Donor colonic CD103+ dendritic cells determine the severity of acute graft-versus-host disease

Journal of Experimental Medicine

Volumn 212, Issue 8, 2015, Pages 1303-1321

  Koyama, Motoko ^a   Cheong, Melody ^a   Markey, Kate A ^a   Gartlan, Kate H ^a   Kuns, Rachel D ^a   Locke, Kelly R ^a   Lineburg, Katie E ^a   Teal, Bianca E ^a   Leveque El Mouttie, Lucie ^a   Bunting, Mark D ^a   Vuckovic, Slavica ^a   Zhang, Ping ^a   Teng, Michele W L ^a   Varelias, Antiopi ^a   Tey, Siok Keen ^a,d   Wockner, Leesa F ^a   Engwerda, Christian R ^a   Smyth, Mark J ^a   Belz, Gabrielle T ^b   McColl, Shaun R ^c   MacDonald, Kelli P A ^a   Hill, Geoffrey R ^a,d   more..

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

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

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; ALPHA E INTEGRINS; ALPHA INTEGRIN; CCR7 PROTEIN, HUMAN; CHEMOKINE RECEPTOR CCR7; IMMUNOGLOBULIN RECEPTOR; INTERLEUKIN 12; INTERLEUKIN 6; LEUKOCYTE ANTIGEN;

ANALYSIS OF VARIANCE; ANIMAL; BAGG ALBINO MOUSE; CELL MOTION; COLON; CYTOLOGY; DENDRITIC CELL; FLOW CYTOMETRY; GRAFT VERSUS HOST REACTION; IMMUNOLOGY; LYMPH NODE; METABOLISM; MOUSE; PATHOPHYSIOLOGY; T LYMPHOCYTE; TRANSGENIC MOUSE;

ADVANCED GLYCOSYLATION END PRODUCT-SPECIFIC RECEPTOR; ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD; CELL MOVEMENT; COLON; DENDRITIC CELLS; FLOW CYTOMETRY; GRAFT VS HOST DISEASE; INTEGRIN ALPHA CHAINS; INTERLEUKIN-12; INTERLEUKIN-6; LYMPH NODES; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; RECEPTORS, CCR7; RECEPTORS, IMMUNOLOGIC; T-LYMPHOCYTES;

EID: 84964697658     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20150329     Document Type: Article

References (62)

1. Alexander, K.A., R. Flynn, K.E. Lineburg, R.D. Kuns, B.E.Teal, S.D. Olver, M. Lor, N.C. Raffelt, M. Koyama, L. Leveque, et al. 2014. CSF-1-dependent donor-derived macrophages mediate chronic graft-versus-host disease. J. Clin. Invest. 124:4266-4280. http://dx.doi.org/10.1172/JCI75935
2. Anderson, B.E., J.M. McNiff, D. Jain, B.R. Blazar, W.D. Shlomchik, and M.J. Shlomchik. 2005. 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. http://dx.doi.org/10.1182/blood-2004-08-3032
3. Auffray, C., M.H. Sieweke, and F. Geissmann. 2009. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 27:669-692. http://dx.doi.org/10.1146/annurev.immunol.021908.132557
4. Banovic, T., K.P. MacDonald, E.S. Morris, V. Rowe, R. Kuns, A. Don, J. Kelly, S. Ledbetter, A.D. Clouston, and G.R. Hill. 2005. TGF-β in allogeneic stem cell transplantation: friend or foe? Blood. 106:2206-2214. http://dx.doi.org/10.1182/blood-2005-01-0062
5. Blazar, B.R., W.J. Murphy, and M. Abedi. 2012. Advances in graft-versus-host disease biology and therapy. Nat. Rev. Immunol. 12:443-458. http://dx.doi.org/10.1038/nri3212
6. Bogunovic, M., F. Ginhoux, J. Helft, L. Shang, D. Hashimoto, M. Greter, K. Liu, C. Jakubzick, M.A. Ingersoll, M. Leboeuf, et al. 2009. Origin of the lamina propria dendritic cell network. Immunity. 31:513-525. http://dx.doi.org/10.1016/j.immuni.2009.08.010
7. Bouillet, P., J.F. Purton, D.I. Godfrey, L.C. Zhang, L. Coultas, H. Puthalakath, M. Pellegrini, S. Cory, J.M. Adams, and A. Strasser. 2002. BH3-only Bcl-2 family member Bim is required for apoptosis of autoreactive thymocytes. Nature. 415:922-926. http://dx.doi.org/10.1038/415922a
8. Bunting, M.D., I. Comerford, N. Seach, M.V. Hammett, D.L. Asquith, H. Körner, R.L. Boyd, R.J. Nibbs, and S.R. McColl. 2013. CCX-CKR deficiency alters thymic stroma impairing thymocyte development and promoting autoimmunity. Blood. 121:118-128. http://dx.doi.org/10.1182/blood-2012-06-434886
9. Chakraverty, R., and M. Sykes. 2007. The role of antigen-presenting cells in triggering graft-versus-host disease and graft-versus-leukemia. Blood. 110:9-17. http://dx.doi.org/10.1182/blood-2006-12-022038
10. Chen, X., R. Das, R. Komorowski, A. Beres, M.J. Hessner, M. Mihara, and W.R. Drobyski. 2009. Blockade of interleukin-6 signaling augments regulatory T-cell reconstitution and attenuates the severity of graft-versus-hostdisease.Blood.114:891-900.http://dx.doi.org/10.1182/blood-2009-01-197178
11. Chen, Y., E.M. Akirav, W. Chen, O. Henegariu, B. Moser, D. Desai, J.M. Shen, J.C. Webster, R.C. Andrews, A.M. Mjalli, et al. 2008. RAGE ligation affects T cell activation and controls T cell differentiation. J. Immunol.. 181:4272-4278. http://dx.doi.org/10.4049/jimmunol.181.6.4272
12. Cochran, W.G., and G.M. Cox. 1957. Experimental Designs. Second edition. Wiley, New York. 617 pp.
13. Cooke, K.R., G.R. Hill, J.M. Crawford, D. Bungard, Y. Brinson, J. Delmonte, and J.L.M. Ferrara. 1998. Tumor necrosis factor-α production to lipopolysaccharide stimulation by donor cells predicts the severity of experimental acute graft-versus-host disease. J. Clin. Invest. 102:1882-1891. http://dx.doi.org/10.1172/JCI4285
14. Cretney, E., A. Xin, W. Shi, M. Minnich, F. Masson, M. Miasari, G.T. Belz, G.K. Smyth, M. Busslinger, S.L. Nutt, and A. Kallies. 2011. The transcription factors Blimp-1 and IRF4 jointly control the differentiation and function of effector regulatory T cells. Nat. Immunol. 12:304-311. http://dx.doi.org/10.1038/ni.2006
15. Domínguez, P.M., and C. Ardavín. 2010. Differentiation and function of mouse monocyte-derived dendritic cells in steady state and inflammation. Immunol. Rev. 234:90-104. http://dx.doi.org/10.1111/j.01052896.2009.00876.x
16. Ferrara, J.L., J.E. Levine, P. Reddy, and E. Holler. 2009. Graft-versus-host disease. Lancet. 373:1550-1561. http://dx.doi.org/10.1016/S0140-6736(09)60237-3
17. + dendritic cells in the small intestine expresses TLR3, TLR7, and TLR9 and induces Th1 response and CTL activity. J. Immunol. 186:6287-6295. http://dx.doi.org/10.4049/jimmunol.1004036
18. Gooley, T.A., J.W. Chien, S.A. Pergam, S. Hingorani, M.L. Sorror, M. Boeckh, P.J. Martin, B.M. Sandmaier, K.A. Marr, F.R. Appelbaum, et al. 2010. Reduced mortality after allogeneic hematopoietic-cell transplantation. N. Engl. J. Med. 363:2091-2101. http://dx.doi.org/10.1056/ NEJMoa1004383
19. Hashimoto, D., A. Chow, M. Greter, Y. Saenger, W.H. Kwan, M. Leboeuf, F. Ginhoux, J.C. Ochando, Y. Kunisaki, N. van Rooijen, et al. 2011. Pretransplant CSF-1 therapy expands recipient macrophages and ameliorates GVHD after allogeneic hematopoietic cell transplantation. J. Exp. Med. 208:1069-1082. http://dx.doi.org/10.1084/jem.20101709
20. Heidegger, S., M.R. van den Brink, T. Haas, and H. Poeck. 2014. The role of pattern-recognition receptors in graft-versus-host disease and graft-versus-leukemia after allogeneic stem cell transplantation. Front. Immunol. 5:337. http://dx.doi.org/10.3389/fimmu.2014.00337
21. Henden, A.S., and G.R. Hill. 2015. Cytokines in Graft-versus-Host Disease. J. Immunol. 194:4604-4612. http://dx.doi.org/10.4049/jimmunol.1500117
22. Hill, G.R., J.M. Crawford, K.R. Cooke, Y.S. Brinson, L. Pan, and J.L.M. Ferrara. 1997. Total body irradiation and acute graft-versus-host disease: the role of gastrointestinal damage and inflammatory cytokines. Blood. 90:3204-3213.
23. Hirano, T. 1998. Interleukin 6 and its receptor: ten years later. Int. Rev. Immunol. 16:249-284. http://dx.doi.org/10.3109/08830189809042997
24. Joffre, O.P., E. Segura, A. Savina, and S. Amigorena. 2012. Cross-presentation by dendritic cells. Nat. Rev. Immunol. 12:557-569. http://dx.doi.org/10.1038/nri3254
25. + dendritic cells in the regulation of tissue-selective T cell homing. J. Exp. Med. 202:1063-1073. http://dx.doi.org/10.1084/jem.20051100
26. Kennedy, G.A., A. Varelias, S. Vuckovic, L. Le Texier, K.H. Gartlan, P. Zhang, G. Thomas, L. Anderson, G. Boyle, N. Cloonan, et al. 2014. Addition of interleukin-6 inhibition with tocilizumab to standard graft-versus-host disease prophylaxis after allogeneic stem-cell transplantation: a phase 1/2 trial. Lancet Oncol. 15:1451-1459. http://dx.doi.org/10.1016/S1470-2045(14)71017-4
27. Kondo, T., T. Kawai, and S. Akira. 2012. Dissecting negative regulation of Toll-like receptor signaling. Trends Immunol. 33:449-458. http://dx.doi.org/10.1016/j.it.2012.05.002
28. Koyama, M., R.D. Kuns, S.D. Olver, N.C. Raffelt, Y.A. Wilson, A.L. Don, K.E. Lineburg, M. Cheong, R.J. Robb, K.A. Markey, et al. 2012. Recipient nonhematopoietic antigen-presenting cells are sufficient to induce lethal acute graft-versus-host disease. Nat. Med. 18:135-142. http://dx.doi.org/10.1038/nm.2597
29. Li, H., C. Matte-Martone, H.S. Tan, S. Venkatesan, J. McNiff, A.J. Demetris, D. Jain, F. Lakkis, D. Rothstein, and W.D. Shlomchik. 2011. Graft-versus-host disease is independent of innate signaling pathways triggered by pathogens in host hematopoietic cells. J. Immunol. 186:230-241. http://dx.doi.org/10.4049/jimmunol.1002965
30. MacDonald, K.P., R.D. Kuns, V. Rowe, E.S. Morris, T. Banovic, H. Bofinger, B. O'Sullivan, K.A. Markey, A.L. Don, R. Thomas, and G.R. Hill. 2007. Effector and regulatory T-cell function is differentially regulated by RelB within antigen-presenting cells during GVHD. Blood. 109:5049-5057. http://dx.doi.org/10.1182/blood-2007-01-067249
31. MacDonald, K.P., J.S. Palmer, S. Cronau, E. Seppanen, S. Olver, N.C. Raffelt, R. Kuns, A.R. Pettit, A. Clouston, B. Wainwright, et al. 2010. 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. http://dx.doi.org/10.1182/blood-2010-02-266296
32. - subclasses of dendritic cells direct the development of distinct T helper cells in vivo. J. Exp. Med. 189:587-592. http:// dx.doi.org/10.1084/jem.189.3.587
33. Markey, K.A., T. Banovic, R.D. Kuns, S.D. Olver, A.L. Don, N.C. Raffelt, Y.A. Wilson, L.J. Raggatt, A.R. Pettit, J.S. Bromberg, et al. 2009. Conventional dendritic cells are the critical donor APC presenting alloantigen after experimental bone marrow transplantation. Blood. 113:5644-5649. http://dx.doi.org/10.1182/blood-2008-12-191833
34. Markey, K.A., A.C. Burman, T. Banovic, R.D. Kuns, N.C. Raffelt,V. Rowe, S.D. Olver, A.L. Don, E.S. Morris, A.R. Pettit, et al. 2010. Soluble lymphotoxin is an important effector molecule in GVHD and GVL. Blood. 115:122-132. http://dx.doi.org/10.1182/blood-2009-01-199927
35. Markey, K.A., M. Koyama, R.D. Kuns, K.E. Lineburg,Y.A.Wilson, S.D. Olver, N.C. Raffelt, A.L. Don, A.Varelias, R.J. Robb, et al. 2012. Immune insufficiency during GVHD is due to defective antigen presentation within dendritic cell subsets. Blood. 119:5918-5930. http://dx.doi.org/10.1182/blood-2011-12-398164
36. Markey, K.A., K.P. MacDonald, and G.R. Hill. 2014. The biology of graft-versus-host disease: experimental systems instructing clinical practice. Blood. 124:354-362. http://dx.doi.org/10.1182/blood-2014-02-514745
37. Massberg, S., P. Schaerli, I. Knezevic-Maramica, M. Köllnberger, N. Tubo, E.A. Moseman, I.V. Huff, T. Junt, A.J. Wagers, I.B. Mazo, and U.H. von Andrian. 2007. Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell. 131:994-1008. http://dx.doi.org/10.1016/j.cell.2007.09.047
38. Matte, C.C., J. Liu, J. Cormier, B.E. Anderson, I. Athanasiadis, D. Jain, J. McNiff, and W.D. Shlomchik. 2004. Donor APCs are required for maximal GVHD but not for GVL. Nat. Med. 10:987-992. http://dx.doi.org/10.1038/nm1089
39. Merad, M., P. Sathe, J. Helft, J. Miller, and A. Mortha. 2013.The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu. Rev. Immunol. 31:563-604. http://dx.doi.org/10.1146/annurev-immunol-020711-074950
40. Mittrücker, H.W., T. Matsuyama, A. Grossman, T.M. Kündig, J. Potter, A. Shahinian, A. Wakeham, B. Patterson, P.S. Ohashi, and T.W. Mak. 1997. Requirement for the transcription factor LSIRF/IRF4 for mature B and T lymphocyte function. Science. 275:540-543. http://dx.doi.org/10.1126/science.275.5299.540
41. Morris, E.S., K.P. MacDonald, V. Rowe, T. Banovic, R.D. Kuns, A.L. Don, H.M. Bofinger, A.C. Burman, S.D. Olver, N. Kienzle, et al. 2005. NKT cell-dependent leukemia eradication following stem cell mobilization with potent G-CSF analogs. J. Clin. Invest. 115:3093-3103. http://dx.doi.org/10.1172/JCI25249
42. Nagai, Y., K.P. Garrett, S. Ohta, U. Bahrun, T. Kouro, S. Akira, K. Takatsu, and P.W. Kincade. 2006. Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity. 24:801-812. http://dx.doi.org/10.1016/j.immuni.2006.04.008
43. Nishimura, R., J. Baker, A. Beilhack, R. Zeiser, J.A. Olson, E.I. Sega, M. Karimi, and R.S. Negrin. 2008. In vivo trafficking and survival of cytokine-induced killer cells resulting in minimal GVHD with retention of antitumor activity. Blood. 112:2563-2574. http://dx.doi.org/10.1182/blood-2007-06-092817
44. Ochando, J.C., C. Homma, Y. Yang, A. Hidalgo, A. Garin, F. Tacke, V. Angeli, Y. Li, P. Boros, Y. Ding, et al. 2006. Alloantigen-presenting plasmacytoid dendritic cells mediate tolerance to vascularized grafts. Nat. Immunol. 7:652-662. http://dx.doi.org/10.1038/ni1333
45. + dendritic cells drive mucosal T helper 17 cell differentiation. Immunity. 38:958-969. http://dx.doi.org/10.1016/j.immuni.2013.03.009
46. Reddy, P., T. Teshima, M. Kukuruga, R. Ordemann, C. Liu, K. Lowler, and J.L. Ferrara. 2001. Interleukin-18 regulates acute graft-versus-host disease by enhancing Fas-mediated donor T cell apoptosis. J. Exp. Med. 194:1433-1440. http://dx.doi.org/10.1084/jem.194.10.1433
47. Saleh, M., and G. Trinchieri. 2011. Innate immune mechanisms of colitis and colitis-associated colorectal cancer. Nat. Rev. Immunol. 11:9-20. http://dx.doi.org/10.1038/nri2891
48. Schlitzer, A., N. McGovern, P. Teo, T. Zelante, K. Atarashi, D. Low, A.W. Ho, P. See, A. Shin, P.S. Wasan, et al. 2013. IRF4 transcription factor-dependent CD11b+ dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity. 38:970-983. http:// dx.doi.org/10.1016/j.immuni.2013.04.011
49. Shlomchik, W.D., M.S. Couzens, C.B. Tang, J. McNiff, M.E. Robert, J. Liu, M.J. Shlomchik, and S.G. Emerson. 1999. Prevention of graft versus host disease by inactivation of host antigen-presenting cells. Science. 285:412-415. http://dx.doi.org/10.1126/science.285.5426.412
50. + dendritic cell subset. Immunol. Rev. 234:18-31. http://dx.doi.org/10.1111/j.0105-2896.2009.00870.x
51. Stagg, A.J., M.A. Kamm, and S.C. Knight. 2002. Intestinal dendritic cells increase T cell expression of α4β7 integrin. Eur. J. Immunol. 32:1445-1454. http://dx.doi.org/10.1002/1521-4141(200205)32:5<1445::AIDIMMU1445>3.0.CO;2-E
52. Tamoutounour, S., S. Henri, H. Lelouard, B. de Bovis, C. de Haar, C.J. van der Woude, A.M. Woltman, Y. Reyal, D. Bonnet, D. Sichien, et al. 2012. CD64 distinguishes macrophages from dendritic cells in the gut and reveals the Th1-inducing role of mesenteric lymph node macrophages during colitis. Eur. J. Immunol. 42:3150-3166. http://dx.doi.org/10.1002/eji.201242847
53. Tawara, I., M. Koyama, C. Liu, T. Toubai, D. Thomas, R. Evers, P. Chockley, E. Nieves, Y. Sun, K.P. Lowler, et al. 2011. Interleukin-6 modulates graft-versus-host responses after experimental allogeneic bone marrow transplantation. Clin. Cancer Res. 17:77-88. http://dx.doi.org/10.1158/1078-0432.CCR-10-1198
54. Teshima, T., R. Ordemann, P. Reddy, S. Gagin, C. Liu, K.R. Cooke, and J.L. Ferrara. 2002. Acute graft-versus-host disease does not require alloantigen expression on host epithelium. Nat. Med. 8:575-581. http://dx.doi.org/10.1038/nm0602-575
55. Tittel, A.P., C. Heuser, C. Ohliger, C. Llanto, S. Yona, G.J. Hämmerling, D.R. Engel, N. Garbi, and C. Kurts. 2012. Functionally relevant neutrophilia in CD11c diphtheria toxin receptor transgenic mice. Nat. Methods. 9:385-390. http://dx.doi.org/10.1038/nmeth.1905
56. Toubai, T., I. Tawara, Y. Sun, C. Liu, E. Nieves, R. Evers, T. Friedman, R. Korngold, and P. Reddy. 2012. Induction of acute GVHD by sex-mismatched H-Y antigens in the absence of functional radiosensitive host hematopoietic-derived antigen-presenting cells. Blood. 119:3844-3853. http://dx.doi.org/10.1182/blood-2011-10-384057
57. Tsou, C.L., W. Peters, Y. Si, S. Slaymaker, A.M. Aslanian, S.P. Weisberg, M. Mack, and I.F. Charo. 2007. Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J. Clin. Invest. 117:902-909. http://dx.doi.org/10.1172/ JCI29919
58. Varelias, A., K.H. Gartlan, E. Kreijveld, S.D. Olver, M. Lor, R.D. Kuns, K.E. Lineburg, B.E. Teal, N.C. Raffelt, M. Cheong, et al. 2015. Lung parenchyma-derived IL-6 promotes IL-17A-dependent acute lung injury after allogeneic stem cell transplantation. Blood. 125:2435-2444. http://dx.doi.org/10.1182/blood-2014-07-590232
59. Varol, C., A.Vallon-Eberhard, E. Elinav, T. Aychek,Y. Shapira, H. Luche, H.J. Fehling,W.D. Hardt, G. Shakhar, and S. Jung. 2009. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity. 31:502-512. http://dx.doi.org/10.1016/j.immuni.2009.06.025
60. Weisdorf, D., M.J. Zhang, M. Arora, M.M. Horowitz, J.D. Rizzo, and M. Eapen. 2012. Graft-versus-host disease induced graft-versus-leukemia effect: greater impact on relapse and disease-free survival after reduced intensity conditioning. Biol. Blood Marrow Transplant. 18:1727-1733. http://dx.doi.org/10.1016/j.bbmt.2012.06.014
61. Yamamoto, M., S. Sato, H. Hemmi, K. Hoshino, T. Kaisho, H. Sanjo, O.Takeuchi, M. Sugiyama, M. Okabe, K.Takeda, and S.Akira. 2003. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science. 301:640-643. http://dx.doi.org/10.1126/science.1087262
62. Zhang, Y., J.P. Louboutin, J. Zhu, A.J. Rivera, and S.G. Emerson. 2002. Preterminal host dendritic cells in irradiated mice prime CD8+ T cell-mediated acute graft-versus-host disease. J. Clin. Invest. 109:1335-1344. http://dx.doi.org/10.1172/JCI0214989