Nitric oxide is a sensory nerve neurotransmitter in the mesenteric artery of guinea pig

Zhongling Zheng, Keiichi Shimamura, Todd L. Anthony, Renato Alberto Travagli, David L. Kreulen

Research output: Contribution to journalArticle

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Abstract

Previous studies have shown that the guinea pig inferior mesenteric artery receives spinal sensory vasodilatory innervation, which can be activated by colon distention and electrical nerve stimulation. In the present study, we investigated the hypotheses that nitric oxide synthase (NOS) is present in guinea pig primary sensory neurons in the dorsal root ganglion (DRG) and in nerve fibers surrounding the mesenteric arteries, and that nitric oxide (NO) is a sensory neurotransmitter in the inferior mesenteric artery in vitro. Double-labeling immunohistochemistry showed that neuronal NOS-IR was found in 12% of cells of guinea pig thoracic and lumbar DRGs; in 95.1% of these cells it was colocalized with substance P (SP), and SP immunoreactivity (SP-IR) was present in 23% of cells of the same DRGs. Neuronal NOS-like immunoreactivity was localized in nerve fibers surrounding guinea pig mesenteric artery and 25% of them were double stained with SP-IR. Endothelium-denuded inferior mesenteric artery preparations in vitro were incubated with guanethidine (30 μM, 30 min) and pre-contracted with methoxamine (30 μM). The NO donors, sodium nitroprusside(1 μM) and L-nitrosocysteine (300 μM), produced 91.0 ± 5.5 and 90.4 ± 9.6% vasodilatation of total vasodilatation in the vessel segments, respectively, which was capsaicin- or tetrodotoxin-insensitive. Repetitive electrical field stimulation of the preparations produced a frequency-dependent vasodilatation which was reduced by pretreatment with capsaicin or by tetrodotoxin (10 μM). The NOS inhibitor N(ω)-nitro-L-arginine (L-NNA) (100 μM, 30 min) diminished the nerve-evoked vasodilatation from 41.8 ± 8.4 to 21.4 ± 9.7% at 2 Hz and from 50.8 ± 5.6 to 19.0 ± 7.3% at 15 Hz (P < 0.05), whereas N(G)-nitro-L-arginine methyl ester (L-NAME, 100 μM - 1 mM) did not significantly inhibit the relaxation. The stereo isomer nitro-D-arginine (D-NNA, 100 μM, 30 min) was ineffective. These findings suggest that NO is a neurotransmitter released from primary sensory nerves which mediates vasodilatation in vitro.

Original languageEnglish (US)
Pages (from-to)137-144
Number of pages8
JournalJournal of the Autonomic Nervous System
Volume67
Issue number3
DOIs
StatePublished - Dec 11 1997

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Mesenteric Arteries
Vasodilation
Neurotransmitter Agents
Inferior Mesenteric Artery
Nitric Oxide
Guinea Pigs
Substance P
Nitric Oxide Synthase Type I
Diagnosis-Related Groups
Capsaicin
NG-Nitroarginine Methyl Ester
Tetrodotoxin
Nerve Fibers
Nitric Oxide Synthase
Electric Stimulation
Arginine
Methoxamine
Guanethidine
Nitric Oxide Donors
Spinal Ganglia

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Physiology
  • Clinical Neurology

Cite this

Zheng, Zhongling ; Shimamura, Keiichi ; Anthony, Todd L. ; Travagli, Renato Alberto ; Kreulen, David L. / Nitric oxide is a sensory nerve neurotransmitter in the mesenteric artery of guinea pig. In: Journal of the Autonomic Nervous System. 1997 ; Vol. 67, No. 3. pp. 137-144.
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Nitric oxide is a sensory nerve neurotransmitter in the mesenteric artery of guinea pig. / Zheng, Zhongling; Shimamura, Keiichi; Anthony, Todd L.; Travagli, Renato Alberto; Kreulen, David L.

In: Journal of the Autonomic Nervous System, Vol. 67, No. 3, 11.12.1997, p. 137-144.

Research output: Contribution to journalArticle

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