Differential effects of AMPA receptor potentiators and glycine reuptake inhibitors on antipsychotic efficacy and prefrontal glutamatergic transmission

Psychopharmacology

Volumn 221, Issue 1, 2012, Pages 115-131

  Jardemark, Kent ^a   Marcus, Monica M ^a   Malmerfelt, Anna ^a   Shahid, Mohammed ^b,c   Svensson, Torgny H ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b MSD   (United Kingdom)

^c PRECLIN 2D Ltd   (United Kingdom)

Author keywords

AMPA receptor potentiators; Antipsychotic; GlyT1 inhibitor; Org 24448; Org 25935; Org 26576; Schizophrenia

Indexed keywords

AMPA RECEPTOR; FARAMPATOR; GLYCINE REUPTAKE INHIBITOR; GLYCINE TRANSPORTER 1; HALOPERIDOL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROLEPTIC AGENT; OLANZAPINE; ORG 25935; ORG 26576; RISPERIDONE; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; CATALEPSY; CATAPLEXY; COGNITIVE DEFECT; CONTROLLED STUDY; DRUG ACTIVITY; DRUG EFFICACY; EXCITATORY POSTSYNAPTIC POTENTIAL; EXTRAPYRAMIDAL SYMPTOM; FACILITATION; IN VITRO STUDY; MALE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT;

ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; ANTIPSYCHOTIC AGENTS; AVOIDANCE LEARNING; BENZODIAZEPINES; CATALEPSY; DRUG SYNERGISM; GLUTAMIC ACID; GLYCINE PLASMA MEMBRANE TRANSPORT PROTEINS; HALOPERIDOL; MALE; MEMBRANE POTENTIALS; OXADIAZOLES; PIPERIDINES; PREFRONTAL CORTEX; RATS; RATS, WISTAR; RECEPTORS, AMPA; RISPERIDONE; SYNAPTIC TRANSMISSION; TETRAHYDRONAPHTHALENES;

EID: 84859648778     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-011-2554-3     Document Type: Article

References (68)

1. Ahlenius S, Hillegaart V (1986) Involvement of extrapyramidal motor mechanisms in the suppression of locomotor activity by antipsychotic drugs: a comparison between the effects produced by pre- and post-synaptic inhibition of dopaminergic neurotransmission. Pharmacol Biochem Behav 24:1409-1415 (Pubitemid 16067429)
2. Akbarian S, Sucher NJ, Bradley D, Tafazzoli A, Trinh D, Hetrick WP, Potkin SG, Sandman CA, Bunney WE Jr, Jones EG (1996) Selective alterations in gene expression for NMDA receptor subunits in prefrontal cortex of schizophrenics. J Neurosci 16:19-30 (Pubitemid 26010694)
3. Arvanov VL, Liang X, Schwartz J, Grossman S, Wang RY (1997) Clozapine and haloperidol modulate N-methyl-D-aspartate- and non-N-methyl-D-aspartate receptor-mediated neurotransmission in rat prefrontal cortical neurons in vitro. J Pharmacol Exp Ther 283:226-234 (Pubitemid 27438966)
4. Arvanov VL, Wang RY (1998) M100907, a selective 5-HT2A receptor antagonist and a potential antipsychotic drug, facilitates N-methyl-D-aspartate- receptor mediated neurotransmission in the rat medial prefrontal cortical neurons in vitro. Neuropsychopharmacology 18:197-209 (Pubitemid 28062583)
5. Beneyto M, Meador-Woodruff JH (2008) Lamina-specific abnormalities of NMDA receptor-associated postsynaptic protein transcripts in the prefrontal cortex in schizophrenia and bipolar disorder. Neuropsychopharmacology 33:2175-2186 (Pubitemid 351992080)
6. Borowsky B, Mezey E, Hoffman BJ (1993) Two glycine transporter variants with distinct localization in the CNS and peripheral tissues are encoded by a common gene. Neuron 10:851-863 (Pubitemid 23152041)
7. Camperi M, Wang XJ (1998) A model of visuospatial working memory in prefrontal cortex: recurrent network and cellular bistability. J Comput Neurosci 5:383-405 (Pubitemid 28554680)
8. Chen G, Greengard P, Yan Z (2004) Potentiation of NMDA receptor currents by dopamine D1 receptors in prefrontal cortex. Proc Natl Acad Sci U S A 101:2596-2600 (Pubitemid 38269356)
9. Chen L, Muhlhauser M, Yang CR (2003) Glycine transporter-1 blockade potentiates NMDA-mediated responses in rat prefrontal cortical neurons in vitro and in vivo. J Neurophysiol 89:691-703 (Pubitemid 36206118)
10. Chen L, Yang CR (2002) Interaction of dopamine D1 and NMDA receptors mediates acute clozapine potentiation of glutamate EPSPs in rat prefrontal cortex. J Neurophysiol 87:2324-2336 (Pubitemid 34670705)
11. Damgaard T, Larsen DB, Hansen SL, Grayson B, Neill JC, Plath N (2010) Positive modulation of alpha-amino-3-hydroxy-5-methyl- 4-isoxazolepropionic acid (AMPA) receptors reverses subchronic PCP-induced deficits in the novel object recognition task in rats. Behav Brain Res 207:144-150
12. Deutsch SI, Mastropaolo J, Schwartz BL, Rosse RB, Morihisa JM (1989) A "glutamatergic hypothesis" of schizophrenia. Rationale for pharmacotherapy with glycine. Clin Neuropharmacol 12:1-13 (Pubitemid 19058128)
13. Dracheva S, Marras SA, Elhakem SL, Kramer FR, Davis KL, Haroutunian V (2001) N-Methyl-D-aspartic acid receptor expression in the dorsolateral prefrontal cortex of elderly patients with schizophrenia. Am J Psychiatry 158:1400-1410 (Pubitemid 32847238)
14. Durstewitz D, Seamans JK, Sejnowski TJ (2000) Neurocomputational models of working memory. Nat Neurosci 3(Suppl):1184-1191
15. Evins AE, Fitzgerald SM, Wine L, Rosselli R, Goff DC (2000) Placebo-controlled trial of glycine added to clozapine in schizophrenia. Am J Psychiatry 157:826-828 (Pubitemid 30249667)
16. Goff DC, Henderson DC, Evins AE, Amico E (1999a) A placebocontrolled crossover trial of D-cycloserine added to clozapine in patients with schizophrenia. Biol Psychiatry 45:512-514 (Pubitemid 29130454)
17. Goff DC, Lamberti JS, Leon AC, Green MF, Miller AL, Patel J, Manschreck T, Freudenreich O, Johnson SA (2008) A placebocontrolled add-on trial of the ampakine, CX516, for cognitive deficits in schizophrenia. Neuropsychopharmacology 33:465-472
18. Goff DC, Leahy L, Berman I, Posever T, Herz L, Leon AC, Johnson SA, Lynch G (2001) A placebo-controlled pilot study of the ampakine CX516 added to clozapine in schizophrenia. J Clin Psychopharmacol 21:484-487 (Pubitemid 32937430)
19. Goff DC, Tsai G, Levitt J, Amico E, Manoach D, Schoenfeld DA, Hayden DL, McCarley R, Coyle JT (1999b) A placebocontrolled trial of D-cycloserine added to conventional neuroleptics in patients with schizophrenia. Arch Gen Psychiatry 56:21-27 (Pubitemid 29055046)
20. Hamlyn E, Brand L, Shahid M, Harvey BH (2009) The ampakine, Org 26576, bolsters early spatial reference learning and retrieval in the Morris water maze: a subchronic, dose-ranging study in rats. Behav Pharmacol 20(7):662-667
21. Heresco-Levy U, Ermilov M, Lichtenberg P, Bar G, Javitt DC (2004) High-dose glycine added to olanzapine and risperidone for the treatment of schizophrenia. Biol Psychiatry 55:165-171 (Pubitemid 38367720)
22. Heresco-Levy U, Javitt DC, Ebstein R, Vass A, Lichtenberg P, Bar G, Catinari S, Ermilov M (2005) D-Serine efficacy as add-on pharmacotherapy to risperidone and olanzapine for treatmentrefractory schizophrenia. Biol Psychiatry 57:577-585 (Pubitemid 40409697)
23. Heresco-Levy U, Javitt DC, Ermilov M, Mordel C, Horowitz A, Kelly D (1996) Double-blind, placebo-controlled, crossover trial of glycine adjuvant therapy for treatment-resistant schizophrenia. Br J Psychiatry 169:610-617
24. Jardemark K, Marcus MM, Konradsson A, Svensson TH (2005) The combination of nicotine with the D2 antagonist raclopride or the weak D4 antagonist L-745,870 generates a clozapine-like facilitation of NMDA receptor-mediated neurotransmission in pyramidal cells of the rat medial prefrontal cortex. Int J Neuropsychopharmacol 8:157-162 (Pubitemid 40769256)
25. Jardemark K, Marcus MM, Shahid M, Svensson TH (2010) Effects of asenapine on prefrontal N-methyl-D-aspartate receptor-mediated transmission: involvement of dopamine D1 receptors. Synapse 64(11):870-874
26. Jardemark K, Ninan I, Svensson TH, Wang RY (2002) Differential effects of atypical and typical antipsychotic drugs on NMDAreceptor- mediated neurotransmission in pyramidal cells of the rat medial prefrontal cortex. Nord J Psychiatry 56:20
27. Jardemark KE, Konradsson A, Schilstrom B, Marcus MM, Svensson TH (2009) Differential effects of topiramate on prefrontal glutamatergic transmission when combined with raclopride or clozapine. Synapse 63:913-920
28. Jardemark KE, Liang X, Arvano V, Wang RY (2000) Subchronic treatment with either clozapine, olanzapine or haloperidol produces a hyposensitive response of the rat cortical cells to Nmethyl- D-aspartate. Neuroscience 100:1-9 (Pubitemid 30670296)
29. Javitt DC (2010) Glutamatergic theories of schizophrenia. Isr J Psychiatry Relat Sci 47:4-16
30. Javitt DC, Zukin SR (1991) Recent advances in the phencyclidine model of schizophrenia [see comments]. Am J Psychiatry 148:1301-1308
31. Johnson JW, Ascher P (1987) Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325:529-531 (Pubitemid 17056733)
32. Johnson SA, Luu NT, Herbst TA, Knapp R, Lutz D, Arai A, Rogers GA, Lynch G (1999) Synergistic interactions between ampakines and antipsychotic drugs. J Pharmacol Exp Ther 289:392-397 (Pubitemid 29156054)
33. Jordan GR, McCulloch J, Shahid M, Hill DR, Henry B, Horsburgh K (2005) Regionally selective and dose-dependent effects of the ampakines Org 26576 and Org 24448 on local cerebral glucose utilisation in the mouse as assessed by 14C-2-deoxyglucose autoradiography. Neuropharmacology 49(2):254-264 (Pubitemid 40933763)
34. Kalinichev M, Starr KR, Teague S, Bradford AM, Porter RA, Herdon HJ (2010) Glycine transporter 1 (GlyT1) inhibitors exhibit anticonvulsant properties in the rat maximal electroshock threshold (MEST) test. Brain Res 1331:105-113
35. Konradsson A, Marcus MM, Hertel P, Svensson TH, Jardemark KE (2006) Inhibition of the glycine transporter GlyT-1 potentiates the effect of risperidone, but not clozapine, on glutamatergic transmission in the rat medial prefrontal cortex. Synapse 60:102-108 (Pubitemid 43878118)
36. Lane HY, Chang YC, Liu YC, Chiu CC, Tsai GE (2005) Sarcosine or D-serine add-on treatment for acute exacerbation of schizophrenia: a randomized, double-blind, placebo-controlled study. Arch Gen Psychiatry 62:1196-1204
37. Lane HY, Huang CL, Wu PL, Liu YC, Chang YC, Lin PY, Chen PW, Tsai G (2006) Glycine transporter I inhibitor, N-methylglycine (sarcosine), added to clozapine for the treatment of schizophrenia. Biol Psychiatry 60:645-649
38. Lane HY, Lin CH, Huang YJ, Liao CH, Chang YC, Tsai GE (2010) A randomized, double-blind, placebo-controlled comparison study of sarcosine (N-methylglycine) and D-serine add-on treatment for schizophrenia. Int J Neuropsychopharmacol 13:451-460
39. Li CC (1964) Change-over design. Introduction to experimental statistics. McGraw-Hill, New York, pp 207-226
40. Lidö HH, Stomberg R, Fagerberg A, Ericson M, Söderpalm B (2009) The glycine reuptake inhibitor org 25935 interacts with basal and ethanol-induced dopamine release in rat nucleus accumbens. Alcohol Clin Exp Res 33(7):1151-1157
41. Luby ED, Cohen BD, Rosenbaum G, Gottlieb JS, Kelley R (1959) Study of a new schizophrenomimetic drug; sernyl. AMA Arch Neurol Psychiatry 81:363-369
42. Marcus MM, Jardemark KE, Wadenberg ML, Langlois X, Hertel P, Svensson TH (2005) Combined alpha2 and D2/3 receptor blockade enhances cortical glutamatergic transmission and reverses cognitive impairment in the rat. Int J Neuropsychopharmacol 8:315-327 (Pubitemid 41002487)
43. Marcus MM, Wiker C, Franberg O, Konradsson-Geuken A, Langlois X, Jardemark K, Svensson TH (2010) Adjunctive alpha2- adrenoceptor blockade enhances the antipsychotic-like effect of risperidone and facilitates cortical dopaminergic and glutamatergic, NMDA receptor-mediated transmission. Int J Neuropsychopharmacol 13:891-903
44. Molander A, Lidö HH, Löf E, Ericson M, Söderpalm B (2007) The glycine reuptake inhibitor Org 25935 decreases ethanol intake and preference in male Wistar rats. Alcohol Alcohol 42(1):11-18 (Pubitemid 46062634)
45. Möhler H, Boison D, Singer P, Feldon J, Pauly-Evers M, Yee BK (2011) Glycine transporter 1 as a potential therapeutic target for schizophrenia-related symptoms: evidence from genetically modified mouse models and pharmacological inhibition. Biochem Pharmacol 81:1065-1077
46. Neill JC, Barnes S, Cook S, Grayson B, Idris NF, McLean SL, Snigdha S, Rajagopal L, Harte MK (2010) Animal models of cognitive dysfunction and negative symptoms of schizophrenia: focus on NMDA receptor antagonism. Pharmacol Ther 128:419-432
47. Ninan I, Jardemark KE, Wang RY (2003a) Olanzapine and clozapine but not haloperidol reverse subchronic phencyclidine-induced functional hyperactivity of N-methyl-D-aspartate receptors in pyramidal cells of the rat medial prefrontal cortex. Neuropharmacology 44:462-472 (Pubitemid 36293978)
48. Ninan I, Jardemark KE, Wang RY (2003b) Differential effects of atypical and typical antipsychotic drugs on N-methyl-D-aspartate- and electrically evoked responses in the pyramidal cells of the rat medial prefrontal cortex. Synapse 48:66-79 (Pubitemid 36374000)
49. Ninan I, Wang RY (2003) Modulation of the ability of clozapine to facilitate NMDA- and electrically evoked responses in pyramidal cells of the rat medial prefrontal cortex by dopamine: pharmacological evidence. Eur J Neurosci 17:1306-1312 (Pubitemid 36459786)
50. Olney JW, Farber NB (1995) Glutamate receptor dysfunction and schizophrenia. Arch Gen Psychiatry 52:998-1007
51. Olsen CK, Kreilgaard M, Didriksen M (2006) Positive modulation of glutamatergic receptors potentiates the suppressive effects of antipsychotics on conditioned avoidance responding in rats. Pharmacol Biochem Behav 84:259-265 (Pubitemid 44107482)
52. Paxinos G, Watson C (2007) The rat brain in sterotaxic coordinates, 6th edn. Academic, London
53. Potkin SG, Jin Y, Bunney BG, Costa J, Gulasekaram B (1999) Effect of clozapine and adjunctive high-dose glycine in treatmentresistant schizophrenia. Am J Psychiatry 156:145-147 (Pubitemid 29034896)
54. Salmi P, Samuelsson J, Ahlenius S (1994) A new computer-assisted two-way avoidance conditioning equipment for rats: behavioral and pharmacological validation. J Pharmacol Toxicol Methods 32:155-159 (Pubitemid 24370739)
55. Shahid M, Walker GB, Zorn SH, Wong EH (2009) Asenapine: a novel psychopharmacologic agent with a unique human receptor signature. J Psychopharmacol 23(1):65-73
56. Shu Y, Hasenstaub A, McCormick DA (2003) Turning on and off recurrent balanced cortical activity. Nature 423:288-293 (Pubitemid 40852698)
57. Siegel S, Castellan NJ Jr (1988) Nonparametric statistics for the behavioral sciences. McGraw-Hill, New York
58. Smith KE, Borden LA, Hartig PR, Branchek T, Weinshank RL (1992) Cloning and expression of a glycine transporter reveal colocalization with NMDA receptors. Neuron 8:927-935
59. Su XW, Li XY, Banasr M, Koo JW, Shahid M, Henry B, Duman RS (2009) Chronic treatment with AMPA receptor potentiator Org 26576 increases neuronal cell proliferation and survival in adult rodent hippocampus. Psychopharmacology (Berl) 206(2):215-222
60. Svensson TH (2000) Dysfunctional brain dopamine systems induced by psychotomimetic NMDA-receptor antagonists and the effects of antipsychotic drugs. Brain Res Brain Res Rev 31:320-329
61. Tsai G, Lane HY, Yang P, Chong MY, Lange N (2004) Glycine transporter I inhibitor, N-methylglycine (sarcosine), added toantipsychotics for the treatment of schizophrenia. Biol Psychiatry 55:452-456 (Pubitemid 38338531)
62. Tsai GE, Yang P, Chung LC, Tsai IC, Tsai CW, Coyle JT (1999) DSerine added to clozapine for the treatment of schizophrenia. Am J Psychiatry 156:1822-1825 (Pubitemid 29517581)
63. Vengeliene V, Leonardi-Essmann F, Sommer WH, Marston HM, Spanagel R (2010) Glycine transporter-1 blockade leads to persistently reduced relapse-like alcohol drinking in rats. Biol Psychiatry 68(8):704-711
64. Wadenberg ML (2010) Conditioned avoidance response in the development of new antipsychotics. Curr Pharm Des 16:358-370
65. Wadenberg ML, Hicks PB (1999) The conditioned avoidance response test re-evaluated: is it a sensitive test for the detection of potentially atypical antipsychotics? Neurosci Biobehav Rev 23:851-862
66. Wadenberg ML, Wiker C, Svensson TH (2007) Enhanced efficacy of both typical and atypical antipsychotic drugs by adjunctive alpha2 adrenoceptor blockade: experimental evidence. Int J Neuropsychopharmacol 10:191-202
67. Wadenberg M-LG, Soliman A, VanderSpek SC, Kapur S (2001) Dopamine d(2) receptor occupancy is a common mechanism underlying animal models of antipsychotics and their clinical effects. Neuropsychopharmacology 25:633-641 (Pubitemid 32995945)
68. Wang XJ (1999) Synaptic basis of cortical persistent activity: the importance of NMDA receptors to working memory. J Neurosci 19:9587-9603