Display options
Cite
Dale N. Real-time measurement of adenosine and ATP release in the central nervous system. Purinergic Signal. 2020;17(1):109-115doi: 10.1007/s11302-020-09733-y.
Dale, N. (2021). Real-time measurement of adenosine and ATP release in the central nervous system. Purinergic signalling, 17(1), 109-115. https://doi.org/10.1007/s11302-020-09733-y
Dale, Nicholas. "Real-time measurement of adenosine and ATP release in the central nervous system." Purinergic signalling vol. 17,1 (2021): 109-115. doi: https://doi.org/10.1007/s11302-020-09733-y
Dale N. Real-time measurement of adenosine and ATP release in the central nervous system. Purinergic Signal. 2021 Mar;17(1):109-115. doi: 10.1007/s11302-020-09733-y. Epub 2020 Oct 06. PMID: 33025425; PMCID: PMC7954901.
Copy Download .nbib Format: NLM
Share it on

Purinergic Signal. 2021 Mar;17(1):109-115. doi: 10.1007/s11302-020-09733-y. Epub 2020 Oct 06.

Real-time measurement of adenosine and ATP release in the central nervous system.

Purinergic signalling

Nicholas Dale

Affiliations

  1. School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK. [email protected].

PMID: 33025425 PMCID: PMC7954901 DOI: 10.1007/s11302-020-09733-y

Abstract

This brief review recounts how, stimulated by the work of Geoff Burnstock, I developed biosensors that allowed direct real-time measurement of ATP and adenosine during neural function. The initial impetus to create an adenosine biosensor came from trying to understand how ATP and adenosine-modulated motor pattern generation in the frog embryo spinal cord. Early biosensor measurements demonstrated slow accumulation of adenosine during motor activity. Subsequent application of these biosensors characterized real-time release of adenosine in in vitro models of brain ischaemia, and this line of work has recently led to clinical measurements of whole blood purine levels in patients undergoing carotid artery surgery or stroke. In parallel, the wish to understand the role of ATP signalling in the chemosensory regulation of breathing stimulated the development of ATP biosensors. This revealed that release of ATP from the chemosensory areas of the medulla oblongata preceded adaptive changes in breathing, triggered adaptive changes in breathing via activation of P2 receptors, and ultimately led to the discovery of connexin26 as a channel that mediates CO

Keywords: Biosensor; Breathing; Chemosensory; Connexin; Ischaemia; Motor pattern generation

References

  1. Dale N, Gilday D (1996) Regulation of rhythmic movements by purinergic neurotransmitters in frog embryos. Nature. 383(6597):259–263 - PubMed
  2. Zimmermann H (1996) Biochemistry, localization and functional roles of ecto-nucleotidases in the nervous system. Prog Neurobiol 49(6):589–618 - PubMed
  3. Gordon EL, Pearson JD, Slakey LL (1986) The hydrolysis of extracellular adenine nucleotides by cultured endothelial cells from pig aorta. Feed-forward inhibition of adenosine production at the cell surface. J Biol Chem 261(33):15496–15507 - PubMed
  4. Slakey LL, Cosimini K, Earls JP, Thomas C, Gordon EL (1986) Simulation of extracellular nucleotide hydrolysis and determination of kinetic constants for the ectonucleotidases. J Biol Chem 261(33):15505–15507 - PubMed
  5. James S, Richardson PJ (1993) Production of adenosine from extracellular ATP at the striatal cholinergic synapse. J Neurochem 60(1):219–227 - PubMed
  6. Dale N (1998) Delayed production of adenosine underlies temporal modulation of swimming in frog embryo. J Physiol Lond 511(Pt 1):265–272 - PubMed
  7. Dale N (2002) Resetting intrinsic Purinergic modulation of neural activity: an associative mechanism? J Neurosci 22(23):10461–10469 - PubMed
  8. Winn HR, Rubio R, Berne RM (1979) Brain adenosine production in the rat during 60 seconds of ischemia. Circ Res 45(4):486–492 - PubMed
  9. Van Wylen DG, Park TS, Rubio R, Berne RM (1986) Increases in cerebral interstitial fluid adenosine concentration during hypoxia, local potassium infusion, and ischemia. J Cereb Blood Flow Metab 6(5):522–528. https://doi.org/10.1038/jcbfm.1986.97 - PubMed
  10. Hillered L, Hallstrom A, Segersvard S, Persson L, Ungerstedt U (1989) Dynamics of extracellular metabolites in the striatum after middle cerebral artery occlusion in the rat monitored by intracerebral microdialysis. J Cereb Blood Flow Metab 9(5):607–616. https://doi.org/10.1038/jcbfm.1989.87 - PubMed
  11. Rudolphi KA, Schubert P, Parkinson FE, Fredholm BB (1992) Adenosine and brain ischemia. Cerebrovasc Brain Metab Rev 4(4):346–369 - PubMed
  12. Fowler JC (1993) Purine release and inhibition of synaptic transmission during hypoxia and hypoglycemia in rat hippocampal slices. Neurosci Lett 157(1):83–86 - PubMed
  13. Phillis JW, Smith-Barbour M, O'Regan MH, Perkins LM (1994) Amino acid and purine release in rat brain following temporary middle cerebral artery occlusion. Neurochem Res 19(9):1125–1130 - PubMed
  14. Zhao H, Asai S, Kanematsu K, Kunimatsu T, Kohno T, Ishikawa K (1997) Real-time monitoring of the effects of normothermia and hypothermia on extracellular glutamate re-uptake in the rat following global brain ischemia. Neuroreport. 8(9–10):2389–2393 - PubMed
  15. Latini S, Bordoni F, Corradetti R, Pepeu G, Pedata F (1998) Temporal correlation between adenosine outflow and synaptic potential inhibition in rat hippocampal slices during ischemia- like conditions. Brain Res 794(2):325–328 - PubMed
  16. Melani A, Pantoni L, Corsi C, Bianchi L, Monopoli A, Bertorelli R, Pepeu G, Pedata F (1999) Striatal outflow of adenosine, excitatory amino acids, gamma-aminobutyric acid, and taurine in awake freely moving rats after middle cerebral artery occlusion: correlations with neurological deficit and histopathological damage. Stroke. 30(11):2448–2454 discussion 55 - PubMed
  17. 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-London 526(1):143–155 - PubMed
  18. 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(6):1506–1515 - PubMed
  19. Tian F, Bibi F, Dale N, Imray CHE (2017) Blood purine measurements as a rapid real-time indicator of reversible brain ischaemia. Purinergic Signal 13:521–528. https://doi.org/10.1007/s11302-017-9578-z - PubMed
  20. 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(7):2298–2307 - PubMed
  21. Cosnier S (1997) Electropolymerization of amphiphilic monomers for designing amperometric biosensors. Electroanalysis. 9(12):894–902 - PubMed
  22. Llaudet E, Botting NP, Crayston JA, Dale N (2003) A three-enzyme microelectrode sensor for detecting purine release from central nervous system. Biosens Bioelectron 18(1):43–52 - PubMed
  23. Dale N, Llaudet E, Droniou M (2003) Sol-gel biosensors. European Patent Number EP 1 565 565 B1 - PubMed
  24. 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(5):1400–1413 - PubMed
  25. Zhou X, Teng B, Tilley S, Mustafa SJ (2013) A1 adenosine receptor negatively modulates coronary reactive hyperemia via counteracting A2A-mediated H2O2 production and KATP opening in isolated mouse hearts. Am J Physiol Heart Circ Physiol 305(11):H1668–H1H79. https://doi.org/10.1152/ajpheart.00495.2013 - PubMed
  26. White BC, Sullivan JM, DeGracia DJ, O'Neil BJ, Neumar RW, Grossman LI et al (2000) Brain ischemia and reperfusion: molecular mechanisms of neuronal injury. J Neurol Sci 179(S 1–2):1–33 - PubMed
  27. Tian F, Llaudet E, Dale N (2007) Ruthenium purple-mediated microelectrode biosensors based on sol-gel film. Anal Chem 79(17):6760–6766. https://doi.org/10.1021/ac070822f - PubMed
  28. Dale N, Tian F, Sagoo R, Phillips N, Imray C, Roffe C (2019) Point-of-care measurements reveal release of purines into venous blood of stroke patients. Purinergic Signal 15:237–246. https://doi.org/10.1007/s11302-019-09647-4 - PubMed
  29. Thomas T, Spyer KM (2000) ATP as a mediator of mammalian central CO - PubMed
  30. Thomas T, Ralevic V, Bardini M, Burnstock G, Spyer KM (2001) Evidence for the involvement of purinergic signalling in the control of respiration. Neuroscience. 107(3):481–490 - PubMed
  31. Gourine AV, Llaudet E, Dale N, Spyer KM (2005) ATP is a mediator of chemosensory transduction in the central nervous system. Nature. 436(7047):108–111. https://doi.org/10.1038/nature03690 - PubMed
  32. Huckstepp RT, Bihi R i, Eason R, Spyer KM, Dicke N, Willecke K et al (2010) Connexin hemichannel-mediated CO - PubMed
  33. Huckstepp RT, Eason R, Sachdev A, Dale N (2010) CO - PubMed
  34. Albery WJ, Galley PT, Murphy LJ (1993) A dialysis electrode for glycerol. J Electroanal Chem 344(1–2):161–166 - PubMed
  35. Llaudet E, Hatz S, Droniou M, Dale N (2005) Microelectrode biosensor for real-time measurement of ATP in biological tissue. Anal Chem 77(10):3267–3273 - PubMed
  36. Gourine AV, Kasymov V, Marina N, Tang F, Figueiredo MF, Lane S, Teschemacher AG, Spyer KM, Deisseroth K, Kasparov S (2010) Astrocytes control breathing through pH-dependent release of ATP. Science. 329(5991):571–575. https://doi.org/10.1126/science.1190721 - PubMed
  37. Turovsky E, Theparambil SM, Kasymov V, Deitmer JW, Del Arroyo AG, Ackland GL et al (2016) Mechanisms of CO - PubMed
  38. Meigh L, Greenhalgh SA, Rodgers TL, Cann MJ, Roper DI, Dale N (2013) CO - PubMed
  39. van de Wiel J, Meigh L, Bhandare A, Cook J, Nijjar S, Huckstepp RT, Dale N (2020) Connexin26 mediates CO - PubMed
  40. Brotherton DH, Savva C, Ragan T, Linthwaite V, Cann M, Dale N, et al. Conformational changes and channel gating induced by CO - PubMed

Publication Types

Grant support