Pretransplant IgG reactivity to apoptotic cells correlates with late kidney allograft loss

American Journal of Transplantation

Volumn 14, Issue 7, 2014, Pages 1581-1591

  Gao, B ^a,b   Moore, C ^b   Porcheray, F ^b   Rong, C ^b,c   Abidoglu, C ^b   Devito, J ^b   Paine, R ^b   Girouard, T C ^b   Saidman, S L ^b   Schoenfeld, D ^b   Levin, B ^d   Wong, W ^e   Elias, N ^b   Schuetz, C ^b   Rosales, I ^b   Fu, Y ^a   Zorn, E ^b,e  

^a THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c CHANGCHUN UNIVERSITY OF CHINESE MEDICINE   (China)

^d Department of Medicine   (United States)

^e NewYork Presbyterian Hospital   (United States)

Author keywords

Anti apoptotic cell antibodies; apoptotic cells; complement; graft loss; kidney transplantation; sensitization

Indexed keywords

HLA ANTIBODY; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G3; HLA ANTIGEN CLASS 1;

ADULT; ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; CORRELATIONAL STUDY; FEMALE; HLA SYSTEM; HUMAN; JURKAT CELL LINE; KIDNEY ALLOGRAFT REJECTION; KIDNEY GRAFT; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; RECIPIENT; RISK ASSESSMENT; TREATMENT OUTCOME; ALLOGRAFT; APOPTOSIS; BLOOD; ENZYME LINKED IMMUNOSORBENT ASSAY; FOLLOW UP; GRAFT REJECTION; GRAFT SURVIVAL; IMMUNOLOGY; KIDNEY FAILURE, CHRONIC; KIDNEY TRANSPLANTATION; MIDDLE AGED; MORTALITY; PROGNOSIS; RISK FACTOR; SURVIVAL RATE;

ALLOGRAFTS; APOPTOSIS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FOLLOW-UP STUDIES; GRAFT REJECTION; GRAFT SURVIVAL; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNOGLOBULIN G; JURKAT CELLS; KIDNEY FAILURE, CHRONIC; KIDNEY TRANSPLANTATION; MALE; MIDDLE AGED; PROGNOSIS; RISK FACTORS; SURVIVAL RATE;

EID: 84903151735     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.12763     Document Type: Article

References (47)

1. Terasaki PI., Humoral theory of transplantation. Am J Transplant 2003; 3: 665-673.
2. Jordan SC, Pescovitz MD., Presensitization: The problem and its management. Clin J Am Soc Nephrol 2006; 1: 421-432.
3. Susal C, Opelz G., Kidney graft failure and presensitization against HLA class I and class II antigens. Transplantation 2002; 73: 1269-1273.
4. Susal C, Dohler B, Opelz G., Presensitized kidney graft recipients with HLA class I and II antibodies are at increased risk for graft failure: A collaborative transplant study report. Hum Immunol 2009; 70: 569-573.
5. Susal C, Dohler B, Sadeghi M, Ovens J, Opelz G., HLA antibodies and the occurrence of early adverse events in the modern era of transplantation: A collaborative transplant study report. Transplantation 2009; 87: 1367-1371.
6. Amico P, Honger G, Mayr M, Steiger J, Hopfer H, Schaub S., Clinical relevance of pretransplant donor-specific HLA antibodies detected by single-antigen flow-beads. Transplantation 2009; 87: 1681-1688.
7. Zou Y, Stastny P, Susal C, Dohler B, Opelz G., Antibodies against MICA antigens and kidney-transplant rejection. N Engl J Med 2007; 357: 1293-1300.
8. Dragun D., Humoral responses directed against non-human leukocyte antigens in solid-organ transplantation. Transplantation 2008; 86: 1019-1025.
9. Sumitran-Holgersson S., Relevance of MICA and other non-HLA antibodies in clinical transplantation. Curr Opin Immunol 2008; 20: 607-613.
10. Jackson AM, Kuperman MB, Montgomery RA., Multiple hyperacute rejections in the absence of detectable complement activation in a patient with endothelial cell reactive antibody. Am J Transplant 2012; 12: 1643-1649.
11. Crespo M, Pascual M, Tolkoff-Rubin N, et al. Acute humoral rejection in renal allograft recipients: I. Incidence, serology and clinical characteristics. Transplantation 2001; 71: 652-658.
12. Opelz G;, Collaborative Transplant Study. Non-HLA transplantation immunity revealed by lymphocytotoxic antibodies. Lancet 2005; 365: 1570-1576.
13. Solgi G, Furst D, Mytilineos J, Pourmand G, Amirzargar AA., Clinical relevance of pre and post-transplant immune markers in kidney allograft recipients: Anti-HLA and MICA antibodies and serum levels of sCD30 and sMICA. Transpl Immunol 2012; 26: 81-87.
14. Dragun D, Muller DN, Brasen JH, et al. Angiotensin II type 1-receptor activating antibodies in renal-allograft rejection. N Engl J Med 2005; 352: 558-569.
15. Kalache S, Dinavahi R, Pinney S, Mehrotra A, Cunningham MW, Heeger PS., Anticardiac myosin immunity and chronic allograft vasculopathy in heart transplant recipients. J Immunol 2011; 187: 1023-1030.
16. Joosten SA, Sijpkens YW, van Ham V, et al. Antibody response against the glomerular basement membrane protein agrin in patients with transplant glomerulopathy. Am J Transplant 2005; 5: 383-393.
17. Rose ML., Role of anti-vimentin antibodies in allograft rejection. Hum Immunol 2013; 74: 1459-1462.
18. Linke AT, Marchant B, Marsh P, Frampton G, Murphy J, Rose ML., Screening of a HUVEC cDNA library with transplant-associated coronary artery disease sera identifies RPL7 as a candidate autoantigen associated with this disease. Clin Exp Immunol 2001; 126: 173-179.
19. Porcheray F, DeVito J, Yeap BY, et al. Chronic humoral rejection of human kidney allografts associates with broad autoantibody responses. Transplantation 2010; 89: 1239-1246.
20. Warraich RS, Pomerance A, Stanley A, Banner NR, Dunn MJ, Yacoub MH., Cardiac myosin autoantibodies and acute rejection after heart transplantation in patients with dilated cardiomyopathy. Transplantation 2000; 69: 1609-1617.
21. Wheeler CH, Collins A, Dunn MJ, Crisp SJ, Yacoub MH, Rose ML., Characterization of endothelial antigens associated with transplant-associated coronary artery disease. J Heart Lung Transplant 1995; 14: S188-S197.
22. Cristol JP, Vela C, Maggi MF, Descomps B, Mourad G., Oxidative stress and lipid abnormalities in renal transplant recipients with or without chronic rejection. Transplantation 1998; 65: 1322-1328.
23. Cardinal H, Dieude M, Brassard N, et al. Antiperlecan antibodies are novel accelerators of immune-mediated vascular injury. Am J Transplant 2013; 13: 861-874.
24. Avrameas S., Natural autoantibodies: From "horror autotoxicus" to "gnothi seauton." Immunol Today 1991; 12: 154-159.
25. Ehrenstein MR, Notley CA., The importance of natural IgM: Scavenger, protector and regulator. Nat Rev Immunol 2010; 10: 778-786.
26. Fu M, Fan PS, Li W, et al. Identification of poly-reactive natural IgM antibody that recognizes late apoptotic cells and promotes phagocytosis of the cells. Apoptosis 2007; 12: 355-362.
27. Silverman GJ, Gronwall C, Vas J, Chen Y., Natural autoantibodies to apoptotic cell membranes regulate fundamental innate immune functions and suppress inflammation. Discov Med 2009; 8: 151-156.
28. Peng Y, Kowalewski R, Kim S, Elkon KB., The role of IgM antibodies in the recognition and clearance of apoptotic cells. Mol Immunol 2005; 42: 781-787.
29. Porcheray F, DeVito J, Helou Y, et al. Expansion of polyreactive B cells cross-reactive to HLA and self in the blood of a patient with kidney graft rejection. Am J Transplant 2012; 12: 2088-2097.
30. Porcheray F, Fraser JW, Gao B, et al. Polyreactive antibodies developing amidst humoral rejection of human kidney grafts bind apoptotic cells and activate complement. Am J Transplant 2013; 13: 2590-2600.
31. Bellucci R, Nguyen HN, Martin A, et al. Tyrosine kinase pathways modulate tumor susceptibility to natural killer cells. J Clin Invest 2012; 122: 2369-2383.
32. Colvin RB., Antibody-mediated renal allograft rejection: Diagnosis and pathogenesis. J Am Soc Nephrol 2007; 18: 1046-1056.
33. Stegall MD, Chedid MF, Cornell LD., The role of complement in antibody-mediated rejection in kidney transplantation. Nat Rev Nephrol 2012; 8: 670-678.
34. Fukuda M., Evaluation and clinical significance of circulating immune complexes after renal transplantation. Transplantation 1983; 36: 155-160.
35. Bohmig GA, Exner M, Habicht A, et al. Capillary C4d deposition in kidney allografts: A specific marker of alloantibody-dependent graft injury. J Am Soc Nephrol 2002; 13: 1091-1099.
36. Magil AB, Tinckam K., Monocytes and peritubular capillary C4d deposition in acute renal allograft rejection. Kidney Int 2003; 63: 1888-1893.
37. Regele H, Bohmig GA, Habicht A, et al. Capillary deposition of complement split product C4d in renal allografts is associated with basement membrane injury in peritubular and glomerular capillaries: A contribution of humoral immunity to chronic allograft rejection. J Am Soc Nephrol 2002; 13: 2371-2380.
38. Lorenz M, Regele H, Schillinger M, et al. Risk factors for capillary C4d deposition in kidney allografts: Evaluation of a large study cohort. Transplantation 2004; 78: 447-452.
39. Liu S, Cerutti A, Casali P, Crow MK., Ongoing immunoglobulin class switch DNA recombination in lupus B cells: Analysis of switch regulatory regions. Autoimmunity 2004; 37: 431-443.
40. Mietzner B, Tsuiji M, Scheid J, et al. Autoreactive IgG memory antibodies in patients with systemic lupus erythematosus arise from nonreactive and polyreactive precursors. Proc Natl Acad Sci USA 2008; 105: 9727-9732.
41. Jofre R, Rodriguez-Benitez P, Lopez-Gomez JM, Perez-Garcia R., Inflammatory syndrome in patients on hemodialysis. J Am Soc Nephrol 2006; 17: S274-S280.
42. Carrero JJ, Qureshi AR, Axelsson J, et al. Comparison of nutritional and inflammatory markers in dialysis patients with reduced appetite. Am J Clin Nutr 2007; 85: 695-701.
43. Zhang J, Jacobi AM, Wang T, Berlin R, Volpe BT, Diamond B., Polyreactive autoantibodies in systemic lupus erythematosus have pathogenic potential. J Autoimmun 2009; 33: 270-274.
44. Colvin RB, Smith RN., Antibody-mediated organ-allograft rejection. Nat Rev Immunol 2005; 5: 807-817.
45. Bruggemann M, Williams GT, Bindon CI, et al. Comparison of the effector functions of human immunoglobulins using a matched set of chimeric antibodies. J Exp Med 1987; 166: 1351-1361.
46. Michaelsen TE, Garred P, Aase A., Human IgG subclass pattern of inducing complement-mediated cytolysis depends on antigen concentration and to a lesser extent on epitope patchiness, antibody affinity and complement concentration. Eur J Immunol 1991; 21: 11-16.
47. Lucisano Valim YM, Lachmann PJ., The effect of antibody isotype and antigenic epitope density on the complement-fixing activity of immune complexes: A systematic study using chimeric anti-NIP antibodies with human Fc regions. Clin Exp Immunol 1991; 84: 1-8.