Neurones express glutamine synthetase when deprived of glutamine or interaction with astrocytes

Journal of Neurochemistry

Volumn 114, Issue 5, 2010, Pages 1527-1536

  Fernandes, Samantha P ^a   Dringen, Ralf ^a,b   Lawen, Alfons ^a   Robinson, Stephen R ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF BREMEN   (Germany)

Author keywords

Alzheimer's disease; cerebellar granule cell; Glia

Indexed keywords

GLUTAMATE AMMONIA LIGASE; GLUTAMINE;

ANIMAL CELL; ANTIBODY LABELING; ARTICLE; ASTROCYTE; CONTROLLED STUDY; ENZYME ACTIVITY; GRAY MATTER; IMMUNOHISTOCHEMISTRY; INCUBATION TIME; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; WESTERN BLOTTING;

ANIMALS; ASTROCYTES; CELL COMMUNICATION; CELLS, CULTURED; COCULTURE TECHNIQUES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUTAMATE-AMMONIA LIGASE; GLUTAMINE; NEURONS; PHENOTYPE; RATS; RATS, WISTAR;

RATTUS;

EID: 77955127868     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06869.x     Document Type: Article

References (62)

1. Albrecht J. Wegrzynowicz M. (2005) Endogenous neuro-protectants in ammonia toxicity in the central nervous system: facts and hypotheses. Metab. Brain Dis. 20, 253 263.
2. Albrecht J., Sonnewald U., Waagepetersen H. S. Schousboe A. (2007) Glutamine in the central nervous system: function and dysfunction. Front Biosci. 12, 332 343.
3. de Almeida L. M., Pineiro C. C., Leite M. C., Brolese G., Tramontina F., Feoli A. M., Gottfried C. Goncalves C. A. (2007) Resveratrol increases glutamate uptake, glutathione content, and S100B secretion in cortical astrocyte cultures. Cell. Mol. Neurobiol. 27, 661 668.
4. Arad G. Kulka R. G. (1978) Effects of glutamine, methionine sulfone and dexamethasone on rates of synthesis of glutamine synthetase in cultured hepatoma cells. Biochim. Biophys. Acta 544, 153 162.
5. Bak L. K., Schousboe A. Waagepetersen H. S. (2006) The glutamate/GABA-glutamine cycle: aspects of transport, neurotransmitter homeostasis and ammonia transfer. J. Neurochem. 98, 641 653.
6. Barakat-Walter I. Droz B. (1990) Glutamine synthetase is expressed by primary sensory neurons from chick embryos in vitro but not in vivo: influence of skeletal muscle extract. Eur. J. Neurosci. 2, 836 844.
7. Bradford M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248 254.
8. Brasse-Lagnel C., Lavoinne A. Husson A. (2009) Control of mammalian gene expression by amino acids, especially glutamine. FEBS J. 276, 1826 1844.
9. Butterfield D. A., Hensley K., Cole P., Subramaniam R., Aksenov M., Aksenova M., Bummer P. M., Haley B. E. Carney J. M. (1997) Oxidatively induced structural alteration of glutamine synthetase assessed by analysis of spin label incorporation kinetics: relevance to Alzheimer's disease. J. Neurochem. 68, 2451 2457.
10. Castegna A., Aksenov M., Aksenova M., Thongboonkerd V., Klein J. B., Pierce W. M., Booze R., Markesbery W. R. Butterfield D. A. (2002) Proteomic identification of oxidatively modified proteins in Alheimer's disease brain. Part I: Creatine kinse BB, glutamine synthase, and ubiquitin carboy-terminal hydrolase L-1. Free Radic. Biol. Med. 33, 562 571.
11. Charriere-Bertrand C., Garner C., Tardy M. Nunez J. (1991) Expression of various microtubule-associated protein 2 forms in the developing mouse brain and in cultured neurons and astrocytes. J. Neurochem. 56, 385 391.
12. Chen W., Aoki C., Mahadomrongkul V., Gruber C. E., Wang G. J., Blitzblau R., Irwin N. Rosenberg P. A. (2002) Expression of a variant form of the glutamate transporter GLT1 in neuronal cultures and in neurons and astrocytes in the rat brain. J. Neurosci. 22, 2142 2152.
13. Cheung N. S., Carroll F. Y., Larm J. A., Beart P. M. Giardina S. F. (1998) Kainate-induced apoptosis correlates with c-Jun activation in cultured cerebellar granule cells. J. Neurosci. Res. 52, 69 82.
14. Couchie D., Fages C., Bridoux A. M., Rolland B., Tardy M. Nunez J. (1985) Microtubule-associated proteins and in vitro astrocyte differentiation. J. Cell Biol. 101, 2095 2103.
15. Csernansky J. G., Bardgett M. E., Sheline Y. I., Morris J. C. Olney J. W. (1996) CSF excitatory amino acids and severity of illness in Alzheimer's disease. Neurology 46, 1715 1720.
16. Curi R., Lagranha C. J., Doi S. Q., Sellitti D. F., Procopio J., Pithon-Curi T. C., Corless M. Newsholme P. (2005) Molecular mechanisms of glutamine action. J. Cell. Physiol. 204, 392 401.
17. Daniels M. Brown D. R. (2002) High extracellular potassium protects against the toxicity of cytosine arabinoside but is not required for the survival of cerebellar granule cells in vitro. Mol. Cell. Neurosci. 19, 281 291.
18. Deuel T. F. Prusiner S. (1974) Regulation of glutamine synthetase from Bacillus subtilis by divalent cations, feedback inhibitors, and l-glutamine. J. Biol. Chem. 249, 257 264.
19. Dolinska M., Zablocka B., Sonnewald U. Albrecht J. (2004) Glutamine uptake and expression of mRNA's of glutamine transporting proteins in mouse cerebellar and cerebral cortical astrocytes and neurons. Neurochem. Int. 44, 75 81.
20. Drejer J., Larsson O. M., Kvamme E., Svenneby G., Hertz L. Schousboe A. (1985) Ontogenetic development of glutamate metabolizing enzymes in cultured cerebellar granule cells and in cerebellum in vivo. Neurochem. Res. 10, 49 62.
21. Edwards M. M. Robinson S. R. (2006) TNF alpha affects the expression of GFAP and S100B: implications for Alzheimer's disease. J. Neural Transm. 113, 1709 1715.
22. Furness D. N., Dehnes Y., Akhtar A. Q. et al. (2008) 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 157, 80 94.
23. Gundersen V., Danbolt N. C., Ottersen O. P. Storm-Mathisen J. (1993) Demonstration of glutamate/aspartate uptake activity in nerve endings by use of antibodies recognizing exogenous d-aspartate. Neuroscience 57, 97 111.
24. Hamprecht B. Löffler F. (1985) Primary glial cultures as a model for studying hormone action. Methods Enzymol. 109, 341 345.
25. Hertz L., Dringen R., Schousboe A. Robinson S. R. (1999) Astrocytes: glutamate producers for neurons. J. Neurosci. Res. 57, 417 428.
26. Huang Y. F., Wang Y. Watford M. (2007) Glutamine directly downregulates glutamine synthetase protein levels in mouse C2C12 skeletal muscle myotubes. J. Nutr. 137, 1357 1362.
27. Jimenez-Jimenez F. J., Molina J. A., Gomez P. et al. (1998) Neurotransmitter amino acids in cerebrospinal fluid of patients with Alzheimer's disease. J. Neural Transm. 105, 269 277. (Pubitemid 28243234)
28. Kaiser L. G., Schuff N., Cashdollar N. Weiner M. W. (2005) Age-related glutamate and glutamine concentration changes in normal human brain: 1H MR spectroscopy study at 4 T. Neurobiol. Aging 26, 665 672.
29. Kanamori K. Ross B. D. (2004) Quantitative determination of extracellular glutamine concentration in rat brain, and its elevation in vivo by system A transport inhibitor, alpha-(methylamino)isobutyrate. J. Neurochem. 90, 203 210.
30. Knorpp T., Robinson S. R., Crack P. J. Dringen R. (2006) Glutathione peroxidase-1 contributes to the protection of glutamine synthetase in astrocytes during oxidative stress. J. Neural Transm. 113, 1145 1155.
31. Kosenko E., Llansola M., Montoliu C., Monfort P., Rodrigo R., Hernandez-Viadel M., Erceg S., Sanchez-Perez A. M. Felipo V. (2003) Glutamine synthetase activity and glutamine content in brain: modulation by NMDA receptors and nitric oxide. Neurochem. Int. 43, 493 499.
32. Laemmli U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680 685.
33. Lauderback C. M., Hackett J. M., Huang F. F., Keller J. N., Szweda L. I., Markesbery W. R. Butterfield D. A. (2001) The glial glutamate transporter, GLT-1, is oxidatively modified by 4-hydroxy-2-nonenal in the Alzheimer's disease brain: the role of Abeta1-42. J. Neurochem. 78, 413 416.
34. Le Prince G., Delaere P., Fages C., Lefrancois T., Touret M., Salanon M. Tardy M. (1995) Glutamine synthetase (GS) expression is reduced in senile dementia of the Alzheimer type. Neurochem. Res. 20, 859 862.
35. Li S., Mallory M., Alford M., Tanaka S. Masliah E. (1997) Glutamate transporter alterations in Alzheimer disease are possibly associated with abnormal APP expression. J. Neuropathol. Exp. Neurol. 56, 901 911.
36. Lowry O. H., Rosebrough N. J., Farr A. L. Randall R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265 275.
37. Martinez-Hernandez A., Bell K. P. Norenberg M. D. (1977) Glutamine synthetase: glial localization in brain. Science 195, 1356 1358.
38. Masliah E., Alford M., DeTeresa R., Mallory M. Hansen L. (1996) Deficient glutamate transport is associated with neurodegeneration in Alzheimer's disease. Ann. Neurol. 40, 759 766.
39. Melone M., Bellesi M. Conti F. (2009) Synaptic localization of GLT-1a in the rat somatic sensory cortex. Glia 57, 108 117.
40. Mennerick S., Dhond R. P., Benz A., Xu W., Rothstein J. D., Danbolt N. C., Isenberg K. E. Zorumski C. F. (1998) Neuronal expression of the glutamate transporter GLT-1 in hippocampal microcultures. J. Neurosci. 18, 4490 4499.
41. Murin R., Mohammadi G., Leibfritz D. Hamprecht B. (2009) Glial metabolism of isoleucine. Neurochem. Res. 34, 194 204.
42. Norenberg M. D. Martinez-Hernandez A. (1979) Fine structural localization of glutamine synthetase in astrocytes of rat brain. Brain Res. 161, 303 310.
43. O'Dowd B. S., Ng K. T. Robinson S. R. (1997) Distribution of glutamine synthetase in the chick forebrain: implications for passive avoidance memory formation. J. Hirnforsch. 38, 147 152.
44. Pow D. V. Cook D. G. (2009) Neuronal expression of splice variants of "glial" glutamate transporters in brains afflicted by Alzheimer's disease: unmasking an intrinsic neuronal property. Neurochem. Res. 34, 1748 1757.
45. Proper E. A., Hoogland G., Kappen S. M. et al. (2002) Distribution of glutamate transporters in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy. Brain, 125, 32 43.
46. Redjems-Bennani N., Jeandel C., Lefebvre E., Blain H., Vidailhet M. Gueant J. L. (1998) Abnormal substrate levels that depend upon mitochondrial function in cerebrospinal fluid from Alzheimer patients. Gerontology, 44, 300 304.
47. Renis M., Cardile V., Russo A., Campisi A. Collova F. (1998) Glutamine synthetase activity and HSP70 levels in cultured rat astrocytes: effect of 1-octadecyl-2-methyl-rac-glycero-3-phosphocholine. Brain Res. 783, 143 150.
48. Robinson S. R. (2000) Neuronal expression of glutamine synthetase in Alzheimer's disease indicates a profound impairment of metabolic interactions with astrocytes. Neurochem. Int. 36, 471 482.
49. Robinson S. R. (2001) Changes in the cellular distribution of glutamine synthetase in Alzheimer's disease. J. Neurosci. Res. 66, 972 980.
50. Ronzio R. A., Rowe W. B. Meister A. (1969) Studies on the mechanism of inhibition of glutamine synthetase by methionine sulfoximine. Biochemistry 8, 1066 1075.
51. Rowe W. B., Ronzio R. A. Meister A. (1969) Inhibition of glutamine synthetase by methionine sulfoximine. Studies on methionine sulfoximine phosphate. Biochemistry 8, 2674 2680.
52. Santoro J. C., Harris G. Sitlani A. (2001) Colorimetric detection of glutamine synthetase-catalyzed transferase activity in glucocorticoid-treated skeletal muscle cells. Anal. Biochem. 289, 18 25.
53. Smith C. C., Bowen D. M., Francis P. T., Snowden J. S. Neary D. (1985) Putative amino acid transmitters in lumbar cerebrospinal fluid of patients with histologically verified Alzheimer's dementia. J. Neurol. Neurosurg. Psychiatry 48, 469 471.
54. Smith C. D., Carney J. M., Starke-Reed P. E., Oliver C. N., Stadtman E. R., Floyd R. A. Markesbery W. R. (1991) Excess brain protein oxidation and enzyme dysfunction in normal aging and in Alzheimer disease. Proc. Natl Acad. Sci. USA 88, 10540 10543.
55. Stafford M. M., Brown M. N., Mishra P., Stanwood G. D. Mathews G. C. (2010) Glutamate spillover augments GABA synthesis and release from axodendritic synapses in rat hippocampus. Hippocampus 20, 134 144.
56. Stanimirovic D. B., Ball R., Small D. L. Muruganandam A. (1999) Developmental regulation of glutamate transporters and glutamine synthetase activity in astrocyte cultures differentiated in vitro. Int. J. Dev. Neurosci. 17, 173 184.
57. Su T. Z., Campbell G. W. Oxender D. L. (1997) Glutamine transport in cerebellar granule cells in culture. Brain Res. 757, 69 78.
58. 2+ interactions. Neurochem. Res. 12, 1041 1047.
59. Tholey G., Ghandour M. S., Bloch S., Ledig M. Mandel P. (1987b) Glutamine synthetase and energy metabolism enzymes in cultivated chick neurons and astrocytes: modulation by serum and hydrocortisone. Brain Res. 428, 73 81.
60. Varoqui H., Zhu H., Yao D., Ming H. Erickson J. D. (2000) Cloning and functional identification of a neuronal glutamine transporter. J. Biol. Chem. 275, 4049 4054.
61. Villafranca J. J., Ash D. E. Wedler F. C. (1975) Evidence for methionine sulfoximine as a transition-state analog for glutamine synthetase from NMR and EPR data. Biochem. Biophys. Res. Commun. 66, 1003 1010.
62. Wang Y. Watford M. (2007) Glutamine, insulin and glucocorticoids regulate glutamine synthetase expression in C2C12 myotubes, Hep G2 hepatoma cells and 3T3 L1 adipocytes. Biochim. Biophys. Acta 1770, 594 600.