Cocaine-mediated circadian reprogramming in the striatum through dopamine D2R and PPARγ activation.
Administration, Oral
Animals
Circadian Clocks
/ drug effects
Cocaine
/ administration & dosage
Cocaine-Related Disorders
/ drug therapy
Dopamine
/ metabolism
Injections, Intraperitoneal
Locomotion
/ physiology
Male
Mice
Mice, Knockout
Neurons
/ drug effects
Nucleus Accumbens
/ drug effects
PPAR gamma
/ agonists
Pioglitazone
/ administration & dosage
Receptors, Dopamine D2
/ genetics
Reward
Signal Transduction
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
07 09 2020
07 09 2020
Historique:
received:
16
01
2020
accepted:
06
08
2020
entrez:
8
9
2020
pubmed:
9
9
2020
medline:
2
10
2020
Statut:
epublish
Résumé
Substance abuse disorders are linked to alteration of circadian rhythms, although the molecular and neuronal pathways implicated have not been fully elucidated. Addictive drugs, such as cocaine, induce a rapid increase of dopamine levels in the brain. Here, we show that acute administration of cocaine triggers reprogramming in circadian gene expression in the striatum, an area involved in psychomotor and rewarding effects of drugs. This process involves the activation of peroxisome protein activator receptor gamma (PPARγ), a nuclear receptor involved in inflammatory responses. PPARγ reprogramming is altered in mice with cell-specific ablation of the dopamine D2 receptor (D2R) in the striatal medium spiny neurons (MSNs) (iMSN-D2RKO). Administration of a specific PPARγ agonist in iMSN-D2RKO mice elicits substantial rescue of cocaine-dependent control of circadian genes. These findings have potential implications for development of strategies to treat substance abuse disorders.
Identifiants
pubmed: 32895370
doi: 10.1038/s41467-020-18200-6
pii: 10.1038/s41467-020-18200-6
pmc: PMC7477550
doi:
Substances chimiques
DRD2 protein, mouse
0
PPAR gamma
0
Pparg protein, mouse
0
Receptors, Dopamine D2
0
Cocaine
I5Y540LHVR
Dopamine
VTD58H1Z2X
Pioglitazone
X4OV71U42S
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4448Subventions
Organisme : NIDA NIH HHS
ID : T32 DA050558
Pays : United States
Références
Green, C. B., Takahashi, J. S. & Bass, J. The meter of metabolism. Cell 134, 728–742 (2008).
pubmed: 18775307
pmcid: 3760165
Scheiermann, C., Kunisaki, Y. & Frenette, P. S. Circadian control of the immune system. Nat. Rev. Immunol. 13, 190–198 (2013).
pubmed: 23391992
pmcid: 4090048
Welsh, D. K., Takahashi, J. S. & Kay, S. A. Suprachiasmatic nucleus: cell autonomy and network properties. Annu. Rev. Physiol. 72, 551–577 (2010).
pubmed: 20148688
pmcid: 3758475
Albrecht, U. Timing to perfection: the biology of central and peripheral circadian clocks. Neuron 74, 246–260 (2012).
pubmed: 22542179
Dyar, K. A. et al. Atlas of circadian metabolism reveals system-wide coordination and communication between clocks. Cell 174, 1571–1585 e1511 (2018).
pubmed: 30193114
pmcid: 6501776
Bass, J. & Lazar, M. A. Circadian time signatures of fitness and disease. Science 354, 994–999 (2016).
pubmed: 27885004
Asher, G. & Sassone-Corsi, P. Time for food: the intimate interplay between nutrition, metabolism, and the circadian clock. Cell 161, 84–92 (2015).
pubmed: 25815987
Panda, S. Circadian physiology of metabolism. Science 354, 1008–1015 (2016).
pubmed: 27885007
pmcid: 7261592
Partch, C. L., Green, C. B. & Takahashi, J. S. Molecular architecture of the mammalian circadian clock. Trends Cell Biol. 24, 90–99 (2014).
pubmed: 23916625
Gallardo, C. M. et al. Dopamine receptor 1 neurons in the dorsal striatum regulate food anticipatory circadian activity rhythms in mice. Elife 3, e03781 (2014).
pubmed: 25217530
pmcid: 4196120
Iijima, M., Nikaido, T., Akiyama, M., Moriya, T. & Shibata, S. Methamphetamine-induced, suprachiasmatic nucleus-independent circadian rhythms of activity and mPer gene expression in the striatum of the mouse. Eur. J. Neurosci. 16, 921–929 (2002).
pubmed: 12372028
Mohawk, J. A., Green, C. B. & Takahashi, J. S. Central and peripheral circadian clocks in mammals. Annu. Rev. Neurosci. 35, 445–462 (2012).
pubmed: 22483041
pmcid: 3710582
Hasler, B. P., Smith, L. J., Cousins, J. C. & Bootzin, R. R. Circadian rhythms, sleep, and substance abuse. Sleep. Med. Rev. 16, 67–81 (2012).
pubmed: 21620743
Logan, R. W., Williams, W. P. 3rd & McClung, C. A. Circadian rhythms and addiction: mechanistic insights and future directions. Behav. Neurosci. 128, 387–412 (2014).
pubmed: 24731209
pmcid: 4041815
Korpi, E. R. et al. Mechanisms of action and persistent neuroplasticity by drugs of abuse. Pharm. Rev. 67, 872–1004 (2015).
pubmed: 26403687
Di Chiara, G. & Bassareo, V. Reward system and addiction: what dopamine does and doesn’t do. Curr. Opin. Pharm. 7, 69–76 (2007).
Girault, J. A. Integrating neurotransmission in striatal medium spiny neurons. Adv. Exp. Med. Biol. 970, 407–429 (2012).
pubmed: 22351066
McClung, C. A. et al. Regulation of dopaminergic transmission and cocaine reward by the Clock gene. Proc. Natl. Acad. Sci. USA 102, 9377–9381 (2005).
pubmed: 15967985
Logan, R. W. et al. NAD+ cellular redox and SIRT1 regulate the diurnal rhythms of tyrosine hydroxylase and conditioned cocaine reward. Mol. Psychiatry 24, 1668–1684 (2019).
pubmed: 29728703
Castaneda, T. R., de Prado, B. M., Prieto, D. & Mora, F. Circadian rhythms of dopamine, glutamate and GABA in the striatum and nucleus accumbens of the awake rat: modulation by light. J. Pineal Res. 36, 177–185 (2004).
pubmed: 15009508
Ferris, M. J. et al. Dopamine transporters govern diurnal variation in extracellular dopamine tone. Proc. Natl Acad. Sci. USA 111, E2751–E2759 (2014).
pubmed: 24979798
Imbesi, M. et al. Dopamine receptor-mediated regulation of neuronal clock gene expression. Neuroscience 158, 537–544 (2009).
pubmed: 19017537
Hood, S. et al. Endogenous dopamine regulates the rhythm of expression of the clock protein PER2 in the rat dorsal striatum via daily activation of D2 dopamine receptors. J. Neurosci. 30, 14046–14058 (2010).
pubmed: 20962226
pmcid: 6634752
Brown, S. A. Circadian metabolism: from mechanisms to metabolomics and medicine. Trends Endocrinol. Metab. 27, 415–426 (2016).
pubmed: 27113082
Ribas-Latre, A. & Eckel-Mahan, K. Interdependence of nutrient metabolism and the circadian clock system: Importance for metabolic health. Mol. Metab. 5, 133–152 (2016).
pubmed: 26977390
pmcid: 4770266
Challet, E. The circadian regulation of food intake. Nat. Rev. Endocrinol. 15, 393–405 (2019).
pubmed: 31073218
Kharkwal, G., Radl, D., Lewis, R. & Borrelli, E. Dopamine D2 receptors in striatal output neurons enable the psychomotor effects of cocaine. Proc. Natl Acad. Sci. USA 113, 11609–11614 (2016).
pubmed: 27671625
Radl, D. et al. Differential regulation of striatal motor behavior and related cellular responses by dopamine D2L and D2S isoforms. Proc. Natl Acad. Sci. USA 115, 198–203 (2018).
pubmed: 29255027
Anzalone, A. et al. Dual control of dopamine synthesis and release by presynaptic and postsynaptic dopamine D2 receptors. J. Neurosci. 32, 9023–9034 (2012).
pubmed: 22745501
pmcid: 3752062
Kliewer, S. A. et al. Differential expression and activation of a family of murine peroxisome proliferator-activated receptors. Proc. Natl Acad. Sci. USA 91, 7355–7359 (1994).
pubmed: 8041794
Khan, M. A. et al. Current progress on peroxisome proliferator-activated receptor gamma agonist as an emerging therapeutic approach for the treatment of alzheimer’s disease: an update. Curr. Neuropharmacol. 17, 232–246 (2019).
pubmed: 30152284
pmcid: 6425074
Lee, C. H., Olson, P. & Evans, R. M. Minireview: lipid metabolism, metabolic diseases, and peroxisome proliferator-activated receptors. Endocrinology 144, 2201–2207 (2003).
pubmed: 12746275
Dobbs, L. K. et al. Dopamine regulation of lateral inhibition between striatal neurons gates the stimulant actions of cocaine. Neuron 90, 1100–1113 (2016).
pubmed: 27181061
pmcid: 4891261
Beuming, T. et al. The binding sites for cocaine and dopamine in the dopamine transporter overlap. Nat. Neurosci. 11, 780–789 (2008).
pubmed: 18568020
pmcid: 2692229
Nestler, E. J. The neurobiology of cocaine addiction. Sci. Pr. Perspect. 3, 4–10 (2005).
Luscher, C. & Malenka, R. C. Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling. Neuron 69, 650–663 (2011).
pubmed: 21338877
pmcid: 4046255
Hughes, M. E., Hogenesch, J. B. & Kornacker, K. JTK_CYCLE: an efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets. J. Biol. Rhythms 25, 372–380 (2010).
pubmed: 20876817
pmcid: 3119870
Vallone, D., Picetti, R. & Borrelli, E. Structure and function of dopamine receptors. Neurosci. Biobehav. Rev. 24, 125–132 (2000).
pubmed: 10654668
Daily, K., Patel, V. R., Rigor, P., Xie, X. & Baldi, P. MotifMap: integrative genome-wide maps of regulatory motif sites for model species. BMC Bioinformatics 12, 495 (2011).
pubmed: 22208852
pmcid: 3293935
Mangelsdorf, D. J. et al. The nuclear receptor superfamily: the second decade. Cell 83, 835–839 (1995).
pubmed: 8521507
pmcid: 6159888
Baik, J. H. et al. Parkinsonian-like locomotor impairment in mice lacking dopamine D2 receptors. Nature 377, 424–428 (1995).
pubmed: 7566118
Kanterman, R. Y. et al. Transfected D2 dopamine receptors mediate the potentiation of arachidonic acid release in Chinese hamster ovary cells. Mol. Pharm. 39, 364–369 (1991).
Neve, K. A., Seamans, J. K. & Trantham-Davidson, H. Dopamine receptor signaling. J. Recept. Signal Transduct. Res. 24, 165–205 (2004).
pubmed: 15521361
Kuehl, F. A. Jr. & Egan, R. W. Prostaglandins, arachidonic acid, and inflammation. Science 210, 978–984 (1980).
pubmed: 6254151
Piomelli, D. et al. Dopamine activation of the arachidonic acid cascade as a basis for D1/D2 receptor synergism. Nature 353, 164–167 (1991).
pubmed: 1909771
Nosjean, O. & Boutin, J. A. Natural ligands of PPARgamma: are prostaglandin J(2) derivatives really playing the part? Cell Signal 14, 573–583 (2002).
pubmed: 11955950
Schinelli, S., Paolillo, M. & Corona, G. L. Opposing actions of D1- and D2-dopamine receptors on arachidonic acid release and cyclic AMP production in striatal neurons. J. Neurochem. 62, 944–949 (1994).
pubmed: 8113815
Scher, J. U. & Pillinger, M. H. 15d-PGJ2: the anti-inflammatory prostaglandin? Clin. Immunol. 114, 100–109 (2005).
pubmed: 15639643
Forman, B. M. et al. 15-Deoxy-delta 12, 14-prostaglandin J2 is a ligand for the adipocyte determination factor PPAR gamma. Cell 83, 803–812 (1995).
pubmed: 8521497
Samikkannu, T. et al. Immunopathogenesis of HIV infection in cocaine users: role of arachidonic acid. PLoS ONE 9, e106348 (2014).
pubmed: 25171226
pmcid: 4149565
Swanson, C. R. et al. The PPAR-gamma agonist pioglitazone modulates inflammation and induces neuroprotection in parkinsonian monkeys. J. Neuroinflammation 8, 91 (2011).
pubmed: 21819568
pmcid: 3166925
Kiyota, Y. et al. Studies on the metabolism of the new antidiabetic agent pioglitazone. Identification of metabolites in rats and dogs.Arzneimittelforschung 47, 22–28 (1997).
pubmed: 9037439
Luscher, C. & Bellone, C. Cocaine-evoked synaptic plasticity: a key to addiction? Nat. Neurosci. 11, 737–738 (2008).
pubmed: 18575469
Ozburn, A. R. et al. NPAS2 Regulation of Anxiety-Like Behavior and GABAA Receptors. Front. Mol. Neurosci. 10, 360 (2017).
pubmed: 29163035
pmcid: 5675889
Brager, A. J., Stowie, A. C., Prosser, R. A. & Glass, J. D. The mPer2 clock gene modulates cocaine actions in the mouse circadian system. Behav. Brain Res. 243, 255–260 (2013).
pubmed: 23333842
pmcid: 4004096
Abarca, C., Albrecht, U. & Spanagel, R. Cocaine sensitization and reward are under the influence of circadian genes and rhythm. Proc. Natl Acad. Sci. USA 99, 9026–9030 (2002).
pubmed: 12084940
Welter, M. et al. Absence of dopamine D2 receptors unmasks an inhibitory control over the brain circuitries activated by cocaine. Proc. Natl Acad. Sci. USA 104, 6840–6845 (2007).
pubmed: 17426149
Caine, S. B. et al. Role of dopamine D2-like receptors in cocaine self-administration: studies with D2 receptor mutant mice and novel D2 receptor antagonists. J. Neurosci. 22, 2977–2988 (2002).
pubmed: 11923462
pmcid: 6758322
Volkow, N. D. et al. Low level of brain dopamine D2 receptors in methamphetamine abusers: association with metabolism in the orbitofrontal cortex. Am. J. Psychiatry 158, 2015–2021 (2001).
pubmed: 11729018
Nader, M. A. et al. PET imaging of dopamine D2 receptors during chronic cocaine self-administration in monkeys. Nat. Neurosci. 9, 1050–1056 (2006).
pubmed: 16829955
Czoty, P. W., Gage, H. D. & Nader, M. A. Differences in D2 dopamine receptor availability and reaction to novelty in socially housed male monkeys during abstinence from cocaine. Psychopharmacology 208, 585–592 (2010).
pubmed: 20066401
pmcid: 2891780
Lewis, R. G. et al. Dopaminergic control of striatal cholinergic interneurons underlies cocaine-induced psychostimulation. Cell Rep. 31, 107527 (2020).
pubmed: 32320647
Korshunov, K. S., Blakemore, L. J. & Trombley, P. Q. Dopamine: a modulator of circadian rhythms in the central nervous system. Front. Cell Neurosci. 11, 91 (2017).
pubmed: 28420965
pmcid: 5376559
Chaturvedi, R. K. & Beal, M. F. PPAR: a therapeutic target in Parkinson’s disease. J. Neurochem. 106, 506–518 (2008).
pubmed: 18384649
Jiang, Q., Heneka, M. & Landreth, G. E. The role of peroxisome proliferator-activated receptor-gamma (PPARgamma) in Alzheimer’s disease: therapeutic implications. CNS Drugs 22, 1–14 (2008).
pubmed: 18072811
Miller, W. R. et al. PPARgamma agonism attenuates cocaine cue reactivity. Addict. Biol. 23, 55–68 (2018).
pubmed: 27862692
Zhang, J. et al. c-Fos facilitates the acquisition and extinction of cocaine-induced persistent changes. J. Neurosci. 26, 13287–13296 (2006).
pubmed: 17182779
pmcid: 6675013
Kelz, M. B. et al. Expression of the transcription factor deltaFosB in the brain controls sensitivity to cocaine. Nature 401, 272–276 (1999).
pubmed: 10499584
Bateup, H. S. et al. Cell type-specific regulation of DARPP-32 phosphorylation by psychostimulant and antipsychotic drugs. Nat. Neurosci. 11, 932–939 (2008).
pubmed: 18622401
pmcid: 2737705
Hikida, T., Kimura, K., Wada, N., Funabiki, K. & Nakanishi, S. Distinct roles of synaptic transmission in direct and indirect striatal pathways to reward and aversive behavior. Neuron 66, 896–907 (2010).
pubmed: 20620875
Parekh, P. K. et al. Cell-type-specific regulation of nucleus accumbens synaptic plasticity and cocaine reward sensitivity by the circadian protein, NPAS2. J. Neurosci. 39, 4657–4667 (2019).
pubmed: 30962277
pmcid: 6561687
Cates, H. M., Lardner, C. K., Bagot, R. C., Neve, R. L. & Nestler, E. J. Fosb induction in nucleus accumbens by cocaine is regulated by E2F3a. eNeuro 6, https://doi.org/10.1523/ENEURO.0325-18.2019 (2019).
Yager, L. M., Garcia, A. F., Wunsch, A. M. & Ferguson, S. M. The ins and outs of the striatum: role in drug addiction. Neuroscience 301, 529–541 (2015).
pubmed: 26116518
pmcid: 4523218
Everitt, B. J. & Robbins, T. W. From the ventral to the dorsal striatum: devolving views of their roles in drug addiction. Neurosci. Biobehav. Rev. 37, 1946–1954 (2013).
pubmed: 23438892
Lobo, M. K. & Nestler, E. J. The striatal balancing act in drug addiction: distinct roles of direct and indirect pathway medium spiny neurons. Front. Neuroanat. 5, 41 (2011).
pubmed: 21811439
pmcid: 3140647
Walker, D. M. et al. Cocaine self-administration alters transcriptome-wide responses in the brain’s reward circuitry. Biol. Psychiatry 84, 867–880 (2018).
pubmed: 29861096
pmcid: 6202276
Chandra, R. & Lobo, M. K. Beyond neuronal activity markers: select immediate early genes in striatal neuron subtypes functionally mediate psychostimulant addiction. Front. Behav. Neurosci. 11, 112 (2017).
pubmed: 28642692
pmcid: 5462953
Aizman, O. et al. Anatomical and physiological evidence for D1 and D2 dopamine receptor colocalization in neostriatal neurons. Nat. Neurosci. 3, 226–230 (2000).
pubmed: 10700253
Trapnell, C. et al. Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat. Biotechnol. 31, 46–53 (2013).
pubmed: 23222703
Patel, V. R., Eckel-Mahan, K., Sassone-Corsi, P. & Baldi, P. CircadiOmics: integrating circadian genomics, transcriptomics, proteomics and metabolomics. Nat. Methods 9, 772–773 (2012).
pubmed: 22847108
Huang da, W., Sherman, B. T. & Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44–57 (2009).
pubmed: 19131956
pmcid: 19131956
Sidiropoulos, K. et al. Reactome enhanced pathway visualization. Bioinformatics 33, 3461–3467 (2017).
pubmed: 29077811
pmcid: 5860170
Fabregat, A. et al. Reactome pathway analysis: a high-performance in-memory approach. BMC Bioinformatics 18, 142 (2017).
pubmed: 28249561
pmcid: 5333408
Soccio, R. E. et al. Genetic variation determines PPARgamma function and anti-diabetic drug response in vivo. Cell 162, 33–44 (2015).
pubmed: 26140591
pmcid: 4493773
Brami-Cherrier, K. et al. Parsing molecular and behavioral effects of cocaine in mitogen- and stress-activated protein kinase-1-deficient mice. J. Neurosci. 25, 11444–11454 (2005).
pubmed: 16339038
pmcid: 6725898
Murakami, M. et al. Gut microbiota directs PPARgamma-driven reprogramming of the liver circadian clock by nutritional challenge. EMBO Rep. 17, 1292–1303 (2016).
pubmed: 27418314
pmcid: 5007574