Regulatory T lymphocytes from ALS mice suppress microglia and effector T lymphocytes through different cytokine-mediated mechanisms

Neurobiology of Disease

Volumn 48, Issue 3, 2012, Pages 418-428

  Zhao, Weihua ^a   Beers, David R ^a   Liao, Bing ^a   Henkel, Jenny S ^a   Appel, Stanley H ^a  

^a HOUSTON METHODIST HOSPITAL   (United States)

Author keywords

ALS; Microglia; T lymphocytes

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 4 ANTIBODY; NITRIC OXIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; TRANSFORMING GROWTH FACTOR BETA;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CELL ACTIVATION; CELL ISOLATION; CONTROLLED STUDY; EFFECTOR CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IN VITRO STUDY; LYMPH NODE; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINAL CORD; SPLEEN; WESTERN BLOTTING;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BLOTTING, WESTERN; CD4-POSITIVE T-LYMPHOCYTES; CELL COMMUNICATION; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MICROGLIA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES, REGULATORY;

EID: 84864928300     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.07.008     Document Type: Article

References (48)

1. Alexianu M.E., Kozovska M., Appel S.H. Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology 2001, 57:1282-1289.
2. Almer G., Vukosavic S., Romero N., Przedborski S. Inducible nitric oxide synthase up-regulation in a transgenic mouse model of familial amyotrophic lateral sclerosis. J. Neurochem. 1999, 72:2415-2425.
3. Almer G., Guegan C., Teismann P., Naini A., Rosoklija G., Hays A.P., Chen C., Przedborski S. Increased expression of the pro-inflammatory enzyme cyclooxygenase-2 in amyotrophic lateral sclerosis. Ann. Neurol. 2001, 49:176-185.
4. 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.
5. Appel S.H., Beers D.R., Henkel J.S. T cell-microglial dialogue in Parkinson's disease and amyotrophic lateral sclerosis: are we listening?. Trends Immunol. 2010, 31:7-17.
6. Asseman C., Mauze S., Leach M.W., Coffman R.L., Powrie F. An essential role for interleukin 10 in function of regulatory T cells that inhibit intestinal inflammation. J. Exp. Med. 1999, 190:995-1004.
7. + T cells. Eur. J. Immunol. 2004, 34:3434-3445.
8. Baecher-Allan C., Wolf E., Hafler D.A. MHC class II expression identifies functionally distinct human regulatory T cells. J. Immunol. 2006, 176:4622-4631.
9. Beers D.R., Henkel J.S., Xiao Q., Zhao W., Wang J., Yen A.A., Siklós L., McKercher S.R., Appel S.H. Wild-type microglia extend survival in PU.1 knockout mice with familial amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:16021-16026.
10. + T cells support glial neuroprotection, slow disease progression, and modify glial morphology in an animal model of inherited ALS. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:15558-15563.
11. Beers D.R., Henkel J.S., Zhao W., Wang J., Wen S., Liao B., Appel S.H. Endogenous regulatory T lymphocytes ameliorate amyotrophic lateral sclerosis in mice and correlate with disease progression in patients with amyotrophic lateral sclerosis. Brain 2011, 134:1293-1314.
12. Bruijn L.I., Miller T.M., Cleveland D.W. Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu. Rev. Neurosci. 2004, 27:723-749.
13. Corti S., Locatelli F., Donadoni C., Guglieri M., Papadimitriou D., Strazzer S., Del Bo R., Comi G.P. Wild-type bone marrow cells ameliorate the phenotype of SOD1-G93A ALS mice and contribute to CNS, heart and skeletal muscle tissues. Brain 2004, 127:2518-2532.
14. Engelhardt J.I., Tajti J., Appel S.H. Lymphocytic infiltrates in the spinal cord in amyotrophic lateral sclerosis. Arch. Neurol. 1993, 50:30-36.
15. Frank M.G., Wieseler-Frank J.L., Watkins L.R., Maier S.F. Rapid isolation of highly enriched and quiescent microglia from adult rat hippocampus: immunophenotypic and functional characteristics. J. Neurosci. Methods 2006, 151:121-130.
16. Hall E.D., Oostveen J.A., Gurney M.E. Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia 1998, 23:249-256.
17. Henkel J.S., Engelhardt J.I., Siklós L., Simpson E.P., Kim S.H., Pan T., Goodman J.C., Siddique T., Beers D.R., Appel S.H. Presence of dendritic cells, MCP-1, and activated microglia/macrophages in amyotrophic lateral sclerosis spinal cord tissue. Ann. Neurol. 2004, 55:221-235.
18. Henkel J.H., Beers D.R., Siklós L., Appel S.H. The chemokine MCP-1 and the dendritic and myeloid cells it attracts are increased in the mSOD1 mouse model of ALS. Mol. Cell. Neurosci. 2006, 31:427-437.
19. Henkel J.S., Beers D.R., Zhao W., Appel S.H. Microglia in ALS: the good, the bad, and the resting. J. Neuroimmune Pharmacol. 2009, 4:389-398.
20. Ince P.G., Shaw P.J., Slade J.Y., Jones C., Hudgson P. Familial amyotrophic lateral sclerosis with a mutation in exon 4 of Cu/Zn superoxide dismutase gene: pathological and immunocytochemical changes. Acta Neuropathol. 1996, 92:395-403.
21. Liao B., Zhao W., Beers D.R., Henkel J.S., Appel S.H. Transformation from a neuroprotective to a neurotoxic microglial phenotype in a mouse model of ALS. Exp. Neurol. 2012, 237:147-152. (Electronic publication ahead of print).
22. + regulatory T cells in a murine model of HIV-1-associated neurodegeneration. J. Immunol. 2009, 182:3855-3865.
23. Lloyd C.M., Hawrylowicz C.M. Regulatory T cells in asthma. Immunity 2009, 31:438-449.
24. Marden J.J., Harraz M.M., Williams A.J., Nelson K., Luo M., Paulson H., Engelhardt J.F. Redox modifier genes in amyotrophic lateral sclerosis in mice. J. Clin. Invest. 2007, 117:2913-2919.
25. Ohkura N., Sakaguchi S. Regulatory T cells: roles of T cell receptor for their development and function. Semin. Immunopathol. 2010, 32:95-106.
26. O'Keefe G.M., Nguyen V.T., Benveniste E.N. Class II transactivator and class II MHC gene expression in microglia: modulation by the cytokines TGF-beta, IL-4, IL-13 and IL-10. Eur. J. Immunol. 1999, 29:1275-1285.
27. Paterson A.M., Sharpe A.H. Taming tissue-specific T cells: CTLA-4 reins in self-reactive T cells. Nat. Immunol. 2010, 11:109-111.
28. Qin H., Wilson C.A., Roberts K.L., Baker B.J., Zhao X., Benveniste E.N. IL-10 inhibits lipopolysaccharide-induced CD40 gene expression through induction of suppressor of cytokine signaling-3. J. Immunol. 2006, 177:7761-7771.
29. + regulatory cells that control intestinal inflammation. J. Exp. Med. 2000, 192:295-302.
30. + regulatory T cells in an animal model of Parkinson's disease. J. Leukoc. Biol. 2007, 82:1083-1094.
31. + T cells. J. Proteome Res. 2009, 8:3497-3511.
32. + regulatory T cells in immunological tolerance to self and non-self. Nat. Immunol. 2005, 6:345-352.
33. Sakaguchi S., Sakaguchi N., Asano M., Itoh M., Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 1995, 155:1151-1164.
34. Sakaguchi S., Yamaguchi T., Nomura T., Ono M. Regulatory T cells and immune tolerance. Cell 2008, 133:775-787.
35. Sakaguchi S., Wing K., Onishi Y., Prieto-Martin P., Yamaguchi T. Regulatory T cells: how do they suppress immune responses?. Int. Immunol. 2009, 21:1105-1111.
36. Schwartz M., Kipnis J. A conceptual revolution in the relationships between the brain and immunity. Brain Behav. Immun. 2011, 25:817-819.
37. + T regulatory cell-mediated suppression. Immunity 2009, 30:636-645.
38. + T cells. J. Autoimmun. 2001, 16:115-123.
39. + naturally anergic and suppressive T cells: induction of autoimmune disease by breaking their anergic/suppressive state. Int. Immunol. 1998, 10:1969-1980.
40. + regulatory T cell: a jack of all trades, master of regulation. Nat. Immunol. 2008, 9:239-244.
41. + immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J. Exp. Med. 1998, 188:287-296.
42. + regulatory T cells induce alternative activation of human monocytes/macrophages. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:19446-19451.
43. Turner M.R., Cagnin A., Turkheimer F.E., Miller C.C., Shaw C.E., Brooks D.J., Leigh P.N., Banati R.B. Evidence of widespread cerebral microglial activation in amyotrophic lateral sclerosis: an [11C](R)-PK11195 position emission tomography study. Neurobiol. Dis. 2004, 15:601-609.
44. Weydt P., Weiss M.D., Moller T., Carter G.T. Neuro-inflammation as a therapeutic target in amyotrophic lateral sclerosis. Curr. Opin. Investig. Drugs 2002, 3:1720-1724.
45. G93A microglia are more neurotoxic relative to wild-type microglia. J. Neurochem. 2007, 102:2008-2019.
46. Yamaguchi T., Wing J.B., Sakaguchi S. Two modes of immune suppression by Foxp3(+) regulatory T cells under inflammatory or non-inflammatory conditions. Semin. Immunol. 2011, 23:424-430.
47. Zhao W., Xie W., Le W., Beers D.R., He Y., Henkel J.S., Simpson E.P., Yen A.A., Xiao Q., Appel S.H. Activated microglia initiate motor neuron injury by a nitric oxide and glutamate-mediated mechanism. J. Neuropathol. Exp. Neurol. 2004, 63:964-977.
48. Zhao W., Xie W., Xiao Q., Beers D.R., Appel S.H. Protective effects of an anti-inflammatory cytokine, interleukin-4, on motoneuron toxicity induced by activated microglia. J. Neurochem. 2006, 99:1176-1187.