Sequential activation of inflammatory signaling pathways during graft-versus-host disease (GVHD): Early role for STAT1 and STAT3

Cellular Immunology

Volumn 268, Issue 1, 2011, Pages 37-46

  Ma, Hui Hui ^a   Ziegler, Judy ^a   Li, Cuiling ^a   Sepulveda, Antonia ^b   Bedeir, Ahmed ^c   Grandis, Jennifer ^d   Lentzsch, Suzanne ^a   Mapara, Markus Y ^a  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

BMT; GVHD; Inflammation; STAT1; STAT3

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 17; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; STAT1 PROTEIN; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW TRANSPLANTATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; COLON; CONTROLLED STUDY; ENZYME ACTIVATION; EPITHELIUM; FEMALE; FLOW CYTOMETRY; GEL MOBILITY SHIFT ASSAY; GENE ACTIVATION; GRAFT VERSUS HOST REACTION; HISTOPATHOLOGY; INFLAMMATION; LIVER; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PARENCHYMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SMALL INTESTINE; SPLEEN; SPLEEN LYMPHOCYTE; T LYMPHOCYTE; TH17 CELL; WESTERN BLOTTING;

ANIMALS; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GRAFT VS HOST DISEASE; INFLAMMATION; LIVER; MICE; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NF-KAPPA B; SIGNAL TRANSDUCTION; SPLEEN; STAT1 TRANSCRIPTION FACTOR; STAT3 TRANSCRIPTION FACTOR; T-LYMPHOCYTES; TH17 CELLS;

EID: 79952484281     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2011.01.008     Document Type: Article

References (39)

1. Beilhack A., Schulz S., Baker J., Beilhack G.F., Wieland C.B., Herman E.I., Baker E.M., Cao Y.A., Contag C.H., Negrin R.S. In vivo analyses of early events in acute graft-versus-host disease reveal sequential infiltration of T-cell subsets. Blood 2005, 106:1113-1122.
2. Wysocki C.A., Panoskaltsis-Mortari A., Blazar B.R., Serody J.S. Leukocyte migration and graft-versus-host disease. Blood 2005, 105:4191-4199.
3. Mapara M.Y., Kim Y.M., Marx J., Sykes M. Donor lymphocyte infusion-mediated graft-versus-leukemia effects in mixed chimeras established with a nonmyeloablative conditioning regimen: extinction of graft-versus-leukemia effects after conversion to full donor chimerism. Transplantation 2003, 76:297-305.
4. Mapara M.Y., Kim Y.M., Wang S.P., Bronson R., Sachs D.H., 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, 100:1903-1909.
5. Billiau A.D., 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, 100:1894-1902.
6. Xia G., Truitt R.L., Johnson B.D. Graft-versus-leukemia and graft-versus-host reactions after donor lymphocyte infusion are initiated by host-type antigen-presenting cells and regulated by regulatory T cells in early and long-term chimeras. Biol. Blood Marrow Transplant. 2006, 12:397-407.
7. Leng C., Gries M., Ziegler J., Lokshin A., Mascagni P., Lentzsch S., Mapara M.Y. Reduction of graft-versus-host disease by histone deacetylase inhibitor suberonylanilide hydroxamic acid is associated with modulation of inflammatory cytokine milieu and involves inhibition of STAT1. Exp. Hematol. 2006, 34:776-787.
8. Reddy P., Maeda Y., Hotary K., Liu C., Reznikov L.L., Dinarello C.A., Ferrara J.L. Histone deacetylase inhibitor suberoylanilide hydroxamic acid reduces acute graft-versus-host disease and preserves graft-versus-leukemia effect. Proc. Natl. Acad. Sci. USA 2004, 101:3921-3926.
9. Reddy P., Sun Y., Toubai T., Duran-Struuck R., Clouthier S.G., Weisiger E., Maeda Y., Tawara I., Krijanovski O., Gatza E., Liu C., Malter C., Mascagni P., Dinarello C.A., Ferrara J.L. Histone deacetylase inhibition modulates indoleamine 2,3-dioxygenase-dependent DC functions and regulates experimental graft-versus-host disease in mice. J. Clin. Invest. 2008, 118:2562-2573.
10. Sun Y., Chin Y.E., Weisiger E., Malter C., Tawara I., Toubai T., Gatza E., Mascagni P., Dinarello C.A., Reddy P. Cutting edge: negative regulation of dendritic cells through acetylation of the nonhistone protein STAT-3. J. Immunol. 2009, 182:5899-5903.
11. Sun K., Wilkins D.E., Anver M.R., Sayers T.J., Panoskaltsis-Mortari A., Blazar B.R., Welniak L.A., Murphy W.J. Differential effects of proteasome inhibition by bortezomib on murine acute graft-versus-host disease (GVHD): delayed administration of bortezomib results in increased GVHD-dependent gastrointestinal toxicity. Blood 2005, 106:3293-3299.
12. Sun K., Welniak L.A., Panoskaltsis-Mortari A., O'Shaughnessy M.J., Liu H., Barao I., Riordan W., Sitcheran R., Wysocki C., Serody J.S., Blazar B.R., Sayers T.J., Murphy W.J. Inhibition of acute graft-versus-host disease with retention of graft-versus-tumor effects by the proteasome inhibitor bortezomib. Proc. Natl. Acad. Sci. USA 2004, 101:8120-8125.
13. Vodanovic-Jankovic S., Hari P., Jacobs P., Komorowski R., Drobyski W.R. NF-kappaB as a target for the prevention of graft-versus-host disease: comparative efficacy of bortezomib and PS-1145. Blood 2006, 107:827-834.
14. Sugerman P.B., Faber S.B., Willis L.M., Petrovic A., Murphy G.F., Pappo J., Silberstein D., van den Brink M.R. Kinetics of gene expression in murine cutaneous graft-versus-host disease. Am. J. Pathol. 2004, 164:2189-2202.
15. Ichiba T., Teshima T., Kuick R., Misek D.E., Liu C., Takada Y., Maeda Y., Reddy P., Williams D.L., Hanash S.M., Ferrara J.L. Early changes in gene expression profiles of hepatic GVHD uncovered by oligonucleotide microarrays. Blood 2003, 102:763-771.
16. Lentzsch S., Gries M., Janz M., Bargou R., Dorken B., Mapara M.Y. Macrophage inflammatory protein 1-alpha (MIP-1 alpha) triggers migration and signaling cascades mediating survival and proliferation in multiple myeloma (MM) cells. Blood 2003, 101:3568-3573.
17. Hill G.R., Cooke K.R., Teshima T., Crawford J.M., Keith J.C., Brinson Y.S., Bungard D., Ferrara J.L. Interleukin-11 promotes T cell polarization and prevents acute graft-versus-host disease after allogeneic bone marrow transplantation. J. Clin. Invest. 1998, 102:115-123.
18. Mathas S., Rickers A., Bommert K., Dorken B., Mapara M.Y. Anti-CD20- and B-cell receptor-mediated apoptosis: evidence for shared intracellular signaling pathways. Cancer Res. 2000, 60:7170-7176.
19. Lu S.X., Alpdogan O., Lin J., Balderas R., Campos-Gonzalez R., Wang X., Gao G.J., Suh D., King C., Chow M., Smith O.M., Hubbard V.M., Bautista J.L., Cabrera-Perez J., Zakrzewski J.L., Kochman A.A., Chow A., Altan-Bonnet G., van den Brink M.R. STAT-3 and ERK 1/2 phosphorylation are critical for T-cell alloactivation and graft-versus-host disease. Blood 2008, 112:5254-5258.
20. Nenci A., Becker C., Wullaert A., Gareus R., van Loo G., Danese S., Huth M., Nikolaev A., Neufert C., Madison B., Gumucio D., Neurath M.F., Pasparakis M. Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature 2007, 446:557-561.
21. Cao S., Zhang X., Edwards J.P., Mosser D.M. NF-kappaB1 (p50) homodimers differentially regulate pro- and anti-inflammatory cytokines in macrophages. J. Biol. Chem. 2006, 281:26041-26050.
22. Chatterjee-Kishore M., Wright K.L., Ting J.P., Stark G.R. How Stat1 mediates constitutive gene expression: a complex of unphosphorylated Stat1 and IRF1 supports transcription of the LMP2 gene. EMBO J. 2000, 19:4111-4122.
23. Meyer T., Gavenis K., Vinkemeier U. Cell type-specific and tyrosine phosphorylation-independent nuclear presence of STAT1 and STAT3. Exp. Cell Res. 2002, 272:45-55.
24. Mapara M.Y., Leng C., Kim Y.M., Bronson R., Lokshin A., Luster A., Sykes M. Expression of chemokines in GVHD target organs is influenced by conditioning and genetic factors and amplified by GVHR. Biol. Blood Marrow Transplant. 2006, 12:623-634.
25. Nikolic B., Lee S., Bronson R.T., Grusby M.J., Sykes M. Th1 and Th2 cells both contribute to acute GVHD, and each subset has distinct end-organ targets. J. Clin. Invest. 2000, 105:1289-1293.
26. Burman A.C., Banovic T., Kuns R.D., Clouston A.D., Stanley A.C., Morris E.S., Rowe V., Bofinger H., Skoczylas R., Raffelt N., Fahy O., McColl S.R., Engwerda C.R., McDonald K.P., Hill G.R. IFNgamma differentially controls the development of idiopathic pneumonia syndrome and GVHD of the gastrointestinal tract. Blood 2007, 110:1064-1072.
27. Graness A., Poli V., Goppelt-Struebe M. STAT3-independent inhibition of lysophosphatidic acid-mediated upregulation of connective tissue growth factor (CTGF) by cucurbitacin I. Biochem. Pharmacol. 2006, 72:32-41.
28. Radojcic V., Pletneva M.A., Yen H.R., Ivcevic S., Panoskaltsis-Mortari A., Gilliam A.C., Drake C.G., Blazar B.R., Luznik L. STAT3 signaling in CD4+ T cells is critical for the pathogenesis of chronic sclerodermatous graft-versus-host disease in a murine model. J. Immunol. 2010, 184:764-774.
29. Stockinger B., Veldhoen M. Differentiation and function of Th17 T cells. Curr. Opin. Immunol. 2007, 19:281-286.
30. Lohr J., Knoechel B., Wang J.J., Villarino A.V., Abbas A.K. Role of IL-17 and regulatory T lymphocytes in a systemic autoimmune disease. J. Exp. Med. 2006, 203:2785-2791.
31. Carlson M.J., West M.L., Coghill J.M., Panoskaltsis-Mortari A., Blazar B.R., Serody J.S. In vitro-differentiated TH17 cells mediate lethal acute graft-versus-host disease with severe cutaneous and pulmonary pathologic manifestations. Blood 2009, 113:1365-1374.
32. Kappel L.W., Goldberg G.L., King C.G., Suh D.Y., Smith O.M., Ligh C., Holland A.M., Grubin J., Mark N.M., Liu C., Iwakura Y., Heller G., van den Brink M.R. IL-17 contributes to CD4-mediated graft-versus-host disease. Blood 2009, 113:945-952.
33. Yi T., Zhao D., Lin C.L., Zhang C., Chen Y., Todorov I., LeBon T., Kandeel F., Forman S., Zeng D. Absence of donor Th17 leads to augmented Th1 differentiation and exacerbated acute graft-versus-host disease. Blood 2008, 112:2101-2110.
34. Chen X., Vodanovic-Jankovic S., Johnson B., Keller M., Komorowski R., Drobyski W.R. Absence of regulatory T-cell control of TH1 and TH17 cells is responsible for the autoimmune-mediated pathology in chronic graft-versus-host disease. Blood 2007, 110:3804-3813.
35. Iclozan C., Yu Y., Liu C., Liang Y., Yi T., Anasetti C., Yu X.Z. T helper17 cells are sufficient but not necessary to induce acute graft-versus-host disease. Biol. Blood Marrow Transplant. 2010, 16:170-178.
36. Yang X.O., Panopoulos A.D., Nurieva R., Chang S.H., Wang D., Watowich S.S., Dong C. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J. Biol. Chem. 2007, 282:9358-9363.
37. Harris T.J., Grosso J.F., Yen H.R., Xin H., Kortylewski M., Albesiano E., Hipkiss E.L., Getnet D., Goldberg M.V., Maris C.H., Housseau F., Yu H., Pardoll D.M., Drake C.G. Cutting edge: an in vivo requirement for STAT3 signaling in TH17 development and TH17-dependent autoimmunity. J. Immunol. 2007, 179:4313-4317.
38. Ivanov, Zhou L., Littman D.R. Transcriptional regulation of Th17 cell differentiation. Semin. Immunol. 2007.
39. Ivanov, McKenzie B.S., Zhou L., Tadokoro C.E., Lepelley A., Lafaille J.J., Cua D.J., Littman D.R. The orphan nuclear receptor ROR gammat directs the differentiation program of proinflammatory IL-17+T helper cells. Cell 2006, 126:1121-1133.