https://doi.org/10.4081/ahr.2024.4

Piezo channels in migraine and trigeminal pain syndromes: a systematic review of their role in pain pathways

Vol. 1 No. 1 (2024)
Published: May 28, 2024
Piezo channels, migraine, trigeminal pain syndromes, pain medicine
Abstract Views: 1149
PDF: 211
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

Thalis Asimakopoulos
https://orcid.org/0009-0002-7268-3720
School of Medicine, National and Kapodistrian University of Athens; 1st Department of Anesthesiology and Pain Medicine, Aretaieion University Hospital, National and Kapodistrian University of Athens, Greece.
Marianna Kourousi
School of Medicine, National and Kapodistrian University of Athens, Greece.
Giustino Varrassi
Paolo Procacci Foundation, Rome, Italy.
Martina Rekatsina
mrekatsina@gmail.com
https://orcid.org/0000-0002-7671-4056
School of Medicine, National and Kapodistrian University of Athens; 1st Department of Anesthesiology and Pain Medicine, Aretaieion University Hospital, National and Kapodistrian University of Athens, Greece.

Piezo channels, a class of mechanosensitive ion channels, have emerged as key players in sensory transduction. Piezo1 and Piezo2 have been implicated in various physiological processes, including touch sensation and nociception. Their association with migraine and their role in pain involving trigeminal nerve have gained significant research attention. Following PRISMA guidelines, we performed a systematic review of the literature, on the role of Piezo1 and Piezo2 channels in migraine and trigeminal pain. From PubMed, Cochrane Library, and Scopus, we deemed 20 studies published between 2014 and 2023 appropriate to be included in this review. Piezo1 emerges as a key player in migraine pathogenesis, contributing to meningeal nociception and pain generation. In trigeminal pain syndromes, Piezo channels, particularly Piezo2, have a role in various pain conditions, from corneal nociception to dental and orofacial pain. Mechanistic insights provide potential therapeutic targets for migraine and other pain conditions involving trigeminal nerve. This systematic review accentuates the emerging significance of Piezo channels in migraine and trigeminal-associated pain, underscoring cross-associations that interconnect Piezo channels, migraine, and trigeminal neurons, as well as suggesting promising avenues for targeted therapeutic interventions and future research directions.

Dimensions

Altmetric

PlumX Metrics

Downloads

Citations

How to Cite

1.
Asimakopoulos T, Kourousi M, Varrassi G, Rekatsina M. Piezo channels in migraine and trigeminal pain syndromes: a systematic review of their role in pain pathways. Adv Health Res [Internet]. 2024 May 28 [cited 2024 Dec. 21];1(1). Available from: https://www.ahr-journal.org/site/article/view/4
Reina F, Salemi G, Capizzi M, et al. Orofacial migraine and other idiopathic non-dental facial pain syndromes: a clinical survey of a social orofacial patient group. Int J Environ Res Public Health 2023;20:6946. DOI: https://doi.org/10.3390/ijerph20206946
Giniatullin R. Ion channels of nociception. Int J Mol Sci 2020;21:3553. DOI: https://doi.org/10.3390/ijms21103553
De Logu F, Geppetti P. Ion channel pharmacology for pain modulation. Handb Exp Pharmacol 2019;260:161-86. DOI: https://doi.org/10.1007/164_2019_336
Coste B, Mathur J, Schmidt M, et al. Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 2010;330:55-60. DOI: https://doi.org/10.1126/science.1193270
McCarter GC, Levine JD. Ionic basis of a mechanotransduction current in adult rat dorsal root ganglion neurons. Mol Pain 2006;2:28. DOI: https://doi.org/10.1186/1744-8069-2-28
Ranade SS, Woo S-H, Dubin AE, et al. Piezo2 is the major transducer of mechanical forces for touch sensation in mice. Nature 2014;516:121-5. DOI: https://doi.org/10.1038/nature13980
Delmas P, Hao J, Rodat-Despoix L. Molecular mechanisms of mechanotransduction in mammalian sensory neurons. Nat Rev Neurosci 2011;12:139-53. DOI: https://doi.org/10.1038/nrn2993
Jiang Y, Yang X, Jiang J, Xiao B. Structural designs and mechanogating mechanisms of the mechanosensitive Piezo channels. Trends Biochem Sci 2021;46:472-88. DOI: https://doi.org/10.1016/j.tibs.2021.01.008
Ferrari MD, Goadsby PJ, Burstein R, et al. Migraine. Nat Rev Dis Primers 2022;8:2. DOI: https://doi.org/10.1038/s41572-021-00328-4
Della Pietra A, Mikhailov N, Giniatullin R. The emerging role of mechanosensitive Piezo channels in migraine pain. Int J Mol Sci 2020;21:696. DOI: https://doi.org/10.3390/ijms21030696
Dussor G. New discoveries in migraine mechanisms and therapeutic targets. Curr Opin Physiol 2019;11:116-24. DOI: https://doi.org/10.1016/j.cophys.2019.10.013
Zhang M, Wang Y, Geng J, et al. Mechanically activated Piezo channels mediate touch and suppress acute mechanical pain response in mice. Cell Rep 2019;26:1419-31.e4. DOI: https://doi.org/10.1016/j.celrep.2019.01.056
LaPaglia DM, Sapio MR, Burbelo PD, et al.:RNA-Seq investigations of human post-mortem trigeminal ganglia. Cephalalgia 2018;38:912-32. DOI: https://doi.org/10.1177/0333102417720216
Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021;372:n71. DOI: https://doi.org/10.1136/bmj.n71
Hooijmans CR, Rovers MM, De Vries RB, et al. SYRCLE’s risk of bias tool for animal studies. BMC Med Res Methodol 2014;14:43. DOI: https://doi.org/10.1186/1471-2288-14-43
Mikhailov N, Leskinen J, Fagerlund I, et al. Mechanosensitive meningeal nociception via Piezo channels: Implications for pulsatile pain in migraine? Neuropharmacology 2019:149:113-23. DOI: https://doi.org/10.1016/j.neuropharm.2019.02.015
Dolgorukova A, Isaeva JE, Verbitskaya E, et al. Differential effects of the Piezo1 agonist Yoda1 in the trigeminovascular system: An electrophysiological and intravital microscopy study in rats. Exp Neurol 2021;339:113634. DOI: https://doi.org/10.1016/j.expneurol.2021.113634
Krivoshein G, Tolner EA, Maagdenberg AVD, Giniatullin RA. Migraine-relevant sex-dependent activation of mouse meningeal afferents by TRPM3 agonists. J Headache Pain 2022;23:4. DOI: https://doi.org/10.1186/s10194-021-01383-8
Mikhailov N, Plotnikova L, Singh P, et al. Functional characterization of mechanosensitive Piezo1 channels in trigeminal and somatic nerves in a neuron-on-chip model. Int J Mol Sci 2022;23:1370. DOI: https://doi.org/10.3390/ijms23031370
Della Pietra A, Mikhailov N, Giniatullin R. FM1-43 dye memorizes Piezo1 activation in the trigeminal nociceptive system implicated in migraine pain. Int J Mol Sci 2023;24:1688. DOI: https://doi.org/10.3390/ijms24021688
Bron R, Wood RJ, Brock JA, Ivanusic JJ. Piezo2 expression in corneal afferent neurons. J Comp Neurol 2014;522:2967-79. DOI: https://doi.org/10.1002/cne.23560
Alamri A, Bron R, Brock JA, Ivanusic JJ. Transient receptor potential cation channel subfamily V member 1 expressing corneal sensory neurons can be subdivided into at least three subpopulations. Front Neuroanat 2015;9:71. DOI: https://doi.org/10.3389/fnana.2015.00071
Fernández-Trillo J, Florez-Paz D, Íñigo-Portugués A, et al. Piezo2 mediates low-threshold mechanically evoked pain in the cornea. J Neurosci 2020;40:8976-93. DOI: https://doi.org/10.1523/JNEUROSCI.0247-20.2020
Emrick JJ, Von Buchholtz LJ, Ryba NJP. Transcriptomic classification of neurons innervating teeth. J Dent Res 2020;99:1478-85. DOI: https://doi.org/10.1177/0022034520941837
Lee PR, Lee JY, Kim HB, et al. TRPM8 mediates hyperosmotic stimuli-induced nociception in dental afferents. J Dent Res 2020;99:107-14. DOI: https://doi.org/10.1177/0022034519886847
Roh J, Hwang S-M, Lee S-H, et al. Functional expression of Piezo1 in dorsal root ganglion (DRG) neurons. Int J Mol Sci 2020;21:3834. DOI: https://doi.org/10.3390/ijms21113834
Sato M, Ogura K, Kimura M, et al. Activation of mechanosensitive transient receptor potential/Piezo channels in odontoblasts generates action potentials in cocultured Isolectin B 4 –negative medium-sized trigeminal ganglion neurons. J Endod 2018;44:984-991.e2. DOI: https://doi.org/10.1016/j.joen.2018.02.020
Sun X-F, Qiao W-W, Meng L-Y, Bian Z. PIEZO1 ion channels mediate mechanotransduction in odontoblasts. J Endod 2022;48:749-58. DOI: https://doi.org/10.1016/j.joen.2022.02.005
Cho YS, Han HM, Jeong SY, et al. Expression of Piezo1 in the trigeminal neurons and in the axons that innervate the dental pulp. Front Cell Neurosci 2022;16:945948. DOI: https://doi.org/10.3389/fncel.2022.945948
Liu M, Li Y, Zhong J, et al. The effect of IL-6/Piezo2 on the trigeminal neuropathic pain. Aging 2021;13:13615-25. DOI: https://doi.org/10.18632/aging.202887
Luo Z, Liao X, Luo L, et al. Extracellular ATP and cAMP signaling promote Piezo2‐dependent mechanical allodynia after trigeminal nerve compression injury. J Neurochem 2022;160:376-91. DOI: https://doi.org/10.1111/jnc.15537
Bai G, Ross H, Zhang Y, et al. The role of DNA methylation in transcriptional regulation of pro-nociceptive genes in rat trigeminal ganglia. Epigenet Insights 2020;13:251686572093867. DOI: https://doi.org/10.1177/2516865720938677
Chung M-K, Park J, Asgar J, Ro JY. Transcriptome analysis of trigeminal ganglia following masseter muscle inflammation in rats. Mol Pain 2016;12:174480691666852. DOI: https://doi.org/10.1177/1744806916668526
Krivoshein G, Bakreen A, Van Den Maagdenberg AMJM, et al. Activation of meningeal afferents relevant to trigeminal headache pain after photothrombotic stroke lesion: a pilot study in mice. Int J Mol Sci 2022;23:12590. DOI: https://doi.org/10.3390/ijms232012590
Schneider ER, Anderson EO, Feketa VV, et al. A cross-species analysis reveals a general role for Piezo2 in mechanosensory specialization of trigeminal ganglia from tactile specialist birds. Cell Rep 2019;26:1979-1987.e3. DOI: https://doi.org/10.1016/j.celrep.2019.01.100
Zakharov A, Vitale C, Kilinc E, et al. Hunting for origins of migraine pain: cluster analysis of spontaneous and capsaicin-induced firing in meningeal trigeminal nerve fibers. Front Cell Neurosci 2015;9:287. DOI: https://doi.org/10.3389/fncel.2015.00287
Lumpkin EA, Caterina MJ. Mechanisms of sensory transduction in the skin. Nature 2007;445:858-65. DOI: https://doi.org/10.1038/nature05662
Chalfie M. Neurosensory mechanotransduction. Nat Rev Mol Cell Biol 2009;10:44-52. DOI: https://doi.org/10.1038/nrm2595
Lopes DM, Denk F, McMahon SB. The molecular fingerprint of dorsal root and trigeminal ganglion neurons. Front Mol Neurosci 2017;10:304. DOI: https://doi.org/10.3389/fnmol.2017.00304
Russell FA, King R, Smillie S-J, et al. Calcitonin gene-related peptide: physiology and pathophysiology. Physiol Rev 2014;94:1099-142. DOI: https://doi.org/10.1152/physrev.00034.2013
Giniatullin R, Nistri A, Fabbretti E. Molecular mechanisms of sensitization of pain-transducing P2X3 receptors by the migraine mediators CGRP and NGF. Mol Neurobiol 2008;37:83-90. DOI: https://doi.org/10.1007/s12035-008-8020-5
Lassen L, Haderslev P, Jacobsen V, et al. Cgrp may play a causative role in migraine. Cephalalgia 2002;22:54-61. DOI: https://doi.org/10.1046/j.1468-2982.2002.00310.x
Cernuda-Morollon E, Larrosa D, Ramon C, et al. Interictal increase of CGRP levels in peripheral blood as a biomarker for chronic migraine. Neurology 2013;81:1191-6. DOI: https://doi.org/10.1212/WNL.0b013e3182a6cb72
Olesen J, Diener H-C, Husstedt IW, et al. Calcitonin gene–related peptide receptor antagonist BIBN 4096 BS for the acute treatment of migraine. N Engl J Med 2004;350:1104-10. DOI: https://doi.org/10.1056/NEJMoa030505
Syeda R. Physiology and pathophysiology of mechanically activated PIEZO channels. Annu Rev Neurosci 2021;44:383-402. DOI: https://doi.org/10.1146/annurev-neuro-093020-120939

How to Cite

1.
Asimakopoulos T, Kourousi M, Varrassi G, Rekatsina M. Piezo channels in migraine and trigeminal pain syndromes: a systematic review of their role in pain pathways. Adv Health Res [Internet]. 2024 May 28 [cited 2024 Dec. 21];1(1). Available from: https://www.ahr-journal.org/site/article/view/4
Copyright (c) 2024 the Author(s) Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

PAGEPress has chosen to apply the Creative Commons Attribution NonCommercial 4.0 International License (CC BY-NC 4.0) to all manuscripts to be published.


Similar Articles

You may also start an advanced similarity search for this article.