Cortical spreading depression induces oxidative stress in the trigeminal nociceptive system

Shatillo, Artem; Koroleva, Kseniia; Giniatullina, Raisa; Naumenko, Nikolay; Slastnikova, A.A.; Алиев, Р. Р.; Bart, Geneviève; Atalay, Mustafa; Gu, Chao; Khazipov, Roustem; Davletov, Bazbek; Gröhn, Olli; Giniatullin, Rashid

doi:10.1016/j.neuroscience.2013.09.002

Cited by 118 publications

(116 citation statements)

References 41 publications

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“…This suggests that oxidative stress may be the primary cause of CSD and not just its consequence. [17][18][19][20] In pathological conditions, the failure to neutralize ROS during the excessive ROS surge and/or deficiency of the neuronal antioxidant system may result in the MC and subsequent ignition of CSD. Indeed, our in vivo results show that when the oxidative stress-induced ROS accumulation is suppressed by an exogenous antioxidant, CSD occurrence is strongly reduced.…”

Section: Discussionmentioning

confidence: 99%

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Reactive Oxygen Species Initiate a Metabolic Collapse in Hippocampal Slices: Potential Trigger of Cortical Spreading Depression

Malkov

Ivanov

Popova

et al. 2014

J Cereb Blood Flow Metab

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Excessive accumulation of reactive oxygen species (ROS) underlies oxidative damage. We find that in hippocampal slices, decreased activity of glucose-based antioxidant system induces a massive, abrupt, and detrimental change in cellular functions. We call this phenomenon metabolic collapse (MC). This collapse manifested in long-lasting silencing of synaptic transmission, abnormal oxidation of NAD(P)H and FADH 2 associated with immense oxygen consumption, and massive neuronal depolarization. MC occurred without any preceding deficiency in neuronal energy supply or disturbances of ionic homeostasis and spread throughout the hippocampus. It was associated with a preceding accumulation of ROS and was largely prevented by application of an efficient antioxidant Tempol (4-hydroxy-2,2,6,6-tetramethylpiperidine-1-oxyl). The consequences of MC resemble cortical spreading depression (CSD), a wave of neuronal depolarization that occurs in migraine, brain trauma, and stroke, the cellular initiation mechanisms of which are poorly understood. We suggest that ROS accumulation might also be the primary trigger of CSD. Indeed, we found that Tempol strongly reduced occurrence of CSD in vivo, suggesting that ROS accumulation may be a key mechanism of CSD initiation.

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Section: Discussionmentioning

confidence: 99%

“…15,16 Similarly, the experimental interventions that induce CSD are also associated with oxidative stress. However, although oxidative stress was noted as a consequence of CSD in a few experimental studies, [17][18][19][20] it did not attract significant attention as a potential cause of CSD.…”

Section: Introductionmentioning

confidence: 99%

Reactive Oxygen Species Initiate a Metabolic Collapse in Hippocampal Slices: Potential Trigger of Cortical Spreading Depression

Malkov

Ivanov

Popova

et al. 2014

J Cereb Blood Flow Metab

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“…Each hemiskull preparation was used for recording spontaneous and drug-induced spikes from the nervus spinosus as we published before [4,29]. The recording w a s p e r f o r m e d w i t h a D A M 8 0 i a m p l i f i e r (bandpass = 0.1-3000 Hz, gain = 10,000) using the firepolished microelectrodes filled with the Krebs solution.…”

Section: Electrophysiologymentioning

confidence: 99%

“…WinEDR version V3.5.6 software (Strathclyde University, UK) was used for recordings and spikes analysis. Signals were visualized and analyzed offline using the software WinEDR as described by us earlier [29]. In brief, a spike was determined as a transient with a duration between 0.3 and 3 ms and which amplitude exceeded four standard deviations [30].…”

Section: Electrophysiologymentioning

confidence: 99%

Nucleotide homeostasis and purinergic nociceptive signaling in rat meninges in migraine-like conditions

Yegutkin

Guerrero-Toro

Kılınç

et al. 2016

Purinergic Signalling

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Extracellular ATP is suspected to contribute to migraine pain but regulatory mechanisms controlling pronociceptive purinergic mechanisms in the meninges remain unknown. We studied the peculiarities of metabolic and signaling pathways of ATP and its downstream metabolites in rat meninges and in cultured trigeminal cells exposed to the migraine mediator calcitonin gene-related peptide (CGRP). Under resting conditions, meningeal ATP and ADP remained at low nanomolar levels, whereas extracellular AMP and adenosine concentrations were one-two orders higher. CGRP increased ATP and ADP levels in meninges and trigeminal cultures and reduced adenosine concentration in trigeminal cells. Degradation rates for exogenous nucleotides remained similar in control and CGRP-treated meninges, indicating that CGRP triggers nucleotide release without affecting nucleotide-inactivating pathways. Lead nitrate-based enzyme histochemistry of whole mount meninges revealed the presence of high ATPase, ADPase, and AMPase activities, primarily localized in the medial meningeal artery. ATP and ADP induced large intracellular Ca 2+ transients both in neurons and in glial cells whereas AMP and adenosine were ineffective. In trigeminal glia, ATP partially operated via P2X7 receptors. ATP, but not other nucleotides, activated nociceptive spikes in meningeal trigeminal nerve fibers providing a rationale for high degradation rate of pro-nociceptive ATP. Pronociceptive effect of ATP in meningeal nerves was reproduced by α,β-meATP operating via P2X3 receptors. Collectively, extracellular ATP, which level is controlled by CGRP, can persistently activate trigeminal nerves in meninges which considered as the origin site of migraine headache. These data are consistent with the purinergic hypothesis of migraine pain and suggest new targets against trigeminal pain.

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“…Markers of oxidative stress, such as 8-isoprostane and other markers of lipid peroxidation, are often elevated in neuroinflammation and CNS dysfunction [19,20].…”

Section: Oxidative Stress: a "Global" Mechanism Of Stress Plasticity?mentioning

confidence: 99%

Stress, Brain Wiring and the Economy

Mascarenhas¹

2017

J Psychol Psychother

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Emerging links between lifestyle stress, psychological traits and the economy are explored by highlighting recent work in which stress has been shown to trigger enduring changes in neural cell metabolism via epigenetic mechanisms. One important target of such changes is the circuitry of the medial prefrontal cortex, which has been implicated in abstract construal, theory of mind functions, agency and other psychometric constructs associated with innovation and entrepreneurship. In an economy increasingly dependent on such psychological traits for its competitiveness our understanding of the impacts of stress on cognition and affect may be especially relevant to future prosperity. One recent approach to designing a pathway-based intervention for epigenetic dysfunction triggered by stress is discussed as an example.

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Cortical spreading depression induces oxidative stress in the trigeminal nociceptive system

Cited by 118 publications

References 41 publications

Reactive Oxygen Species Initiate a Metabolic Collapse in Hippocampal Slices: Potential Trigger of Cortical Spreading Depression

Reactive Oxygen Species Initiate a Metabolic Collapse in Hippocampal Slices: Potential Trigger of Cortical Spreading Depression

Nucleotide homeostasis and purinergic nociceptive signaling in rat meninges in migraine-like conditions

Stress, Brain Wiring and the Economy

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