Neuroprotection of interleukin-6 against NMDA-induced neurotoxicity is mediated by JAK/STAT3, MAPK/ERK, and PI3K/AKT signaling pathways

Cellular and Molecular Neurobiology

Volumn 33, Issue 2, 2013, Pages 241-251

  Fang, Xiao Xia ^a   Jiang, Xiao Lin ^a   Han, Xin Hua ^a   Peng, Yu Ping ^a   Qiu, Yi Hua ^a  

^a NANTONG MEDICAL COLLEGE   (China)

Author keywords

Ca2+ overload; Cerebellar granule neurons; cPLA2; Gp130; IL 6; NMDA

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; CALCIUM ION; CYTOSOLIC PHOSPHOLIPASE A2; GLYCOPROTEIN GP 130; INTERLEUKIN 6; JANUS KINASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; STAT3 PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELL DEATH; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; INTRACELLULAR SIGNALING; NERVE CELL; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; REAL TIME POLYMERASE CHAIN REACTION; STAINING; UPREGULATION; WESTERN BLOTTING;

ANIMALS; ANTIBODIES, MONOCLONAL; CALCIUM; CELL DEATH; CHROMONES; CYTOKINE RECEPTOR GP130; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLAVONOIDS; INTERLEUKIN-6; JANUS KINASES; MAP KINASE SIGNALING SYSTEM; MORPHOLINES; N-METHYLASPARTATE; NEURONS; NEUROPROTECTIVE AGENTS; NEUROTOXINS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHOLIPASES A2, CYTOSOLIC; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TYRPHOSTINS; UP-REGULATION;

RATTUS;

EID: 84878441683     PISSN: 02724340     EISSN: 15736830     Source Type: Journal    
DOI: 10.1007/s10571-012-9891-6     Document Type: Article

References (40)

1. Ali C, Nicole O, Docagne F, Lesne S, MacKenzie ET, Nouvelot A, Buisson A, Vivien D (2000) Ischemia-induced interleukin-6 as a potential endogenous neuroprotective cytokine against NMDA receptor-mediated excitotoxicity in the brain. J Cereb Blood Flow Metab 20:956-966
2. Arundine M, Tymianski M (2003) Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity. Cell Calcium 34:325-337
3. Baker DG, Ekhator NN, Kasckow JW, Hill KK, Zoumakis E, Dashevsky BA, Chrousos GP, Geracioti TD Jr (2001) Plasma and cerebrospinal fluid interleukin-6 concentrations in posttraumatic stress disorder. NeuroImmunoModulation 9:209-217
4. Baranzini SE, Elfstrom C, Chang SY, Butunoi C, Murray R, Higuchi R, Oksenberg JR (2000) Transcriptional analysis of multiple sclerosis brain lesions reveals a complex pattern of cytokine expression. J Immunol 165:6576-6582
5. Bauer J, Strauss S, Volk B, Berger M (1991) IL-6-mediated events in Alzheimer's disease pathology. Immunol Today 12:422
6. 2 in brain cell and tissue injury associated with ischemia and excitotoxicity. J Lipid Mediat Cell Signall 14:15-23
7. Burke JE, Dennis EA (2009) Phospholipase A2 structure/function, mechanism, and signaling. J Lipid Res 50:S237-S242
8. Campbell IL, Abraham CR, Masliah E, Kemper P, Inglis JD, Oldstone MB, Mucke L (1993) Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6. Proc Natl Acad Sci USA 90:10061-10065
9. Chang JY, Tsai PF (2009) IL-6 release from mouse glia caused by MeHg requires cytosolic phospholipase A2 activation. Neurosci Lett 461:85-89
10. Cucchiaroni ML, Viscomi MT, Bernardi G, Molinari M, Guatteo E, Mercuri NB (2010) Metabotropic glutamate receptor 1 mediates the electrophysiological and toxic actions of the cycad derivative beta-N-methylamino-l-alanine on substantia nigra pars compacta DAergic neurons. J Neurosci 30:5176-5188
11. D' Arcangelo G, Tancredi V, Onofri F, D' Antuono M, Giovedi S, Benfenati F (2000) Interleukin-6 inhibits neurotransmitter release and the spread of excitation in the rat cerebral cortex. Eur J Neurosci 12:1241-1252
12. Farooqui AQA, Ong WY, Horrocks LA (2006) Inhibitors of brain phospholipase A2 activity: their neuropharmacological effects and therapeutic importance for the treatment of neurologic disorders. Pharmacol Rev 58:591-620
13. Fernández-Sánchez MT, Novelli A (1993) Basic fibroblast growth factor protects cerebellar neurons in primary culture from NMDA and non-NMDA receptor mediated neurotoxicity. FEBS Lett 235:124-131
14. Frei K, Fredrikson S, Fontana A, Link H (1991) Interleukin-6 is elevated in plasma in multiple sclerosis. J Neuroimmunol 31:147-153
15. Fukada T, Hibi M, Yamanaka Y, Takahashi-Tezuka M, Fujitani Y, Yamaguchi T, Nakajima K, 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
16. Gadient RA, Otten U (1993) Differential expression of interleukin-6 (IL-6) and interleukin-6 receptor (IL-6R) mRNAs in rat hypothalamus. Neurosci Lett 153:13-16
17. Gadient RA, Otten U (1994) Identification of interleukin-6 (IL-6)-expressing neurons in the cerebellum and hippocampus of normal adult rats. Neurosci Lett 182:243-246
18. Gentile MT, Reccia MG, Sorrentino PP, Vitale E, Sorrentino G, Puca AA, Colucci-D'Amato L (2012) Role of cytosolic calcium-dependent phospholipase A2 in Alzheimer's disease pathogenesis. Mol Neurobiol 45:596-604
19. Gruol DL, Nelson TE (2005) Purkinje neuron physiology is altered by the inflammatory factor interleukin-6. Cerebellum 4:198-205
20. Ha BK, King JS (2000) Localization of gp130 in the developing and adult mouse cerebellum. J Chem Neuroanat 19:129-141
21. Hibi M, Hirano T (2000) Gab-family adapter molecules in signal transduction of cytokine and growth factor receptors, and T and B cell antigen receptors. Leuk Lymphoma 37:299-307
22. Inomata Y, Hirata A, Yonemura N, Koga T, Kido N, Tanihara H (2003) Neuroprotective effects of interleukin-6 on NMDA-induced rat retinal damage. Biochem Biophys Res Commun 302:226-232
23. Kamimura D, Ishihara K, Hirano T (2003) IL-6 signal transduction and its physiological roles: the signal orchestration model. Rev Physiol Biochem Pharmacol 149:1-38
24. Kriem B, Sponne I, Fifre A, Malaplate-Armand C, Lozac'h-Pillot K, Koziel V, Yen-Potin FT, Bihain B, Oster T, Jean-Luc Olivier, Pillot T (2005) Cytosolic phospholipase A2 mediates neuronal apoptosis induced by soluble oligomers of the amyloid-β peptide. FASEB J 19:85-87
25. Kushima Y, Hama T, Hatanaka H (1992) Interleukin-6 as a neurotrophic factor for promoting the survival of cultured catecholaminergic neurons in a chemically defined medium from fetal and postnatal rat midbrains. Neurosci Res 13:267-280
26. Liu Z, Qiu YH, Li B, Ma SH, Peng YP (2011) Neuroprotection of interleukin-6 against NMDA-induced apoptosis and its signal-transduction mechanisms. Neurotox Res 19:484-495
27. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using Real-Time quantitative PCR and the 2-44Ct method. Methods 25:402-408
28. Merrill JE, Chen IS (1991) HIV-1, macrophages, glial ells, and cytokines in AIDS nervous system disease. FASEB J 5:2391-2397
29. Nelson TE, Olde Engberink A, Hernandez R, Puro A, Huitron-Resendiz S, Hao C, De Graan PN, Gruol DL (2012) Altered synaptic transmission in the hippocampus of transgenic mice with enhanced central nervous systems expression of interleukin-6. Brain Behav Immun 26:959-971
30. Peng YP, Qiu YH, Lu JH, Wang JJ (2005) Interleukin-6 protects cultured cerebellar granule neurons against glutamate-induced neurotoxicity. Neurosci Lett 374:192-196
31. Pizzi M, Sarnico I, Boroni F, Benarese M, Dreano M, Garotta G, Valerio A, Spano P (2004) Prevention of neuron and oligodendrocyte degeneration by interleukin-6 (IL-6) and IL-6 receptor/IL-6 fusion protein in organotypic hippocampal slices. Mol Cell Neurosci 25:301-311
32. Qiu Z, Gruol DL (2003) Interleukin-6, beta-amyloid peptide and NMDA interactions in rat cortical neurons. J Neuroimmunol 139:51-57
33. Sharp JD, White DL (1993) Cytosolic PLA2: mRNA levels and potential for transcriptional regulation. J Lipid Mediat 8:183-189
34. Shelat PB, Chalimoniuk M, Wang JH, Strosznajder JB, Lee JC, Sun AY, Simonyi A, Sun GY (2008) Amyloid beta peptide and NMDA induce ROS from NADPH oxidase and AA release from cytosolic phospholipase A2 in cortical neurons. J Neurochem 106:45-55
35. Spooren A, Kolmus K, Laureys G, Clinckers R, De Keyser J, Haegeman G, Gerlo S (2011) Interleukin-6, a mental cytokine. Brain Res Rev 67:157-183
36. Stahl N, Farruggella TJ, Boulton TG, Zhong Z, Darnell JE Jr, Yancopoulos GD (1995) Choice of STATs and other substrates specified by modular tyrosine-based motifs in cytokine receptors. Science 267:1349-1353
37. 2+ release from intracellular store. Int J Neurosci 121:423-429
38. Tran HY, Shin EJ, Saito K, Nguyen XK, Chung YH, Jeong JH, Bach JH, Park DH, Yamada K, Nabeshima T, Yoneda Y, Kim HC (2012) Protective potential of IL-6 against trimethyltin-induced neurotoxicity in vivo. Free Radic Biol Med 52:1159-1174
39. Van Wagoner NJ, Benveniste EN (1999) Interleukin-6 expression and regulation in astrocytes. J Neuroimmunol 100:124-139
40. Wang XQ, Peng YP, Lu JH, Cao BB, Qiu YH (2009) Neuroprotection of interleukin-6 against NMDA attack and its signal transduction by JAK and MAPK. Neurosci Lett 450:122-126