Skip to main content

Advertisement

SpringerLink
Log in

Region-specific changes in markers of neuroplasticity revealed in HIV-1 transgenic rats by low-dose methamphetamine

  • Short Communication
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

Methamphetamine abuse co-occurring with HIV infection presents neuropathology in brain regions that mediate reward and motivation. A neuronal signaling cascade altered acutely by meth and some HIV-1 proteins is the mitogen-activated protein kinase (MAPK) pathway. It remains unknown if chronic co-exposure to meth and HIV-1 proteins converge on MAPK in vivo. To make this determination, we studied young adult Fischer 344 HIV-1 transgenic (Tg) and non-Tg rats that self-administered meth (0.02–0.04 mg/kg/0.05 ml iv infusion, 2 h/day for 21 days) and their saline-yoked controls. One day following the operant task, rats were killed. Brain regions involved in reward-motivation [i.e., nucleus accumbens (NA) and ventral pallidum (VP)], were assayed for a MAPK cascade protein, extracellular signal-regulated kinase (ERK), and a downstream transcription factor, ΔFosB. In the NA, activated (phosphorylated; p) ERK-to-ERK ratio (pERK/ERK) was increased in meth-exposed Tg rats versus saline Tg controls, and versus meth non-Tg rats. ΔFosB was increased in meth Tg rats versus saline and meth non-Tg rats. Assessment of two targets of ΔFosB-regulated transcription revealed (1) increased dopamine D1 receptor (D1R) immunoreactivity in the NA shell of Tg-meth rats versus saline Tg controls, but (2) no changes in the AMPA receptor subunit, GluA2. No changes related to genotype or meth occurred for ERK, ΔFosB or D1R protein in the VP. Results reveal a region-specific activation of ERK, and increases in ΔFosB and D1R expression induced by HIV-1 proteins and meth. Such effects may contribute to the neuronal and behavioral pathology associated with meth/HIV comorbidity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

References

  • Abekawa T, Ohmori T, Koyama T (1994) Effects of repeated administration of a high dose of methamphetamine on dopamine and glutamate release in rat striatum and nucleus accumbens. Brain Res 643:276–281

    CAS  PubMed  Google Scholar 

  • Ambrosio E, Goldberg SR, Elmer GI (1995) Behavior genetic investigation of the relationship between spontaneous locomotor activity and the acquisition of morphine self-administration behavior. Behav Pharmacol 6:229–237

    CAS  PubMed  Google Scholar 

  • Austin MC, Kalivas PW (1991) Dopaminergic involvement in locomotion elicited from the ventral pallidum/substantia innominata. Brain Res 542:123–131

    CAS  PubMed  Google Scholar 

  • Boudreau AC, Wolf ME (2005) Behavioral sensitization to cocaine is associated with increased AMPA receptor surface expression in the nucleus accumbens. J Neurosci 25:9144–9151

    CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Brand T, Spanagel R, Schneider M (2012) Decreased reward sensitivity in rats from the Fischer344 strain compared to Wistar rats is paralleled by differences in endocannabinoid signaling. PLoS One 7:e31169

    CAS  PubMed  PubMed Central  Google Scholar 

  • Britt JP, Benaliouad F, McDevitt RA, Stuber GD, Wise RA, Bonci A (2012) Synaptic and behavioral profile of multiple glutamatergic inputs to the nucleus accumbens. Neuron 76:790–803

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bruce-Keller AJ, Chauhan A, Dimayuga FO, Gee J, Keller JN, Nath A (2003) Synaptic transport of human immunodeficiency virus-Tat protein causes neurotoxicity and gliosis in rat brain. J Neurosci 23:8417–8422

    CAS  PubMed  Google Scholar 

  • Busca R, Pouyssegur J, Lenormand P (2016) ERK1 and ERK2 map kinases: specific roles or functional redundancy? Front Cell Dev Biol 4:53

    PubMed  PubMed Central  Google Scholar 

  • Cadet JL, Ladenheim B, Hirata H (1998) Effects of toxic doses of methamphetamine (METH) on dopamine D1 receptors in the mouse brain. Brain Res 786:240–242

    CAS  PubMed  Google Scholar 

  • Chen J, Kelz MB, Hope BT, Nakabeppu Y, Novakova J (1997) Chronic Fos-related antigens: stable variants of FosB induced in brain by chronic treatments. J Neurosci 17:4933–4941

    CAS  PubMed  Google Scholar 

  • Colby CR, Whisler K, Steffen C, Nestler EJ, Self DW (2003) Striatal cell type-specific overexpression of DeltaFosB enhances incentive for cocaine. J Neurosci 23:2488–2493

    CAS  PubMed  Google Scholar 

  • Day JJ, Carelli RM (2007) The nucleus accumbens and Pavlovian reward learning. Neuroscientist 13:148–159

    PubMed  PubMed Central  Google Scholar 

  • Di Chiara G (2002) Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav Brain Res 137(1–2):75–114

    PubMed  Google Scholar 

  • Dougan S, Patel B, Tosswill JH, Sinka K (2005) Diagnoses of HIV-1 and HIV-2 in England, Wales, and Northern Ireland associated with west Africa. Sex Transm Infect 81:338–341

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ferris MJ, Mactutus CF, Booze RM (2008) Neurotoxic profiles of HIV, psychostimulant drugs of abuse, and their concerted effect on the brain: current status of dopamine system vulnerability in NeuroAIDS. Neurosci Biobehav Rev 32:883–909

    CAS  PubMed  PubMed Central  Google Scholar 

  • Filip M, Siwanowicz J (2001) Implication of the nucleus accumbens shell, but not core, in the acute and sensitizing effects of cocaine in rats. Pol J Pharmacol 53:459–466

    CAS  PubMed  Google Scholar 

  • Fremeau RT Jr, Duncan GE, Fornaretto M-G, Dearry A, Gingrich JA, Breese GR, Caron MG (1991) Localization of D1 dopamine receptor mRNA in brain supports a role in cognitive, affective, and neuroendocrine aspects of dopaminergic neurotransmission. Proc Natl Acad Sci USA 88:3772–3776

    CAS  PubMed  Google Scholar 

  • Ghasemzadeh MB, Mueller C, Vasudevan P (2009) Behavioral sensitization to cocaine is associated with increased glutamate receptor trafficking to the postsynaptic density after extended withdrawal period. Neuroscience 159:414–426

    CAS  PubMed  Google Scholar 

  • Graves SM, Napier TC (2011) Mirtazapine alters cue-associated methamphetamine seeking in rats. Biol Psychiatry 69:275–281

    CAS  PubMed  Google Scholar 

  • Graves SM, Clark MJ, Traynor JR, Hu XT, Napier TC (2015) Nucleus accumbens shell excitability is decreased by methamphetamine self-administration and increased by 5-HT receptor inverse agonism and agonism. Neuropharmacology 89:113–121

    Google Scholar 

  • Hayashi T, Justinova Z, Hayashi E, Cormaci G, Mori T, Tsai SY, Barnes C, Goldberg SR, Su TP (2010) Regulation of sigma-1 receptors and endoplasmic reticulum chaperones in the brain of methamphetamine self-administering rats. J Pharmacol Exp Ther 332:1054–1063

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hebert MA, O’Callaghan JP (2000) Protein phosphorylation cascades associated with methamphetamine- induced glial activation. Ann N Y Acad Sci 914:238–262

    CAS  PubMed  Google Scholar 

  • Herrold AA, Shen F, Graham MP, Harper LK, Specio SE, Tedford CE, Napier TC (2009) Mirtazapine treatment after conditioning with methamphetamine alters subsequent expression of place preference. Drug Alcohol Depend 99:231–239

    CAS  PubMed  Google Scholar 

  • Herrold AA, Persons AL, Napier TC (2013) Cellular distribution of AMPA receptor subunits and mGlu5 following acute and repeated administration of morphine or methamphetamine. J Neurochem 126(4):503–517

    CAS  PubMed  Google Scholar 

  • Hostetler CM, Bales KL (2012) DeltaFosB is increased in the nucleus accumbens by amphetamine but not social housing or isolation in the prairie vole. Neuroscience 210:266–274

    CAS  PubMed  Google Scholar 

  • Ingersoll K (2004) The impact of psychiatric symptoms, drug use, and medication regimen on non-adherence to HIV treatment. AIDS Care 16:199–211

    CAS  PubMed  Google Scholar 

  • Keeler BE, Lallemand P, Patel MM, de Castro Bras LE, Clemens S (2016) Opposing aging-related shift of excitatory dopamine D1 and inhibitory D3 receptor protein expression in striatum and spinal cord. J Neurophysiol 115:363–369

    CAS  PubMed  Google Scholar 

  • Kelly MA, Low MJ, Rubinstein M, Phillips TJ (2008) Role of dopamine D1-like receptors in methamphetamine locomotor responses of D2 receptor knockout mice. Genes Brain Behav 7:568–577

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kelz MB, Chen J, Carlezon WA Jr, Whisler K, Gilden L, Beckmann AM, Steffen C, Zhang YJ, Marotti L, Self DW, Tkatch T, Baranauskas G, Surmeier DJ, Neve RL, Duman RS, Picciotto MR, Nestler EJ (1999) Expression of the transcription factor deltaFosB in the brain controls sensitivity to cocaine. Nature 401:272–276

    CAS  PubMed  Google Scholar 

  • Kosten TA, Miserendino MJD, Haile CN, DeCaprio JL, Jatlow PI, Nestler EJ (1997) Acquisition and maintenance of intravenous cocaine self- administration in Lewis and Fischer inbred rat strains. Brain Res 778:418–429

    CAS  PubMed  Google Scholar 

  • Kousik SM, Napier TC, Ross RD, Sumner DR, Carvey PM (2014) Dopamine receptors and the persistent neurovascular dysregulation induced by methamphetamine self-administration in rats. J Pharmacol Exp Ther 351:432–439

    PubMed  Google Scholar 

  • Krasnova IN, Chiflikyan M, Justinova Z, McCoy MT, Ladenheim B, Jayanthi S, Quintero C, Brannock C, Barnes C, Adair JE, Lehrmann E, Kobeissy FH, Gold MS, Becker KG, Goldberg SR, Cadet JL (2013) CREB phosphorylation regulates striatal transcriptional responses in the self-administration model of methamphetamine addiction in the rat. Neurobiol Dis 58:132–143

    Google Scholar 

  • Kuroda KO, Meaney MJ, Uetani N, Fortin Y, Ponton A, Kato T (2007) ERK-FosB signaling in dorsal MPOA neurons plays a major role in the initiation of parental behavior in mice. Mol Cell Neurosci 36:121–131

    CAS  PubMed  Google Scholar 

  • Liu HF, Zhou WH, Zhu HQ, Lai MJ, Chen WS (2007) Microinjection of M(5) muscarinic receptor antisense oligonucleotide into VTA inhibits FosB expression in the NAc and the hippocampus of heroin sensitized rats. Neurosci Bull 23:1–8

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lu XY, Ghasemzadeh MB, Kalivas PW (1998) Expression of D1 receptor, D2 receptor, substance P and enkephalin messenger RNAs in the neurons projecting from the nucleus accumbens. Neuroscience 82:767–780

    CAS  PubMed  Google Scholar 

  • Mahler SV, Vazey EM, Beckley JT, Keistler CR, McGlinchey EM, Kaufling J, Wilson SP, Deisseroth K, Woodward JJ, Aston-Jones G (2014) Designer receptors show role for ventral pallidum input to ventral tegmental area in cocaine seeking. Nat Neurosci 17:577–585

    CAS  PubMed  PubMed Central  Google Scholar 

  • Malik AN, Vierbuchen T, Hemberg M, Rubin AA, Ling E, Couch CH, Stroud H, Spiegel I, Farh KK, Harmin DA, Greenberg ME (2014) Genome-wide identification and characterization of functional neuronal activity-dependent enhancers. Nat Neurosci 17:1330–1339

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maragos WF, Young KL, Turchan JT, Guseva M, Pauly JR, Nath A, Cass WA (2002) Human immunodeficiency virus-1 Tat protein and methamphetamine interact synergistically to impair striatal dopaminergic function. J Neurochem 83:955–963

    CAS  PubMed  Google Scholar 

  • Martin S, Manzanares J, Corchero J, Garcia-Lecumberri C, Crespo JA, Fuentes JA, Ambrosio E (1999) Differential basal proenkephalin gene expression in dorsal striatum and nucleus accumbens, and vulnerability to morphine self-administration in Fischer 344 and Lewis rats. Brain Res 821:350–355

    CAS  PubMed  Google Scholar 

  • Maslowski-Cobuzzi RJ, Napier TC (1994) Activation of dopaminergic neurons modulates ventral pallidal responses evoked by amygdala stimulation. Neuroscience 62:1103–1120

    CAS  PubMed  Google Scholar 

  • Mazzucchelli C, Vantaggiato C, Ciamei A, Fasano S, Pakhotin P, Krezel W, Welzl H, Wolfer DP, Pagès G, Valverde O, Marowsky A, Porrazzo A, Orban PC, Maldonado R, Ehrengruber MU, Cestari V, Lipp HP, Chapman PF, Pouysségur J, Brambilla R (2002) Knockout of ERK1 MAP kinase enhances synaptic plasticity in the striatum and facilitates striatal-mediated learning and memory. Neuron 34(5):807–820

    CAS  PubMed  Google Scholar 

  • McClung CA, Nestler EJ (2003) Regulation of gene expression and cocaine reward by CREB and DeltaFosB. Nat Neurosci 6:1208–1215

    CAS  PubMed  Google Scholar 

  • McCutcheon JE, Wang X, Tseng KY, Wolf ME, Marinelli M (2011) Calcium-permeable AMPA receptors are present in nucleus accumbens synapses after prolonged withdrawal from cocaine self-administration but not experimenter-administered cocaine. J Neurosci 31:5737–5743

    CAS  PubMed  PubMed Central  Google Scholar 

  • McDaid J, Dallimore JE, Mackie A, Napier TC (2006a) Changes in accumbal and ventral pallidal pCREB and deltaFosB in morphine-sensitized rats: correlations with receptor-evoked electrophysiological measures in the ventral pallidum. Neuropsychopharmacology 31:1212–1226

    CAS  PubMed  PubMed Central  Google Scholar 

  • McDaid J, Graham MP, Napier TC (2006b) Methamphetamine-induced sensitization differentially alters pCREB and FosB throughout the limbic circuit of the mammalian brain. Mol Pharmacol 70:2064–2074

    CAS  PubMed  Google Scholar 

  • McIntosh S, Sexton T, Pattison LP, Childers SR, Hemby SE (2015) Increased sensitivity to cocaine self-administration in HIV-1 transgenic rats is associated with changes in striatal dopamine transporter binding. J Neuroimmune Pharmacol 10:493–505

    PubMed  PubMed Central  Google Scholar 

  • Mellins CA, Kang E, Leu CS, Havens JF, Chesney MA (2003) Longitudinal study of mental health and psychosocial predictors of medical treatment adherence in mothers living with HIV disease. AIDS Patient Care STDS 17:407–416

    PubMed  Google Scholar 

  • Mellins CA, Havens JF, McDonnell C, Lichtenstein C, Uldall K, Chesney M, Santamaria EK, Bell J (2009) Adherence to antiretroviral medications and medical care in HIV-infected adults diagnosed with mental and substance abuse disorders. AIDS Care 21:168–177

    PubMed  PubMed Central  Google Scholar 

  • Mickiewicz AL, Napier TC (2011) Repeated exposure to morphine alters surface expression of AMPA receptors in the rat medial prefrontal cortex. Eur J Neurosci 33:259–265

    PubMed  Google Scholar 

  • Midde NM, Gomez AM, Harrod SB, Zhu J (2011) Genetically expressed HIV-1 viral proteins attenuate nicotine-induced behavioral sensitization and alter mesocorticolimbic ERK and CREB signaling in rats. Pharmacol Biochem Behav 98:587–597

    CAS  PubMed  PubMed Central  Google Scholar 

  • Muller DL, Unterwald EM (2005) D1 dopamine receptors modulate deltaFosB induction in rat striatum after intermittent morphine administration. J Pharmacol Exp Ther 314:148–154

    CAS  PubMed  Google Scholar 

  • Nakabeppu Y, Nathans D (1991) A naturally occurring truncated form of fosB that inhibits Fos/Jun transcriptional activity. Cell 64:751–759

    CAS  PubMed  Google Scholar 

  • Napier TC, Maslowski RJ (1994) Electrophysiological verification for the presence of D1 and D2 dopamine receptors within the ventral pallidum. Synapse 17:160–166

    CAS  PubMed  Google Scholar 

  • Nestler EJ, Barrot M, Self DW (2001) Delta FosB: a sustained molecular switch for addiction. Proc Natl Acad Sci USA 98:11042–11046

    CAS  PubMed  Google Scholar 

  • New DR, Maggirwar SB, Epstein LG, Dewhurst S, Gelbard HA (1998) HIV-1 Tat induces neuronal death via tumor necrosis factor-alpha and activation of non-N-methyl-D-aspartate receptors by a NFkappaB-independent mechanism. J Biol Chem 273:17852–17858

    CAS  PubMed  Google Scholar 

  • O’Dell SJ, Weihmuller FB, Marshall JF (1991) Multiple methamphetamine injections induce marked increases in extracellular striatal dopamine which correlate with subsequent neurotoxicity. Brain Res 564:256–260

    PubMed  Google Scholar 

  • Okubo T, Sato A, Okamoto H, Sato T, Sasaoka T (2017) Differential behavioral phenotypes of dopamine D1 receptor knockdown mice at the embryonic, postnatal, and adult stages. Int J Dev Neurosci 66:1–8

    PubMed  Google Scholar 

  • Paris JJ, Carey AN, Shay CF, Gomes SM, He JJ, McLaughlin JP (2014) Effects of conditional central expression of HIV-1 Tat protein to potentiate cocaine-mediated psychostimulation and reward among male mice. Neuropsychopharmacology 39:380–388

    CAS  PubMed  Google Scholar 

  • Parkinson JA, Olmstead MC, Burns LH, Robbins TW, Everitt BJ (1999) Dissociation in effects of lesions of the nucleus accumbens core and shell on appetitive pavlovian approach behavior and the potentiation of conditioned reinforcement and locomotor activity by D-amphetamine. J Neurosci 19:2401–2411

    CAS  PubMed  Google Scholar 

  • Paxinos G, Watson C (2009) The rat brain in stereotaxic coordinates, 6th edn. Academic Press, London, UK

    Google Scholar 

  • Peng J, Vigorito M, Liu X, Zhou D, Wu X, Chang SL (2010) The HIV-1 transgenic rat as a model for HIV-1 infected individuals on HAART. J Neuroimmunol 218:94–101

    CAS  PubMed  Google Scholar 

  • Persons AL, Bradaric BD, Dodiya HB, Ohene-Nyako M, Forsyth CB, Keshavarzian A, Shaikh M, Napier TC (2018) Colon dysregulation in methamphetamine self-administering HIV-1 transgenic rats. PLoS ONE 13:e0190078

    PubMed  PubMed Central  Google Scholar 

  • Picetti R, Ho A, Butelman ER, Kreek MJ (2010) Dose preference and dose escalation in extended-access cocaine self-administration in Fischer and Lewis rats. Psychopharmacology 211:313–323

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rajasingham R, Mimiaga MJ, White JM, Pinkston MM, Baden RP, Mitty JA (2012) A systematic review of behavioral and treatment outcome studies among HIV-infected men who have sex with men who abuse crystal methamphetamine. AIDS Patient Care STDS 26:36–52

    PubMed  PubMed Central  Google Scholar 

  • Reid W, Sadowska M, Denaro F, Rao S, Foulke J Jr, Hayes N, Jones O, Doodnauth D, Davis H, Sill A, O’Driscoll P, Huso D, Fouts T, Lewis G, Hill M, Kamin-Lewis R, Wei C, Ray P, Gallo RC, Reitz M, Bryant J (2001) An HIV-1 transgenic rat that develops HIV-related pathology and immunologic dysfunction. Proc Natl Acad Sci USA 98:9271–9276

    CAS  PubMed  Google Scholar 

  • Riviere GJ, Byrnes KA, Gentry WB, Owens SM (1999) Spontaneous locomotor activity and pharmacokinetics of intravenous methamphetamine and its metabolite amphetamine in the rat. J Pharmacol Exp Ther 291:1220–1226

    CAS  PubMed  Google Scholar 

  • Robison AJ, Vialou V, Mazei-Robison M, Feng J, Kourrich S, Collins M, Wee S, Koob G, Turecki G, Neve R, Thomas M, Nestler EJ (2013) Behavioral and structural responses to chronic cocaine require a feedforward loop involving DeltaFosB and calcium/calmodulin-dependent protein kinase II in the nucleus accumbens shell. J Neurosci 33:4295–4307

    CAS  PubMed  PubMed Central  Google Scholar 

  • Root DH, Melendez RI, Zaborszky L, Napier TC (2015) The ventral pallidum: Subregion-specific functional anatomy and roles in motivated behaviors. Prog Neurobiol 130:29–70

    PubMed  PubMed Central  Google Scholar 

  • Ruffle JK (2014) Molecular neurobiology of addiction: what’s all the (Delta)FosB about? Am J Drug Alcohol Abuse 40:428–437

    PubMed  Google Scholar 

  • Schrager JA, Der M, Marsh V JW (2002) HIV Nef increases T cell ERK MAP kinase activity. J Biol Chem 277:6137–6142

    CAS  PubMed  Google Scholar 

  • Sellings LH, Clarke PB (2003) Segregation of amphetamine reward and locomotor stimulation between nucleus accumbens medial shell and core. J Neurosci 23:6295–6303

    CAS  PubMed  Google Scholar 

  • Silvers JM, Aksenova MV, Aksenov MY, Mactutus CF, Booze RM (2007) Neurotoxicity of HIV-1 Tat protein: involvement of D1 dopamine receptor. Neurotoxicology 28:1184–1190

    CAS  PubMed  PubMed Central  Google Scholar 

  • Somkuwar SS, Fannon MJ, Head BP, Mandyam CD (2016) Methamphetamine reduces expression of caveolin-1 in the dorsal striatum: Implication for dysregulation of neuronal function. Neuroscience 328:147–156

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stuber GD, Sparta DR, Stamatakis AM, van Leeuwen WA, Hardjoprajitno JE, Cho S, Tye KM, Kempadoo KA, Zhang F, Deisseroth K, Bonci A (2011) Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature 475:377–380

    CAS  PubMed  PubMed Central  Google Scholar 

  • Swanson LW (1982) The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 9:321–353

    CAS  PubMed  Google Scholar 

  • Toggas SM, Masliah E, Mucke L (1996) Prevention of HIV-1 gp120-induced neuronal damage in the central nervous system of transgenic mice by the NMDA receptor antagonist memantine. Brain Res 706:303–307

    CAS  PubMed  Google Scholar 

  • Tornatore C, Nath A, Amemiya K, Major EO (1991) Persistent human immunodeficiency virus type 1 infection in human fetal glial cells reactivated by T-cell factor(s) or by the cytokines tumor necrosis factor alpha and interleukin-1 beta. J Virol 65:6094–6100

    CAS  PubMed  PubMed Central  Google Scholar 

  • Toschi E, Bacigalupo I, Strippoli R, Chiozzini C, Cereseto A, Falchi M, Nappi F, Sgadari C, Barillari G, Mainiero F, Ensoli B (2006) HIV-1 Tat regulates endothelial cell cycle progression via activation of the Ras/ERK MAPK signaling pathway. Mol Biol Cell 17:1985–1994

    CAS  PubMed  PubMed Central  Google Scholar 

  • Unger HV, Collins PY (2005) Transforming the meaning of HIV/AIDS in recovery from substance use: a qualitative study of HIV-positive women in New York. Health Care Women Int 26:308–324

    PubMed  Google Scholar 

  • Valjent E, Corvol JC, Pages C, Besson MJ, Maldonado R, Caboche J (2000) Involvement of the extracellular signal-regulated kinase cascade for cocaine-rewarding properties. J Neurosci 20:8701–8709

    CAS  PubMed  Google Scholar 

  • Valjent E, Pages C, Herve D, Girault JA, Caboche J (2004) Addictive and non-addictive drugs induce distinct and specific patterns of ERK activation in mouse brain. Eur J Neurosci 19:1826–1836

    PubMed  Google Scholar 

  • Valjent E, Pascoli V, Svenningsson P, Paul S, Enslen H, Corvol JC, Stipanovich A, Caboche J, Lombroso PJ, Nairn AC, Greengard P, Herve D, Girault JA (2005) Regulation of a protein phosphatase cascade allows convergent dopamine and glutamate signals to activate ERK in the striatum. Proc Natl Acad Sci USA 102:491–496

    CAS  PubMed  Google Scholar 

  • Vigorito M, Connaghan KP, Chang SL (2015) The HIV-1 transgenic rat model of neuroHIV. Brain Behav Immun 48:336–349

    CAS  PubMed  PubMed Central  Google Scholar 

  • Von KA, Baiocchi D, Birtwistle M, Sumpton D, Bienvenut W, Morrice N, Yamada K, Lamond A, Kalna G, Orton R, Gilbert D, Kolch W (2009) Cell fate decisions are specified by the dynamic ERK interactome. Nat Cell Biol 11:1458–1464

    Google Scholar 

  • Wakabayashi KT, Weiss MJ, Pickup KN, Robinson TE (2010) Rats markedly escalate their intake and show a persistent susceptibility to reinstatement only when cocaine is injected rapidly. J Neurosci 30:11346–11355

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang GJ, Smith L, Volkow ND, Telang F, Logan J, Tomasi D, Wong CT, Hoffman W, Jayne M, Alia-Klein N, Thanos P, Fowler JS (2012) Decreased dopamine activity predicts relapse in methamphetamine abusers. Mol Psychiatry 17:918–925

    CAS  PubMed  Google Scholar 

  • Wayman WN, Chen L, Hu XT, Napier TC (2016) HIV-1 transgenic rat prefrontal cortex hyper-excitability is enhanced by cocaine self-administration. Neuropsychopharmacology 41:1965–1973

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weiner DM, Levey AI, Sunahara RK, Niznik HB, O’Dowd BF, Seeman P, Brann MR (1991) D1 and D2 dopamine receptor mRNA in rat brain. Proc Natl Acad Sci USA 88:1859–1863

    CAS  PubMed  Google Scholar 

  • White FJ, Bednarz LM, Wachtel SR, Hjorth S, Brooderson RJ (1988) Is stimulation of both D1 and D2 receptors necessary for the expression of dopamine-mediated behaviors? Pharmacol Biochem Behav 30:189–193

    CAS  PubMed  Google Scholar 

  • Wiley CA, Schrier RD, Nelson JA, Lampert PW, Oldstone MB (1986) Cellular localization of human immunodeficiency virus infection within the brains of acquired immune deficiency syndrome patients. Proc Natl Acad Sci USA 83:7089–7093

    CAS  PubMed  Google Scholar 

  • Wiley CA, Baldwin M, Achim CL (1996) Expression of HIV regulatory and structural mRNA in the central nervous system. AIDS 10:843–847

    CAS  PubMed  Google Scholar 

  • Wolf ME, Ferrario CR (2010) AMPA receptor plasticity in the nucleus accumbens after repeated exposure to cocaine. Neurosci Biobehav Rev 35:185–211

    CAS  PubMed  PubMed Central  Google Scholar 

  • Worsley JN, Moszczynska A, Falardeau P, Kalasinsky KS, Schmunk G, Guttman M, Furukawa Y, Ang L, Adams V, Reiber G, Anthony RA, Wickham D, Kish SJ (2000) Dopamine D1 receptor protein is elevated in nucleus accumbens of human, chronic methamphetamine users. Mol Psychiatry 5:664–672

    CAS  PubMed  Google Scholar 

  • Yuan Y, Quizon PM, Sun WL, Yao J, Zhu J, Zhan CG (2016) Role of histidine 547 of human dopamine transporter in molecular interaction with HIV-1 Tat and dopamine uptake. Sci Rep 6:27314

    CAS  PubMed  PubMed Central  Google Scholar 

  • Záborszky L, Alheid GF, Beinfeld MC, Eiden LE, Heimer L, Palkovits M (1985) Cholecystokinin innervation of the ventral striatum: A morphological and radioimmunological study. Neuroscience 14(2):427–453

    PubMed  Google Scholar 

  • Zhu J, Ananthan S, Mactutus CF, Booze RM (2011) Recombinant human immunodeficiency virus-1 transactivator of transcription1-86 allosterically modulates dopamine transporter activity. Synapse 65:1251–1254

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank Dr. Gabrielle Rodenko of the Department of Pharmacology and Toxicology, Sealy Center for Structural Biology & Biophysics, University of Texas Medical Branch, for providing recombinant ΔFosB protein for antibody verification. The authors also thank Dr. Brinda Bradaric for her intellectual contributions to the experiments.

Funding

This study was funded by USPHSGs R21ES025920 and P30A1082151.

Author information

Authors and Affiliations

  1. Department of Pharmacology, Rush University, Chicago, IL, USA

    Michael Ohene-Nyako

  2. Department of Physician Assistant Studies, Rush University, Chicago, IL, USA

    Amanda L. Persons

  3. Department of Psychiatry, Rush University Medical Center, 1735 W. Harrison Street, Cohn Research Building Suite #424, Chicago, IL, 60612, USA

    Amanda L. Persons & T. Celeste Napier

  4. Center for Compulsive Behavior and Addiction, Rush University, Chicago, IL, USA

    Michael Ohene-Nyako, Amanda L. Persons & T. Celeste Napier

Authors
  1. Michael Ohene-Nyako
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amanda L. Persons
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. Celeste Napier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T. Celeste Napier.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

“All applicable international, national, and/or institutional guidelines for the care and use of animals were followed”.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 1121 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ohene-Nyako, M., Persons, A.L. & Napier, T.C. Region-specific changes in markers of neuroplasticity revealed in HIV-1 transgenic rats by low-dose methamphetamine. Brain Struct Funct 223, 3503–3513 (2018). https://doi.org/10.1007/s00429-018-1701-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-018-1701-6

Keywords

Search

Navigation