Abstract
Lymphocyte recruitment and activation have been implicated in the progression of cerebral ischemia-reperfusion (I/R) injury, but the roles of specific lymphocyte subpopulations and cytokines during stroke remain to be clarified. Here we demonstrate that the infiltration of T cells into the brain, as well as the cytokines interleukin-23 (IL-23) and IL-17, have pivotal roles in the evolution of brain infarction and accompanying neurological deficits. Blockade of T cell infiltration into the brain by the immunosuppressant FTY720 reduced I/R-induced brain damage. The expression of IL-23, which was derived mostly from infiltrated macrophages, increased on day 1 after I/R, whereas IL-17 levels were elevated after day 3, and this induction of IL-17 was dependent on IL-23. These data, together with analysis of mice genetically disrupted for IL-17 and IL-23, suggest that IL-23 functions in the immediate stage of I/R brain injury, whereas IL-17 has an important role in the delayed phase of I/R injury during which apoptotic neuronal death occurs in the penumbra. Intracellular cytokine staining revealed that gammadeltaT lymphocytes, but not CD4(+) helper T cells, were a major source of IL-17. Moreover, depletion of gammadeltaT lymphocytes ameliorated the I/R injury. We propose that T lymphocytes, including gammadeltaT lymphocytes, could be a therapeutic target for mitigating the inflammatory events that amplify the initial damage in cerebral ischemia.
MeSH Terms
Animals
Brain Injuries/etiology,genetics,immunology,metabolism
Brain Ischemia/complications,genetics,immunology,metabolism
DNA-Binding Proteins/genetics
Interferon-gamma/genetics
Interleukin-17/genetics,metabolism
Interleukin-23 Subunit p19/genetics
Mice
Mice, Knockout
Receptors, Antigen, T-Cell, gamma-delta/genetics,metabolism
Reperfusion Injury/genetics,immunology,metabolism
T-Lymphocytes/metabolism,physiology
Time Factors
Chemicals
DNA-Binding Proteins
Interleukin-17
Interleukin-23 Subunit p19
Rag2 protein, mouse
Receptors, Antigen, T-Cell, gamma-delta
Interferon-gamma
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Shichita Takashi
Department of Microbiology and Immunology, School of Medicine, Keio University, Tokyo, Japan.
Sugiyama Yuki
Ooboshi Hiroaki
Sugimori Hiroshi
Nakagawa Ryusuke
Takada Ichiro
Iwaki Toru
Okada Yasunori
Iida Mitsuo
Cua Daniel J
Iwakura Yoichiro
Yoshimura Akihiko
References (33)
33 references, click to expand
-
A role for interferon-gamma in focal cerebral ischemia in mice.
J Neuropathol Exp Neurol. 2004 Sep;63(9):942-55
PMID: 15453093
-
Inhibition of interleukin 1beta converting enzyme family proteases reduces ischemic and excitotoxic neuronal damage.
Proc Natl Acad Sci U S A. 1997 Mar 4;94(5):2007-12
PMID: 9050895
-
Matrix metalloproteinase expression increases after cerebral focal ischemia in rats: inhibition of matrix metalloproteinase-9 reduces infarct size.
Stroke. 1998 May;29(5):1020-30
PMID: 9596253
-
Tyk2-signaling plays an important role in host defense against Escherichia coli through IL-23-induced IL-17 production by gammadelta T cells.
J Immunol. 2008 Aug 1;181(3):2071-5
PMID: 18641345
-
Role of T lymphocytes and interferon-gamma in ischemic stroke.
Circulation. 2006 May 2;113(17):2105-12
PMID: 16636173
-
Apoptosis and necrosis after reversible focal ischemia: an in situ DNA fragmentation analysis.
J Cereb Blood Flow Metab. 1996 Mar;16(2):186-94
PMID: 8594049
-
Expression of interleukin-17 in ischemic brain tissue.
Scand J Immunol. 2005 Nov;62(5):481-6
PMID: 16305645
-
Tissue inhibitor of metalloproteinases protect blood-brain barrier disruption in focal cerebral ischemia.
J Cereb Blood Flow Metab. 2008 Oct;28(10):1674-85
PMID: 18560439
-
Resident Vdelta1+ gammadelta T cells control early infiltration of neutrophils after Escherichia coli infection via IL-17 production.
J Immunol. 2007 Apr 1;178(7):4466-72
PMID: 17372004
-
Lymphocytic infiltration and expression of intercellular adhesion molecule-1 in photochemically induced ischemia of the rat cortex.
J Cereb Blood Flow Metab. 1995 Jan;15(1):42-51
PMID: 7528223
-
Postischemic gene transfer of interleukin-10 protects against both focal and global brain ischemia.
Circulation. 2005 Feb 22;111(7):913-9
PMID: 15710762
-
Thymic selection determines gammadelta T cell effector fate: antigen-naive cells make interleukin-17 and antigen-experienced cells make interferon gamma.
Immunity. 2008 Jul 18;29(1):90-100
PMID: 18585064
-
Krypton laser-induced photothrombotic distal middle cerebral artery occlusion without craniectomy in mice.
Brain Res Brain Res Protoc. 2004 Aug;13(3):189-96
PMID: 15296857
-
Interleukin-1 as a pathogenetic mediator of ischemic brain damage in rats.
Stroke. 1995 Apr;26(4):676-80; discussion 681
PMID: 7709417
-
Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis.
Nat Med. 2002 May;8(5):500-8
PMID: 11984595
-
A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17.
Nat Immunol. 2005 Nov;6(11):1133-41
PMID: 16200068
-
Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation.
Nat Med. 2007 Oct;13(10):1173-5
PMID: 17828272
-
Metabolic penumbra of acute brain infarction: a correlation with infarct growth.
Ann Neurol. 2005 Apr;57(4):495-504
PMID: 15786459
-
IL-23 drives a pathogenic T cell population that induces autoimmune inflammation.
J Exp Med. 2005 Jan 17;201(2):233-40
PMID: 15657292
-
Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses.
Immunity. 2002 Sep;17(3):375-87
PMID: 12354389
-
Regulatory T cells are key cerebroprotective immunomodulators in acute experimental stroke.
Nat Med. 2009 Feb;15(2):192-9
PMID: 19169263
-
Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain.
Nature. 2003 Feb 13;421(6924):744-8
PMID: 12610626
-
A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis.
J Exp Med. 2006 Jul 10;203(7):1685-91
PMID: 16818675
-
Astrocytic activation and delayed infarct expansion after permanent focal ischemia in rats. Part I: enhanced astrocytic synthesis of s-100beta in the periinfarct area precedes delayed infarct expansion.
J Cereb Blood Flow Metab. 2002 Jun;22(6):711-22
PMID: 12045670
-
Expression of a dominant negative mutant of interleukin-1 beta converting enzyme in transgenic mice prevents neuronal cell death induced by trophic factor withdrawal and ischemic brain injury.
J Exp Med. 1997 Mar 3;185(5):933-40
PMID: 9120399
-
Local immune responses in the rat cerebral cortex after middle cerebral artery occlusion.
J Neuroimmunol. 1994 Dec;55(2):195-203
PMID: 7530260
-
Anti-IL-23 therapy inhibits multiple inflammatory pathways and ameliorates autoimmune encephalomyelitis.
J Clin Invest. 2006 May;116(5):1317-26
PMID: 16670771
-
Flow cytometric analysis of inflammatory cells in ischemic rat brain.
Stroke. 2002 Feb;33(2):586-92
PMID: 11823674
-
Metalloproteinases in biology and pathology of the nervous system.
Nat Rev Neurosci. 2001 Jul;2(7):502-11
PMID: 11433375
-
The blood-brain barrier induces differentiation of migrating monocytes into Th17-polarizing dendritic cells.
Brain. 2008 Mar;131(Pt 3):785-99
PMID: 18156156
-
Loss of suppressor of cytokine signaling 1 in helper T cells leads to defective Th17 differentiation by enhancing antagonistic effects of IFN-gamma on STAT3 and Smads.
J Immunol. 2008 Mar 15;180(6):3746-56
PMID: 18322180
-
Establishing final infarct volume: stroke lesion evolution past 30 days is insignificant.
Stroke. 2008 Oct;39(10):2765-8
PMID: 18635854
-
Experimental treatments for acute ischaemic stroke.
Lancet. 2007 Jan 27;369(9558):331-41
PMID: 17258673