Autoimmune Responses to Brain Following Stroke

Translational Stroke Research

Volumn 3, Issue 3, 2012, Pages 310-317

  Becker, Kyra ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Autoimmune; Infection; Stroke; Th1

Indexed keywords

BRAIN ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 10; MYELIN BASIC PROTEIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; BLOOD BRAIN BARRIER; BRAIN ISCHEMIA; CELLULAR IMMUNITY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; HUMAN; INNATE IMMUNITY; LYMPH NODE; LYMPHOCYTE; LYMPHOCYTE PROLIFERATION; MIDDLE CEREBRAL ARTERY OCCLUSION; MONOCYTE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE ACTIVATION; TH1 CELL;

EID: 84865763910     PISSN: 18684483     EISSN: 1868601X     Source Type: Journal    
DOI: 10.1007/s12975-012-0154-0     Document Type: Review

References (85)

1. Chapman KZ, Dale VQ, Denes A, Bennett G, Rothwell NJ, Allan SM, et al. A rapid and transient peripheral inflammatory response precedes brain inflammation after experimental stroke. J Cereb Blood Flow Metab. 2009; 29(11): 1764-8.
2. Kleinig TJ, Vink R. Suppression of inflammation in ischemic and hemorrhagic stroke: therapeutic options. Curr Opin Neurol. 2009; 22(3): 294-301.
3. Wang Q, Tang XN, Yenari MA. The inflammatory response in stroke. J Neuroimmunol. 2007; 184(1-2): 53-68.
4. Iadecola C, Anrather J. The immunology of stroke: from mechanisms to translation. Nat Med. 2011; 17(7): 796-808.
5. Jander S, Kraemer M, Schroeter M, Witte OW, 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.
6. Schroeter M, Jander S, Witte OW, Stoll G. Local immune responses in the rat cerebral cortex after middle cerebral artery occlusion. J Neuroimmunol. 1994; 55(2): 195-203.
7. Braun JS, Jander S, Schroeter M, Witte OW, Stoll G. Spatiotemporal relationship of apoptotic cell death to lymphomonocytic infiltration in photochemically induced focal ischemia of the rat cerebral cortex. Acta Neuropathol (Berl). 1996; 92(3): 255-63.
8. Campanella M, Sciorati C, Tarozzo G, Beltramo M. Flow cytometric analysis of inflammatory cells in ischemic rat brain. Stroke. 2002; 33(2): 586-92.
9. Jauch EC, Lindsell C, Broderick J, Fagan SC, Tilley BC, Levine SR. Association of serial biochemical markers with acute ischemic stroke: the National Institute of Neurological Disorders and Stroke recombinant tissue plasminogen activator stroke study. Stroke. 2006; 37(10): 2508-13.
10. van Zwam M, Huizinga R, Melief MJ, Wierenga-Wolf AF, van Meurs M, Voerman JS, et al. Brain antigens in functionally distinct antigen-presenting cell populations in cervical lymph nodes in MS and EAE. J Mol Med. 2009; 87(3): 273-86.
11. Planas AM, Gomez-Choco M, Urra X, Gorina R, Caballero M, Chamorro A. Brain-derived antigens in lymphoid tissue of patients with acute stroke. J Immunol. 2012; 188(5): 2156-63.
12. Youngchaiyud U, Coates AS, Whittingham S, Mackay IR. Cellular-immune response to myelin protein: absence in multiple sclerosis and presence in cerebrovascular accidents. Aust N Z J Med. 1974; 4(6): 535-8.
13. Wang WZ, Olsson T, Kostulas V, Hojeberg B, Ekre HP, Link H. Myelin antigen reactive T cells in cerebrovascular diseases. Clin Exp Immunol. 1992; 88(1): 157-62.
14. Kallen B, Nilsson O, Thelin C. Effect of encephalitogenic protein on migration in agarose of leukoytes from patients with multiple sclerosis. A longitudinal study of patients with relapsing multiple sclerosis or with cerebral infarction. Acta Neurol Scand. 1977; 55(1): 47-56.
15. Rocklin RE, Sheremata WA, Feldman RG, Kies MW, David JR. The Guillain-Barre syndrome and multiple sclerosis. In vitro cellular responses to nervous-tissue antigens. N Engl J Med. 1971; 284(15): 803-8.
16. Bornstein NM, Aronovich B, Korczyn AD, Shavit S, Michaelson DM, Chapman J. Antibodies to brain antigens following stroke. Neurology. 2001; 56(4): 529-30.
17. Dambinova SA, Khounteev GA, Izykenova GA, Zavolokov IG, Ilyukhina AY, Skoromets AA. Blood test detecting autoantibodies to N-methyl-d-aspartate neuroreceptors for evaluation of patients with transient ischemic attack and stroke. Clin Chem. 2003; 49(10): 1752-62.
18. Becker KJ, Kindrick DL, Lester MP, Shea C, Ye ZC. Sensitization to brain antigens after stroke is augmented by lipopolysaccharide. J Cereb Blood Flow Metab. 2005; 25(12): 1634-44.
19. Yan J, Greer JM, Etherington K, Cadigan GP, Cavanagh H, Henderson RD, et al. Immune activation in the peripheral blood of patients with acute ischemic stroke. J Neuroimmunol. 2009; 206(1-2): 112-7.
20. Fontana A, Constam DB, Frei K, Malipiero U, Pfister HW. Modulation of the immune response by transforming growth factor beta. Int Arch Allergy Immunol. 1992; 99(1): 1-7.
21. Suter T, Biollaz G, Gatto D, Bernasconi L, Herren T, Reith W, et al. The brain as an immune privileged site: dendritic cells of the central nervous system inhibit T cell activation. Eur J Immunol. 2003; 33(11): 2998-3006.
22. Bailey SL, Carpentier PA, McMahon EJ, Begolka WS, Miller SD. Innate and adaptive immune responses of the central nervous system. Crit Rev Immunol. 2006; 26(2): 149-88.
23. Perry VH. A revised view of the central nervous system microenvironment and major histocompatibility complex class II antigen presentation. J Neuroimmunol. 1998; 90(2): 113-21.
24. Buttini M, Limonta S, Boddeke HW. Peripheral administration of lipopolysaccharide induces activation of microglial cells in rat brain. Neurochem Int. 1996; 29(1): 25-35.
25. Janeway Jr CA, Medzhitov R. Innate immune recognition. Annu Rev Immunol. 2002; 20: 197-216.
26. Oppenheim JJ, Tewary P, de la Rosa G, Yang D. Alarmins initiate host defense. Adv Exp Med Biol. 2007; 601: 185-94.
27. Yang D, de la Rosa G, Tewary P, Oppenheim JJ. Alarmins link neutrophils and dendritic cells. Trends Immunol. 2009; 30(11): 531-7.
28. Bianchi ME, Manfredi AA. High-mobility group box 1 (HMGB1) protein at the crossroads between innate and adaptive immunity. Immunol Rev. 2007; 220: 35-46.
29. Mannie M, Swanborg RH, Stepaniak JA. Experimental autoimmune encephalomyelitis in the rat. Curr Protoc Immunol. 2009; Chapter 15: Unit 15 2.
30. Becker KJ, McCarron RM, Ruetzler C, Laban O, Sternberg E, Flanders KC, et al. Immunologic tolerance to myelin basic protein decreases stroke size after transient focal cerebral ischemia. Proc Natl Acad Sci U S A. 1997; 94(20): 10873-8.
31. Ren X, Akiyoshi K, Grafe MR, Vandenbark AA, Hurn PD, Herson PS et al. Myelin specific cells infiltrate MCAO lesions and exacerbate stroke severity. Metab Brain Dis. 27(1): 7-15.
32. Zierath D, Thullbery M, Hadwin J, Gee JM, Savos A, Kalil A, et al. CNS immune responses following experimental stroke. Neurocrit Care. 2010; 12: 274-84.
33. Gee JM, Zierath D, Hadwin J, Savos A, Kalil A, Thullbery M, et al. Long term immunologic consequences of experimental stroke and mucosal tolerance. Exp Transl Stroke Med. 2009; 1: 3.
34. Pohjasvaara T, Erkinjuntti T, Ylikoski R, Hietanen M, Vataja R, Kaste M. Clinical determinants of poststroke dementia. Stroke. 1998; 29(1): 75-81.
35. Leys D, Henon H, Mackowiak-Cordoliani MA, Pasquier F. Poststroke dementia. Lancet Neurol. 2005; 4(11): 752-9.
36. Fillit HM, Kemeny E, Luine V, Weksler ME, Zabriskie JB. Antivascular antibodies in the sera of patients with senile dementia of the Alzheimer's type. J Gerontol. 1987; 42(2): 180-4.
37. Ishida K, Kaneko K, Kubota T, Itoh Y, Miyatake T, Matsushita M, et al. Identification and characterization of an anti-glial fibrillary acidic protein antibody with a unique specificity in a demented patient with an autoimmune disorder. J Neurol Sci. 1997; 151(1): 41-8.
38. Karczewski P, Hempel P, Kunze R, Bimmler M. Agonistic autoantibodies to the alpha(1)-adrenergic receptor and the beta(2)-adrenergic receptor in Alzheimer's and vascular dementia. Scand J Immunol. 2012; epub ahead of print.
39. Rosenmann H, Meiner Z, Geylis V, Abramsky O, Steinitz M. Detection of circulating antibodies against tau protein in its unphosphorylated and in its neurofibrillary tangles-related phosphorylated state in Alzheimer's disease and healthy subjects. Neurosci Lett. 2006; 410(2): 90-3.
40. Zierath D, Hadwin J, Savos A, Carter KT, Kunze A, Becker KJ. Anamnestic recall of stroke-related deficits: an animal model. Stroke. 2010; 41(11): 2653-60.
41. Liesz A, Suri-Payer E, Veltkamp C, Doerr H, Sommer C, Rivest S, et al. Regulatory T cells are key cerebroprotective immunomodulators in acute experimental stroke. Nat Med. 2009; 15(2): 192-9.
42. Frenkel D, Huang Z, Maron R, Koldzic DN, Moskowitz MA, Weiner HL. Neuroprotection by IL-10-producing MOG CD4+ T cells following ischemic stroke. J Neurol Sci. 2005; 233(1-2): 125-32.
43. Chen Y, Ruetzler C, Pandipati S, Spatz M, McCarron RM, Becker K, et al. Mucosal tolerance to E-selectin provides cell-mediated protection against ischemic brain injury. Proc Natl Acad Sci U S A. 2003; 100(25): 15107-12.
44. Becker K, Kindrick D, McCarron R, Hallenbeck J, Winn R. Adoptive transfer of myelin basic protein-tolerized splenocytes to naive animals reduces infarct size: a role for lymphocytes in ischemic brain injury? Stroke. 2003; 34(7): 1809-15.
45. Miller A, Lider O, Weiner HL. Antigen-driven bystander suppression after oral administration of antigens. J Exp Med. 1991; 174(4): 791-8.
46. Sharma S, Yang B, Xi X, Grotta JC, Aronowski J, Savitz SI. IL-10 directly protects cortical neurons by activating PI-3 kinase and STAT-3 pathways. Brain Res. 1373: 189-94.
47. Zhou Z, Peng X, Insolera R, Fink DJ, Mata M. Interleukin-10 provides direct trophic support to neurons. J Neurochem. 2009; 110(5): 1617-27.
48. Buisson A, Lesne S, Docagne F, Ali C, Nicole O, MacKenzie ET, et al. Transforming growth factor-beta and ischemic brain injury. Cell Mol Neurobiol. 2003; 23(4-5): 539-50.
49. Ren X, Akiyoshi K, Dziennis S, Vandenbark AA, Herson PS, Hurn PD et al. Regulatory B cells limit CNS inflammation and neurologic deficits in murine experimental stroke. J Neurosci. 31(23): 8556-63.
50. Gee JM, Kalil A, Thullbery M, Becker KJ. Induction of immunologic tolerance to myelin basic protein prevents central nervous system autoimmunity and improves outcome after stroke. Stroke. 2008; 39(5): 1575-82.
51. Aslanyan S, Weir CJ, Diener HC, Kaste M, Lees KR. Pneumonia and urinary tract infection after acute ischaemic stroke: a tertiary analysis of the GAIN International trial. Eur J Neurol. 2004; 11(1): 49-53.
52. Davenport RJ, Dennis MS, Wellwood I, Warlow CP. Complications after acute stroke. Stroke. 1996; 27(3): 415-20.
53. Grau AJ, Buggle F, Schnitzler P, Spiel M, Lichy C, Hacke W. Fever and infection early after ischemic stroke. J Neurol Sci. 1999; 171(2): 115-20.
54. Langhorne P, Stott DJ, Robertson L, MacDonald J, Jones L, McAlpine C, et al. Medical complications after stroke: a multicenter study. Stroke. 2000; 31(6): 1223-9.
55. Indredavik B, Rohweder G, Naalsund E, Lydersen S. Medical complications in a comprehensive stroke unit and an early supported discharge service. Stroke. 2008; 39(2): 414-20.
56. Hong KS, Kang DW, Koo JS, Yu KH, Han MK, Cho YJ, et al. Impact of neurological and medical complications on 3-month outcomes in acute ischaemic stroke. Eur J Neurol. 2008; 15(12): 1324-31.
57. Minnerup J, Wersching H, Browinkel B, Dziewas R, Heuschmann PU, Nabavi D, et al. The impact of lesion location and lesion size on post-stroke infection frequency. J Neurol Neurosurg Psychiatry. 2010; 81: 198-202.
58. Vermeij FH, Scholte op Reimer WJ, de Man P, van Oostenbrugge RJ, Franke CL, de Jong G, et al. Stroke-associated infection is an independent risk factor for poor outcome after acute ischemic stroke: data from the Netherlands Stroke Survey. Cerebrovasc Dis. 2009; 27(5): 465-71.
59. Chamorro A, Urra X, Planas AM. Infection after acute ischemic stroke: a manifestation of brain-induced immunodepression. Stroke. 2007; 38(3): 1097-103.
60. Chamorro A, Amaro S, Vargas M, Obach V, Cervera A, Torres F, et al. Interleukin 10, monocytes and increased risk of early infection in ischaemic stroke. J Neurol Neurosurg Psychiatry. 2006; 77(11): 1279-81.
61. Haeusler KG, Schmidt WU, Fohring F, Meisel C, Helms T, Jungehulsing GJ, et al. Cellular immunodepression preceding infectious complications after acute ischemic stroke in humans. Cerebrovasc Dis. 2008; 25(1-2): 50-8.
62. Hug A, Dalpke A, Wieczorek N, Giese T, Lorenz A, Auffarth G, et al. Infarct volume is a major determiner of post-stroke immune cell function and susceptibility to infection. Stroke. 2009; 40(10): 3226-32.
63. Offner H, Vandenbark AA, Hurn PD. Effect of experimental stroke on peripheral immunity: CNS ischemia induces profound immunosuppression. Neuroscience. 2009; 158(3): 1098-111.
64. Prass K, Braun JS, Dirnagl U, Meisel C, Meisel A. Stroke propagates bacterial aspiration to pneumonia in a model of cerebral ischemia. Stroke. 2006; 37(10): 2607-12.
65. Schulte-Herbruggen O, Klehmet J, Quarcoo D, Meisel C, Meisel A. Mouse strains differ in their susceptibility to poststroke infections. Neuroimmunomodulation. 2006; 13(1): 13-8.
66. Vogelgesang A, Grunwald U, Langner S, Jack R, Broker BM, Kessler C, et al. Analysis of lymphocyte subsets in patients with stroke and their influence on infection after stroke. Stroke. 2008; 39(1): 237-41.
67. Johnston KC, Li JY, Lyden PD, Hanson SK, Feasby TE, Adams RJ, et al. Medical and neurological complications of ischemic stroke: experience from the RANTTAS trial. RANTTAS Investigators. Stroke. 1998; 29(2): 447-53.
68. Katzan IL, Cebul RD, Husak SH, Dawson NV, Baker DW. The effect of pneumonia on mortality among patients hospitalized for acute stroke. Neurology. 2003; 60(4): 620-5.
69. Becker KJ, Kalil AJ, Tanzi P, Zierath DK, Savos AV, Gee JM, et al. Autoimmune responses to the brain after stroke are associated with worse outcome. Stroke. 2011; 42: 2763-9.
70. Tanzi P, Cain K, Kalil A, Zierath D, Savos A, Gee JM, et al. Post-stroke infection: a role for IL-1ra? Neurocrit Care. 2011; 14(2): 244-52.
71. Kovacevic-Jovanovic V, Laban O, Stanojevic S, Miletic T, Dimitrijevic M, Radulovic J. Changes in immunological and neuronal conditions markedly altered antibody response to intracerebroventricularly injected ovalbumin in the rat. Neuroimmunomodulation. 1997; 4(4): 181-7.
72. Siegmund K, Feuerer M, Siewert C, Ghani S, Haubold U, Dankof A, et al. Migration matters: regulatory T-cell compartmentalization determines suppressive activity in vivo. Blood. 2005; 106(9): 3097-104.
73. Hofstetter HH, Grau C, Buttmann M, Forsthuber TG, Gaupp S, Toyka KV, et al. The PLPp-specific T-cell population promoted by pertussis toxin is characterized by high frequencies of IL-17-producing cells. Cytokine. 2007; 40(1): 35-43.
74. Attinger A, MacDonald HR, Acha-Orbea H. Lymphoid environment limits superantigen and antigen-induced T cell proliferation at high precursor frequency. Eur J Immunol. 2001; 31(3): 884-93.
75. Chow LH, Feurer C, Borel JF. Chronic relapsing experimental allergic encephalomyelitis in the Lewis rat: studies on immune regulation. J Neuroimmunol. 1988; 19(4): 329-38.
76. Zhang X, Reddy J, Ochi H, Frenkel D, Kuchroo VK, Weiner HL. Recovery from experimental allergic encephalomyelitis is TGF-beta dependent and associated with increases in CD4 + LAP + and CD4 + CD25+ T cells. Int Immunol. 2006; 18(4): 495-503.
77. Hofstetter HH, Targoni OS, Karulin AY, Forsthuber TG, Tary-Lehmann M, Lehmann PV. Does the frequency and avidity spectrum of the neuroantigen-specific T cells in the blood mirror the autoimmune process in the central nervous system of mice undergoing experimental allergic encephalomyelitis? J Immunol. 2005; 174(8): 4598-605.
78. 'Bischof F, Hofmann M, Schumacher TN, Vyth-Dreese FA, Weissert R, Schild H, et al. Analysis of autoreactive CD4 T cells in experimental autoimmune encephalomyelitis after primary and secondary challenge using MHC class II tetramers. J Immunol. 2004; 172(5): 2878-84.
79. Gordon FL, Nguyen KB, White CA, Pender MP. Rapid entry and downregulation of T cells in the central nervous system during the reinduction of experimental autoimmune encephalomyelitis. J Neuroimmunol. 2001; 112(1-2): 15-27.
80. Tan LJ, Vanderlugt CL, McRae BL, Miller SD. Regulation of the effector stages of experimental autoimmune encephalomyelitis via neuroantigen-specific tolerance induction. III. A role for anergy/deletion. Autoimmunity. 1998; 27(1): 13-28.
81. Targoni OS, Baus J, Hofstetter HH, Hesse MD, Karulin AY, Boehm BO, et al. Frequencies of neuroantigen-specific T cells in the central nervous system versus the immune periphery during the course of experimental allergic encephalomyelitis. J Immunol. 2001; 166(7): 4757-64.
82. Prass K, Meisel C, Hoflich C, Braun J, Halle E, Wolf T, et al. Stroke-induced immunodeficiency promotes spontaneous bacterial infections and is mediated by sympathetic activation reversal by poststroke T helper cell type 1-like immunostimulation. J Exp Med. 2003; 198(5): 725-36.
83. Wong CH, Jenne CN, Lee WY, Leger C, Kubes P. Functional innervation of hepatic iNKT cells is immunosuppressive following stroke. Science. 334(6052): 101-5.
84. Meisel C, Schwab JM, Prass K, Meisel A, Dirnagl U. Central nervous system injury-induced immune deficiency syndrome. Nat Rev Neurosci. 2005; 6(10): 775-86.
85. Dirnagl U, Klehmet J, Braun JS, Harms H, Meisel C, Ziemssen T, et al. Stroke-induced immunodepression: experimental evidence and clinical relevance. Stroke. 2007; 38(2 Suppl): 770-3.