Home LiteratureArticle Details
PMID: 3313392 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Naturally occurring anti-band-3 antibodies and complement together mediate phagocytosis of oxidatively stressed human erythrocytes.

Lutz HU, Bussolino F, Flepp R, Fasler S, Stammler P, Kazatchkine MD, Arese P

Abstract

Treatment of erythrocytes with the thiol-specific oxidant azodicarboxylic acid bis(dimethylamide) (diamide) enhances their phagocytosis by adherent monocytes. Phagocytosis of diamide-treated erythrocytes required that the cells were opsonized with whole serum, since complement inactivation abolished phagocytosis. Opsonization with whole serum containing 20-100 times the physiological concentration of naturally occurring anti-band-3 antibodies enhanced phagocytosis of diamide-treated erythrocytes. High inputs of anti-band-3 also restored phagocytosis of erythrocytes that had been incubated with complement-inactivated serum. Elevated concentrations of anti-spectrin antibodies were ineffective in whole and complement-inactivated serum. Specific recognition of diamide-treated erythrocytes by anti-band-3 antibodies may be due to generation of anti-band-3 reactive protein oligomers on intact diamide-treated erythrocytes. Generation of such oligomers was dose-dependent with respect to diamide. Bound anti-band-3 alone was not sufficient to mediate phagocytosis. It resulted in deposition of complement component C3b on the cells through activation of the alternative complement pathway in amounts exceeding that of bound antibodies by two orders of magnitude. Thus, anti-band-3 and complement together mediate phagocytosis of oxidatively stressed erythrocytes, which stimulate senescent erythrocytes with respect to bound antibody and complement.

MeSH Terms
Anion Exchange Protein 1, Erythrocyte/immunology,physiology Antibodies Antigen-Antibody Complex Complement C3b/metabolism Diamide/pharmacology Erythrocytes/drug effects,immunology,physiology Humans Kinetics Macrophage-1 Antigen Phagocytosis Receptors, Complement/metabolism
Chemicals
Anion Exchange Protein 1, Erythrocyte Antibodies Antigen-Antibody Complex Macrophage-1 Antigen Receptors, Complement Diamide Complement C3b
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Lutz H U
Department of Biochemistry, Swiss Federal Institute of Technology, Zurich.
Bussolino F
Flepp R
Fasler S
Stammler P
Kazatchkine M D
Arese P
References (45)
45 references, click to expand
  1. Interaction of IgG and its fragments with red cells.
    Immunology. 1967 Nov;13(5):489-99 PMID: 4169337
  2. Measurement of phagocytosis utilizing [14C]cyanate-labelled human red cells and monocytes.
    Br J Haematol. 1987 Jun;66(2):271-4 PMID: 3606963
  3. Diamide, a new reagent for the intracellular oxidation of glutathione to the disulfide.
    Biochem Biophys Res Commun. 1969 Nov 6;37(4):593-6 PMID: 5353890
  4. The use of 14C-cyanate as a method for determining erythrocyte survival.
    Proc Soc Exp Biol Med. 1973 Oct 1;144(1):326-8 PMID: 4203822
  5. Properdin factor D: characterization of its active site and isolation of the precursor form.
    J Exp Med. 1974 Feb 1;139(2):355-66 PMID: 4855753
  6. Mechanism of removal of senescent cells by human macrophages in situ.
    Proc Natl Acad Sci U S A. 1975 Sep;72(9):3521-5 PMID: 1059140
  7. The removal of leukocytes and platelets from whole blood.
    J Lab Clin Med. 1976 Aug;88(2):328-33 PMID: 956688
  8. Third component of human complement: purification from plasma and physicochemical characterization.
    Biochemistry. 1976 Oct 5;15(20):4513-21 PMID: 823964
  9. The role of membrane receptors for C3b and C3d in phagocytosis.
    J Exp Med. 1977 Feb 1;145(2):357-71 PMID: 833545
  10. Intra- and intermolecular cross-linking of membrane proteins in intact erythrocytes and ghosts by SH-oxidizing agents.
    Biochim Biophys Acta. 1977 Sep 5;469(2):226-30 PMID: 901784
  11. Interaction of divalent antibody with cell surface antigens.
    Biochemistry. 1979 Jan 23;18(2):264-9 PMID: 420783
  12. Expression of multivalency in the affinity chromatography of antibodies. Appendix: Derivation and evaluation of equations for independent bivalent interacting systems in quantitative affinity chromatography.
    Biochemistry. 1979 Mar 6;18(5):790-5 PMID: 420816
  13. Role of physiologic autoantibody in the removal of senescent human red cells.
    J Supramol Struct. 1978;9(4):555-67 PMID: 108480
  14. Enhancing role of IgG in lysis of rabbit erythrocytes by the alternative pathway of human complement.
    J Immunol. 1979 May;122(5):1994-9 PMID: 376729
  15. The physiological role of the lymphoid system. V. The binding of autologous (erythrophilic) gamma globulin to human red blood cells.
    Biochemistry. 1967 Nov;6(11):3378-85 PMID: 4169271
  16. Role of binding through C3b and IgG in polymorphonuclear neutrophil function: studies with trypsin-generated C3b.
    J Immunol. 1979 Oct;123(4):1839-46 PMID: 573303
  17. Total sialic acid content of glycophorins during senescence of human red blood cells.
    J Biol Chem. 1979 Nov 25;254(22):11177-80 PMID: 500635
  18. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  19. Polymerization of membrane components in aging red blood cells.
    Biochem Biophys Res Commun. 1980 Jan 15;92(1):247-54 PMID: 7356456
  20. Membrane protein complexes in GSH-depleted red cells.
    Blood. 1980 Aug;56(2):159-67 PMID: 7397373
  21. Molecular biology and chemistry of the alternative pathway of complement.
    Adv Immunol. 1980;29:1-53 PMID: 6158260
  22. Decreased survival in vivo of diamide-incubated dog erythrocytes. A model of oxidant-induced hemolysis.
    J Clin Invest. 1980 Nov;66(5):955-61 PMID: 7430352
  23. Phagocytosis requires repeated triggering of macrophage phagocytic receptors during particle ingestion.
    Nature. 1981 Jan 29;289(5796):409-11 PMID: 7464909
  24. Large scale isolation of functionally active components of the human complement system.
    J Biol Chem. 1981 Apr 25;256(8):3995-4006 PMID: 6783652
  25. [Elimination of old erythrocytes from the circulation: exposure of a cell-age specific antigen on aging erythrocytes].
    Schweiz Med Wochenschr. 1981 Oct 10;111(41):1507-17 PMID: 6171880
  26. Naturally occurring autoantibodies to skeletal proteins from human red blood cells.
    J Immunol. 1982 Apr;128(4):1695-9 PMID: 7061846
  27. Detection of IgG sensitization of red cells with 125I staphylococcal protein A.
    Am J Hematol. 1982 Jun;12(4):337-46 PMID: 7114050
  28. 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 Apr 6;729(2):249-57 PMID: 6830791
  29. Phagocytosis of senescent erythrocytes by autologous monocytes: requirement of membrane-specific autologous IgG for immune elimination of aging red blood cells.
    Cell Immunol. 1983 May;78(1):114-21 PMID: 6687842
  30. Phagocytosis of sickle erythrocytes: immunologic and oxidative determinants of hemolytic anemia.
    Blood. 1984 Sep;64(3):733-41 PMID: 6466875
  31. 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 Nov;133(5):2610-8 PMID: 6481164
  32. Localization of senescent cell antigen on band 3.
    Proc Natl Acad Sci U S A. 1984 Sep;81(18):5753-7 PMID: 6207531
  33. Membrane-bound immunoglobulins and complement components on young and old red cells.
    Transfusion. 1984 Nov-Dec;24(6):477-81 PMID: 6506177
  34. C3b covalently bound to IgG demonstrates a reduced rate of inactivation by factors H and I.
    J Exp Med. 1984 Dec 1;160(6):1640-55 PMID: 6239898
  35. The role of hemoglobin denaturation and band 3 clustering in red blood cell aging.
    Science. 1985 Feb 1;227(4686):531-3 PMID: 2578228
  36. Cell-bound autologous immunoglobulin in erythrocyte subpopulations from patients with sickle cell disease.
    Blood. 1985 May;65(5):1127-33 PMID: 3888304
  37. Abnormal redox status of membrane-protein thiols in sickle erythrocytes.
    J Clin Invest. 1985 May;75(5):1531-7 PMID: 3998148
  38. Relationship between the third component of human complement (C3) bound to stored preserved erythrocytes and their viability in vivo.
    Vox Sang. 1985;49(1):34-41 PMID: 4013142
  39. Mouse monoclonal antibodies to the human C3b receptor.
    Mol Immunol. 1985 May;22(5):531-9 PMID: 3160931
  40. Complement ligand-receptor interactions that mediate biological responses.
    Annu Rev Immunol. 1983;1:243-71 PMID: 6242465
  41. Binding of fluid phase C3b to nonsensitized bystander human red cells. A model for in vivo effects of complement activation on blood cells.
    Transfusion. 1985 Nov-Dec;25(6):528-34 PMID: 3907025
  42. Excessive binding of natural anti-alpha-galactosyl immunoglobin G to sickle erythrocytes may contribute to extravascular cell destruction.
    J Clin Invest. 1986 Jan;77(1):27-33 PMID: 3944254
  43. Oxidation as a possible mechanism of cellular aging: vitamin E deficiency causes premature aging and IgG binding to erythrocytes.
    Proc Natl Acad Sci U S A. 1986 Apr;83(8):2463-7 PMID: 3458208
  44. 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 U S A. 1986 Aug;83(16):6137-41 PMID: 3461480
  45. Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g.
    Scand J Clin Lab Invest Suppl. 1968;97:77-89 PMID: 4179068
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1987-11-00
Pages
7368-72
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC299297
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]