IL-10-producing B-cells limit CNS inflammation and infarct volume in experimental stroke (original) (raw)
Ajmo CT Jr, Vernon DO, Collier L, Hall AA, Garbuzova-Davis S, Willing A, Pennypacker KR (2008) The spleen contributes to stroke-induced neurodegeneration. J Neurosci Res 86:2227–2234 ArticlePubMedCAS Google Scholar
Amantea D, Nappi G, Bernardi G, Bagetta G, Corasaniti MT (2009) Post-ischemic brain damage: pathophysiology and role of inflammatory mediators. FEBS J 276:13–26 ArticlePubMedCAS Google Scholar
Baird TA, Parsons MW, Barber PA, Butcher KS, Desmond PM, Tress BM, Colman PG, Jerums G, Chambers BR, Davis SM (2002) The influence of diabetes mellitus and hyperglycaemia on stroke incidence and outcome. J Clin Neurosci 9:618–626 ArticlePubMed Google Scholar
Becker KJ (2002) Anti-leukocyte antibodies: LeukArrest (Hu23F2G) and Enlimomab (R6.5) in acute stroke. Curr Med Res Opin 18(Suppl 2):s18–s22 ArticlePubMed Google Scholar
Blair PA, Chavez-Rueda KA, Evans JG, Shlomchik MJ, Eddaoudi A, Isenberg DA, Ehrenstein MR, Mauri C (2009) Selective targeting of B cells with agonistic anti-CD40 is an efficacious strategy for the generation of induced regulatory T2-like B cells and for the suppression of lupus in MRL/lpr mice. J Immunol 182:3492–3502 ArticlePubMedCAS Google Scholar
Buck BH, Liebeskind DS, Saver JL, Bang OY, Yun SW, Starkman S, Ali LK, Kim D, Villablanca JP, Salamon N, Razinia T, Ovbiagele B (2008) Early neutrophilia is associated with volume of ischemic tissue in acute stroke. Stroke 39:355–360 ArticlePubMed Google Scholar
Campanella M, Sciorati C, Tarozzo G, Beltramo M (2002) Flow cytometric analysis of inflammatory cells in ischemic rat brain. Stroke 33:586–592 ArticlePubMed Google Scholar
Carter NA, Vasconcellos R, Rosser EC, Tulone C, Munoz-Suano A, Kamanaka M, Ehrenstein MR, Flavell RA, Mauri C (2011) Mice lacking endogenous IL-10-producing regulatory B cells develop exacerbated disease and present with an increased frequency of Th1/Th17 but a decrease in regulatory T cells. J Immunol 186:5569–5579 ArticlePubMedCAS Google Scholar
Castillo J, Davalos A, Noya M (1997) Progression of ischaemic stroke and excitotoxic aminoacids. Lancet 349:79–83 ArticlePubMedCAS Google Scholar
Chen Y, Bodhankar S, Murphy SJ, Vandenbark AA, Alkayed NJ, Offner H (2012) Intrastriatal B-cell administration limits infarct size after stroke in B-cell deficient mice. Metab Brain Dis 27:487–493 ArticlePubMedCAS Google Scholar
Davalos A, Toni D, Iweins F, Lesaffre E, Bastianello S, Castillo J (1999) Neurological deterioration in acute ischemic stroke: potential predictors and associated factors in the European cooperative acute stroke study (ECASS) I. Stroke 30:2631–2636 ArticlePubMedCAS Google Scholar
de Bilbao F, Arsenijevic D, Moll T, Garcia-Gabay I, Vallet P, Langhans W, Giannakopoulos P (2009) In vivo over-expression of interleukin-10 increases resistance to focal brain ischemia in mice. J Neurochem 110:12–22 ArticlePubMed Google Scholar
DiLillo DJ, Matsushita T, Tedder TF (2010) B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann N Y Acad Sci 1183:38–57 ArticlePubMedCAS Google Scholar
Emsley HC, Hopkins SJ (2008) Acute ischaemic stroke and infection: recent and emerging concepts. Lancet Neurol 7:341–353 ArticlePubMed Google Scholar
Endharti AT, Rifa IM, Shi Z, Fukuoka Y, Nakahara Y, Kawamoto Y, Takeda K, Isobe K, Suzuki H (2005) Cutting edge: CD8+CD122+ regulatory T cells produce IL-10 to suppress IFN-gamma production and proliferation of CD8+ T cells. J Immunol 175:7093–7097 PubMedCAS Google Scholar
Evans JG, Chavez-Rueda KA, Eddaoudi A, Meyer-Bahlburg A, Rawlings DJ, Ehrenstein MR, Mauri C (2007) Novel suppressive function of transitional 2 B cells in experimental arthritis. J Immunol 178:7868–7878 PubMedCAS Google Scholar
Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM (2002) B cells regulate autoimmunity by provision of IL-10. Nat Immunol 3:944–950 ArticlePubMedCAS Google Scholar
Frenkel D, Huang Z, Maron R, Koldzic DN, Moskowitz MA, Weiner HL (2005) Neuroprotection by IL-10-producing MOG CD4+ T cells following ischemic stroke. J Neurol Sci 233:125–132 ArticlePubMedCAS Google Scholar
Gee JM, Kalil A, Shea C, Becker KJ (2007) Lymphocytes: potential mediators of postischemic injury and neuroprotection. Stroke 38:783–788 ArticlePubMed Google Scholar
Gray M, Miles K, Salter D, Gray D, Savill J (2007) Apoptotic cells protect mice from autoimmune inflammation by the induction of regulatory B cells. Proc Natl Acad Sci U S A 104:14080–14085 ArticlePubMedCAS Google Scholar
Hurn PD, Subramanian S, Parker SM, Afentoulis ME, Kaler LJ, Vandenbark AA, Offner H (2007) T- and B-cell-deficient mice with experimental stroke have reduced lesion size and inflammation. J Cereb Blood Flow Metab 27:1798–1805 ArticlePubMedCAS Google Scholar
Investigators EAST (2001) Use of anti-ICAM-1 therapy in ischemic stroke: Results of the enlimomab acute stroke trial. In: Neurology, 2001/10/24 Edition, pp 1428–1434
Kriz J (2006) Inflammation in ischemic brain injury: timing is important. Crit Rev Neurobiol 18:145–157 ArticlePubMedCAS Google Scholar
Liesz A, Suri-Payer E, Veltkamp C, Doerr H, Sommer C, Rivest S, Giese T, Veltkamp R (2009) Regulatory T cells are key cerebroprotective immunomodulators in acute experimental stroke. Nat Med 15:192–199 ArticlePubMedCAS Google Scholar
Lindsberg PJ, Carpen O, Paetau A, Karjalainen-Lindsberg ML, Kaste M (1996) Endothelial ICAM-1 expression associated with inflammatory cell response in human ischemic stroke. Circulation 94:939–945 ArticlePubMedCAS Google Scholar
Madan R et al (2009) Nonredundant roles for B cell-derived IL-10 in immune counter-regulation. J Immunol 183:2312–2320 ArticlePubMedCAS Google Scholar
Mann MK, Maresz K, Shriver LP, Tan Y, Dittel BN (2007) B cell regulation of CD4+CD25+ T regulatory cells and IL-10 via B7 is essential for recovery from experimental autoimmune encephalomyelitis. J Immunol 178:3447–3456 PubMedCAS Google Scholar
Matsushita T, Horikawa M, Iwata Y, Tedder TF (2010) Regulatory B cells (B10 cells) and regulatory T cells have independent roles in controlling experimental autoimmune encephalomyelitis initiation and late-phase immunopathogenesis. J Immunol 185:2240–2252 ArticlePubMedCAS Google Scholar
McColl BW, Rothwell NJ, Allan SM (2007) Systemic inflammatory stimulus potentiates the acute phase and CXC chemokine responses to experimental stroke and exacerbates brain damage via interleukin-1- and neutrophil-dependent mechanisms. J Neurosci 27:4403–4412 ArticlePubMedCAS Google Scholar
McColl BW, Allan SM, Rothwell NJ (2009) Systemic infection, inflammation and acute ischemic stroke. Neuroscience 158:1049–1061 ArticlePubMedCAS Google Scholar
Mohrs M, Shinkai K, Mohrs K, Locksley RM (2001) Analysis of type 2 immunity in vivo with a bicistronic IL-4 reporter. Immunity 15:303–311 ArticlePubMedCAS Google Scholar
Moore KW, de Waal MR, Coffman RL, O’Garra A (2001) Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19:683–765 ArticlePubMedCAS Google Scholar
Offner H, Hurn PD (2012) A novel hypothesis: regulatory b lymphocytes shape outcome from experimental stroke. Transl Stroke Res 3:324–330 ArticlePubMedCAS Google Scholar
Offner H, Subramanian S, Parker SM, Wang C, Afentoulis ME, Lewis A, Vandenbark AA, Hurn PD (2006b) Splenic atrophy in experimental stroke is accompanied by increased regulatory T cells and circulating macrophages. J Immunol 176:6523–6531 PubMedCAS Google Scholar
Offner H, Vandenbark AA, Hurn PD (2009) Effect of experimental stroke on peripheral immunity: CNS ischemia induces profound immunosuppression. Neuroscience 158:1098–1111 ArticlePubMedCAS Google Scholar
Ooboshi H, Ibayashi S, Shichita T, Kumai Y, Takada J, Ago T, Arakawa S, Sugimori H, Kamouchi M, Kitazono T, Iida M (2005) Postischemic gene transfer of interleukin-10 protects against both focal and global brain ischemia. Circulation 111:913–919 ArticlePubMedCAS Google Scholar
Pelidou SH, Kostulas N, Matusevicius D, Kivisakk P, Kostulas V, Link H (1999) High levels of IL-10 secreting cells are present in blood in cerebrovascular diseases. Eur J Neurol 6:437–442 ArticlePubMedCAS Google Scholar
Prestigiacomo CJ, Kim SC, Connolly ES Jr, Liao H, Yan SF, Pinsky DJ (1999) CD18-mediated neutrophil recruitment contributes to the pathogenesis of reperfused but not nonreperfused stroke. Stroke 30:1110–1117 ArticlePubMedCAS Google Scholar
Ren X, Akiyoshi K, Vandenbark AA, Hurn PD, Offner H (2011a) Programmed death-1 pathway limits central nervous system inflammation and neurologic deficits in murine experimental stroke. Stroke 42:2578–2583 ArticlePubMed Google Scholar
Ren X, Akiyoshi K, Vandenbark AA, Hurn PD, Offner H (2011b) CD4+FoxP3+ regulatory T-cells in cerebral ischemic stroke. Metab Brain Dis 26:87–90 ArticlePubMed Google Scholar
Ren X, Akiyoshi K, Dziennis S, Vandenbark AA, Herson PS, Hurn PD, Offner H (2011c) Regulatory B cells limit CNS inflammation and neurologic deficits in murine experimental stroke. J Neurosci 31:8556–8563 ArticlePubMedCAS Google Scholar
Rifa’i M, Kawamoto Y, Nakashima I, Suzuki H (2004) Essential roles of CD8+CD122+ regulatory T cells in the maintenance of T cell homeostasis. J Exp Med 200:1123–1134 ArticlePubMed Google Scholar
Rifa’i M, Shi Z, Zhang SY, Lee YH, Shiku H, Isobe K, Suzuki H (2008) CD8+CD122+ regulatory T cells recognize activated T cells via conventional MHC class I-alphabetaTCR interaction and become IL-10-producing active regulatory cells. Int Immunol 20:937–947 ArticlePubMed Google Scholar
Schilling M, Besselmann M, Leonhard C, Mueller M, Ringelstein EB, Kiefer R (2003) Microglial activation precedes and predominates over macrophage infiltration in transient focal cerebral ischemia: a study in green fluorescent protein transgenic bone marrow chimeric mice. Exp Neurol 183:25–33 ArticlePubMed Google Scholar
Spera PA, Ellison JA, Feuerstein GZ, Barone FC (1998) IL-10 reduces rat brain injury following focal stroke. Neurosci Lett 251:189–192 ArticlePubMedCAS Google Scholar
Strle K, Zhou JH, Shen WH, Broussard SR, Johnson RW, Freund GG, Dantzer R, Kelley KW (2001) Interleukin-10 in the brain. Crit Rev Immunol 21:427–449 ArticlePubMedCAS Google Scholar
Stubbe T, Ebner F, Richter D, Randolf Engel O, Klehmet J, Royl G, Meisel A, Nitsch R, Meisel C, Brandt C (2013) Regulatory T cells accumulate and proliferate in the ischemic hemisphere for up to 30 days after MCAO. J Cereb Blood Flow Metab 33:37–47 ArticlePubMedCAS Google Scholar
Subramanian S, Yates M, Vandenbark AA, Offner H (2011) Oestrogen-mediated protection of experimental autoimmune encephalomyelitis in the absence of Foxp3+ regulatory T cells implicates compensatory pathways including regulatory B cells. Immunology 132:340–347 ArticlePubMedCAS Google Scholar
Tanaka R, Komine-Kobayashi M, Mochizuki H, Yamada M, Furuya T, Migita M, Shimada T, Mizuno Y, Urabe T (2003) Migration of enhanced green fluorescent protein expressing bone marrow-derived microglia/macrophage into the mouse brain following permanent focal ischemia. Neuroscience 117:531–539 ArticlePubMedCAS Google Scholar
Tarkowski E, Rosengren L, Blomstrand C, Wikkelso C, Jensen C, Ekholm S, Tarkowski A (1997) Intrathecal release of pro- and anti-inflammatory cytokines during stroke. Clin Exp Immunol 110:492–499 ArticlePubMedCAS Google Scholar
van Exel E, Gussekloo J, de Craen AJ, Bootsma-van der Wiel A, Frolich M, Westendorp RG (2002) Inflammation and stroke: the Leiden 85-Plus Study. Stroke 33:1135–1138 ArticlePubMed Google Scholar
Wang X (2005) Investigational anti-inflammatory agents for the treatment of ischaemic brain injury. Expert Opin Investig Drugs 14:393–409 ArticlePubMedCAS Google Scholar
Wang Q, Tang XN, Yenari MA (2007) The inflammatory response in stroke. J Neuroimmunol 184:53–68 ArticlePubMedCAS Google Scholar
Yanaba K, Bouaziz JD, Haas KM, Poe JC, Fujimoto M, Tedder TF (2008) A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 28:639–650 ArticlePubMedCAS Google Scholar
Yanaba K, Bouaziz JD, Matsushita T, Tsubata T, Tedder TF (2009) The development and function of regulatory B cells expressing IL-10 (B10 cells) requires antigen receptor diversity and TLR signals. J Immunol 182:7459–7472 ArticlePubMedCAS Google Scholar
Yilmaz G, Granger DN (2008) Cell adhesion molecules and ischemic stroke. Neurol Res 30:783–793 ArticlePubMed Google Scholar
Yilmaz G, Arumugam TV, Stokes KY, Granger DN (2006) Role of T lymphocytes and interferon-gamma in ischemic stroke. Circulation 113:2105–2112 ArticlePubMed Google Scholar
Zhang RL, Chopp M, Jiang N, Tang WX, Prostak J, Manning AM, Anderson DC (1995) Anti-intercellular adhesion molecule-1 antibody reduces ischemic cell damage after transient but not permanent middle cerebral artery occlusion in the Wistar rat. Stroke 26:1438–1442, discussion 1443 ArticlePubMedCAS Google Scholar
Zhang L, Zhang ZG, Zhang RL, Lu M, Krams M, Chopp M (2003) Effects of a selective CD11b/CD18 antagonist and recombinant human tissue plasminogen activator treatment alone and in combination in a rat embolic model of stroke. Stroke 34:1790–1795 ArticlePubMedCAS Google Scholar
Zhang B, Subramanian S, Dziennis S, Jia J, Uchida M, Akiyoshi K, Migliati E, Lewis AD, Vandenbark AA, Offner H, Hurn PD (2010) Estradiol and G1 reduce infarct size and improve immunosuppression after experimental stroke. J Immunol 184:4087–4094 ArticlePubMedCAS Google Scholar