Interleukin-11 promotes T cell polarization and prevents acute graff- versus-host disease after allogeneic bone marrow transplantation

Journal of Clinical Investigation

Volumn 102, Issue 1, 1998, Pages 115-123

  Hill, Geoffrey R ^a   Cooke, Kenneth R ^a   Teshima, Takanori ^a   Crawford, James M ^b   Keith Jr , James C ^c   Brinson, Yani S ^a   Bungard, David ^a   Ferrara, James L M ^a,d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c PFIZER INC   (United States)

^d DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

Endotoxin; Gastrointestinal tract; Inflammatory cytokines; T cells; Total body irradiation

Indexed keywords

CYTOKINE; ENDOTOXIN; INTERLEUKIN 11;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW TRANSPLANTATION; CELL POLARITY; CELL SURVIVAL; CONTROLLED STUDY; GASTROINTESTINAL TRACT; GRAFT VERSUS HOST REACTION; INFLAMMATORY CELL; MEGAKARYOPOIESIS; MIXED LYMPHOCYTE CULTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RADIATION INJURY; T LYMPHOCYTE ACTIVATION; WHOLE BODY RADIATION;

EID: 0032128206     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI3132     Document Type: Article

References (62)

1. Du, X., and D.A. Williams. 1997. Interleukin IL-11: review of molecular, cell biology, and clinical use. Blood. 11:3897-3908.
2. Du, X., T. Neben, S. Goldman, and D.A. Williams. 1993. Effects of recombinant human interleukin-11 on hematopoietic reconstitution in transplant mice: acceleration of recovery of peripheral blood neutrophils and platelets. Blood. 81:27-34.
3. Teicher, B.A., Y.N. Chen, G. Ara, Y. Emi, Y. Kakeji, Y. Maehara, S. Keyes, and D. Northey. 1996. Interaction of interleukin-11 with cytotoxic therapies in vitro against CEM cells and in vivo against EMT-6 murine mammary carcinoma. Int. J. Cancer. 67:864-870.
4. Maze, R., T. Moritz, and D.A. Williams. 1994. Increased survival and multilineage hematopoietic protection from delayed and severe myelosuppressive effects of a nitrosourea with recombinant interleukin-11. Cancer Res. 54: 4947-4951.
5. Trepicchio, W.L., M. Bozza, G. Pedneault, and A.J. Dorner. 1996. Recombinant human IL-11 attenuates the inflammatory response through down regulation of proinflammatory cytokine release and nitric oxide production. J. Immunol. 157:3627-3634.
6. Trepicchio, W.L., L. Wang, M. Bozza, and A.J. Dorner. 1997. Interleukin-11 regulates macrophage effector function through the inhibition of NF-κB. J. Immunol. 159:5661-5671.
7. Redlich, C.A., X. Gao, and S. Rockwell. 1996. IL-11 enhances survival and decreases TNF production after radiation-induced thoracic injury. J. Immunol. 157:1705-1710.
8. Qui, B.S., C.J. Pfieffer, and J.C. Keith. 1996. Protection by recombinant interleukin-11 against experimental TNB-induced colitis. Dig. Dis. Sci. 41: 1625-1630.
9. Chang, M., A. Williams, L. Ishizawa, A. Knoppel, C. van de Ven, and M.S. Cairo. 1996. Endogenous interleukin-11 expression is increased and prophylactic use of exogenous IL-11 enhances platelet recovery and improves survival during thrombocytopenia associated with experimental group B streptococcal sepsis in neonatal rats. Blood Cells Mol. Dis. 22:57-67.
10. Leng, S.X., and J.A. Elias. 1997. Interleukin-11 inhibits macrophage inierleukin-12 production. J. Immunol. 159:2161-2168.
11. Krenger, W., G.R. Hill, and J.L.M. Ferrara. 1997. Cytokine cascades in acute graft-versus-host disease. Transplantation (Baltimore). 64:553-558.
12. Kichian, K., F.P. Nestel, D. Kim, P. Ponka, and W.S. Lapp. 1996. IL-12 p40 message RNA expression in target organs during acute graft-versus-host disease. Possible involvement of IFN-gamma. J. Immunol. 157:2851-2856.
13. Nestel, F.P., K.S. Price, T.A. Seemayer, and W.S. Lapp. 1992. Macrophage priming and lipopolysaccharidc-triggered release of tumor necrosis factor alpha during graft-versus-host disease. J. Exp. Med. 175:405-413.
14. Hill, G.R., W. Krenger, and J.L.M. Ferrara. 1997. The role of cytokines in acute graft-versus-host disease. Cytokines: cellular and molecular therapy. 3: 257-265.
15. Morse, H.C., F.W. Shen, and U. Hammerling. 1987. Genetic nomenclature for loci controlling mouse lymphocyte antigens. Immunogenetics. 25:71-78.
16. Krenger, W., K.M. Snyder, C.H. Byon, G. Falzarano, and J.L.M. Ferrara. 1995. Polarized type 2 alloreactive CD4+ and CD8+ donor T cells fail to induce experimental acute graft-versus-host disease. J. Immunol. 155:585-593.
17. Paul, S.R., B.A. Barut, F. Bennett, M.A. Cochran, and K.C. Anderson. 1992. Lack of a role of intcrleukin-11 in the growth of multiple myeloma. Leuk. Res. 16:247-252.
18. Cooke, K.R., L. Kobzik, T.R. Martin, J. Brewer, J. Delmonte, J.M. Crawford, and J.L.M. Ferrara. 1996. An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation. I. The roles of minor H antigens and endotoxin. Blood. 88:3230-3239.
19. Hill, G.R., J.M. Crawford, K.J. Cooke, Y.S. Brinson, L. Pan, and J.L.M. Ferrara. 1997. Total body irradiation effects on acute graft versus host disease. The role of gastrointestinal damage and inflammatory cytokines. Blood. 90: 3204-3213.
20. Blatter, D.D., J.M. Crawford, and J.L.M. Ferrara. 1990. Nuclear magnetic resonance of hepatic graft-versus-host disease in mice. Transplantation (Baltimore). 50:1011-1018.
21. Snover, D.C., S.A. Weisdorf, G.M. Vercellotti, B. Rank, S. Hutton, and P. McGlave. 1985. A histopathologic study of gastric and small intestinal graft-versus-host disease following allogeneic bone marrow transplantation. Hum. Pathol. 16:387-392.
22. Snover, D.C., S.A. Weisdorf, N.K. Ramsay, P. McGlave, and J.H. Kersey. 1984. Hepatic graft-versus-host disease: a study of the predictive value of liver biopsy in diagnosis. Hepatology. 4:123-130.
23. Du, X.X., C.M. Doerschuk, A. Orazi, and D.A. Williams. 1994. A bone marrow stromal-derived growth factor, interleukin-11, stimulates recovery of small intestinal mucosal cells after cytoablative therapy. Blood. 83:33-37.
24. Potten, C.S. 1996. Protection of the small intestinal clonogenic stem cells from radiation-induced damage by pretreatment with interleukin 11 also increases murine survival time. Int. J. Cancer. 14:452-459.
25. Ferrara, J.L.M., and H.J. Deeg. 1991. Graft versus host disease. N. Engl. J. Med. 324:667-674.
26. Szebeni, J., M.G. Wang, D.A. Pearson, G.L. Szot, and M. Sykes. 1994. IL-2 inhibits early increases in serum gamma interferon levels associated with graft-versus-host disease. Transplantation (Baltimore). 58:1385-1393.
27. Sykes, M., G.L. Szot, P.L. Nguyen, and D.A. Pearson. 1995. Interleukin-12 inhibits murine graft-versus-host disease. Blood. 86:2429-2438.
28. Williamson, E., P. Garside, J.A. Bradley, I.A.R. More, and A.M. Mowat. 1997. Neutralizing IL-12 during induction of murine acute graft-versus-host disease polarizes the cytokine profile toward a Th2-type alloimmune response and confers long term protection from disease. J. Immunol. 159:1208-1215.
29. Orazi, A., X. Du, Z. Yang, M. Kashai, and D.A. Williams. 1996. Interleukin-11 prevents apoptosis and accelerates recovery of small intestinal mucosa in mice treated with combined chemotherapy and radiation. Lab. Invest. 75:33-42.
30. Antin, J.H., and J.L.M. Ferrara. 1992. Cytokine dysregulation and acute graft-versus-host disease. Blood. 80:2964-2968.
31. Fowler, D.H., K. Kurasawa, R. Smith, and R.E. Gress. 1994. Donor lymphoid cells of Th2 cytokine phenotype reduce lethal graft versus host disease and facilitate fully allogeneic cell transfers in sublethally irradiated mice. Prog. Clin. Biol. Res. 389:533-540.
32. Krenger, W., K.R. Cooke, S.T. Sonis, J. Crawford, R. Simmons, L. Pan, L. Kobzik, J. Delmonte, M. Karandikar, and J.L.M. Ferrara. 1996. Transplantation of polarized type 2 donor T cells reduces mortality caused by experimental grall-versus-hosl disease. Transplantation (Baltimore). 62:1278-1285.
33. Ringden, O., and H.J. Deeg. 1997. Clinical spectrum of graft-versus-host disease. In Graft-vs-Host Disease. 2nd edition. J.L.M. Ferrara, H.J. Deeg, and S.J. Burakoff, editors. Marcel Dekker, Inc., NY. 525-559.
34. Hakim, F.T., S. Payne, and G.M. Shearer. 1994. Recovery of T cell populations alter acute graft-vs-host reaction. J. Immunol. 152:58-64.
35. Storek, J., and A. Saxon. 1992. Reconstitution of B cell immunity following bone marrow transplantation. Bone Marrow Transplant. 9:395-408.
36. Keith, J.C., L. Albert, S.T. Sonis, C.J. Pfeiffer, and R.G. Schaub. 1994. IL-11, a pleotropic cytokine: exciting new effects of IL-11 on gastrointestinal mucosal biology. Stem Cells. 12:79-90.
37. Sonis, S., A. Muska, J. O'Brien, A. Van Vugt, P. Langer-Safer, and J. Keith. 1945. Alteration in the frequency severity and duration of chemotherapy-induced mucositis in hamsters by IL-11. Eur. J. Cancer. 318:261-266.
38. Pfieffer, C.J., S. Sato, B.S. Qiu, J.C. Keith, and S. Evangelistia. 1997. Cellular pathology of experimental colitis induced by trinitrobenzenesulfonic acid (TNBS): protective effects of recombinant human interleukin-11. Immunopharmacology. 5:363-381.
39. Peterson, K.L., M.M. Bozza, and A.J. Dorner. 1996. Interleukin-11 induces epithelial cell growth arrest through effects on retinoblastoma protein phosphorylation. Am. J. Pathol. 149:895-902.
40. Liu, Q., X.X. Du, D.T. Schindel, Z.X. Yang, F.J. Rescorla, D.A. Williams, and J.L. Grosfeld. 1996. Trophic effects of IL-11 in rats with experimental short bowel syndrome. J. Pediatr. Surg. 31:1047-1050.
41. Piguet, P.F., G.E. Grau, B. Allet, and P.J. Vassalli. 1987. Tumor necrosis factor/cachectin is an effector of skin and gut lesions of the acute phase of graft-versus-host disease. J. Exp. Med. 166:1280-1289.
42. Madara, J.L., and J. Stafford. 1989. Interferon-γ directly affects barrier function of cultured intestinal epithelial monolayers. J. Clin. Invest. 83:724-727.
43. Adams, R.B., S.M. Planchon, and J.K. Roche. 1993. IFN-γ modulation of epithelial barrier function. J. Immunol. 150:2356-2363.
44. Mowat, A. 1989. Antibodies to IFN-gamma prevent immunological mediated intestinal damage in murine graft-versus-host reactions. Immunology. 68:18-24.
45. Baker, M.B., N.H. Altman, E.R. Podack, and R.B. Levy. 1996. The role of cell-mediated cytotoxicity in acute GVHD after MHC-matched allogeneic bone marrow transplantation in mice. J. Exp. Med. 183:2645-2656.
46. Hattori, K., T. Hirano, M. Tateno, K. Oshimi, N. Kayagaki, H. Yagita, and K. Okumura. 1997. The synergistic effects of anti-Fas ligand and TNF-α antibody on the prevention of lethal acute graft-versus-host disease in mice. Blood. 90:206a. (Abstr.)
47. Rus, V., A. Svetic, P. Nguyen, W.C. Gause, and C.S. Via. 1995. Kinetics of Th1 and Th2 cytokine production during the early course of acute and chronic murine graft-versus-host disease. J. Immunol. 155:2396-2406.
48. Lichtman, A., W. Krenger, and J.L.M. Ferrara. 1997. Cytokine networks. In Graft-vs-Host Disease, 2nd edition. J.L.M. Ferrara, H.J. Deeg, and S.J. Burakoff, editors. Marcel Dekker, Inc., NY. 179-218.
49. Fowler, D.H., J. Breglio, G. Nagel, M.A. Eckhaus, and R.E. Gress. 1996. Allospecific CD8+ Tc1 and Tc2 populations in GVL and GVHD. J. Immunol. 157:4811-4821.
50. Via, C.S., S.O. Sharrow, and G.M. Shearer. 1987. Role of cytotoxic T lymphocytes in prevention of lupus-like disease occurring in a murine model of graft-versus-host disease. J. Immunol. 139:1840-1849.
51. Sykes, M., V.S. Abraham, M.W. Harty, and D.A. Pearson. 1993. IL-2 reduces graft-versus-host disease and preserves a graft-versus-leukemia effect by selectively inhibiting CD4+ T cell activity. J. Immunol. 150:197-205.
52. Yang, Y., J.J. Sergio, D.A. Pearson, G.L. Szot, A. Shimizu, and M. Sykes. 1997. Interleukin-12 preserves the graft-versus-leukemia effect of allogeneic CD8 T cells while inhibiting CD4-dependent graft-versus-host disease in mice. Blood. 90:4651-4660.
53. Fowler, D.H., K. Kurasawa, A. Husebekk, P.A. Cohen, and R.E. Gress. 1994. Cells of the Th2 cytokine phenotype prevent LPS-induced lethality during murine graft-versus-host reaction. J. Immunol. 152:1004-1011.
54. Pan, L., J. Delmonte, C.K. Jalonen, and J.L.M. Ferrara. 1995. Pretreatment of donors with granulocyte colony-stimulating factor polarizes donor T lymphocytes toward type 2 cytokine production and reduces severity of experimental graft versus host disease. Blood. 86:4422-4429.
55. Bensinger, W.I., R. Clift, P. Martin, F.R. Appelbaum, T. Demirer, T. Gooley, K. Lilleby, S. Rowley, J. Sanders, R. Storb, and C.D. Buckner. 1996. Allogeneic peripheral blood stem cell transplantation in patients with advanced hematologic malignancies: A retrospective comparison with marrow transplantation. Blood. 88:2794-2800.
56. Schmitz, N., P. Dreger, M. Suttorp, E.B. Rohwedder, T. Haferlach, H. Loffler, A. Hunter, and N.H. Russell. 1995. Primary transplantation of allogeneic peripheral blood progenitor cells mobilized by Filgrastim (granulocyte colony-stimulating factor). Blood. 85:1666-1672.
57. Storeck, J., T. Gooley, M. Siadak, W.I. Besinger, D.G. Maloney, T.R. Chauncey, M. Flowers, K.M. Sullivan, R.P. Witherspoon, S.D. Rowley, et al. 1997. Allogeneic peripheral blood stem cell transplantation may be associated with a high risk of chronic graft-versus-host disease. Blood. 90:4705-4709.
58. Neissner, M., and B.A. Volk. 1995. Altered Th1/Th2 cytokine profiles in the intestinal mucosa of patients with inflammatory bowel disease as assessed by quantitative reversed transcribed polymerase chain reaction. (RT-PCR). Clin. Exp. Immunol. 101:428-135.
59. Desreumaux, P., E. Brandt, L. Gambiez, K. Geboes, O. Klein, N. Ecters, A. Cortet, M. Capron, and J.F. Colomhel. 1997. Distinct cytokine patterns in early and chronic ileal lesions of Chron's disease. Gastroenterology. 113:118-126.
60. Briscoe, D.M., L.E. Henault, C. Geehan, S.I. Alexander, and A.H. Lichtman. 1997. Human endothelial cell costimulation of T cell IFN-γ production. J. Immunol. 159:3247-3256.
61. Nicholson, L.B., and V.K. Kuchroo. 1996. Manipulation of the Th1/Th2 Balance in Autoimmune Disease. Curr. Opin. Immunol. 8:837-842.
62. Strom, T.B., P. Roy-Chaudhury, R. Manfro, X.X. Zhen, P.W. Nickerson, K. Wood, and A. Bushell. 1996. The Th1/Th2 paradigm and the allograft response. Curr. Opin. Immunol. 8:688-693.