Effects of docosanyl ferulate, a constituent of Withania somnifera, on ethanol- and morphine-elicited conditioned place preference and ERK phosphorylation in the accumbens shell of CD1 mice.
Conditioned place preference
Docosanyl ferulate
ERK
Ethanol
Morphine
Withania somnifera
pERK
Journal
Psychopharmacology
ISSN: 1432-2072
Titre abrégé: Psychopharmacology (Berl)
Pays: Germany
ID NLM: 7608025
Informations de publication
Date de publication:
Mar 2022
Mar 2022
Historique:
received:
06
09
2021
accepted:
17
01
2022
pubmed:
29
1
2022
medline:
5
3
2022
entrez:
28
1
2022
Statut:
ppublish
Résumé
Docosanyl ferulate (DF) is a behaviourally active GABA The study aimed at determining (a) whether DF contributes to WSE's ability to affect the acquisition and expression of ethanol- and morphine-elicited CPP and, given that phosphorylation of extracellular signal-regulated kinase (pERK) in the AcbSh is involved in associative learning and motivated behaviours, (b) whether WSE and DF may affect ethanol- and morphine-induced ERKs phosphorylation in the AcbSh. In adult male CD1 mice, DF's effects on the acquisition and expression of ethanol- and morphine-elicited CPP were evaluated by a classical place conditioning paradigm, whereas the effects of WSE and DF on ethanol- and morphine-elicited pERK in the AcbSh were evaluated by immunohistochemistry. The study shows that DF, differently from WSE, affects only the acquisition but not the expression of ethanol- and morphine-induced CPP. Moreover, the study shows that both WSE and DF can prevent ethanol- and morphine-elicited pERK expression in the AcbSh. Overall, these results highlight subtle but critical differences for the role of GABA
Sections du résumé
BACKGROUND
BACKGROUND
Docosanyl ferulate (DF) is a behaviourally active GABA
AIMS
OBJECTIVE
The study aimed at determining (a) whether DF contributes to WSE's ability to affect the acquisition and expression of ethanol- and morphine-elicited CPP and, given that phosphorylation of extracellular signal-regulated kinase (pERK) in the AcbSh is involved in associative learning and motivated behaviours, (b) whether WSE and DF may affect ethanol- and morphine-induced ERKs phosphorylation in the AcbSh.
METHODS
METHODS
In adult male CD1 mice, DF's effects on the acquisition and expression of ethanol- and morphine-elicited CPP were evaluated by a classical place conditioning paradigm, whereas the effects of WSE and DF on ethanol- and morphine-elicited pERK in the AcbSh were evaluated by immunohistochemistry.
RESULTS AND CONCLUSIONS
CONCLUSIONS
The study shows that DF, differently from WSE, affects only the acquisition but not the expression of ethanol- and morphine-induced CPP. Moreover, the study shows that both WSE and DF can prevent ethanol- and morphine-elicited pERK expression in the AcbSh. Overall, these results highlight subtle but critical differences for the role of GABA
Identifiants
pubmed: 35088095
doi: 10.1007/s00213-022-06069-w
pii: 10.1007/s00213-022-06069-w
pmc: PMC8891193
doi:
Substances chimiques
Plant Extracts
0
Ethanol
3K9958V90M
Morphine
76I7G6D29C
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
795-806Informations de copyright
© 2022. The Author(s).
Références
Abrahao KP, Salinas AG, Lovinger DM (2017) Alcohol and the brain: neuronal molecular targets, synapses, and circuits. Neuron 96(6):1223–1238. https://doi.org/10.1016/j.neuron.2017.10.032
doi: 10.1016/j.neuron.2017.10.032
pubmed: 29268093
pmcid: 6566861
Acquas E, Di Chiara G (1994) D1 receptor blockade stereospecifically impairs the acquisition of drug-conditioned place preference and place aversion. Behav Pharmacol 5(6):555–569. https://doi.org/10.1097/00008877-199410000-00001
doi: 10.1097/00008877-199410000-00001
pubmed: 11224235
Acquas E, Pisanu A, Spiga S et al (2007) Differential effects of intravenous R, S-(±)-3,4 methylenedioxymethamphetamine (MDMA, Ecstasy) and its S(+)- and R(−)-enantiomers on dopamine transmission and extracellular signal regulated kinase phosphorylation (pERK) in the rat nucleus accumbens shell and core. J Neurochem 102:121–132. https://doi.org/10.1111/j.1471-4159.2007.04451.x
doi: 10.1111/j.1471-4159.2007.04451.x
pubmed: 17564678
Axley PD, Richardson CT, Singal AK (2019) Epidemiology of alcohol consumption and societal burden of alcoholism and alcoholic liver disease. Clin Liver Dis 23(1):39–50. https://doi.org/10.1016/j.cld.2018.09.011
doi: 10.1016/j.cld.2018.09.011
pubmed: 30454831
Bagherpasand N, Mehri S, JafariShahroudi M, Tabatabai SM, Khezri A, Fathi M, Abnous K, Imenshahidi M, Hosseinzadeh H (2019) Effect of topiramate on morphine-induced conditioned place preference (CPP) in rats: role of ERK and CREB proteins in hippocampus and cerebral cortex. Iran J Pharm Res. 18(4):2000–2010. https://doi.org/10.22037/ijpr.2019.1100873
doi: 10.22037/ijpr.2019.1100873
pubmed: 32184865
pmcid: 7059042
Bardo MT (1998) Neuropharmacological mechanisms of drug reward: beyond dopamine in the nucleus accumbens. Crit Rev Neurobiol 12(1–2):37–67. https://doi.org/10.1615/critrevneurobiol.v12.i1-2.30
doi: 10.1615/critrevneurobiol.v12.i1-2.30
pubmed: 9444481
Bassareo V, Talani G, Frau R et al (2019) Inhibition of morphine- and ethanol-mediated stimulation of mesolimbic dopamine neurons by Withania somnifera. Front Neurosci 13:545. https://doi.org/10.3389/fnins.2019.00545
doi: 10.3389/fnins.2019.00545
pubmed: 31275092
pmcid: 6593272
Bassareo V, Frau R, Maccioni R et al (2021) Ethanol-dependent synthesis of salsolinol in the posterior ventral tegmental area as key mechanism of ethanol’s action on mesolimbic dopamine. Front Neurosci 15:675061. https://doi.org/10.3389/fnins.2021.675061
doi: 10.3389/fnins.2021.675061
pubmed: 34262429
pmcid: 8273231
Bell-Horner CL, Dohi A, Nguyen Q et al (2006) ERK/MAPK pathway regulates GABAA receptors. J Neurobiol 66(13):1467–1474. https://doi.org/10.1002/neu.20327
doi: 10.1002/neu.20327
pubmed: 17013930
Benyamin R, Trescot AM, Datta S et al (2008) Opioid complications and side effects. Pain Physician 11(2 Suppl):S105–S120
doi: 10.36076/ppj.2008/11/S105
Berhow MT, Hiroi N, Nestler EJ (1996) Regulation of ERK (extracellular signal regulated kinase), part of the neurotrophin signal transduction cascade, in the rat mesolimbic dopamine system by chronic exposure to morphine or cocaine. J Neurosci 16(15):4707–4715. https://doi.org/10.1523/jneurosci.16-15-04707.1996
doi: 10.1523/jneurosci.16-15-04707.1996
pubmed: 8764658
pmcid: 6579030
Berke JD, Hyman SE (2000) Addiction, dopamine, and the molecular mechanisms of memory. Neuron 25(3):515–532. https://doi.org/10.1016/s0896-6273(00)81056-9
doi: 10.1016/s0896-6273(00)81056-9
pubmed: 10774721
Brami-Cherrier K, Valjent E, Hervé D et al (2006) Parsing molecular and behavioral effects of cocaine in mitogen- and stress-activated protein kinase-1-deficient mice. Neuroscience 25(49):11444–11454. https://doi.org/10.1523/jneurosci.1711-05.2005
doi: 10.1523/jneurosci.1711-05.2005
Chester JA, Cunningham CL (1999) GABA(A) receptors modulate ethanol-induced conditioned place preference and taste aversion in mice. Psychopharmacology 144(4):363–372. https://doi.org/10.1007/s002130051019
doi: 10.1007/s002130051019
pubmed: 10435409
Correa M, Salamone JD, Segovia KN et al (2012) Piecing together the puzzle of acetaldehyde as a neuroactive agent. Neurosci Biobehav Rev. 36(1):404–430. https://doi.org/10.1016/j.neubiorev.2011.07.009
doi: 10.1016/j.neubiorev.2011.07.009
pubmed: 21824493
Dar NJ, Hamid A, Ahmad M (2015) Pharmacological overview of Withania somnifera, the Indian Ginseng. Cell Mol Life Sci 72:4445–4460. https://doi.org/10.1007/s00018-015-2012-1
doi: 10.1007/s00018-015-2012-1
pubmed: 26306935
Di Chiara G (1998) A motivational learning hypothesis of the role of mesolimbic dopamine in compulsive drug use. J Psychopharmacol 12:54–67. https://doi.org/10.1177/026988119801200108
doi: 10.1177/026988119801200108
pubmed: 9584969
Di Chiara G (1999) Drug addiction as dopamine-dependent associative learning disorder. Eur J Pharmacol 375(1–3):13–30. https://doi.org/10.1016/s0014-2999(99)00372-6
doi: 10.1016/s0014-2999(99)00372-6
pubmed: 10443561
Di Chiara G, Bassareo V (2007) Reward system and addiction: what dopamine does and doesn’t do. Curr Opin Pharmacol 7(1):69–76. https://doi.org/10.1016/j.coph.2006.11.003
doi: 10.1016/j.coph.2006.11.003
pubmed: 17174602
Di Chiara G, Bassareo V, Fenu S et al (2004) Dopamine and drug addiction: the nucleus accumbens shell connection. Neuropharmacology 47(Suppl 1):227–241. https://doi.org/10.1016/j.neuropharm.2004.06.032
doi: 10.1016/j.neuropharm.2004.06.032
pubmed: 15464140
Fenu S, Spina L, Rivas E et al (2006) Morphine-conditioned single-trial place preference: role of nucleus accumbens shell dopamine receptors in acquisition, but not expression. Psychopharmacology 187(2):143–153. https://doi.org/10.1007/s00213-006-0415-2
doi: 10.1007/s00213-006-0415-2
pubmed: 16724186
Gerdjikov TV, Ross GM, Beninger RJ (2004) Place preference induced by nucleus accumbens amphetamine is impaired by antagonists of ERK or p38 MAP kinases in rats. Behav Neurosci 118:740–750. https://doi.org/10.1037/0735-7044.118.4.740
doi: 10.1037/0735-7044.118.4.740
pubmed: 15301601
Gupta GL, Rana AC (2008) Effect of Withania somnifera Dunal in ethanol-induced anxiolysis and withdrawal anxiety in rats. Indian J Exp Biol 46(6):470–475
pubmed: 18697607
Hodge CW, Chappelle AM, Samson HH (1995) GABAergic transmission in the nucleus accumbens is involved in the termination of ethanol self-administration in rats. Alcohol Clin Exp Res 19(6):1486–1493. https://doi.org/10.1111/j.1530-0277.1995.tb01012.x
doi: 10.1111/j.1530-0277.1995.tb01012.x
pubmed: 8749815
Ibba F, Vinci S, Spiga S et al (2009) Ethanol-induced extracellular signal regulated kinase: role of dopamine D1 receptors. Alcohol Clin Exp Res 33:858–867. https://doi.org/10.1111/j.1530-0277.2009.00907.x
doi: 10.1111/j.1530-0277.2009.00907.x
pubmed: 19320634
June HL, Devaraju SL, Eggers MW et al (1998) Benzodiazepine receptor antagonists modulate the actions of ethanol in alcohol-preferring and -nonpreferring rats. Eur J Pharmacol 342(2–3):139–151. https://doi.org/10.1016/s0014-2999(97)01489-1
doi: 10.1016/s0014-2999(97)01489-1
pubmed: 9548379
Kasture S, Vinci S, Ibba F et al (2009) Withania somnifera prevents morphine withdrawal-induced decrease in spine density in nucleus accumbens shell of rats: a confocal laser scanning microscopy study. Neurotox Res 16(4):343–355. https://doi.org/10.1007/s12640-009-9069-2
doi: 10.1007/s12640-009-9069-2
pubmed: 19551457
Koob GF (2006) The neurobiology of addiction: a neuroadaptational view relevant for diagnosis. Addiction 101(Suppl 1):23–30. https://doi.org/10.1111/j.1360-0443.2006.01586.x
doi: 10.1111/j.1360-0443.2006.01586.x
pubmed: 16930158
Koob GF, Le Moal M (2001) Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 2:97–129. https://doi.org/10.1016/s0893-133x(00)00195-0
doi: 10.1016/s0893-133x(00)00195-0
Kulkarni SK, Ninan I (1997) Inhibition of morphine tolerance and dependence by Withania somnifera in mice. J Ethnopharmacol 57(3):213–217. https://doi.org/10.1016/s0378-8741(97)00064-0
doi: 10.1016/s0378-8741(97)00064-0
pubmed: 9292416
Lin X, Wang Q, Ji J et al (2010) Role of MEK-ERK pathway in morphine-induced conditioned place preference in ventral tegmental area of rats. J Neurosci Res. 88(7):1595–604. https://doi.org/10.1002/jnr.22326
doi: 10.1002/jnr.22326
pubmed: 20091775
Lu L, Koya E, Zhai H et al (2006) Role of ERK in cocaine addiction. Trends Neurosci 29:695–703. https://doi.org/10.1016/j.tins.2006.10.005
doi: 10.1016/j.tins.2006.10.005
pubmed: 17084911
Maccioni R, Setzu MD, Talani G et al (2018) Standardized phytotherapic extracts rescue anomalous locomotion and electrophysiological responses of TDP-43 Drosophila melanogaster model of ALS. Sci Rep 8(1):16002. https://doi.org/10.1038/s41598-018-34452-1
doi: 10.1038/s41598-018-34452-1
pubmed: 30375462
pmcid: 6207707
Maccioni R, Cottiglia F, Maccioni E et al (2021) The biologically active compound of Withania somnifera (L.) Dunal, docosanyl ferulate, is endowed with potent anxiolytic properties but devoid of typical benzodiazepine-like side effects. J Psychopharmacol. 3:2698811211008588. https://doi.org/10.1177/02698811211008588
doi: 10.1177/02698811211008588
Marotta R, Fenu S, Scheggi S, Vinci S, Rosas M, Falqui A, Gambarana C, De Montis MG, Acquas E (2014) Acquisition and expression of conditioned taste aversion differentially affects extracellular signal regulated kinase and glutamate receptor phosphorylation in rat prefrontal cortex and nucleus accumbens. Frontiers in Behavioral Neuroscience 8. https://doi.org/10.3389/fnbeh.2014.00153
Mazzucchelli C, Vantaggiato C, Ciamei A et al (2002) Knockout of ERK1 MAP kinase enhances synaptic plasticity in the striatum and facilitates striatal-mediated learning and memory. Neuron 34(5):807–820. https://doi.org/10.1016/s0896-6273(02)00716-x
doi: 10.1016/s0896-6273(02)00716-x
pubmed: 12062026
Muller DL, Unterwald EM (2004) In vivo regulation of extracellular signal-regulated protein kinase (ERK) and protein kinase B (Akt) phosphorylation by acute and chronic morphine. J Pharmacol Exp Ther 310(2):774–782. https://doi.org/10.1124/jpet.104.066548
doi: 10.1124/jpet.104.066548
pubmed: 15056728
Nestler EJ (2001) Molecular neurobiology of addiction. Am J Addict 10:201–217. https://doi.org/10.1080/105504901750532094
doi: 10.1080/105504901750532094
pubmed: 11579619
Nutt DJ, Blier P (2016) Neuroscience-based Nomenclature (NbN) for Journal of Psychopharmacology. J Psychopharmacol 30:413–415. https://doi.org/10.1177/0269881116642903
doi: 10.1177/0269881116642903
pubmed: 27098017
Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, 2nd edn. Academic, Sydney
Peana AT, Muggironi G, Spina L et al (2014) Effects of Withania somnifera on oral ethanol self-administration in rats. Behav Pharmacol 25(7):618–628. https://doi.org/10.1097/fbp.0000000000000078
doi: 10.1097/fbp.0000000000000078
pubmed: 25115596
Porru S, Maccioni R, Bassareo V et al (2020) Effects of caffeine on ethanol-elicited place preference, place aversion and ERK phosphorylation in CD-1 mice. J Psychopharmacol 12:1357–1370. https://doi.org/10.1177/0269881120965892
doi: 10.1177/0269881120965892
Porru S, López-Cruz L, Carratalá-Ros C et al (2021) Impact of caffeine on ethanol-induced stimulation and sensitization: changes in ERK and DARPP-32 phosphorylation in nucleus accumbens. Alcohol Clin Exp Res 45(3):608–619. https://doi.org/10.1111/acer.14553
doi: 10.1111/acer.14553
pubmed: 33471948
Rehm J, Gmel GE, Gmel G et al (2017) The relationship between different dimensions of alcohol use and the burden of disease-an update. Addiction 112:968. https://doi.org/10.1111/add.13757
doi: 10.1111/add.13757
pubmed: 28220587
pmcid: 5434904
Rosas M, Porru S, Fenu S et al (2016) Role of nucleus accumbens μ opioid receptors in the effects of morphine on ERK1/2 phosphorylation. Psychopharmacology 233(15–16):2943–2954. https://doi.org/10.1007/s00213-016-4340-8
doi: 10.1007/s00213-016-4340-8
pubmed: 27245230
Rosas M, Porru S, Longoni R et al (2017) Differential effects of the MEK inhibitor SL327 on the acquisition and expression of ethanol-elicited conditioned place preference and aversion in mice. J Psychopharmacol 31(1):105–114. https://doi.org/10.1177/0269881116675514
doi: 10.1177/0269881116675514
pubmed: 28072036
Rosas M, Porru S, Sabariego M et al (2018) Effects of morphine on place conditioning and ERK1/2 phosphorylation in the nucleus accumbens of psychogenetically selected Roman low- and high-avoidance rats. Psychopharmacology 235:59–69. https://doi.org/10.1007/s00213-017-4740-4
doi: 10.1007/s00213-017-4740-4
pubmed: 28971231
Ruiu S, Longoni R, Spina L et al (2013) Withania somnifera prevents acquisition and expression of morphine-elicited conditioned place preference. Behav Pharmacol 24(2):133–143. https://doi.org/10.1097/fbp.0b013e32835f3d15
doi: 10.1097/fbp.0b013e32835f3d15
pubmed: 23455447
Salzmann J, Marie-Claire C, Le Guen S et al (2003) Importance of ERK activation in behavioral and biochemical effects induced by MDMA in mice. Br J Pharmacol 140:831–838. https://doi.org/10.1016/j.ejphar.2005.09.012
doi: 10.1016/j.ejphar.2005.09.012
pubmed: 14517176
pmcid: 1574098
Singh N, Bhalla M, de Jager P et al (2011) An overview on ashwagandha: a Rasayana (rejuvenator) of Ayurveda. Afr J Tradit Complement Altern Med 8(5 Suppl):208–213. https://doi.org/10.4314/ajtcam.v8i5s.9
doi: 10.4314/ajtcam.v8i5s.9
pubmed: 22754076
pmcid: 3252722
Smith JP, Book SW (2008) Anxiety and substance use disorders: a review. Psychiatr times 25(10):19–23
pubmed: 20640182
pmcid: 2904966
Sonar VP, Fois B, Distinto S et al (2019) Ferulic acid esters and withanolides: in search of Withania somnifera GABAA receptor modulators. J Nat Prod 82:1250–1257. https://doi.org/10.1021/acs.jnatprod.8b01023
doi: 10.1021/acs.jnatprod.8b01023
pubmed: 30998355
Spina L, Longoni R, Vinci S et al (2010) Role of dopamine D1 receptors and extracellular signal regulated kinase in the motivational properties of acetaldehyde as assessed by place preference conditioning. Alcohol Clin Exp Res 34:607–616. https://doi.org/10.1111/j.1530-0277.2009.01129.x
doi: 10.1111/j.1530-0277.2009.01129.x
pubmed: 20102564
Spina L, Longoni R, Rosas M et al (2015) Withania somnifera Dunal (Indian ginseng) impairs acquisition and expression of ethanol-elicited conditioned place preference and conditioned place aversion. J Psychopharmacol 29:1191–1199. https://doi.org/10.1177/0269881115600132
doi: 10.1177/0269881115600132
pubmed: 26349555
Sweatt JD (2004) Mitogen-activated protein kinases in synaptic plasticity and memory. Curr Opin Neurobiol 14:311–317. https://doi.org/10.1016/j.conb.2004.04.001
doi: 10.1016/j.conb.2004.04.001
pubmed: 15194111
Tzschentke TM (2007) Measuring reward with the conditioned place preference (CPP) paradigm: Update of the last decade. Addict Biol 12:227–462. https://doi.org/10.1111/j.1369-1600.2007.00070.x
doi: 10.1111/j.1369-1600.2007.00070.x
Valjent E, Corvol J, Page C et al (2000) Involvement of the extracellular signal-regulated kinase cascade for cocaine-rewarding properties. J Neurosci 20:8701–8709. https://doi.org/10.1523/jneurosci.20-23-08701.2000
doi: 10.1523/jneurosci.20-23-08701.2000
pubmed: 11102476
pmcid: 6773075
Valjent E, Caboche J, Vanhoutte P (2001) Mitogen-activated protein kinase/extracellular signal-regulated kinase induced gene regulation in brain. Mol Neurobiol 23:83–99. https://doi.org/10.1385/mn:23:2-3:083
doi: 10.1385/mn:23:2-3:083
pubmed: 11817219
Valjent E, Pagès C, Hervé D et al (2004) Addictive and non-addictive drugs induce distinct and specific patterns of ERK activation in mouse brain. Eur J Neurosci 19(7):1826–1836. https://doi.org/10.1111/j.1460-9568.2004.03278.x
doi: 10.1111/j.1460-9568.2004.03278.x
pubmed: 15078556
Valjent E, Pascoli V, Corvol J et al (2005) Regulation of a protein phosphatase cascade allows convergent dopamine and glutamate signals to activate ERK in the striatum. PNAS 102:491–496. https://doi.org/10.1073/pnas.0408305102
doi: 10.1073/pnas.0408305102
pubmed: 15608059
Volkow ND, Morales M (2015) The brain on drugs: from reward to addiction. Cell 162(4):712–25. https://doi.org/10.1016/j.cell.2015.07.046
doi: 10.1016/j.cell.2015.07.046
pubmed: 26276628
pmcid: 26276628
Zhang J, Wang N, Chen B, Wang Y, He J, Cai X, Zhang H, Wei S, Li S (2016) Blockade of Cannabinoid CB1 receptor attenuates the acquisition of morphine-induced conditioned place preference along with a downregulation of ERK, CREB phosphorylation, and BDNF expression in the nucleus accumbens and hippocampus. Neurosci Lett 630:70–76. https://doi.org/10.1016/j.neulet.2016.07.047
doi: 10.1016/j.neulet.2016.07.047
pubmed: 27461790