The Cytokines Interleukin 27 and Interferon-γ Promote Distinct Treg Cell Populations Required to Limit Infection-Induced Pathology

Aisling O Hara Hall; Daniel P. Beiting; Cristina Tato; Beena John; Guillaume Oldenhove; Claudia Gonzalez Lombana; Gretchen Harms Pritchard; Jonathan S. Silver; Nicolas Bouladoux; Jason S. Stumhofer; Tajie H. Harris; John Grainger; Elia D Tait Wojno; Sagie Wagage; David S. Roos; Philip Scott; Laurence A. Turka; Sara Cherry; Steven L. Reiner; Daniel Cua; Yasmine Belkaid; M. Merle Elloso; Christopher A. Hunter

doi:10.1016/j.immuni.2012.06.014

The Cytokines Interleukin 27 and Interferon-γ Promote Distinct Treg Cell Populations Required to Limit Infection-Induced Pathology

Aisling O Hara Hall, Daniel P. Beiting, Cristina Tato, Beena John, Guillaume Oldenhove, Claudia Gonzalez Lombana, Gretchen Harms Pritchard, Jonathan S. Silver, Nicolas Bouladoux, Jason S. Stumhofer, Tajie H. Harris, John Grainger, Elia D Tait Wojno, Sagie Wagage, David S. Roos, Philip Scott, Laurence A. Turka, Sara Cherry, Steven L. Reiner, Daniel CuaYasmine Belkaid, M. Merle Elloso, Christopher A. Hunter

Research output: Contribution to journal › Article › peer-review

Abstract

Interferon-γ (IFN-γ) promotes a population of T-bet+ CXCR3+ regulatory T (Treg) cells that limit T helper 1 (Th1) cell-mediated pathology. Our studies demonstrate that interleukin-27 (IL-27) also promoted expression of T-bet and CXCR3 in Treg cells. During infection with Toxoplasma gondii, a similar population emerged that limited T cell responses and was dependent on IFN-γ in the periphery but on IL-27 at mucosal sites. Transfer of Treg cells ameliorated the infection-induced pathology observed in Il27-/- mice, and this was dependent on their ability to produce IL-10. Microarray analysis revealed that Treg cells exposed to either IFN-γ or IL-27 have distinct transcriptional profiles. Thus, IFN-γ and IL-27 have different roles in Treg cell biology and IL-27 is a key cytokine that promotes the development of Treg cells specialized to control Th1 cell-mediated immunity at local sites of inflammation. © 2012 Elsevier Inc.

Original language	English
Pages (from-to)	511-523
Number of pages	12
Journal	Immunity
Volume	37
Issue number	3
DOIs	https://doi.org/10.1016/j.immuni.2012.06.014
Publication status	Published - 21 Sept 2012

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Hall, A. O. H., Beiting, D. P., Tato, C., John, B., Oldenhove, G., Lombana, C. G., Pritchard, G. H., Silver, J. S., Bouladoux, N., Stumhofer, J. S., Harris, T. H., Grainger, J., Wojno, E. D. T., Wagage, S., Roos, D. S., Scott, P., Turka, L. A., Cherry, S., Reiner, S. L., ... Hunter, C. A. (2012). The Cytokines Interleukin 27 and Interferon-γ Promote Distinct Treg Cell Populations Required to Limit Infection-Induced Pathology. Immunity, 37(3), 511-523. https://doi.org/10.1016/j.immuni.2012.06.014

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title = "The Cytokines Interleukin 27 and Interferon-γ Promote Distinct Treg Cell Populations Required to Limit Infection-Induced Pathology",

abstract = "Interferon-γ (IFN-γ) promotes a population of T-bet+ CXCR3+ regulatory T (Treg) cells that limit T helper 1 (Th1) cell-mediated pathology. Our studies demonstrate that interleukin-27 (IL-27) also promoted expression of T-bet and CXCR3 in Treg cells. During infection with Toxoplasma gondii, a similar population emerged that limited T cell responses and was dependent on IFN-γ in the periphery but on IL-27 at mucosal sites. Transfer of Treg cells ameliorated the infection-induced pathology observed in Il27-/- mice, and this was dependent on their ability to produce IL-10. Microarray analysis revealed that Treg cells exposed to either IFN-γ or IL-27 have distinct transcriptional profiles. Thus, IFN-γ and IL-27 have different roles in Treg cell biology and IL-27 is a key cytokine that promotes the development of Treg cells specialized to control Th1 cell-mediated immunity at local sites of inflammation. {\textcopyright} 2012 Elsevier Inc.",

author = "Hall, {Aisling O Hara} and Beiting, {Daniel P.} and Cristina Tato and Beena John and Guillaume Oldenhove and Lombana, {Claudia Gonzalez} and Pritchard, {Gretchen Harms} and Silver, {Jonathan S.} and Nicolas Bouladoux and Stumhofer, {Jason S.} and Harris, {Tajie H.} and John Grainger and Wojno, {Elia D Tait} and Sagie Wagage and Roos, {David S.} and Philip Scott and Turka, {Laurence A.} and Sara Cherry and Reiner, {Steven L.} and Daniel Cua and Yasmine Belkaid and Elloso, {M. Merle} and Hunter, {Christopher A.}",

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year = "2012",

month = sep,

day = "21",

doi = "10.1016/j.immuni.2012.06.014",

language = "English",

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journal = "Immunity",

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Hall, AOH, Beiting, DP, Tato, C, John, B, Oldenhove, G, Lombana, CG, Pritchard, GH, Silver, JS, Bouladoux, N, Stumhofer, JS, Harris, TH, Grainger, J, Wojno, EDT, Wagage, S, Roos, DS, Scott, P, Turka, LA, Cherry, S, Reiner, SL, Cua, D, Belkaid, Y, Elloso, MM & Hunter, CA 2012, 'The Cytokines Interleukin 27 and Interferon-γ Promote Distinct Treg Cell Populations Required to Limit Infection-Induced Pathology', Immunity, vol. 37, no. 3, pp. 511-523. https://doi.org/10.1016/j.immuni.2012.06.014

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T1 - The Cytokines Interleukin 27 and Interferon-γ Promote Distinct Treg Cell Populations Required to Limit Infection-Induced Pathology

AU - Hall, Aisling O Hara

AU - Beiting, Daniel P.

AU - Tato, Cristina

AU - John, Beena

AU - Oldenhove, Guillaume

AU - Lombana, Claudia Gonzalez

AU - Pritchard, Gretchen Harms

AU - Silver, Jonathan S.

AU - Bouladoux, Nicolas

AU - Stumhofer, Jason S.

AU - Harris, Tajie H.

AU - Grainger, John

AU - Wojno, Elia D Tait

AU - Wagage, Sagie

AU - Roos, David S.

AU - Scott, Philip

AU - Turka, Laurence A.

AU - Cherry, Sara

AU - Reiner, Steven L.

AU - Cua, Daniel

AU - Belkaid, Yasmine

AU - Elloso, M. Merle

AU - Hunter, Christopher A.

N1 - AI 071302, NIAID NIH HHS, United StatesAI055428, NIAID NIH HHS, United StatesAI084882, NIAID NIH HHS, United StatesP01 AI043620, NIAID NIH HHS, United StatesR01 AI042334, NIAID NIH HHS, United StatesR21-AI090234-01, NIAID NIH HHS, United StatesR37-AI28724, NIAID NIH HHS, United StatesT32 AI007532, NIAID NIH HHS, United StatesT32 AI055400, NIAID NIH HHS, United States

PY - 2012/9/21

Y1 - 2012/9/21

N2 - Interferon-γ (IFN-γ) promotes a population of T-bet+ CXCR3+ regulatory T (Treg) cells that limit T helper 1 (Th1) cell-mediated pathology. Our studies demonstrate that interleukin-27 (IL-27) also promoted expression of T-bet and CXCR3 in Treg cells. During infection with Toxoplasma gondii, a similar population emerged that limited T cell responses and was dependent on IFN-γ in the periphery but on IL-27 at mucosal sites. Transfer of Treg cells ameliorated the infection-induced pathology observed in Il27-/- mice, and this was dependent on their ability to produce IL-10. Microarray analysis revealed that Treg cells exposed to either IFN-γ or IL-27 have distinct transcriptional profiles. Thus, IFN-γ and IL-27 have different roles in Treg cell biology and IL-27 is a key cytokine that promotes the development of Treg cells specialized to control Th1 cell-mediated immunity at local sites of inflammation. © 2012 Elsevier Inc.

AB - Interferon-γ (IFN-γ) promotes a population of T-bet+ CXCR3+ regulatory T (Treg) cells that limit T helper 1 (Th1) cell-mediated pathology. Our studies demonstrate that interleukin-27 (IL-27) also promoted expression of T-bet and CXCR3 in Treg cells. During infection with Toxoplasma gondii, a similar population emerged that limited T cell responses and was dependent on IFN-γ in the periphery but on IL-27 at mucosal sites. Transfer of Treg cells ameliorated the infection-induced pathology observed in Il27-/- mice, and this was dependent on their ability to produce IL-10. Microarray analysis revealed that Treg cells exposed to either IFN-γ or IL-27 have distinct transcriptional profiles. Thus, IFN-γ and IL-27 have different roles in Treg cell biology and IL-27 is a key cytokine that promotes the development of Treg cells specialized to control Th1 cell-mediated immunity at local sites of inflammation. © 2012 Elsevier Inc.

U2 - 10.1016/j.immuni.2012.06.014

DO - 10.1016/j.immuni.2012.06.014

M3 - Article

C2 - 22981537

SN - 1097-4180

VL - 37

SP - 511

EP - 523

JO - Immunity

JF - Immunity

IS - 3

ER -

The Cytokines Interleukin 27 and Interferon-γ Promote Distinct Treg Cell Populations Required to Limit Infection-Induced Pathology

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