Impact of STZ-induced hyperglycemia and insulin-induced hypoglycemia in plasma amino acids and cortical synaptosomal neurotransmitters

Synapse

Volumn 65, Issue 6, 2011, Pages 457-466

  Cardoso, Susana ^a,b   Carvalho, Cristina ^a,b   Santos, Renato ^a,b   Correia, Sónia ^a,b   Santos, Maria S ^a,b   Seiça, Raquel ^c   Oliveira, Catarina R ^a,c   Moreira, Paula I ^a,c  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Amino acids; Diabetes; Hypoglycemia; Neurotransmitters; Plasma; Synaptosomes

Indexed keywords

4 AMINOBUTYRIC ACID; ADENOSINE TRIPHOSPHATE; ASPARTIC ACID; CITRIC ACID; GLUCOSE; GLUTAMIC ACID; INSULIN; IODOACETIC ACID; NEUROTRANSMITTER; OUABAIN; POTASSIUM CHLORIDE; STREPTOZOCIN; TAURINE; VERATRIDINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; HYPOGLYCEMIA; MALE; MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN SECRETION; RAT; SYNAPTOSOME;

AMINO ACIDS; ANIMALS; CEREBRAL CORTEX; DIABETES MELLITUS, EXPERIMENTAL; DISEASE MODELS, ANIMAL; HYPERGLYCEMIA; HYPOGLYCEMIA; MALE; NEUROTRANSMITTER AGENTS; RATS; RATS, WISTAR; SYNAPTIC TRANSMISSION; SYNAPTOSOMES;

EID: 79953276927     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.20863     Document Type: Article

References (64)

1. Aerts L, Van Assche FA. 2002. Taurine and taurine-deficiency in the perinatal period. J Perinat Med 30: 281-286.
2. Alberdi E, Sánchez-Gómez MV, Cavaliere F, Pérez-Samartín A, Zugaza JL, Trullas R, Domercq M, Matute C. 2010. Amyloid beta oligomers induce Ca(2+) dysregulation and neuronal death through activation of ionotropic glutamate receptors. Cell Calcium 47: 264-272.
3. Alvarez EO, Beauquis J, Revsin Y, Banzan AM, Roig P, De Nicola AF, Saravia F. 2009. Cognitive dysfunction and hippocampal changes in experimental type 1 diabetes. Behav Brain Res 198: 224-230.
4. Auer RN. 2004. Hypoglycemic brain damage. Metab Brain Dis 19: 169-175.
5. Bak LK, Schousboe A, Waagepetersen HS. 2006. The glutamate/GABA-glutamine cycle: aspects of transport, neurotransmitter homeostasis and ammonia transfer. J Neurochem 98: 641-653.
6. Battezzati A, Benedini S, Fattorini A, Piceni Sereni L, Luzi L. 2000. Effect of hypoglycemia on amino acid and protein metabolism in healthy humans. Diabetes 49: 1543-1551.
7. Battezzati A, Benedini S, Sereni LP, DeTaddeo F, Maffi P, Secchi A, Luzi L. 2009. Protein and glutamine kinetics during counter-regulatory failure in type 1 diabetes. Nutr Metab Cardiovasc Dis 19: 352-357.
8. Cardoso S, Correia S, Santos RX, Carvalho C, Santos MS, Oliveira CR, Perry G, Smith MA, Zhu X, Moreira PI. 2009. Insulin is a two-edged knife on the brain. J Alzheimers Dis 18: 483-507.
9. Cardoso S, Santos MS, Seiça R, Moreira PI. 2010. Cortical and hippocampal mitochondria bioenergetics and oxidative status during hyperglycemia and insulin-induced hypoglycemia. Biochim Biophys Acta 1802: 942-951.
10. Engelsen B, Westerberg E, Fonnum F, Wieloch T. 1986. Effect of insulin-induced hypoglycemia on the concentrations of glutamate and related amino acids and energy metabolites in the intact and decorticated rat neostriatum. J Neurochem 47: 1634-1641.
11. Engelsen B, Fonnum F. 1983. Effects of hypoglycemia on the transmitter pool and the metabolic pool of glutamate in rat brain. Neurosci Lett 42: 317-322.
12. Erecinska M, Zaleska MM, Nissim I, Nelson D, Dagani F, Yudkoff M. 1988. Glucose and synaptosomal glutamate metabolism: Studies with [15N]glutamate. J Neurochem 51: 892-902.
13. Fleck MW, Henze DA, Barrionuevo G, Palmer AM. 1993. Aspartate and glutamate mediate excitatory synaptic transmission in area CA1 of the hippocampus. J Neurosci 13: 3944-3955.
14. Franconi F, Bennardini F, Mattana A, Miceli M, Ciuti M, Mian M, Gironi A, Anichini R, Seghieri G. 1995. Plasma and platelet taurine are reduced in subjects with insulin-dependent diabetes mellitus: effects of taurine supplementation. Am J Clin Nutr 61: 1115-1119.
15. French ED, Vezzani A, Whetsell WOJr, Schwarcz R. 1986. Antiexcitotoxic actions of taurine in the rat hippocampus studied in vivo and in vitro. Adv Exp Med Biol 203: 349-362.
16. Frigerio F, Casimir M, Carobbio S, Maechler P. 2008. Tissue specificity of mitochondrial glutamate pathways and the control of metabolic homeostasis. Biochim Biophys Acta 1777: 965-972.
17. Gispen WH, Biessels GJ. 2000. Cognition and synaptic plasticity in diabetes mellitus. Trends Neurosci 23: 542-549.
18. Gornall AG, Bardawill CJ, David MM. 1949. Determination of serum proteins by means of the biuret reaction. J Biol Chem 177: 751-766.
19. Gundersen V, Chaudhry FA, Bjaalie JG, Fonnum F, Ottersen OP, Storm-Mathisen J. 1998. Synaptic vesicular localization and exocytosis of L-aspartate in excitatory nerve terminals: A quantitative immunogold analysis in rat hippocampus. J Neurosci 18: 6059-6070.
20. Gundersen V, Danbolt NC, Ottersen OP, 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.
21. Gundersen V, Fonnum F, Ottersen OP, Storm-Mathisen J. 2001. Redistribution of neuroactive amino acids in hippocampus and striatum during hypoglycemia: A quantitative immunogold study. J Cereb Blood Flow Metab 21: 41-51.
22. Gundersen V, Ottersen OP, Storm-Mathisen J. 1996. Selective excitatory amino acid uptake in glutamatergic nerve terminals and in glia in the rat striatum: Quantitative electron microscopic immunocytochemistry of exogenous (D)-aspartate and endogenous glutamate and GABA. Eur J Neurosci 8: 758-765.
23. Hansen SH. 2001. The role of taurine in diabetes and the development of diabetic complications. Diabetes Metab Res Rev 17: 330-346.
24. Herrero MT, Oset-Gasque MJ, Cañadas S, Vicente S, González MP. 1998. Effect of various depolarizing agents on endogenous amino acid neurotransmitter release in rat cortical neurons in culture. Neurochem Int 32: 257-264.
25. Herzog RI, Chan O, Yu S, Dziura J, McNay EC, Sherwin RS. 2008. Effect of acute and recurrent hypoglycemia on changes in brain glycogen concentration. Endocrinology 149: 1499-1504.
26. Kamo N, Muratsugu M, Hongoh R, Kobatake V. 1979. Membrane potential of mitochondria measured with an electrode sensitive to tetraphenyl phosphonium and relationship between proton electrochemical potential and phosphorylation potential in steady state. J Membr Biol 49: 105-121.
27. Kauppinen RA, McMahon HT, Nicholls DG. 1988. Ca2+-dependent and Ca2+-independent glutamate release, energy status and cytosolic free Ca2+ concentration in isolated nerve terminals following metabolic inhibition: Possible relevance to hypoglycaemia and anoxia. Neuroscience 27: 175-182.
28. Kim SJ, Ramesh C, Gupta H, Lee W. 2007. Taurine-diabetes interaction: From involvement to protection. J Biol Regul Homeost Agents 21: 63-77.
29. Kodl CT, Seaquist ER. 2008. Cognitive dysfunction and diabetes mellitus. Endocr Rev 29: 494-511.
30. Li F, Obrosova IG, Abatan O, Tian D, Larkin D, Stuenkel EL, Stevens MJ. 2005. Taurine replacement attenuates hyperalgesia and abnormal calcium signaling in sensory neurons of STZ-D rats. Am J Physiol Endocrinol Metab 288: E29-E36.
31. Madl JE, Royer SM. 2000. Glutamate dependence of GABA levels in neurons of hypoxic and hypoglycemic rat hippocampal slices. Neuroscience 96: 657-664.
32. McCrimmon RJ, Frier BM. 1994. Hypoglycaemia, the most feared complication of insulin therapy. Diabetes Metab 20: 503-512.
33. McGowan JE, Zanelli SA, Haynes-Laing AG, Mishra OP, Delivoria-Papadopoulos M. 2002. Modification of glutamate binding sites in newborn brain during hypoglycemia. Brain Res 927: 80-86.
34. McNay EC, Williamson A, McCrimmon RJ, Sherwin RS. 2006. Cognitive and neural hippocampal effects of long-term moderate recurrent hypoglycemia. Diabetes 55: 1088-1095.
35. Menge BA, Schrader H, Ritter PR, Ellrichmann M, Uhl W, Schmidt WE, Meier JJ. 2010. Selective amino acid deficiency in patients with impaired glucose tolerance and type 2 diabetes. Regul Pept 160: 75-80.
36. Moreira PI, Santos MS, Sena C, Seiça R, Oliveira CR. 2005. Insulin protects against amyloid β-peptide toxicity in brain mitochondria of diabetic rats. Neurobiol Dis 18: 628-637.
37. Nicholls DG. 2003. Bioenergetics and transmitter release in the isolated nerve terminal. Neurochem Res 28: 1433-1441.
38. Obrosova IG, Drel VR, Kumagai AK, Szábo C, Pacher P, Stevens MJ. 2006. Early diabetes-induced biochemical changes in the retina: Comparison of rat and mouse models. Diabetologia 49: 2525-2533.
39. Palmeira CM, Santos MS, Carvalho AP, Oliveira CR. 1993. Membrane lipid peroxidation induces changes in aminobutyric acid transport and calcium uptake by synaptosomes. Brain Res 609: 117-123.
40. Raiteri M, Cerrito F, Cervoni AM, Levi G. 1979. Dopamine can be released by two mechanisms differentially affected by the dopamine transport inhibitor nomifensine. J Pharmacol Exp Ther 208: 195-202.
41. Ramakrishna V, Jailkhani R. 2007. Evaluation of oxidative stress in insulin dependent diabetes mellitus (IDDM) patients. Diagn Pathol 2: 22.
42. Ravindran J, Shuaib A, Ijaz S, Galazka P, Waqar T, Ishaqzay R, Miyashita H, Liu L. 1994. High extracellular GABA levels in hippocampus as a mechanism of neuronal protection in cerebral ischemia in adrenalectomized gerbils. Neurosci Lett 176: 209-211.
43. Sah R, Schwartz-Bloom RD. 1999. Optical imaging reveals elevated intracellular chloride in hippocampal pyramidal neurons after oxidative stress. J Neurosci 19: 9209-9217.
44. Sánchez-Prieto J, González P. 1988. Occurrence of a large Ca2+-independent release of glutamate during anoxia in isolated nerve terminals (synaptosomes). J Neurochem 50: 1322-1324.
45. Sandberg M, Butcher SP, Hagberg H. 1986. Extracellular overflow of neuroactive amino acids during severe insulin-induced hypoglycemia: In vivo dialysis of the rat hippocampus. J Neurochem 47: 178-184.
46. Santos MS, Gonçalves PP, Carvalho AP. 1990. Effect of ouabain on the gamma-[3H]aminobutyric acid uptake and release in the absence of Ca(+)+ and K(+)-depolarization. J Pharmacol Exp Ther 253: 620-627.
47. Santos MS, Moreno AJ, Carvalho AP. 1996. Relationships between ATP depletion, membrane potential, and the release of neurotransmitters in rat nerve terminals. An in vitro study under conditions that mimic anoxia, hypoglycemia, and ischemia. Stroke 27: 941-950.
48. Santos MS, Rodriguez R, Carvalho AP. 1992. Effect of depolarizing agents on the Ca(2+)-independent and Ca(2+)-dependent release of [3H]GABA from sheep brain synaptosomes. Biochem Pharmacol 44: 301-308.
49. Saransaari P, Oja SS. 1999. Alanine release from the adult and developing hippocampus is enhanced by ionotropic glutamate receptor agonists and cell-damaging conditions. Neurochem Res 24: 407-414.
50. Satoh E, Takahashi A. 2008. Experimental diabetes enhances Ca2+ mobilization and glutamate exocytosis in cerebral synaptosomes from mice. Diabetes Res Clin Pract 81: 14-17.
51. Shuaib A, Ijaz S, Hasan S, Kalra J. 1992. Gamma-vinyl GABA prevents hippocampal and substantia nigra reticulata damage in repetitive transient forebrain ischemia. Brain Res 590: 13-17.
52. Sitges M, Nekrassov V, Guarneros A. 2000. Simultaneous action of MK-801 (dizclopine) on dopamine, glutamate, aspartate and GABA release from striatum isolated nerve endings. Brain Res 854: 48-56.
53. Smith MA, Sayre LM, Perry G. 1996. Diabetes mellitus and Alzheimer's disease: Glycation as a biochemical link. Diabetologia 39: 247.
54. Sonnewald U, McKenna M. 2002. Metabolic compartmentation in cortical synaptosomes: Influence of glucose and preferential incorporation of endogenous glutamate into GABA. Neurochem Res 27: 43-50.
55. Steen E, Terry BM, Rivera EJ, Cannon JL, Neely TR, Tavares R, Xu XJ, Wands JR, de la Monte SM. 2005. Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease-Is this type 3 diabetes? J Alzheimers Dis 7: 63-80.
56. Suh SW, Hamby AM, Swanson RA. 2007. Hypoglycemia, brain energetics, and hypoglycemic neuronal death. Glia 55: 1280-1286.
57. Szerb JC, O'Regan PA. 1987. Reversible shifts in the Ca2+-dependent release of aspartate and glutamate from hippocampal slices with changing glucose concentrations. Synapse 1: 265-272.
58. Tomiyama M, Furusawa K, Kamijo M, Kimura T, Matsunaga M, Baba M. 2005. Upregulation of mRNAs coding for AMPA and NMDA receptor subunits and metabotropic glutamate receptors in the dorsal horn of the spinal cord in a rat model of diabetes mellitus. Brain Res Mol Brain Res 136: 275-281.
59. Trenkner E. 1990. The role of taurine and glutamate during early postnatal cerebellar development of normal and weaver mutant mice. Adv Exp Med Biol 268: 239-244.
60. Vilchis C, Salceda R. 1996. Effect of diabetes on levels and uptake of putative amino acid neurotransmitters in rat retina and retinal pigment epithelium. Neurochem Res 21: 1167-1171.
61. Waagepetersen HS, Bakken IJ, Larsson OM, Sonnewald U, Schousboe A. 1998. Comparison of lactate and glucose metabolism in cultured neocortical neurons and astrocytes using 13C-NMR spectroscopy. Dev Neurosci 20: 310-320.
62. Whitton PS, Nicholson RA, Strang RH. 1998. Effect of taurine on calcium accumulation in resting and depolarised insect synaptosomes. J Neurochem 50: 1743-1746.
63. Wu QD, Wang JH, Fennessy F, Redmond HP, Bouchier-Hayes D. 1999. Taurine prevents high-glucose-induced human vascular endothelial cell apoptosis. Am J Physiol 277: 1229-1238.
64. Yudkoff M, Nelson D, Daikhin Y, Erecínska M. 1994. Tricarboxylic acid cycle in rat brain synaptosomes. Fluxes and interactions with aspartate aminotransferase and malate/aspartate shuttle. J Biol Chem 269: 27414-27420.