GluN2D N-methyl-D-aspartate receptor subunit contribution to the stimulation of brain activity and gamma oscillations by ketamine: Implications for schizophrenia

Journal of Pharmacology and Experimental Therapeutics

Volumn 356, Issue 3, 2016, Pages 702-711

  Sapkota, Kiran ^a   Mao, Zhihao ^a   Synowicki, Paul ^a   Lieber, Dillon ^a   Liu, Meng ^a   Ikezu, Tsuneya ^b   Gautam, Vivek ^c   Monaghan, Daniel T ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KETAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR EPSILON 4; PARVALBUMIN; UNCLASSIFIED DRUG; AMINO ACID RECEPTOR BLOCKING AGENT; NR2D NMDA RECEPTOR; PROTEIN SUBUNIT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; ENTORHINAL CORTEX; FREQUENCY MODULATION; GAMMA RHYTHM; INFERIOR COLLICULUS; LOCOMOTION; MALE; MEDIAL PREFRONTAL CORTEX; MOUSE; NEUROPATHOLOGY; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUTAMEN; SCHIZOPHRENIA; SENSORY GATING; SOMATOSENSORY CORTEX; SPATIAL LEARNING; SPATIAL MEMORY; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; C57BL MOUSE; DEFICIENCY; DRUG EFFECTS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; PROTEIN SUBUNIT;

ANIMALS; BRAIN; EXCITATORY AMINO ACID ANTAGONISTS; GAMMA RHYTHM; KETAMINE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTEIN SUBUNITS; RECEPTORS, N-METHYL-D-ASPARTATE; SCHIZOPHRENIA;

EID: 84959019728     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.115.230391     Document Type: Article

References (88)

1. Abekawa T, Ito K, Nakagawa S, and Koyama T (2007) Prenatal exposure to an NMDA receptor antagonist, MK-801 reduces density of parvalbumin-immunoreactive GABAergic neurons in the medial prefrontal cortex and enhances phencyclidineinduced hyperlocomotion but not behavioral sensitization to methamphetamine in postpubertal rats. Psychopharmacology (Berl) 192:303-316.
2. Abel KM, Allin MP, Hemsley DR, and Geyer MA (2003) Low dose ketamine increases prepulse inhibition in healthy men. Neuropharmacology 44:729-737.
3. Allen NC, Bagade S, McQueen MB, Ioannidis JP, Kavvoura FK, Khoury MJ, Tanzi RE, and Bertram L (2008) Systematic meta-analyses and field synopsis of genetic association studies in schizophrenia: the SzGene database. Nat Genet 40:827-834.
4. Anis NA, Berry SC, Burton NR, and Lodge D (1983) The dissociative anaesthetics, ketamine and phencyclidine, selectively reduce excitation of central mammalian neurones by N-methyl-aspartate. Br J Pharmacol 79:565-575.
5. Balu DT and Coyle JT (2011) Neuroplasticity signaling pathways linked to the pathophysiology of schizophrenia. Neurosci Biobehav Rev 35:848-870.
6. Beaton JA, Stemsrud K, and Monaghan DT (1992) Identification of a novel N-methyl-D-aspartate receptor population in the rat medial thalamus. J Neurochem 59: 754-757.
7. Behrens MM, Ali SS, Dao DN, Lucero J, Shekhtman G, Quick KL, and Dugan LL (2007) Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase. Science 318:1645-1647.
8. Belforte JE, Zsiros V, Sklar ER, Jiang Z, Yu G, Li Y, Quinlan EM, and Nakazawa K (2010) Postnatal NMDA receptor ablation in corticolimbic interneurons confers schizophrenia-like phenotypes. Nat Neurosci 13:76-83.
9. Benneyworth MA, Roseman AS, Basu AC, and Coyle JT (2011) Failure of NMDA receptor hypofunction to induce a pathological reduction in PV-positive GABAergic cell markers. Neurosci Lett 488:267-271.
10. Billingslea EN, Tatard-Leitman VM, Anguiano J, Jutzeler CR, Suh J, Saunders JA, Morita S, Featherstone RE, Ortinski PI, and Gandal MJ, et al. (2014) Parvalbumin cell ablation of NMDA-R1 causes increased resting network excitability with associated social and self-care deficits. Neuropsychopharmacology 39:1603-1613.
11. Buller AL, Larson HC, Schneider BE, Beaton JA, Morrisett RA, and Monaghan DT (1994) The molecular basis of NMDA receptor subtypes: native receptor diversity is predicted by subunit composition. J Neurosci 14:5471-5484.
12. Bullock WM, Bolognani F, Botta P, Valenzuela CF, and Perrone-Bizzozero NI (2009) Schizophrenia-like GABAergic gene expression deficits in cerebellar Golgi cells from rats chronically exposed to low-dose phencyclidine. Neurochem Int 55: 775-782.
13. Carlén M, Meletis K, Siegle JH, Cardin JA, Futai K, Vierling-Claassen D, Rühlmann C, Jones SR, Deisseroth K, and Sheng M, et al. (2012) A critical role for NMDA receptors in parvalbumin interneurons for gamma rhythm induction and behavior. Mol Psychiatry 17:537-548.
14. Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser MB, and Moser EI (2009) Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462:353-357.
15. Coyle JT (2006) Glutamate and schizophrenia: beyond the dopamine hypothesis. Cell Mol Neurobiol 26:365-384.
16. Coyle JT, Tsai G, and Goff D (2003) Converging evidence of NMDA receptor hypofunction in the pathophysiology of schizophrenia. Ann N Y Acad Sci 1003:318-327.
17. Dravid SM, Erreger K, Yuan H, Nicholson K, Le P, Lyuboslavsky P, Almonte A, Murray E, Mosely C, and Barber J, et al. (2007) Subunit-specific mechanisms and proton sensitivity of NMDA receptor channel block. J Physiol 581:107-128.
18. Duan AR, Varela C, Zhang Y, Shen Y, Xiong L, Wilson MA, and Lisman J (2015) Delta frequency optogenetic stimulation of the thalamic nucleus reuniens is sufficient to produce working memory deficits: relevance to schizophrenia. Biol Psychiatry 77:1098-1107.
19. Duncan G, Miyamoto S, Gu H, Lieberman J, Koller B, and Snouwaert J (2002) Alterations in regional brain metabolism in genetic and pharmacological models of reduced NMDA receptor function. Brain Res 951:166-176.
20. Duncan GE, Miyamoto S, Leipzig JN, and Lieberman JA (1999) Comparison of brain metabolic activity patterns induced by ketamine, MK-801 and amphetamine in rats: support for NMDA receptor involvement in responses to subanesthetic dose of ketamine. Brain Res 843:171-183.
21. Duncan GE, Miyamoto S, Leipzig JN, and Lieberman JA (2000) Comparison of the effects of clozapine, risperidone, and olanzapine on ketamine-induced alterations in regional brain metabolism. J Pharmacol Exp Ther 293:8-14.
22. Fields RD (2008) White matter in learning, cognition and psychiatric disorders. Trends Neurosci 31:361-370.
23. Fradley RL, O'Meara GF, Newman RJ, Andrieux A, Job D, and Reynolds DS (2005) STOP knockout and NMDA NR1 hypomorphic mice exhibit deficits in sensorimotor gating. Behav Brain Res 163:257-264.
24. Frassoni C, Bentivoglio M, Spreafico R, Sánchez MP, Puelles L, and Fairen A (1991) Postnatal development of calbindin and parvalbumin immunoreactivity in the thalamus of the rat. Brain Res Dev Brain Res 58:243-249.
25. Goda SA, Olszewski M, Piasecka J, Rejniak K, Whittington MA, Kasicki S, and Hunt MJ (2015) Aberrant high frequency oscillations recorded in the rat nucleus accumbens in the methylazoxymethanol acetate neurodevelopmental model of schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 61:44-51.
26. Gonzalez-Burgos G, Hashimoto T, and Lewis DA (2010) Alterations of cortical GABA neurons and network oscillations in schizophrenia. Curr Psychiatry Rep 12: 335-344.
27. Gonzalez-Burgos G and Lewis DA (2008) GABA neurons and the mechanisms of network oscillations: implications for understanding cortical dysfunction in schizophrenia. Schizophr Bull 34:944-961.
28. Greenwood TA, Light GA, Swerdlow NR, Radant AD, and Braff DL (2012) Association analysis of 94 candidate genes and schizophrenia-related endophenotypes. PLoS One 7:e29630.
29. Griffin AL (2015) Role of the thalamic nucleus reuniens in mediating interactions between the hippocampus and medial prefrontal cortex during spatial working memory. Front Syst Neurosci 9:29.
30. Hagino Y, Kasai S, Han W, Yamamoto H, Nabeshima T, Mishina M, and Ikeda K (2010) Essential role of NMDA receptor channel 4 subunit (GluN2D) in the effects of phencyclidine, but not methamphetamine. PLoS One 5:e13722.
31. Halene TB, Ehrlichman RS, Liang Y, Christian EP, Jonak GJ, Gur TL, Blendy JA, Dow HC, Brodkin ES, and Schneider F, et al. (2009) Assessment of NMDA receptor NR1 subunit hypofunction in mice as a model for schizophrenia. Genes Brain Behav 8:661-675.
32. Hillman BG, Gupta SC, Stairs DJ, Buonanno A, and Dravid SM (2011) Behavioral analysis of NR2C knockout mouse reveals deficit in acquisition of conditioned fear and working memory. Neurobiol Learn Mem 95:404-414.
33. Hizue M, Pang CH, and Yokoyama M (2005) Involvement of N-methyl-D-aspartatetype glutamate receptor epsilon1 and epsilon4 subunits in tonic inflammatory pain and neuropathic pain. Neuroreport 16:1667-1670.
34. Homayoun H and Moghaddam B (2007) NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons. J Neurosci 27:11496-11500.
35. Hunt MJ and Kasicki S (2013) A systematic review of the effects of NMDA receptor antagonists on oscillatory activity recorded in vivo. J Psychopharmacol 27: 972-986.
36. Hunt MJ, Olszewski M, Piasecka J, Whittington MA, and Kasicki S (2015) Effects of NMDA receptor antagonists and antipsychotics on high frequency oscillations recorded in the nucleus accumbens of freely moving mice. Psychopharmacology (Berl) 232:4525-4535.
37. Ikeda K, Araki K, Takayama C, Inoue Y, Yagi T, Aizawa S, and Mishina M (1995) Reduced spontaneous activity of mice defective in the epsilon 4 subunit of the NMDA receptor channel. Brain Res Mol Brain Res 33:61-71.
38. Ikeda K, Nagasawa M, Mori H, Araki K, Sakimura K, Watanabe M, Inoue Y, and Mishina M (1992) Cloning and expression of the epsilon 4 subunit of the NMDA receptor channel. FEBS Lett 313:34-38.
39. Ishii T, Moriyoshi K, Sugihara H, Sakurada K, Kadotani H, Yokoi M, Akazawa C, Shigemoto R, Mizuno N, and Masu M, et al. (1993) Molecular characterization of the family of the N-methyl-D-aspartate receptor subunits. J Biol Chem 268: 2836-2843.
40. Ito HT, Zhang SJ, Witter MP, Moser EI, and Moser MB (2015) A prefrontal-thalamohippocampal circuit for goal-directed spatial navigation. Nature 522:50-55.
41. Javitt DC (2007) Glutamate and schizophrenia: phencyclidine, N-methyl-D-aspartate receptors, and dopamine-glutamate interactions. Int Rev Neurobiol 78:69-108.
42. Jeffrey M, Lang M, Gane J, Wu C, Burnham WM, and Zhang L (2013) A reliable method for intracranial electrode implantation and chronic electrical stimulation in the mouse brain. BMC Neurosci 14:82.
43. Kantrowitz JT and Javitt DC (2010) N-methyl-D-aspartate (NMDA) receptor dysfunction or dysregulation: the final common pathway on the road to schizophrenia? Brain Res Bull 83:108-121.
44. Kennedy C, Des Rosiers MH, Jehle JW, Reivich M, Sharpe F, and Sokoloff L (1975) Mapping of functional neural pathways by autoradiographic survey of local metabolic rate with (14C)deoxyglucose. Science 187:850-853.
45. Kinney JW, Davis CN, Tabarean I, Conti B, Bartfai T, and Behrens MM (2006) A specific role for NR2A-containing NMDA receptors in the maintenance of parvalbumin and GAD67 immunoreactivity in cultured interneurons. J Neurosci 26:1604-1615.
46. Kocsis B (2012) Differential role of NR2A and NR2B subunits in N-methyl-D-aspartate receptor antagonist-induced aberrant cortical gamma oscillations. Biol Psychiatry 71: 987-995.
47. Kocsis B, Brown RE, McCarley RW, and Hajos M (2013) Impact of ketamine on neuronal network dynamics: translational modeling of schizophrenia-relevant deficits. CNS Neurosci Ther 19:437-447.
48. Korotkova T, Fuchs EC, Ponomarenko A, von Engelhardt J, and Monyer H (2010) NMDA receptor ablation on parvalbumin-positive interneurons impairs hippocampal synchrony, spatial representations, and working memory. Neuron 68: 557-569.
49. Kotermanski SE and Johnson JW (2009) Mg21 imparts NMDA receptor subtype selectivity to the Alzheimer's drug memantine. J Neurosci 29:2774-2779.
50. Lahti AC, Koffel B, LaPorte D, and Tamminga CA (1995) Subanesthetic doses of ketamine stimulate psychosis in schizophrenia. Neuropsychopharmacology 13:9-19.
51. Li Q, Clark S, Lewis DV, and Wilson WA (2002) NMDA receptor antagonists disinhibit rat posterior cingulate and retrosplenial cortices: a potential mechanism of neurotoxicity. J Neurosci 22:3070-3080.
52. Lisman JE, Coyle JT, Green RW, Javitt DC, Benes FM, Heckers S, and Grace AA (2008) Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends Neurosci 31:234-242.
53. Lisman JE, Pi HJ, Zhang Y, and Otmakhova NA (2010) A thalamo-hippocampalventral tegmental area loop may produce the positive feedback that underlies the psychotic break in schizophrenia. Biol Psychiatry 68:17-24.
54. Llinás R, Urbano FJ, Leznik E, Ramírez RR, and van Marle HJ (2005) Rhythmic and dysrhythmic thalamocortical dynamics: GABA systems and the edge effect. Trends Neurosci 28:325-333.
55. Lodge D and Mercier MS (2015) Ketamine and phencyclidine: the good, the bad and the unexpected. Br J Pharmacol 172:4254-4276.
56. Makino C, Shibata H, Ninomiya H, Tashiro N, and Fukumaki Y (2005) Identification of single-nucleotide polymorphisms in the human N-methyl-D-aspartate receptor subunit NR2D gene, GRIN2D, and association study with schizophrenia. Psychiatr Genet 15:215-221.
57. McNally JM, McCarley RW, McKenna JT, Yanagawa Y, and Brown RE (2011) Complex receptor mediation of acute ketamine application on in vitro gamma oscillations in mouse prefrontal cortex: modeling gamma band oscillation abnormalities in schizophrenia. Neuroscience 199:51-63.
58. Micu I, Plemel JR, Lachance C, Proft J, Jansen AJ, Cummins K, van Minnen J, and Stys PK (2015) The molecular physiology of the axo-myelinic synapse. Exp Neurol DOI: [published ahead of print].
59. Mishina M, Mori H, Araki K, Kushiya E, Meguro H, Kutsuwada T, Kashiwabuchi N, Ikeda K, Nagasawa M, and Yamazaki M, et al. (1993) Molecular and functional diversity of the NMDA receptor channel. Ann N Y Acad Sci 707:136-152.
60. Miyamoto S, Leipzig JN, Lieberman JA, and Duncan GE (2000) Effects of ketamine, MK-801, and amphetamine on regional brain 2-deoxyglucose uptake in freely moving mice. Neuropsychopharmacology 22:400-412.
61. Mohn AR, Gainetdinov RR, Caron MG, and Koller BH (1999) Mice with reduced NMDA receptor expression display behaviors related to schizophrenia. Cell 98:427-436.
62. Monyer H, Burnashev N, Laurie DJ, Sakmann B, and Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529-540.
63. Nakazawa K, Zsiros V, Jiang Z, Nakao K, Kolata S, Zhang S, and Belforte JE (2012) GABAergic interneuron origin of schizophrenia pathophysiology. Neuropharmacology 62:1574-1583.
64. Olszewski M, Piasecka J, Goda SA, Kasicki S, and Hunt MJ (2013) Antipsychotic compounds differentially modulate high-frequency oscillations in the rat nucleus accumbens: a comparison of first-and second-generation drugs. Int J Neuropsychopharmacol 16:1009-1020.
65. Phillips KG, Cotel MC, McCarthy AP, Edgar DM, Tricklebank M, O'Neill MJ, Jones MW, and Wafford KA (2012) Differential effects of NMDA antagonists on high frequency and gamma EEG oscillations in a neurodevelopmental model of schizophrenia. Neuropharmacology 62:1359-1370.
66. Sodhi MS, Simmons M, McCullumsmith R, Haroutunian V, and Meador-Woodruff JH (2011) Glutamatergic gene expression is specifically reduced in thalamocortical projecting relay neurons in schizophrenia. Biol Psychiatry 70:646-654.
67. Sohal VS, Zhang F, Yizhar O, and Deisseroth K (2009) Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459:698-702.
68. Spooren W, Mombereau C, Maco M, Gill R, Kemp JA, Ozmen L, Nakanishi S, and Higgins GA (2004) Pharmacological and genetic evidence indicates that combined inhibition of NR2A and NR2B subunit containing NMDA receptors is required to disrupt prepulse inhibition. Psychopharmacology (Berl) 175:99-105.
69. Standaert DG, Landwehrmeyer GB, Kerner JA, Penney JB, Jr, and Young AB (1996) Expression of NMDAR2D glutamate receptor subunit mRNA in neurochemically identified interneurons in the rat neostriatum, neocortex and hippocampus. Brain Res Mol Brain Res 42:89-102.
70. Sun J, Jia P, Fanous AH, van den Oord E, Chen X, Riley BP, Amdur RL, Kendler KS, and Zhao Z (2010) Schizophrenia gene networks and pathways and their applications for novel candidate gene selection. PLoS One 5:e11351.
71. Suryavanshi PS, Ugale RR, Yilmazer-Hanke D, Stairs DJ, and Dravid SM (2014) GluN2C/GluN2D subunit-selective NMDA receptor potentiator CIQ reverses MK-801-induced impairment in prepulse inhibition and working memory in Y-maze test in mice. Br J Pharmacol 171:799-809.
72. Takeuchi T, Kiyama Y, Nakamura K, Tsujita M, Matsuda I, Mori H, Munemoto Y, Kuriyama H, Natsume R, and Sakimura K, et al. (2001) Roles of the glutamate receptor epsilon2 and delta2 subunits in the potentiation and prepulse inhibition of the acoustic startle reflex. Eur J Neurosci 14:153-160.
73. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H, Myers SJ, and Dingledine R (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62:405-496.
74. Uhlhaas PJ and Singer W (2013) High-frequency oscillations and the neurobiology of schizophrenia. Dialogues Clin Neurosci 15:301-313.
75. Vollenweider FX, Leenders KL, Scharfetter C, Antonini A, Maguire P, Missimer J, and Angst J (1997) Metabolic hyperfrontality and psychopathology in the ketamine model of psychosis using positron emission tomography (PET) and [18F]fluorodeoxyglucose (FDG). Eur Neuropsychopharmacol 7:9-24.
76. von Engelhardt J, Bocklisch C, Tönges L, Herb A, Mishina M, and Monyer H (2015) GluN2D-containing NMDA receptors-mediate synaptic currents in hippocampal interneurons and pyramidal cells in juvenile mice. Front Cell Neurosci 9:95.
77. Vreugdenhil M, Jefferys JG, Celio MR, and Schwaller B (2003) Parvalbumindeficiency facilitates repetitive IPSCs and gamma oscillations in the hippocampus. J Neurophysiol 89:1414-1422.
78. Wang C, McInnis J, Ross-Sanchez M, Shinnick-Gallagher P, Wiley JL, and Johnson KM (2001) Long-term behavioral and neurodegenerative effects of perinatal phencyclidine administration: implications for schizophrenia. Neuroscience 107: 535-550.
79. Watanabe M, Inoue Y, Sakimura K, and Mishina M (1992) Developmental changes in distribution of NMDA receptor channel subunit mRNAs. Neuroreport 3:1138-1140.
80. Watanabe M, Inoue Y, Sakimura K, and Mishina M (1993a) Distinct distributions of five N-methyl-D-aspartate receptor channel subunit mRNAs in the forebrain. J Comp Neurol 338:377-390.
81. Watanabe M, Inoue Y, Sakimura K, and Mishina M (1993b) Distinct spatio-temporal distributions of the NMDA receptor channel subunit mRNAs in the brain. Ann N Y Acad Sci 707:463-466.
82. Weickert CS, Fung SJ, Catts VS, Schofield PR, Allen KM, Moore LT, Newell KA, Pellen D, Huang XF, and Catts SV, et al. (2013) Molecular evidence of N-methyl-Daspartate receptor hypofunction in schizophrenia. Mol Psychiatry 18:1185-1192.
83. Wöhr M, Orduz D, Gregory P, Moreno H, Khan U, Vörckel KJ, Wolfer DP, Welzl H, Gall D, and Schiffmann SN, et al. (2015) Lack of parvalbumin in mice leads to behavioral deficits relevant to all human autism core symptoms and related neural morphofunctional abnormalities. Transl Psychiatry 5:e525.
84. Yamamoto T, Nakayama T, Yamaguchi J, Matsuzawa M, Mishina M, Ikeda K, and Yamamoto H (2015) Role of the NMDA receptor GluN2D subunit in the expression of ketamine-induced behavioral sensitization and region-specific activation of neuronal nitric oxide synthase. Neurosci Lett 610:48-53.
85. Yamasaki M, Okada R, Takasaki C, Toki S, Fukaya M, Natsume R, Sakimura K, Mishina M, Shirakawa T, and WatanabeM (2014) Opposing role of NMDA receptor GluN2B and GluN2D in somatosensory development and maturation. J Neurosci 34:11534-11548.
86. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, O'Shea DJ, Sohal VS, Goshen I, Finkelstein J, and Paz JT, et al. (2011) Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477:171-178.
87. Zhang Y, Buonanno A, Vertes RP, Hoover WB, and Lisman JE (2012) NR2C in the thalamic reticular nucleus; effects of the NR2C knockout. PLoS One 7:e41908.
88. Zhang Y, Llinas RR, and Lisman JE (2009) Inhibition of NMDARs in the nucleus reticularis of the thalamus produces delta frequency bursting. Front Neural Circuits 3:20.