Dynamic seizure-related changes in extracellular signal-regulated kinase activation in a mouse model of temporal lobe epilepsy

Neuroscience

Volumn 156, Issue 1, 2008, Pages 222-237

  Houser, C R ^a,b   Huang, C S ^a,b   Peng, Z ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

Author keywords

dentate gyrus; ERK; hippocampus; immunohistochemistry; pilocarpine; spontaneous seizures

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PILOCARPINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; EXCITABILITY; HIPPOCAMPUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SEIZURE; TEMPORAL LOBE EPILEPSY;

ANIMALS; BIOLOGICAL MARKERS; CELL COUNT; CONVULSANTS; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; EPILEPSY; EPILEPSY, TEMPORAL LOBE; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; NEURAL PATHWAYS; NEURONS; PHOSPHORYLATION; PILOCARPINE; TIME FACTORS; UP-REGULATION;

EID: 51449121855     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.07.010     Document Type: Article

References (66)

1. Adams J.P., Anderson A.E., Varga A.W., Dineley K.T., Cook R.G., Pfaffinger P.J., and Sweatt J.D. The A-type potassium channel Kv4.2 is a substrate for the mitogen-activated protein kinase ERK. J Neurochem 75 (2000) 2277-2287
2. Arabadzisz D., Antal K., Parpan F., Emri Z., and Fritschy J.M. Epileptogenesis and chronic seizures in a mouse model of temporal lobe epilepsy are associated with distinct EEG patterns and selective neurochemical alterations in the contralateral hippocampus. Exp Neurol 194 (2005) 76-90
3. Baraban J.M., Fiore R.S., Sanghera J.S., Paddon H.B., and Pelech S.L. Identification of p42 mitogen-activated protein kinase as a tyrosine kinase substrate activated by maximal electroconvulsive shock in hippocampus. J Neurochem 60 (1993) 330-336
4. Berkeley J.L., Decker M.J., and Levey A.I. The role of muscarinic acetylcholine receptor-mediated activation of extracellular signal-regulated kinase 1/2 in pilocarpine-induced seizures. J Neurochem 82 (2002) 192-201
5. Berkeley J.L., and Levey A.I. Cell-specific extracellular signal-regulated kinase activation by multiple G protein-coupled receptor families in hippocampus. Mol Pharmacol 63 (2003) 128-135
6. Bernard C., Anderson A., Becker A., Poolos N.P., Beck H., and Johnston D. Acquired dendritic channelopathy in temporal lobe epilepsy. Science 305 (2004) 532-535
7. MAPK signaling in rat brain. J Neurochem 70 (1998) 558-571
8. Brisman J.L., Cosgrove G.R., and Cole A.J. Phosphorylation of P42/P44 MAP kinase and DNA fragmentation in the rat perforant pathway stimulation model of limbic epilepsy. Brain Res 933 (2002) 50-59
9. Choi Y.S., Lin S.L., Lee B., Kurup P., Cho H.Y., Naegele J.R., Lombroso P.J., and Obrietan K. Status epilepticus-induced somatostatinergic hilar interneuron degeneration is regulated by striatal enriched protein tyrosine phosphatase. J Neurosci 27 (2007) 2999-3009
10. Chronister R.B., and White S.R. Fiberarchitecture of the hippocampal formation: anatomy, projections, and structural significance. In: Isaacson R.L., and Pribram K.H. (Eds). The hippocampus: structure and development Vol. 1 (1975), Plenum Press, New York 9-39
11. Colom L.V., Garcia-Hernandez A., Castaneda M.T., Perez-Cordova M.G., and Garrido-Sanabria E.R. Septo-hippocampal networks in chronically epileptic rats: potential antiepileptic effects of theta rhythm generation. J Neurophysiol 95 (2006) 3645-3653
12. Davis S., Vanhoutte P., Pagès C., Caboche J., and Laroche S. The MAPK/ERK cascade targets both ELK-1 and cAMP response element-binding protein to control long-term potentiation-dependent gene expression in the dentate gyrus in vivo. J Neurosci 20 (2000) 4563-4572
13. Dudek S.M., and Fields R.D. Mitogen-activated protein kinase/extracellular signal-regulated kinase activation in somatodendritic compartments: roles of action potentials, frequency, and mode of calcium entry. J Neurosci 21 (2001) RC122
14. Dugladze T., Vida I., Tort A.B., Gross A., Otahal J., Heinemann U., Kopell N.J., and Gloveli T. Impaired hippocampal rhythmogenesis in a mouse model of mesial temporal lobe epilepsy. Proc Natl Acad Sci U S A 104 (2007) 17530-17535
15. Engel Jr. J., Kuhl D.E., Phelps M.E., and Mazziotta J.C. Interictal cerebral glucose metabolism in partial epilepsy and its relation to EEG changes. Ann Neurol 12 (1982) 510-517
16. English J.D., and Sweatt J.D. Activation of p42 mitogen-activated protein kinase in hippocampal long term potentiation. J Biol Chem 271 40 (1996) 24329-24332
17. Fiore R.S., Bayer V.E., Pelech S.L., Posada J., Cooper J.A., and Baraban J.M. p42 Mitogen-activated protein kinase in brain: prominent localization in neuronal cell bodies and dendrites. Neuroscience 55 (1993) 463-472
18. Flood D.G., Finn J.P., Walton K.M., Dionne C.A., Contreras P.C., Miller M.S., and Bhat R.V. Immunolocalization of the mitogen-activated protein kinases p42MAPK and JNK1, and their regulatory kinases MEK1 and MEK4, in adult rat central nervous system. J Comp Neurol 398 (1998) 373-392
19. Fox S.E., and Ranck Jr. J.B. Localization and anatomical identification of theta and complex spike cells in dorsal hippocampal formation of rats. Exp Neurol 49 (1975) 299-313
20. Fujise N., Hunziker W., Heizmann C.W., and Kosaka T. Distribution of the calcium binding proteins, calbindin D-28K and parvalbumin, in the subicular complex of the adult mouse. Neurosci Res 22 (1995) 89-107
21. Garrido Y.C.S., Sanabria E.R.G., Funke M.G., Cavalheiro E.A., and Naffah-Mazzacoratti M.G. Mitogen-activated protein kinase is increased in the limbic structures of the rat brain during the early stages of status epilepticus. Brain Res Bull 47 (1998) 223-229
22. Gass P., Kiessling M., and Bading H. Regionally selective stimulation of mitogen activated protein (MAP) kinase tyrosine phosphorylation after generalized seizures in the rat brain. Neurosci Lett 162 (1993) 39-42
23. Haneda M., Sugimoto T., and Kikkawa R. Mitogen-activated protein kinase phosphatase: a negative regulator of the mitogen-activated protein kinase cascade. Eur J Pharmacol 365 (1999) 1-7
24. Hao Y., Creson T., Zhang L., Li P., Du F., Yuan P., Gould T.D., Manji H.K., and Chen G. Mood stabilizer valproate promotes ERK pathway-dependent cortical neuronal growth and neurogenesis. J Neurosci 24 (2004) 6590-6599
25. Houser C.R., Huang C.S., and Peng Z. Decreased basal levels of phosphorylated ERK in pilocarpine-treated mice with recurrent seizures. Program No. 279.22. 2006 Neuroscience Meeting Planner (2006), Society for Neuroscience, Atlanta, GA. http://www.sfn.org/am2006/ http://www.sfn.org/am2006/
26. Huang F., Chotiner J.K., and Steward O. Actin polymerization and ERK phosphorylation are required for Arc/Arg3.1 mRNA targeting to activated synaptic sites on dendrites. J Neurosci 27 (2007) 9054-9067
27. Karlsson M., Mandl M., and Keyse S.M. Spatio-temporal regulation of mitogen-activated protein kinase (MAPK) signalling by protein phosphatases. Biochem Soc Trans 34 (2006) 842-845
28. Kim Y.S., Hong K.S., Seong Y.-S., Park J.-B., Kuroda S., Kishi K., Kaibuchi K., and Takai Y. Phosphorylation and activation of mitogen-activated protein kinase by kainic acid-induced seizure in rat hippocampus. Biochem Biophys Res Comm 202 (1994) 1163-1168
29. Kodama M., Russell D.S., and Duman R.S. Electroconvulsive seizures increase the expression of MAP kinase phosphatases in limbic regions of rat brain. Neuropsychopharmacology 30 (2005) 360-371
30. Komiyama N.H., Watabe A.M., Carlisle H.J., Porter K., Charlesworth P., Monti J., Strathdee D.J., O'Carroll C.M., Martin S.J., Morris R.G., O'Dell T.J., and Grant S.G. SynGAP regulates ERK/MAPK signaling, synaptic plasticity, and learning in the complex with postsynaptic density 95 and NMDA receptor. J Neurosci 22 (2002) 9721-9732
31. 18F]FDG-PET reveals temporal hypometabolism in patients with temporal lobe epilepsy even when quantitative MRI and histopathological analysis show only mild hippocampal damage. Arch Neurol 58 (2001) 933-939
32. Lisman J.E. Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci 20 (1997) 38-43
33. Merlo D., Cifelli P., Cicconi S., Tancredi V., and Avoli M. 4-Aminopyridine-induced epileptogenesis depends on activation of mitogen-activated protein kinase ERK. J Neurochem 89 (2004) 654-659
34. Mohajerani M.H., Sivakumaran S., Zacchi P., Aguilera P., and Cherubini E. Correlated network activity enhances synaptic efficacy via BDNF and the ERK pathway at immature CA3 CA1 connections in the hippocampus. Proc Natl Acad Sci U S A 104 (2007) 13176-13181
35. Nateri A.S., Raivich G., Gebhardt C., Da Costa C., Naumann H., Vreugdenhil M., Makwana M., Brandner S., Adams R.H., Jefferys J.G., Kann O., and Behrens A. ERK activation causes epilepsy by stimulating NMDA receptor activity. EMBO J 26 (2007) 4891-4901
36. O'Brien T.J., Newton M.R., Cook M.J., Berlangieri S.U., Kilpatrick C., Morris K., and Berkovic S.F. Hippocampal atrophy is not a major determinant of regional hypometabolism in temporal lobe epilepsy. Epilepsia 38 (1997) 74-80
37. Oyegbile T.O., Dow C., Jones J., Bell B., Rutecki P., Sheth R., Seidenberg M., and Hermann B.P. The nature and course of neuropsychological morbidity in chronic temporal lobe epilepsy. Neurology 62 (2004) 1736-1742
38. Peng Z., and Houser C.R. Temporal patterns of fos expression in the dentate gyrus after spontaneous seizures in a mouse model of temporal lobe epilepsy. J Neurosci 25 (2005) 7210-7220
39. Peng Z., Huang C.S., and Houser C.R. Transitory activation of extracellular signal-regulated kinase (ERK) by spontaneous seizures in a mouse model of temporal lobe epilepsy. Epilepsia 47 Suppl 4 (2006) 231
40. A receptor in a mouse model of temporal lobe epilepsy. J Neurosci 24 (2004) 8629-8639
41. Racine R.J. Modification of seizure activity by electrical stimulation: II. Motor seizure. Electroencephalogr Clin Neurophysiol 32 (1972) 281-294
42. Ren X., and Mody I. Gamma-hydroxybutyrate reduces mitogen-activated protein kinase phosphorylation via GABA B receptor activation in mouse frontal cortex and hippocampus. J Biol Chem 278 (2003) 42006-42011
43. Riban V., Bouilleret V., Pham-Le B.T., Fritschy J.M., Marescaux C., and Depaulis A. Evolution of hippocampal epileptic activity during the development of hippocampal sclerosis in a mouse model of temporal lobe epilepsy. Neuroscience 112 (2002) 101-111
44. Rosenberg G. The mechanisms of action of valproate in neuropsychiatric disorders: can we see the forest for the trees?. Cell Mol Life Sci 64 (2007) 2090-2103
45. Satoh Y., Endo S., Ikeda T., Yamada K., Ito M., Kuroki M., Hiramoto T., Imamura O., Kobayashi Y., Watanabe Y., Itohara S., and Takishima K. Extracellular signal-regulated kinase 2 (ERK2) knockdown mice show deficits in long-term memory; ERK2 has a specific function in learning and memory. J Neurosci 27 (2007) 10765-10776
46. Schrader L.A., Birnbaum S.G., Nadin B.M., Ren Y., Bui D., Anderson A.E., and Sweatt J.D. ERK/MAPK regulates the Kv4.2 potassium channel by direct phosphorylation of the pore-forming subunit. Am J Physiol Cell Physiol 290 (2006) C852-C861
47. Selcher J.C., Weeber E.J., Christian J., Nekrasova T., Landreth G.E., and Sweatt J.D. A role for ERK MAP kinase in physiologic temporal integration in hippocampal area CA1. Learn Mem 10 (2003) 26-39
48. 2+-stimulated adenylyl cyclases regulate ERK-dependent activation of MSK1 during fear conditioning. Neuron 53 (2007) 79-89
49. Steward O., Huang F., and Guzowski J.F. A form of perforant path LTP can occur without ERK1/2 phosphorylation or immediate early gene induction. Learn Mem 14 (2007) 433-445
50. Sweatt J.D. Mitogen-activated protein kinases in synaptic plasticity and memory. Curr Opin Neurobiol 14 (2004) 311-317
51. Theodosiou A., and Ashworth A. MAP kinase phosphatases. Genome Biol 3 (2002) REVIEWS3009
52. Thomas G.M., and Huganir R.L. MAPK cascade signalling and synaptic plasticity. Nat Rev Neurosci 5 (2004) 173-183
53. Thomas K.L., and Hunt S.P. The regional distribution of extracellularly regulated kinase-1 and -2 messenger RNA in the adult rat central nervous system. Neuroscience 56 (1993) 741-757
54. Thomas M.J., Watabe A.M., Moody T.D., Makhinson M., and O'Dell T.J. Postsynaptic complex spike bursting enables the induction of LTP by theta frequency synaptic stimulation. J Neurosci 18 (1998) 7118-7126
55. Turrigiano G. Homeostatic signaling: the positive side of negative feedback. Curr Opin Neurobiol 17 (2007) 318-324
56. Varga A.W., Anderson A.E., Adams J.P., Vogel H., and Sweatt J.D. Input-specific immunolocalization of differentially phosphorylated Kv4.2 in the mouse brain. Learn Mem 7 (2000) 321-332
57. Wang C.A., Lai M.C., Lui C.C., Yang S.N., Tiao M.M., Hsieh C.S., Lin H.H., and Huang L.T. An enriched environment improves cognitive performance after early-life status epilepticus accompanied by an increase in phosphorylation of extracellular signal-regulated kinase 2. Epilepsy Behav 11 (2007) 303-309
58. Watabe A.M., Zaki P.A., and O'Dell T.J. Coactivation of β-adrenergic and cholinergic receptors enhances the induction of long-term potentiation and synergistically activates mitogen-activated protein kinase in the hippocampal CA1 region. J Neurosci 20 (2000) 5924-5931
59. Winder D.G., Martin K.C., Muzzio I.A., Rohrer D., Chruscinski A., Kobilka B., and Kandel E.R. ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by beta-adrenergic receptors. Neuron 24 (1999) 715-726
60. Xi Z.Q., Wang X.F., He R.Q., Li M.W., Liu X.Z., Wang L.Y., Zhu X., Xiao F., Sun J.J., Li J.M., Gong Y., and Guan L.F. Extracellular signal-regulated protein kinase in human intractable epilepsy. Eur J Neurol 14 (2007) 865-872
61. Xia Z., Dudek H., Miranti C.K., and Greenberg M.E. Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J Neurosci 16 (1996) 5425-5436
62. + channels in hippocampus involves a mitogen-activated protein kinase pathway. J Neurosci 22 (2002) 4860-4868
63. Yuan P.X., Huang L.D., Jiang Y.M., Gutkind J.S., Manji H.K., and Chen G. The mood stabilizer valproic acid activates mitogen-activated protein kinases and promotes neurite growth. J Biol Chem 276 (2001) 31674-31683
64. Zhao M., Adams J.P., and Dudek S.M. Pattern-dependent role of NMDA receptors in action potential generation: consequences on extracellular signal-regulated kinase activation. J Neurosci 25 (2005) 7032-7039
65. Zhao W., Bianchi R., Wang M., and Wong R.K. Extracellular signal-regulated kinase 1/2 is required for the induction of group I metabotropic glutamate receptor-mediated epileptiform discharges. J Neurosci 24 (2004) 76-84
66. Zhou J.L., Lenck-Santini P.P., Zhao Q., and Holmes G.L. Effect of interictal spikes on single-cell firing patterns in the hippocampus. Epilepsia 48 (2007) 720-731