IFN-γ signaling to astrocytes protects from autoimmune mediated neurological disability

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Hindinger, Claudia ^a,c   Bergmann, Cornelia C ^a   Hinton, David R ^b   Phares, Timothy W ^a   Parra, Gabriel I ^a   Hussain, Shabbir ^a   Savarin, Carine ^a   Atkinson, Roscoe D ^b   Stohlman, Stephen A ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GAMMA INTERFERON RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 27;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AUTOIMMUNE DISEASE; BLOOD BRAIN BARRIER; CELL ACTIVITY; CENTRAL NERVOUS SYSTEM DISEASE; CONTROLLED STUDY; DEMYELINATION; DISEASE ACTIVITY; DISEASE COURSE; GRAY MATTER; INCIDENCE; LYMPHOCYTIC INFILTRATION; MORTALITY; MOUSE; NERVE CELL STIMULATION; NERVE FIBER DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUROLOGIC DISEASE; NEUROPROTECTION; NONHUMAN; PROTEIN FUNCTION; REMISSION; SIGNAL TRANSDUCTION; SYMPTOM; TRANSGENIC MOUSE;

ANIMALS; ASTROCYTES; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; INTERFERON-GAMMA; MICE; MICE, INBRED C57BL; MYELIN SHEATH; RECEPTORS, INTERFERON; SIGNAL TRANSDUCTION;

MUS MUSCULUS;

EID: 84864414689     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042088     Document Type: Article

References (48)

1. McFarland HF, Martin R, ((2007)) Multiple sclerosis: a complicated picture of autoimmunity. Nat Immunol 8:: 913--919.
2. Bar-Or A, ((2008)) The immunology of multiple sclerosis. Semin Neurol 28:: 29--45.
3. Sofroniew MV, Vinters HV, ((2010)) Astrocytes: biology and pathology. Acta Neuropathol 119:: 7--35.
4. Miljković D, Timotijević G, Stojković MM, ((2011)) Astrocytes in the tempest of multiple sclerosis. FEBS Lett 585:: 3781--3788.
5. Williams A, Piaton G, Lubetzki C, ((2007)) Astrocytes-friends or foes in multiple sclerosis? Glia 55:: 1300--1312.
6. Bush TG, Puvanachandra N, Horner CH, Polito A, Ostenfeld T, et al. ((1999)) Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice. Neuron 23:: 297--308.
7. Voskuhl RR, Peterson RS, Song B, Ao Y, Morales LB, et al. ((2009)) Reactive astrocytes form scar-like perivascular barriers to leukocytes during adaptive immune inflammation of the CNS. J Neurosci 29:: 11511--11522.
8. Silver J, Miller JH, ((2004)) Regeneration beyond the glial scar. Nat Rev Neurosci 5:: 146--156.
9. Goverman J, ((2009)) Autoimmune T cell responses in the central nervous system. Nat Rev Immunol 9:: 393--407.
10. Kelchtermans H, Billiau A, Matthys P, ((2008)) How interferon-gamma keeps autoimmune diseases in check. Trends Immunol 29:: 479--486.
11. Lin W, Bailey SL, Ho H, Harding HP, Ron D, et al. ((2007)) The integrated stress response prevents demyelination by protecting oligodendrocytes against immune-mediated damage. J Clin Invest 117:: 448--456.
12. Furlan R, Brambilla E, Ruffini F, Poliani PL, Bergami A, et al. ((2001)) Intrathecal delivery of IFN-gamma protects C57BL/6 mice from chronic-progressive experimental autoimmune encephalomyelitis by increasing apoptosis of central nervous system-infiltrating lymphocytes. J Immunol 167:: 1821--1829.
13. Krakowski M, Owens T, ((1996)) Interferon-gamma confers resistance to experimental allergic encephalomyelitis. Eur J Immunol 26:: 1641--1646.
14. Ferber IA, Brocke S, Taylor-Edwards C, Ridgway W, Dinisco C, et al. ((1996)) Mice with a disrupted IFN-gamma gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE). J Immunol 156:: 5--7.
15. Willenborg DO, Fordham S, Bernard CC, Cowden WB, Ramshaw IA, ((1996)) IFN-gamma plays a critical down-regulatory role in the induction and effector phase of myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis. J Immunol 157:: 3223--3227.
16. Hu X, Ivashkiv LB, ((2009)) Cross-regulation of signaling pathways by interferon-gamma: implications for immune responses and autoimmune diseases. Immunity 31:: 539--550.
17. Baker BJ, Akhtar LN, Benveniste EN, ((2009)) SOCS1 and SOCS3 in the control of CNS immunity. Trends Immunol 30:: 392--400.
18. Hindinger C, Gonzalez JM, Bergmann CC, Fuss B, Hinton DR, et al. ((2005)) Astrocyte expression of a dominant-negative interferon-gamma receptor. J Neurosci Res 82:: 20--31.
19. Lees JR, Golumbek PT, Sim J, Dorsey D, Russell JH, ((2008)) Regional CNS responses to IFN-gamma determine lesion localization patterns during EAE pathogenesis. J Exp Med 205:: 2633--2642.
20. Veldhoen M, Seddon B, ((2010)) Empowering T helper 17 cells in autoimmunity. Nat Med 16:: 166--168.
21. Haroon F, Drögemüller K, Händel U, Brunn A, Reinhold D, et al. ((2011)) Gp130-dependent astrocyte survival is critical for the control of autoimmune central nervous system inflammation. J. Immunol 186:: 6521--6531.
22. Balasingam V, Yong VW, ((1996)) Attenuation of astroglial reactivity by interleukin-10. J Neurosci 16:: 2945--2955.
23. Fitzgerald DC, Ciric B, Touil T, Harle H, Grammatikopolou J, et al. ((2007)) Suppressive effect of IL-27 on encephalitogenic Th17 cells and the effector phase of experimental autoimmune encephalomyelitis. J Immunol 179:: 3268--3275.
24. Gran B, Chu N, Zhang GX, Yu S, Li Y, et al. ((2004)) Early administration of IL-12 suppresses EAE through induction of interferon-gamma. J Neuroimmunol 156:: 123--131.
25. Fitzgerald DC, Zhang GX, El-Behi M, Fonseca-Kelly Z, Li H, et al. ((2007)) Suppression of autoimmune inflammation of the central nervous system by interleukin 10 secreted by interleukin 27-stimulated T cells. Nat Immunol 8:: 1372--1379.
26. Farina C, Aloisi F, Meinl E, ((2007)) Astrocytes are active players in cerebral innate immunity. Trends Immunol 28:: 138--145.
27. Wang D, Ayers MM, Catmull DV, Hazelwood LJ, Bernard CC, et al. ((2005)) Astrocyte-associated axonal damage in pre-onset stages of experimental autoimmune encephalomyelitis. Glia 51:: 235--240.
28. van Loo G, De Lorenzi R, Schmidt H, Huth M, Mildner A, et al. ((2006)) Inhibition of transcription factor NF-kappaB in the central nervous system ameliorates autoimmune encephalomyelitis in mice. Nat Immunol 7:: 954--961.
29. Brambilla R, Persaud T, Hu X, Karmally S, Shestopalov VI, et al. ((2009)) Transgenic inhibition of astroglial NF-kappa B improves functional outcome in experimental autoimmune encephalomyelitis by suppressing chronic central nervous system inflammation. J Immunol 182:: 2628--2640.
30. Faulkner JR, Herrmann JE, Woo MJ, Tansey KE, Doan NB, et al. ((2004)) Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci 24:: 2143--2155.
31. Liedtke W, Edelmann W, Chiu FC, Kucherlapati R, Raine CS, ((1998)) Experimental autoimmune encephalomyelitis in mice lacking glial fibrillary acidic protein is characterized by a more severe clinical course and an infiltrative central nervous system lesion. Am J Pathol 152:: 251--259.
32. Pender MP, Rist MJ, ((2001)) Apoptosis of inflammatory cells in immune control of the nervous system: role of glia. Glia 36:: 137--144.
33. Tran EH, Prince EN, Owens T, ((2000)) IFN-gamma shapes immune invasion of the central nervous system via regulation of chemokines. J Immunol 164:: 2759--2768.
34. Campbell IL, Abraham CR, Masliah E, Kemper P, Inglis JD, et al. ((1993)) Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6. Proc Natl Acad Sci USA 90:: 10061--10065.
35. Beck J, Rondot P, Catinot L, Falcoff E, Kirchner H, et al. ((1988)) Increased production of interferon gamma and tumor necrosis factor precedes clinical manifestation in multiple sclerosis: do cytokines trigger off exacerbations? Acta Neurol Scand 78:: 318--323.
36. Probert L, Eugster HP, Akassoglou K, Bauer J, Frei K, et al. ((2000)) TNFR1 signalling is critical for the development of demyelination and the limitation of T-cell responses during immune-mediated CNS disease. Brain 123:: 2005--2019.
37. Aloisi F, Penna G, Cerase J, Menéndez Iglesias B, Adorini L, ((1997)) IL-12 production by central nervous system microglia is inhibited by astrocytes. J Immunol 159:: 1604--1612.
38. Ambrosini E, Aloisi F, ((2004)) Chemokines and glial cells: a complex network in the central nervous system. Neurochem Res 29:: 1017--1038.
39. Clarke DL, Clifford RL, Jindarat S, Proud D, Pang L, et al. ((2010)) TNFα and IFNγ synergistically enhance transcriptional activation of CXCL10 in human airway smooth muscle cells via STAT-1, NF-κB, and the transcriptional coactivator CREB-binding protein. J Biol Chem 285:: 29101--29110.
40. Aricò E, Castiello L, Urbani F, Rizza P, Panelli MC, et al. ((2011)) Concomitant detection of IFNα signature and activated monocyte/dendritic cell precursors in the peripheral blood of IFNα-treated subjects at early times after repeated local cytokine treatments. J Transl Med 9:: 67--82.
41. Kang Z, Altuntas CZ, Gulen MF, Liu C, Giltiay N, et al. ((2010)) Astrocyte-restricted ablation of interleukin-17-induced Act1-mediated signaling ameliorates autoimmune encephalomyelitis. Immunity 32:: 414--425.
42. Ouyang W, Rutz S, Crellin NK, Valdez PA, Hymowitz SG, ((2011)) Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu Rev Immunol. 29:: 71--109.
43. Bettelli E, Das MP, Howard ED, Weiner HL, Sobel RA, et al. ((1998)) IL-10 is critical in the regulation of autoimmune encephalomyelitis as demonstrated by studies of IL-10- and IL-4-deficient and transgenic mice. J Immunol 161:: 3299--3306.
44. Cua DJ, Hutchins B, LaFace DM, Stohlman SA, Coffman RL, ((2001)) Central nervous system expression of IL-10 inhibits autoimmune encephalomyelitis. J Immunol 166:: 602--608.
45. Cannella B, Raine CS, ((2004)) Multiple sclerosis: cytokine receptors on oligodendrocytes predict innate regulation. Ann Neurol 55:: 46--57.
46. Menet V, Prieto M, Privat A, Gimenez y Ribotta M, ((2003)) Axonal plasticity and functional recovery after spinal cord injury in mice deficient in both glial fibrillary acidic protein and vimentin genes. Proc Natl Acad Sci USA 100:: 8999--9004.
47. Gonzalez JM, Bergmann CC, Ramakrishna C, Hinton DR, Atkinson R, et al. ((2006)) Inhibition of interferon-gamma signaling in oligodendroglia delays coronavirus clearance without altering demyelination. Am J Pathol 168:: 796--804.
48. Hamo L, Stohlman SA, Otto-Duessel M, Bergmann CC, ((2007)) Distinct regulation of MHC molecule expression on astrocytes and microglia during viral encephalomyelitis. Glia 55:: 1169--1177.