Lyse or not to lyse: Clinical significance of red blood cell autoantibodies

Blood Reviews

Volumn 29, Issue 6, 2015, Pages 369-376

  Meulenbroek, Elisabeth M ^a   Wouters, Diana ^a   Zeerleder, Sacha S ^b  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Autoantibodies; Autoimmune hemolytic anemia; Clinical significance; Diagnostic assays; Direct antiglobulin test; Red blood cells

Indexed keywords

CD59 ANTIGEN; COMPLEMENT COMPONENT C3; ERYTHROCYTE ANTIBODY; FC RECEPTOR; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; AUTOANTIBODY; IMMUNOGLOBULIN CLASS; PROTEIN BINDING;

ANTIBODY DETECTION; ANTIBODY SPECIFICITY; ANTIBODY TITER; ANTIGEN ANTIBODY REACTION; AUTOIMMUNE HEMOLYTIC ANEMIA; COMPLEMENT ACTIVATION; COOMBS TEST; GLYCOSYLATION; HEMAGGLUTINATION; HEMOLYSIS; HUMAN; NEONATAL ALLOIMMUNE THROMBOCYTOPENIA; NONHUMAN; OPSONIZATION; PATHOGENICITY; PHAGOCYTOSIS; PREDICTIVE VALUE; PRIORITY JOURNAL; REVIEW; ANEMIA, HEMOLYTIC, AUTOIMMUNE; ANTIBODY AFFINITY; BIOSYNTHESIS; BLOOD; CHEMISTRY; ERYTHROCYTE; IMMUNOLOGY; PATHOLOGY; STATISTICS AND NUMERICAL DATA;

ANEMIA, HEMOLYTIC, AUTOIMMUNE; ANTIBODY AFFINITY; ANTIBODY SPECIFICITY; AUTOANTIBODIES; COOMBS TEST; ERYTHROCYTES; HEMOLYSIS; HUMANS; IMMUNOGLOBULIN ISOTYPES; PHAGOCYTOSIS; PROTEIN BINDING;

EID: 84948083965     PISSN: 0268960X     EISSN: 15321681     Source Type: Journal    
DOI: 10.1016/j.blre.2015.05.001     Document Type: Article

References (94)

1. Gorst D.W., Ralinson V.I., Merry A.H., Stratton F. Positive direct antiglobulin test in normal individuals. Vox Sang 1980, 38:99-105.
2. Dacie J.V., Worlledge S.M. Auto-immune hemolytic anemias. Prog Hematol 1969, 6:82-120.
3. Freedman J. False-positive antiglobulin tests in healthy subjects and in hospital patients. J Clin Pathol 1979, 32:1014-1018.
4. Kaplan H.S., Garratty G. Predictive value of direct antiglobulin test results. Diagn Med 1985, 8:29-33.
5. Garratty G. Immune hemolytic anemia associated with negative routine serology. Semin Hematol 2005, 42:156-164.
6. Zeerleder S. Autoimmune haemolytic anaemia - a practical guide to cope with a diagnostic and therapeutic challenge. Neth J Med 2011, 69:177-184.
7. Lai M., Leone G., Landolfi R. Autoimmune hemolytic anemia with gel-based immunohematology tests. Am J Clin Pathol 2013, 138:457-463.
8. Lin J.S., Hao T.C., Lyou J.Y., Chen Y.J., Liu H.M., Tzeng C.H., et al. Clinical application of a flow cytometric direct antiglobulin test. Transfusion 2009, 49:1335-1346.
9. Garratty G., Nance S.J. Correlation between in vivo hemolysis and the amount of red cell-bound IgG measured by flow cytometry. Transfusion 1990, 30:617-621.
10. Shi J., Rose E.L., Singh A., Hussain S., Stagliano N.E., Parry G.C., et al. TNT003, an inhibitor of the serine protease C1s, prevents complement activation induced by cold agglutinins. Blood 2014, 123:4015-4022.
11. Berentsen S., Tjonnfjord G.E. Diagnosis and treatment of cold agglutinin mediated autoimmune hemolytic anemia. Blood Rev 2012, 26:107-115.
12. Petz L.S. Cold antibody autoimmune hemolytic anemia. Blood Rev 2008, 22:1-15.
13. Zantek N.D., Koepsell S.A., Tharp D.R., Cohn C.S. The direct antiglobulin test: a critical step in the evaluation of hemolysis. Am J Hematol 2012, 87:707-709.
14. Bicakci Z., Ozturkmen S., Akyay A., Olcay L. False positive result of the direct antiglobulin test (DAT): the role of the elevated level of immunoglobulin G. Pediatr Hematol Oncol 2012, 29:611-619.
15. Ness P.M., Shirey R.S., Thoman S.K., Buck S.A. The differentiation of delayed serologic and delayed hemolytic transfusion reactions: incidence, long-term serologic findings and clinical significance. Transfusion 1990, 30:688-693.
16. Linden J.V., Paul B., Dressler K.P. A report of 104 transfusion errors in New York state. Transfusion 1992, 32:601-608.
17. Segel G.B., Lichtman M.A. Direct antiglobulin ("Coombs") test-negative autoimmune hemolytic anemia: a review. Blood Cells Mol Dis 2014, 52:152-160.
18. Zupanska B., Brojer E., Thomson E.E., Merry A.H., Seyfried H. Monocyte-erythrocyte interaction in autoimmune haemolytic anaemia in relation to the number of erythrocyte-bound IgG molecules and subclass specificity of autoantibodies. Vox Sang 1987, 52:212-218.
19. Zupanska B., Thompson E., Brojer E., Merry A.H. Phagocytosis of erythrocytes sensitized with known amounts of IgG1 and IgG3 anti-Rh antibodies. Vox Sang 1987, 53:96-101.
20. Boven L.A., de Haar-Holleman A., Folman C.C., Kraaijenhagen R.J., Fijnheer R. Diagnostic and therapeutic challenges of severe Rh e-specific IgA-mediated autoimmune hemolytic anemia. Ann Hematol 2012, 91:641-642.
21. Kamesaki T., Toyoysuji T., Kajii E. Characterization of direct antiglobulin test-negative autoimmune hemolytic anemia: a study of 154 cases. Am J Hematol 2013, 88:93-96.
22. Van Dijk B.A., Dooren M.C., Overbeeke M.A. Red cell antibodies in pregnancy: there is no 'critical titre'. Transfus Med 1995, 5:199-202.
23. Hadley A.G., Zupanska B., Kumpel B.M., Pilkington C., Griffiths H.L., Leader K.A., et al. The glycosylation of red cell autoantibodies affects their functional activity in vitro. Br J Haemotol 1995, 91:587-594.
24. Schwartz R.S., Costea N. Autoimmune hemolytic anemia: clinical correlations and biological implications. Semin Hematol 1966, 3:2-26.
25. Fossati-Jimack L., Reininger L., Chicheportiche Y., Clynes R., Ravetch J.V., Honjo T., et al. High pathogenic potential of low-affinity autoantibodies in experimental autoimmune hemolytic anemia. J Exp Med 1999, 190:1689-1696.
26. Izui S., Fossati-Jimack L., Azeredo da Silveira S., Moll T. Isotype-dependent pathogenicity of autoantibodies: analysis in experimental autoimmune hemolytic anemia. Springer Semin Immunopathol 2001, 23:433-445.
27. Suwannalai P., Britsemmer K., Knevel R., Scherer H.U., Levarht E.W.N., Van der Helm-Van Mil A.H., et al. Low-avidity anticitrullinated protein antibodies (ACPA) are associated with a higher rate of joint destruction in rheumatoid arthritis. Ann Rheum Dis 2014, 73:270-276.
28. Rosse W.F., Adams J.P. The variability of hemolysis in the cold agglutinin syndrome. Blood 1980, 56:409-416.
29. Garratty G., Petz L.D., Hoops J.K. The correlation of cold agglutinin titrations in saline and albumin with haemolytic anaemia. Br J Haematol 1977, 35:587-595.
30. Petz L.D. Diagnostic complexities in autoimmune hemolytic anemias. Transfusion 2009, 49:202-203.
31. Bass G.F., Tuscano E.T., Tuscano J.M. Diagnosis and classification of autoimmune hemolytic anemia. Autoimmun Rev 2014, 13:560-564.
32. Hadley A.G. Laboratory assays for predicting the severity of haemolytic disease of the fetus and newborn. Transpl Immunol 2002, 10:191-198.
33. Sokol R.J., Hewitt S., Booker D.J., Bailey A. Red cell autoantibodies, multiple immunoglobulin classes, and autoimmune haemolysis. Transfusion 1990, 30:714-717.
34. Das S.S., Nityanand S., Chaudhary R. Clinical and serological characterization of autoimmune hemolytic anemia in a tertiary care hospital in North India. Ann Hematol 2009, 88:727-732.
35. Garratty G. Effect of cell-bound proteins on the in vivo survival of circulating blood cells. Gerontology 1991, 37:68-94.
36. Engelfriet C.P., Overbeeke M.A., Von dem Borne A.E. Autoimmune hemolytic anemia. Semin Hematol 1992, 29:3-12.
37. Sokol R.J., Booker D.J., Stamps R. The pathology of autoimmune haemolytic anemia. J Clin Pathol 1992, 45:1047-1052.
38. Sokol R.J., Hewitt S., Booker D.J., Bailey A. Erythrocyte autoantibodies, subclasses of IgG and autoimmune haemolysis. Autoimmunity 1990, 6:99-104.
39. Kapur R., Kustiawan I., Vestrheim A., Koeleman C.A.M., Visser R., Einarsdottir H.K., et al. A prominent lack of IgG1-Fc fucosylation of platelet alloantibodies in pregnancy. Blood 2014, 123:471-480.
40. Wright A., Morrison S.L. Effect of glycosylation on antibody function: implications for genetic engineering. Trends Biotechnol 1997, 15:26-32.
41. Ito K., Furukawa J., Yamada K., Tran N.L., Shinohara Y., Izui S. Lack of galactosylation enhances the pathogenic activity of IgG1 but not IgG2a anti-erythrocyte autoantibodies. J Immunol 2014, 192:581-588.
42. Barker R.N., Young R.D., Leader K.A., Elson C.J. Galactosylation of serum IgG and autoantibodies in murine models of autoimmune haemolytic anaemia. Clin Exp Immunol 1999, 117:449-454.
43. Barker R.N., Leader K.A., Elson C.J. Serial changes in the galactosylation of autoantibodies and serum IgG in autoimmune haemolytic anaemia. Autoimmunity 1999, 31:103-108.
44. Malhotra R., Wormald M.R., Rudd P.M., Fischer P.B., Dwek R.A., Sim R.B. Glycosylation changes of IgG associated with rheumatoid arthritis can activate complement via the mannose-binding protein. Nat Med 1995, 1:237-243.
45. Kapur R., Einarssdottir H.K., Vidarsson G. IgG-effector functions: "The good, the bad and the ugly". Immunol Lett 2014, 160:139-144.
46. Kumpel B.M., Van de Winkel J.G.J., Westerdaal N.A.C., Hadley A.G., Dugoujon J.M., Blancher A. Antigen topogrpahy is critical for interaction of IgG2 anti-red-cell antibodies with Fc receptors. Br J Haematol 1996, 94:175-183.
47. Kurlander R.J., Rosse W.F., Logue G.L. Quantitative influence of antibody and complement coating of red cells on monocyte-mediated cell lysis. Clin Invest 1978, 61:1309-1319.
48. Engelfriet C.P., Ouwehand W.H. ADCC and other cellular bioassays for predicting the clinical significance of red cell alloantibodies. Ballieres Clin Haematol 1990, 3:321-327.
49. Janvier D., Lam Y., Lopez I., Elakredar L., Bierling P. A major target for warm immunoglobulin G autoantibodies: the third external loop of Band 3. Transfusion 2013, 53:1948-1955.
50. Diebolder C.A., Beurskens F.J., De Jong R.N., Koning R.I., Strumane K., Lindorfer M.A., et al. Complement is activated by IgG hexamers assembled at the cell surface. Science 2014, 343:1260-1263.
51. Izui S., Berney T., Shibata T., Fulpius T., Fossati L., Merino R. Molecular and cellular basis for pathogenicity of autoantibodies. Tohoku J Exp Med 1994, 173:15-30.
52. Cushing M., Degtyaryova D., Lomas-Francis C. The role of plasmapheresis in the multimodal treatment of anti-Pr cold agglutinin disease. Transfusion 2010, 50:2100-2101.
53. Brain M.C., Prevost J.M., Pihl C.E., Brown C.B. Glycophorin A-mediated haemolysis of normal human erythrocytes: evidence of antigen aggregation in the pathogenesis of immune haemolysis. Br J Haematol 2002, 118:899-908.
54. Brain M.C., Pihl C., Robertson L., Brown C.B. Evidence for a mechanosensitive calcium influx into red cells. Blood Cells Mol Dis 2004, 32:349-352.
55. Brain M., Ruether B., Valentine K., Brown C., ter Keurs H. Life-threatening hemolytic anemia due to an autoanti-Pr cold agglutinin: evidence that glycophorin A antibodies may induce lipid bilayer exposure and cation permeability independent of agglutination. Transfusion 2010, 50:292-301.
56. Garratty G. A new mechanism for immune destruction of red blood cells. Transfusion 2010, 50:274-277.
57. Barker R.N., Casswell K.M., Reid M.E., Sokol R.J., Elson C.J. Identification of autoantigens in autoimmune haemolytic anaemia by a non-radioisotope immunoprecipitation method. Br J Haemotol 1992, 82:126-132.
58. Leddy J.P., Wilkonson S.L., Kissel G.E., Passador S.T., Falany J.L., Rosenfelt S.I. Erythrocyte membrane proteins reactive with IgG (warm-reacting) anti-red blood cell autoantibodies: II. Antibodies coprecipitating band 3 and glycophorin A. Blood 1994, 84:650-656.
59. Iwamoto S., Kamesaki T., Oyamada Y., Okuda H., Kumada M., Omi T., et al. Reactivity of autoantibodies of autoimmune hemolytic anemia with recombinant Rhesus blood group antigens or anion transporter Band 3. Am J Hematol 2001, 68:106-114.
60. a antigen. Transfusion 1977, 16:621-624.
61. a in a Spanish population. Transfusion 2005, 45:1324-1326.
62. Stahl D., Lacroix-Desmazes S., Kaveri S.V., Kazatchkine M.D. Polyreactivity of disease-associated anti-RBC IgG autoantibodies of patients with warm autoimmune haemolytic anaemia and natural anti-RBC IgG autoantibodies of healthy individuals. Scand J Immunol 2000, 52:190-199.
63. Hughey C.T., Brewer J.W., Colosia A.D., Rosse W.F., Corley R.B. Production of IgM hexamers by normal and autoimmune B cells: implications for the physiologic role of hexameric IgM. J Immunol 1998, 161:4091-4097.
64. Collins C., Tsui F.W.L., Shulman M.J. Differential activation of human and guinea pig complement by pentameric and hexameric IgM. Eur J Immunol 2002, 32:1802-1810.
65. Zimring J.C., Cadwell C.M., Spitalnik S.L. Antigen loss from antibody-coated red blood cells. Transfus Med Rev 2009, 23:189-204.
66. Zimring J.C., Cadwell C.M., Chadwick T.E., Spitalnik S.L., Schirmer D.A., Wu T., et al. Nonhemolytic antigen loss from red blood cells requires cooperative binding of multiple antibodies recognizing different epitopes. Blood 2007, 110:2201-2208.
67. Attanasio P., Shumilina E., Hermle T., Kiedaisch V., Lang P.A., Huber S.M., et al. Stimulation of eryptosis by anti-A IgG antibodies. Cell Physiol Biochem 2007, 20:591-600.
68. Baudino L., Fossati-Jimack L., Chevalley C., Martinez-Soria E., Shulman M.J., Izui S. IgM and IgA anti-erythrocyte autoantibodies induce anaemia in a mouse model through multivalency-dependent hemagglutination but not through complement activation. Blood 2007, 109:5355-5362.
69. Chen X., Ghaffar H., Jen C.C., Lazarus A.H. Antibody specific for the glycophorin A complex mediates intravenous immune globulin-resistant anemia in a murine model. Transfusion 2014, 54:655-664.
70. Chadebech P., Michel M., Janvier D., Yamada K., Copie-Bergman C., Bodivit G., et al. IgA-mediated human autoimmune hemolytic anemia as a result of hemagglutination in the spleen, but independent of complement activation and FcaR1. Blood 2010, 116:4141-4147.
71. Liepkalns J.S., Hod E.A., Stowell S.R., Cadwell C.M., Spitalnik S.L., Zimring J.C. Biphasic clearance of incompatible red blood cells through a novel mechanism requiring neither complement nor Fcg receptors in a murine model. Transfusion 2012, 52:2631-2645.
72. Zupanska B. Assays to predict the clinical significance of blood group antibodies. Curr Opin Hematol 1998, 5:412-416.
73. Nance S.J., Arndt P., Garratty G. Predicting the clinical significance of red cell alloantibodies using a monocyte monolayer assay. Transfusion 1987, 27:449-452.
74. Arndt P.A., Garratty G. A retrospective analysis of the vaue of monocyte monolayer assay results for predicting the clinical significance of blood group alloantibodies. Transfusion 2004, 44:1273-1281.
75. Van der Meulen F.W., Van der Hart M., Fleer A., Von dem Borne A.E.G., Engelfriet C.P., Van Loghem J.J. The role of adherence to mononuclear phagocytes in the destruction of red cells sensitized with non-complement binding IgG antibodies. Br J Haematol 1978, 38:541-549.
76. Wikman A., Axdorph U., Gryfelt G., Gustafsson L., Bjorkholm M., Lundahl J. Characterization of red cell autoantibodies in consecutive DAT-positive patients with relation to in vivo haemolysis. Ann Hematol 2005, 84:150-158.
77. Gallagher M.T., Branch D.R., Mison A., Petz L.D. Evaluation of reticuloendothelial function in autoimmune hemolytic anaemia using an in vitro assay of monocyte-macrophage interaction with erythrocytes. Exp Hematol 1983, 11:82-89.
78. Miescher S., Spycher M.O., Amstutz H., De Haas M., Kleijer M., Kalus U.J., et al. A single recombinant anti-RhD IgG prevents RhD immunization: association of RhD-positive red blood cell clearance rate with polymorphisms in FcgamamRIIA and FcgammaIIIA genes. Blood 2004, 103:4028-4035.
79. Breunis W.B., Van Mirre E., Bruin M., Geissler J., De Boer M., Peters M., et al. Copy number variation of the activating FCGR2C gene predisposes to idiopathic thrombocytopenic purpura. Blood 2008, 111:1029-1038.
80. Sunada M., Suzuki S., Ota Z. Reticuloendothelial cell function in autoimmune hemolytic anemia (AIHA): studies on the mechanism of peripheral monocyte activation. Acta Med Okayama 1985, 39:375-384.
81. Gilsanz F., De La Serna J., Molto L., Alvarez-Mon M. Hemolytic anemia in chronic large granular lymphocytic leukemia of natural killer cells: cytotoxicity of natural killer cells against autologous red cells is associated with hemolysis. Transfusion 1996, 36:463-466.
82. Rondelli T., Risitano A.M., De Latour R.P., Sica N., Peruzzi B., Ricci P., et al. Polymorphism of the complement receptor 1 gene correlates with the hematologic response to eculizumab in patients with paroxysmal nocturnal hemoglobinuria. Haemoatologica 2014, 99:262-266.
83. Barros M.M., Yamamoto M., Figueiredo M.S., Cancado R., Kimura E.Y.S., Langhi D.M., et al. Expression levels of CD47, CD35, CD55, CD59 on red blood cells and signal refulatory protein alpha, beta on monocytes from patients with warm autoimmune hemolytic anemia. Transfusion 2009, 49:154-160.
84. Richaud-Patin Y., Perez-Romano B., Carrillo-Maravilla E., Rodriguez A.B., Simon A.J., Cabiedes J., et al. Deficiency of red cell bound CD55 and CD59 in patients with systemic lupus erythematosus. Immunol Lett 2003, 88:95-99.
85. Ruiz-Delgado G.J., Vazguez-Garza E., Mendez-Ramirez N., Gomez-Almaguer D. Abnormalities in the xpression of CD55 and CD59 surface molecules on peripheral blood cells are not specific to paroxysmal nocturnal hemoglobinuria. Hematology 2009, 14:33-37.
86. Fayek M.H., Saad A.A., Eissa D.G., Tawfik L.M., Kamal G. Role of gel test and flow cytometry in diagnosis of Coombs' negative autoimmune haemolytic anaemia. Int J Lab Hematol 2012, 34:311-319.
87. Kamesaki T., Oyamada T., Omine M., Ozawa K., Kajii E. Cut-off value of red-blood-cell-bound IgG for the diagnosis of Coombs-negative autoimmune hemolytic anemia. Am J Hematol 2009, 84:98-101.
88. Brouwer H.A., Overbeeke M.A., Van Ertbruggen I., Schaasberg W., Alsbach G.F., Van der Heiden C., et al. What is the best predictor of the severity of ABO-haemolytic disease of the newborn?. Lancet 1988, 2:641-644.
89. Engelfriet C.P., Overbeeke M.A., Dooren M.C., Ouwehand W.H., Von dem Borne A.E. Bioassays to determine the clinical significance of red cell alloantibodies based on Fc receptor-induced destruction of red cells sensitized by IgG. Transfusion 1994, 34:617-626.
90. Biondi C.S., Cotorruelo C.M., Ensinck A., Racca L.L., Racca A.L. Use of the erythrophagocytosis assay for predicting the clinical consequences of immune blood cell destruction. Clin Lab 2004, 50:265-270.
91. Barcellini W., Fattizzo B., Zaninoni A., Radice T., Nichele I., Di Bona E., et al. Clinical heterogeneity and predictors of outcome in primary hemolytic anemia: a GIMEMA study of 308 patients. Blood 2014, 124:2930-2936.
92. Fischer J.T., Petz L.D., Garratty G., Cooper N.R. Correlations between quantitative assay of red cell-bound C3, serologic reactions, and hemolytic anemia. Blood 1974, 44:359-373.
93. Wheeler C.A., Calhoun L., Blackall D.P. Warm reactive autoantibodies. Clinical and serological correlations. Am J Clin Pathol 2004, 122:680-685.
94. Blackall D.P. Warm-reactive autoantibodies in pediatric patients: clinical and serologic correlations. J Pediatr Hematol Oncol 2007, 29:792-796.