Loss of dynorphin-mediated inhibition of voltage-dependent Ca2+ currents in hippocampal granule cells isolated from epilepsy patients is associated with mossy fiber sprouting

Neuroscience

Volumn 94, Issue 2, 1999, Pages 465-471

  Jeub, M ^a   Lie, A ^a   Blumcke I ^a   Elger, C E ^a   Beck, H ^a  

^a UNIVERSITY HOSPITAL BONN   (Germany)

Author keywords

Receptor; Dynorphin; Human temporal lobe epilepsy; Opioid; Recurrent sprouting; Voltage dependent Ca2+ current

Indexed keywords

DYNORPHIN; KAPPA OPIATE RECEPTOR; NALOXONE; OPIATE AGONIST; OPIATE ANTAGONIST; OPIATE PEPTIDE;

ADOLESCENT; ADULT; ARTICLE; CALCIUM CURRENT; CHILD; CLINICAL ARTICLE; CONCENTRATION RESPONSE; DENTATE GYRUS; FEMALE; HIPPOCAMPUS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOREACTIVITY; MALE; MOSSY FIBER; NERVE EXCITABILITY; NERVE SPROUTING; PRIORITY JOURNAL; TEMPORAL LOBE EPILEPSY;

ADOLESCENT; ADULT; AGE OF ONSET; AXONS; CALCIUM CHANNELS, N-TYPE; CHILD; DENTATE GYRUS; DYNORPHINS; ELECTRIC STIMULATION; EPILEPSY, TEMPORAL LOBE; FEMALE; HIPPOCAMPUS; HUMANS; MALE; MIDDLE AGED; NALOXONE; NERVE ENDINGS; NERVE FIBERS; NEURONS; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; SCLEROSIS;

EID: 0032835098     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(99)00249-3     Document Type: Article

References (37)

1. Babb T.L., Kupfer W.R., Pretorius J.K., Crandall P.H., Levesque M.F. Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience. 42:1991;351-363.
2. Barry P.H., Lynch J.W. Liquid junction potentials and small cell effects in patch-clamp analysis. J. Membr. Biol. 121:1991;101-117.
3. Bean B.P. Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage dependence. Nature. 340:1989;153-156.
4. Beck H., Steffens R., Heinemann U., Elger C.E. Properties of voltage-activated calcium currents in acutely dissociated human hippocampal granule cells. J. Neurophysiol. 77:1998;1526-1537.
5. Buhl E.H., Otis T.S., Mody I. Zinc-induced collapse of augmented inhibition by GABA in temporal lobe epilepsy model. Science. 271:1996;369-373.
6. Chavkin C., James I.F., Goldstein A. Dynorphin is a specific endogenous ligand of the kappa opioid receptor. Science. 215:1982;413-415.
7. Chen L., Gu Y., Huang L.-Y. M. The opioid peptide dynorphin directly blocks NMDA receptor channels in the rat. J. Physiol., Lond. 482:1995;575-581.
8. Chen L., Gu Y., Mae Huang L.-Y. The mechanism of action for the block of NMDA receptor channels by the opioid peptide dynorphin. J. Neurosci. 15:1995;4602-4611.
9. 3H)U69,593 binding in the human epileptogenic hippocampus. Epilepsy Res. 28:1997;189-205.
10. Douglass J., Grimes L., Shook J., Lee P.H.K., Hong J.-S. Systemic administration of kainic acid differentially regulates the levels of prodynorphin and proenkephalin mRNA and peptides in the rat hippocampus. Molec. Brain Res. 9:1991;79-86.
11. Drake C.T., Terman G.W., Simmons M.L., Milner T.A., Kunkel D.D., Schwartzkroin P.A., Chavkin C. Dynorphin opioids present in dentate granule cells may function as retrograde inhibitory neurotransmitters. J. Neurosci. 14:1994;3736-3750.
12. Gall C., Lauterborn J., Isackson P., White J. Seizures, neuropeptide regulation, and mRNA expression in the hippocampus. Prog. Brain Res. 83:1990;371-390.
13. Gross R.A., Moises H.C., Uhler M.D., Macdonald R.L. Dynorphin A and cAMP-dependent protein kinase independently regulate neuronal calcium currents. Proc. natn. Acad. Sci. U.S.A. 87:1990;7025-7029.
14. Hamill O.P., Marty A., Neher E., Sakmann B., Sigworth F.J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch. 391:1981;85-100.
15. Houser C.R., Miyashiro J.E., Swartz B.E., Walsh G.O., Rich J.R., Delgado-Escueta A.V. Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J. Neurosci. 10:1990;267-282.
16. Ingram S., Wilding T.J., McClesky E.W., Williams J.T. Efficacy and kinetics of opioid action on acutely dissociated neurons. Molec. Pharmac. 52:1997;136-143.
17. Khachaturian H., Schäfer M. K. H. and Lewis M. E. (1993) Anatomy and function of the endogenous opioid system. In Opioids (ed. Herz A.), Vol. 1, pp. 471-479. Springer-Verlag, Berlin.
18. Macdonald R.L., Werz M.A. Dynorphin A decreases voltage-dependent calcium conductances of mouse dorsal root ganglion neurones. J. Physiol., Lond. 377:1986;237-249.
19. Margerison J.H., Corsellis J.A.N. A clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain. 89:1966;499-530.
20. McGinty J.F., Henriksen S.J., Goldstein A., Terenius L., Bloom F.E. Dynorphin is contained within hippocampal mossy fibers: immunochemical alterations after kainic acid administration and colchicine-induced neurotoxicity. Proc. natn. Acad. Sci. U.S.A. 80:1983;589-593.
21. Morris B.J., Johnston H.M. A role for hippocampal opioid in long-term functional plasticity. Trends Neurosci. 18:1998;350-355.
22. Patrylo P.R., Dudek F.E. Physiological unmasking of new glutamatergic pathways in the dentate gyrus of hippocampal slices from kainate-induced epileptic rats. J. Neurophysiol. 79:1998;418-429.
23. Przewlocka B., Stala L., Lason W., Przewlocki R. The effect of various opiate receptor agonists on the seizure threshold in the rat. Is dynorphin an endogenous anticonvulsant? Life Sci. 33:1983;595-598.
24. Romualdi P., Donatini A., Bregola G., Bianchi C., Beani L., Ferroni S., Simonato M. Early changes in prodynorphin mRNA and ir-dynorphin A levels after kindled seizures in the rat. Eur. J. Neurosci. 7:1995;1850-1856.
25. Sigworth F.J., Affolter H., Neher E. Design of the EPC-9, a computer-controlled patch-clamp amplifier. 2 Software. J. Neurosci. Meth. 56:1995;203-215.
26. Snead O. C. and Simonato M. (1991) Opioid peptides and seizures. In Neurotransmitters and Epilepsy (eds Fisher R. S. and Coyle J.), pp. 181-200. Wiley-Liss, New York.
27. Sutula T., Cascino G., Cavazos J., Parada I., Ramirez L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann. Neurol. 26:1989;321-330.
28. Terrian D.M., Johnston D., Claiborne B.J., Ansah-Yiadom R., Strittmatter W.J., Rea M.A. Glutamate and dynorphin release from a subcellular fraction enriched in hippocampal mossy fiber synaptosomes. Brain Res. Bull. 21:1988;343-351.
29. Tortella F.C. Endogenous opioid peptides and epilepsy: quieting the seizing brain. Trends pharmac. Sci. 9:1988;366-372.
30. VonVoigtlander P.F., Hall E.D., Camacho-Ochoa M., Lewis R.A., Triezenberg H.J. U-54494A: a unique anticonvulsant related to kappa opioid agonists. J. Pharmac. exp. Ther. 243:1987;542-547.
31. Wagner J.J., Caudle R.M., Chavkin C. Kappa opioids decrease excitatory transmission in the dentate gyrus of the guinea pig hippocampus. J. Neurosci. 12:1992;132-141.
32. Wagner J.J., Terman G.W., Chavkin C. Endogenous dynorphins inhibit excitatory neurotransmission and block LTP induction in the hippocampus. Nature. 363:1993;451-454.
33. Weisskopf M.G., Zalutsky R.A., Nicoll R.A. The opioid peptide dynorphin mediates heterosynaptic depression of hippocampal mossy fibre synapses and modulates long-term potentiation. Nature. 362:1993;423-427.
34. 0α-subtype G protein in rat primary afferent neurons. J. Neurophysiol. 77:1997;1338-1348.
35. Wuarin J.P., Dudek F.E. Electrographic seizures and new recurrent excitatory circuits in the dentate gyrus of hippocampal slices from kainate treated epileptic rats. J. Neurosci. 16:1996;4438-4448.
36. Wyler A.R., Dohan F.C. Jr., Schweitzer J.B., Berry A.D. III. A grading system for mesial temporal pathology (hippocampal sclerosis) from anterior temporal lobectomy. J. Epilepsy. 5:1992;220-225.
37. 45Ca into rat cortical synaptosomes by inhibiting N- but not L-type calcium channels. Neuropharmacology. 29:1990;439-444.