Adenosine A1 receptors control the metabolic recovery after hypoxia in rat hippocampal slices

Journal of Neurochemistry

Volumn 136, Issue 5, 2016, Pages 947-957

  Duarte, João M N ^a,b,d   Cunha, Rodrigo A ^a,c   Carvalho, Rui A ^a,b  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d EPFL   (Switzerland)

Author keywords

13C isotopomer analysis; adenosine; energy metabolism; hippocampus; hypoxia; NMR spectroscopy

Indexed keywords

ADENOSINE A1 RECEPTOR; CREATINE PHOSPHATE; GLUTAMINE; 1,3-DIPROPYL-8-CYCLOPENTYLXANTHINE; ADENOSINE; XANTHINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN HYPOXIA; BRAIN NERVE CELL; BRAIN SLICE; CARBON NUCLEAR MAGNETIC RESONANCE; CITRIC ACID CYCLE; CONTROLLED STUDY; HIPPOCAMPUS; MALE; METABOLIC REGULATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; RAT; REOXYGENATION; ANIMAL; ANOXIA; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; METABOLISM; NERVE CELL; SYNAPTIC TRANSMISSION;

ADENOSINE; ANIMALS; ANOXIA; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; MALE; NEURONS; RECEPTOR, ADENOSINE A1; SYNAPTIC TRANSMISSION; XANTHINES;

EID: 84958122057     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13512     Document Type: Article

References (61)

1. 2B receptor activation promotes glycogen synthesis in astrocytes through modulation of gene expression. Am. J. Physiol. 284, C696-C704.
2. 1 receptors impairs the recovery of synaptic transmission after hypoxia. Neuroscience 132, 575-580.
3. Atkinson D. E., (1968) The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry 7, 4030-4034.
4. Balestrino M., Lensman M., Parodi M., Perasso L., Rebaudo R., Melani R., Polenov S., Cupello A., (2002) Role of creatine and phosphocreatine in neuronal protection from anoxic and ischemic damage. Amino Acids 23, 221-229.
5. Baslow M. H., (2003) N-Acetylaspartate in the vertebrate brain: Metabolism and function. Neurochem. Res. 28, 941-953.
6. 31P-n.m.r. study. Biochem. J. 291, 915-919.
7. Blood A. B., Hunter C. J., and, Power G. G., (2003) Adenosine mediates decreased cerebral metabolic rate and increased cerebral blood flow during acute moderate hypoxia in the near-term fetal sheep. J. Physiol. 553, 935-945.
8. Bouzier-Sore A. K., Voisin P., Canioni P., Magistretti P. J., and, Pellerin L., (2003) Lactate is a preferential oxidative energy substrate over glucose for neurons in culture. J. Cereb. Blood Flow Metab. 23, 1298-1306.
9. 31P nuclear magnetic resonance. J. Neurochem. 52, 604-610.
10. 13C]acetate in the hypoxic rat brain. Neurochem. Int. 38, 399-407.
11. Cunha R. A., (2001) Adenosine as a neuromodulator and as a homeostatic regulator in the nervous system: Different roles, different sources and different receptors. Neurochem. Int. 38, 107-125.
12. 2A receptor-mediated facilitation of plasticity. Neurochem. Int. 52, 65-72.
13. 1 receptors. J. Neurosci. 18, 1987-1995.
14. Dale N., and, Frenguelli B. G., (2009) Release of adenosine and ATP during ischemia and epilepsy. Curr. Neuropharmacol. 7, 160-179.
15. 13C NMR spectroscopy at 14.1 T. J. Neurochem. 126, 579-590.
16. Duarte J. M. N., Cunha R. A., and, Carvalho R. A., (2007a) Different metabolism of Glutamatergic and GABAergic compartments in superfused hippocampal slices characterized by nuclear magnetic resonance spectroscopy. Neurosci. 144, 1305-1313.
17. Duarte J. M. N., Oses J. P., Rodrigues R. J., and, Cunha R. A., (2007b) Modification of purinergic signaling in the hippocampus of streptozotocin-induced diabetic rats. Neurosci. 149, 382-391.
18. 13C NMR spectroscopy at 14.1 T. Frontiers in Neuroenergetics 3, 3
19. Duarte J. M. N., Ferreira S. G., Carvalho R. A., Cunha R. A., and, Köfalvi A., (2012a) CB1 receptor activation inhibits neuronal and astrocytic intermediary metabolism in the rat hippocampus. Neurochem. Int. 60, 1-8.
20. 1H NMR spectroscopy. NeuroImage 61, 342-362.
21. 13C]lactate. J. Neurosci. Res. 93, 1009-1018.
22. Dunwiddie T. V., and, Masino S. A., (2001) The role and regulation of adenosine in the central nervous system. Annu. Rev. Neurosci. 24, 31-55.
23. 1 receptor stimulation during reperfusion following ischaemia. Br. J. Pharmacol. 118, 355-363.
24. Fowler J. C., (1989) Adenosine antagonists delay hypoxia-induced depression of neuronal activity in hippocampal brain slice. Brain Res. 490, 378-384.
25. Fowler J. C., (1993) Purine release and inhibition of synaptic transmission during hypoxia and hypoglycemia in rat hippocampal slices. Neurosci. Lett. 157, 83-86.
26. 1-receptor stimulation alters glycogen and glucose metabolism. Br. J. Pharmacol. 128, 197-205.
27. Fredholm B. B., Dunwiddie T. V., Bergman B., and, Lindström K., (1984) Levels of adenosine and adenine nucleotides in slices of rat hippocampus. Brain Res. 295, 127-136.
28. Fredholm B. B., Chen J. F., Cunha R. A., Svenningsson P., and, Vaugeois J. M., (2005) Adenosine and brain function. Int. Rev. Neurobiol. 63, 191-270.
29. Frenguelli B. G., Llaudet E., and, Dale N., (2003) High-resolution real-time recording with microelectrode biosensors reveals novel aspects of adenosine release during hypoxia in rat hippocampal slices. J. Neurochem. 86, 1506-1515.
30. Gao Z., Downey H. F., Sun J., He M., and, Mallet R. T., (1997) Adenosine receptor blockade enhances glycolysis in hypoperfused guinea-pig myocardium. Cardiovasc. Res. 33, 31-44.
31. Gribkoff V. K., Bauman L. A., and, VanderMaelen C. P., (1990) The adenosine antagonist 8-cyclopentyltheophylline reduces the depression of hippocampal neuronal responses during hypoxia. Brain Res. 512, 353-357.
32. 13C NMR spectroscopy. J. Neurochem. 74, 327-333.
33. 13C MR spectroscopy. J. Neurochem. 79, 885-892.
34. Hertz L., Dringen R., Schousboe A., and, Robinson S. R., (1999) Astrocytes: Glutamate producers for neurons. J. Neurosci. Res. 57, 417-428.
35. Ikeda M., Busto R., Yoshida S., Santiso M., Martinez E., and, Ginsberg M. D., (1988) Cerebral phosphoinositide, triacylglycerol and energy metabolism during severe hypoxia and recovery. Brain Res. 459, 344-350.
36. 1 receptor. Proc. Natl Acad. Sci. USA 98, 9407-9412.
37. 13C] nuclear magnetic resonance spectroscopy in the guinea pig cerebral cortex in vitro. J. Neurosci. Res. 26, 356-369.
38. Lanz B., Gruetter R., and, Duarte J. M. N., (2013) Metabolic flux and compartmentation analysis in the brain in vivo. Front. Endocrinol. 4, 156.
39. Latini S., and, Pedata F., (2001) Adenosine in the central nervous system: Release mechanisms and extracellular concentrations. J. Neurochem. 79, 463-484.
40. A-mediated actions during hypoxia in the rat hippocampus. Brain Res. 732, 261-266.
41. Magistretti P. J., Hof P. R., and, Martin J. L., (1986) Adenosine stimulates glycogenolysis in mouse cerebral cortex: A possible coupling mechanism between neuronal activity and energy metabolism. J. Neurosci. 6, 2558-2562.
42. Martin R. L., Lloyd H. G. E., and, Cowan A. I., (1994) The early events of oxygen and glucose deprivation: Setting the scene for neuronal death? Trends Neurosci. 17, 251-257.
43. Martin E. D., Fernandez M., Perea G., Pascual O., Haydon P. G., Araque A., and, Cena V., (2007) Adenosine released by astrocytes contributes to hypoxia-induced modulation of synaptic transmission. Glia 55, 36-45.
44. de Mendonça A., Sebastião A. M., and, Ribeiro J. A., (2000) Adenosine: Does it have a neuroprotective role after all? Brain Res. Rev. 33, 258-274.
45. 13C NMR spectroscopy study of cortical nerve cell cultures exposed to hypoxia. J. Neurosci. Res. 38, 319-326.
46. Nicholls D. G., (2003) Bioenergetics and transmitter release in the isolated nerve terminal. Neurochem. Res. 28, 1433-1441.
47. Pellerin L., and, Magistretti P. J., (2012) Sweet sixteen for ANLS. J. Cereb. Blood Flow Metab. 32, 1152-1166.
48. Perreault P., and, Avoli M., (1989) Effects of low concentrations of 4-aminopyridine on CA1 pyramidal cells of the hippocampus. J. Neurophysiol. 61, 953-970.
49. Saransaari P., and, Oja S. S., (1998) Release of endogenous glutamate, aspartate, GABA, and taurine from hippocampal slices from adult and developing mice under cell-damaging conditions. Neurochem. Res. 23, 563-570.
50. Saransaari P., and, Oja S. S., (2000) Modulation of the ischemia-induced taurine release by adenosine receptors in the developing and adult mouse hippocampus. Neuroscience 97, 425-430.
51. Sebastião A. M., Cunha R. A., de Mendonça A., and, Ribeiro J. A., (2000) Modification of adenosine modulation of synaptic transmission in the hippocampus of aged rats. Br. J. Pharmacol. 131, 1629-1634.
52. Sebastião A. M., de Mendonça A., Moreira T., and, Ribeiro J. A., (2001) Activation of synaptic NMDA receptors by action potential-dependent release of transmitter during hypoxia impairs recovery of synaptic transmission on reoxygenation. J. Neurosci. 21, 8564-8571.
53. Sonnewald U., Müller T. B., Westergaard N., Unsgard G., Petersen S. B., and, Schousboe A., (1994) NMR spectroscopic study of cell cultures of astrocytes and neurons exposed to hypoxia: Compartmentation of astrocyte metabolism. Neurochem. Int. 24, 473-483.
54. 2+ and glutamate release. J. Neurochem. 53, 1693-1699.
55. Tretter L., and, Adam-Vizi V., (2004) Generation of reactive oxygen species in the reaction catalyzed by α-ketoglutarate dehydrogenase. J. Neurosci. 24, 7771-7778.
56. 13C-Labeled substrates and the cerebral metabolic compartmentalization of acetate and lactate. Brain Res. 992, 43-52.
57. Waniewski R. A., and, Martin D. L., (1998) Preferential utilization of acetate by astrocytes is attributable to transport. J. Neurosci. 18, 5225-5233.
58. Westergaard N., Sonnewald U., and, Schousboe A., (1995) Metabolic trafficking between neurons and astrocytes: The glutamate/glutamine cycle revisited. Dev. Neurosci. 17, 203-211.
59. Whittingham T. S., Lust W. D., Christakis D. A., and, Passonneau J. V., (1984) Metabolic stability of hippocampal slice preparations during prolonged incubation. J. Neurochem. 43, 689-696.
60. 1-adenosine receptors. Am. J. Physiol. 257, H1952-H1957.
61. Yang X., Hamner M. A., Brown A. M., Evans R. D., Ye Z. C., Chen S., and, Ransom B. R., (2014) Novel hypoglycemic injury mechanism: N-methyl-D-aspartate receptor-mediated white matter damage. Ann. Neurol. 75, 492-507.