The Library
Intracellular ATP influences synaptic plasticity in area CA1 of rat hippocampus via metabolism to adenosine and activity-dependent activation of adenosine A1 receptors
Tools
Zur Nedden, Stephanie, Hawley, Simon, Pentland, Naomi, Hardie, D. G. (D. Grahame), Doney, Alexander S. and Frenguelli, Bruno G.. (2011) Intracellular ATP influences synaptic plasticity in area CA1 of rat hippocampus via metabolism to adenosine and activity-dependent activation of adenosine A1 receptors. The Journal of Neuroscience, Vol.31 (No.16). pp. 6221-6234. ISSN 1529-2401
|
PDF
WRAP_Frenguelli_6221.full.pdf - Published Version - Requires a PDF viewer such as GSview, Xpdf or Adobe Acrobat Reader Download (1857Kb) |
Official URL: http://dx.doi.org/10.1523/JNEUROSCI.4039-10.2011
Abstract
The extent to which brain slices reflect the energetic status of the in vivo brain has been a subject of debate. We addressed this issue to investigate the recovery of energetic parameters and adenine nucleotides in rat hippocampal slices and the influence this has on synaptic transmission and plasticity.Weshow that, although adenine nucleotide levels recover appreciably within 10minof incubation, it takes 3 h for a full recovery of the energy charge (to >= 0.93) and that incubation of brain slices at 34°C results in a significantly higher ATP/AMP ratio and a threefold lower activity of AMP-activated protein kinase compared with slices incubated at room temperature. Supplementation of artificial CSF with D-ribose and adenine (Rib/Ade) increased the total adenine nucleotide pool of brain slices, which, when corrected for the influence of the dead cut edges, closely approached in vivo values. Rib/Ade did not affect basal synaptic transmission or paired-pulse facilitation but did inhibit long-term potentiation (LTP) induced by tetanic or weak theta-burst stimulation. This decrease in LTP was reversed by strong theta-burst stimulation or antagonizing the inhibitory adenosine A1 receptor suggesting that the elevated tissue ATP levels had resulted in greater activity-dependent adenosine release during LTP induction. This was confirmed by direct measurement of adenosine release with adenosine biosensors. These observations provide new insight into the recovery of adenine nucleotides after slice preparation, the sources of loss of such compounds in brain slices, the means by which to restore them, and the functional consequences of doing so.
| Item Type: | Journal Article |
|---|---|
| Subjects: | Q Science > QP Physiology |
| Divisions: | Faculty of Science > Life Sciences (2010- ) |
| Library of Congress Subject Headings (LCSH): | Neurophysiology, Rats -- Physiology, Adenine nucleotides |
| Journal or Publication Title: | The Journal of Neuroscience |
| Publisher: | Society for Neuroscience |
| ISSN: | 1529-2401 |
| Date: | 20 April 2011 |
| Volume: | Vol.31 |
| Number: | No.16 |
| Page Range: | pp. 6221-6234 |
| Identification Number: | 10.1523/JNEUROSCI.4039-10.2011 |
| Status: | Peer Reviewed |
| Access rights to Published version: | Restricted or Subscription Access |
| Funder: | Research into Ageing (Charitable trust), European Commission (EC) |
| Grant number: | LSHM-CT-2004-005272 (EC) |
| References: | Almeida T, Rodrigues RJ, de Mendonc¸a A, Ribeiro JA, Cunha RA (2003) Purinergic P2 receptors trigger adenosine release leading to adenosine A2A receptor activation and facilitation of long-term potentiation in rat hippocampal slices. Neuroscience 122:111–121. Arai A, Lynch G (1992) Factors regulating the magnitude of long-term potentiation induced by theta pattern stimulation. Brain Res 598:173–184. Atkinson DE (1968) The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry 7:4030 – 4034. Baldwin SA, Beal PR, Yao SY, King AE, Cass CE, Young JD (2004) The equilibrative nucleoside transporter family, SLC29. Pflugers Arch 447:735–743. Barsotti C, Ipata PL (2002) Pathways for alpha-D-ribose utilization for nucleobase salvage and 5-fluorouracil activation in rat brain. Biochem Pharmacol 63:117–122. Bender E, Buist A, Jurzak M, Langlois X, Baggerman G, Verhasselt P, Ercken M, Guo HQ, Wintmolders C, Van den Wyngaert I, Van Oers I, Schoofs L, Luyten W (2002) Characterization of an orphan G protein-coupled receptor localized in the dorsal root ganglia reveals adenine as a signaling molecule. Proc Natl Acad Sci U S A 99:8573– 8578. Boison D, Stewart KA (2009) Therapeutic epilepsy research: from pharmacological rationale to focal adenosine augmentation. Biochem Pharmacol 78:1428 –1437. Camilo O, Goldstein LB (2004) Seizures and epilepsy after ischemic stroke. Stroke 35:1769 –1775. Chen LY, Rex CS, Sanaiha Y, Lynch G, Gall CM (2010) Learning induces neurotrophin signaling at hippocampal synapses. Proc Natl Acad Sci U S A 107:7030 –7035. Costenla AR, Lopes LV, de Mendonc¸a A, Ribeiro JA (2001) Afunctional role for adenosine A3 receptors: modulation of synaptic plasticity in the rat hippocampus. Neurosci Lett 302:53–57. Dale N, Frenguelli BG (2009) Release of adenosine and ATP during ischemia and epilepsy. Curr Neuropharmacol 7:160 –179. Dale N, Pearson T, Frenguelli BG (2000) Direct measurement of adenosine release during hypoxia in the CA1 region of the rat hippocampal slice. J Physiol 526:143–155. de Mendonc¸a A, Ribeiro JA (1994) Endogenous adenosine modulates longterm potentiation in the hippocampus. Neuroscience 62:385–390. de Mendonc¸a A, Ribeiro JA (2000) Long-term potentiation observed upon blockade of adenosine A1 receptors in rat hippocampus is N-methyl-Daspartate receptor-dependent. Neurosci Lett 291:81– 84. Edwards FA, Konnerth A, Sakmann B, Takahashi T (1989) Athin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system. Pflugers Arch 414:600–612. Etherington LA, Patterson GE, Meechan L, Boison D, Irving AJ, Dale N, Frenguelli BG (2009) Astrocytic adenosine kinase regulates basal synaptic adenosine levels and seizure activity but not activity-dependent adenosine release in the hippocampus. Neuropharmacology 56:429–437. Feig S, Lipton P (1990) N-methyl-D-aspartate receptor activation and Ca2 account for poor pyramidal cell structure in hippocampal slices. J Neurochem 55:473– 483. Forghani R, Krnjevic´ K (1995) Adenosine antagonists have differential effects on induction of long-term potentiation in hippocampal slices. Hippocampus 5:71–77. Fredholm BB, Dunwiddie TV, Bergman B, Lindstro¨m K (1984) Levels of adenosine and adenine nucleotides in slices of rat hippocampus. Brain Res 295:127–136. 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. 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. Fujii S, Kuroda Y, Ito K, Kaneko K, Kato H (1999) Effects of adenosine receptors on the synaptic and EPSP-spike components of long-term potentiation and depotentiation in the guinea-pig hippocampus. J Physiol 521:451– 466. Fujii S, Kato H, Ito K, Itoh S, Yamazaki Y, Sasaki H, Kuroda Y (2000) Effects of A1 and A2 adenosine receptor antagonists on the induction and reversal of long-term potentiation in guinea pig hippocampal slices of CA1 neurons. Cell Mol Neurobiol 20:331–350. Gadalla AE, Pearson T, Currie AJ, Dale N, Hawley SA, Sheehan M, Hirst W, Michel AD, Randall A, Hardie DG, Frenguelli BG (2004) AICA riboside both activates AMP-activated protein kinase and competes with adenosine for the nucleoside transporter in the CA1 region of the rat hippocampus. J Neurochem 88:1272–1282. Gerlach E, Marko P, Zimmer HG, Pechan I, Trendelenburg C (1971) Different response of adenine nucleotide synthesis de novo in kidney and brain during aerobic recovery from anoxia and ischemia. Experientia 27:876–878. Hardie DG (2007) AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 8:774 –785. Hardie DG, Frenguelli BG (2007) A neural protection racket: AMPK and the GABA(B) receptor. Neuron 53:159 –162. Hardie DG, Hawley SA (2001) AMP-activated protein kinase: the energy charge hypothesis revisited. Bioessays 23:1112–1119. Hardie DG, Salt IP, Davies SP (2000) Analysis of the role of the AMPactivated protein kinase in the response to cellular stress. Methods Mol Biol 99:63–74. Hardie DG, Hawley SA, Scott JW (2006) AMP-activated protein kinase– development of the energy sensor concept. J Physiol 574:7–15. Hawley SA, Boudeau J, Reid JL, Mustard KJ, Udd L, Ma¨kela¨ TP, Alessi DR, Hardie DG (2003) Complexes between the LKB1 tumor suppressor, STRAD alpha/beta and MO25 alpha/beta are upstream kinases in the AMP-activated protein kinase cascade. J Biol 2:28. Hawley SA, Pan DA, Mustard KJ, Ross L, Bain J, Edelman AM, Frenguelli BG, Hardie DG (2005) Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab 2:9 –19. Ho OH, Delgado JY, O’Dell TJ (2004) Phosphorylation of proteins involved in activity-dependent forms of synaptic plasticity is altered in hippocampal slices maintained in vitro. J Neurochem 91:1344 –1357. Hossmann KA (2008) Cerebral ischemia: models, methods and outcomes. Neuropharmacology 55:257–270. Kadam SD, WhiteAM,Staley KJ, Dudek FE (2010) Continuous electroencephalographic monitoring with radio-telemetry in a rat model of perinatal hypoxia-ischemia reveals progressive post-stroke epilepsy. J Neurosci 30:404–415. Kass IS, Lipton P (1982) Mechanisms involved in irreversible anoxic damage to the in vitro rat hippocampal slice. J Physiol 332:459–472. Kawamura M Jr, Ruskin DN, Masino SA (2010) Metabolic autocrine regulation of neurons involves cooperation among pannexin hemichannels, adenosine receptors, and KATP channels. J Neurosci 30:3886 –3895. Kessey K, Mogul DJ (1998) Adenosine A2 receptors modulate hippocampal synaptic transmission via a cyclic-AMP-dependent pathway. Neuroscience 84:59–69. Klyuch BP, Richardson MJ, Dale N, Wall MJ (2011) The dynamics of single spike-evoked adenosine release in the cerebellum. J Physiol 589:283–295. Kobayashi M, Lust WD, Passonneau JV (1977) Concentrations of energy metabolites and cyclic nucleotides during and after bilateral ischemia in the gerbil cerebral cortex. J Neurochem 29:53–59. Kuramoto N, Wilkins ME, Fairfax BP, Revilla-Sanchez R, Terunuma M, Tamaki K, Iemata M, Warren N, Couve A, Calver A, Horvath Z, Freeman K, Carling D,HuangL, Gonzales C, Cooper E, Smart TG, PangalosMN,MossSJ (2007) Phospho-dependent functional modulation of GABA(B) receptors by the metabolic sensor AMP-dependent protein kinase. Neuron 53:233–247. Larson J, Wong D, Lynch G (1986) Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res 368:347–350. Ljunggren B, Ratcheson RA, Siesjo¨ BK (1974) Cerebral metabolic state following complete compression ischemia. Brain Res 73:291–307. Lu Q, Wang J (2008) Single molecule conformational dynamics of adenylate kinase: energy landscape, structural correlations, and transition state ensembles. J Am Chem Soc 130:4772– 4783. Mascia L, Cappiello M, Cherri S, Ipata PL (2000) In vitro recycling of alpha- D-ribose 1-phosphate for the salvage of purine bases. Biochim Biophys Acta 1474:70 –74. Masino SA, Geiger JD (2008) Are purines mediators of the anticonvulsant/ neuroprotective effects of ketogenic diets? Trends Neurosci 31:273–278. McIlwain H (1952) Phosphates of brain during in vitro metabolism: effects of oxygen, glucose, glutamate, glutamine, and calcium and potassium salts. Biochem J 52:289 –295. McIlwain H, Buchel L, Cheshire JD (1951) The inorganic phosphate and phosphocreatine of Brain especially during metabolism in vitro. Biochem J 48:12–20. Milusheva EA, Do´da M, Baranyi M, Vizi ES (1996) Effect of hypoxia and glucose deprivation on ATP level, adenylate energy charge and [Ca 2]odependent and independent release of [ 3H]dopamine in rat striatal slices. Neurochem Int 28:501–507. Mu¨ller CE, Iqbal J, Baqi Y, Zimmermann H, Ro¨llich A, Stephan H (2006) Polyoxometalates: a new class of potent ecto-nucleoside triphosphate diphosphohydrolase (NTPDase) inhibitors. Bioorg Med Chem Lett 16:5943–5947. Nowak TS Jr, Fried RL, Lust WD, Passonneau JV (1985) Changes in brain energy metabolism and protein synthesis following transient bilateral ischemia in the gerbil. J Neurochem 44:487– 494. Omran H, Illien S, MacCarter D, St Cyr J, Lu¨deritz B (2003) D-Ribose improves diastolic function and quality of life in congestive heart failure patients: a prospective feasibility study. Eur J Heart Fail 5:615– 619. Paschen W, Djuricic B (1995) Comparison of in vitro ischemia-induced disturbances in energy metabolism and protein synthesis in the hippocampus of rats and gerbils. J Neurochem 65:1692–1697. Pearson T, Nuritova F, Caldwell D, Dale N, Frenguelli BG (2001) A depletable pool of adenosine in area CA1 of the rat hippocampus. J Neurosci 21:2298 –2307. Phillis JW, Perkins LM, Smith-Barbour M, O’Regan MH (1995) Oxypurinolenhanced postischemic recovery of the rat brain involves preservation of adenine nucleotides. J Neurochem 64:2177–2184. Potter WB, O’Riordan KJ, Barnett D, Osting SM, Wagoner M, Burger C, Roopra A (2010) Metabolic regulation of neuronal plasticity by the energy sensor AMPK. PLoS One 5:e8996. Redondo RL, Okuno H, Spooner PA, Frenguelli BG, Bito H, Morris RG (2010) Synaptic tagging and capture: differential role of distinct calcium/ calmodulin kinases in protein synthesis-dependent long-term potentiation. J Neurosci 30:4981– 4989. Rex CS, Krama´r EA, Colgin LL, Lin B, Gall CM, Lynch G (2005) Long-term potentiation is impaired in middle-aged rats: regional specificity and reversal by adenosine receptor antagonists. J Neurosci 25:5956 –5966. Sajikumar S, Frey JU (2004) Late-associativity, synaptic tagging, and the role of dopamine during LTP and LTD. Neurobiol Learn Mem 82:12–25. Sajikumar S, Navakkode S, Frey JU (2005) Protein synthesis-dependent long-term functional plasticity: methods and techniques. Curr Opin Neurobiol 15:607– 613. Sanders MJ, Grondin PO, Hegarty BD, Snowden MA, Carling D (2007) Investigating the mechanism for AMP activation of the AMP-activated protein kinase cascade. Biochem J 403:139 –148. Schurr A, Rigor BM (1989) Cerebral ischemia revisited: new insights as revealed using in vitro brain slice preparations. Experientia 45:684–695. Shecterle LM, Terry KR, St Cyr JA (2010) The patented uses of D-ribose in cardiovascular diseases. Recent Pat Cardiovasc Drug Discov 5:138 –142. Sheng XR, Li X, Pan XM (1999) An iso-random Bi Bi mechanism for adenylate kinase. J Biol Chem 274:22238 –22242. Siklo´ s L, Kuhnt U, Pa´rducz A, Szerdahelyi P (1997) Intracellular calcium redistribution accompanies changes in total tissue Na, K and water during the first two hours of in vitro incubation of hippocampal slices. Neuroscience 79:1013–1022. Simmonds HA (1986) 2,8-Dihydroxyadenine lithiasis–epidemiology, pathogenesis and therapy. Verh Dtsch Ges Inn Med 92:503–508. Sperla´gh B, Szabo´ G, Erde´lyi F, Baranyi M, Vizi ES (2003) Homo- and heteroexchange of adenine nucleotides and nucleosides in rat hippocampal slices by the nucleoside transport system. Br J Pharmacol 139:623– 633. Thomas J (1957) The composition of isolated cerebral tissue; purines. Biochem J 66:655– 658. Tuerk RD, Thali RF, Auchli Y, Rechsteiner H, Brunisholz RA, Schlattner U, Wallimann T, Neumann D (2007) New candidate targets of AMPactivated protein kinase in murine brain revealed by a novel multidimensional substrate-screen for protein kinases. J Proteome Res 6:3266 –3277. von Ku¨gelgen I, Schiedel AC, Hoffmann K, Alsdorf BB, Abdelrahman A, Mu¨ller CE (2008) Cloning and functional expression of a novel Gi protein-coupled receptor for adenine from mouse brain. Mol Pharmacol 73:469–477. Wall M, Dale N (2008) Activity-dependent release of adenosine: a critical re-evaluation of mechanism. Curr Neuropharmacol 6:329 –337. Wall MJ, Wigmore G, Lopata´r J, Frenguelli BG, Dale N (2008) The novel NTPDase inhibitor sodium polyoxotungstate (POM-1) inhibits ATP breakdown but also blocks central synaptic transmission, an action independent of NTPDase inhibition. Neuropharmacology 55:1251–1258. Watts RW, McKeran RO, Brown E, Andrews TM, Griffiths MI (1974) Clinical and biochemical studies on treatment of Lesch-Nyhan syndrome. Arch Dis Child 49:693–702. Whittingham TS, Lust WD, Passonneau JV (1984a) An in vitro model of ischemia: metabolic and electrical alterations in the hippocampal slice. J Neurosci 4:793– 802. Whittingham TS, Lust WD, Christakis DA, Passonneau JV (1984b) Metabolic stability of hippocampal slice preparations during prolonged incubation. J Neurochem 43:689–696. Whittingham TS, Warman E, Assaf H, Sick TJ, LaManna JC (1989) Manipulating the intracellular environment of hippocampal slices:pHand highenergy phosphates. J Neurosci Methods 28:83–91. Woods A, Salt I, Scott J, Hardie DG, Carling D (1996) The alpha1 and alpha2 isoforms of the AMP-activated protein kinase have similar activities in rat liver but exhibit differences in substrate specificity in vitro. FEBS Lett 397:347–351. Woods A, Dickerson K, Heath R, Hong SP, Momcilovic M, Johnstone SR, Carlson M, Carling D (2005) Ca2/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab 2:21–33. Wyatt CN, Mustard KJ, Pearson SA, Dallas ML, Atkinson L, Kumar P, Peers C, Hardie DG, Evans AM (2007) AMP-activated protein kinase mediates carotid body excitation by hypoxia. J Biol Chem 282:8092– 8098. Zimmer HG (1998) Significance of the 5-phosphoribosyl-1-pyrophosphate pool for cardiac purine and pyrimidine nucleotide synthesis: studies with ribose, adenine, inosine, and orotic acid in rats. Cardiovasc Drugs Ther 12 [Suppl 2]:179 –187. zur Nedden S, Eason R, Doney AS, Frenguelli BG (2009) An ion-pair reversed-phase HPLC method for determination of fresh tissue adenine nucleotides avoiding freeze-thaw degradation of ATP. Anal Biochem 388: 108–114. |
| URI: | http://wrap.warwick.ac.uk/id/eprint/36117 |
Data sourced from Thomson Reuters' Web of Knowledge
Actions (login required)
![]() |
View Item |
Tools
Tools

