Pilocarpine-induced status epilepticus increases Homer1a and changes mGluR5 expression

Epilepsy Research

Volumn 101, Issue 3, 2012, Pages 253-260

  Cavarsan, C F ^a   Tescarollo, F ^a   Tesone Coelho, C ^a   Morais, R L T ^a   Motta, F L T ^a   Blanco, M M ^a   Mello, L E ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Epilepsy; Hippocampus; Homer1a; Immediate early genes; Pilocarpine model; Rat

Indexed keywords

MESSENGER RNA; METABOTROPIC RECEPTOR 5; PILOCARPINE; PROTEIN HOMER 1A;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENTORHINAL CORTEX; EPILEPTIC STATE; EPILEPTOGENESIS; GENE OVEREXPRESSION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; NERVE EXCITABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRIFORM CORTEX; RAT; RNA ANALYSIS;

ANIMALS; CARRIER PROTEINS; MALE; PILOCARPINE; RATS; RATS, WISTAR; RECEPTORS, METABOTROPIC GLUTAMATE; SEIZURES; STATUS EPILEPTICUS;

EID: 84866150660     PISSN: 09201211     EISSN: 18726844     Source Type: Journal    
DOI: 10.1016/j.eplepsyres.2012.04.011     Document Type: Article

References (60)

1. Ango F., Pin J.P., Tu J.C., Xiao B., Worley P.F., Bockaert J., Fagni L. Dendritic and axonal targeting of type 5 metabotropic glutamate receptor is regulated by homer1 proteins and neuronal excitation. J. Neurosci. 2000, 20:8710-8716.
2. Aronica E., Gorter J.A. Gene expression profile in temporal lobe epilepsy. Neuroscientist 2007, 13:100-108.
3. Avanzi R.D., Cavarsan C.F., Santos J.G., Hamani C., Mello L.E., Covolan L. Basal dendrites are present in newly born dentate granule cells of young but not aged pilocarpine-treated chronic epileptic rats. Neuroscience 2010, 170:687-691.
4. Avedissian M., Longo B.M., Jaqueta C.B., Schnabel B., Paiva P.B., Mello L.E., Briones M.R. Hippocampal gene expression analysis using the ORESTES methodology shows that homer 1a mRNA is upregulated in the acute period of the pilocarpine epilepsy model. Hippocampus 2007, 17:130-136.
5. Bottai D., Guzowski J.F., Schwarz M.K., Kang S.H., Xiao B., Lanahan A., Worley P.F., Seeburg P.H. Synaptic activity-induced conversion of intronic to exonic sequence in Homer 1 immediate early gene expression. J. Neurosci. 2002, 22:167-175.
6. Brakeman P.R., Lanahan A.A., O'Brien R., Roche K., Barnes C.A., Huganir R.L., Worley P.F. Homer: a protein that selectively binds metabotropic glutamate receptors.[see comment]. Nature 1997, 386:284-288.
7. Browne T.R., Holmes G.L. Epilepsy. N. Engl. J. Med. 2001, 344:1145-1151. [see comment] [erratum appears in N Engl J Med 2001 June 21, 344(25), 1956].
8. Cavalheiro E.A., Leite J.P., Bortolotto Z.A., Turski W.A., Ikonomidou C., Turski L. Long-term effects of pilocarpine in rats: structural damage of the brain triggers kindling and spontaneous recurrent seizures. Epilepsia 1991, 32:778-782.
9. Cavarsan C.F., Avanzi R.D.T., Queiroz C.M., Mello L.E., Covolan L. m1 acetylcholine receptor expression is decreased in hippocampal CA1 region of aged animals after pilocarpine-induced seizures. Aging Dis. 2011, 2(4). p. 301-3-7.
10. Christie B.R., Kerr D.S., Abraham W.C. Flip side of synaptic plasticity: long-term depression mechanisms in the hippocampus. Hippocampus 1994, 4:127-135.
11. Covolan L., Mello L.E. Temporal profile of neuronal injury following pilocarpine or kainic acid-induced status epilepticus. Epilepsy Res. 2000, 39:133-152.
12. Covolan L., Mello L.E. Assessment of the progressive nature of cell damage in the pilocarpine model of epilepsy. Braz. J. Med. Biol. Res. 2006, 39:915-924.
13. Duncan R.S., Hwang S.Y., Koulen P. Effects of Vesl/Homer proteins on intracellular signaling. Exp. Biol. Med. 2005, 230:527-535.
14. Ehrengruber M.U., Kato A., Inokuchi K., Hennou S. Homer/Vesl proteins and their roles in CNS neurons. Mol. Neurobiol. 2004, 29:213-227.
15. Elliott R.C., Lowenstein D.H. Gene expression profiling of seizure disorders. Neurochem. Res. 2004, 29:1083-1092.
16. 2+ stores and ion channels in neurons. Trends Neurosci. 2000, 23:80-88.
17. Feng W., Tu J., Yang T., Vernon P.S., Allen P.D., Worley P.F., Pessah I.N. Homer regulates gain of ryanodine receptor type 1 channel complex. J. Biol. Chem. 2002, 277:44722-44730.
18. Fotuhi M., Standaert D.G., Testa C.M., Penney J.B., Young A.B. Differential expression of metabotropic glutamate receptors in the hippocampus and entorhinal cortex of the rat. Brain Res. Mol. Brain Res. 1994, 21:283-292.
19. French P.J., O'Connor V., Jones M.W., Davis S., Errington M.L., Voss K., Truchet B., Wotjak C., Stean T., Doyere V., Maroun M., Laroche S., Bliss T.V. Subfield-specific immediate early gene expression associated with hippocampal long-term potentiation in vivo. Eur. J. Neurol. 2001, 13:968-976.
20. Hatazaki S., Bellver-Estelles C., Jimenez-Mateos E.M., Meller R., Bonner C., Murphy N., Matsushima S., Taki W., Prehn J.H., Simon R.P., Henshall D.C. Microarray profile of seizure damage-refractory hippocampal CA3 in a mouse model of epileptic preconditioning. Neuroscience 2007, 150:467-477.
21. Hunsberger J.G., Bennett A.H., Selvanayagam E., Duman R.S., Newton S.S. Gene profiling the response to kainic acid induced seizures. Brain Res. Mol. Brain Res. 2005, 141:95-112.
22. Irie K., Nakatsu T., Mitsuoka K., Miyazawa A., Sobue K., Hiroaki Y., Doi T., Fujiyoshi Y., Kato H. Crystal structure of the Homer 1 family conserved region reveals the interaction between the EVH1 domain and own proline-rich motif. J Mol Biol. 2002, 318:1117-1126.
23. Jacobs M.P., Fischbach G.D., Davis M.R., Dichter M.A., Dingledine R., Lowenstein D.H., Morrell M.J., Noebels J.L., Rogawski M.A., Spencer S.S., Theodore W.H. Future directions for epilepsy research. Neurology 2001, 57:1536-1542.
24. Jung K.H., Chu K., Lee S.T., Kim J.H., Kang K.M., Song E.C., Kim S.J., Park H.K., Kim M., Lee S.K., Roh J.K. Region-specific plasticity in the epileptic rat brain: a hippocampal and extrahippocampal analysis. Epilepsia 2009, 50:537-549.
25. Kammermeier P.J., Xiao B., Tu J.C., Worley P.F., Ikeda S.R. Homer proteins regulate coupling of group I metabotropic glutamate receptors to N-type calcium and M-type potassium channels. J. Neurosci. 2000, 20:7238-7245.
26. Kammermeier P.J., Worley P.F. Homer 1a uncouples metabotropic glutamate receptor 5 from postsynaptic effectors. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:6055-6060.
27. Kato A., Ozawa F., Saitoh Y., Hirai K., Inokuchi K. vesl, a gene encoding VASP/Ena family related protein, is upregulated during seizure, long-term potentiation and synaptogenesis. FEBS Lett. 1997, 412:183-189.
28. Kato A., Ozawa F., Saitoh Y., Fukazawa Y., Sugiyama H., Inokuchi K. Novel members of the Vesl/Homer family of PDZ proteins that bind metabotropic glutamate receptors. J. Biol. Chem. 1998, 273:23969-23975.
29. Kharatishvili I., Pitkanen A. Association of the severity of cortical damage with the occurrence of spontaneous seizures and hyperexcitability in an animal model of posttraumatic epilepsy. Epilepsy Res. 2010, 90:47-59.
30. Kirschstein T., Bauer M., Muller L., Ruschenschmidt C., Reitze M., Becker A.J., Schoch S., Beck H. Loss of metabotropic glutamate receptor-dependent long-term depression via downregulation of mGluR5 after status epilepticus. J. Neurosci. 2007, 27:7696-7704.
31. Lee T.S., Mane S., Eid T., Zhao H., Lin A., Guan Z., Kim J.H., Schweitzer J., King-Stevens D., Weber P., Spencer S.S., Spencer D.D., de Lanerolle N.C. Gene expression in temporal lobe epilepsy is consistent with increased release of glutamate by astrocytes. Mol. Med. 2007, 13:1-13.
32. Lemos T., Cavalheiro E.A. Suppression of pilocarpine-induced status epilepticus and the late development of epilepsy in rats. Exp. Brain Res. 1995, 102:423-428.
33. Linden D.J. Input-specific induction of cerebellar long-term depression does not require presynaptic alteration. Learn Mem. 1994, 1:121-128.
34. Loscher W. Current status and future directions in the pharmacotherapy of epilepsy. Trends Pharmacol. Sci. 2002, 23:113-118.
35. Lukasiuk K., Kontula L., Pitkanen A. cDNA profiling of epileptogenesis in the rat brain. Eur. J. Neurol. 2003, 17:271-279.
36. Majores M., Schoch S., Lie A., Becker A.J. Molecular neuropathology of temporal lobe epilepsy: complementary approaches in animal models and human disease tissue. Epilepsia 2007, 48(Suppl 2):4-12.
37. Mello L.E., Cavalheiro E.A., Tan A.M., Kupfer W.R., Pretorius J.K., Babb T.L., Finch D.M. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia 1993, 34:985-995.
38. Morioka R., Kato A., Fueta Y., Sugiyama H. Expression of vesl-1S/homer-1a, a gene associated with long-term potentiation, in the brain of the epileptic EI mouse. Neurosci. Lett. 2001, 313:99-101.
39. Mu Y., Otsuka T., Horton A.C., Scott D.B., Ehlers M.D. Activity-dependent mRNA splicing controls ER export and synaptic delivery of NMDA receptors. Neuron 2003, 40:581-594.
40. Naisbitt S., Kim E., Tu J.C., Xiao B., Sala C., Valtschanoff J., Weinberg R.J., Worley P.F., Sheng M. Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin. Neuron 1999, 23:569-582.
41. Paxinos G., Watson C. The Rat Brain in Sterotaxic Coordinates 1986, A. Press, San Diego, CA.
42. Perez-Otano I., Ehlers M.D. Homeostatic plasticity and NMDA receptor trafficking. Trends Neurosci. 2005, 28:229-238.
43. Potschka H., Krupp E., Ebert U., Gumbel C., Leichtlein C., Lorch B., Pickert A., Kramps S., Young K., Grune U., Keller A., Welschof M., Vogt G., Xiao B., Worley P.F., Loscher W., Hiemisch H. Kindling-induced overexpression of Homer 1A and its functional implications for epileptogenesis. Eur. J. Neurosci. 2002, 16:2157-2165.
44. Sakagami Y., Yamamoto K., Sugiura S., Inokuchi K., Hayashi T., Kato N. Essential roles of Homer-1a in homeostatic regulation of pyramidal cell excitability: a possible link to clinical benefits of electroconvulsive shock. Eur. J. Neurol. 2005, 21:3229-3239.
45. Sala C., Piech V., Wilson N.R., Passafaro M., Liu G., Sheng M. Regulation of dendritic spine morphology and synaptic function by Shank and Homer. Neuron 2001, 31:115-130.
46. 2+ homeostasis at dendritic spines in hippocampal neurons. J. Neurosci. 2005, 25:4587-4592.
47. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 2008, 3:1101-1108.
48. Silva I.R., Nehlig A., Rosim F.E., Vignoli T., Persike D.S., Ferrandon A., Sinigaglia-Coimbra R., Fernandes M.J. The A1 receptor agonist R-Pia reduces the imbalance between cerebral glucose metabolism and blood flow during status epilepticus: could this mechanism be involved with neuroprotection?. Neurobiol. Dis. 2011, 41:169-176.
49. Temkin N.R., Jarell A.D., Anderson G.D. Antiepileptogenic agents: how close are we?. Drugs 2001, 61:1045-1055.
50. Tu J.C., Xiao B., Yuan J.P., Lanahan A.A., Leoffert K., Li M., Linden D.J., Worley P.F. Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors. Neuron 1998, 21:717-726.
51. Tu J.C., Xiao B., Naisbitt S., Yuan J.P., Petralia R.S., Brakeman P., Doan A., Aakalu V.K., Lanahan A.A., Sheng M., Worley P.F. Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron 1999, 23:583-592.
52. Turski L., Ikonomidou C., Turski W.A., Bortolotto Z.A., Cavalheiro E.A. Review: cholinergic mechanisms and epileptogenesis. The seizures induced by pilocarpine: a novel experimental model of intractable epilepsy. Synapse 1989, 3:154-171.
53. Turski W.A., Cavalheiro E.A., Schwarz M., Czuczwar S.J., Kleinrok Z., Turski L. Limbic seizures produced by pilocarpine in rats: behavioural, electroencephalographic and neuropathological study. Behav. Brain Res. 1983, 9:315-335.
54. Turski W.A., Cavalheiro E.A., Bortolotto Z.A., Mello L.M., Schwarz M., Turski L. Seizures produced by pilocarpine in mice: a behavioral, electroencephalographic and morphological analysis. Brain Res. 1984, 321:237-253.
55. Velisek L., Veliskova J. New avenue of research: antiepileptic drug and estradiol neuroprotection in epilepsy. Recent Pat. CNS Drug Discov. 2008, 3:128-137.
56. Wang N.C., Good L.B., Marsh S.T., Treiman D.M. EEG stages predict treatment response in experimental status epilepticus. Epilepsia 2009, 50:949-952.
57. Weiss S.R., Eidsath A., Li X.L., Heynen T., Post R.M. Quenching revisited: low level direct current inhibits amygdala-kindled seizures. Exp Neurol. 1998, 154:185-192.
58. Xiao B., Tu J.C., Petralia R.S., Yuan J.P., Doan A., Breder C.D., Ruggiero A., Lanahan A.A., Wenthold R.J., Worley P.F. Homer regulates the association of group 1 metabotropic glutamate receptors with multivalent complexes of homer-related, synaptic proteins. Neuron 1998, 21:707-716.
59. Xiao B., Tu J.C., Worley P.F. Homer: a link between neural activity and glutamate receptor function. Curr. Opin. Neurobiol. 2000, 10:370-374.
60. Yuan J.P., Kiselyov K., Shin D.M., Chen J., Shcheynikov N., Kang S.H., Dehoff M.H., Schwarz M.K., Seeburg P.H., Muallem S., Worley P.F. Homer binds TRPC family channels and is required for gating of TRPC1 by IP3 receptors. Cell 2003, 114:777-789.