NAAG peptidase inhibitor increases dialysate NAAG and reduces glutamate, aspartate and GABA levels in the dorsal hippocampus following fluid percussion injury in the rat

Journal of Neurochemistry

Volumn 97, Issue 4, 2006, Pages 1015-1025

  Zhong, Chunlong ^a,b   Zhao, Xueren ^a   Van, Ken C ^a   Bzdega, Tomasz ^c   Smyth, Aoife ^d   Zhou, Jia ^e   Kozikowski, Alan P ^e,f   Jiang, Jiyao ^b   O'Connor, William T ^d   Berman, Robert F ^a   Neale, Joseph H ^c   Lyeth, Bruce G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c GEORGETOWN UNIVERSITY   (United States)

^d UNIVERSITY COLLEGE DUBLIN   (Ireland)

^e Acenta Discovery Incorporated   (United States)

^f UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Gamma aminobutyric acid; Glutamate; Metabotropic glutamate receptor; Microdialysis; N acetylaspartylglutamate; Traumatic brain injury

Indexed keywords

2 AMINO 2 (2 CARBOXYCYCLOPROPYL) 3 (XANTHEN 9 YL)PROPIONIC ACID; 4 AMINOBUTYRIC ACID; ASPARTIC ACID; GLUTAMATE CARBOXYPEPTIDASE II INHIBITOR; GLUTAMATE RECEPTOR ANTAGONIST; GLUTAMIC ACID; METABOTROPIC RECEPTOR; N ACETYLASPARTYLGLUTAMIC ACID; UNCLASSIFIED DRUG; ZJ 43;

AMINO ACID BRAIN LEVEL; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DIALYSATE LEVEL; DORSAL HIPPOCAMPUS; DRUG EFFECT; DRUG MECHANISM; ENZYME INHIBITION; EXCITOTOXICITY; HIPPOCAMPUS; MICRODIALYSIS; NERVE CELL NECROSIS; NEUROPROTECTION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; TRAUMATIC BRAIN INJURY;

ANIMALS; ASPARTIC ACID; BRAIN INJURIES; CYTOPROTECTION; DIPEPTIDES; DISEASE MODELS, ANIMAL; DOWN-REGULATION; ENZYME INHIBITORS; EXTRACELLULAR FLUID; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE CARBOXYPEPTIDASE II; GLUTAMIC ACID; HIPPOCAMPUS; MALE; MICRODIALYSIS; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; NEUROTOXINS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUTAMATE; UP-REGULATION;

ANIMALIA;

EID: 33646078096     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.03786.x     Document Type: Article

References (70)

1. Allen J. W. Ivanova S. A. Fan L. Espey M. G. Basile A. S. Faden A. I. 1999 Group II metabotropic glutamate receptor activation attenuates traumatic neuronal injury and improves neurological recovery after traumatic brain injury. J. Pharm. Exper. Ther. 290 112 120.
2. Alves O. L. Bullock R. Clausen T. Reinert M. Reeves T. M. 2005 Concurrent monitoring of cerebral electrophysiology and metabolism after traumatic brain injury: an experimental and clinical study. J. Neurotrauma 22 733 749.
3. Aronica E. Gorter J. A. Ijlst-Keizers H. Rozemuller A. J. Yankaya B. Leenstra S. Troost D. 2003 Expression and functional role of mGluR3 and mGluR5 in human astrocytes and glioma cells: opposite regulation of glutamate transporter proteins. Eur. J. Neurosci. 17 2106 2118.
4. Bentzer P. Davidsson H. Grande P. O. 2000 Microdialysis-based long-term measurements of energy-related metabolites in the rat brain following a fluid percussion trauma. J. Neurotrauma 17 441 447.
5. Benveniste H. Drejer J. Schousboe A. Diemer N. H. 1984 Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J. Neurochem. 43 1369 1374.
6. Bischofberger J. Schild D. 1996 Glutamate and N-acetylaspartylglutamate block HVA calcium currents in frog olfactory bulb interneurons via an mGluR2/3-like receptor. J. Neurophysiol. 76 2089 2092.
7. Bruno V. Wroblewska B. Wroblewski J. T. Fiore L. Nicoletti F. 1998 Neuroprotective activity of N-acetylaspartylglutamate in cultured cortical cells. Neuroscience 85 751 757.
8. Bullock R. Zauner A. Woodward J. J. Myseros J. Choi S. C. Ward J. D. Marmarou A. Young H. F. 1998 Factors affecting excitatory amino acid release following severe human head injury. J. Neurosurg. 89 507 518.
9. Bullock R. Lyeth B. G. Muizelaar J. P. 1999 Current status of neuroprotection trials for traumatic brain injury: lessons from animal models and clinical studies. Neurosurgery 45 207 217.
10. Bzdega T. Crowe S. L. Ramadan E. R. Sciarretta K. H. Olszewski R. T. Ojeifo O. A. Rafalski V. A. Wroblewska B. Neale J. H. 2004 The cloning and characterization of a second brain enzyme with NAAG peptidase activity. J. Neurochem. 89 627 635.
11. Choi D. W. Rothman S. M. 1990 The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu. Rev. Neurosci. 13 171 182.
12. Coyle J. T. 1997 The nagging question of the function of N-acetylaspartylglutamate. Neurobiol. Dis 4 231 238.
13. Dixon C. E. Lyeth B. G. Povlishock J. T. Findling R. L. Hamm R. J. Marmarou A. Young H. F. Hayes R. L. 1987 A fluid percussion model of experimental brain injury in the rat. J. Neurosurg. 67 110 119.
14. Dixon C. E. Bao J. Long D. A. Hayes R. L. 1996 Reduced evoked release of acetylcholine in the rodent hippocampus following traumatic brain injury. Pharmacol. Biochem. Behav. 53 679 686.
15. Faden A. I. Demediuk P. Panter S. S. Vink R. 1989 The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 244 798 800.
16. Ferraguti F. Corti C. Valerio E. Mion S. Xuereb J. 2001 Activated astrocytes in areas of kainate-induced neuronal injury upregulate the expression of the metabotropic glutamate receptors 2/3 and 5. Exp. Brain Res. 137 1 11.
17. Garrido-Sanabria E. R. Wozniak K. M. Slusher B. S. Keller A. 2004 GCP II (NAALADase) inhibition suppresses mossy fiber-CA3 synaptic neurotransmission by a presynaptic mechanism. J. Neurophysiol. 91 182 193.
18. Ghadge G. D. Slusher B. S. Bodner A. et al. 2003 Glutamate carboxypeptidase II inhibition protects motor neurons from death in familial amyotrophic lateral sclerosis models. Proc. Natl Acad. Sci. USA 100 9554 9559.
19. Globus M. Y. Busto R. Dietrich W. D. Martinez E. Valdes I. Ginsberg M. D. 1988 Effect of ischemia on the in vivo release of striatal dopamine, glutamate, and γ-aminobutyric acid studied by intracerebral microdialysis. J. Neurochem. 51 1455 1464.
20. Globus M. Y. Busto R. Martinez E. Valdes I. Dietrich W. D. Ginsberg M. D. 1991 Comparative effect of transient global ischemia on extracellular levels of glutamate, glycine, and γ-aminobutyric acid in vulnerable and non-vulnerable brain regions in the rat. J. Neurochem. 57 470 478.
21. Globus M. Y. Alonso O. Dietrich W. D. Busto R. Ginsberg M. D. 1995 Glutamate release and free radical production following brain injury. J. Neurochem. 65 1704 1711.
22. Hayes R. L. Jenkins L. W. Lyeth B. G. Balster R. L. Robinson S. E. Clifton G. L. Stubbins J. F. Young H. F. 1988 Pretreatment with phencyclidine, an N-methyl- d -aspartate antagonist, attenuates long-term behavioral deficits in the rat produced by traumatic brain injury. J. Neurotrauma 5 259 274.
23. Hillered L. Vespa P. M. Hovda D. A. 2005 Translational neurochemical research in acute human brain injury: the current status and potential future for cerebral microdialysis. J. Neurotrauma 22 3 41.
24. Hsiao J. K. Ball B. A. Morrison P. F. Mefford I. N. Bungay P. M. 1990 Effects of different semipermeable membranes on in vitro and in vivo performance of microdialysis probes. J. Neurochem. 54 1449 1452.
25. Jackson P. F. Slusher B. S. 2001 Design of NAALADase inhibitors: a novel neuroprotective strategy. Curr. Med. Chem. 8 949 957.
26. Jackson P. F. Cole D. C. Slusher B. S. Stetz S. L. Ross L. E. Donzanti B. A. Trainor D. A. 1996 Design, synthesis, and biological activity of a potent inhibitor of the neuropeptidase N-acetylated-linked acidic dipeptidase. J. Med. Chem. 39 619 622.
27. Jiang J. Y. Lyeth B. G. Kapasi M. Z. Jenkins L. W. Povlishock J. T. 1992 Moderate hypothermia reduces blood-brain barrier disruption following traumatic brain injury in the rat. Acta Neuropathologica 84 495 500.
28. Jones C. K. Eberle E. L. Peters S. C. Monn J. A. Shannon H. E. 2005 Analgesic effects of the selective group II (mGlu2/3) metabotropic glutamate receptor agonists LY379268 and LY389795 in persistent and inflammatory pain models after acute and repeated dosing. Neuropharmacology 49 206 218.
29. Katayama Y. Becker D. P. Tamura T. Hovda D. A. 1990 Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J. Neurosurg. 73 889 900.
30. Kawamata T. Katayama Y. Hovda D. A. Yoshino A. Becker D. P. 1992 Administration of excitatory amino acid antagonists via microdialysis attenuates the increase in glucose utilization seen following concussive brain injury. J. Cereb. Blood Flow Metab. 12 12 24.
31. Kawamata T. Katayama Y. Hovda D. A. Yoshino A. Becker D. P. 1995 Lactate accumulation following concussive brain injury: the role of ion fluxes induced by excitatory amino acids. Brain Res. 674 196 204.
32. Kingston A. E. Ornstein P. L. Wright R. A. Johnson B. G. Mayne N. G. Burnett J. P. Belagaje R. Wu S. Schoepp D. D. 1998 LY341495 is a nanomolar potent and selective antagonist of group II metabotropic glutamate receptors. Neuropharmacology 37 1 12.
33. Koura S. S. Doppenberg E. M. Marmarou A. Choi S. Young H. F. Bullock R. 1998 Relationship between excitatory amino acid release and outcome after severe human head injury. Acta Neurochir. Suppl. 71 244 246.
34. Kozikowski A. P. Nan F. Conti P. Zhang J. Ramadan E. Bzdega T. Wroblewska B. Neale J. H. Pshenichkin S. Wroblewski J. T. 2001 Design of remarkably simple, yet potent urea-based inhibitors of glutamate carboxypeptidase II (NAALADase). J. Med. Chem. 44 298 301.
35. Kozikowski A. P. Zhang J. Nan F. Petukhov P. A. Grajkowska E. Wroblewski J. T. Yamamoto T. Bzdega T. Wroblewska B. Neale J. H. 2004 Synthesis of urea-based inhibitors as active site probes of glutamate carboxypeptidase II: efficacy as analgesic agents. J. Med. Chem. 47 1729 1738.
36. Luthi-Carter R. Berger U. V. Barczak A. K. Enna M. Coyle J. T. 1998 Isolation and expression of a rat brain cDNA encoding glutamate carboxypeptidase II. Proc. Natl Acad. Sci. USA 95 3215 3220.
37. McIntosh T. K. Vink R. Noble L. Yamakami I. Fernyak S. Soares H. Faden A. L. 1989 Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience 28 233 244.
38. Monn J. A. Valli M. J. Massey S. M. et al. 1999 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 1027 1040
39. 2 receptor antagonism differentially modulates stimulation of striatal neurotransmitter levels by N-methyl- d -aspartic acid. Eur. J. Pharmacol. 256 23 30.
40. Narayan R. K. Michel M. E. Ansell B. et al. 2002 Clinical trials in head injury. J. Neurotrauma 19 503 557.
41. Neale J. H. Bzdega T. Wroblewska B. 2000 N-acetylaspartylglutamate: the most abundant peptide neurotransmitter in the mammalian central nervous system. J. Neurochem. 75 443 452.
42. Neale J. H. Olszewski R. T. Gehl L. M. Wroblewska B. Bzdega T. 2005 The neurotransmitter N-acetylaspartylglutamate in models of pain, ALS, diabetic neuropathy, CNS injury and schizophrenia. Trends Pharmacol. Sci. 26 477 484.
43. National Institutes of Health. 1999 Consensus conference. Rehabilitation of persons with traumatic brain injury. NIH Consensus Development Panel on Rehabilitation of Persons with Traumatic Brain Injury. J Am Med Assoc 282 974 983.
44. Nilsson P. Hillered L. Ponten U. Ungerstedt U. 1990 Changes in cortical extracellular levels of energy-related metabolites and amino acids following concussive brain injury in rats. J. Cereb. Blood Flow Metab. 10 631 637.
45. Olszewski R. Buhkari N. Zhou J. et al. 2004 NAAG peptidase inhibition reduces locomotor activity and some stereotypes in the PCP model of schizophrenia via group II mGluR. J. Neurochem. 89 876 885.
46. Palmer A. M. Marion D. W. Botscheller M. L. Bowen D. M. DeKosky S. T. 1994 Increased transmitter amino acid concentration in human ventricular CSF after brain trauma. Neuroreport 30 153 156.
47. Parsons L. H. Justice J. B. Jr. 1994 Quantitative approaches to in vivo brain microdialysis. Crit. Rev. Neurobiol. 8 189 220.
48. Paxinos G. Watson C. 1998 The Rat Brain in Stereotaxic Coordinates 4th edn. Academic Press, San Diego.
49. Pinheiro J. C. Bates D. M. 2000 Mixed-Effects Models in S and S-Plus pp. 11 86. Springer-Verlag New York.
50. R Development Core Team. 2005 R: A Language and Environment for Statistical Computing. R. Foundation for Statistical Computing Vienna, Austria. Available from: http://www.R-project.org (accessed on 17 August 2005).
51. Rong S. B. Zhang J. Neale J. H. Wroblewski J. T. Wang S. Kozikowski A. P. 2002 Molecular modeling of the interactions of glutamate carboxypeptidase II with its potent NAAG-based inhibitors. J. Med. Chem. 45 4140 4152.
52. Schweitzer C. Kratzeisen C. Adam G. Lundstrom K. Malherbe P. Ohresser S. Stadler H. Wichmann J. Woltering T. Mutel V. 2000 Characterization of-LY354740 binding to rat mGlu2 and mGlu3 receptors expressed in CHO cells using Semliki Forest virus vectors. Neuropharmacology 39 1700 1706.
53. Slusher B. S. Vornov J. J. Thomas A. G. et al. 1999 Selective inhibition of NAALADase, which converts NAAG to glutamate, reduces ischemic brain injury. Nat. Med. 5 1396 1402.
54. Smyth A. Gilchrist M. Kelly J. A. O'Connor W. T. 2005a Perfusion with TRH into the medial prefrontal cortex following a mild local injury increases local glutamate release in the rat. Acta Neurobiol. Exp. 65 90.
55. Smyth A. Gilchrist M. O'Connor W. T. 2005b Traumatic injury to the medial prefrontal cortex results in immediate, prolonged increases in glutamate aspartate and GABA release remote from the site of injury. Proceedings of Molecular Mechanisms of Neurodegeneration; a Joint Biochemical Society/Neuroscience Ireland Focused Meeting. University College Dublin, Ireland 14-16 March 2005 25.
56. Smyth G. K. Verbyla A. P. 1996 A conditional approach to residual maximum likelihood estimation in generalized linear models. J. Royal Statist. Soc. B 58 565 572.
57. Wroblewska B. Wroblewski J. T. Saab O. H. Neale J. H. 1993 N-acetylaspartylglutamate inhibits forskolin-stimulated cyclic AMP levels via a metabotropic glutamate receptor in cultured cerebellar granule cells. J. Neurochem. 61 943 948.
58. Wroblewska B. Wroblewski J. T. Pshenichkin S. Surin A. Sullivan S. E. Neale J. H. 1997 N-acetylaspartylglutamate selectively activates mGluR3 receptors in transfected cells. J. Neurochem. 69 174 181.
59. Wroblewska B. Santi M. R. Neale J. H. 1998 N-acetylaspartylglutamate activates cyclic AMP-coupled metabotropic glutamate receptors in cerebellar astrocytes. Glia 24 172 179.
60. Xi Z. X. Baker D. A. Shen H. Carson D. S. Kalivas P. W. 2002 Group II metabotropic glutamate receptors modulate extracellular glutamate in the nucleus accumbens. J. Pharmacol. Exp. Ther. 300 162 171.
61. Yamamoto T. Nozaki-Taguchi N. Sakashita Y. Inagaki T. 2001a Inhibition of spinal N-acetylated-α-linked acidic dipeptidase produces an anti-nociceptive effect in the rat formalin test. Neuroscience 102 473 479.
62. Yamamoto T. Nozaki-Taguchi N. Yoshihiko S. 2001b Spinal N-acetyl-α-linked acidic dipeptidase (NAALADase) inhibition attenuates mechanical allodynia induced by paw carrageenan injection in the rat. Brain Res. 909 138 144.
63. Yamamoto T. Hirasawa S. Wroblewska B. Grajkowska E. Zhou J. Kozikowski A. P. Wroblewska J. Neale J. H. 2004 Anti-nociceptive 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. 20 483 494.
64. Zauner A. Bullock R. Kuta A. J. Woodward J. Young H. F. 1996 Glutamate release and cerebral blood flow after severe human head injury in Clinical Aspects of Microdialysis Mendelowitsch A. Langemann H. Alessandri B. Landholt H. Gratzl O. eds) pp. 40 44. Springer Wien.
65. Zeevalk G. D. Nicklas W. J. 1993 Hypothermia, metabolic stress, and NMDA-mediated excitotoxicity. J. Neurochem. 61 1445 1453.
66. Zhang W. Slusher B. Murakawa Y. Wozniak K. M. Tsukamoto T. Jackson P. F. Sima A. A. 2002 GCPII (NAALADase) inhibition prevents long-term diabetic neuropathy in type 1 diabetic BB/Wor rats. J. Neurol. Sci. 194 21 28.
67. 3H]-GABA release via mGluR3, cAMP, PKA and 1-type calcium conductance. Eur. J. Neurosci. 13 340 346.
68. Zhong C. Zhao X. Sarva J. Kozikowski A. Neale J. H. Lyeth B. G. 2005 NAAG peptidase inhibitor reduces acute neuronal degeneration and astrocyte damage following lateral fluid percussion TBI in rats. J. Neurotrauma 22 266 276.
69. Zhou J. Neale J. H. Pomper M. G. Kozikowski A. P. 2005 NAAG peptidase inhibitors and their potential for diagnosis and therapy. Nature Rev. Drug Discovery 4 1015 1026.
70. Zwienenberg M. Gong Q.-Z. Berman R. F. Muizelaar J. P. Lyeth B. G. 2001 The effect of groups II and III metabotropic glutamate receptor activation on neuronal injury in a rodent model of traumatic brain injury. Neurosurgery 48 1119 1126.