Increased glutamate receptor and transporter expression in the cerebral cortex and striatum of Gcdh-/- mice: Possible implications for the neuropathology of glutaric acidemia type I

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Lagranha, Valeska Lizzi ^a   Matte, Ursula ^b   De Carvalho, Talita Giacomet ^b   Seminotti, Bianca ^a   Pereira, Carolina Coffi ^a   Koeller, David M ^c   Woontner, Michael ^d   Goodman, Stephen I ^d   De Souza, Diogo Onofre Gomes ^a   Wajner, Moacir ^a,b  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b HOSPITAL DE CLÍNICAS DE PORTO ALEGRE   (Brazil)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXCITATORY AMINO ACID TRANSPORTER; GLUTAMATE RECEPTOR 2; GLUTAMATE RECEPTOR 6; GLUTAMATE TRANSPORTER; GLUTARYL COENZYME A DEHYDROGENASE; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; SODIUM GLUCOSE COTRANSPORTER 1; GLUTAMATE RECEPTOR; LYSINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN LEVEL; BRAIN REGION; CONTROLLED STUDY; CORPUS STRIATUM; DEVELOPMENTAL STAGE; DISEASE DURATION; FEMALE; GENE LOCATION; GENE OVEREXPRESSION; MALE; MOUSE; MULTIPLE ACYL COA DEHYDROGENASE DEFICIENCY; NEUROPATHOLOGY; NONHUMAN; ONSET AGE; PERINATAL PERIOD; TISSUE DISTRIBUTION; ANIMAL; DEFICIENCY; DIET; DISORDERS OF AMINO ACID AND PROTEIN METABOLISM; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLIC ENCEPHALOPATHY; METABOLISM; NEOSTRIATUM; PATHOLOGY;

AMINO ACID METABOLISM, INBORN ERRORS; AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; BRAIN DISEASES, METABOLIC; CEREBRAL CORTEX; DIET; FEMALE; GENE EXPRESSION REGULATION; GLUTARYL-COA DEHYDROGENASE; LYSINE; MALE; MICE; NEOSTRIATUM; RECEPTORS, GLUTAMATE; RNA, MESSENGER;

EID: 84897052921     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0090477     Document Type: Article

References (99)

1. Goodman SI, Norenberg MD, Shikes RH, Breslich DJ, Moe PG (1977) Glutaric aciduria: biochemical and morphologic considerations. J Pediatr 90(5):746-50. (Pubitemid 8082242)
2. Goodman SI (2001) In: Scriver CR, Beaudet AL, Sly WS, Valle D, editors. The metabolic and molecular basis of inherited disease. New York: McGraw-Hill, pp. 1971-2001.
3. Lindner M, Kölker S, Schulze A, Christensen E, Greenberg CR, et al. (2004) Neonatal screening for glutaryl-CoA dehydrogenase deficiency. J Inherit Metab Dis 27:851-859. (Pubitemid 39433620)
4. Morton DH, Bennett MJ, Seargeant LE, Nichter CA, Kelley RI (1991) Glutaric aciduria type I: a common cause of episodic encephalopathy and spastic paralysis in the Amish of Lancaster County, Pennsylvania. Am J Med Genet 41(1):89-95.
5. Funk CB, Prasad AN, Frosk P, Sauer S, Kölker S, et al. (2005) Neuropathological, biochemical and molecular findings in a glutaric acidemia type1 cohort. Brain 128(Pt 4):711-22. (Pubitemid 40516910)
6. Strauss KA, Morton DH (2003) Type I glutaric aciduria, part 2: a model of acute striatal necrosis. Am J Med Genet C Semin Med Genet 15;121C(1):53-70.
7. Strauss KA, Puffenberger EG, Robinson DL, Morton DH (2003) Type I glutaric aciduria, part 1: natural history of 77 patients. Am J Med Genet C Semin Med Genet 15; 121C(1):38-52.
8. Sauer SW, Okun JG, Fricker G, Mahringer A, Müller I, et al. (2006) Intracerebral accumulation of glutaric and 3-hydroxyglutaric acids secondary to limited flux across the blood-brain barrier constitute a biochemical risk factor for neurodegeneration in glutaryl-CoA dehydrogenase deficiency. J Neurochem 97(3): 899-910.
9. Hoffmann GF, Zschocke J (1999) Glutaric aciduria type I: from clinical, biochemical and molecular diversity to successful therapy. J Inherit Metab Dis 22:381-91. (Pubitemid 29281031)
10. Neumaier-Probst E, Harting I, Seitz A, Ding C, Kolker S (2004) Neuroradiological findings in glutaric aciduria type I (glutaryl-CoA dehydrogenase deficiency). J Inherit Metab Dis 27(6):869-76. (Pubitemid 39433622)
11. Pérez-Dueñas B, De La Osa A, Capdevila A, Navarro-Sastre A, Leist A, et al. (2009) Brain injury in glutaric aciduria type I: the value of functional techniques in magnetic resonanceimaging. Eur J Paediatr Neurol 13(6):534-40.
12. Harting I, Neumaier-Probst E, Seitz A, Maier EM, Assmann B, et al. (2009) Dynamic changes of striatal and extrastriatal abnormalities in glutaric aciduria type I. Brain 132(Pt 7):1764-82.
13. Bodamer OA, Gruber S, Stöckler-Ipsiroglu S (2004) Nuclear magnetic resonance spectroscopy in glutaryl-CoA dehydrogenase deficiency. J Inherit Metab Dis 27(6):877-83. (Pubitemid 39433623)
14. Hedlund GL, Longo N, Pasquali M (2006) Glutaric acidemia type 1. Am J Med Genet C Semin Med Genet 142C(2):86-94.
15. Das AM, Lücke T, Ullrich K (2003) Glutaric aciduria I: creatine supplementation restores creatinephosphate levels in mixed cortex cells from rat incubated with 3-hydroxyglutarate. Mol Genet Metab 78(2):108-11. (Pubitemid 36279625)
16. da C Ferreira G, Viegas CM, Schuck PF, Latini A, Dutra-Filho CS, et al. (2005) Glutaric acid moderately compromises energy metabolism in rat brain. Int J Dev Neurosci 23(8):687-93.
17. Wajner M, Goodman SI (2011) Disruption of mitochondrial homeostasis in organic acidurias: insights from human and animal studies. J Bioenerg Biomembr 43(1):31-8.
18. +-ATPase activity and expression in cerebral cortex of glutaryl-CoA dehydrogenase deficient mice: a possible mechanism for brain injury in glutaric aciduria type I. Mol Genet Metab 107(3):375-82.
19. (+)-ATPase and creatine kinase activities induced by acute lysine administration in glutaryl-CoA dehydrogenase deficient mice. Mol Genet Metab 107(1-2):81-6.
20. de Oliveira Marques F, Hagen ME, Pederzolli CD, Sgaravatti AM, Durigon K, et al. (2003) Glutaric acid induces oxidative stress in brain of young rats. Brain Res 964(1):153-8. (Pubitemid 36165080)
21. Latini A, Borba Rosa R, Scussiato K, Llesuy S, Belló-Klein A, et al. (2002) 3-Hydroxyglutaric acid induces oxidative stress and decreases the antioxidant defenses in cerebral cortex of young rats. Brain Res956(2):367 73.
22. Wajner M, Latini A, Wyse AT, Dutra-Filho CS (2004) The role of oxidative damage in the neuropathology of organic acidurias: insights from animal studies. J Inherit Metab Dis 27(4):427-48. (Pubitemid 39140134)
23. Latini A, Scussiato K, Leipnitz G, Dutra-Filho CS, Wajner M (2005) Promotion of oxidative stress by 3-hydroxyglutaric acid in rat striatum. J Inherit Metab Dis 28(1):57-67. (Pubitemid 40253984)
24. Latini A, Ferreira GC, Scussiato K, Schuck PF, Solano AF, et al. (2007) Induction of oxidative stress by chronic and acute glutaric acid administration to rats. Cell Mol Neurobiol 27(4):423-38. (Pubitemid 46763889)
25. Seminotti B, da Rosa MS, Fernandes CG, Amaral AU, Braga LM, et al. (2012). Induction of oxidative stress in brain of glutaryl-CoA dehydrogenase deficient mice by acute lysine administration. Mol Genet Metab 106(1):31-8.
26. Seminotti B, Amaral AU, da Rosa MS, Fernandes CG, Leipnitz G, et al. (2013) Disruption of brain redox homeostasis in glutaryl-CoA dehydrogenase deficient mice treated with high dietary lysine supplementation. Mol Genet Metab 108(1):30-9.
27. Flott-Rahmel B, Falter C, Schluff P, Fingerhut R, Christensen E, et al. (1997) Nerve cell lesions caused by 3-hydroxyglutaric acid: a possible mechanism for neurodegeneration in glutaric acidemia I. J Inherit Metab Dis20(3): 387-90. 1997. (Pubitemid 27354622)
28. Ullrich K, Flott-Rahmel B, Schluff P, Musshoff U, Das A, et al. (1999) Glutaric aciduria type I: pathomechanisms of neurodegeneration. J Inherit Metab Dis 22(4):392-403. (Pubitemid 29281032)
29. Kölker S, Ahlemeyer B, Krieglstein J, Hoffmann GF (2000) Evaluation of trigger factors of acute encephalopathy in glutaric aciduria type I: fever and tumour necrosis factor-alpha. J Inherit Metab Dis 23(4):359-62. (Pubitemid 30364771)
30. Kölker S, Ahlemeyer B, Krieglstein J, Hoffmann GF (2000) Maturation-dependent neurotoxicity of 3-hydroxyglutaric and glutaric acids in vitro: a new pathophysiologic approach to glutaryl-CoA dehydrogenase deficiency. Pediatr Res 47(4 Pt 1):495-503. (Pubitemid 30183225)
31. (+) dependence of 3-hydroxyglutarate-induced excitotoxicity in primary neuronal cultures from chick embryo telencephalons. Pediatr Res 52(2):199-206.
32. Dalcin KB, Rosa RB, Schmidt AL, Winter JS, Leipnitz G, et al. (2007) Age and brain structural related effects of glutaric and 3-hydroxyglutaric acids on glutamate binding to plasma membranes during rat brain development. Cell Mol Neurobiol 27:805-818. (Pubitemid 47476614)
33. Rosa RB, Schwarzbold C, Dalcin KB, Ghisleni GC, Ribeiro CA, et al (2004) Evidence that 3-hydroxyglutaric acid interacts with NMDA receptors in synaptic plasma membranes from cerebral cortex of young rats. Neurochem Int 45(7):1087-94. (Pubitemid 39164933)
34. Porciúncula LO, Emanuelli T, Tavares RG, Schwarzbold C, Frizzo ME, et al. (2004) Glutaric acid stimulates glutamate binding and astrocytic uptake and inhibits vesicular glutamate uptake in forebrain from young rats. Neurochem Int 45(7):1075-86. (Pubitemid 39164932)
35. Frizzo ME, Schwarzbold C, Porciúncula LO, Dalcin KB, Rosa RB, et al. (2004) 3-hydroxyglutaric acid enhances glutamate uptake into astrocytes from cerebral cortex of young rats. Neurochem Int 44(5):345-53. (Pubitemid 37485866)
36. Wajner M, Kölker S, Souza DO, Hoffmann GF, de Mello CF (2004) Modulation of glutamatergic and GABAergic neurotransmission in glutaryl-CoA dehydrogenase deficiency. J Inherit Metab Dis 27(6):825-8. (Pubitemid 39433616)
37. Jafari P, Braissant O, Bonafé L, Ballhausen D (2011) The unsolved puzzle of neuropathogenesis in glutaric aciduria type I. Mol Genet Metab 104(4):425-37.
38. Bjugstad KB, Zawada WM, Goodman S, Freed CR (2001) IGF-1 and bFGF reduce glutaric acid and 3-hydroxyglutaric acid toxicity in striatal cultures. J Inherit Metab Dis 24(6):631-47. (Pubitemid 33130085)
39. Lund TM, Christensen E, Kristensen AS, Schousboe A, Lund AM (2004) On theneurotoxicity of glutaric, 3-hydroxyglutaric, and trans-glutaconic acids in glutaric acidemia type 1. J Neurosci Res 77(1):143-7, 2004. (Pubitemid 38850064)
40. Freudenberg F, Lukacs Z, Ullrich K (2004) 3-Hydroxyglutaric acid fails to affect the viability of primary neuronal rat cells. Neurobiol Dis 16(3):581-4. (Pubitemid 38942991)
41. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65: 1-105.
42. 2+ permeation through the ionotropic glutamate receptor. Tanpakushitsu Kakusan Koso 43(12 Suppl):1589-95.
43. McDonald JW, Johnston MV (1990) Physiological and pathophysiological roles of excitatory amino acids during central nervous system development. Brain Res Brain Res Rev 15(1):41-70. (Pubitemid 20158154)
44. Conn PJ, Pin JP (1997) Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 37:205-37. (Pubitemid 27238875)
45. Nakanishi S (1992) Molecular diversity of glutamate receptors and implications for brain function. Science 23;258(5082):597-603.
46. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, et al. (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62(3):405-96.
47. Insel TR, Miller LP, Gelhard RE (1990) The ontogeny of excitatory amino acid receptors in rat forebrain-I. N-methyl-D-aspartate and quisqualate receptors. Neuroscience 35(1):31-43. (Pubitemid 20113965)
48. Petralia RS, Esteban JA, Wang YX, Partridge JG, Zhao HM, et al. (1999) Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Nat Neurosci 2(1):31-6. (Pubitemid 30488937)
49. Colwell CS, Cepeda C, Crawford C, Levine MS (1998) Postnatal development of glutamate receptor-mediated responses in the neostriatum. Dev Neurosci 20(2-3):154-63. (Pubitemid 28349871)
50. Nansen EA, Jokel ES, Lobo MK, Micevych PE, Ariano MA, et al. (2000) Striatal ionotropic glutamate receptor ontogeny in the rat. Dev Neurosci 22(4):329-40.
51. Amara SG, Fontana AC (2002) Excitatory amino acid transporters: keeping up with glutamate. Neurochem Int 41(5):313-8.
52. Furuta A, Rothstein JD, Martin LJ (1997) Glutamate transporter protein subtypes are expressed differentially during rat CNS development. J Neurosci 17(21):8363-75. (Pubitemid 27461059)
53. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, et al. (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16(3):675-86. (Pubitemid 26103145)
54. Ullensvang K, Lehre KP, Storm-Mathisen J, Danbolt NC (1997) Differential developmental expression of the two rat brain glutamate transporter proteins GLAST and GLT. Eur J Neurosci 9(8):1646-55. (Pubitemid 27348323)
55. Lau A, Tymianski M (2010) Glutamate receptors, neurotoxicity and neurodegeneration. Pflugers Arch 460(2):525-42.
56. Wang Y, Qin ZH (2010) Molecular and cellular mechanisms of excitotoxic neuronal death. Apoptosis 15(11):1382-402.
57. Barbon A, Barlati S (2011) Glutamate receptor RNA editing in health and disease. Biochemistry (Mosc) 76(8):882-9.
58. Olney JW (1969) Glutamate-induced retinal degeneration in neonatal mice. Electron microscopy of the acutely evolving lesion. J Neuropathol Exp Neurol 28(3):455-74.
59. Lipton SA, Rosenberg PA (1994) Excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med 330(9):613-22.
60. Maragakis NJ, Rothstein JD (2001) Glutamate transporters in neurologic disease. Arch Neurol 58(3):365-70. (Pubitemid 32217452)
61. Dong XX, Wang Y, Qin ZH (2009) Molecular mechanisms of excitotoxicity and theirrelevance to pathogenesis of neurodegenerative diseases. Acta Pharmacol Sin 30(4):379-87.
62. Novelli A, Reilly JA, Lysko PG, Henneberry RC (1988) Glutamate becomes neurotoxic via the N-methyl-D-aspartate receptor when intracellular energy levels are reduced. Brain Res. 451(1-2):205-12.
63. Koeller DM, Woontner M, Crnic LS, Kleinschmidt-DeMasters B, Stephens J, et al. (2002) Biochemical, pathologic and behavioral analysis of a mouse model of glutaric acidemia type I. Hum Mol Genet 11(4):347-57. (Pubitemid 34213608)
64. Zinnanti WJ, Lazovic J, Wolpert EB, Antonetti DA, Smith MB, et al. (2006) A diet-induced mouse model for glutaric aciduria type I. Brain 129(Pt 4):899-910.
65. Zinnanti WJ, Lazovic J, Housman C, LaNoue K, O'Callaghan JP, et al. (2007) Mechanism of age-dependent susceptibility and novel treatment strategy in glutaric acidemia type I. J Clin Invest 117(11):3258-70. (Pubitemid 350096983)
66. Haberny KA, Paule MG, Scallet AC, Sistare FD, Lester DS, et al. (2002) Ontogeny of the N-methyl-D-aspartate (NMDA) receptor system and susceptibility to neurotoxicity. Toxicol Sci 68(1):9-17. (Pubitemid 34785224)
67. Jensen FE (2002) The role of glutamate receptor maturation in perinatal seizures and brain injury. Int J Dev Neurosci 20(3-5):339-47.
68. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402-8. (Pubitemid 34164012)
69. Arzberger T, Krampfl K, Leimgruber S, Weindl A (1997) Changes of NMDA receptor subunit (NR1, NR2B) and glutamate transporter (GLT1) mRNA expression in Huntington's disease an in situ hybridization study. J Neuropathol Exp Neurol 56(4):440-54. (Pubitemid 27465027)
70. McDonald JW, Silverstein FS, Johnston MV (1988) Neurotoxicity of N-methyl- D-aspartate is markedly enhanced in developing rat central nervous system. Brain Res 30; 459(1):200-3.
71. Miyamoto K, Nakanishi H, Moriguchi S, Fukuyama N, Eto K, et al. (2001) Involvement of enhanced sensitivity of N-methyl-D-aspartate receptors in vulnerability of developing cortical neurons to methylmercury neurotoxicity. Brain Res18;901(1-2):252-8.
72. Watanabe M, Inoue Y, Sakimura K, Mishina M (1992) Developmental changes in distribution of NMDA receptor channel subunit mRNAs. Euroreport 3(12):1138-40. (Pubitemid 23034721)
73. Akazawa C, Shigemoto R, Bessho Y, Nakanishi S, Mizuno N (1994) Differential expression of five N-methyl-D-aspartate receptor subunit mRNAs in the cerebellum of developing and adult rats. J Comp Neurol 347(1):150-60. (Pubitemid 24262237)
74. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12(3):529-40. (Pubitemid 24100885)
75. Peit DS, Wang XT, Liu Y, Sun YF, Guan QH, et al. (2006) Neuroprotection against ischaemic brain injury by a GluR6-9c peptide containing the TAT protein transduction sequence. Brain 129(Pt 2):465-79. (Pubitemid 43164369)
76. 2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 252(5007):851-3.
77. Wisden W, Seeburg PH (1993) Mammalian ionotropic glutamate receptors. Curr Opin Neurobiol 3(3):291-8. (Pubitemid 23210937)
78. de Sousa Abreu R, Penalva LO, Marcotte EM, Vogel C (2009) Global signatures of protein and mRNA expression levels. Mol Biosyst 5 (12):1512-26.
79. Matsuda K, Fletcher M, Kamiya Y, Yuzaki M (2003) Specific assembly with the NMDA receptor 3B subunit controls surface expression and calcium permeability of NMDA receptors. J Neurosci. 23:10064-10073. (Pubitemid 37392553)
80. Henson MA, Roberts AC, Salimi K, Vadlamudi S, Hamer RM, et al. (2008) Developmental regulation ofthe NMDA receptor subunits, NR3A and NR1 in human prefrontal cortex. Cereb Cortex.18(11):2560-73.
81. Kolker S, Ahlemeyer B, Krieglstein J, Hoffmann GF (2000) Cerebral organic acid disorders induce neuronal damage via excitotoxic organic acids in vitro. Amino Acids 18(1): 31-40. (Pubitemid 30093311)
82. Kölker S, Okun JG, Ahlemeyer B, Wyse AT, Hörster F, et al. (2002) Chronic treatment with glutaric acid induces partial tolerance to excitotoxicity in neuronal cultures from chick embryo telencephalons. J Neurosci Res 68(4):424-31.
83. Kölker S, Ahlemeyer B, Krieglstein J, Hoffmann GF (1999) 3-Hydroxyglutaric and glutaric acids are neurotoxic through NMDA receptors in vitro. J Inherit Metab Dis 22(3):259-62. (Pubitemid 29259490)
84. Kölker S, Koeller DM, Sauer S, Hörster F, Schwab MA, et al. (2004) Excitotoxicity and bioenergetics in glutaryl-CoA dehydrogenase deficiency. J Inherit Metab Dis 27(6):805-12. (Pubitemid 39433613)
85. Farooqui AA, Horrocks LA (1994) Involvement of glutamate receptors, lipases, and phospholipases in long-term potentiation and neurodegeneration. J Neurosci Res 38(1):6-11. (Pubitemid 24143178)
86. Clinton SM, Haroutunian V, Meador-Woodruff JH (2006) Up-regulation of NMDA receptor subunit and post-synaptic density protein expression in the thalamus of elderly patients with schizophrenia. J Neurochem 98(4):1114-25. (Pubitemid 44127787)
87. Blanke ML, Van Dongen AMJ (2009) Activation Mechanisms of the NMDA Receptor. In: Van Dongen AM, editor. Biology of the NMDA Receptor. Boca Raton (FL): CRC Press, chapter 13.
88. Wroge CM, Hogins J, Eisenman L, Mennerick S (2012) Synaptic NMDA receptors mediate hypoxic excitotoxic death. J Neurosci 32(19):6732-42.
89. Aida T, Ito Y, Takahashi YK, Tanaka K (2012) Overstimulation of NMDA receptors impairs early brain development in vivo. PLoS One 7(5):e36853.
90. Spalloni A, Nutini M, Longone P (2013) Role of the N-methyl-d-aspartate receptors complex in amyotrophic lateral sclerosis. Biochim Biophys Acta 1832 (2):312-22.
91. Duan S, Anderson CM, Stein BA, Swanson RA (1999) Glutamate induces rapid upregulation of astrocyte glutamate transport and cell-surface expression of GLAST. J Neurosci 19(23):10193-200. (Pubitemid 30228026)
92. Swanson RA, Liu J, Miller JW, Rothstein JD, Farrell K, et al. (1997) Neuronal regulation of glutamate transporter subtype expression in astrocytes. J Neurosci 17:932-940. (Pubitemid 27043952)
93. Lima TT, Begnini J, de Bastiani J, Fialho DB, Jurach A, et al. (1998) Pharmacological evidence for GABAergic and glutamatergic involvement in the convulsant and behavioral effects of glutaric acid. Brain Res 17;802(1-2):55-60.
94. 3[H]glutamate binding to plasma membranes from brain of young rats by glutaric acid in vitro. J Neurol Sci 15; 173(2):93-6.
95. Satoh E, Nakazato Y (1992) On the mechanism of ouabain-induced release of acetylcholine from synaptosomes J Neurochem 58:1038-1044.
96. Erecinska M, Silver IA (1994) Ions and energy in mammalian brain. Prog Neurobiol 43, 37-71. (Pubitemid 24221854)
97. Erecinska M, Cherian S, Silver IA (2004) Energy metabolism in mammalian brain during development. Prog Neurobiol 73, 397-445. (Pubitemid 39099270)
98. Fighera MR, Royes LF, Furian AF, Oliveira MS, Fiorenza NG, et al. (2006) GM1 ganglioside prevents seizures, Na+,K+-ATPase activity inhibition and oxidative stress induced by glutaric acid and pentylenetetrazole. Neurobiol Dis 22(3):611-23. (Pubitemid 43832132)
99. Forstner R, Hoffmann GF, Gassner I, Heideman P, De Klerk JB, et al. (1999) Glutaric aciduria type I: ultrasonographic demonstration of early signs. Pediatr Radiol 29(2):138-43. (Pubitemid 29134456)