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. 1995 Nov;116(6):2557–2562. doi: 10.1111/j.1476-5381.1995.tb17207.x

Heterogeneity of neurogenic responses in intra- and extrameningeal arteries of dogs.

Y Kohno 1, T Saito 1, H Saito 1, H Aoyama 1, Y Nojyo 1, S Kigoshi 1, I Muramatsu 1
PMCID: PMC1909147  PMID: 8590970

Abstract

1. Neurogenic responses to transmural electrical stimulation were examined in endothelium-denuded extrameningeal (vertebral and carotid) and intrameningeal (spinal, basilar and middle cerebral) arteries isolated from dogs. 2. In the extrameningeal arteries, transmural electrical stimulation produced a phasic contraction. This contraction was abolished by tetrodotoxin, prazosin and guanethidine. However, alpha,beta-methylene ATP and NG-nitro-L-arginine (L-NOARG) had no significant effect on the contractile responses. 3. In the intrameningeal arteries, the neurogenic responses to electrical stimulation were composed of a transient contraction and relaxation. The transient contraction was selectively inhibited by guanethidine L-NOARG abolished the relaxation but not the contraction induced by electrical stimulation. Prazosin had no effect on either neurogenic response. 4. Noradrenaline produced a large contraction in the extrameningeal arteries which was selectively inhibited by prazosin. alpha,beta-Methylene ATP produced neither contraction nor inhibition of the response to noradrenaline in the extrameningeal arteries. 5. In the intrameningeal arteries, alpha,beta-methylene ATP produced a greater contraction than noradrenaline. The response to alpha,beta-methylene ATP was selectively abolished by desensitization of P2x-purinoceptors with alpha,beta-methylene ATP itself. The contractile response to noradrenaline was inhibited by rauwolscine but not by prazosin. 6. ATP produced endothelium-dependent relaxations in the extrameningeal and intrameningeal arteries, which were attenuated by endothelium removal. 7. NADPH diaphorase-positive fibres were dense in the middle cerebral and basilar arteries but rare or absent in the spinal artery. In the extrameningeal arteries diaphorase-positive traces were observed in the vasa vasorum. 8. The present findings indicate that the neurogenic responses of intrameningeal arteries of dogs are composed of NO-ergic and sympathetic purinergic components, while the extrameningeal arteries tested produced only sympathetic adrenergic responses, suggesting that regional heterogeneity may be associated with a sudden transition in innervation and receptor expression at the meninx.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alafaci C., Cowen T., Crockard H. A., Burnstock G. Noradrenergic innervation of gerbil large cerebral arteries. Blood Vessels. 1986;23(3):154–159. doi: 10.1159/000158633. [DOI] [PubMed] [Google Scholar]
  2. Bredt D. S., Hwang P. M., Snyder S. H. Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature. 1990 Oct 25;347(6295):768–770. doi: 10.1038/347768a0. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Burnstock G. The changing face of autonomic neurotransmission. Acta Physiol Scand. 1986 Jan;126(1):67–91. doi: 10.1111/j.1748-1716.1986.tb07790.x. [DOI] [PubMed] [Google Scholar]
  5. D'Alecy L. G., Feigl E. O. Sympathetic control of cerebral blood flow in dogs. Circ Res. 1972 Aug;31(2):267–283. doi: 10.1161/01.res.31.2.267. [DOI] [PubMed] [Google Scholar]
  6. Duckles S. P., Bevan J. A. Pharmacological characterization of adrenergic receptors of a rabbit cerebral artery in vitro. J Pharmacol Exp Ther. 1976 May;197(2):371–378. [PubMed] [Google Scholar]
  7. Iadecola C., Beitz A. J., Renno W., Xu X., Mayer B., Zhang F. Nitric oxide synthase-containing neural processes on large cerebral arteries and cerebral microvessels. Brain Res. 1993 Mar 19;606(1):148–155. doi: 10.1016/0006-8993(93)91583-e. [DOI] [PubMed] [Google Scholar]
  8. Iwayama T., Furness J. B., Burnstock G. Dual adrenergic and cholinergic innervation of the cerebral arteries of the rat. An ultrastructural study. Circ Res. 1970 May;26(5):635–646. doi: 10.1161/01.res.26.5.635. [DOI] [PubMed] [Google Scholar]
  9. Kajikawa H. Fluorescence histochemical studies on the distribution of adrenergic nerve fibers to intracranial blood vessels. Nihon Geka Hokan. 1968 Jul 1;37(4):473–484. [PubMed] [Google Scholar]
  10. Kasakov L., Burnstock G. The use of the slowly degradable analog, alpha, beta-methylene ATP, to produce desensitisation of the P2-purinoceptor: effect on non-adrenergic, non-cholinergic responses of the guinea-pig urinary bladder. Eur J Pharmacol. 1982 Dec 24;86(2):291–294. doi: 10.1016/0014-2999(82)90330-2. [DOI] [PubMed] [Google Scholar]
  11. Kohno Y., Saito H., Takita M., Kigoshi S., Muramatsu I. Heterogeneity of alpha 1-adrenoceptor subtypes involved in adrenergic contractions of dog blood vessels. Br J Pharmacol. 1994 Aug;112(4):1167–1173. doi: 10.1111/j.1476-5381.1994.tb13206.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lee T. J., Su C., Bevan J. A. Neurogenic sympathetic vasoconstriction of the rabbit basilar artery. Circ Res. 1976 Jul;39(1):120–126. doi: 10.1161/01.res.39.1.120. [DOI] [PubMed] [Google Scholar]
  13. Marcus M. L., Heistad D. D. Effects of sympathetic nerves on cerebral blood flow in awake dogs. Am J Physiol. 1979 Apr;236(4):H549–H553. doi: 10.1152/ajpheart.1979.236.4.H549. [DOI] [PubMed] [Google Scholar]
  14. Muramatsu I., Fujiwara M., Miura A., Sakakibara Y. Possible involvement of adenine nucleotides in sympathetic neuroeffector mechanisms of dog basilar artery. J Pharmacol Exp Ther. 1981 Feb;216(2):401–409. [PubMed] [Google Scholar]
  15. Muramatsu I., Fujiwara M., Osumi Y., Shibata S. Vasoconstrictor and dilator actions of nicotine and electrical transmural stimulation on isolated dog cerebral arteries. Blood Vessels. 1978;15(1-3):110–118. doi: 10.1159/000158157. [DOI] [PubMed] [Google Scholar]
  16. Muramatsu I., Kigoshi S. Purinergic and non-purinergic innervation in the cerebral arteries of the dog. Br J Pharmacol. 1987 Dec;92(4):901–908. doi: 10.1111/j.1476-5381.1987.tb11396.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Muramatsu I., Ohmura T., Oshita M. Comparison between sympathetic adrenergic and purinergic transmission in the dog mesenteric artery. J Physiol. 1989 Apr;411:227–243. doi: 10.1113/jphysiol.1989.sp017570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Muramatsu I. Relation between adrenergic neurogenic contraction and alpha 1-adrenoceptor subtypes in dog mesenteric and carotid arteries and rabbit carotid arteries. Br J Pharmacol. 1991 Jan;102(1):210–214. doi: 10.1111/j.1476-5381.1991.tb12155.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nielsen K. C., Owman C. Contractile response and amine receptor mechanisms in isolated middle cerebral artery of the cat. Brain Res. 1971 Mar 19;27(1):33–42. doi: 10.1016/0006-8993(71)90370-2. [DOI] [PubMed] [Google Scholar]
  20. Sakakibara Y., Fujiwara M., Muramatsu I. Pharmacological characterization of the alpha adrenoceptors of the dog basilar artery. Naunyn Schmiedebergs Arch Pharmacol. 1982 Apr;319(1):1–7. doi: 10.1007/BF00491469. [DOI] [PubMed] [Google Scholar]
  21. Su C. Purinergic inhibition of adrenergic transmission in rabbit blood vessels. J Pharmacol Exp Ther. 1978 Feb;204(2):351–361. [PubMed] [Google Scholar]
  22. Tsukahara T., Taniguchi T., Usui H., Miwa S., Shimohama S., Fujiwara M., Handa H. Sympathetic denervation and alpha adrenoceptors in dog cerebral arteries. Naunyn Schmiedebergs Arch Pharmacol. 1986 Dec;334(4):436–443. doi: 10.1007/BF00569383. [DOI] [PubMed] [Google Scholar]
  23. von Kügelgen I., Starke K. Noradrenaline and adenosine triphosphate as co-transmitters of neurogenic vasoconstriction in rabbit mesenteric artery. J Physiol. 1985 Oct;367:435–455. doi: 10.1113/jphysiol.1985.sp015834. [DOI] [PMC free article] [PubMed] [Google Scholar]

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