AG490 prevents cell death after exposure of rat astrocytes to hydrogen peroxide or proinflammatory cytokines: Involvement of the Jak2/STAT pathway

Journal of Neurochemistry

Volumn 92, Issue 3, 2005, Pages 505-518

  Gorina, Roser ^a   Petegnief, Valérie ^a   Chamorro, Ángel ^b   Planas, Anna M ^a,b  

^a INST D INVESTIGACIONS B   (Spain)

^b INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

Author keywords

Antioxidant; Interferon ; Interleukin 10; Interleukin 6; Stat1; Stat3

Indexed keywords

CYTOKINE; GAMMA INTERFERON; HYDROGEN PEROXIDE; INTERLEUKIN 10; INTERLEUKIN 6; JANUS KINASE; JANUS KINASE 2; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; SERINE; STAT PROTEIN; STAT1 PROTEIN; STAT3 PROTEIN;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; NERVE CELL CULTURE; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; ASTROCYTES; CELL DEATH; CELLS, CULTURED; CYTOKINES; CYTOPROTECTION; DNA-BINDING PROTEINS; HYDROGEN PEROXIDE; INFLAMMATION MEDIATORS; INTERFERON TYPE II; INTERLEUKIN-10; INTERLEUKIN-6; JANUS KINASE 2; OXIDANTS; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; STAT3 TRANSCRIPTION FACTOR; TRANS-ACTIVATORS; TYRPHOSTINS;

ANIMALIA; JANUS;

EID: 13244277665     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02878.x     Document Type: Article

References (89)

1. Aloisi F., Penna G., Cerase J., Menendez Iglesias B. and Adorini L. (1997) IL-12 production by central nervous system microglia is inhibited by astrocytes. J. Immunol. 159, 1604-1612.
2. Beamer N. B., Coull B. M., Clark W. M., Haze J. S. and Silberger J. R. (1995) Interleukin-6 and interleukin-1 receptor antagonist in acute stroke. Ann. Neurol. 37, 800-805.
3. Bolin L. M., Strycharska-Orczyk I., Murray R., Langston J. W. and Di Monte D. (2002) Increased vulnerability of dopaminergic neurons in MPTP-lesioned interleukin-6 deficient mice. J. Neurochem. 83, 167-175.
4. Bolli R., Dawn B. and Xuan Y. T. (2003) Role of the JAK-STAT pathway in protection against myocardial ischemia/reperfusion injury. Trends Cardiovasc. Med. 13, 72-79.
5. Boyd Z. S., Kriatchko A., Yang J., Agarwal N., Wax M. B. and Paul R. V. (2003) Interleukin-10 receptor signaling through STAT-3 regulates the apoptosis of retinal ganglion cells in response to stress. Invest. Ophthalmol. Vis. Sci. 44, 5206-5211.
6. Catlett-Falcone R., Landowski T. H., Oshiro M. M. et al (1999) Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 10, 105-115.
7. Chan P. H. (2001) Reactive oxygen radicals in signalling and damage in the ischemic brain. J. Cereb. Blood Flow Metab. 21, 2-14.
8. Chung J., Uchida E., Grammer T. C. and Blenis J. (1997) STAT3 serine phosphorylation by ERK-dependent and -independent pathways negatively modulates its tyrosine phosphorylation. Mol. Cell. Biol 17, 6508-6516.
9. Chung J., Park E. S., Kim D. et al. (2000) Thyrotropin modulates interferon-gamma-mediated intercellular adhesion molecule-1 gene expression by inhibiting Janus kinase-1 and signal transducer and activator of transcription-1 activation in thyroid cells. Endocrinology 141, 2090-2097.
10. Darnell J. E. (1997) STATs and gene regulation. Science 277, 1630-1635.
11. Darnell J. E. Jr (1998) Studies of IFN-induced transcriptional activation uncover the Jak-Stat pathway. J. Interferon Cytokine Res. 18, 549-554.
12. Darnell J. E. Jr, Kerr I. M. and Stark G. R. (1994) Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264, 1415-1421.
13. Debonera F., Aldeguer X., Shen X., Gelman A. E., Gao F., Que X., Greenbaum L. E., Furth E. E., Taub R. and Olthoff K. M. (2001) Activation of interleukin-6/STAT3 and liver regeneration following transplantation. J. Surg. Res. 96, 289-295.
14. De-Fraja C., Conti L., Magrassi L., Govoni S. and Cattaneo E. (1998) Members of the JAK/STAT proteins are expressed and regulated during development in the mammalian forebrain. J. Neurosci. Res. 54, 320-330.
15. Dell'Albani P., Santangelo R., Torrisi L., Nicoletti V. G., de Vellis J. and Giuffrida Stella A. M. (2001) JAK/STAT signaling pathway mediates cytokine-induced iNOS expression in primary astroglial cell cultures. J. Neurosci. Res. 65, 417-424.
16. De Vos J., Jourdan M., Tarte K., Jasmin C. and Klein B. (2000) JAK2 tyrosine kinase inhibitor tyrphostin AG490 downregulates the mitogen-activated protein kinase (MAPK) and signal transducer and activator of transcription STAT pathways and induces apoptosis in myeloma cells. Br. J. Haematol. 109, 823-828.
17. Dimagl U., Iadecola C. and Moskowitz M. A. (1999) Pathobiology of ischemic stroke: an integrated view. Trends Neurosci. 22, 391-397.
18. Donnelly R. P., Dickensheets H. and Finbloom D. S. (1999) The interleukin-10 signal transduction pathway and regulation of gene expression in mononuclear phagocytes. J. Interferon Cytokine Res. 19, 563-573.
19. Duhé R. J., Clark E. A. and Farrar W. L. (2002) Characterization of the in vitro kinase activity of a partially purified soluble GST/JAK2 fusion protein. Mol. Cell. Biochem. 236, 23-35.
20. Durbin J. E., Hackenmiller R., Simon M. C. and Levy D. E. (1996) Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 84, 443-450.
21. Fauconneau B., Petegnief V., Sanfeliu C., Piriou A. and Planas A. M. (2002) Induction of heat shock proteins HSPs by sodium arsenite in cultured astrocytes and reduction of hydrogen peroxide-induced cell death. J. Neurochem. 83, 1338-1348.
22. Fukada T., Hibi M., Yamanaka Y., Takahashi-Tezuka M., Fujitani Y., Yamaguchi T., Nakajima K. and Hirano T. (1996) Two signals are necessary for cell proliferation induced by a cytokine receptor gp130: involvement of STAT3 in anti-apoptosis. Immunity 5, 449-460.
23. Ganster R. W., Taylor B. S., Shao L. and Geller D. A. (2001) Complex regulation of human inducible nitric oxide synthase gene transcription by Stat 1 and NF-kappa B. Proc. Natl. Acad. Sci. USA 98, 8638-8643.
24. Gautron L., Lafon P., Chaigniau M., Tramu G. and Laye S. (2002) Spatiotemporal analysis of signal transducer and activator of transcription 3 activation in rat brain astrocytes and pituitary following peripheral immune challenge. Neuroscience 112, 717-729.
25. Gerard C., Bruyns C., Marchant A., Abramowicz D., Vandenabeele P., Delvaux A., Fiers W., Goldman M. and Velu T. (1993) Interleukin 10 reduces the release of tumor necrosis factor and prevents lethality in experimental endotoxemia. J. Exp. Med. 177, 547-550.
26. Gerhartz, C., Heesel B., Sasse J., Hemmarm U., Landgraf C., Schneider-Mergener J., Horn F., Heinrich P. C. and Graeve L. (1996) Differential activation of acute phase response factor/STAT3 and STAT1 via the cytoplasmic domain of the interleukin-6 signal transducer gp130. 1. Definition of a novel phosphotyrosine motif mediating STAT1 activation. J. Biol. Chem. 271, 12 991-12 998.
27. Goh K. C., Haque S. J. and Williams B. R. (1999) p38 MAP kinase is required for STAT1 serine phosphorylation and transcriptional activation induced by interferons. EMBO J. 18, 5601-5608.
28. Guschin D., Rogers N., Briscoe J. et al. (1995) A major role for the protein tyrosine kinase JAK1 in the JAK/STAT signal transduction pathway in response to interleukin-6. EMBO J. 14, 1421-1429.
29. Haan C., Heinrich P. C. and Behrmann I. (2002) Structural requirements of the interleukin-6 signal transducer gp130 for its interaction with Janus kinase 1: the receptor is crucial for kinase activation. Biochem. J. 361, 105-111.
30. Hansen M. B., Nielsen S. E. and Berg K. (1989) Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J. Immunol. Meth. 119, 203-210.
31. Hattori R., Maulik N., Otani H., Zhu L., Cordis G., Engelman R. M., Siddiqui M. A. and Das D. K. (2001) Role of STAT3 in ischemic preconditioning. J. Mol. Cell Cardiol. 33, 1929-1936.
32. Heinrich P. C., Behrmann I., Müller-Newen G., Schaper F. and Graeve L. (1998) IL-6-type cytokine signalling through the gp130/JAK/STAT pathway. Biochem. J. 334, 297-314.
33. Heinrich P. C., Behrmann I., Haan S., Hermanns H. M., Muller-Newen G. and Schaper F. (2003) Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem. J. 374, 1-20.
34. Herrero C., Hu X., Li W. P., Samuels S., Sharif M. N., Kotenko S. and Ivashkiv L. B. (2003) Reprogramming of IL-10 activity and signaling by INF-γ. J. Immunol. 171, 5034-5041.
35. Hibi M., Nakajima K. and Hirano T. (1996) IL-6 cytokine family and signal transduction: a model of the cytokine system. J. Mol. Med. 74, 1-12.
36. Hirano T., Nakajima K. and Hibi M. (1997) Signaling mechanisms through gp130: a model of the cytokine system. Cytokine Growth Factor Rev. 8, 241-252.
37. Ihle J. N. (1995) The Janus protein tyrosine kinase family and its role in cytokine signaling. Adv. Immunol. 60, 1-35.
38. Ihle J. N. (2001) The Stat family in cytokine signaling. Curr. Opin. Cell Biol. 13, 211-217.
39. Imada K. and Leonard W. (2000) The Jak-STAT pathway. Mol. Immunol. 37, 1-11.
40. Jee Y., Kim G., Tanuma N. and Matsumoto Y. (2001) STAT expression and localization in the central nervous system during autoimmune encephalomyelitis in Lewis rats. J. Neuroimmunol. 114, 40-47.
41. Jenab S. and Quinones-Jenab V. (2002) The effects of interleukin-6, leukemia inhibitory factor and interferon-γ on STAT DNA binding and c-fos mRNA levels in cortical astrocytes and C6 glioma cells. Neuroendocrinol. Lett. 23, 325-328.
42. Justicia C., Gabriel C. and Planas A. M. (2000) Activation of the JAK/STAT pathway after transient focal cerebral ischemia: signalling through Jak1 and Stat3 in astrocytes. Glia 30, 253-270.
43. Juurlink B. H., Hertz L. and Yager J. Y. (1992) Astrocyte maturation and susceptibility to ischaemia or substrate deprivation. Neuroreport 3, 1135-1137.
44. Kim W. H., Hong F., Radaeva S., Jaruga B., Fan S. and Gao B. (2003) STAT1 plays an essential role in LPS/D-galactosamine-induced liver apoptosis and injury. Am. J. Physiol. Gastrointest. Liver Physiol. 285, G761-G768.
45. Kristof A. S., Marks-Konczalik J., Billings E. and Moss J. (2003) Stimulation of signal transducer and activator of transcription-1 (STAT1)-dependent gene transcription by lipopolysaccharide and interferon-γ is regulated by mammalian target of rapamycin. J. Biol. Chem. 278, 33 637-33 644.
46. LeBel; C. P., Ischiropoulos H. and Bondy S. C. (1992) Evaluation of the probe 2′,7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem. Res. Toxicol. 5, 227-231.
47. Lee J., Shin J. S., Park J. Y., Kwon D., Choi S. J., Kim S. J. and Choi I. H. (2003) p38 mitogen-activated protein kinase modulates expression of tumor necrosis factor-related apoptosis-inducing ligand induced by interferon-gamma in fetal brain astrocytes. J. Neurosci. Res. 15, 884-890.
48. Lee S. J., Park J. Y., Hou J. and Benveniste E. N. (1999) Transcriptional regulation of the intercellular adhesion molecule-1 gene by proinflammatory cytokines in human astrocytes. Glia 25, 21-32.
49. Lee Y. J. and Benveniste E. N. (1996) Stat1 alpha expression is involved in IFN-γ induction of the class II transactivator and class II MHC genes. J. Immunol. 157, 1559-1568.
50. Leonard W. J. and O'Shea J. J. (1998) Jaks and STATs: biological implications. Annu. Rev. Immunol. 16, 293-322.
51. Leu C. M., Wong F. H., Chang C., Huang S. F. and Hu C. P. (2003) Interleukin-6 acts as an antiapoptotic factor in human esophageal carcinoma cells through the activation of both STAT3 and mitogen-activated protein kinase pathways. Oncogene 22, 7809-7818.
52. Luo C. and Laaja P. (2004) Inhibitors of JAKs/STATs and the kinases: a possible new cluster of drugs. Drug Discov. Today 9, 268-275.
53. Madamanchi N. R., Li S., Patterson C. and Runge M. S. (2001) Reactive oxygen species regulate heat-shock protein 70 via the JAK/STAT pathway. Arterioscler. Thromb. Vasc. Biol. 21, 321-326.
54. Makuta Y., Sonoda Y., Yamamoto D., Funakoshi-Tago M., Aizu-Yokota E., Takebe Y. and Kasahara T. (2003) Interleukin-10-induced CCR5 expression in macrophage like HL-60 cells: involvement of Erk1/2 and STAT-3. Biol. Pharm. Bull. 26, 1076-1081.
55. Maziere C., Conte M. A. and Maziere J. C. (2001) Activation of JAK2 by the oxidative stress generated with oxidized low-density lipoprotein. Free Radic. Biol. Med. 31, 1334-1340.
56. Meraz M. A., White J. M., Sheehan K. C. et al. (1996) Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 84, 431-442.
57. Meydan N., Grunberger T., Dadi H. et al. (1996) Inhibition of acute lymphoblastic leukaemia by a Jak-2 inhibitor. Nature 379, 645-648.
58. Niehof M., Streetz K., Rakemann T., Bischoff S. C., Manns M. P., Horn F. and Trautwein C. (2001) Interleukin-6-induced tethering of STAT3 to the LAP/C/EBPbeta promoter suggests a new mechanism of transcriptional regulation by STAT3. J. Biol. Chem. 276, 9016-9027.
59. Park H., Ahn Y, Park C. K., Chung H. Y. and Park Y. (2003) Interleukin-6 protects MIN6 beta cells from cytokine-induced apoptosis. Ann. NY Acad. Sci. 1005, 242-249.
60. Pavelko K. D., Howe C. L., Drescher K. M., Gamez J. D., Johnson A. J., Wei T., Ransohoff R. M. and Rodriguez M. (2003) Interleukin-6 protects anterior horn neurons from lethal virus-induced injury. J. Neurosci. 23, 481-492.
61. Penkowa M., Giralt M., Lago N., Camats J., Carrasco J., Hernandez J., Molinero A., Campbell I. L. and Hidalgo J. (2003) Astrocyte-targeted expression of IL-6 protects the CNS against a focal brain injury. Exp. Neurol. 181, 130-148.
62. Planas A. M., Soriano M. A., Berruezo M., Justicia C., Estrada A., Pitarch S. and Ferrer I. (1996) Induction of Stat3, a signal transducer and transcription factor, in reactive microglia following transient focal cerebral ischaemia. Eur. J. Neurosci. 8, 2612-2618.
63. Planas A. M., Berruezo M., Justicia C., Barron S. and Ferrer I. (1997a) Stat3 is present in the developing and adult rat cerebellum and participates in the formation of transcription complexes binding DNA at the sis-inducible element. J. Neurochem. 68, 1345-1351.
64. Planas A. M., Justicia C. and Ferrer I. (1997b) Stat1 in developing and adult rat brain. Induction after transient focal ischemia. Neuroreport 8, 1359-1362.
65. Robinson K. A., Stewart C. A., Pye Q. N., Nguyen X., Kenney L., Salzman S., Floyd R. A. and Hensley K. (1999) Redox-sensitive protein phosphatase activity regulates the phosphorylation state of p38 protein kinase in primary astrocyte culture. J. Neurosci. Res. 55, 724-732.
66. Rodig S. J., Meraz M. A., White J. M. et al. (1998) Disruption of the Jak1 gene demonstrates obligatory and nonredundant roles of the Jaks in cytokine-induced biologic responses. Cell 93, 373-383.
67. Schindler C. and Darnell J. E. Jr (1995) Transcriptional responses to polypeptide ligands: the JAK-STAT pathway. Annu. Rev. Biochem. 64, 621-651.
68. Schumann G., Huell M., Machein U., Hocke G. and Fiebich B. L. (1999) Interleukin-6 activates signal transducer and activator of transcription and mitogen-activated protein kinase signal transduction pathways and induces de novo protein synthesis in human neuronal cells. J. Neurochem. 73, 2009-2017.
69. Simon A. M., Rai U., Fanburg B. L. and Cochran B. H. (1998) Activation of the JAK-STAT pathway by reactive oxygen species. Am. J. Physiol. 275 (Cell Physiol. 44), C1640-C1652.
70. Sriram K., Benkovic S. A., Hebert M. A., Miller D. B. and O'Callaghan J. P. (2004) Induction of gp130-related cytokines and activation of JAK2/STAT3 pathway in astrocytes precedes up-regulation of glial fibrillary acidic protein in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of neurodegeneration: key signaling pathway for astrogliosis in vivo? J. Biol. Chem. 19, 19 936-19 947.
71. Stahl N., Farruggella T. J., Boulton T. G., Zhong Z., Darnell J. E. Jr and Yancopoulos G. D. (1995) Choice of STATs and other substrates specified by modular tyrosine-based motifs in cytokine receptors. Science 267, 1349-1353.
72. Stephanou A., Scarabelli T. M., Townsend P. A., Bell R., Yellon D., Knigh R. A. and Latchman D. S. (2002) Induction of apoptosis and Fas receptor/Fas ligand expression by ischemia/reperfusion in cardiac myocytes requires serine 727 of the STAT-1 transcription factor but not tyrosine 701. FASEB J. 16, 1841-1843.
73. Suzuki S., Tanaka K., Nogawa S., Dembo T., Kosakai A. and Fukuuchi Y. (2001) Phosphorylation of signal transducer and activator of transcription-3 (Stat3) after focal cerebral ischemia in rats. Exp. Neurol. 170, 63-71.
74. Tacchini L., Fusar-Poli D. and Bernelli-Zazzera A. (2002) Activation of transcription factors by drugs inducing oxidative stress in rat liver. Biochem. Pharmacol. 63, 139-148.
75. Takagi Y., Harada J., Chiarugi A. and Moskowitz M. A. (2002) STAT1 is activated in neurons after ischemia and contributes to ischemic brain injury. J. Cereb. Blood Flow Metab. 22, 1311-1318.
76. Tarkowski E., Rosengren L., Blomstrand C., Wikkeisö C., Jensen C., Ekholm S. and Tarkowski A. (1995) Early intrathecal production of interleukin-6 predicts the size of brain lesion in stroke. Stroke 26, 1393-1398.
77. Terui K., Haga S., Enosawa S., Ohnuma N. and Ozaki M. (2004) Hypoxia/reoxygenation-induced, redox-dependent activation of Stat1 confers resistance to apoptotic cell death via hsp70 induction. Biochem. J. 380, 203-209.
78. Vila N., Castillo J., Davalos A. and Chamorro A. (2000) Proinflammatory cytokines and early neurological worsening in ischemic stroke. Stroke 31, 2325-2329.
79. Vila N., Castillo J., Davalos A., Esteve A., Planas A. M. and Chamorro A. (2003) Levels of anti-inflammatory cytokines and neurological worsening in acute ischemic stroke. Stroke 34, 671-675.
80. Walmsley M., Katsikis P. D., Abney E., Parry S., Williams R. O., Maini R. N. and Feldmann M. (1996) Interleukin-10 inhibition of the progression of established collagen-induced arthritis. Arthritis Rheum. 39, 495-503.
81. Wang L. H., Kirken R. A., Erwin R. A., Yu C. R. and Farrar W. L. (1999) JAK3, STAT, and MAPK signaling pathways as novel molecular targets for the tyrphostin AG-490 regulation of IL-2-mediated T cell response. J. Immunol. 162, 3897-3904.
82. Wen T. C., Peng H., Hata R., Desaki J. and Sakanaka M. (2001) Induction of phosphorylated-Stat3 following focal cerebral ischemia in mice. Neurosci. Lett. 303, 153-156.
83. Wen Z. and Darnell J. E. Jr (1997) Mapping of Stat3 serine phosphorylation to a single residue 727 and evidence that serine phosphorylation has no influence on DNA binding of Stat1 and Stat3. Nucl. Acids Res. 25, 2062-2067.
84. Wen Z. Z., Zhong Z. and Darnell J. E. Jr (1995) Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 82, 241-250.
85. Wesemann D. R. and Benveniste E. N. (2003) STAT-1 alpha and IFN-gamma as modulators of TNF-alpha signaling in macrophages: regulation and functional implications of the TNF receptor 1: STAT-1 alpha complex. J. Immunol. 171, 5313-5319.
86. Williams L., Bradley L., Smith A. and Foxwell B. (2004) Signal transducer and activator of transcription 3 is the dominant mediator of the anti-inflammatory effects of IL-10 in human macrophages. J. Immunol. 172, 567-576.
87. Wroblewski F. and LaDue J. S. (1955) Lactic dehydrogenase activity in blood. Proc. Soc. Exp. Biol. Med. 90, 210-213.
88. Yu X., Kennedy R. H. and Liu S. J. (2003) JAK2/STAT3, not ERK1/2, mediates interleukin-6-induced activation of inducible nitric-oxide synthase and decrease in contractility of adult ventricular myocytes. J. Biol. Chem. 278, 16 304-16 309.
89. Zhang Y., Turkson J., Carter-Su C., Smithgall T., Levitzki A., Kraker A., Krolewski J. J., Medveczky P. and Jove R. (2000) Activation of Stat3 in v-Src-transformed fibroblasts requires cooperation of Jak1 kinase activity. J. Biol. Chem. 275, 24 935-24 944.