki Y., Yoshida M., et al. Human EVI9, a homologue of the mouse myeloid leukemia gene, is expressed in the hematopoietic progenitors and down-regulated during myeloid differentiation of HL60 cells. Genomics 2000, 70(3):387-391.
29. Sankaran V.G., Menne T.F., Xu J., et al. Human fetal hemoglobin expression is regulated by the developmental stage-specific repressor BCL11A. Science 2008, 322(5909):1839-1842.
30. Sedgewick A.E., Timofeev N., Sebastiani P., et al. BCL11A is a major HbF quantitative trait locus in three different populations with beta-hemoglobinopathies. Blood Cells Mol Dis 2008, 41(3):255-258.
31. Senawong T., Peterson V.J., Leid M. BCL11A-dependent recruitment of SIRT1 to a promoter template in mammalian cells results in histone deacetylation and transcriptional repression. Arch Biochem Biophys 2005, 434(2):316-325.
32. Ma Q., Wyszynski D.F., Farrell J.J., et al. Fetal hemoglobin in sickle cell anemia: genetic determinants of response to hydroxyurea. Pharmacogenomics J 2007, 7(6):386-394.
33. Hankins J.S., Wynn L.W., Brugnara C., et al. Phase I study of magnesium pidolate in combination with hydroxycarbamide for children with sickle cell anaemia. Br J Haematol 2008, 140(1):80-85. 10.1111/j.1365-2141.2007.06884.
34. Nagababu E., Fabry M.E., Nagel R.L., et al. Heme degradation and oxidative stress in murine models for hemoglobinopathies: thalassemia, sickle cell disease and hemoglobin C disease. Blood Cells Mol Dis 2008, 41(1):60-66. 10.1016/j.bcmd.2007.12.003.
35. Takahashi T., Shimizu H., Morimatsu H., et al. Heme oxygenase-1: a fundamental guardian against oxidative tissue injuries in acute inflammation. Mini Rev Med Chem 2007, 7(7):745-753.
36. Pan W., Uzunova V.V., Vekilov P.G. Free heme in micromolar amounts enhances the attraction between sickle cell hemoglobin molecules. Biopolymers 2009, 91(12):1108-1116. 10.1002/bip.21191.
37. Uzunova V.V., Pan W., Galkin O., et al. Free heme and the polymerization of sickle cell hemoglobin. Biophys J 2010, 99(6):1976-1985. 10.1016/j.bpj.2010.07.024.
38. Wang J.C., Kwong S., Ferrone F.A., et al. Fiber depolymerization: fracture, fragments, vanishing times, and stochastics in sickle hemoglobin. Biophys J 2009, 96(2):655-670. 10.1016/j.bpj.2008.04.001.
39. Weinkam P., Sali A. Mapping polymerization and allostery of hemoglobin S using point mutations. JPhys Chem B 2013, 117(42):13058-13068. 10.1021/jp4025156.
40. Dash B.P., Archana Y., Satapathy N., et al. Search for antisickling agents from plants. Pharmacogn Rev 2013, 7(13):53-60. 10.4103/0973-7847.112849.
41. Zhang Y., Xia Y. Adenosine signaling in normal and sickle erythrocytes and beyond. Microbes Infect 2012, 14(10):863-873. 10.1016/j.micinf.2012.05.005.
42. Stefanovic M., Puchulu-Campanella E., Kodippili G., et al. Oxygen regulates the band 3-ankyrin bridge in the human erythrocyte membrane. Biochem J 2013, 449(1):143-150. 10.1042/BJ20120869.
43. Rogers S.C., Ross J.G., d'Avignon A., et al. Sickle hemoglobin disturbs normal coupling among erythrocyte O2 content, glycolysis, and antioxidant capacity. Blood 2013, 121(9):1651-1662. 10.1182/blood-2012-02-414037.
44. Goodman S.R., Daescu O., Kakhniashvili D.G., et al. The proteomics and interactomics of human erythrocytes. Exp Biol Med 2013, 238(5):509-518. 10.1177/1535370213488474.
45. Biondani A., Turrini F., Carta F., et al. Heat-shock protein-27, -70 and peroxiredoxin-II show molecular chaperone function in sickle red cells: evidence from transgenic sickle cell mouse model. Proteomics Clin Appl 2008, 2(5):706-719. 10.1002/prca.200780058.
46. Kaore S.N., Amane H.S., Kaore N.M. Citrulline: pharmacological perspectives and its role as an emerging biomarker in future. Fundam Clin Pharmacol 2013, 27(1):35-50. 10.1111/j.1472-8206.2012.01059.
47. Ellory J.C., Robinson H.C., Browning J.A., et al. Abnormal permeability pathways in human red blood cells. Blood Cells Mol Dis 2007, 39(1):1-6. 10.1016/j.bcmd.2007.02.011.
48. Raghupathy R., Billett H.H. Promising therapies in sickle cell disease. Cardiovasc Hematol Disord Drug Targets 2009, 9(1):1-8.
49. Darghouth D., Koehl B., Junot C., et al. Metabolomic analysis of normal and sickle cell erythrocytes. Transfus Clin Biol 2010, 17(3):148-150. 10.1016/j.tracli.2010.06.011.
50. Thomas S.L., Bouyer G., Cueff A., et al. Ion channels in human red blood cell membrane: actors or relics?. Blood Cells Mol Dis 2011, 46(4):261-265. 10.1016/j.bcmd.2011.02.007.
51. Lei H., Karniadakis G.E. Probing vasoocclusion phenomena in sickle cell anemia via mesoscopic simulations. Proc Natl Acad Sci USA 2013, 110(28):11326-11330. 10.1073/pnas.1221297110.
52. Hebbel R.P., Mohandas N. Reversible deformation-dependent erythrocyte cation leak. Extreme sensitivity conferred by minimal peroxidation. Biophys J 1991, 60(3):712-715. 10.1016/S0006-3495(91)82100-2.
53. Bogdanova A., Makhro A., Wang J., et al. Calcium in red blood cells-a perilous balance. Int J Mol Sci 2013, 14(5):9848-9872. 10.3390/ijms14059848.
54. 2+-permeable cation conductance sensitive to carbon monoxide and to GsMTx-4 in human and mouse sickle erythrocytes. PloS one 2010, 5(1):e8732. 10.1371/journal.pone.0008732.
55. Kuypers F.A., de Jong K. The role of phosphatidylserine in recognition and removal of erythrocytes. Cell Mol Biol 2004, 50(2):147-158.
56. George A., Pushkaran S., Konstantinidis D.G., et al. Erythrocyte NADPH oxidase activity modulated by Rac GTPases, PKC, and plasma cytokines contributes to oxidative stress in sickle cell disease. Blood 2013, 121(11):2099-2107. 10.1182/blood-2012-07-441188.
57. Fibach E., Rachmilewitz E. The role of oxidative stress in hemolytic anemia. Curr Mol Med 2008, 8(7):609-619.
58. Schrier S.L. Thalassemia: pathophysiology of red cell changes. Annu Rev Med 1994, 45:211-218.
59. Schrier S.L. Pathophysiology of thalassemia. Curr Opin Hematol 2002, 9(2):123-126.
60. 2 levels in erythrocytes. Free Radic BiolMed 2005, 39(11):1407-1417. 10.1016/j.freeradbiomed.2005.07.002.
61. Scott M.D., Lubin B.H., Zuo L., et al. Erythrocyte defense against hydrogen peroxide: preeminent importance of catalase. JLab Clin Med 1991, 118(1):7-16.
62. Hiner A.N., Raven E.L., Thorneley R.N., et al. Mechanisms of compound I formation in heme peroxidases. JInorg Biochem 2002, 91(1):27-34.
63. Reeder B.J. The redox activity of hemoglobins: from physiologic functions to pathologic mechanisms. Antioxid Redox Signal 2010, 13(7):1087-1123. 10.1089/ars.2009.2974.
64. Svistunenko D.A., Dunne J., Fryer M., et al. Comparative study of tyrosine radicals in hemoglobin and myoglobins treated with hydrogen peroxide. Biophys J 2002, 83(5):2845-2855. 10.1016/S0006-3495(02)75293-4.
65. Reeder B.J., Svistunenko D.A., Sharpe M.A., et al. Characteristics and mechanism of formation of peroxide-induced heme to protein cross-linking in myoglobin. Biochemistry 2002, 41(1):367-375.
66. Low F.M., Hampton M.B., Peskin A.V., et al. Peroxiredoxin 2 functions as a noncatalytic scavenger of low-level hydrogen peroxide in the erythrocyte. Blood 2007, 109(6):2611-2617. 10.1182/blood-2006-09-048728.
67. Ey J., Schomig E., Taubert D. Dietary sources and antioxidant effects of ergothioneine. JAgric Food Chem 2007, 55(16):6466-6474. 10.1021/jf071328f.
68. Suh J.H., Kim R., Yavuz B., et al. Clinical assay of four thiol amino acid redox couples by LC-MS/MS: utility in thalassemia. JChromatogr B Analyt Technol Biomed Life Sci 2009, 877(28):3418-3427. 10.1016/j.jchromb.2009.06.041.
69. Grigat S., Harlfinger S., Pal S., et al. Probing the substrate specificity of the ergothioneine transporter with methimazole, hercynine, and organic cations. Biochem Pharmacol 2007, 74(2):309-316. 10.1016/j.bcp.2007.04.015.
70. Grundemann D., Harlfinger S., Golz S., et al. Discovery of the ergothioneine transporter. Proc Natl Acad Sci USA 2005, 102(14):5256-5261. 10.1073/pnas.0408624102.
71. Akanmu D., Cecchini R., Aruoma O.I., et al. The antioxidant action of ergothioneine. Arch Biochem Biophys 1991, 288(1):10-16.
72. Zhu B.Z., Mao L., Fan R.M., et al. Ergothioneine prevents copper-induced oxidative damage to DNA and protein by forming a redox-inactive ergothioneine-copper complex. Chem Res Toxicol 2011, 24(1):30-34. 10.1021/tx100214t.
73. Robinson S.R., Dang T.N., Dringen R., et al. Hemin toxicity: a preventable source of brain damage following hemorrhagic stroke. Redox Rep 2009, 14(6):228-235. 10.1179/135100009X12525712409931.
74. Wicher K.B., Fries E. Evolutionary aspects of hemoglobin scavengers. Antioxid Redox Signal 2010, 12(2):249-259. 10.1089/ars.2009.2760.
75. Xue H., Guo H., Li Y.C., et al. Heme oxygenase-1 induction by hemin protects liver cells from ischemia/reperfusion injury in cirrhotic rats. World J Gastroenterol 2007, 13(40):5384-5390.
76. Reeder B.J., Wilson M.T. Hemoglobin and myoglobin associated oxidative stress: from molecular mechanisms to disease states. Curr Med Chem 2005, 12(23):2741-2751.
77. Galaris D., Eddy L., Arduini A., et al. Mechanisms of reoxygenation injury in myocardial infarction: implications of a myoglobin redox cycle. Biochem Biophys Res Commun 1989, 160(3):1162-1168.
78. Cassidy R.A., Burleson D.G., Delgado A.V., et al. Effects of heme proteins on nitric oxide levels and cell viability in isolated PMNs: a mechanism of toxicity. JLeukoc Biol 2000, 67(3):357-368.
79. Atamna H. Amino acids variations in amyloid-beta peptides, mitochondrial dysfunction, and new therapies for Alzheimer's disease. JBioenerg Biomembr 2009, 41(5):457-464. 10.1007/s10863-009-9246-2.
80. Atamna H., Boyle K. Amyloid-beta peptide binds with heme to form a peroxidase: relationship to the cytopathologies of Alzheimer's disease. Proc Natl Acad Sci USA 2006, 103(9):3381-3386. 10.1073/pnas.0600134103.
81. Atamna H. Heme binding to Amyloid-beta peptide: mechanistic role in Alzheimer's disease. JAlzheimers Dis 2006, 10(2-3):255-266.
82. Kosicek M., Malnar M., Goate A., et al. Cholesterol accumulation in Niemann Pick type C (NPC) model cells causes a shift in APP localization to lipid rafts. Biochem Biophys Res Commun 2010, 393(3):404-409. 10.1016/j.bbrc.2010.02.007.
83. Burns M., Gaynor K., Olm V., et al. Presenilin redistribution associated with aberrant cholesterol transport enhances beta-amyloid production invivo. JNeurosci 2003, 23(13):5645-5649.
84. Nagy E., Eaton J.W., Jeney V., et al. Red cells, hemoglobin, heme, iron, and atherogenesis. Arterioscler Thromb Vasc Biol 2010, 30(7):1347-1353. 10.1161/ATVBAHA.110.206433.
85. Piccin A., Murphy W.G., Smith O.P. Circulating microparticles: pathophysiology and clinical implications. Blood Rev 2007, 21(3):157-171. 10.1016/j.blre.2006.09.001.
86. Nebor D., Romana M., Santiago R., et al. Fetal hemoglobin and hydroxycarbamide modulate both plasma concentration and cellular origin of circulating microparticles in sickle cell anemia children. Haematologica 2013, 98(6):862-867. 10.3324/haematol.2012.073619.
87. Westerman M., Pizzey A., Hirschman J., et al. Microvesicles in haemoglobinopathies offer insights into mechanisms of hypercoagulability, haemolysis and the effects of therapy. Br J Haematol 2008, 142(1):126-135. 10.1111/j.1365-2141.2008.07155.x.
88. Villaescusa R., Arce A.A., Lalanne-Mistrih M.L., et al. Natural antiband 3 antibodies in patients with sickle cell disease. CR Biol 2013, 336(3):173-176. 10.1016/j.crvi.2012.09.002.
89. Ferru E., Giger K., Pantaleo A., et al. Regulation of membrane-cytoskeletal interactions by tyrosine phosphorylation of erythrocyte band 3. Blood 2011, 117(22):5998-6006. 10.1182/blood-2010-11-317024.
90. Camus S.M., Gausseres B., Bonnin P., et al. Erythrocyte microparticles can induce kidney vaso-occlusions in a murine model of sickle cell disease. Blood 2012, 120(25):5050-5058. 10.1182/blood-2012-02-413138.
91. Myher J.J., Kuksis A., Pind S. Molecular species of glycerophospholipids and sphingomyelins of human erythrocytes: improved method of analysis. Lipids 1989, 24(5):396-407.
92. Van Den Berg J.J., Op den Kamp J.A., Lubin B.H., et al. Conformational changes in oxidized phospholipids and their preferential hydrolysis by phospholipase A2: a monolayer study. Biochemistry 1993, 32(18):4962-4967.
93. Lubin B.H., Kuypers F.A. Phospholipid repair in human erythrocytes 1991, Pergamon Press, New York. 1st edition.
94. Lands W.E. Lipid metabolism. Annu Rev Biochem 1965, 34:313-346.
95. Fyrst H., Knudsen J., Lubin B.H., et al. Detection of AcylCoA binding protein in human red cells and investigation of its role in membrane phospholipid renewal. Biochem J 1995, 306:793-799.
96. Malhotra K., Malhotra K., Lubin B., et al. Identification and molecular characterization of acyl-CoA synthetase in human erythrocytes and erythroid precursors. Biochem J 1999, 344(1):135-141.
97. Soupene E., Serikov V., Kuypers F.A. Characterization of an acyl-coenzyme A binding protein predominantly expressed in human primitive progenitor cells. JLipid Res 2008, 49(5):1103-1112.
98. Soupene E., Kuypers F.A. Multiple erythroid isoforms of human long-chain acyl-CoA synthetases are produced by switch of the fatty acid gate domains. BMC Mol Biol 2006, 7(1):21.
99. Soupene E., Fyrst H., Kuypers F.A. Mammalian acyl-CoA:lysophosphatidylcholine acyltransferase enzymes. Proc Natl Acad Sci USA 2008, 105(1):88-93.
100. Soupene E., Kuypers F.A. Phosphatidylcholine formation by LPCAT1 is regulated by Ca(2+) and the redox status of the cell. BMC Biochem 2012, 13:8. 10.1186/1471-2091-13-8.
101. Andrick C., Broring K., Deuticke B., et al. Fast translocation of phosphatidylcholine to the outer membrane leaflet after its synthesis at the inner membrane surface in human erythrocytes. Biochim Biophys Acta 1991, 1064(2):235-241.
102. Bretscher M.S. Phosphatidyl-ethanolamine: differential labelling in intact cells and cell ghosts of human erythrocytes by a membrane-impermeable reagent. JMol Biol 1972, 71(3):523-528.
103. Bretscher M.S. Asymmetrical lipid bilayer structure for biological membranes. Nature New Biol 1972, 236(61):11-12.
104. Haest C.W., Deuticke B. Possible relationship between membrane proteins and phospholipid asymmetry in the human erythrocyte membrane. Biochim Biophys Acta 1976, 436(2):353-365.
105. Haest C.W., Plasa G., Kamp D., et al. Spectrin as a stabilizer of the phospholipid asymmetry in the human erythrocyte membrane. Biochim Biophys Acta 1978, 509(1):21-32.
106. Haest C.W., Erusalimsky J., Dressler V., et al. Transbilayer mobility of phospholipids in the erythrocyte membrane. Influence of the membrane skeleton. Biomed Biochim Acta 1983, 42(11-12):S17-S21.
107. Dressler V., Haest C.W., Plasa G., et al. Stabilizing factors of phospholipid asymmetry in the erythrocyte membrane. Biochim Biophys Acta 1984, 775(2):189-196.
108. Seigneuret M., Devaux P.F. ATP-dependent asymmetric distribution of spin-labeled phospholipids in the erythrocyte membrane: relation to shape changes. Proc Natl Acad Sci USA 1984, 81(12):3751-3755.
109. Balasubramanian K., Schroit A.J. Aminophospholipid asymmetry: a matter of life and death. Annu Rev Physiol 2003, 65:701-734.
110. Dekkers D.W., Comfurius P., Schroit A.J., et al. Transbilayer movement of NBD-labeled phospholipids in red blood cell membranes: outward-directed transport by the multidrug resistance protein 1 (MRP1). Biochemistry 1998, 37(42):14833-14837.
111. Dekkers D.W., Comfurius P., van Gool R.G., et al. Multidrug resistance protein 1 regulates lipid asymmetry in erythrocyte membranes. Biochem J 2000, 350(Pt 2):531-535.
112. Soupene E., Kuypers F.A. Identification of an erythroid ATP-dependent aminophospholipid transporter. Br J Haematol 2006, 133(4):436-438. 10.1111/j.1365-2141.2006.06051.x.
113. Pasini E.M., Kirkegaard M., Mortensen P., et al. In-depth analysis of the membrane and cytosolic proteome of red blood cells. Blood 2006, 108(3):791-801.
114. Pasini E.M., Kirkegaard M., Salerno D., et al. Deep coverage mouse red blood cell proteome: a first comparison with the human red blood cell. Mol Cell Proteomics 2008, 7(7):1317-1330.
115. Soupene E., Utami Kemaladewi D., Kuypers F.A. ATP8A1 activity and phosphatidylserine transbilayer movement. JReceptor Ligand Channel Res 2008, 1:1-10.
116. Zwaal R.F., Comfurius P., Bevers E.M. Lipid-protein interactions in blood coagulation. Biochim Biophys Acta 1998, 1376(3):433-453.
117. Williamson P., Schlegel R.A. Transbilayer phospholipid movement and the clearance of apoptotic cells. Biochim Biophys Acta 2002, 1585(2-3):53-63.
118. Elliott J.I., Surprenant A., Marelli-Berg F.M., et al. Membrane phosphatidylserine distribution as a non-apoptotic signalling mechanism in lymphocytes. Nat Cell Biol 2005, 7(8):808-816.
119. Fadok V.A., Bratton D.L., Rose D.M., et al. Areceptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 2000, 405(6782):85-90.
120. Fadok V.A., de Cathelineau A., Daleke D.L., et al. Loss of phospholipid asymmetry and surface exposure of phosphatidylserine is required for phagocytosis of apoptotic cells by macrophages and fibroblasts. JBiol Chem 2001, 276(2):1071-1077.
121. Savill J., Fadok V. Corpse clearance defines the meaning of cell death. Nature 2000, 407(6805):784-788.
122. Gaipl U.S., Voll R.E., Sheriff A., et al. Impaired clearance of dying cells in systemic lupus erythematosus. Autoimmun Rev 2005, 4(4):189-194.
123. Kuhtreiber W.M., Hayashi T., Dale E.A., et al. Central role of defective apoptosis in autoimmunity. JMol Endocrinol 2003, 31(3):373-399.
124. Mirnikjoo B., Balasubramanian K., Schroit A.J. Mobilization of lysosomal calcium regulates the externalization of phosphatidylserine during apoptosis. JBiol Chem 2009, 284(11):6918-6923.
125. Kagan V.E., Tyurina Y.Y., Bayir H., et al. The "pro-apoptotic genies" get out of mitochondria: oxidative lipidomics and redox activity of cytochrome c/cardiolipin complexes. Chem Biol Interact 2006, 163(1-2):15-28.
126. Foller M., Huber S.M., Lang F. Erythrocyte programmed cell death. IUBMB Life 2008, 60(10):661-668. 10.1002/iub.106.
127. Kuypers F.A. Membrane lipid alterations in hemoglobinopathies. Hematology AmSoc Hematol Educ Program 2007, 68-73. 10.1182/asheducation-2007.1.68.
128. Dressler V., Schwister K., Haest C.W., et al. Dielectric breakdown of the erythrocyte membrane enhances transbilayer mobility of phospholipids. Biochim Biophys Acta 1983, 732(1):304-307.
129. Haest C.W., Oslender A., Kamp D. Nonmediated flip-flop of anionic phospholipids and long-chain amphiphiles in the erythrocyte membrane depends on membrane potential. Biochemistry 1997, 36(36):10885-10891.
130. Henseleit U., Plasa G., Haest C. Effects of divalent cations on lipid flip-flop in the human erythrocyte membrane. Biochim Biophys Acta 1990, 1029(1):127-135.
131. Shiffer K.A., Rood L., Emerson R.K., et al. The effects of phosphatidylinositol diphosphate on phospholipid asymmetry in the human erythrocyte membrane. Biochemistry 1998, 37(10):3449-3458.
132. 2+-induced loss of phospholipid asymmetry in the human erythrocyte: a study in Scott syndrome, a disorder of calcium-induced phospholipid scrambling. Blood 1995, 86(5):1983-1991.
133. Schwichtenhovel C., Deuticke B., Haest C.W. Alcohols produce reversible and irreversible acceleration of phospholipid flip-flop in the human erythrocyte membrane. Biochim Biophys Acta 1992, 1111(1):35-44.
134. Serra M.V., Kamp D., Haest C.W. Pathways for flip-flop of mono- and di-anionic phospholipids in the erythrocyte membrane. Biochim Biophys Acta 1996, 1282(2):263-273.
135. Vondenhof A., Oslender A., Deuticke B., et al. Band 3, an accidental flippase for anionic phospholipids?. Biochemistry 1994, 33(15):4517-4520.
136. Kleinhorst A., Oslender A., Haest C.W., et al. Band 3-mediated flip-flop and phosphatase-catalyzed cleavage of a long-chain alkyl phosphate anion in the human erythrocyte membrane. JMembr Biol 1998, 165(2):111-124.
137. Axelsen K.B., Palmgren M.G. Inventory of the superfamily of P-type ion pumps in Arabidopsis. Plant Physiol 2001, 126(2):696-706.
138. Franck P.F., Chiu D.T., Op den Kamp J.A., et al. Accelerated transbilayer movement of phosphatidylcholine in sickled erythrocytes. A reversible process. JBiol Chem 1983, 258(13):8436-8442.
139. Lubin B., Chiu D., Bastacky J., et al. Abnormalities in membrane phospholipid organization in sickled erythrocytes. JClin Invest 1981, 67(6):1643-1649.
140. Franck P.F., Bevers E.M., Lubin B.H., et al. Uncoupling of the membrane skeleton from the lipid bilayer. The cause of accelerated phospholipid flip-flop leading to an enhanced procoagulant activity of sickled cells. JClin Invest 1985, 75(1):183-190. 10.1172/JCI111672.
141. de Jong K., Emerson R., Butler H., et al. Short survival of PS exposing red blood cells in murine sickle cell anemia. Blood 2001, 98(5):1577-1584.
142. Kuypers F.A., Lewis R.A., Ernst J.D., et al. Detection of altered membrane phospholipid asymmetry in subpopulations of human red cells using fluorescently labeled annexin V. Blood 1996, 87(3):1179-1187.
143. Kuypers F.A., Yuan J., Lewis R.A., et al. Membrane phospholipid asymmetry in human thalassemia. Blood 1998, 91(8):3044-3051.
144. Setty B.N., Kulkarni S., Stuart M.J. Role of erythrocyte phosphatidylserine in sickle red cell-endothelial adhesion. Blood 2002, 99(5):1564-1571.
145. Lane P.A. The spleen in children. Curr Opin Pediatr 1995, 7(1):36-41.
146. Singer S.T., Kuypers F., Olivieri N., et al. Fetal haemoglobin augmentation in E/b0 thalassaemia: clinical and haematological outcome. Br J Haematol 2005, 131:378-388.
147. Yasin Z., Witting S., Palascak M.B., et al. Phosphatidylserine externalization in sickle red blood cells: associations with cell age, density, and hemoglobin F. Blood 2003, 102(1):365-370. 10.1182/blood-2002-11-3416.
148. Blumenfeld N., Zachowski A., Galacteros F., et al. Transmembrane mobility of phospholipids in sickle erythrocytes: effect of deoxygenation on diffusion and asymmetry. Blood 1991, 77(4):849-854.
149. 2+-CaM activation of AMP deaminase contributes to adenine nucleotide dysregulation and phosphatidylserine externalization in human sickle erythrocytes. Br J Haematol 2009, 144(3):434-445.
150. de Jong K., Larkin S.K., Styles L.A., et al. Characterization of the phosphatidylserine-exposing subpopulation of sickle cells. Blood 2001, 98(3):860-867.
151. Banerjee T., Kuypers F.A. Reactive oxygen species and phosphatidylserine externalization in murine sickle red cells. Br J Haematol 2004, 124(3):391-402.
152. de Jong K., Kuypers F.A. Sulphydryl modifications alter scramblase activity in murine sickle cell disease. Br J Haematol 2006, 133(4):427-432. 10.1111/j.1365-2141.2006.06045.x.
153. De Jong K., Geldwerth D., Kuypers F.A. Oxidative damage does not alter membrane phospholipid asymmetry in human erythrocytes. Biochemistry 1997, 36(22):6768-6776.
154. Geldwerth D., Kuypers F.A., Bütikofer P., et al. Transbilayer mobility and distribution of red cell phospholipids during storage. JClin Invest 1993, 92:308-314.
155. Cappellini M.D. Coagulation in the pathophysiology of hemolytic anemias. Hematology Am Soc Hematol Educ Program 2007, 74-78. 10.1182/asheducation-2007.1.74.
156. Zwaal R.F., Comfurius P., Bevers E.M. Surface exposure of phosphatidylserine in pathological cells. Cell Mol Life Sci 2005, 62(9):971-988.
157. Adedeji M.O., Cespedes J., Allen K., et al. Pulmonary thrombotic arteriopathy in patients with sickle cell disease. Arch Pathol Lab Med 2001, 125(11):1436-1441.
158. Marfaing-Koka A., Boyer-Neumann C., Wolf M., et al. Decreased protein S activity in sickle cell disease. Nouv Rev Fr Hematol 1993, 35(4):425-430.
159. Kuypers F.A., Styles L.A. The role of secretory phospholipase A2 in acute chest syndrome. Cell Mol Biol 2004, 50(1):87-94.
160. Kuypers F.A., Larkin S.K., Emeis J.J., et al. Interaction of an annexin V homodimer (Diannexin) with phosphatidylserine on cell surfaces and consequent antithrombotic activity. Thromb Haemost 2007, 97(3):478-486.
161. Neidlinger N.A., Larkin S.K., Bhagat A., et al. Hydrolysis of phosphatidylserine-exposing red blood cells by secretory phospholipase A2 generates lysophosphatidic acid and results in vascular dysfunction. JBiol Chem 2006, 281(2):775-781.
162. Chadebech P., Habibi A., Nzouakou R., et al. Delayed hemolytic transfusion reaction in sickle cell disease patients: evidence of an emerging syndrome with suicidal red blood cell death. Transfusion 2009, 49(9):1785-1792.
163. Morris C.R., Kuypers F.A., Kato G.J., et al. Hemolysis-associated pulmonary hypertension in thalassemia. Ann N Y Acad Sci 2005, 1054:481-485.
164. Gladwin M.T., Kato G.J. Hemolysis-associated hypercoagulability in sickle cell disease: the plot (and blood) thickens!. Haematologica 2008, 93(1):1-3.
165. Kato G.J., Gladwin M.T., Steinberg M.H. Deconstructing sickle cell disease: reappraisal of the role of hemolysis in the development of clinical subphenotypes. Blood Rev 2007, 21(1):37-47.
166. Bütikofer P., Yee M.C., Schott M.A., et al. Generation of phosphatidic acid during calcium-loading of human erythrocytes-evidence for a phosphatidylcholine-hydrolyzing phospholipase D. Eur J Biochem 1993, 213(1):367-375.
167. van Tits L.J., van Heerde W.L., Landburg P.P., et al. Plasma annexin A5 and microparticle phosphatidylserine levels are elevated in sickle cell disease and increase further during painful crisis. Biochem Biophys Res Commun 2009, 390(1):161-164. 10.1016/j.bbrc.2009.09.102.
168. Rand M.L., Wang H., Pluthero F.G., et al. Diannexin, an annexin A5 homodimer, binds phosphatidylserine with high affinity and is a potent inhibitor of platelet-mediated events during thrombus formation. JThromb Haemost 2012, 10(6):1109-1119. 10.1111/j.1538-7836.2012.04716.x.
169. Hale S.L., Allison A.C., Kloner R.A. Diannexin reduces no-reflow after reperfusion in rabbits with large ischemic myocardial risk zones. Cardiovasc Ther 2011, 29(4):e42-e52. 10.1111/j.1755-5922.2010.00223.x.
170. Wever K.E., Wagener F.A., Frielink C., et al. Diannexin protects against renal ischemia reperfusion injury and targets phosphatidylserines in ischemic tissue. PloS one 2011, 6(8):e24276. 10.1371/journal.pone.0024276.