Donor-specific indirect pathway analysis reveals a B-cell-independent signature which reflects outcomes in kidney transplant recipients

American Journal of Transplantation

Volumn 12, Issue 3, 2012, Pages 640-648

  Haynes, L D ^a   Jankowska Gan, E ^a   Sheka, A ^a   Keller, M R ^a   Hernandez Fuentes, M P ^b   Lechler, R I ^b   Seyfert Margolis, V ^c   Turka, L A ^d,f   Newell, K A ^e   Burlingham, W J ^a  

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

^b KING'S COLLEGE LONDON   (United Kingdom)

^c CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e EMORY UNIVERSITY   (United States)

^f Immune Tolerance Network   (United States)

Author keywords

DTH assay; human; immunological monitoring; indirect pathway; renal transplantation; transplant tolerance

Indexed keywords

ALLOANTIGEN; BIOLOGICAL MARKER; PREDNISONE;

ARTICLE; B LYMPHOCYTE; BLOOD SAMPLING; CHRONIC GRAFT REJECTION; CLINICAL ARTICLE; CLINICAL ASSESSMENT; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DELAYED HYPERSENSITIVITY; EFFECTOR CELL; GRAFT RECIPIENT; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; IMMUNOSUPPRESSIVE TREATMENT; KIDNEY DONOR; KIDNEY TRANSPLANTATION; MONOTHERAPY; MONOZYGOTIC TWINS; OUTCOME ASSESSMENT; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; STEROID THERAPY;

B-LYMPHOCYTES; GRAFT REJECTION; HUMANS; IMMUNE TOLERANCE; IMMUNOSUPPRESSION; KIDNEY TRANSPLANTATION; PROGNOSIS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TISSUE DONORS;

EID: 84857653996     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2011.03869.x     Document Type: Article

References (32)

1. VanBuskirk AM, Burlingham WJ, Jankowska-Gan E, et al,. Human allograft acceptance is associated with immune regulation. J Clin Invest 2000; 106: 145-155. (Pubitemid 30437250)
2. Lafferty KJ, Babcock SK, Gill RG,. Prevention of rejection by treatment of the graft: An overview. Prog Clin Biol Res 1986; 224: 87-117.
3. Torrealba JR, Katayama M, Fechner JH Jr., et al,. Metastable tolerance to rhesus monkey renal transplants is correlated with allograft TGF-beta 1+CD4+ T regulatory cell infiltrates. J Immunol 2004; 172: 5753-5764. (Pubitemid 38542081)
4. Xu Q, Lee J, Jankowska-Gan E, et al,. Human CD4+CD25low adaptive T regulatory cells suppress delayed-type hypersensitivity during transplant tolerance. J Immunol 2007; 178: 3983-3995. (Pubitemid 46417669)
5. Burlingham WJ, Love RB, Jankowska-Gan E, et al,. IL-17-dependent cellular immunity to collagen type V predisposes to obliterative bronchiolitis in human lung transplants. J Clin Invest 2007; 117: 3498-3506. (Pubitemid 350097005)
6. Cai J, Lee J, Jankowska-Gan E, et al,. Minor H antigen HA-1-specific regulator and effector CD8+ T cells, and HA-1 microchimerism, in allograft tolerance. J Exp Med 2004; 199: 1017-1023. (Pubitemid 38481093)
7. Iwata Y, Matsushita T, Horikawa M, et al,. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood 2011; 117: 530-541.
8. Wang C, Cordoba S, Hu M, et al,. Spontaneous acceptance of mouse kidney allografts is associated with increased Foxp3 expression and differences in the B and T cell compartments. Transpl Immunol 2011; 24: 149-156.
9. Le Texier L, Thebault P, Lavault A, et al,. Long-term allograft tolerance is characterized by the accumulation of B cells exhibiting an inhibited profile. Am J Transplant 2011; 11: 429-438.
10. Newell KA, Asare A, Kirk AD, et al,. Identification of a B cell signature associated with renal transplant tolerance in humans. J Clin Invest 2010; 120: 1836-1847.
11. Sagoo P, Perucha E, Sawitzki B, et al,. Development of a cross-platform biomarker signature to detect renal transplant tolerance in humans. J Clin Invest 2010; 120: 1848-1861.
12. Pallier A, Hillion S, Danger R, et al,. Patients with drug-free long-term graft function display increased numbers of peripheral B cells with a memory and inhibitory phenotype. Kidney Int 2010; 78: 503-513.
13. Burlingham WJ, Jankowska-Gan E,. Mouse strain and injection site are crucial for detecting linked suppression in transplant recipients by trans-vivo DTH assay. Am J Transplant 2007; 7: 466-470. (Pubitemid 46096342)
14. Hegde S, Jankowska-Gan E, Roenneburg DA, Torrealba J, Burlingham WJ, Gumperz JE,. Human NKT cells promote monocyte differentiation into suppressive myeloid antigen-presenting cells. J Leukoc Biol 2009; 86: 757-768.
15. VanBuskirk AM, Wakely ME, Sirak JH, Orosz CG,. Patterns of allosensitization in allograft recipients: Long-term cardiac allograft acceptance is associated with active alloantibody production in conjunction with active inhibition of alloreactive delayed-type hypersensitivity. Transplantation 1998; 65: 1115-1123. (Pubitemid 28208431)
16. Xu Q, Lee J, Keller M, Burlingham WJ,. Analysis of indirect pathway CD4+ T cells in a patient with metastable tolerance to a kidney allograft: Possible relevance to superior graft survival of HLA class II closely matched renal allografts. Transpl Immunol 2009; 20: 203-208.
17. Yamada A, Chandraker A, Laufer TM, Gerth AJ, Sayegh MH, Auchincloss H Jr., Recipient MHC class II expression is required to achieve long-term survival of murine cardiac allografts after costimulatory blockade. J Immunol 2001; 167: 5522-5526. (Pubitemid 33062737)
18. Kishimoto K, Yuan X, Auchincloss H Jr., Sharpe AH, Mandelbrot DA, Sayegh MH,. Mechanism of action of donor-specific transfusion in inducing tolerance: Role of donor MHC molecules, donor co-stimulatory molecules, and indirect antigen presentation. J Am Soc Nephrol 2004; 15: 2423-2428. (Pubitemid 39159342)
19. Steele DJ, Laufer TM, Smiley ST, et al,. Two levels of help for B cell alloantibody production. J Exp Med 1996 183: 699-703. (Pubitemid 26059527)
20. Burlingham WJ, Fechner JH, DeVito LD, Sollinger HW, Knechtle SJ, Grailer AP,. Human interleukin-2 and lymphoproliferative (T-helper cell) responses to soluble HLA class I antigens in vitro: I. Specificity for polymorphic domains. Tissue Antigens 1993; 42: 35-38. (Pubitemid 23272645)
21. Poggio ED, Clemente M, Riley J, et al,. Alloreactivity in renal transplant recipients with and without chronic allograft nephropathy. J Am Soc Nephrol 2004; 15: 1952-1960. (Pubitemid 38822077)
22. Niederkorn JY, Streilein JW,. Alloantigens placed into the anterior chamber of the eye induce specific suppression of delayed-type hypersensitivity but normal cytotoxic T lymphocyte and helper T lymphocyte responses. J Immunol 1983; 131: 2670-2674. (Pubitemid 14208812)
23. Warnecke G, Chapman SJ, Bushell A, Hernandez-Fuentes M, Wood KJ,. Dependency of the trans vivo delayed type hypersensitivity response on the action of regulatory T cells: Implications for monitoring transplant tolerance. Transplantation 2007; 84: 392-399. (Pubitemid 47258329)
24. Molitor-Dart ML, Andrassy J, Kwun J, et al,. Developmental exposure to noninherited maternal antigens induces CD4+ T regulatory cells: Relevance to mechanism of heart allograft tolerance. J Immunol 2007; 179: 6749-6761.
25. Cook CH, Bickerstaff AA, Wang JJ, et al,. Spontaneous renal allograft acceptance associated with "regulatory" dendritic cells and IDO. J Immunol 2008; 180: 3103-3112.
26. Jankowska-Gan E, Sollinger HW, Pirsch JD, et al,. Successful reduction of immunosuppression in older renal transplant recipients who exhibit donor-specific regulation. Transplantation 2009; 88: 533-541.
27. Callaghan CJ, Rouhani FJ, Negus MC, et al,. Abrogation of antibody-mediated allograft rejection by regulatory CD4 T cells with indirect allospecificity. J Immunol 2007; 178: 2221-2228. (Pubitemid 46233420)
28. Jankowska-Gan E, Rhein T, Haynes LD, et al,. Human liver allograft acceptance and the "tolerance assay". II. Donor HLA-A, -B but not DR antigens are able to trigger regulation of DTH. Hum Immunol 2002; 63: 862-870. (Pubitemid 35246766)
29. DiLillo DJ, Griffiths R, Seshan SV, et al,. B lymphocytes differentially influence acute and chronic allograft rejection in mice. J Immunol 2011; 186: 2643-2654.
30. Zarkhin V, Chalasani G, Sarwal MM,. The yin and yang of B cells in graft rejection and tolerance. Transplant Rev (Orlando) 2010; 24: 67-78.
31. Martinez-Llordella M, Lozano JJ, Puig-Pey I, et al,. Using transcriptional profiling to develop a diagnostic test of operational tolerance in liver transplant recipients. J Clin Invest 2008; 118: 2845-2857.
32. Matzinger P, Kamala T,. Tissue-based class control: The other side of tolerance. Nat Rev Immunol 2011; 11: 221-230.