Protection against glucose-induced neuronal death by NAAG and GCP II inhibition is regulated by mGluR3

Journal of Neurochemistry

Volumn 89, Issue 1, 2004, Pages 90-99

  Berent Spillson, Alison ^a   Robinson, Amanda M ^a   Golovoy, David ^a   Slusher, Barbara ^b   Rojas, Camilo ^b   Russell, James W ^a,c  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b GUILFORD PHARMACEUTICALS INC   (United States)

^c VA ANN ARBOR HEALTHCARE SYSTEM   (United States)

Author keywords

Apoptosis; Diabetes; Dorsal root ganglia; Glutamate carboxypeptidase II; Metabotropic glutamate receptor; N acetyl aspartyl glutamate

Indexed keywords

2 (PHOSPHONOMETHYL)PENTANEDIOIC ACID; 4 AMINOPYRROLIDINE 2,4 DICARBOXYLATE; ALPHA ETHYLGLUTAMIC ACID; CASPASE; DICARBOXYLIC ACID; GAMMA GLUTAMYL HYDROLASE; GAMMA GLUTAMYL HYDROLASE 2; GLUCOSE; GLUTAMIC ACID DERIVATIVE; METABOTROPIC RECEPTOR 3; METABOTROPIC RECEPTOR AGONIST; METABOTROPIC RECEPTOR ANTAGONIST; N ACETYLASPARTYLGLUTAMIC ACID; PEPTIDE HYDROLASE INHIBITOR; PYRROLIDINE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC NEUROPATHY; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME INHIBITION; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROPROTECTION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SPINAL GANGLION;

ANIMALIA;

EID: 1842562427     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2003.02321.x     Document Type: Article

References (50)

1. Arias C., Becerra-Garcia F. and Tapia R. (1998) Glutamic acid and Alzheimer's disease. Neurobiology (Bp) 6, 33-43.
2. Aronica E., van Vliet E. A., Mayboroda O. A., Troost D., da Silva F. H. and Gorter J. A. (2000) Upregulation of metabotropic glutamate receptor subtype mGluR3 and mGluR5 in reactive astrocytes in a rat model of mesial temporal lobe epilepsy. Eur. J. Neurosci. 12, 2333-2344.
3. Atlante A., Calissano P., Bobba A., Giannattasio S., Marra E. and Passarella S. (2001) Glutamate neurotoxicity, oxidative stress and mitochondria. FEBS Lett. 497, 1-5.
4. Azkue J. J., Mateos J. M., Elezgarai I., Benitez R., Osorio A., Diez J., Bilbao A., Bidaurrazaga A. and Grandes P. (2000) The metabotropic glutamate receptor subtype mGluR 2/3 is located at extrasynaptic loci in rat spinal dorsal horn synapses. Neurosci. Lett. 287, 236-238.
5. Beal M. F. (1998) Excitotoxicity and nitric oxide in Parkinson's disease pathogenesis. Ann. Neurol. 44, S110-S114.
6. Bottenstein J. E. (1989) Serum-free culture of dissociated chick embryo sensory neurons, in A Dissection and Tissue Culture Manual of the Nervous System (Shahar, A., de Vellis, J., Vernadakis, A. and Haber, B., eds), pp. 227-229. Alan R. Liss Inc, New York.
7. Brockes J. P., Raff M. C., Nishiguchi D. J. and Winter J. (1980) Studies on cultured rat Schwann cells III: assays for peripheral myelin proteins. J. Neurocytol. 9, 67-77.
8. Bruno V., Sureda F. X., Storto M., Casabona G., Caruso A., Knopfel T., Kuhn R. and Nicoletti F. (1997) The neuroprotective activity of group-II metabotropic glutamate receptors requires new protein synthesis and involves a glial-neuronal signaling, J. Neurosci. 17, 1891-1897.
9. Bruno V., Battaglia G., Casabona G., Copani A., Caciagli F. and Nicoletti F. (1998) Neuroprotection by glial metabotropic glutamate receptors is mediated by transforming growth factor-beta. J. Neurosci. 18, 9594-9600.
10. Cai Z., Lin S. and Rhodes P. G. (2002) Neuroprotective effects of N-acetylaspartylglutamate in a neonatal rat model of hypoxia-ischemia. Eur. J. Pharmacol. 437, 139-145.
11. Cameron N. E., Cotter M. A. and Maxfield E. K. (1993) Anti-oxidant treatment prevents the development of peripheral nerve dysfunction in streptozotocm-diabetic rats. Diabetologia 36, 299-304.
12. Cameron N. E., Cotter M. A., Basso M. and Hohman T. C. (1997) Comparison of the effects of inhibitors of aldose reductase and sorbitol dehydrogenase on neurovascular function, nerve conduction and tissue polyol pathway metabolites in streptozotocin-diabetic rats. Diabetologia 40, 271-281.
13. Cartmell J. and Schoepp D. D. (2000) Regulation of neurotransmitter release by metabotropic glutamate receptors. J. Neurochem. 75, 889-907.
14. Cheng C. and Zochodne D. W. (2003) Sensory neurons with activated caspase-3 survive long-term experimental diabetes. Diabetes 52, 2363-2371.
15. Ciccarelli R., Di Iorio P., Bruno V., Battaglia G., D'Alimonte I., D'Onofrio M., Nicoletti F. and Caciagli F. (1999) Activation of A(1) adenosine or mGlu3 metabotropic glutamate receptors enhances the release of nerve growth factor and S-100beta protein from cultured astrocytes. Glia 27, 275-281.
16. D'Onofrio M., Cuomo L., Battaglia G. et al. (2001) Neuroprotection mediated by glial group-II metabotropic glutamate receptors requires the activation of the MAP kinase and the phosphatidy-linositol-3-kinase pathways. J. Neurochem. 78, 435-445.
17. Davies A. M. (1998) Neuronal survival: early dependence on Schwann cells. Curr. Biol. 8, R15-R18.
18. De Blasi A., Conn P. J., Pin J. and Nicoletti F. (2001) Molecular determinants of metabotropic glutamate receptor signaling. Trends Pharmacol. Sci. 22, 114-120.
19. De Giorgi F., Lartigue L., Bauer M. K., Schubert A., Grimm S., Hanson G. T., Remington S. J., Youle R. J. and Ichas F. (2002) The permeability transition pore signals apoptosis by directing Bax translocation and multimerization. FASEB J. 16, 607-609.
20. Delaney C. L., Cheng H.-L. and Feldman E. L. (1999) Insulin-like growth factor-I prevents caspase mediated apoptosis in Schwann cells. J. Neurobiol. 41, 540-548.
21. Delaney C. L., Russell J. W., Cheng H.-L. and Feldman E. L. (2001) Insulin-like growth factor-I and over-expression of Bcl-xL prevent glucose-mediated apoptosis in Schwann cells. J. Neuropathol. Exp. Neurol. 60, 147-160.
22. Goswami R., Dawson S. A. and Dawson G. (2000) Multiple polyphosphoinositide pathways regulate apoptotic signalling in a dorsal root ganglion derived cell line. J. Neurosci. Res. 59, 136-144.
23. Huang T. J., Price S. A., Chilton L., Calcutt N. A., Tomlinson D. R., Verkhratsky A. and Fernyhough P. (2003) Insulin prevents depolarization of the mitochondrial inner membrane in sensory neurons of type 1 diabetic rats in the presence of sustained hyperglycemia. Diabetes 52, 2129-2136,
24. Korinkova P. and Lodin Z. (1976) The metabolism of glucose of nerve cells cultivated under different conditions. Acta Histochem. 56, 47-65.
25. Moldrich R. X., Giardina S. F. and Beart P. M. (2001) Group II mGlu receptor agonists fail to protect against various neurotoxic insults induced in murine cortical, striatal and cerebellar granular pure neuronal cultures. Neuropharmacology 41, 19-31.
26. Montal M. (1998) Mitochondria, glutamate neurotoxicity and the death cascade. Biochim. Biophys. Acta 1366, 113-126.
27. Neale J. H., Bzdega T. and Wroblewska B. (2000) N-Acetylaspartyl-glutamate: the most abundant peptide neurotransmitter in the mammalian central nervous system. J. Neurochem. 75, 443-452.
28. Ravenscroft A. J., Valentine J. M. and Knappett P. A. (1999) Severe hypophosphataemia and insulin resistance in diabetic ketoacidosis. Anaesthesia 54, 198.
29. Russell J. W. and Feldman E. L. (1999) Insulin-like growth factor-I prevents apoptosis in sympathetic neurons exposed to high glucose. Horm. Metab. Res. 31, 90-96.
30. Russell J. W., Windebank A. J. and Podratz J. L. (1994) Role of nerve growth factor in suramin neurotoxicity studied in vitro. Ann. Neurol. 36, 221-228.
31. Russell J. W., Windebank A. J., Schenone A. and Feldman E. L. (1998) Insulin-like growth factor-I prevents apoptosis in neurons after nerve growth factor withdrawal. J. Neurobiol. 36, 455-467.
32. Russell J. W., Sullivan K. A., Windebank A. J., Herrmann D. N. and Feldman E. L. (1999) Neurons undergo apoptosis in animal and cell culture models of diabetes. Neurobiol. Dis. 6, 347-363.
33. Russell J. W., Golovoy D., Vincent A. M., Mahendru P., Olzmann J. A., Mentzer A. and Feldman E. L. (2002) High glucose-induced oxidative stress and mitochondrial dysfunction in neurons. FASEB J. 16, 1738-1748.
34. Sayers N. M., Beswick L. J., Middlemas A., Calcutt N. A., Mizisin A. P., Tomlinson D. R. and Femyhough P. (2003) Neurotrophin-3 prevents the proximal accumulation of neurofilament proteins in sensory neurons of streptozocin-induced diabetic rats. Diabetes 52, 2372-2380.
35. Schmeichel A. M., Schmelzer J. D. and Low P. A. (2003) Oxidative injury and apoptosis of dorsal root ganglion neurons in chronic experimental diabetic neuropathy. Diabetes 52, 165-171.
36. Slusher B. S., Robinson M. B., Tsai G., Simmons M. L., Richards S. S. and Coyle J. T. (1990) Rat brain N-acetylated alpha-linked acidic dipeptidase activity: purification and immunologic characterization. J. Biol. Chem. 265, 21297-21301.
37. Slusher B. S., Vornov J. J., Thomas A. G., Hum P. D., Harukuni I., Bhardwaj A., Traystman R. J., Robinson M. B., Britton P., Lu X. C. et al. (1999) Selective inhibition of NAALADase, which converts NAAG to glutamate, reduces ischemic brain injury. Nat. Med. 5, 1396-1402.
38. Srinivasan S., Stevens M. J. and Wiley J. W. (2000) Diabetic peripheral neuropathy: evidence for apoptosis and associated mitochondrial dysfunction. Diabetes 49, 1932-1938.
39. Tanabe Y., Masu M., Ishii T., Shigemoto R. and Nakanishi S. (1992) A family of metabotropic glutamate receptors. Neuron 8, 169-179.
40. Thomas A. G., Olkowski J. L. and Slusher B. S. (2001) Neuroprotection afforded by NAAG and NAALADase inhibition requires glial cells and metabotropic glutamate receptor activation. Eur. J. Pharmacol. 426, 35-38.
41. Thomas A. G., Liu W., Olkowski J. L., Lu X.-C. M. and Slusher B. S. (1999a) The role of TGF-B in the neuroprotection mediated by naaladase inhibition in cortical cell cultures. Soc. Neurosci. Abstr. 888.12.
42. Thomas A. G., Olkowski J. L., Tang Z., Lu X. C. and Slusher B. S. (2001) Neuroprotection mediated by glutamate carboxypeptidase II (NAALA Dase) inhibition requires TGF-beta. Eur. J. Pharmacol. 430, 33-40.
43. Thomas A. G., Vomov J. J., Olkowski J. L., Merion A. T. and Slusher B. S. (2000) N-Acetylated alpha-linked acidic dipeptidase converts N-acetylaspartylglutamate from a neuroprotectant to a neurotoxin. J. Pharmacol. Exp. Ther. 295, 16-22.
44. Tomlinson D. R., Fernyhough P., Diemel L. T. and Maeda K. (1996) Deficient neurotrophic support in the aetiology of diabetic neuropathy. Diabet. Med. 13, 679-681.
45. Tsai G., Stauch B. L., Vomov J. J., Deshpande J. K. and Coyle J. T. (1990) Selective release of N-acetylaspartylglutamate from rat optic nerve terminals in vivo. Brain Res. 518, 313-316.
46. Valivullah H. M., Lancaster J., Sweetnam P. M. and Neale J. H. (1994) Interactions between N-acetylaspartylglutamate and AMPA, kainate, and NMDA binding sites. J. Neurochem. 63, 1714-1719.
47. Vincent A. M. and Maiese K. (2000) The metabotropic glutamate system promotes neuronal survival through distinct pathways of programmed cell death. Exp. Neurol. 166, 65-82.
48. Vincent A. M., Brownlee M. and Russell J. W. (2002) Oxidative stress and programmed cell death in diabetic neuropathy. Ann. NY Acad. Sci. 959, 368-383.
49. Wroblewska B., Wroblewski J. T., Pshenichkin S., Surin A., Sullivan S. E. and Neale J. H. (1997) N-Acetylaspartylglutamate selectively activates mGluR3 receptors in transfected cells. J. Neurochem. 69, 174-181.
50. Wroblewska B., Wroblewski J. T., Saab O. H. and 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.