Targeted inactivation of murine band 3 (AE1) gene produces a hypercoagulable state causing widespread thrombosis in vivo

Blood

Volumn 92, Issue 5, 1998, Pages 1785-1792

  Hassoun, Hani ^a   Wang, Ylng ^a   Vassiliadis, John ^a   Lutchman, Mohini ^a   Palek, Jiri ^a   Aish, Leo ^a   Aish, Irene S ^a   Liu, Shih Chun ^a   Chishti, Athar H ^a,b  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ST ELIZABETH'S MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SUBPOPULATION; CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HISTOPATHOLOGY; HUMAN; HYPERCOAGULABILITY; INTRACARDIAC THROMBOSIS; LIVER NECROSIS; MORTALITY; MOUSE; PRIORITY JOURNAL; VEIN THROMBOSIS;

EID: 0032170547     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood.v92.5.1785.417k17_1785_1792     Document Type: Article

References (60)

1. Tanner MJA: Molecular and cellular biology of the erythrocyte anion exchanger (AE1). Semin Hematol 30:34, 1993
2. Low PS: Structure and function of the cytoplasmic domain of band 3: Center of erythrocyte membrane-peripheral protein interactions. Biochim Biophys Acta 864:145, 1986
3. Lux SE, John KM, Kopito RR, Lodish HF: Cloning and characterization of band 3, the human erythrocyte anion exchange protein (AE1). Proc Natl Acad Sci USA 86:9089, 1989
4. Tanner MJA, Martin PG, High S: The complete amino acid sequence of the human erythrocyte membrane an ion-transport protein deduced from the cDNA. Biochem J 256:703, 1988
5. Jennings ML: Structure and function of the red blood cell anion transport protein. Annu Rev Biophys Chem 18:397, 1989
6. Nakao M, Nakao T, Yamazoe S: Adenosine triphosphate and maintenance of shape of the human red cells. Nature 187:945, 1960
7. Tsai I, Prasanna Murthy SN, Steck TL: Effect of red cell membrane binding on the catalytic activity of glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem 257:1438, 1982
8. Yu J, Steck TL: Associations of band 3, the predominant polypeptide of the human erythrocyte membrane. J Biol Chem 250: 9176, 1975
9. Waugh SM, Walder JA, Low PS: Partial characterization of the copolymerization reaction of erythrocyte membrane band 3 with hemichromes. Biochemistry 26:1777, 1987
10. Kannan R, Labotka R, Low PS: Isolation and characterization of the hemichrome-stabilized membrane protein aggregates from sickle erythrocytes. J Biol Chem 263:13766, 1988
11. McPherson RA, Sawyer WH, Tilley L: Rotational diffusion of the erythrocyte integral membrane protein band 3: Effect of hemichrome binding. Biochemistry 31:512, 1992
12. Bennett V, Stenbuck PJ: The membrane attachment protein for spectrin is associated with band 3 in human erythrocyte membranes. Nature 280:468, 1979
13. Davis L, Lux SE, Bennett V: Mapping the ankyrin-binding site on the human erythrocyte anion exchanger. J Biol Chem 264:9665, 1989
14. Hargreaves WR, Giedd KM, Verkleij A, Branton D: Reassociation of ankyrin with band 3 in erythrocyte membranes and in lipid vesicles. J Biol Chem 255:11965, 1980
15. Thevenin BJM, Low PS: Kinetics and regulation of the ankyrinband 3 interactions of the human red blood cell membrane. T Biot Chem 265:16166, 1990
16. Southgate CD, Chishti AH, Mitchell B, Yi SJ, Palek J: Targeted disruption of the murine erythroid band 3 gene results in spherocytosis and severe hemolytic anemia despite a normal membrane skeleton. Nat Genet 14:227, 1997
17. Peters LL, Shivdasani RA, Liu S, Hanspal M, John KM, Gonzalez JM, Brugnara C, Gwynn B, Mohandas N, Alper SL, Orkin SH, Lux SE: Anion exchanger 1 (Band 3) is required to prevent erythrocyte membrane surface loss but not to form the membrane skeleton. Cell 86:917, 1996
18. Inaba M, Yawata A, Koshino I, Sato K, Takeushi M, Takakuwa Y, Manno S, Yawata Y, Kanzaki A, Sakai J, Ban A, Ono K, Maede Y: Defective anion transport and marked spherocytosis with membrane instability caused by hereditary total deficiency of red cell band 3 in cattle due to a nonsense mutation. J Clin Invest 97:1804, 1996
19. Chiu D, Lubin B, Roelofsen B, VanDeenen LLM: Sickled erythrocytes accelerate clotting in vitro: An effect of abnormal membrane lipid asymmetry. Blood 58:398, 1981
20. Fadok VA, Voelker DR, Campbell PA, Cohen JJ, Bratton DL, Henson PM: Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol 148:2207, 1992
21. Dachary-Prigent J, Freyssinet J, Pasquet J, Carron J, Nurden AT: Annexin V as a probe of aminophospholipid exposure and platelet membrane vesiculation: A flow cytometry study showing a role for free sulfhydryl groups. Blood 81:2554, 1993
22. Koopman G, Reutelingsperger CPM, Kuijten GAM, Keehnen RMJ, Pals ST, VanOers MHU: Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84:1415, 1994
23. Tait JF, Gibson D: Measurement of membrane phospholipid asymmetry in normal and sickle cell erythrocytes by means of annexin V binding, J Lab Clin Med 123:741, 1994
24. Wood BL, Gibson DF, Tait JF: Increased erythrocyte phosphatidylserine exposure in sickle cell disease: Flow-cytometric measurement and clinical associations. Blood 88:1873, 1996
25. Kuypers FA, Lewis RA, Hua M, Schott MA, Discher D, Ernst JD, Lubin BH: Detection of altered membrane phospholipid asymmetry in subpopulations of human red blood cells using fluorescently-labeled annexin V. Blood 87:1179, 1996
26. Vondenhof A, Oslender A, Deuticke B, Haest CWM: Band 3, and accidental flippase for anionic phospholipids? Biochemistry 38:4517, 1994
27. Ortwein R, Oslender-Kohnen A, Deuticke B: Band 3, the anion exchanger of the erythrocyte membrane, is also a flippase. Biochim Biophys Acta 1191:317, 1994
28. Serra MV, Kamp D, Haest CWM: Pathways for flip-flop of mono- and di-anionic phospholipids in the erythrocyte membrane. Biochim Biophys Acta 1282:263, 1996
29. Zwaal RFA, Schroit AJ: Pathophysiologic implications of membrane phospholipid asymmetry in blood cells. Blood 89:1121, 1997
30. Williamson P, Schlegel RA: Back and forth: The regulation and function of transbilayer phospholipid movement in eukaryotic cells (Review). Mol Membr Biol 11:199, 1994
31. Bach R, Gentry R, Nemerson Y: Factor VII binding to tissue factor in reconsituted phospholipid vesicles: Induction of cooperativity by phosphatidylserine. Biochemistry 25:4007, 1986
32. Bach R, Rifkin DB: Expression of tissue factor procoagulant activity: Regulation by cytosolic calcium. Proc Natl Acad Sci USA 87:6995, 1990
33. Rosing J, Tans G, Govers-Riemslag JWP, Zwaal RFA, Hemker HC: The role of phospholipids and factor Va in the prothrombinase complex. J Biol Chem 255:274, 1980
34. Morrot G, Herve P, Zachowski A, Fellmann P, Devaux PF: Aminophospholipid translocase of human erythrocytes: Phospholipid substrate specificity and effect of cholesterol. Biochemistry 28:3456, 1989
35. Connor J, Pak CH, Zwaal RFA, Schroit AJ: Bidirectional transbilayer movement of phospholipid analogs in human red blood cells. Evidence for an ATP-dependent and protein-mediated process. J Biol Chem 267:19412, 1992
36. Beleznay Z, Zachowski A, Devaux PF, Navazo MP, Ott P: ATP-dependent aminophospholipid translocation in erythrocyte vesicles: Stoichiometry of transport. Biochemistry 32:3146, 1993
37. Bitbol M, Devaux PF: Measurement of outward translocation of phospholipids across human erythrocyte membrane. Proc Natl Acad Sci USA 85:6783, 1988
38. Connor J, Gillum K, Schroit AJ: Maintenance of lipid asymmetry in red blood cells and ghosts: Effect of divalent cations and serum albumin on the transbilayer distribution of phosphatidylserine. Biochim Biophys Acta 1025:82, 1990
39. Zwaal RFA, Comfurius P, Bevers EM: Mechanism and function of changes in membrane-phospholipid asymmetry in platelets and erythrocytes. Biochem Soc Trans 21:248, 1993
40. Bevers EM, Comfurius P, Zwaal RFA: Changes in membrane phospholipid distribution during platelet activiation. Biochim Biophys Acta 736:57, 1983
41. Blumenfeld N, Zachowski A, Galacteros F, Beuzard Y, Devaux PF: Transmembrane mobility of phospholipids in sickle erythrocytes: Effect of deoxygenation on diffusion and asymmetry. Blood 77:849, 1991
42. Borenstain-Ben Yashar V, Barenholz Y, Hy-Am E, Rachmilewitz EA, Eldor A: Phosphatidylserine in the outer leaflet of red blood cells from beta-thalassemia patients may explain the chronic hypercoagulable state and thrombotic episodes. Am J Hematol 44:63, 1993
43. Srinivasan PT, Basu J: Altered membrane phospholipid organization and erythrophagocytosis in E beta-thalassemia. Biochim Biophys Acta 1285:65, 1996
44. McEvoy L, Williamson P, Schlegel RA: Membrane phospholipid asymmetry as a determinant of erythrocyte recognition by macrophages. Proc Natl Acad Sci USA 83:3311, 1986
45. Pradhan D, Williamson P, Schlegel RA: Phosphatidylserine vesicles inhibit phagocytosis of erythrocytes with a symmetric transbilayer distribution of phospholipids. Mol Membr Biol 11:181, 1994
46. Allen RM, Austin GA, Chonn A, Lin L, Lee KC: Uptake of liposomes by cultured mouse bone marrow macrophages: Influence of liposome composition and size. Biochim Biophys Acta 1061:56, 1991
47. Schroit AJ, Madsen J, Tanaka Y: In-vivo recogniton and clearance of red blood cells containing phosphatidylserine in their plasma membranes. J Biol Chem 260:5131, 1985
48. Martin SJ, Reutelingsperger CPM, McGahon AJ, Rader JA, VanSchie RCAA, Laface DM, Green DR: Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: Inhibition by overexpression of Bcl-2 and Abl. J Exp Med 182:1545, 1995
49. Comfurius P, Senden JM, Tilly RH, Schroit AJ, Bevers EM, Zwaal RFA: 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. BiochimBiophysActa 1026:153, 1990
50. Sims PJ, Wiedmer T, Esmon CT, Weiss HJ, Shattil SJ: Assembly of the platelet prothrombinase complex is linked to vesiculation of the platelet plasma membrane. Studies in Scott syndrome: An isolated defect in platelet procoagulant activity. J Biol Chem 264:17049, 1989
51. Zwaal RFA, Comfurius R Bevers EM: Platelet procoagulant activity and microvesicle formation. Its putative role in hemoatasis and thrombosis. Biochim Biophys Acta 1180:1, 1992
52. Lucy JA: Loss of phospholipid asymmetry in cell fusion. Biochem Soc Trans 21:280, 1993
53. Song LY, Baldwin JM, O'Reilly R, Lucy JA: Relationships between the surface exposure of acidic phospholipids and cell fusion in erythrocytes subjected to electrical breakdown. Biochim Biophys Acta 1104:1, 1992
54. Schewe M, Muller P, Korte T, Herrmann A: The role of phospholipid asymmetry in calcium-phosphate-induced fusion of human erythrocytes. J Biol Chem 267:5910, 1992
55. Kaysser TM, Wandersee NJ, Bronson RT, Barker JE: Thrombosis and secondary hemochromatosis play major roles in the pathogenesis of jaundiced and spherocytic mice, murine models for hereditary spherocytosis. Blood 90:4610, 1997
56. Hassoun H, Hanada T, Lutchman M, Sahr EK, Palek J, Hanspal M, Chishti AH: Complete deficiency of glycophorin A in red blood cells from mice with targeted inactivation of the band 3 (AE1) gene. Blood 91:2146, 1998
57. Ong RL: 31Pand 19FNMR studies of glycophorin-reconstituted membranes: Preferential interaction of glycophorin with phosphatidylserine. J Membr Biol 78:1, 1984
58. Mendelsohn R, Dluhy RA, Crawford T, Mantsch HH: Interaction of glycophorin with phosphatidylserine: A fourier transform infrared investigation. Biochemistry 23:1498, 1984
59. Armitage IM, Shapiro DL, Furthmayr H, Marchesi VT: 31P Nuclear magnetic resonance evidence of polyphosphoinositide associated with the hydrophobic segment of glycophorin A. Biochemistry 16:1317, 1977
60. Yeagle PL, Kelsey D: Phosphorous nuclear magnetic resonance studies of lipid-protein interactions: Human erythrocyte glycophorin and phospholipids. Biochemistry 28:2210, 1989