554 VOLUME 15 NUMBER 6 JUNE 2014 NATURE IMMUNOLOGY
The thymic microenvironment is unique in its capacity to promote
the development of naive T cells. TECs are essential for this function
as they control the attraction of blood-borne lymphoid precursors and
subsequently facilitate their proliferation, differentiation and selec-
tion to functionally competent T cells
1
. Based on their phenotype,
anatomical localization and function, TECs can be distinguished into
separate and functionally distinct subpopulations. Cortical (c)TECs
initiate and control early stages of thymocyte development includ-
ing the T cell antigen receptor (TCR)-mediated positive selection of
cells that express a functional TCR
2,3
. In contrast, mTECs enforce the
negative selection of thymocytes, control the formation of regulatory
T cells, and influence the postselection maturation of naive T cells
and their subsequent exit to the periphery
1,4
.
TEC differentiation itself relies on signals mediated by developing
T cells at distinct stages of their maturation, which provides
an instructive illustration of cellular cross-talk in the thymus
5
. For
example, engagement of the receptors RANK, CD40 or LTβ activates
the noncanonical NF-κB pathway and consequently controls the
differentiation of mTECs
6–11
as well as their capacity to express
a broad range of tissue-restricted antigens (TRAs)
12
. These TRAs
provide a largely comprehensive array of an individual’s antigens
and thus present a molecular mirror of ‘immunological self’.
Transcriptional regulation of the expression of TRAs is partly depend-
ent on the transcriptional factor Aire, which is typically expressed
by a subpopulation of mature mTECs
13,14
. A failure to correctly
induce differentiation of mTECs and consequently expression of Aire
compromises expression of TRAs and thus impacts the deletion of
autoreactive T cells
15
.
TGF-β is a widely expressed, highly conserved cytokine that acts
on a large variety of cells
16
. TGF-β transmits its signals via binding
to the type II receptor TGFβRII that consequently associates with the
type I receptor TGFβRI and thus activates its serine/threonine kinase
activity. In the thymus, TGF-β is expressed by cortical epithelial cells
and immature thymocytes that release bioactive TGF-β as part of
their programmed cell death
17,18
. A positive regulatory role for TGF-β
signaling in development of intrathymic T cell has been proposed for
CD8
+
T cells, thymic regulatory T cells (tT
reg
cells) in very young mice
and natural killer T cells
19
. In contrast, the importance of TGF-β sig-
naling for TEC biology has not been sufficiently investigated though
a loss of TGFβRII expression on TECs mitigates the physiological
process of thymic senescence
20
. In this study, we provide evidence
for a negative role of TGF-β signaling in mTECs, which limits their
growth, differentiation and ultimately function.
RESULTS
TGF-b signaling controls the population expansion of mTECs
cTECs and mTECs express mRNAs for both chains of the TGF-β
receptor (ref. 20 and data not shown). To assess the role of TGF-β
signaling for TEC growth, differentiation and function, we investi-
gated mice with a targeted inactivation of Tgfbr2, the gene encoding
the TGFβRII, in TECs. To delete TGFβRII specifically in TECs, we
crossed mice with a loxP-flanked Tgfbr2 allele (Tgfbr2
fl/fl
) to mice
expressing the Cre recombinase under the transcriptional control of
the Foxn1 promoter
21
(FN1-Cre). We observed complete deletion of
the targeted allele in TECs isolated from resultant homozygous mice
(designated Tgfbr2
fl/fl
FN1-Cre mice) as early as embryonic day 14
(E14) (Supplementary Fig. 1a).
We first determined the frequency and phenotype of thymic
epithelia isolated from mutant and control mice. We restricted this
analysis to Tgfbr2
fl/fl
FN1-Cre mice not older than 4 weeks of life
1
Immunology Program, Benaroya Research Institute at Virginia Mason, Seattle, Washington, USA.
2
Laboratory of Pediatric Immunology, Department of Biomedicine,
University of Basel, Basel, Switzerland.
3
Basel University’s Hospital, Basel, Switzerland.
4
Developmental Immunology, Department of Pediatrics, University of Oxford,
Oxford, UK.
5
These authors contributed equally to this work. Correspondence should be addressed to S.F.Z. (sziegler@benaroyaresearch.org).
Received 16 September 2013; accepted 11 March 2014; published online 13 April 2014; doi:10.1038/ni.2869
A regulatory role for TGF-b signaling in the
establishment and function of the thymic medulla
Mathias Hauri-Hohl
1
, Saulius Zuklys
2,3
, Georg A Holländer
2–5
& Steven F Ziegler
1,5
Medullary thymic epithelial cells (mTECs) are critical in establishing and maintaining the appropriate microenvironment
for negative selection and maturation of immunocompetent T cells with a self-tolerant T cell antigen receptor repertoire.
Cues that direct proliferation and maturation of mTECs are provided by members of the tumor necrosis factor (TNF)
superfamily expressed on developing thymocytes. Here we demonstrate a negative role of the morphogen TGF- b in
tempering these signals under physiological conditions, limiting both growth and function of the thymic medulla.
Eliminating TGF-b signaling specifically in TECs or by pharmacological means increased the size of the mTEC compartment,
enhanced negative selection and functional maturation of medullary thymocytes as well as the production of regulatory
T cells, thus reducing the autoreactive potential of peripheral T cells.
ARTICLES
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