IFN-γ ameliorates autoimmune encephalomyelitis by limiting myelin lipid peroxidation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 36, 2015, Pages E5038-E5047

  Sosa, Rebecca A ^a   Murphey, Cathi ^a   Robinson, Rachel R ^a   Forsthuber, Thomas G ^a  

^a UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

Author keywords

APC; EAE; Interferon gamma; Myelin debris; T cell

Indexed keywords

ACETYLCYSTEINE; ANTIGEN; GAMMA INTERFERON; GAMMA INTERFERON RECEPTOR; MYELIN; INTERFERON RECEPTOR;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; LIPID PEROXIDATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; ANTIGEN PRESENTING CELL; APOPTOSIS; C57BL MOUSE; CELL CULTURE; DEFICIENCY; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; MYELIN SHEATH; PHAGOCYTOSIS; TRANSGENIC MOUSE;

ANIMALS; ANTIGEN-PRESENTING CELLS; APOPTOSIS; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FLOW CYTOMETRY; INTERFERON-GAMMA; LIPID PEROXIDATION; LYMPHOCYTE ACTIVATION; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MYELIN SHEATH; PHAGOCYTOSIS; RECEPTORS, INTERFERON; SIGNAL TRANSDUCTION;

EID: 84941242991     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1505955112     Document Type: Article

References (69)

1. Zamvil SS, Steinman L (1990) The T lymphocyte in experimental allergic encephalomyelitis. Annu Rev Immunol 8:579-621.
2. Panitch HS, Hirsch RL, Schindler J, Johnson KP (1987) Treatment of multiple sclerosis with gamma interferon: Exacerbations associated with activation of the immune system. Neurology 37(7):1097-1102.
3. Ferber IA, et al. (1996) Mice with a disrupted IFN-gamma gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE). J Immunol 156(1):5-7.
4. Chu CQ, Wittmer S, Dalton DK (2000) Failure to suppress the expansion of the activated CD4 T cell population in interferon gamma-deficient mice leads to exacerbation of experimental autoimmune encephalomyelitis. J Exp Med 192(1):123-128.
5. Dalton DK, Haynes L, Chu CQ, Swain SL, Wittmer S (2000) Interferon gamma eliminates responding CD4 T cells during mycobacterial infection by inducing apoptosis of activated CD4 T cells. J Exp Med 192(1):117-122.
6. Langrish CL, et al. (2005) IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 201(2):233-240.
7. Codarri L, et al. (2011) RORγt drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation. Nat Immunol 12(6):560-567.
8. El-Behi M, et al. (2011) The encephalitogenicity of T (H) 17 cells is dependent on IL-1- and IL-23-induced production of the cytokine GM-CSF. Nat Immunol 12(6):568-575.
9. Hirota K, et al. (2011) Fate mapping of IL-17-producing T cells in inflammatory responses. Nat Immunol 12(3):255-263.
10. Wang Y, et al. (2014) The transcription factors T-bet and Runx are required for the ontogeny of pathogenic interferon-γ-producing T helper 17 cells. Immunity 40(3):355-366.
11. Lee Y, et al. (2012) Induction and molecular signature of pathogenic TH17 cells. Nat Immunol 13(10):991-999.
12. Kebir H, et al. (2009) Preferential recruitment of interferon-gamma-expressing TH17 cells in multiple sclerosis. Ann Neurol 66(3):390-402.
13. McGeer PL, et al. (1993) Microglia in degenerative neurological disease. Glia 7(1):84-92.
14. Ponomarev ED, Shriver LP, Maresz K, Dittel BN (2005) Microglial cell activation and proliferation precedes the onset of CNS autoimmunity. J Neurosci Res 81(3):374-389.
15. Becher B, Antel JP (1996) Comparison of phenotypic and functional properties of immediately ex vivo and cultured human adult microglia. Glia 18(1):1-10.
16. Liu Y, et al. (2006) Suppression of microglial inflammatory activity by myelin phagocytosis: Role of p47-PHOX-mediated generation of reactive oxygen species. J Neurosci 26(50):12904-12913.
17. Christen S, Peterhans E, Stocker R (1990) Antioxidant activities of some tryptophan metabolites: Possible implication for inflammatory diseases. Proc Natl Acad Sci USA 87(7):2506-2510.
18. Sosa RA, Murphey C, Ji N, Cardona AE, Forsthuber TG (2013) The kinetics of myelin antigen uptake by myeloid cells in the central nervous system during experimental autoimmune encephalomyelitis. J Immunol 191(12):5848-5857.
19. Li X, McKinstry KK, Swain SL, Dalton DK (2007) IFN-gamma acts directly on activated CD4+ T cells during mycobacterial infection to promote apoptosis by inducing components of the intracellular apoptosis machinery and by inducing extracellular proapoptotic signals. J Immunol 179(2):939-949.
20. Neumann H, Kotter MR, Franklin RJM (2009) Debris clearance by microglia: An essential link between degeneration and regeneration. Brain 132(Pt 2):288-295.
21. Nielsen HH, et al. (2009) Enhanced microglial clearance of myelin debris in T Cellinfiltrated central nervous system. Journal of Neuropathology & Experimental Neurology 68(8):845-856.
22. Barbarese E, Nielson ML, Carson JH (1983) The effect of the shiverer mutation on myelin basic protein expression in homozygous and heterozygous mouse brain. J Neurochem 40(6):1680-1686.
23. Zarkovic N (2003) 4-hydroxynonenal as a bioactive marker of pathophysiological processes. Mol Aspects Med 24(4-5):281-291.
24. Mylonas C, Kouretas D (1999) Lipid peroxidation and tissue damage. In Vivo 13(3):295-309.
25. Pizzimenti S, et al. (2013) Interaction of aldehydes derived from lipid peroxidation and membrane proteins. Front Physiol 4(242):1-17.
26. Toshniwal PK, Zarling EJ (1992) Evidence for increased lipid peroxidation in multiple sclerosis. Neurochem Res 17(2):205-207.
27. Hunter MI, Nlemadim BC, Davidson DL (1985) Lipid peroxidation products and antioxidant proteins in plasma and cerebrospinal fluid from multiple sclerosis patients. Neurochem Res 10(12):1645-1652.
28. Koch M, et al. (2007) Plasma lipid peroxidation and progression of disability in multiple sclerosis. Eur J Neurol 14(5):529-533.
29. Naidoo R, Knapp ML (1992) Studies of lipid peroxidation products in cerebrospinal fluid and serum in multiple sclerosis and other conditions. Clin Chem 38(12):2449-2454.
30. Ljubisavljevic S, et al. (2013) Suppression of the lipid peroxidation process in the CNS reduces neurological expression of experimentally induced autoimmune encephalomyelitis. Folia Neuropathol 51(1):51-57.
31. Pasichna EP, Morozova RP, Donchenko HV, Vinychuk SM, Kopchak OO (2007) [Lipid peroxidation and antioxidant defence enzyme activity in multiple sclerosis]. Ukr Biokhim Zh (1999) 79(5):165-174.
32. Yoshida R, Murray HW, Nathan CF (1988) Agonist and antagonist effects of interferon alpha and beta on activation of human macrophages. Two classes of interferon gamma receptors and blockade of the high-affinity sites by interferon alpha or beta. J Exp Med 167(3):1171-1185.
33. Németh H, Toldi J, Vécsei L (2006) Kynurenines, Parkinson's disease and other neurodegenerative disorders: Preclinical and clinical studies. Parkinson's Disease and Related Disorders, Journal of Neural Transmission. Supplementa, eds Riederer P, Reichmann H, Youdim MBH, Gerlach M (Springer, Vienna), Vol 70, pp 285-304.
34. Werner-Felmayer G, et al. (1989) Characteristics of interferon induced tryptophan metabolism in human cells in vitro. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 1012(2):140-147.
35. Boven LA, et al. (2006) Myelin-laden macrophages are anti-inflammatory, consistent with foam cells in multiple sclerosis. Brain 129(Pt 2):517-526.
36. Haider L, et al. (2011) Oxidative damage in multiple sclerosis lesions. Brain 134(Pt 7):1914-1924.
37. Bisaga GN, Odinak MM, Boïko AN, Mel'nik IuB, Popova NF (2011) [Possibilities of treatment of multiple sclerosis exacerbations without corticosteroids: A role of metabolic and antioxidant therapy]. Zh Nevrol Psikhiatr Im S S Korsakova 111(2):44-48.
38. Smirnova LP, et al. (2011) [State of antioxidant system in patients with multiple sclerosis during therapy]. Biomed Khim 57(6):661-670.
39. Pentón-Rol G, et al. (2011) C-Phycocyanin ameliorates experimental autoimmune encephalomyelitis and induces regulatory T cells. Int Immunopharmacol 11(1):29-38.
40. Fiebiger SM, et al. (2013) The antioxidant idebenone fails to prevent or attenuate chronic experimental autoimmune encephalomyelitis in the mouse. J Neuroimmunol 262(1-2):66-71.
41. Rajda C, Bergquist J, Vécsei L (2007) Kynurenines, redox disturbances and neurodegeneration in multiple sclerosis. J Neural Transm Suppl 72:323-329.
42. Stüve O, et al. (2002) The role of the MHC class II transactivator in class II expression and antigen presentation by astrocytes and in susceptibility to central nervous system autoimmune disease. J Immunol 169(12):6720-6732.
43. Greter M, et al. (2005) Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis. Nat Med 11(3):328-334.
44. Dittel BN, Urbania TH, Janeway CA, Jr (2000) Relapsing and remitting experimental autoimmune encephalomyelitis in B cell deficient mice. J Autoimmun 14(4):311-318.
45. Gitik M, Liraz-Zaltsman S, Oldenborg PA, Reichert F, Rotshenker S (2011) Myelin down-regulates myelin phagocytosis by microglia and macrophages through interactions between CD47 on myelin and SIRPα (signal regulatory protein-α) on phagocytes. J Neuroinflammation 8(24):1-10.
46. Hosmane S, et al. (2012) Toll/interleukin-1 receptor domain-containing adapter inducing interferon-β mediates microglial phagocytosis of degenerating axons. J Neurosci 32(22):7745-7757.
47. Wang KC, et al. (2002) Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 417(6892):941-944.
48. Magnus T, Chan A, Grauer O, Toyka KV, Gold R (2001) Microglial phagocytosis of apoptotic inflammatory T cells leads to down-regulation of microglial immune activation. J Immunol 167(9):5004-5010.
49. Olah M, et al. (2012) Identification of a microglia phenotype supportive of remyelination. Glia 60(2):306-321.
50. Lampron A, et al. (2015) Inefficient clearance of myelin debris by microglia impairs remyelinating processes. J Exp Med 212(4):481-495.
51. Takahashi K, Prinz M, Stagi M, Chechneva O, Neumann H (2007) TREM2-transduced myeloid precursors mediate nervous tissue debris clearance and facilitate recovery in an animal model of multiple sclerosis. PLoS Med 4(4):e124.
52. Hsieh CL, et al. (2009) A role for TREM2 ligands in the phagocytosis of apoptotic neuronal cells by microglia. J Neurochem 109(4):1144-1156.
53. Paloneva J, et al. (2002) Mutations in two genes encoding different subunits of a receptor signaling complex result in an identical disease phenotype. Am J Hum Genet 71(3):656-662.
54. Ramprasad MP, et al. (1995) The 94- to 97-kDa mouse macrophage membrane protein that recognizes oxidized low density lipoprotein and phosphatidylserine-rich liposomes is identical to macrosialin, the mouse homologue of human CD68. Proc Natl Acad Sci USA 92(21):9580-9584.
55. Song L, Lee C, Schindler C (2011) Deletion of the murine scavenger receptor CD68. J Lipid Res 52(8):1542-1550.
56. Toni W, et al. (2012) In-vivo effects of GM-CSF treated monocytes in chronic DSS colitis. Ann Paediatr Rheumatol 1(4):26-26.
57. Matozaki T, Murata Y, Okazawa H, Ohnishi H (2009) Functions and molecular mechanisms of the CD47-SIRPalpha signalling pathway. Trends Cell Biol 19(2):72-80.
58. Takizawa H, Manz MG (2007) Macrophage tolerance: CD47-SIRP-alpha-mediated signals matter. Nat Immunol 8(12):1287-1289.
59. Kinchen JM, Ravichandran KS (2008) Phagocytic signaling: You can touch, but you can't eat. Curr Biol 18(12):R521-R524.
60. Perrin-Cocon L, et al. (2001) Oxidized low-density lipoprotein promotes mature dendritic cell transition from differentiating monocyte. J Immunol 167(7):3785-3791.
61. Shen LH, et al. (2008) Oxidized low-density lipoprotein induces differentiation of RAW264.7 murine macrophage cell line into dendritic-like cells. Atherosclerosis 199(2):257-264.
62. Raivich G, et al. (1999) Neuroglial activation repertoire in the injured brain: Graded response, molecular mechanisms and cues to physiological function. Brain Res Brain Res Rev 30(1):77-105.
63. Hanisch U-K, Kettenmann H (2007) Microglia: Active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10(11):1387-1394.
64. Bogie JF, Stinissen P, Hellings N, Hendriks JJ (2011) Myelin-phagocytosing macrophages modulate autoreactive T cell proliferation. J Neuroinflammation 8(85):1-13.
65. Popko B, Corbin JG, Baerwald KD, Dupree J, Garcia AM (1997) The effects of interferongamma on the central nervous system. Mol Neurobiol 14(1-2):19-35.
66. Delarasse C, et al. (2003) Myelin/oligodendrocyte glycoprotein-deficient (MOGdeficient) mice reveal lack of immune tolerance to MOG in wild-type mice. J Clin Invest 112(4):544-553.
67. Hövelmeyer N, et al. (2005) Apoptosis of oligodendrocytes via Fas and TNF-R1 is a key event in the induction of experimental autoimmune encephalomyelitis. J Immunol 175(9):5875-5884.
68. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351-358.
69. Ji N, et al. (2013) Small molecule inhibitor of antigen binding and presentation by HLA-DR2b as a therapeutic strategy for the treatment of multiple sclerosis. J Immunol 191(10):5074-5084.