Host-derived CD81 dendritic cells are required for induction of optimal graft-versus-tumor responses after experimental allogeneic bone marrow transplantation

Blood

Volumn 121, Issue 20, 2013, Pages 4231-4241

  Toubai, Tomomi ^a   Sun, Yaping ^a   Luker, Gary ^b   Liu, Jun ^b   Luker, Kathryn E ^b   Tawara, Isao ^a   Evers, Rebecca ^a   Liu, Chen ^c   Mathewson, Nathan ^a   Malter, Chelsea ^a   Nieves, Evelyn ^a   Choi, Sung ^a   Murphy, Kenneth M ^d   Reddy, Pavan ^a  

^a UNIVERSITY OF MICHIGAN COMPREHENSIVE CANCER CENTER   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOANTIGEN; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CD8 ANTIGEN; GAG PROTEIN; GAMMA INTERFERON; INTERLEUKIN 17; TOLL LIKE RECEPTOR 3; TUMOR ANTIGEN;

ACUTE LEUKEMIA; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; CANCER SURVIVAL; CD8+ T LYMPHOCYTE; CELL SUBPOPULATION; CONTROLLED STUDY; CROSS PRESENTATION; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; EXPERIMENTAL LEUKEMIA; FEMALE; GASTROINTESTINAL TRACT; GRAFT VERSUS HOST REACTION; GRAFT VERSUS TUMOR EFFECT; HISTOPATHOLOGY; HLA MATCHING; HOST RESISTANCE; IMMUNOSTIMULATION; IN VIVO STUDY; LIVER GRAFT REJECTION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLONEY MURINE LEUKEMIA VIRUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; T CELL LYMPHOMA; ALLOTRANSPLANTATION; ANIMAL; BAGG ALBINO MOUSE; BONE MARROW TRANSPLANTATION; C57BL MOUSE; CELL CULTURE; DONOR; GRAFT VERSUS LEUKEMIA EFFECT; IMMUNOLOGY; LEUKEMIA; LYMPHOMA; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE; UPREGULATION;

ANIMALS; ANTIGENS, CD8; BONE MARROW TRANSPLANTATION; CELLS, CULTURED; DENDRITIC CELLS; FEMALE; GRAFT VS TUMOR EFFECT; LEUKEMIA; LYMPHOMA; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; TISSUE DONORS; TRANSPLANTATION, HOMOLOGOUS; UP-REGULATION;

MLCS; MLOWN;

EID: 84880971029     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-05-432872     Document Type: Article

References (46)

1. Appelbaum FR. Haematopoietic cell transplantation as immunotherapy. Nature. 2001; 411(6835):385-389.
2. Welniak LA, Blazar BR, Murphy WJ. Immunobiology of allogeneic hematopoietic stem cell transplantation. Annu Rev Immunol. 2007;25: 139-170.
3. Bleakley M, Riddell SR. Molecules and mechanisms of the graft-versus-leukaemia effect. Nat Rev Cancer. 2004;4(5):371-380.
4. Vincent K, Roy DC, Perreault C. Next-generation leukemia immunotherapy. Blood. 2011;118(11): 2951-2959.
5. van den Brink MR, Burakoff SJ. Cytolytic pathways in haematopoietic stem-cell transplantation. Nat Rev Immunol. 2002;2(4): 273-281.
6. Reddy P, Maeda Y, Liu C, Krijanovski OI, Korngold R, Ferrara JL. A crucial role for antigen-presenting cells and alloantigen expression in graft-versus-leukemia responses. Nat Med. 2005; 11(11):1244-1249.
7. Mapara MY, Kim YM, Wang SP, Bronson R, Sachs DH, Sykes M. Donor lymphocyte infusions mediate superior graft-versus-leukemia effects in mixed compared to fully allogeneic chimeras: a critical role for host antigen-presenting cells. Blood. 2002;100(5):1903-1909.
8. Billiau AD, Fevery S, Rutgeerts O, Landuyt W, Waer M. Crucial role of timing of donor lymphocyte infusion in generating dissociated graft-versus-host and graft-versus-leukemia responses in mice receiving allogeneic bone marrow transplants. Blood. 2002;100(5): 1894-1902.
9. Hildner K, Edelson BT, Purtha WE, et al. Batf3 deficiency reveals a critical role for CD8alpha1 dendritic cells in cytotoxic T cell immunity. Science. 2008;322(5904):1097-1100.
10. Toubai T, Tawara I, Sun Y, et al. Article I. Induction of acute GVHD by sex-mismatched H-Y antigens in the absence of functional radio-sensitive host hematopoietic-derived antigen-presenting cells. Blood. 2012;119(16):18:3844-3853.
11. Shlomchik WD, Couzens MS, Tang CB, et al. Prevention of graft versus host disease by inactivation of host antigen-presenting cells. Science. 1999;285(5426):412-415.
12. Reddy P, Sun Y, Toubai T, et al. Histone deacetylase inhibition modulates indoleamine 2,3-dioxygenase-dependent DC functions and regulates experimental graft-versus-host disease in mice. J Clin Invest. 2008;118(7):2562-2573.
13. Toubai T, Sun Y, Tawara I, et al. Ikaros-Notch axis in host hematopoietic cells regulates experimental graft-versus-host disease. Blood. 2011;118(1):192-204.
14. Teshima T, Ordemann R, Reddy P, Gagin S, Liu C, Cooke KR, Ferrara JL. Acute graft-versus-host disease does not require alloantigen expression on host epithelium. Nat Med. 2002;8(6):575-581.
15. Chen W, Qin H, Chesebro B, Cheever MA. Identification of a gag-encoded cytotoxic T-lymphocyte epitope from FBL-3 leukemia shared by Friend, Moloney, and Rauscher murine leukemia virus-induced tumors. J Virol. 1996; 70(11):7773-7782.
16. Facchinetti A, Dalla Santa S, Mezzalira S, Rosato A, Biasi G. A large number of T lymphocytes recognize Moloney-murine leukemia virus-induced antigens, but a few mediate long-lasting tumor immunosurveillance. J Immunol. 2005; 174(9):5398-5406.
17. van Hall T, van Bergen J, van Veelen PA, et al. Identification of a novel tumor-specific CTL epitope presented by RMA, EL-4, and MBL-2 lymphomas reveals their common origin. J Immunol. 2000;165(2):869-877.
18. Reddy P, Maeda Y, Hotary K, Liu C, Reznikov LL, Dinarello CA, Ferrara JL. Histone deacetylase inhibitor suberoylanilide hydroxamic acid reduces acute graft-versus-host disease and preserves graft-versus-leukemia effect. Proc Natl Acad Sci USA. 2004;101(11):3921-3926.
19. Cooke KR, Kobzik L, Martin TR, Brewer J, Delmonte J Jr, Crawford JM, Ferrara JL. An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation: I. The roles of minor H antigens and endotoxin. Blood. 1996;88(8):3230-3239.
20. Hill GR, Cooke KR, Teshima T, et al. Interleukin-11 promotes T cell polarization and prevents acute graft-versus-host disease after allogeneic bone marrow transplantation. J Clin Invest. 1998; 102(1):115-123.
21. Smith MC, Luker KE, Garbow JR, Prior JL, Jackson E, Piwnica-Worms D, Luker GD. CXCR4 regulates growth of both primary and metastatic breast cancer. Cancer Res. 2004;64(23): 8604-8612.
22. Contag CH, Jenkins D, Contag PR, Negrin RS. Use of reporter genes for optical measurements of neoplastic disease in vivo. Neoplasia. 2000; 2(1-2):41-52.
23. Duran-Struuck R, Tawara I, Lowler K, et al. A novel role for the semaphorin Sema4D in the induction of allo-responses. Biol Blood Marrow Transplant. 2007;13(11):1294-1303.
24. Satpathy AT, Murphy KM, Kc W. Transcription factor networks in dendritic cell development. Semin Immunol. 2011;23(5):388-397.
25. Mashayekhi M, Sandau MM, Dunay IR, et al. CD8a(1) dendritic cells are the critical source of interleukin-12 that controls acute infection by Toxoplasma gondii tachyzoites. Immunity. 2011; 35(2):249-259.
26. Edelson BT, Bradstreet TR, Hildner K, et al. CD8a (1) dendritic cells are an obligate cellular entry point for productive infection by Listeria monocytogenes. Immunity. 2011;35(2):236-248.
27. Chakraverty R, Sykes M. The role of antigen-presenting cells in triggering graft-versus-host disease and graft-versus-leukemia. Blood. 2007; 110(1):9-17.
28. Tussiwand R, Lee WL, Murphy TL, et al. Compensatory dendritic cell development mediated by BATF-IRF interactions. Nature. 2012;490(7421):502-507.
29. Amigorena S, Savina A. Intracellular mechanisms of antigen cross presentation in dendritic cells. Curr Opin Immunol. 2010;22(1):109-117.
30. Kurts C, Robinson BW, Knolle PA. Cross-priming in health and disease. Nat Rev Immunol. 2010; 10(6):403-414.
31. Miyake T, Kumagai Y, Kato H, et al. Poly I:C-induced activation of NK cells by CD8 alpha1 dendritic cells via the IPS-1 and TRIF-dependent pathways. J Immunol. 2009;183(4):2522-2528.
32. Schulz O, Diebold SS, Chen M, et al. Toll-like receptor 3 promotes cross-priming to virus-infected cells. Nature. 2005;433(7028):887-892.
33. Appelbaum FR. Hematopoietic-cell transplantation at 50. N Engl J Med. 2007; 357(15):1472-1475.
34. Dunn GP, Old LJ, Schreiber RD. The immunobiology of cancer immunosurveillance and immunoediting. Immunity. 2004;21(2):137-148.
35. Fuertes MB, Kacha AK, Kline J, Woo SR, Kranz DM, Murphy KM, Gajewski TF. Host type I IFN signals are required for antitumor CD81 T cell responses through CD8alpha1 dendritic cells. J Exp Med. 2011;208(10):2005-2016.
36. Lauterbach H, Bathke B, Gilles S, et al. Mouse CD8alpha1 DCs and human BDCA31 DCs are major producers of IFN-lambda in response to poly IC. J Exp Med. 2010;207(12):2703-2717.
37. Poulin LF, Salio M, Griessinger E, et al. Characterization of human DNGR-11 BDCA31 leukocytes as putative equivalents of mouse CD8alpha1 dendritic cells. J Exp Med. 2010; 207(6):1261-1271.
38. Bachem A, Güttler S, Hartung E, et al. Superior antigen cross-presentation and XCR1 expression define human CD11c1CD1411 cells as homologues of mouse CD81 dendritic cells. J Exp Med. 2010;207(6):1273-1281.
39. Crozat K, Guiton R, Contreras V, et al. The XC chemokine receptor 1 is a conserved selective marker of mammalian cells homologous to mouse CD8alpha1 dendritic cells. J Exp Med. 2010; 207(6):1283-1292.
40. Jongbloed SL, Kassianos AJ, McDonald KJ, et al. Human CD1411 (BDCA-3)1 dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J Exp Med. 2010; 207(6):1247-1260.
41. Edwards AD, Diebold SS, Slack EM, et al. Toll-like receptor expression in murine DC subsets: lack of TLR7 expression by CD8 alpha1 DC correlates with unresponsiveness to imidazoquinolines. Eur J Immunol. 2003;33(4): 827-833.
42. Merad M, Hoffmann P, Ranheim E, et al. Depletion of host Langerhans cells before transplantation of donor alloreactive T cells prevents skin graft-versus-host disease. Nat Med. 2004;10(5):510-517.
43. Reddy P, Negrin R, Hill GR. Mouse models of bone marrow transplantation. Biol Blood Marrow Transplant. 2008;14(1 Suppl 1):129-135.
44. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646-674.
45. Koyama M, Kuns RD, Olver SD, et al. Recipient nonhematopoietic antigen-presenting cells are sufficient to induce lethal acute graft-versus-host disease. Nat Med. 2011;18(1):135-142.
46. Li H, Demetris AJ, McNiff J, et al. Profound depletion of host conventional dendritic cells, plasmacytoid dendritic cells, and B cells does not prevent graft-versus-host disease induction. J Immunol. 2012;188(8):3804-3811.