Immunomodulation by interleukin-33 is protective in stroke through modulation of inflammation

Brain, Behavior, and Immunity

Volumn 49, Issue , 2015, Pages 322-336

  Korhonen, Paula ^a   Kanninen, Katja M ^a   Lehtonen, Šárka ^a   Lemarchant, Sighild ^a   Puttonen, Katja A ^a   Oksanen, Minna ^a   Dhungana, Hiramani ^a   Loppi, Sanna ^a   Pollari, Eveliina ^a   Wojciechowski, Sara ^a   Kidin, Iurii ^a   García Berrocoso, Teresa ^b   Giralt, Dolors ^b   Montaner, Joan ^c   Koistinaho, Jari ^a   Malm, Tarja ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

Author keywords

Cerebral stroke; Cytokines; Inflammation; Interleukin; Peripheral immune system

Indexed keywords

ARGINASE 1; INTERLEUKIN 33; INTERLEUKIN 4; INTERLEUKIN 4 ANTIBODY; INTERLEUKIN RECEPTOR; RECOMBINANT CYTOKINE; RECOMBINANT INTERLEUKIN 33; SOLUBLE ST2 RECEPTOR; UNCLASSIFIED DRUG; CYTOKINE; IL33 PROTEIN, MOUSE; RECOMBINANT PROTEIN; SOMATOSTATIN RECEPTOR;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN CORTEX; BRAIN LEVEL; CELL ACTIVATION; CELL DEATH; CELLULAR IMMUNITY; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE ASSOCIATION; DISEASE COURSE; EMBRYO; FEMALE; FOREFOOT; HUMAN; HUMAN CELL; IMMUNOMODULATION; IMMUNOREACTIVITY; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; MICROGLIA; MOUSE; NEUROPROTECTION; NONHUMAN; PHYSICAL SENSITIVITY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SINGLE BLIND PROCEDURE; SPLEEN; TH2 CELL; ANIMAL; BAGG ALBINO MOUSE; BLOOD; BRAIN; BRAIN ISCHEMIA; CELL CULTURE; DRUG EFFECTS; IMMUNOLOGY; INFLAMMATION; METABOLISM; MOTOR ACTIVITY; STROKE; T LYMPHOCYTE;

AGED; ANIMALS; ASTROCYTES; BRAIN; BRAIN ISCHEMIA; CELLS, CULTURED; CYTOKINES; FEMALE; HUMANS; INFLAMMATION; INTERLEUKIN-33; INTERLEUKIN-4; MACROPHAGES; MALE; MICE; MICE, INBRED BALB C; MICROGLIA; MOTOR ACTIVITY; RECEPTORS, SOMATOSTATIN; RECOMBINANT PROTEINS; SPLEEN; STROKE; T-LYMPHOCYTES;

EID: 84940598082     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2015.06.013     Document Type: Article

References (59)

1. Aoki S., Hayakawa M., Ozaki H., Takezako N., Obata H., Ibaraki N., Tsuru T., Tominaga S., Yanagisawa K. ST2 gene expression is proliferation-dependent and its ligand, IL-33, induces inflammatory reaction in endothelial cells. Mol. Cell. Biochem. 2010, 335(1-2):75-81.
2. Besnard A.G., Togbe D., Guillou N., Erard F., Quesniaux V., Ryffel B. IL-33-activated dendritic cells are critical for allergic airway inflammation. Eur. J. Immunol. 2011, 41(6):1675-1686. 10.1002/eji.201041033.
3. Bouet V., Boulouard M., Toutain J., Divoux D., Bernaudin M., Schumann-Bard P., Freret T. The adhesive removal test: a sensitive method to assess sensorimotor deficits in mice. Nat. Protoc. 2009, 4(10):1560-1564. 10.1038/nprot.2009.125.
4. Brodie C., Goldreich N., Haiman T., Kazimirsky G. Functional IL-4 receptors on mouse astrocytes: IL-4 inhibits astrocyte activation and induces NGF secretion. J. Neuroimmunol. 1998, 81(1-2):20-30.
5. Brown M.E., Rondon E., Rajesh D., Mack A., Lewis R., Feng X., Nuwaysir E.F. Derivation of induced pluripotent stem cells from human peripheral blood T lymphocytes. PLoS One 2010, 5(6):e11373. 10.1371/journal.pone.0011373.
6. Butovsky O., Ziv Y., Schwartz A., Landa G., Talpalar A.E., Pluchino S., Schwartz M. Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol. Cell. Neurosci. 2006, 31(1):149-160. S1044-7431(05)00248-4 [pii].
7. Carriere V., Roussel L., Ortega N., Lacorre D.A., Americh L., Aguilar L., Girard J.P. IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-associated nuclear factor in vivo. Proc. Natl. Acad. Sci. U.S.A. 2007, 104(1):282-287. 10.1073/pnas.0606854104.
8. Chen C.J., Kono H., Golenbock D., Reed G., Akira S., Rock K.L. Identification of a key pathway required for the sterile inflammatory response triggered by dying cells. Nat. Med. 2007, 13(7):851-856. 10.1038/nm1603.
9. Christophi G.P., Gruber R.C., Panos M., Christophi R.L., Jubelt B., Massa P.T. Interleukin-33 upregulation in peripheral leukocytes and CNS of multiple sclerosis patients. Clin. Immunol. (Orlando, Fla) 2012, 142(3):308-319. 10.1016/j.clim.2011.11.007.
10. Clausen B.H., Lambertsen K.L., Babcock A.A., Holm T.H., Dagnaes-Hansen F., Finsen B. Interleukin-1beta and tumor necrosis factor-alpha are expressed by different subsets of microglia and macrophages after ischemic stroke in mice. J. Neuroinflamm. 2008, 5:46. 10.1186/1742-2094-5-46.
11. Denes A., Humphreys N., Lane T.E., Grencis R., Rothwell N. Chronic systemic infection exacerbates ischemic brain damage via a CCL5 (regulated on activation, normal T-cell expressed and secreted)-mediated proinflammatory response in mice. J. Neurosci. 2010, 30(30):10086-10095. 10.1523/JNEUROSCI.1227-10.2010.
12. Dhungana H., Malm T., Denes A., Valonen P., Wojciechowski S., Magga J., Koistinaho J. Aging aggravates ischemic stroke-induced brain damage in mice with chronic peripheral infection. Aging Cell 2013, 12(5):842-850. 10.1111/acel.12106.
13. Dhungana H., Rolova T., Savchenko E., Wojciechowski S., Savolainen K., Ruotsalainen A.K., Malm T. Western-type diet modulates inflammatory responses and impairs functional outcome following permanent middle cerebral artery occlusion in aged mice expressing the human apolipoprotein E4 allele. J. Neuroinflamm. 2013, 10:102. 10.1186/1742-2094-10-102.
14. Duan L., Chen J., Zhang H., Yang H., Zhu P., Xiong A., Fang M. Interleukin-33 ameliorates experimental colitis through promoting Th2/Foxp3(+) regulatory T-cell responses in mice. Mol. Med. (Cambridge, Mass) 2012, 18:753-761. 10.2119/molmed.2011.00428.
15. Estes M.L., Iwasaki K., Jacobs B.S., Barna B.P. Interleukin-4 down-regulates adult human astrocyte DNA synthesis and proliferation. Am. J. Pathol. 1993, 143(2):337-341.
16. Gelderblom M., Leypoldt F., Steinbach K., Behrens D., Choe C.U., Siler D.A., Magnus T. Temporal and spatial dynamics of cerebral immune cell accumulation in stroke. Stroke 2009, 40(5):1849-1857. 10.1161/STROKEAHA.108.534503.
17. Girard S., Brough D., Lopez-Castejon G., Giles J., Rothwell N.J., Allan S.M. Microglia and macrophages differentially modulate cell death after brain injury caused by oxygen-glucose deprivation in organotypic brain slices. Glia 2013, 61(5):813-824. 10.1002/glia.22478.
18. Gordon S. Alternative activation of macrophages. Nat. Rev. Immunol. 2003, 3(1):23-35. 10.1038/nri978.
19. Hallenbeck J.M. The many faces of tumor necrosis factor in stroke. Nat. Med. 2002, 8(12):1363-1368. 10.1038/nm1202-1363.
20. Hayakawa H., Hayakawa M., Kume A., Tominaga S. Soluble ST2 blocks interleukin-33 signaling in allergic airway inflammation. J. Biol. Chem. 2007, 282(36):26369-26380. 10.1074/jbc.M704916200.
21. Hill J.K., Gunion-Rinker L., Kulhanek D., Lessov N., Kim S., Clark W.M., Eckenstein F.P. Temporal modulation of cytokine expression following focal cerebral ischemia in mice. Brain Res. 1999, 820(1-2):45-54. S0006-8993(98)01140-8 [pii].
22. Hu X., Li P., Guo Y., Wang H., Leak R.K., Chen S., Chen J. Microglia/macrophage polarization dynamics reveal novel mechanism of injury expansion after focal cerebral ischemia. Stroke 2012, 43(11):3063-3070. 10.1161/STROKEAHA.112.659656.
23. Hudson C.A., Christophi G.P., Gruber R.C., Wilmore J.R., Lawrence D.A., Massa P.T. Induction of IL-33 expression and activity in central nervous system glia. J. Leukoc. Biol. 2008, 84(3):631-643. 10.1189/jlb.1207830.
24. Iadecola C., Anrather J. The immunology of stroke: from mechanisms to translation. Nat. Med. 2011, 17(7):796-808. 10.1038/nm.2399.
25. Jander S., Kraemer M., Schroeter M., Witte O.W., Stoll G. Lymphocytic infiltration and expression of intercellular adhesion molecule-1 in photochemically induced ischemia of the rat cortex. J. Cereb. Blood Flow Metab. 1995, 15(1):42-51. 10.1038/jcbfm.1995.5.
26. Jiang H.R., Milovanovic M., Allan D., Niedbala W., Besnard A.G., Fukada S.Y., Liew F.Y. IL-33 attenuates EAE by suppressing IL-17 and IFN-gamma production and inducing alternatively activated macrophages. Eur. J. Immunol. 2012, 42(7):1804-1814. 10.1002/eji.201141947.
27. Jin Q., Cheng J., Liu Y., Wu J., Wang X., Wei S., Zhen X. Improvement of functional recovery by chronic metformin treatment is associated with enhanced alternative activation of microglia/macrophages and increased angiogenesis and neurogenesis following experimental stroke. Brain Behav. Immun. 2014, 40:131-142. 10.1016/j.bbi.2014.03.003.
28. Kamel A., Iadecola C. Brain-immune interactions and ischemic stroke: clinical implications. Arch. Neurol. 2012, 69(5):576-581. 10.1001/archneurol.2011.3590.
29. Kigerl K.A., Gensel J.C., Ankeny D.P., Alexander J.K., Donnelly D.J., Popovich P.G. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J. Neurosci. 2009, 29(43):13435-13444. 10.1523/JNEUROSCI.3257-09.2009.
30. Kurowska-Stolarska M., Stolarski B., Kewin P., Murphy G., Corrigan C.J., Ying S., Liew F.Y. IL-33 amplifies the polarization of alternatively activated macrophages that contribute to airway inflammation. J. Immunol. (Baltimore, Md.: 1950) 2009, 183(10):6469-6477. 10.4049/jimmunol.0901575.
31. Lambertsen K.L., Meldgaard M., Ladeby R., Finsen B. A quantitative study of microglial-macrophage synthesis of tumor necrosis factor during acute and late focal cerebral ischemia in mice. J. Cereb. Blood Flow Metab. 2005, 25(1):119-135. 9600014 [pii].
32. Liesz A., Suri-Payer E., Veltkamp C., Doerr H., Sommer C., Rivest S., Veltkamp R. Regulatory T cells are key cerebroprotective immunomodulators in acute experimental stroke. Nat. Med. 2009, 15(2):192-199. 10.1038/nm.1927.
33. Luo Y., Zhou Y., Xiao W., Liang Z., Dai J., Weng X., Wu X. Interleukin-33 ameliorates ischemic brain injury in experimental stroke through promoting Th2 response and suppressing Th17 response. Brain Res. 2014, S0006-8993(14)01674-6 [pii].
34. Mantovani A., Sica A., Sozzani S., Allavena P., Vecchi A., Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004, 25(12):677-686. S1471-4906(04)00295-9 [pii].
35. Martinez F.O., Sica A., Mantovani A., Locati M. Macrophage activation and polarization. Front. Biosci. 2008, 13:453-461. 2692 [pii].
36. Mildner M., Storka A., Lichtenauer M., Mliz V., Ghannadan M., Hoetzenecker K., Nickl S., Dome B., Tschachler E., Ankersmit H.J. Primary sources and immunological prerequisites for sST2 secretion in humans. Cardiovasc. Res. 2010, 87(4):769-777.
37. Miller A.M., Xu D., Asquith D.L., Denby L., Li Y., Sattar N., Liew F.Y. IL-33 reduces the development of atherosclerosis. J. Exp. Med. 2008, 205(2):339-346. 10.1084/jem.20071868.
38. Milovanovic M., Volarevic V., Ljujic B., Radosavljevic G., Jovanovic I., Arsenijevic N., Lukic M.L. Deletion of IL-33R (ST2) abrogates resistance to EAE in BALB/C mice by enhancing polarization of APC to inflammatory phenotype. PLoS One 2012, 7(9):e45225. 10.1371/journal.pone.0045225.
39. Montgomery S.L., Bowers W.J. Tumor necrosis factor-alpha and the roles it plays in homeostatic and degenerative processes within the central nervous system. J. Neuroimmune Pharmacol. 2012, 7(1):42-59. 10.1007/s11481-011-9287-2.
40. Moulin D., Donze O., Talabot-Ayer D., Mezin F., Palmer G., Gabay C. Interleukin (IL)-33 induces the release of pro-inflammatory mediators by mast cells. Cytokine 2007, 40(3):216-225. S1043-4666(07)00428-0 [pii].
41. Murray K.N., Buggey H.F., Denes A., Allan S.M. Systemic immune activation shapes stroke outcome. Mol. Cell. Neurosci. 2013, 53:14-25. 10.1016/j.mcn.2012.09.00.
42. Pecaric-Petkovic T., Didichenko S.A., Kaempfer S., Spiegl N., Dahinden C.A. Human basophils and eosinophils are the direct target leukocytes of the novel IL-1 family member IL-33. Blood 2009, 113(7):1526-1534. 10.1182/blood-2008-05-157818.
43. Pihlaja R., Koistinaho J., Kauppinen R., Sandholm J., Tanila H., Koistinaho M. Multiple cellular and molecular mechanisms are involved in human abeta clearance by transplanted adult astrocytes. Glia 2011, 59(11):1643-1657. 10.1002/glia.21212.
44. Pomeshchik Y., Kidin I., Korhonen P., Savchenko E., Jaronen M., Lehtonen S., Malm T. Interleukin-33 treatment reduces secondary injury and improves functional recovery after contusion spinal cord injury. Brain Behav. Immun. 2014, S0889-1591(14)00419-X [pii].
45. Raskob G.E., Angchaisuksiri P., Blanco A.N., Buller H., Gallus A., Hunt B.J. Thrombosis: a major contributor to global disease burden. Arterioscler. Thromb. Vasc. Biol. 2014, 34(11):2363-2371. ISTH Steering Committee for World Thrombosis Day. 10.1161/ATVBAHA.114.304488.
46. Schallert T., Fleming S.M., Leasure J.L., Tillerson J.L., Bland S.T. CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 2000, 39(5):777-787. S0028390800000058 [pii].
47. Schellinger P.D., Fiebach J.B., Mohr A., Ringleb P.A., Jansen O., Hacke W. Thrombolytic therapy for ischemic stroke - a review. Part II - intra-arterial thrombolysis, vertebrobasilar stroke, phase IV trials, and stroke imaging. Crit. Care Med. 2001, 29(9):1819-1825.
48. Schmitz J., Owyang A., Oldham E., Song Y., Murphy E., McClanahan T.K., Kastelein R.A. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 2005, 23(5):479-490. 10.1016/j.immuni.2005.09.015.
49. Schroeter M., Jander S. T-cell cytokines in injury-induced neural damage and repair. Neuromol. Med. 2005, 7(3):183-195. 10.1385/NMM:7:3:183.
50. Shimpo M., Morrow D.A., Weinberg E.O., Sabatine M.S., Murphy S.A., Antman E.M., Lee R.T. Serum levels of the interleukin-1 receptor family member ST2 predict mortality and clinical outcome in acute myocardial infarction. Circulation 2004, 109(18):2186-2190. 10.1161/01.CIR.0000127958.21003.5A.
51. Shuaib A., Xu Wang C., Yang T., Noor R. Effects of nonpeptide V(1) vasopressin receptor antagonist SR-49059 on infarction volume and recovery of function in a focal embolic stroke model. Stroke 2002, 33(12):3033-3037.
52. Stein M., Keshav S., Harris N., Gordon S. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J. Exp. Med. 1992, 176(1):287-292.
53. Turnquist H.R., Zhao Z., Rosborough B.R., Liu Q., Castellaneta A., Isse K., Thomson A.W. IL-33 expands suppressive CD11b+ gr-1(int) and regulatory T cells, including ST2L+ Foxp3+ cells, and mediates regulatory T cell-dependent promotion of cardiac allograft survival. J. Immunol. (Baltimore, Md.: 1950) 2011, 187(9):4598-4610. 10.4049/jimmunol.1100519.
54. Wajant H., Pfizenmaier K., Scheurich P. Tumor necrosis factor signaling. Cell Death Differ. 2003, 10(1):45-65. 10.1038/sj.cdd.4401189.
55. Wang X., Yue T.L., Barone F.C., White R.F., Gagnon R.C., Feuerstein G.Z. Concomitant cortical expression of TNF-alpha and IL-1 beta mRNAs follows early response gene expression in transient focal ischemia. Mol. Chem. Neuropathol. 1994, 23(2-3):103-114.
56. Wasserman A., Ben-Shoshan J., Entin-Meer M., Maysel-Auslender S., Guzner-Gur H., Keren G. Interleukin-33 augments treg cell levels: a flaw mechanism in atherosclerosis. Isr. Med. Assoc. J. 2012, 14(10):620-623.
57. Xiong X., Barreto G.E., Xu L., Ouyang Y.B., Xie X., Giffard R.G. Increased brain injury and worsened neurological outcome in interleukin-4 knockout mice after transient focal cerebral ischemia. Stroke 2011, 42(7):2026-2032. 10.1161/STROKEAHA.110.593772.
58. Yasuoka S., Kawanokuchi J., Parajuli B., Jin S., Doi Y., Noda M., Suzumura A. Production and functions of IL-33 in the central nervous system. Brain Res. 2011, 1385:8-17. 10.1016/j.brainres.2011.02.045.
59. Zhang K., Zhang X.C., Mi Y.H., Liu J. Predicting value of serum soluble ST2 and interleukin-33 for risk stratification and prognosis in patients with acute myocardial infarction. Chin. Med. J. 2013, 126(19):3628-3631.