Antigen modulation as a potential mechanism of anti-KEL immunoprophylaxis in mice

Blood

Volumn 128, Issue 26, 2016, Pages 3159-3168

  Liu, Jingchun ^a   Santhanakrishnan, Manjula ^a   Natarajan, Prabitha ^a   Gibb, David R ^a   Eisenbarth, Stephanie C ^a   Tormey, Christopher A ^a,b   Siddon, Alexa J ^a   Stowell, Sean R ^c   Branch, Donald R ^d   Hendrickson, Jeanne E ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d CANADIAN BLOOD SERVICES   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3; FC RECEPTOR; GLYCOPROTEIN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; KEL GLYCOPROTEIN; KEL GLYCOPROTEIN ANTIBODY; POLYCLONAL ANTIBODY; UNCLASSIFIED DRUG; ANTIGEN; ANTIIDIOTYPIC ANTIBODY; IMMUNOGLOBULIN RECEPTOR; KEL PROTEIN, HUMAN; MEMBRANE PROTEIN; METALLOPROTEINASE; OPSONIN;

ALLOIMMUNIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD GROUP KELL SYSTEM; CIRCULATION; CONTROLLED STUDY; ERYTHROCYTE TRANSFUSION; FLOW CYTOMETRY; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOPROPHYLAXIS; IN VITRO STUDY; KNOCKOUT MOUSE; MOUSE; NONHUMAN; OPSONIZATION; PHAGOCYTOSIS; PRIORITY JOURNAL; SPLEEN CELL; WESTERN BLOTTING; WILD TYPE MOUSE; ANIMAL; BLOOD TRANSFUSION; C57BL MOUSE; CROSS BREEDING; CYTOLOGY; ERYTHROCYTE; HUMAN; IMMUNIZATION; IMMUNOLOGY; METABOLISM; SPLEEN;

ANIMALS; ANTIBODIES, ANTI-IDIOTYPIC; ANTIGENS; BLOOD TRANSFUSION; BLOTTING, WESTERN; COMPLEMENT C3; CROSSES, GENETIC; ERYTHROCYTES; HUMANS; IMMUNIZATION; MEMBRANE GLYCOPROTEINS; METALLOENDOPEPTIDASES; MICE, INBRED C57BL; MICE, KNOCKOUT; OPSONIN PROTEINS; PHAGOCYTOSIS; RECEPTORS, IMMUNOLOGIC; SPLEEN;

EID: 85015087549     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2016-06-724732     Document Type: Article

References (38)

1. Reid ME, Mohandas N. Red blood cell blood group antigens: structure and function. Semin Hematol. 2004;41(2):93-117.
2. Fasano RM. Hemolytic disease of the fetus and newborn in the molecular era. Semin Fetal Neonatal Med. 2016;21(1):28-34.
3. US Department of Health and Human Services (FDA). Fatalities reported to the FDA following blood collection. http://www.fda.gov/BiologicsBloodVaccines/SafetyAvailability. 2014. Accessed 1 July 2016.
4. Hendrickson JE, Tormey CA, Shaz BH. Red blood cell alloimmunization mitigation strategies. Transfus Med Rev. 2014;28(3):137-144.
5. Chou ST, Jackson T, Vege S, Smith-Whitley K, Friedman DF, Westhoff CM. High prevalence of red blood cell alloimmunization in sickle cell disease despite transfusion from Rh-matched minority donors. Blood. 2013;122(6):1062-1071.
6. Bowman JM. Controversies in Rh prophylaxis. Who needs Rh immune globulin and when should it be given? Am J Obstet Gynecol. 1985;151(3):289-294.
7. Brinc D, Lazarus AH. Mechanisms of anti-D action in the prevention of hemolytic disease of the fetus and newborn. Hematology Am Soc Hematol Educ Program. 2009;2009:185-191.
8. Kumpel BM. On the mechanism of tolerance to the Rh D antigen mediated by passive anti-D (Rh D prophylaxis). Immunol Lett. 2002;82(1-2):67-73.
9. Kapur R, Della Valle L, Verhagen OJ, et al. Prophylactic anti-D preparations display variable decreases in Fc-fucosylation of anti-D. Transfusion. 2015;55(3):553-562.
10. Kapur R, Della Valle L, Sonneveld M, et al. Low anti-RhD IgG-Fc-fucosylation in pregnancy: a new variable predicting severity in haemolytic disease of the fetus and newborn. Br J Haematol. 2014;166(6):936-945.
11. Kumpel BM. Efficacy of RhD monoclonal antibodies in clinical trials as replacement therapy for prophylactic anti-D immunoglobulin: more questions than answers. Vox Sang. 2007;93(2):99-111.
12. Kumpel BM. Lessons learnt from many years of experience using anti-D in humans for prevention of RhD immunization and haemolytic disease of the fetus and newborn. Clin Exp Immunol. 2008;154(1):1-5.
13. Goossens D, da Silva N, Metral S, et al. Mice expressing RHAG and RHD human blood group genes. PLoS One. 2013;8(11):e80460.
14. Brinc D, Le-Tien H, Crow AR, Freedman J, Lazarus AH. IgG-mediated immunosuppression is not dependent on erythrocyte clearance or immunological evasion: implications for the mechanism of action of anti-D in the prevention of haemolytic disease of the newborn? Br J Haematol. 2007;139(2):275-279.
15. Getahun A, Heyman B. Studies on the mechanism by which antigen-specific IgG suppresses primary antibody responses: evidence for epitope masking and decreased localization of antigen in the spleen. Scand J Immunol. 2009;70(3):277-287.
16. Yu H, Stowell SR, Bernardo L, et al. Antibody-mediated immune suppression of erythrocyte alloimmunization can occur independently from red cell clearance or epitope masking in a murine model. JImmunol.2014;193(6):2902-2910.
17. Stowell SR, Arthur CM, Girard-Pierce KR, et al. Anti-KEL sera prevents alloimmunization to transfused KEL RBCs in a murine model. Haematologica. 2015;100(10):e394-e397.
18. Bernardo L, Yu H, Amash A, Zimring JC, Lazarus AH. IgG-mediated immune suppression to erythrocytes by polyclonal antibodies can occur in the absence of activating or inhibitory Fcγ receptors in a full mouse model. J Immunol. 2015;195(5):2224-2230.
19. Bergström JJ, Heyman B. IgG suppresses antibody responses in mice lacking C1q, C3, complement receptors 1 and 2, or IgG Fc-receptors. PLoS One. 2015;10(11):e0143841.
20. Girard-Pierce KR, Stowell SR, Smith NH, et al. A novel role for C3 in antibody-induced red blood cell clearance and antigen modulation. Blood. 2013;122(10):1793-1801.
21. Smith NH, Henry KL, Cadwell CM, et al. Generation of transgenic mice with antithetical KEL1 and KEL2 human blood group antigens on red blood cells. Transfusion. 2012;52(12):2620-2630.
22. Stowell SR, Girard-Pierce KR, Smith NH, et al. Transfusion of murine red blood cells expressing the human KEL glycoprotein induces clinically significant alloantibodies. Transfusion. 2014;54(1):179-189.
23. Branch DR, Gallahger MT. Correlation of in vivo alloantibody significance or insignificance with an in vitro monocyte-macrophage phagocytosis assay. Br J Haematol. 1986;62(4):783-785.
24. Taylor RP, Lindorfer MA. Fcγ-receptor-mediated trogocytosis impacts mAb-based therapies: historical precedence and recent developments. Blood. 2015;125(5):762-766.
25. Zimring JC, Cadwell CM, Spitalnik SL. Antigen loss from antibody-coated red blood cells. Transfus Med Rev. 2009;23(3):189-204.
26. Sullivan HC, Arthur CM, Patel SR, Hendrickson JE, Lazarus AH, Stowell SR. Anti-RhD mediates loss of RhD antigen following anti-RhD infusion. Blood. 2015;126(23):3570.
27. Béliard R. Monoclonal anti-D antibodies to prevent alloimmunization: lessons from clinical trials. Transfus Clin Biol. 2006;13(1-2):58-64.
28. Stowell SR, Liepkalns JS, Hendrickson JE, et al. Antigen modulation confers protection to red blood cells from antibody through Fcγ receptor ligation. J Immunol. 2013;191(10):5013-5025.
29. Freedman J, Massey A, Chaplin H, Monroe MC. Assessment of complement binding by anti-D and anti-M antibodies employing labelled antiglobulin antibodies. Br J Haematol. 1980;45(2):309-318.
30. Yi T, Li J, Chen H, et al. Splenic dendritic cells survey red blood cells for missing Self-CD47 to trigger adaptive immune responses. Immunity. 2015;43(4):764-775.
31. Branch DR, Shabani F, Lund N, Denomme GA. Antenatal administration of Rh-immune globulin causes significant increases in the immunomodulatory cytokines transforming growth factor-beta and prostaglandin E2. Transfusion. 2006;46(8):1316-1322.
32. Pepys MB. Role of complement in induction of antibody production in vivo. Effect of cobra factor and other C3-reactive agents on thymus-dependent and thymus-independent antibody responses. J Exp Med. 1974;140(1):126-145.
33. Sörman A, Zhang L, Ding Z, Heyman B. How antibodies use complement to regulate antibody responses. Mol Immunol. 2014;61(2):79-88.
34. Rutemark C, Alicot E, Bergman A, et al. Requirement for complement in antibody responses is not explained by the classic pathway activator IgM. Proc Natl Acad Sci USA. 2011;108(43):E934-E942.
35. Carter RH, Fearon DT. CD19: lowering the threshold for antigen receptor stimulation of B lymphocytes. Science. 1992;256(5053):105-107.
36. Stowell SR, Winkler AM, Maier CL, et al. Initiation and regulation of complement during hemolytic transfusion reactions. Clin Dev Immunol. 2012;2012:307093.
37. Engelfriet CP, Von dem Borne AE, Beckers D, Reynierse E, Van Loghem JJ. Autoimmune haemolytic anaemias. V. studies on the resistance against complement haemolysis of the red cells of patients with chronic cold agglutinin disease. Clin Exp Immunol. 1972;11(2):255-264.
38. Nimmerjahn F, Ravetch JV. Fcgamma receptors as regulators of immune responses. Nat Rev Immunol. 2008;8(1):34-47.