Treatment of experimental stroke with IL-10-producing B-cells reduces infarct size and peripheral and CNS inflammation in wild-type B-cell-sufficient mice

Metabolic Brain Disease

Volumn 29, Issue 1, 2014, Pages 59-73

  Bodhankar, Sheetal ^a,b   Chen, Yingxin ^b   Vandenbark, Arthur A ^a,b   Murphy, Stephanie J ^b   Offner, Halina ^a,b  

^a PORTLAND VA MEDICAL CENTER   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

IL 10; Inflammatory cells; MCAO; Regulatory B cells

Indexed keywords

CD11B ANTIGEN; CD19 ANTIGEN; CD4 ANTIGEN; CD69 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; GELATINASE A; HERMES ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2 RECEPTOR BETA; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA; IL10 PROTEIN, MOUSE;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BRAIN INFARCTION SIZE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; EX VIVO STUDY; EXPERIMENTAL STROKE; FLOW CYTOMETRY; HEMISPHERE; IMMUNE RESPONSE; IMMUNOREGULATION; IN VIVO STUDY; INFLAMMATORY CELL; LYMPHOCYTE SUBPOPULATION; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MONOCYTE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PROTEIN EXPRESSION; REPERFUSION; WILD TYPE; ANIMAL; BRAIN; C57BL MOUSE; EVALUATION STUDY; IMMUNOCOMPETENCE; IMMUNOLOGY; IMMUNOMAGNETIC SEPARATION; IMMUNOMODULATION; INFARCTION, MIDDLE CEREBRAL ARTERY; INFLAMMATION; MICROGLIA; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; REPORTER GENE; SECRETION (PROCESS); SPLEEN; T LYMPHOCYTE SUBPOPULATION; TRANSGENIC MOUSE; TRANSPLANTATION;

MUS;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD19; B-LYMPHOCYTE SUBSETS; BRAIN; CHEMOTAXIS, LEUKOCYTE; GENES, REPORTER; IMMUNOCOMPETENCE; IMMUNOMAGNETIC SEPARATION; IMMUNOMODULATION; INFARCTION, MIDDLE CEREBRAL ARTERY; INFLAMMATION; INTERLEUKIN-10; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; SPLEEN; T-LYMPHOCYTE SUBSETS;

EID: 84895877893     PISSN: 08857490     EISSN: 15737365     Source Type: Journal    
DOI: 10.1007/s11011-013-9474-3     Document Type: Article

References (47)

1. Arumugam TV, Granger DN, Mattson MP (2005) Stroke and T-cells. Neuromolecular Med 7(3):229-242. doi:10.1385/NMM:7:3:229 (Pubitemid 41507146)
2. Bodhankar S, Chen Y, Vandenbark AA, Murphy SJ, Offner H (2013a) IL-10-producing B-cells limit CNS inflammation and infarct volume in experimental stroke. Metab Brain Dis 28(3):375-386. doi:10.1007/s11011-013-9413- 3
3. Bodhankar S, Chen Y, Vandenbark AA, Murphy SJ, Offner H (2013b) PD-L1 enhances CNS inflammation and infarct volume following experimental stroke in mice in opposition to PD-1. J Neuroinflammation 10(1):111. doi:10.1186/1742- 2094-10-111
4. Brait VH, Jackman KA, Walduck AK, Selemidis S, Diep H, Mast AE, Guida E, Broughton BR, Drummond GR, Sobey CG (2010) Mechanisms contributing to cerebral infarct size after stroke: gender, reperfusion, T lymphocytes, and Nox2-derived superoxide. J Cereb Blood Flow Metab : Off J Int Soc Cereb Blood Flow Metab 30(7): 1306-1317. doi:10.1038/jcbfm.2010.14
5. Campanella M, Sciorati C, Tarozzo G, Beltramo M (2002) Flow cytometric analysis of inflammatory cells in ischemic rat brain. Stroke 33(2):586-592 (Pubitemid 34123411)
6. Castillo J, Davalos A, Noya M (1997) Progression of ischaemic stroke and excitotoxic aminoacids. Lancet 349(9045):79-83. doi:10.1016/S0140-6736(96)04453- 4 (Pubitemid 27023423)
7. 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 deficientmice. Metab Brain Dis 27(4):487-493. doi:10.1007/s11011-012- 9317-7
8. Chen S, Wu H, Klebe D, Hong Y, Zhang J, Tang J (2013) Regulatory T cell in stroke: a new paradigm for immune regulation. Clin Dev Immunol 2013:689827. doi:10.1155/2013/689827
9. 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(12):2631-2636
10. Dirnagl U (2004) Inflammation in stroke: the good, the bad, and the unknown. Ernst Schering Res Found Workshop 47:87-99
11. Donnan GA, Fisher M, Macleod M, Davis SM (2008) Stroke. Lancet 371(9624):1612-1623. doi:10.1016/S0140-6736(08)60694-7 (Pubitemid 351626845)
12. Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM (2002) B cells regulate autoimmunity by provision of IL-10. Nat Immunol 3(10):944-950. doi:10.1038/ni833 (Pubitemid 35154008)
13. Gelderblom M, Leypoldt F, Steinbach K, Behrens D, Choe CU, Siler DA, Arumugam TV, Orthey E, Gerloff C, Tolosa E, Magnus T (2009) Temporal and spatial dynamics of cerebral immune cell accumulation in stroke. Stroke 40(5):1849-1857. doi:10.1161/STROKEAHA.108.534503
14. Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Borden WB, Bravata DM, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Magid D, Marcus GM, Marelli A, Matchar DB, McGuire DK, Mohler ER, Moy CS, Mussolino ME, Nichol G, Paynter NP, Schreiner PJ, Sorlie PD, Stein J, Turan TN, Virani SS, Wong ND, Woo D, Turner MB (2013) Heart disease and stroke statistics-2013 update: a report from the American Heart Association. Circulation 127(1):e6-e245. doi:10.1161/CIR.0b013e31828124ad
15. 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(11):1798-1805. doi:10.1038/sj.jcbfm.9600482 (Pubitemid 47624547)
16. Iadecola C, Anrather J (2011) The immunology of stroke: from mechanisms to translation. NatMed 17(7):796-808. doi:10.1038/nm.2399
17. Investigators EAST (2001) Use of anti-ICAM-1 therapy in ischemic stroke: results of the Enlimomab Acute Stroke Trial. Neurology, vol 57, 2001/10/24 edn
18. Kleinschnitz C, Schwab N, Kraft P, Hagedorn I, Dreykluft A, Schwarz T, Austinat M, Nieswandt B, Wiendl H, Stoll G (2010) Early detrimental T-cell effects in experimental cerebral ischemia are neither related to adaptive immunity nor thrombus formation. Blood 115(18):3835-3842. doi:10.1182/blood- 2009-10-249078
19. Konoeda F, Shichita T, Yoshida H, Sugiyama Y, Muto G, Hasegawa E, Morita R, Suzuki N, Yoshimura A (2010) Therapeutic effect of IL-12/23 and their signaling pathway blockade on brain ischemia model. Biochem Biophys Res Commun 402(3):500-506. doi:10.1016/j.bbrc.2010.10.058
20. Korpos E, Wu C, Song J, Hallmann R, Sorokin L (2010) Role of the extracellular matrix in lymphocyte migration. Cell Tissue Res 339(1):47-57. doi:10.1007/s00441-009-0853-3
21. Kowarik MC, Cepok S, Sellner J, Grummel V, Weber MS, Korn T, Berthele A, Hemmer B (2012) CXCL13 is the major determinant for B cell recruitment to the CSF during neuroinflammation. J Neuroinflammation 9:93. doi:10.1186/1742-2094-9- 93
22. 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(2):192-199. doi:10.1038/nm.1927
23. Liesz A, Zhou W, Mracsko E, Karcher S, Bauer H, Schwarting S, Sun L, Bruder D, Stegemann S, Cerwenka A, Sommer C, Dalpke AH, Veltkamp R (2011) Inhibition of lymphocyte trafficking shields the brain against deleterious neuroinflammation after stroke. Brain 134(Pt 3):704-720. doi:10.1093/brain/ awr008
24. Lo EH, Dalkara T, Moskowitz MA (2003) Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 4(5):399-415. doi:10.1038/nrn1106 (Pubitemid 37280178)
25. Mabuchi T, Kitagawa K, Ohtsuki T, Kuwabara K, Yagita Y, Yanagihara T, Hori M, Matsumoto M (2000) Contribution of microglia/macrophages to expansion of infarction and response of oligodendrocytes after focal cerebral ischemia in rats. Stroke 31(7):1735-1743 (Pubitemid 30437531)
26. Macrez R, Ali C, Toutirais O, Le Mauff B, Defer G, Dirnagl U, Vivien D (2011) Stroke and the immune system: from pathophysiology to new therapeutic strategies. Lancet Neurol 10(5):471-480. doi:10.1016/S1474-4422(11)70066-7
27. Madan R, Demircik F, Surianarayanan S, Allen JL, Divanovic S, Trompette A, Yogev N, Gu Y, Khodoun M, Hildeman D, Boespflug N, Fogolin MB, Grobe L, Greweling M, Finkelman FD, Cardin R, Mohrs M, MullerW,Waisman A, Roers A, Karp CL (2009) Nonredundant roles for B cell-derived IL-10 in immune counter-regulation. J Immunol 183(4):2312-2320. doi:10.4049/jimmunol.0900185
28. 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(6):3447-3456 (Pubitemid 46417609)
29. 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 latephase immunopathogenesis. J Immunol 185(4):2240-2252. doi:10.4049/jimmunol.1001307
30. Mena H, Cadavid D, Rushing EJ (2004) Human cerebral infarct: a proposed histopathologic classification based on 137 cases. Acta Neuropathol 108(6):524-530. doi:10.1007/s00401-004-0918-z (Pubitemid 39534594)
31. Offner H, Hurn PD (2012)A novel hypothesis: regulatory B lymphocytes shape outcome from experimental stroke. Transl Stroke Res 3(3):324-330. doi:10.1007/s12975-012-0187-4
32. Offner H, Subramanian S, Parker SM, Afentoulis ME, Vandenbark AA, Hurn PD (2006a) Experimental stroke induces massive, rapid activation of the peripheral immune system. J Cereb Blood Flow Metab 26(5):654-665. doi:10.1038/sj.jcbfm. 9600217
33. 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 Tcells and circulating macrophages. J Immunol 176(11):6523-6531 (Pubitemid 43787834)
34. Offner H, Vandenbark AA, Hurn PD (2009) Effect of experimental stroke on peripheral immunity: CNS ischemia induces profound immunosuppression. Neuroscience 158(3):1098-1111. doi:10.1016/j.neuroscience.2008.05.033
35. Ren X, Akiyoshi K, Dziennis S, Vandenbark AA, Herson PS, Hurn PD, Offner H (2011) Regulatory B cells limit CNS inflammation and neurologic deficits in murine experimental stroke. J Neurosci 31(23):8556-8563. doi:10.1523/JNEUROSCI. 1623-11.2011
36. 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(9):1123-1134. doi:10.1084/jem.20040395 (Pubitemid 39507052)
37. 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(7):937-947. doi:10.1093/intimm/dxn052 (Pubitemid 351865868)
38. Shichita T, Sugiyama Y, Ooboshi H, Sugimori H, Nakagawa R, Takada I, Iwaki T, Okada Y, Iida M, Cua DJ, Iwakura Y, Yoshimura A (2009) Pivotal role of cerebral interleukin-17-producing gammadeltaT cells in the delayed phase of ischemic brain injury. Nat Med 15(8):946-950. doi:10.1038/nm.1999
39. 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(1):37-47. doi:10.1038/jcbfm.2012.128
40. Subramanian S, Yates M, Vandenbark AA, Offner H (2011) Oestrogen-mediated protection of experimental autoimmune encephalomyelitis in the absence of Foxp3+ regulatory Tcells implicates compensatory pathways including regulatory B cells. Immunology 132(3):340-347. doi:10.1111/j.1365-2567.2010.03380.x
41. Tuttolomondo A, Di Raimondo D, di Sciacca R, Pinto A, Licata G (2008) Inflammatory cytokines in acute ischemic stroke. Curr Pharm Des 14(33):3574-3589
42. Wang Q, Tang XN, Yenari MA (2007) The inflammatory response in stroke. J Neuroimmunol 184(1-2):53-68. doi:10.1016/j.jneuroim.2006.11.014 (Pubitemid 46365991)
43. Woodruff TM, Thundyil J, Tang SC, Sobey CG, Taylor SM, Arumugam TV (2011) Pathophysiology, treatment, and animal and cellular models of human ischemic stroke. Mol Neurodegener 6(1):11. doi:10.1186/1750-1326-6-11
44. 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(5):639-650. doi:10.1016/j.immuni.2008.03.017 (Pubitemid 351636247)
45. Yang L, Froio RM, Sciuto TE, Dvorak AM, Alon R, Luscinskas FW (2005) ICAM-1 regulates neutrophil adhesion and transcellular migration of TNF-alpha-activated vascular endothelium under flow. Blood 106(2):584-592. doi:10.1182/blood-2004-12-4942 (Pubitemid 40981255)
46. 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(8):4087-4094. doi:10.4049/jimmunol.0902339
47. Zhou W, Liesz A, Bauer H, Sommer C, Lahrmann B, Valous N, Grabe N, Veltkamp R (2013) Postischemic brain infiltration of leukocyte subpopulations differs among murine permanent and transient focal cerebral ischemia models. Brain Pathol 23(1):34-44. doi:10.1111/j.1750-3639.2012.00614.x