Crucial Role of the Interleukin 1 Receptor Family Member T1/St2 in T Helper Cell Type 2-Mediated Lung Mucosal Immune Responses

doi:10.1084/jem.190.7.895

This Article

	Full Text
	Full Text (PDF, 342K)
	PPT slides of all figures
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JEM
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Coyle, A. J.
	Articles by Gutierrez-Ramos, J. C.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Coyle, A. J.
	Articles by Gutierrez-Ramos, J. C.


Social Bookmarking

	What's this?

© The Rockefeller University Press, 0022-1007/1999/10/895/ $5.00
The Journal of Experimental Medicine, Volume 190, Number 7, October 4, 1999 895-902

Original Article

Crucial Role of the Interleukin 1 Receptor Family Member T1/St2 in T Helper Cell Type 2–Mediated Lung Mucosal Immune Responses

Anthony J. Coyle^a, Clare Lloyd^a, Jane Tian^a, Trang Nguyen^a, Christina Erikkson^b, Lin Wang^a, Par Ottoson^b, Per Persson^b, Tracy Delaney^a, Sophie Lehar^a, Steve Lin^a, Louis Poisson^a, Christian Meisel^c^,d, Thomas Kamradt^c^,d, Torbjorn Bjerke^b, Douglas Levinson^a, and Jose Carlos Gutierrez-Ramos^a

^a Department of Biology, Inflammation Division, Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts 02139
^b Astra Draco, Inflammation Pharmacology, Preclinical Research and Development, S-221 00 Lund, Sweden
^c Deutsches Rheumaforschungs Zentrum, Berlin D-10117, Germany
^d Universitätsklinikum Charite, Rheumatologie und Klinische Immunologie, D-10098 Berlin, Germany
Inflammation Division, Millennium Pharmaceuticals, Inc., 75 Sidney St., Cambridge, MA 02139.617-551-8910617-679-7347

coyle{at}mpi.com

T1/ST2 is an orphan receptor of unknown function that is expressedon the surface of murine T helper cell type 2 (Th2), but notTh1 effector cells. In vitro blockade of T1/ST2 signaling withan immunoglobulin (Ig) fusion protein suppresses both differentiationto and activation of Th2, but not Th1 effector populations.In a nascent Th2-dominated response, anti-T1/ST2 monoclonalantibody (mAb) inhibited eosinophil infiltration, interleukin5 secretion, and IgE production. To determine if these effectswere mediated by a direct effect on Th2 cells, we next useda murine adoptive transfer model of Th1- and Th2-mediated lungmucosal immune responses. Administration of either T1/ST2 mAbor T1/ST2-Ig abrogated Th2 cytokine production in vivo and theinduction of an eosinophilic inflammatory response, but failedto modify Th1-mediated inflammation. Taken together, our datademonstrate an important role of T1/ST2 in Th2-mediated inflammatoryresponses and suggest that T1/ST2 may prove to be a novel targetfor the selective suppression of Th2 immune responses.

Key Words: inflammation • eosinophil • asthma • cytokines • immunoglobulin superfamily

1used in this paper: BAL, bronchoalveolar lavage; CCR, CC chemokinereceptor; TLR, Toll-like receptor

Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Murphy, G E J, Xu, D, Liew, F Y, McInnes, I B (2010). Role of interleukin 33 in human immunopathology. Ann Rheum Dis 69: i43-i47 [Abstract] [Full Text]
Prefontaine, D., Lajoie-Kadoch, S., Foley, S., Audusseau, S., Olivenstein, R., Halayko, A. J., Lemiere, C., Martin, J. G., Hamid, Q. (2009). Increased Expression of IL-33 in Severe Asthma: Evidence of Expression by Airway Smooth Muscle Cells. J. Immunol. 183: 5094-5103 [Abstract] [Full Text]
Schneider, E., Petit-Bertron, A.-F., Bricard, R., Levasseur, M., Ramadan, A., Girard, J.-P., Herbelin, A., Dy, M. (2009). IL-33 Activates Unprimed Murine Basophils Directly In Vitro and Induces Their In Vivo Expansion Indirectly by Promoting Hematopoietic Growth Factor Production. J. Immunol. 183: 3591-3597 [Abstract] [Full Text]
Guo, L., Wei, G., Zhu, J., Liao, W., Leonard, W. J., Zhao, K., Paul, W. (2009). IL-1 family members and STAT activators induce cytokine production by Th2, Th17, and Th1 cells. Proc. Natl. Acad. Sci. USA 106: 13463-13468 [Abstract] [Full Text]
Hagenow, K., Gelderman, K. A., Hultqvist, M., Merky, P., Backlund, J., Frey, O., Kamradt, T., Holmdahl, R. (2009). Ncf1-Associated Reduced Oxidative Burst Promotes IL-33R+ T Cell-Mediated Adjuvant-Free Arthritis in Mice. J. Immunol. 183: 874-881 [Abstract] [Full Text]
Campbell, J. D., Buckland, K. F., McMillan, S. J., Kearley, J., Oldfield, W. L.G., Stern, L. J., Gronlund, H., van Hage, M., Reynolds, C. J., Boyton, R. J., Cobbold, S. P., Kay, A. B., Altmann, D. M., Lloyd, C. M., Larche, M. (2009). Peptide immunotherapy in allergic asthma generates IL-10-dependent immunological tolerance associated with linked epitope suppression. JEM 206: 1535-1547 [Abstract] [Full Text]
Okazaki, T., Ni, A., Baluk, P., Ayeni, O. A., Kearley, J., Coyle, A. J., Humbles, A., McDonald, D. M. (2009). Capillary Defects and Exaggerated Inflammatory Response in the Airways of EphA2-Deficient Mice. Am. J. Pathol. 174: 2388-2399 [Abstract] [Full Text]
Kearley, J., Buckland, K. F., Mathie, S. A., Lloyd, C. M. (2009). Resolution of Allergic Inflammation and Airway Hyperreactivity Is Dependent upon Disruption of the T1/ST2-IL-33 Pathway. Am. J. Respir. Crit. Care Med. 179: 772-781 [Abstract] [Full Text]
Bulek, K., Swaidani, S., Qin, J., Lu, Y., Gulen, M. F., Herjan, T., Min, B., Kastelein, R. A., Aronica, M., Kosz-Vnenchak, M., Li, X. (2009). The Essential Role of Single Ig IL-1 Receptor-Related Molecule/Toll IL-1R8 in Regulation of Th2 Immune Response. J. Immunol. 182: 2601-2609 [Abstract] [Full Text]
Al-Garawi, A. A., Fattouh, R., Walker, T. D., Jamula, E. B., Botelho, F., Goncharova, S., Reed, J., Stampfli, M. R., O'Byrne, P. M., Coyle, A. J., Jordana, M. (2009). Acute, but Not Resolved, Influenza A Infection Enhances Susceptibility to House Dust Mite-Induced Allergic Disease. J. Immunol. 182: 3095-3104 [Abstract] [Full Text]
Suzukawa, M., Iikura, M., Koketsu, R., Nagase, H., Tamura, C., Komiya, A., Nakae, S., Matsushima, K., Ohta, K., Yamamoto, K., Yamaguchi, M. (2008). An IL-1 Cytokine Member, IL-33, Induces Human Basophil Activation via Its ST2 Receptor. J. Immunol. 181: 5981-5989 [Abstract] [Full Text]
Kurowska-Stolarska, M., Kewin, P., Murphy, G., Russo, R. C., Stolarski, B., Garcia, C. C., Komai-Koma, M., Pitman, N., Li, Y., McKenzie, A. N. J., Teixeira, M. M., Liew, F. Y., Xu, D. (2008). IL-33 Induces Antigen-Specific IL-5+ T Cells and Promotes Allergic-Induced Airway Inflammation Independent of IL-4. J. Immunol. 181: 4780-4790 [Abstract] [Full Text]
Smithgall, M. D., Comeau, M. R., Park Yoon, B.-R., Kaufman, D., Armitage, R., Smith, D. E. (2008). IL-33 amplifies both Th1- and Th2-type responses through its activity on human basophils, allergen-reactive Th2 cells, iNKT and NK Cells. Int Immunol 20: 1019-1030 [Abstract] [Full Text]
Turnquist, H. R., Sumpter, T. L., Tsung, A., Zahorchak, A. F., Nakao, A., Nau, G. J., Liew, F. Y., Geller, D. A., Thomson, A. W. (2008). IL-1{beta}-Driven ST2L Expression Promotes Maturation Resistance in Rapamycin-Conditioned Dendritic Cells. J. Immunol. 181: 62-72 [Abstract] [Full Text]
Verri, W. A. Jr., Guerrero, A. T. G., Fukada, S. Y., Valerio, D. A., Cunha, T. M., Xu, D., Ferreira, S. H., Liew, F. Y., Cunha, F. Q. (2008). IL-33 mediates antigen-induced cutaneous and articular hypernociception in mice. Proc. Natl. Acad. Sci. USA 105: 2723-2728 [Abstract] [Full Text]
Humphreys, N. E., Xu, D., Hepworth, M. R., Liew, F. Y., Grencis, R. K. (2008). IL-33, a Potent Inducer of Adaptive Immunity to Intestinal Nematodes. J. Immunol. 180: 2443-2449 [Abstract] [Full Text]
Ho, L. H., Ohno, T., Oboki, K., Kajiwara, N., Suto, H., Iikura, M., Okayama, Y., Akira, S., Saito, H., Galli, S. J., Nakae, S. (2007). IL-33 induces IL-13 production by mouse mast cells independently of IgE-Fc{epsilon}RI signals. J. Leukoc. Biol. 82: 1481-1490 [Abstract] [Full Text]
Huang, X., Du, W., Barrett, R. P., Hazlett, L. D. (2007). ST2 Is Essential for Th2 Responsiveness and Resistance to Pseudomonas aeruginosa Keratitis. IOVS 48: 4626-4633 [Abstract] [Full Text]
Allakhverdi, Z., Smith, D. E., Comeau, M. R., Delespesse, G. (2007). Cutting Edge: The ST2 Ligand IL-33 Potently Activates and Drives Maturation of Human Mast Cells. J. Immunol. 179: 2051-2054 [Abstract] [Full Text]
Amatucci, A., Novobrantseva, T., Gilbride, K., Brickelmaier, M., Hochman, P., Ibraghimov, A. (2007). Recombinant ST2 boosts hepatic Th2 response in vivo. J. Leukoc. Biol. 82: 124-132 [Abstract] [Full Text]
Fagundes, C. T., Amaral, F. A., Souza, A. L. S., Vieira, A. T., Xu, D., Liew, F. Y., Souza, D. G., Teixeira, M. M. (2007). ST2, an IL-1R family member, attenuates inflammation and lethality after intestinal ischemia and reperfusion. J. Leukoc. Biol. 81: 492-499 [Abstract] [Full Text]
Carriere, V., Roussel, L., Ortega, N., Lacorre, D.-A., Americh, L., Aguilar, L., Bouche, G., Girard, J.-P. (2007). IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-associated nuclear factor in vivo. Proc. Natl. Acad. Sci. USA 104: 282-287 [Abstract] [Full Text]
Tschopp, C. M., Spiegl, N., Didichenko, S., Lutmann, W., Julius, P., Virchow, J. C., Hack, C. E., Dahinden, C. A. (2006). Granzyme B, a novel mediator of allergic inflammation: its induction and release in blood basophils and human asthma. Blood 108: 2290-2299 [Abstract] [Full Text]
Yu, F.-S. X., Hazlett, L. D. (2006). Toll-like Receptors and the Eye.. IOVS 47: 1255-1263 [Full Text]
Shimizu, M., Matsuda, A., Yanagisawa, K., Hirota, T., Akahoshi, M., Inomata, N., Ebe, K., Tanaka, K., Sugiura, H., Nakashima, K., Tamari, M., Takahashi, N., Obara, K., Enomoto, T., Okayama, Y., Gao, P.-S., Huang, S.-K., Tominaga, S.-i., Ikezawa, Z., Shirakawa, T. (2005). Functional SNPs in the distal promoter of the ST2 gene are associated with atopic dermatitis. Hum Mol Genet 14: 2919-2927 [Abstract] [Full Text]
Kuipers, H., Heirman, C., Hijdra, D., Muskens, F., Willart, M., van Meirvenne, S., Thielemans, K., Hoogsteden, H. C., Lambrecht, B. N. (2004). Dendritic cells retrovirally overexpressing IL-12 induce strong Th1 responses to inhaled antigen in the lung but fail to revert established Th2 sensitization. J. Leukoc. Biol. 76: 1028-1038 [Abstract] [Full Text]
Leung, B. P., Xu, D., Culshaw, S., McInnes, I. B., Liew, F. Y. (2004). A Novel Therapy of Murine Collagen-Induced Arthritis with Soluble T1/ST2. J. Immunol. 173: 145-150 [Abstract] [Full Text]
Wiley, R. E., Cwiartka, M., Alvarez, D., Mackenzie, D. C., Johnson, J. R., Goncharova, S., Lundblad, L., Jordana, M. (2004). Transient Corticosteroid Treatment Permanently Amplifies the Th2 Response in a Murine Model of Asthma. J. Immunol. 172: 4995-5005 [Abstract] [Full Text]
Towne, J. E., Garka, K. E., Renshaw, B. R., Virca, G. D., Sims, J. E. (2004). Interleukin (IL)-1F6, IL-1F8, and IL-1F9 Signal through IL-1Rrp2 and IL-1RAcP to Activate the Pathway Leading to NF-{kappa}B and MAPKs. J. Biol. Chem. 279: 13677-13688 [Abstract] [Full Text]
Kamp, D. W. (2003). Idiopathic Pulmonary Fibrosis: The Inflammation Hypothesis Revisited. Chest 124: 1187-1190 [Full Text]
Tajima, S., Oshikawa, K., Tominaga, S.-i., Sugiyama, Y. (2003). The Increase in Serum Soluble ST2 Protein Upon Acute Exacerbation of Idiopathic Pulmonary Fibrosis. Chest 124: 1206-1214 [Abstract] [Full Text]
Wiley, R. E., Goncharova, S., Shea, T., Johnson, J. R., Coyle, A. J., Jordana, M. (2003). Evaluation of Inducible Costimulator/B7-Related Protein-1 as a Therapeutic Target in a Murine Model of Allergic Airway Inflammation. Am. J. Respir. Cell Mol. Bio. 28: 722-730 [Abstract] [Full Text]
Bishop, B., Lloyd, C. M. (2003). CC Chemokine Ligand 1 Promotes Recruitment of Eosinophils But Not Th2 Cells During the Development of Allergic Airways Disease. J. Immunol. 170: 4810-4817 [Abstract] [Full Text]
Kropf, P., Herath, S., Klemenz, R., Muller, I. (2003). Signaling through the T1/ST2 Molecule Is Not Necessary for Th2 Differentiation but Is Important for the Regulation of Type 1 Responses in Nonhealing Leishmaniamajor Infection. Infect. Immun. 71: 1961-1971 [Abstract] [Full Text]
Dunne, A., O'Neill, L. A. J. (2003). The Interleukin-1 Receptor/Toll-Like Receptor Superfamily: Signal Transduction During Inflammation and Host Defense. Sci Signal 2003: re3-re3 [Abstract] [Full Text]
Brint, E. K., Fitzgerald, K. A., Smith, P., Coyle, A. J., Gutierrez-Ramos, J.-C., Fallon, P. G., O'Neill, L. A. J. (2002). Characterization of Signaling Pathways Activated by the Interleukin 1 (IL-1) Receptor Homologue T1/ST2. A ROLE FOR JUN N-TERMINAL KINASE IN IL-4 INDUCTION. J. Biol. Chem. 277: 49205-49211 [Abstract] [Full Text]
Weinberg, E. O., Shimpo, M., De Keulenaer, G. W., MacGillivray, C., Tominaga, S.-i., Solomon, S. D., Rouleau, J.-L., Lee, R. T. (2002). Expression and Regulation of ST2, an Interleukin-1 Receptor Family Member, in Cardiomyocytes and Myocardial Infarction. Circulation 106: 2961-2966 [Abstract] [Full Text]
Kropf, P., Herath, S., Tewari, R., Syed, N., Klemenz, R., Muller, I. (2002). Identification of Two Distinct Subpopulations of Leishmania major-Specific T Helper 2 Cells. Infect. Immun. 70: 5512-5520 [Abstract] [Full Text]
Swirski, F. K., Sajic, D., Robbins, C. S., Gajewska, B. U., Jordana, M., Stampfli, M. R. (2002). Chronic Exposure to Innocuous Antigen in Sensitized Mice Leads to Suppressed Airway Eosinophilia That Is Reversed by Granulocyte Macrophage Colony-Stimulating Factor. J. Immunol. 169: 3499-3506 [Abstract] [Full Text]
Caamano, J., Hunter, C. A. (2002). NF-{kappa}B Family of Transcription Factors: Central Regulators of Innate and Adaptive Immune Functions. Clin. Microbiol. Rev. 15: 414-429 [Abstract] [Full Text]
Oshikawa, K., Yanagisawa, K., Ohno, S., Tominaga, S.-I., Sugiyama, Y. (2002). Expression of ST2 in Helper T Lymphocytes of Malignant Pleural Effusions. Am. J. Respir. Crit. Care Med. 165: 1005-1009 [Abstract] [Full Text]
Sabroe, I., Lloyd, C.M., Whyte, M.K.B., Dower, S.K., Williams, T.J., Pease, J.E. (2002). Chemokines, innate and adaptive immunity, and respiratory disease. Eur Respir J 19: 350-355 [Abstract] [Full Text]
McGuirk, P., McCann, C., Mills, K. H.G. (2002). Pathogen-specific T Regulatory 1 Cells Induced in the Respiratory Tract by a Bacterial Molecule that Stimulates Interleukin 10 Production by Dendritic Cells: A Novel Strategy for Evasion of Protective T Helper Type 1 Responses by Bordetella pertussis. JEM 195: 221-231 [Abstract] [Full Text]
McMillan, S. J., Bishop, B., Townsend, M. J., McKenzie, A. N., Lloyd, C. M. (2002). The Absence of Interleukin 9 Does Not Affect the Development of Allergen-induced Pulmonary Inflammation nor Airway Hyperreactivity. JEM 195: 51-57 [Abstract] [Full Text]
Gajewska, B. U., Swirski, F. K., Alvarez, D., Ritz, S. A., Goncharova, S., Cundall, M., Snider, D. P., Coyle, A. J., Gutierrez-Ramos, J.-C., Stampfli, M. R., Jordana, M. (2001). Temporal-Spatial Analysis of the Immune Response in a Murine Model of Ovalbumin-Induced Airways Inflammation. Am. J. Respir. Cell Mol. Bio. 25: 326-334 [Abstract] [Full Text]
Chan, W. L., Pejnovic, N., Lee, C. A., Al-Ali, N. A. (2001). Human IL-18 Receptor and ST2L Are Stable and Selective Markers for the Respective Type 1 and Type 2 Circulating Lymphocytes. J. Immunol. 167: 1238-1244 [Abstract] [Full Text]
OSHIKAWA, K., KUROIWA, K., TAGO, K., IWAHANA, H., YANAGISAWA, K., OHNO, S., TOMINAGA, S.-I., SUGIYAMA, Y. (2001). Elevated Soluble ST2 Protein Levels in Sera of Patients with Asthma with an Acute Exacerbation. Am. J. Respir. Crit. Care Med. 164: 277-281 [Abstract] [Full Text]
Nawijn, M. C., Dingjan, G. M., Ferreira, R., Lambrecht, B. N., Karis, A., Grosveld, F., Savelkoul, H., Hendriks, R. W. (2001). Enforced Expression of GATA-3 in Transgenic Mice Inhibits Th1 Differentiation and Induces the Formation of a T1/ST2-Expressing Th2-Committed T Cell Compartment In Vivo. J. Immunol. 167: 724-732 [Abstract] [Full Text]
Sweet, M. J., Leung, B. P., Kang, D., Sogaard, M., Schulz, K., Trajkovic, V., Campbell, C. C., Xu, D., Liew, F. Y. (2001). A Novel Pathway Regulating Lipopolysaccharide-Induced Shock by ST2/T1 Via Inhibition of Toll-Like Receptor 4 Expression. J. Immunol. 166: 6633-6639 [Abstract] [Full Text]
Walzl, G., Matthews, S., Kendall, S., Gutierrez-Ramos, J. C., Coyle, A. J., Openshaw, P. J.M., Hussell, T. (2001). Inhibition of T1/St2 during Respiratory Syncytial Virus Infection Prevents T Helper Cell Type 2 (Th2)- but Not Th1-Driven Immunopathology. JEM 193: 785-792 [Abstract] [Full Text]
Meisel, C., Bonhagen, K., Lohning, M., Coyle, A. J., Gutierrez-Ramos, J.-C., Radbruch, A., Kamradt, T. (2001). Regulation and Function of T1/ST2 Expression on CD4+ T Cells: Induction of Type 2 Cytokine Production by T1/ST2 Cross-Linking. J. Immunol. 166: 3143-3150 [Abstract] [Full Text]
Wiley, R. E., Palmer, K., Gajewska, B. U., Stampfli, M. R., Alvarez, D., Coyle, A. J., Gutierrez-Ramos, J.-C., Jordana, M. (2001). Expression of the Th1 Chemokine IFN-{{gamma}}-Inducible Protein 10 in the Airway Alters Mucosal Allergic Sensitization in Mice. J. Immunol. 166: 2750-2759 [Abstract] [Full Text]
COYLE, A. J., LLOYD, C. M., GUTIERREZ-RAMOS, J.-C. (2000). Biotherapeutic Targets for the Treatment of Allergic Airway Disease. Am. J. Respir. Crit. Care Med. 162: S179-184 [Abstract] [Full Text]
O'Neill, L. A. J. (2000). The Interleukin-1 Receptor/Toll-like Receptor Superfamily: Signal Transduction During Inflammation and Host Defense. Sci Signal 2000: re1-re1 [Abstract] [Full Text]
Bowie, A., Kiss-Toth, E., Symons, J. A., Smith, G. L., Dower, S. K., O'Neill, L. A. J. (2000). A46R and A52R from vaccinia virus are antagonists of host IL-1 and toll-like receptor signaling. Proc. Natl. Acad. Sci. USA 10.1073/pnas.160027697v1 [Abstract] [Full Text]
Glimcher, L. H., Murphy, K. M. (2000). Lineage commitment in the immune system: the T helper lymphocyte grows up. Genes Dev. 14: 1693-1711 [Full Text]
Townsend, M. J., Fallon, P. G., Matthews, D. J., Jolin, H. E., McKenzie, A. N.J. (2000). T1/St2-Deficient Mice Demonstrate the Importance of T1/St2 in Developing Primary T Helper Cell Type 2 Responses. JEM 191: 1069-1076 [Abstract] [Full Text]
Bowie, A., Kiss-Toth, E., Symons, J. A., Smith, G. L., Dower, S. K., O'Neill, L. A. J. (2000). A46R and A52R from vaccinia virus are antagonists of host IL-1 and toll-like receptor signaling. Proc. Natl. Acad. Sci. USA 97: 10162-10167 [Abstract] [Full Text]