Differential expression of preproenkephalin and preprodynorphin mRNAs in striatal neurons: high levels of preproenkephalin expression depend on cerebral cortical afferents

Gr, Uhl; Navia, Bradford; Douglas, Janice G.

doi:10.1523/jneurosci.08-12-04755.1988

Cited by 120 publications

(62 citation statements)

References 28 publications

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“…This conclusion is consistent with previous evidence that although all striatal neurons respond to glutamatergic cortical input, the input to indirect pathway striatal neurons somehow differs from that to direct pathway neurons (Uhl et al, 1988;Zemanick et al, 1991;Berretta et al, 1997;Parthasarathy and Graybiel 1997).…”

Section: Discussionsupporting

confidence: 93%

“…The larger size of PT-type terminals than IT-type and their tendency to be apposed to perforated postsynaptic densities may augment their synaptic efficacy (Geinisman, 1993;Sulzer and Pothos, 2000). This might explain why striato-GP neurons appear more responsive to cortical input than striato-EP-SNr neurons (Uhl et al, 1988;Parthasarathy and Graybiel 1997) and more avidly take up and anterogradely transmit the cortically injected H129 strain of herpes simplex virus (Zemanick et al, 1991). Perforated postsynaptic densities also indicate sites of synaptic potentiation (Geinisman, 1993;Geinisman et al, 1996;Sulzer and Pothos, 2000;Topni et al, 2001).…”

Section: Functional Implicationsmentioning

confidence: 99%

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Evidence for Differential Cortical Input to Direct Pathway versus Indirect Pathway Striatal Projection Neurons in Rats

Lei

Jiao²,

Mar³

et al. 2004

J. Neurosci.

253

258

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The two main types of corticostriatal neurons are those that project only intratelencephalically (IT-type), the intrastriatal terminals of which are 0.41 m in mean diameter, and those that send their main axon into pyramidal tract and have a collateral projection to striatum (PT-type), the intrastriatal terminals of which are 0.82 m in mean diameter. We used three approaches to examine whether the two striatal projection neuron types (striatonigral direct pathway vs striatopallidal indirect pathway) differ in their input from IT-type and PT-type neurons. First, we retrogradely labeled one striatal projection neuron type or the other with biotinylated dextran amine (BDA)-3000 molecular weight. We found that terminals making asymmetric axospinous contact with striatonigral neurons were 0.43 m in mean diameter, whereas those making asymmetric axospinous contact with striatopallidal neurons were 0.69 m. Second, we preferentially immunolabeled striatonigral neurons for D 1 dopamine receptors or striatopallidal neurons for D 2 dopamine receptors and found that axospinous terminals had a smaller mean size (0.45 m) on D 1 ϩ spines than on D 2 ϩ spines (0.61 m). Finally, we combined selective BDA labeling of IT-type or PT-type terminals with immunolabeling for D 1 or D 2 , and found that IT-type terminals were twice as common as PT-type on D 1 ϩ spines, whereas PT-type terminals were four times as common as IT-type on D 2 ϩ spines. These various results suggest that striatonigral neurons preferentially receive input from IT-type cortical neurons, whereas striatopallidal neurons receive greater input from PT-type cortical neurons. This differential cortical connectivity may further the roles of the direct and indirect pathways in promoting desired movements and suppressing unwanted movements, respectively.

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Section: Discussionsupporting

confidence: 93%

Section: Functional Implicationsmentioning

confidence: 99%

Evidence for Differential Cortical Input to Direct Pathway versus Indirect Pathway Striatal Projection Neurons in Rats

Lei

Jiao²,

Mar³

et al. 2004

J. Neurosci.

253

258

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“…A similar pattern emerges for CPE mRNA. Studies of enkephalin-and dynorphin-containing neurons have employed immunohistochemistry (Sar et al, 1978;Uhl et al, 1978Uhl et al, , 1979aPickel et al, 1980;Finley et al, 198 1;Watson et al, 1982) and in situ hybridization (Young et al, 1986a;Morris et al, 1988a, b;Uhl et al, 1988). Regions with neurons enriched in both enkephalins or dynorphin and CPE mRNA include the periglomerula neurons in the olfactory bulb, the lateral septum, the nucleus of the stria terminalis, the anterior olfactory nucleus, the paraventricular and supraoptic nuclei of the hypothalamus, the ventral tegmental nucleus, the dorsal tegmental nucleus, the parabrachial nucleus, the nucleus of the tractus solitarius, and the lateral reticular nucleus.…”

Section: Discussionmentioning

confidence: 99%

“…A subpopulation of granule cells in the olfactory bulb is strongly immunoreactive for enkephalin (Finley et al, 1981) but does not display CPE mRNA. The corpus striatum has very high levels of preproenkephalin and preprodynorphin mRNA (Young et al, 1986a;Morris et al, 1988a,b;Uhl et al, 1988) and enkephalin immunoreactivity (Pickel et al, 1980) but relatively low levels of CPE mRNA. Moreover, enkephalin expression is highest in the ventral striatum, nucleus accumbens, and ventral pallidum, while CPE mRNA is homogeneously distributed throughout these areas.…”

Section: Discussionmentioning

confidence: 99%

“…For instance, hypothalamic magnocellular neurons contain vasopressin and oxytocin (Uhl et al, 1985;Young et al, 1986b), while hypothalamic paraventricular parvocellular neurons contain CRF and neuropeptide Y (Chronwall et al, 1985;Antoni and Linton, 1989). Neurotensin (Uhl et al, 1979b) and atriopeptin (Saper et al, 1985) are concentrated in the nucleus ofthe tractus solitarius and the parabrachial nucleus, as well as other brain regions. In the hippocampus, somatostatin occurs in the large pyramidal neurons immediately lateral to the dentate gyrus, which are enriched in CPE mRNA.…”

Section: Discussionmentioning

confidence: 99%

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Carboxypeptidase E (enkephalin convertase): mRNA distribution in rat brain by in situ hybridization

1990

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Carboxypeptidase E (CPE), also referred to as enkephalin convertase or carboxypeptidase H (EC 3.4.17.10), is present in neurotransmitter secretory granules and can remove C-terminal basic residues following endopeptidase cleavage during peptide processing. Using in situ hybridization with 35S-labeled oligonucleotide probes, we have mapped the localization of CPE mRNA in the rat brain. Specificity for CPE was confirmed by control experiments, which included production of identical patterns hybridization with 3 different antisense oligonucleotide probes, loss of label with RNase pretreatment of sections or co-incubation with excess unlabeled probe, and lack of labeling with sense orientation probes. In addition, the regional distribution of CPE mRNA by Northern blot analysis corresponded with distribution of labeling by in situ hybridization. The highest levels of CPE mRNA were found to be present in the pyramidal cells of the hippocampus, the pituitary anterior and intermediate lobes, the ependymal cells of the lateral ventricle, the endopiriform nucleus, the basolateral amygdala, the supraoptic nucleus, and the paraventricular nucleus. Intermediate levels were present in the thalamus, medial geniculate nucleus, lateral septal nucleus, piriform and entorhinal cortex, nucleus of the tractus solitarius, cerebellar cortex, pontine nuclei, and inferior olive. The lowest levels were found in the hippocampal granule cell layer, lateral hypothalamus, globus pallidus, and brain stem reticular formation. Ibotenic acid lesions of the hippocampus eliminated the majority of the label, which had been present over pyramidal cells, though labeling was increased over areas of reactive gliosis, suggesting that activated astrocytes can also synthesize CPE mRNA. In general, the localization of CPE mRNA in the rat brain corresponded to the distribution of enkephalin and other peptide neurotransmitter-synthesizing neurons, though CPE mRNA was also present in neurons that do not secrete known peptides and in reactive glia. The widespread yet specific localization of CPE mRNA in the rat brain suggests it may be an excellent marker for peptide synthesizing cells in the CNS.

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Anatomical and functional evidence for lesion-specific sprouting of corticostriatal input in the adult rat

1996

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Previous studies in our laboratory have shown that cortical lesions induced by thermocoagulation of pial blood vessels, but not by acute aspiration, result in 1) the preservation of control levels of the growth-associated protein (GAP)-43 and 2) a prolonged increase in neurotransmitter gene expression in the denervated dorsolateral striatum. We have examined whether corticostriatal projections from the spared homotypic contralateral cortex contribute to these effects. Adult rats received either a thermocoagulatory or aspiration lesion of the cerebral cortex and, after 30 days, received an injection of the anterograde tracer, Fluoro-Ruby, in the contralateral homotypic cortex. Rats were killed 7 days later, and labeled fibers were examined with fluorescence microscopy in the ipsilateral and contralateral striata. Ipsilateral corticostriatal projections were detected in lesioned and unlesioned rats. Numerous labeled fibers were detected in the contralateral striatum of thermocoagulatory-lesioned but not aspiration-lesioned or control animals, suggesting that contralateral cortical neurons may undergo axonal sprouting in the denervated striatum following a thermocoagulatory lesion of the cortex. To determine whether contralateral corticostriatal fibers play a role in the changes in striatal gene expression induced by the thermocoagulatory lesions, the effects of aspiration lesions, as well as unilateral and bilateral thermocoagulatory lesions of the cortex were compared. Confirming previous results, striatal enkephalin mRNA levels were increased after a unilateral thermocoagulatory lesion. However, they were unchanged after aspiration or bilateral thermocoagulatory lesions, suggesting that sprouting or overactivity of contralateral corticostriatal input contributes to the increase seen after unilateral thermocoagulatory lesions.

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Differential expression of preproenkephalin and preprodynorphin mRNAs in striatal neurons: high levels of preproenkephalin expression depend on cerebral cortical afferents

Cited by 120 publications

References 28 publications

Evidence for Differential Cortical Input to Direct Pathway versus Indirect Pathway Striatal Projection Neurons in Rats

Evidence for Differential Cortical Input to Direct Pathway versus Indirect Pathway Striatal Projection Neurons in Rats

Carboxypeptidase E (enkephalin convertase): mRNA distribution in rat brain by in situ hybridization

Anatomical and functional evidence for lesion-specific sprouting of corticostriatal input in the adult rat

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