Prosapip1-Dependent Synaptic Adaptations in the Nucleus Accumbens Drive Alcohol Intake, Seeking, and Reward

Actin; Addiction; Alcohol; Dendritic spines; Plasticity; Prosapip1; AMPA receptor; GluA2 protein; Prosapip1 protein; ProSAPiP1 protein, mouse; Article; RNA sequence; RNA translation; Actin Cytoskeleton; Alcohol Drinking; Animals; Carrier Proteins; Drug-Seeking Behavior; Ethanol; Male; Membrane Proteins; Mice; Multiprotein Complexes; Neuronal Plasticity; Nucleus Accumbens; Receptors, AMPA; Reward; Self Administration; TOR Serine-Threonine Kinases

Abstract :

[en] The mammalian target of rapamycin complex 1 (mTORC1), a transducer of local dendritic translation, participates in learning and memory processes as well as in mechanisms underlying alcohol-drinking behaviors. Using an unbiased RNA-seq approach, we identified Prosapip1 as a novel downstream target of mTORC1 whose translation and consequent synaptic protein expression are increased in the nucleus accumbens (NAc) of mice excessively consuming alcohol. We demonstrate that alcohol-dependent increases in Prosapip1 levels promote the formation of actin filaments, leading to changes in dendritic spine morphology of NAc medium spiny neurons (MSNs). We further demonstrate that Prosapip1 is required for alcohol-dependent synaptic localization of GluA2 lacking AMPA receptors in NAc shell MSNs. Finally, we present data implicating Prosapip1 in mechanisms underlying alcohol self-administration and reward. Together, these data suggest that Prosapip1 in the NAc is a molecular transducer of structural and synaptic alterations that drive and/or maintain excessive alcohol use. Laguesse et al. identified Prosapip1 as a novel downstream target of mTORC1 in the nucleus accumbens that promotes actin reorganization as well as morphological and synaptic alterations that in turn drive alcohol drinking and seeking behaviors. © 2017 Elsevier Inc.

Disciplines :

Neurology

Author, co-author :

Laguesse, Sophie ; Université de Liège - ULiège > Giga - Neurosciences

Morisot, N.; Department of Neurology, University of California, San Francisco, CA, United States, N.M. Brains On-line LLC, South San Francisco, CA, United States

Shin, J. H.; Laboratory on Neurobiology of Compulsive Behaviors, National Institute of Alcohol Abuse and Alcoholism, US National Institutes of Health, Bethesda, MD, United States

Liu, F.; Department of Neurology, University of California, San Francisco, CA, United States, School of Life Sciences, Sun Yat-sen University, Guangzhou, China

Adrover, M. F.; Laboratory on Neurobiology of Compulsive Behaviors, National Institute of Alcohol Abuse and Alcoholism, US National Institutes of Health, Bethesda, MD, United States

Sakhai, S. A.; Department of Neurology, University of California, San Francisco, CA, United States

Lopez, M.

Phamluong, K.; Department of Neurology, University of California, San Francisco, CA, United States

Griffin, W. C.; III, Charleston Alcohol Research Center, Department of Psychiatry and Behavioral Sciences, Medical University of South Carolina, Charleston, SC, United States

Becker, H. C.; Charleston Alcohol Research Center, Department of Psychiatry and Behavioral Sciences, Medical University of South Carolina, Charleston, SC, United States, Department of Neurosciences, Medical University of South Carolina, Charleston, SC, United States, RHJ Department of Veterans Affairs Medical Center, Charleston, SC, United States

More authors (3 more)

Language :

English

Title :

Prosapip1-Dependent Synaptic Adaptations in the Nucleus Accumbens Drive Alcohol Intake, Seeking, and Reward

Publication date :

September 2017

Journal title :

Neuron

ISSN :

0896-6273

eISSN :

1097-4199

Publisher :

Cell Press

Volume :

Issue :

Pages :

145-159.e8

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 04 February 2019

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Bibliography

Baik, J.H., Dopamine signaling in reward-related behaviors. Front. Neural Circuits, 7, 2013, 152.
Barak, S., Liu, F., Ben Hamida, S., Yowell, Q.V., Neasta, J., Kharazia, V., Janak, P.H., Ron, D., Disruption of alcohol-related memories by mTORC1 inhibition prevents relapse. Nat. Neurosci. 16 (2013), 1111–1117.
Becker, H.C., Lopez, M.F., Increased ethanol drinking after repeated chronic ethanol exposure and withdrawal experience in C57BL/6 mice. Alcohol. Clin. Exp. Res. 28 (2004), 1829–1838.
Beckley, J.T., Laguesse, S., Phamluong, K., Morisot, N., Wegner, S.A., Ron, D., The First Alcohol Drink Triggers mTORC1-Dependent Synaptic Plasticity in Nucleus Accumbens Dopamine D1 Receptor Neurons. J. Neurosci. 36 (2016), 701–713.
Ben Hamida, S., Neasta, J., Lasek, A.W., Kharazia, V., Zou, M., Carnicella, S., Janak, P.H., Ron, D., The small G protein H-Ras in the mesolimbic system is a molecular gateway to alcohol-seeking and excessive drinking behaviors. J. Neurosci. 32 (2012), 15849–15858.
Bokoch, G.M., Biology of the Rap proteins, members of the ras superfamily of GTP-binding proteins. Biochem. J. 289 (1993), 17–24.
Buffington, S.A., Huang, W., Costa-Mattioli, M., Translational control in synaptic plasticity and cognitive dysfunction. Annu. Rev. Neurosci. 37 (2014), 17–38.
Cingolani, L.A., Goda, Y., Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat. Rev. Neurosci. 9 (2008), 344–356.
Collart, M.A., Panasenko, O.O., The Ccr4–not complex. Gene 492 (2012), 42–53.
Corbit, L.H., Nie, H., Janak, P.H., Habitual alcohol seeking: time course and the contribution of subregions of the dorsal striatum. Biol. Psychiatry 72 (2012), 389–395.
Corbit, L.H., Fischbach, S.C., Janak, P.H., Nucleus accumbens core and shell are differentially involved in general and outcome-specific forms of Pavlovian-instrumental transfer with alcohol and sucrose rewards. Eur. J. Neurosci. 43 (2016), 1229–1236.
del Prete, M.J., Vernal, R., Dolznig, H., Müllner, E.W., Garcia-Sanz, J.A., Isolation of polysome-bound mRNA from solid tissues amenable for RT-PCR and profiling experiments. RNA 13 (2007), 414–421.
Enoch, M.A., Goldman, D., Problem drinking and alcoholism: diagnosis and treatment. Am. Fam. Physician 65 (2002), 441–448.
Fischer, C., Christ, E., Korf, H.W., von Gall, C., Tafa-3 encoding for a secretory peptide is expressed in the mouse pars tuberalis and is affected by melatonin 1 receptor deficiency. Gen. Comp. Endocrinol. 177 (2012), 98–103.
Floresco, S.B., The nucleus accumbens: an interface between cognition, emotion, and action. Annu. Rev. Psychol. 66 (2015), 25–52.
Gandin, V., Masvidal, L., Hulea, L., Gravel, S.P., Cargnello, M., McLaughlan, S., Cai, Y., Balanathan, P., Morita, M., Rajakumar, A., et al. nanoCAGE reveals 5′ UTR features that define specific modes of translation of functionally related MTOR-sensitive mRNAs. Genome Res. 26 (2016), 636–648.
Gentry, R.T., Dole, V.P., Why does a sucrose choice reduce the consumption of alcohol in C57BL/6J mice?. Life Sci. 40 (1987), 2191–2194.
Griffin, W.C. 3rd, Lopez, M.F., Becker, H.C., Intensity and duration of chronic ethanol exposure is critical for subsequent escalation of voluntary ethanol drinking in mice. Alcohol. Clin. Exp. Res. 33 (2009), 1893–1900.
Hanley, J.G., Actin-dependent mechanisms in AMPA receptor trafficking. Front. Cell. Neurosci., 8, 2014, 381.
Hearing, M.C., Jedynak, J., Ebner, S.R., Ingebretson, A., Asp, A.J., Fischer, R.A., Schmidt, C., Larson, E.B., Thomas, M.J., Reversal of morphine-induced cell-type-specific synaptic plasticity in the nucleus accumbens shell blocks reinstatement. Proc. Natl. Acad. Sci. USA 113 (2016), 757–762.
Hering, H., Sheng, M., Dendritic spines: structure, dynamics and regulation. Nat. Rev. Neurosci. 2 (2001), 880–888.
Hotulainen, P., Hoogenraad, C.C., Actin in dendritic spines: connecting dynamics to function. J. Cell Biol. 189 (2010), 619–629.
Huang, W., Zhu, P.J., Zhang, S., Zhou, H., Stoica, L., Galiano, M., Krnjević K., Roman, G., Costa-Mattioli, M., mTORC2 controls actin polymerization required for consolidation of long-term memory. Nat. Neurosci. 16 (2013), 441–448.
Huston, J.P., Silva, M.A., Topic, B., Müller, C.P., What's conditioned in conditioned place preference?. Trends Pharmacol. Sci. 34 (2013), 162–166.
Hwa, L.S., Chu, A., Levinson, S.A., Kayyali, T.M., DeBold, J.F., Miczek, K.A., Persistent escalation of alcohol drinking in C57BL/6J mice with intermittent access to 20% ethanol. Alcohol. Clin. Exp. Res. 35 (2011), 1938–1947.
Hyman, S.E., Addiction: a disease of learning and memory. Am. J. Psychiatry 162 (2005), 1414–1422.
Jewell, J.L., Flores, F., Guan, K.L., Micro(RNA) managing by mTORC1. Mol. Cell 57 (2015), 575–576.
Kasai, H., Matsuzaki, M., Noguchi, J., Yasumatsu, N., Nakahara, H., Structure-stability-function relationships of dendritic spines. Trends Neurosci. 26 (2003), 360–368.
Laguesse, S., Morisot, N., Phamluong, K., Ron, D., Region specific activation of the AKT and mTORC1 pathway in response to excessive alcohol intake in rodents. Addict. Biol., 2016, 10.1111/adb.12464 Published online October 20, 2016.
Lasek, A.W., Janak, P.H., He, L., Whistler, J.L., Heberlein, U., Downregulation of mu opioid receptor by RNA interference in the ventral tegmental area reduces ethanol consumption in mice. Genes Brain Behav. 6 (2007), 728–735.
Lee, K.W., Kim, Y., Kim, A.M., Helmin, K., Nairn, A.C., Greengard, P., Cocaine-induced dendritic spine formation in D1 and D2 dopamine receptor-containing medium spiny neurons in nucleus accumbens. Proc. Natl. Acad. Sci. USA 103 (2006), 3399–3404.
Legastelois, R., Darcq, E., Wegner, S.A., Lombroso, P.J., Ron, D., Striatal-enriched protein tyrosine phosphatase controls responses to aversive stimuli: implication for ethanol drinking. PLoS ONE, 10, 2015, e0127408.
Li, Z., Wu, Y., Baraban, J.M., The Translin/Trax RNA binding complex: clues to function in the nervous system. Biochim. Biophys. Acta 1779 (2008), 479–485.
Li, J., Kim, S.G., Blenis, J., Rapamycin: one drug, many effects. Cell Metab. 19 (2014), 373–379.
Li, G., Wang, Y., Yan, M., Xu, Y., Song, X., Li, Q., Zhang, J., Ma, H., Wu, Y., Inhibition of actin polymerization in the NAc shell inhibits morphine-induced CPP by disrupting its reconsolidation. Sci. Rep., 5, 2015, 16283.
Liu, F., Laguesse, S., Legastelois, R., Morisot, N., Ben Hamida, S., Ron, D., mTORC1-dependent translation of collapsin response mediator protein-2 drives neuroadaptations underlying excessive alcohol-drinking behaviors. Mol. Psychiatry 22 (2017), 89–101.
Ma, X.M., Blenis, J., Molecular mechanisms of mTOR-mediated translational control. Nat. Rev. Mol. Cell Biol. 10 (2009), 307–318.
Man, H.Y., GluA2-lacking, calcium-permeable AMPA receptors–inducers of plasticity?. Curr. Opin. Neurobiol. 21 (2011), 291–298.
Maruoka, H., Konno, D., Hori, K., Sobue, K., Collaboration of PSD-Zip70 with its binding partner, SPAR, in dendritic spine maturity. J. Neurosci. 25 (2005), 1421–1430.
McCutcheon, J.E., Wang, X., Tseng, K.Y., Wolf, M.E., Marinelli, M., Calcium-permeable AMPA receptors are present in nucleus accumbens synapses after prolonged withdrawal from cocaine self-administration but not experimenter-administered cocaine. J. Neurosci. 31 (2011), 5737–5743.
Morisot, N., Novotny, C.J., Shokat, K.M., Ron, D., A new generation of mTORC1 inhibitor attenuates alcohol intake and reward in mice. Addict Biol., 2017 Published online July 6, 2017. http://dx.doi.org/10.1111/adb.12528.
Morita, M., Gravel, S.P., Chénard, V., Sikström, K., Zheng, L., Alain, T., Gandin, V., Avizonis, D., Arguello, M., Zakaria, C., et al. mTORC1 controls mitochondrial activity and biogenesis through 4E-BP-dependent translational regulation. Cell Metab. 18 (2013), 698–711.
Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L., Wold, B., Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5 (2008), 621–628.
Neasta, J., Ben Hamida, S., Yowell, Q., Carnicella, S., Ron, D., Role for mammalian target of rapamycin complex 1 signaling in neuroadaptations underlying alcohol-related disorders. Proc. Natl. Acad. Sci. USA 107 (2010), 20093–20098.
Neasta, J., Barak, S., Hamida, S.B., Ron, D., mTOR complex 1: a key player in neuroadaptations induced by drugs of abuse. J. Neurochem. 130 (2014), 172–184.
Pak, D.T., Yang, S., Rudolph-Correia, S., Kim, E., Sheng, M., Regulation of dendritic spine morphology by SPAR, a PSD-95-associated RapGAP. Neuron 31 (2001), 289–303.
Pfaff, J., Hennig, J., Herzog, F., Aebersold, R., Sattler, M., Niessing, D., Meister, G., Structural features of Argonaute-GW182 protein interactions. Proc. Natl. Acad. Sci. USA 110 (2013), E3770–E3779.
Potter, L.R., Guanylyl cyclase structure, function and regulation. Cell. Signal. 23 (2011), 1921–1926.
Reim, D., Weis, T.M., Halbedl, S., Delling, J.P., Grabrucker, A.M., Boeckers, T.M., Schmeisser, M.J., The Shank3 Interaction Partner ProSAPiP1 Regulates Postsynaptic SPAR Levels and the Maturation of Dendritic Spines in Hippocampal Neurons. Front. Synaptic Neurosci., 8, 2016, 13.
Renteria, R., Buske, T.R., Morrisett, R.A., Long-term subregion-specific encoding of enhanced ethanol intake by D1DR medium spiny neurons of the nucleus accumbens. Addict. Biol., 2017, 10.1111/adb.12526 Published online June 28, 2017.
Russo, S.J., Dietz, D.M., Dumitriu, D., Morrison, J.H., Malenka, R.C., Nestler, E.J., The addicted synapse: mechanisms of synaptic and structural plasticity in nucleus accumbens. Trends Neurosci. 33 (2010), 267–276.
Ryu, J., Futai, K., Feliu, M., Weinberg, R., Sheng, M., Constitutively active Rap2 transgenic mice display fewer dendritic spines, reduced extracellular signal-regulated kinase signaling, enhanced long-term depression, and impaired spatial learning and fear extinction. J. Neurosci. 28 (2008), 8178–8188.
Shirao, T., González-Billault, C., Actin filaments and microtubules in dendritic spines. J. Neurochem. 126 (2013), 155–164.
Sholl, D.A., Dendritic organization in the neurons of the visual and motor cortices of the cat. J. Anat. 87 (1953), 387–406.
Smith, D.L., Pozueta, J., Gong, B., Arancio, O., Shelanski, M., Reversal of long-term dendritic spine alterations in Alzheimer disease models. Proc. Natl. Acad. Sci. USA 106 (2009), 16877–16882.
Sonenberg, N., Hinnebusch, A.G., Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136 (2009), 731–745.
Spiga, S., Talani, G., Mulas, G., Licheri, V., Fois, G.R., Muggironi, G., Masala, N., Cannizzaro, C., Biggio, G., Sanna, E., Diana, M., Hampered long-term depression and thin spine loss in the nucleus accumbens of ethanol-dependent rats. Proc. Natl. Acad. Sci. USA 111 (2014), E3745–E3754.
Spilker, C., Kreutz, M.R., RapGAPs in brain: multipurpose players in neuronal Rap signalling. Eur. J. Neurosci. 32 (2010), 1–9.
Thoreen, C.C., Chantranupong, L., Keys, H.R., Wang, T., Gray, N.S., Sabatini, D.M., A unifying model for mTORC1-mediated regulation of mRNA translation. Nature 485 (2012), 109–113.
Tom Tang, Y., Emtage, P., Funk, W.D., Hu, T., Arterburn, M., Park, E.E., Rupp, F., TAFA: a novel secreted family with conserved cysteine residues and restricted expression in the brain. Genomics 83 (2004), 727–734.
Trapnell, C., Pachter, L., Salzberg, S.L., TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25 (2009), 1105–1111.
Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D.R., Pimentel, H., Salzberg, S.L., Rinn, J.L., Pachter, L., Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7 (2012), 562–578.
Uys, J.D., McGuier, N.S., Gass, J.T., Griffin, W.C. 3rd, Ball, L.E., Mulholland, P.J., Chronic intermittent ethanol exposure and withdrawal leads to adaptations in nucleus accumbens core postsynaptic density proteome and dendritic spines. Addict. Biol. 21 (2016), 560–574.
Volkow, N.D., Morales, M., The Brain on Drugs: From Reward to Addiction. Cell 162 (2015), 712–725.
Wang, Z., Gerstein, M., Snyder, M., RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10 (2009), 57–63.
Wang, J., Lanfranco, M.F., Gibb, S.L., Yowell, Q.V., Carnicella, S., Ron, D., Long-lasting adaptations of the NR2B-containing NMDA receptors in the dorsomedial striatum play a crucial role in alcohol consumption and relapse. J. Neurosci. 30 (2010), 10187–10198.
Wang, J., Cheng, Y., Wang, X., Roltsch Hellard, E., Ma, T., Gil, H., Ben Hamida, S., Ron, D., Alcohol Elicits Functional and Structural Plasticity Selectively in Dopamine D1 Receptor-Expressing Neurons of the Dorsomedial Striatum. J. Neurosci. 35 (2015), 11634–11643.
Warnault, V., Darcq, E., Levine, A., Barak, S., Ron, D., Chromatin remodeling–a novel strategy to control excessive alcohol drinking. Transl. Psychiatry, 3, 2013, e231.
Wendholt, D., Spilker, C., Schmitt, A., Dolnik, A., Smalla, K.H., Proepper, C., Bockmann, J., Sobue, K., Gundelfinger, E.D., Kreutz, M.R., Boeckers, T.M., ProSAP-interacting protein 1 (ProSAPiP1), a novel protein of the postsynaptic density that links the spine-associated Rap-Gap (SPAR) to the scaffolding protein ProSAP2/Shank3. J. Biol. Chem. 281 (2006), 13805–13816.
Wolf, M.E., Tseng, K.Y., Calcium-permeable AMPA receptors in the VTA and nucleus accumbens after cocaine exposure: when, how, and why?. Front. Mol. Neurosci., 5, 2012, 72.
World Health Organization. WHO Global Status Report on Alcohol 2004. 2004, World Health Organization.
Xie, Z., Huganir, R.L., Penzes, P., Activity-dependent dendritic spine structural plasticity is regulated by small GTPase Rap1 and its target AF-6. Neuron 48 (2005), 605–618.
Young, E.J., Aceti, M., Griggs, E.M., Fuchs, R.A., Zigmond, Z., Rumbaugh, G., Miller, C.A., Selective, retrieval-independent disruption of methamphetamine-associated memory by actin depolymerization. Biol. Psychiatry 75 (2014), 96–104.
Zapata, A., Gonzales, R.A., Shippenberg, T.S., Repeated ethanol intoxication induces behavioral sensitization in the absence of a sensitized accumbens dopamine response in C57BL/6J and DBA/2J mice. Neuropsychopharmacology 31 (2006), 396–405.
Zhang, J., Liu, H., Yao, Q., Yu, X., Chen, Y., Cui, R., Wu, B., Zheng, L., Zuo, J., Huang, Z., et al. Structural basis for single-stranded RNA recognition and cleavage by C3PO. Nucleic Acids Res. 44 (2016), 9494–9504.
Zhu, J.J., Qin, Y., Zhao, M., Van Aelst, L., Malinow, R., Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell 110 (2002), 443–455.
Zhu, Y., Pak, D., Qin, Y., McCormack, S.G., Kim, M.J., Baumgart, J.P., Velamoor, V., Auberson, Y.P., Osten, P., van Aelst, L., et al. Rap2-JNK removes synaptic AMPA receptors during depotentiation. Neuron 46 (2005), 905–916.