Piepke et al. Journal of Neuroinflammation (2021) 18:265
https://doi.org/10.1186/s12974-021-02316-7
RESEARCH
Interleukin-10 improves stroke outcome
by controlling the detrimental Interleukin-17A
response
Marius Piepke
1
, Bettina H. Clausen
2
, Peter Ludewig
1
, Jonas H. Vienhues
1
, Tanja Bedke
3
, Ehsan Javidi
1
,
Björn Rissiek
1
, Larissa Jank
1
, Leonie Brockmann
3
, Inga Sandrock
4
, Karoline Degenhardt
1
, Alina Jander
1
,
Vanessa Roth
1
, Ines S. Schädlich
1
, Immo Prinz
5
, Richard A. Flavell
6
, Yasushi Kobayashi
6
, Thomas Renné
7
,
Christian Gerloff
1
, Samuel Huber
3
, Tim Magnus
1
and Mathias Gelderblom
1*
Abstract
Background: Lymphocytes have dichotomous functions in ischemic stroke. Regulatory T cells are protective, while
IL-17A from innate lymphocytes promotes the infarct growth. With recent advances of T cell-subtype specific trans-
genic mouse models it now has become possible to study the complex interplay of T cell subpopulations in ischemic
stroke.
Methods: In a murine model of experimental stroke we analyzed the effects of IL-10 on the functional outcome for
up to 14 days post-ischemia and defined the source of IL-10 in ischemic brains based on immunohistochemistry, flow
cytometry, and bone-marrow chimeric mice. We used neutralizing IL-17A antibodies, intrathecal IL-10 injections, and
transgenic mouse models which harbor a deletion of the IL-10R on distinct T cell subpopulations to further explore
the interplay between IL-10 and IL-17A pathways in the ischemic brain.
Results: We demonstrate that IL-10 deficient mice exhibit significantly increased infarct sizes on days 3 and 7 and
enlarged brain atrophy and impaired neurological outcome on day 14 following tMCAO. In ischemic brains IL-10
producing immune cells included regulatory T cells, macrophages, and microglia. Neutralization of IL-17A follow-
ing stroke reversed the worse outcome in IL-10 deficient mice and intracerebral treatment with recombinant IL-10
revealed that IL-10 controlled IL-17A positive lymphocytes in ischemic brains. Importantly, IL-10 acted differentially on
αβ and γδ T cells. IL-17A producing CD4
+
αβ T cells were directly controlled via their IL-10-receptor (IL-10R), whereas
IL-10 by itself had no direct effect on the IL-17A production in γδ T cells. The control of the IL-17A production in γδ T
cells depended on an intact IL10R signaling in regulatory T cells (Tregs).
Conclusions: Taken together, our data indicate a key function of IL-10 in restricting the detrimental IL-17A-signaling
in stroke and further supports that IL-17A is a therapeutic opportunity for stroke treatment.
Keywords: Stroke, Ischemia, Inflammation, T cells, Interleukin-10, Interleukin-17
© The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which
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Background
Worldwide, stroke is one of the leading causes of mortal-
ity and sustained disability, with 5.5 million deaths and
11 million disability-adjusted life-years in 2016 [1].
Inflammation is a key component of stroke pathophysi-
ology, with dichotomous effects on the affected tissue.
Open Access
*Correspondence: m.gelderblom@uke.de
1
Department of Neurology, University Medical Center Hamburg-
Eppendorf, Martinistraße 52, 20246 Hamburg, Germany
Full list of author information is available at the end of the article