Naturally occurring anti-band 3 antibodies in clearance of senescent and oxidatively stressed human red blood cells

Transfusion Medicine and Hemotherapy

Volumn 39, Issue 5, 2012, Pages 321-327

  Lutz, Hans U ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Anion transport protein; Band 3; Complement C3b deposition; Naturally occurring antibody; Opsonization

Indexed keywords

ANTIBODY; ERYTHROCYTE BAND 3 PROTEIN; ERYTHROCYTE BAND 3 PROTEIN ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; LACTOFERRIN; PROTEIN KINASE SYK; UNCLASSIFIED DRUG;

ANTIGEN BINDING; BINDING AFFINITY; CELL AGING; CELL STRESS; ERYTHROCYTE; HUMAN; OXIDATIVE STRESS; PLASMA; PROTEIN BINDING; PROTEIN FUNCTION; REVIEW; SENESCENCE;

EID: 84867023102     PISSN: 16603796     EISSN: 16603818     Source Type: Journal    
DOI: 10.1159/000342171     Document Type: Review

References (87)

1. Lutz HU: Elimination of old erythrocytes from the circulation: Exposure of a cell-age specific antigen on aging erythrocytes (in German). Schweiz Med Wochenschr 1981; 111:1507-1517.
2. Luner SJ Szklarek D, Knox RJ, Seaman GVF, Josefowicz JY, Ware BR: Red cell charge is not a function of cell age. Nature 1977;269:719-721.
3. Lutz HU, Fehr J: Total sialic acid content of glycophorins during senescence of human red blood cells. J Biol Chem 1979;254:11177-11180.
4. Kay MMB: Mechanism of removal of senescent cells by human macrophages in situ. Proc Natl Acad Sci USA 1975;72:3521-3525.
5. Lutz HU, Wipf G: Naturally occurring autoantibodies to skeletal proteins from human red blood cells. J Immunol 1982;128:1695-1699.
6. Kay MMB: Isolation of the phagocytosis-inducing IgG-binding antigen on senescent somatic cells. Nature 1981;289:491-494.
7. Lutz HU, Liu S-C, Palek J: Release of spectrin-free vesicles from human erythrocytes during ATP depletion. J Cell Biol 1977;73:548-560.
8. Mueller H, Lutz HU: Binding of autologous IgG to human red blood cells before and after ATP-depletion. Selective exposure of binding sites (autoantigens) on spectrin-free vesicles. Biochim Biophys Acta 1983;729:249-257.
9. Nigg E, Cherry RJ: Dimeric association of band 3 in the erythrocyte membrane demonstrated by protein diffusion measurements. Nature 1979 277:493-494.
10. Staros JV, Morgan DG, Appling DR: A membrane-impermeant, cleavable cross-linker. J Biol Chem 1981;256:5890-5893.
11. Schweizer E, Angst W, Lutz HU: Glycoprotein topology on intact human red blood cells reevaluated by cross-linking following amino-group supplementation. Biochemistry 1982;21:6807-6818.
12. Lutz HU: A cell-age specific antigen on senescent human red blood cells. Acta Biol Med Ger 1981;40: 393-400.
13. Beutler E, West C, Blume K-G: The removal of leukocytes and platelets from whole blood. J Lab Clin Med 1976;88:328-333.
14. Pappert G, Schubert D: The state of association of band 3 protein of the human erythrocyte membrane in solutions of nonionic detergents. Biochim Biophys Acta 1983;730:32-40.
15. Lutz HU, Stringaro-Wipf G: Senescent red cellbound IgG is attached to band 3 protein. Biomed Biochim Acta 1983;42:117-121.
16. Lutz HU, Flepp R, Stringaro-Wipf G: Naturally occurring autoantibodies to exoplasmic and cryptic regions of band 3 protein, the major integral membrane protein of human red blood cells. J Immunol 1984;133:2610-2618.
17. Bussolino F, Turrini F, Arese P: Measurement of phagocytosis utilizing 14C-cyanate-labelled human red cells and monocytes. Br J Haematol 1987;66: 271-274.
18. Lutz HU, Bussolino F, Flepp R, Fasler S, Stammler P, Kazatchkine MD, Arese P: Naturally occurring anti-band 3 antibodies and complement together mediate phagocytosis of oxidatively stressed human red blood cells. Proc Natl Acad Sci USA 1987;84:7368-7372.
19. Giger U, Sticher B, Naef R, Burger R, Lutz HU: Naturally occurring human anti-band 3 autoantibodies accelerate clearance of erythrocytes in guinea pigs. Blood 1995;85:1920-1928.
20. Beppu M, Mizukami A, Ando K, Kikugawa K: Antigenic determinants of senescent antigen of human erythrocytes are located in sialylated carbohydrate chains of band-3 glycoprotein. J Biol Chem 1992;267:14691-14696.
21. Lutz HU, Gianora O, Nater M, Schweizer E, Stammler P: Naturally occurring anti-band 3 antibodies bind to protein rather than to carbohydrate on band 3. J Biol Chem 1993;268:23562-23566.
22. Beppu M, Mizukami A, Nagoya M, Kikugawa K: Binding of anti-band 3 autoantibody to oxidatively damaged erythrocytes. J Biol Chem 1990;265:3226-3233
23. Ando K, Kikugawa K, Beppu M: Binding of antiband autoantibody to sialylated poly-N-acetyllactosaminyl sugar chains of band 3 glycoprotein on polyvinylidene difluoride membrane and sepharose gel: Further evidence for anti-band 3 autoantibody binding to the sugar chains of oxidized and senescent erythrocytes. J Biochem 1996 119:639-647.
24. Ando K, Kikugawa K, Beppu M: Involvement of sialylated poly-N-acetyllactosaminyl sugar chains of band 3 glycoprotein on senescent erythrocytes in anti-band 3 autoantibody binding. J Biol Chem 1994;269:19394-19398.
25. Chikazawa H, Nishiya K, Matsumori A, Hashimoto K: Immunoglobulin isotypes of anti-myeloperoxidase and anti-lactoferrin antibodies in patients with collagen diseases. J Clin Immunol 2000;20:279-286.
26. Roozendaal C, Pogany K, Horst G, Jagt TG, Kleibeuker JH, Nelis GF, Limburg PC, Kallenberg CGM: Does analysis of the antigenic specificities of anti-neutrophil cytoplasmic antibodies contribute to their clinical significance in the inflammatory bowel diseases? Scand J Gastroenterol 1999;34: 1123-1131.
27. Peen E, Almer S, Bodemar G, Ryden BO, Sjolin C, Tejle K, Skogh T: Antilactoferrin antibodies and other types of ANCA in ulcerative colitis, primary sclerosing cholangitis, and crohns disease. Gut 1993;34:56-62.
28. Esnault VL, Short AK, Audrain MA, Jones SJ, Martin SJ, Skehel JM, Lockwood CM: Autoantibodies to lactoferrin and histone in systemic vasculitis identified by anti-myeloperoxidase solid phase assays. Kidney Int 1994;46:153-160.
29. Brimnes J, Halberg P, Jacobsen S, Wiik A, Heegaard NHH: Specificities of anti-neutrophil autoantibodies in patients with rheumatoid arthritis (RA). Clin Exp Immunol1997;110:250-256.
30. Nsberger L, Hultquist R, Sturfelt G: Occurrence of anti-lactoferrin antibodies in patients with systemic lupus erythematosus, hydralazine-induced lupus, and rheumatoid arthritis. Scand J Rheumatol 1994;23:206-210.
31. Caccavo D, Rigon A, Picardi A, Galluzzo S, Vadacca M, Ferri GM, Amoroso A, Afeltra A: Anti-lactoferrin antibodies in systemic lupus erythematosus: Isotypes and clinical correlates. Clin Rheumatol 2005;24:381-387.
32. Manolova I, Dancheva M, Halacheva K: Predominance of IgG1 and IgG3 subclasses of autoantibodies to neutrophil cytoplasmic antigens in patients with systemic lupus erythematosus. Rheumatol Int 2002;21:227-233.
33. Nappi C, Tommaselli GA, Morra I, Massaro M, Formisano C, Di Carlo C: Efficacy and tolerability of oral bovine lactoferrin compared to ferrous sulfate in pregnant women with iron deficiency anemia: a prospective controlled randomized study. Acta Obstet Gynecol Scand 2009;88:1031-1035.
34. Malaise MG, Hoyoux C, Franchimont P, Foidart JB, Mahieu PR: Effects of mannose and mannose derivatives on the clearance of IgG antibodycoated erythrocytes in the rat. Immunology 1989; 68:126-132.
35. Hernell O, Lonnerdal B: Iron status of infants fed low-iron formula: No effect of added bovine lactoferrin or nucleotides. Am J Clin Nutr 2002;76:858-864.
36. Rodman TC, Winston R, Sullivan JJ, Yan XJ, Chiorazzi N: An innate natural antibody is reactive with a cryptic sequence of lactoferrin exposed on sperm head surface. Proc Soc Exp Biol Med 1997; 216:404-409.
37. Troost FJ, Steijns J, Saris WH, Brummer RJ: Gastric digestion of bovine lactoferrin in vivo in adults. J Nutr 2001;131:2101-2104.
38. Victoria EJ, Mahan LC, Masouredis SP: The IgG binding function of the normal red cell plasma membrane: Identification of integral polypeptides that bind IgG. Br J Haematol 1982;50:101-110.
39. Turrini F, Arese P, Yuan J, Low PS: Clustering of integral membrane proteins of the human erythrocyte membrane stimulates autologous IgG binding, complement deposition, and phagocytosis. J Biol Chem 1991;266:23611-23617.
40. Rettig MP, Low PS, Gimm JA, Mohandas N, Wang JZ, Christian JA: Evaluation of biochemical changes during in vivo erythrocyte senescence in the dog. Blood 1999;93:376-384.
41. Pantaleo A, Giribaldi G, Mannu F, Arese P, Turrini F: Naturally occurring anti-band 3 antibodies and red blood cell removal under physiological and pathological conditions. Autoimmun Rev 2008;7:457-462.
42. Kannan R, Labotka R, Low PS: Isolation and characterization of the hemichrome-stabilized membrane protein aggregates from sickle erythrocytes. J Biol Chem 1988;263:13766-13773.
43. Waugh SM, Low PS: Hemichrome binding to band 3: Nucleation of Heinz bodies on the erythrocyte membrane. Biochemistry 1985;24:34-39.
44. Mannu F, Arese P, Cappellini MD, Fiorelli G, Cappadoro M, Giribaldi G, Turrini F: Role of hemichrome binding to erythrocyte membrane in the generation of band-3 alterations in beta-thalassemia intermedia erythrocytes. Blood 1995;86:2014-2020.
45. Turrini F, Giribaldi G, Carta F, Mannu F, Arese P: Mechanisms of band 3 oxidation and clustering in the phagocytosis of Plasmodium falciparum-infected erythrocytes. Redox Rep 2003;8:300-303.
46. Schler 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 USA 1986; 83:6137-6141.
47. Turrini F, Mannu F, Arese P, Yuan J, Low PS: Characterization of the autologous antibodies that opsonize erythrocytes with clustered integral membrane proteins. Blood 1993;81:3146-3152.
48. Casey JR, Reithmeier RAF: 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.
49. Willardson BM, Thevenin BJ, Harrison ML, Kuster WM, Benson MD, Low PS: Localization of the ankyrin-binding site on erythrocyte membrane protein, band-3. J Biol Chem 1989;264:15893-15899.
50. Pantaleo A, Ferru E, Giribaldi G, Mannu F, Carta F, Matte A, de Franceschi L, Turrini F: Oxidized and poorly glycosylated band 3 is selectively phosphorylated by Syk kinase to form large membrane clusters in normal and G6PD-deficient red blood cells. Biochem J 2009;418:359-367.
51. Harrison ML, Isaacson CC, Burg DL, Geahlen RL, Low PS: Phosphorylation of human erythrocyte band-3 by endogenous p72(syk). J Biol Chem 1994; 269:955-959.
52. Bordin L, Ion-Popa F, Brunati AM, Clari G, Low PS: Effector-induced Syk-mediated phosphorylation in human erythrocytes. Biochim Biophys Acta 2005;1745:20-28.
53. Ferru E, Giger K, Pantaleo A, Campanella E, Grey J, Ritchie K, Vono R, Turrini F, Low PS: Regulation of membrane-cytoskeletal interactions by tyrosine phosphorylation of erythrocyte band 3. Blood 2011;117:5998-6006.
54. Turrini F, Mannu F, Cappadoro M, Ulliers D, Giribaldi G, Arese P: Binding of naturally occurring antibodies to oxidatively and nonoxidatively modified erythrocyte band 3. Biochim Biophys Acta 1994;1190:297-303.
55. Fukuda MN, Masri KA, Dell A, Luzzatto L, Moremen KW: Incomplete synthesis of N-glycans in congenital dyserythropoietic anemia type-II caused by a defect in the gene encoding alpha-mannosidase-II. Proc Natl Acad Sci USA 1990;87:7443-7447.
56. Defranceschi L, Turrini F, Delgiudice EM, Perrotta S, Olivieri O, Corrocher R, Mannu F, Iolascon A: Decreased band 3 anion transport activity and band 3 clusterization in congenital dyserythropoietic anemia type II. Exp Hematol 1998; 26: 869-873.
57. Szymanski IO, Odgren PR, Fortier N, Snyder LM: Red blood cell associated IgG in normal and pathologic states. Blood 1980;55:48-54.
58. Muller H, Lutz HU: Binding of autologous IgG to human red blood cells before and after ATP-depletion. Selective exposure of binding sites (autoantigens) on spectrin-free vesicles. Biochim Biophys Acta 1983;729:249-257
59. Lutz HU, Stammler P, Furter C, Fasler S: Alternative complement pathway activation by antiband clusterization in congenital dyserythropoietic anemia type II. Exp Hematol 1998;26:869-873.
60. Szymanski IO, Odgren PR, Fortier N, Snyder LM: Red blood cell associated IgG in normal and pathologic states. Blood 1980;55:48-54.
61. Muller H, Lutz HU: Binding of autologous IgG to human red blood cells before and after ATP-depletion. Selective exposure of binding sites (autoantigens) on spectrin-free vesicles. Biochim Biophys Acta 1983;729:249-257.
62. Lutz HU, Stammler P, Furter C, Fasler S: Alternative complement pathway activation by antiband 3. antibodies (in German). Schweiz Med Wochenschr 1987;117:1821-1824.
63. Lutz HU, Stammler P, Fasler S: How naturally occurring anti-band 3-antibodies stimulate C3b deposition to senescent and oxidatively stressed red blood cells. Biomed Biochim Acta 1990;49:224-229.
64. Lutz HU: Erythrocyte clearance; in Harris JR (ed): Blood Cell Biochemistry, vol 1, Erythroid Cells. New York and London: Plenum Press, 1990, pp 81-120.
65. Lutz HU, Nater M, Stammler P: Naturally occurring anti-band 3 antibodies have a unique affinity for C3. Immunology 1993;80:191-196.
66. Lutz HU, Stammler P, Fasler S: Preferential formation of C3b-IgG complexes in vitro and in vivo from nascent C3b and naturally occurring anti-band 3 antibodies. J Biol Chem 1993;268:17418-17426.
67. Gadd KJ, Reid KBM: The binding of complement component C3 to antibody-antigen aggregates after activation of the alternative pathway in human serum. Biochem J 1981;195:471-480.
68. Jelezarova E, Vogt A, Lutz HU: Interaction of C3b2-IgG complexes with complement proteins properdin, factor B and factor H: implications for amplification. Biochem J 2000;349:217-223.
69. Jelezarova E, Lutz HU: Assembly and regulation of the complement amplification loop in blood: The role of C3b-C3b-IgG complexes. Mol Immunol 1999;36:837-842.
70. Jelezarova E, Luginbuehl A, Lutz HU: C3b2-IgG complexes retain dimeric C3 fragments at all levels of inactivation. J Biol Chem 2003;278:51806-51812.
71. Schroit AJ, Madsen JW, Tanaka Y: In vivo recognition and clearance of red blood cells containing phosphatidylserine in their plasma membranes. J Biol Chem 1985;260:5131-5138.
72. Connor J, Pak CC, Schroit AJ: Exposure of phosphatidylserine in the outer leaflet of human red blood cells-relationship to cell density, cell age, and clearance by mononuclear cells. J Biol Chem 1994;269:2399-2404.
73. Boas FE, Forman L, Beutler E: Phosphatidylserine exposure and red cell viability in red cell aging and in hemolytic anemia. Proc Natl Acad Sci USA 1998;95:3077-3081.
74. vanEngeland M, Nieland LJW, Ramaekers FCS, Schutte B, Reutelingsperger CPM: Annexin Vaffinity assay: a review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 1998;31:1-9.
75. Khandelwal S, Saxena RK: A role of phosphatidylserine externalization in clearance of erythrocytes exposed to stress but not in eliminating aging populations of erythrocyte in mice. Exp Gerontol 2008; 43:764-770.
76. Khandelwal S, Saxena RK: Age-dependent increase in green autofluorescence of blood erythrocytes. J Biosci 2007;32:1139-1145.
77. Foller M, Huber SM, Lang F: Erythrocyte programmed cell death. IUBMB Life 2008;60:661-668.
78. Miyanishi M, Tada K, Koike M, Uchiyama Y, Kitamura T, Nagata S: Identification of Tim4 as a phosphatidylserine receptor. Nature 2007;450:435-439.
79. Lang PA, Beringer O, Nicolay JP, Amon O, Kempe DS, Hermle T, Attanasio P, Akel A, Schafer R, Friedrich B, Risler T, Baur M, Olbricht CJ, Zimmerhackl LB, Zipfel PF, Wieder T, Lang F: Suicidal death of erythrocytes in recurrent hemolytic uremic syndrome. J Mol Med 2006;84:378-388.
80. Risso A, Turello M, Biffoni F, Antonutto G: Red blood cell senescence and neocytolysis in humans after high altitude acclimatization. Blood Cells Mol Dis 2007;38:83-92.
81. Galili U: The natural anti-gal antibody: Evolution and autoimmunity in man; in Bona CA, Kaushik AK (eds): Molecular Immunobiology of Self-Reactivity. New York, Marcel Dekker, 1992, pp 355-373.
82. Sorette MP, Galili U, Clark MR: Comparison of serum anti-band-3 and anti-gal antibody binding to density-separated human red blood cells. Blood 1991;77:628-636.
83. Oldenborg PA, Gresham HD, Lindberg FP: CD47-signal regulatory protein alpha (SIRPα alpha) regulates Fc gamma and complement receptor-mediated phagocytosis. J Exp Med 2001;193:855-861.
84. Oldenborg PA, Gresham HD, Chen Y, Izui S, Lindberg FP: Lethal autoimmune hemolytic anemia in CD47-deficient nonobese diabetic (NOD) mice. Blood 2002;99:3500-3504.
85. Arndt PA, Garratty G: Rh(null) red blood cells with reduced CD47 do not show increased interactions with peripheral blood monocytes. Br J Haematol 2004;125:412-414.
86. Bruce LJ, Ghosh S, King MJ, Layton DM, Mawby WJ, Stewart GW, Oldenborg PA, Delaunay J, Tanner MJA: 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.
87. Subramanian S, Parthasarathy R, Sen S, Boder ET, Discher DE: Species-and cell type-specific interactions between CD47 and human SIRPα. Blood 2006;107:2548-2556.