Mechanosensitive Piezo Channels in Cancer: Focus on altered Calcium Signaling in Cancer Cells and in Tumor Progression
Abstract
1. Introduction
2. Piezo Channels
3. Piezo Channels in Cancer
3.1. Gastric Cancer
3.2. Breast Cancer
3.3. Prostate Cancer
3.4. Glioma
3.5. Osteosarcoma
3.6. Other Cancers
4. Piezo Channels as a Potential Therapeutic Target in Cancer
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Weaver, V.M. Cell and tissue mechanics: The new cell biology frontier. Mol. Biol. Cell 2017, 28, 1815–1818. [Google Scholar] [CrossRef] [PubMed]
- LeGoff, L.; Lecuit, T. Mechanical forces and growth in animal tissues. Cold Spring Harb. Perspect. Biol. 2016, 8, a019232. [Google Scholar] [CrossRef] [PubMed]
- Jansen, K.A.; Donato, D.M.; Balcioglu, H.E.; Schmidt, T.; Danen, E.H.J.; Koenderink, G.H. A guide to mechanobiology: Where biology and physics meet. Biochim. Biophys. Acta Mol. Cell Res. 2015, 1853, 3043–3052. [Google Scholar] [CrossRef] [PubMed]
- Iskratsch, T.; Wolfenson, H.; Sheetz, M.P. Appreciating force and shape-the rise of mechanotransduction in cell biology. Nat. Rev. Mol. Cell Biol. 2014, 15, 825–833. [Google Scholar] [CrossRef]
- Paluch, E.K.; Nelson, C.M.; Biais, N.; Fabry, B.; Moeller, J.; Pruitt, B.L.; Wollnik, C.; Kudryasheva, G.; Rehfeldt, F.; Federle, W. Mechanotransduction: Use the force(s). BMC Biol. 2015, 13, 47. [Google Scholar] [CrossRef] [PubMed]
- Chen, C.S. Mechanotransduction—A field pulling together? J. Cell Sci. 2008, 121, 3285–3292. [Google Scholar] [CrossRef]
- Wang, N. Review of cellular mechanotransduction. J. Phys. D: Appl. Phys. 2017, 50, 233002. [Google Scholar] [CrossRef]
- Kirby, T.J.; Lammerding, J. Cell mechanotransduction: Stretch to express. Nat. Mater. 2016, 15, 1227–1229. [Google Scholar] [CrossRef]
- Martino, F.; Perestrelo, A.R.; Vinarský, V.; Pagliari, S.; Forte, G. Cellular mechanotransduction: From tension to function. Front. Physiol. 2018, 9, 824. [Google Scholar] [CrossRef]
- Strzyz, P. Mechanotransduction: May the force be with you. Nat. Rev. Mol. Cell Biol. 2016, 17, 533. [Google Scholar] [CrossRef]
- Ehmke, H. The mechanotransduction of blood pressure. Science 2018, 362, 398–399. [Google Scholar] [CrossRef] [PubMed]
- Lyon, R.C.; Zanella, F.; Omens, J.H.; Sheikh, F. Mechanotransduction in cardiac hypertrophy and failure. Circ. Res. 2015, 116, 1462–1476. [Google Scholar] [CrossRef]
- Garoffolo, G.; Pesce, M. Mechanotransduction in the Cardiovascular System: From Developmental Origins to Homeostasis and Pathology. Cells 2019, 8, 1607. [Google Scholar] [CrossRef] [PubMed]
- Duscher, D.; Maan, Z.N.; Wong, V.W.; Rennert, R.C.; Januszyk, M.; Rodrigues, M.; Hu, M.; Whitmore, A.J.; Whittam, A.J.; Longaker, M.T.; et al. Mechanotransduction and fibrosis. J. Biomech. 2014, 47, 1997–2005. [Google Scholar] [CrossRef] [PubMed]
- Cooper, J.; Giancotti, F.G. Integrin Signaling in Cancer: Mechanotransduction, Stemness, Epithelial Plasticity, and Therapeutic Resistance. Cancer Cell 2019, 35, 347–367. [Google Scholar] [CrossRef] [PubMed]
- Jang, I.; Beningo, K.A. Integrins, CAFs and mechanical forces in the progression of cancer. Cancers 2019, 11, 721. [Google Scholar] [CrossRef]
- Northey, J.J.; Przybyla, L.; Weaver, V.M. Tissue force programs cell fate and tumor aggression. Cancer Discov. 2017, 7, 1224–1237. [Google Scholar] [CrossRef]
- Basson, M.D.; Zeng, B.; Downey, C.; Sirivelu, M.P.; Tepe, J.J. Increased extracellular pressure stimulates tumor proliferation by a mechanosensitive calcium channel and PKC-β. Mol. Oncol. 2015, 9, 513–526. [Google Scholar] [CrossRef]
- Kai, F.B.; Laklai, H.; Weaver, V.M. Force Matters: Biomechanical Regulation of Cell Invasion and Migration in Disease. Trends Cell Biol. 2016, 26, 486–497. [Google Scholar] [CrossRef]
- Aw Yong, K.M.; Sun, Y.; Merajver, S.D.; Fu, J. Mechanotransduction-Induced Reversible Phenotypic Switching in Prostate Cancer Cells. Biophys. J. 2017, 112, 1236–1245. [Google Scholar] [CrossRef]
- Mohammadi, H.; Sahai, E. Mechanisms and impact of altered tumour mechanics. Nat. Cell Biol. 2018, 20, 766–774. [Google Scholar] [CrossRef] [PubMed]
- Chaudhuri, P.K.; Low, B.C.; Lim, C.T. Mechanobiology of Tumor Growth. Chem. Rev. 2018, 118, 6499–6515. [Google Scholar] [CrossRef]
- Chin, L.K.; Xia, Y.; Discher, D.E.; Janmey, P.A. Mechanotransduction in cancer. Curr. Opin. Chem. Eng. 2016, 11, 77–84. [Google Scholar] [CrossRef] [PubMed]
- Storch, U.; Mederos y Schnitzler, M.; Gudermann, T. G protein-mediated stretch reception. Am. J. Physiol. Hear. Circ. Physiol. 2012, 302, H1241–H1249. [Google Scholar] [CrossRef] [PubMed]
- Dupont, S.; Morsut, L.; Aragona, M.; Enzo, E.; Giulitti, S.; Cordenonsi, M.; Zanconato, F.; Le Digabel, J.; Forcato, M.; Bicciato, S.; et al. Role of YAP/TAZ in mechanotransduction. Nature 2011, 474, 179–184. [Google Scholar] [CrossRef] [PubMed]
- Martinac, B. The ion channels to cytoskeleton connection as potential mechanism of mechanosensitivity. Biochim. Biophys. Acta Biomembr. 2014, 1838, 682–691. [Google Scholar] [CrossRef] [PubMed]
- Yui, S.; Azzolin, L.; Maimets, M.; Pedersen, M.T.; Fordham, R.P.; Hansen, S.L.; Larsen, H.L.; Guiu, J.; Alves, M.R.P.; Rundsten, C.F.; et al. YAP/TAZ-Dependent Reprogramming of Colonic Epithelium Links ECM Remodeling to Tissue Regeneration. Cell Stem Cell 2018, 22, 35–49. [Google Scholar] [CrossRef]
- Ranade, S.S.; Syeda, R.; Patapoutian, A. Mechanically Activated Ion Channels. Neuron 2015, 87, 1162–1179. [Google Scholar] [CrossRef]
- Prevarskaya, N.; Skryma, R.; Shuba, Y. Ion channels in cancer: Are cancer hallmarks oncochannelopathies? Physiol. Rev. 2018, 98, 559–621. [Google Scholar] [CrossRef]
- Douguet, D.; Honoré, E. Mammalian Mechanoelectrical Transduction: Structure and Function of Force-Gated Ion Channels. Cell 2019, 179, 340–354. [Google Scholar] [CrossRef]
- Pethő, Z.; Najder, K.; Bulk, E.; Schwab, A. Mechanosensitive ion channels push cancer progression. Cell Calcium 2019, 80, 79–90. [Google Scholar] [CrossRef]
- Plant, T.D. TRPs in mechanosensing and volume regulation. Handb. Exp. Pharmacol. 2014, 223, 743–766. [Google Scholar] [PubMed]
- Eijkelkamp, N.; Quick, K.; Wood, J.N. Transient Receptor Potential Channels and Mechanosensation. Annu. Rev. Neurosci. 2013, 36, 519–546. [Google Scholar] [CrossRef]
- 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, 55–60. [Google Scholar] [CrossRef] [PubMed]
- Honoré, E.; Martins, J.R.; Penton, D.; Patel, A.; Demolombe, S. The piezo mechanosensitive ion channels: May the force be with you! In Reviews of Physiology, Biochemistry and Pharmacology; Springer: Berlin/Heidelberg, Germany, 2015; Volume 169, pp. 25–42. [Google Scholar]
- Ridone, P.; Vassalli, M.; Martinac, B. Piezo1 mechanosensitive channels: What are they and why are they important. Biophys. Rev. 2019, 11, 795–805. [Google Scholar] [CrossRef] [PubMed]
- Cox, C.D.; Bae, C.; Ziegler, L.; Hartley, S.; Nikolova-Krstevski, V.; Rohde, P.R.; Ng, C.A.; Sachs, F.; Gottlieb, P.A.; Martinac, B. Removal of the mechanoprotective influence of the cytoskeleton reveals PIEZO1 is gated by bilayer tension. Nat. Commun. 2016, 7, 10366. [Google Scholar] [CrossRef]
- Ranade, S.S.; Qiu, Z.; Woo, S.H.; Hur, S.S.; Murthy, S.E.; Cahalan, S.M.; Xu, J.; Mathur, J.; Bandell, M.; Coste, B.; et al. Piezo1, a mechanically activated ion channel, is required for vascular development in mice. Proc. Natl. Acad. Sci. USA 2014, 111, 10347–10352. [Google Scholar] [CrossRef]
- Gottlieb, P.A. A Tour de Force: The Discovery, Properties, and Function of Piezo Channels. In Current Topics in Membranes; Academic Press Inc.: Cambridge, MA, USA, 2017; Volume 79, pp. 1–36. [Google Scholar]
- Geng, J.; Zhao, Q.; Zhang, T.; Xiao, B. In Touch With the Mechanosensitive Piezo Channels: Structure, Ion Permeation, and Mechanotransduction. In Current Topics in Membranes; Academic Press Inc.: Cambridge, MA, USA, 2017; Volume 79, pp. 159–195. [Google Scholar]
- Moroni, M.; Servin-Vences, M.R.; Fleischer, R.; Sánchez-Carranza, O.; Lewin, G.R. Voltage gating of mechanosensitive PIEZO channels. Nat. Commun. 2018, 9, 1096. [Google Scholar] [CrossRef]
- Kamajaya, A.; Kaiser, J.T.; Lee, J.; Reid, M.; Rees, D.C. The structure of a conserved piezo channel domain reveals a topologically distinct β sandwich fold. Structure. 2014, 22, 1520–1527. [Google Scholar] [CrossRef]
- Lin, Y.C.; Guo, Y.R.; Miyagi, A.; Levring, J.; MacKinnon, R.; Scheuring, S. Force-induced conformational changes in PIEZO1. Nature 2019, 573, 230–234. [Google Scholar] [CrossRef]
- Zhao, Q.; Zhou, H.; Chi, S.; Wang, Y.; Wang, J.; Geng, J.; Wu, K.; Liu, W.; Zhang, T.; Dong, M.Q.; et al. Structure and mechanogating mechanism of the Piezo1 channel. Nature 2018, 554, 487–492. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Saotome, K.; Murthy, S.E.; Kefauver, J.M.; Whitwam, T.; Patapoutian, A.; Ward, A.B. Structure of the mechanically activated ion channel Piezo1. Nature 2018, 554, 481–486. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Zhou, H.; Zhang, M.; Liu, W.; Deng, T.; Zhao, Q.; Li, Y.; Lei, J.; Li, X.; Xiao, B. Structure and mechanogating of the mammalian tactile channel PIEZO2. Nature 2019, 573, 225–229. [Google Scholar] [CrossRef] [PubMed]
- Cahalan, S.M.; Lukacs, V.; Ranade, S.S.; Chien, S.; Bandell, M.; Patapoutian, A. Piezo1 links mechanical forces to red blood cell volume. Elife 2015, 4, e07370. [Google Scholar] [CrossRef] [PubMed]
- Dalghi, M.G.; Clayton, D.R.; Ruiz, W.G.; Al-Bataineh, M.M.; Satlin, L.M.; Kleyman, T.R.; Ricke, W.A.; Carattino, M.D.; Apodaca, G. Expression and distribution of PIEZO1 in the mouse urinary tract. Am. J. Physiol. Ren. Physiol. 2019, 317, F303–F321. [Google Scholar] [CrossRef]
- Gudipaty, S.A.; Lindblom, J.; Loftus, P.D.; Redd, M.J.; Edes, K.; Davey, C.F.; Krishnegowda, V.; Rosenblatt, J. Mechanical stretch triggers rapid epithelial cell division through Piezo1. Nature 2017, 543, 118–121. [Google Scholar] [CrossRef]
- Nonomura, K.; Woo, S.H.; Chang, R.B.; Gillich, A.; Qiu, Z.; Francisco, A.G.; Ranade, S.S.; Liberles, S.D.; Patapoutian, A. Piezo2 senses airway stretch and mediates lung inflation-induced apnoea. Nature 2017, 541, 176–181. [Google Scholar] [CrossRef]
- Wu, Z.; Grillet, N.; Zhao, B.; Cunningham, C.; Harkins-Perry, S.; Coste, B.; Ranade, S.; Zebarjadi, N.; Beurg, M.; Fettiplace, R.; et al. Mechanosensory hair cells express two molecularly distinct mechanotransduction channels. Nat. Neurosci. 2017, 20, 24–33. [Google Scholar] [CrossRef]
- Miyamoto, T.; Mochizuki, T.; Nakagomi, H.; Kira, S.; Watanabe, M.; Takayama, Y.; Suzuki, Y.; Koizumi, S.; Takeda, M.; Tominaga, M. Functional role for Piezo1 in stretch-evoked Ca2+ influx and ATP release in Urothelial cell cultures. J. Biol. Chem. 2014, 289, 16565–16575. [Google Scholar] [CrossRef]
- Martins, J.R.; Penton, D.; Peyronnet, R.; Arhatte, M.; Moro, C.; Picard, N.; Kurt, B.; Patel, A.; Honoré, E.; Demolombe, S. Piezo1-dependent regulation of urinary osmolarity. Pflugers Arch. Eur. J. Physiol. 2016, 468, 1197–1206. [Google Scholar] [CrossRef] [PubMed]
- Ihara, T.; Mitsui, T.; Nakamura, Y.; Kanda, M.; Tsuchiya, S.; Kira, S.; Nakagomi, H.; Sawada, N.; Kamiyama, M.; Hirayama, Y.; et al. The oscillation of intracellular Ca2+ influx associated with the circadian expression of Piezo1 and TRPV4 in the bladder urothelium. Sci. Rep. 2018, 8, 5699. [Google Scholar] [CrossRef]
- Faucherre, A.; Nargeot, J.; Mangoni, M.E.; Jopling, C. piezo2b regulates vertebrate light touch response. J. Neurosci. 2013, 33, 17089–17094. [Google Scholar] [CrossRef]
- McHugh, B.J.; Murdoch, A.; Haslett, C.; Sethi, T. Loss of the integrin-activating transmembrane protein Fam38A (Piezo1) promotes a switch to a reduced integrin-dependent mode of cell migration. PLoS ONE 2012, 7, e40346. [Google Scholar] [CrossRef] [PubMed]
- Schrenk-Siemens, K.; Wende, H.; Prato, V.; Song, K.; Rostock, C.; Loewer, A.; Utikal, J.; Lewin, G.R.; Lechner, S.G.; Siemens, J. PIEZO2 is required for mechanotransduction in human stem cell-derived touch receptors. Nat. Neurosci. 2015, 18, 10–16. [Google Scholar] [CrossRef] [PubMed]
- Woo, S.H.; Lukacs, V.; De Nooij, J.C.; Zaytseva, D.; Criddle, C.R.; Francisco, A.; Jessell, T.M.; Wilkinson, K.A.; Patapoutian, A. Piezo2 is the principal mechanotransduction channel for proprioception. Nat. Neurosci. 2015, 18, 1756–1762. [Google Scholar] [CrossRef]
- Chubinskiy-Nadezhdin, V.I.; Vasileva, V.Y.; Vassilieva, I.O.; Sudarikova, A.V.; Morachevskaya, E.A.; Negulyaev, Y.A. Agonist-induced Piezo1 activation suppresses migration of transformed fibroblasts. Biochem. Biophys. Res. Commun. 2019, 514, 173–179. [Google Scholar] [CrossRef]
- Li, J.; Hou, B.; Tumova, S.; Muraki, K.; Bruns, A.; Ludlow, M.J.; Sedo, A.; Hyman, A.J.; McKeown, L.; Young, R.S.; et al. Piezo1 integration of vascular architecture with physiological force. Nature 2014, 515, 279–282. [Google Scholar] [CrossRef]
- Albuisson, J.; Murthy, S.E.; Bandell, M.; Coste, B.; Louis-Dit-Picard, H.; Mathur, J.; Fénéant-Thibault, M.; Tertian, G.; De Jaureguiberry, J.P.; Syfuss, P.Y.; et al. Dehydrated hereditary stomatocytosis linked to gain-of-function mutations in mechanically activated PIEZO1 ion channels. Nat. Commun. 2013, 4, 1884. [Google Scholar] [CrossRef]
- Beneteau, C.; Thierry, G.; Blesson, S.; Le Vaillant, C.; Picard, V.; Béné, M.C.; Eveillard, M.; Le Caignec, C. Recurrent mutation in the PIEZO1 gene in two families of hereditary xerocytosis with fetal hydrops. Clin. Genet. 2014, 85, 293–295. [Google Scholar] [CrossRef]
- Fotiou, E.; Martin-Almedina, S.; Simpson, M.A.; Lin, S.; Gordon, K.; Brice, G.; Atton, G.; Jeffery, I.; Rees, D.C.; Mignot, C.; et al. Novel mutations in PIEZO1 cause an autosomal recessive generalized lymphatic dysplasia with non-immune hydrops fetalis. Nat. Commun. 2015, 6, 8085. [Google Scholar] [CrossRef] [PubMed]
- Imashuku, S.; Muramatsu, H.; Sugihara, T.; Okuno, Y.; Wang, X.; Yoshida, K.; Kato, A.; Kato, K.; Tatsumi, Y.; Hattori, A.; et al. PIEZO1 gene mutation in a Japanese family with hereditary high phosphatidylcholine hemolytic anemia and hemochromatosis-induced diabetes mellitus. Int. J. Hematol. 2016, 104, 125–129. [Google Scholar] [CrossRef] [PubMed]
- Zarychanski, R.; Schulz, V.P.; Houston, B.L.; Maksimova, Y.; Houston, D.S.; Smith, B.; Rinehart, J.; Gallagher, P.G. Mutations in the mechanotransduction protein PIEZO1 are associated with hereditary xerocytosis. Blood 2012, 120, 1908–1915. [Google Scholar] [CrossRef] [PubMed]
- Glogowska, E.; Schneider, E.R.; Maksimova, Y.; Schulz, V.P.; Lezon-Geyda, K.; Wu, J.; Radhakrishnan, K.; Keel, S.B.; Mahoney, D.; Freidmann, A.M.; et al. Novel mechanisms of PIEZO1 dysfunction in hereditary xerocytosis. Blood 2017, 130, 1845–1856. [Google Scholar] [CrossRef]
- Chesler, A.T.; Szczot, M.; Bharucha-Goebel, D.; Čeko, M.; Donkervoort, S.; Laubacher, C.; Hayes, L.H.; Alter, K.; Zampieri, C.; Stanley, C.; et al. The role of PIEZO2 in human mechanosensation. N. Engl. J. Med. 2016, 375, 1355–1364. [Google Scholar] [CrossRef]
- McMillin, M.J.; Beck, A.E.; Chong, J.X.; Shively, K.M.; Buckingham, K.J.; Gildersleeve, H.I.S.; Aracena, M.I.; Aylsworth, A.S.; Bitoun, P.; Carey, J.C.; et al. Mutations in PIEZO2 cause Gordon syndrome, Marden-Walker Syndrome, and distal arthrogryposis type 5. Am. J. Hum. Genet. 2014, 94, 734–744. [Google Scholar] [CrossRef]
- Gargalionis, A.N.; Basdra, E.K.; Papavassiliou, A.G. Tumor mechanosensing and its therapeutic potential. J. Cell. Biochem. 2018, 119, 4304–4308. [Google Scholar] [CrossRef]
- Monteith, G.R.; Prevarskaya, N.; Roberts-Thomson, S.J. The calcium-cancer signalling nexus. Nat. Rev. Cancer 2017, 17, 367–380. [Google Scholar] [CrossRef]
- Marchi, S.; Pinton, P. Alterations of calcium homeostasis in cancer cells. Curr. Opin. Pharmacol. 2016, 29, 1–6. [Google Scholar] [CrossRef]
- Prevarskaya, N.; Ouadid-Ahidouch, H.; Skryma, R.; Shuba, Y. Remodelling of Ca2+ transport in cancer: How it contributes to cancer hallmarks? Philos. Trans. R. Soc. B Biol. Sci. 2014, 369, 20130097. [Google Scholar] [CrossRef]
- Yang, X.N.; Lu, Y.P.; Liu, J.J.; Huang, J.K.; Liu, Y.P.; Xiao, C.X.; Jazag, A.; Ren, J.L.; Guleng, B. Piezo1 is as a novel trefoil factor family 1 binding protein that promotes gastric cancer cell mobility in vitro. Dig. Dis. Sci. 2014, 59, 1428–1435. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.; Zhou, Y.; Huang, T.; Wu, F.; Liu, L.; Kwan, J.S.H.; Cheng, A.S.L.; Yu, J.; To, K.F.; Kang, W. PIEZO1 functions as a potential oncogene by promoting cell proliferation and migration in gastric carcinogenesis. Mol. Carcinog. 2018, 57, 1144–1155. [Google Scholar] [CrossRef]
- Li, C.; Rezania, S.; Kammerer, S.; Sokolowski, A.; Devaney, T.; Gorischek, A.; Jahn, S.; Hackl, H.; Groschner, K.; Windpassinger, C.; et al. Piezo1 forms mechanosensitive ion channels in the human MCF-7 breast cancer cell line. Sci. Rep. 2015, 5, 8364. [Google Scholar] [CrossRef] [PubMed]
- Pardo-Pastor, C.; Rubio-Moscardo, F.; Vogel-González, M.; Serra, S.A.; Afthinos, A.; Mrkonjic, S.; Destaing, O.; Abenza, J.F.; Fernández-Fernández, J.M.; Trepat, X.; et al. Piezo2 channel regulates RhoA and actin cytoskeleton to promote cell mechanobiological responses. Proc. Natl. Acad. Sci. USA 2018, 115, 1925–1930. [Google Scholar] [CrossRef] [PubMed]
- Valiente, M.; Obenauf, A.C.; Jin, X.; Chen, Q.; Zhang, X.H.F.; Lee, D.J.; Chaft, J.E.; Kris, M.G.; Huse, J.T.; Brogi, E.; et al. Serpins promote cancer cell survival and vascular Co-option in brain metastasis. Cell 2014, 156, 1002–1016. [Google Scholar] [CrossRef] [PubMed]
- Lou, W.; Liu, J.; Ding, B.; Jin, L.; Xu, L.; Li, X.; Chen, J.; Fan, W. Five miRNAs-mediated PIEZO2 downregulation, accompanied with activation of Hedgehog signaling pathway, predicts poor prognosis of breast cancer. Aging 2019, 11, 2628–2652. [Google Scholar] [CrossRef]
- Hoyt, K.; Castaneda, B.; Zhang, M.; Nigwekar, P.; di Sant’Agnese, P.A.; Joseph, J.V.; Strang, J.; Rubensd, D.J.; Parkera, K.J. Tissue elasticity properties as biomarkers for prostate cancer. Cancer Biomarkers 2008, 4, 213–225. [Google Scholar] [CrossRef]
- Hegarty, P.K.; Watson, R.W.G.; Coffey, R.N.T.; Webber, M.M.; Fitzpatrick, J.M. Effects of cyclic stretch on prostatic cells in culture. J. Urol. 2002, 168, 2291–2295. [Google Scholar] [CrossRef]
- Wadhera, P. An introduction to acinar pressures in BPH and prostate cancer. Nat. Rev. Urol. 2013, 10, 358–366. [Google Scholar] [CrossRef]
- Han, Y.; Liu, C.; Zhang, D.; Men, H.; Huo, L.; Geng, Q.; Wang, S.; Gao, Y.; Zhang, W.; Zhang, Y.; et al. Mechanosensitive ion channel piezo1 promotes prostate cancer development through the activation of the akt/mtorpathway and acceleration of cell cycle. Int. J. Oncol. 2019, 55, 629–644. [Google Scholar]
- Weller, M.; Wick, W.; Aldape, K.; Brada, M.; Berger, M.; Pfister, S.M.; Nishikawa, R.; Rosenthal, M.; Wen, P.Y.; Stupp, R.; et al. Glioma. Nat. Rev. Dis. Prim. 2015, 1, 15017. [Google Scholar] [CrossRef] [PubMed]
- Yang, H.; Liu, C.; Zhou, R.M.; Yao, J.; Li, X.M.; Shen, Y.; Cheng, H.; Yuan, J.; Yan, B.; Jiang, Q. Piezo2 protein: A novel regulator of tumor angiogenesis and hyperpermeability. Oncotarget 2016, 7, 44630–44643. [Google Scholar] [CrossRef]
- Chen, X.; Wanggou, S.; Bodalia, A.; Zhu, M.; Dong, W.; Fan, J.J.; Yin, W.C.; Min, H.K.; Hu, M.; Draghici, D.; et al. A Feedforward Mechanism Mediated by Mechanosensitive Ion Channel PIEZO1 and Tissue Mechanics Promotes Glioma Aggression. Neuron 2018, 100, 799–815. [Google Scholar] [CrossRef] [PubMed]
- Holenstein, C.N.; Horvath, A.; Schär, B.; Schoenenberger, A.D.; Bollhalder, M.; Goedecke, N.; Bartalena, G.; Otto, O.; Herbig, M.; Guck, J.; et al. The relationship between metastatic potential and in vitro mechanical properties of osteosarcoma cells. Mol. Biol. Cell 2019, 30, 887–898. [Google Scholar] [CrossRef] [PubMed]
- Jiang, L.; Zhao, Y.D.; Chen, W.X. The function of the novel mechanical activated ion channel piezo1 in the human osteosarcoma cells. Med. Sci. Monit. 2017, 23, 5070–5082. [Google Scholar] [CrossRef] [PubMed]
- Suzuki, T.; Muraki, Y.; Hatano, N.; Suzuki, H.; Muraki, K. PIEZO1 channel is a potential regulator of synovial sarcoma cell-viability. Int. J. Mol. Sci. 2018, 19, 1452. [Google Scholar] [CrossRef]
- Huang, Z.; Sun, Z.; Zhang, X.; Niu, K.; Wang, Y.; Zheng, J.; Li, H.; Liu, Y. Loss of stretch-activated channels, PIEZOs, accelerates non-small cell lung cancer progression and cell migration. Biosci. Rep. 2019, 39, BSR20181679. [Google Scholar] [CrossRef]
- Gyorffy, B.; Surowiak, P.; Budczies, J.; Lánczky, A. Online survival analysis software to assess the prognostic value of biomarkers using transcriptomic data in non-small-cell lung cancer. PLoS ONE 2013, 8, e82241. [Google Scholar] [CrossRef]
- Etem, E.Ö.; Ceylan, G.G.; Özaydın, S.; Ceylan, C.; Özercan, I.; Kuloğlu, T. The increased expression of Piezo1 and Piezo2 ion channels in human and mouse bladder carcinoma. Adv. Clin. Exp. Med. 2018, 27, 1025–1031. [Google Scholar] [CrossRef]
- Coste, B.; Xiao, B.; Santos, J.S.; Syeda, R.; Grandl, J.; Spencer, K.S.; Kim, S.E.; Schmidt, M.; Mathur, J.; Dubin, A.E.; et al. Piezo proteins are pore-forming subunits of mechanically activated channels. Nature 2012, 483, 176–181. [Google Scholar] [CrossRef]
- Bae, C.; Sachs, F.; Gottlieb, P.A. The mechanosensitive ion channel Piezo1 is inhibited by the peptide GsMTx4. Biochemistry 2011, 50, 6295–6300. [Google Scholar] [CrossRef]
- Gnanasambandam, R.; Ghatak, C.; Yasmann, A.; Nishizawa, K.; Sachs, F.; Ladokhin, A.S.; Sukharev, S.I.; Suchyna, T.M. GsMTx4: Mechanism of Inhibiting Mechanosensitive Ion Channels. Biophys. J. 2017, 112, 31–45. [Google Scholar] [CrossRef] [PubMed]
- Suchyna, T.M.; Johnson, J.H.; Hamer, K.; Leykam, J.F.; Gage, D.A.; Clemo, H.F.; Baumgarten, C.M.; Sachs, F. Identification of a peptide toxin from Grammostola spatulata spider venom that blocks cation-selective stretch-activated channels. J. Gen. Physiol. 2000, 115, 583–598. [Google Scholar] [CrossRef] [PubMed]
- Syeda, R.; Xu, J.; Dubin, A.E.; Coste, B.; Mathur, J.; Huynh, T.; Matzen, J.; Lao, J.; Tully, D.C.; Engels, I.H.; et al. Chemical activation of the mechanotransduction channel Piezo1. Elife 2015, 4, e07369. [Google Scholar] [CrossRef]
- 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, 9, 1300. [Google Scholar] [CrossRef] [PubMed]
- 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.; et al. Yoda1 analogue (Dooku1) which antagonizes Yoda1-evoked activation of Piezo1 and aortic relaxation. Br. J. Pharmacol. 2018, 175, 1744–1759. [Google Scholar] [CrossRef]
- Guo, Y.R.; MacKinnon, R. Structure-based membrane dome mechanism for piezo mechanosensitivity. Elife 2017, 6, e33660. [Google Scholar] [CrossRef]
- Szczot, M.; Pogorzala, L.A.; Solinski, H.J.; Young, L.; Yee, P.; Le Pichon, C.E.; Chesler, A.T.; Hoon, M.A. Cell-Type-Specific Splicing of Piezo2 Regulates Mechanotransduction. Cell Rep. 2017, 21, 2760–2771. [Google Scholar] [CrossRef]
Cancer Type | Piezo Channel | Expression | Described Roles in Cancer | References |
---|---|---|---|---|
Gastric | Piezo1 | Upregulation | Migration, Invasion, Proliferation | [74,75] |
Breast | Piezo1 Piezo2 | Upregulation Upregulation | Migration Migration, Invasion, Proliferation | [76] [77] |
Prostate | Piezo1 | Upregulation | Migration, Proliferation | [83] |
Glioma | Piezo2 Piezo1 | Upregulation Upregulation | Migration, Angiogenesis, Apoptosis resistance Proliferation | [85] [86] |
Osteosarcoma | Piezo1 | Upregulation | Oncosuppressor | [88] |
Synovial Sarcoma | Piezo1 | Upregulation | Migration | [89] |
Lung | Piezo1, Piezo2 | Downregulation | Oncosuppressor | [57,90,91] |
Bladder | Piezo1, Piezo2 | Upregulation | Unknown | [92] |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
De Felice, D.; Alaimo, A. Mechanosensitive Piezo Channels in Cancer: Focus on altered Calcium Signaling in Cancer Cells and in Tumor Progression. Cancers 2020, 12, 1780. https://doi.org/10.3390/cancers12071780
De Felice D, Alaimo A. Mechanosensitive Piezo Channels in Cancer: Focus on altered Calcium Signaling in Cancer Cells and in Tumor Progression. Cancers. 2020; 12(7):1780. https://doi.org/10.3390/cancers12071780
Chicago/Turabian StyleDe Felice, Dario, and Alessandro Alaimo. 2020. "Mechanosensitive Piezo Channels in Cancer: Focus on altered Calcium Signaling in Cancer Cells and in Tumor Progression" Cancers 12, no. 7: 1780. https://doi.org/10.3390/cancers12071780
APA StyleDe Felice, D., & Alaimo, A. (2020). Mechanosensitive Piezo Channels in Cancer: Focus on altered Calcium Signaling in Cancer Cells and in Tumor Progression. Cancers, 12(7), 1780. https://doi.org/10.3390/cancers12071780