1054 VOLUME 14 NUMBER 10 OCTOBER 2013 NATURE IMMUNOLOGY
ARTICLES
The dysregulated activity of effector cells of the T
H
1 and T
H
17 subsets
of helper T cells results in the development of tissue inflammation
and autoimmunity. Myelin-specific T
H
1 and T
H
17 cells, for example,
contribute to disease pathogenesis in multiple sclerosis (MS)
1
and its
animal model, experimental autoimmune encephalomyelitis (EAE)
2
.
During EAE, dendritic cells (DCs) control the activation and differen-
tiation of myelin-specific effector T cells and regulatory T cells (T
reg
cells)
3,4
. Moreover, DCs isolated from patients with MS produce large
amounts of T
H
1- and T
H
17-polarizing cytokines
5
, which suggests
that DCs promote the generation of the pathogenic T cell response in
MS. Indeed, DCs control several pathogenic mechanisms associated
with the development of central nervous system (CNS) autoimmunity.
DCs promote the entry of T cells into the CNS
6
, the activation and
differentiation of pathogenic T cells in the CNS
3
and the spreading of
the autoimmune response to new CNS epitopes
7
. Thus, it is important
to study the pathways that regulate DC activity during the course of
autoimmunity, to identify mechanisms of disease pathogenesis and
also to develop new approaches for therapeutic intervention.
IL-27 is a cytokine structurally related to IL-12 and is composed of
a p28 subunit and the product of Epstein-Barr virus–induced gene 3
(Ebi3)
8
. IL-27 signals through a receptor composed of the common
IL-6 receptor chain gp130 (which is used by several other members
of the IL-6 and IL-12 families) and a unique IL-27 receptor α-chain
(IL-27RA) that is homologous to the IL-12Rβ2 chain of the IL-12
receptor
8
. IL-27 is produced by DCs in response to activation via
Toll-like receptors through a mechanism that involves the autocrine
effects of interferon-β (IFN-β)
9
. Indeed, the therapeutic effects of
IFN-β administration on relapsing-remitting MS have been linked
to the induction of IL-27 production by DCs
10
.
On the basis of its structural homology to IL-12 and its ability to
trigger IFN-γ production, IL-27 was initially thought to be a proin-
flammatory cytokine
11
. However, it was subsequently discovered
that IL-27 suppresses T
H
1, T
H
2 and T
H
17 responses and limits CNS
inflammation in several experimental models
8
. In the EAE model, the
administration of IL-27 inhibits disease development
12
. Conversely,
the lack of a functional IL-27 receptor results in exacerbated T
H
17
responses and the worsening of EAE
12,13
. IL-27 acts directly on T cells
to inhibit the development of pathogenic T
H
17 cells and to promote
the differentiation of IL-10-producing type 1 T
reg
cells (Tr1 cells)
12–17
.
Thus, the arrest of EAE by IL-27 is thought to reflect its direct effects
on T cells. However, several cell types beyond T cells express the
IL-27 receptor, but the relevance of IL-27 signaling in those cells for
the control of EAE and autoimmunity is unknown.
DCs express a functional IL-27 receptor
18
; however, although IL-27
has been reported to interfere with the activation of DCs in vitro
18–20
,
the physiological relevance of IL-27 signaling in DCs and its effects on
the control of the T cell response and autoimmunity are unknown. In
this work, we studied the effects of IL-27 signaling in DCs on the dif-
ferentiation of effector T cells and T
reg
cells and CNS autoimmunity.
We found that IL-27 signaling in DCs upregulated expression of the
immunoregulatory molecule CD39 (encoded by Entpd1) and lim-
ited the development of EAE. CD39 expressed by conventional DCs
(cDCs) reduced the extracellular concentration of ATP and decreased
ATP-triggered activation of the NLRP3 inflammasome. Moreover, we
1
Center for Neurologic Diseases, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts, USA.
2
The Mina and Everard Goodman Faculty of
Life Sciences, Bar Ilan University, Ramat Gan, Israel.
3
Division of Gastroenterology and Hepatology, Beth Israel Deaconess Medical Center, Harvard Medical School,
Boston, Massachusetts, USA.
4
These authors contributed equally to this work. Correspondence should be addressed to F.J.Q. (fquintana@rics.bwh.harvard.edu).
Received 18 March; accepted 19 July; published online 1 September 2013; doi:10.1038/ni.2695
IL-27 acts on DCs to suppress the T cell response
and autoimmunity by inducing expression of the
immunoregulatory molecule CD39
Ivan D Mascanfroni
1,4
, Ada Yeste
1,4
, Silvio M Vieira
1
, Evan J Burns
1
, Bonny Patel
1
, Ido Sloma
2
, Yan Wu
3
,
Lior Mayo
1
, Rotem Ben-Hamo
2
, Sol Efroni
2
, Vijay K Kuchroo
1
, Simon C Robson
3
& Francisco J Quintana
1
Dendritic cells (DCs) control the balance between effector T cells and regulatory T cells in vivo. Hence, the study of DCs might
identify mechanisms of disease pathogenesis and guide new therapeutic approaches for disorders mediated by the immune
system. We found that interleukin 27 (IL-27) signaling in mouse DCs limited the generation of effector cells of the T
H
1 and T
H
17
subsets of helper T cells and the development of experimental autoimmune encephalomyelitis (EAE). The effects of IL-27 were
mediated at least in part through induction of the immunoregulatory molecule CD39 in DCs. IL-27-induced CD39 decreased the
extracellular concentration of ATP and downregulated nucleotide-dependent activation of the NLRP3 inflammasome. Finally,
therapeutic vaccination with IL-27-conditioned DCs suppressed established relapsing-remitting EAE. Thus, IL-27 signaling in
DCs limited pathogenic T cell responses and the development of autoimmunity.
npg
© 2013 Nature America, Inc. All rights reserved.