Role of Neuroinflammation and Blood-Brain Barrier Permutability on Migraine

Gaku Yamanaka, Shinji Suzuki, Natsumi Morishita, Mika Takeshita, Kanako Kanou, Tomoko Takamatsu, Shunsuke Suzuki, Shinichiro Morichi, Yusuke Watanabe, Yu Ishida, Soken Go, Shingo Oana, Yasuyo Kashiwagi, Hisashi Kawashima, Gaku Yamanaka, Shinji Suzuki, Natsumi Morishita, Mika Takeshita, Kanako Kanou, Tomoko Takamatsu, Shunsuke Suzuki, Shinichiro Morichi, Yusuke Watanabe, Yu Ishida, Soken Go, Shingo Oana, Yasuyo Kashiwagi, Hisashi Kawashima

Abstract

Currently, migraine is treated mainly by targeting calcitonin gene-related peptides, although the efficacy of this method is limited and new treatment strategies are desired. Neuroinflammation has been implicated in the pathogenesis of migraine. In patients with migraine, peripheral levels of pro-inflammatory cytokines, such as interleukin-1β (IL-1β) and tumor necrosis factor-α, are known to be increased. Additionally, animal models of headache have demonstrated that immunological responses associated with cytokines are involved in the pathogenesis of migraine. Furthermore, these inflammatory mediators might alter the function of tight junctions in brain vascular endothelial cells in animal models, but not in human patients. Based on clinical findings showing elevated IL-1β, and experimental findings involving IL-1β and both the peripheral trigeminal ganglion and central trigeminal vascular pathways, regulation of the Il-1β/IL-1 receptor type 1 axis might lead to new treatments for migraine. However, the integrity of the blood-brain barrier is not expected to be affected during attacks in patients with migraine.

Keywords: IL-1β; anakinra; blood-brain barrier; chemokine; migraine; neuroinflammation.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
CGRP and the trigemino-vascular system in migraine.
Figure 2
Figure 2
Potential for therapies using the IL-1β/IL-1R1 axis.

References

    1. Global, regional, and national incidence, prevalence, and years lived with disability for 328 diseases and injuries for 195 countries, 1990–2016: A systematic analysis for the Global Burden of Disease Study 2016. Lancet. 2017;390:1211–1259. doi: 10.1016/S0140-6736(17)32154-2.
    1. Feigin V.L., Vos T., Alahdab F., Amit A.M.L., Bärnighausen T.W., Beghi E., Beheshti M., Chavan P.P., Criqui M.H., Desai R., et al. Burden of Neurological Disorders Across the US From 1990–2017: A Global Burden of Disease Study. JAMA Neurol. 2021;78:165–176. doi: 10.1001/jamaneurol.2020.4152.
    1. Humphrey P.P., Feniuk W., Perren M.J., Beresford I.J., Skingle M., Whalley E.T. Serotonin and migraine. Ann. N. Y. Acad. Sci. 1990;600:587–598; discussion 598–600. doi: 10.1111/j.1749-6632.1990.tb16912.x.
    1. Edvinsson L., Uddman R. Neurobiology in primary headaches. Brain Res. Brain Res. Rev. 2005;48:438–456. doi: 10.1016/j.brainresrev.2004.09.007.
    1. Edvinsson L., Haanes K.A., Warfvinge K., Krause D.N. CGRP as the target of new migraine therapies—successful translation from bench to clinic. Nat. Rev. Neurol. 2018;14:338–350. doi: 10.1038/s41582-018-0003-1.
    1. Raddant A.C., Russo A.F. Calcitonin gene-related peptide in migraine: Intersection of peripheral inflammation and central modulation. Expert Rev. Mol. Med. 2011;13:e36. doi: 10.1017/S1462399411002067.
    1. Ramachandran R. Neurogenic inflammation and its role in migraine. Semin. Immunopathol. 2018;40:301–314. doi: 10.1007/s00281-018-0676-y.
    1. Malhotra R. Understanding migraine: Potential role of neurogenic inflammation. Ann. Indian Acad. Neurol. 2016;19:175–182. doi: 10.4103/0972-2327.182302.
    1. Gao Y.J., Ji R.R. Chemokines, neuronal-glial interactions, and central processing of neuropathic pain. Pharmacol. Ther. 2010;126:56–68. doi: 10.1016/j.pharmthera.2010.01.002.
    1. Edvinsson L., Haanes K.A., Warfvinge K. Does inflammation have a role in migraine? Nat. Rev. Neurol. 2019;15:483–490. doi: 10.1038/s41582-019-0216-y.
    1. DiSabato D.J., Quan N., Godbout J.P. Neuroinflammation: The devil is in the details. J. Neurochem. 2016;139(Suppl. 2):136–153. doi: 10.1111/jnc.13607.
    1. Norden D.M., Trojanowski P.J., Villanueva E., Navarro E., Godbout J.P. Sequential activation of microglia and astrocyte cytokine expression precedes increased Iba-1 or GFAP immunoreactivity following systemic immune challenge. Glia. 2016;64:300–316. doi: 10.1002/glia.22930.
    1. Armulik A., Genové G., Betsholtz C. Pericytes: Developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell. 2011;21:193–215. doi: 10.1016/j.devcel.2011.07.001.
    1. Yamanaka G., Takata F., Kataoka Y., Kanou K., Morichi S., Dohgu S., Kawashima H. The Neuroinflammatory Role of Pericytes in Epilepsy. Biomedicines. 2021;9:759. doi: 10.3390/biomedicines9070759.
    1. Covelli V., Munno I., Pellegrino N.M., Di Venere A., Jirillo E., Buscaino G.A. Exaggerated spontaneous release of tumor necrosis factor-alpha/cachectin in patients with migraine without aura. Acta Neurol. 1990;12:257–263.
    1. Perini F., D’Andrea G., Galloni E., Pignatelli F., Billo G., Alba S., Bussone G., Toso V. Plasma Cytokine Levels in Migraineurs and Controls. Headache J. Head Face Pain. 2005;45:926–931. doi: 10.1111/j.1526-4610.2005.05135.x.
    1. Kacinski M., Gergont A., Kubik A., Steczkowska-Klucznik M. Proinflammatory cytokines in children with migraine with or without aura. Przegl. Lek. 2005;62:1276–1280.
    1. Sarchielli P., Alberti A., Baldi A., Coppola F., Rossi C., Pierguidi L., Floridi A., Calabresi P. Proinflammatory cytokines, adhesion molecules, and lymphocyte integrin expression in the internal jugular blood of migraine patients without aura assessed ictally. Headache. 2006;46:200–207. doi: 10.1111/j.1526-4610.2006.00337.x.
    1. Wang F., He Q., Ren Z., Li F., Chen W., Lin X., Zhang H., Tai G. Association of serum levels of intercellular adhesion molecule-1 and interleukin-6 with migraine. Neurol. Sci. 2015;36:535–540. doi: 10.1007/s10072-014-2010-3.
    1. Yücel M., Kotan D., Gurol Çiftçi G., Çiftçi I.H., Cikriklar H.I. Serum levels of endocan, claudin-5 and cytokines in migraine. Eur. Rev. Med. Pharmacol. Sci. 2016;20:930–936.
    1. Van Hilten J.J., Ferrari M.D., Van der Meer J.W.M., Gijsman H.J., Looij B.J., Jr. Plasma interleukin-1, tumour necrosis factor and hypothalamic-pituitary-adrenal axis responses during migraine attacks. Cephalalgia. 1991;11:65–67. doi: 10.1046/j.1468-2982.1991.1102065.x.
    1. Tanure M.T., Gomez R.S., Hurtado R.C., Teixeira A.L., Domingues R.B. Increased serum levels of brain-derived neurotropic factor during migraine attacks: A pilot study. J. Headache Pain. 2010;11:427–430. doi: 10.1007/s10194-010-0233-0.
    1. Martelletti P., Stirparo G., Morrone S., Rinaldi C., Giacovazzo M. Inhibition of intercellular adhesion molecule-1 (ICAM-1), soluble ICAM-1 and interleukin-4 by nitric oxide expression in migraine patients. J. Mol. Med. 1997;75:448–453. doi: 10.1007/s001090050130.
    1. Fidan I., Yüksel S., Ymir T., Irkeç C., Aksakal F.N. The importance of cytokines, chemokines and nitric oxide in pathophysiology of migraine. J. Neuroimmunol. 2006;171:184–188. doi: 10.1016/j.jneuroim.2005.10.005.
    1. Munno I., Marinaro M., Bassi A., Cassiano M.A., Causarano V., Centonze V. Immunological aspects in migraine: Increase of IL-10 plasma levels during attack. Headache. 2001;41:764–767. doi: 10.1046/j.1526-4610.2001.01140.x.
    1. Boćkowski L., Sobaniec W., Zelazowska-Rutkowska B. Proinflammatory plasma cytokines in children with migraine. Pediatr. Neurol. 2009;41:17–21. doi: 10.1016/j.pediatrneurol.2009.02.001.
    1. Uzar E., Evliyaoglu O., Yucel Y., Ugur Cevik M., Acar A., Guzel I., Islamoglu Y., Colpan L., Tasdemir N. Serum cytokine and pro-brain natriuretic peptide (BNP) levels in patients with migraine. Eur. Rev. Med. Pharmacol. Sci. 2011;15:1111–1116.
    1. Oliveira A.B., Bachi A.L.L., Ribeiro R.T., Mello M.T., Tufik S., Peres M.F.P. Unbalanced plasma TNF-α and IL-12/IL-10 profile in women with migraine is associated with psychological and physiological outcomes. J. Neuroimmunol. 2017;313:138–144. doi: 10.1016/j.jneuroim.2017.09.008.
    1. Duarte H., Teixeira A.L., Rocha N.P., Domingues R.B. Increased interictal serum levels of CXCL8/IL-8 and CCL3/MIP-1α in migraine. Neurol. Sci. 2015;36:203–208. doi: 10.1007/s10072-014-1931-1.
    1. Empl M., Sostak P., Riedel M., Schwarz M., Müller N., Förderreuther S., Straube A. Decreased sTNF-RI in migraine patients? Cephalalgia. 2003;23:55–58. doi: 10.1046/j.1468-2982.2003.00453.x.
    1. Michalak S., Kalinowska-Lyszczarz A., Wegrzyn D., Niezgoda A., Losy J., Osztynowicz K., Kozubski W. Increased Serum CD14 Level Is Associated with Depletion of TNF-alpha in Monocytes in Migraine Patients during Interictal Period. Int. J. Mol. Sci. 2017;18:398. doi: 10.3390/ijms18020398.
    1. Sarchielli P., Alberti A., Vaianella L., Pierguidi L., Floridi A., Mazzotta G., Floridi A., Gallai V. Chemokine levels in the jugular venous blood of migraine without aura patients during attacks. Headache. 2004;44:961–968. doi: 10.1111/j.1526-4610.2004.04189.x.
    1. Sarchielli P., Floridi A., Mancini M.L., Rossi C., Coppola F., Baldi A., Pini L.A., Calabresi P. NF-kappaB activity and iNOS expression in monocytes from internal jugular blood of migraine without aura patients during attacks. Cephalalgia. 2006;26:1071–1079. doi: 10.1111/j.1468-2982.2006.01164.x.
    1. Rozen T., Swidan S.Z. Elevation of CSF Tumor Necrosis Factor α Levels in New Daily Persistent Headache and Treatment Refractory Chronic Migraine. Headache J. Head Face Pain. 2007;47:1050–1055. doi: 10.1111/j.1526-4610.2006.00722.x.
    1. Bø S.H., Davidsen E.M., Gulbrandsen P., Dietrichs E., Bovim G., Stovner L.J., White L.R. Cerebrospinal fluid cytokine levels in migraine, tension-type headache and cervicogenic headache. Cephalalgia. 2009;29:365–372. doi: 10.1111/j.1468-2982.2008.01727.x.
    1. Gormley P., Anttila V., Winsvold B.S., Palta P., Esko T., Pers T.H., Farh K.H., Cuenca-Leon E., Muona M., Furlotte N.A., et al. Meta-analysis of 375,000 individuals identifies 38 susceptibility loci for migraine. Nat. Genet. 2016;48:856–866. doi: 10.1038/ng.3598.
    1. Yilmaz I.A., Ozge A., Erdal M.E., Edgünlü T.G., Cakmak S.E., Yalin O.O. Cytokine polymorphism in patients with migraine: Some suggestive clues of migraine and inflammation. Pain Med. 2010;11:492–497. doi: 10.1111/j.1526-4637.2009.00791.x.
    1. Perry C.J., Blake P., Buettner C., Papavassiliou E., Schain A.J., Bhasin M.K., Burstein R. Upregulation of inflammatory gene transcripts in periosteum of chronic migraineurs: Implications for extracranial origin of headache. Ann. Neurol. 2016;79:1000–1013. doi: 10.1002/ana.24665.
    1. Somjen G.G., Aitken P.G., Czéh G.L., Herreras O., Jing J., Young J.N. Mechanism of spreading depression: A review of recent findings and a hypothesis. Can. J. Physiol. Pharmacol. 1992;70:S248–S254. doi: 10.1139/y92-268.
    1. Somjen G.G. Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol. Rev. 2001;81:1065–1096. doi: 10.1152/physrev.2001.81.3.1065.
    1. Leao A.A. Further observations on the spreading depression of activity in the cerebral cortex. J. Neurophysiol. 1947;10:409–414. doi: 10.1152/jn.1947.10.6.409.
    1. Dreier J.P., Fabricius M., Ayata C., Sakowitz O.W., Shuttleworth C.W., Dohmen C., Graf R., Vajkoczy P., Helbok R., Suzuki M., et al. Recording, analysis, and interpretation of spreading depolarizations in neurointensive care: Review and recommendations of the COSBID research group. J. Cereb. Blood Flow Metab. 2017;37:1595–1625. doi: 10.1177/0271678X16654496.
    1. Hartings J.A., Shuttleworth C.W., Kirov S.A., Ayata C., Hinzman J.M., Foreman B., Andrew R.D., Boutelle M.G., Brennan K.C., Carlson A.P., et al. The continuum of spreading depolarizations in acute cortical lesion development: Examining Leão’s legacy. J. Cereb. Blood Flow Metab. 2017;37:1571–1594. doi: 10.1177/0271678X16654495.
    1. Zhang X., Levy D., Kainz V., Noseda R., Jakubowski M., Burstein R. Activation of central trigeminovascular neurons by cortical spreading depression. Ann. Neurol. 2011;69:855–865. doi: 10.1002/ana.22329.
    1. Ayata C., Jin H., Kudo C., Dalkara T., Moskowitz M.A. Suppression of cortical spreading depression in migraine prophylaxis. Ann. Neurol. 2006;59:652–661. doi: 10.1002/ana.20778.
    1. Karatas H., Erdener S.E., Gursoy-Ozdemir Y., Lule S., Eren-Koçak E., Sen Z.D., Dalkara T. Spreading depression triggers headache by activating neuronal Panx1 channels. Science. 2013;339:1092–1095. doi: 10.1126/science.1231897.
    1. Kraig R.P., Mitchell H.M., Christie-Pope B., Kunkler P.E., White D.M., Tang Y.P., Langan G. TNF-alpha and Microglial Hormetic Involvement in Neurological Health & Migraine. Dose Response. 2010;8:389–413. doi: 10.2203/dose-response.09-056.Kraig.
    1. Levy D. Endogenous mechanisms underlying the activation and sensitization of meningeal nociceptors: The role of immuno-vascular interactions and cortical spreading depression. Curr. Pain Headache Rep. 2012;16:270–277. doi: 10.1007/s11916-012-0255-1.
    1. Jander S., Schroeter M., Peters O., Witte O.W., Stoll G. Cortical spreading depression induces proinflammatory cytokine gene expression in the rat brain. J. Cereb. Blood Flow Metab. 2001;21:218–225. doi: 10.1097/00004647-200103000-00005.
    1. Ghaemi A., Sajadian A., Khodaie B., Lotfinia A.A., Lotfinia M., Aghabarari A., Khaleghi Ghadiri M., Meuth S., Gorji A. Immunomodulatory Effect of Toll-Like Receptor-3 Ligand Poly I:C on Cortical Spreading Depression. Mol. Neurobiol. 2016;53:143–154. doi: 10.1007/s12035-014-8995-z.
    1. Ghaemi A., Alizadeh L., Babaei S., Jafarian M., Khaleghi Ghadiri M., Meuth S.G., Kovac S., Gorji A. Astrocyte-mediated inflammation in cortical spreading depression. Cephalalgia. 2018;38:626–638. doi: 10.1177/0333102417702132.
    1. Kunkler P.E., Hulse R.E., Kraig R.P. Multiplexed cytokine protein expression profiles from spreading depression in hippocampal organotypic cultures. J. Cereb. Blood Flow Metab. 2004;24:829–839. doi: 10.1097/01.WCB.0000126566.34753.30.
    1. Thompson C.S., Hakim A.M. Cortical spreading depression modifies components of the inflammatory cascade. Mol. Neurobiol. 2005;32:51–57. doi: 10.1385/MN:32:1:051.
    1. Chen S.P., Qin T., Seidel J.L., Zheng Y., Eikermann M., Ferrari M.D., van den Maagdenberg A., Moskowitz M.A., Ayata C., Eikermann-Haerter K. Inhibition of the P2X7-PANX1 complex suppresses spreading depolarization and neuroinflammation. Brain. 2017;140:1643–1656. doi: 10.1093/brain/awx085.
    1. Choudhuri R., Cui L., Yong C., Bowyer S., Klein R.M., Welch K.M., Berman N.E. Cortical spreading depression and gene regulation: Relevance to migraine. Ann. Neurol. 2002;51:499–506. doi: 10.1002/ana.10158.
    1. Urbach A., Bruehl C., Witte O.W. Microarray-based long-term detection of genes differentially expressed after cortical spreading depression. Eur. J. Neurosci. 2006;24:841–856. doi: 10.1111/j.1460-9568.2006.04862.x.
    1. Wang H., Peca J., Matsuzaki M., Matsuzaki K., Noguchi J., Qiu L., Wang D., Zhang F., Boyden E., Deisseroth K., et al. High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice. Proc. Natl. Acad. Sci. USA. 2007;104:8143–8148. doi: 10.1073/pnas.0700384104.
    1. Arenkiel B.R., Peca J., Davison I.G., Feliciano C., Deisseroth K., Augustine G.J., Ehlers M.D., Feng G. In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron. 2007;54:205–218. doi: 10.1016/j.neuron.2007.03.005.
    1. Chung D.Y., Sadeghian H., Qin T., Lule S., Lee H., Karakaya F., Goins S., Oka F., Yaseen M.A., Houben T., et al. Determinants of Optogenetic Cortical Spreading Depolarizations. Cereb. Cortex. 2019;29:1150–1161. doi: 10.1093/cercor/bhy021.
    1. Takizawa T., Qin T., Lopes de Morais A., Sugimoto K., Chung J.Y., Morsett L., Mulder I., Fischer P., Suzuki T., Anzabi M., et al. Non-invasively triggered spreading depolarizations induce a rapid pro-inflammatory response in cerebral cortex. J. Cereb. Blood Flow Metab. 2019;40:1117–1131. doi: 10.1177/0271678X19859381.
    1. Friedman B.W., Greenwald P., Bania T.C., Esses D., Hochberg M., Solorzano C., Corbo J., Chu J., Chew E., Cheung P., et al. Randomized trial of IV dexamethasone for acute migraine in the emergency department. Neurology. 2007;69:2038–2044. doi: 10.1212/01.WNL.0000281105.78936.1d.
    1. Rowe B.H., Colman I., Edmonds M.L., Blitz S., Walker A., Wiens S. Randomized controlled trial of intravenous dexamethasone to prevent relapse in acute migraine headache. Headache. 2008;48:333–340. doi: 10.1111/j.1526-4610.2007.00959.x.
    1. Donaldson D., Sundermann R., Jackson R., Bastani A. Intravenous dexamethasone vs placebo as adjunctive therapy to reduce the recurrence rate of acute migraine headaches: A multicenter, double-blinded, placebo-controlled randomized clinical trial. Am. J. Emerg. Med. 2008;26:124–130. doi: 10.1016/j.ajem.2007.03.029.
    1. Demartini C., Greco R., Zanaboni A.M., Sances G., De Icco R., Borsook D., Tassorelli C. Nitroglycerin as a comparative experimental model of migraine pain: From animal to human and back. Prog. Neurobiol. 2019;177:15–32. doi: 10.1016/j.pneurobio.2019.02.002.
    1. Reuter U., Bolay H., Jansen-Olesen I., Chiarugi A., Sanchez del Rio M., Letourneau R., Theoharides T.C., Waeber C., Moskowitz M.A. Delayed inflammation in rat meninges: Implications for migraine pathophysiology. Brain. 2001;124:2490–2502. doi: 10.1093/brain/124.12.2490.
    1. Reuter U., Chiarugi A., Bolay H., Moskowitz M.A. Nuclear factor-kappaB as a molecular target for migraine therapy. Ann. Neurol. 2002;51:507–516. doi: 10.1002/ana.10159.
    1. Greco R., Demartini C., Zanaboni A.M., Redavide E., Pampalone S., Toldi J., Fülöp F., Blandini F., Nappi G., Sandrini G., et al. Effects of kynurenic acid analogue 1 (KYNA-A1) in nitroglycerin-induced hyperalgesia: Targets and anti-migraine mechanisms. Cephalalgia. 2017;37:1272–1284. doi: 10.1177/0333102416678000.
    1. Greco R., Demartini C., Zanaboni A., Casini I., De Icco R., Reggiani A., Misto A., Piomelli D., Tassorelli C. Characterization of the peripheral FAAH inhibitor, URB937, in animal models of acute and chronic migraine. Neurobiol. Dis. 2021;147:105157. doi: 10.1016/j.nbd.2020.105157.
    1. He W., Long T., Pan Q., Zhang S., Zhang Y., Zhang D., Qin G., Chen L., Zhou J. Microglial NLRP3 inflammasome activation mediates IL-1β release and contributes to central sensitization in a recurrent nitroglycerin-induced migraine model. J. Neuroinflammation. 2019;16:78. doi: 10.1186/s12974-019-1459-7.
    1. Sparaco M., Feleppa M., Lipton R.B., Rapoport A.M., Bigal M.E. Mitochondrial dysfunction and migraine: Evidence and hypotheses. Cephalalgia. 2006;26:361–372. doi: 10.1111/j.1468-2982.2005.01059.x.
    1. Yilmaz G., Sürer H., Inan L.E., Coskun O., Yücel D. Increased nitrosative and oxidative stress in platelets of migraine patients. Tohoku J. Exp. Med. 2007;211:23–30. doi: 10.1620/tjem.211.23.
    1. Rajamäki K., Nordström T., Nurmi K., Åkerman K.E., Kovanen P.T., Öörni K., Eklund K.K. Extracellular acidosis is a novel danger signal alerting innate immunity via the NLRP3 inflammasome. J. Biol. Chem. 2013;288:13410–13419. doi: 10.1074/jbc.M112.426254.
    1. Gölöncsér F., Sperlágh B. Effect of genetic deletion and pharmacological antagonism of P2X7 receptors in a mouse animal model of migraine. J. Headache Pain. 2014;15:24. doi: 10.1186/1129-2377-15-24.
    1. Gursoy-Ozdemir Y., Qiu J., Matsuoka N., Bolay H., Bermpohl D., Jin H., Wang X., Rosenberg G.A., Lo E.H., Moskowitz M.A. Cortical spreading depression activates and upregulates MMP-9. J. Clin. Investig. 2004;113:1447–1455. doi: 10.1172/JCI200421227.
    1. Cottier K.E., Galloway E.A., Calabrese E.C., Tome M.E., Liktor-Busa E., Kim J., Davis T.P., Vanderah T.W., Largent-Milnes T.M. Loss of Blood-Brain Barrier Integrity in a KCl-Induced Model of Episodic Headache Enhances CNS Drug Delivery. eNeuro. 2018;5 doi: 10.1523/ENEURO.0116-18.2018.
    1. Sadeghian H., Lacoste B., Qin T., Toussay X., Rosa R., Oka F., Chung D.Y., Takizawa T., Gu C., Ayata C. Spreading depolarizations trigger caveolin-1-dependent endothelial transcytosis. Ann. Neurol. 2018;84:409–423. doi: 10.1002/ana.25298.
    1. Harriott A.M., Takizawa T., Chung D.Y., Chen S.P. Spreading depression as a preclinical model of migraine. J. Headache Pain. 2019;20:45. doi: 10.1186/s10194-019-1001-4.
    1. Lundblad C., Haanes K.A., Grände G., Edvinsson L. Experimental inflammation following dural application of complete Freund’s adjuvant or inflammatory soup does not alter brain and trigeminal microvascular passage. J. Headache Pain. 2015;16:91. doi: 10.1186/s10194-015-0575-8.
    1. Edvinsson L., Tfelt-Hansen P. The blood-brain barrier in migraine treatment. Cephalalgia. 2008;28:1245–1258. doi: 10.1111/j.1468-2982.2008.01675.x.
    1. Imamura K., Takeshima T., Fusayasu E., Nakashima K. Increased plasma matrix metalloproteinase-9 levels in migraineurs. Headache. 2008;48:135–139. doi: 10.1111/j.1526-4610.2007.00958.x.
    1. Martins-Oliveira A., Gonçalves F.M., Speciali J.G., Fontana V., Izidoro-Toledo T.C., Belo V.A., Dach F., Tanus-Santos J.E. Specific matrix metalloproteinase 9 (MMP-9) haplotype affect the circulating MMP-9 levels in women with migraine. J. Neuroimmunol. 2012;252:89–94. doi: 10.1016/j.jneuroim.2012.07.016.
    1. Dong L., Qiao H., Zhang X., Zhang X., Wang C., Wang L., Cui L., Zhao J., Xing Y., Li Y., et al. Parthenolide is neuroprotective in rat experimental stroke model: Downregulating NF-κB, phospho-p38MAPK, and caspase-1 and ameliorating BBB permeability. Mediat. Inflamm. 2013;2013:370804. doi: 10.1155/2013/370804.
    1. Sarrazin S., Adam E., Lyon M., Depontieu F., Motte V., Landolfi C., Lortat-Jacob H., Bechard D., Lassalle P., Delehedde M. Endocan or endothelial cell specific molecule-1 (ESM-1): A potential novel endothelial cell marker and a new target for cancer therapy. Biochim. Biophys. Acta. 2006;1765:25–37. doi: 10.1016/j.bbcan.2005.08.004.
    1. Hougaard A., Amin F.M., Christensen C.E., Younis S., Wolfram F., Cramer S.P., Larsson H.B.W., Ashina M. Increased brainstem perfusion, but no blood-brain barrier disruption, during attacks of migraine with aura. Brain. 2017;140:1633–1642. doi: 10.1093/brain/awx089.
    1. Amin F.M., Hougaard A., Cramer S.P., Christensen C.E., Wolfram F., Larsson H.B.W., Ashina M. Intact blood-brain barrier during spontaneous attacks of migraine without aura: A 3T DCE-MRI study. Eur. J. Neurol. 2017;24:1116–1124. doi: 10.1111/ene.13341.
    1. Schankin C.J., Maniyar F.H., Seo Y., Kori S., Eller M., Chou D.E., Blecha J., Murphy S.T., Hawkins R.A., Sprenger T., et al. Ictal lack of binding to brain parenchyma suggests integrity of the blood-brain barrier for 11C-dihydroergotamine during glyceryl trinitrate-induced migraine. Brain. 2016;139:1994–2001. doi: 10.1093/brain/aww096.
    1. Jansson D., Rustenhoven J., Feng S., Hurley D., Oldfield R.L., Bergin P.S., Mee E.W., Faull R.L., Dragunow M. A role for human brain pericytes in neuroinflammation. J. Neuroinflamm. 2014;11:104. doi: 10.1186/1742-2094-11-104.
    1. Sweeney M.D., Zhao Z., Montagne A., Nelson A.R., Zlokovic B.V. Blood-Brain Barrier: From Physiology to Disease and Back. Physiol. Rev. 2019;99:21–78. doi: 10.1152/physrev.00050.2017.
    1. Khennouf L., Gesslein B., Brazhe A., Octeau J.C., Kutuzov N., Khakh B.S., Lauritzen M. Active role of capillary pericytes during stimulation-induced activity and spreading depolarization. Brain. 2018;141:2032–2046. doi: 10.1093/brain/awy143.
    1. Kovac A., Erickson M.A., Banks W.A. Brain microvascular pericytes are immunoactive in culture: Cytokine, chemokine, nitric oxide, and LRP-1 expression in response to lipopolysaccharide. J. Neuroinflammation. 2011;8:139. doi: 10.1186/1742-2094-8-139.
    1. Alcendor D.J., Charest A.M., Zhu W.Q., Vigil H.E., Knobel S.M. Infection and upregulation of proinflammatory cytokines in human brain vascular pericytes by human cytomegalovirus. J. Neuroinflammation. 2012;9:95. doi: 10.1186/1742-2094-9-95.
    1. Matsumoto J., Takata F., Machida T., Takahashi H., Soejima Y., Funakoshi M., Futagami K., Yamauchi A., Dohgu S., Kataoka Y. Tumor necrosis factor-α-stimulated brain pericytes possess a unique cytokine and chemokine release profile and enhance microglial activation. Neurosci. Lett. 2014;578:133–138. doi: 10.1016/j.neulet.2014.06.052.
    1. Montagne A., Barnes S.R., Sweeney M.D., Halliday M.R., Sagare A.P., Zhao Z., Toga A.W., Jacobs R.E., Liu C.Y., Amezcua L., et al. Blood-brain barrier breakdown in the aging human hippocampus. Neuron. 2015;85:296–302. doi: 10.1016/j.neuron.2014.12.032.
    1. Matsumoto J., Dohgu S., Takata F., Machida T., Bölükbaşi Hatip F.F., Hatip-Al-Khatib I., Yamauchi A., Kataoka Y. TNF-α-sensitive brain pericytes activate microglia by releasing IL-6 through cooperation between IκB-NFκB and JAK-STAT3 pathways. Brain Res. 2018;1692:34–44. doi: 10.1016/j.brainres.2018.04.023.
    1. Klement W., Garbelli R., Zub E., Rossini L., Tassi L., Girard B., Blaquiere M., Bertaso F., Perroy J., de Bock F., et al. Seizure progression and inflammatory mediators promote pericytosis and pericyte-microglia clustering at the cerebrovasculature. Neurobiol. Dis. 2018;113:70–81. doi: 10.1016/j.nbd.2018.02.002.
    1. Dziewulska D., Kierdaszuk B. Ultrastructural changes in microvessels in familial hemiplegic migraine with CACNA1A mutation. Clin. Neuropathol. 2018;37:283–287. doi: 10.5414/NP300619.
    1. Kossoff E.H., Andermann F. Migraine and Epilepsy. Semin. Pediatr. Neurol. 2010;17:117–122. doi: 10.1016/j.spen.2010.04.005.
    1. Mantegazza M., Cestèle S. Pathophysiological mechanisms of migraine and epilepsy: Similarities and differences. Neurosci. Lett. 2018;667:92–102. doi: 10.1016/j.neulet.2017.11.025.
    1. Cheng J., Korte N., Nortley R., Sethi H., Tang Y., Attwell D. Targeting pericytes for therapeutic approaches to neurological disorders. Acta Neuropathol. 2018;136:507–523. doi: 10.1007/s00401-018-1893-0.
    1. Zhang X., Burstein R., Levy D. Local action of the proinflammatory cytokines IL-1β and IL-6 on intracranial meningeal nociceptors. Cephalalgia. 2012;32:66–72. doi: 10.1177/0333102411430848.
    1. Franceschini A., Vilotti S., Ferrari M.D., van den Maagdenberg A.M., Nistri A., Fabbretti E. TNFα levels and macrophages expression reflect an inflammatory potential of trigeminal ganglia in a mouse model of familial hemiplegic migraine. PLoS ONE. 2013;8:e52394. doi: 10.1371/journal.pone.0052394.
    1. Lombardo S.D., Mazzon E., Basile M.S., Cavalli E., Bramanti P., Nania R., Fagone P., Nicoletti F., Petralia M.C. Upregulation of IL-1 Receptor Antagonist in a Mouse Model of Migraine. Brain Sci. 2019;9:172. doi: 10.3390/brainsci9070172.
    1. De Corato A., Lisi L., Capuano A., Tringali G., Tramutola A., Navarra P., Russo C.D. Trigeminal satellite cells express functional calcitonin gene-related peptide receptors, whose activation enhances interleukin-1β pro-inflammatory effects. J. Neuroimmunol. 2011;237:39–46. doi: 10.1016/j.jneuroim.2011.05.013.
    1. Vezzani A., French J., Bartfai T., Baram T.Z. The role of inflammation in epilepsy. Nat. Rev. Neurol. 2011;7:31–40. doi: 10.1038/nrneurol.2010.178.
    1. Van Vliet E.A., Aronica E., Vezzani A., Ravizza T. Review: Neuroinflammatory pathways as treatment targets and biomarker candidates in epilepsy: Emerging evidence from preclinical and clinical studies. Neuropathol. Appl. Neurobiol. 2018;44:91–111. doi: 10.1111/nan.12444.
    1. Kenney-Jung D.L., Vezzani A., Kahoud R.J., LaFrance-Corey R.G., Ho M.L., Muskardin T.W., Wirrell E.C., Howe C.L., Payne E.T. Febrile infection-related epilepsy syndrome treated with anakinra. Ann. Neurol. 2016;80:939–945. doi: 10.1002/ana.24806.
    1. Jyonouchi H., Geng L. Intractable Epilepsy (IE) and Responses to Anakinra, a Human Recombinant IL-1 Receptor Agonist (IL-1ra): Case Reports. J. Clin. Cell. Immunol. 2016;7:456. doi: 10.4172/2155-9899.1000456.
    1. Yamanaka G., Ishida Y., Kanou K., Suzuki S., Watanabe Y., Takamatsu T., Morichi S., Go S., Oana S., Yamazaki T., et al. Towards a Treatment for Neuroinflammation in Epilepsy: Interleukin-1 Receptor Antagonist, Anakinra, as a Potential Treatment in Intractable Epilepsy. Int. J. Mol. Sci. 2021;22:6282. doi: 10.3390/ijms22126282.
    1. Smith C.J., Hulme S., Vail A., Heal C., Parry-Jones A.R., Scarth S., Hopkins K., Hoadley M., Allan S.M., Rothwell N.J., et al. SCIL-STROKE (Subcutaneous Interleukin-1 Receptor Antagonist in Ischemic Stroke): A Randomized Controlled Phase 2 Trial. Stroke. 2018;49:1210–1216. doi: 10.1161/STROKEAHA.118.020750.
    1. Galea J., Ogungbenro K., Hulme S., Patel H., Scarth S., Hoadley M., Illingworth K., McMahon C.J., Tzerakis N., King A.T., et al. Reduction of inflammation after administration of interleukin-1 receptor antagonist following aneurysmal subarachnoid hemorrhage: Results of the Subcutaneous Interleukin-1Ra in SAH (SCIL-SAH) study. J. Neurosurg. 2018;128:515–523. doi: 10.3171/2016.9.JNS16615.
    1. Sibley C.H., Plass N., Snow J., Wiggs E.A., Brewer C.C., King K.A., Zalewski C., Kim H.J., Bishop R., Hill S., et al. Sustained response and prevention of damage progression in patients with neonatal-onset multisystem inflammatory disease treated with anakinra: A cohort study to determine three- and five-year outcomes. Arthritis Rheum. 2012;64:2375–2386. doi: 10.1002/art.34409.
    1. Kullenberg T., Löfqvist M., Leinonen M., Goldbach-Mansky R., Olivecrona H. Long-term safety profile of anakinra in patients with severe cryopyrin-associated periodic syndromes. Rheumatology. 2016;55:1499–1506. doi: 10.1093/rheumatology/kew208.
    1. Oby E., Janigro D. The blood-brain barrier and epilepsy. Epilepsia. 2006;47:1761–1774. doi: 10.1111/j.1528-1167.2006.00817.x.
    1. Yamanaka G., Morichi S., Takamatsu T., Watanabe Y., Suzuki S., Ishida Y., Oana S., Yamazaki T., Takata F., Kawashima H. Links between Immune Cells from the Periphery and the Brain in the Pathogenesis of Epilepsy: A Narrative Review. Int. J. Mol. Sci. 2021;22:4395. doi: 10.3390/ijms22094395.
    1. Landmann E.C., Walker U.A. Pharmacological treatment options for cryopyrin-associated periodic syndromes. Expert Rev. Clin. Pharmacol. 2017;10:855–864. doi: 10.1080/17512433.2017.1338946.
    1. Gonçalves N.P., Teixeira-Coelho M., Saraiva M.J. Protective role of anakinra against transthyretin-mediated axonal loss and cell death in a mouse model of familial amyloidotic polyneuropathy. J. Neuropathol. Exp. Neurol. 2015;74:203–217. doi: 10.1097/NEN.0000000000000164.
    1. Gonçalves N.P., Vieira P., Saraiva M.J. Interleukin-1 signaling pathway as a therapeutic target in transthyretin amyloidosis. Amyloid. 2014;21:175–184. doi: 10.3109/13506129.2014.927759.
    1. Coll R.C., Robertson A.A., Chae J.J., Higgins S.C., Muñoz-Planillo R., Inserra M.C., Vetter I., Dungan L.S., Monks B.G., Stutz A., et al. A small-molecule inhibitor of the NLRP3 inflammasome for the treatment of inflammatory diseases. Nat. Med. 2015;21:248–255. doi: 10.1038/nm.3806.
    1. Cho J.W., Lee K.S., Kim C.W. Curcumin attenuates the expression of IL-1beta, IL-6, and TNF-alpha as well as cyclin E in TNF-alpha-treated HaCaT cells; NF-kappaB and MAPKs as potential upstream targets. Int. J. Mol. Med. 2007;19:469–474.
    1. Ferreira N., Gonçalves N.P., Saraiva M.J., Almeida M.R. Curcumin: A multi-target disease-modifying agent for late-stage transthyretin amyloidosis. Sci. Rep. 2016;6:26623. doi: 10.1038/srep26623.
    1. Fan C., Song Q., Wang P., Li Y., Yang M., Yu S.Y. Neuroprotective Effects of Curcumin on IL-1β-Induced Neuronal Apoptosis and Depression-Like Behaviors Caused by Chronic Stress in Rats. Front. Cell. Neurosci. 2018;12:516. doi: 10.3389/fncel.2018.00516.
    1. Ferreira N., Saraiva M.J., Almeida M.R. Uncovering the Neuroprotective Mechanisms of Curcumin on Transthyretin Amyloidosis. Int. J. Mol. Sci. 2019;20:1287. doi: 10.3390/ijms20061287.
    1. Bulboacă A.E., Bolboacă S.D., Stănescu I.C., Sfrângeu C.A., Bulboacă A.C. Preemptive Analgesic and Antioxidative Effect of Curcumin for Experimental Migraine. Biomed. Res. Int. 2017;2017:4754701. doi: 10.1155/2017/4754701.
    1. Chen L., Li X., Huang L., Wu Q., Chen L., Wan Q. Chemical stimulation of the intracranial dura activates NALP3 inflammasome in trigeminal ganglia neurons. Brain Res. 2014;1566:1–11. doi: 10.1016/j.brainres.2014.04.019.

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