Recipient NK cell inactivation and intestinal barrier loss are required for MHC-matched graft-versus-host disease

Science Translational Medicine

Volumn 6, Issue 243, 2014, Pages

  Nalle, Sam C ^a   Kwak, H Aimee ^a   Edelblum, Karen L ^a   Joseph, Nora E ^a   Singh, Gurminder ^a   Khramtsova, Galina F ^a   Mortenson, Eric D ^a   Savage, Peter A ^a   Turner, Jerrold R ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G; MAJOR HISTOCOMPATIBILITY ANTIGEN; MYELOID DIFFERENTIATION FACTOR 88; RAG1 PROTEIN; TOLL LIKE RECEPTOR 4; DNA BINDING PROTEIN; LIPOPOLYSACCHARIDE; RAG2 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE;

ALLOGENEIC STEM CELL TRANSPLANTATION; ALLOIMMUNITY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL EXPANSION; CONTROLLED STUDY; DISEASE SEVERITY; ENGRAFTMENT; GRAFT RECIPIENT; GRAFT VERSUS HOST REACTION; HISTOPATHOLOGY; HUMAN; IMMUNOPATHOGENESIS; IMMUNOREGULATION; INTESTINAL BARRIER LOSS; INTESTINE; INTESTINE FLORA; LEUKOPENIA; LYMPHOCYTIC INFILTRATION; MISMATCH REPAIR; MOUSE; MYD88 GENE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; RAG1 GENE; SIGNAL TRANSDUCTION; SPLEEN CELL; T LYMPHOCYTE; TLR4 GENE; ANIMAL; DEFICIENCY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; MAJOR HISTOCOMPATIBILITY COMPLEX; METABOLISM; MUTANT MOUSE STRAIN;

ANIMALS; DNA-BINDING PROTEINS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GRAFT VS HOST DISEASE; KILLER CELLS, NATURAL; LIPOPOLYSACCHARIDES; MAJOR HISTOCOMPATIBILITY COMPLEX; MICE; MICE, MUTANT STRAINS; TOLL-LIKE RECEPTOR 4;

EID: 84904512053     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3008941     Document Type: Article

References (47)

1. J. R. Turner, Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol. 9, 799-809 (2009).
2. P. J. Heidt, J. M. Vossen, Experimental and clinical gnotobiotics: Influence of the microflora on graft-versus-host disease after allogeneic bone marrow transplantation. J. Med. 23, 161-173 (1992).
3. D. W. Beelen, A. Elmaagacli, K. D. Müller, H. Hirche, U. W. Schaefer, Influence of intestinal bacterial decontamination using metronidazole and ciprofloxacin or ciprofloxacin alone on the development of acute graft-versus-host disease after marrow transplantation in patients with hematologic malignancies: Final results and long-term follow-up of an open-label prospective randomized trial. Blood 93, 3267-3275 (1999).
4. W. J. van der Velden, N. M. Blijlevens, F. M. Maas, N. P. Schaap, J. H. Jansen, B. A. van der Reijden, T. Feuth, H. Dolstra, J. P. Donnelly, NOD2 polymorphisms predict severe acute graft-versus-host and treatment-related mortality in T-cell-depleted haematopoietic stem cell transplantation. Bone Marrow Transplant. 44, 243-248 (2009).
5. K. R. Cooke, A. Gerbitz, J. M. Crawford, T. Teshima, G. R. Hill, A. Tesolin, D. P. Rossignol, J. L. Ferrara, LPS antagonism reduces graft-versus-host disease and preserves graft-versus-leukemia activity after experimental bone marrow transplantation. J. Clin. Invest. 107, 1581-1589 (2001).
6. K. R. Cooke, G. R. Hill, J. M. Crawford, D. Bungard, Y. S. Brinson, J. Delmonte Jr., J. L. Ferrara, 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 (1998).
7. J. D. Down, J. C. Yanch, Identifying the high radiosensitivity of the lungs of C57L mice in a model of total-body irradiation and bone marrow transplantation. Radiat. Res. 174, 258-263 (2010).
8. E. S. Morris, K. P. MacDonald, R. D. Kuns, H. M. Morris, T. Banovic, A. L. Don, V. Rowe, Y. A. Wilson, N. C. Raffelt, C. R. Engwerda, A. C. Burman, K. A. Markey, D. I. Godfrey, M. J. Smyth, G. R. Hill, 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).
9. G. R. Hill, J. M. Crawford, K. R. Cooke, Y. S. Brinson, L. Pan, J. L. Ferrara, Total body irradiation and acute graft-versus-host disease: The role of gastrointestinal damage and inflammatory cytokines. Blood 90, 3204-3213 (1997).
10. J. E. Johansson, M. Brune, T. Ekman, The gut mucosa barrier is preserved during allogeneic, haemopoietic stem cell transplantation with reduced intensity conditioning. Bone Marrow Transplant. 28, 737-742 (2001).
11. J. E. Johansson, T. Ekman, Gut toxicity during hemopoietic stem cell transplantation may predict acute graft-versus-host disease severity in patients. Dig. Dis. Sci. 52, 2340-2345 (2007).
12. W. J. van der Velden, A. H. Herbers, T. Feuth, N. P. Schaap, J. P. Donnelly, N. M. Blijlevens, Intestinal damage determines the inflammatory response and early complications in patients receiving conditioning for a stem cell transplantation. PLOS One 5, e15156 (2010).
13. 7R. Nat. Med. 16, 1434-1438 (2010).
14. + graft-versus-host-reactive effector cells. J. Immunol. 181, 6820-6828 (2008).
15. K. Hamby, A. Trexler, T. C. Pearson, C. P. Larsen, M. R. Rigby, L. S. Kean, NK cells rapidly reject allogeneic bone marrow in the spleen through a perforin- and Ly49D-dependent, but NKG2D-independent mechanism. Am. J. Transplant. 7, 1884-1896 (2007).
16. M. Noval Rivas, M. Hazzan, K. Weatherly, F. Gaudray, I. Salmon, M. Y. Braun, NK cell regulation of CD4 T cell-mediated graft-versus-host disease. J. Immunol. 184, 6790-6798 (2010).
17. Y. Yan, V. Kolachala, G. Dalmasso, H. Nguyen, H. Laroui, S. V. Sitaraman, D. Merlin, Temporal and spatial analysis of clinical and molecular parameters in dextran sodium sulfate induced colitis. PLOS One 4, e6073 (2009).
18. S. L. Brown, T. E. Riehl, M. R. Walker, M. J. Geske, J. M. Doherty, W. F. Stenson, T. S. Stappenbeck, Myd88-dependent positioning of Ptgs2-expressing stromal cells maintains colonic epithelial proliferation during injury. J. Clin. Invest. 117, 258-269 (2007).
19. + T cells. J. Immunol. 184, 6649-6657 (2010).
20. + T cell priming in the absence of NK cells leads to enhanced memory responses. J. Immunol. 186, 3304-3308 (2011).
21. E. Lorenz, D. A. Schwartz, P. J. Martin, T. Gooley, M. T. Lin, J. W. Chien, J. A. Hansen, J. G. Clark, Association of TLR4 mutations and the risk for acute GVHD after HLA-matched-sibling hematopoietic stemcell transplantation. Biol. Blood Marrow Transplant. 7, 384-387 (2001).
22. J. Sivula, Z. M. Cordova, J. Tuimala, T. Jaatinen, J. Partanen, L. Volin, H. Turpeinen, Toll-like receptor gene polymorphisms confer susceptibility to graft-versus-host disease in allogenic hematopoietic stem cell transplantation. Scand. J. Immunol. 76, 336-341 (2012).
23. M. Yamamoto, S. Sato, H. Hemmi, K. Hoshino, T. Kaisho, H. Sanjo, O. Takeuchi, M. Sugiyama, M. Okabe, K. Takeda, S. Akira, Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 301, 640-643 (2003).
24. L. Ruggeri, M. Capanni, E. Urbani, K. Perruccio, W. D. Shlomchik, A. Tosti, S. Posati, D. Rogaia, F. Frassoni, F. Aversa, M. F. Martelli, A. Velardi, Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295, 2097-2100 (2002).
25. L. Ruggeri, M. Capanni, M. Casucci, I. Volpi, A. Tosti, K. Perruccio, E. Urbani, R. S. Negrin, M. F. Martelli, A. Velardi, Role of natural killer cell alloreactivity in HLA-mismatched hematopoietic stem cell transplantation. Blood 94, 333-339 (1999).
26. B. R. Blazar, C. C. Soderling, G. C. Koo, D. A. Vallera, Absence of a facilitory role for NK 1.1-positive donor cells in engraftment across a major histocompatibility barrier in mice. Transplantation 45, 876-883 (1988).
27. G. J. Prud'homme, D. C. Bocarro, Natural suppressor-like cells in local graft-vs-host disease. Cell. Immunol. 118, 516-525 (1989).
28. J. R. Passweg, M. Stern, U. Koehl, L. Uharek, A. Tichelli, Use of natural killer cells in hematopoetic stem cell transplantation. Bone Marrow Transplant. 35, 637-643 (2005).
29. J. A. Olson, R. Zeiser, A. Beilhack, J. J. Goldman, R. S. Negrin, Tissue-specific homing and expansion of donor NK cells in allogeneic bone marrow transplantation. J. Immunol. 183, 3219-3228 (2009).
30. S. Sivori, S. Carlomagno, M. Falco, E. Romeo, L. Moretta, A. Moretta, Natural killer cells expressing the KIR2DS1-activating receptor efficiently kill T-cell blasts and dendritic cells: Implications in haploidentical HSCT. Blood 117, 4284-4292 (2011).
31. J. A. Olson, D. B. Leveson-Gower, S. Gill, J. Baker, A. Beilhack, R. S. Negrin, NK cells mediate reduction of GVHD by inhibiting activated, alloreactive T cells while retaining GVT effects. Blood 115, 4293-4301 (2010).
32. D. B. Leveson-Gower, J. A. Olson, E. I. Sega, R. H. Luong, J. Baker, R. Zeiser, R. S. Negrin, Low doses of natural killer T cells provide protection from acute graft-versus-host disease via an IL-4-dependent mechanism. Blood 117, 3220-3229 (2011).
33. M. Koyama, R. D. Kuns, S. D. Olver, K. E. Lineburg, M. Lor, B. E. Teal, N. C. Raffelt, L. Leveque, C. J. Chan, R. J. Robb, K. A. Markey, K. A. Alexander, A. Varelias, A. D. Clouston, M. J. Smyth, K. P. MacDonald, G. R. Hill, Promoting regulation via the inhibition of DNAM-1 after transplantation. Blood 121, 3511-3520 (2013).
34. B. A. Rabinovich, J. Li, J. Shannon, R. Hurren, J. Chalupny, D. Cosman, R. G. Miller, Activated, but not resting, T cells can be recognized and killed by syngeneic NK cells. J. Immunol. 170, 3572-3576 (2003).
35. + T cells in a transfer model of colitis. J. Immunol. 161, 3256-3261 (1998).
36. + T cells, leading to prolonged viral persistence and altered pathogenesis. J. Clin. Invest. 120, 1925-1938 (2010).
37. F. P. Nestel, K. S. Price, T. A. Seemayer, W. S. Lapp, Macrophage priming and lipopolysaccharide-triggered release of tumor necrosis factor α during graft-versus-host disease. J. Exp. Med. 175, 405-413 (1992).
38. M. Murai, H. Yoneyama, T. Ezaki, M. Suematsu, Y. Terashima, A. Harada, H. Hamada, H. Asakura, H. Ishikawa, K. Matsushima, Peyer's patch is the essential site in initiating murine acute and lethal graft-versus-host reaction. Nat. Immunol. 4, 154-160 (2003).
39. P. Reddy, R. Negrin, G. R. Hill, Mouse models of bone marrow transplantation. Biol. Blood Marrow Transplant. 14, 129-135 (2008).
40. P. Reddy, Y. Maeda, C. Liu, O. I. Krijanovski, R. Korngold, J. L. Ferrara, A crucial role for antigen-presenting cells and alloantigen expression in graft-versus-leukemia responses. Nat. Med. 11, 1244-1249 (2005).
41. R. Chakraverty, D. Côté, J. Buchli, P. Cotter, R. Hsu, G. Zhao, T. Sachs, C. M. Pitsillides, R. Bronson, T. Means, C. Lin, M. Sykes, An inflammatory checkpoint regulates recruitment of graft-versus-host reactive T cells to peripheral tissues. J. Exp. Med. 203, 2021-2031 (2006).
42. G. R. Hill, J. L. Ferrara, The primacy of the gastrointestinal tract as a target organ of acute graft-versus-host disease: Rationale for the use of cytokine shields in allogeneic bone marrow transplantation. Blood 95, 2754-2759 (2000).
43. S. I. Bearman, F. R. Appelbaum, C. D. Buckner, F. B. Petersen, L. D. Fisher, R. A. Clift, E. D. Thomas, Regimen-related toxicity in patients undergoing bone marrow transplantation. J. Clin. Oncol. 6, 1562-1568 (1988).
44. J. E. Johansson, T. Ekman, Gastro-intestinal toxicity related to bone marrow transplantation: Disruption of the intestinal barrier precedes clinical findings. Bone Marrow Transplant. 19, 921-925 (1997).
45. J. M. Vossen, P. J. Heidt, H. van den Berg, E. J. Gerritsen, J. Hermans, L. J. Dooren, Prevention of infection and graft-versus-host disease by suppression of intestinal microflora in children treated with allogeneic bone marrow transplantation. Eur. J. Clin. Microbiol. Infect. Dis. 9, 14-23 (1990).
46. S. M. Opal, P. F. Laterre, B. Francois, S. P. LaRosa, D. C. Angus, J. P. Mira, X. Wittebole, T. Dugernier, D. Perrotin, M. Tidswell, L. Jauregui, K. Krell, J. Pachl, T. Takahashi, C. Peckelsen, E. Cordasco, C. S. Chang, S. Oeyen, N. Aikawa, T. Maruyama, R. Schein, A. C. Kalil, M. Van Nuffelen, M. Lynn, D. P. Rossignol, J. Gogate, M. B. Roberts, J. L. Wheeler, J. L. Vincent, A. S. Group, Effect of eritoran, an antagonist of MD2-TLR4, on mortality in patients with severe sepsis: The ACCESS randomized trial. JAMA 309, 1154-1162 (2013).
47. K. A. Shirey, W. Lai, A. J. Scott, M. Lipsky, P. Mistry, L. M. Pletneva, C. L. Karp, J. McAlees, T. L. Gioannini, J. Weiss, W. H. Chen, R. K. Ernst, D. P. Rossignol, F. Gusovsky, J. C. Blanco, S. N. Vogel, The TLR4 antagonist Eritoran protects mice from lethal influenza infection. Nature 497, 498-502 (2013).