Clozapine N-oxide administration produces behavioral effects in long-evans rats: Implications for designing DREADD experiments

eNeuro

Volumn 3, Issue 5, 2016, Pages

  MacLaren, Duncan A A ^a   Browne, Richard W ^a   Shaw, Jessica K ^b   Radhakrishnan, Sandhya Krishnan ^a   Khare, Prachi ^a   España, Rodrigo A ^b   Clark, Stewart D ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Behavior; CNO; DREADDs; Voltammetry

Indexed keywords

AMPHETAMINE; CLOZAPINE; CLOZAPINE N OXIDE; DIMETHYL SULFOXIDE; DOPAMINE; DRUG METABOLITE; DRUG VEHICLE; G PROTEIN COUPLED RECEPTOR KINASE; NORCLOZAPINE; PHENCYCLIDINE; SCOPOLAMINE; SODIUM CHLORIDE; CENTRAL NERVOUS SYSTEM AGENTS; CLOZAPINE N-OXIDE; DESIGNER DRUG; MUSCARINIC RECEPTOR; NEUROTRANSMITTER RECEPTOR; SCOPOLAMINE BROMIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR ASSESSMENT; CONTROLLED STUDY; CYCLIC POTENTIOMETRY; ELECTROCHEMICAL ANALYSIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYPERACTIVITY; LONG EVANS RAT; MALE; MASS SPECTROMETRY; NONHUMAN; PREPULSE INHIBITION; PREPULSE INHIBITION DISRUPTION TEST; PRIORITY JOURNAL; RAT; RECOMMENDED DRUG DOSE; SOLID PHASE EXTRACTION; SPIKE WAVE; STARTLE REFLEX; ANALOGS AND DERIVATIVES; ANIMAL; ANIMAL BEHAVIOR; BLOOD; DOSE RESPONSE; DRUG EFFECTS; HEARING; METABOLISM; METHODOLOGY; MOTOR ACTIVITY; NUCLEUS ACCUMBENS; SENSORY GATING;

AMPHETAMINE; ANIMALS; AUDITORY PERCEPTION; BEHAVIOR, ANIMAL; CENTRAL NERVOUS SYSTEM AGENTS; CLOZAPINE; DESIGNER DRUGS; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; MALE; MOTOR ACTIVITY; NUCLEUS ACCUMBENS; PHENCYCLIDINE; RATS, LONG-EVANS; RECEPTORS, MUSCARINIC; RECEPTORS, NEUROTRANSMITTER; RESEARCH DESIGN; SCOPOLAMINE HYDROBROMIDE; SENSORY GATING;

EID: 84995594791     PISSN: None     EISSN: 23732822     Source Type: Journal    
DOI: 10.1523/ENEURO.0219-16.2016     Document Type: Article

References (63)

1. Agulhon C, Boyt KM, Xie AX, Friocourt F, Roth BL, McCarthy KD (2013) Modulation of the autonomic nervous system and behaviour by acute glial cell Gq protein-coupled receptor activation in vivo. J Physiol 591:5599-5609.
2. Alexander GM, Rogan SC, Abbas AI, Armbruster BN, Pei Y, Allen JA, Nonneman RJ, Hartmann J, Moy SS, Nicolelis MA, McNamara JO, Roth BL (2009) Remote control of neuronal activity in transgenic mice expressing evolved G protein-coupled receptors. Neuron 63:27-39.
3. Alves-Rodrigues A, Leurs R, Willems E, Timmerman H (1996) Binding of clozapine metabolites and analogues to the histamine H3 receptor in rat brain cortex. Arch Pharm (Weinheim) 329:413-416.
4. Anderson SA, Michaelides M, Zarnegar P, Ren Y, Fagergren P, Thanos PK, Wang GJ, Bannon M, Neumaier JF, Keller E, Volkow ND, Hurd YL (2013) Impaired periamygdaloid-cortex prodynorphin is characteristic of opiate addiction and depression. J Clin Invest 123:5334-5341.
5. Armbruster BN, Li X, Pausch MH, Herlitze S, Roth BL (2007) Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc Natl Acad Sci U S A 104:5163-5168.
6. Baldessarini RJ, Centorrino F, Flood JG, Volpicelli SA, Huston-Lyons D, Cohen BM (1993) Tissue concentrations of clozapine and its metabolites in the rat. Neuropsychopharmacology 9:117-124.
7. Boender AJ, de Jong JW, Boekhoudt L, Luijendijk MC, van der Plasse G, Adan RA (2014) Combined use of the canine adenovirus-2 and DREADD-technology to activate specific neural pathways in vivo. PLoS One 9:e95392.
8. Bull C, Freitas KC, Zou S, Poland RS, Syed WA, Urban DJ, Minter SC, Shelton KL, Hauser KF, Negus SS, Knapp PE, Bowers MS (2014) Rat nucleus accumbens core astrocytes modulate reward and the motivation to self-administer ethanol after abstinence. Neuropsychopharmacology 39:2835-2845.
9. Bun H, Disdier B, Aubert C, Catalin J (1999) Interspecies variability and drug interactions of clozapine metabolism by microsomes. Fundam Clin Pharmacol 13:577-581.
10. Chang SE, Todd TP, Bucci DJ, Smith KS (2015) Chemogenetic manipulation of ventral pallidal neurons impairs acquisition of sign-tracking in rats. Eur J Neurosci 42:3105-3116.
11. Chang WH, Lin SK, Lane HY, Wei FC, Hu WH, Lam YW, Jann MW (1998) Reversible metabolism of clozapine and clozapine N-oxide in schizophrenic patients. Prog Neuropsychopharmacol Biol Psychiatry 22:723-739.
12. Chen X, Choo H, Huang XP, Yang X, Stone O, Roth BL, Jin J (2015) The first structure-activity relationship studies for designer receptors exclusively activated by designer drugs. ACS Chem Neurosci 6:476-484.
13. Conti LH, Costill JE, Flynn S, Tayler JE (2005) Effects of a typical and an atypical antipsychotic on the disruption of prepulse inhibition caused by corticotropin-releasing factor and by rat strain. Behav Neurosci 119:1052-1060.
14. Coward DM (1992) General pharmacology of clozapine. Br J Psychiatry Suppl (17):511.
15. Coward P, Wada HG, Falk MS, Chan SD, Meng F, Akil H, Conklin BR (1998) Controlling signaling with a specifically designed Gi-coupled receptor. Proc Natl Acad Sci U S A 95:352-357.
16. Cremers TI, Flik G, Hofland C, Stratford RE Jr.. (2012) Microdialysis evaluation of clozapine and N-desmethylclozapine pharmacokinetics in rat brain. Drug Metab Dispos 40:1909-1916.
17. Davies MA, Compton-Toth BA, Hufeisen SJ, Meltzer HY, Roth BL (2005) The highly efficacious actions of N-desmethylclozapine at muscarinic receptors are unique and not a common property of either typical or atypical antipsychotic drugs: is M1 agonism a pre-requisite for mimicking clozapine’s actions. Psychopharmacology (Berl) 178:451-460.
18. Dell’Anno MT, Caiazzo M, Leo D, Dvoretskova E, Medrihan L, Colasante G, Giannelli S, Theka I, Russo G, Mus L, Pezzoli G, Gainetdinov RR, Benfenati F, Taverna S, Dityatev A, Broccoli V (2014) Remote control of induced dopaminergic neurons in parkinsonian rats. J Clin Invest 124:3215-3229.
19. España RA, Oleson EB, Locke JL, Brookshire BR, Roberts DC, Jones SR (2010) The hypocretin-orexin system regulates cocaine self-administration via actions on the mesolimbic dopamine system. Eur J Neurosci 31:336-348.
20. España RA, Melchior JR, Roberts DC, Jones SR (2011) Hypocretin 1/orexin A in the ventral tegmental area enhances dopamine responses to cocaine and promotes cocaine self-administration. Psychopharmacology 214:415-426.
21. Farrell MS, Pei Y, Wan Y, Yadav PN, Daigle TL, Urban DJ, Lee HM, Sciaky N, Simmons A, Nonneman RJ, Huang XP, Hufeisen SJ, Guettier JM, Moy SS, Wess J, Caron MG, Calakos N, Roth BL (2013) A Gas DREADD mouse for selective modulation of cAMP production in striatopallidal neurons. Neuropsychopharmacology 38:854-862.
22. Feifel D, Shilling PD, Melendez G (2011) Clozapine and PD149163 elevate prepulse inhibition in Brown Norway rats. Behav Neurosci 125:268-272.
23. Ferguson SM, Eskenazi D, Ishikawa M, Wanat MJ, Phillips PE, Dong Y, Roth BL, Neumaier JF (2011) Transient neuronal inhibition reveals opposing roles of indirect and direct pathways in sensitization. Nat Neurosci 14:22-24.
24. Ferguson SM, Phillips PE, Roth BL, Wess J, Neumaier JF (2013) Direct-pathway striatal neurons regulate the retention of decision-making strategies. J Neurosci 33:11668-11676.
25. Gompf HS, Budygin EA, Fuller PM, Bass CE (2015) Targeted genetic manipulations of neuronal subtypes using promoter-specific combinatorial AAVs in wild-type animals. Front Behav Neurosci 9:152.
26. Grace PM, Strand KA, Galer EL, Urban DJ, Wang X, Baratta MV, Fabisiak TJ, Anderson ND, Cheng K, Greene LI, Berkelhammer D, Zhang Y, Ellis AL, Yin HH, Campeau S, Rice KC, Roth BL, Maier SF, Watkins LR (2016) Morphine paradoxically prolongs neuropathic pain in rats by amplifying spinal NLRP3 inflammasome activation. Proc Natl Acad Sci U S A 113:E3441-E3450.
27. Guettier JM, Gautam D, Scarselli M, Ruiz de Azua I, Li JH, Rosemond E, Ma X, Gonzalez FJ, Armbruster BN, Lu H, Roth BL, Wess J (2009) A chemical-genetic approach to study G protein regulation of beta cell function in vivo. Proc Natl Acad Sci U S A 106:19197-19202.
28. Huang XF, Tan YY, Huang X, Wang Q (2007) Effect of chronic treatment with clozapine and haloperidol on 5-HT(2A and 2C) receptor mRNA expression in the rat brain. Neurosci Res 59:314-321.
29. Jann MW, Grimsley SR, Gray EC, Chang WH (1993) Pharmacokinetics and pharmacodynamics of clozapine. Clin Pharmacokinet 24:161-176.
30. Jann MW, Lam YW, Chang WH (1994) Rapid formation of clozapine in guinea-pigs and man following clozapine-N-oxide administration. Arch Int Pharmacodyn Ther 328:243-250.
31. Kätzel D, Nicholson E, Schorge S, Walker MC, Kullmann DM (2014) Chemical-genetic attenuation of focal neocortical seizures. Nat Commun 5:38-47.
32. Keith VA, Mansbach RS, Geyer MA (1991) Failure of haloperidol to block the effects of phencyclidine and dizocilpine on prepulse inhibition of startle. Biol Psychiatry 30:557-566.
33. Lin G, McKay G, Hubbard JW, Midha KK (1994) Decomposition of clozapine N-oxide in the qualitative and quantitative analysis of clozapine and its metabolites. J Pharm Sci 83:1412-1417.
34. Lin G, McKay G, Midha KK (1996) Characterization of metabolites of clozapine N-oxide in the rat by micro-column high performance liquid chromatography/mass spectrometry with electrospray interface. J Pharm Biomed Anal 14:1561-1577.
35. Ma S, Allocca G, Ong-Palsson EK, Singleton CE, Hawkes D, McDougall SJ, Williams SJ, Bathgate RA, Gundlach AL (2016) Nucleus incertus promotes cortical desynchronization and behavioral arousal. Brain Struct Funct. Advance online publication. Retrieved October 13, 2016. doi:10.1007/s00429-016-1230-0.
36. Marchant NJ, Whitaker LR, Bossert JM, Harvey BK, Hope BT, Kaganoversusky K, Adhikary S, Prisinzano TE, Vardy E, Roth BL, Shaham Y (2016) Behavioral and physiological effects of a novel kappa-opioid receptor-based DREADD in rats. Neuropsychopharmacology 41:402-409.
37. Michaelides M, Anderson SA, Ananth M, Smirnov D, Thanos PK, Neumaier JF, Wang GJ, Volkow ND, Hurd YL (2013) Whole-brain circuit dissection in free-moving animals reveals cell-specific mesocorticolimbic networks. J Clin Invest 123:5342-5350.
38. Mizoguchi H, Katahira K, Inutsuka A, Fukumoto K, Nakamura A, Wang T, Nagai T, Sato J, Sawada M, Ohira H, Yamanaka A, Yamada K (2015) Insular neural system controls decision-making in healthy and methamphetamine-treated rats. Proc Natl Acad Sci U S A 112:E3930-E3939.
39. Mosier KE, Song J, McKay G, Hubbard JW, Fang J (2003) Determination of clozapine, and its metabolites, N-desmethylclozapine and clozapine N-oxide in dog plasma using high-performance liquid chromatography. J Chromatogr B Analyt Technol Biomed Life Sci 783:377-382.
40. Natesan S, Reckless GE, Barlow KB, Nobrega JN, Kapur S (2007) Evaluation of N-desmethylclozapine as a potential antipsychoticpreclinical studies. Neuropsychopharmacology 32:1540-1549.
41. Peters J-U (2012) Polypharmacology in drug discovery. Hoboken, NJ: Wiley.
42. Pienaar IS, Gartside SE, Sharma P, De Paola V, Gretenkord S, Withers D, Elson JL, Dexter DT (2015) Pharmacogenetic stimulation of cholinergic pedunculopontine neurons reverses motor deficits in a rat model of Parkinson’s disease. Mol Neurodegener 10:47.
43. Pirmohamed M, Williams D, Madden S, Templeton E, Park BK (1995) Metabolism and bioactivation of clozapine by human liver in vitro. J Pharmacol Exp Ther 272:984-990.
44. Qiu MH, Chen MC, Fuller PM, Lu J (2016) Stimulation of the pontine parabrachial nucleus promotes wakefulness via extra-thalamic forebrain circuit nodes. Curr Biol 26:2301-2312.
45. Ray RS, Corcoran AE, Brust RD, Kim JC, Richerson GB, Nattie E, Dymecki SM (2011) Impaired respiratory and body temperature control upon acute serotonergic neuron inhibition. Science 333:637-642.
46. Redfern CH, Coward P, Degtyarev MY, Lee EK, Kwa AT, Hennighausen L, Bujard H, Fishman GI, Conklin BR (1999) Conditional expression and signaling of a specifically designed Gi-coupled receptor in transgenic mice. Nat Biotechnol 17:165-169.
47. Robinson S, Todd TP, Pasternak AR, Luikart BW, Skelton PD, Urban DJ, Bucci DJ (2014) Chemogenetic silencing of neurons in retrosplenial cortex disrupts sensory preconditioning. J Neurosci 34:10982-10988.
48. Salmi P, Ahlenius S (1996) Further evidence for clozapine as a dopamine D1 receptor agonist. Eur J Pharmacol 307:27-31.
49. Schotte A, Janssen PF, Megens AA, Leysen JE (1993) Occupancy of central neurotransmitter receptors by risperidone, clozapine and haloperidol, measured ex vivo by quantitative autoradiography. Brain Res 631:191-202.
50. Scofield MD, Boger HA, Smith RJ, Li H, Haydon PG, Kalivas PW (2015) Gq-DREADD selectively initiates glial glutamate release and inhibits cue-induced cocaine seeking. Biol Psychiatry 78:441-451.
51. Sengupta A, Winters B, Bagley EE, McNally GP (2016) Disrupted prediction error links excessive amygdala activation to excessive fear. J Neurosci 36:385-395.
52. Sur C, Mallorga PJ, Wittmann M, Jacobson MA, Pascarella D, Williams JB, Brandish PE, Pettibone DJ, Scolnick EM, Conn PJ (2003) N-desmethylclozapine, an allosteric agonist at muscarinic 1 receptor, potentiates N-methyl-D-aspartate receptor activity. Proc Natl Acad Sci U S A 100:13674-13679.
53. Swerdlow NR, Bakshi V, Geyer MA (1996) Seroquel restores sensorimotor gating in phencyclidine-treated rats. J Pharmacol Exp Ther 279:1290-1299.
54. Swerdlow NR, Weber M, Qu Y, Light GA, Braff DL (2008) Realistic expectations of prepulse inhibition in translational models for schizophrenia research. Psychopharmacology (Berl) 199:331-388.
55. Thomas DR, Dada A, Jones GA, Deisz RA, Gigout S, Langmead CJ, Werry TD, Hendry N, Hagan JJ, Davies CH, Watson JM (2010) N-desmethylclozapine (NDMC) is an antagonist at the human native muscarinic M(1) receptor. Neuropharmacology 58:1206-1214.
56. Wang S, Tan Y, Zhang JE, Luo M (2013) Pharmacogenetic activation of midbrain dopaminergic neurons induces hyperactivity. Neurosci Bull 29:517-524.
57. Wicker E, Forcelli PA (2016) Chemogenetic silencing of the midline and intralaminar thalamus blocks amygdala-kindled seizures. Exp Neurol 283:404-412.
58. Wirtshafter D, Stratford TR (2016) Chemogenetic inhibition of cells in the paramedian midbrain tegmentum increases locomotor activity in rats. Brain Res 1632:98-106.
59. Witten IB, Steinberg EE, Lee SY, Davidson TJ, Zalocusky KA, Brodsky M, Yizhar O, Cho SL, Gong S, Ramakrishnan C, Stuber GD, Tye KM, Janak PH, Deisseroth K (2011) Recombinase-driver rat lines: tools, techniques, and optogenetic application to dopamine-mediated reinforcement. Neuron 72:721-733.
60. Wong G, Kuoppamäki M, Hietala J, Lüddens H, Syvälahti E, Korpi ER (1996) Effects of clozapine metabolites and chronic clozapine treatment on rat brain GABAA receptors. Eur J Pharmacol 314:319-323.
61. Yau JO, McNally GP (2015) Pharmacogenetic excitation of dorsomedial prefrontal cortex restores fear prediction error. J Neurosci 35:74-83.
62. Yorgason JT, España RA, Jones SR (2011) Demon voltammetry and analysis software: analysis of cocaine-induced alterations in dopamine signaling using multiple kinetic measures. J Neurosci Methods 202:158-164.
63. Zhu H, Pleil KE, Urban DJ, Moy SS, Kash TL, Roth BL (2014) Chemogenetic inactivation of ventral hippocampal glutamatergic neurons disrupts consolidation of contextual fear memory. Neuropsychopharmacology 39:1880-1892.