Characterization of transfusion-elicited acute antibody-mediated rejection in a rat model of kidney transplantation

American Journal of Transplantation

Volumn 14, Issue 5, 2014, Pages 1061-1072

  Huang, G ^a,b   Wilson, N A ^a   Reese, S R ^a   Jacobson, L M ^a   Zhong, W ^a   Djamali, A ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

Animal model; antibody mediated rejection; C4d; donor specific antibody; phenotype; transfusion

Indexed keywords

CD3 ANTIGEN; CHLORDANE; COMPLEMENT COMPONENT C4D; GAMMA INTERFERON; IMMUNOGLOBULIN; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN G2C; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERFERON REGULATORY FACTOR 5; INTERLEUKIN 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; UNCLASSIFIED DRUG; ALLOANTIBODY; COMPLEMENT C4D; COMPLEMENT COMPONENT C4B; CYTOKINE; MESSENGER RNA; PEPTIDE FRAGMENT;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY MEDIATED REJECTION; ARTICLE; BLOOD DONOR; BLOOD TRANSFUSION; CAPILLARITIS; CONTROLLED STUDY; GLOMERULITIS; HISTOPATHOLOGY; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; KIDNEY ALLOGRAFT; KIDNEY FUNCTION; MACROPHAGE; MALE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; RAT; SPLEEN CELL; UPREGULATION; ADVERSE EFFECTS; ALLOTRANSPLANTATION; ANIMAL; BROWN NORWAY RAT; DISEASE MODEL; DONOR; GENETICS; GRAFT REJECTION; HUMAN; IMMUNOLOGY; KIDNEY TRANSPLANTATION; LEWIS RAT; METABOLISM; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; BLOOD TRANSFUSION; BLOTTING, WESTERN; COMPLEMENT C4B; CYTOKINES; DISEASE MODELS, ANIMAL; GRAFT REJECTION; HUMANS; INFLAMMATION; ISOANTIBODIES; KIDNEY TRANSPLANTATION; MALE; PEPTIDE FRAGMENTS; RATS; RATS, INBRED BN; RATS, INBRED LEW; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TISSUE DONORS; TRANSPLANTATION, HOMOLOGOUS;

EID: 84899439959     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.12674     Document Type: Article

References (54)

1. Wiebe C, Gibson IW, Blydt-Hansen TD, et al. Evolution and clinical pathologic correlations of de novo donor-specific HLA antibody post kidney transplant. Am J Transplant 2012; 12: 1157-1167.
2. Djamali A, Kaufman DB, Ellis TM, Zhong W, Matas A, Samaniego M., Diagnosis and management of antibody-mediated rejection: Current status and novel approaches. Am J Transplant 2014; 14: 255-271.
3. El-Zoghby ZM, Stegall MD, Lager DJ, et al. Identifying specific causes of kidney allograft loss. Am J Transplant 2009; 9: 527-535.
4. Sellares J, de Freitas DG, Mengel M, et al. Understanding the causes of kidney transplant failure: The dominant role of antibody-mediated rejection and nonadherence. Am J Transplant 2012; 12: 388-399.
5. Halloran PF, Wadgymar A, Ritchie S, Falk J, Solez K, Srinivasa NS., The significance of the anti-class I antibody response. I. Clinical and pathologic features of anti-class I-mediated rejection. Transplantation 1990; 49: 85-91.
6. Halloran PF, Schlaut J, Solez K, Srinivasa NS., The significance of the anti-class I response. II. Clinical and pathologic features of renal transplants with anti-class I-like antibody. Transplantation 1992; 53: 550-555.
7. Feucht HE, Schneeberger H, Hillebrand G, et al. Capillary deposition of C4d complement fragment and early renal graft loss. Kidney Int 1993; 43: 1333-1338.
8. Mauiyyedi S, Pelle PD, Saidman S, et al. Chronic humoral rejection: Identification of antibody-mediated chronic renal allograft rejection by C4d deposits in peritubular capillaries. J Am Soc Nephrol 2001; 12: 574-582.
9. Sis B, Mengel M, Haas M, et al. Banff '09 meeting report: Antibody mediated graft deterioration and implementation of Banff Working Groups. Am J Transplant 2010; 10: 464-471.
10. Haas M, Sis B, Racusen L, et al. Banff 2013 meeting report: Findings of Banff working groups and inclusion of C4d-negative antibody-mediated rejection. Am J Transplant 2014; 14: 272-283.
11. Farkash EA, Colvin RB., Diagnostic challenges in chronic antibody-mediated rejection. Nat Rev Nephrol 2012; 8: 255-257.
12. Hidalgo LG, Sis B, Sellares J, et al. NK cell transcripts and NK cells in kidney biopsies from patients with donor-specific antibodies: Evidence for NK cell involvement in antibody-mediated rejection. Am J Transplant 2010; 10: 1812-1822.
13. Sis B, Halloran PF., Endothelial transcripts uncover a previously unknown phenotype: C4d-negative antibody-mediated rejection. Curr Opin Organ Transplant 2010; 15: 42-48.
14. Jane-Wit D, Manes TD, Yi T, et al. Alloantibody and complement promote T cell-mediated cardiac allograft vasculopathy through non-canonical NF-kappaB signaling in endothelial cells. Circulation 2013; 128: 2504-2516.
15. Mannon R., Macrophages: Contributors to allograft dysfunction, repair, or innocent bystanders ? Curr Opin Organ Transplant 2012; 17: 20-25.
16. Lefaucheur C, Nochy D, Hill G, et al. Determinants of poor graft outcome in patients with antibody-mediated acute rejection. Am J Transplant 2007; 7: 832-841.
17. Mannon RB., Macrophages: Contributors to allograft dysfunction, repair, or innocent bystanders ? Curr Opin Organ Transplant 2012; 17: 20-25.
18. Cao Q, Wang Y, Harris DC., Pathogenic and protective role of macrophages in kidney disease. Am J Physiol Renal Physiol 2013; 305: F3-F11.
19. Archdeacon P, Chan M, Neuland C, et al. Summary of FDA antibody-mediated rejection workshop. Am J Transplant 2011; 11: 896-906.
20. Djamali A, Vidyasagar A, Adulla M, Hullett D, Reese S., Nox-2 is a modulator of fibrogenesis in kidney allografts. Am J Transplant 2009; 9: 74-82.
21. Djamali A, Reese S, Yracheta J, Oberley T, Hullett D, Becker B., Epithelial-to-mesenchymal transition and oxidative stress in chronic allograft nephropathy. Am J Transplant 2005; 5: 500-509.
22. Djamali A, Reese S, Oberley T, Hullett D, Becker B., Heat shock protein 27 in chronic allograft nephropathy: A local stress response. Transplantation 2005; 79: 1645-1657.
23. Djamali A, Muth BL, Ellis TM, et al. Increased C4d in post-reperfusion biopsies and increased donor specific antibodies at one-week post transplant are risk factors for acute rejection in mild to moderately sensitized kidney transplant recipients. Kidney Int 2013; 83: 1185-1192.
24. Niederhaus SV, Muth B, Lorentzen DF, et al. Luminex-based desensitization protocols: The University of Wisconsin initial experience. Transplantation 2011; 1: 12-17.
25. Sicard A, Phares TW, Yu H, et al. The spleen is the major source of antidonor antibody-secreting cells in murine heart allograft recipients. Am J Transplant 2012; 12: 1708-1719.
26. Hattori Y, Bucy RP, Kubota Y, Baldwin WM III, Fairchild RL., Antibody-mediated rejection of single class I MHC-disparate cardiac allografts. Am J Transplant 2012; 12: 2017-2028.
27. Minami K, Murata K, Lee C, et al. C4d deposition and clearance in cardiac transplants correlates with alloantibody levels and rejection in rats. Am J Transplant 2006; 6: 923-932.
28. Qian Z, Lee C, Murata K, et al. Antibody and complement mediated injury in transplants following sensitization by allogeneic blood transfusion. Transplantation 2006; 82: 857-864.
29. Mengel M, Sis B, Haas M, et al. Banff 2011 meeting report: New concepts in antibody-mediated rejection. Am J Transplant 2012; 12: 563-570.
30. Sis B, Mengel M, Haas M, et al. Banff '09 meeting report: Antibody mediated graft deterioration and implementation of Banff working groups. Am J Transplant 2010; 10: 464-471.
31. Swanlund JM, Kregel KC, Oberley TD., Investigating autophagy: Quantitative morphometric analysis using electron microscopy. Autophagy 2010; 6: 270-277.
32. Vidyasagar A, Reese S, Acun Z, Hullett D, Djamali A., HSP27 is involved in the pathogenesis of kidney tubulointerstitial fibrosis. Am J Physiol Renal Physiol 2008; 295: F707-F716.
33. Krausgruber T, Blazek K, Smallie T, et al. IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses. Nat Immunol 2011; 12: 231-238.
34. Djamali A, Reese S, Hafez O, et al. Nox2 is a mediator of chronic CsA nephrotoxicity. Am J Transplant 2012; 12: 1997-2997.
35. Mason JC, Yarwood H, Sugars K, Morgan BP, Davies KA, Haskard DO., Induction of decay-accelerating factor by cytokines or the membrane-attack complex protects vascular endothelial cells against complement deposition. Blood 1999; 94: 1673-1682.
36. Kohei N, Tanabe T, Horita S, et al. Sequential analysis of donor-specific antibodies and pathological findings in acute antibody-mediated rejection in a rat renal transplantation model. Kidney Int 2013; 84: 722-732.
37. Toyoda M, Ge S, Pao A, et al. Cellular allo reactivity against paternal HLA antigens in normal multiparous females as detected by intracellular cytokine flow cytometry remains elevated over years despite diminution of anti-HLA antibody levels. Transpl Immunol 2010; 23: 133-140.
38. Opelz G, Terasaki PI., Improvement of kidney-graft survival with increased numbers of blood transfusions. N Engl J Med 1978; 299: 799-803.
39. Salvatierra O Jr, Vincenti F, Amend W, et al. Deliberate donor-specific blood transfusions prior to living related renal transplantation. A new approach. Ann Surg 1980; 192: 543-552.
40. Sollinger HW, Kalayoglu M, Belzer FO., Use of the donor specific transfusion protocol in living-unrelated donor-recipient combinations. Ann Surg 1986; 204: 315-321.
41. Burlingham WJ, Grailer A, Sparks-Mackety EM, Sondel PM, Sollinger HW., Improved renal allograft survival following donor-specific transfusions. II. In vitro correlates of early (DST-type) rejection episodes. Transplantation 1987; 43: 41-46.
42. Brunson ME, Alexander JW., Mechanisms of transfusion-induced immunosuppression. Transfusion 1990; 30: 651-658.
43. Ibrahim H, Skeans M, Li Q, Ishani A, Snyder J., Blood transfusions in kidney transplant candidates are common and associated with adverse outcomes. Clin Transplant 2011; 25: 653-659.
44. Murata K, Baldwin WM III., Mechanisms of complement activation, C4d deposition, and their contribution to the pathogenesis of antibody-mediated rejection. Transplant Rev (Orlando) 2009; 23: 139-150.
45. Akiyoshi T, Hirohashi T, Alessandrini A, et al. Role of complement and NK cells in antibody mediated rejection. Hum Immunol 2012; 73: 1226-1232.
46. Kaneku H, O'Leary J, Taniguchi M, Susskind B, Terasaki P, Klintmalm G., Donor-specific human leukocyte antigen antibodies of the immunoglobulin G3 subclass are associated with chronic rejection and graft loss after liver transplantation. Liver Transpl 2012; 18: 984-992.
47. Lee C, Lotfi-Emran S, Erdinc M, et al. The involvement of FcR mechanisms in antibody-mediated rejection. Transplantation 2007; 84: 1324-1334.
48. Murata K, Fox-Talbot K, Qian Z, et al. Synergistic deposition of C4d by complement-activating and non-activating antibodies in cardiac transplants. Am J Transplant 2007; 7: 2605-2614.
49. Rahimi S, Qian Z, Layton J, Fox-Talbot K, Baldwin WM III, Wasowska B., Non-complement- and complement-activating antibodies synergize to cause rejection of cardiac allografts. Am J Transplant 2004; 4: 326-334.
50. Baldwin WM III, Pruitt S, Brauer R, Daha M, Sanfilippo F., Complement in organ transplantation. Contributions to inflammation, injury, and rejection. Transplantation 1995; 59: 797-808.
51. Hidalgo LG, Campbell PM, Sis B, et al. De novo donor-specific antibody at the time of kidney transplant biopsy associates with microvascular pathology and late graft failure. Am J Transplant 2009; 9: 2532-2541.
52. Sis B, Jhangri GS, Riopel J, et al. A new diagnostic algorithm for antibody-mediated microcirculation inflammation in kidney transplants. Am J Transplant 2012; 12: 1168-1179.
53. Magil A, Tinckam K., Monocytes and peritubular capillary C4d deposition in acute renal allograft rejection. Kidney Int 2003; 63: 1888-1893.
54. Baldwin WM III, Halushka M, Valujskikh A, Fairchild R., B cells in cardiac transplants: From clinical questions to experimental models. Semin Immunol 2012; 24: 122-130. Kidney Diseases