NAAG peptidase inhibitors and deletion of NAAG peptidase gene enhance memory in novel object recognition test

European Journal of Pharmacology

Volumn 701, Issue 1-3, 2013, Pages 27-32

  Janczura, Karolina J ^a   Olszewski, Rafal T ^a   Bzdega, Tomasz ^a   Bacich, Dean J ^b   Heston, Warren D ^c   Neale, Joseph H ^a  

^a GEORGETOWN UNIVERSITY   (United States)

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

^c LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Glutamate carboxypeptidase II knockout mice; Memory; MGluR3; N acetylaspartylglutamate; NAAG

Indexed keywords

GLUTAMATE CARBOXYPEPTIDASE II; GLUTAMATE CARBOXYPEPTIDASE II INHIBITOR; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ARTICLE; C57BL MOUSE; CONTROLLED STUDY; ENZYME INHIBITION; FEMALE; GENE; GENE DELETION; HETEROZYGOSITY; LATENT PERIOD; LONG TERM MEMORY; MALE; MEMORY CONSOLIDATION; MOUSE; NAAG PEPTIDASE GENE; NONHUMAN; PASSIVE AVOIDANCE; PATTERN RECOGNITION; PRIORITY JOURNAL; RECALL; TASK PERFORMANCE;

ANIMALS; EXPLORATORY BEHAVIOR; GENE DELETION; GENE KNOCKOUT TECHNIQUES; GLUTAMATE CARBOXYPEPTIDASE II; MALE; MEMORY; MICE; MICE, INBRED C57BL; ORGANOPHOSPHORUS COMPOUNDS; PROTEASE INHIBITORS; RECOGNITION (PSYCHOLOGY); UREA;

EID: 84873475193     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2012.11.027     Document Type: Article

References (61)

1. M.O. Adedoyin, S. Vicini, and J.H. Neale Endogenous N- acetylaspartylglutamate (NAAG) inhibits synaptic plasticity/transmission in the amygdala in a mouse inflammatory pain model Mol. Pain 6 2010 60 78
2. S. Akkerman, J. Prickaerts, H.W. Steinbusch, and A. Blokland Object recognition testing: statistical considerations Behav. Brain Res. 232 2012 317 322
3. M. Antunes, and G. Biala The novel object recognition memory: neurobiology, test procedure, and its modifications Cognit. Processes 13 2012 93 110
4. J.M. Aultman, and B. Moghaddam Distinct contributions of glutamate and dopamine receptors to temporal aspects of rodent working memory using a clinically relevant task Psychopharmacology (Berlin) 153 2001 353 364
5. D.J. Bacich, E. Ramadan, D.S. O'Keefe, N. Bukhari, I. Wegorzewska, O. Ojeifo, R.T. Olszewski, C.C. Wrenn, T. Bzdega, B. Wroblewska, W.D. Heston, and J.H. Neale Deletion of the glutamate carboxypeptidase II gene in mice reveals a second enzyme activity that hydrolyzes N-acetylaspartylglutamate J. Neurochem. 83 2002 20 29
6. G.R. Barker, Z.I. Bashir, M.W. Brown, and E.C. Warburton A temporally distinct role for group I and group II metabotropic glutamate receptors in object recognition memory Learn. Mem. 13 2006 178 186
7. J. Boyle, L. Trick, S. Soo-ampon, S. Lilley, L. Levine, and I. Hindmarch Evaluation of cognitive and psychomotor profile of a novel anxiolytic, LY544344, compared to lorazepam in normal volunteers Eur. Neurophychopharmacol. 13 2003 S355 Supplement
8. R.E. Clark, S.M. Zola, and L.R. Squire Impaired recognition memory in rats after damage to the hippocampus J. Neurosci. 20 2000 8853 8860
9. J. Dhawan, H. Benveniste, Z. Luo, M. Nawrocky, SD. Smith, and A. Biegon A new look at glutamate and ischemia: NMDA agonist improves long-term functional outcome in a rat model of stroke Future Neurol. 6 2011 823 834
10. E. Dunayevich, J. Erickson, L. Levine, R. Landbloom, D.D. Schoepp, and G.D. Tollefson Efficacy and tolerability of an mGlu2/3 agonist in the treatment of generalized anxiety disorder Neuropsychopharmacology 33 2008 1603 1610
11. A. Ennaceur, and J. Delacour A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data Behav. Brain Res. 31 1988 47 59
12. M.J. Fell, K.A. Svensson, B.G. Johnson, and D.D. Schoepp Evidence for the role of metabotropic glutamate (mGlu)2 not mGlu3 receptors in the preclinical antipsychotic pharmacology of the mGlu2/3 receptor agonist (-)-(1R,4S,5S,6S)-4- amino-2-sulfonylbicyclo[3.1.0]hexane-4,6-dicarboxylic acid (LY404039) J. Pharmacol. Exp. Ther. 326 2008 209 217
13. S.B. Floresco, and J.D. Jentsch Pharmacological enhancement of memory and executive functioning in laboratory animals Neuropsychopharmacology 36 2011 227 250
14. A. Giralt, A. Saavedra, O. Carretón, X. Xifró, J. Alberch, and E. Pérez-Navarro Increased PKA signaling disrupts recognition memory and spatial memory: role in Huntington's disease Hum. Mol. Genet. 20 2011 4232 4247
15. A. Gravius, M. Pietraszek, A. Dekundy, and W. Danysz Metabotropic glutamate receptors as therapeutic targets for cognitive disorders Curr. Top. Med. Chem. 10 2010 187 206
16. S.J. Greco, K.J. Bryan, S. Sarkar, X. Zhu, M.A. Smith, J.W. Ashford, J.M. Johnston, N. Tezapsidis, and G. Casadesus Leptin reduces pathology and improves memory in a transgenic mouse model of Alzheimer's disease J. Alzheimers Dis. 19 2010 1155 1167
17. K.J. Gregory, E.N. Dong, J. Meiler, and P.J. Conn Allosteric modulation of metabotropic glutamate receptors: structural insights and therapeutic potential Neuropharmacology 60 2011 66 81
18. S. Harich, G. Gross, and A. Bespalov Stimulation of the metabotropic glutamate 2/3 receptor attenuates social novelty discrimination deficits induced by neonatal phencyclidine treatment Psychopharmacology (Berlin) 192 2007 511 519
19. G.A. Higgins, T.M. Ballard, J.N. Kew, J.G. Richards, J.A. Kemp, G. Adam, T. Woltering, S. Nakanishi, and V. Mutel Pharmacological manipulation of mGlu2 receptors influences cognitive performance in the rodent Neuropharmacology 46 2004 907 917
20. P.F. Jackson, and S. Slusher Design of NAALADase inhibitors: a novel neuroprotective strategy Curr. Med. Chem. 8 2001 949 957
21. C.A. Jones, A.M. Brown, D.P. Auer., and K.C. Fone The mGluR2/3 agonist LY379268 reverses post-weaning social isolation-induced recognition memory deficits in the rat Psychopharmacology (Berlin) 214 2010 269 283
22. A.E. Kingston, P.L. Ornstein, R.A. Wright, B.G. Johnson, N.G. Mayne, J.P. Burnett, R. Belagaje, S. Wu, and D.D. Schoepp LY341495 is a nanomolar potent and selective antagonist of group II metabotropic glutamate receptors Neuropharmacology 37 1998 1 12
23. B.J. Kinon, L. Zhang, B.,A. Millen, O.O. Osuntokun, J.E. Williams, S. Kollack-Walker, K. Jackson, L. Kryzhanovskaya, N. Jarkova, and the HBBI Study Group A multicenter, inpatient, phase 2, double-blind, placebo-controlled dose-ranging study of LY2140023 monohydrate in patients with DSM-IV schizophrenia J. Clin. Psychopharmacol. 31 2011 349 355
24. J.H. Krystal, W. Abi-Saab, E. Perry, D.C. D'Souza, N. Liu, R. Gueorguieva, L. McDougall, T. Hunsberger, A. Belger, L. Levine, and A. Breier Preliminary evidence of attenuation of the disruptive effects of the NMDA glutamate receptor antagonist, ketamine, on working memory by pretreatment with the group II metabotropic glutamate receptor agonist, LY354740, in healthy human subjects Psychopharmacology (Berlin) 179 2005 303 309
25. A.C. Lee, S. Rahman, J.R. Hodges, B.J. Sahakian, and K.S. Graham Associative and recognition memory for novel objects in dementia: implications for diagnosis Eur. J. Neurosci. 18 2003 1660 1670
26. E.D. Levin, P.J. Bushnell, and A.H. Rezvani Attention-modulating effects of cognitive enhancers Pharmacol. Biochem. Behav. 99 2011 146 154
27. A.M. Linden, B.G. Johnson, N. Trokovic, E.R. Korpi, and D.D. Schoepp Use of MGLUR2 and MGLUR3 knockout mice to explore in vivo receptor specificity of the MGLUR2/3 selective antagonist LY341495 Neuropharmacology 57 2009 172 182
28. K. Lukawski, R.M. Kamiński, and S.J. Czuczwar Effects of selective inhibition of N-acetylated-alpha-linked-acidic dipeptidase (NAALADase) on mice in learning and memory tasks Eur. J. Pharmacol. 579 2008 202 207
29. O. Lykhmus, L. Koval, M. Skok, M. Zouridakis, P. Zisimopoulou, S. Tzartos, V. Tsetlin, S. Granon, J.P. Changeux, S. Komisarenko, and I. Cloëz-Tayaranie Antibodies against extracellular domains of α4 and α7 subunits alter the levels of nicotinic receptors in the mouse brain and affect memory: possible relevance to Alzheimer's pathology J. Alzheimers. Dis. 24 2011 693 704
30. L. Lyon, L.M. Saksida, and T.J. Bussey Spontaneous object recognition and its relevance to schizophrenia: a review of findings from pharmacological, genetic, lesion and developmental rodent models Psychopharmacology (Berlin) 220 2012 647 672
31. J.R. Manns, C.E. Stark, and L.R. Squire The visual paired-comparison task as a measure of declarative memory Proc. Natl. Acad. Sci. U.S.A 97 2000 12375 12379
32. G.J. Marek Metabotropic glutamate2/3 (mGlu2/3) receptors, schizophrenia and cognition Eur. J. Pharmacol. 639 2010 81 90
33. B. Moghaddam, and B.W. Adams Reversal of phencyclidine effects by a group II metabotropic glutamate receptor agonist in rats Science 281 1998 1349 1352
34. J.A. Monn, M.J. Valli, S.M. Massey, E.R. Korpi, and D.D. Schoepp Synthesis, pharmacological characterization, and molecular modeling of heterobicyclic amino acids related to (+)-2-aminobicyclo[3.1.0] hexane-2,6-dicarboxylic acid (LY354740): identification of two new potent, selective, and systemically active agonists for group II metabotropic glutamate receptors J. Med. Chem. 42 1999 1027 1040
35. J.H. Neale N-acetylaspartylglutamate (NAAG) IS an agonist at mGluR3 in vivo and in vitro J. Neurochem. 119 2011 891 895
36. J.H. Neale, R.T. Olszewski, L.M. Gehl, B. Wroblewska, and T. Bzdega The neurotransmitter N-acetylaspartylglutamate in models of pain, ALS, diabetic neuropathy, CNS injury and schizophrenia Trends Pharmacol. Sci. 26 2005 477 484
37. J.H. Neale, R.T. Olszewski, D. Zuo, K.J. Janczura, C.P. Profaci, K.M. Lavin, J.C. Madore, and T. Bzdega Advances in understanding the peptide neurotransmitter NAAG and appearance of a new member of the NAAG neuropeptide family J. Neurochem. 118 2011 490 498
38. A. Nikiforuk, P. Popik, K.U. Drescher, M. van Gaalen, A.L. Relo, M. Mezler, G. Marek, H. Schoemaker, G. Gross, and A. Bespalov Effects of a positive allosteric modulator of group II metabotropic glutamate receptors, LY487379, on cognitive flexibility and impulsive-like responding in rats J. Pharmacol. Exp. Ther. 335 2010 665 673
39. R.T. Olszewski, N. Bukhari, J. Zhou, A.P. Kozikowski, J.T. Wroblewski, S. Shamimi-Noori, B. Wroblewska, T. Bzdega, S. Vicini, F.B. Barton, and J.H. Neale NAAG peptidase inhibition reduces locomotor activity and some stereotypes in the PCP model of schizophrenia via group II mGluR J. Neurochem. 89 2004 876 885
40. R.T. Olszewski, T. Bzdega, and J.H. Neale mGluR3 and not mGluR2 receptors mediate the efficacy of NAAG peptidase inhibitor in PCP model of schizophrenia Schizophrenia Res. 136 2012 160 161
41. R.T. Olszewski, K.J. Janczura, S.R. Ball, J.C. Madore, K.M. Lavin, J.C-M. Lee, M.J. Lee, E.K. Der, T. Bzdega, and J.H. Neale NAAG peptidase inhibitors block cognitive deficit induced by MK-801 and motor activation induced by d-amphetamine and PCP in animal models of schizophrenia Transl. Psychiatry 31 2 2012 e145 (e-pub)
42. M.R. Pazos, V. Cinquina, A. Gómez, R. Layunta, M. Santos, J. Fernández-Ruiz, and J. Martínez-Orgado Cannabidiol administration after hypoxia-ischemia to newborn rats reduces long-term brain injury and restores neurobehavioral function Neuropharmacology 63 2012 776 783
43. N. Pitsikas, E. Kaffe, and A. Markou The metabotropic glutamate 2/3 receptor antagonist LY341495 differentially affects recognition memory in rats Behav. Brain. Res. 230 2012 374 379
44. N. Plath, L. Lerdrup, P.H. Larsen, and J.P. Redrobe Can small molecules provide truly effective enhancement of cognition? Current achievements and future directions Expert Opin. Investig. Drugs 20 2011 795 811
45. L.M. Rorick-Kehn, B.G. Johnson, J.L. Burkey, R.A. Wright, D.O. Calligaro, G.J. Marek, E.S. Nisenbaum, J.T. Catlow, A.E. Kingston, D.D. Giera, M.F. Herin, J.A. Monn, D.L. McKinzie, and D.D. Schoepp Pharmacological and pharmacokinetic properties of a structurally novel, potent, and selective metabotropic glutamate 2/3 receptor agonist: in vitro characterization of agonist (-)-(1R,4S,5S,6S)-4- amino-2-sulfonylbicyclo[3.1.0]-hexane-4,6-dicarboxylic acid (LY404039) J. Pharmacol Exp. Ther. 321 2007 308 317
46. T. Sato, K. Tanaka, Y. Ohnishi, T. Teramoto, M. Irifune, and T. Nishikawa Inhibitory effects of group II mGluR-related drugs on memory performance in mice Physiol. Behav. 80 2004 747 758
47. C. Schlumberger, D. Schäfer, C. Barberi, L. Morè, J. Nagel, M. Pietraszek, W.J. Schmidt, and W. Danysz Effects of a metabotropic glutamate receptor group II agonist LY354740 in animal models of positive schizophrenia symptoms and cognition Behav. Pharmacol. 20 2009 56 66
48. T. Shimazaki, A. Kaku, and S. Chaki Blockade of the metabotropic glutamate 2/3 receptors enhances social memory via the AMPA receptor in rats Eur. J. Pharmacol. 575 2007 94 97
49. B.S. Slusher, J.J. Vornov, A.G. Thomas, P.D. Hurn, I. Harukuni, A. Bhardwaj, R.J. Traystman, M.B. Robinson, P. Britton, X.C. Lu, F.C. Tortella, K.M. Wozniak, M. Yudkoff, B.M. Potter, and P.F. Jackson Selective inhibition of NAALADase, which converts NAAG to glutamate, reduces ischemic brain injury Nat. Med. 5 1999 1396 1402
50. S. Spinelli, T. Ballard, S. Gatti-McArthur, G.J. Richards, M. Kapps, T. Woltering, J. Wichmann, H. Stadler, J. Feldon, and C.R. Pryce Effects of the mGluR2/3 agonist LY354740 on computerized tasks of attention and working memory in marmoset monkeys Psychopharmacology (Berlin) 179 2005 292 302
51. G. Taglialatela, D. Hogan, W.R. Zhang, and K.T. Dineley Intermediate- and long-term recognition memory deficits in Tg2576 mice are reversed with acute calcineurin inhibition Behav. Brain Res. 200 2009 95 99
52. A.G. Thomas, K.M. Wozniak, T. Tsukamoto, D. Calvin, Y. Wu, C. Rojas, J. Vornov, and B.S. Slusher Glutamate carboxypeptidase II (NAALADase) inhibition as a novel therapeutic strategy Adv. Exp. Med. Biol. 576 327-337 2006 361 363 discussion
53. T. Tsukamoto, K.M. Wozniak, and B.S. Slusher Progress in the discovery and development of glutamate carboxypeptidase II inhibitors Drug Discov. Today 12 2007 767 776
54. M.L. Woolley, D.J. Pemberton, S. Bate, C. Corti, and D.N. Jones The mGlu2 but not the mGlu3 receptor mediates the actions of the mGluR2/3 agonist, LY379268, in mouse models predictive of antipsychotic activity Psychopharmacology (Berlin) 196 2008 431 440
55. T. Yamamoto, S. Hirasawa, B. Wroblewska, E. Grajkowska, J. Zhou, A. Kozikowski, J. Wroblewski, and J.H. Neale Antinociceptive effects of N-acetylaspartylglutamate (NAAG) peptidase inhibitors ZJ-11, ZJ-17 and ZJ-43 in the rat formalin test and in the rat neuropathic pain model Eur. J. Neurosci. 20 2004 483 494
56. T. Yamamoto, O. Saito, T. Aoe, A. Bartolozzi, J. Sarva, J. Zhou, A. Kozikowski, B. Wroblewska, T. Bzdega, and J.H. Neale Local administration of N-acetylaspartylglutamate (NAAG) peptidase inhibitors is analgesic in peripheral pain in rats Eur. J. Neurosci. 25 2007 147 158
57. J.W. Young, S.B. Powell, V. Risbrough, H.M. Marston, and M.A. Geyer Using the MATRICS to guide development of a preclinical cognitive test battery for research in schizophrenia Pharmacol. Ther. 122 2009 150 202
58. R. Zhang, G. Xue, S. Wang, L. Zhang, C. Shi, and X. Xie Novel object recognition as a facile behavior test for evaluating drug effects in AβPP/PS1 Alzheimer's disease mouse model J. Alzheimers Dis. 31 2012 801 812
59. C. Zhong, X. Zhao, K.C. Van, T. Bzdega, A. Smyth, J. Zhou, A.P. Kozikowski, J. Jiang, W.T. O'Connor, R.F. Berman, J.H. Neale, and B.G. Lyeth NAAG peptidase inhibitor increases dialysate NAAG and reduces glutamate, aspartate and GABA levels in the dorsal hippocampus following fluid percussion injury in the rat J. Neurochem. 97 2006 1015 1025
60. D. Zuo, T. Bzdega, R.T. Olszewski, J.R. Moffett, and J.H. Neale Effects of NAAG peptidase inhibition on release of glutamate and dopamine in the prefrontal cortex and nucleus accumbens in the phencyclidine model of schizophrenia J. Biol. Chem. 287 2012 21773 21783
61. K.M. Wozniak, C. Rojas, Y. Wu, and B.S. Slusher The role of glutamate signaling in pain processes and its regulation by GCP II inhibition Curr. Med. Chem. 19 2012 1323 1334