Neuroprotective effects of selective group II mGluR activation in brain trauma and traumatic neuronal injury

Journal of Neurotrauma

Volumn 23, Issue 2, 2006, Pages 117-127

  Movsesyan, Vilen A ^a   Faden, Alan I ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Agonist; Brain trauma; mGluR; Neuronal cell death

Indexed keywords

4 AMINO 2 OXABICYCLO[3.1.0]HEXANE 4,6 DICARBOXYLIC ACID; ALPHA ETHYLGLUTAMIC ACID; GLUTAMATE RECEPTOR 2; GLUTAMATE RECEPTOR 3; GLUTAMATE RECEPTOR ANTAGONIST; GLUTAMIC ACID DERIVATIVE; N ACETYLASPARTYLGLUTAMIC ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; CONVALESCENCE; CULTURE MEDIUM; DISEASE MODEL; DRUG EFFECT; GLIA CELL; MALE; MOTOR ACTIVITY; MOUSE; MOUSE STRAIN; NERVE CELL CULTURE; NERVE CELL LESION; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; RAT; RECEPTOR INTRINSIC ACTIVITY; TRAUMATIC BRAIN INJURY;

AMINO ACIDS; ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; BRAIN INJURIES; CELL CULTURE TECHNIQUES; DIPEPTIDES; GLUTAMATES; LEARNING; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; NEURONS; NEUROPROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE;

EID: 33644895744     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2006.23.117     Document Type: Article

References (75)

1. 2+ signal transduction. J. Biol. Chem. 267, 13361-13368.
2. ALLEN, J.W., IVANOVA, S.A., FAN, L., ESPEY, M.G., BASILE, A.S., and FADEN, A.I. (1999). Group II metabotropic glutamate receptor activation attenuates traumatic neuronal injury and improves neurological recovery after traumatic brain injury. J. Pharmacol. Exp. Ther. 290, 112-120.
3. ALLEN, J.W., KNOBLACH, S.M., and FADEN, A.I. (2000). Activation of group I metabotropic glutamate receptors reduces neuronal apoptosis but increases necrotic cell death in vitro. Cell Death Differ. 7, 470-476.
4. ALLEN, J.W., VICINI, S., and FADEN, A.I. (2001). Exacerbation of neuronal cell death by activation of group I metabotropic glutamate receptors: role of NMDA receptors and arachidonic acid release. Exp. Neurol. 169, 449-460.
5. ANWYL, R. (1999). Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res. Brain Res. Rev. 29, 83-120.
6. 2+ accumulation. Neuropharmacology 32, 1351-1358.
7. BOLSHAKOV, V.Y., and SIEGELBAUM, S.A. (1994). Postsynaptic induction and presynaptic expression of hippocampal long-term depression. Science 264, 1148-1152.
8. BOND, A., O'NEILL, M.J., HICKS, C.A., MONN, J.A., and LODGE, D. (1998). Neuroprotective effects of a systemically active group II metabotropic glutamate receptor agonist LY354740 in a gerbil model of global ischaemia. Neuroreport 9, 1191-1193.
9. BOND, A., RAGUMOORTHY, N., MONN, J.A., et al. (1999). LY379268, a potent and selective group II metabotropic glutamate receptor agonist, is neuroprotective in gerbil global, but not focal, cerebral ischaemia. Neurosci. Lett. 273, 191-194.
10. BOND, A., JONES, N.M., HICKS, C.A., et al. (2000). Neuroprotective effects of LY379268, a selective mGlu2/3 receptor agonist: investigations into possible mechanism of action in vivo. J. Pharmacol. Exp. Ther. 294, 800-809.
11. BRUNO, V., COPANI, A., BATTAGLIA, G., RAFFAELE, R., SHINOZAKI, H., and NICOLETTI, F. (1994). Protective effect of the metabotropic glutamate receptor agonist, DCG-, I.V., against excitotoxic neuronal death. Eur. J. Pharmacol. 256, 109-112.
12. BRUNO, V., BATTAGLIA, G., COPANI, A., et al. (1995). Activation of class II or III metabotropic glutamate receptors protects cultured cortical neurons against excitotoxic degeneration. Eur. J. Neurosci. 7, 1906-1913.
13. BRUNO, V., BATTAGLIA, G., KSIAZEK, I., et al. (2000). Selective activation of mGlu4 metabotropic glutamate receptors is protective against excitotoxic neuronal death. J. Neurosci. 20, 6413-6420.
14. BUISSON, A., and CHOI, D.W. (1995). The inhibitory mGluR agonist, S-4-carboxy-3-hydroxy-phenylglycine selectively attenuates NMDA neurotoxicity and oxygen-glucose deprivation-induced neuronal death. Neuropharmacology 34, 1081-1087.
15. CHIAMULERA, C., ALBERTINI, P., VALERIO, E., and REGGIANI, A. (1992). Activation of metabotropic receptors has a neuroprotective effect in a rodent model of focal ischaemia. Eur. J. Pharmacol. 216, 335-336.
16. CONN, P.J., and PIN, J.P. (1997). Pharmacology and functions of metabotropic glutamate receptors. Annu. Rev. Pharmacol. Toxicol. 37, 205-237.
17. COPANI, A., BRUNO, V., BATTAGLIA, G., et al. (1995). Activation of metabotropic glutamate receptors protects cultured neurons against apoptosis induced by beta-amyloid peptide. Mol. Pharmacol. 47, 890-897.
18. DI IORIO, P., BATTAGLIA, G., CICCARELLI, R., et al. (1996). Interaction between Al adenosine and class II metabotropic glutamate receptors in the regulation of purine and glutamate release from rat hippocampal slices. J. Neurochem. 67, 302-309.
19. DUVOISIN, R.M., ZHANG, C., and RAMONELL, K. (1995). A novel metabotropic glutamate receptor expressed in the retina and olfactory bulb. J. Neurosci. 15, 3075-3083.
20. FADEN, A.I. (1993). Comparison of single and combination drug treatment strategies in experimental brain trauma. J. Neurotrauma 10, 91-100.
21. FADEN, A.E., and NOBLE, L.J. (1990). Effects of competitive and noncompetitive NMDA receptor antagonists in spinal cord injury. Eur. J. Pharmacol. 175, 165.
22. FADEN, A.I., and SIMON, R.P. (1988). A potential role for excitotoxins in the pathophysiology of spinal cord injury. Ann. Neurol. 23, 623-626.
23. FADEN, A.I., DEMEDIUK, P., PANTER, S.S., and VINK, R. (1989). The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 244, 798-800.
24. FADEN, A.I., IVANOVA, S.A., YAKOVLEV, A.G., and MUKHIN, A.G. (1997). Neuroprotective effects of group III mGluR in traumatic neuronal injury. J. Neurotrauma 14, 885-895.
25. FADEN, A.I., O'LEARY, D.M., FAN, L., BAO, W., MULLINS, P.G., and MOVSESYAN, V.A. (2001). Selective blockade of the mGluR1 receptor reduces traumatic neuronal injury in vitro and improves outcome after brain trauma. Exp. Neurol. 167, 435-444.
26. FADEN, A.I., FOX, G.B., D.I., X., et al. (2003a). Neuroprotective and nootropic actions of a novel cyclized dipeptide after controlled cortical impact injury in mice. J. Cereb. Blood Flow Metab. 23, 355-363.
27. FADEN, A.I., KNOBLACH, S.M., CERNAK, I., et al. (2003b). Novel diketopiperazine enhances motor and cognitive recovery after traumatic brain injury in rats and shows neuroprotection in vitro and in vivo. J. Cereb. Blood Flow Metab. 23, 342-354.
28. FERRAGUTI, F., BALDANI-GUERRA, B., CORSI, M., NAKANISHI, S., and CORTI, C. (1999). Activation of the extracellular signal-regulated kinase 2 by metabotropic glutamate receptors. Eur. J. Neurosci. 11, 2073-2082.
29. FOX, G.B., FAN, L., LEVASSEUR, R.A., and FADEN, A.I. (1998). Sustained sensory/motor and cognitive deficits with neuronal apoptosis following controlled cortical impact brain injury in the mouse. J. Neurotrauma 15, 599-614.
30. GONG, Q.Z., DELAHUNTY, T.M., HAMM, R.J., and LYETH, B.G. (1995). Metabotropic glutamate antagonist, MCPG, treatment of traumatic brain injury in rats. Brain Res. 700, 299-302.
31. HAYES, R.L., JENKINS, L.W., LYETH, B.G., et al. (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.
32. HENRICH-NOACK, P., HATTON, C.D., and REYMANN, K.G. (1998). The mGlu receptor ligand (S)-4C3HPG protects neurons after global ischaemia in gerbils. Neuroreport 9, 985-988.
33. HOLLMANN, M., and HEINEMANN, S. (1994). Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31-108.
34. HOUAMED, K.M., KUIJPER, J.L., GILBERT, T.L., et al. (1991). Cloning, expression, and gene structure of a G protein-coupled glutamate receptor from rat brain. Science 252, 1318-1321.
35. IACOVELLI, L., BRUNO, V., SALVATORE, L., et al. (2002). Native group-III metabotropic glutamate receptors are coupled to the mitogen-activated protein kinase/phosphatidylinositol-3-kinase pathways. J. Neurochem. 82, 216-223.
36. KOH, J.Y., PALMER, E., and COTMAN, C.W. (1991). Activation of the metabotropic glutamate receptor attenuates N-methyl-D-aspartate neurotoxicity in cortical cultures. Proc. Natl. Acad. Sci. USA 88, 9431-9435.
37. KORNHUBER, J., and WELLER, M. (1997). Psychotogenicity and N-methyl-D-aspartate receptor antagonism: implications for neuroprotective pharmacotherapy. Biol. Psychiatry 41, 135-144.
38. LEA, P.M.I., MOVSESYAN, V.A., and FADEN, A.I. (2005). Neuroprotective activity of the mGluR5 antagonists MPEP and MTEP against acute excitotoxicity differs and does not reflect actions at mGluR5 receptors. Br. J. Pharmacol. 145, 527-534.
39. MASU, M., TANABE, Y., TSUCHIDA, K., SHIGEMOTO, R., and NAKANISHI, S. (1991). Sequence and expression of a metabotropic glutamate receptor. Nature 349, 760-765.
40. MCDONALD, J.W., and SCHOEPP, D.D. (1992). The metabotropic excitatory amino acid receptor agonist, 1.S.,3R-ACPD selectively potentiates N-methyl-D-aspartate-induced brain injury. Eur. J. Pharmacol. 215, 353-354.
41. MCINTOSH, T.K., VINK, R., SOARES, H., HAYES, R., and SIMON, R. (1990). Effect of noncompetitive blockade of N-methyl-D-aspartate receptors on the neurochemical sequelae of experimental brain injury. J. Neurochem. 55, 1170-1179.
42. MCINTOSH, T.K., VINK, R., SOARES, H., HAYES, R., SIMON, R. (1989). Effects of the N-methyl-D-aspartate receptor blocker MK-801 on neurologic function after experimental brain injury. J Neurotrauma 6, 247-259.
43. MELI, E., PICCA, R., ATTUCCI, S., et al. (2002). Activation of mGlu1 but not mGlu5 metabotropic glutamate receptors contributes to postischemic neuronal injury in vitro and in vivo. Pharmacol. Biochem. Behav. 73, 439-446.
44. MILLS, C.D., XU, G.Y., MCADOO, D.J., and HULSEBOSCH, C.E. (2001). Involvement of metabotropic glutamate receptors in excitatory amino acid and GABA release following spinal cord injury in rat. J. Neurochem. 79, 835-848.
45. MINAKAMI, R., KATSUKI, F., and SUGIYAMA, H. (1993). A variant of metabotropic glutamate receptor subtype 5, an evolutionally conserved insertion with no termination codon. Biochem. Biophys. Res. Commun. 194, 622-627.
46. MONN, J.A., VALLI, M.J., MASSEY, S.M., et al. (1999). Synthesis, pharmacological characterization, and molecular modeling of heterobicyclic amino acids related, t.o. (+)-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.
47. MOVSESYAN, V.A., O'LEARY, D.M., FAN, L., et al. (2001). mGluR5 antagonists 2-methyl-6-(phenylethynyl)-pyridine and (E)-2-methyl- 6-(2-phenylethenyl)-pyridine reduce traumatic neuronal injury in vitro and in vivo by antagonizing N-methyl-D-aspartate receptors. J. Pharmacol. Exp. Ther. 296, 41-47.
48. MOVSESYAN, V.A., STOICA, B.A., and FADEN, A.I. (2004). MGLuR5 activation reduces beta-amyloid-induced cell death in primary neuronal cultures and attenuates translocation of cytochrome c and apoptosis-inducing factor. J. Neurochem. 89, 1528-1536.
49. MUKHIN, A., FAN, L., and FADEN, A.I. (1996). Activation of metabotropic glutamate receptor subtype mGluR1 contributes to post-traumatic neuronal injury. J. Neurosci. 16, 6012-6020.
50. MUKHIN, A.G., IVANOVA, S.A., KNOBLACH, S.M., and FADEN, A.I. (1997). New in vitro model of traumatic neuronal injury: evaluation of secondary injury and glutamate receptor-mediated neurotoxicity. J. Neurotrauma 14, 651-663.
51. MUKHIN, A.G., IVANOVA, S.A., ALLEN, J.W., and FADEN, A.I. (1998). Mechanical injury to neuronal/glial cultures in microplates: role of NMDA receptors and pH in secondary neuronal cell death. J. Neurosci. Res. 51, 748-758.
52. NAKAJIMA, Y., IWAKABE, H., AKAZAWA, C., et al. (1993). Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. J. Biol. Chem. 268, 11868-11873.
53. NAKANISHI, S. (1994). Metabotropic glutamate receptors: synaptic transmission, modulation, and plasticity. Neuron 13, 1031-1037.
54. NILSSON, P., HILLERED, L., PONTEN, U., and 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.
55. OKAMOTO, N., HORI, S., AKAZAWA, C., et al. (1994). Molecular characterization of a new metabotropic glutamate receptor mGluR7 coupled to inhibitory cyclic AMP signal transduction. J. Biol. Chem. 269, 1231-1236.
56. O'LEARY, D.M., MOVSESYAN, V., VICINI, S., and FADEN, A.I. (2000). Selective mGluR5 antagonists MPEP and SIB-1893 decrease NMDA or glutamate-mediated neuronal toxicity through actions that reflect NMDA receptor antagonism. Br. J. Pharmacol. 131, 1429-1437.
57. OLNEY, J. (1989). Excitotoxins and neuropsychiatric disorders. Biol. Psychiatry 26, 505-525.
58. OPITZ, T., RICHTER, P., and REYMANN, K.G. (1994). The metabotropic glutamate receptor antagonist (+)-alpha-methyl-4-carboxyphenylglycine protects hippocampal CA1 neurons of the rat from in vitro hypoxia/hypoglycemia. Neuropharmacology 33, 715-717.
59. PANTER, S.S., YUM, S.W., and FADEN, A.I. (1990). Alteration in extracellular amino acids after traumatic spinal cord injury. Ann. Neurol. 27, 96-99.
60. PIN, J.P. (1995). Review. Neurotransmitter receptors I - The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34, 1-26.
61. PIN, J.P., and BOCKAERT, J. (1993). The metabotropic glutamate receptors; targets for new pharmacologically active drugs. Curr. Drugs Neurodegen. Dis. 1, 111-137.
62. PIN, J.P., WAEBER, C., PREZEAU, L., BOCKAERT, J., and HEINEMANN, S.F. (1992). Alternative splicing generates metabotropic glutamate receptors inducing different patterns of calcium release in Xenopus oocytes. Proc. Natl. Acad. Sci. USA 89, 10331-10335.
63. POLI, A., BERAUDI, A., VILLANI, L., et al. (2003). Group II metabotropic glutamate receptors regulate the vulnerability to hypoxic brain damage. J. Neurosci. 23, 6023-6029.
64. SACAAN, A.I., and SCHOEPP, D.D. (1992). Activation of hippocampal metabotropic excitatory amino acid receptors leads to seizures and neuronal damage. Neurosci. Lett. 139, 77-82.
65. SAUGSTAD, J.A., KINZIE, J.M., MULVIHILL, E.R., SEGERSON, T.P., and WESTBROOK, G.L. (1994). Cloning and expression of a new member of the L-2-amino-4-phosphonobutyric acid-sensitive class of metabotropic glutamate receptors. Mol. Pharmacol. 45, 367-372.
66. SCHOEPP, D.D., and CONN, P.J. (1993). Metabotropic glutamate receptors in brain function and pathology. Trends Pharmacol. Sci. 14, 13-20.
67. SCHOEPP, D.D., JANE, D.E., and MONN, J.A. (1999). Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology 38, 1431-1476.
68. SHAPIRA, Y., YADID, G., COTEV, S., NISKA, A., and SHOHAMI, E. (1990). Protective effect of MK801 in experimental brain injury. J. Neurotrauma 7, 131-139.
69. SILIPRANDI, R., LIPARTITI, M., FADDA, E., SAUTTER, J., and MANEV, H. (1992). Activation of the glutamate metabotropic receptor protects retina against N-methyl-D-aspartate toxicity. Eur. J. Pharmacol. 219, 173-174.
70. STOVER, J.F., SAKOWITZ, O.W., BEYER, T.F., et al. (2003). Effects of LY379268, a selective group II metabotropic glutamate receptor agonist on EEG activity, cortical perfusion, tissue damage, and cortical glutamate, glucose, and lactate levels in brain-injured rats. J. Neurotrauma 20, 315-326.
71. TANABE, Y., NOMURA, A., MASU, M., SHIGEMOTO, R., MIZUNO, N., and NAKANISHI, S. (1993). Signal transduction, pharmacological properties, and expression patterns of two rat metabotropic glutamate receptors, mGluR3 and mGluR4. J. Neurosci. 13, 1372-1378.
72. VIGNES, M., CLARKE, V.R., DAVIES, C.H., et al. (1995). Pharmacological evidence for an involvement of group II and group III mGluRs in the presynaptic regulation of excitatory synaptic responses in the CA1 region of rat hippocampal slices. Neuropharmacology 34, 973-982.
73. WATKINS, J., and COLLINGRIDGE, G. (1994). Phenylglycine derivatives as antagonists of metabotropic glutamate receptors. Trends Pharmacol. Sci. 15, 333-342.
74. WIGMORE, M.A., and LACEY, M.G. (1998). Metabotropic glutamate receptors depress glutamate-mediated synaptic input to rat midbrain dopamine neurones in vitro. Br. J. Pharmacol. 123, 667-674.
75. WRATHALL, J.R., TENG, Y.D., CHOINIERE, D., and MUNDT, D.J. (1992). Evidence that local non-NMDA receptors contribute to functional deficits in contusive spinal cord injury. Brain Res. 586, 140-143.