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. 1990 Jun;100(2):269–276. doi: 10.1111/j.1476-5381.1990.tb15794.x

The actions of adenosine 5'-triphosphate on guinea-pig intracardiac neurones in culture.

T G Allen 1, G Burnstock 1
PMCID: PMC1917406  PMID: 2379032

Abstract

1. The actions of adenosine 5'-triphosphate (ATP) and related nucleotides and nucleosides on the membrane ion conductances of M and AH type intracardiac neurones cultured from ganglia within the atria and interatrial septum of newborn guinea-pig heart were studied with intracellular current- and voltage-clamp techniques. 2. Approximately 74% (120 out of 161) of AH type cells and 41% (5 out of 12) M cells responded to direct application of ATP (500 microM) onto their soma. 3. In 41% of M and 43% of AH type cells, focal application of ATP (500 microM) evoked rapid depolarization with an increase in conductance which frequently elicited action potential discharge. The underlying inward current had a null potential of -11.2 mV and was reduced in solutions containing low extracellular sodium and calcium but unaffected by reduced chloride-containing solutions. 4. In a further 31% of AH type cells, ATP evoked a multi-component response consisting of an initial depolarization followed by a hyperpolarization and a slow prolonged depolarization. The current underlying the initial depolarization resulted from an increase in conductance and had a null potential of -19.1 mV. The current was increased in low chloride-containing solutions and was only slightly reduced in low sodium- and calcium-containing solutions. The subsequent hyperpolarization and outward current resulted from an increase in membrane conductance and had a null potential of -88.5 mV, which was close to the potassium equilibrium potential in these cells. The slow depolarization and inward current was not associated with change in membrane conductance. 5. In less than 2% of AH cells, ATP evoked a second type of slow depolarization.(ABSTRACT TRUNCATED AT 250 WORDS)

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Selected References

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  1. Akasu T., Hirai K., Koketsu K. Modulatory actions of ATP on membrane potentials of bullfrog sympathetic ganglion cells. Brain Res. 1983 Jan 10;258(2):313–317. doi: 10.1016/0006-8993(83)91157-5. [DOI] [PubMed] [Google Scholar]
  2. Akasu T., Koketsu K. Effect of adenosine triphosphate on the sensitivity of the nicotinic acetylcholine-receptor in the bullfrog sympathetic ganglion cell. Br J Pharmacol. 1985 Feb;84(2):525–531. doi: 10.1111/j.1476-5381.1985.tb12937.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Akasu T., Shinnick-Gallagher P., Gallagher J. P. Adenosine mediates a slow hyperpolarizing synaptic potential in autonomic neurones. Nature. 1984 Sep 6;311(5981):62–65. doi: 10.1038/311062a0. [DOI] [PubMed] [Google Scholar]
  4. Allen T. G., Burnstock G. Intracellular studies of the electrophysiological properties of cultured intracardiac neurones of the guinea-pig. J Physiol. 1987 Jul;388:349–366. doi: 10.1113/jphysiol.1987.sp016618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Allen T. G., Burnstock G. M1 and M2 muscarinic receptors mediate excitation and inhibition of guinea-pig intracardiac neurones in culture. J Physiol. 1990 Mar;422:463–480. doi: 10.1113/jphysiol.1990.sp017995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Berne R. M. The role of adenosine in the regulation of coronary blood flow. Circ Res. 1980 Dec;47(6):807–813. doi: 10.1161/01.res.47.6.807. [DOI] [PubMed] [Google Scholar]
  7. Burnstock G., Kennedy C. Is there a basis for distinguishing two types of P2-purinoceptor? Gen Pharmacol. 1985;16(5):433–440. doi: 10.1016/0306-3623(85)90001-1. [DOI] [PubMed] [Google Scholar]
  8. Burnstock G. Purinergic nerves. Pharmacol Rev. 1972 Sep;24(3):509–581. [PubMed] [Google Scholar]
  9. Burnstock G., Warland J. J. P2-purinoceptors of two subtypes in the rabbit mesenteric artery: reactive blue 2 selectively inhibits responses mediated via the P2y-but not the P2x-purinoceptor. Br J Pharmacol. 1987 Feb;90(2):383–391. doi: 10.1111/j.1476-5381.1987.tb08968.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Crowe R., Burnstock G. Fluorescent histochemical localisation of quinacrine-positive neurones in the guinea-pig and rabbit atrium. Cardiovasc Res. 1982 Jul;16(7):384–390. doi: 10.1093/cvr/16.7.384. [DOI] [PubMed] [Google Scholar]
  11. Dolphin A. C., Forda S. R., Scott R. H. Calcium-dependent currents in cultured rat dorsal root ganglion neurones are inhibited by an adenosine analogue. J Physiol. 1986 Apr;373:47–61. doi: 10.1113/jphysiol.1986.sp016034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Drury A. N., Szent-Györgyi A. The physiological activity of adenine compounds with especial reference to their action upon the mammalian heart. J Physiol. 1929 Nov 25;68(3):213–237. doi: 10.1113/jphysiol.1929.sp002608. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gordon J. L. Extracellular ATP: effects, sources and fate. Biochem J. 1986 Jan 15;233(2):309–319. doi: 10.1042/bj2330309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Haas H. L., Greene R. W. Adenosine enhances afterhyperpolarization and accommodation in hippocampal pyramidal cells. Pflugers Arch. 1984 Nov;402(3):244–247. doi: 10.1007/BF00585506. [DOI] [PubMed] [Google Scholar]
  15. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  16. Hassall C. J., Burnstock G. Intrinsic neurones and associated cells of the guinea-pig heart in culture. Brain Res. 1986 Jan 29;364(1):102–113. doi: 10.1016/0006-8993(86)90991-1. [DOI] [PubMed] [Google Scholar]
  17. Hopwood A. M., Burnstock G. ATP mediates coronary vasoconstriction via P2x-purinoceptors and coronary vasodilatation via P2y-purinoceptors in the isolated perfused rat heart. Eur J Pharmacol. 1987 Apr 7;136(1):49–54. doi: 10.1016/0014-2999(87)90777-1. [DOI] [PubMed] [Google Scholar]
  18. Houston D. A., Burnstock G., Vanhoutte P. M. Different P2-purinergic receptor subtypes of endothelium and smooth muscle in canine blood vessels. J Pharmacol Exp Ther. 1987 May;241(2):501–506. [PubMed] [Google Scholar]
  19. Hume R. I., Thomas S. A. Multiple actions of adenosine 5'-triphosphate on chick skeletal muscle. J Physiol. 1988 Dec;406:503–524. doi: 10.1113/jphysiol.1988.sp017393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. IRVIN J. L., IRVIN E. M. The interaction of quinacrine with adenine nucleotides. J Biol Chem. 1954 Sep;210(1):45–56. [PubMed] [Google Scholar]
  21. Jahr C. E., Jessell T. M. ATP excites a subpopulation of rat dorsal horn neurones. Nature. 1983 Aug 25;304(5928):730–733. doi: 10.1038/304730a0. [DOI] [PubMed] [Google Scholar]
  22. KING T. S., COAKLEY J. B. The intrinsic nerve cells of the cardiac atria of mammals and man. J Anat. 1958 Jul;92(3):353–376. [PMC free article] [PubMed] [Google Scholar]
  23. Katayama Y., Morita K. Adenosine 5'-triphosphate modulates membrane potassium conductance in guinea-pig myenteric neurones. J Physiol. 1989 Jan;408:373–390. doi: 10.1113/jphysiol.1989.sp017464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kobayashi Y., Hassall C. J., Burnstock G. Culture of intramural cardiac ganglia of the newborn guinea-pig. I. Neuronal elements. Cell Tissue Res. 1986;244(3):595–604. doi: 10.1007/BF00212539. [DOI] [PubMed] [Google Scholar]
  25. Krishtal O. A., Marchenko S. M., Pidoplichko V. I. Receptor for ATP in the membrane of mammalian sensory neurones. Neurosci Lett. 1983 Jan 31;35(1):41–45. doi: 10.1016/0304-3940(83)90524-4. [DOI] [PubMed] [Google Scholar]
  26. Londos C., Cooper D. M., Wolff J. Subclasses of external adenosine receptors. Proc Natl Acad Sci U S A. 1980 May;77(5):2551–2554. doi: 10.1073/pnas.77.5.2551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Manzini S., Hoyle C. H., Burnstock G. An electrophysiological analysis of the effect of reactive blue 2, a putative P2-purinoceptor antagonist, on inhibitory junction potentials of rat caecum. Eur J Pharmacol. 1986 Aug 15;127(3):197–204. doi: 10.1016/0014-2999(86)90364-x. [DOI] [PubMed] [Google Scholar]
  28. Morita K., Katayama Y., Koketsu K., Akasu T. Actions of ATP on the soma of bullfrog primary afferent neurons and its modulating action on the GABA-induced response. Brain Res. 1984 Feb 20;293(2):360–363. doi: 10.1016/0006-8993(84)91243-5. [DOI] [PubMed] [Google Scholar]
  29. Palmer J. M., Wood J. D., Zafirov D. H. Purinergic inhibition in the small intestinal myenteric plexus of the guinea-pig. J Physiol. 1987 Jun;387:357–369. doi: 10.1113/jphysiol.1987.sp016577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Phillis J. W., Wu P. H. The role of adenosine and its nucleotides in central synaptic transmission. Prog Neurobiol. 1981;16(3-4):187–239. doi: 10.1016/0301-0082(81)90014-9. [DOI] [PubMed] [Google Scholar]
  31. Salt T. E., Hill R. G. Excitation of single sensory neurones in the rat caudal trigeminal nucleus by iontophoretically applied adenosine 5'-triphosphate. Neurosci Lett. 1983 Jan 31;35(1):53–57. doi: 10.1016/0304-3940(83)90526-8. [DOI] [PubMed] [Google Scholar]
  32. Segal M. Intracellular analysis of a postsynaptic action of adenosine in the rat hippocampus. Eur J Pharmacol. 1982 Apr 23;79(3-4):193–199. doi: 10.1016/0014-2999(82)90625-2. [DOI] [PubMed] [Google Scholar]
  33. Stone T. W. Physiological roles for adenosine and adenosine 5'-triphosphate in the nervous system. Neuroscience. 1981;6(4):523–555. doi: 10.1016/0306-4522(81)90145-7. [DOI] [PubMed] [Google Scholar]
  34. Su C. Purinergic neurotransmission and neuromodulation. Annu Rev Pharmacol Toxicol. 1983;23:397–411. doi: 10.1146/annurev.pa.23.040183.002145. [DOI] [PubMed] [Google Scholar]
  35. Trussell L. O., Jackson M. B. Adenosine-activated potassium conductance in cultured striatal neurons. Proc Natl Acad Sci U S A. 1985 Jul;82(14):4857–4861. doi: 10.1073/pnas.82.14.4857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. West G. A., Belardinelli L. Sinus slowing and pacemaker shift caused by adenosine in rabbit SA node. Pflugers Arch. 1985 Jan;403(1):66–74. doi: 10.1007/BF00583284. [DOI] [PubMed] [Google Scholar]
  37. Yatani A., Goto M., Tsuda Y. Nature of catecholamine-like actions of ATP and other energy rich nucleotides on the bullfrog atrial muscle. Jpn J Physiol. 1978;28(1):47–61. doi: 10.2170/jjphysiol.28.47. [DOI] [PubMed] [Google Scholar]
  38. van Calker D., Müller M., Hamprecht B. Adenosine regulates via two different types of receptors, the accumulation of cyclic AMP in cultured brain cells. J Neurochem. 1979 Nov;33(5):999–1005. doi: 10.1111/j.1471-4159.1979.tb05236.x. [DOI] [PubMed] [Google Scholar]

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