Copper-uptake is critical for the down regulation of synapsin and dynamin induced by neocuproine: Modulation of synaptic activity in hippocampal neurons

Frontiers in Aging Neuroscience

Volumn 6, Issue OCT, 2014, Pages

  Castro, Patricio A ^a   Ramirez, Alejandra ^b,c   Sepúlveda, Fernando J ^b   Peters, Christian ^b   Fierro, Humberto ^b   Waldron, Javier ^b   Luza, Sandra ^c   Fuentealba, Jorge ^b   Muñoz, Francisco J ^d   De Ferrari, Giancarlo V ^e   Bush, Ashley I ^c   Aguayo, Luis G ^b   Opazo, Carlos ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CONCEPCIÓN   (Chile)

^c FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^d UNIVERSITAT POMPEU FABRA   (Spain)

^e UNIVERSIDAD ANDRÉS BELLO   (Chile)

Author keywords

Copper; Dynamin; Epileptiform like activity; Hyperexcitability; Neocuproine; Synapsin; Synaptic activity; Zinc

Indexed keywords

2,9 DIMETHYL 1,10 PHENANTHROLINE; COPPER; DYNAMIN; SYNAPSIN; ZINC;

ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; DOWN REGULATION; EPILEPTIC FOCUS; FEMALE; HIPPOCAMPUS; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; RAT; SYNAPSE; WESTERN BLOTTING;

EID: 84909595659     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2014.00319     Document Type: Article

References (41)

1. Amatniek, J.C., Hauser, W.A., Delcastillo-Castaneda, C., Jacobs, D.M., Marder, K., Bell, K., Albert, M., Brandt, J., and Stern, Y. (2006). Incidence and predictors of seizures in patients with Alzheimer's disease. Epilepsia 47, 867-872.
2. Bush, A.I. (2003). The metallobiology of Alzheimer's disease. Trends Neurosci 26, 207-214.
3. Calderaro, M., Martins, E.A., and Meneghini, R. (1993). Oxidative stress by menadione affects cellular copper and iron homeostasis. Mol Cell Biochem 126, 17-23.
4. Carrasco, M.A., Castro, P.A., Sepulveda, F.J., Cuevas, M., Tapia, J.C., Izaurieta, P., Van Zundert, B., and Aguayo, L.G. (2007). Anti-homeostatic synaptic plasticity of glycine receptor function after chronic strychnine in developing cultured mouse spinal neurons. J Neurochem 100, 1143-1154.
5. Chavez-Crooker, P., Garrido, N., Pozo, P., and Ahearn, G.A. (2003). Copper transport by lobster (Homarus americanus) hepatopancreatic lysosomes. Comp Biochem Physiol C Toxicol Pharmacol 135, 107-118.
6. Chen, S.H., Lin, J.K., Liu, S.H., Liang, Y.C., and Lin-Shiau, S.Y. (2008). Apoptosis of cultured astrocytes induced by the copper and neocuproine complex through oxidative stress and JNK activation. Toxicol Sci 102, 138-149.
7. Colledge, M., Snyder, E.M., Crozier, R.A., Soderling, J.A., Jin, Y., Langeberg, L.K., Lu, H., Bear, M.F., and Scott, J.D. (2003). Ubiquitination regulates PSD-95 degradation and AMPA receptor surface expression. Neuron 40, 595-607.
8. Cully, M. (2014). Drug development: Illuminated targets. Nature 511, S12-13.
9. Fukahori, M., and Itoh, M. (1990). Effects of dietary zinc status on seizure susceptibility and hippocampal zinc content in the El (epilepsy) mouse. Brain Res 529, 16-22.
10. Gaier, E.D., Eipper, B.A., and Mains, R.E. (2013). Copper signaling in the mammalian nervous system: synaptic effects. J Neurosci Res 91, 2-19.
11. Gaier, E.D., Eipper, B.A., and Mains, R.E. (2014a). Pam heterozygous mice reveal essential role for Cu in amygdalar behavioral and synaptic function. Ann N Y Acad Sci 1314, 15-23.
12. Gaier, E.D., Rodriguiz, R.M., Zhou, J., Ralle, M., Wetsel, W.C., Eipper, B.A., and Mains, R.E. (2014b). In vivo and in vitro analyses of amygdalar function reveal a role for copper. J Neurophysiol 111, 1927-1939.
13. Gillard, M., Fuks, B., Leclercq, K., and Matagne, A. (2011). Binding characteristics of brivaracetam, a selective, high affinity SV2A ligand in rat, mouse and human brain: relationship to anti-convulsant properties. Eur J Pharmacol 664, 36-44.
14. Gocmen, C., Giesselman, B., and De Groat, W.C. (2005). Effect of neocuproine, a copper(I) chelator, on rat bladder function. J Pharmacol Exp Ther 312, 1138-1143.
15. Gocmen, C., Gokturk, H.S., Ertug, P.U., Onder, S., Dikmen, A., and Baysal, F. (2000). Effect of neocuproine, a selective Cu(I) chelator, on nitrergic relaxations in the mouse corpus cavernosum. Eur J Pharmacol 406, 293-300.
16. Goldschmith, A., Infante, C., Leiva, J., Motles, E., and Palestini, M. (2005).
17. Grabrucker, S., Jannetti, L., Eckert, M., Gaub, S., Chhabra, R., Pfaender, S., Mangus, K., Reddy, P.P., Rankovic, V., Schmeisser, M.J., Kreutz, M.R., Ehret, G., Boeckers, T.M., and Grabrucker, A.M. (2014). Zinc deficiency dysregulates the synaptic ProSAP/Shank scaffold and might contribute to autism spectrum disorders. Brain 137, 137-152.
18. Hartter, D.E., and Barnea, A. (1988). Evidence for release of copper in the brain: depolarization-induced release of newly taken-up 67copper. Synapse 2, 412-415.
19. Hopt, A., Korte, S., Fink, H., Panne, U., Niessner, R., Jahn, R., Kretzschmar, H., and Herms, J. (2003). Methods for studying synaptosomal copper release. J Neurosci Methods 128, 159-172.
20. James, S.A., Volitakis, I., Adlard, P.A., Duce, J.A., Masters, C.L., Cherny, R.A., and Bush, A.I. (2012). Elevated labile Cu is associated with oxidative pathology in Alzheimer disease. Free Radic Biol Med 52, 298-302.
21. Kardos, J., Kovacs, I., Hajos, F., Kalman, M., and Simonyi, M. (1989). Nerve endings from rat brain tissue release copper upon depolarization. A possible role in regulating neuronal excitability. Neurosci Lett 103, 139-144.
22. Leiva, J., Palestini, M., Infante, C., Goldschmidt, A., and Motles, E. (2009). Copper suppresses hippocampus LTP in the rat, but does not alter learning or memory in the morris water maze. Brain Res 1256, 69-75.
23. Mackenzie, G.G., Salvador, G.A., Romero, C., Keen, C.L., and Oteiza, P.I. (2011). A deficit in zinc availability can cause alterations in tubulin thiol redox status in cultured neurons and in the developing fetal rat brain. Free Radic Biol Med 51, 480-489.
24. Marchetti, C., Baranowska-Bosiacka, I., and Gavazzo, P. (2014). Multiple effects of copper on NMDA receptor currents. Brain Res 1542, 20-31.
25. Mathie, A., Sutton, G.L., Clarke, C.E., and Veale, E.L. (2006). Zinc and copper: pharmacological probes and endogenous modulators of neuronal excitability. Pharmacol Ther 111, 567-583.
26. Maynard, C.J., Cappai, R., Volitakis, I., Cherny, R.A., White, A.R., Beyreuther, K., Masters, C.L., Bush, A.I., and Li, Q.X. (2002). Overexpression of Alzheimer's disease amyloid-beta opposes the age-dependent elevations of brain copper and iron. J Biol Chem 277, 44670-44676.
27. Mohindru, A., Fisher, J.M., and Rabinovitz, M. (1983). Bathocuproine sulphonate: a tissue culture-compatible indicator of copper-mediated toxicity. Nature 303, 64-65.
28. Nuttall, J.R., and Oteiza, P.I. (2012). Zinc and the ERK kinases in the developing brain. Neurotox Res 21, 128-141.
29. Opazo, C.M., Greenough, M.A., and Bush, A.I. (2014). Copper: From neurotransmission to neuroproteostasis. Frontiers in Aging Neuroscience 6, 143.
30. Palop, J.J., Jones, B., Kekonius, L., Chin, J., Yu, G.Q., Raber, J., Masliah, E., and Mucke, L. (2003). Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer's disease-related cognitive deficits. Proc Natl Acad Sci U S A 100, 9572-9577.
31. Peters, C., Munoz, B., Sepulveda, F.J., Urrutia, J., Quiroz, M., Luza, S., De Ferrari, G.V., Aguayo, L.G., and Opazo, C. (2011). Biphasic effects of copper on neurotransmission in rat hippocampal neurons. J Neurochem 119, 78-88.
32. Prasad, A.N., Levin, S., Rupar, C.A., and Prasad, C. (2011). Menkes disease and infantile epilepsy. Brain Dev 33, 866-876.
33. Schrag, M., Mueller, C., Oyoyo, U., Smith, M.A., and Kirsch, W.M. (2011). Iron, zinc and copper in the Alzheimer's disease brain: a quantitative meta-analysis. Some insight on the influence of citation bias on scientific opinion. Prog Neurobiol 94, 296-306.
34. Sensi, S.L., Paoletti, P., Koh, J.Y., Aizenman, E., Bush, A.I., and Hershfinkel, M. (2011). The neurophysiology and pathology of brain zinc. J Neurosci 31, 16076-16085.
35. Sepulveda, F.J., Opazo, C., and Aguayo, L.G. (2009). Alzheimer beta-amyloid blocks epileptiform activity in hippocampal neurons. Mol Cell Neurosci 41, 420-428.
36. Takeda, A., Minami, A., Takefuta, S., Tochigi, M., and Oku, N. (2001). Zinc homeostasis in the brain of adult rats fed zinc-deficient diet. J Neurosci Res 63, 447-452.
37. Tarohda, T., Yamamoto, M., and Amamo, R. (2004). Regional distribution of manganese, iron, copper, and zinc in the rat brain during development. Anal Bioanal Chem 380, 240-246.
38. Trombley, P.Q., and Shepherd, G.M. (1996). Differential modulation by zinc and copper of amino acid receptors from rat olfactory bulb neurons. J Neurophysiol 76, 2536-2546.
39. Vlachova, V., Zemkova, H., and Vyklicky, L., Jr. (1996). Copper modulation of NMDA responses in mouse and rat cultured hippocampal neurons. Eur J Neurosci 8, 2257-2264.
40. Weiser, T., and Wienrich, M. (1996). The effects of copper ions on glutamate receptors in cultured rat cortical neurons. Brain Res 742, 211-218.
41. Westmark, C.J., Westmark, P.R., Beard, A.M., Hildebrandt, S.M., and Malter, J.S. (2008). Seizure susceptibility and mortality in mice that over-express amyloid precursor protein. Int J Clin Exp Pathol 1, 157-168.