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Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
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Altered PLCβ-1 expression in the gerbil hippocampal complex following spontaneous seizure

  • Lee, Saet-Byeol (Department of Anatomy, College of Medicine, Soonchunhyang University) ;
  • Oh, Yun-Jung (Department of Anatomy, College of Medicine, Soonchunhyang University) ;
  • Chung, Jae-Kwang (Department of Anatomy, College of Medicine, Soonchunhyang University) ;
  • Jeong, Ji-Heon (Department of Anatomy, College of Medicine, Soonchunhyang University) ;
  • Lee, Sang-Duk (Department of Physical Education, Hallym University) ;
  • Park, Dae-Kyoon (Department of Anatomy, College of Medicine, Soonchunhyang University) ;
  • Park, Kyung-Ho (Department of Anatomy, College of Medicine, Soonchunhyang University) ;
  • Ko, Jeong-Sik (Department of Anatomy, College of Medicine, Soonchunhyang University) ;
  • Kim, Duk-Soo (Department of Anatomy, College of Medicine, Soonchunhyang University)
  • Received : 2011.03.28
  • Accepted : 2011.06.27
  • Published : 2011.09.30
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Abstract

Although the phospholipase C (PLC)${\beta}$-1 isoform is associated with spontaneous seizure and distinctively expressed in the telencephalon, the distribution of PLC${\beta}$-1 expression in the epileptic gerbil hippocampus remains controversial. Therefore, we determined whether PLC${\beta}$-1 is associated with spontaneous seizure in an animal model of genetic epilepsy. In the present study, PLC${\beta}$-1 immunoreactivity was down-regulated in seizure-sensitive (SS) gerbils more than in seizure-resistant (SR) gerbils. The expression of PLC${\beta}$-1 within calretinin (CR)-positive neurons was rarely detected within the dentate hilar region of SS gerbils. PLC${\beta}$-1 immunoreactivity in the hippocampus was significantly elevated as compared to that in pre-seizure SS gerbil 3 h post-ictal. These findings suggest that alterations in PLC${\beta}$-1 immunoreactivity in the SS gerbil hippocampus may be closely related to the epileptic state of the gerbil brain and transiently elevated PLC${\beta}$-1 protein levels following seizure episodes. Such alterations may be compensatory responses in the SS gerbil hippocampus.

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References

  1. Fukaya, M., Uchigashima, M., Nomura, S., Hasegawa, Y., Kikuchi, H. and Watanabe, M. (2008) Predominant expression of phospholipase C beta1 in telencephalic principal neurons and cerebellar interneurons, and its close association with related signaling molecules in somatodendritic neuronal elements. Eur. J. Neurosci. 28, 1744-1759. https://doi.org/10.1111/j.1460-9568.2008.06495.x
  2. Nishizuka, Y. (1988) The molecular heterogeneity of protein kinase C and its implication for cellular regulation. Nature 334, 661-665. https://doi.org/10.1038/334661a0
  3. Berridge, M. J. (1993) Inositol trisphosphate and calcium signaling. Nature 36, 315-325.
  4. Berridge, M. J. (1993) Inositol trisphosphate and calcium signaling. Nature 36, 315-325.
  5. Ross, C. A., MacCumber, M. W., Glatt, C. E. and Snyder, S. H. (1989) Brain phospholipase C isozymes: differential mRNA localizations by in situ hybridization. Proc. Natl. Acad. Sci. 86, 2923-2927. https://doi.org/10.1073/pnas.86.8.2923
  6. Watanabe, M., Nakamura, M., Sato, K., Kano, M., Simon, M. I. and Inoue, Y. (1998) Patterns of expression for the mRNA corresponding to the four isoforms of phospholipase Cbeta in mouse brain. Eur. J. Neurosci. 10, 2016-2025. https://doi.org/10.1046/j.1460-9568.1998.00213.x
  7. Kim, D., Jun, K. S., Lee, S. B., Kang, N. G., Min, D. S., Kim, Y. H., Ryu, S. H., Suh, P. G. and Shin, H. S. (1997) Phospholipase C isozymes selectively couple to specific neurotransmitter receptors. Nature 389, 290-293. https://doi.org/10.1038/38508
  8. Chuang, S. C., Bianchi, R., Kim, D. S., Shin, H. S. and Wong, R. K. S. (2001) Group I metabotropic glutamate receptor elicit epileptiform discharges in the hippocampus through PCLbeta1 signaling. J. Neurosci. 21, 6387-6394.
  9. Shin, J., Kim, D., Bianchi, R., Wong, R. K. and Shin, H. S. (2005) Genetic dissection of theta rhythm heterogeneity in mice. Proc. Natl. Acad. Sci. 102, 18165-18170. https://doi.org/10.1073/pnas.0505498102
  10. de Lanerolle, N. C., Kim, J. H., Robbins, R. J. and Spencer, D. D. (1989) Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain. Res. 495, 387-395. https://doi.org/10.1016/0006-8993(89)90234-5
  11. Mello, L. E., Cavalheiro, E. A., Tan, A. M., Kupfer, W. R., Pretorius, J. K., Babb, T. L. and Finch, D. M. (1993) Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia 34, 985-995. https://doi.org/10.1111/j.1528-1157.1993.tb02123.x
  12. Buckmaster, P. and Dudek, F. E. (1997) Neuron loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kainate-treated rats. J. Comp. Neurol. 385, 385-404. https://doi.org/10.1002/(SICI)1096-9861(19970901)385:3<385::AID-CNE4>3.0.CO;2-#
  13. El Bahh, B., Lespinet, V., Lurton, D., Coussemacq, M. and Le Gal La Salle, G. (1999) Rougier, Correlations between granule cell dispersion, mossy fiber sprouting, and hippocampal cell loss in temporal lobe epilepsy. Epilepsia 40, 1393-1401. https://doi.org/10.1111/j.1528-1157.1999.tb02011.x
  14. Matyas, F., Freund, T. F. and Gulyas, A. I. (2004) Immunocytochemically defined interneuron populations in the hippocampus of mouse strains used in transgenic technology. Hippocampus. 14, 460-481. https://doi.org/10.1002/hipo.10191
  15. Tanaka, O. and Kondo, H. (1994) Localization of mRNAs for three novel members (b3, b4 and c2) of phospholipase C family in mature rat brain. Neurosci. Lett. 182, 17-20. https://doi.org/10.1016/0304-3940(94)90194-5
  16. Roustan, P., Abitbol, M., Ménini, C., Ribeaudeau, F., Gérard, M., Vekemans, M., Mallet, J. and Dufier, J. L. (1995) The rat phospholipase Cβ4 gene is expressed at high abundance in cerebellar Purkinje cells. Neuroreport 6, 1837-1841. https://doi.org/10.1097/00001756-199510020-00004
  17. Johnston, D. and Amaral, D. G. (2004) Hippocampus; in Shepherd, G. M., ed, The synaptic organization of the brain. pp. 455-498, Oxford University Press, Oxford, UK.
  18. Bohm, D., Schwegler, H., Kotthaus, L., Nayernia, K., Rickmann, M., Kohler, M., Rosenbusch, J., Engel, W., Flugge, G. and Burfeind, P. (2002) Disruption of PLCβ-1-mediated signal transduction in mutant mice causes age-dependent hippocampal mossy fiber sprouting and neurodegeneration. Mol. Cell. Neurosci. 21, 584-601. https://doi.org/10.1006/mcne.2002.1199
  19. Fisher, R. S. (1989) Animal models of the epilepsies. Brain Res. Brain. Res. Rev. 14, 245-278. https://doi.org/10.1016/0165-0173(89)90003-9
  20. Noebels, J. L. (1999) Single-gene models of epilepsy. Adv. Neurol. 79, 227-238.
  21. Puranam, R. S. and McNamara, J. O. (1999) Seizure disorders in mutant mice: relevance to human epilepsies. Curr. Opin. Neurobiol. 9, 281-287. https://doi.org/10.1016/S0959-4388(99)80041-5
  22. Lu, W. Y., Jackson, M. F., Bai, D., Orser, B. A. and Mac- Donald, J. F. (2000) In CA1 pyramidal neurons of the hippocampus protein kinase C regulates calcium-dependent inactivation of NMDA receptors. J. Neurosci. 20, 4452-4461.
  23. Buzsaki, G., Ponomareff, G. L., Bayardo, F., Ruiz, R. and Gage, F. H. (1989) Neuronal activity in the subcortically denervated hippocampus: a chronic model for epilepsy. Neuroscience 28, 527-538. https://doi.org/10.1016/0306-4522(89)90002-X
  24. Pitler, T. A. and Alger, B. E. (1992) Cholinergic excitation of GABAergic interneurons in the rat hippocampal slice. J. Physiol. 450, 127-142. https://doi.org/10.1113/jphysiol.1992.sp019119
  25. Klausberger, T., Magill, P. J., Márton, L. F., Roberts, J. D., Cobden, P. M., Buzsáki, G. and Somogyi, P. (2003) Brainstate- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421, 844-848. https://doi.org/10.1038/nature01374
  26. Klausberger, T., Marton, L. F., Baude, A., Roberts, J. D., Magill, P. J. and Somogyi, P. (2004) Spike timing of dendrite- targeting bistratified cells during hippocampal network oscillations in vivo. Nat. Neurosci. 7, 41-47. https://doi.org/10.1038/nn1159
  27. Kwak, S. E., Kim, J. E., Kim, D. S., Jung, J. Y., Won, M. H., Kwon, O. S., Choi, S. Y., Kang, T. C. (2005) Effects of GABAergic transmissions on the immunoreactivities of calcium binding proteins in the gerbil hippocampus. J. Comp. Neurol. 485, 153-164 https://doi.org/10.1002/cne.20482
  28. Buckmaster, P. A. (2005) Inherited epilepsy in Mongolian gerbils: models of seizures and epilepsy; in Schwartzkroin P. A., ed. pp. 273-294, Academic press, Elsevier, USA.
  29. Baskys, A., Bayazitov, I., Fang, L., Blaabjerg, M., Poulsen, R. R. and Zimmer, J. (2005) Group I metabotropic glutamate receptors reduce excitotoxic injury and may facilitate neurogenesis. Neuropharmacology 49, 146-156. https://doi.org/10.1016/j.neuropharm.2005.04.029
  30. Kang, T. C., Kim, D. S., Kwak, S. E., Kim, J. E., Kim, D. W., Kang, J. H., Won, M. H., Kwon, O. S. and Choi, S. Y. (2005) Valproic acid reduces enhanced vesicular glutamate transporter immunoreactivities in the dentate gyrus of the seizure prone gerbil. Neuropharmacology 49, 912-921. https://doi.org/10.1016/j.neuropharm.2005.08.007
  31. Kim, D. S., Kim, J. E., Kwak, S. E., Won, M. H. and Kang, T. C. (2007a) Seizure activity affects neuroglial Kv1 channel immunoreactivities in the gerbil hippocampus. Brain. Res. 1151, 172-187. https://doi.org/10.1016/j.brainres.2007.03.017
  32. Kim, D. S., Kim, J. E., Kwak, S. E., Choi, H. C., Song, H. K., Kim, Y. I., Choi, S. Y. and Kang, T. C. (2007b) Upregulated astroglial TWIK-related acid-sensitive $K^+$ channel-1 (TASK-1) in the hippocampus of seizure-sensitive gerbils : a target of anti-epileptic drugs. Brain. Res. 1185, 346-358. https://doi.org/10.1016/j.brainres.2007.09.043
  33. Paul, L. A., Fried, I., Watanabe, K., Forsythe, A. B. and Schibel, A. B. (1981) Structural correlates of seizure behavior in the Mongolian gerbil. Science 213, 924-926. https://doi.org/10.1126/science.7256289
  34. Kim, J. E., Kwak, S. E. and Kang, T. C. (2009) Upregulated TWIK-related acid-sensitive $K^+$ channel-2 in neurons and perivascular astrocytes in the hippocampus of experimental temporal lobe epilepsy. Epilepsia 50, 654-663. https://doi.org/10.1111/j.1528-1167.2008.01957.x
  35. Lee, S. M., Kim, J. E., Sohn, J. H., Choi, H. C., Lee, J. S., Kim, S. H., Kim, M. J., Choi, I. G. and Kang, T. C. (2009) Down-regulation of delayed rectifier $K^+$ channels in the hippocampus of seizure sensitive gerbils. Brain. Res. Bull. 80, 433-442. https://doi.org/10.1016/j.brainresbull.2009.07.016
  36. Kim, D. S., Kim, J. E., Kwak, S. E., Choi, K. C., Kim, D. W., Kwon, O. S., Choi, S. Y. and Kang, T. C. (2008) Spatiotemoral characteristics of astroglial death in the rat hippocampo-entorhinal complex following pilocarpine-induced status epilepticus. J. Comp. Neurol. 511, 581-598. https://doi.org/10.1002/cne.21851

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