c-Jun N-terminal kinase activation responses induced by hippocampal kindling are mediated by reactive astrocytes

Journal of Neuroscience

Volumn 26, Issue 32, 2006, Pages 8295-8304

  Cole Edwards, Kasie K ^a   Musto, Alberto E ^a   Bazan, Nicolas G ^a,b  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Lion's Eye Research Laboratories   (United States)

Author keywords

c Jun N terminal kinase; Epileptogenesis; Hippocampus; JNK; Kindling; p38; Reactive astrogliosis

Indexed keywords

CYCLIN DEPENDENT KINASE; ENZYME ANTIBODY; MITOGEN ACTIVATED PROTEIN KINASE; PAXILLIN; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; VIMENTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; CONTROLLED STUDY; ENZYME ACTIVATION; GENETIC TRANSCRIPTION; HIPPOCAMPUS; IMMUNOFLUORESCENCE TEST; KINDLING; MALE; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; SEIZURE; SYNAPTIC TRANSMISSION;

ANIMALS; ASTROCYTES; CELLS, CULTURED; DEEP BRAIN STIMULATION; ENZYME ACTIVATION; EPILEPSY, TEMPORAL LOBE; HIPPOCAMPUS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MAP KINASE SIGNALING SYSTEM; RATS; RATS, WISTAR;

EID: 33748205569     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1986-05.2006     Document Type: Article

References (47)

1. Adams B, Von Ling E, Vaccarella L, Ivy GO, Fahnestock M, Racine RJ (1998) Time course for kindling-induced changes in the hilar area of the dentate gyrus: reactive gliosis as a potential mechanism. Brain Res 804:331-336.
2. Aronica E, van Vliet EA, Mayboroda OA, Troost D, da Silva FH, Gorter JA (2000) Upregulation of metabotropic glutamate receptor subtype mGluR3 and mGluR5 in reactive astrocytes in a rat model of mesial temporal lobe epilepsy. Eur J Neurosci 12:2333-2344.
3. Bazan NG, Tu B, Rodriguez de Turco EB (2002) What synaptic lipid signaling tells us about seizure-induced damage and epileptogenesis. Prog Brain Res 135:175-185.
4. Bengzon J, Kokaia Z, Elmer E, Nanobashvili A, Kokaia M, Lindvall O (1997) Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc Natl Acad Sci USA 94:10432-10437.
5. Berman DE, Hazvi S, Rosenblum K, Seger R, Dudai Y (1998) Specific and differential activation of mitogen-activated protein kinase cascades by unfamiliar taste in the insular cortex of the behaving rat. J Neurosci 18:10037-10044.
6. Brecht S, Simler S, Vergnes M, Mielke K, Marescaux C, Herdegen T (1999) Repetitive electroconvulsive seizures induce activity of c-Jun N-terminal kinase and compartment-specific desensitization of c-Jun phosphorylation in the rat brain. Brain Res Mol Brain Res 68:101-108.
7. Cavazos JE, Das I, Sutula TP (1994) Neuronal loss induced in limbic pathways by kindling: evidence for induction of hippocampal sclerosis by repeated brief seizures. J Neurosci 14:3106-3121.
8. Coffey ET, Hongisto V, Dickens M, Davis RJ, Courtney MJ (2000) Dual roles for c-Jun N-terminal kinase in developmental and stress responses in cerebellar granule neurons. J Neurosci 20:7602-7613.
9. Colombo JA, Puissant VI (2002) Fluoro Jade stains early and reactive astroglia in the primate cerebral cortex. J Histochem Cytochem 50:1135-1137.
10. Curran BP, Murray HJ, O'Connor JJ (2003) A role for c-Jun N-terminal kinase in the inhibition of long-term potentiation by interleukin-1beta and long-term depression in the rat dentate gyrus in vitro. Neuroscience 118:347-357.
11. Falsig J, Porzgen P, Lotharius J, Leist M (2004) Specific modulation of astrocyte inflammation by inhibition of mixed lineage kinases with CEP-1347. J Immunol 173:2762-2770.
12. Ferrer I, Barrachina M, Tolnay M, Rey MJ, Vidal N, Carmona M, Blanco R, Puig B (2003a) Phosphorylated protein kinases associated with neuronal and glial tau deposits in argyrophilic grain disease. Brain Pathol 13:62-78.
13. Ferrer I, Pastor P, Rey MJ, Munoz E, Puig B, Pastor E, Oliva R, Tolosa E (2003b) Tau phosphorylation and kinase activation in familial tauopathy linked to deln296 mutation. Neuropathol Appl Neurobiol 29:23-34.
14. Goddard GV, McIntyre DC, Leech CK (1969) A permanent change in brain function resulting from daily electrical stimulation. Exp Neurol 25:295-330.
15. Gorter JA, van Vliet EA, Lopes da Silva FH, Isom LL, Aronica E (2002) Sodium channel beta1-subunit expression is increased in reactive astrocytes in a rat model for mesial temporal lobe epilepsy. Eur J Neurosci 16:360-364.
16. Herdegen T, Claret FX, Kallunki T, Martin-Villalba A, Winter C, Hunter T, Karin M (1998) Lasting N-terminal phosphorylation of c-Jun and activation of c-Jun N-terminal kinases after neuronal injury. J Neurosci 18:5124-5135.
17. Hua LL, Zhao ML, Cosenza M, Kim MO, Huang H, Tanowitz HB, Brosnan CF, Lee SC (2002) Role of mitogen-activated protein kinases in inducible nitric oxide synthase and TNFalpha expression in human fetal astrocytes. J Neuroimmunol 126:180-189.
18. Jeon SH, Kim YS, Bae CD, Park JB (2000) Activation of JNK and p38 in rat hippocampus after kainic acid induced seizure. Exp Mol Med 32:227-230.
19. Kaneko K, Itoh K, Berliner LJ, Miyasaka K, Fujii H (2002) Consequences of nitric oxide generation in epileptic-seizure rodent models as studied by in vivo EPR. Magn Reson Med 48:1051-1056.
20. Kashihara K, Sato K, Akiyama K, Okada S, Ishihara T, Hayabara T, Shomori T (1997) Temporal pattern of AP-1 DNA-binding activity in the rat hippocampus following a kindled seizure. Neuroscience 80:753-761.
21. Khurgel M, Ivy GO (1996) Astrocytes in kindling: relevance to epileptogenesis. Epilepsy Res 26:163-175.
22. Khurgel M, Racine RJ, Ivy GO (1992) Kindling causes changes in the composition of the astrocytic cytoskeleton. Brain Res 592:338-342.
23. Kim MO, Suh HS, Brosnan CF, Lee SC (2004) Regulation of RANTES/CCL5 expression in human astrocytes by interleukin-1 and interferon-beta. J Neurochem 90:297-308.
24. Ma W, Quirion R (2002) Partial sciatic nerve ligation induces increase in the phosphorylation of extracellular signal-regulated kinase (ERK) and c-Jun N-terminal kinase (JNK) in astrocytes in the lumbar spinal dorsal horn and the gracile nucleus. Pain 99:175-184.
25. Majkowski J (1999) Kindling: clinical relevance for epileptogenicity in humans. Adv Neurol 81:105-113.
26. Marcheselli VL, Bazan NG (1994) Platelet-activating factor is a messenger in the electroconvulsive shock-induced transcriptional activation of c-fos and zif-268 in hippocampus. J Neurosci Res 37:54-61.
27. Marcheselli VL, Bazan NG (1996) Sustained induction of prostaglandin endoperoxide synthase-2 by seizures in hippocampus. Inhibition by a platelet-activating factor antagonist. J Biol Chem 271:24794-24799.
28. Mattson MP, Bazan NG (2006) Apoptosis and necrosis. In: Basic neurochemistry, Ed 7 (Siegel G, Albers RW, Brady S, Price D, eds), in press. London: Elsevier.
29. Mielke K, Brecht S, Dorst A, Herdegen T (1999) Activity and expression of JNK1, p38 and ERK kinases, c-Jun N-terminal phosphorylation, and c-jun promoter binding in the adult rat brain following kainate-induced seizures. Neuroscience 91:471-483.
30. Migheli A, Piva R, Atzori C, Troost D, Schiffer D (1997) c-Jun, JNK/SAPK kinases and transcription factor NF-kappa B are selectively activated in astrocytes, but not motor neurons, in amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 56:1314-1322.
31. Minami M, Kuraishi Y, Satoh M (1991) Effects of kainic acid on messenger RNA levels of IL-1 beta, IL-6, TNF alpha and LIF in the rat brain. Biochem Biophys Res Commun 176:593-598.
32. Mukherjee PK, DeCoster MA, Campbell FZ, Davis RJ, Bazan NG (1999) Glutamate receptor signaling interplay modulates stress-sensitive mitogen-activated protein kinases and neuronal cell death. J Biol Chem 274:6493-6498.
33. Peltola J, Hurme M, Miettinen A, Keranen T (1998) Elevated levels of interleukin-6 may occur in cerebrospinal fluid from patients with recent epileptic seizures. Epilepsy Res 31:129-133.
34. Plata-Salaman CR, Ilyin SE, Turrin NP, Gayle D, Flynn MC, Romanovitch AE, Kelly ME, Bureau Y, Anisman H, McIntyre DC (2000) Kindling modulates the IL-1beta system, TNF-alpha, TGF-beta1, and neuropeptide mRNAs in specific brain regions. Brain Res Mol Brain Res 75:248-258.
35. Pretel S, Applegate CD, Piekut D (1997) Apoptotic and necrotic cell death following kindling induced seizures. Acta Histochem 99:71-79.
36. Racine RJ (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281-294.
37. Reibel S, Larmet Y, Le BT, Carnahan J, Marescaux C, Depaulis A (2000) Brain-derived neurotrophic factor delays hippocampal kindling in the rat. Neuroscience 100:777-788.
38. Schmued LC, Hopkins KJ (2000) Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 874:123-130.
39. Sheng JG, Boop FA, Mrak RE, Griffin WS (1994) Increased neuronal beta-amyloid precursor protein expression in human temporal lobe epilepsy: association with interleukin-1 alpha immunoreactivity. J Neurochem 63:1872-1879.
40. Shin T, Ahn M, Jung K, Heo S, Kim D, Jee Y, Lim YK, Yeo EJ (2003) Activation of mitogen-activated protein kinases in experimental autoimmune encephalomyelitis. J Neuroimmunol 140:118-125.
41. Sutula T, Cascino G, Cavazos J, Parada I, Ramirez L (1989) Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann Neurol 26:321-330.
42. Tu B, Bazan NG (2003) Hippocampal kindling epileptogenesis upregulates neuronal cyclooxygenase-2 expression in neocortex. Exp Neurol 179:167-175.
43. Ullian EM, Christopherson KS, Barres BA (2004) Role for glia in synaptogenesis. Glia 47:209-216.
44. Vezzani A, Moneta D, Richichi C, Aliprandi M, Burrows SJ, Ravizza T, Perego C, De Simoni MG (2002) Functional role of inflammatory cytokines and antiinflammatory molecules in seizures and epileptogenesis. Epilepsia 43 [Suppl 5]:30-35.
45. Xie Z, Smith CJ, Van Eldik LJ (2004) Activated glia induce neuron death via MAP kinase signaling pathways involving JNK and p38. Glia 45:170-179.
46. Xu X, Raber J, Yang D, Su B, Mucke L (1997) Dynamic regulation of c-Jun N-terminal kinase activity in mouse brain by environmental stimuli. Proc Natl Acad Sci USA 94:12655-12660.
47. Yang DD, Kuan CY, Whitmarsh AJ, Rincon M, Zheng TS, Davis RJ, Rakic P, Flavell RA (1997) Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature 389:865-870.