Nitric Oxide Release from Trigeminal Satellite Glial Cells is Attenuated by Glial Modulators and Glutamate

Overview

Journal Int J Physiol Pathophysiol Pharmacol

Date 2014 Jan 1

PMID 24379907

Citations 8

Authors

Jens Christian Laursen

Brian Edwin Cairns

Ujendra Kumar

Rishi Kumar Somvanshi

Xu-Dong Dong

Lars Arendt-Nielsen

Parisa Gazerani

Affiliations

Soon will be listed here.

Abstract

Nitric oxide (NO) is suggested to play an important role in primary headaches. It has been proposed that release of NO from satellite glial cells (SGCs) of the trigeminal ganglion (TG) could contribute to the pathogenesis of these headaches. The principal aim of this study was to investigate if the phosphodiesterase inhibitor Ibudilast (Ibu) and 1α,25-dihydroxyvitamin D3 (Vit D3) could interfere with NO release from trigeminal SGCs. Since glutamate is released from activated TG neurons, the ability of glutamate to alter NO release from SGCs was also investigated. To study this, we isolated SGCs from the TG of adult male Sprague-Dawley rats, provoked NO release from SGCs with forskolin (FSK; 0.1, 1, 10 μM), and examined the effect of graded concentrations of Ibu (1, 10, 100 μM), Vit D3 (5, 50, 500 nM), and glutamate (10, 100, 1000 μM). Our results indicate that both Ibu and Vit D3 are capable of attenuating the FSK-mediated increased NO release from SGCs after 48 hours of incubation. Lower glutamate concentrations (10 and 100 μM) significantly decreased NO release not only under basal conditions after 24 and 48 hours, but also after SGCs were stimulated with FSK for 48 hours. In conclusion, NO release from SGCs harvested from the TG can be attenuated by glial modulators and glutamate. As NO is thought to increase TG neuron excitability, the findings suggest that targeting SGCs may provide a novel therapeutic approach for management of craniofacial pain conditions such as migraine in the future.

Citing Articles

A systematic literature review on the role of glial cells in the pathomechanisms of migraine.

Zhang S, Azubuine J, Schmeer C Front Mol Neurosci. 2023; 16:1219574.

PMID: 37456527 PMC: 10347403. DOI: 10.3389/fnmol.2023.1219574.

Peripheral role of glutamate in orofacial pain.

Liu J, Jia S, Huang F, He H, Fan W Front Neurosci. 2022; 16:929136.

PMID: 36440288 PMC: 9682037. DOI: 10.3389/fnins.2022.929136.

Satellite Glial Cells in Pain Research: A Targeted Viewpoint of Potential and Future Directions.

Gazerani P Front Pain Res (Lausanne). 2022; 2:646068.

PMID: 35295432 PMC: 8915641. DOI: 10.3389/fpain.2021.646068.

Antidromic Spike Propagation and Dissimilar Expression of P2X, 5-HT, and TRPV1 Channels in Peripheral vs. Central Sensory Axons in Meninges.

Gafurov O, Koroleva K, Giniatullin R Front Cell Neurosci. 2021; 14:623134.

PMID: 33519387 PMC: 7845021. DOI: 10.3389/fncel.2020.623134.

Micronized palmitoylethanolamide reduces joint pain and glial cell activation.

Bartolucci M, Marini I, Bortolotti F, Impellizzeri D, Di Paola R, Bruschetta G Inflamm Res. 2018; 67(10):891-901.

PMID: 30121836 DOI: 10.1007/s00011-018-1179-y.

References

Chow E, Quach H, Vieth R, Pang K . Temporal changes in tissue 1α,25-dihydroxyvitamin D3, vitamin D receptor target genes, and calcium and PTH levels after 1,25(OH)2D3 treatment in mice. Am J Physiol Endocrinol Metab. 2013; 304(9):E977-89. DOI: 10.1152/ajpendo.00489.2012. View

Castillo C, Norcini M, Martin Hernandez L, Correa G, Blanck T, Recio-Pinto E . Satellite glia cells in dorsal root ganglia express functional NMDA receptors. Neuroscience. 2013; 240:135-46. DOI: 10.1016/j.neuroscience.2013.02.031. View

Hanani M . Satellite glial cells in sensory ganglia: from form to function. Brain Res Brain Res Rev. 2005; 48(3):457-76. DOI: 10.1016/j.brainresrev.2004.09.001. View

Lassen L, Ashina M, Christiansen I, Ulrich V, Grover R, Donaldson J . Nitric oxide synthase inhibition: a new principle in the treatment of migraine attacks. Cephalalgia. 1998; 18(1):27-32. DOI: 10.1046/j.1468-2982.1998.1801027.x. View

. Alleviation of migraines with therapeutic vitamin D and calcium. Headache. 1994; 34(10):590-2. DOI: 10.1111/j.1526-4610.1994.hed3410590.x. View

Yoshikawa M, Suzumura A, Ito A, Tamaru T, Takayanagi T . Effect of phosphodiesterase inhibitors on nitric oxide production by glial cells. Tohoku J Exp Med. 2002; 196(3):167-77. DOI: 10.1620/tjem.196.167. View

Vause C, Durham P . CGRP stimulation of iNOS and NO release from trigeminal ganglion glial cells involves mitogen-activated protein kinase pathways. J Neurochem. 2009; 110(3):811-21. PMC: 2748229. DOI: 10.1111/j.1471-4159.2009.06154.x. View

Bellamy J, Bowen E, Russo A, Durham P . Nitric oxide regulation of calcitonin gene-related peptide gene expression in rat trigeminal ganglia neurons. Eur J Neurosci. 2006; 23(8):2057-66. PMC: 1486900. DOI: 10.1111/j.1460-9568.2006.04742.x. View

Muindi J, Johnson C, Trump D, Christy R, Engler K, Fakih M . A phase I and pharmacokinetics study of intravenous calcitriol in combination with oral dexamethasone and gefitinib in patients with advanced solid tumors. Cancer Chemother Pharmacol. 2009; 65(1):33-40. PMC: 2746253. DOI: 10.1007/s00280-009-1000-2. View

10.

Taylor D, Diemel L, Pocock J . Activation of microglial group III metabotropic glutamate receptors protects neurons against microglial neurotoxicity. J Neurosci. 2003; 23(6):2150-60. PMC: 6742009. View

11.

Matsuka Y, Neubert J, Maidment N, Spigelman I . Concurrent release of ATP and substance P within guinea pig trigeminal ganglia in vivo. Brain Res. 2001; 915(2):248-55. DOI: 10.1016/s0006-8993(01)02888-8. View

12.

Knutsen K, Brekke M, Gjelstad S, Lagerlov P . Vitamin D status in patients with musculoskeletal pain, fatigue and headache: a cross-sectional descriptive study in a multi-ethnic general practice in Norway. Scand J Prim Health Care. 2010; 28(3):166-71. PMC: 3442332. DOI: 10.3109/02813432.2010.505407. View

13.

Ledeboer A, Hutchinson M, Watkins L, Johnson K . Ibudilast (AV-411). A new class therapeutic candidate for neuropathic pain and opioid withdrawal syndromes. Expert Opin Investig Drugs. 2007; 16(7):935-50. DOI: 10.1517/13543784.16.7.935. View

14.

Durham P, Masterson C . Two mechanisms involved in trigeminal CGRP release: implications for migraine treatment. Headache. 2012; 53(1):67-80. PMC: 3540191. DOI: 10.1111/j.1526-4610.2012.02262.x. View

15.

Kung L, Gong K, Adedoyin M, Ng J, Bhargava A, Ohara P . Evidence for glutamate as a neuroglial transmitter within sensory ganglia. PLoS One. 2013; 8(7):e68312. PMC: 3699553. DOI: 10.1371/journal.pone.0068312. View

16.

Li J, Vause C, Durham P . Calcitonin gene-related peptide stimulation of nitric oxide synthesis and release from trigeminal ganglion glial cells. Brain Res. 2008; 1196:22-32. PMC: 2268710. DOI: 10.1016/j.brainres.2007.12.028. View

17.

Garcion E, Sindji L, Leblondel G, Brachet P, DArcy F . 1,25-dihydroxyvitamin D3 regulates the synthesis of gamma-glutamyl transpeptidase and glutathione levels in rat primary astrocytes. J Neurochem. 1999; 73(2):859-66. DOI: 10.1046/j.1471-4159.1999.0730859.x. View

18.

Muindi J, Modzelewski R, Peng Y, Trump D, Johnson C . Pharmacokinetics of 1alpha,25-dihydroxyvitamin D3 in normal mice after systemic exposure to effective and safe antitumor doses. Oncology. 2004; 66(1):62-6. DOI: 10.1159/000076336. View

19.

Rolan P, Gibbons J, He L, Chang E, Jones D, Gross M . Ibudilast in healthy volunteers: safety, tolerability and pharmacokinetics with single and multiple doses. Br J Clin Pharmacol. 2008; 66(6):792-801. PMC: 2675769. DOI: 10.1111/j.1365-2125.2008.03270.x. View

20.

Ledeboer A, Liu T, Shumilla J, Mahoney J, Vijay S, Gross M . The glial modulatory drug AV411 attenuates mechanical allodynia in rat models of neuropathic pain. Neuron Glia Biol. 2008; 2(4):279-91. PMC: 2174834. DOI: 10.1017/S1740925X0700035X. View