Antigen density dictates immune responsiveness following red blood cell transfusion

Journal of Immunology

Volumn 198, Issue 7, 2017, Pages 2671-2680

  Arthur, Connie M ^a   Patel, Seema R ^a   Smith, Nicole H ^a   Bennett, Ashley ^a   Kamili, Nourine A ^a   Mener, Amanda ^a   Gerner Smidt, Christian ^a   Sullivan, Harold C ^a   Hale, J Scott ^a   Wieland, Andreas ^a   Youngblood, Benjamin ^a   Zimring, James C ^b,c   Hendrickson, Jeanne E ^d   Stowell, Sean R ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Bloodworks Northwest Research Institute   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOANTIBODY; ALLOANTIGEN; KEL PROTEIN, HUMAN; MEMBRANE PROTEIN; METALLOPROTEINASE;

ADOPTIVE TRANSFER; ALLOIMMUNIZATION; ANIMAL EXPERIMENT; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; BLOOD TRANSFUSION REACTION; CONTROLLED STUDY; ERYTHROCYTE TRANSFUSION; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOPHENOTYPING; LYMPHOCYTE DEPLETION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECIPIENT; REGULATORY T LYMPHOCYTE; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; ERYTHROCYTE; FLOW CYTOMETRY; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; TRANSGENIC MOUSE;

ANIMALS; ERYTHROCYTE TRANSFUSION; ERYTHROCYTES; FLOW CYTOMETRY; HUMANS; IMMUNE TOLERANCE; IMMUNOPHENOTYPING; ISOANTIBODIES; ISOANTIGENS; MEMBRANE GLYCOPROTEINS; METALLOENDOPEPTIDASES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC;

EID: 85016236021     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1601736     Document Type: Article

References (72)

1. Goodnough, L. T., M. E. Brecher, M. H. Kanter, and J. P. AuBuchon. 1999. Transfusion medicine. First of two parts-blood transfusion. N. Engl. J. Med. 340: 438-447.
2. Landsteiner, K. 1900. Zur Kenntnis der antifermativen, lytischen und agglutinierenden Wirkungendes Blutserums und der Lymphe. Zentbl. Bakt. Parasitkde (Abt.) 27: 357-363.
3. Reali, G. 2007. Forty years of anti-D immunoprophylaxis. Blood Transfus. 5: 3-6.
4. Evers, D., R. A. Middelburg, M. de Haas, S. Zalpuri, K. M. de Vooght, D. van de Kerkhof, O. Visser, N. C. Péquériaux, F. Hudig, H. Schonewille, et al. 2016. Red-blood-cell alloimmunisation in relation to antigens' exposure and their immunogenicity: a cohort study. Lancet Haematol. 3: e284-e292.
5. Hillyer, C. D., B. H. Shaz, A. M. Winkler, and M. Reid. 2008. Integrating molecular technologies for red blood cell typing and compatibility testing into blood centers and transfusion services. Transfus. Med. Rev. 22: 117-132.
6. U.S. Food and Drug Administration. 2015. Fatalities Reported to FDA Following Blood Collection and Transfusion. Annual Summary for Fiscal Year 2015. Available at: http://www.fda.gov/downloads/BiologicsBloodVaccines/SafetyAvailability/ ReportaProblem/TransfusionDonationFatalities/UCM518148.pdf.
7. Nickel, R. S., J. E. Hendrickson, R. M. Fasano, E. K. Meyer, A. M. Winkler, M. M. Yee, P. A. Lane, Y. A. Jones, F. D. Pashankar, T. New, et al. 2016. Impact of red blood cell alloimmunization on sickle cell disease mortality: a case series. Transfusion 56: 107-114.
8. Brand, A. 2016. Immunological complications of blood transfusions. Presse Med. 45: e313-e324.
9. Higgins, J. M., and S. R. Sloan. 2008. Stochastic modeling of human RBC alloimmunization: evidence for a distinct population of immunologic responders. Blood 112: 2546-2553.
10. Yazdanbakhsh, K., R. E. Ware, and F. Noizat-Pirenne. 2012. Red blood cell alloimmunization in sickle cell disease: pathophysiology, risk factors, and transfusion management. Blood 120: 528-537.
11. Bussel, J. B., R. L. Berkowitz, J. G. McFarland, L. Lynch, and U. Chitkara. 1988. Antenatal treatment of neonatal alloimmune thrombocytopenia. N. Engl. J. Med. 319: 1374-1378.
12. Chou, S. T., T. Jackson, S. Vege, K. Smith-Whitley, D. F. Friedman, and C. M. Westhoff. 2013. High prevalence of red blood cell alloimmunization in sickle cell disease despite transfusion from Rh-matched minority donors. Blood 122: 1062-1071.
13. Reid, M. E., and N. Mohandas. 2004. Red blood cell blood group antigens: structure and function. Semin. Hematol. 41: 93-117.
14. Hod, E. A., S. A. Arinsburg, R. O. Francis, J. E. Hendrickson, J. C. Zimring, and S. L. Spitalnik. 2010. Use of mouse models to study the mechanisms and consequences of RBC clearance. Vox Sang. 99: 99-111.
15. Ryder, A. B., J. C. Zimring, and J. E. Hendrickson. 2014. Factors influencing RBC alloimmunization: lessons learned from murine models. Transfus. Med. Hemother. 41: 406-419.
16. Vaughan, J. I., M. Manning, R. M. Warwick, E. A. Letsky, N. A. Murray, and I. A. Roberts. 1998. Inhibition of erythroid progenitor cells by anti-Kell antibodies in fetal alloimmune anemia. N. Engl. J. Med. 338: 798-803.
17. Stowell, S. R., K. L. Henry, N. H. Smith, K. E. Hudson, G. R. Halverson, J. C. Park, A. M. Bennett, K. R. Girard-Pierce, C. M. Arthur, S. T. Bunting, et al. 2013. Alloantibodies to a paternally derived RBC KEL antigen lead to hemolytic disease of the fetus/newborn in a murine model. Blood 122: 1494-1504.
18. Smith, N. H., K. L. Henry, C. M. Cadwell, A. Bennett, J. E. Hendrickson, T. Frame, and J. C. Zimring. 2012. Generation of transgenic mice with antithetical KEL1 and KEL2 human blood group antigens on red blood cells. Transfusion 52: 2620-2630.
19. Arthur, C. M., S. R. Patel, H. C. Sullivan, A. M. Winkler, C. A. Tormey, J. E. Hendrickson, and S. R. Stowell. 2016. CD8+ T cells mediate antibodyindependent platelet clearance in mice. Blood 127: 1823-1827.
20. Wan, Y. Y., and R. A. Flavell. 2005. Identifying Foxp3-expressing suppressor T cells with a bicistronic reporter. Proc. Natl. Acad. Sci. USA 102: 5126-5131.
21. Desmarets, M., C. M. Cadwell, K. R. Peterson, R. Neades, and J. C. Zimring. 2009. Minor histocompatibility antigens on transfused leukoreduced units of red blood cells induce bone marrow transplant rejection in a mouse model. Blood 114: 2315-2322.
22. Girard-Pierce, K. R., S. R. Stowell, N. H. Smith, C. M. Arthur, H. C. Sullivan, J. E. Hendrickson, and J. C. Zimring. 2013. A novel role for C3 in antibodyinduced red blood cell clearance and antigen modulation. Blood 122: 1793-1801.
23. Stowell, S. R., J. S. Liepkalns, J. E. Hendrickson, K. R. Girard-Pierce, N. H. Smith, C. M. Arthur, and J. C. Zimring. 2013. Antigen modulation confers protection to red blood cells from antibody through Fcg receptor ligation. J. Immunol. 191: 5013-5025.
24. McHugh, R. S., and E.M. Shevach. 2002. Cutting edge: depletion of CD4+CD25+ regulatory T cells is necessary, but not sufficient, for induction of organ-specific autoimmune disease. J. Immunol. 168: 5979-5983.
25. Matsushita, T., M. Horikawa, Y. Iwata, and T. F. Tedder. 2010. Regulatory B cells (B10 cells) and regulatory T cells have independent roles in controlling experimental autoimmune encephalomyelitis initiation and late-phase immunopathogenesis. J. Immunol. 185: 2240-2252.
26. Cabatingan, M. S., M. R. Schmidt, R. Sen, and R. T. Woodland. 2002. Naive B lymphocytes undergo homeostatic proliferation in response to B cell deficit. J. Immunol. 169: 6795-6805.
27. Lan, Y. Y., Z. Wang, G. Raimondi, W. Wu, B. L. Colvin, A. de Creus, and A. W. Thomson. 2006. "Alternatively activated" dendritic cells preferentially secrete IL-10, expand Foxp3+CD4+ T cells, and induce long-term organ allograft survival in combination with CTLA4-Ig. J. Immunol. 177: 5868-5877.
28. Ren, X., K. Akiyoshi, S. Dziennis, A. A. Vandenbark, P. S. Herson, P. D. Hurn, and H. Offner. 2011. Regulatory B cells limit CNS inflammation and neurologic deficits in murine experimental stroke. J. Neurosci. 31: 8556-8563.
29. Mizoguchi, A., E. Mizoguchi, H. Takedatsu, R. S. Blumberg, and A. K. Bhan. 2002. Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity 16: 219-230.
30. Mizoguchi, E., A. Mizoguchi, F. I. Preffer, and A. K. Bhan. 2000. Regulatory role of mature B cells in a murine model of inflammatory bowel disease. Int. Immunol. 12: 597-605.
31. Baumgarth, N., G. C. Jager, O. C. Herman, and L. A. Herzenberg. 2000. CD4+ T cells derived from B cell-deficient mice inhibit the establishment of peripheral B cell pools. Proc. Natl. Acad. Sci. USA 97: 4766-4771.
32. Tedder, T. F. 2015. B10 cells: a functionally defined regulatory B cell subset. J. Immunol. 194: 1395-1401.
33. Yanaba, K., J. D. Bouaziz, K. M. Haas, J. C. Poe, M. Fujimoto, and T. F. Tedder. 2008. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 28: 639-650.
34. Maynard, C. L., L. E. Harrington, K. M. Janowski, J. R. Oliver, C. L. Zindl, A. Y. Rudensky, and C. T. Weaver. 2007. Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp32 precursor cells in the absence of interleukin 10. Nat. Immunol. 8: 931-941.
35. Vieira, P. L., J. R. Christensen, S. Minaee, E. J. O'Neill, F. J. Barrat, A. Boonstra, T. Barthlott, B. Stockinger, D. C. Wraith, and A. O'Garra. 2004. IL-10-secreting regulatory T cells do not express Foxp3 but have comparable regulatory function to naturally occurring CD4+CD25+ regulatory T cells. J. Immunol. 172: 5986-5993.
36. Smith, N. H., E. A. Hod, S. L. Spitalnik, J. C. Zimring, and J. E. Hendrickson. 2012. Transfusion in the absence of inflammation induces antigen-specific tolerance to murine RBCs. Blood 119: 1566-1569.
37. Alexopoulou, L., A. C. Holt, R. Medzhitov, and R. A. Flavell. 2001. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413: 732-738.
38. Hendrickson, J. E., M. Desmarets, S. S. Deshpande, T. E. Chadwick, C. D. Hillyer, J. D. Roback, and J. C. Zimring. 2006. Recipient inflammation affects the frequency and magnitude of immunization to transfused red blood cells. Transfusion 46: 1526-1536.
39. Rawlings, D. J., M. A. Schwartz, S. W. Jackson, and A. Meyer-Bahlburg. 2012. Integration of B cell responses through Toll-like receptors and antigen receptors. Nat. Rev. Immunol. 12: 282-294.
40. Vanderlugt, C. L., and S. D. Miller. 2002. Epitope spreading in immune-mediated diseases: implications for immunotherapy. Nat. Rev. Immunol. 2: 85-95.
41. Mauri, C., and A. Bosma. 2012. Immune regulatory function of B cells. Annu. Rev. Immunol. 30: 221-241.
42. Hori, S., T. Nomura, and S. Sakaguchi. 2003. Control of regulatory T cell development by the transcription factor Foxp3. Science 299: 1057-1061.
43. Mauri, C., D. Gray, N. Mushtaq, and M. Londei. 2003. Prevention of arthritis by interleukin 10-producing B cells. J. Exp. Med. 197: 489-501.
44. Toscano, M. A., A. G. Commodaro, J. M. Ilarregui, G. A. Bianco, A. Liberman, H. M. Serra, J. Hirabayashi, L. V. Rizzo, and G. A. Rabinovich. 2006. Galectin-1 suppresses autoimmune retinal disease by promoting concomitant Th2- and T regulatory-mediated anti-inflammatory responses. J. Immunol. 176: 6323-6332.
45. Gauld, S. B., J. M. Dal Porto, and J. C. Cambier. 2002. B cell antigen receptor signaling: roles in cell development and disease. Science 296: 1641-1642.
46. Brinc, D., H. Le-Tien, A. R. Crow, V. Siragam, J. Freedman, and A. H. Lazarus. 2008. Transfusion of IgG-opsonized foreign red blood cells mediates reduction of antigen-specific B cell priming in a murine model. J. Immunol. 181: 948-953.
47. Noizat-Pirenne, F., C. Tournamille, P. Bierling, F. Roudot-Thoraval, P. Y. Le Pennec, P. Rouger, and H. Ansart-Pirenne. 2006. Relative immunogenicity of Fya and K antigens in a Caucasian population, based on HLA class II restriction analysis. Transfusion 46: 1328-1333.
48. Reviron, D., I. Dettori, V. Ferrera, D. Legrand, M. Touinssi, P. Mercier, P. de Micco, and J. Chiaroni. 2005. HLA-DRB1 alleles and Jk(a) immunization. Transfusion 45: 956-959.
49. Brantley, S. G., and G. Ramsey. 1988. Red cell alloimmunization in multitransfused HLA-typed patients. Transfusion 28: 463-466.
50. Fasano, R. M., G. S. Booth, M. Miles, L. Du, T. Koyama, E. R. Meier, and N. L. Luban. 2015. Red blood cell alloimmunization is influenced by recipient inflammatory state at time of transfusion in patients with sickle cell disease. Br. J. Haematol. 168: 291-300.
51. Bernardo, L., G. A. Denomme, K. Shah, and A. H. Lazarus. 2014. RhD specific antibodies are not detectable in HLA-DRB1(∗)1501 mice challenged with human RhD positive erythrocytes. Adv. Hematol. 2014: 470242.
52. Scornik, J. C., J. S. Bromberg, D. J. Norman, M. Bhanderi,M. Gitlin, and J. Petersen. 2013. An update on the impact of pre-transplant transfusions and allosensitization on time to renal transplant and on allograft survival. BMC Nephrol. 14: 217.
53. Daniels, G. 2013. Variants of RhD-current testing and clinical consequences. Br. J. Haematol. 161: 461-470.
54. Flegel, W. A., S. R. Khull, and F. F. Wagner. 2000. Primary anti-D immunization by weak D type 2 RBCs. Transfusion 40: 428-434.
55. Gassner, C., A. Doescher, T. D. Drnovsek, P. Rozman, N. I. Eicher, T. J. Legler, S. Lukin, H. Garritsen, T. Kleinrath, B. Egger, et al. 2005. Presence of RHD in serologically D2, C/E+ individuals: a European multicenter study. Transfusion 45: 527-538.
56. Rosse, W. F., D. Gallagher, T. R. Kinney, O. Castro, H. Dosik, J. Moohr, W. Wang, and P. S. Levy, The Cooperative Study of Sickle Cell Disease. 1990. Transfusion and alloimmunization in sickle cell disease. Blood 76: 1431-1437.
57. Seyfried, H., and I. Walewska. 1990. Analysis of immune response to red blood cell antigens in multitransfused patients with different diseases. Mater. Med. Pol. 22: 21-25.
58. Bachmann, M. F., U. H. Rohrer, T. M. Kündig, K. Bürki, H. Hengartner, and R. M. Zinkernagel. 1993. The influence of antigen organization on B cell responsiveness. Science 262: 1448-1451.
59. Batista, F. D., and M. S. Neuberger. 1998. Affinity dependence of the B cell response to antigen: a threshold, a ceiling, and the importance of off-rate. Immunity 8: 751-759.
60. Goodnow, C. C. 1996. Balancing immunity and tolerance: deleting and tuning lymphocyte repertoires. Proc. Natl. Acad. Sci. USA 93: 2264-2271.
61. Donjerković, D., and D. W. Scott. 2000. Activation-induced cell death in B lymphocytes. Cell Res. 10: 179-192.
62. Yarkoni, Y., A. Getahun, and J. C. Cambier. 2010. Molecular underpinning of B-cell anergy. Immunol. Rev. 237: 249-263.
63. Russell, D. M., Z. Dembić, G. Morahan, J. F. Miller, K. Bürki, and D. Nemazee. 1991. Peripheral deletion of self-reactive B cells. Nature 354: 308-311.
64. Ji, P., M. Murata-Hori, and H. F. Lodish. 2011. Formation of mammalian erythrocytes: chromatin condensation and enucleation. Trends Cell Biol. 21: 409-415.
65. Muir, A. R., and D. N. Kerr. 1958. Erythropoiesis: an electron microscopical study. Q. J. Exp. Physiol. Cogn. Med. Sci. 43: 106-114.
66. Steck, T. L. 1974. The organization of proteins in the human red blood cell membrane. A review. J. Cell Biol. 62: 1-19.
67. Moini, M., M. L. Schilsky, and E. M. Tichy. 2015. Review on immunosuppression in liver transplantation. World J. Hepatol. 7: 1355-1368.
68. Fishman, J. A. 2007. Infection in solid-organ transplant recipients. N. Engl. J. Med. 357: 2601-2614.
69. Kunisaki, K.M., and E. N. Janoff. 2009. Influenza in immunosuppressed populations: a review of infection frequency, morbidity, mortality, and vaccine responses. Lancet Infect. Dis. 9: 493-504.
70. Kang, I., and S. H. Park. 2003. Infectious complications in SLE after immunosuppressive therapies. Curr. Opin. Rheumatol. 15: 528-534.
71. Villanueva, C., A. Colomo, A. Bosch, M. Concepción, V. Hernandez-Gea, C. Aracil, I. Graupera, M. Poca, C. Alvarez-Urturi, J. Gordillo, et al. 2013. Transfusion strategies for acute upper gastrointestinal bleeding. N. Engl. J. Med. 368: 11-21.
72. Lacroix, J., P. C. Hébert, D. A. Fergusson, A. Tinmouth, D. J. Cook, J. C. Marshall, L. Clayton, L. McIntyre, J. Callum, A. F. Turgeon, et al; ABLE Investigators; Canadian Critical Care Trials Group. 2015. Age of transfused blood in critically ill adults. N. Engl. J. Med. 372: 1410-1418.