Kappa opioid receptor agonist U50,488 inhibits dopamine more in caudal than rostral nucleus accumbens core.
U50,488
dopamine
kappa opioid receptors
nucleus accumbens core
rostro-caudal
Journal
Basic & clinical pharmacology & toxicology
ISSN: 1742-7843
Titre abrégé: Basic Clin Pharmacol Toxicol
Pays: England
ID NLM: 101208422
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
revised:
07
06
2023
received:
04
03
2023
accepted:
14
07
2023
pubmed:
4
8
2023
medline:
4
8
2023
entrez:
4
8
2023
Statut:
ppublish
Résumé
The nucleus accumbens (NAc) core is involved in regulating stress and shaping reward seeking behaviours. Multiple neuromodulators, including dynorphin/kappa opioid receptor (KOR) and dopamine systems, converge in this area to influence behavioural outcomes. KOR activation acutely inhibits dopamine release and chronically depresses overall dopamine transmission. Recently, studies in the NAc shell have revealed that the impact of KOR activation on behaviour is regionally specific, and these rostro-caudal differences are likely driven by greater control of KORs over dopamine inhibition in the caudal compared with rostral subregion. Given the importance of NAc core, particularly the interaction between KORs and dopamine in regulating reward seeking behaviours, we examined the impact of KOR activation on dopamine release and uptake along the rostro-caudal axis in the NAc core of male and female mice. Using ex vivo fast scan cyclic voltammetry, we observed that KOR mediated inhibition of dopamine release was significantly greater in caudal compared with rostral NAc core with no significant sex differences observed. These data suggest that KORs regulate dopamine release differentially along the rostro-caudal axis, providing a new axis on which to examine the process by which the KOR/dopamine system controls reward encoding.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
526-534Subventions
Organisme : NIH HHS
ID : K01AA023874
Pays : United States
Organisme : NIH HHS
ID : P50AA026117
Pays : United States
Organisme : NIH HHS
ID : R01AA028228
Pays : United States
Organisme : NIH HHS
ID : T32AA007565
Pays : United States
Organisme : NIH HHS
ID : U01AA014091
Pays : United States
Organisme : NIH HHS
ID : T32DA041349
Pays : United States
Organisme : NIH HHS
ID : R01DA048490
Pays : United States
Organisme : NIH HHS
ID : R01DA054694
Pays : United States
Organisme : NIH HHS
ID : K01AA023874
Pays : United States
Organisme : NIH HHS
ID : P50AA026117
Pays : United States
Organisme : NIH HHS
ID : R01AA028228
Pays : United States
Organisme : NIH HHS
ID : T32AA007565
Pays : United States
Organisme : NIH HHS
ID : U01AA014091
Pays : United States
Organisme : NIH HHS
ID : T32DA041349
Pays : United States
Organisme : NIH HHS
ID : R01DA048490
Pays : United States
Organisme : NIH HHS
ID : R01DA054694
Pays : United States
Informations de copyright
© 2023 The Authors. Basic & Clinical Pharmacology & Toxicology published by John Wiley & Sons Ltd on behalf of Nordic Association for the Publication of BCPT (former Nordic Pharmacological Society).
Références
Britt JP, Benaliouad F, McDevitt RA, Stuber GD, Wise RA, Bonci A. Synaptic and behavioral profile of multiple glutamatergic inputs to the nucleus accumbens. Neuron. 2012;76(4):790-803. doi:10.1016/j.neuron.2012.09.040
Ma L, Chen W, Yu D, Han Y. Brain-wide mapping of afferent inputs to accumbens nucleus core subdomains and accumbens nucleus subnuclei. Front Syst Neurosci. 2020;14:14. doi:10.3389/fnsys.2020.00015
Tejeda HA, Wu J, Kornspun AR, et al. Pathway- and cell-specific kappa-opioid receptor modulation of excitation-inhibition balance differentially gates D1 and D2 accumbens neuron activity. Neuron. 2017;93(1):147-163. doi:10.1016/j.neuron.2016.12.005
Van Bockstaele EJ, Biswas A, Pickel VM. Topography of serotonin neurons in the dorsal raphe nucleus that send axon collaterals to the rat prefrontal cortex and nucleus accumbens. Brain Res. 1993;624(1):188-198. doi:10.1016/0006-8993(93)90077-Z
Aitken TJ, Greenfield VY, Wassum KM. Nucleus accumbens core dopamine signaling tracks the need-based motivational value of food-paired cues. J Neurochem. 2016;136(5):1026-1036. doi:10.1111/jnc.13494
Di Chiara G. Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav Brain Res. 2002;137(1-2):75-114. doi:10.1016/s0166-4328(02)00286-3
Mohebi A, Pettibone JR, Hamid AA, et al. Dissociable dopamine dynamics for learning and motivation. Nature. 2019;570(7759):65-70. doi:10.1038/s41586-019-1235-y
West EA, Carelli RM. Nucleus accumbens core and shell differentially encode reward-associated cues after reinforcer devaluation. J Neurosci. 2016;36(4):1128-1139. doi:10.1523/JNEUROSCI.2976-15.2016
Margolis EB, Karkhanis AN. Dopaminergic cellular and circuit contributions to kappa opioid receptor mediated aversion. Neurochem Int. 2019;129:104504. doi:10.1016/j.neuint.2019.104504
Van Bockstaele EJ, Gracy KN, Pickel VM. Dynorphin-immunoreactive neurons in the rat nucleus accumbens: ultrastructure and synaptic input from terminals containing substance P and/or dynorphin. J Comp Neurol. 1995;351(1):117-133. doi:10.1002/cne.903510111
Caputi FF, Caffino L, Candeletti S, Fumagalli F, Romualdi P. Short-term withdrawal from repeated exposure to cocaine during adolescence modulates dynorphin mRNA levels and BDNF signaling in the rat nucleus accumbens. Drug Alcohol Depend. 2019;197:127-133. doi:10.1016/j.drugalcdep.2019.01.006
Marinelli PW, Lam M, Bai L, Quirion R, Gianoulakis C. A microdialysis profile of dynorphin A(1-8) release in the rat nucleus accumbens following alcohol administration. Alcohol Clin Exp Res. 2006;30(6):982-990. doi:10.1111/j.1530-0277.2006.00112.x
Shirayama Y, Ishida H, Iwata M, Hazama GI, Kawahara R, Duman RS. Stress increases dynorphin immunoreactivity in limbic brain regions and dynorphin antagonism produces antidepressant-like effects. J Neurochem. 2004;90(5):1258-1268. doi:10.1111/j.1471-4159.2004.02589.x
Chavkin C, James IF, Goldstein A. Dynorphin is a specific endogenous ligand of the kappa opioid receptor. Science. 1982;215(4531):413-415. doi:10.1126/science.6120570
Cox BM. Recent developments in the study of opioid receptors. Mol Pharmacol. 2013;83(4):723-728. doi:10.1124/mol.112.083279
Hjelmstad GO, Fields HL. Kappa opioid receptor inhibition of glutamatergic transmission in the nucleus accumbens shell. J Neurophysiol. 2001;85(3):1153-1158. doi:10.1152/jn.2001.85.3.1153
Spanagel R, Herz A, Shippenberg TS. Opposing tonically active endogenous opioid systems modulate the mesolimbic dopaminergic pathway. Proc Natl Acad Sci. 1992;89(6):2046-2050. doi:10.1073/pnas.89.6.2046
Svingos AL, Chavkin C, Colago EE, Pickel VM. Major coexpression of kappa-opioid receptors and the dopamine transporter in nucleus accumbens axonal profiles. Synap N Y N. 2001;42(3):185-192. doi:10.1002/syn.10005
Di Chiara G, Imperato A. Opposite effects of mu and kappa opiate agonists on dopamine release in the nucleus accumbens and in the dorsal caudate of freely moving rats. J Pharmacol Exp Ther. 1988;244(3):1067-1080.
Ebner SR, Roitman MF, Potter DN, Rachlin AB, Chartoff EH. Depressive-like effects of the kappa opioid receptor agonist salvinorin A are associated with decreased phasic dopamine release in the nucleus accumbens. Psychopharmacology (Berl). 2010;210(2):241-252. doi:10.1007/s00213-010-1836-5
Ehrich JM, Messinger DI, Knakal CR, et al. Kappa opioid receptor-induced aversion requires p38 MAPK activation in VTA dopamine neurons. J Neurosci. 2015;35(37):12917-12931. doi:10.1523/JNEUROSCI.2444-15.2015
Karkhanis AN, Huggins KN, Rose JH, Jones SR. Switch from excitatory to inhibitory actions of ethanol on dopamine levels after chronic exposure: role of kappa opioid receptors. Neuropharmacology. 2016;110(Pt A):190-197. doi:10.1016/j.neuropharm.2016.07.022
Karkhanis AN, Rose JH, Weiner JL, Jones SR. Early-life social isolation stress increases kappa opioid receptor responsiveness and downregulates the dopamine system. Neuropsychopharmacology. 2016;41(9):2263-2274. doi:10.1038/npp.2016.21
Rose JH, Karkhanis AN, Chen R, et al. Supersensitive kappa opioid receptors promotes ethanol withdrawal-related behaviors and reduce dopamine signaling in the nucleus accumbens. Int J Neuropsychopharmacol. 2016;19(5):pyv127. doi:10.1093/ijnp/pyv127
Kivell B, Uzelac Z, Sundaramurthy S, et al. Salvinorin A regulates dopamine transporter function via a kappa opioid receptor and ERK1/2-dependent mechanism. Neuropharmacology. 2014;86:228-240. doi:10.1016/j.neuropharm.2014.07.016
Thompson AC, Zapata A, Justice JB, Vaughan RA, Sharpe LG, Shippenberg TS. Kappa-opioid receptor activation modifies dopamine uptake in the nucleus accumbens and opposes the effects of cocaine. J Neurosci. 2000;20(24):9333-9340. doi:10.1523/JNEUROSCI.20-24-09333.2000
Escobar AP, González MP, Meza RC, et al. Mechanisms of kappa opioid receptor potentiation of dopamine D2 receptor function in quinpirole-induced locomotor sensitization in rats. Int J Neuropsychopharmacol. 2017;20(8):660-669. doi:10.1093/ijnp/pyx042
Chartoff EH, Ebner SR, Sparrow A, et al. Relative timing between kappa opioid receptor activation and cocaine determines the impact on reward and dopamine release. Neuropsychopharmacology. 2016;41(4):989-1002. doi:10.1038/npp.2015.226
Ehrich JM, Phillips PEM, Chavkin C. Kappa opioid receptor activation potentiates the cocaine-induced increase in evoked dopamine release recorded in vivo in the mouse nucleus accumbens. Neuropsychopharmacology. 2014;39(13):3036-3048. doi:10.1038/npp.2014.157
Land BB, Bruchas MR, Lemos JC, Xu M, Melief EJ, Chavkin C. The dysphoric component of stress is encoded by activation of the dynorphin kappa-opioid system. J Neurosci. 2008;28(2):407-414. doi:10.1523/JNEUROSCI.4458-07.2008
Groblewski PA, Zietz C, Willuhn I, Phillips PEM, Chavkin C. Repeated stress exposure causes strain-dependent shifts in the behavioral economics of cocaine in rats. Addict Biol. 2015;20(2):297-301. doi:10.1111/adb.12123
McLaughlin JP, Li S, Valdez J, Chavkin TA, Chavkin C. Social defeat stress-induced behavioral responses are mediated by the endogenous kappa opioid system. Neuropsychopharmacology. 2006;31(6):1241-1248. doi:10.1038/sj.npp.1300872
Conway SM, Puttick D, Russell S, Potter D, Roitman MF, Chartoff EH. Females are less sensitive than males to the motivational- and dopamine-suppressing effects of kappa opioid receptor activation. Neuropharmacology. 2019;146:231-241. doi:10.1016/j.neuropharm.2018.12.002
Chartoff EH, Mavrikaki M. Sex differences in kappa opioid receptor function and their potential impact on addiction. Front Neurosci. 2015;9:466. doi:10.3389/fnins.2015.00466
Morales M, Anderson RI, Spear LP, Varlinskaya EI. Effects of the kappa opioid receptor antagonist, nor-binaltorphimine, on ethanol intake: impact of age and sex. Dev Psychobiol. 2014;56(4):700-712. doi:10.1002/dev.21137
Castro DC, Berridge KC. Opioid hedonic hotspot in nucleus accumbens shell: mu, delta, and kappa maps for enhancement of sweetness “liking” and “wanting”. J Neurosci. 2014;34(12):4239-4250. doi:10.1523/JNEUROSCI.4458-13.2014
Al-Hasani R, McCall JG, Shin G, et al. Distinct subpopulations of nucleus accumbens dynorphin neurons drive aversion and reward. Neuron. 2015;87(5):1063-1077. doi:10.1016/j.neuron.2015.08.019
Pirino BE, Spodnick MB, Gargiulo AT, Curtis GR, Barson JR, Karkhanis AN. Kappa-opioid receptor-dependent changes in dopamine and anxiety-like or approach-avoidance behavior occur differentially across the nucleus accumbens shell rostro-caudal axis. Neuropharmacology. 2020;181:108341. doi:10.1016/j.neuropharm.2020.108341
Tveden-Nyborg P, Bergmann TK, Jessen N, Simonsen U, Lykkesfeldt J. BCPT policy for experimental and clinical studies. Basic Clin Pharmacol Toxicol. 2021;128(1):4-8. doi:10.1111/bcpt.13492
Von Voigtlander PF, Lewis RA. U-50,488, a selective kappa opioid agonist: comparison to other reputed kappa agonists. Prog Neuropsychopharmacol Biol Psychiatry. 1982;6(4-6):467-470. doi:10.1016/s0278-5846(82)80130-9
Vonvoigtlander PF, Lahti RA, Ludens JH. U-50,488: a selective and structurally novel non-mu (kappa) opioid agonist. J Pharmacol Exp Ther. 1983;224(1):7-12.
John CE, Jones SR. Voltammetric characterization of the effect of monoamine uptake inhibitors and releasers on dopamine and serotonin uptake in mouse caudate-putamen and substantia nigra slices. Neuropharmacology. 2007;52(8):1596-1605. doi:10.1016/j.neuropharm.2007.03.004
Franklin KB, Paxinos G. The mouse brain in stereotaxic coordinates. Third ed. Elsevier; 2007.
Spodnick MB, Amirault RT, Towner TT, Varlinskaya EI, Spear LP, Karkhanis AN. Adolescent intermittent ethanol exposure effects on kappa opioid receptor mediated dopamine transmission: sex and age of exposure matter. Brain Sci. 2020;10(8):472. doi:10.3390/brainsci10080472
Yorgason JT, España RA, Jones SR. Demon voltammetry and analysis software: analysis of cocaine-induced alterations in dopamine signaling using multiple kinetic measures. J Neurosci Methods. 2011;202(2):158-164. doi:10.1016/j.jneumeth.2011.03.001
Everett AC, Graul BE, Ronström JW, et al. Effectiveness and relationship between biased and unbiased measures of dopamine release and clearance. ACS Chem Nerosci. 2022;13(10):1534-1548. doi:10.1021/acschemneuro.2c00033
Poulin JF, Caronia G, Hofer C, et al. Mapping projections of molecularly defined dopamine neuron subtypes using intersectional genetic approaches. Nat Neurosci. 2018;21(9):1260-1271. doi:10.1038/s41593-018-0203-4
Pitts EG, Stowe TA, Christensen BA, Ferris MJ. Comparing dopamine release, uptake, and D2 autoreceptor function across the ventromedial to dorsolateral striatum in adolescent and adult male and female rats. Neuropharmacology. 2020;175:108163. doi:10.1016/j.neuropharm.2020.108163
Walker QD, Rooney MB, Wightman RM, Kuhn CM. Dopamine release and uptake are greater in female than male rat striatum as measured by fast cyclic voltammetry. Neuroscience. 2000;95(4):1061-1070. doi:10.1016/s0306-4522(99)00500-x
Jameson AN, Siemann JK, Melchior J, Calipari ES, McMahon DG, Grueter BA. Photoperiod impacts nucleus accumbens dopamine dynamics. eNeuro. 2023;10(2):ENEURO.0361-22.2023. doi:10.1523/ENEURO.0361-22.2023
Dhawan BN, Cesselin F, Raghubir R, et al. International Union of Pharmacology. XII. Classification of opioid receptors. Pharmacol Rev. 1996;48(4):567-592.
Xu W, Yoon SI, Huang P, et al. Localization of the κ opioid receptor in lipid rafts. J Pharmacol Exp Ther. 2006;317(3):1295-1306. doi:10.1124/jpet.105.099507
Yan F, Mosier PD, Westkaemper RB, Roth BL. Gα-subunits differentially alter the conformation and agonist affinity of κ-opioid receptors. Biochemistry. 2008;47(6):1567-1578. doi:10.1021/bi701476b
Russell SE, Rachlin AB, Smith KL, et al. Sex differences in sensitivity to the depressive-like effects of the kappa opioid receptor agonist U-50488 in rats. Biol Psychiatry. 2014;76(3):213-222. doi:10.1016/j.biopsych.2013.07.042
Abraham AD, Schattauer SS, Reichard KL, et al. Estrogen regulation of GRK2 inactivates kappa opioid receptor signaling mediating analgesia, but not aversion. J Neurosci. 2018;38(37):8031-8043. doi:10.1523/JNEUROSCI.0653-18.2018
Castro DC, Bruchas MR. A motivational and neuropeptidergic hub: anatomical and functional diversity within the nucleus accumbens shell. Neuron. 2019;102(3):529-552. doi:10.1016/j.neuron.2019.03.003