Peptidergic and nitrergic inhibitory neurotransmissions in the hamster jejunum: regulation of vasoactive intestinal peptide release by nitric oxide

doi:10.1016/S0306-4522(01)00580-2

Neuroscience

Volume 110, Issue 4, 3 April 2002, Pages 779-788

https://doi.org/10.1016/S0306-4522(01)00580-2 Get rights and content

Abstract

Regulation of vasoactive intestinal peptide (VIP) release by nitric oxide (NO) was investigated in the hamster jejunum. Electrical field stimulation and applied NO (3–100 μM) evoked biphasic hyperpolarizations consisting of an initial transient hyperpolarizing component followed by a second more slowly developing component (late component). The NO synthase inhibitor N^G-nitro-L-arginine methyl ester (200 μM) abolished the biphasic inhibitory junction potential evoked by electrical field stimulation. The NO scavenger oxyhemoglobin (50 μM) and the guanylate cyclase inhibitor 1H-[1,2,4]oxadiazolo-[4,3-a]quinoxalin-1-one (ODQ; 10 μM) abolished both components of the inhibitory junction potentials and the NO-induced hyperpolarizations. VIP(6–28) (1 μM), which abolished VIP (3 μM)-induced hyperpolarizations, also inhibited the late components of the inhibitory junction potentials and the NO-induced hyperpolarizations. ODQ inhibited VIP release and cAMP production by electrical field stimulation and NO application. N⁶-2,0-Dibutyryladenosine 3′,5′-cyclic monophosphate (0.1–3 mM) caused a membrane hyperpolarization.

These results suggest that NO may stimulate VIP release from enteric nerves in the hamster jejunum. In addition, we propose that NO and NO-stimulated VIP contribute to the early and late components of the inhibitory junction potentials, respectively, in the circular smooth muscle cells of the hamster jejunum.

Section snippets

Tissue preparation

Male Syrian hamsters (80–120 g) were obtained from SLC (Japan) and were anesthetized with diethyl ether and exsanguinated via the carotid arteries. Tissue preparations and electrophysiological techniques were similar to those previously described (Matsuyama et al., 1999b). After the abdominal cavity was opened, a length of about 3–4 cm of jejunum was removed and immediately immersed in physiological salt solution (PSS; see below) at room temperature. The contents of the excised segment were

Membrane potential responses to electrical field stimulation

The circular smooth muscle cells of the hamster jejunum displayed either electrical quiescence (in 74/248 cells) or spontaneous rhythmic potentials (in 174/248 cells), which represented slow wave activity. Quiescent cells had an average resting membrane potential of −44.2±0.3 mV, while the most negative potential between the slow waves in unquiescent cells was −47.5±0.2 mV. There was no significant difference between the average resting membrane potentials of the quiescent cells and most

Discussion

The results of the present study suggest that the induction of VIP release by NO contributes to the late components of the IJPs and hyperpolarizations in the hamster jejunum. These conclusions are supported by the following observations: (i) the late components of the nitrergic IJPs and the NO-induced hyperpolarizations were inhibited by VIP(6–28) and ODQ; (ii) EFS-stimulated VIP release was inhibited by L-NAME; (iii) VIP release produced by EFS and NO application was abolished by ODQ; and (iv)

Conclusion

In conclusion, our studies suggest that NO and NO-stimulated VIP are involved in the early and late components of the nitrergic IJPs, respectively, in the hamster jejunum. Furthermore, we propose that endogenous and exogenous NO cause membrane hyperpolarization not only via production of cGMP but also by VIP released from enteric nerves which in turn produces cAMP in the hamster jejunum.

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Peptidergic and nitrergic inhibitory neurotransmissions in the hamster jejunum: regulation of vasoactive intestinal peptide release by nitric oxide

Abstract

Section snippets

Tissue preparation

Membrane potential responses to electrical field stimulation

Discussion

Conclusion

Neurosci. Lett.

Neuroscience

J. Auton. Nerv. Syst.

J. Biol. Chem.

Regulation of VIP release from rat enteric nerve terminals: evidence for a stimulatory effect of NO

Am. J. Physiol.

Parallel pathways mediate inhibitory effects of vasoactive intestinal polypeptide and nitric oxide in canine fundus

Br. J. Pharmacol.

Ultrastructural localization of nitric oxide synthase in canine small intestine and colon

Am. J. Physiol.

Role of sarcoplasmic reticulum in inhibitory junction potentials and hyperpolarizations by nitric oxide donors in opossum oesophagus

Br. J. Pharmacol.

Involvement of cAMP and cGMP in relaxation of internal anal sphincter by neural stimulation, VIP, and NO

Am. J. Physiol.

Evidence for VIP-induced increase in NO production in myenteric neurons of opossum internal anal sphincter

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Interplay of VIP and nitric oxide in regulation of the descending relaxation phase of peristalsis

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Nature