Expression of the mu-opioid receptor is induced in dentate gyrus granule cells after focal cerebrocortical ischaemia and stimulation of entorhinal afferents

European Journal of Neuroscience

Volumn 22, Issue 5, 2005, Pages 1032-1044

  Stumm, Ralf ^a   Rüthrich, Heinz ^a   Schulz, Stefan ^a   Zhou, Chun ^a   Hollt, Volker ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

Long term potentiation; Opiate; Plasticity; Rat

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; MESSENGER RNA; MU OPIATE RECEPTOR; NERVE PROTEIN; PROTEIN ARG 3.1 ARC; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; BRAIN ISCHEMIA; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; ELECTROSTIMULATION; ENTORHINAL CORTEX; GRANULE CELL; HIPPOCAMPUS; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NERVE STIMULATION; NONHUMAN; OCCLUSIVE CEREBROVASCULAR DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSORY NERVE;

ANIMALS; BRAIN ISCHEMIA; CYTOSKELETAL PROTEINS; DIAGNOSTIC IMAGING; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; ENTORHINAL CORTEX; FUNCTIONAL LATERALITY; GENE EXPRESSION REGULATION; GLUTAMATE DECARBOXYLASE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INFARCTION, MIDDLE CEREBRAL ARTERY; LONG-TERM POTENTIATION; MALE; NERVE TISSUE PROTEINS; NEURONS; PERFORANT PATHWAY; RATS; RECEPTORS, OPIOID, MU; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 25844530985     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.04296.x     Document Type: Article

References (45)

1. Acsady, L., Kamondi, A., Sik, A., Freund, T. & Buzsaki, G. (1998) GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J. Neurosci., 18, 3386-3403.
2. Angerer, L.M., Cox, K.H. & Angerer, R.C. (1987) Demonstration of tissue-specific gene expression by in situ hybridization. Meth. Enzymol., 152, 649-661.
3. Bausch, S.B. & Chavkin, C. (1997) Changes in hippocampal circuitry after pilocarpine-induced seizures as revealed by opioid receptor distribution and activation. J. Neurosci., 17, 477-492.
4. Bliss, T.V. & Collingridge, G.L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature, 361, 31-39.
5. Bramham, C.R. & Sarvey, J.M. (1996) Endogenous activation of mu and delta-1 opioid receptors is required for long-term potentiation induction in the lateral perforant path: dependence on GABAergic inhibition. J. Neurosci., 16, 8123-8131.
6. Cohen, G.A., Doze, V.A. & Madison, D.V. (1992) Opioid inhibition of GABA release from presynaptic terminals of rat hippocampal interneurons. Neuron, 9, 325-335.
7. Drake, C.T. & Milner, T.A. (1999) Mu opioid receptors are in somatodendritic and axonal compartments of GABAergic neurons in rat hippocampal formation. Brain Res., 849, 203-215.
8. Drake, C.T. & Milner, T.A. (2002) Mu opioid receptors are in discrete hippocampal interneuron subpopulations. Hippocampus, 12, 119-136.
9. Fredens, K., Stengaard-Pedersen, K. & Larsson, L.I. (1984) Localization of enkephalin and cholecystokinin immunoreactivities in the perforant path terminal fields of the rat hippocampal formation. Brain Res., 304, 255-263.
10. Fremeau, R.T. Jr, Troyer, M.D., Pahner, I., Nygaard, G.O., Tran, C.H., Reimer, R.J., Bellocchio, E.E., Fortin, D., Storm-Mathisen, J. & Edwards, R.H. (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron, 31, 247-260.
11. Freund, T.F. & Buzsaki, G. (1996) Interneurons of the hippocampus. Hippocampus, 6, 347-470.
12. Gall, C., Brecha, N., Karten, H.J. & Chang, K.J. (1981) Localization of enkephalin-like immunoreactivity to identified axonal and neuronal populations of the rat hippocampus. J. Comp. Neurol., 198, 335-350.
13. Goelet, P., Castellucci, V.F., Schacher, S. & Kandel, E.R. (1986) The long and the short of long-term memory - a molecular framework. Nature, 322, 419-422.
14. Guzowski, J.F., McNaughton, B.L., Barnes, C.A. & Worley, P.F. (1999) Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat. Neurosci., 2, 1120-1124.
15. Hassan, H., Pohle, W., Ruthrich, H., Brodemann, R. & Krug, M. (2000) Repeated long-term potentiation induces mossy fibre sprouting and changes the sensibility of hippocampal granule cells to subconvulsive doses of pentylenetetrazol. Eur. J. Neurosci., 12, 1509-1515.
16. Hossmann, K.A. (1994) Glutamate-mediated injury in focal cerebral ischemia: the excitotoxin hypothesis revised. Brain Pathol., 4, 23-36.
17. Kalyuzhny, A.E. & Wessendorf, M.W. (1997) CNS GABA neurons express the mu-opioid receptor: immunocytochemical studies. Neuroreport, 8, 3367-3372.
18. Kalyuzhny, A.E. & Wessendorf, M.W. (1998) Relationship of mu- and delta-opioid receptors to GABAergic neurons in the central nervous system, including antinociceptive brainstem circuits. J. Comp. Neurol., 392, 528-547.
19. Krug, M., Brodemann, R., Matthies, R., Ruthrich, H. & Wagner, M. (2001) Activation of the dentate gyrus by stimulation of the contralateral perforant pathway: evoked potentials and long-term potentiation after ipsi- and contralateral induction. Hippocampus, 11, 157-167.
20. Kunizuka, H., Kinouchi, H., Arai, S., Izaki, K., Mikawa, S., Kamii, H., Sugawara, T., Suzuki, A., Mizoi, K. & Yoshimoto, T. (1999) Activation of Arc gene, a dendritic immediate early gene, by middle cerebral artery occlusion in rat brain. Neuroreport, 10, 1717-1722.
21. Liao, D., Lin, H., Law, P.Y. & Loh, H.H. (2005) Mu-opioid receptors modulate the stability of dendritic spines. Proc. Natl. Acad. Sci. USA, 102, 1725-1730.
22. Link, W., Konietzko, U., Kauselmann, G., Krug, M., Schwanke, B., Frey, U. & Kuhl, D. (1995) Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc. Natl. Acad. Sci. USA, 92, 5734-5738.
23. Loh, H.H., Liu, H.C., Cavalli, A., Yang, W., Chen, Y.F. & Wei, L.N. (1998) mu Opioid receptor knockout in mice: effects on ligand-induced analgesia and morphine lethality. Brain Res. Mol. Brain Res., 54, 321-326.
24. Lyford, G.L., Yamagata, K., Kaufmann, W.E., Barnes, C.A., Sanders, L.K., Copeland, N.G., Gilbert, D.J., Jenkins, N.A., Lanahan, A.A. & Worley, P.F. (1995) Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron, 14, 433-445.
25. Mansour, A., Fox, C.A., Burke, S., Meng, F., Thompson, R.C., Akil, H. & Watson, S.J. (1994) Mu, delta, and kappa opioid receptor mRNA expression in the rat CNS: an in situ hybridization study. J. Comp. Neurol., 350, 412-438.
26. Moore, S.D., Madamba, S.G., Schweitzer, P. & Siggins, G.R. (1994) Voltage-dependent effects of opioid peptides on hippocampal CA3 pyramidal neurons in vitro. J. Neurosci., 14, 809-820.
27. Morris, B.J., Feasey, K.J., ten Bruggencate, G., Herz, A. & Hollt, V. (1988) Electrical stimulation in vivo increases the expression of proenkephalin mRNA and decreases the expression of prodynorphin mRNA in rat hippocampal granule cells. Proc. Natl. Acad. Sci. USA, 85, 3226-3230.
28. Najlerahim, A., Harrison, P.J., Barton, A.J., Heffernan, J. & Pearson, R.C. (1990) Distribution of messenger RNAs encoding the enzymes glutaminase, aspartate aminotransferase and glutamic acid decarboxylase in rat brain. Brain Res. Mol. Brain Res., 7, 317-333.
29. Nyakas, C., Luiten, P.G., Spencer, D.G. & Traber, J. (1987) Detailed projection patterns of septal and diagonal band efferents to the hippocampus in the rat with emphasis on innervation of CA1 and dentate gyrus. Brain Res. Bull., 18, 533-545.
30. Przewlocki, R., Kaminska, B., Lukasiuk, K., Nowicka, D.Z., Przewlocka, B., Kaczmarek, L. & Lason, W. (1995) Seizure related changes in the regulation of opioid genes and transcription factors in the dentate gyrus of rat hippocampus. Neuroscience, 68, 73-81.
31. Schulz, S., Schreff, M., Koch, T., Zimprich, A., Gramsch, C., Elde, R. & Hollt, V. (1998) Immunolocalization of two mu-opioid receptor isoforms (MOR1 and MOR1B) in the rat central nervous system. Neuroscience, 82, 613-622.
32. Schulz, S., Siemer, H., Krug, M. & Hollt, V. (1999) Direct evidence for biphasic cAMP responsive element-binding protein phosphorylation during long-term potentiation in the rat dentate gyrus in vivo. J. Neurosci., 19, 5683-5692.
33. Schuster, T., Krug, M., Hassan, H. & Schachner, M. (1998) Increase in proportion of hippocampal spine synapses expressing neural cell adhesion molecule NCAM 180 following long-term potentiation. J. Neurobiol., 37, 359-372.
34. Simmons, M.L. & Chavkin, C. (1996) Endogenous opioid regulation of hippocampal function. Int. Rev. Neurobiol., 39, 145-196.
35. Skyers, P.S., Einheber, S., Pierce, J.P. & Milner, T.A. (2003) Increased mu-opioid receptor labeling is found on inner molecular layer terminals of the dentate gyrus following seizures. Exp. Neurol., 179, 200-209.
36. Sopala, M., Frankiewicz, T., Parsons, C. & Danysz, W. (2000) Middle cerebral artery occlusion produces secondary, remote impairment in hippocampal plasticity of rats - involvement of N-methyl-D-aspartate receptors? Neurosci. Lett., 281, 143-146.
37. Strong, A.J., Fabricius, M., Boutelle, M.G., Hibbins, S.J., Hopwood, S.E., Jones, R., Parkin, M.C. & Lauritzen, M. (2002) Spreading and synchronous depressions of cortical activity in acutely injured human brain. Stroke, 33, 2738-2743.
38. Stumm, R., Culmsee, C., Schafer, M.K., Krieglstein, J. & Weihe, E. (2001) Adaptive plasticity in tachykinin and tachykinin receptor expression after focal cerebral ischemia is differentially linked to gabaergic and glutamatergic cerebrocortical circuits and cerebrovenular endothelium. J. Neurosci., 21, 798-811.
39. Stumm, R.K., Zhou, C., Schulz, S. & Hollt, V. (2004) Neuronal types expressing mu- and delta-opioid receptor mRNA in the rat hippocampal formation. J. Comp. Neurol., 469, 107-118.
40. Tamura, A., Graham, D.I., McCulloch, J. & Teasdale, G.M. (1981) Focal cerebral ischaemia in the rat: 1. Description of technique and early neuropathological consequences following middle cerebral artery occlusion. J. Cereb. Blood Flow Metab., 1, 53-60.
41. Tan, A., Moratalla, R., Lyford, G.L., Worley, P. & Graybiel, A.M. (2000) The activity-regulated cytoskeletal-associated protein arc is expressed in different striosome-matrix patterns following exposure to amphetamine and cocaine. J. Neurochem., 74, 2074-2078.
42. Temple, M.D., Worley, P.F. & Steward, O. (2003) Visualizing changes in circuit activity resulting from denervation and reinnervation using immediate early gene expression. J. Neurosci., 23, 2779-2788.
43. Vazdarjanova, A., McNaughton, B.L., Barnes, C.A., Worley, P.F. & Guzowski, J.F. (2002) Experience-dependent coincident expression of the effector immediate-early genes arc and Homer 1a in hippocampal and neocortical neuronal networks. J. Neurosci., 22, 10067-10071.
44. Wolf, T., Lindauer, U., Reuter, U., Back, T., Villringer, A., Einhaupl, K. & Dirnagl, U. (1997) Noninvasive near infrared spectroscopy monitoring of regional cerebral blood oxygenation changes during peri-infarct depolarizations in focal cerebral ischemia in the rat. J. Cereb. Blood Flow Metab., 17, 950-954.
45. Zieglgansberger, W., French, E.D., Siggins, G.R. & Bloom, F.E. (1979) Opioid peptides may excite hippocampal pyramidal neurons by inhibiting adjacent inhibitory interneurons. Science, 205, 415-417.