Open Access Open Access  Restricted Access Subscription or Fee Access

Administration of copper reduced the hyper-excitability of neurons in CA1 hippocampal slices from epileptic rats.

Juan Leiva, Claudio Infante

Abstract


Copper as a trace metal is involved in several neurodegenerative illnesses, such as Menkes, Wilson’s, Alzheimer’s, amyotrophic lateral sclerosis (ALS), and Creutzfeldt-Jakob. Electrophysiological evidence indicates that acute perfusion of copper can inhibit long-term synaptic potentiation in hippocampal slices. The objective of this work is to determine whether Cu perfusion can perturb synaptic transmission in hippocampal slices derived from pilocarpinetreated epileptic rats. Field potential (FP) recordings of the CA1 neurons of rats with chronic epilepsy showed voltage and response duration decrease following copper sulfate perfusion. However, voltage and response duration were higher after removing copper by washing. The discharge frequency of the CA1 neurons of hippocampal slices from nonepileptic control rats was increased after acute perfusion of 10 μM of pilocarpine. This increase was blocked by administering copper sulphate 10 μM. Krebs-Ringer solution washing re-established the discharges, with a higher frequency than that provoked by pilocarpine perfusion. We discuss the blocking effect of copper and the synaptic hyper-excitability generated by its removal.

Keywords


Key words: Copper; field potential (FP); hippocampus slices; pilocarpine-induced chronic epilepsy; rats.

Full Text:

PDF

References


References.

(1) Azimi, S. and Rauk, Arvi. On the involvement of copper binding to the N-terminus of the amyloid beta peptide of Alzheimer´s disease: A computational study on model systems. Int. J. Alzheimer´s dis. Vol 2011: Article. ID. 539762, 15 pages. Doi:10.4061/2011/539762.

(2) Bush, A.I. The metallobiology of Alzheimer´s disease. Trends. Neurosci. 26: 207-214, 2003.

(3) Cavalheiro, E.A., Leite, J.P., Bortolott, 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. 32: 778-782, 1991.

(4) Cavazos, J.E., Jones, S.M., and Cross, D.J. Sprouting and synaptic reorganization in the subiculum and CA1 region of the hippocampus in acute and chronic models of partial–onset epilepsy. Neuroscience. 126: 677-688, 2004.

(5) Christodoulou, J., Danks, D.M., Sarkar, B., Baerlocher, K.E., Casey. R., Horn, N., Tumer, Z, Clarke, J.T. Early treatment of Menkes disease with parenteral copper-histidine: long term follow up of four treated patients. Am J. Med. Genet. 76: 154-164, 1998.

(6) Collindridge, G.L., Kehl, S.J., Mcllennan, H. Excitatory amino acids in synaptic transmission in the Schaffer collateral-commisural pathway of the rat hippocampus. J. Physiol.(London). 3345: 33-46, 1983.

(7) Collingridge, G.L. The induction of N-methyl-D-aspartate receptor-dependent long-term potentiation. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 358: 635-641, 2003.

(8) Cousins, R.J. Metal elements and gene expression. Ann. Rev. Nutr. 14: 449-469, 1994.

(9) Danks, D.M. Disorders of copper transport. pp. 2211-2235. in: Scriver CR, Beaudet AL, Sly WM, Valle D. (Eds). The metabolic and molecular basis of inherited disease. 7th ed,. Mc. Graw-Hill, New York. 1995.

(10) Doroulee, Y., Yanovky, H., Haas, H. Suppression of long-term potentiation in hippocampal slices by copper. Hippocampus. 7: 666-669, 1997.

(11) Erreger, K., Dravid, Sh. M., Banke, T.G., Wyllie, D.J.A., Traynelis, S.F. Subunit-specific gating control rat NR1/NR2A and NR1/NR2B NMDA channel kinetics and synaptic signaling profiles. J. Physiol. 563: 345-358, 2005.

(12) Fujikawa, D.G. The temporal evolution of neuronal damage from pilocarpine-induced status epilepticus. Brain Res. 725: 11-22, 1996.

(13) Gaier, E.D., Eipper, B.A., and Mains, R.E. Copper signaling in the mammalian nervous system: synaptic effects. J. of Neurosci. Res. 91: 2-19, 2013

(14) Goldschmith, A., Infante, C., Leiva, J., Motles, E., Palestini M. Interference of chronically ingested copper in long-term potentiation(LTP) of rat hippocampus. Brain Res. 1056: 176-182, 2005.

(15) Isokawa, M., Levesque, M.F., Babb, T.L., Engel, J. Jr. Single mossy fiber axonal systems of human dentate granule cell studies in hippocampal slices from patients with temporal lobe epilepsy. J. Neurosci. 13: 1511-1522, 1990.

(16) Kandel, E.R., Schwartz, J.H., Jessel, T.M. pp. 730-738. Neurociencia y conducta, in Cap. 36, Prentice Hall, Madrid, pp. 730-738, 1997.

(17) Kardos, J., Kovacs, I., Hajos, F., Kalman, M., Somoyi, M. Nerve ending from rat brain tissue release copper upon depolarization. A possible role in regulating neural excitability. Neurosci Lett. 103: 139-144. 1989.

(18) Károly, N., Milhály, A., Dobó, E. Comparative inmunohistochemistry of

synaptic markers in the rodent hippocampus in pilocarpine epilepsy. Acta.

Histochemica. 113: 656-662, 2011.

(19) Kirkwood, A. and Bear, M.F. Hebbian synapses in visual cortex. J. of

Neuroscience. 14(3): 1634-1645, 1994.

(20) Kreuder, J., Otten, A., Fuder, H., Tuner, Z., Tonnesen, T., Horn, N.,

Dralle, D. Clinical and biochemical consequences of copper-histidine

theraphy in Menkes disease. Eur J. Pediatr. 152: 828-832, 1993.

(21) Leite, J.P., Bortolotto, Z.A., and Cavalheiro, E.A. Spontaneous recurrent seizures in rats: An experimental model of partial epilepsy. Neuroscience & Biobeh Rev. 14: 511-517, 1990.

(22) Leiva, J., Palestini, M., Tetas, M., López, J. Copper sensitivity in dorsal hippocampus slices. Arch. ital. biol. 138: 175-184, 2000.

(23) Leiva, J., Gaete, P., Palestini, M. Copper interaction on the long-term potentiation. Arch. Ital. Biol. 141: 149-155, 2003.

(24) Leiva, J., Palestini, M,. Infante, C., Goldschmidt, A., Motles, E. Copper suppresses hippocampus LTP in the rat, but does not alter learning or memory in the Morris water maze. Brain Res. 1256: 69-75, 2009.

(25) Leiva, J., Palestini, M., Infante, C. Administration copper blocks CA1 neuron hyper-excitability in rat hippocampal slices. JBBS. 3: 403-408, 2013. http://dx.doi.org/10.4236/jbbs.2013.35041

(26) Linder, MC., Hazegh-Azam. Copper biochemistry and molecular biology. Am. J. Clin. Nutr. 63: 797S- 811S, 1996.

(27) Madsen, E., and Gitlin, J.D. Copper and iron disorders of the brain. Annu. Rev. Neurosci. 30: 317-337, 2007.

(28) Marchetti, C. Baronowska-Bosiacka, I. Gavazzo, P. Multiple effects of copper on NMDA receptor currents. Brain Res. 1542: 20-31, 2014.

(29) Martin, S.J., Grimwood, P.D., Morris, R.G.M. Synaptic plasticity and memory. Ann. Rev. Neurosci. 23: 649 -777, 2000.

(30) Mello, L.E., Cavalheiro, E.A., Tan, A.M., Kupfer, W.R., Pretorius, J.K., Babb, T.L., Finch, D.M. Circuit mechanism of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia. 34: 985-995, 1993.

(31) Müller-Dahlhaus, F., Ziemann, U., and Classen, J., 2010. Platicity resembling spike-timing dependent synaptic plasticity: the evidence in human cortex. Front. Synaptic. Neurosci. 2:34. 1-10. 2010. doi: 10.3389/fnsyn.2010.00034.

(32) Opaso, C.M., Greennough, M.A., Bush, A.I. Copper from neurotransmission to neuroproteostasis. Front. Aging Neurosci. 6:143. 1-7, 2014.

(33) Park, J.H., Cho, H., Kim, H., and Kim, K. Repeated brief epileptic seizures by pentylenetetrazole cause neurodegeneration and promote neurogenesis in discrete brain regions of freely moving adult rats. Neuroscience. 140: 673-684. 2006.

(34) Peters, Ch., Muñoz, B., Sepúlveda, F.J., Urrutia, J., Quiroz, M., Luza,

S., De Ferrari, G.V., Aguayo, L.G., and Opazo, C. Biphasic effects of copper on

neurotransmission in rat hippocampal neurons. J. of Neurochem. 119: 78-88,

(35) Prasad, A.N., Levin, S., Rupar, C.A., Prasad, Ch. Menkes disease and infantile epilepsy. Brain & Development. 33: 866-876, 2011.

(36) Priel, M.R., Ferreira dos Santos, N., Cavalheiro, E.A. Developmental aspects of the pilocarpine model of epilepsy. Epilepsy Res. 26: 115-121, 1996.

(37) Radley, J.J., and Jacobs, B.L. Pilocarpine-induced status epilepticus

increases cell proliferation in the dentatus gyrus of adult rats via a 5-HT¹A

receptor-dependent. Brain Res. 966: 1-12, 2003.

(38) Revest, P., Longstaff, A. Molecular Neuroscience. pp. 151-190. Spring-Verlag, Inc., New York, 1998.

(39) Rutecki, P.A., and Yang, Y. Ictal epileptiform activity in the CA3 region of

hippocampal slices produced by pilocarpine. J. of Neurophysiol. 79: 3019-

, 1998.

(40) Sahin, D., Ilbay, G., Ates, N. Changes in the blood brain Barrier

permeability and in the brain tissue trace element concentrations after Single

and repeated pentylenetetrazole-induce seizures in rats. Pharmacological. Res.

: 69-73, 2003.

(41) Sparks, L.D., and Schreurs, B.G. Trace amounts of copper in water induce β-amyloid plaques and learning deficits in a rabbit model of Alzheimer´s disease. Proc. Nat. Acad. Sci. USA. 100: 11065-9, 2003.

(42) Stys, P.K., You, H., and Zamponi, G.W. Copper-dependent regulation of NMDA receptors by cellular prion protein: implications for neurodegenerative disorders. J. Physiol. 590: 1357-1368, 2012.

(43) Tauck, D.L., Nadler, J.V. Evidence of mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J. Neurosci. 5: 1016-1022. 1985.

(44) Tumer, Z., Moller, L.B. Menkes disease. Eur J. Hum. Genet. 18: 511-518. 2010.

(45) Turski, W.A., Cavalheiro, E.A., Bortolotto, Z.A., Mello, L.M., Shwarz, M., and Turski, L. Seizures produced by pilocarpine in mice: A behavioral, electroencephalographic and morphological analysis. Brain Res. 321: 237- 253, 1984.

(46) Wuarin, J.P., Dudek, F.E. Electrographic seizures in new recurrent

excitatory circuits in the dentate gyrus of hippocampal slices from kainate-

treated rats. J. Neurosci. 16: 4438 – 4448. 1996.




DOI: https://doi.org/10.4449/aib.v154i1.4316

Refbacks

  • There are currently no refbacks.