Adenosine and autocrine metabolic regulation of neuronal activity

Adenosine: A Key Link between Metabolism and Brain Activity

Volumn , Issue , 2013, Pages 71-85

  Kawamura, Masahito ^a   Ruskin, David N ^b  

^a JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b TRINITY COLLEGE   (United States)

Author keywords

Adenosine; Adenosine A1< inf> receptors; ATP; ATP release; ATP sensitive potassium channels; Autocrine regulation; Hippocampal CA3 pyramidal neurons; Pannexin 1 channels

Indexed keywords

EID: 84930328987     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4614-3903-5_4     Document Type: Chapter

References (105)

1. Anderson CM, Bergher JP, Swanson RA (2004) ATP-induced ATP release from astrocytes. J Neurochem 88:246-256
2. Andoh T, Ishiwa D, Kamiya Y, Echigo N, Goto T, Yamada Y (2006) A 1 adenosine receptormediated modulation of neuronal ATP-sensitive K channels in rat substantia nigra. Brain Res 1124:55-61
3. Anschel DJ, Ortega EL, Kraus AC, Fisher RS (2004) Focally injected adenosine prevents seizures in the rat. Exp Neurol 190:544-547
4. Baldwin SA, Beal PR, Yao SY, King AE, Cass CE, Young JD (2004) The equilibrative nucleoside transporter family, SLC29. P fl ugers Arch 447:735-743
5. Ballanyi K (2004) Protective role of neuronal K ATP channels in brain hypoxia. J Exp Biol 207: 3201-3212
6. Ballarin M, Fredholm BB, Ambrosio S, Mahy N (1991) Extracellular levels of adenosine and its metabolites in the striatum of awake rats: inhibition of uptake and metabolism. Acta Physiol Scand 142:97-103
7. Biber K, Klotz KN, Berger M, Gebicke-Härter PJ, van Calker D (1997) Adenosine A 1 receptormediated activation of phospholipase C in cultured astrocytes depends on the level of receptor expression. J Neurosci 17:4956-4964
8. Bough KJ, Wetherington J, Hassel B, Pare JF, Gawryluk JW, Greene JG, Shaw R, Smith Y, Geiger JD, Dingledine RJ (2006) Mitochondrial biogenesis in the anticonvulsant mechanism of the ketogenic diet. Ann Neurol 60:223-235
9. Brundege JM, Diao L, Proctor WR, Dunwiddie TV (1997) The role of cyclic AMP as a precursor of extracellular adenosine in the rat hippocampus. Neuropharmacology 36:1201-1210
10. Chen Y, Rathbone MP, Hertz L (2001) Guanosine-induced increase in free cytosolic calcium concentration in mouse astrocytes in primary cultures: does it act on an A3 adenosine receptor? J Neurosci Res 65:184-189
11. Coco S, Calegari F, Pravettoni E, Pozzi D, Taverna E, Rosa P, Matteoli M, Verderio C (2003) Storage and release of ATP from astrocytes in culture. J Biol Chem 278:1354-1362
12. Cunha RA, Ribeiro JA, Sebastiao AM (1994) Purinergic modulation of the evoked release of [ 3 H] acetylcholine from the hippocampus and cerebral cortex of the rat: role of the ectonucleotidases. Eur J Neurosci 6:33-42
13. Darby M, Kuzmiski JB, Panenka W, Feighan D, MacVicar BA (2003) ATP released from astrocytes during swelling activates chloride channels. J Neurophysiol 89:1870-1877
14. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8: 752-758
15. Davis LM, Pauly JR, Readnower RD, Rho JM, Sullivan PG (2008) Fasting is neuroprotective following traumatic brain injury. J Neurosci Res 86:1812-1822
16. Deng-Bryant Y, Prins ML, Hovda DA, Harris NG (2011) Ketogenic diet prevents alterations in brain metabolism in young but not adult rats after traumatic brain injury. J Neurotrauma 28: 1813-1825
17. DeVivo DC, Leckie MP, Ferrendelli JS, McDougal DB Jr. (1978) Chronic ketosis and cerebral metabolism. Ann Neurol 3:331-337
18. Dixon AK, Gubitz AK, Sirinathsinghji DJ, Richardson PJ, Freeman TC (1996) Tissue distribution of adenosine receptor mRNAs in the rat. Br J Pharmacol 118:1461-1468
19. Dunwiddie TV (1999) Adenosine and suppression of seizures. Adv Neurol 79:1001-1010
20. Dunwiddie TV, Diao L (2000) Regulation of extracellular adenosine in rat hippocampal slices is temperature dependent: role of adenosine transporters. Neuroscience 95:81-88
21. Dunwiddie TV, Diao L, Proctor WR (1997) Adenine nucleotides undergo rapid, quantitative conversion to adenosine in the extracellular space in rat hippocampus. J Neurosci 17:7673-7682
22. Dunwiddie TV, Hoffer BJ (1980) Adenine nucleotides and synaptic transmission in the in vitro rat hippocampus. Br J Pharmacol 69:59-68
23. Dunwiddie TV, Masino SA (2001) The role and regulation of adenosine in the central nervous system. Annu Rev Neurosci 24:31-55
24. El-Mallakh RS, Paskitti ME (2001) The ketogenic diet may have mood-stabilizing properties. Med Hypotheses 57:724-726
25. Ferré S, Ciruela F, Woods AS, Lluis C, Franco R (2007) Functional relevance of neurotransmitter receptor heteromers in the central nervous system. Trends Neurosci 30:440-446
26. Fields RD, Ni Y (2010) Nonsynaptic communication through ATP release from volume-activated anion channels in axons. Sci Signal 3:73
27. Fowler JC (1993) Purine release and inhibition of synaptic transmission during hypoxia and hypoglycemia in rat hippocampal slices. Neurosci Lett 157:83-86
28. Fredholm BB (1995) Purinoceptors in the nervous system. Pharmacol Toxicol 76:228-239
29. Fredholm BB (1997) Adenosine and neuroprotection. Int Rev Neurobiol 40:259-280
30. Fredholm BB, Arslan G, Halldner L, Kull B, Schulte G, Wasserman W (2000) Structure and function of adenosine receptors and their genes. Naunyn Schmiedebergs Arch Pharmacol 362:364-374
31. Fredholm BB, Lindström K, Wallman-Johansson A (1994) Propentofylline and other adenosine transport inhibitors increase the ef fl ux of adenosine following electrical or metabolic stimulation of rat hippocampal slices. J Neurochem 62:563-573
32. Freeman JM, Kossoff EH, Hartman AL (2007) The ketogenic diet: one decade later. Pediatrics 119:535-543
33. Frenguelli BG, Llaudet E, 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
34. Frenguelli BG, Wigmore G, Llaudet E, Dale N (2007) Temporal and mechanistic dissociation of ATP and adenosine release during ischaemia in the mammalian hippocampus. J Neurochem 101:1400-1413
35. Garré JM, Retamal MA, Cassina P, Barbeito L, Bukauskas FF, Sáez JC, Bennett MV, Abudara V (2010) FGF-1 induces ATP release from spinal astrocytes in culture and opens pannexin and connexin hemichannels. Proc Natl Acad Sci U S A 107:22659-22664
36. Goodman RR, Snyder SH (1982) Autoradiographic localization of adenosine receptors in rat brain using [ 3 H] cyclohexyladenosine. J Neurosci 2:1230-1241
37. Gray JH, Owen RP, Giacomini KM (2004) The concentrative nucleoside transporter family, SLC28. P fl ugers Arch 447:728-734
38. Greene AE, Todorova MT, McGowan R, Seyfried TN (2001) Caloric restriction inhibits seizure susceptibility in epileptic EL mice by reducing blood glucose. Epilepsia 42:1371-1378
39. Greene AE, Todorova MT, Seyfried TN (2003) Perspectives on the metabolic management of epilepsy through dietary reduction of glucose and elevation of ketone bodies. J Neurochem 86: 529-537
40. Hallböök T, Köhler S, Rosén I, Lundgren J (2007) Effects of ketogenic diet on epileptiform activity in children with therapy resistant epilepsy. Epilepsy Res 77:134-140
41. Hansen AJ, Hounsgaard J, Jahnsen H (1982) Anoxia increases potassium conductance in hippocampal nerve cells. Acta Physiol Scand 115:301-310
42. Hartman AL, Lyle M, Rogawski MA, Gasior M (2008) Ef fi cacy of the ketogenic diet in the 6-Hz seizure test. Epilepsia 49:334-339
43. Henderson GB, Strauss BP (1991) Evidence for cAMP and cholate extrusion in C6 rat glioma cells by a common anion ef fl ux pump. J Biol Chem 266:1641-1645
44. Hertz L, Peng L, Dienel GA (2007) Energy metabolism in astrocytes: high rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis. J Cereb Blood Flow Metab 27:219-249
45. Hu K, Li GR, Nattel S (1999) Adenosine-induced activation of ATP-sensitive K + channels in excised membrane patches is mediated by PKC. Am J Physiol 276:H488-495
46. Huttenlocher PR (1976) Ketonemia and seizures: metabolic and anticonvulsant effects of two ketogenic diets in childhood epilepsy. Pediatr Res 10:536-540
47. Inoue K (1998) ATP receptors for the protection of hippocampal functions. Jpn J Pharmacol 78: 405-410
48. Iwabuchi S, Kawahara K (2011) Functional signi fi cance of the negative-feedback regulation of ATP release via pannexin-1 hemichannels under ischemic stress in astrocytes. Neurochem Int 58:376-384
49. Johansson B, Halldner L, Dunwiddie TV, Masino SA, Poelchen W, Gimenez-Llort L, Escorihuela RM, Fernandez-Teruel A, Wiesenfeld-Hallin Z, Xu XJ et al (2001) Hyperalgesia, anxiety, and decreased hypoxic neuroprotection in mice lacking the adenosine A1 receptor. Proc Natl Acad Sci U S A 98:9407-9412
50. Jonzon B, Fredholm BB (1985) Release of purines, noradrenaline, and GABA from rat hippocampal slices by fi eld stimulation. J Neurochem 44:217-224
51. Joseph SM, Buchakjian MR, Dubyak GR (2003) Colocalization of ATP release sites and ecto-ATPase activity at the extracellular surface of human astrocytes. J Biol Chem 278: 23331-23342
52. Kaminogo M, Suyama K, Ichikura A, Onizuka M, Shibata S (1998) Anoxic depolarization determines ischemic brain injury. Neurol Res 20:343-348
53. Kang J, Kang N, Lovatt D, Torres A, Zhao Z, Lin J, Nedergaard M (2008) Connexin 43 hemichannels are permeable to ATP. J Neurosci 28:4702-4711
54. Kann O, Kovács R (2007) Mitochondria and neuronal activity. Am J Physiol Cell Physiol 292: C641-C657
55. Kawamura M Jr, Kawamura M (2011) Long-term facilitation of spontaneous calcium oscillations in astrocytes with endogenous adenosine in hippocampal slice cultures. Cell Calcium 49:249-258
56. Kawamura M Jr, Ruskin DN, Masino SA (2010) Metabolic autocrine regulation of neurons involves cooperation among pannexin hemichannels, adenosine receptors, and K ATP channels. J Neurosci 30:3886-3895
57. Kraft BD, Westman EC (2009) Schizophrenia, gluten, and low-carbohydrate, ketogenic diets: A case report and review of the literature. Nutr Metab (Lond) 6:10
58. Kulik A, Trapp S, Ballanyi K (2000) Ischemia but not anoxia evokes vesicular and Ca 2+-independent glutamate release in the dorsal vagal complex in vitro. J Neurophysiol 83:2905-2915
59. Latini S, Pedata F (2001) Adenosine in the central nervous system: release mechanisms and extracellular concentrations. J Neurochem 79:463-484
60. Liu GJ, Kalous A, Werry EL, Bennett MR (2006) Purine release from spinal cord microglia after elevation of calcium by glutamate. Mol Pharmacol 70:851-859
61. Liu HT, Sabirov RZ, Okada Y (2008a) Oxygen-glucose deprivation induces ATP release via maxianion channels in astrocytes. Purinergic Signal 4:147-154
62. Liu HT, Toychiev AH, Takahashi N, Sabirov RZ, Okada Y (2008b) Maxi-anion channel as a candidate pathway for osmosensitive ATP release from mouse astrocytes in primary culture. Cell Res 18:558-565
63. Lloyd HG, Lindström K, Fredholm BB (1993) Intracellular formation and release of adenosine from rat hippocampal slices evoked by electrical stimulation or energy depletion. Neurochem Int 23:173-185
64. MacVicar BA, Thompson RJ (2009) Non-junction functions of pannexin-1 channels. Trends Neurosci 33:93-102
65. Madry C, Haglerod C, Attwell D (2010) The role of pannexin hemichannels in the anoxic depolarization of hippocampal pyramidal cells. Brain 133:3755-3763
66. Mahan LC, McVittie LD, Smyk-Randall EM, Nakata H, Monsma FJ Jr, Gerfen CR, Sibley DR (1991) Cloning and expression of an A 1 adenosine receptor from rat brain. Mol Pharmacol 40:1-7
67. Mantis JG, Centeno NA, Todorova MT, McGowan R, Seyfried TN (2004) Management of multifactorial idiopathic epilepsy in EL mice with caloric restriction and the ketogenic diet: role of glucose and ketone bodies. Nutr Metab (Lond) 1:11
68. Martín ED, Fernández M, Perea G, Pascual O, Haydon PG, Araque A, Ceña V (2007) Adenosine released by astrocytes contributes to hypoxia-induced modulation of synaptic transmission. Glia 55:36-45
69. Masino SA, Diao L, Illes P, Zahniser NR, Larson GA, Johansson B, Fredholm BB, Dunwiddie TV (2002) Modulation of hippocampal glutamatergic transmission by ATP is dependent on adenosine A 1 receptors. J Pharmacol Exp Ther 303:356-363
70. Masino SA, Geiger JD (2008) Are purines mediators of the anticonvulsant/neuroprotective effects of ketogenic diets? Trends Neurosci 31:273-278
71. Masino SA, Kawamura M, Wasser CA, Pomeroy LT, Ruskin DN (2009) Adenosine, ketogenic diet and epilepsy: The emerging therapeutic relationship between metabolism and brain activity. Curr Neuropharmacol 7:257-268
72. Masino SA, Latini S, Bordini F, Pedata F, Dunwiddie TV (2001) Changes in hippocampal adenosine ef fl ux, ATP levels, and synaptic transmission induced by increased temperature. Synapse 41: 58-64
73. Masino SA, Li T, Theo fi las P, Sandau US, Ruskin DN, Fredholm BB, Geiger JD, Aronica E, Boison D (2011) A ketogenic diet suppresses seizures in mice through adenosine A 1 receptors. J Clin Invest 121:2679-2683
74. Miller LP, Hsu C (1992) Therapeutic potential for adenosine receptor activation in ischemic brain injury. J Neurotrauma 9(Suppl 2):S563-577
75. Muzykewicz DA, Lyczkowski DA, Memon N, Conant KD, Pfeifer HH, Thiele EA (2009) Ef fi cacy, safety, and tolerability of the low glycemic index treatment in pediatric epilepsy. Epilepsia 50:1118-1126
76. Nakazawa M, Kodama S, Matsuo T (1983) Effects of ketogenic diet on electroconvulsive threshold and brain contents of adenosine nucleotides. Brain Dev 5:375-380
77. Nylen K, Velazquez JL, Sayed V, Gibson KM, Burnham WM, Snead OC 3rd (2009) The effects of a ketogenic diet on ATP concentrations and the number of hippocampal mitochondria in Aldh5a1-/-mice. Biochim Biophys Acta 1790:208-212
78. Olah J, Klivenyi P, Gardian G, Vecsei L, Orosz F, Kovacs GG, Westerhoff HV, Ovadi J (2008) Increased glucose metabolism and ATP level in brain tissue of Huntington's disease transgenic mice. FEBS J 275:4740-4755
79. Pan JW, Bebin EM, Chu WJ, Hetherington HP (1999) Ketosis and epilepsy: 31 P spectroscopic imaging at 4.1T. Epilepsia 40:703-707
80. Pan WJ, Osmanovi SS, Shefner SA (1995) Characterization of the adenosine A 1 receptor-activated potassium current in rat locus ceruleus neurons. J Pharmacol Exp Ther 273:537-544
81. Pankratov Y, Lalo U, Verkhratsky A, North RA (2006) Vesicular release of ATP at central synapses. P fl ugers Arch Eur J Physiol 452:589-597
82. Parkinson FE, Xiong W, Zamzow CR (2005) Astrocytes and neurons: different roles in regulating adenosine levels. Neurol Res 27:153-160
83. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, Takano H, Moss SJ, McCarthy K, Haydon PG (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310:113-116
84. Peakman MC, Hill SJ (1994) Adenosine A 2B-receptor-mediated cyclic AMP accumulation in primary rat astrocytes. Br J Pharmacol 111:191-198
85. Ralevic V, Burnstock G (1998) Receptors for purines and pyrimidines. Pharmacol Rev 50: 413-492
86. Rezin GT, Amboni G, Zugno AI, Quevedo J, Streck EL (2009) Mitochondrial dysfunction and psychiatric disorders. Neurochem Res 34:1021-1029
87. Rho JM, Kim DW, Robbins CA, Anderson GD, Schwartzkroin PA (1999) Age-dependent differences in fl urothyl seizure sensitivity in mice treated with a ketogenic diet. Epilepsy Res 37: 233-240
88. Rosenberg PA, Knowles R, Knowles KP, Li Y (1994) Beta-adrenergic receptor-mediated regulation of extracellular adenosine in cerebral cortex in culture. J Neurosci 14:2953-2965
89. Rosin DL, Hettinger BD, Lee A, Linden J (2003) Anatomy of adenosine A 2A receptors in brain: morphological substrates for integration of striatal function. Neurology 61:S12-18
90. Rossi DJ, Oshima T, Attwell D (2000) Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 403:316-321
91. Rudolphi KA, Schubert P, Parkinson FE, Fredholm BB (1992) Adenosine and brain ischemia. Cerebrovasc Brain Metab Rev 4:346-369
92. Sas K, Robotka H, Toldi J, Vecsei L (2007) Mitochondria, metabolic disturbances, oxidative stress and the kynurenine system, with focus on neurodegenerative disorders. J Neurol Sci 257:221-239
93. Schock SC, Leblanc D, Hakim AM, Thompson CS (2008) ATP release by way of connexin 36 hemichannels mediates ischemic tolerance in vitro . Biochem Biophys Res Commun 368: 138-144
94. Schulte G, Fredholm BB (2003) Signalling from adenosine receptors to mitogen-activated protein kinases. Cell Signal 15:813-827
95. Sebastião AM, de Mendonca A, Moreira T, Ribeiro JA (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
96. Signoretti S, Marmarou A, Tavazzi B, Lazzarino G, Beaumont A, Vagnozzi R (2001) N-Acetylaspartate reduction as a measure of injury severity and mitochondrial dysfunction following diffuse traumatic brain injury. J Neurotrauma 18:977-991
97. Stone TW (2002) Purines and neuroprotection. Adv Exp Med Biol 513:249-280
98. Stout CE, Costantin JL, Naus CC, Charles AC (2002) Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem 277:10482-10488
99. Sweeney MI (1996) Adenosine release and uptake in cerebellar granule neurons both occur via an equilibrative nucleoside carrier that is modulated by G proteins. J Neurochem 67:81-88
100. Thompson RJ, Zhou N, MacVicar BA (2006) Ischemia opens neuronal gap junction hemichannels. Science 312:924-927
101. Thompson SM, Haas HL, Gähwiler BH (1992) Comparison of the actions of adenosine at pre-and postsynaptic receptors in the rat hippocampus in vitro . J Physiol 451:347-363
102. Uhlemann ER, Neims AH (1972) Anticonvulsant properties of the ketogenic diet in mice. J Pharmacol Exp Ther 180:231-238
103. Wardas J (2002) Neuroprotective role of adenosine in the CNS. Pol J Pharmacol 54:313-326
104. Wilder RM (1921) The effects of ketonemia on the course of epilepsy. Mayo Clin Bull 2: 307-308
105. Zhang L, Krnjevi K (1993) Whole-cell recording of anoxic effects on hippocampal neurons in slices. J Neurophysiol 69:118-127