JAK2-STAT3 signaling pathway mediates thrombin-induced proinflammatory actions of microglia in vitro

Journal of Neuroimmunology

Volumn 204, Issue 1-2, 2008, Pages 118-125

  Huang, Chengfang ^a   Ma, Rong ^a   Sun, Shenggang ^a   Wei, Guirong ^a   Fang, Yuan ^a   Liu, Rengang ^a   Li, Gang ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Dopaminergic neuron; iNOS; JAK2 STAT3 pathway; Microglia; Thrombin; TNF

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; JANUS KINASE 2; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; NITRIC OXIDE; STAT3 PROTEIN; THROMBIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL CULTURE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; GENE ACTIVATION; GENETIC TRANSCRIPTION; IN VITRO STUDY; MICROGLIA; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD11B; CELLS, CULTURED; COCULTURE TECHNIQUES; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; JANUS KINASE 2; MESENCEPHALON; MICROGLIA; NERVE DEGENERATION; NEURONS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; THROMBIN; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA; TYRPHOSTINS;

EID: 54849427454     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2008.07.004     Document Type: Article

References (54)

1. Aloisi F. Immune function of microglia. Glia 36 (2001) 165-179
2. Carreno-Müller E., Herrera A.J., de Pablos R.M., Tomas-Camardiel M., Venero J.L., Cano J., and Machado A. Thrombin induces in vivo degeneration of nigral dopaminergic neurons along with the activation of microglia. J. Neurochem. 84 (2003) 1201-1214
3. Choi S.H., Joe E.H., Kim S.U., and Jin B.K. Thrombin-induced microglial activation produces degeneration of nigral dopaminergic neurons in vivo. J. Neurosci. 23 (2003) 5877-5886
4. Choi S.H., Lee D.Y., Ryu J.K., Kim J., Joe E.H., and Jin B.K. Thrombin induces nigral dopaminergic neurodegeneration in vivo by altering expression of death-related proteins. Neurobiol. Dis. 14 (2003) 181-193
5. Choi S.H., Lee D.Y., Kim S.U., and Jin B.K. Thrombin-induced oxidative stress contributes to the death of hippocampal neurons in vivo: role of microglial NADPH oxidase. J. Neurosci. 25 (2005) 4082-4090
6. Chung E.S., Joe E.H., Ryu J.K., Kim J., Lee Y.B., Cho K.G., Oh Y.J., Maeng S.H., Baik H.H., Kim S.U., and Jin B.K. GT1b ganglioside induces death of dopaminergic neurons in rat mesencephalic cultures. Neuroreport 12 (2001) 611-614
7. Dihanich M., Kaser M., Reinhard E., Cunningham D., and Monard D. Prothrombin mRNA is expressed by cells of the nervous system. Neuron 6 (1991) 575-581
8. Darnell Jr. J.E., Kerr I.M., and Stark G.R. JAK-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264 (1994) 1415-1421
9. De Vos J., Jourdan M., Tarte K., Jasmin C., and Klein B. 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 (2000) 823-828
10. Donovan F.M., and Cunningham D.D. Signaling pathways involved in thrombin-induced cell protection. J. Biol. Chem. 273 (1998) 12746-12752
11. Donovan F.M., Pike C.J., Cotman C.W., and Cunningham D.D. Thrombin induces apoptosis in cultured neurons and astrocytes via a pathway requiring tyrosine kinase and RhoA activities. J. Neurosci. 17 (1997) 5316-5326
12. Ehret G.B., Reichenbach P., Schindler U., Horvath C.M., Fritz S., Nabholz M., and Bucher P. DNA binding specificity of different STAT proteins. Comparison of in vitro specificity with natural target sites. J. Biol. Chem. 276 (2001) 6675-6688
13. Flynn A.N., and Buret A.G. Proteinase-activated receptor 1 (PAR-1) and cell apoptosis. Apoptosis 9 (2004) 729-737
14. Fujimoto S., Katsuki H., Kume T., and Akaike A. Thrombin-induced delayed injury involves multiple and distinct signaling pathways in the cerebral cortex and the striatum in organotypic slice cultures. Neurobiol. Dis. 22 (2006) 130-142
15. Fujimoto S., Katsuki H., Ohnishi M., Takagi M., Kume T., and Akaike A. Thrombin induces striatal neurotoxicity depending on mitogen-activated protein kinase pathways in vivo. Neuroscience 144 (2007) 694-701
16. Gao H.M., Hong J.S., Zhang W., and Liu B. Distinct role for microglia in rotenone-induced degeneration of dopaminergic neurons. J. Neurosci. 22 (2002) 782-790
17. Gao J., Morrison D.C., Parmely T.J., Russell S.W., and Murphy W.J. An interferon-gamma-activated site (GAS) is necessary for full expression of the mouse iNOS gene in response to interferon-gamma and lipopolysaccharide. J. Biol. Chem. 272 (1997) 1226-1230
18. Han B.S., Hong H.S., Choi W.S., Markelonis G.J., Oh T.H., and Oh Y.J. Caspase-dependent and -independent cell death pathways in primary cultures of mesencephalic dopaminergic neurons after neurotoxin treatment. J. Neurosci. 23 (2003) 5069-5078
19. Herrera A.J., Tomas-Camardiel M., Venero J.L., Cano J., and Machado A. Inflammatory process as a determinant factor for the degeneration of substantia nigra dopaminergic neurons. J. Neural Transm. 112 (2005) 111-119
20. Herrera A.J., de Pablos R.M., Carreño-Müller E., Villarán R.F., Venero J.L., Tomás-Camardiel M., Cano J., and Machado A. The intrastriatal injection of thrombin in rat induced a retrograde apoptotic degeneration of nigral dopaminergic neurons through synaptic elimination. J. Neurochem. 3 (2008) 750-762
21. Katsuki H., Okawara M., Shibata H., Kume T., and Akaike A. Nitric oxide-producing microglia mediates thrombin-induced degeneration of dopaminergic neurons in rat midbrain slice culture. J. Neurochem. 97 (2006) 1232-1242
22. Kim O.S., Park E.J., Joe E.H., and Jou I. JAK-STAT signaling mediates gangliosides-induced inflammatory responses in brain microglial cells. J. Biol. Chem. 277 (2002) 40594-40601
23. Kim H.Y., Park E.J., Joe E.H., and Jou I. Curcumin suppresses Janus kinase-STAT inflammatory signaling through activation of Src homology 2 domain-containing tyrosine phosphatase 2 in brain microglia. J. Immunol. 171 (2003) 6072-6079
24. Kim W.G., Mohney R.P., Wilson B., Jeohn G.H., Liu B., and Hong J.S. Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J. Neurosci. 20 (2000) 6309-6316
25. Kishimoto T., Taga T., and Akira S. Cytokine signal transduction. Cell 76 (1994) 253-262
26. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19 (1996) 312-318
27. Lee D.Y., Oh Y.J., and Jin B.K. Thrombin-activated microglia contribute to death of dopaminergic neurons in rat mesencephalic cultures: dual roles of mitogen-activated protein kinase signaling pathways. Glia 51 (2005) 98-110
28. Liberatore G.T., Jackson-Lewis V., Vukosavic S., Mandir A.S., Vila M., McAuliffe W.G., Dawsib V.L., Dawson T.M., and Przedborski S. Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease. Nat. Med. 5 (1999) 1403-1409
29. Liu B., Wang K., Gao H.M., Mandavilli B., Wang J.Y., and Hong J.S. Molecular consequences of activated microglia in the brain: overactivation induces apoptosis. J. Neurochem. 77 (2001) 182-189
30. Madamanchi N.R., Li S., Patterson C., and Runge M.S. Thrombin regulates vascular smooth muscle cell growth and heat shock proteins via the JAK-STAT pathway. J. Biol. Chem. 276 (2001) 18915-18924
31. Marinissen M.J., Servitja J.M., Offermanns S., Simon M.I., and Gutkind J.S. Thrombin protease-activated receptor-1 signals through Gq- and G13-initiated MAPK cascades regulating c-Jun expression to induce cell transformation. J. Biol. Chem. 278 (2003) 46814-46825
32. McGuire S.O., Ling Z.D., lipton J.W., Sortwell C.E., Collier T.J., and Carvey P.M. Tumor necrosis factor alpha is toxic to embryonic mesencephalic dopamine neurons. Exp. Neurol. 169 (2001) 219-230
33. Merrill J.E., Ignarro L.J., Sherman M.P., Melinek J., and Lane T.E. Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide. J. Immunol. 151 (1993) 2132-2141
34. Mogi M., Harada M., Riederer P., Narabayashi H., Fujita K., and Nagatsu T. Tumor necrosis factor-alpha, (TNF-alpha) increases both in the brain and in the cerebrospinal fluid from parkinsonian patients. Neurosci. Lett. 165 (1994) 208-210
35. Noorbakhsh F., Vergnolle N., Hollenberg M.D., and Power C. Proteinase-activated receptors in the nervous system. Nat. Rev. Neurosci. 4 (2003) 981-990
36. Ohnishi M., Katsuki H., Fujimoto S., Takagi M., Kume T., and Akaike A. Involvement of thrombin and mitogen-activated protein kinase pathways in hemorrhagic brain injury. Exp. Neurol. 206 (2007) 43-52
37. O'Shea J.J., Pesu M., Borie D.C., and Changelian P.S. A new modality for immunosuppression: targeting the JAK/STAT pathway. Nat. Rev. Drug Discov. 3 (2004) 555-564
38. Park E.J., Park S.Y., Joe E., and Jou I. 15d-PGJ2 and rosiglitazone suppress Janus kinase-STAT inflammatory signaling through induction of suppressor of cytokine signaling 1 (SOCS 1) and SOCS3 in glia. J. Biol.Chem. 278 (2003) 14747
39. Ryu J., Pyo H., Jou I., and Joe E. Thrombin induces NO release from cultured rat microglia via protein kinase C, mitogen-activated protein kinase, and NF-kappa B. J. Biol. Chem. 275 (2000) 29955-29959
40. Smith-Swintosky V.L., Zimmer S., Fenton II J.W., and Mattson M.P. Protease nexin-1 and thrombin modulate neuronal Ca2+ homeostasis and sensitivity to glucose deprivation-induced injury. J. Neurosci. 15 (1995) 5840-5850
41. Soifer S.J., Peters K.G., O'Keefe J., and Coughlin S.R. Disparate temporal expression of the prothrombin and thrombin receptor genes during mouse development. Am. J. Pathol. 144 (1994) 60-69
42. Sriram K., Benkovic S.A., Hebert M.A., Miller D.B., and O'Callaghan J.P. 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. 279 (2004) 19936-19947
43. Stark G.R., Kerr I.M., Williams B.R., Silverman R.H., and Schreiber R.D. How cells respond to interferons?. Annu. Rev. Biochem. 67 (1998) 227-264
44. Stence N., Waite M., and Dailey M.E. Dynamics of microglial activation: a confocal time-lapse analysis in hippocampal slices. Glia 33 (2001) 256-266
45. Striggow F., Riek M., Breder J., Henrich-Noack P., Reymann K.G., and Reiser G. The protease thrombin is an endogenous mediator of hippocampal neuroprotection against ischemia at low concentrations but causes degeneration at high concentrations. Proc. Natl. Acad. Sci.U. S. A. 97 (2000) 2264-2269
46. Suo Z., Wu M., Ameenuddin S., Anderson H.E., Zoloty J.E., Citron B.A., Andrade-Gordon P., and Festoff B.W. Participation of protease-activated receptor-1 in thrombin-induced microglial activation. J. Neurochem. 80 (2002) 655-666
47. Suo Z., Wu M., Citron B.A., Palazzo R.E., and Festoff B.W. Rapid tau aggregation and delayed hippocampal neuronal death induced by persistent thrombin signaling. J. Biol. Chem. 278 (2003) 37681-37689
48. Turgeon V.L., Lloyd E.D., Wang S., Festoff B.W., and Houenou L.J. Thrombin perturbs neurite outgrowth and induces apoptotic cell death in enriched chick spinal motoneuron cultures through caspase activation. J. Neurosci. 18 (1998) 6882-6891
49. Vaughan P.J., Pike C.J., Cotman C.W., and Cunningham D.D. Thrombin receptor activation protects neurons and astrocytes from cell death produced by environmental insults. J. Neurosci. 15 (1995) 5389-5401
50. Wang H., Ubl J.J., Stricker R., and Reiser G. Thrombin (PAR-1)-induced proliferation in astrocytes via MAPK involves multiple signaling pathways. Am. J. Physiol., Cell Physiol. 283 (2002) C1351-C1364
51. Weinstein J.R., Gold S.J., Cunningham D.D., and Gall C.M. Cellular localization of thrombin receptor mRNA in rat brain: expression by mesencephalic dopaminergic neurons and codistribution with prothrombin mRNA. J. Neurosci. 15 (1995) 2906-2919
52. Xi G., Reiser G., and Keep R.F. The role of thrombin and thrombin receptors in ischemic, hemorrhagic and traumatic brain injury: deleterious or protective?. J. Neurochem. 84 (2003) 3-9
53. Yang M.S., Park E.J., Sohn S., Kwon H.J., Shin W.H., Pyo H.K., Jin B., Choi K.S., Jou I., and Joe E.H. Interleukin-13 and -4 induce death of activated microglia. Glia 38 (2002) 273-280
54. Yang Y., Akiyama H., Fenton II J.W., and Brewer G.J. Thrombin receptor on rat primary hippocampal neurons: coupled calcium and cAMP responses. Brain Res. 761 (1997) 11-18