Positive allosteric modulation of GABAB receptors ameliorates sensorimotor gating in rodent models

CNS Neuroscience and Therapeutics

Volumn 20, Issue 7, 2014, Pages 679-684

  Frau, Roberto ^a   Bini, Valentina ^a   Pillolla, Giuliano ^a   Malherbe, Pari ^b   Pardu, Alessandra ^a   Thomas, Andrew W ^b   Devoto, Paola ^a   Bortolato, Marco ^a,c  

^a UNIVERSITY OF CAGLIARI   (Italy)

^b F HOFFMANN LA ROCHE LTD   (Switzerland)

^c UNIVERSITY OF KANSAS   (United States)

Author keywords

DBA 2J mice; NMDA receptors; Prepulse inhibition of the startle; Schizophrenia; Sensorimotor gating

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR BLOCKING AGENT; BACLOFEN; CLOZAPINE; DIZOCILPINE; RAC BHFF; UNCLASSIFIED DRUG; (R,S)-5,7-DI-TERT-BUTYL-3-HYDROXY-3-TRIFLUOROMETHYL-3H-BENZOFURAN-2-ONE; 4 AMINOBUTYRIC ACID B RECEPTOR; BENZOFURAN DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; MALE; MOUSE; NONHUMAN; PREPULSE INHIBITION; RAT; SCANNING ELECTRON MICROSCOPY; SENSORY GATING; STARTLE REFLEX; ALLOSTERISM; ANIMAL; C57BL MOUSE; DBA MOUSE; DRUG EFFECTS; PHYSIOLOGY; RANDOMIZATION; SPRAGUE DAWLEY RAT;

ALLOSTERIC REGULATION; ANIMALS; BENZOFURANS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MODELS, ANIMAL; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-B; SENSORY GATING;

EID: 84902546231     PISSN: 17555930     EISSN: 17555949     Source Type: Journal    
DOI: 10.1111/cns.12261     Document Type: Article

References (58)

1. Benes FM, Berretta S. GABAergic interneurons: Implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacology 2001;25:1-27.
2. Blum BP, Mann JJ. The GABAergic system in schizophrenia. Int J Neuropsychopharmacol 2002;5:159-179.
3. Wassef A, Baker J, Kochan LD. GABA and schizophrenia: A review of basic science and clinical studies. J Clin Psychopharmacol 2003;23:601-640.
4. Mizukami K, Ishikawa M, Hidaka S, Iwakiri M, Sasaki M, Iritani S. Immunohistochemical localization of GABAB receptor in the entorhinal cortex and inferior temporal cortex of schizophrenic brain. Prog Neuropsychopharmacol Biol Psychiatry 2002;26:393-396.
5. Ishikawa M, Mizukami K, Iwakiri M, Asada T. Immunohistochemical and immunoblot analysis of gamma-aminobutyric acid B receptor in the prefrontal cortex of subjects with schizophrenia and bipolar disorder. Neurosci Lett 2005;383:272-277.
6. Fatemi SH, Folsom TD, Thuras PD. Deficits in GABA(B) receptor system in schizophrenia and mood disorders: A postmortem study. Schizophr Res 2011;128:37-43.
7. Gandal MJ, Sisti J, Klook K, et al. GABAB-mediated rescue of altered excitatory-inhibitory balance, gamma synchrony and behavioral deficits following constitutive NMDAR-hypofunction. Transl Psychiatry 2012;2:e142.
8. Hasan A, Wobrock T, Grefkes C, et al. Deficient inhibitory cortical networks in antipsychotic-naive subjects at risk of developing first-episode psychosis and first-episode schizophrenia patients: A cross-sectional study. Biol Psychiatry 2012;72:744-751.
9. Kehrer C, Maziashvili N, Dugladze T, Gloveli T. Altered excitatory-inhibitory balance in the NMDA-hypofunction model of schizophrenia. Front Mol Neurosci 2008;8:1-7.
10. Yizhar O, Fenno LE, Prigge M, et al. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 2011;477:171-178.
11. Bortolato M, Frau R, Aru GN, Orrù M, Gessa GL. Baclofen reverses the reduction in prepulse inhibition of the acoustic startle response induced by dizocilpine, but not by apomorphine. Psychopharmacology 2004;171:322-330.
12. Fejgin K, Pålsson E, Wass C, Finnerty N, Lowry J, Klamer D. Prefrontal GABA(B) receptor activation attenuates phencyclidine-induced impairments of prepulse inhibition: Involvement of nitric oxide. Neuropsychopharmacology 2009;7:1673-1684.
13. Arai S, Takuma K, Mizoguchi H, et al. Involvement of pallidotegmental neurons in methamphetamine- and MK-801-induced impairment of prepulse inhibition of the acoustic startle reflex in mice: Reversal by GABAB receptor agonist baclofen. Neuropsychopharmacology 2008;33:3164-3175.
14. Vollenweider FX, Geyer MA. A systems model of altered consciousness: Integrating natural and drug-induced psychoses. Brain Res Bull 2001;56:495-507.
15. Braff DL, Geyer MA, Swerdlow NR. Human studies of prepulse inhibition of startle: Normal subjects, patient groups, and pharmacological studies. Psychopharmacology 2001;156:234-258.
16. Koch M. Clinical relevance of animal models of schizophrenia. Suppl Clin Neurophysiol 2013;62:113-120.
17. Bortolato M, Frau R, Orrù M, et al. Activation of GABA(B) receptors reverses spontaneous gating deficits in juvenile DBA/2J mice. Psychopharmacology 2007;194:361-369.
18. Olivier B, Leahy C, Mullen T, et al. The DBA/2J strain and prepulse inhibition of startle: A model system to test antipsychotics? Psychopharmacology 2001;156:284-290.
19. Daskalakis ZJ, George TP. Clozapine, GABA(B), and the treatment of resistant schizophrenia. Clin Pharmacol Ther 2009;86:442-446.
20. Gulmann NC, Bahr B, Andersen B, Eliassen HM. A double-blind trial of baclofen against placebo in the treatment of schizophrenia. Acta Psychiatr Scand 1976;54:287-293.
21. Frederiksen PK. Letter: Baclofen in the treatment of schizophrenia. Lancet 1975;1:702.
22. Schöpf J, Hucker H. Baclofen in the treatment of schizophrenia: A pilot study. Pharmakopsychiatr Neuropsychopharmakol 1977;10:89-91.
23. Bowery NG. GABAB receptor: A site of therapeutic benefit. Curr Opin Pharmacol 2006;6:37-43.
24. Sullivan R, Hodgman MJ, Kao L, Tormoehlen LM. Baclofen overdose mimicking brain death. Clin Toxicol (Phila) 2012;50:141-144.
25. Malherbe P, Masciadri R, Norcross RD, et al. Characterization of (R, S)-5, 7-di-tert-butyl-3-hydroxy-3-trifluoromethyl-3H-benzofuran-2-one as a positive allosteric modulator of GABAB receptors. Br J Pharmacol 2008;154:797-811.
26. Urwyler S, Mosbacher J, Lingenhoehl K, et al. Positive allosteric modulation of native and recombinant gamma-aminobutyric acid(B) receptors by 2, 6-Di-tert-butyl-4-(3-hydroxy-2, 2-dimethyl-propyl)-phenol (CGP7930) and its aldehyde analog CGP13501. Mol Pharmacol 2001;60:963-971.
27. Urwyler S, Pozza MF, Lingenhoehl K, et al. N, N'-Dicyclopentyl-2-methylsulfanyl-5-nitro-pyrimidine-4, 6-diamine (GS39783) and structurally related compounds: Novel allosteric enhancers of gamma-aminobutyric acidB receptor function. J Pharmacol Exp Ther 2003;307:322-330.
28. Carai MA, Colombo G, Froestl W, Gessa GL. In vivo effectiveness of CGP7930, a positive allosteric modulator of the GABAB receptor. Eur J Pharmacol 2004;504:213-216.
29. Cryan JF, Kelly PH, Chaperon F, et al. Behavioral characterization of the novel GABAB receptor-positive modulator GS39783 (N, N'-dicyclopentyl-2-methylsulfanyl-5-nitro-pyrimidine-4, 6-diamine): Anxiolytic-like activity without side effects associated with baclofen or benzodiazepines. J Pharmacol Exp Ther 2004;310:952-963.
30. Jacobson LH, Cryan JF. Evaluation of the anxiolytic-like profile of the GABAB receptor positive modulator CGP7930 in rodents. Neuropharmacology 2008;54:854-862.
31. Koek W, France CP, Cheng K, Rice KC. GABAB receptor-positive modulators: Enhancement of GABAB receptor agonist effects in vivo. J Pharmacol Exp Ther 2010;335:163-171.
32. Frau R, Orrù M, Fà M, et al. Effects of topiramate on the prepulse inhibition of the acoustic startle in rats. Neuropsychopharmacology 2007;32:320-331.
33. Koek W, France CP, Cheng K, Rice KC. Effects of the GABAB receptor-positive modulators CGP7930 and rac-BHFF in baclofen- and γ-hydroxybutyrate-discriminating pigeons. J Pharmacol Exp Ther 2012;341:369-376.
34. Koek W, Cheng K, Rice KC. Discriminative stimulus effects of the GABAB receptor-positive modulator rac-BHFF: Comparison with GABAB receptor agonists and drugs of abuse. J Pharmacol Exp Ther 2013;344:553-560.
35. Swerdlow NR, Geyer MA. Using an animal model of deficient sensorimotor gating to study the pathophysiology and new treatments of schizophrenia. Schizophr Bull 1998;24:285-301.
36. Bakshi VP, Swerdlow NR, Geyer MA. Clozapine antagonizes phencyclidine-induced deficits in sensorimotor gating of the startle response. J Pharmacol Exp Ther 1994;2:787-794.
37. Bakshi VP, Geyer MA. Antagonism of phencyclidine-induced deficits in prepulse inhibition by the putative atypical antipsychotic olanzapine. Psychopharmacology 1995;2:198-201.
38. Geyer MA, Krebs-Thomson K, Braff DL, Swerdlow NR. Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: A decade in review. Psychopharmacology 2001;156:117-154.
39. Javitt DC, Zukin SR. Recent advances in the phencyclidine model of schizophrenia. Am J Psychiatry 1991;10:1301-1308.
40. Umbricht D, Schmid L, Koller R, Vollenweider FX, Hell D, Javitt DC. Ketamine-induced deficits in auditory and visual context-dependent processing in healthy volunteers: Implications for models of cognitive deficits in schizophrenia. Arch Gen Psychiatry 2000;57:1139-1147.
41. Bakshi VP, Geyer MA. Multiple limbic regions mediate the disruption of prepulse inhibition produced in rats by the noncompetitive NMDA antagonist dizocilpine. J Neurosci 1998;18:8394-8401.
42. Bowery NG. Historical perspective and emergence of the GABAB receptor. Adv Pharmacol 2010;58:1-18.
43. Roenker NL, Gudelsky GA, Ahlbrand R, Horn PS, Richtand NM. Evidence for involvement of nitric oxide and GABA(B) receptors in MK-801- stimulated release of glutamate in rat prefrontal cortex. Neuropharmacology 2012;63:575-581.
44. Moghaddam B, Adams B, Verma A, Daly D. Activation of glutamatergic neurotransmission by ketamine: A novel step in the pathway from NMDA receptor blockade to dopaminergic and cognitive disruptions associated with the prefrontal cortex. J Neurosci 1997;17:2921-2927.
45. Takahashi K, Nagai T, Kamei H, et al. Neural circuits containing pallidotegmental GABAergic neurons are involved in the prepulse inhibition of the startle reflex in mice. Biol Psychiatry 2007;62:148-157.
46. Elias PK, Elias MF, Eleftheriou BE. Emotionality, exploratory behavior, and locomotion in aging inbred strains of mice. Gerontologia 1975;1:46-55.
47. Randt CT, Blizard DA, Friedman E. Early life undernutrition and aggression in two mouse strains. Dev Psychobiol 1975;3:275-279.
48. Anisman H. Differential effects of scopolamine and D-amphetamine on avoidance: Strain interactions. Pharmacol Biochem Behav 1975;3:809-817.
49. Stavnes KL, Sprott RL. Genetic analysis of active avoidance performance in mice. Psychol Rep 1975;36:515-521.
50. Lu Y, Wehner JM. Enhancement of contextual fear-conditioning by putative (+/-)-alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) receptor modulators and N-methyl-D-aspartate (NMDA) receptor antagonists in DBA/2J mice. Brain Res 1997;768:197-207.
51. Rajagopal L, Massey BW, Huang M, Oyamada Y, Meltzer HY. The novel object recognition test in rodents in relation to cognitive impairment in schizophrenia. Curr Pharm Des 2013 [Epub ahead of print].
52. Jones CA, Watson DJ, Fone KC. Animal models of schizophrenia. Br J Pharmacol 2011;164:1162-1194.
53. Hikida T, Jaaro-Peled H, Seshadri S, et al. Dominant-negative DISC1 transgenic mice display schizophrenia-associated phenotypes detected by measures translatable to humans. Proc Natl Acad Sci 2007;104:14501-14506.
54. Karl T, Duffy L, Scimone A, Harvey RP, Schofield PR. Altered motor activity, exploration and anxiety in heterozygous neuregulin 1 mutant mice: Implications for understanding schizophrenia. Genes Brain Behav 2007;6:677-687.
55. Kvajo M, McKellar H, Arguello PA, et al. A mutation in mouse Disc1 that models a schizophrenia risk allele leads to specific alterations in neuronal architecture and cognition. Proc Natl Acad Sci 2008;105:7076-7081.
56. Neill JC, Barnes S, Cook S, et al. Animal models of cognitive dysfunction and negative symptoms of schizophrenia: Focus on NMDA receptor antagonism. Pharmacol Ther 2010;128:419-432.
57. Savage S, Kehr J, Olson L, Mattsson A. Impaired social interaction and enhanced sensitivity to phencyclidine-induced deficits in novel object recognition in rats with cortical cholinergic denervation. Neuroscience 2011;195:60-69.
58. Meltzer HY, Rajagopal L, Huang M, Oyamada Y, Kwon S, Horiguchi M. Translating the N-methyl-D-aspartate receptor antagonist model of schizophrenia to treatments for cognitive impairment in schizophrenia. Int J Neuropsychopharmacol 2013;16:2181-2194.