Complementary roles of tumor necrosis factor alpha and interferon gamma in inducible microglial nitric oxide generation

Journal of Neuroimmunology

Volumn 204, Issue 1-2, 2008, Pages 101-109

  Mir, Margalida ^a   Tolosa, Laia ^a   Asensio, Víctor J ^a   Lladó, Jerònia ^a   Olmos, Gabriel ^a  

^a UNIVERSITAT DE LES ILLES BALEARS   (Spain)

Author keywords

Inducible nitric oxide synthase (iNOS); Interferon gamma (IFN ); Microglia; Nitric oxide; Tumor necrosis factor alpha (TNF )

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; ALPHA TUBULIN; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERFERON REGULATORY FACTOR 1; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE ACTIVATION; GENETIC TRANSCRIPTION; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; CEREBRAL CORTEX; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; INTERFERON-GAMMA; MICE; MICE, INBRED C57BL; MICROGLIA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; NITRITES; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 54849410809     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2008.07.002     Document Type: Article

References (62)

1. Bal-Price A., and Brown G.C. Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity. J. Neurosci. 21 (2001) 6480-6491
2. Bezzi P., Domercq M., Brambilla L., Galli R., Schols D., De Clercq E., Vescovi A., Bagetta G., Kollias G., Meldolesi J., and Volterra A. CXCR4-activated astrocyte glutamate release via TNFalpha: amplification by microglia triggers neurotoxicity. Nat. Neurosci. 4 (2001) 702-710
3. Blanchette J., Jaramillo M., and Olivier M. Signalling events involved in interferon-gamma-inducible macrophage nitric oxide generation. Immunology 108 (2003) 513-522
4. Blasi E., Barluzzi R., Bocchini V., Mazzolla R., and Bistoni F. Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus. J. Neuroimmunol. 27 (1990) 229-237
5. Block M.L., Zecca L., and Hong J.S. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev., Neurosci. 8 (2007) 57-69
6. Bocchini V., Mazzolla R., Barluzzi R., Blasi E., Sick P., and Kettenmann H. An immortalized cell line expresses properties of activated microglial cells. J. Neurosci. Res. 31 (1992) 616-621
7. Chao C.C., Molitor T.W., and Hu S. Neuroprotective role of IL-4 against activated microglia. J. Immunol. 151 (1993) 1473-1481
8. de Vera M.E., Shapiro R.A., Nussler A.K., Mudgett J.S., Simmons R.L., Morris Jr. S.M., Billiar T.R., and Geller D.A. Transcriptional regulation of human inducible nitric oxide synthase (NOS2) gene by cytokines: initial analysis of the human NOS2 promoter. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 1054-1059
9. Ding M., St Pierre B.A., Parkinson J.F., Medberry P., Wong J.L., Rogers N.E., Ignarro L.J., and Merrill J.E. Inducible nitric-oxide synthase and nitric oxide production in human fetal astrocytes and microglia. A kinetic analysis. J. Biol. Chem. 272 (1997) 11327-11335
10. Duncia J.V., Santella III J.B., Higley C.A., Pitts W.J., Wityak J., Frietze W.E., Rankin F.W., Sun J.H., Earl R.A., Tabaka A.C., Teleha C.A., Blom K.F., Favata M.F., Manos E.J., Daulerio A.J., Stradley D.A., Horiuchi K., Copeland R.A., Scherle P.A., Trzaskos J.M., Magolda R.L., Trainor G.L., Wexler R.R., Hobbs F.W., and Olson R.E. MEK inhibitors: the chemistry and biological activity of U0126, its analogs, and cyclization products. Bioorg. Med. Chem. Lett. 8 (1998) 2839-2844
11. Falsig J., Latta M., and Leist M. Defined inflammatory states in astrocyte cultures: correlation with susceptibility towards CD95-driven apoptosis. J. Neurochem. 88 (2004) 181-193
12. Fillit H., Ding W.H., Buee L., Kalman J., Altstiel L., Lawlor B., and Wolf-Klein G. Elevated circulating tumor necrosis factor levels in Alzheimer's disease. Neurosci. Lett. 129 (1991) 318-320
13. Green L.C., Wagner D.A., Glogowski J., Skipper P.L., Wishnok J.S., and Tannenbaum S.R. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal. Biochem. 126 (1982) 131-138
14. Guha M., O'Connell M.A., Pawlinski R., Hollis A., McGovern P., Yan S.F., Stern D., and Mackman N. Lipopolysaccharide activation of the MEK-ERK1/2 pathway in human monocytic cells mediates tissue factor and tumor necrosis factor alpha expression by inducing Elk-1 phosphorylation and Egr-1 expression. Blood 98 (2001) 1429-1439
15. Han I.O., Kim H.S., Kim H.C., Joe E.H., and Kim W.K. Synergistic expression of inducible nitric oxide synthase by phorbol ester and interferon-gamma is mediated through NF-κB and ERK in microglial cells. J. Neurosci. Res. 73 (2003) 659-669
16. Hanisch U.K. Microglia as a source and target of cytokines. Glia 40 (2002) 140-155
17. Harada H., Takahashi E., Itoh S., Harada K., Hori T.A., and Taniguchi T. Structure and regulation of the human interferon regulatory factor 1 (IRF-1) and IRF-2 genes: implications for a gene network in the interferon system. Mol. Cell. Biol. 14 (1994) 1500-1509
18. Hellendall R.P., and Ting J.P. Differential regulation of cytokine-induced major histocompatibility complex class II expression and nitric oxide release in rat microglia and astrocytes by effectors of tyrosine kinase, protein kinase C, and cAMP. J. Neuroimmunol. 74 (1997) 19-29
19. Hsiao H.Y., Mak O.T., Yang C.S., Liu Y.P., Fang K.M., and Tzeng S.F. TNF-alpha/IFN-gamma-induced iNOS expression increased by prostaglandin E2 in rat primary astrocytes via EP2-evoked cAMP/PKA and intracellular calcium signaling. Glia 55 (2007) 214-223
20. Iglesias M., Segura M.F., Comella J.X., and Olmos G. Mu-opioid receptor activation prevents apoptosis following serum withdrawal in differentiated SH-SY5Y cells and cortical neurons via phosphatidylinositol 3-kinase. Neuropharmacology 44 (2003) 482-492
21. Kim H.S., Whang S.Y., Woo M.S., Park J.S., Kim W.K., and Han I.O. Sodium butyrate suppresses interferon-gamma-, but not lipopolysaccharide-mediated induction of nitric oxide and tumor necrosis factor-alpha in microglia. J. Neuroimmunol. 151 (2004) 85-93
22. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19 (1996) 312-318
23. Kuno R., Wang J., Kawanokuchi J., Takeuchi H., Mizuno T., and Suzumura A. Autocrine activation of microglia by tumor necrosis factor-alpha. J. Neuroimmunol. 162 (2005) 89-96
24. Kuo M.L., and Yang N.C. Reversion of v-H-ras-transformed NIH 3T3 cells by apigenin through inhibiting mitogen activated protein kinase and its downstream oncogenes. Biochem. Biophys. Res. Commun. 212 (1995) 767-775
25. Levitzki A. Tyrphostins-potential antiproliferative agents and novel molecular tools. Biochem. Pharmacol. 40 (1990) 913-918
26. Liu Z.G., Hsu H., Goeddel D.V., and Karin M. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-κB activation prevents cell death. Cell 87 (1996) 565-576
27. Martin E., Nathan C., and Xie Q.W. Role of interferon regulatory factor 1 in induction of nitric oxide synthase. J. Exp Med. 180 (1994) 977-984
28. McGeer P.L., and McGeer E.G. Inflammatory processes in amyotrophic lateral sclerosis. Muscle Nerve 26 (2002) 459-470
29. Mhatre M., Floyd R.A., and Hensley K. Oxidative stress and neuroinflammation in Alzheimer's disease and amyotrophic lateral sclerosis: common links and potential therapeutic targets. J. Alzheimer's Dis. 6 (2004) 147-157
30. Minghetti L. Role of inflammation in neurodegenerative diseases. Curr. Opin. Neurol. 18 (2005) 315-321
31. Mount M.P., Lira A., Grimes D., Smith P.D., Faucher S., Slack R., Anisman H., Hayley S., and Park D.S. Involvement of interferon-gamma in microglial-mediated loss of dopaminergic neurons. J. Neurosci. 27 (2007) 3328-3337
32. Nakane M., Klinghofer V., Kuk J.E., Donnelly J.L., Budzik G.P., Pollock J.S., Basha F., and Carter G.W. Novel potent and selective inhibitors of inducible nitric oxide synthase. Mol. Pharmacol. 47 (1995) 831-834
33. Natarajan K., Singh S., Burke Jr. T.R., Grunberger D., and Aggarwal B.B. Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-κ B. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 9090-9095
34. Nathan C., and Xie Q.W. Regulation of biosynthesis of nitric oxide. J. Biol. Chem. 269 (1994) 13725-13728
35. Ohmori Y., Schreiber R.D., and Hamilton T.A. Synergy between interferon-gamma and tumor necrosis factor-alpha in transcriptional activation is mediated by cooperation between signal transducer and activator of transcription 1 and nuclear factor κB. J. Biol. Chem. 272 (1997) 14899-14907
36. Paludan S.R., Malmgaard L., Ellermann-Eriksen S., Bosca L., and Mogensen S.C. Interferon (IFN)-gamma and Herpes simplex virus/tumor necrosis factor-alpha synergistically induce nitric oxide synthase 2 in macrophages through cooperative action of nuclear factor-κ B and IFN regulatory factor-1. Eur. Cytokine Netw. 12 (2001) 297-308
37. Park J.S., Woo M.S., Kim S.Y., Kim W.K., and Kim H.S. Repression of interferon-gamma-induced inducible nitric oxide synthase (iNOS) gene expression in microglia by sodium butyrate is mediated through specific inhibition of ERK signaling pathways. J. Neuroimmunol. 168 (2005) 56-64
38. Pedranzini L., Dechow T., Berishaj M., Comenzo R., Zhou P., Azare J., Bornmann W., and Bromberg J. Pyridone 6, a pan-Janus-activated kinase inhibitor, induces growth inhibition of multiple myeloma cells. Cancer Res. 66 (2006) 9714-9721
39. Poloni M., Facchetti D., Mai R., Micheli A., Agnoletti L., Francolini G., Mora G., Camana C., Mazzini L., and Bachetti T. Circulating levels of tumour necrosis factor-alpha and its soluble receptors are increased in the blood of patients with amyotrophic lateral sclerosis. Neurosci. Lett. 287 (2000) 211-214
40. Saha R.N., and Pahan K. Regulation of inducible nitric oxide synthase gene in glial cells. Antioxid. Redox Signal. 8 (2006) 929-947
41. Sargsyan S.A., Monk P.N., and Shaw P.J. Microglia as potential contributors to motor neuron injury in amyotrophic lateral sclerosis. Glia 51 (2005) 241-253
42. Saura J., Tusell J.M., and Serratosa J. High-yield isolation of murine microglia by mild trypsinization. Glia 44 (2003) 183-189
43. Saura M., Zaragoza C., Bao C., McMillan A., and Lowenstein C.J. Interaction of interferon regulatory factor-1 and nuclear factor κB during activation of inducible nitric oxide synthase transcription. J. Mol. Biol. 289 (1999) 459-471
44. Schroder K., Hertzog P.J., Ravasi T., and Hume D.A. Interferon-gamma: an overview of signals, mechanisms and functions. J. Leukoc. Biol. 75 (2004) 163-189
45. Shen S., Yu S., Binek J., Chalimoniuk M., Zhang X., Lo S.C., Hannink M., Wu J., Fritsche K., Donato R., and Sun G.Y. Distinct signaling pathways for induction of type II NOS by IFNgamma and LPS in BV-2 microglial cells. Neurochem. Int. 47 (2005) 298-307
46. Sims S.H., Cha Y., Romine M.F., Gao P.Q., Gottlieb K., and Deisseroth A.B. A novel interferon-inducible domain: structural and functional analysis of the human interferon regulatory factor 1 gene promoter. Mol. Cell. Biol. 13 (1993) 690-702
47. Streit W.J. Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 40 (2002) 133-139
48. Streit W.J., Graeber M.B., and Kreutzberg G.W. Functional plasticity of microglia: a review. Glia 1 (1988) 301-307
49. Tansey M.G., McCoy M.K., and Frank-Cannon T.C. Neuroinflammatory mechanisms in Parkinson's disease: potential environmental triggers, pathways, and targets for early therapeutic intervention. Exp. Neurol. 208 (2007) 1-25
50. Tolosa L., Morla M., Iglesias A., Busquets X., Llado J., and Olmos G. IFN-gamma prevents TNF-alpha-induced apoptosis in C2C12 myotubes through down-regulation of TNF-R2 and increased NF-κB activity. Cell. Signal. 17 (2005) 1333-1342
51. Vila-del Sol V., Diaz-Munoz M.D., and Fresno M. Requirement of tumor necrosis factor alpha and nuclear factor-κB in the induction by IFN-gamma of inducible nitric oxide synthase in macrophages. J. Leukoc. Biol. 81 (2007) 272-283
52. Wajant H., Pfizenmaier K., and Scheurich P. Tumor necrosis factor signaling. Cell Death Differ. 10 (2003) 45-65
53. Wang Y., Wu T.R., Cai S., Welte T., and Chin Y.E. Stat1 as a component of tumor necrosis factor alpha receptor 1-TRADD signaling complex to inhibit NF-κB activation. Mol. Cell. Biol. 20 (2000) 4505-4512
54. Wei T., Chen C., Hou J., Xin W., and Mori A. Nitric oxide induces oxidative stress and apoptosis in neuronal cells. Biochim. Biophys. Acta 1498 (2000) 72-79
55. Wesemann D.R., and Benveniste E.N. 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 (2003) 5313-5319
56. Weydt P., and Moller T. Neuroinflammation in the pathogenesis of amyotrophic lateral sclerosis. NeuroReport 16 (2005) 527-531
57. Whitton P.S. Inflammation as a causative factor in the aetiology of Parkinson's disease. Br. J. Pharmacol. 150 (2007) 963-976
58. Wyss-Coray T., and Mucke L. Inflammation in neurodegenerative disease - a double-edged sword. Neuron 35 (2002) 419-432
59. Xie Q.W., and Nathan C. Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon-gamma and bacterial lipopolysaccharide. Trans. Assoc. Am. Physicians 106 (1993) 1-12
60. Xie Q.W., Kashiwabara Y., and Nathan C. Role of transcription factor NF-κ B/Rel in induction of nitric oxide synthase. J. Biol. Chem. 269 (1994) 4705-4708
61. Zhao M.L., Liu J.S., He D., Dickson D.W., and Lee S.C. Inducible nitric oxide synthase expression is selectively induced in astrocytes isolated from adult human brain. Brain Res. 813 (1998) 402-405
62. Zhao W., Xie W., Le W., Beers D.R., He Y., Henkel J.S., Simpson E.P., Yen A.A., Xiao Q., and Appel S.H. Activated microglia initiate motor neuron injury by a nitric oxide and glutamate-mediated mechanism. J. Neuropathol. Exp. Neurol. 63 (2004) 964-977