Direct Evidence Against a Role of ATP As the Nonadrenergic, Noncholinergic Inhibitory Neurotransmitter in Guinea Pig Tenia Coli

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1982 Nov 1

PMID 6129625

Citations 11

Authors

D P Westfall

G K Hogaboom

J Colby

J P Odonnell

J S Fedan

Affiliations

Soon will be listed here.

Abstract

Electrical field stimulation of the isolated guinea pig tenia coli in the presence of a muscarinic receptor antagonist (atropine) and an adrenergic neuron blocker (guanethidine) produces relaxation. A large amount of indirect evidence has suggested that the neurotransmitter that is released from these nonadrenergic, noncholinergic inhibitory neurons is ATP or a related nucleotide, and the nerves have been termed "purinergic." A photoaffinity analog of ATP, arylazido aminopropionyl ATP, which produces a specific pharmacological antagonism of P2 purinergic receptors in isolated guinea pig vas deferens and urinary bladder, was utilized in the present study to evaluate directly whether ATP is the nonadrenergic, noncholinergic inhibitory neurotransmitter in tenia coli. By blocking postjunctional P2 receptors, arylazido aminopropionyl ATP produced a pronounced antagonism of relaxations induced by exogenously added ATP. Responses produced by ADP, AMP, and adenosine also were antagonized by arylazido aminopropionyl ATP, but to a lesser extent. Inhibitory responses to isoproterenol were not antagonized. Under these conditions of established, specific P2-receptor blockade of responses to exogenously added ATP, relaxations induced by field stimulation of intrinsic inhibitory nerves in the presence of atropine (1 microM) and guanethidine (1 microM) were not antagonized. Though these results provide no indication of the actual substance involved, they suggest strongly that the nonadrenergic, noncholinergic inhibitory neurotransmitter in the guinea pig tenia coli is not ATP.

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References

Burnstock G, Campbell G, Satchell D, Smythe A . Evidence that adenosine triphosphate or a related nucleotide is the transmitter substance released by non-adrenergic inhibitory nerves in the gut. Br J Pharmacol. 1970; 40(4):668-88. PMC: 1702901. DOI: 10.1111/j.1476-5381.1970.tb10646.x. View

Burnstock G . Neural nomenclature. Nature. 1971; 229(5282):282-3. DOI: 10.1038/229282d0. View

Burnstock G, Dumsday B, Smythe A . Atropine resistant excitation of the urinary bladder: the possibility of transmission via nerves releasing a purine nucleotide. Br J Pharmacol. 1972; 44(3):451-61. PMC: 1665813. DOI: 10.1111/j.1476-5381.1972.tb07283.x. View

Burnstock G . Purinergic nerves. Pharmacol Rev. 1972; 24(3):509-81. View

COBURN R, Tomita T . Evidence for nonadrenergic inhibitory nerves in the guinea pig trachealis muscle. Am J Physiol. 1973; 224(5):1072-80. DOI: 10.1152/ajplegacy.1973.224.5.1072. View

Satchell D, Burnstock G, Dann P . Antagonism of the effects of purinergic nerve stimulation and exogenously applied ATP on the guinea-pig taenia coli by 2-substituted imidazolines and related compounds. Eur J Pharmacol. 1973; 23(3):264-9. DOI: 10.1016/0014-2999(73)90093-9. View

Coleman R, Levy G . A non-adrenergic inhibitory nervous pathway in guinea-pig trachea. Br J Pharmacol. 1974; 52(2):167-74. PMC: 1776879. DOI: 10.1111/j.1476-5381.1974.tb09697.x. View

Spedding M, Sweetman A, WEETMAN D . Antagonism of adenosine 5'-triphosphate-induced relaxation by 2-2'-pyridylisatogen in the taenia of guinea-pig caecum. Br J Pharmacol. 1975; 53(4):575-83. PMC: 1666311. DOI: 10.1111/j.1476-5381.1975.tb07397.x. View

Burnstock G, Cocks T, Paddle B, STASZEWSKA-BARCZAK J . Evidence that prostaglandin is responsible for the 'rebound contraction' following stimulation of non-adrenergic, non-cholinergic ('purinergic') inhibitory nerves. Eur J Pharmacol. 1975; 31(2):360-2. DOI: 10.1016/0014-2999(75)90060-6. View

10.

Jeng S, Guillory R . The use of aryl azido ATP analogs as photoaffinity labels for myosin ATPase. J Supramol Struct. 1975; 3(5-6):448-68. DOI: 10.1002/jss.400030506. View

11.

Coleman R . Effects of some purine derivatives on the guinea-pig trachea and their interaction with drugs that block adenosine uptake. Br J Pharmacol. 1976; 57(1):51-7. PMC: 1667005. DOI: 10.1111/j.1476-5381.1976.tb07655.x. View

12.

Kamikawa Y, Shimo Y . Mediation of prostaglandin E2 in the biphasic response to ATP of the isolated tracheal muscle of guinea-pigs. J Pharm Pharmacol. 1976; 28(4):294-7. DOI: 10.1111/j.2042-7158.1976.tb04156.x. View

13.

Richardson J, Beland J . Nonadrenergic inhibitory nervous system in human airways. J Appl Physiol. 1976; 41(5 Pt. 1):764-71. DOI: 10.1152/jappl.1976.41.5.764. View

14.

Burnstock G . Purinergic receptors. J Theor Biol. 1976; 62(2):491-503. DOI: 10.1016/0022-5193(76)90133-8. View

15.

CARPENTER F . Atropine resistance and muscarinic receptors in the rat urinary bladder. Br J Pharmacol. 1977; 59(1):43-9. PMC: 1667706. DOI: 10.1111/j.1476-5381.1977.tb06975.x. View

16.

Downie J, Dean D . The contribution of cholinergic postganglionic neurotransmission to contractions of rabbit detrusor. J Pharmacol Exp Ther. 1977; 203(2):417-25. View

17.

Okwuasaba F, Hamilton J, COOK M . Relaxations of guinea-pig fundic strip by adenosine, adenine nucleotides and electrical stimulation: antagonsism by theophylline and desensitization to adenosine and its derivatives. Eur J Pharmacol. 1977; 46(3):181-98. DOI: 10.1016/0014-2999(77)90333-8. View

18.

Dean D, Downie J . Contribution of adrenergic and "purinergic" neurotransmission to contraction in rabbit detrusor. J Pharmacol Exp Ther. 1978; 207(2):431-45. View

19.

CARPENTER F . Potentiation of nerve-induced bladder responses by tetraethylammonium in relation to junctional and extrajunctional muscarinic receptors. Br J Pharmacol. 1978; 64(3):331-9. PMC: 1668510. DOI: 10.1111/j.1476-5381.1978.tb08654.x. View

20.

Irvin C, Boileau R, Tremblay J, Martin R, Macklem P . Bronchodilatation: noncholinergic, nonadrenergic mediation demonstrated in vivo in the cat. Science. 1980; 207(4432):791-2. DOI: 10.1126/science.7352292. View