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Donor interleukin-22 and host type I interferon signaling pathway participate in intestinal graft-versus-host disease via STAT1 activation and CXCL10.

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Lamarthée, B Malard, F Gamonet, C Bossard, C Couturier, M Renauld, Jean-Christophe [UCL] Gaugler, B

Acute graft-versus-host disease (aGVHD) remains a major complication following allogeneic hematopoietic cell transplantation, limiting the success of this therapy. We previously reported that interleukin-22 (IL-22) participates to aGVHD development, but the underlying mechanisms of its contribution remain poorly understood. In this study, we analyzed the mechanism of the pathological function of IL-22 in intestinal aGVHD. Ex-vivo colon culture experiments indicated that IL-22 was able to induce Th1-like inflammation via signal transducer and activator of transcription factor-1 (STAT1) and CXCL10 induction in the presence of type I interferon (IFN). To evaluate a potential synergy between IL-22 and type I IFN in aGVHD, we transplanted recipient mice, either wild-type (WT) or type I IFN receptor deficient (IFNAR(-/-)), with bone marrow cells and WT or IL-22 deficient (IL-22(-/-)) T cells. We observed a decreased GVHD severity in IFNAR(-/-) recipient of IL-22(-/-) T cells, which was associated with a lower level of STAT1 activation and reduced CXCL10 expression in the large intestine. Finally, immunohistochemistry staining of STAT1 performed on gastrointestinal biopsies of 20 transplanted patients showed exacerbated STAT1 activation in gastrointestinal tissues of patients with aGVHD as compared with those without aGVHD. Thus, interfering with both IL-22 and type I IFN signaling may provide a novel approach to limit aGVHD.

Document type Article de périodique (Journal article)
Access type Accès libre
Publication date 2016
Language Anglais
Journal information "Mucosal Immunology" - Vol. 9, no.2, p. 309-321 (2015)
Peer reviewed yes
Publisher Nature Publishing Group (New York)
issn 1933-0219
e-issn 1935-3456
Publication status Publié
Affiliation UCL - SSS/DDUV - Institut de Duve
MESH Subject Animals ; Interleukins ; Intestinal Mucosa ; Intestine, Large ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Mice, Knockout ; Receptor, Interferon alpha-beta ; STAT1 Transcription Factor ; Signal Transduction ; Bone Marrow ; Th1 Cells ; Tissue Donors ; Transplantation, Homologous ; Whole-Body Irradiation ; Bone Marrow Transplantation ; Chemokine CXCL10 ; Gene Expression Regulation ; Graft vs Host Disease ; Hematologic Neoplasms ; Humans ; Interferon Type I
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  1. Wingard John R., Majhail Navneet S., Brazauskas Ruta, Wang Zhiwei, Sobocinski Kathleen A., Jacobsohn David, Sorror Mohamed L., Horowitz Mary M., Bolwell Brian, Rizzo J. Douglas, Socié Gérard, Long-Term Survival and Late Deaths After Allogeneic Hematopoietic Cell Transplantation, 10.1200/jco.2010.33.7212
  2. Antin J.H., Blood, 80, 2964 (1992)
  3. Mohty M., Inflammatory cytokines and acute graft-versus-host disease after reduced-intensity conditioning allogeneic stem cell transplantation, 10.1182/blood-2005-07-2919
  4. Rutz Sascha, Eidenschenk Céline, Ouyang Wenjun, IL-22, not simply a Th17 cytokine, 10.1111/imr.12027
  5. Wolk Kerstin, Kunz Stefanie, Witte Ellen, Friedrich Markus, Asadullah Khusru, Sabat Robert, IL-22 Increases the Innate Immunity of Tissues, 10.1016/j.immuni.2004.07.007
  6. Couturier M, Lamarthée B, Arbez J, Renauld J-C, Bossard C, Malard F, Bonnefoy F, Mohty M, Perruche S, Tiberghien P, Saas P, Gaugler B, IL-22 deficiency in donor T cells attenuates murine acute graft-versus-host disease mortality while sparing the graft-versus-leukemia effect, 10.1038/leu.2013.39
  7. Zenewicz L. A., Flavell R. A., Recent advances in IL-22 biology, 10.1093/intimm/dxr001
  8. Sonnenberg Gregory F, Fouser Lynette A, Artis David, Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22, 10.1038/ni.2025
  9. Kamanaka Masahito, Huber Samuel, Zenewicz Lauren A., Gagliani Nicola, Rathinam Chozhavendan, O'Connor William, Wan Yisong Y., Nakae Susumu, Iwakura Yoichiro, Hao Liming, Flavell Richard A., Memory/effector (CD45RBlo) CD4 T cells are controlled directly by IL-10 and cause IL-22–dependent intestinal pathology, 10.1084/jem.20102149
  10. Bachmann Malte, Ulziibat Solongo, Härdle Lorena, Pfeilschifter Josef, Mühl Heiko, IFNα converts IL-22 into a cytokine efficiently activating STAT1 and its downstream targets, 10.1016/j.bcp.2012.11.004
  11. Mühl Heiko, Pro-Inflammatory Signaling by IL-10 and IL-22: Bad Habit Stirred Up by Interferons?, 10.3389/fimmu.2013.00018
  12. Muñoz Melba, Heimesaat Markus M., Danker Kerstin, Struck Daniela, Lohmann Uwe, Plickert Rita, Bereswill Stefan, Fischer André, Dunay Ildikò Rita, Wolk Kerstin, Loddenkemper Christoph, Krell Hans-Willi, Libert Claude, Lund Leif R., Frey Oliver, Hölscher Christoph, Iwakura Yoichiro, Ghilardi Nico, Ouyang Wenjun, Kamradt Thomas, Sabat Robert, Liesenfeld Oliver, Interleukin (IL)-23 mediatesToxoplasma gondii–induced immunopathology in the gut via matrixmetalloproteinase-2 and IL-22 but independent of IL-17, 10.1084/jem.20090900
  13. Dumoutier L., Lejeune D., Colau D., Renauld J.-C., Cloning and Characterization of IL-22 Binding Protein, a Natural Antagonist of IL-10-Related T Cell-Derived Inducible Factor/IL-22, 10.4049/jimmunol.166.12.7090
  14. Zhao Kai, Zhao Dongmei, Huang Dong, Yin Lingling, Chen Chong, Pan Bin, Wu Qingyun, Li Zhenyu, Yao Yao, Shen Erxia, Zeng Lingyu, Xu Kailin, Interleukin-22 Aggravates Murine Acute Graft-Versus-Host Disease by Expanding Effector T Cell and Reducing Regulatory T Cell, 10.1089/jir.2013.0099
  15. Sonnenberg Gregory F., Nair Meera G., Kirn Thomas J., Zaph Colby, Fouser Lynette A., Artis David, Pathological versus protective functions of IL-22 in airway inflammation are regulated by IL-17A, 10.1084/jem.20092054
  16. Zenewicz Lauren A., Yancopoulos George D., Valenzuela David M., Murphy Andrew J., Stevens Sean, Flavell Richard A., Innate and Adaptive Interleukin-22 Protects Mice from Inflammatory Bowel Disease, 10.1016/j.immuni.2008.11.003
  17. Izaguirre A., Comparative analysis of IRF and IFN-alpha expression in human plasmacytoid and monocyte-derived dendritic cells, 10.1189/jlb.0603255
  18. Ihle James N., Kerr Ian M., Jaks and Stats in signaling by the cytokine receptor superfamily, 10.1016/s0168-9525(00)89000-9
  19. Liang S. C., Nickerson-Nutter C., Pittman D. D., Carrier Y., Goodwin D. G., Shields K. M., Lambert A.-J., Schelling S. H., Medley Q. G., Ma H.-L., Collins M., Dunussi-Joannopoulos K., Fouser L. A., IL-22 Induces an Acute-Phase Response, 10.4049/jimmunol.0904091
  20. Hanash Alan M., Dudakov Jarrod A., Hua Guoqiang, O’Connor Margaret H., Young Lauren F., Singer Natalie V., West Mallory L., Jenq Robert R., Holland Amanda M., Kappel Lucy W., Ghosh Arnab, Tsai Jennifer J., Rao Uttam K., Yim Nury L., Smith Odette M., Velardi Enrico, Hawryluk Elena B., Murphy George F., Liu Chen, Fouser Lynette A., Kolesnick Richard, Blazar Bruce R., van den Brink Marcel R.M., Interleukin-22 Protects Intestinal Stem Cells from Immune-Mediated Tissue Damage and Regulates Sensitivity to Graft versus Host Disease, 10.1016/j.immuni.2012.05.028
  21. Korn L L, Thomas H L, Hubbeling H G, Spencer S P, Sinha R, Simkins H MA, Salzman N H, Bushman F D, Laufer T M, Conventional CD4+ T cells regulate IL-22-producing intestinal innate lymphoid cells, 10.1038/mi.2013.121
  22. Ma H.L., J. Clin. Invest., 118, 597 (2008)
  23. Takaoka A., Cross Talk Between Interferon-gamma and -alpha /beta Signaling Components in Caveolar Membrane Domains, 10.1126/science.288.5475.2357
  24. Mitani Yukiko, Takaoka Akinori, Kim Sun Hwa, Kato Yukiko, Yokochi Taeko, Tanaka Nobuyuki, Taniguchi Tadatsugu, Cross talk of the interferon-alpha/beta signalling complex with gp130 for effective interleukin-6 signalling, 10.1046/j.1365-2443.2001.00448.x
  25. Leng Corinna, Gries Margarethe, Ziegler Judy, Lokshin Anna, Mascagni Paolo, Lentzsch Suzanne, Mapara Markus 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, 10.1016/j.exphem.2006.02.014
  26. Imanguli M. M., Swaim W. D., League S. C., Gress R. E., Pavletic S. Z., Hakim F. T., Increased T-bet+ cytotoxic effectors and type I interferon-mediated processes in chronic graft-versus-host disease of the oral mucosa, 10.1182/blood-2008-07-168351
  27. Schreiber S, Activation of signal transducer and activator of transcription (STAT) 1 in human chronic inflammatory bowel disease, 10.1136/gut.51.3.379
  28. Capitini C. M., Nasholm N. M., Chien C. D., Larabee S. M., Qin H., Song Y. K., Klover P. J., Hennighausen L., Khan J., Fry T. J., Absence of STAT1 in donor-derived plasmacytoid dendritic cells results in increased STAT3 and attenuates murine GVHD, 10.1182/blood-2013-05-500876
  29. Spoerl S., Mathew N. R., Bscheider M., Schmitt-Graeff A., Chen S., Mueller T., Verbeek M., Fischer J., Otten V., Schmickl M., Maas-Bauer K., Finke J., Peschel C., Duyster J., Poeck H., Zeiser R., von Bubnoff N., Activity of therapeutic JAK 1/2 blockade in graft-versus-host disease, 10.1182/blood-2013-12-543736
  30. Robb R. J., Kreijveld E., Kuns R. D., Wilson Y. A., Olver S. D., Don A. L. J., Raffelt N. C., De Weerd N. A., Lineburg K. E., Varelias A., Markey K. A., Koyama M., Clouston A. D., Hertzog P. J., MacDonald K. P. A., Hill G. R., Type I-IFNs control GVHD and GVL responses after transplantation, 10.1182/blood-2010-12-325746
  31. Bossard C, Malard F, Arbez J, Chevallier P, Guillaume T, Delaunay J, Mosnier J-F, Tiberghien P, Saas P, Mohty M, Gaugler B, Plasmacytoid dendritic cells and Th17 immune response contribution in gastrointestinal acute graft-versus-host disease, 10.1038/leu.2012.41
  32. Zhao Kai, Zhao Dongmei, Huang Dong, Song Xuguang, Chen Chong, Pan Bin, Wu Qingyun, Cao Jiang, Yao Yao, Zeng Lingyu, Xu Kailin, The identification and characteristics of IL-22-producing T cells in acute graft-versus-host disease following allogeneic bone marrow transplantation, 10.1016/j.imbio.2013.05.005
  33. He S., Cao Q., Qiu Y., Mi J., Zhang J. Z., Jin M., Ge H., Emerson S. G., Zhang Y., Zhang Y., A New Approach to the Blocking of Alloreactive T Cell-Mediated Graft-versus-Host Disease by In Vivo Administration of Anti-CXCR3 Neutralizing Antibody, 10.4049/jimmunol.181.11.7581
  34. Zohar Yaniv, Wildbaum Gizi, Novak Rostislav, Salzman Andrew L., Thelen Marcus, Alon Ronen, Barsheshet Yiftah, Karp Christopher L., Karin Nathan, CXCL11-dependent induction of FOXP3-negative regulatory T cells suppresses autoimmune encephalomyelitis, 10.1172/jci71951
  35. Turner Jerrold R., Intestinal mucosal barrier function in health and disease, 10.1038/nri2653
  36. Stacey Maria A., Marsden Morgan, Pham N Tu Anh, Clare Simon, Dolton Garry, Stack Gabrielle, Jones Emma, Klenerman Paul, Gallimore Awen M., Taylor Philip R., Snelgrove Robert J., Lawley Trevor D., Dougan Gordon, Benedict Chris A., Jones Simon A., Wilkinson Gavin W.G., Humphreys Ian R., Neutrophils Recruited by IL-22 in Peripheral Tissues Function as TRAIL-Dependent Antiviral Effectors against MCMV, 10.1016/j.chom.2014.03.003
  37. Schwab Lukas, Goroncy Luise, Palaniyandi Senthilnathan, Gautam Sanjivan, Triantafyllopoulou Antigoni, Mocsai Attila, Reichardt Wilfried, Karlsson Fridrik J, Radhakrishnan Sabarinath V, Hanke Kathrin, Schmitt-Graeff Annette, Freudenberg Marina, von Loewenich Friederike D, Wolf Philipp, Leonhardt Franziska, Baxan Nicoleta, Pfeifer Dietmar, Schmah Oliver, Schönle Anne, Martin Stefan F, Mertelsmann Roland, Duyster Justus, Finke Jürgen, Prinz Marco, Henneke Philipp, Häcker Hans, Hildebrandt Gerhard C, Häcker Georg, Zeiser Robert, Neutrophil granulocytes recruited upon translocation of intestinal bacteria enhance graft-versus-host disease via tissue damage, 10.1038/nm.3517
Bibliographic reference Lamarthée, B ; Malard, F ; Gamonet, C ; Bossard, C ; Couturier, M ; et. al. Donor interleukin-22 and host type I interferon signaling pathway participate in intestinal graft-versus-host disease via STAT1 activation and CXCL10.. In: Mucosal Immunology, Vol. 9, no.2, p. 309-321 (2015)
Permanent URL http://hdl.handle.net/2078.1/184272