Recipient nonhematopoietic antigen-presenting cells are sufficient to induce lethal acute graft-versus-host disease

Nature Medicine

Volumn 18, Issue 1, 2012, Pages 135-142

  Koyama, Motoko ^a   Kuns, Rachel D ^a   Olver, Stuart D ^a   Raffelt, Neil C ^a   Wilson, Yana A ^a   Don, Alistair L J ^a   Lineburg, Katie E ^a   Cheong, Melody ^a   Robb, Renee J ^a   Markey, Kate A ^a   Varelias, Antiopi ^a   Malissen, Bernard ^b   Hämmerling, Günter J ^c   Clouston, Andrew D ^d   Engwerda, Christian R ^a   Bhat, Purnima ^e   MacDonald, Kelli P A ^a   Hill, Geoffrey R ^a,f  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d Envoi Pathology   (Australia)

^e UNIVERSITY OF QUEENSLAND   (Australia)

^f ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ACUTE GRAFT VERSUS HOST DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; BONE MARROW TRANSPLANTATION; CELL DIFFERENTIATION; CELL EXPANSION; DENDRITIC CELL; FEMALE; GASTROINTESTINAL TRACT; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; WHOLE BODY RADIATION;

ANIMALS; ANTIGEN PRESENTATION; ANTIGEN-PRESENTING CELLS; BONE MARROW TRANSPLANTATION; CD4-POSITIVE T-LYMPHOCYTES; CYTOKINES; DENDRITIC CELLS; GRAFT VS HOST DISEASE; HEMATOPOIETIC SYSTEM; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; TRANSPLANT DONOR SITE; TRANSPLANTATION, HOMOLOGOUS;

MUS;

EID: 84855546719     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.2597     Document Type: Article

References (41)

1. Shlomchik, W.D. et al. Prevention of graft versus host disease by inactivation of host antigen-presenting cells. Science 285, 412-415 (1999). (Pubitemid 29343964)
2. Matte, C.C. et al. Donor APCs are required for maximal GVHD but not for GVL. Nat. Med. 10, 987-992 (2004). (Pubitemid 39273741)
3. Teshima, T. et al. Acute graft-versus-host disease does not require alloantigen expression on host epithelium. Nat. Med. 8, 575-581 (2002). (Pubitemid 34633434)
4. Anderson, B.E. et al. Distinct roles for donor-and host-derived antigen-presenting cells and costimulatory molecules in murine chronic graft-versus-host disease: requirements depend on target organ. Blood 105, 2227-2234 (2005). (Pubitemid 40731817)
5. Markey, K.A. et al. Conventional dendritic cells are the critical donor APC presenting alloantigen after experimental bone marrow transplantation. Blood 113, 5644-5649 (2009).
6. MacDonald, K.P. et al. Effector and regulatory T-cell function is differentially regulated by RelB within antigen-presenting cells during GVHD. Blood 109, 5049-5057 (2007). (Pubitemid 46827805)
7. Zhang, Y., Louboutin, J.P., Zhu, J., Rivera, A.J. & Emerson, S.G. Preterminal host dendritic cells in irradiated mice prime CD8+ T cell-mediated acute graft-versus-host disease. J. Clin. Invest. 109, 1335-1344 (2002). (Pubitemid 34546898)
8. Duffner, U.A. et al. Host dendritic cells alone are sufficient to initiate acute graftversus-host disease. J. Immunol. 172, 7393-7398 (2004). (Pubitemid 38747600)
9. Koyama, M. et al. Plasmacytoid dendritic cells prime alloreactive T cells to mediate graft-versus-host disease as antigen-presenting cells. Blood 113, 2088-2095 (2009).
10. Rowe, V. et al. Host B cells produce IL-10 following TBI and attenuate aGVHD after allogeneic bone marrow transplantation. Blood 108, 2485-2492 (2006). (Pubitemid 44497537)
11. Matte-Martone, C. et al. Recipient B cells are not required for graft-versus-host disease induction. Biol. Blood Marrow Transplant. 16, 1222-1230 (2010).
12. MacDonald, K.P. et al. An antibody against the colony-stimulating factor 1 receptor depletes the resident subset of monocytes and tissue-and tumor-associated macrophages but does not inhibit inflammation. Blood 116, 3955-3963 (2010).
13. Li, H. et al. Langerhans cells are not required for graft-versus-host disease. Blood 117, 697-707 (2011).
14. Ochando, J.C. et al. Alloantigen-presenting plasmacytoid dendritic cells mediate tolerance to vascularized grafts. Nat. Immunol. 7, 652-662 (2006). (Pubitemid 43797347)
15. Morris, E.S. et al. Induction of natural killer T cell-dependent alloreactivity by administration of granulocyte colony-stimulating factor after bone marrow transplantation. Nat. Med. 15, 436-441 (2009).
16. Hochweller, K., Striegler, J., Hammerling, G.J. & Garbi, N. A novel CD11c.DTR transgenic mouse for depletion of dendritic cells reveals their requirement for homeostatic proliferation of natural killer cells. Eur. J. Immunol. 38, 2776-2783 (2008).
17. Jung, S. et al. In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8(+) T cells by exogenous cell-associated antigens. Immunity 17, 211-220 (2002). (Pubitemid 35245963)
18. Pinchuk, I.V. et al. PD-1 ligand expression by human colonic myofibroblasts/fibroblasts regulates CD4+ T-cell activity. Gastroenterology 135, 1228-1237 (2008).
19. Saada, J.I. et al. Subepithelial myofibroblasts are novel nonprofessional APCs in the human colonic mucosa. J. Immunol. 177, 5968-5979 (2006). (Pubitemid 44628810)
20. Jones, S.C., Murphy, G.F., Friedman, T.M. & Korngold, R. Importance of minor histocompatibility antigen expression by nonhematopoietic tissues in a CD4+ T cellmediated graft-versus-host disease model. J. Clin. Invest. 112, 1880-1886 (2003). (Pubitemid 38063711)
21. Sandner, S.E. et al. Mechanisms of tolerance induced by donor-specific transfusion and ICOS-B7h blockade in a model of CD4+ T-cell-mediated allograft rejection. Am. J. Transplant. 5, 31-39 (2005). (Pubitemid 40095125)
22. Wang, H., Wu, X., Wang, Y., Oldenborg, P.A. & Yang, Y.G. CD47 is required for suppression of allograft rejection by donor-specific transfusion. J. Immunol. 184, 3401-3407 (2010).
23. Anderson, B.E. et al. Memory CD4+ T cells do not induce graft-versus-host disease. J. Clin. Invest. 112, 101-108 (2003). (Pubitemid 38056381)
24. Chen, B.J., Cui, X., Sempowski, G.D., Liu, C. & Chao, N.J. Transfer of allogeneic CD62L-memory T cells without graft-versus-host disease. Blood 103, 1534-1541 (2004). (Pubitemid 38168675)
25. Beilhack, A. et al. In vivo analyses of early events in acute graft-versus-host disease reveal sequential infiltration of T-cell subsets. Blood 106, 1113-1122 (2005). (Pubitemid 41076462)
26. Beilhack, A. et al. Prevention of acute graft-versus-host disease by blocking T-cell entry to secondary lymphoid organs. Blood 111, 2919-2928 (2008).
27. Anderson, B.E. et al. Effects of donor T-cell trafficking and priming site on graftversus-host disease induction by naive and memory phenotype CD4 T cells. Blood 111, 5242-5251 (2008).
28. Juchem, K.W. et al. A repertoire-independent and cell intrinsic defect in murine GVHD induction by effector memory T cells. Blood published online, doi:10.1182/blood-2011-01-330035 (18 July 2011).
29. Chen, B.J. et al. Inability of memory T cells to induce graft-versus-host disease is a result of an abortive alloresponse. Blood 109, 3115-3123 (2007). (Pubitemid 46482115)
30. Kündig, T.M. et al. Fibroblasts as efficient antigen-presenting cells in lymphoid organs. Science 268, 1343-1347 (1995).
31. Powell, D.W., Pinchuk, I.V., Saada, J.I., Chen, X. & Mifflin, R.C. Mesenchymal cells of the intestinal lamina propria. Annu. Rev. Physiol. 73, 213-237 (2011).
32. Hershberg, R.M. et al. Highly polarized HLA class II antigen processing and presentation by human intestinal epithelial cells. J. Clin. Invest. 102, 792-803 (1998). (Pubitemid 28399612)
33. Hershberg, R.M. et al. Intestinal epithelial cells use two distinct pathways for HLA class II antigen processing. J. Clin. Invest. 100, 204-215 (1997). (Pubitemid 27311259)
34. Beers, C. et al. Cathepsin S controls MHC class II-mediated antigen presentation by epithelial cells in vivo. J. Immunol. 174, 1205-1212 (2005).
35. Hill, G.R. et al. Total body irradiation and acute graft versus host disease. The role of gastrointestinal damage and inflammatory cytokines. Blood 90, 3204-3213 (1997). (Pubitemid 27444217)
36. Kissenpfennig, A. et al. Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 22, 643-654 (2005). (Pubitemid 40719199)
37. Morris, E.S. et al. NKT cell-dependent leukemia eradication following stem cell mobilization with potent G-CSF analogs. J. Clin. Invest. 115, 3093-3103 (2005). (Pubitemid 41567574)
38. Markey, K.A. et al. Soluble lymphotoxin is an important effector molecule in GVHD and GVL. Blood 115, 122-132 (2010).
39. Banovic, T. et al. TGF-αin allogeneic stem cell transplantation: friend or foe? Blood 106, 2206-2214 (2005). (Pubitemid 41291742)
40. Reddy, P. et al. Interleukin-18 regulates acute graft-versus-host disease by enhancing Fas-mediated donor T cell apoptosis. J. Exp. Med. 194, 1433-1440 (2001). (Pubitemid 33081518)
41. Burman, A.C. et al. IFNαβdifferentially controls the development of idiopathic pneumonia syndrome and GVHD of the gastrointestinal tract. Blood 110, 1064-1072 (2007). (Pubitemid 47267449)