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Is There a Role for Nitric Oxide in Methamphetamine-Induced Dopamine Terminal Degeneration?

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Abstract

Methamphetamine (METH) abuse results in long-term damage to the dopaminergic system, manifesting as decreases in dopamine (DA) tissue content, DA transporter binding, as well as tyrosine hydroxylase and vesicular monoamine transporter immunostaining. However, the exact cascade of events that ultimately result in this damage has not been clearly elucidated. One factor that has been heavily implicated in METH-induced DA terminal degeneration is the production of nitric oxide (NO). Unfortunately, many of the studies attempting to clarify the role of NO in METH-induced neurotoxicity have been confounded by issues such as the disruption of METH-induced hyperthermia, preventing the formation of strong conclusions. As a result, there is a body of work suggesting that NO is sufficient for METH-induced neurotoxicity, while other studies suggest that NO does not play a role in METH-induced degeneration of DA nerve terminals. This review summarizes the existing studies investigating the role of NO in METH-induced neurotoxicity, and argues that while NO may be necessary for METH-induced neurotoxicity, it is not sufficient. Finally, important areas of future investigation are highlighted and discussed.

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References

  • Ali SF, Itzhak Y (1998) Effects of 7-nitroindazole, an NOS inhibitor on methamphetamine-induced dopaminergic and serotonergic neurotoxicity in mice. Ann N Y Acad Sci 844:122–130

    CAS  PubMed  Google Scholar 

  • Ali SF, Newport GD, Holson RR, Slikker W Jr, Bowyer JF (1994) Low environmental temperatures or pharmacologic agents that produce hypothermia decrease methamphetamine neurotoxicity in mice. Brain Res 658:33–38

    CAS  PubMed  Google Scholar 

  • Anderson KL, Itzhak Y (2006) Methamphetamine-induced selective dopaminergic neurotoxicity is accompanied by an increase in striatal nitrate in the mouse. Ann N Y Acad Sci 1074:225–233

    CAS  PubMed  Google Scholar 

  • Arbones ML, Ribera J, Agullo L, Baltrons MA, Casanovas A, Riveros-Moreno V, Garcia A (1996) Characteristics of nitric oxide synthase type I of rat cerebellar astrocytes. Glia 18:224–232

    CAS  PubMed  Google Scholar 

  • Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 87:1620–1624

    CAS  PubMed  Google Scholar 

  • Bellomo M, Giuffrida R, Palmeri A, Sapienza S (1998) Excitatory amino acids as neurotransmitters of corticostriatal projections: immunocytochemical evidence in the rat. Arch Ital Biol 136:215–223

    CAS  PubMed  Google Scholar 

  • Blackshaw S, Eliasson MJ, Sawa A, Watkins CC, Krug D, Gupta A, Arai T, Ferrante RJ, Snyder SH (2003) Species, strain and developmental variations in hippocampal neuronal and endothelial nitric oxide synthase clarify discrepancies in nitric oxide-dependent synaptic plasticity. Neuroscience 119:979–990

    CAS  PubMed  Google Scholar 

  • Blanchard-Fillion B, Souza JM, Friel T, Jiang GC, Vrana K, Sharov V, Barron L, Schoneich C, Quijano C, Alvarez B, Radi R, Przedborski S, Fernando GS, Horwitz J, Ischiropoulos H (2001) Nitration and inactivation of tyrosine hydroxylase by peroxynitrite. J Biol Chem 276:46017–46023

    CAS  PubMed  Google Scholar 

  • Bo L, Dawson TM, Wesselingh S, Mork S, Choi S, Kong PA, Hanley D, Trapp BD (1994) Induction of nitric oxide synthase in demyelinating regions of multiple sclerosis brains. Ann Neurol 36:778–786

    CAS  PubMed  Google Scholar 

  • Bowyer JF, Davies DL, Schmued L, Broening HW, Newport GD, Slikker W Jr, Holson RR (1994) Further studies of the role of hyperthermia in methamphetamine neurotoxicity. J Pharmacol Exp Ther 268:1571–1580

    CAS  PubMed  Google Scholar 

  • Bredt DS, Snyder SH (1989) Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc Natl Acad Sci USA 86:9030–9033

    CAS  PubMed  Google Scholar 

  • Bredt DS, Snyder SH (1990) Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc Natl Acad Sci USA 87:682–685

    CAS  PubMed  Google Scholar 

  • Bredt DS, Hwang PM, Snyder SH (1990) Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347:768–770

    CAS  PubMed  Google Scholar 

  • Callaghan RC, Cunningham JK, Sajeev G, Kish SJ (2010) Incidence of Parkinson’s disease among hospital patients with methamphetamine-use disorders. Mov Disord 25:2333–2339

    PubMed  Google Scholar 

  • Callaghan RC, Cunningham JK, Sykes J, Kish SJ (2012) Increased risk of Parkinson’s disease in individuals hospitalized with conditions related to the use of methamphetamine or other amphetamine-type drugs. Drug Alcohol Depend 120:35–40

    CAS  PubMed  Google Scholar 

  • Callahan BT, Ricaurte GA (1998) Effect of 7-nitroindazole on body temperature and methamphetamine-induced dopamine toxicity. Neuroreport 9:2691–2695

    CAS  PubMed  Google Scholar 

  • Centonze D, Pisani A, Bonsi P, Giacomini P, Bernardi G, Calabresi P (2001) Stimulation of nitric oxide-cGMP pathway excites striatal cholinergic interneurons via protein kinase G activation. J Neurosci 21:1393–1400

    CAS  PubMed  Google Scholar 

  • Centonze D, Grande C, Saulle E, Martin AB, Gubellini P, Pavon N, Pisani A, Bernardi G, Moratalla R, Calabresi P (2003) Distinct roles of D1 and D5 dopamine receptors in motor activity and striatal synaptic plasticity. J Neurosci 23:8506–8512

    CAS  PubMed  Google Scholar 

  • Clementi E, Brown GC, Feelisch M, Moncada S (1998) Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione. Proc Natl Acad Sci USA 95:7631–7636

    CAS  PubMed  Google Scholar 

  • Dawson TM, Bredt DS, Fotuhi M, Hwang PM, Snyder SH (1991) Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc Natl Acad Sci USA 88:7797–7801

    CAS  PubMed  Google Scholar 

  • Deng X, Cadet JL (1999) Methamphetamine administration causes overexpression of nNOS in the mouse striatum. Brain Res 851:254–257

    CAS  PubMed  Google Scholar 

  • Di Monte DA, Royland JE, Jakowec MW, Langston JW (1996) Role of nitric oxide in methamphetamine neurotoxicity: protection by 7-nitroindazole, an inhibitor of neuronal nitric oxide synthase. J Neurochem 67:2443–2450

    PubMed  Google Scholar 

  • Dinerman JL, Dawson TM, Schell MJ, Snowman A, Snyder SH (1994) Endothelial nitric oxide synthase localized to hippocampal pyramidal cells: implications for synaptic plasticity. Proc Natl Acad Sci USA 91:4214–4218

    CAS  PubMed  Google Scholar 

  • Endoh M, Maiese K, Wagner J (1994) Expression of the inducible form of nitric oxide synthase by reactive astrocytes after transient global ischemia. Brain Res 651:92–100

    CAS  PubMed  Google Scholar 

  • Faraci FM, Breese KR (1993) Nitric oxide mediates vasodilatation in response to activation of N-methyl-d-aspartate receptors in brain. Circ Res 72:476–480

    CAS  PubMed  Google Scholar 

  • Figueredo-Cardenas G, Morello M, Sancesario G, Bernardi G, Reiner A (1996) Colocalization of somatostatin, neuropeptide Y, neuronal nitric oxide synthase and NADPH-diaphorase in striatal interneurons in rats. Brain Res 735:317–324

    CAS  PubMed  Google Scholar 

  • Forstermann U, Pollock JS, Schmidt HH, Heller M, Murad F (1991) Calmodulin-dependent endothelium-derived relaxing factor/nitric oxide synthase activity is present in the particulate and cytosolic fractions of bovine aortic endothelial cells. Proc Natl Acad Sci USA 88:1788–1792

    CAS  PubMed  Google Scholar 

  • Fricks-Gleason AN, Keefe KA (2013) Evaluating the role of neuronal nitric oxide synthase-containing striatal interneurons in methamphetamine-induced dopamine neurotoxicity. Neurotox Res 24:288–297

    CAS  PubMed  Google Scholar 

  • Friend DM, Son JH, Keefe KA, Fricks-Gleason AN (2013) Expression and activity of nitric oxide synthase isoforms in methamphetamine-induced striatal dopamine toxicity. J Pharmacol Exp Ther 344:511–521

    CAS  PubMed  Google Scholar 

  • Garthwaite J, Charles SL, Chess-Williams R (1988) Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature 336:385–388

    CAS  PubMed  Google Scholar 

  • Geller DA, Lowenstein CJ, Shapiro RA, Nussler AK, Di Silvio M, Wang SC, Nakayama DK, Simmons RL, Snyder SH, Billiar TR (1993) Molecular cloning and expression of inducible nitric oxide synthase from human hepatocytes. Proc Natl Acad Sci USA 90:3491–3495

    CAS  PubMed  Google Scholar 

  • Gerfen CR (1989) The neostriatal mosaic: striatal patch-matrix organization is related to cortical lamination. Science 246:385–388

    CAS  PubMed  Google Scholar 

  • Gerfen CR, Herkenham M, Thibault J (1987) The neostriatal mosaic. II. Patch- and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems. J Neurosci 7:3915–3934

    CAS  PubMed  Google Scholar 

  • Gibson CL, Coughlan TC, Murphy SP (2005) Glial nitric oxide and ischemia. Glia 50:417–426

    PubMed  Google Scholar 

  • Gracy KN, Pickel VM (1997) Ultrastructural localization and comparative distribution of nitric oxide synthase and N-methyl-d-aspartate receptors in the shell of the rat nucleus accumbens. Brain Res 747:259–272

    CAS  PubMed  Google Scholar 

  • Guilarte TR, Nihei MK, McGlothan JL, Howard AS (2003) Methamphetamine-induced deficits of brain monoaminergic neuronal markers: distal axotomy or neuronal plasticity. Neuroscience 122:499–513

    CAS  PubMed  Google Scholar 

  • Hall AV, Antoniou H, Wang Y, Cheung AH, Arbus AM, Olson SL, Lu WC, Kau CL, Marsden PA (1994) Structural organization of the human neuronal nitric oxide synthase gene (NOS1). J Biol Chem 269:33082–33090

    CAS  PubMed  Google Scholar 

  • Hanson JE, Birdsall E, Seferian KS, Crosby MA, Keefe KA, Gibb JW, Hanson GR, Fleckenstein AE (2009) Methamphetamine-induced dopaminergic deficits and refractoriness to subsequent treatment. Eur J Pharmacol 607:68–73

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hope BT, Michael GJ, Knigge KM, Vincent SR (1991) Neuronal NADPH diaphorase is a nitric oxide synthase. Proc Natl Acad Sci USA 88:2811–2814

    CAS  PubMed  Google Scholar 

  • Hoque KE, Indorkar RP, Sammut S, West AR (2010) Impact of dopamine–glutamate interactions on striatal neuronal nitric oxide synthase activity. Psychopharmacology 207:571–581

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hunot S, Boissiere F, Faucheux B, Brugg B, Mouatt-Prigent A, Agid Y, Hirsch EC (1996) Nitric oxide synthase and neuronal vulnerability in Parkinson’s disease. Neuroscience 72:355–363

    CAS  PubMed  Google Scholar 

  • Imam SZ, Crow JP, Newport GD, Islam F, Slikker W Jr, Ali SF (1999) Methamphetamine generates peroxynitrite and produces dopaminergic neurotoxicity in mice: protective effects of peroxynitrite decomposition catalyst. Brain Res 837:15–21

    CAS  PubMed  Google Scholar 

  • Imam SZ, Islam F, Itzhak Y, Slikker W Jr, Ali SF (2000) Prevention of dopaminergic neurotoxicity by targeting nitric oxide and peroxynitrite: implications for the prevention of methamphetamine-induced neurotoxic damage. Ann N Y Acad Sci 914:157–171

    CAS  PubMed  Google Scholar 

  • Iravani MM, Millar J, Kruk ZL (1998) Differential release of dopamine by nitric oxide in subregions of rat caudate putamen slices. J Neurochem 71:1969–1977

    CAS  PubMed  Google Scholar 

  • Itzhak Y, Ali SF (1996) The neuronal nitric oxide synthase inhibitor, 7-nitroindazole, protects against methamphetamine-induced neurotoxicity in vivo. J Neurochem 67:1770–1773

    CAS  PubMed  Google Scholar 

  • Itzhak Y, Gandia C, Huang PL, Ali SF (1998) Resistance of neuronal nitric oxide synthase-deficient mice to methamphetamine-induced dopaminergic neurotoxicity. J Pharmacol Exp Ther 284:1040–1047

    CAS  PubMed  Google Scholar 

  • Itzhak Y, Martin JL, Ali SF (1999) Methamphetamine- and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced dopaminergic neurotoxicity in inducible nitric oxide synthase-deficient mice. Synapse 34:305–312

    CAS  PubMed  Google Scholar 

  • Itzhak Y, Martin JL, Ail SF (2000a) nNOS inhibitors attenuate methamphetamine-induced dopaminergic neurotoxicity but not hyperthermia in mice. Neuroreport 11:2943–2946

    CAS  PubMed  Google Scholar 

  • Itzhak Y, Martin JL, Ali SF (2000b) Comparison between the role of the neuronal and inducible nitric oxide synthase in methamphetamine-induced neurotoxicity and sensitization. Ann N Y Acad Sci 914:104–111

    CAS  PubMed  Google Scholar 

  • Janssens SP, Shimouchi A, Quertermous T, Bloch DB, Bloch KD (1992) Cloning and expression of a cDNA encoding human endothelium-derived relaxing factor/nitric oxide synthase. J Biol Chem 267:14519–14522

    CAS  PubMed  Google Scholar 

  • Kawaguchi Y (1993) Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13:4908–4923

    CAS  PubMed  Google Scholar 

  • Kawaguchi Y, Wilson CJ, Augood SJ, Emson PC (1995) Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci 18:527–535

    CAS  PubMed  Google Scholar 

  • Kemp JM, Powell TP (1971) The termination of fibres from the cerebral cortex and thalamus upon dendritic spines in the caudate nucleus: a study with the Golgi method. Philos Trans R Soc Lond B Biol Sci 262:429–439

    CAS  PubMed  Google Scholar 

  • Kitai ST, Kocsis JD, Wood J (1976) Origin and characteristics of the cortico-caudate afferents: an anatomical and electrophysiological study. Brain Res 118:137–141

    CAS  PubMed  Google Scholar 

  • Kogan FJ, Nichols WK, Gibb JW (1976) Influence of methamphetamine on nigral and striatal tyrosine hydroxylase activity and on striatal dopamine levels. Eur J Pharmacol 36:363–371

    CAS  PubMed  Google Scholar 

  • Konorev EA, Hogg N, Kalyanaraman B (1998) Rapid and irreversible inhibition of creatine kinase by peroxynitrite. FEBS Lett 427:171–174

    CAS  PubMed  Google Scholar 

  • Kubota Y, Inagaki S, Kito S, Shimada S, Okayama T, Hatanaka H, Pelletier G, Takagi H, Tohyama M (1988) Neuropeptide Y-immunoreactive neurons receive synaptic inputs from dopaminergic axon terminals in the rat neostriatum. Brain Res 458:389–393

    CAS  PubMed  Google Scholar 

  • LaVoie MJ, Card JP, Hastings TG (2004) Microglial activation precedes dopamine terminal pathology in methamphetamine-induced neurotoxicity. Exp Neurol 187:47–57

    CAS  PubMed  Google Scholar 

  • Le Moine C, Normand E, Bloch B (1991) Phenotypical characterization of the rat striatal neurons expressing the D1 dopamine receptor gene. Proc Natl Acad Sci USA 88:4205–4209

    PubMed  Google Scholar 

  • Lin HL, Murphy S (1997) Regulation of astrocyte nitric oxide synthase type II expression by ATP and glutamate involves loss of transcription factor binding to DNA. J Neurochem 69:612–616

    CAS  PubMed  Google Scholar 

  • Lin LH, Taktakishvili O, Talman WT (2007) Identification and localization of cell types that express endothelial and neuronal nitric oxide synthase in the rat nucleus tractus solitarii. Brain Res 1171:42–51

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu J, Zhao ML, Brosnan CF, Lee SC (1996) Expression of type II nitric oxide synthase in primary human astrocytes and microglia: role of IL-1beta and IL-1 receptor antagonist. J Immunol 157:3569–3576

    CAS  PubMed  Google Scholar 

  • Louin G, Marchand-Verrecchia C, Palmier B, Plotkine M, Jafarian-Tehrani M (2006) Selective inhibition of inducible nitric oxide synthase reduces neurological deficit but not cerebral edema following traumatic brain injury. Neuropharmacology 50:182–190

    CAS  PubMed  Google Scholar 

  • Lowenstein CJ, Alley EW, Raval P, Snowman AM, Snyder SH, Russell SW, Murphy WJ (1993) Macrophage nitric oxide synthase gene: two upstream regions mediate induction by interferon gamma and lipopolysaccharide. Proc Natl Acad Sci USA 90:9730–9734

    CAS  PubMed  Google Scholar 

  • Mark KA, Soghomonian JJ, Yamamoto BK (2004) High-dose methamphetamine acutely activates the striatonigral pathway to increase striatal glutamate and mediate long-term dopamine toxicity. J Neurosci 24:11449–11456

    CAS  PubMed  Google Scholar 

  • McCann UD, Kuwabara H, Kumar A, Palermo M, Abbey R, Brasic J, Ye W, Alexander M, Dannals RF, Wong DF, Ricaurte GA (2008) Persistent cognitive and dopamine transporter deficits in abstinent methamphetamine users. Synapse 62:91–100

    CAS  PubMed  Google Scholar 

  • Mohammadi MT, Shid-Moosavi SM, Dehghani GA (2012) Contribution of nitric oxide synthase (NOS) in blood–brain barrier disruption during acute focal cerebral ischemia in normal rat. Pathophysiology 19:13–20

    CAS  PubMed  Google Scholar 

  • Morris BJ, Simpson CS, Mundell S, Maceachern K, Johnston HM, Nolan AM (1997) Dynamic changes in NADPH-diaphorase staining reflect activity of nitric oxide synthase: evidence for a dopaminergic regulation of striatal nitric oxide release. Neuropharmacology 36:1589–1599

    CAS  PubMed  Google Scholar 

  • Nash JF, Yamamoto BK (1992) Methamphetamine neurotoxicity and striatal glutamate release: comparison to 3,4-methylenedioxymethamphetamine. Brain Res 581:237–243

    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 

  • O’Dell SJ, Weihmuller FB, Marshall JF (1993) Methamphetamine-induced dopamine overflow and injury to striatal dopamine terminals: attenuation by dopamine D1 or D2 antagonists. J Neurochem 60:1792–1799

    PubMed  Google Scholar 

  • O’Dell TJ, Huang PL, Dawson TM, Dinerman JL, Snyder SH, Kandel ER, Fishman MC (1994) Endothelial NOS and the blockade of LTP by NOS inhibitors in mice lacking neuronal NOS. Science 265:542–546

    PubMed  Google Scholar 

  • Park DJ, West AR (2009) Regulation of striatal nitric oxide synthesis by local dopamine and glutamate interactions. J Neurochem 111:1457–1465

    CAS  PubMed Central  PubMed  Google Scholar 

  • Park SK, Lin HL, Murphy S (1997) Nitric oxide regulates nitric oxide synthase-2 gene expression by inhibiting NF-kappaB binding to DNA. Biochem J 322(Pt 2):609–613

    CAS  PubMed  Google Scholar 

  • Radi R, Beckman JS, Bush KM, Freeman BA (1991) Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide. Arch Biochem Biophys 288:481–487

    CAS  PubMed  Google Scholar 

  • Radi R, Rodriguez M, Castro L, Telleri R (1994) Inhibition of mitochondrial electron transport by peroxynitrite. Arch Biochem Biophys 308:89–95

    CAS  PubMed  Google Scholar 

  • Riobo NA, Clementi E, Melani M, Boveris A, Cadenas E, Moncada S, Poderoso JJ (2001) Nitric oxide inhibits mitochondrial NADH:ubiquinone reductase activity through peroxynitrite formation. Biochem J 359:139–145

    CAS  PubMed  Google Scholar 

  • Rivera A, Alberti I, Martin AB, Narvaez JA, de la Calle A, Moratalla R (2002) Molecular phenotype of rat striatal neurons expressing the dopamine D5 receptor subtype. Eur J Neurosci 16:2049–2058

    PubMed  Google Scholar 

  • Rossetti ZL, Crespi F (2004) Inhibition of nitric oxide release in vivo by ethanol. Alcohol Clin Exp Res 28:1746–1751

    CAS  PubMed  Google Scholar 

  • Rubbo H, Radi R, Trujillo M, Telleri R, Kalyanaraman B, Barnes S, Kirk M, Freeman BA (1994) Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation. Formation of novel nitrogen-containing oxidized lipid derivatives. J Biol Chem 269:26066–26075

    CAS  PubMed  Google Scholar 

  • Salgo MG, Bermudez E, Squadrito GL, Pryor WA (1995) Peroxynitrite causes DNA damage and oxidation of thiols in rat thymocytes [corrected]. Arch Biochem Biophys 322:500–505

    CAS  PubMed  Google Scholar 

  • SAMHSA/OSM (2011) Results from the 2010 National Survey on Drug Use and Health. SAMHSA, Rockville

    Google Scholar 

  • Sammut S, Dec A, Mitchell D, Linardakis J, Ortiguela M, West AR (2006) Phasic dopaminergic transmission increases NO efflux in the rat dorsal striatum via a neuronal NOS and a dopamine D(1/5) receptor-dependent mechanism. Neuropsychopharmacology 31:493–505

    CAS  PubMed  Google Scholar 

  • Sammut S, Park DJ, West AR (2007) Frontal cortical afferents facilitate striatal nitric oxide transmission in vivo via a NMDA receptor and neuronal NOS-dependent mechanism. J Neurochem 103:1145–1156

    CAS  PubMed  Google Scholar 

  • Sattler R, Xiong Z, Lu WY, Hafner M, MacDonald JF, Tymianski M (1999) Specific coupling of NMDA receptor activation to nitric oxide neurotoxicity by PSD-95 protein. Science 284:1845–1848

    CAS  PubMed  Google Scholar 

  • Seidel B, Stanarius A, Wolf G (1997) Differential expression of neuronal and endothelial nitric oxide synthase in blood vessels of the rat brain. Neurosci Lett 239:109–112

    CAS  PubMed  Google Scholar 

  • Serulle Y, Zhang S, Ninan I, Puzzo D, McCarthy M, Khatri L, Arancio O, Ziff EB (2007) A GluR1–cGKII interaction regulates AMPA receptor trafficking. Neuron 56:670–688

    CAS  PubMed Central  PubMed  Google Scholar 

  • Son H, Hawkins RD, Martin K, Kiebler M, Huang PL, Fishman MC, Kandel ER (1996) Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell 87:1015–1023

    CAS  PubMed  Google Scholar 

  • Stanarius A, Topel I, Schulz S, Noack H, Wolf G (1997) Immunocytochemistry of endothelial nitric oxide synthase in the rat brain: a light and electron microscopical study using the tyramide signal amplification technique. Acta Histochem 99:411–429

    CAS  PubMed  Google Scholar 

  • Stone JR, Marletta MA (1996) Spectral and kinetic studies on the activation of soluble guanylate cyclase by nitric oxide. Biochemistry 35:1093–1099

    CAS  PubMed  Google Scholar 

  • Sultana R, Poon HF, Cai J, Pierce WM, Merchant M, Klein JB, Markesbery WR, Butterfield DA (2006) Identification of nitrated proteins in Alzheimer’s disease brain using a redox proteomics approach. Neurobiol Dis 22:76–87

    CAS  PubMed  Google Scholar 

  • Taraska T, Finnegan KT (1997) Nitric oxide and the neurotoxic effects of methamphetamine and 3,4-methylenedioxymethamphetamine. J Pharmacol Exp Ther 280:941–947

    CAS  PubMed  Google Scholar 

  • Thomas DM, Kuhn DM (2005) Attenuated microglial activation mediates tolerance to the neurotoxic effects of methamphetamine. J Neurochem 92:790–797

    CAS  PubMed  Google Scholar 

  • Volkow ND, Chang L, Wang GJ, Fowler JS, Franceschi D, Sedler M, Gatley SJ, Miller E, Hitzemann R, Ding YS, Logan J (2001a) Loss of dopamine transporters in methamphetamine abusers recovers with protracted abstinence. J Neurosci 21:9414–9418

    CAS  PubMed  Google Scholar 

  • Volkow ND, Chang L, Wang GJ, Fowler JS, Leonido-Yee M, Franceschi D, Sedler MJ, Gatley SJ, Hitzemann R, Ding YS, Logan J, Wong C, Miller EN (2001b) Association of dopamine transporter reduction with psychomotor impairment in methamphetamine abusers. Am J Psychiatry 158:377–382

    CAS  PubMed  Google Scholar 

  • Vuillet J, Kerkerian L, Kachidian P, Bosler O, Nieoullon A (1989) Ultrastructural correlates of functional relationships between nigral dopaminergic or cortical afferent fibers and neuropeptide Y-containing neurons in the rat striatum. Neurosci Lett 100:99–104

    CAS  PubMed  Google Scholar 

  • Wagner GC, Ricaurte GA, Seiden LS, Schuster CR, Miller RJ, Westley J (1980) Long-lasting depletions of striatal dopamine and loss of dopamine uptake sites following repeated administration of methamphetamine. Brain Res 181:151–160

    CAS  PubMed  Google Scholar 

  • Wang J, Angulo JA (2011) Synergism between methamphetamine and the neuropeptide substance P on the production of nitric oxide in the striatum of mice. Brain Res 1369:131–139

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang HG, Lu FM, Jin I, Udo H, Kandel ER, de Vente J, Walter U, Lohmann SM, Hawkins RD, Antonova I (2005) Presynaptic and postsynaptic roles of NO, cGK, and RhoA in long-lasting potentiation and aggregation of synaptic proteins. Neuron 45:389–403

    CAS  PubMed  Google Scholar 

  • Wang J, Xu W, Ali SF, Angulo JA (2008) Connection between the striatal neurokinin-1 receptor and nitric oxide formation during methamphetamine exposure. Ann N Y Acad Sci 1139:164–171

    CAS  PubMed Central  PubMed  Google Scholar 

  • West AR (2010) Nitric oxide signaling in striatum. In: Steiner H, Tseng KY (eds) Handbook of the basal ganglia structure and function. Elsevier Inc., Amsterdam, pp 187–196

    Google Scholar 

  • West AR, Grace AA (2004) The nitric oxide-guanylyl cyclase signaling pathway modulates membrane activity states and electrophysiological properties of striatal medium spiny neurons recorded in vivo. J Neurosci 24:1924–1935

    CAS  PubMed  Google Scholar 

  • Xie QW, Whisnant R, Nathan C (1993) Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial lipopolysaccharide. J Exp Med 177:1779–1784

    CAS  PubMed  Google Scholar 

  • Yermilov V, Rubio J, Ohshima H (1995) Formation of 8-nitroguanine in DNA treated with peroxynitrite in vitro and its rapid removal from DNA by depurination. FEBS Lett 376:207–210

    CAS  PubMed  Google Scholar 

  • Yermilov V, Yoshie Y, Rubio J, Ohshima H (1996) Effects of carbon dioxide/bicarbonate on induction of DNA single-strand breaks and formation of 8-nitroguanine, 8-oxoguanine and base-propenal mediated by peroxynitrite. FEBS Lett 399:67–70

    CAS  PubMed  Google Scholar 

  • Yui Y, Hattori R, Kosuga K, Eizawa H, Hiki K, Kawai C (1991) Purification of nitric oxide synthase from rat macrophages. J Biol Chem 266:12544–12547

    CAS  PubMed  Google Scholar 

  • Zhang F, Chen L, Liu C, Qiu P, Wang A, Li L, Wang H (2013) Up-regulation of protein tyrosine nitration in methamphetamine-induced neurotoxicity through DDAH/ADMA/NOS pathway. Neurochem Int 62:1055–1064

    CAS  PubMed  Google Scholar 

  • Zhu JP, Xu W, Angulo JA (2006) Distinct mechanisms mediating methamphetamine-induced neuronal apoptosis and dopamine terminal damage share the neuropeptide substance p in the striatum of mice. Ann N Y Acad Sci 1074:135–148

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu J, Xu W, Wang J, Ali SF, Angulo JA (2009) The neurokinin-1 receptor modulates the methamphetamine-induced striatal apoptosis and nitric oxide formation in mice. J Neurochem 111:656–668

    CAS  PubMed Central  PubMed  Google Scholar 

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  1. Interdepartmental Program in Neuroscience, University of Utah, 401 MREB, 20 North 1900 East, Salt Lake City, UT, 84132, USA

    Danielle M. Friend & Kristen A. Keefe

  2. Department of Pharmacology and Toxicology, University of Utah, 30 South 2000 East, Room 105, Salt Lake City, UT, 84112, USA

    Ashley N. Fricks-Gleason & Kristen A. Keefe

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  1. Danielle M. Friend
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Friend, D.M., Fricks-Gleason, A.N. & Keefe, K.A. Is There a Role for Nitric Oxide in Methamphetamine-Induced Dopamine Terminal Degeneration?. Neurotox Res 25, 153–160 (2014). https://doi.org/10.1007/s12640-013-9415-2

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