D1 and D2 receptor regulation of preproenkephalin and preprodynorphin mRNA in rat striatum following acute injection of amphetamine or methamphetamine

Abstract

Our previous work has demonstrated a dose‐dependent induction of striatal preprodynorphin (PPD) in response to a single injection of the psychostimulants amphetamine (AMPH) or methamphetamine (METH). In the present study, dose‐response effects of acute administration of these stimulants on preproenkephalin (PPE) mRNA expression in the rat striatum were investigated with quantitative in situ hybridization histochemistry 3 h after injection. Acute AMPH or METH at equimolar doses (3.75, 7.5, 15, and 30 μmol/kg) significantly increased PPE mRNA expression in dorsal (caudoputamen), but not ventral (nucleus accumbens), striatum in a dose‐dependent fashion. In addition, the role of D1 and D2 dopamine receptors in mediating AMPH‐ and METH‐stimulated PPE and PPD expression was also evaluated by using subtype‐specific antagonists. Pretreatment of rats with SCH 23390 (0.1 mg/kg, i.p.), a selective D1 receptor antagonist, completely blocked acute AMPH (21 μmol/kg, i.p.)‐ or METH (21 μmol/kg, i.p.)‐induced PPE as well as PPD mRNA expression in the caudoputamen. Pretreatment with eticlopride (0.5 mg/kg, i.p.), a selective D2 receptor antagonist, also blocked PPD induction by the two stimulants, but PPE induction was unaffected. Furthermore, SCH 23390 decreased, and eticlopride elevated, constitutive PPE mRNA levels in the caudoputamen. Neither antagonist had a significant effect on the basal level of PPE or PPD mRNA in the nucleus accumbens. These results demonstrate a clear dose‐related responsiveness of PPE gene expression in striatal neurons in response to acute administration of amphetamines, although the intensity of the response is far less than that for striatal PPD. Furthermore, both D1 and D2 subtypes of dopamine receptors mediate AMPH‐ and METH‐stimulated striatal PPD mRNA expression, whereas D1 receptor activation alone mediates amphetamine‐stimulated PPE mRNA expression in the rat striatum. © 1996 Wiley‐Liss, Inc.

Microdialysis and mass spectrometric monitoring of dopamine and enkephalins in the globus pallidus reveal reciprocal interactions that regulate movement

“…Thus, DA acts at pre‐synaptic D 1 Rs on striatopallidal terminals to enhance GABA and ENK release and may be required to fine tune pallidal inhibition. These results are consistent with a previous study showing acute AMPH‐induced increases in PENK mRNA expression in striatal MSNs (Wang and McGinty 1996). Therefore, D 1 R stimulation facilitates ENK release and subsequent increases in PENK mRNA expression (Wang and McGinty 1996) possibly to maintain ENK stores.…”

Microdialysis and mass spectrometric monitoring of dopamine and enkephalins in the globus pallidus reveal reciprocal interactions that regulate movement

“…Thus, DA acts at pre‐synaptic D 1 Rs on striatopallidal terminals to enhance GABA and ENK release and may be required to fine tune pallidal inhibition. These results are consistent with a previous study showing acute AMPH‐induced increases in PENK mRNA expression in striatal MSNs (Wang and McGinty 1996). Therefore, D 1 R stimulation facilitates ENK release and subsequent increases in PENK mRNA expression (Wang and McGinty 1996) possibly to maintain ENK stores.…”

Ciproxifan, a histamine H3‐receptor antagonist/inverse agonist, modulates the effects of methamphetamine on neuropeptide mRNA expression in rat striatum

“…As previously reported (Smith & McGinty, 1994; Wang & McGinty, 1995, 1996a,b; Adams et al ., 2000), we observed a significant increase in prodynorphin mRNAs after treatment with MET. Although the up‐regulation induced by a higher dose (15 mg/kg) was restricted to the caudate–putamen (Smith & McGinty, 1994; Adams et al ., 2000), the increase was also observed in the nucleus accumbens, as previously found with similar doses of MET (Wang & McGinty, 1995, 1996a,b). Whereas it potentiated the MET‐induced decrease of proenkephalin mRNAs, ciproxifan suppressed the MET‐induced up‐regulation of prodynorphin mRNAs in the same animals.…”

Differential Regulation of Striatal Preproenkephalin and Preprotachykinin mRNA Levels in MPTP‐Lesioned Monkeys Chronically Treated with Dopamine D1 or D2 Receptor Agonists

“…In fact, administration of the dopamine D 2 agonist cabergoline led to correction of PPE mRNA levels compared with the control, whereas elevated PPE mRNA levels observed in untreated MPTP‐lesioned monkeys were unaltered by continuous and further increased by pulsatile administration of the dopamine D 1 agonist SKF‐82958. This is consistent with previous studies using different dopamine D 1 (SKF‐38393) or D 2 (quinpirole) agonists administered in a pulsatile mode in 6‐OHDA‐denervated rats (Gerfen et al, 1990 ; Pollack and Wooten, 1992) as well as with those using selective dopamine D 1 (SCH23390) or D 2 (YM‐091510M and eticlopride) antagonists in normal rats (Morris et al, 1988 ; Morris and Hunt, 1991) and in rats treated with amphetamine or methamphetamine (Wang and McGinty, 1996 a ). Rats were killed 3 h after their last dopamine agonist treatment in the above references, whereas in our present results a 3‐day washout period was used ; the agreement between our findings and those above suggest that the changes of peptide expression are due to the agonist treatment rather than a consequence of its withdrawal, although we cannot totally rule out such a mechanism.…”

Microdialysis and mass spectrometric monitoring of dopamine and enkephalins in the globus pallidus reveal reciprocal interactions that regulate movement

“…Thus, DA acts at pre‐synaptic D 1 Rs on striatopallidal terminals to enhance GABA and ENK release and may be required to fine tune pallidal inhibition. These results are consistent with a previous study showing acute AMPH‐induced increases in PENK mRNA expression in striatal MSNs (Wang and McGinty 1996). Therefore, D 1 R stimulation facilitates ENK release and subsequent increases in PENK mRNA expression (Wang and McGinty 1996) possibly to maintain ENK stores.…”

Ciproxifan, a histamine H3‐receptor antagonist/inverse agonist, modulates the effects of methamphetamine on neuropeptide mRNA expression in rat striatum

“…As previously reported (Smith & McGinty, 1994; Wang & McGinty, 1995, 1996a,b; Adams et al ., 2000), we observed a significant increase in prodynorphin mRNAs after treatment with MET. Although the up‐regulation induced by a higher dose (15 mg/kg) was restricted to the caudate–putamen (Smith & McGinty, 1994; Adams et al ., 2000), the increase was also observed in the nucleus accumbens, as previously found with similar doses of MET (Wang & McGinty, 1995, 1996a,b). Whereas it potentiated the MET‐induced decrease of proenkephalin mRNAs, ciproxifan suppressed the MET‐induced up‐regulation of prodynorphin mRNAs in the same animals.…”

Differential Regulation of Striatal Preproenkephalin and Preprotachykinin mRNA Levels in MPTP‐Lesioned Monkeys Chronically Treated with Dopamine D1 or D2 Receptor Agonists

“…In fact, administration of the dopamine D 2 agonist cabergoline led to correction of PPE mRNA levels compared with the control, whereas elevated PPE mRNA levels observed in untreated MPTP‐lesioned monkeys were unaltered by continuous and further increased by pulsatile administration of the dopamine D 1 agonist SKF‐82958. This is consistent with previous studies using different dopamine D 1 (SKF‐38393) or D 2 (quinpirole) agonists administered in a pulsatile mode in 6‐OHDA‐denervated rats (Gerfen et al, 1990 ; Pollack and Wooten, 1992) as well as with those using selective dopamine D 1 (SCH23390) or D 2 (YM‐091510M and eticlopride) antagonists in normal rats (Morris et al, 1988 ; Morris and Hunt, 1991) and in rats treated with amphetamine or methamphetamine (Wang and McGinty, 1996 a ). Rats were killed 3 h after their last dopamine agonist treatment in the above references, whereas in our present results a 3‐day washout period was used ; the agreement between our findings and those above suggest that the changes of peptide expression are due to the agonist treatment rather than a consequence of its withdrawal, although we cannot totally rule out such a mechanism.…”

Microdialysis and mass spectrometric monitoring of dopamine and enkephalins in the globus pallidus reveal reciprocal interactions that regulate movement

“…Thus, DA acts at pre‐synaptic D 1 Rs on striatopallidal terminals to enhance GABA and ENK release and may be required to fine tune pallidal inhibition. These results are consistent with a previous study showing acute AMPH‐induced increases in PENK mRNA expression in striatal MSNs (Wang and McGinty 1996). Therefore, D 1 R stimulation facilitates ENK release and subsequent increases in PENK mRNA expression (Wang and McGinty 1996) possibly to maintain ENK stores.…”

Ciproxifan, a histamine H3‐receptor antagonist/inverse agonist, modulates the effects of methamphetamine on neuropeptide mRNA expression in rat striatum

“…As previously reported (Smith & McGinty, 1994; Wang & McGinty, 1995, 1996a,b; Adams et al ., 2000), we observed a significant increase in prodynorphin mRNAs after treatment with MET. Although the up‐regulation induced by a higher dose (15 mg/kg) was restricted to the caudate–putamen (Smith & McGinty, 1994; Adams et al ., 2000), the increase was also observed in the nucleus accumbens, as previously found with similar doses of MET (Wang & McGinty, 1995, 1996a,b). Whereas it potentiated the MET‐induced decrease of proenkephalin mRNAs, ciproxifan suppressed the MET‐induced up‐regulation of prodynorphin mRNAs in the same animals.…”

Differential Regulation of Striatal Preproenkephalin and Preprotachykinin mRNA Levels in MPTP‐Lesioned Monkeys Chronically Treated with Dopamine D1 or D2 Receptor Agonists

“…In fact, administration of the dopamine D 2 agonist cabergoline led to correction of PPE mRNA levels compared with the control, whereas elevated PPE mRNA levels observed in untreated MPTP‐lesioned monkeys were unaltered by continuous and further increased by pulsatile administration of the dopamine D 1 agonist SKF‐82958. This is consistent with previous studies using different dopamine D 1 (SKF‐38393) or D 2 (quinpirole) agonists administered in a pulsatile mode in 6‐OHDA‐denervated rats (Gerfen et al, 1990 ; Pollack and Wooten, 1992) as well as with those using selective dopamine D 1 (SCH23390) or D 2 (YM‐091510M and eticlopride) antagonists in normal rats (Morris et al, 1988 ; Morris and Hunt, 1991) and in rats treated with amphetamine or methamphetamine (Wang and McGinty, 1996 a ). Rats were killed 3 h after their last dopamine agonist treatment in the above references, whereas in our present results a 3‐day washout period was used ; the agreement between our findings and those above suggest that the changes of peptide expression are due to the agonist treatment rather than a consequence of its withdrawal, although we cannot totally rule out such a mechanism.…”