Activation of mixed glia by Aβ-specific Th1 and Th17 cells and its regulation by Th2 cells

Brain, Behavior, and Immunity

Volumn 24, Issue 4, 2010, Pages 598-607

  McQuillan, K ^a,b   Lynch, Marina A ^a   Mills, Kingston H G ^b  

^a FLINDERS UNIVERSITY   (Australia)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Amyloid beta; Astrocytes; IFN ; IL 17; Microglia; Th1 cell; Th17 cell; Th2 cell

Indexed keywords

AMYLOID BETA PROTEIN; B7 ANTIGEN; CD11B ANTIGEN; CD40 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; AMYLOID;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; ASTROCYTE; CELL CULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; GENE REPRESSION; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH17 CELL; TH2 CELL; ANIMAL; BRAIN; C57BL MOUSE; CELL LINE; CLASSIFICATION; COCULTURE; CYTOLOGY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GLIA; HELPER CELL; IMMUNOLOGY; NEWBORN; SECRETION (PROCESS);

AMYLOID; ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD40; ANTIGENS, CD86; ASTROCYTES; BRAIN; CELL LINE; CELLS, CULTURED; COCULTURE TECHNIQUES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; INTERFERON-GAMMA; INTERLEUKIN-17; INTERLEUKIN-1BETA; INTERLEUKIN-6; MICE; MICE, INBRED C57BL; MICROGLIA; NEUROGLIA; T-LYMPHOCYTES, HELPER-INDUCER; TH1 CELLS; TH2 CELLS;

EID: 77951880336     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2010.01.003     Document Type: Article

References (70)

1. Abbas N., Bednar I., Mix E., Marie S., Paterson D., Ljungberg A., Morris C., Winblad B., Nordberg A., Zhu J. Up-regulation of the inflammatory cytokines IFN-gamma and IL-12 and down-regulation of IL-4 in cerebral cortex regions of APP(SWE) transgenic mice. J. Neuroimmunol. 2002, 126:50-57.
2. Aloisi F., De Simone R., Columba-Cabezas S., Penna G., Adorini L. Functional maturation of adult mouse resting microglia into an APC is promoted by granulocyte-macrophage colony-stimulating factor and interaction with Th1 cells. J. Immunol. 2000, 164:1705-1712.
3. Aloisi F., Ria F., Adorini L. Regulation of T-cell responses by CNS antigen-presenting cells: different roles for microglia and astrocytes. Immunol. Today 2000, 21:141-147.
4. Aloisi F., Ria F., Penna G., Adorini L. Microglia are more efficient than astrocytes in antigen processing and in Th1 but not Th2 cell activation. J. Immunol. 1998, 160:4671-4680.
5. Battaglia M., Gregori S., Bacchetta R., Roncarolo M.G. Tr1 cells: from discovery to their clinical application. Semin. Immunol. 2006, 18:120-127.
6. Becher B., Blain M., Antel J.P. CD40 engagement stimulates IL-12 p70 production by human microglial cells: basis for Th1 polarization in the CNS. J. Neuroimmunol. 2000, 102:44-50.
7. Benveniste E.N. Inflammatory cytokines within the central nervous system: sources, function, and mechanism of action. Am. J. Physiol. 1992, 263:C1-C16.
8. Benzing W.C., Wujek J.R., Ward E.K., Shaffer D., Ashe K.H., Younkin S.G., Brunden K.R. Evidence for glial-mediated inflammation in aged APP(SW) transgenic mice. Neurobiol. Aging 1999, 20:581-589.
9. Boche D., Nicoll J.A. The role of the immune system in clearance of Aβ from the brain. Brain Pathol. 2008, 18:267-278.
10. Calingasan N.Y., Erdely H.A., Altar C.A. Identification of CD40 ligand in Alzheimer's disease and in animal models of Alzheimer's disease and brain injury. Neurobiol. Aging 2002, 23:31-39.
11. Cao C., Arendash G.W., Dickson A., Mamcarz M.B., Lin X., Ethell D.W. Aβ-specific Th2 cells provide cognitive and pathological benefits to Alzheimer's mice without infiltrating the CNS. Neurobiol. Dis. 2009, 34:63-70.
12. Chabot S., Williams G., Yong V.W. Microglial production of TNF-alpha is induced by activated T lymphocytes. Involvement of VLA-4 and inhibition by interferonβ-1b. J. Clin. Invest. 1997, 100:604-612.
13. Chao C.C., Molitor T.W., Hu S. Neuroprotective role of IL-4 against activated microglia. J. Immunol. 1993, 151:1473-1481.
14. Dasgupta S., Jana M., Liu X., Pahan K. Myelin basic protein-primed T cells of female but not male mice induce nitric-oxide synthase and proinflammatory cytokines in microglia: implications for gender bias in multiple sclerosis. J. Biol. Chem. 2005, 280:32609-32617.
15. Diveu C., McGeachy M.J., Cua D.J. Cytokines that regulate autoimmunity. Curr. Opin. Immunol. 2008, 20:663-668.
16. Dong Y., Benveniste E.N. Immune function of astrocytes. Glia 2001, 36:180-190.
17. Downer E.J., Cowley T.R., Lyons A., Mills K.H., Berezin V., Bock E., Lynch M.A. A novel anti-inflammatory role of NCAM-derived mimetic peptide, FGL. Neurobiol. Aging 2008, 31:118-128.
18. Floden A.M., Combs C.K. Beta-amyloid stimulates murine postnatal and adult microglia cultures in a unique manner. J. Neurosci. 2006, 26:4644-4648.
19. Fontana A., Fierz W., Wekerle H. Astrocytes present myelin basic protein to encephalitogenic T-cell lines. Nature 1984, 307:273-276.
20. Gasic-Milenkovic J., Dukic-Stefanovic S., Deuther-Conrad W., Gartner U., Munch G. Beta-amyloid peptide potentiates inflammatory responses induced by lipopolysaccharide, interferon-gamma and 'advanced glycation endproducts' in a murine microglia cell line. Eur. J. Neurosci. 2003, 17:813-821.
21. Gately M.K., Renzetti L.M., Magram J., Stern A.S., Adorini L., Gubler U., Presky D.H. The interleukin-12/interleukin-12-receptor system: role in normal and pathologic immune responses. Annu. Rev. Immunol. 1998, 16:495-521.
22. Glimcher L.H., Murphy K.M. Lineage commitment in the immune system: the T helper lymphocyte grows up. Genes Dev. 2000, 14:1693-1711.
23. Goodwin J.L., Uemura E., Cunnick J.E. Microglial release of nitric oxide by the synergistic action of beta-amyloid and IFN-gamma. Brain Res. 1995, 692:207-214.
24. Gottfried-Blackmore A., Kaunzner U.W., Idoyaga J., Felger J.C., McEwen B.S., Bulloch K. Acute in vivo exposure to interferon-{gamma} enables resident brain dendritic cells to become effective antigen presenting cells. Proc. Natl. Acad. Sci. USA. 2009, [Epub ahead of print].
25. Griffin W.S., Stanley L.C., Ling C., White L., MacLeod V., Perrot L.J., White C.L., Araoz C. Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proc. Natl. Acad. Sci. USA 1989, 86:7611-7615.
26. Halle A., Hornung V., Petzold G.C., Stewart C.R., Monks B.G., Reinheckel T., Fitzgerald K.A., Latz E., Moore K.J., Golenbock D.T. The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat. Immunol. 2008, 9:857-865.
27. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 2005, 6:1123-1132.
28. Hoek R.M., Ruuls S.R., Murphy C.A., Wright G.J., Goddard R., Zurawski S.M., Blom B., Homola M.E., Streit W.J., Brown M.H., Barclay A.N., Sedgwick J.D. Down-regulation of the macrophage lineage through interaction with OX2 (CD200). Science 2000, 290:1768-1771.
29. Holmes C., Boche D., Wilkinson D., Yadegarfar G., Hopkins V., Bayer A., Jones R.W., Bullock R., Love S., Neal J.W., Zotova E., Nicoll J.A. Long-term effects of Abeta42 immunisation in Alzheimer's disease: follow-up of a randomised, placebo-controlled phase I trial. Lancet 2008, 372:216-223.
30. Ii M., Sunamoto M., Ohnishi K., Ichimori Y. Beta-amyloid protein-dependent nitric oxide production from microglial cells and neurotoxicity. Brain Res. 1996, 720:93-100.
31. Issazadeh S. Kinetics of expression of costimulatory molecules and their ligands in murine relapsing experimental autoimmune encephalomyelitis in vivo. J. Immunol. 1998, 161:1104-1112.
32. Kebir H., Kreymborg K., Ifergan I., Dodelet-Devillers A., Cayrol R., Bernard M., Giuliani F., Arbour N., Becher B., Prat A. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat. Med. 2007, 13:1173-1175.
33. Kroenke M.A., Carlson T.J., Andjelkovic A.V., Segal B.M. IL-12- and IL-23-modulated T cells induce distinct types of EAE based on histology, CNS chemokine profile, and response to cytokine inhibition. J. Exp. Med. 2008, 205:1535-1541.
34. Laporte V., Ait-Ghezala G., Volmar C.H., Mullan M. CD40 deficiency mitigates Alzheimer's disease pathology in transgenic mouse models. J. Neuroinflamm. 2006, 3:3.
35. Ledeboer A., Breve J.J.P., Wierinckx A., van der Jagt S., Bristow A.F., Leysen J.E., Tilder F.J.H., Van Dam A. Expression and regulation of interleukin-10 and interleukin-10 receptor in rat astroglial and microglial cells. Eur. J. Neurosci. 2002, 16:1175-1185.
36. Li M., Pisalyaput K., Galvan M., Tenner A.J. Macrophage colony stimulatory factor and interferon-gamma trigger distinct mechanisms for augmentation of beta-amyloid-induced microglia-mediated neurotoxicity. J. Neurochem. 2004, 91:623-633.
37. Li M., Wang Y., Guo R., Bai Y., Yu Z. Glucocorticoids impair microglia ability to induce T cell proliferation and Th1 polarization. Immunol. Lett. 2007, 109:129-137.
38. Loewenbrueck K.F., Tigno-Aranjuez J.T., Boehm B.O., Lehmann P.V., Tary-Lehmann M. Th1 responses to beta-amyloid in young humans convert to regulatory IL-10 responses in Down syndrome and Alzheimer's disease. Neurobiol. Aging. 2008, [Epub ahead of print].
39. Luber-Narod J., Rogers J. Immune system associated antigens expressed by cells of the human central nervous system. Neurosci. Lett. 1988, 94:17-22.
40. Lue L.F., Rydel R., Brigham E.F., Yang L.B., Hampel H., Murphy G.M., Brachova L., Yan S.D., Walker D.G., Shen Y., Rogers J. Inflammatory repertoire of Alzheimer's disease and nondemented elderly microglia in vitro. Glia 2001, 35:72-79.
41. Lyons A., Griffin R.J., Costelloe C.E., Clarke R.M., Lynch M.A. IL-4 attenuates the neuroinflammation induced by amyloid-beta in vivo and in vitro. J. Neurochem. 2007, 101:771-781.
42. Lyons A., Lynch A.M., Downer E.J., Hanley R., O'Sullivan J.B., Smith A., Lynch M.A. Fractalkine-induced activation of the phosphatidylinositol-3 kinase pathway attenuates microglial activation in vivo and in vitro. J. Neurochem. 2009, 110:1547-1556.
43. Lyons A., McQuillan K., Deighan B.F., O'Reilly J.A., Downer E.J., Murphy A.C., Watson M., Piazza A., O'Connell F., Griffin R., Mills K.H., Lynch M.A. Decreased neuronal CD200 expression in IL-4-deficient mice results in increased neuroinflammation in response to lipopolysaccharide. Brain Behav. Immun. 2009, 23:1020-1027.
44. Mathur A.N., Chang H.C., Zisoulis D.G., Kapur R., Belladonna M.L., Kansas G.S., Kaplan M.H. T-bet is a critical determinant in the instability of the IL-17-secreting T-helper phenotype. Blood 2006, 108:1595-1601.
45. Matsumoto Y., Ohmori K., Fujiwara M. Immune regulation by brain cells in the central nervous system: microglia but not astrocytes present myelin basic protein to encephalitogenic T cells under in vivo-mimicking conditions. Immunology 1992, 76:209-216.
46. Meda L., Baron P., Prat E., Scarpini E., Scarlato G., Cassatella M.A., Rossi F. Proinflammatory profile of cytokine production by human monocytes and murine microglia stimulated with beta-amyloid [25-35]. J. Neuroimmunol. 1999, 93:45-52.
47. Meda L., Cassatella M.A., Szendrei G.I., Otvos L., Baron P., Villalba M., Ferrari D., Rossi F. Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature 1995, 374:647-650.
48. Mills K.H. Induction, function and regulation of IL-17-producing T cells. Eur. J. Immunol. 2008, 38:2636-2649.
49. Moser M., Murphy K.M. Dendritic cell regulation of TH1-TH2 development. Nat. Immunol. 2000, 1:199-205.
50. Mosmann T.R., Cherwinski H., Bond M.W., Giedlin M.A., Coffman R.L. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J. Immunol. 1986, 136:2348-2357.
51. Murphy G.M., Yang L., Cordell B. Macrophage colony-stimulating factor augments beta-amyloid-induced interleukin-1, interleukin-6, and nitric oxide production by microglial cells. J. Biol. Chem. 1998, 273:20967-20971.
52. Nguyen V.T., Benveniste E.N. IL-4-activated STAT-6 inhibits IFN-gamma-induced CD40 gene expression in macrophages/microglia. J. Immunol. 2000, 165:6235-6243.
53. O'Connor R.A., Prendergast C.T., Sabatos C.A., Lau C.W., Leech M.D., Wraith D.C., Anderton S.M. Cutting edge: Th1 cells facilitate the entry of Th17 cells to the central nervous system during experimental autoimmune encephalomyelitis. J. Immunol. 2008, 181:3750-3754.
54. O'Keefe G.M., Nguyen V.T., Benveniste E.N. Regulation and function of class II major histocompatibility complex, CD40, and B7 expression in macrophages and microglia: implications in neurological diseases. J. Neurovirol. 2002, 8:496-512.
55. Park H., Li Z., Yang X.O., Chang S.H., Nurieva R., Wang Y.H., Wang Y., Hood L., Zhu Z., Tian Q., Dong C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 2005, 6:1133-1141.
56. + T cells in vitro. J. Immunol. 1996, 156:2406-2412.
57. Rao A., Avni O. Molecular aspects of T-cell differentiation. Br. Med. Bull. 2000, 56:969-984.
58. Rogers J., Luber-Narod J., Styren S.D., Civin W.H. Expression of immune system-associated antigens by cells of the human central nervous system: relationship to the pathology of Alzheimer's disease. Neurobiol. Aging 1988, 9:339-349.
59. Rowan A.G., Fletcher J.M., Ryan E.J., Moran B., Hegarty J.E., O'Farrelly C., Mills K.H. Hepatitis C virus-specific Th17 cells are suppressed by virus-induced TGF-beta. J. Immunol. 2008, 181:4485-4494.
60. Sawada M., Suzumura A., Hosoya H., Marunouchi T., Nagatsu T. Interleukin-10 inhibits both production of cytokines and expression of cytokine receptors in microglia. J. Neurochem. 1999, 72:1466-1471.
61. Sutton C., Brereton C., Keogh B., Mills K.H., Lavelle E.C. A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis. J. Exp. Med. 2006, 203:1685-1691.
62. Szczepanik A.M., Funes S., Petko W., Ringheim G.E. IL-4, IL-10 and IL-13 modulate A beta(1-42)-induced cytokine and chemokine production in primary murine microglia and a human monocyte cell line. J. Neuroimmunol. 2001, 113:49-62.
63. Tan J., Town T., Crawford F., Mori T., DelleDonne A., Crescentini R., Obregon D., Flavell R.A., Mullan M.J. Role of CD40 ligand in amyloidosis in transgenic Alzheimer's mice. Nat. Neurosci. 2002, 5:1288-1293.
64. Townsend K.P., Town T., Mori T., Lue L.F., Shytle D., Sanberg P.R., Morgan D., Fernandez F., Flavell R.A., Tan J. CD40 signaling regulates innate and adaptive activation of microglia in response to amyloid beta-peptide. Eur. J. Immunol. 2005, 35:901-910.
65. Trajkovic V., Vuckovic O., Stosic-Grujicic S., Miljkovic D., Popadic D., Markovic M., Bumbasirevic V., Backovic A., Cvetkovic I., Harhaji L., Ramic Z., Mostarica Stojkovic M. Astrocyte-induced regulatory T cells mitigate CNS autoimmunity. Glia 2004, 47:168-179.
66. Vignali D.A., Collison L.W., Workman C.J. How regulatory T cells work. Nat. Rev. Immunol. 2008, 8:523-532.
67. Walsh K.P., Brady M.T., Finlay C.M., Boon L., Kingston H.G. Infection with a Helminth parasite attenuates autoimmunity through TGF-{beta}-mediated suppression of Th17 and Th1 responses. J. Immunol. 2009, 183:1577-1586.
68. Wekerle H., Sun D., Oropeza-Wekerle R.L., Meyermann R. Immune reactivity in the nervous system: modulation of T-lymphocyte activation by glial cells. J. Exp. Biol. 1987, 132:43-57.
69. Wood J.A., Wood P.L., Ryan R., Graff-Radford N.R., Pilapil C., Robitaille Y., Quirion R. Cytokine indices in Alzheimer's temporal cortex: no changes in mature IL-1 beta or IL-1RA but increases in the associated acute phase proteins IL-6, alpha 2-macroglobulin and C-reactive protein. Brain Res. 1993, 629:245-252.
70. Zubiaga A.M., Munoz E., Huber B.T. IL-4 and IL-2 selectively rescue Th cell subsets from glucocorticoid-induced apoptosis. J. Immunol. 1992, 149:107-112.