Band 3 multiprotein complexes in the red cell membrane; of mice and men

Blood Cells, Molecules, and Diseases

Volumn 45, Issue 1, 2010, Pages 1-8

  van den Akker, Emile ^a,b   Satchwell, Timothy J ^a   Williamson, Rosalind C ^a   Toye, Ashley M ^a  

^a Queens Building 239   (United Kingdom)

^b NHS BLOOD AND TRANSPLANT   (United Kingdom)

Author keywords

Band 3; Erythrocyte; Junctional complex; Macrocomplex

Indexed keywords

ANKYRIN; ANKYRIN 1; CD47 ANTIGEN; CELL PROTEIN; ERYTHROCYTE BAND 3 PROTEIN; ERYTHROCYTE BAND 4.1 PROTEIN; ERYTHROCYTE BAND 4.2 PROTEIN; GLYCOPHORIN A; GLYCOPROTEIN; HERMES ANTIGEN; MULTIPROTEIN COMPLEX; RH PROTEIN; RHAG PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; ERYTHROCYTE MEMBRANE; ERYTHROPOIESIS; HEREDITARY SPHEROCYTOSIS; HUMAN; KNOCKOUT MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; SPECIES DIFFERENCE;

ANIMALS; ANION EXCHANGE PROTEIN 1, ERYTHROCYTE; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; HUMANS; MICE; MULTIPROTEIN COMPLEXES;

MUS;

EID: 77953130023     PISSN: 10799796     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcmd.2010.02.019     Document Type: Article

References (113)

1. Alper S.L., Vandorpe D.H., Peters L.L., Brugnara C. Reduced DIDS-sensitive chloride conductance in Ae1-/- mouse erythrocytes. Blood Cells Mol. Dis. 2008, 41:22-34.
2. Romero M.F., Fulton C.M., Boron W.F. The SLC4 family of HCO 3-transporters. Pflugers Arch. 2004, 447:495-509.
3. Tanner M.J. Band 3 anion exchanger and its involvement in erythrocyte and kidney disorders. Curr. Opin. Hematol. 2002, 9:133-139.
4. Tanner M.J. The structure and function of band 3 (AE1): recent developments (review). Mol. Membr. Biol. 1997, 14:155-165.
5. Alper S.L., Darman R.B., Chernova M.N., Dahl N.K. The AE gene family of Cl/HCO3- exchangers. J. Nephrol. 2002, 15(Suppl 5):S41-S53.
6. Williamson R.C., Toye A.M. Glycophorin A: Band 3 aid. Blood Cells Mol. Dis. 2008, 41:35-43.
7. Zhang D., Kiyatkin A., Bolin J.T., Low P.S. Crystallographic structure and functional interpretation of the cytoplasmic domain of erythrocyte membrane band 3. Blood 2000, 96:2925-2933.
8. Toye A.M., Ghosh S., Young M.T., Jones G.K., Sessions R.B., Ramauge M., Leclerc P., Basu J., Delaunay J., Tanner M.J. Protein-4.2 association with band 3 (AE1, SLCA4) in Xenopus oocytes: effects of three natural protein-4.2 mutations associated with hemolytic anemia. Blood 2005, 105:4088-4095.
9. Anong W.A., Franco T., Chu H., Weis T.L., Devlin E.E., Bodine D.M., An X., Mohandas N., Low P.S. Adducin forms a bridge between the erythrocyte membrane and its cytoskeleton and regulates membrane cohesion. Blood 2009.
10. Low P.S. Structure and function of the cytoplasmic domain of band 3: center of erythrocyte membrane-peripheral protein interactions. Biochim. Biophys. Acta 1986, 864:145-167.
11. Campanella M.E., Chu H., Low P.S. Assembly and regulation of a glycolytic enzyme complex on the human erythrocyte membrane. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:2402-2407.
12. Vince J.W., Reithmeier R.A. Carbonic anhydrase II binds to the carboxyl terminus of human band 3, the erythrocyte C1-/HCO3- exchanger. J. Biol. Chem. 1998, 273:28430-28437.
13. Vince J.W., Reithmeier R.A. Identification of the carbonic anhydrase II binding site in the Cl(-)/HCO(3)(-) anion exchanger AE1. Biochemistry 2000, 39:5527-5533.
14. Groves J.D., Tanner M.J. Glycophorin A facilitates the expression of human band 3-mediated anion transport in Xenopus oocytes. J. Biol. Chem. 1992, 267:22163-22170.
15. Bruce L.J., Beckmann R., Ribeiro M.L., Peters L.L., Chasis J.A., Delaunay J., Mohandas N., Anstee D.J., Tanner M.J. A band 3-based macrocomplex of integral and peripheral proteins in the RBC membrane. Blood 2003, 101:4180-4188.
16. Beckmann R., Smythe J.S., Anstee D.J., Tanner M.J. Coexpression of band 3 mutants and Rh polypeptides: differential effects of band 3 on the expression of the Rh complex containing D polypeptide and the Rh complex containing CcEe polypeptide. Blood 2001, 97:2496-2505.
17. Reithmeier R.A. A membrane metabolon linking carbonic anhydrase with chloride/bicarbonate anion exchangers. Blood Cells Mol. Dis. 2001, 27:85-89.
18. Bruce L.J., Pan R.J., Cope D.L., Uchikawa M., Gunn R.B., Cherry R.J., Tanner M.J. Altered structure and anion transport properties of band 3 (AE1, SLC4A1) in human red cells lacking glycophorin A. J. Biol. Chem. 2004, 279:2414-2420.
19. Steck T.L. Cross-linking the major proteins of the isolated erythrocyte membrane. J. Mol. Biol. 1972, 66:295-305.
20. Jennings M.L., Nicknish J.S. Localization of a site of intermolecular cross-linking in human red blood cell band 3 protein. J. Biol. Chem. 1985, 260:5472-5479.
21. Staros J.V., Kakkad B.P. Cross-linking and chymotryptic digestion of the extracytoplasmic domain of the anion exchange channel in intact human erythrocytes. J. Membr. Biol. 1983, 74:247-254.
22. Wang J., Kimura T., Asada R., Harada S., Yokota S., Kawamoto Y., Fujimura Y., Tsuji T., Ikehara S., Sonoda Y. SCID-repopulating cell activity of human cord blood-derived CD34- cells assured by intra-bone marrow injection. Blood 2003, 101:2924-2931.
23. Che A., Morrison I.E., Pan R., Cherry R.J. Restriction by ankyrin of band 3 rotational mobility in human erythrocyte membranes and reconstituted lipid vesicles. Biochemistry 1997, 36:9588-9595.
24. Michaely P., Bennett V. The ANK repeats of erythrocyte ankyrin form two distinct but cooperative binding sites for the erythrocyte anion exchanger. J. Biol. Chem. 1995, 270:22050-22057.
25. Rybicki A.C., Schwartz R.S., Hustedt E.J., Cobb C.E. Increased rotational mobility and extractability of band 3 from protein 4.2-deficient erythrocyte membranes: evidence of a role for protein 4.2 in strengthening the band 3-cytoskeleton linkage. Blood 1996, 88:2745-2753.
26. Thevenin B.J., Low P.S. Kinetics and regulation of the ankyrin-band 3 interaction of the human red blood cell membrane. J. Biol. Chem. 1990, 265:16166-16172.
27. Casey J.R., Reithmeier R.A. Analysis of the oligomeric state of band 3, the anion transport protein of the human erythrocyte membrane, by size exclusion high performance liquid chromatography. Oligomeric stability and origin of heterogeneity. J. Biol. Chem. 1991, 266:15726-15737.
28. Pinder J.C., Pekrun A., Maggs A.M., Brain A.P., Gratzer W.B. Association state of human red blood cell band 3 and its interaction with ankyrin. Blood 1995, 85:2951-2961.
29. Yi S.J., Liu S.C., Derick L.H., Murray J., Barker J.E., Cho M.R., Palek J., Golan D.E. Red cell membranes of ankyrin-deficient nb/nb mice lack band 3 tetramers but contain normal membrane skeletons. Biochemistry 1997, 36:9596-9604.
30. Schuck P., Schubert D. Band 3-hemoglobin associations. The band 3 tetramer is the oxyhemoglobin binding site. FEBS Lett. 1991, 293:81-84.
31. Huber E., Baumert H.G., Spatz-Kumbel G., Schubert D. Associations between erythrocyte band 3 protein and aldolase in detergent solution. Determining their stoichiometry by analytical ultracentrifugation. Eur. J. Biochem. 1996, 242:293-300.
32. Cartron J.P. RH blood group system and molecular basis of Rh-deficiency. Baillieres Best Pract. Res. Clin. Haematol. 1999, 12:655-689.
33. Beckmann R., Smythe J.S., Anstee D.J., Tanner M.J. Functional cell surface expression of band 3, the human red blood cell anion exchange protein (AE1), in K562 erythroleukemia cells: band 3 enhances the cell surface reactivity of Rh antigens. Blood 1998, 92:4428-4438.
34. Toye A.M., Williamson R.C., Khanfar M., Bader-Meunier B., Cynober T., Thibault M., Tchernia G., Dechaux M., Delaunay J., Bruce L.J. Band 3 Courcouronnes (Ser667Phe): a trafficking mutant differentially rescued by wild-type band 3 and glycophorin A. Blood 2008, 111:5380-5389.
35. Liu S.C., Palek J., Yi S.J., Nichols P.E., Derick L.H., Chiou S.S., Amato D., Corbett J.D., Cho M.R., Golan D.E. Molecular basis of altered red blood cell membrane properties in Southeast Asian ovalocytosis: role of the mutant band 3 protein in band 3 oligomerization and retention by the membrane skeleton. Blood 1995, 86:349-358.
36. Schofield A.E., Reardon D.M., Tanner M.J. Defective anion transport activity of the abnormal band 3 in hereditary ovalocytic red blood cells. Nature 1992, 355:836-838.
37. Salomao M., Zhang X., Yang Y., Lee S., Hartwig J.H., Chasis J.A., Mohandas N., An X. Protein 4.1R-dependent multiprotein complex: new insights into the structural organization of the red blood cell membrane. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:8026-8031.
38. Korsgren C., Peters L.L., Lux S.E. Protein 4.2 binds to the carboxyterminal EF-hands of erythroid alpha spectrin in a calcium and calmodulin dependent manner. J. Biol. Chem. 2010, 285(7):4757-4770.
39. Eber S., Lux S.E. Hereditary spherocytosis-defects in proteins that connect the membrane skeleton to the lipid bilayer. Semin. Hematol. 2004, 41:118-141.
40. An X., Mohandas N. Disorders of red cell membrane. Br. J. Haematol. 2008, 141:367-375.
41. Gallagher P.G. Red cell membrane disorders. Hematology Am. Soc. Hematol. Educ. Program 2005, 13-18.
42. Perrotta S., Gallagher P.G., Mohandas N. Hereditary spherocytosis. Lancet 2008, 372:1411-1426.
43. Delaunay J. The molecular basis of hereditary red cell membrane disorders. Blood Rev. 2007, 21:1-20.
44. Gallagher P.G. Hereditary elliptocytosis: spectrin and protein 4.1R. Semin. Hematol. 2004, 41:142-164.
45. Nigg E.A., Bron C., Girardet M., Cherry R.J. Band 3-glycophorin A association in erythrocyte membrane demonstrated by combining protein diffusion measurements with antibody-induced cross-linking. Biochemistry 1980, 19:1887-1893.
46. Che A., Cherry R.J. Loss of rotational mobility of band 3 proteins in human erythrocyte membranes induced by antibodies to glycophorin A. Biophys. J. 1995, 68:1881-1887.
47. Knowles D.W., Chasis J.A., Evans E.A., Mohandas N. Cooperative action between band 3 and glycophorin A in human erythrocytes: immobilization of band 3 induced by antibodies to glycophorin A. Biophys. J. 1994, 66:1726-1732.
48. Telen M.J., Chasis J.A. Relationship of the human erythrocyte Wrb antigen to an interaction between glycophorin A and band 3. Blood 1990, 76:842-848.
49. Young M.T., Tanner M.J. Distinct regions of human glycophorin A enhance human red cell anion exchanger (band 3; AE1) transport function and surface trafficking. J. Biol. Chem. 2003, 278:32954-32961.
50. Young M.T., Beckmann R., Toye A.M., Tanner M.J. Red-cell glycophorin A-band 3 interactions associated with the movement of band 3 to the cell surface. Biochem. J. 2000, 350(Pt 1):53-60.
51. Groves J.D., Tanner M.J. The effects of glycophorin A on the expression of the human red cell anion transporter (band 3) in Xenopus oocytes. J. Membr. Biol. 1994, 140:81-88.
52. Gahmberg C.G., Myllyla G., Leikola J., Pirkola A., Nordling S. Absence of the major sialoglycoprotein in the membrane of human En(a-) erythrocytes and increased glycosylation of band 3. J. Biol. Chem. 1976, 251:6108-6116.
53. Auffray I., Marfatia S., de Jong K., Lee G., Huang C.H., Paszty C., Tanner M.J., Mohandas N., Chasis J.A. Glycophorin A dimerization and band 3 interaction during erythroid membrane biogenesis: in vivo studies in human glycophorin A transgenic mice. Blood 2001, 97:2872-2878.
54. Karnchanaphanurach P., Mirchev R., Ghiran I., Asara J.M., Papahadjopoulos-Sternberg B., Nicholson-Weller A., Golan D.E. C3b deposition on human erythrocytes induces the formation of a membrane skeleton-linked protein complex. J. Clin. Invest. 2009, 119:788-801.
55. Hassoun H., Hanada T., Lutchman M., Sahr K.E., Palek J., Hanspal M., Chishti A.H. Complete deficiency of glycophorin A in red blood cells from mice with targeted inactivation of the band 3 (AE1) gene. Blood 1998, 91:2146-2151.
56. Beckmann R., Toye A.M., Smythe J.S., Anstee D.J., Tanner M.J. An N-terminal GFP tag does not alter the functional expression to the plasma membrane of red cell and kidney anion exchanger (AE1) in mammalian cells. Mol. Membr. Biol. 2002, 19:187-200.
57. Peters L.L., Lux S.E. Ankyrins: structure and function in normal cells and hereditary spherocytes. Semin. Hematol. 1993, 30:85-118.
58. Kennedy S.P., Warren S.L., Forget B.G., Morrow J.S. Ankyrin binds to the 15th repetitive unit of erythroid and nonerythroid beta-spectrin. J. Cell Biol. 1991, 115:267-277.
59. Platt O.S., Lux S.E., Falcone J.F. A highly conserved region of human erythrocyte ankyrin contains the capacity to bind spectrin. J. Biol. Chem. 1993, 268:24421-24426.
60. Peters L.L., Shivdasani R.A., Liu S.C., Hanspal M., John K.M., Gonzalez J.M., Brugnara C., Gwynn B., Mohandas N., Alper S.L., Orkin S.H., Lux S.E. Anion exchanger 1 (band 3) is required to prevent erythrocyte membrane surface loss but not to form the membrane skeleton. Cell 1996, 86:917-927.
61. Liu S.C., Derick L.H., Zhai S., Palek J. Uncoupling of the spectrin-based skeleton from the lipid bilayer in sickled red cells. Science 1991, 252:574-576.
62. Korsgren C., Lawler J., Lambert S., Speicher D., Cohen C.M. Complete amino acid sequence and homologies of human erythrocyte membrane protein band 4.2. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:613-617.
63. Satchwell T.J., Shoemark D.K., Sessions R.B., Toye A.M. Protein 4.2: a complex linker. Blood Cells Mol. Dis. 2009, 42(3):201-210.
64. Korsgren C., Cohen C.M. Purification and properties of human erythrocyte band 4.2. Association with the cytoplasmic domain of band 3. J. Biol. Chem. 1986, 261:5536-5543.
65. Korsgren C., Cohen C.M. Associations of human erythrocyte band 4.2. Binding to ankyrin and to the cytoplasmic domain of band 3. J. Biol. Chem. 1988, 263:10212-10218.
66. Rank G., Sutton R., Marshall V., Lundie R.J., Caddy J., Romeo T., Fernandez K., McCormack M.P., Cooke B.M., Foote S.J., Crabb B.S., Curtis D.J., Hilton D.J., Kile B.T., Jane S.M. Novel roles for erythroid ankyrin-1 revealed through an ENU-induced null mouse mutant. Blood 2009.
67. Wada H., Kanzaki A., Yawata A., Inoue T., Kaku M., Takezono M., Sugihara T., Yamada O., Yawata Y. Late expression of red cell membrane protein 4.2 in normal human erythroid maturation with seven isoforms of the protein 4.2 gene. Exp. Hematol. 1999, 27:54-62.
68. Chen K., Liu J., Heck S., Chasis J.A., An X., Mohandas N. Resolving the distinct stages in erythroid differentiation based on dynamic changes in membrane protein expression during erythropoiesis. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:17413-17418.
69. Golan D.E., Corbett J.D., Korsgren C., Thatte H.S., Hayette S., Yawata Y., Cohen C.M. Control of band 3 lateral and rotational mobility by band 4.2 in intact erythrocytes: release of band 3 oligomers from low-affinity binding sites. Biophys. J. 1996, 70:1534-1542.
70. Rybicki A.C., Heath R., Wolf J.L., Lubin B., Schwartz R.S. Deficiency of protein 4.2 in erythrocytes from a patient with a Coombs negative hemolytic anemia. Evidence for a role of protein 4.2 in stabilizing ankyrin on the membrane. J. Clin. Invest. 1988, 81:893-901.
71. Bouhassira E.E., Schwartz R.S., Yawata Y., Ata K., Kanzaki A., Qiu J.J., Nagel R.L., Rybicki A.C. An alanine-to-threonine substitution in protein 4.2 cDNA is associated with a Japanese form of hereditary hemolytic anemia (protein 4.2NIPPON). Blood 1992, 79:1846-1854.
72. Kanzaki A., Yasunaga M., Okamoto N., Inoue T., Yawata A., Wada H., Andoh A., Hodohara K., Fujiyama Y., Bamba T., et al. Band 4.2 Shiga: 317 CGC→TGC in compound heterozygotes with 142 GCT→ACT results in band 4.2 deficiency and microspherocytosis. Br. J. Haematol. 1995, 91:333-340.
73. Takaoka Y., Ideguchi H., Matsuda M., Sakamoto N., Takeuchi T., Fukumaki Y. A novel mutation in the erythrocyte protein 4.2 gene of Japanese patients with hereditary spherocytosis (protein 4.2 Fukuoka). Br. J. Haematol. 1994, 88:527-533.
74. Matsuda M., Hatano N., Ideguchi H., Takahira H., Fukumaki Y. A novel mutation causing an aberrant splicing in the protein 4.2 gene associated with hereditary spherocytosis (protein 4.2Notame). Hum. Mol. Genet. 1995, 4:1187-1191.
75. Hayette S., Morle L., Bozon M., Ghanem A., Risinger M., Korsgren C., Tanner M.J., Fattoum S., Cohen C.M., Delaunay J. A point mutation in the protein 4.2 gene (allele 4.2 Tozeur) associated with hereditary haemolytic anaemia. Br. J. Haematol. 1995, 89:762-770.
76. Beauchamp-Nicoud A., Morle L., Lutz H.U., Stammler P., Agulles O., Petermann-Khder R., Iolascon A., Perrotta S., Cynober T., Tchernia G., Delaunay J., Baudin-Creuza V. Heavy transfusions and presence of an anti-protein 4.2 antibody in 4.2(-) hereditary spherocytosis (949delG). Haematologica 2000, 85:19-24.
77. Bruce L.J., Ghosh S., King M.J., Layton D.M., Mawby W.J., Stewart G.W., Oldenborg P.A., Delaunay J., Tanner M.J. Absence of CD47 in protein 4.2-deficient hereditary spherocytosis in man: an interaction between the Rh complex and the band 3 complex. Blood 2002, 100:1878-1885.
78. Mouro-Chanteloup I., Delaunay J., Gane P., Nicolas V., Johansen M., Brown E.J., Peters L.L., Van Kim C.L., Cartron J.P., Colin Y. Evidence that the red cell skeleton protein 4.2 interacts with the Rh membrane complex member CD47. Blood 2003, 101:338-344.
79. Subramanian S., Tsai R., Sen S., Dahl K.N., Discher D.E. Membrane mobility and clustering of integrin associated protein (IAP, CD47)-major differences between mouse and man and implications for signaling. Blood Cells Mol. Dis. 2006, 36:364-372.
80. Oldenborg P.A., Zheleznyak A., Fang Y.F., Lagenaur C.F., Gresham H.D., Lindberg F.P. Role of CD47 as a marker of self on red blood cells. Science 2000, 288:2051-2054.
81. Khandelwal S., van Rooijen N., Saxena R.K. Reduced expression of CD47 during murine red blood cell (RBC) senescence and its role in RBC clearance from the circulation. Transfusion 2007, 47:1725-1732.
82. Krettek A., Sjoberg S. CD44-a new cardiovascular drug target or merely an innocent bystander?. Cardiovasc. Hematol. Disord. Drug Targets 2009, 9:293-302.
83. Nunomura W., Takakuwa Y., Tokimitsu R., Krauss S.W., Kawashima M., Mohandas N. Regulation of CD44-protein 4.1 interaction by Ca2+ and calmodulin. Implications for modulation of CD44-ankyrin interaction. J. Biol. Chem. 1997, 272:30322-30328.
84. Huang C.H., Ye M. The Rh protein family: gene evolution, membrane biology, and disease association. Cell. Mol. Life Sci. 2009.
85. Marini A.M., Urrestarazu A., Beauwens R., Andre B. The Rh (rhesus) blood group polypeptides are related to NH4+ transporters. Trends Biochem. Sci. 1997, 22:460-461.
86. Ripoche P., Bertrand O., Gane P., Birkenmeier C., Colin Y., Cartron J.P. Human Rhesus-associated glycoprotein mediates facilitated transport of NH(3) into red blood cells. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:17222-17227.
87. Hemker M.B., Cheroutre G., van Zwieten R., Maaskant-van Wijk P.A., Roos D., Loos J.A., van der Schoot C.E., von dem Borne A.E. The Rh complex exports ammonium from human red blood cells. Br. J. Haematol. 2003, 122:333-340.
88. Benjelloun F., Bakouh N., Fritsch J., Hulin P., Lipecka J., Edelman A., Planelles G., Thomas S.R., Cherif-Zahar B. Expression of the human erythroid Rh glycoprotein (RhAG) enhances both NH3 and NH4+ transport in HeLa cells. Pflugers Arch. 2005, 450:155-167.
89. Ripoche P., Goossens D., Devuyst O., Gane P., Colin Y., Verkman A.S., Cartron J.P. Role of RhAG and AQP1 in NH3 and CO2 gas transport in red cell ghosts: a stopped-flow analysis. Transfus. Clin. Biol. 2006, 13:117-122.
90. Kustu S., Inwood W. Biological gas channels for NH3 and CO2: evidence that Rh (Rhesus) proteins are CO2 channels. Transfus. Clin. Biol. 2006, 13:103-110.
91. Endeward V., Cartron J.P., Ripoche P., Gros G. RhAG protein of the Rhesus complex is a CO2 channel in the human red cell membrane. FASEB J. 2008, 22:64-73.
92. Bruce L.J., Guizouarn H., Burton N.M., Gabillat N., Poole J., Flatt J.F., Brady R.L., Borgese F., Delaunay J., Stewart G.W. The monovalent cation leak in overhydrated stomatocytic red blood cells results from amino acid substitutions in the Rh-associated glycoprotein. Blood 2009, 113:1350-1357.
93. Brown A.C., Hallouane D., Mawby W.J., Karet F.E., Saleem M.A., Howie A.J., Toye A.M. RhCG is the major putative ammonia transporter expressed in the human kidney, and RhBG is not expressed at detectable levels. Am. J. Physiol. Renal. Physiol. 2009, 296:F1279-F1290.
94. Ridgwell K., Eyers S.A., Mawby W.J., Anstee D.J., Tanner M.J. Studies on the glycoprotein associated with Rh (Rhesus) blood group antigen expression in the human red blood cell membrane. J. Biol. Chem. 1994, 269:6410-6416.
95. Dahr W., Kordowicz M., Moulds J., Gielen W., Lebeck L., Kruger J. Characterization of the Ss sialoglycoprotein and its antigens in Rhnull erythrocytes. Blut 1987, 54:13-24.
96. Callebaut I., Dulin F., Bertrand O., Ripoche P., Mouro I., Colin Y., Mornon J.P., Cartron J.P. Hydrophobic cluster analysis and modeling of the human Rh protein three-dimensional structures. Transfus. Clin. Biol. 2006, 13:70-84.
97. Goossens D., Trinh-Trang-Tan M.M., Debbia M., Ripoche P., Vilela-Lamego C., Louache F., Vainchenker W., Colin Y., Cartron J.P. Generation and characterisation of Rhd and Rhag null mice. Br. J. Haematol. 2009.
98. Ballas S.K., Clark M.R., Mohandas N., Colfer H.F., Caswell M.S., Bergren M.O., Perkins H.A., Shohet S.B. Red cell membrane and cation deficiency in Rh null syndrome. Blood 1984, 63:1046-1055.
99. Nicolas V., Le Van Kim C., Gane P., Birkenmeier C., Cartron J.P., Colin Y., Mouro-Chanteloup I. Rh-RhAG/ankyrin-R, a new interaction site between the membrane bilayer and the red cell skeleton, is impaired by Rh(null)-associated mutation. J. Biol. Chem. 2003, 278:25526-25533.
100. Nicolas V., Mouro-Chanteloup I., Lopez C., Gane P., Gimm A., Mohandas N., Cartron J.P., Le Van Kim C., Colin Y. Functional interaction between Rh proteins and the spectrin-based skeleton in erythroid and epithelial cells. Transfus. Clin. Biol. 2006, 13:23-28.
101. Zhu D., Bourguignon L.Y. Interaction between CD44 and the repeat domain of ankyrin promotes hyaluronic acid-mediated ovarian tumor cell migration. J. Cell Physiol. 2000, 183:182-195.
102. R.F. Robledo, A.J. Lambert, C.S. Birkenmeier, M.V. Cirlan, A.F. Cirlan, D.R. Campagna, S.E. Lux, and L.L. Peters, Analysis of novel sph (spherocytosis) alleles in mice reveals allele-specific loss of band 3 and adducin in {alpha}-spectrin deficient red cells. Blood. 115 (9) (2010) 1804-1814.
103. Wichterle H., Hanspal M., Palek J., Jarolim P. Combination of two mutant alpha spectrin alleles underlies a severe spherocytic hemolytic anemia. J. Clin. Invest. 1996, 98:2300-2307.
104. Jons T., Drenckhahn D. Identification of the binding interface involved in linkage of cytoskeletal protein 4.1 to the erythrocyte anion exchanger. Embo J. 1992, 11:2863-2867.
105. Robledo R.F., Ciciotte S.L., Gwynn B., Sahr K.E., Gilligan D.M., Mohandas N., Peters L.L. Targeted deletion of alpha-adducin results in absent beta- and gamma-adducin, compensated hemolytic anemia, and lethal hydrocephalus in mice. Blood 2008, 112:4298-4307.
106. Southcott M.J., Tanner M.J., Anstee D.J. The expression of human blood group antigens during erythropoiesis in a cell culture system. Blood 1999, 93:4425-4435.
107. Bony V., Gane P., Bailly P., Cartron J.P. Time-course expression of polypeptides carrying blood group antigens during human erythroid differentiation. Br. J. Haematol. 1999, 107:263-274.
108. Chang H., Langer P.J., Lodish H.F. Asynchronous synthesis of erythrocyte membrane proteins. Proc. Natl. Acad. Sci. U.S.A. 1976, 73:3206-3210.
109. Woods C.M., Boyer B., Vogt P.K., Lazarides E. Control of erythroid differentiation: asynchronous expression of the anion transporter and the peripheral components of the membrane skeleton in AEV- and S13-transformed cells. J. Cell Biol. 1986, 103:1789-1798.
110. Hanspal M., Golan D.E., Smockova Y., Yi S.J., Cho M.R., Liu S.C., Palek J. Temporal synthesis of band 3 oligomers during terminal maturation of mouse erythroblasts. Dimers and tetramers exist in the membrane as preformed stable species. Blood 1998, 92:329-338.
111. Leberbauer C., Boulme F., Unfried G., Huber J., Beug H., Mullner E.W. Different steroids co-regulate long-term expansion versus terminal differentiation in primary human erythroid progenitors. Blood 2005, 105:85-94.
112. von Lindern M., Zauner W., Mellitzer G., Steinlein P., Fritsch G., Huber K., Lowenberg B., Beug H. The glucocorticoid receptor cooperates with the erythropoietin receptor and c-Kit to enhance and sustain proliferation of erythroid progenitors in vitro. Blood 1999, 94:550-559.
113. A.E. vondem Borne, M.J. Bos, C. Lomas, P. Tippett, C. Bloy, P. Hermand, L.G. Admiraal, J. van de Graaf, M.A. Overbeeke, Murine monoclonal antibodies against a unique determinant of erythrocytes, related to Rh and U antigens: expression on normal and malignant erythrocyte precursors and Rhnull red cells, Br. J. Haematol. 75 (2), 254-261.