Excitotoxic neonatal damage induced by monosodium glutamate reduces several GABAergic markers in the cerebral cortex and hippocampus in adulthood

International Journal of Developmental Neuroscience

Volumn 27, Issue 8, 2009, Pages 845-855

  Ureña Guerrero, Mónica E ^a   Orozco Suárez, Sandra ^b   López Pérez, Silvia J ^a   Flores Soto, Mario E ^a   Beas Zárate, Carlos ^a,c  

^a UNIVERSITY OF GUADALAJARA   (Mexico)

^b INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^c CENTRO DE INVESTIGACIÓN BIOMÉDICA DE OCCIDENTE   (Mexico)

Author keywords

Cerebral cortex; Excitotoxicity; GABA uptake; GABA positive cells; GAD65; GAD67; GAT 1; GAT 3; Hippocampus; Monosodium glutamate

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID CARRIER; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; GLUTAMATE SODIUM; MESSENGER RNA;

ADULTHOOD; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DAMAGE; CONTROLLED STUDY; EXCITOTOXICITY; GABAERGIC TRANSMISSION; GENE EXPRESSION; HIPPOCAMPUS; MALE; NERVE DEGENERATION; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; ANIMALS, NEWBORN; CEREBRAL CORTEX; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; HIPPOCAMPUS; MALE; RADIOLIGAND ASSAY; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; SODIUM GLUTAMATE;

RATTUS;

EID: 70449699655     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2009.07.011     Document Type: Article

References (83)

1. Akbar M.T., Rattray M., Williams R.J., Chong N.W.S., and Meldrum B.S. Reduction of GABA and glutamate transporter messenger RNAs in the severe-seizure genetically epilepsy-prone rat. Neuroscience 85 (1998) 1235-1251
2. Amaral D.G., and Kurz J. The time of origin of cells demonstrating glutamic acid decarboxylase-like immunoreactivity in the hippocampal formation of the rat. Neurosci. Lett. 59 (1985) 33-39
3. Bahn S., Volk B., and Wisden W. Kainate receptor gene expression in the developing rat brain. J. Neurosci. 14 (1994) 5525-5547
4. Bain G., Ramkumar T.P., Cheng J.M., and Gottlieb D.I. Expression of the genes coding for glutamic acid decaboxilase in pluripotent cell lines. Mol. Brain Res. 17 (1993) 23-30
5. Balland B., Lachamp P., Kessler J.P., and Tell F. Silent synapses in developing rat nucleus tractus solitarii have AMPA receptors. J. Neurosci. 28 (2008) 4624-4634
6. Beas-Zárate C., Sánchez-Ruíz M.Y., Ureña-Guerrero M.E., and Feria-Velasco A. Effect of neonatal exposure to monosodium l-glutamate on regional GABA release during postnatal development. Neurochem. Int. 33 (1998) 217-232
7. Beas-Zárate C., Ureña-Guerrero M.E., Flores-Soto M., Armendariz-Borunda J., and Ortuño-Sahagun D. The expression and binding of kainate receptors is modified in different brain regions by glutamate neurotoxicity during postnatal rat development. Int. J. Dev. Neurosci. 25 (2007) 53-61
8. Ben-Ari Y. Developing networks play a similar melody. Trends Neurosci. 24 (2001) 353-360
9. Bernal F., Andres N., Samuel D., Kerkerian-LeGoff L., and Mahy N. Age-related resistance to alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid-induced hippocampal lesion. Hippocampus 10 (2000) 296-304
10. Borden L.A., Smith K.E., Harting P.R., Branchek T.A., and Weinshank R.L. Molecular heterogeneity of the gamma-aminobutyric acid (GABA) transport system. Cloning of two novel high affinity GABA transporters from rat brain. J. Biol. Chem. 267 (1992) 21098-21104
11. Boutz P.L., Stoilov P., Li Q., Lin C.H., Chawla G., Onstrow K., Shiue L., Ares Jr. A., and Black D.L. A post-transcriptional regulatory switch in polypyrimidine tract-binging proteins reprograms alternative splicing in developing neurons. Genes Dev. 21 (2007) 1636-1652
12. Bubenikova-Valesova V., Balcar V.J., Tejkalova H., Langmeier M., and Stastny F. Neonatal administration of N-acetyl-l-aspartyl-l-glutamate induces early neurodegeneration in hippocampus and alters behaviour in young adult rats. Neurochem. Int. 48 (2006) 515-522
13. Chaparro-Huerta V., Rivera-Cervantes M.C., Torres-Mendoza B.M., and Beas-Zárate C. Neuronal death and tumor necrosis factor-alpha response to glutamate-induced excitotoxicity in the cerebral cortex of neonatal rats. Neurosci. Lett. 333 (2002) 95-98
14. Chomczynski P., and Sacchi N. Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162 (1987) 156-159
15. Conti F., Minelli A., and Melone A. GABA transporters in the mammalian cerebral cortex: localization, development and pathological implications. Brain Res. Rev. 5 (2004) 196-212
16. Dawson Jr. R., Valdes J.J., and Annau Z. High-affinity uptake of hypothalamic neurotransmitters in mice treated neonatally with monosodium glutamate. Neuroendocrinology 34 (1982) 292-296
17. Di Giorgio R.M., De Luca G.C., Garofalo M.P., Conti C., and Ientile R. GABA-ergic system in brain regions of glutamate-lesioned rats. Ital. J. Biochem. 34 (1985) 19-28
18. Diaz-Cintra Y., Gonzalez-Maciel A., Morales M.A., Aguilar A., Cintra L., and Prado-Alcala R. Protein malnutrition differentially alters the Lumber of glutamic acid decarboxilase-67 interneurons in dentate gyrus and CA1-3 subfields of dorsal hippocampus. Exp. Neurol. 2008 (2007) 47-53
19. du Bois T.M., and Huang X.F. Early brain development disruption from NMDA receptor hypofunction: relevance to schizophrenia. Brain Res. Rev. 53 (2007) 260-270
20. Earnheart J.C., Schweizer C., Crestani F., Iwasato T., Itohara S., Mohler H., and Luscher B. GABAergic control of adult hippocampal neurogenesis in relation to behavior indicative of trait anxiety and depression states. J. Neurosci. 27 (2007) 3845-3854
21. Erlander M.G., and Tobin A.J. The structural and functional heterogeneity of glutamic acid decarboxylase: a review. Neurochem. Res. 16 (1991) 215-226
22. Esclapez M., and Houser C.R. Up-regulation of GAD65 and GAD67 in remaining hippocampal GABA neurons in a model of temporal epilepsy. J. Comp. Neurol. 412 (1999) 488-505
23. Frahm C., Haupt C., Weinandy F., Siegel G., Bruehl C., and Witte O.W. Regulation of GABA transporter mRNA and protein after photothrombotic infarct in rat brain. J. Comp. Neurol. 478 (2004) 176-188
24. Franceschetti S., Buzio S., Panzica F., Sancini G., and Avanzani G. Postnatal development of EAA-mediated excitation in rat neocortex. In: Avanzini G., Fariello R., Heinemann U., and Mutani R. (Eds). Epileptogenic and Excitotoxic Mechanisms (1993), John Libbey & Company Ltd., London 107-114
25. Gonchar Y., Wang Q., and Burkhalter A. Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front. Neuroanat. 1 (2008) 1-11
26. Greenamyre J.T., Penney J.B., Young A.B., D'Amato C.J., Hicks S.P., and Shoulson I. Alterations in l-glutamate binding in Alzheimer's and Huntington's diseases. Science 227 (1985) 1496-1499
27. Guastella J., Nelson N., Nelson H., Czyzyk L., Keynan S., Miedel M.C., Davidson N., Lester H.A., and Kanner B.I. Cloning and expression of a rat brain GABA transporter. Science 249 (1990) 1303-1306
28. Gutierrez R., Romo-Parra H., Maqueda J., Vivar C., Ramírez M., Morales M.A., and Lamas M. Plasticity of the GABAergic phenotype of the "glutamatergic" granulle cells of the rat dentate gyrus. J. Neurosci. 23 (2003) 5594-5598
29. Halees A.S., El-Badrwi R., and Khabar K.S.A. ARED organism: expansion of ARED reveals AU-rich element cluster variations between human and mouse. Nucl. Acid Res. 36 Database Issue (2008) D137-D140
30. Hilton G.D., Ndubuizu A., Nunez J.L., and McCarthy M.M. Simultaneous glutamate and GABA(A) receptor agonist administration increases calbindin levels and prevents hippocampal damage induced by either agent alone in a model of perinatal brain injury. Dev. Brain Res. 159 (2005) 99-111
31. Hitzemann R.J., and Loh H.H. High-affinity GABA and glutamate transport in developing nerve ending particles. Brain Res. 159 (1978) 29-40
32. Hua J.Y., and Smith S.J. Neuronal activity and the dynamics of central nervous system development. Nat. Neurosci. 7 (2004) 327-332
33. Huang Z.J., Di Cristo G., and Ango F. Development of GABA innervation in the cerebral and cerebellar cortices. Nat. Rev. Neurosci. 8 (2007) 673-686
34. Insel T.R., Miller L.P., and Gelhard R.E. The ontogeny of excitatory receptors in rat forebrain. I. N-Methyl-d-aspartate and quiscualate receptors. Neuroscience 35 (1990) 45-52
35. Jiao Y., Sun Z., Lee T., Fusco F.R., Kimble T.D., Meade C.A., Cuthberson S., and Reiner A. A simple and sensitive antigen retrieval method for free-floating and slide-mounted tissue sections. J. Neurosci. Meth. 93 (1999) 149-162
36. Kang T.C., Park S.K., Hwang I.K., An S.J., Choi S.Y., Cho S.W., and Won M.H. Spatial and temporal alterations in the GABA shunt in the gerbil hippocampus following transient ischemia. Brain Res. 944 (2002) 10-18
37. Kaufman D.L., Houser C.R., and Tobin A.J. Two forms of the GABA synthetic enzyme glutamate decarboxylase have distinct intraneuronal distributions and cofactor interactions. J. Neurochem. 56 (1991) 720-723
38. Kiser P.J., Cooper N.G.F., and Mower G.D. Expression of two forms of glutamic acid decarboxilase (GAD67 and GAD65) during posntal development of rat somatosensory barrel cortex. J. Comp. Neurol. 402 (1998) 62-74
39. Kobayashi Y., Kaufman D.L., and Tobin A.J. Glutamic acid decarboxylase cDNA: nucleotide sequence encoding an enzymatically active fusion protein. J. Neurosci. 7 (1987) 2768-2772
40. 2+ concentrations in rat hippocampal slices. Epilepsy Res. 4 (1989) 187-200
41. Komuro H., and Rakic P. Modulation of neuronal migration by NMDA receptors. Science 260 (1993) 95-97
42. Kuppers E., Sabolek M., Anders U., Pilgrim C., and Beyer C. Developmental regulation of glutamic decarboxilase mRNA expression and splicing in the rat striatum by dopamine. Mol. Brain Res. 81 (2000) 19-28
43. Lowry O.H., Rosenburgh N.J., Farr A.L., and Randall R.J. Protein measurement with the folin phenol reagent. J. Biol. Chem. 193 (1951) 265-275
44. Lu J.Y., and Schneider R.J. Tissue distribution of AU-rich mRNA-binding proteins involved in regulation of mRNA decay. J. Biol. Chem. 279 (2004) 12974-12979
45. Manent J.B., Demarque M., Jorquera I., Pellegrino C., Ben-Ari Y., Aniksztejn L., and Represa A. A noncanonical release of GABA and glutamate modulates neuronal migration. J. Neurosci. 25 (2005) 4755-4765
46. Maqueda J., Ramírez M., Lamas M., and Gutierrez R. Glutamic acid decarboxylase (GAD)67, but not GAD65, is constitutively expressed during development and transiently overexpressed by activity in the granule cells of the rat. Neurosci. Lett. 353 (2003) 69-71
47. 67 associated with specific pools of GABA in brain?. Dev. Neurobiol. Pespect. 5 (1998) 119-129
48. Martin D.L., and Rimvall K. Regulation of γ-aminobutyric acid synthesis in the brain. J. Neurochem. 60 (1993) 395-407
49. Martinez-Contreras A., Huerta M., López-Pérez S., Garcia-Estrada J., Luquin S., and Beas-Zárate C. Astrocytic and microglia cells reactivity induced by neonatal administration of glutamate in cerebral cortex of the adult rats. J. Neurosci. Res. 67 (2002) 200-210
50. Mattson M.P. Neurotransmitters in the regulation of neuronal cytoarchitecture. Brain Res. Rev. 13 (1988) 179-212
51. Maus M., Glowinski J., and Premont J. GABA is toxic for mouse striatal neurones through a transporter-mediated process. J. Neurochem. 82 (2002) 763-773
52. McLean H.A., Caillard O., Ben-Ari Y., and Gaiarsa J.L. Bidirectional plasticity expressed by GABAergic synapses in the neonatal rat hippocampus. J. Physiol. 496 (1996) 471-477
53. Michaels R.L., and Rothman S.M. Glutamate neurotoxicity in vitro: antagonist pharmacology and intracellular calcium concentrations. J. Neurosci. 10 (1990) 283-292
54. Minelli A., Barbaresi P., and Conti F. Postnatal development of high affinity plasma membrane GABA transporters GAT-2 and GAT-3 in the rat cerebral cortex. Dev. Brain Res. 142 (2003) 7-18
55. Monnerie H., and Le Roux P.D. Glutamate alteration of glutamic acid decarboxilase (GAD) in GABAergic neurons: the role of cysteine proteases. Exp. Neurol. 213 (2008) 145-153
56. Muller G.J., Moller A., and Johansen F.F. Stereological cell counts of GABAergic neurons in rat dentate hilus following transient cerebral ischemia. Exp. Brain Res. 141 (2001) 380-388
57. Nudel U., Zakut R., Shani M., Neuman S., Levy Z., and Yaffe D. The nucleotide sequence of the rat cytoplasmic β-actin gene. Nucl. Acids Res. 11 (1983) 1759-1771
58. Obenaus A., Esclapez M., and Houser C.R. Loss of glutamate decarboxylase mRNA-containing neurons in the rat dentate gyrus following pilocarpine-iduced seizures. J. Neurosci. 13 (1993) 4470-4485
59. Olney J.W. New insights and new issues in developmental neurotoxicology. Neurotoxicology 6 (2002) 659-668
60. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates. 4th ed. (1998), Academic Press, New York
61. Rivera-Cervantes M.C., Torres J.S., Feria-Velasco A., Armendariz-Borunda J., and Beas-Zárate C. NMDA and AMPA receptor expression and cortical neuronal death are associated with p38 in glutamate-induced excitotoxicity in vivo. J. Neurosci. Res. 76 (2004) 678-687
62. Rivera-Cervantes M.C., Flores-Soto M.E., Chaparro-Huerta V., Reyes-Gómez J., Feria-Velasco A., Schliebs R., and Beas-Zárate C. Changes in hippocampal NMDA-R subunit composition induced by exposure of neonatal rats to l-glutamate. Int. J. Dev. Neurosci. 27 (2009) 197-204
63. Romijn H.J., Janszen A.W.J.W., van Voorst M.J.D., Buijs R.M., Balazs R., and Swaab D.F. Perinatal hypoxic-ischemic encephalopathy affects the proportion of GABA-immunoreactive neurons in the cerebral cortex of the rat. Brain Res. 592 (1992) 17-28
64. Root C.M., Velazquez-Ulloa N.A., Monsalve G.C., Minakova E., and Spitzer N.C. Embryonically expressed GABA and glutamate drive electrical activity regulating neurotransmitter specification. J. Neurosci. 28 (2008) 4777-4784
65. Rozenberg F., Robain O., Jardin L., and Ben-Ari Y. Distribution of GABAergic neurons in late fetal and early postnatal rat hippocampus. Dev. Brain Res. 50 (1989) 177-187
66. Salceda R., and Pasantes-Morales H. Uptake, release, and binding of taurine in degenerated rat retinas. J. Neurosci. Res. 8 (1982) 631-642
67. Schousboe A., Sarup A., Bak L.K., Waagepetersen H.S., and Larsson O.M. Role astrocytic transport processes in glutamatergic and GABAergic neurotransmission. Neurochem. Int. 45 (2004) 521-527
68. Segura-Torres J.E., Chaparro-Huerta V., Rivera-Cervantres M.C., Montes-Gonzalez R., Flores-Soto M.E., and Beas-Zárate C. Neuronal cell death due to glutamate excitotocity is mediated by p38 activation in the rat cerebral cortex. Neurosci. Lett. 403 (2006) 233-238
69. Seress L., and Ribak C.E. The development of GABAergic neurons in the rat hippocampal formation. An immunocytochemical study. Dev. Brain Res. 44 (1988) 197-209
70. Sheikh S.N., Martin S.B., and Martin D.L. Regional distribution and relative amounts of glutamate decarboxilase isoforms in rat and mouse brain. Neurochem. Int. 35 (1999) 73-80
71. Siesjo B.K., and Bengtsson F. Calcium fluxes, calcium antagonists, a calcium-related pathology in brain ischemia, hypoglycemia, and spreading depression: a unifying hypothesis. J. Cereb. Blood Flow Metab. 9 (1989) 127-140
72. Sperk G., Schwarzer C., Heilman J., Furtinger S., Reimer R.J., Edwards R.H., and Nelson N. Expression of plasma membrane GABA transporters but not of vesicular GABA transporter in dentate granule cells after kainic acid seizures. Hippocampus 13 (2003) 806-815
73. Spreafico R., and Frassoni C. Morphological aspects of neocortical maturation. In: Avanzini G., Fariello R., Heinemann U., and Mutani R. (Eds). Epileptogenic and Excitotoxic Mechanisms (1993), John Libbey & Company Ltd., London 59-66
74. Struzynska L., and Sulkowski G. Relationships between glutamine, glutamate, and GABA in nerve endings under Pb-toxicity conditions. J. Inorg. Biochem. 98 (2004) 951-958
75. Szabo G., Kartarova Z., Hoertnagl B., Somogyi R., and Sperk G. Differential regulation of adult and embryonic glutamate decarboxilase in rat dentate granule cells after kainate-induced limbic seizures. Neuroscience 100 (2000) 287-295
76. Towfighi J., and Mauger D. Temporal evolution of neuronal changes in cerebral hypoxia-ischemia in developing rats: a quantitative light microscopic study. Dev. Brain Res. 109 (1998) 169-177
77. Ureña-Guerrero M.E., López-Pérez S.J., and Beas-Zárate C. Neonatal monosodium glutamate treatment modifies glutamic acid decarboxylase activity during rat brain postnatal development. Neurochem. Int. 42 (2003) 269-276
78. Varju P., Katarova Z., Madarasz E., and Szabo G. Sequential induction of embryonic and adult forms of glutamic acid decarboxylase during in vitro-induced neurogenesis in cloned neuroectodermal cell-line, NE-7C2. J. Neurochem. 80 (2002) 605-615
79. Vincent S.L., Pabreza L., and Benes F.M. Postnatal maturation of GABA-immunoreactive neurons of rat medial prefrontal cortex. J. Comp. Neurol. 355 (1995) 81-92
80. Wong P.T.H., and McGeer E.G. Postnatal changes of GABAergic and glutamatergic parameters. Dev. Brain Res. 1 (1981) 519-529
81. Xiao M.Y., Wasling P., Hanse E., and Gustafsson B. Creation of AMPA-silent synapses in the neonatal hippocampus. Nat. Neurosci. 7 (2004) 236-243
82. Young A.B., Greenamyre J.T., Hollingsworth Z., Albin R., D'Amato C., Shoulson I., and Penney J.B. NMDA receptor losses in putamen from patients with Huntington's disease. Science 241 (1988) 981-983
83. Zhu X.M., and Ong W.Y. Changes in GABA transporters in the rat hippocampus after kainate-induced neuronal injury: decrease in GAT-1 and GAT-3 but upregulation of betaine/GABA transporter BGT-1. J. Neurosci. Res. 77 (2004) 402-409