Alterations in metabotropic glutamate receptor 1α and regulator of G protein signaling 4 in the prefrontal cortex in schizophrenia

American Journal of Psychiatry

Volumn 167, Issue 12, 2010, Pages 1489-1498

  Volk, David W ^a   Eggan, Stephen M ^a   Lewis, David A ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 ARACHIDONOYLGLYCEROL; 4 AMINOBUTYRIC ACID; ACYLGLYCEROL LIPASE; ENDOCANNABINOID; GLUTAMIC ACID; HALOPERIDOL; LIPOPROTEIN LIPASE; MESSENGER RNA; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 1ALPHA; OLANZAPINE; RGS4 PROTEIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; ENZYME METABOLISM; ENZYME SYNTHESIS; FEMALE; GABAERGIC SYSTEM; HUMAN; HUMAN TISSUE; MALE; MONKEY; NEUROTRANSMISSION; NONHUMAN; POLYMERASE CHAIN REACTION; PREFRONTAL CORTEX; PRIORITY JOURNAL; RNA ANALYSIS; SCHIZOPHRENIA;

ANIMALS; ANTIPSYCHOTIC AGENTS; BENZODIAZEPINES; FEMALE; HALOPERIDOL; HUMANS; LIPOPROTEIN LIPASE; MACACA FASCICULARIS; MALE; MIDDLE AGED; MONOACYLGLYCEROL LIPASES; PREFRONTAL CORTEX; RECEPTORS, METABOTROPIC GLUTAMATE; RGS PROTEINS; SCHIZOPHRENIA;

EID: 78649743311     PISSN: 0002953X     EISSN: 15357228     Source Type: Journal    
DOI: 10.1176/appi.ajp.2010.10030318     Document Type: Article

References (46)

1. Green MF: What are the functional consequences of neurocognitive deficits in schizophrenia? Am J Psychiatry 1996; 153:321-330
2. Elvevag B, Goldberg TE: Cognitive impairment in schizophrenia is the core of the disorder. Crit Rev Neurobiol 2000; 14:1-21
3. Lewis DA, Hashimoto T, Volk DW: Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 2005; 6:312-324
4. Hashimoto T, Arion D, Unger T, Maldonado-Aviles JG, Morris HM, Volk DW, Mirnics K, Lewis DA: Alterations in GABA-related transcriptome in the dorsolateral prefrontal cortex of subjects with schizophrenia. Mol Psychiatry 2008; 13:147-161
5. Lisman JE, Coyle JT, Green RW, Javitt DC, Benes FM, Heckers S, Grace AA: Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends Neurosci 2008; 31:234-242
6. Morishita W, Kirov SA, Alger BE: Evidence for metabotropic glutamate receptor activation in the induction of depolarizationinduced suppression of inhibition in hippocampal CA1. J Neurosci 1998; 18:4870-4882
7. Varma N, Carlson GC, Ledent C, Alger BE: Metabotropic glutamate receptors drive the endocannabinoid system in hippocampus. J Neurosci 2001; 21:RC188
8. Ohno-Shosaku T, Shosaku J, Tsubokawa H, Kano M: Cooperative endocannabinoid production by neuronal depolarization and group I metabotropic glutamate receptor activation. Eur J Neurosci 2002; 15:953-961
9. Edwards DA, Kim J, Alger BE: Multiple mechanisms of endocannabinoid response initiation in hippocampus. J Neurophysiol 2006; 95:67-75
10. Chevaleyre V, Castillo PE: Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 2003; 38:461-472
11. Anwyl R: Metabotropic glutamate receptor-dependent long-term potentiation. Neuropharmacology 2009; 56:735-740
12. Gupta DS, McCullumsmith RE, Beneyto M, Haroutunian V, Davis KL, Meador-Woodruff JH: Metabotropic glutamate receptor protein expression in the prefrontal cortex and striatum in schizophrenia. Synapse 2005; 57:123-131
13. Saugstad JA, Marino MJ, Folk JA, Hepler JR, Conn PJ: RGS4 inhibits signaling by group I metabotropic glutamate receptors. J Neurosci 1998; 18:905-913
14. Chowdari KV, Mirnics K, Semwal P, Wood J, Lawrence E, Bhatia T, Deshpande SN, Thelma BK, Ferrell RE, Middleton FA, Devlin B, Levitt P, Lewis DA, Nimgaonkar VL: Association and linkage analyses of RGS4 polymorphisms in schizophrenia. Hum Mol Genet 2002; 11:1373-1380
15. Mirnics K, Middleton FA, Stanwood GD, Lewis DA, Levitt P: Disease-specific changes in regulator of G-protein signaling 4 (RGS4) expression in schizophrenia. Mol Psychiatry 2001; 6:293-301
16. Erdely HA, Tamminga CA, Roberts RC, Vogel MW: Regional alterations in RGS4 protein in schizophrenia. Synapse 2006; 59:472-479
17. Stella N, Schweitzer P, Piomelli D: A second endogenous cannabinoid that modulates long-term potentiation. Nature 1997; 388:773-778
18. Yoshida T, Fukaya M, Uchigashima M, Miura E, Kamiya H, Kano M, Watanabe M: Localization of diacylglycerol lipase-alpha around postsynaptic spine suggests close proximity between production site of an endocannabinoid, 2-arachidonoyl-glycerol, and presynaptic cannabinoid CB1 receptor. J Neurosci 2006; 26:4740-4751
19. Katona I, Urban GM, Wallace M, Ledent C, Jung KM, Piomelli D, Mackie K, Freund TF: Molecular composition of the endocannabinoid system at glutamatergic synapses. J Neurosci 2006; 26:5628-5637
20. Katona I, Sperlagh B, Sik A, Kafalvi A, Vizi ES, Mackie K, Freund TF: Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 1999; 19:4544-4558
21. Kawamura Y, Fukaya M, Maejima T, Yoshida T, Miura E, Watanabe M, Ohno-Shosaku T, Kano M: The CB1 cannabinoid receptor is the major cannabinoid receptor at excitatory presynaptic sites in the hippocampus and cerebellum. J Neurosci 2006; 26:2991-3001
22. Katona I, Freund TF: Endocannabinoid signaling as a synaptic circuit breaker in neurological disease. Nat Med 2008; 14:923-930
23. Dinh TP, Carpenter D, Leslie FM, Freund TF, Katona I, Sensi SL, Kathuria S, Piomelli D: Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc Natl Acad Sci U S A 2002; 99:10819-10824
24. Jung KM, Mangieri R, Stapleton C, Kim J, Fegley D, Wallace M, Mackie K, Piomelli D: Stimulation of endocannabinoid formation in brain slice cultures through activation of group I metabotropic glutamate receptors. Mol Pharmacol 2005; 68:1196-1202
25. Eggan SM, Hashimoto T, Lewis DA: Reduced cortical cannabinoid 1 receptor messenger RNA and protein expression in schizophrenia. Arch Gen Psychiatry 2008; 65:772-784
26. Palkovits M, Harvey-White J, Liu J, Kovacs ZS, Bobest M, Lovas G, Bago AG, Kunos G: Regional distribution and effects of postmortal delay on endocannabinoid content of the human brain. Neuroscience 2008; 152:1032-1039
27. Glantz LA, Lewis DA: Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch Gen Psychiatry 2000; 57:65-73
28. Imbeaud S, Graudens E, Boulanger V, Barlet X, Zaborski P, Eveno E, Mueller O, Schroeder A, Auffray C: Towards standardization of RNA quality assessment using user-independent classifiers of microcapillary electrophoresis traces. Nucleic Acids Res 2005; 33:1-12
29. Volk DW, Austin MC, Pierri JN, Sampson AR, Lewis DA: Decreased glutamic acid decarboxylase67 messenger RNA expression in a subset of prefrontal cortical gamma-aminobutyric acid neurons in subjects with schizophrenia. Arch Gen Psychiatry 2000; 57:237-245
30. Hashimoto T, Bazmi HH, Mirnics K, Wu Q, Sampson AR, Lewis DA: Conserved regional patterns of GABA-related transcript expression in the neocortex of subjects with schizophrenia. Am J Psychiatry 2008; 165:479-489
31. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F: Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002; 3:34.1-34.11
32. Bisogno T, Howell F, Williams G, Minassi A, Cascio MG, Ligresti A, Matias I, Schiano-Moriello A, Paul P, Williams EJ, Gangadharan U, Hobbs C, Di Marzo V, Doherty P: Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J Cell Biol 2003; 163:463-468
33. Dorph-Petersen KA, Pierri JN, Perel JM, Sun Z, Sampson AR, Lewis DA: The influence of chronic exposure to antipsychotic medications on brain size before and after tissue fixation: a comparison of haloperidol and olanzapine in macaque monkeys. Neuropsychopharmacology 2005; 30:1649-1661
34. Neter J, Kutner MH, Nachtsheim CJ, Wasserman W: Applied Linear Statistical Models, 4th ed, Vol 1. Boston, McGraw-Hill, 1996
35. Niehaus JL, Liu Y, Wallis KT, Egertova M, Bhartur SG, Mukhopadhyay S, Shi S, He H, Selley DE, Howlett AC, Elphick MR, Lewis DL: CB1 cannabinoid receptor activity is modulated by the cannabinoid receptor interacting protein CRIP 1a. Mol Pharmacol 2007; 72:1557-1566
36. Berman DM, Wilkie TM, Gilman AG: GAIP and RGS4 are GTPase-activating proteins for the Gi subfamily of G protein alpha subunits. Cell 1996; 86:445-452
37. 2 receptor-mediated signaling and adenylyl cyclase activity. Cell Signal 2004; 16:711-721
38. Yan Y, Chi PP, Bourne HR: RGS4 inhibits Gq-mediated activation of mitogen-activated protein kinase and phosphoinositide synthesis. J Biol Chem 1997; 272:11924-11927
39. Leontiadis LJ, Papakonstantinou MP, Georgoussi Z: Regulator of G protein signaling 4 confers selectivity to specific G proteins to modulate mu- and delta-opioid receptor signaling. Cell Signal 2009; 21:1218-1228
40. Sanders AR, Duan J, Levinson DF, Shi J, He D, Hou C, Burrell GJ, Rice JP, Nertney DA, Olincy A, Rozic P, Vinogradov S, Buccola NG, Mowry BJ, Freedman R, Amin F, Black DW, Silverman JM, Byerley WF, Crowe RR, Cloninger CR, Martinez M, Gejman PV: No significant association of 14 candidate genes with schizophrenia in a large European ancestry sample: implications for psychiatric genetics. Am J Psychiatry 2008; 165:497-506
41. Talkowski ME, Seltman H, Bassett AS, Brzustowicz LM, Chen X, Chowdari KV, Collier DA, Cordeiro Q, Corvin AP, Deshpande SN, Egan MF, Gill M, Kendler KS, Kirov G, Heston LL, Levitt P, Lewis DA, Li T, Mirnics K, Morris DW, Norton N, O'Donovan MC, Owen MJ, Richard C, Semwal P, Sobell JL, St Clair D, Straub RE, Thelma BK, Vallada H, Weinberger DR, Williams NM, Wood J, Zhang F, Devlin B, Nimgaonkar VL: Evaluation of a susceptibility gene for schizophrenia: genotype based meta-analysis of RGS4 polymorphisms from thirteen independent samples. Biol Psychiatry 2006; 60:152-162
42. Prasad KM, Chowdari KV, Nimgaonkar VL, Talkowski ME, Lewis DA, Keshavan MS: Genetic polymorphisms of the RGS4 and dorsolateral prefrontal cortex morphometry among first episode schizophrenia patients. Mol Psychiatry 2005; 10: 213-219
43. Buckholtz JW, Meyer-Lindenberg A, Honea RA, Straub RE, Pezawas L, Egan MF, Vakkalanka R, Kolachana B, Verchinski BA, Sust S, Mattay VS, Weinberger DR, Callicott JH: Allelic variation in RGS4 impacts functional and structural connectivity in the human brain. J Neurosci 2007; 27:1584-1593
44. Muly EC, Maddox M, Smith Y: Distribution of mGluR1alpha and m GluR5 immunolabeling in primate prefrontal cortex. J Comp Neurol 2003; 467:521-535
45. Paspalas CD, Selemon LD, Arnsten AF: Mapping the regulator of G protein signaling 4 (RGS4): presynaptic and postsynaptic substrates for neuroregulation in prefrontal cortex. Cereb Cortex 2009; 19:2145-2155
46. Chevaleyre V, Takahashi KA, Castillo PE: Endocannabinoid-mediated synaptic plasticity in the CNS. Annu Rev Neurosci 2006; 29:37-76