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Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Commentary

Mechanotransductive Receptor Piezo1 as a Promising Target in the Treatment of Neurological Diseases

Author(s): Natalia Bryniarska-Kubiak, Andrzej Kubiak and Agnieszka Basta-Kaim*

Volume 21, Issue 10, 2023

Published on: 08 March, 2023

Page: [2030 - 2035] Pages: 6

DOI: 10.2174/1570159X20666220927103454

Abstract

In recent years, increasing attention has been paid to the role of physical factors in biological processes. This direction was ultimately confirmed by the recent 2021 Nobel Prize in medicine and physiology awarded in ½ to Ardem Patapoutian for his discovery of Piezo1 and Piezo2 mechanosensitive receptors. Among them, Piezo2 is responsible for sensing touch, while Piezo1 is engaged in a variety of mechanotransduction events. Piezo1 is expressed in various central nervous system cells, while its expression may be affected in the course of various pathological conditions. Recently, thanks to the development of Piezo1 modulators (i.e. Yoda1, Jedi1/2 and Dooku2), it is possible to study the role of Piezo1 in the pathogenesis of various neurological diseases including ischemia, glioma, and age-related dementias. The results obtained in this field suggest that proper modulation of Piezo1 receptor might be beneficial in the course of various neurological diseases.

Keywords: Piezo1 receptor, Alzheimer's disease, ischemic stroke, GsMTx4, mechanotransduction, biomechanics.

[1]
Hayward, M.K.; Muncie, J.M.; Weaver, V.M. Tissue mechanics in stem cell fate, development, and cancer. Dev. Cell, 2021, 56(13), 1833-1847.
[http://dx.doi.org/10.1016/j.devcel.2021.05.011] [PMID: 34107299]
[2]
Gattazzo, F.; Urciuolo, A.; Bonaldo, P. Extracellular matrix: A dynamic microenvironment for stem cell niche. Biochim. Biophys. Acta, Gen. Subj., 2014, 1840(8), 2506-2519.
[http://dx.doi.org/10.1016/j.bbagen.2014.01.010] [PMID: 24418517]
[3]
Bryniarska, N.; Kubiak, A.; Anna Łabędź-Masłowska Ewa Zuba-Surma, Impact of developmental origin, niche mechanics and oxygen availability on osteogenic differentiation capacity of mesenchymal stem/stromal cells. Acta Biochim. Pol., 2019, 66(4), 491-498.
[http://dx.doi.org/10.18388/abp.2019_2893] [PMID: 31883439]
[4]
Butcher, D.T.; Alliston, T.; Weaver, V.M. A tense situation: forcing tumour progression. Nat. Rev. Cancer, 2009, 9(2), 108-122.
[http://dx.doi.org/10.1038/nrc2544] [PMID: 19165226]
[5]
Pickup, M.W.; Mouw, J.K.; Weaver, V.M. The extracellular matrix modulates the hallmarks of cancer. EMBO Rep., 2014, 15(12), 1243-1253.
[http://dx.doi.org/10.15252/embr.201439246] [PMID: 25381661]
[6]
Dufrêne, Y.F. Using nanotechniques to explore microbial surfaces. Nat. Rev. Microbiol., 2004, 2(6), 451-460.
[http://dx.doi.org/10.1038/nrmicro905]
[7]
Harrison, D.G.; Widder, J.; Grumbach, I.; Chen, W.; Weber, M.; Searles, C. Endothelial mechanotransduction, nitric oxide and vascular inflammation. J. Intern. Med., 2006, 259(4), 351-363.
[http://dx.doi.org/10.1111/j.1365-2796.2006.01621.x] [PMID: 16594903]
[8]
Stalnikowitz, D.K.; Weissbrod, A.B. Liver fibrosis and inflammation. A review. Ann. Hepatol., 2003, 2(4), 159-163.
[http://dx.doi.org/10.1016/S1665-2681(19)32127-1] [PMID: 15115954]
[9]
Bryniarska-Kubiak, N.; Kubiak, A.; Lekka, M.; Basta-Kaim, A. The emerging role of mechanical and topographical factors in the development and treatment of nervous system disorders: dark and light sides of the force. Pharmacol. Rep., 2021, 73(6), 1626-1641.
[http://dx.doi.org/10.1007/s43440-021-00315-2] [PMID: 34390472]
[10]
Chighizola, M.; Dini, T.; Lenardi, C.; Milani, P.; Podestà, A.; Schulte, C. Mechanotransduction in neuronal cell development and functioning. Biophys. Rev., 2019, 11(5), 701-720.
[http://dx.doi.org/10.1007/s12551-019-00587-2] [PMID: 31617079]
[11]
Reeh, P.W.; Fischer, M.J.M. Nobel somatosensations and pain. Pflugers Arch., 2022, 474(4), 405-420.
[http://dx.doi.org/10.1007/s00424-022-02667-x] [PMID: 35157132]
[12]
Coste, B.; Mathur, J.; Schmidt, M.; Earley, T.J.; Ranade, S.; Petrus, M.J.; Dubin, A.E.; Patapoutian, A. Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science, 2010, 330(6000), 55-60.
[http://dx.doi.org/10.1126/science.1193270]
[13]
Velasco-Estevez, M.; Gadalla, K.K.E.; Liñan-Barba, N.; Cobb, S.; Dev, K.K.; Sheridan, G.K. Inhibition of Piezo1 attenuates demyelination in the central nervous system. Glia, 2020, 68(2), 356-375.
[http://dx.doi.org/10.1002/glia.23722] [PMID: 31596529]
[14]
Solis, A.G.; Bielecki, P.; Steach, H.R.; Sharma, L.; Harman, C.C.D.; Yun, S.; de Zoete, M.R.; Warnock, J.N.; To, S.D.F. Mechanosensation of cyclical force by PIEZO1 is essential for innate immunity. Nature, 2019, 573(7772), 69-74.
[http://dx.doi.org/10.1038/s41586-019-1485-8] [PMID: 31435009]
[15]
Wang, Y.; Chi, S.; Guo, H.; Li, G.; Wang, L.; Zhao, Q.; Rao, Y.; Zu, L.; He, W.; Xiao, B. A lever-like transduction pathway for long-distance chemical- and mechano-gating of the mechanosensitive Piezo1 channel. Nat. Commun., 2018, 91(1), 1-12.
[16]
Ge, J.; Li, W.; Zhao, Q.; Li, N.; Chen, M.; Zhi, P.; Li, R.; Gao, N.; Xiao, B.; Yang, M. Architecture of the mammalian mechanosensitive Piezo1 channel. Nature, 2015, 527, 64-69.
[http://dx.doi.org/10.1038/nature15247]
[17]
Zhao, Q.; Zhou, H.; Chi, S.; Wang, Y.; Wang, J.; Geng, J.; Wu, K.; Liu, W.; Zhang, T.; Dong, M-Q.; Wang, J.; Li, X.; Xiao, B. Structure and mechanogating mechanism of the Piezo1 channel. Nature, 2018, 554(7693), 487-492.
[http://dx.doi.org/10.1038/nature25743]
[18]
Guo, Y.R.; MacKinnon, R. Structure-based membrane dome mechanism for Piezo mechanosensitivity. eLife, 2017, 6, e33660.
[http://dx.doi.org/10.7554/eLife.33660] [PMID: 29231809]
[19]
Saotome, K.; Murthy, S.E.; Kefauver, J.M.; Whitwam, T.; Patapoutian, A.; Ward, A.B. Structure of the mechanically activated ion channel Piezo1. Nature, 2017, 554(7693), 481-486.
[20]
Yang, X.; Lin, C.; Chen, X.; Li, S.; Li, X.; Xiao, B. Structure deformation and curvature sensing of PIEZO1 in lipid membranes. Nature, 2022, 604(7905), 377-383.
[http://dx.doi.org/10.1038/s41586-022-04574-8] [PMID: 35388220]
[21]
Botello-Smith, W.M.; Jiang, W.; Zhang, H.; Ozkan, A.D.; Lin, Y-C.; Pham, C.N.; Lacroix, J.J.; Luo, Y. A mechanism for the activation of the mechanosensitive Piezo1 channel by the small molecule Yoda1. Nat. Commun., 2019, 10(1), 1-10.
[http://dx.doi.org/10.1038/s41467-019-12501-1]
[22]
Evans, E.L.; Cuthbertson, K.; Endesh, N.; Rode, B.; Blythe, N.M.; Hyman, A.J.; Hall, S.J.; Gaunt, H.J.; Ludlow, M.J.; Foster, R.; Beech, D.J. Yoda1 analogue (Dooku1) which antagonizes Yoda1-evoked activation of Piezo1 and aortic relaxation. Br. J. Pharmacol., 2018, 175(10), 1744-1759.
[http://dx.doi.org/10.1111/bph.14188] [PMID: 29498036]
[23]
Bae, C.; Sachs, F.; Gottlieb, P.A. The mechanosensitive ion channel Piezo1 is inhibited by the peptide GsMTx4. Biochemistry, 2011, 50(29), 6295-6300.
[http://dx.doi.org/10.1021/bi200770q] [PMID: 21696149]
[24]
Gottlieb, P.A.; Suchyna, T.M.; Sachs, F. Properties and mechanism of the mechanosensitive ion channel inhibitor GsMTx4, a therapeutic peptide derived from tarantula venom. Curr. Top. Membr., 2007, 59, 81-109.
[http://dx.doi.org/10.1016/S1063-5823(06)59004-0] [PMID: 25168134]
[25]
Romero, L.O.; Massey, A.E.; Mata-Daboin, A.D.; Sierra-Valdez, F.J.; Chauhan, S.C.; Cordero-Morales, J.F.; Vásquez, V. Dietary fatty acids fine-tune Piezo1 mechanical response. Nat. Commun., 2019, 10(1), 1-14.
[26]
Pathak, M.M.; Nourse, J.L.; Tran, T.; Hwe, J.; Arulmoli, J.; Le, D.T.T.; Bernardis, E.; Flanagan, L.A.; Tombola, F. Stretch-activated ion channel Piezo1 directs lineage choice in human neural stem cells. Proc. Natl. Acad. Sci. USA, 2014, 111(45), 16148-16153.
[http://dx.doi.org/10.1073/pnas.1409802111] [PMID: 25349416]
[27]
Szade, K.; Gulati, G.S.; Chan, C.K.F.; Kao, K.S.; Miyanishi, M.; Marjon, K.D.; Sinha, R.; George, B.M.; Chen, J.Y.; Weissman, I.L. Where hematopoietic stem cells live: The bone marrow niche. Antioxid. Redox Signal., 2018, 29(2), 191-204.
[http://dx.doi.org/10.1089/ars.2017.7419] [PMID: 29113449]
[28]
Bianco, P.; Cao, X.; Frenette, P.S.; Mao, J.J.; Robey, P.G.; Simmons, P.J.; Wang, C-Y. The meaning, the sense and the significance: translating the science of mesenchymal stem cells into medicine. Nat. Med., 2013, 19(1), 35-42.
[http://dx.doi.org/10.1038/nm.3028]
[29]
Song, Y.; Li, D.; Farrelly, O.; Miles, L.; Li, F.; Kim, S.E.; Lo, T.Y.; Wang, F.; Li, T.; Thompson-Peer, K.L.; Gong, J.; Murthy, S.E.; Coste, B.; Yakubovich, N.; Patapoutian, A.; Xiang, Y.; Rompolas, P.; Jan, L.Y.; Jan, Y.N. The mechanosensitive ion channel piezo inhibits axon regeneration. Neuron, 2019, 102(2), 373-389.
[http://dx.doi.org/10.1016/j.neuron.2019.01.050]
[30]
Zhou, W.; Liu, X.; van Wijnbergen, J.W.M.; Yuan, L.; Liu, Y.; Zhang, C.; Jia, W. Identification of PIEZO1 as a potential prognostic marker in gliomas. Sci. Reports, 2020, 10(1), 1-14.
[http://dx.doi.org/10.1038/s41598-020-72886-8]
[31]
Qu, S.; Hu, T.; Qiu, O.; Su, Y.; Gu, J.; Xia, Z. Effect of piezo1 overexpression on peritumoral brain edema in glioblastomas. AJNR Am. J. Neuroradiol., 2020, 41(8), 1423-1429.
[http://dx.doi.org/10.3174/ajnr.A6638] [PMID: 32675337]
[32]
Wang, Y.Y.; Zhang, H.; Ma, T.; Lu, Y.; Xie, H.Y.; Wang, W.; Ma, Y.H.; Li, G.H.; Li, Y.W. Piezo1 mediates neuron oxygen-glucose deprivation/reoxygenation injury via Ca2+/calpain signaling. Biochem. Biophys. Res. Commun., 2019, 513(1), 147-153.
[http://dx.doi.org/10.1016/j.bbrc.2019.03.163] [PMID: 30948157]
[33]
Velasco-Estevez, M.; Mampay, M.; Boutin, H.; Chaney, A.; Warn, P.; Sharp, A.; Burgess, E.; Moeendarbary, E.; Dev, K.K.; Sheridan, G.K. Infection augments expression of mechanosensing piezo1 channels in amyloid plaque-reactive astrocytes. Front. Aging Neurosci., 2018, 10, 332.
[http://dx.doi.org/10.3389/fnagi.2018.00332] [PMID: 30405400]
[34]
Liu, H.; Bian, W.; Yang, D.; Yang, M.; Luo, H. Inhibiting the Piezo1 channel protects microglia from acute hyperglycaemia damage through the JNK1 and mTOR signalling pathways. Life Sci., 2021, 264, 118667.
[http://dx.doi.org/10.1016/j.lfs.2020.118667] [PMID: 33127514]
[35]
Maneshi, M.M.; Ziegler, L.; Sachs, F.; Hua, S.Z.; Gottlieb, P.A. Enantiomeric Aβ peptides inhibit the fluid shear stress response of PIEZO1. Sci. Rep., 2018, 8(1), 14267.
[http://dx.doi.org/10.1038/s41598-018-32572-2] [PMID: 30250223]
[36]
Ivkovic, S.; Major, T.; Mitic, M.; Loncarevic-Vasiljkovic, N.; Jovic, M.; Adzic, M. Fatty acids as biomodulators of Piezo1 mediated glial mechanosensitivity in Alzheimer’s disease. Life Sci., 2022, 297, 120470.
[http://dx.doi.org/10.1016/j.lfs.2022.120470] [PMID: 35283177]
[37]
Li, J.; Hou, B.; Tumova, S.; Muraki, K.; Bruns, A.; Ludlow, M.J.; Sedo, A.; Hyman, A.J.; McKeown, L.; Young, R.S.; Yuldasheva, N.Y.; Majeed, Y.; Wilson, L.A.; Rode, B.; Bailey, M.A.; Kim, H.R.; Fu, Z.; Carter, D.A.L.; Bilton, J.; Imrie, H.; Ajuh, P.; Dear, T.N.; Cubbon, R.M.; Kearney, M.T.; Prasad, K.R.; Evans, P.C.; Ainscough, J.F.X.; Beech, D.J. Piezo1 integration of vascular architecture with physiological force. Nature, 2014, 515(7526), 279-282.
[http://dx.doi.org/10.1038/nature13701] [PMID: 25119035]
[38]
Harraz, O.F.; Klug, N.R.; Senatore, A.; Koide, M.; Nelson, M.T. Piezo1 is a mechanosensor channel in CNS capillaries. J. Gen. Physiol., 2022, 154(9), e2021ecc12.
[http://dx.doi.org/10.1085/jgp.2021ecc12]
[39]
Scimone, C.; Donato, L.; Alibrandi, S.; D’Angelo, R.; Sidoti, A. Evidences of PIEZO1 involvement in cerebral cavernous malformation pathogenesis. Microvasc. Res., 2022, 141, 104342.
[http://dx.doi.org/10.1016/j.mvr.2022.104342] [PMID: 35176291]
[40]
Freedman, L.P.; Cockburn, I.M.; Simcoe, T.S. The economics of reproducibility in preclinical research. PLoS Biol., 2015, 13(6), e1002165.
[http://dx.doi.org/10.1371/journal.pbio.1002165] [PMID: 26057340]
[41]
Ioannidis, J.P.A. How to make more published research true. PLoS Med., 2014, 11(10), e1001747.
[http://dx.doi.org/10.1371/journal.pmed.1001747] [PMID: 25334033]
[42]
Goriely, A.; Budday, S.; Kuhl, E. Neuromechanics: From neurons to brain. Advances in Applied Mechanics; Elsevier: Amsterdam, 2015.
[43]
Seano, G.; Nia, H.T.; Emblem, K.E.; Datta, M.; Ren, J.; Krishnan, S.; Kloepper, J.; Pinho, M.C.; Ho, W.W.; Ghosh, M.; Askoxylakis, V.; Ferraro, G.B.; Riedemann, L.; Gerstner, E.R.; Batchelor, T.T.; Wen, P.Y.; Lin, N.U.; Grodzinsky, A.J.; Fukumura, D.; Huang, P.; Baish, J.W.; Padera, T.P.; Munn, L.L.; Jain, R.K. Solid stress in brain tumours causes neuronal loss and neurological dysfunction and can be reversed by lithium. Nat. Biomed. Eng., 2019, 3(3), 230-245.
[http://dx.doi.org/10.1038/s41551-018-0334-7] [PMID: 30948807]
[44]
Schulte, C.; Rodighiero, S.; Cappelluti, M.A.; Puricelli, L.; Maffioli, E.; Borghi, F.; Negri, A.; Sogne, E.; Galluzzi, M.; Piazzoni, C.; Tamplenizza, M.; Podestà, A.; Tedeschi, G.; Lenardi, C.; Milani, P. Conversion of nanoscale topographical information of cluster-assembled zirconia surfaces into mechanotransductive events promotes neuronal differentiation. J. Nanobiotechnology, 2016, 14(1), 18.
[http://dx.doi.org/10.1186/s12951-016-0171-3] [PMID: 26955876]

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