STAT1/IRF-1 signaling pathway mediates the injurious effect of interferon-gamma on oligodendrocyte progenitor cells

GLIA

Volumn 58, Issue 2, 2010, Pages 195-208

  Wang, Yan ^a   Ren, Zhihua ^a   Tao, Duan ^a   Tilwalli, Shilpa ^a   Goswami, Rajendra ^a   Balabanov, Roumen ^a  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Cell signaling; Interferon gamma; IRF 1; Oligodendrocyte progenitor cells; STAT1

Indexed keywords

GAMMA INTERFERON; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 1BETA CONVERTING ENZYME; PROTEIN KINASE R; STAT1 PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENETIC IDENTIFICATION; IN VITRO STUDY; NERVE CELL NECROSIS; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; STEM CELL; UPREGULATION;

ANIMALS; APOPTOSIS; CASPASE 1; CELL DEATH; EIF-2 KINASE; INTERFERON REGULATORY FACTOR-1; INTERFERON-GAMMA; JANUS KINASES; OLIGODENDROGLIA; RATS; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; STEM CELLS; UP-REGULATION;

EID: 73149097207     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20912     Document Type: Article

References (46)

1. Agresti C, Bernardo A, Del Russo N, Marziali G, Battistini A, Aloisi F, Levi G, Coccia E. 1998. Synergistic stimulation of MHC class I, IRF-1 gene expression by IFN-gamma and TNF-alpha in oligodendrocytes. Eur J Neurosci 10:2975-2983.
2. Agresti C, D'Urso D, Levi G. 1996. Reversible inhibitory effects of interferon-gamma and tumor necrosis factor-alpha on oligodendroglial lineage cell proliferation and differentiation in vitro. Eur J Neurosci 8:1106-1116.
3. Andrews T, Zhang P, Bhat N. 1998. TNF alpha potentiates IFN gamma-induced cell death in oligodendrocyte progenitors. J Neurosci Res 54:574-583.
4. Bach E, Aguet M, Schreiber R. 1997. The IFN-γ receptor: A paradigm for cytokine receptor signaling. Annu Rev Immunol 15:563-591.
5. Baerwald K, Corbin J, Popko B. 2000. Major histocompatibility complex heavy chain accumulation in the endoplasmic reticulum of oligodendrocytes results in myelin abnormalities. J Neurosci Res 15:160-169.
6. Baerwald K, Popko B. 1998. Developing and mature oligodendrocytes respond differently to the immune cytokine interferon-gamma. J Neurosci Res 52:230-239.
7. Balabanov R, Strand K, Goswami R, McMahon E, Begolka W, Miller S, Popko B. 2007. Interferon-gamma-oligodendrocyte interactions in the regulation of experimental autoimmune encephalomyelitis. J Neurosci 27:2013-2024.
8. Balabanov R, Strand K, Kemper A, Lee J, Popko B. 2006. Suppressor of cytokine signaling 1 expression protects oligodendrocytes from the deleterious effects of interferon-gamma. J Neuroscience 26:1543-1552.
9. Bouker K, Skaar T, Riggis R, Harburger D, Fernandez D, Zwart A, Wand A, Clark R. 2005. Interferon regulatory factor-1 (IRF-1) exhibits tumor suppressor activities in breast cancer associated with caspase activation and induction of apoptosis. Carcinogenesis 26:1527-1535.
10. Chew L, King W, Kennedy A, Gallo V. 2005. Interferon-gamma inhibits cell cycle exit in differentiating oligodendrocyte progenitor cells. Glia 52:127-143.
11. Corbin J, Kelly D, Rath E, Baerwald K, Suzuki K, Popko B. 1996. Targeted CNS expression of interferon-gamma in transgenic mice leads to hypomyelination, reactive gliosis, and abnormal cerebellar development. Mol Cell Neurosci 7:354-370.
12. Decker T, Kovarik P, Meinke A. 1997. GAS elements: A few nucleotides with a major impact on cytokine-induced gene expression. J Interferon Cytokine Res 17:121-134.
13. D'souza SD, Bonetti B, Balasingam V, Cashman NR, Barker PA, Troutt AB, Raine CS, Antel JP. 1996. Multiple sclerosis: Fas signaling in oligodendrocyte cell death. J Exp Med 184:2361-2370.
14. Egwuagu C, Li W, Yu C, Lin M, Chan C, Nakamura T, Chapelinski A. 2006. Interferon-g induces regression of epithelial cell carcinoma: Critical roles of IRF-1 and ICSBP transcriptional factors. Oncogene 25:3670-3679.
15. Feng Q, Li P, Salamanca C, Huntsman D, Leung PC, Auersperg N. 2005. Caspase-1 alpha is down-regulated in human ovarian cancer cells and the overexpression of caspase-1alpha induces apoptosis. Cancer Res 65:8591-8596.
16. Fortunato G, Calcagno G, Bresciamorra V, Salvatore E, Filla A, Capone S, Liquori R, Borelli S, Gentile L, Borelli F, Borgia G, Sachetti L. 2008. Multiple sclerosis and hepatitis C virus infection are associated with single nucleotide polymorphisms in interferon pathway genes. J Interferon Cytokine Res 28:141-152.
17. Gil J, Alcaḿ J, Esteban M. 1999. Induction of apoptosis by double-stranded-RNA-dependent protein kinase (PKR) involves the alpha subunit of eukaryotic translation initiation factor 2 and NF-kappaB. Mol Cell Biol 19:4653-4663.
18. Gonzalez J, Bergmann C, Ramakrishna C, Hinton D, Atkinson R, Hoskin J, Macklin W, Stohlman S. 2006. Inhibition of interferon-gamma signaling in oligodendroglia delays coronavirus clearance without altering demyelination. Am J Pathol 168:796-804.
19. Gottschalk A, Joseph L, Quintáns J. 1993. Differential induction of Egr-1 expression in WEHI-231 sublines does not correlate with apoptosis. Eur J Immunol 23:2011-2015.
20. Höftberger R, Aboul-Enein F, Brueck W, Lucchinetti C, Rodriguez M, Schmidbauer M, Jellinger K, Lassmann H. 2004. Expression of major histocompatibility complex class I molecules on the different cell types in multiple sclerosis lesions. Brain Pathol 14:43-50.
21. Horiuchi M, Itoh A, Pleasure D, Itoh T. 2006. MEK-ERK signaling is involved in interferon-gamma-induced death of oligodendroglial progenitor cells. J Biol Chem 281:2095-2106.
22. Horwitz M, Evans C, McGavern D, Rodriguez M, Oldstone M. 1997. Primary demyelination in transgenic mice expressing interferongamma. Nature Med 3:1037-1041.
23. Huseby E, Liggit D, Brabb T, Schnamel B, Ohlen C, Goverman J. 2001. A pathogenic role for myelin-specific CD8(1) T cells in a model for multiple sclerosis. J Exp Med 194:669-676.
24. Kim E, Lee J, Namkoong S, Um S, Park J. 2002. Interferon regulatory factor-1 mediates interferon-γ-induced apoptosis in ovarian carcinoma cells. J Cell Biochem 85:369-380.
25. Kröger A, Köster M, Schroeder K, Hauser H, Mueller P. 2002. Activities of IRF-1. J Interferon Cytokine Res 22:5-14.
26. Lee E, Yoon C, Kim Y, Bae Y. 2007. The double stranded RNA-dependent protein kinase PKR plays a significant role in a sustained ER-stress induced apoptosis. FASEB Lett 581:4325-4332.
27. Lin W, Harding H, Ron D, Popko B. 2005. Endoplasmic reticulum stress modulates the response of myelinating oligodendrocytes to the immune cytokine interferon-gamma. J Cell Biol 169:603-612.
28. Lin W, Kemper A, Dupree J, Harding H, Ron D, Popko B. 2006. Interferon-gamma inhibits central nervous system remyelination through a process modulated by endoplasmic reticulum stress. Brain 129:1306-1318.
29. Matsuyama T, Kimura T, Kitagawa M, Pfeffer K, Kawakami T, Watanabe N, Kündig TM, Amakawa R, Kishihara K, Wakeham A. 1993. Targeted disruption of IRF-1 or IRF-2 results in abnormal type I IFN gene induction and aberrant lymphocyte development. Cell 75:83-97.
30. Meraz M, White J, Sheehan K, Bach E, Rodig S, Dighe A, Kaplan D, Riley J, Greenlund A, Camplee D, Carver-Moore K, Schreiber R. 1996. Targeted disruption of the Stat1 gene in mice reveals unexpected physiological specificity in the Jak-STAT signaling pathway. Cell 84:431-442.
31. Ming X, Li W, Maeda Y, Cook S, Chapin J, Husar W, Dowling P. 2002. Caspase 1 expression in multiple sclerosis plaques and cultured glial cells. J Neurol Sci 197:9-18.
32. Panitch N, Hirsch R, Haley A, Johnson K. 1987. Exacerbations of multiple sclerosis in patients treated with gamma interferon. Lancet 1:893-895.
33. Pouly S, Becher B, Blain M, Antel J. 2000. Interferon-gamma modulates human oligodendrocyte susceptibility to Fas-mediated injury. J Neuropathol Exp Neurol 59:280-286.
34. Ramana C, Gil M, Schreiber R, Stark G. 2002. STAT1-dependent and independent pathways in IFN-g-dependent signaling. Trends Immunol 23:96-101.
35. Romeo G, Fiorucci G, Chiantore M, Percario Z, Vannucchi S, Affabris E. 2002. IRF-1 as a negative regulator of cell proliferation. J Interferon Cytokine Res 22:39-47.
36. Rubinson DA, Dillon CP, Kwiatkowski AV, Sievers C, Yang L, Kopinja J, Rooney DL, Zhang M, Ihrig MM, McManus MT, Gertler FB, Scott ML, Van Parijs L. 2003. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat Genet 33:401-406.
37. Sato T, Selleri C, Young N, Maciejewski J. 1997. Inhibition of interferon regulatory factor-1 expression results in predominance of cell growth stimulatory effects of interferon-γ due to phosphorylation of Stat1 and Stat3. Blood 90:4749-4758.
38. Scheuner D, Patel R, Wang F, Lee K, Kumar K, Wu J, Nilson A, Karin M, Kaufman R. 2006. Double-stranded RNA-dependent protein kinase phosphorylation of the a-subunit of eukaryotic translation initiation factor 2 mediates apoptosis. J Biol Chem 30:21458-21468.
39. Schrijver HM, Hooper-van Veen T, van Belzen MJ, Crusius JB, Peña AS, Barkhof F, Polman CH, Uitdehaag BM. 2004. Polymorphisms in the genes encoding interferon-gamma and interferon-gamma receptors in multiple sclerosis. Eur J Immunogenet 31:133-140.
40. Tada Y, Ho A, Matsuyma T, Mak T. 1997. Reduced incidence and severity of antigen-induced autoimmune diseases in mice lacking interferon regulatory factor-1. J Exp Med 185:231-238.
41. Tamunara T, Ishihara M, Lamphier M, Tanaka N, Oishi I, Aizawa S, Matsuyama T., Mak T, Taki S, Tanuguchi T. 1995. An IRF-1-dependent pathway of DNA damage-induced apoptosis in mitogen activated T lymphocytes. Nature 376:586-589.
42. Taniguchi T, Ogasavara K, Takaoka A, Tanaka N. 2001. IRF family of transcription factors as regulators of host defense. Annu Rev Immunol 19:623-655.
43. Torres C, Aranguez I, Rubino N. 1995. Expression of interferon-gamma receptor on murine oligodendrocytes and its regulation by cytokines and mitogens. Immunology 86:250-255.
44. Vartanian T, Li Y, Zhao M, Stefansson K. 1995. Interferon-γ induced oligodendrocyte cell death: Implications for the pathogenesis of multiple sclerosis. Mol Med 1:732-743.
45. Watson G, de Oliveira P, Stang M, Armstrong M, Gooding W, Kuan S, Yim J, Hughes S. 2006. Ad-IRF-1 induces apoptosis in esophageal adenocarcinoma. Neoplasia 8:31-37.
46. Xu J, Chen S, Ahmet H, Chen H, Ku G, Goldberg M, Hsu C. 2001. Amyloid-β peptides are cytotoxic to oligodendrocytes. J Neurosci 21:1-5.