Polyreactive antibodies developing amidst humoral rejection of human kidney grafts bind apoptotic cells and activate complement

American Journal of Transplantation

Volumn 13, Issue 10, 2013, Pages 2590-2600

  Porcheray, F ^a   Fraser, J W ^a   Gao, B ^a,b   McColl, A ^a   Devito, J ^a   Dargon, I ^a   Helou, Y ^a   Wong, W ^a   Girouard, T C ^a   Saidman, S L ^a   Colvin, R B ^a   Palmisano, A ^c   Maggiore, U ^c   Vaglio, A ^c   Smith, R N ^a   Zorn, E ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

^c UNIVERSITY HOSPITAL OF PARMA   (Italy)

Author keywords

Antibody mediated rejection; apoptosis; C4d; polyreactive antibodies

Indexed keywords

COMPLEMENT COMPONENT C3D; COMPLEMENT COMPONENT C4D; IMMUNOGLOBULIN G; MONOCLONAL ANTIBODY; THYMOCYTE ANTIBODY;

ADULT; AGED; ANTIBODY MEDIATED REJECTION; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; APOPTOSIS; ARTICLE; B LYMPHOCYTE; BLOOD SAMPLING; CELL STRAIN HEK293; CLINICAL ARTICLE; COMPLEMENT ACTIVATION; CONTROLLED STUDY; CROSS REACTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; FOCAL GLOMERULOSCLEROSIS; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATORY CELL; KIDNEY BIOPSY; KIDNEY GRAFT; KIDNEY GRAFT REJECTION; LEUKEMIA CELL LINE; LYMPHOCYTE CLONE; MALE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; TARGET CELL; WESTERN BLOTTING;

ANTIBODY-MEDIATED REJECTION; APOPTOSIS; C4D; POLYREACTIVE ANTIBODIES;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; APOPTOSIS; AUTOANTIBODIES; BLOTTING, WESTERN; CASE-CONTROL STUDIES; COMPLEMENT ACTIVATION; COMPLEMENT C4B; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GRAFT REJECTION; HUMANS; IMMUNITY, HUMORAL; IMMUNOGLOBULIN G; KIDNEY TRANSPLANTATION; MIDDLE AGED; PEPTIDE FRAGMENTS; TRANSPLANTATION, HOMOLOGOUS; YOUNG ADULT;

EID: 84884910756     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.12394     Document Type: Article

References (34)

1. Pascual M, Theruvath T, Kawai T, Tolkoff-Rubin N, Cosimi AB., Strategies to improve long-term outcomes after renal transplantation. N Engl J Med 2002; 346: 580-590.
2. 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.
3. Forman JP, Lin J, Pascual M, Denton MD, Tolkoff-Rubin N., Significance of anticardiolipin antibodies on short and long term allograft survival and function following kidney transplantation. Am J Transplant 2004; 4: 1786-1791.
4. 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.
5. Jurcevic S, Ainsworth ME, Pomerance A, et al. Antivimentin antibodies are an independent predictor of transplant-associated coronary artery disease after cardiac transplantation. Transplantation 2001; 71: 886-892.
6. 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.
7. Porcheray F, DeVito J, Yeap BY, et al. Chronic humoral rejection of human kidney allografts associates with broad autoantibody responses. Transplantation 89: 1239-1246.
8. 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.
9. 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.
10. 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 12: 2088-2097.
11. Pierangeli SS, Harris EN., A protocol for determination of anticardiolipin antibodies by ELISA. Nat Protoc 2008; 3: 840-848.
12. Notkins AL., Polyreactivity of antibody molecules. Trends Immunol 2004; 25: 174-179.
13. Avrameas S., Natural autoantibodies: From 'horror autotoxicus' to 'gnothi seauton.' Immunol Today 1991; 12: 154-159.
14. Casali P, Schettino EW., Structure and function of natural antibodies. Curr Top Microbiol Immunol 1996; 210: 167-179.
15. 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.
16. Colvin RB., Antibody-mediated renal allograft rejection: Diagnosis and pathogenesis. J Am Soc Nephrol 2007; 18: 1046-1056.
17. Kim SJ, Gershov D, Ma X, Brot N, Elkon KB., I-PLA(2) activation during apoptosis promotes the exposure of membrane lysophosphatidylcholine leading to binding by natural immunoglobulin M antibodies and complement activation. J Exp Med 2002; 196: 655-665.
18. Ikematsu H, Kasaian MT, Schettino EW, Casali P., Structural analysis of the VH-D-JH segments of human polyreactive IgG mAb. Evidence for somatic selection. J Immunol 1993; 151: 3604-3616.
19. Zhou ZH, Tzioufas AG, Notkins AL., Properties and function of polyreactive antibodies and polyreactive antigen-binding B cells. J Autoimmun 2007; 29: 219-228.
20. 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.
21. Gronwall C, Akhter E, Oh C, Burlingame RW, Petri M, Silverman GJ., IgM autoantibodies to distinct apoptosis-associated antigens correlate with protection from cardiovascular events and renal disease in patients with SLE. Clin Immunol (Orlando, FL.) 142: 390-398.
22. Gronwall C, Vas J, Silverman GJ., Protective roles of natural IgM antibodies. Front Immunol 3: 66.
23. Silverman GJ., Regulatory natural autoantibodies to apoptotic cells: Pallbearers and protectors. Arthritis Rheum 63: 597-602.
24. 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.
25. Kabelitz D., Apoptosis graft rejection, and transplantation tolerance. Transplantation 1998; 65: 869-875.
26. Laine J, Etelamaki P, Holmberg C, Dunkel L., Apoptotic cell death in human chronic renal allograft rejection. Transplantation 1997; 63: 101-105.
27. Noronha IL, Oliveira SG, Tavares TS, et al. Apoptosis in kidney and pancreas allograft biopsies. Transplantation 2005; 79: 1231-1235.
28. Shimizu A, Yamada K, Sachs DH, Colvin RB., Intragraft events preceding chronic renal allograft rejection in a modified tolerance protocol. Kidney Int 2000; 58: 2546-2558.
29. 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. Epub 2013/02/26.
30. Mevorach D, Zhou JL, Song X, Elkon KB., Systemic exposure to irradiated apoptotic cells induces autoantibody production. J Exp Med 1998; 188: 387-392.
31. Haidar F, Kisserli A, Tabary T, et al. Comparison of C4d detection on erythrocytes and PTC-C4d to histological signs of antibody-mediated rejection in kidney transplantation. Am J Transplant 12: 1564-1575.
32. Liu CC, Manzi S, Kao AH, Navratil JS, Ruffing MJ, Ahearn JM., Reticulocytes bearing C4d as biomarkers of disease activity for systemic lupus erythematosus. Arthritis Rheum 2005; 52: 3087-3099.
33. Manzi S, Navratil JS, Ruffing MJ, et al. Measurement of erythrocyte C4d and complement receptor 1 in systemic lupus erythematosus. Arthritis Rheum 2004; 50: 3596-3604.
34. Singh V, Mahoney JA, Petri M., Erythrocyte C4d and complement receptor 1 in systemic lupus erythematosus. J Rheumatol 2008; 35: 1989-1993. Diseases