Adolescent self-administration of the synthetic cannabinoid receptor agonist JWH-018 induces neurobiological and behavioral alterations in adult male mice.
Chemokines
Cytokines
GFAP
IBA-1
Neuroinflammation
Synthetic cannabinoid receptor agonist
Journal
Psychopharmacology
ISSN: 1432-2072
Titre abrégé: Psychopharmacology (Berl)
Pays: Germany
ID NLM: 7608025
Informations de publication
Date de publication:
Oct 2022
Oct 2022
Historique:
received:
17
01
2022
accepted:
10
07
2022
pubmed:
10
8
2022
medline:
21
9
2022
entrez:
9
8
2022
Statut:
ppublish
Résumé
The use of synthetic cannabinoid receptor agonists (SCRAs) is growing among adolescents, posing major medical and psychiatric risks. JWH-018 represents the reference compound of SCRA-containing products. This study was performed to evaluate the enduring consequences of adolescent voluntary consumption of JWH-018. The reinforcing properties of JWH-018 were characterized in male CD1 adolescent mice by intravenous self-administration (IVSA). Afterwards, behavioral, neurochemical, and molecular evaluations were performed at adulthood. Adolescent mice acquired operant behavior (lever pressing, Fixed Ratio 1-3; 7.5 µg/kg/inf); this behavior was specifically directed at obtaining JWH-018 since it increased under Progressive Ratio schedule of reinforcement, and was absent in vehicle mice. JWH-018 IVSA was reduced by pretreatment of the CB1-antagonist/inverse agonist AM251. Adolescent exposure to JWH-018 by IVSA increased, at adulthood, both nestlet shredding and marble burying phenotypes, suggesting long-lasting repetitive/compulsive-like behavioral effects. JWH-018 did not affect risk proclivity in the wire-beam bridge task. In adult brains, there was an increase of ionized calcium binding adaptor molecule 1 (IBA-1) positive cells in the caudate-putamen (CPu) and nucleus accumbens (NAc), along with a decrease of glial fibrillary acidic protein (GFAP) immunoreactivity in the CPu. These glial alterations in adult brains were coupled with an increase of the chemokine RANTES and a decrease of the cytokines IL2 and IL13 in the cortex, and an increase of the chemokine MPC1 in the striatum. This study suggests for the first time that male mice self-administer the prototypical SCRA JWH-018 during adolescence. The adolescent voluntary consumption of JWH-018 leads to long-lasting behavioral and neurochemical aberrations along with glia-mediated inflammatory responses in adult brains.
Identifiants
pubmed: 35943523
doi: 10.1007/s00213-022-06191-9
pii: 10.1007/s00213-022-06191-9
pmc: PMC9481487
doi:
Substances chimiques
Cannabinoid Receptor Agonists
0
Chemokine CCL5
0
Glial Fibrillary Acidic Protein
0
Indoles
0
Interleukin-13
0
Interleukin-2
0
Naphthalenes
0
Receptor, Cannabinoid, CB1
0
1-pentyl-3-(1-naphthoyl)indole
G391998J57
Calcium Carbonate
H0G9379FGK
Calcium
SY7Q814VUP
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3083-3102Commentaires et corrections
Type : ErratumIn
Informations de copyright
© 2022. The Author(s).
Références
Angoa-Pérez M, Kane MJ, Briggs DI et al (2013) Mephedrone does not damage dopamine nerve endings of the striatum, but enhances the neurotoxicity of methamphetamine, amphetamine, and MDMA. J Neurochem 125:102–110. https://doi.org/10.1111/jnc.12114
doi: 10.1111/jnc.12114
pubmed: 23205838
pmcid: 3604033
Araque A, Carmignoto G, Haydon PG et al (2014) Gliotransmitters travel in time and space. Neuron 81:728–739. https://doi.org/10.1016/j.neuron.2014.02.007
doi: 10.1016/j.neuron.2014.02.007
pubmed: 24559669
pmcid: 4107238
Atwood BK, Huffman J, Straiker A, MacKie K (2010) JWH018, a common constituent of “Spice” herbal blends, is a potent and efficacious cannabinoid CB1 receptor agonist. Br J Pharmacol 160:585–593. https://doi.org/10.1111/j.1476-5381.2009.00582.x
doi: 10.1111/j.1476-5381.2009.00582.x
pubmed: 20100276
pmcid: 2931559
Bayazit H, Selek S, Karababa IF et al (2017) Evaluation of oxidant/antioxidant status and cytokine levels in patients with cannabis use disorder. Clin Psychopharmacol Neurosci 15:237–242. https://doi.org/10.9758/cpn.2017.15.3.237
doi: 10.9758/cpn.2017.15.3.237
pubmed: 28783932
pmcid: 5565077
Becker MP, Collins PF, Schultz A et al (2018) Longitudinal changes in cognition in young adult cannabis users. J Clin Exp Neuropsychol 40:529–543. https://doi.org/10.1080/13803395.2017.1385729
doi: 10.1080/13803395.2017.1385729
pubmed: 29058519
Bhatt HK, Song D, Musgrave G, Rao PSS (2021) Cannabinoid-induced changes in the immune system: the role of microRNAs. Int Immunopharmacol 98:107832. https://doi.org/10.1016/j.intimp.2021.107832
doi: 10.1016/j.intimp.2021.107832
pubmed: 34107381
Bisogno T, Di Marzo V (2010) Cannabinoid receptors and endocannabinoids: role in neuroinflammatory and neurodegenerative disorders. CNS Neurol Disord Drug Targets 9(5):564–573. https://doi.org/10.2174/187152710793361568
doi: 10.2174/187152710793361568
pubmed: 20632970
Bortolato M, Godar SC, Davarian S, Chen K, Shih JC (2009) Behavioral disinhibition and reduced anxiety-like behaviors in monoamine oxidase B-deficient mice.Neuropsychopharmacology 34(13):2746–2757. https://doi.org/10.1038/npp.2009.118
Castelli MP, Madeddu C, Casti A et al (2014) Δ9-Tetrahydrocannabinol prevents methamphetamine-induced neurotoxicity. PLoS ONE 9:1–11. https://doi.org/10.1371/journal.pone.0098079
doi: 10.1371/journal.pone.0098079
Cha HJ, Seong YH, Song MJ et al (2015) Neurotoxicity of synthetic cannabinoids JWH-081 and JWH-210. Biomol Ther 23:597–603. https://doi.org/10.4062/biomolther.2015.057
doi: 10.4062/biomolther.2015.057
Chambers RA, Taylor JR, Potenza MN (2003) Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability. Am J Psychiatry 160:1041–1052. https://doi.org/10.1176/appi.ajp.160.6.1041
doi: 10.1176/appi.ajp.160.6.1041
pubmed: 12777258
pmcid: 2919168
Claus ED, Feldstein Ewing SW, Magnan RE, Montanaro E, Hutchison KE, Bryan AD (2018) Neural mechanisms of risky decision making in adolescents reporting frequent alcohol and/or marijuana use. Brain Imaging Behav 12:564–576. https://doi.org/10.1007/s11682-017-9723-x
Clayton HB, Lowry R, Ashley C et al (2017) Health risk behaviors with synthetic cannabinoids versus Marijuana. Pediatrics 139:e20162675. https://doi.org/10.1542/peds.2016-2675
doi: 10.1542/peds.2016-2675
pubmed: 28289138
Cohen K, Weinstein AM (2018) Synthetic and non-synthetic cannabinoid drugs and their adverse effects-a review from public health prospective. Front Public Heal 6:13–16. https://doi.org/10.3389/fpubh.2018.00162
doi: 10.3389/fpubh.2018.00162
Coller JK, Hutchinson MR (2012) Implications of central immune signaling caused by drugs of abuse: mechanisms, mediators and new therapeutic approaches for prediction and treatment of drug dependence. Pharmacol Ther 134:219–245. https://doi.org/10.1016/j.pharmthera.2012.01.008
doi: 10.1016/j.pharmthera.2012.01.008
pubmed: 22316499
Crews FT, Zou J, Qin L (2011) Induction of innate immune genes in brain create the neurobiology of addiction. Brain Behav Immun 25:S4–S12. https://doi.org/10.1016/j.bbi.2011.03.003
doi: 10.1016/j.bbi.2011.03.003
pubmed: 21402143
pmcid: 3552373
Cutando L, Busquets-Garcia A, Puighermanal E et al (2013) Microglial activation underlies cerebellar deficits produced by repeated cannabis exposure. J Clin Invest 123:2816–2831. https://doi.org/10.1172/JCI67569
doi: 10.1172/JCI67569
pubmed: 23934130
pmcid: 3696568
da Rocha FF, Correa H, Teixeira AL (2008) Obsessive-compulsive disorder and immunology: a review. Prog Neuropsychopharmacol Biol Psychiatry. 32(5):1139–46. https://doi.org/10.1016/j.pnpbp.2007.12.026
doi: 10.1016/j.pnpbp.2007.12.026
pubmed: 18262706
de Brouwer G, Fick A, Harvey BH, Wolmarans W (2019) A critical inquiry into marble-burying as a preclinical screening paradigm of relevance for anxiety and obsessive-compulsive disorder: Mapping the way forward. Cogn Affect Behav Neurosci 19:1–39. https://doi.org/10.3758/s13415-018-00653-4
De Luca MA, Valentini V, Bimpisidis Z et al (2014) Endocannabinoid 2-arachidonoylglycerol self-administration by Sprague-Dawley rats and stimulation of in vivo dopamine transmission in the nucleus accumbens shell. Front Psychiatry 5:1–9. https://doi.org/10.3389/fpsyt.2014.00140
doi: 10.3389/fpsyt.2014.00140
De Luca MA, Bimpisidis Z, Melis M et al (2015) Stimulation of in vivo dopamine transmission and intravenous self-administration in rats and mice by JWH-018, a Spice cannabinoid. Neuropharmacology 99:705–714. https://doi.org/10.1016/j.neuropharm.2015.08.041
doi: 10.1016/j.neuropharm.2015.08.041
pubmed: 26327678
De Luca MA, Castelli MP, Loi B et al (2016) Native CB1 receptor affinity, intrinsic activity and accumbens shell dopamine stimulant properties of third generation SPICE/K2 cannabinoids: BB-22, 5F-PB-22, 5F-AKB-48 and STS-135. Neuropharmacology 105:630–638. https://doi.org/10.1016/j.neuropharm.2015.11.017
doi: 10.1016/j.neuropharm.2015.11.017
pubmed: 26686391
Di Chiara G (2002) Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav Brain Res 137:75–114. https://doi.org/10.1016/S0166-4328(02)00286-3
doi: 10.1016/S0166-4328(02)00286-3
pubmed: 12445717
Di Chiara G, Bassareo V, Fenu S et al (2004) Dopamine and drug addiction: the nucleus accumbens shell connection. Neuropharmacology 47:227–241. https://doi.org/10.1016/j.neuropharm.2004.06.032
doi: 10.1016/j.neuropharm.2004.06.032
pubmed: 15464140
Ellgren M, Spano SM, Hurd YL (2007) Adolescent cannabis exposure alters opiate intake and opioid limbic neuronal populations in adult rats. Neuropsychopharmacology 32:607–615. https://doi.org/10.1038/sj.npp.1301127
doi: 10.1038/sj.npp.1301127
pubmed: 16823391
EMCDDA (2019) European drug report 2019: trends an developments, European Monitoring Centre for Drugs and Drug Addiction. European Union Publications Office, Luxembourg
Festucci F, Buccheri C, Parvopassu A, Oggiano M, Bortolato M, Laviola G, Curcio G, Adriani W (2021) “Himalayan Bridge”: a new unstable suspended bridge to investigate rodents’ venturesome behavior. Front Behav Neurosci 15:637074. https://doi.org/10.3389/fnbeh.2021.637074
doi: 10.3389/fnbeh.2021.637074
pubmed: 33994967
pmcid: 8113634
Fields JA, Swinton MK, Montilla-Perez P, Ricciardelli E, Telese F (2020) The cannabinoid receptor agonist, WIN, suppresses the activation of proinflammatory genes induced by interleukin 1 beta in human astrocytes. Cannabis Cannabinoid Res. https://doi.org/10.1089/can.2020.0128
doi: 10.1089/can.2020.0128
pubmed: 33998879
Fishbein-kaminietsky M, Gafni M, Sarne Y (2014) Ultralow Doses of Cannabinoid Drugs Protect the Mouse Brain from Inflammation-Induced Cognitive Damage. J Neurosci Res 1677:1669–1677. https://doi.org/10.1002/jnr.23452
doi: 10.1002/jnr.23452
Franke H (1995) Influence of chronic alcohol treatment on the GFAP-immunoreactivity in astrocytes of the hippocampus in rats. Acta Histochem 97:263–271. https://doi.org/10.1016/S0065-1281(11)80187-X
doi: 10.1016/S0065-1281(11)80187-X
pubmed: 8525783
Frau R, Bini V, Soggiu A, Scheggi S, Pardu A, Fanni S, Roncada P, Puligheddu M, Marrosu F, Caruso D, Devoto P, Bortolato M (2017) The neurosteroidogenic enzyme 5α-reductase mediates psychotic-like complications of sleep deprivation. Neuropsychopharmacology 42(11):2196–2205. https://doi.org/10.1038/npp.2017.13
doi: 10.1038/npp.2017.13
pubmed: 28102229
pmcid: 5603808
Frau R, Miczán V, Traccis F, Aroni S, Pongor CI, Saba P, Serra V, Sagheddu C, Fanni S, Congiu M, Devoto P, Cheer JF, Katona I, Melis M (2019) Prenatal THC exposure produces a hyperdopaminergic phenotype rescued by pregnenolone. Nat Neurosci 22(12):1975–1985. https://doi.org/10.1038/s41593-019-0512-2
doi: 10.1038/s41593-019-0512-2
pubmed: 31611707
pmcid: 6884689
Gabaglio M, Zamberletti E, Manenti C et al (2021) Long-term consequences of adolescent exposure to thc-rich/cbd-poor and cbd-rich/thc-poor combinations: a comparison with pure thc treatment in female rats. Int J Mol Sci 22:8899. https://doi.org/10.3390/ijms22168899
doi: 10.3390/ijms22168899
pubmed: 34445602
pmcid: 8396365
Gilman JM, Calderon V, Curran MT (2015) Evins AE (2014) Young adult cannabis users report greater propensity for risk-taking only in non-monetary domains. Drug Alcohol Depend 147:26–31. https://doi.org/10.1016/j.drugalcdep.2014.12.020
doi: 10.1016/j.drugalcdep.2014.12.020
pubmed: 25577478
Glass M, Dragunow M, Faull RL (1997) Cannabinoid receptors in the human brain: a detailed anatomical and quantitative autoradiographic study in the fetal, neonatal and adult human brain. Neuroscience 77:299–318
doi: 10.1016/S0306-4522(96)00428-9
pubmed: 9472392
Goodman J, Packard MG (2015) The memory system engaged during acquisition determines the effectiveness of different extinction protocols. Front Behav Neurosci 9:314. https://doi.org/10.3389/fnbeh.2015.00314
doi: 10.3389/fnbeh.2015.00314
pubmed: 26635564
pmcid: 4657229
Greer JM, Capecchi MR (2002) Hoxb8 is required for normal grooming behavior in mice. Neuron 33:23–34. https://doi.org/10.1016/S0896-6273(01)00564-5
doi: 10.1016/S0896-6273(01)00564-5
pubmed: 11779477
Higuera-Matas A, Miguéns M, Coria SM et al (2012) Sex-specific disturbances of the glutamate/GABA balance in the hippocampus of adult rats subjected to adolescent cannabinoid exposure. Neuropharmacology 62:1975–1984. https://doi.org/10.1016/j.neuropharm.2011.12.028
doi: 10.1016/j.neuropharm.2011.12.028
pubmed: 22245681
Hilário M, Clouse E, Yin H, Costa R (2007) Endocannabinoid signaling is critical for habit formation. Front Integr Neurosci 1:6. https://doi.org/10.3389/neuro.07.006.2007
doi: 10.3389/neuro.07.006.2007
pubmed: 18958234
pmcid: 2526012
Hurd YL, Michaelides M, Miller ML, Jutras-Aswad D (2014) Trajectory of adolescent cannabis use on addiction vulnerability. Neuropharmacology 76:416–424. https://doi.org/10.1016/j.neuropharm.2013.07.028
doi: 10.1016/j.neuropharm.2013.07.028
pubmed: 23954491
Jacobus J, Bava S, Cohen-Zion M et al (2009) Functional consequences of marijuana use in adolescents. Pharmacol Biochem Behav 92:559–565. https://doi.org/10.1016/j.pbb.2009.04.001
doi: 10.1016/j.pbb.2009.04.001
pubmed: 19348837
pmcid: 2697065
Justinova Z, Goldberg SR, Heishman SJ, Tanda G (2005) Self-administration of cannabinoids by experimental animals and human marijuana smokers. Pharmacol Biochem Behav 81:285–299. https://doi.org/10.1016/j.pbb.2005.01.026
doi: 10.1016/j.pbb.2005.01.026
pubmed: 15932767
pmcid: 2679508
Kevin RC, Wood KE, Stuart J et al (2017) Acute and residual effects in adolescent rats resulting from exposure to the novel synthetic cannabinoids AB-PINACA and AB-FUBINACA. J Psychopharmacol 31:757–769. https://doi.org/10.1177/0269881116684336
doi: 10.1177/0269881116684336
pubmed: 28093016
Kim R, Healey KL, Sepulveda-Orengo MT, Reissner KJ (2018) Astroglial correlates of neuropsychiatric disease: from astrocytopathy to astrogliosis. Prog Neuro-Psychopharmacology Biol Psychiatry 87:126–146. https://doi.org/10.1016/j.pnpbp.2017.10.002
doi: 10.1016/j.pnpbp.2017.10.002
Koob GF, Volkow ND (2010) Erratum: Neurocircuitry of addiction (Neuropsychopharmacology (2010) 35 (217–238) https://doi.org/10.1038/npp.2009.110 ). Neuropsychopharmacology 35:1051. https://doi.org/10.1038/npp.2010.4
Kronfol Z, Remick DG (2000) Cytokines and the brain: implications for clinical psychiatry. Am J Psychiatry 157:683–694. https://doi.org/10.1176/appi.ajp.157.5.683
doi: 10.1176/appi.ajp.157.5.683
pubmed: 10784457
Lacagnina MJ, Rivera PD, Bilbo SD (2017) Glial and neuroimmune mechanisms as critical modulators of drug use and abuse. Neuropsychopharmacology 42:156–177. https://doi.org/10.1038/npp.2016.121
doi: 10.1038/npp.2016.121
pubmed: 27402494
Lane SD, Cherek DR, Lieving LM, Tcheremissine OV (2005) Marijuana effects on human forgetting functions. J Exp Anal Behav 83:67–83. https://doi.org/10.1901/jeab.2005.22-04
doi: 10.1901/jeab.2005.22-04
pubmed: 15762381
pmcid: 1193701
Linker KE, Cross SJ, Leslie FM (2018) Glial mechanisms underlying substance use disorders. Eur J Neurosci 1–16. https://doi.org/10.1111/ejn.14163
López-Gallardo M, López-Rodríguez AB, Llorente-Berzal Á et al (2012) Maternal deprivation and adolescent cannabinoid exposure impact hippocampal astrocytes, CB1 receptors and brain-derived neurotrophic factor in a sexually dimorphic fashion. Neuroscience 204:90–103. https://doi.org/10.1016/j.neuroscience.2011.09.063
doi: 10.1016/j.neuroscience.2011.09.063
pubmed: 22001306
Lopez-Rodriguez AB, Llorente-Berzal A, Garcia-Segura LM, Viveros MP (2014) Sex-dependent long-term effects of adolescent exposure to THC and/or MDMA on neuroinflammation and serotoninergic and cannabinoid systems in rats. Br J Pharmacol 171:1435–1447. https://doi.org/10.1111/bph.12519
doi: 10.1111/bph.12519
pubmed: 24236988
pmcid: 3954483
Manitt C, Labelle-Dumais C, Eng C et al (2010) Peri-pubertal emergence of UNC-5 homologue expression by dopamine neurons in rodents. PLoS ONE 5:e11463. https://doi.org/10.1371/journal.pone.0011463
doi: 10.1371/journal.pone.0011463
pubmed: 20628609
pmcid: 2900213
Martellotta MC, Cossu G, Fattore L et al (1998) Self-administration of the cannabinoid receptor agonist WIN 55,212–2 in drug-naive mice. Neuroscience 85:327–330. https://doi.org/10.1016/S0306-4522(98)00052-9
doi: 10.1016/S0306-4522(98)00052-9
pubmed: 9622233
McDonald J, Schleifer L, Richards JB, De Wit H (2003) Effects of THC on behavioral measures of impulsivity in humans. Neuropsychopharmacology 28:1356–1365. https://doi.org/10.1038/sj.npp.1300176
doi: 10.1038/sj.npp.1300176
pubmed: 12784123
Mendizábal V, Zimmer A, Maldonado R (2006) Involvement of kappa/dynorphin system in WIN 55,212–2 self-administration in mice. Neuropsychopharmacology 31(9):1957–1966. https://doi.org/10.1038/sj.npp.1300957
doi: 10.1038/sj.npp.1300957
pubmed: 16292318
Mensen VT, Vreeker A, Nordgren J, Atkinson A, de la Torre R, Farré M, Ramaekers JG, Brunt TM (2019) Psychopathological symptoms associated with synthetic cannabinoid use: a comparison with natural cannabis. Psychopharmacology (Berl) 236(9):2677–2685. https://doi.org/10.1007/s00213-019-05238-8
doi: 10.1007/s00213-019-05238-8
pubmed: 30968175
Meyer HC, Lee FS, Gee DG (2018) The role of the endocannabinoid system and genetic variation in adolescent brain development. Neuropsychopharmacology 43:21–23. https://doi.org/10.1038/npp.2017.143
doi: 10.1038/npp.2017.143
pubmed: 28685756
Miguel-Hidalgo JJ (2005) Lower packing density of glial fibrillary acidic protein–immunoreactive astrocytes in the prelimbic cortex of alcohol-naive and alcohol-drinking alcohol-preferring rats as compared with alcohol-nonpreferring and Wistar rats. Alcohol Clin Exp Res 29:766–772. https://doi.org/10.1097/01.ALC.0000164378.92680.FA
doi: 10.1097/01.ALC.0000164378.92680.FA
pubmed: 15897721
pmcid: 2923206
Miguel-Hidalgo JJ (2009) The role of glial cells in drug abuse. Curr Drug Abuse Rev 2:72–82. https://doi.org/10.2174/1874473710902010076
doi: 10.2174/1874473710902010076
pubmed: 19630738
Miliano C, Margiani G, Fattore L, De Luca MA (2018) Sales and advertising channels of new psychoactive substances (NPS): Internet, social networks, and smartphone apps. Brain Sci 8:123. https://doi.org/10.3390/brainsci8070123
doi: 10.3390/brainsci8070123
pubmed: 29966280
pmcid: 6071095
Murphy M, Mills S, Winstone J et al (2017) Chronic adolescent Δ 9 -tetrahydrocannabinol treatment of male mice leads to long-term cognitive and behavioral dysfunction, which are prevented by concurrent cannabidiol treatment. Cannabis Cannabinoid Res 2:235–246. https://doi.org/10.1089/can.2017.0034
doi: 10.1089/can.2017.0034
pubmed: 29098186
pmcid: 5655843
Musa A, Simola N, Piras G et al (2020) Neurochemical and behavioral characterization after acute and repeated exposure to novel synthetic cannabinoid agonist 5-mdmb-pica. Brain Sci 10:1–14. https://doi.org/10.3390/brainsci10121011
doi: 10.3390/brainsci10121011
Namba MD, Kupchik YM, Spencer SM et al (2020) Accumbens neuroimmune signaling and dysregulation of astrocytic glutamate transport underlie conditioned nicotine-seeking behavior. Addict Biol 25:e12797. https://doi.org/10.1111/adb.12797
doi: 10.1111/adb.12797
pubmed: 31330570
Naneix F, Marchand AR, Di Scala G et al (2012) Parallel maturation of goal-directed behavior and dopaminergic systems during adolescence. J Neurosci 32:16223–16232. https://doi.org/10.1523/JNEUROSCI.3080-12.2012
doi: 10.1523/JNEUROSCI.3080-12.2012
pubmed: 23152606
pmcid: 6794026
Navarro M, Carrera MR, Fratta W et al (2001) Functional interaction between opioid and cannabinoid receptors in drug self-administration. J Neurosci 21:5344–5350. https://doi.org/10.1523/JNEUROSCI.21/14/5344[pii]
doi: 10.1523/JNEUROSCI.21/14/5344[pii]
pubmed: 11438610
pmcid: 6762870
Ninnemann AL, Choi HJ, Stuart GL, Temple JR (2017) Longitudinal predictors of synthetic cannabinoid use in adolescents. Pediatrics 139:e20163009. https://doi.org/10.1542/peds.2016-3009
doi: 10.1542/peds.2016-3009
pubmed: 28289139
O’Donnell BF, Skosnik PD, Hetrick WP, Fridberg DJ (2021) Decision making and impulsivity in young adult cannabis users. Front Psychol. 12:679904. https://doi.org/10.3389/fpsyg.2021.679904
doi: 10.3389/fpsyg.2021.679904
pubmed: 34276500
pmcid: 8280309
Pacifici R, Zuccaro P, Farré M et al (2002) Cell-mediated immune response in MDMA users after repeated dose administration: studies in controlled versus noncontrolled settings. Ann N Y Acad Sci 965:421–433. https://doi.org/10.1111/j.1749-6632.2002.tb04183.x
doi: 10.1111/j.1749-6632.2002.tb04183.x
pubmed: 12105117
Pacifici R, Zuccaro P, Pichini S et al (2003) Modulation of the immune system in cannabis users. JAMA 289:1929–1931. https://doi.org/10.1001/jama.289.15.1929-a
doi: 10.1001/jama.289.15.1929-a
pubmed: 12697794
Pacifici R, Zuccaro P, Farré M et al (2007) Combined immunomodulating properties of 3,4-methylenedioxymethamphetamine (MDMA) and cannabis in humans. Addiction 102:931–936. https://doi.org/10.1111/j.1360-0443.2007.01805.x
doi: 10.1111/j.1360-0443.2007.01805.x
pubmed: 17523988
Palamar JJ, Barratt MJ, Coney L, Martins SS (2017) Synthetic cannabinoid use among high school seniors. Pediatrics. https://doi.org/10.1542/peds.2017-1330
doi: 10.1542/peds.2017-1330
pubmed: 28893851
Parsons LH, Hurd YL (2015) Endocannabinoid signalling in reward and addiction. Nat Rev Neurosci 16:579–94. https://doi.org/10.1038/nrn4004
doi: 10.1038/nrn4004
pubmed: 26373473
pmcid: 4652927
Paule MG, Allen RR, Bailey JR et al (1992) Chronic marijuana smoke exposure in the rhesus monkey. II: Effects on progressive ratio and conditioned position responding. J Pharmacol Exp Ther 260:210–222
pubmed: 1731038
Pekny M, Pekna M, Messing A et al (2016) Astrocytes: a central element in neurological diseases. Acta Neuropathol 131:323–345. https://doi.org/10.1007/s00401-015-1513-1
doi: 10.1007/s00401-015-1513-1
pubmed: 26671410
Pintori N, Loi B, Mereu M (2017) Synthetic cannabinoids: the hidden side of Spice drugs. Behav Pharmacol 28:409–419. https://doi.org/10.1097/FBP.0000000000000323
doi: 10.1097/FBP.0000000000000323
pubmed: 28692429
Pintori N, Castelli MP, Miliano C et al (2021) Repeated exposure to JWH-018 induces adaptive changes in the mesolimbic and mesocortical dopaminergic pathways, glial cells alterations, and behavioural correlates. Br J Pharmacol 178:3476–3497. https://doi.org/10.1111/bph.15494
doi: 10.1111/bph.15494
pubmed: 33837969
Pocock JM, Kettenmann H (2007) Neurotransmitter receptors on microglia. Trends Neurosci 30:527–535. https://doi.org/10.1016/j.tins.2007.07.007
doi: 10.1016/j.tins.2007.07.007
pubmed: 17904651
Ransohoff RM, Brown MA (2012) Innate immunity in the central nervous system Find the latest version : review series Innate immunity in the central nervous system. J Clin Invest 122:1164–1171. https://doi.org/10.1172/JCI58644.1164
doi: 10.1172/JCI58644.1164
pubmed: 22466658
pmcid: 3314450
Rao PSS, Bell RL, Engleman EA, Sari Y (2015) Targeting glutamate uptake to treat alcohol use disorders. Front Neurosci 9:144. https://doi.org/10.3389/fnins.2015.00144
doi: 10.3389/fnins.2015.00144
pubmed: 25954150
pmcid: 4407613
Rintala J, Jaatinen P, Kiianmaa K et al (2001) Dose-dependent decrease in glial fibrillary acidic protein-immunoreactivity in rat cerebellum after lifelong ethanol consumption. Alcohol 23:1–8. https://doi.org/10.1016/S0741-8329(00)00116-6
doi: 10.1016/S0741-8329(00)00116-6
pubmed: 11282445
Robson MJ, Turner RC, Naser ZJ et al (2013) SN79, a sigma receptor ligand, blocks methamphetamine-induced microglial activation and cytokine upregulation. Exp Neurol 247:134–142. https://doi.org/10.1016/j.expneurol.2013.04.009
doi: 10.1016/j.expneurol.2013.04.009
pubmed: 23631864
pmcid: 3742718
Rubino T, Vigano D, Realini N et al (2008) Chronic Δ9-tetrahydrocannabinol during adolescence provokes sex-dependent changes in the emotional profile in adult rats: behavioral and biochemical correlates. Neuropsychopharmacology 33:2760–2771. https://doi.org/10.1038/sj.npp.1301664
doi: 10.1038/sj.npp.1301664
pubmed: 18172430
Salter MW, Beggs S (2014) Sublime microglia: expanding roles for the guardians of the CNS. Cell 158:15–24. https://doi.org/10.1016/j.cell.2014.06.008
doi: 10.1016/j.cell.2014.06.008
pubmed: 24995975
Schneider M (2013) Adolescence as a vulnerable period to alter rodent behavior. Cell Tissue Res 354:99–106. https://doi.org/10.1007/s00441-013-1581-2
doi: 10.1007/s00441-013-1581-2
pubmed: 23430475
Smith ACW, Scofield MD, Kalivas PW (2015) The tetrapartite synapse: extracellular matrix remodeling contributes to corticoaccumbens plasticity underlying drug addiction. Brain Res 1628:29–39. https://doi.org/10.1016/j.brainres.2015.03.027
doi: 10.1016/j.brainres.2015.03.027
pubmed: 25838241
pmcid: 4589426
Solowij N, Jones KA, Rozman ME, Davis SM, Ciarrochi J, Heaven PC, Pesa N, Lubman DI, Yücel M (2012) Reflection impulsivity in adolescent cannabis users: a comparison with alcohol-using and non-substance-using adolescents. Psychopharmacology 219(2):575–586. https://doi.org/10.1007/s00213-011-2486-y
doi: 10.1007/s00213-011-2486-y
pubmed: 21938415
Spear LP (2016) Consequences of adolescent use of alcohol and other drugs: studies using rodent models. Neurosci Biobehav Rev 70:228–243. https://doi.org/10.1016/j.neubiorev.2016.07.026
doi: 10.1016/j.neubiorev.2016.07.026
pubmed: 27484868
pmcid: 5074861
Stella N (2010) Cannabinoid and cannabinoid-like receptors in microglia, astrocytes, and astrocytomas. Glia 58:1017–1030. https://doi.org/10.1002/glia.20983
doi: 10.1002/glia.20983
pubmed: 20468046
pmcid: 2919281
Suárez I, Bodega G, Ramos JA et al (2000) Neuronal and astroglial response to pre- and perinatal exposure to delta-9-tetra- hydrocannabinol in the rat substantia nigra. Dev Neurosci 22:253–263. https://doi.org/10.1159/000017449
doi: 10.1159/000017449
pubmed: 10965147
Tahir SK, Trogadis JE, Stevens JK, Zimmerman AM (1992) Cytoskeletal organization following cannabinoid treatment in undifferentiated and differentiated PC12 cells. Biochem Cell Biol 70:1159–1173. https://doi.org/10.1139/o92-162
doi: 10.1139/o92-162
pubmed: 1297339
Tanaka M, Sackett S, Zhang Y (2020) Endocannabinoid modulation of microglial phenotypes in neuropathology. Front Neurol 11:87. https://doi.org/10.3389/fneur.2020.00087
doi: 10.3389/fneur.2020.00087
pubmed: 32117037
pmcid: 7033501
Tanda G, Goldberg SR (2003) Cannabinoids : reward , dependence , and underlying neurochemical mechanisms — a review of recent preclinical data. 115–134. https://doi.org/10.1007/s00213-003-1485-z
Thomas A, Burant A, Bui N, Graham D, Yuva-Paylor LA, Paylor R (2009) Marble burying reflects arepetitive and perseverative behavior more than novelty-induced anxiety. Psychopharmacology (Berl) 204:361–373. https://doi.org/10.1007/s00213-009-1466-y
Tomiyama K, Funada M (2014) Cytotoxicity of synthetic cannabinoids on primary neuronal cells of the forebrain: the involvement of cannabinoid CB1 receptors and apoptotic cell death. Toxicol Appl Pharmacol. https://doi.org/10.1016/j.taap.2013.10.028
doi: 10.1016/j.taap.2013.10.028
pubmed: 24211273
Valentini V, Piras G, De Luca MA, Perra V, Bordi F, Borsini F, Frau R, Di Chiara G (2013) Evidence for a role of a dopamine/5-HT6 receptor interaction in cocaine reinforcement. Neuropharmacology 65:58–64. https://doi.org/10.1016/j.neuropharm.2012.08.025
Wagner KD, Armenta RF, Roth AM et al (2014) Use of synthetic cathinones and cannabimimetics among injection drug users in San Diego, California. Drug Alcohol Depend 141:99–106. https://doi.org/10.1016/j.drugalcdep.2014.05.007
doi: 10.1016/j.drugalcdep.2014.05.007
pubmed: 24916748
pmcid: 4114932
Wrege J, Schmidt A, Walter A et al (2014) Effects of cannabis on impulsivity: a systematic review of neuroimaging findings. Curr Pharm Des 20(13):2126–2137. https://doi.org/10.2174/13816128113199990428
doi: 10.2174/13816128113199990428
pubmed: 23829358
pmcid: 4052819
Wu N, Lu XQ, Yan HT et al (2008) Aquaporin 4 deficiency modulates morphine pharmacological actions. Neurosci Lett 448:221–225. https://doi.org/10.1016/j.neulet.2008.10.065
doi: 10.1016/j.neulet.2008.10.065
pubmed: 18973795
Zamberletti E, Gabaglio M, Prini P et al (2015) Cortical neuroinflammation contributes to long-term cognitive dysfunctions following adolescent delta-9-tetrahydrocannabinol treatment in female rats. Eur Neuropsychopharmacol 25:2404–2415. https://doi.org/10.1016/j.euroneuro.2015.09.021
doi: 10.1016/j.euroneuro.2015.09.021
pubmed: 26499171
Zamberletti E, Gabaglio M, Grilli M et al (2016) Long-term hippocampal glutamate synapse and astrocyte dysfunctions underlying the altered phenotype induced by adolescent THC treatment in male rats. Pharmacol Res 111:459–470. https://doi.org/10.1016/j.phrs.2016.07.008
doi: 10.1016/j.phrs.2016.07.008
pubmed: 27422357
Zou J, Crews F (2010) Induction of innate immune gene expression cascades in brain slice cultures by ethanol: key role of NF-κB and proinflammatory cytokines. Alcohol Clin Exp Res 34:777–789. https://doi.org/10.1111/j.1530-0277.2010.01150.x
doi: 10.1111/j.1530-0277.2010.01150.x
pubmed: 20201932