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Effects of Nitric Oxide on the Electrical Activity of the Rat Trigeminal Nerve and Mast Cell Morphology

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Abstract

Nitric oxide (NO) is a member of the family of gasotransmitters involved in the regulation of various biological processes. Nitroglycerin, an NO donor, is widely used to simulate migraine in both humans and animals. However, the role of peripheral neuronal structures in the effects of NO is practically unstudied. The aim of the work was to reveal the effects of NO on the electrical activity of the trigeminal nerve and the state of mast cells in the rat brain meninges. We recorded action potentials (APs) in the rat trigeminal nerve innervating the dura mater, in a rat hemiskull preparation. To analyze electrical activity, we used the clustering method, which allows АРs generated by individual fibers to be divided into groups with similar characteristics. Mast cell morphology was assessed by staining the rat dura matter with toluidine blue. L-arginine, the substrate for NO synthesis, increased the electrical activity of the trigeminal nerve in a dose-dependent manner, and this effect was abolished by pre-application of L-NAME (100 µM), an NO synthesis inhibitor. Sodium nitroprusside (SNP 200 µM), an exogenous NO donor, caused an increase in the AP frequency, while light-inactivated SNP had no effect thereupon. Cluster analysis revealed that SNP induced first an increase in the frequency of low-amplitude APs propagating at a low speed in capsaicin-sensitive C-type fibers; later, high-amplitude APs followed, propagating in Aδ-fibers. ODQ (10 µM), a soluble guanylate cyclase inhibitor, prevented SNP-induced increase in electrical activity. At the same time, incubation of the dura matter in SNP had no effect on the morphology of mast cells. Our data suggest that both exogenous and endogenous NO increases the electrical activity of the trigeminal nerve by activating guanylate cyclase, thus contributing to the peripheral neuronal mechanisms of pain in migraine.

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ACKNOWLEDGMENTS

The study was implemented within the Strategic Academic Leadership Program of the Kazan Federal University.

Funding

This work was supported by the Russian Science Foundation (RSF grant 21-75-00042) and the grant of the President of the Russian Federation (MK-4584.2022.1.4).

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Authors and Affiliations

  1. Kazan Federal University, Kazan, Russia

    K. S. Koroleva, S. O. Svitko, D. A. Nurmieva, O. Sh. Gafurov, A. D. Buglinina & G. F. Sitdikova

Authors
  1. K. S. Koroleva
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  2. S. O. Svitko
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  3. D. A. Nurmieva
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  4. O. Sh. Gafurov
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  5. A. D. Buglinina
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  6. G. F. Sitdikova
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Contributions

Conceptualization and experimental design (G.F.S., K.S.K.); data collection (S.O.S., D.A.N.); data processing (A.D.B., O.Sh.G.); manuscript writing and editing (G.F.S., K.S.K.).

Corresponding author

Correspondence to K. S. Koroleva.

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CONFLICT OF INTEREST

The authors declare that they have neither evident nor potential conflict of interest related to the publication of this article.

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Translated by A. Polyanovsky

Russian Text © The Author(s), 2022, published in Rossiiskii Fiziologicheskii Zhurnal imeni I.M. Sechenova, 2022, Vol. 108, No. 6, pp. 745–761https://doi.org/10.31857/S0869813922060048.

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Koroleva, K.S., Svitko, S.O., Nurmieva, D.A. et al. Effects of Nitric Oxide on the Electrical Activity of the Rat Trigeminal Nerve and Mast Cell Morphology. J Evol Biochem Phys 58, 901–914 (2022). https://doi.org/10.1134/S0022093022030243

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  • DOI: https://doi.org/10.1134/S0022093022030243

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