NAAG, NMDA receptor and psychosis

Current Medicinal Chemistry

Volumn 19, Issue 9, 2012, Pages 1360-1364

  Bergeron, Richard ^a   Coyle, Joseph T ^b  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b MCLEAN HOSPITAL   (United States)

Author keywords

GCP II; Glutamate; hippocampus; mGluR; NMDAR hypofunction; schizophrenia

Indexed keywords

G PROTEIN COUPLED RECEPTOR; GLUTAMATE CARBOXYPEPTIDASE II; GLUTAMIC ACID; N ACETYLASPARTIC ACID; N ACETYLASPARTYLGLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PHENCYCLIDINE;

ASTROCYTE; DEPOLARIZATION; GABAERGIC SYSTEM; HUMAN; NEUROTRANSMISSION; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PSYCHOSIS; REVIEW; SCHIZOPHRENIA; SYNAPTIC TRANSMISSION;

ANIMALS; DIPEPTIDES; GLUTAMATE CARBOXYPEPTIDASE II; HIPPOCAMPUS; HUMANS; PSYCHOTIC DISORDERS; RECEPTORS, N-METHYL-D-ASPARTATE; SCHIZOPHRENIA;

EID: 84858146355     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/092986712799462685     Document Type: Review

References (96)

1. Schoepp DD, Jane DE, Monn JA. Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology 1999 October; 38(10): 1431-76. (Pubitemid 29457728)
2. Ffrench-Mullen JM, Koller K, Zaczek R, Coyle JT, Hori N, Carpenter DO. N-Acetylaspartylglutamate: possible role as the neurotransmitter of the lateral olfactory tract. Proc Natl Acad Sci U S A 1985 June; 82(11): 3897-900. (Pubitemid 15246460)
3. Bernstein J, Fisher RS, Zaczek R, Coyle J. Dipeptides of glutamate and aspartate may be endogenous neuroexcitants in the rat hippocampal slice. J Neurosci 1985 June; 5(6): 1429-33.
4. Henderson Z, Salt TE. The effects of N-acetylaspartylglutamate and distribution of N-acetylaspartylglutamate-like immunoreactivity in the rat somatosensory thalamus. Neuroscience 1988 June; 25(3): 899-906.
5. Forloni G, Grzanna R, Blakely RD, Coyle JT. Co-localization of N-acetyl-aspartyl-glutamate in central cholinergic, noradrenergic, and serotonergic neurons. Synapse 1987; 1(5): 455-60.
6. Valivullah HM, Lancaster J, Sweetnam PM, Neale JH. Interactions between N-acetylaspartylglutamate and AMPA, kainate, and NMDA binding sites. J Neurochem 1994 November; 63(5): 1714-9.
7. Westbrook GL, Mayer ML, Namboodiri MA, Neale JH. High concentrations of N-acetylaspartylglutamate (NAAG) selectively activate NMDA receptors on mouse spinal cord neurons in cell culture. J Neurosci 1986 November; 6(11): 3385-92. (Pubitemid 17186063)
8. Sekiguchi M, Okamoto K, Sakai Y. Low-concentration N- acetylaspartylglutamate suppresses the climbing fiber response of Purkinje cells in guinea pig cerebellar slices and the responses to excitatory amino acids of Xenopus laevis oocytes injected with cerebellar mRNA. Brain Res 1989 March 13; 482(1): 87-96. (Pubitemid 19063153)
9. Puttfarcken PS, Handen JS, Montgomery DT, Coyle JT, Werling LL. N-acetyl-aspartylglutamate modulation of N-methyl-D-aspartate-stimulated [3H]norepinephrine release from rat hippocampal slices. J Pharmacol Exp Ther 1993 August; 266(2): 796-803. (Pubitemid 23318693)
10. Clark BA, Cull-Candy SG. Activity-dependent recruitment of extrasynaptic NMDA receptor activation at an AMPA receptor-only synapse. J Neurosci 2002 June 1; 22(11): 4428-36. (Pubitemid 37465659)
11. van Zundert B, Yoshii A, Constantine-Paton M. Receptor compartmentalization and trafficking at glutamate synapses: a developmental proposal. Trends Neurosci 2004 July; 27(7): 428-37.
12. Townsend M, Yoshii A, Mishina M, Constantine-Paton M. Developmental loss of miniature N-methyl-D-aspartate receptor currents in NR2A knockout mice. Proc Natl Acad Sci U S A 2003 February 4; 100(3): 1340-5. (Pubitemid 36184003)
13. Erreger K, Dravid SM, Banke TG, Wyllie DJ, Traynelis SF. Subunit-specific gating controls rat NR1/NR2A and NR1/NR2B NMDA channel kinetics and synaptic signalling profiles. J Physiol 2005 March 1; 563(Pt 2): 345-58. (Pubitemid 40360896)
14. Rosenmund C, Feltz A, Westbrook GL. Synaptic NMDA receptor channels have a low open probability. J Neurosci 1995 April; 15(4): 2788-95.
15. Chen N, Luo T, Raymond LA. Subtype-dependence of NMDA receptor channel open probability. J Neurosci 1999 August 15; 19(16): 6844-54. (Pubitemid 29380113)
16. Popescu G, Auerbach A. Modal gating of NMDA receptors and the shape of their synaptic response. Nat Neurosci 2003 May; 6(5): 476-83. (Pubitemid 36514695)
17. Carmignoto G, Vicini S. Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science 1992 November 6; 258(5084): 1007-11.
18. Hestrin S. Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse. Nature 1992 June 25; 357(6380): 686-9.
19. Crair MC, Malenka RC. A critical period for long-term potentiation at thalamocortical synapses. Nature 1995 May 25; 375(6529): 325-8.
20. Legendre P, Westbrook GL. Ifenprodil blocks N-methyl-D-aspartate receptors by a two-component mechanism. Mol Pharmacol 1991 August; 40(2): 289-98.
21. Williams K. Ifenprodil discriminates subtypes of the N-methyl-D-aspartate receptor: selectivity and mechanisms at recombinant heteromeric receptors. Mol Pharmacol 1993 October; 44(4): 851-9. (Pubitemid 23317299)
22. Sheng M, Cummings J, Roldan LA, Jan YN, Jan LY. Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 1994 March 10; 368(6467): 144-7. (Pubitemid 24101524)
23. Rumbaugh G, Vicini S. Distinct synaptic and extrasynaptic NMDA receptors in developing cerebellar granule neurons. J Neurosci 1999 December 15; 19(24): 10603-10. (Pubitemid 30235707)
24. Stocca G, Vicini S. Increased contribution of NR2A subunit to synaptic NMDA receptors in developing rat cortical neurons. J Physiol 1998 February 15; 507 (Pt 1): 13-24. (Pubitemid 28102672)
25. Tovar KR, Westbrook GL. The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J Neurosci 1999 May 15; 19(10): 4180-8. (Pubitemid 29222289)
26. Li B, Otsu Y, Murphy TH, Raymond LA. Developmental decrease in NMDA receptor desensitization associated with shift to synapse and interaction with postsynaptic density-95. J Neurosci 2003 December 3; 23(35): 11244-54. (Pubitemid 37548961)
27. Li B, Chen N, Luo T, Otsu Y, Murphy TH, Raymond LA. Differential regulation of synaptic and extra-synaptic NMDA receptors. Nat Neurosci 2002 September; 5(9): 833-4. (Pubitemid 34976643)
28. Beique JC, Andrade R. PSD-95 regulates synaptic transmission and plasticity in rat cerebral cortex. J Physiol 2003 February 1; 546(Pt 3): 859-67. (Pubitemid 36204519)
29. Sattler R, Xiong Z, Lu WY, MacDonald JF, Tymianski M. Distinct roles of synaptic and extrasynaptic NMDA receptors in excitotoxicity. J Neurosci 2000 January 1; 20(1): 22-33. (Pubitemid 30220487)
30. Hardingham GE, Fukunaga Y, Bading H. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 2002 May; 5(5): 405-14. (Pubitemid 34454245)
31. Scimemi A, Fine A, Kullmann DM, Rusakov DA. NR2B-containing receptors mediate cross talk among hippocampal synapses. J Neurosci 2004 May 19; 24(20): 4767-77. (Pubitemid 38668201)
32. Vanhoutte P, Bading H. Opposing roles of synaptic and extrasynaptic NMDA receptors in neuronal calcium signalling and BDNF gene regulation. Curr Opin Neurobiol 2003 June; 13(3): 366-71. (Pubitemid 36792249)
33. Arundine M, Tymianski M. Molecular mechanisms of glutamate-dependent neurodegeneration in ischemia and traumatic brain injury. Cell Mol Life Sci 2004 March; 61(6): 657-68. (Pubitemid 38446410)
34. Fellin T, Pascual O, Gobbo S, Pozzan T, Haydon PG, Carmignoto G. Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 2004 September 2; 43(5): 729-43. (Pubitemid 39179731)
35. Hardingham GE, Bading H. Coupling of extrasynaptic NMDA receptors to a CREB shut-off pathway is developmentally regulated. Biochim Biophys Acta 2002 November 4; 1600(1-2): 148-53. (Pubitemid 38224409)
36. Prybylowski K, Wenthold RJ. N-Methyl-D-aspartate receptors: subunit assembly and trafficking to the synapse. J Biol Chem 2004 March 12; 279(11): 9673-6. (Pubitemid 38372561)
37. Sattler R, Tymianski M. Molecular mechanisms of glutamate receptor-mediated excitotoxic neuronal cell death. Mol Neurobiol 2001 August; 24(1-3): 107-29. (Pubitemid 34066681)
38. Ziff EB. Enlightening the postsynaptic density. Neuron 1997 December; 19(6): 1163-74. (Pubitemid 28030537)
39. Wroblewska B, Santi MR, Neale JH. N-acetylaspartylglutamate activates cyclic AMP-coupled metabotropic glutamate receptors in cerebellar astrocytes. Glia 1998 October; 24(2): 172-9. (Pubitemid 28403995)
40. Wroblewska B, Wroblewski JT, Saab OH, Neale JH. N-acetylaspartylglutamate inhibits forskolin-stimulated cyclic AMP levels via a metabotropic glutamate receptor in cultured cerebellar granule cells. J Neurochem 1993 September; 61(3): 943-8. (Pubitemid 23241231)
41. Hayashi Y, Momiyama A, Takahashi T et al. Role of a metabotropic glutamate receptor in synaptic modulation in the accessory olfactory bulb. Nature 1993 December 16; 366(6456): 687-90. (Pubitemid 24036016)
42. Sanchez-Prieto J, Budd DC, Herrero I, Vazquez E, Nicholls DG. Presynaptic receptors and the control of glutamate exocytosis. Trends Neurosci 1996 June; 19(6): 235-9. (Pubitemid 26167817)
43. Sanabria ER, Wozniak KM, Slusher BS, Keller A. GCP II (NAALADase) inhibition suppresses mossy fiber-CA3 synaptic neurotransmission by a presynaptic mechanism. J Neurophysiol 2004 January; 91(1): 182-93. (Pubitemid 38084363)
44. Wroblewska B, Wegorzewska IN, Bzdega T, Olszewski RT, Neale JH. Differential negative coupling of type 3 metabotropic glutamate receptor to cyclic GMP levels in neurons and astrocytes. J Neurochem 2006 February; 96(4): 1071-7.
45. Cartmell J, Schoepp DD. Regulation of neurotransmitter release by metabotropic glutamate receptors. J Neurochem 2000 September; 75(3): 889-907. (Pubitemid 30660476)
46. Olszewski RT, Wegorzewska MM, Monteiro AC et al. Phencyclidine and dizocilpine induced behaviors reduced by N-acetylaspartylglutamate peptidase inhibition via metabotropic glutamate receptors. Biol Psychiatry 2008 January 1; 63(1): 86-91. (Pubitemid 350234887)
47. Wroblewska B, Wroblewski JT, Pshenichkin S, Surin A, Sullivan SE, Neale JH. N-acetylaspartylglutamate selectively activates mGluR3 receptors in transfected cells. J Neurochem 1997 July; 69(1): 174-81. (Pubitemid 27274170)
48. Bischofberger J, Schild D. Glutamate and N-acetylaspartylglutamate block HVA calcium currents in frog olfactory bulb interneurons via an mGluR2/3-like receptor. J Neurophysiol 1996 September; 76(3): 2089-92. (Pubitemid 26322643)
49. Neale JH, Olszewski RT, Zuo D et al. Advances in understanding the peptide neurotransmitter NAAG and appearance of a new member of the NAAG neuropeptide family. J Neurochem 2011 August; 118(4): 490-8.
50. Slusher BS, Vornov JJ, Thomas AG et al. Selective inhibition of NAALADase, which converts NAAG to glutamate, reduces ischemic brain injury. Nat Med 1999 December; 5(12): 1396-402.
51. Thomas AG, Olkowski JL, Slusher BS. Neuroprotection afforded by NAAG and NAALADase inhibition requires glial cells and metabotropic glutamate receptor activation. Eur J Pharmacol 2001 August 24; 426(1-2): 35-8. (Pubitemid 32781785)
52. Blakely RD, Ory-Lavollee L, Thompson RC, Coyle JT. Synaptosomal transport of radiolabel from N-acetyl-aspartyl-[3H]glutamate suggests a mechanism of inactivation of an excitatory neuropeptide. J Neurochem 1986 October; 47(4): 1013-9. (Pubitemid 16032456)
53. Bzdega T, Turi T, Wroblewska B et al. Molecular cloning of a peptidase against N-acetylaspartylglutamate from a rat hippocampal cDNA library. J Neurochem 1997 December; 69(6): 2270-7. (Pubitemid 27495411)
54. Robinson MB, Blakely RD, Couto R, Coyle JT. Hydrolysis of the brain dipeptide N-acetyl-L-aspartyl-L-glutamate. Identification and characterization of a novel N-acetylated alpha-linked acidic dipeptidase activity from rat brain. J Biol Chem 1987 October 25; 262(30): 14498-506. (Pubitemid 17157357)
55. Luthi-Carter R, Berger UV, Barczak AK, Enna M, Coyle JT. Isolation and expression of a rat brain cDNA encoding glutamate carboxypeptidase II. Proc Natl Acad Sci U S A 1998 March 17; 95(6): 3215-20. (Pubitemid 28135882)
56. Mahadevan D, Saldanha JW. The extracellular regions of PSMA and the transferrin receptor contain an aminopeptidase domain: implications for drug design. Protein Sci 1999 November; 8(11): 2546-9. (Pubitemid 29536427)
57. Davis MI, Bennett MJ, Thomas LM, Bjorkman PJ. Crystal structure of prostate-specific membrane antigen, a tumor marker and peptidase. Proc Natl Acad Sci U S A 2005 April 26; 102(17): 5981-6. (Pubitemid 40594241)
58. Halsted CH, Ling EH, Luthi-Carter R, Villanueva JA, Gardner JM, Coyle JT. Folylpoly-gamma-glutamate carboxypeptidase from pig jejunum. Molecular characterization and relation to glutamate carboxypeptidase II. J Biol Chem 1998 August 7; 273(32): 20417-24. (Pubitemid 28377608)
59. Speno HS, Luthi-Carter R, Macias WL, Valentine SL, Joshi AR, Coyle JT. Site-directed mutagenesis of predicted active site residues in glutamate carboxypeptidase II. Mol Pharmacol 1999 January; 55(1): 179-85. (Pubitemid 29042536)
60. Blakely RD, Robinson MB, Thompson RC, Coyle JT. Hydrolysis of the brain dipeptide N-acetyl-L-aspartyl-L-glutamate: subcellular and regional distribution, ontogeny, and the effect of lesions on N-acetylated-alpha-linked acidic dipeptidase activity. J Neurochem 1988 April; 50(4): 1200-9.
61. Berger UV, Luthi-Carter R, Passani LA et al. Glutamate carboxypeptidase II is expressed by astrocytes in the adult rat nervous system. J Comp Neurol 1999 December 6; 415(1): 52-64. (Pubitemid 29519885)
62. Sacha P, Zamecnik J, Barinka C et al. Expression of glutamate carboxypeptidase II in human brain. Neuroscience 2007 February 23; 144(4): 1361-72. (Pubitemid 46123795)
63. Tiffany CW, Cai NS, Rojas C, Slusher BS. Binding of the glutamate carboxypeptidase II (NAALADase) inhibitor 2-PMPA to rat brain membranes. Eur J Pharmacol 2001 September 14; 427(2): 91-6. (Pubitemid 32835289)
64. Jackson PF, Slusher BS. Design of NAALADase inhibitors: a novel neuroprotective strategy. Curr Med Chem 2001 July; 8(8): 949-57. (Pubitemid 32633553)
65. Rojas C, Frazier ST, Flanary J, Slusher BS. Kinetics and inhibition of glutamate carboxypeptidase II using a microplate assay. Anal Biochem 2002 November 1; 310(1): 50-4. (Pubitemid 35387330)
66. Lukawski K, Kaminski RM, Czuczwar SJ. Effects of selective inhibition of N-acetylated-alpha-linked-acidic dipeptidase (NAALADase) on mice in learning and memory tasks. Eur J Pharmacol 2008 January 28; 579(1-3): 202-7.
67. Yamamoto T, Saito O, Aoe T et al. Local administration of N-acetylaspartylglutamate (NAAG) peptidase inhibitors is analgesic in peripheral pain in rats. Eur J Neurosci 2007 January; 25(1): 147-58. (Pubitemid 46098894)
68. Mateo Z, Porter JT. Group II metabotropic glutamate receptors inhibit glutamate release at thalamocortical synapses in the developing somatosensory cortex. Neuroscience 2007 May 25; 146(3): 1062-72. (Pubitemid 46694151)
69. Baslow MH. The astrocyte surface NAAG receptor and NAAG peptidase signaling complex as a therapeutic target. Drug News Perspect 2008 June; 21(5): 251-7.
70. Bergeron R, Imamura Y, Frangioni JV, Greene RW, Coyle JT. Endogenous N-acetylaspartylglutamate reduced NMDA receptor-dependent current neurotransmission in the CA1 area of the hippocampus. J Neurochem 2007 January; 100(2): 346-57. (Pubitemid 46010996)
71. Jentsch JD, Roth RH. The neuropsychopharmacology of phencyclidine: from NMDA receptor hypofunction to the dopamine hypothesis of schizophrenia. Neuropsychopharmacology 1999 April; 20(3): 201-25. (Pubitemid 29067401)
72. Bonta IL. Schizophrenia, dissociative anaesthesia and near-death experience; three events meeting at the NMDA receptor. Med Hypotheses 2004; 62(1): 23-8. (Pubitemid 38200001)
73. Javitt DC, Zukin SR. Recent advances in the phencyclidine model of schizophrenia. Am J Psychiatry 1991 October; 148(10): 1301-8.
74. Kristiansen LV, Huerta I, Beneyto M, Meador-Woodruff JH. NMDA receptors and schizophrenia. Curr Opin Pharmacol 2007 February; 7(1): 48-55.
75. Javitt DC, Coyle JT. Decoding schizophrenia. Sci Am 2004 January; 290(1): 48-55.
76. Javitt DC. Glutamate as a therapeutic target in psychiatric disorders. Mol Psychiatry 2004 July 27.
77. Javitt DC. Glutamate and schizophrenia: Phencyclidine, N-methyl-Daspartate receptors, and dopamine-glutamate interactions. Int Rev Neurobiol 2007; 78: 69-108.
78. Martin D, Lodge D. Phencyclidine receptors and N-methyl-D-aspartate antagonism: electrophysiologic data correlates with known behaviours. Pharmacol Biochem Behav 1988 October; 31(2): 279-86. (Pubitemid 19275141)
79. Kegeles LS, bi-Dargham A, Zea-Ponce Y et al. Modulation of amphetamine-induced striatal dopamine release by ketamine in humans: implications for schizophrenia. Biol Psychiatry 2000 October 1; 48(7): 627-40.
80. 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 December; 57(12): 1139-47.
81. Mohn AR, Gainetdinov RR, Caron MG, Koller BH. Mice with reduced NMDA receptor expression display behaviors related to schizophrenia. Cell 1999 August 20; 98(4): 427-36. (Pubitemid 29402481)
82. Kreczmanski P, Heinsen H, Mantua V et al. Volume, neuron density and total neuron number in five subcortical regions in schizophrenia. Brain 2007 March; 130(Pt 3): 678-92. (Pubitemid 46410744)
83. Tsai G, Passani LA, Slusher BS et al. Abnormal excitatory neurotransmitter metabolism in schizophrenic brains. Arch Gen Psychiatry 1995 October; 52(10): 829-36.
84. Tkachev D, Mimmack ML, Huffaker SJ, Ryan M, Bahn S. Further evidence for altered myelin biosynthesis and glutamatergic dysfunction in schizophrenia. Int J Neuropsychopharmacol 2007 August; 10(4): 557-63. (Pubitemid 46985260)
85. Ghose S, Chin R, Gallegos A, Roberts R, Coyle J, Tamminga C. Localization of NAAG-related gene expression deficits to the anterior hippocampus in schizophrenia. Schizophr Res 2009 June; 111(1-3): 131-7.
86. Guilarte TR, Hammoud DA, McGlothan JL et al. Dysregulation of glutamate carboxypeptidase II in psychiatric disease. Schizophr Res 2008 February; 99(1-3): 324-32.
87. Coyle JT. The glutamatergic dysfunction hypothesis for schizophrenia. Harv Rev Psychiatry 1996 January; 3(5): 241-53. (Pubitemid 26058365)
88. Semple CA, Devon RS, Le Hellard S, Porteous DJ. Identification of genes from a schizophrenia-linked translocation breakpoint region. Genomics 2001 April 1; 73(1): 123-6. (Pubitemid 32382395)
89. Bacich DJ, Ramadan E, O'Keefe DS et al. Deletion of the glutamate carboxypeptidase II gene in mice reveals a second enzyme activity that hydrolyzes N-acetylaspartylglutamate. J Neurochem 2002 October; 83(1): 20-9.
90. Bacich DJ, Wozniak KM, Lu XC et al. Mice lacking glutamate carboxypeptidase II are protected from peripheral neuropathy and ischemic brain injury. J Neurochem 2005 October; 95(2): 314-23. (Pubitemid 41457500)
91. Tsai G, Dunham KS, Drager U et al. Early embryonic death of glutamate carboxypeptidase II (NAALADase) homozygous mutants. Synapse 2003 December 15; 50(4): 285-92. (Pubitemid 37420583)
92. Han L, Picker JD, Schaevitz LR et al. Phenotypic characterization of mice heterozygous for a null mutation of glutamate carboxypeptidase II. Synapse 2009 August; 63(8): 625-35.
93. Lisman JE, Coyle JT, Green RW et al. Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends Neurosci 2008 May; 31(5): 234-42.
94. Moghaddam B, Adams BW. Reversal of phencyclidine effects by a group II metabotropic glutamate receptor agonist in rats. Science 1998 August 28; 281(5381): 1349-52. (Pubitemid 28406826)
95. Patil ST, Zhang L, Martenyi F et al. Activation of mGlu2/3 receptors as a new approach to treat schizophrenia: a randomized Phase 2 clinical trial. Nat Med 2007 September; 13(9): 1102-7. (Pubitemid 47517511)
96. Takatsu Y, Fujita Y, Tsukamoto T, Slusher BS, Hashimoto K. Orally active glutamate carboxypeptidase II inhibitor 2-MPPA attenuates dizocilpine-induced prepulse inhibition deficits in mice. Brain Res 2011 January 31; 1371: 82-6.