Tags

Type your tag names separated by a space and hit enter

Cortical spreading depression induces oxidative stress in the trigeminal nociceptive system.
Neuroscience 2013; 253:341-9N

Abstract

Indirect evidence suggests the increased production of reactive oxygen species (ROS) in migraine pathophysiology. In the current study we measured lipid peroxidation product in the rat cortex, trigeminal ganglia and meninges after the induction of cortical spreading depression (CSD), a phenomenon known to be associated with migraine aura, and tested nociceptive firing triggered by ROS in trigeminal nerves ex vivo. Application of KCl to dura mater in anesthetized rats induced several waves of CSD recorded by an extracellular electrode in the cortex. Following CSD, samples of cortex (affected regions were identified with blood oxygen level-dependent (BOLD) functional magnetic resonance imaging (fMRI)), meninges from left and right hemispheres and trigeminal ganglia were taken for biochemical analysis. We found that CSD increased the level of the lipid peroxidation product malondialdehyde (MDA) in the ipsilateral cerebral cortex and meninges, but also in both ipsi- and contralateral trigeminal ganglia. In order to test the pro-nociceptive action of ROS, we applied the mild oxidant hydrogen peroxide to isolated rat hemiskull preparations including preserved trigeminal innervations. Application of hydrogen peroxide to meninges transiently enhanced electrical spiking activity of trigeminal nerves showing a pro-nociceptive action of ROS. In the presence of hydrogen peroxide trigeminal nerves still responded to capsaicin by burst of spiking activity indicating integrity of neuronal structures. The action of hydrogen peroxide was mediated by TRPA1 receptors as it was abolished by the specific TRPA1 antagonist TCS-5861528. Using dorsal root ganglion sensory neurons as test system we found that hydrogen peroxide promoted the release of the migraine mediator calcitonin gene-related peptide (CGRP), which we previously identified as a trigger of delayed sensitization of trigeminal neurons. Our data suggest that, after CSD, oxidative stress spreads downstream within the trigeminal nociceptive system and could be involved in the coupling of CSD with the activation of trigeminovascular system in migraine pathology.

Authors+Show Affiliations

Department of Neurobiology, A.I. Virtanen Institute for Molecular Sciences, University of Eastern Finland, Kuopio, Finland.No affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

24036374

Citation

Shatillo, A, et al. "Cortical Spreading Depression Induces Oxidative Stress in the Trigeminal Nociceptive System." Neuroscience, vol. 253, 2013, pp. 341-9.
Shatillo A, Koroleva K, Giniatullina R, et al. Cortical spreading depression induces oxidative stress in the trigeminal nociceptive system. Neuroscience. 2013;253:341-9.
Shatillo, A., Koroleva, K., Giniatullina, R., Naumenko, N., Slastnikova, A. A., Aliev, R. R., ... Giniatullin, R. (2013). Cortical spreading depression induces oxidative stress in the trigeminal nociceptive system. Neuroscience, 253, pp. 341-9. doi:10.1016/j.neuroscience.2013.09.002.
Shatillo A, et al. Cortical Spreading Depression Induces Oxidative Stress in the Trigeminal Nociceptive System. Neuroscience. 2013 Dec 3;253:341-9. PubMed PMID: 24036374.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Cortical spreading depression induces oxidative stress in the trigeminal nociceptive system. AU - Shatillo,A, AU - Koroleva,K, AU - Giniatullina,R, AU - Naumenko,N, AU - Slastnikova,A A, AU - Aliev,R R, AU - Bart,G, AU - Atalay,M, AU - Gu,C, AU - Khazipov,R, AU - Davletov,B, AU - Grohn,O, AU - Giniatullin,R, Y1 - 2013/09/11/ PY - 2013/05/08/received PY - 2013/08/16/revised PY - 2013/09/03/accepted PY - 2013/9/17/entrez PY - 2013/9/17/pubmed PY - 2014/6/20/medline KW - ANOVA KW - BOLD KW - CGRP KW - CSD KW - DRG KW - LFP KW - MDA KW - ROS KW - TBARS KW - analysis of variance KW - blood oxygen level-dependent KW - calcitonin gene-related peptide KW - cortical spreading depression KW - dorsal root ganglion KW - fMRI KW - functional magnetic resonance imaging KW - local field potential KW - malondialdehyde KW - migraine KW - reactive oxygen species KW - thiobarbituric acid reactive substances KW - trigeminal ganglion KW - trigeminal neurons SP - 341 EP - 9 JF - Neuroscience JO - Neuroscience VL - 253 N2 - Indirect evidence suggests the increased production of reactive oxygen species (ROS) in migraine pathophysiology. In the current study we measured lipid peroxidation product in the rat cortex, trigeminal ganglia and meninges after the induction of cortical spreading depression (CSD), a phenomenon known to be associated with migraine aura, and tested nociceptive firing triggered by ROS in trigeminal nerves ex vivo. Application of KCl to dura mater in anesthetized rats induced several waves of CSD recorded by an extracellular electrode in the cortex. Following CSD, samples of cortex (affected regions were identified with blood oxygen level-dependent (BOLD) functional magnetic resonance imaging (fMRI)), meninges from left and right hemispheres and trigeminal ganglia were taken for biochemical analysis. We found that CSD increased the level of the lipid peroxidation product malondialdehyde (MDA) in the ipsilateral cerebral cortex and meninges, but also in both ipsi- and contralateral trigeminal ganglia. In order to test the pro-nociceptive action of ROS, we applied the mild oxidant hydrogen peroxide to isolated rat hemiskull preparations including preserved trigeminal innervations. Application of hydrogen peroxide to meninges transiently enhanced electrical spiking activity of trigeminal nerves showing a pro-nociceptive action of ROS. In the presence of hydrogen peroxide trigeminal nerves still responded to capsaicin by burst of spiking activity indicating integrity of neuronal structures. The action of hydrogen peroxide was mediated by TRPA1 receptors as it was abolished by the specific TRPA1 antagonist TCS-5861528. Using dorsal root ganglion sensory neurons as test system we found that hydrogen peroxide promoted the release of the migraine mediator calcitonin gene-related peptide (CGRP), which we previously identified as a trigger of delayed sensitization of trigeminal neurons. Our data suggest that, after CSD, oxidative stress spreads downstream within the trigeminal nociceptive system and could be involved in the coupling of CSD with the activation of trigeminovascular system in migraine pathology. SN - 1873-7544 UR - https://www.unboundmedicine.com/medline/citation/24036374/Cortical_spreading_depression_induces_oxidative_stress_in_the_trigeminal_nociceptive_system_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S0306-4522(13)00772-0 DB - PRIME DP - Unbound Medicine ER -