Inhibitors of glutamate dehydrogenase block sodium-dependent glutamate uptake in rat brain membranes

Frontiers in Endocrinology

Volumn 4, Issue SEP, 2013, Pages

  Whitelaw, Brendan S ^a   Robinson, Michael B ^a,b  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

EAAT2; Epigallocatechin monogallate; GABA; GLAST; GLT 1; Glutamate; Glutamate dehydrogenase; Sodium dependent uptake

Indexed keywords

EID: 84885998103     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2013.00123     Document Type: Article

References (69)

1. Sheng M, Hoogenraad CC. The postsynaptic architecture of excitatory synapses:a more quantitative view. Annu Rev Biochem (2007) 76:823-47. doi:10.1146/annurev.biochem.76.060805.160029.
2. Doble A. The role of excitotoxicity in neurodegenerative disease:implications for therapy. Pharmacol Ther (1999) 81:163-221. doi:10.1016/S0163-7258(98)00042-4.
3. Olney J. Excitotoxicity, apoptosis and neuropsychiatric disorders. Curr Opin Pharmacol (2003) 3:101-9. doi:10.1016/S1471489202000024.
4. Sims KD, Robinson MB. Expression patterns and regulation of glutamate transporters in the developing and adult nervous system. Crit Rev Neurobiol (1999) 13:169-97.
5. Danbolt NC. Glutamate uptake. Prog Neurobiol (2001) 65:1-105. doi:10.1016/S0301-0082(00)00067-8.
6. Sheldon AL, Robinson MB. The role of glutamate transporters in neurodegenerative diseases and potential opportunities for intervention. Neurochem Int (2007) 51:333-55. doi:10.1016/j.neuint.2007.03.012.
7. Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M, Jin L, Wu D, et al. Localization of neuronal and glial glutamate transporters. Neuron (1994) 13:713-25. doi:10.1016/0896-6273(94)90038-8.
8. Chen W, Mahadomrongkul V, Berger UV, Bassan M, Desilva T, Tanaka K, et al. The glutamate transporter GLT1a is expressed in excitatory terminals of mature hippocampal neurons. J Neurosci (2004) 24:1136-48. doi:10.1523/JNEUROSCI.1586-03.2004.
9. Tanaka K, Watase K, Manabe T, Yamada K, Watanabe M, Takahashi K, et al. Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science (1997) 276:1699-702. doi:10.1126/science.276.5319.1699.
10. Robinson MB. The family of sodium-dependent glutamate transporters:a focus on the GLT-1/EAAT2 subtype. Neurochem Int (1999) 33:479-91. doi:10.1016/S0197-0186(98)00055-2.
11. Torres GE, Gainetdinov RR, Caron MG. Plasma membrane monoamine transporters:structure, regulation and function. Nat Rev Neurosci (2003) 4:13-25. doi:10.1038/nrn1008.
12. Gether U, Andersen PH, Larsson OM, Schousboe A. Neurotransmitter transporters:molecular function of important drug targets. Trends Pharmacol Sci (2006) 27:375-83. doi:10.1016/j.tips.2006.05.003.
13. Zerangue N, Kavanaugh MP. Flux coupling in a neuronal glutamate transporter. Nature (1996) 383:634-7. doi:10.1038/383634a0.
14. Attwell D, Gibb A. Neuroenergetics and the kinetic design of excitatory synapses. Nat Rev Neurosci (2005) 6:841-9. doi:10.1038/nrn1784.
15. Chaudhry FA, Lehre KP, Campagne MVL, Ottersen OP, Danbolt NC, Storm-Mathisen J. Glutamate transporters in glial plasma membranes:highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron (1995) 15:711-20. doi:10.1016/0896-6273(95)90158-2.
16. Lehre KP, Levy LM, Ottersen OP, Storm-Mathisen J, Danbolt NC. Differential expression of two glial glutamate transporters in the rat brain:quantitative and immunocytochemical observations. J Neurosci (1995) 15:1835-53.
17. Genda EN, Jackson JG, Sheldon AL, Locke SF, Greco TM, O'Donnell JC, et al. Co-compartmentalization of the astroglial glutamate transporter, GLT-1, with glycolytic enzymes and mitochondria. J Neurosci (2011) 31:18275-88. doi:10.1523/JNEUROSCI.3305-11.2011.
18. Rose EM, Koo JC, Antflick JE, Ahmed SM, Angers S, Hampson DR. Glutamate transporter coupling to Na, K-ATPase. J Neurosci (2009) 29:8143-55. doi:10.1523/JNEUROSCI.1081-09.2009.
19. Bauer DE, Jackson JG, Genda EN, Montoya MM, YudkoffM, Robinson MB. The glutamate transporter, GLAST, participates in a macromolecular complex that supports glutamate metabolism. Neurochem Int (2012) 61:566-74.
20. Robinson MB, Hunter-Ensor M, Sinor J. Pharmacologically distinct sodium-dependent L-[3H]glutamate transport processes in rat brain. Brain Res (1991) 544:196-202. doi:10.1016/0006-8993(91)90054-Y.
21. Li C, Allen A, Kwagh J, Doliba NM, Qin W, NajafiH, et al. Green tea polyphenols modulate insulin secretion by inhibiting glutamate dehydrogenase. J Biol Chem (2006) 281:10214-21. doi:10.1074/jbc. M512792200.
22. Swanson RA, Liu J, Miller JW, Rothstein JD, Farrell K, Stein BA, et al. Neuronal regulation of glutamate transporter subtype expression in astrocytes. J Neurosci (1997) 17:932-40.
23. Schlag BD, Vondrasek JR, Munir M, Kalandadze A, Zelenaia OA, Rothstein JD, et al. Regulation of the glial Na+-dependent glutamate transporters by cyclic AMP analogs and neurons. Mol Pharmacol (1998) 53:355-69.
24. Arriza JL, Fairman WA, Wadiche JI, Murdoch GH, Kavanaugh MP, Amara SG. Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J Neurosci (1994) 14:5559-69.
25. Henn FA, Anderson DJ, Rustad DG. Glial contamination of synaptosomal fractions. Brain Res (1976) 101:341-4. doi:10.1016/0006-8993(76)90274-2.
26. Gylys KH, Fein JA, Cole GM. Quantitative characterization of crude synaptosomal fraction (P-2) components by flow cytometry. J Neurosci Res (2000) 61:186-92. doi:10.1002/1097-4547(20000715)61:2<186::AID-JNR9>3.0.CO;2-X.
27. Fuchs E, Weber K. Intermediate filaments:structure, dynamics, function, and disease. Annu Rev Biochem (1994) 63:345-82. doi:10.1146/annurev.bi.63.070194.002021.
28. Li M, Allen A, Smith TJ. High throughput screening reveals several new classes of glutamate dehydrogenase inhibitors. Biochemistry (2007) 46:15089-102. doi:10.1021/bi7018783.
29. Hong J, Lu H, Meng X, Ryu JH, Hara Y, Yang CS. Stability, cellular uptake, biotransformation, and efflux of tea polyphenol (-)-epigallocatechin-3-gallate in HT-29 human colon adenocarcinoma cells. Cancer Res (2002) 62:7241-6.
30. Li M, Smith CJ, Walker MT, Smith TJ. Novel inhibitors complexed with glutamate dehydrogenase:allosteric regulation by control of protein dynamics. J Biol Chem (2009) 284:22988-3000. doi:10.1074/jbc. M109.020222.
31. Robinson MB, Dowd LA. Heterogeneity and functional properties of subtypes of sodium-dependent glutamate transporters in the mammalian central nervous system. Adv Pharmacol (1997) 37:69-115. doi:10.1016/S1054-3589(08)60948-5.
32. Ferkany J, Coyle JT. Heterogeneity of sodium-dependent excitatory amino acid uptake mechanisms in rat brain. J Neurosci Res (1986) 16:491-503. doi:10.1002/jnr.490160305.
33. Fosse VM, Kolstad J, Fonnum F. A bioluminescence method for the measurement of L-glutamate:applications to the study of changes in the release of L-glutamate from lateral geniculate nucleus and superior colliculus after visual cortex ablation in rats. J Neurochem (1986) 47:340-9. doi:10.1111/j.1471-4159.1986.tb04507.x.
34. Schousboe I, Bro B, Schousboe A. Intramitochondrial localization of the 4-aminobutyrate-2-oxoglutarate transaminase from ox brain. Biochem J (1977) 162:303-7.
35. Kreft M, Bak LK, Waagepetersen HS, Schousboe A. Aspects of astrocyte energy metabolism, amino acid neurotransmitter homoeostasis and metabolic compartmentation. ASN Neuro (2012) 4:187-99. doi:10.1042/AN20120007.
36. Zhong Y, Chiou YS, Pan MH, Shahidi F. Anti-inflammatory activity of lipophilic epigallocatechin gallate (EGCG) derivatives in LPS-stimulated murine macrophages. Food Chem (2012) 134:742-8. doi:10.1016/j.foodchem.2012.02.172.
37. Li C, Li M, Chen P, Narayan S, Matschinsky FM, Bennett MJ, et al. Green tea polyphenols control dysregulated glutamate dehydrogenase in transgenic mice by hijacking the ADP activation site. J Biol Chem (2011) 286:34164-74. doi:10.1074/jbc. M111.268599.
38. Nelson N. The family of Na+/Cl- neurotransmitter transporters. J Neurochem (1998) 71:1785-803. doi:10.1046/j.1471-4159.1998.71051785.x.
39. Garlin AB, Sinor AD, Sinor JD, Jee SH, Grinspan JB, Robinson MB. Pharmacology of sodium-dependent high-affinity L-[3H]glutamate transport in glial cultures. J Neurochem (1995) 64:2572-80. doi:10.1046/j.1471-4159.1995.64062572.x.
40. Frigerio F, Karaca M, De Roo M, Mlynarik V, Skytt DM, Carobbio S, et al. Deletion of glutamate dehydrogenase 1 (Glud1) in the central nervous system affects glutamate handling without altering synaptic transmission. J Neurochem (2012) 123:342-8. doi:10.1111/j.1471-4159.2012.07933.x.
41. Skytt DM, Klawonn AM, Stridh MH, Pajecka K, Patruss Y, Quintana-Cabrera R, et al. siRNA knock down of glutamate dehydrogenase in astrocytes affects glutamate metabolism leading to extensive accumulation of the neuroactive amino acids glutamate and aspartate. Neurochem Int (2012) 61:490-7. doi:10.1016/j.neuint.2012.04.014.
42. Demarque M, Villeneuve N, Manent JB, Becq H, Represa A, Ben-Ari Y, et al. Glutamate transporters prevent the generation of seizures in the developing rat neocortex. J Neurosci (2004) 24:3289-94. doi:10.1523/JNEUROSCI.5338-03.2004.
43. Shimamoto K, Sakai R, Takaoka K, Yumoto N, Nakajima T, Amara SG, et al. Characterization of novel L-threo-β-benzyloxy aspartate derivatives, potent blockers of the glutamate transporters. Mol Pharmacol (2004) 65:1008-15. doi:10.1124/mol.65.4.1008.
44. Schousboe A, Westergaard N, Sonnewald U, Petersen SB, Huang R, Peng L, et al. Glutamate and glutamine metabolism and compartmentation in astrocytes. Dev Neurosci (1993) 15:359-66. doi:10.1159/000111356.
45. McKenna MC. The glutamate-glutamine cycle is not stoichiometric:fates of glutamate in brain. J Neurosci Res (2007) 85:3347-58. doi:10.1002/jnr.21444.
46. Torp R, Danbolt NC, Babaie E, Bjoras M, Seeberg E, Storm-Mathisen J, et al. Differential expression of two glial glutamate transporters in the rat brain:an in situ hybridization study. Eur J Neurosci (1994) 6:936-42. doi:10.1111/j.1460-9568.1994.tb00587.x.
47. Schmitt A, Asan E, Puschel B, Jons T, Kugler P. Expression of the glutamate transporter GLT1 in neural cells of the rat central nervous system:non-radioactive in situ hybridization and comparative immunocytochemistry. Neuroscience (1996) 71:989-1004. doi:10.1016/0306-4522(95)00477-7.
48. Regan MR, Huang YH, Kim YS, Dykes-Hoberg MI, Jin L, Watkins AM, et al. Variations in promoter activity reveal a differential expression and physiology of glutamate transporters by glia in the developing and mature CNS. J Neurosci (2007) 27:6607-19. doi:10.1523/JNEUROSCI.0790-07.2007.
49. Furness DN, Dehnes Y, Akhtar AQ, Rossi DJ, Hamann M, Grutle NJ, et al. A quantitative assessment of glutamate uptake into hippocampal synaptic terminals and astrocytes:new insights into a neuronal role for excitatory amino acid transporter 2 (EAAT2). Neuroscience (2008) 157:80-94. doi:10.1016/j.neuroscience.2008.08.043.
50. Sutch RJ, Davies CC, Bowery NG. GABA release and uptake measured in crude synaptosomes from genetic absence epilepsy rats from Strasbourg (GAERS). Neurochem Int (1999) 34:415-25. doi:10.1016/S0197-0186(99)00046-7.
51. Ghasemi A, Sadidi A, Mohammadi M, Khoshbaten A, Asgari A. Paraoxon inhibits GABA uptake in brain synaptosomes. Toxicol In vitro (2007) 21:1499-504. doi:10.1016/j.tiv.2007.06.009.
52. Borden LA. GABA transporter heterogeneity:pharmacology and cellular localization. Neurochem Int (1996) 29:335-56. doi:10.1016/0197-0186(95)00158-1.
53. Plaitakis A, Zaganas I. Regulation of human glutamate dehydrogenases:implications for glutamate, ammonia and energy metabolism in brain. J Neurosci Res (2001) 66:899-908. doi:10.1002/jnr.10054.
54. Li M, Li C, Allen A, Stanley CA, Smith TJ. The structure and allosteric regulation of mammalian]. Arch Biochem Biophys (2012) 519:69-80. doi:10.1016/j.abb.2011.10.015.
55. Palmieri L, Pardo B, Lasorsa FM, Del Arco A, Kobayashi K, Iijima M, et al. Citrin and aralar1 are Ca(2+)-stimulated aspartate/glutamate transporters in mitochondria. EMBO J (2001) 20:5060-9. doi:10.1093/emboj/20.18.5060.
56. Fiermonte G, Palmieri L, Todisco S, Agrimi G, Palmieri F, Walker JE. Identification of the mitochondrial glutamate transporter. Bacterial expression, reconstitution, functional characterization, and tissue distribution of two human isoforms. J Biol Chem (2002) 277:19289-94. doi:10.1074/jbc. M201572200.
57. Erecinska M, Zaleska MM, Nissim I, Nelson D, Dagani F, YudkoffM. Glucose and synaptosomal glutamate metabolism:studies with [15N]glutamate. J Neurochem (1988) 51:892-902. doi:10.1111/j.1471-4159.1988.tb01826.x.
58. Swanson RA, Farrell K, Simon RP. Acidosis causes failure of astrocyte glutamate uptake during hypoxia. J Cereb Blood Flow Metab (1995) 15:417-24. doi:10.1038/jcbfm.1995.52.
59. Di Monte DA, Tokar I, Langston JW. Impaired glutamate clearance as a consequence of energy failure caused by MPP(+) in astrocytic cultures. Toxicol Appl Pharmacol (1999) 158:296-302. doi:10.1006/taap.1999.8717.
60. Yang YL, Meng CH, Ding JH, He HR, Ellsworth K, Wu J, et al. Iptakalim hydrochloride protects cells against neurotoxin-induced glutamate transporter dysfunction in in vitro and in vivo models. Brain Res (2005) 1049:80-8. doi:10.1016/j.brainres.2005.04.073.
61. Sun XL, Zeng XN, Zhou F, Dai CP, Ding JH, Hu G. KATP channel openers facilitate glutamate uptake by GluTs in rat primary cultured astrocytes. Neuropsychopharmacology (2008) 33:1336-42. doi:10.1038/sj.npp.1301501.
62. Bernardinelli Y, Azarias G, Chatton JY. In situ fluorescence imaging of glutamate-evoked mitochondrial Na+ responses in astrocytes. Glia (2006) 54:460-70. doi:10.1002/glia.20387.
63. Azarias G, Perreten H, Lengacher S, Poburko D, Demaurex N, Magistretti PJ, et al. Glutamate transport decreases mitochondrial pH and modulates oxidative metabolism in astrocytes. J Neurosci (2011) 31:3550-9. doi:10.1523/JNEUROSCI.4378-10.2011.
64. Mandel S, Youdim MB. Catechin polyphenols:neurodegeneration and neuroprotection in neurodegenerative diseases. Free Radic Biol Med (2004) 37:304-17. doi:10.1016/j.freeradbiomed.2004.04.012.
65. Haque AM, Hashimoto M, Katakura M, Tanabe Y, Hara Y, Shido O. Long-term administration of green tea catechins improves spatial cognition learning ability in rats. J Nutr (2006) 136:1043-7.
66. Renno WM, Al-Maghrebi M, Alshammari A, George P. (-)-Epigallocatechin-3-gallate (EGCG) attenuates peripheral nerve degeneration in rat sciatic nerve crush injury. Neurochem Int (2013) 62:221-31. doi:10.1016/j.neuint.2012.12.018.
67. Lee S, Suh S, Kim S. Protective effects of the green tea polyphenol (-)-epigallocatechin gallate against hippocampal neuronal damage after transient global ischemia in gerbils. Neurosci Lett (2000) 287:191-4. doi:10.1016/S0304-3940(00)01159-9.
68. Levites Y, Amit T, Youdim MB, Mandel S. Involvement of protein kinase C activation and cell survival/cell cycle genes in green tea polyphenol (-)-epigallocatechin 3-gallate neuroprotective action. J Biol Chem (2002) 277:30574-80. doi:10.1074/jbc. M202832200.
69. Chou CW, Huang WJ, Tien LT, Wang SJ. (-)-Epigallocatechin gallate, the most active polyphenolic catechin in green tea, presynaptically facilitates Ca2+-dependent glutamate release via activation of protein kinase C in rat cerebral cortex. Synapse (2007) 61:889-902. doi:10.1002/syn.20444.