Mechanosensitive Ion Channels: Their Physiological Importance and Potential Key Role in Cancer
Abstract
:1. Introduction
2. Classification of Mechanoreceptors and Their Physiological Importance
2.1. The Epithelial Sodium Channel/Degenerin Superfamily
2.2. Transient Receptor Potential Channel Family
2.3. Two-Pore-Domain Potassium Channel Family
2.4. PIEZO Channel Family
3. Mechanoreceptors in Cancer
3.1. TRPM7
Cancer Type | Expression | Function | Clinical Features | Molecular Mechanism | References |
---|---|---|---|---|---|
Ovarian | Upregulated | Proliferation, migration, invasion. | Poor disease-free survival and poor overall survival. | EMT factors upregulation. PI3K/Akt signaling activation. Indirect HIF-1α regulation. | [63,64,65,66] |
Breast | Upregulated | Proliferation, migration, invasion. | Poor prognosis. | Proliferation mechanisms are unclear. High TRPM7 promoter methylation is a good prognostic marker in the luminal A subtype. | [67,68,69,70,71] |
Bladder | Upregulated | Proliferation, migration, invasion. | Poor clinical outcomes. | Proliferation mechanisms are unclear. Pro-apoptotic ERK1/2 pathway activation and metastasis markers are downregulated in TRPM7 KD. Src, Akt and JNK upregulation. | [69,70,71] |
Cervical | Undetermined | Proliferation, migration, invasion. | Undetermined. | Necrotic cell death regulation miR-543 and miR-192-5p target TRPM7 directly. | [76,77,78] |
Glioblastoma | Upregulated | Proliferation, migration, invasion. | Tumor aggravation. | JAK2/STAT3 and Notch1 signaling activation. Glioma stem marker expression. | [79,80,81] |
Prostate | Upregulated | Tumorigeneses, migration, invasion. | Undetermined. | Activation of the Akt and ERK signaling pathways. TRPM7-HIF1α-Annexin A1 axis activation. | [84,85,86,94,95] |
3.2. TRPV4
3.3. Piezo1
3.4. Piezo2
4. Mechanosensation of the Immune System and Immune Response to Cancer
4.1. TRPA1
4.2. TRPV4
4.3. Piezo1
5. Discussion
6. Challenges and Future Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Rømer, A.M.A.; Thorseth, M.-L.; Madsen, D.H. Immune Modulatory Properties of Collagen in Cancer. Front. Immunol. 2021, 12, 791453. [Google Scholar] [CrossRef] [PubMed]
- 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. 2014, 9, 513–526. [Google Scholar] [CrossRef] [PubMed]
- Kudou, M.; Shiozaki, A.; Yamazato, Y.; Katsurahara, K.; Kosuga, T.; Shoda, K.; Arita, T.; Konishi, H.; Komatsu, S.; Kubota, T.; et al. The expression and role of TRPV2 in esophageal squamous cell carcinoma. Sci. Rep. 2019, 9, 16055. [Google Scholar] [CrossRef]
- Canales Coutiño, B.; Mayor, R. Mechanosensitive ion channels in cell migration. Cells Dev. 2021, 166, 203683. [Google Scholar] [CrossRef]
- Martino, F.; Perestrelo, A.R.; Vinarsky, V.; Pagliari, S.; Forte, G. Cellular Mechanotransduction: From Tension to Function. Front. Physiol. 2018, 9, 824. [Google Scholar] [CrossRef]
- Gu, Y.; Gu, C. Physiological and Pathological Functions of Mechanosensitive Ion Channels. Mol. Neurobiol. 2014, 50, 339–347. [Google Scholar] [CrossRef]
- Árnadóttir, J.; Chalfie, M. Eukaryotic Mechanosensitive Channels. Annu. Rev. Biophys. 2010, 39, 111–137. [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]
- Kellenberger, S.; Schild, L. Epithelial Sodium Channel/Degenerin Family of Ion Channels: A Variety of Functions for a Shared Structure. Physiol. Rev. 2002, 82, 735–767. [Google Scholar] [CrossRef]
- Hanukoglu, I.; Hanukoglu, A. Epithelial sodium channel (ENaC) family: Phylogeny, structure–function, tissue distribution, and associated inherited diseases. Gene 2016, 579, 95–132. [Google Scholar] [CrossRef]
- Cheng, Y.-R.; Jiang, B.-Y.; Chen, C.-C. Acid-sensing ion channels: Dual function proteins for chemo-sensing and mechano-sensing. J. Biomed. Sci. 2018, 25, 46. [Google Scholar] [CrossRef] [PubMed]
- Hanukoglu, I. ASIC and ENaC type sodium channels: Conformational states and the structures of the ion selectivity filters. FEBS J. 2017, 284, 525–545. [Google Scholar] [CrossRef] [PubMed]
- Christensen, B.M.; Perrier, R.; Wang, Q.; Zuber, A.M.; Maillard, M.; Mordasini, D.; Malsure, S.; Ronzaud, C.; Stehle, J.-C.; Rossier, B.C.; et al. Sodium and Potassium Balance Depends on αENaC Expression in Connecting Tubule. J. Am. Soc. Nephrol. 2010, 21, 1942–1951. [Google Scholar] [CrossRef] [PubMed]
- Bhalla, V.; Hallows, K.R. Mechanisms of ENaC Regulation and Clinical Implications. J. Am. Soc. Nephrol. 2008, 19, 1845–1854. [Google Scholar] [CrossRef]
- Matalon, S.; Bartoszewski, R.; Collawn, J.F.; Hakansson, A.P.; Orihuela, C.J.; Bogaert, D.; Terryah, S.T.; Fellner, R.C.; Ahmad, S.; Moore, P.J.; et al. Role of epithelial sodium channels in the regulation of lung fluid homeostasis. Am. J. Physiol.-Lung Cell. Mol. Physiol. 2015, 309, L1229–L1238. [Google Scholar] [CrossRef]
- Barth, D.; Fronius, M. Shear force modulates the activity of acid-sensing ion channels at low pH or in the presence of non-proton ligands. Sci. Rep. 2019, 9, 6781. [Google Scholar] [CrossRef]
- Wemmie, J.A.; Chen, J.; Askwith, C.C.; Hruska-Hageman, A.M.; Price, M.P.; Nolan, B.C.; Yoder, P.G.; Lamani, E.; Hoshi, T.; Freeman, J.H.; et al. The Acid-Activated Ion Channel ASIC Contributes to Synaptic Plasticity, Learning, and Memory. Neuron 2002, 34, 463–477. [Google Scholar] [CrossRef]
- Eijkelkamp, N.; Quick, K.; Wood, J.N. Transient Receptor Potential Channels and Mechanosensation. Annu. Rev. Neurosci. 2013, 36, 519–546. [Google Scholar] [CrossRef]
- Venkatachalam, K.; Montell, C. TRP channels. Annu. Rev. Biochem. 2007, 76, 387–417. [Google Scholar] [CrossRef]
- Samanta, A.; Hughes, T.E.T.; Moiseenkova-Bell, V.Y. Transient Receptor Potential (TRP) Channels. Subcell. Biochem. 2018, 87, 141–165. [Google Scholar]
- Tang, Y.Q.; Lee, S.A.; Rahman, M.; Vanapalli, S.A.; Lu, H.; Schafer, W.R. Ankyrin Is an Intracellular Tether for TMC Mechanotransduction Channels. Neuron 2020, 107, 112–125.e10. [Google Scholar] [CrossRef] [PubMed]
- Dong, X.-P.; Wang, X.; Xu, H. TRP channels of intracellular membranes. J. Neurochem. 2010, 113, 313–328. [Google Scholar] [CrossRef] [PubMed]
- Chen, C.C.; Krogsaeter, E.; Grimm, C. Two-pore and TRP cation channels in endolysosomal osmo-/mechanosensation and volume regulation. Biochim. Biophys. Acta Mol. Cell Res. 2021, 1868, 118921. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.; Cheng, X.; Tian, J.; Xiao, Y.; Tian, T.; Xu, F.; Hong, X.; Zhu, M.X. TRPC channels: Structure, function, regulation and recent advances in small molecular probes. Pharmacol. Ther. 2020, 209, 107497. [Google Scholar] [CrossRef] [PubMed]
- Chen, X.; Sooch, G.; Demaree, I.S.; White, F.A.; Obukhov, A.G. Transient Receptor Potential Canonical (TRPC) Channels: Then and Now. Cells 2020, 9, 1983. [Google Scholar] [CrossRef]
- Naert, R.; López-Requena, A.; Talavera, K. TRPA1 Expression and Pathophysiology in Immune Cells. Int. J. Mol. Sci. 2021, 22, 11460. [Google Scholar] [CrossRef]
- Wu, L.-J.; Sweet, T.-B.; Clapham, D.E. International Union of Basic and Clinical Pharmacology. LXXVI. Current Progress in the Mammalian TRP Ion Channel Family. Pharmacol. Rev. 2010, 62, 381–404. [Google Scholar] [CrossRef]
- Feliciangeli, S.; Chatelain, F.C.; Bichet, D.; Lesage, F. The family of K2P channels: Salient structural and functional properties. J. Physiol. 2015, 593, 2587–2603. [Google Scholar] [CrossRef]
- Patel, A.J.; Honore, E. 2P domain K+ channels: Novel pharmacological targets for volatile general anesthetics. Adv. Exp. Med. Biol. 2003, 536, 9–23. [Google Scholar] [CrossRef]
- Kennard, L.E.; Chumbley, J.R.; Ranatunga, K.M.; Armstrong, S.J.; Veale, E.L.; Mathie, A. Inhibition of the human two-pore domain potassium channel, TREK-1, by fluoxetine and its metabolite norfluoxetine. Br. J. Pharmacol. 2005, 144, 821–829. [Google Scholar] [CrossRef]
- Schneider, E.R.; Anderson, E.O.; Gracheva, E.O.; Bagriantsev, S.N. Temperature Sensitivity of Two-Pore (K2P) Potassium Channels. Curr. Top Membr. 2014, 74, 113–133. [Google Scholar] [CrossRef] [PubMed]
- Enyedi, P.; Czirják, G. Molecular Background of Leak K+ Currents: Two-Pore Domain Potassium Channels. Physiol. Rev. 2010, 90, 559–605. [Google Scholar] [CrossRef] [PubMed]
- Lengyel, M.; Enyedi, P.; Czirják, G. Negative Influence by the Force: Mechanically Induced Hyperpolarization via K2P Background Potassium Channels. Int. J. Mol. Sci. 2021, 22, 9062. [Google Scholar] [CrossRef] [PubMed]
- Zúñiga, L.; Zúñiga, R. Understanding the Cap Structure in K2P Channels. Front. Physiol. 2016, 7, 228. [Google Scholar] [CrossRef] [PubMed]
- Lotshaw, D.P. Biophysical, pharmacological, and functional characteristics of cloned and native mammalian two-pore domain K+ channels. Cell Biochem. Biophys. 2007, 47, 209–256. [Google Scholar] [CrossRef] [PubMed]
- Mathie, A.; Veale, E.L. Therapeutic potential of neuronal two-pore domain potassium-channel modulators. Curr. Opin. Investig. Drugs 2007, 8, 555–562. [Google Scholar] [PubMed]
- Dadi, P.K.; Luo, B.; Vierra, N.C.; Jacobson, D.A. TASK-1 Potassium Channels Limit Pancreatic α-Cell Calcium Influx and Glucagon Secretion. Mol. Endocrinol. 2015, 29, 777–787. [Google Scholar] [CrossRef]
- Schwingshackl, A.; Lopez, B.; Teng, B.; Luellen, C.; Lesage, F.; Belperio, J.; Olcese, R.; Waters, C.M. Hyperoxia treatment of TREK-1/TREK-2/TRAAK-deficient mice is associated with a reduction in surfactant proteins. Am. J. Physiol. Lung Cell. Mol. Physiol. 2017, 313, L1030–L1046. [Google Scholar] [CrossRef]
- Schulte-Mecklenbeck, A.; Bittner, S.; Ehling, P.; Döring, F.; Wischmeyer, E.; Breuer, J.; Herrmann, A.M.; Wiendl, H.; Meuth, S.G.; Gross, C.C. The two-pore domain K2P channel TASK2 drives human NK-cell proliferation and cytolytic function. Eur. J. Immunol. 2015, 45, 2602–2614. [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]
- 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] [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]
- Zhao, Q.; Wu, K.; Geng, J.; Chi, S.; Wang, Y.; Zhi, P.; Zhang, M.; Xiao, B. Ion Permeation and Mechanotransduction Mechanisms of Mechanosensitive Piezo Channels. Neuron 2016, 89, 1248–1263. [Google Scholar] [CrossRef] [PubMed]
- Syeda, R.; Florendo, M.N.; Cox, C.D.; Kefauver, J.M.; Santos, J.S.; Martinac, B.; Patapoutian, A. Piezo1 Channels Are Inherently Mechanosensitive. Cell Rep. 2016, 17, 1739–1746. [Google Scholar] [CrossRef]
- 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]
- Sun, D.; Liu, S.; Li, S.; Zhang, M.; Yang, F.; Wen, M.; Shi, P.; Wang, T.; Pan, M.; Chang, S.; et al. Structural insights into human acid-sensing ion channel 1a inhibition by snake toxin mambalgin1. eLife 2020, 9, e57096. [Google Scholar] [CrossRef] [PubMed]
- Nadezhdin, K.D.; Talyzina, I.A.; Parthasarathy, A.; Neuberger, A.; Zhang, D.X.; Sobolevsky, A.I. Structure of human TRPV4 in complex with GTPase RhoA. Nat. Commun. 2023, 14, 3733. [Google Scholar] [CrossRef]
- Brohawn, S.G.; del Mármol, J.; MacKinnon, R. Crystal structure of the human K2P TRAAK, a lipid- and mechano-sensitive K+ ion channel. Science 2012, 335, 436–441. [Google Scholar] [CrossRef]
- Levental, K.R.; Yu, H.; Kass, L.; Lakins, J.N.; Egeblad, M.; Erler, J.T.; Fong, S.F.T.; Csiszar, K.; Giaccia, A.; Weninger, W.; et al. Matrix Crosslinking Forces Tumor Progression by Enhancing Integrin Signaling. Cell 2009, 139, 891–906. [Google Scholar] [CrossRef]
- Pickup, M.W.; Mouw, J.K.; Weaver, V.M. The extracellular matrix modulates the hallmarks of cancer. EMBO Rep. 2014, 15, 1243–1253. [Google Scholar] [CrossRef]
- Jain, R.K.; Martin, J.D.; Stylianopoulos, T. The Role of Mechanical Forces in Tumor Growth and Therapy. Annu. Rev. Biomed. Eng. 2014, 16, 321–346. [Google Scholar] [CrossRef] [PubMed]
- Reid, S.E.; Kay, E.J.; Neilson, L.J.; Henze, A.T.; Serneels, J.; McGhee, E.J.; Dhayade, S.; Nixon, C.; Mackey, J.B.; Santi, A.; et al. Tumor matrix stiffness promotes metastatic cancer cell interaction with the endothelium. EMBO J. 2017, 36, 2373–2389. [Google Scholar] [CrossRef] [PubMed]
- Kuchuk, I.; Hutton, B.; Moretto, P.; Ng, T.; Addison, C.; Clemons, M. Incidence, consequences and treatment of bone metastases in breast cancer patients—Experience from a single cancer centre. J. Bone Oncol. 2013, 2, 137–144. [Google Scholar] [CrossRef]
- Weil, R.J.; Palmieri, D.C.; Bronder, J.L.; Stark, A.M.; Steeg, P.S. Breast Cancer Metastasis to the Central Nervous System. Am. J. Pathol. 2005, 167, 913–920. [Google Scholar] [CrossRef] [PubMed]
- Akoury, E.; Luna, A.S.R.G.; Ahangar, P.; Gao, X.; Zolotarov, P.; Weber, M.H.; Rosenzweig, D.H. Anti-Tumor Effects of Low Dose Zoledronate on Lung Cancer-Induced Spine Metastasis. J. Clin. Med. 2019, 8, 1212. [Google Scholar] [CrossRef]
- Barnholtz-Sloan, J.S.; Sloan, A.E.; Davis, F.G.; Vigneau, F.D.; Lai, P.; Sawaya, R.E. Incidence Proportions of Brain Metastases in Patients Diagnosed (1973 to 2001) in the Metropolitan Detroit Cancer Surveillance System. J. Clin. Oncol. 2004, 22, 2865–2872. [Google Scholar] [CrossRef]
- Roudier, M.P.; Corey, E.; True, L.D.; Hiagno, C.S.; Ott, S.M.; Vessella, R.L. Histological, Immunophenotypic and Histomorphometric Characterization of Prostate Cancer Bone Metastases. Cancer Treat. Res. 2004, 118, 311–339. [Google Scholar] [CrossRef]
- Boxley, P.J.; Smith, D.E.; Gao, D.; Kessler, E.R.; Echalier, B.; Bernard, B.; Ormond, D.R.; Lam, E.T.; Kavanagh, B.D.; Flaig, T.W. Prostate Cancer Central Nervous System Metastasis in a Contemporary Cohort. Clin. Genitourin. Cancer 2021, 19, 217–222.e1. [Google Scholar] [CrossRef]
- Tang, K.; Xin, Y.; Li, K.; Chen, X.; Tan, Y. Cell Cytoskeleton and Stiffness Are Mechanical Indicators of Organotropism in Breast Cancer. Biology 2021, 10, 259. [Google Scholar] [CrossRef]
- Li, X.; Wang, J. Mechanical tumor microenvironment and transduction: Cytoskeleton mediates cancer cell invasion and metastasis. Int. J. Biol. Sci. 2020, 16, 2014–2028. [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] [PubMed]
- Yee, N.S.; Kazi, A.A.; Yee, R.K. Cellular and Developmental Biology of TRPM7 Channel-Kinase: Implicated Roles in Cancer. Cells 2014, 3, 751–777. [Google Scholar] [CrossRef] [PubMed]
- Liu, L.; Wu, N.; Wang, Y.; Zhang, X.; Xia, B.; Tang, J.; Cai, J.; Zhao, Z.; Liao, Q.; Wang, J. TRPM7 promotes the epithelial-mesenchymal transition in ovarian cancer through the calcium-related PI3K/AKT oncogenic signaling. J. Exp. Clin. Cancer Res. 2019, 38, 106. [Google Scholar] [CrossRef]
- Chen, Y.; Liu, L.; Xia, L.; Wu, N.; Wang, Y.; Li, H.; Chen, X.; Zhang, X.; Liu, Z.; Zhu, M.; et al. TRPM7 silencing modulates glucose metabolic reprogramming to inhibit the growth of ovarian cancer by enhancing AMPK activation to promote HIF-1α degradation. J. Exp. Clin. Cancer Res. 2022, 41, 44. [Google Scholar] [CrossRef]
- Wang, J.; Xiao, L.; Luo, C.-H.; Zhou, H.; Hu, J.; Tang, Y.-X.; Fang, K.-N.; Zhang, Y. Overexpression of TRPM7 is Associated with Poor Prognosis in Human Ovarian Carcinoma. Asian Pac. J. Cancer Prev. 2014, 15, 3955–3958. [Google Scholar] [CrossRef]
- Wang, J.; Liao, Q.-J.; Zhang, Y.; Zhou, H.; Luo, C.-H.; Tang, J.; Wang, Y.; Tang, Y.; Zhao, M.; Zhao, X.-H.; et al. TRPM7 is required for ovarian cancer cell growth, migration and invasion. Biochem. Biophys. Res. Commun. 2014, 454, 547–553. [Google Scholar] [CrossRef]
- Davis, F.M.; Azimi, I.; Faville, R.A.; Peters, A.A.; Jalink, K.; Putney, J.W.; Goodhill, G.J.; Thompson, E.W.; Roberts-Thomson, S.J.; Monteith, G.R. Induction of epithelial–mesenchymal transition (EMT) in breast cancer cells is calcium signal dependent. Oncogene 2014, 33, 2307–2316. [Google Scholar] [CrossRef]
- Middelbeek, J.; Kuipers, A.J.; Henneman, L.; Visser, D.; Eidhof, I.; van Horssen, R.; Wieringa, B.; Canisius, S.V.; Zwart, W.; Wessels, L.F.; et al. TRPM7 Is Required for Breast Tumor Cell Metastasis. Cancer Res 2012, 72, 4250–4261. [Google Scholar] [CrossRef]
- Wang, Y.; Lu, R.; Chen, P.; Cui, R.; Ji, M.; Zhang, X.; Hou, P.; Qu, Y. Promoter methylation of transient receptor potential melastatin-related 7 (TRPM7) predicts a better prognosis in patients with Luminal A breast cancers. BMC Cancer 2022, 22, 951. [Google Scholar] [CrossRef]
- Guilbert, A.; Gautier, M.; Dhennin-Duthille, I.; Haren, N.; Sevestre, H.; Ouadid-Ahidouch, H. Evidence that TRPM7 is required for breast cancer cell proliferation. Am. J. Physiol. Cell Physiol. 2009, 297, C493–C502. [Google Scholar] [CrossRef]
- Guilbert, A.; Gautier, M.; Dhennin-Duthille, I.; Rybarczyk, P.; Sahni, J.; Sevestre, H.; Scharenberg, A.M.; Ouadid-Ahidouch, H. Transient receptor potential melastatin 7 is involved in oestrogen receptor-negative metastatic breast cancer cells migration through its kinase domain. Eur. J. Cancer 2013, 49, 3694–3707. [Google Scholar] [CrossRef] [PubMed]
- Gao, S.-L.; Kong, C.-Z.; Zhang, Z.; Li, Z.-L.; Bi, J.-B.; Liu, X.-K. TRPM7 is overexpressed in bladder cancer and promotes proliferation, migration, invasion and tumor growth. Oncol. Rep. 2017, 38, 1967–1976. [Google Scholar] [CrossRef] [PubMed]
- Cao, R.; Meng, Z.; Liu, T.; Wang, G.; Qian, G.; Cao, T.; Guan, X.; Dan, H.; Xiao, Y.; Wang, X. Decreased TRPM7 inhibits activities and induces apoptosis of bladder cancer cells via ERK1/2 pathway. Oncotarget 2016, 7, 72941–72960. [Google Scholar] [CrossRef] [PubMed]
- Cagnol, S.; Chambard, J.C. ERK and cell death: Mechanisms of ERK-induced cell death--apoptosis, autophagy and senescence. FEBS J. 2010, 277, 2–21. [Google Scholar] [CrossRef]
- Lee, E.H.; Chun, S.Y.; Kim, B.; Yoon, B.H.; Lee, J.N.; Kim, B.S.; Yoo, E.S.; Lee, S.; Song, P.H.; Kwon, T.G.; et al. Knockdown of TRPM7 prevents tumor growth, migration, and invasion through the Src, Akt, and JNK pathway in bladder cancer. BMC Urol. 2020, 20, 145. [Google Scholar] [CrossRef]
- Numata, T.; Okada, Y.; Sato-Numata, K. TRPM7 is involved in acid-induced necrotic cell death in a manner sensitive to progesterone in human cervical cancer cells. Physiol. Rep. 2019, 7, e14157. [Google Scholar] [CrossRef]
- Liu, X.; Gan, L.; Zhang, J. miR-543 inhibites cervical cancer growth and metastasis by targeting TRPM7. Chem. Biol. Interact. 2019, 302, 83–92. [Google Scholar] [CrossRef]
- Dong, R.F.; Zhuang, Y.J.; Wang, Y.; Zhang, Z.Y.; Xu, X.Z.; Mao, Y.R.; Yu, J.J. Tumor suppressor miR-192-5p targets TRPM7 and inhibits proliferation and invasion in cervical cancer. Kaohsiung J. Med. Sci. 2021, 37, 699–708. [Google Scholar] [CrossRef]
- Wan, J.; Guo, A.A.; King, P.; Guo, S.; Saafir, T.; Jiang, Y.; Liu, M. TRPM7 Induces Tumorigenesis and Stemness Through Notch Activation in Glioma. Front. Pharmacol. 2020, 11, 590723. [Google Scholar] [CrossRef]
- Leng, T.-D.; Li, M.-H.; Shen, J.-F.; Liu, M.-L.; Li, X.-B.; Sun, H.-W.; Branigan, D.; Zeng, Z.; Si, H.-F.; Li, J.; et al. Suppression of TRPM7 Inhibits Proliferation, Migration, and Invasion of Malignant Human Glioma Cells. CNS Neurosci. Ther. 2015, 21, 252–261. [Google Scholar] [CrossRef]
- Liu, M.; Inoue, K.; Leng, T.; Guo, S.; Xiong, Z.-G. TRPM7 channels regulate glioma stem cell through STAT3 and Notch signaling pathways. Cell Signal. 2014, 26, 2773–2781. [Google Scholar] [CrossRef] [PubMed]
- Middelbeek, J.; Visser, D.; Henneman, L.; Kamermans, A.; Kuipers, A.J.; Hoogerbrugge, P.M.; Jalink, K.; van Leeuwen, F.N. TRPM7 maintains progenitor-like features of neuroblastoma cells: Implications for metastasis formation. Oncotarget 2015, 6, 8760–8776. [Google Scholar] [CrossRef] [PubMed]
- Visser, D.; Langeslag, M.; Kedziora, K.M.; Klarenbeek, J.; Kamermans, A.; Horgen, F.D.; Fleig, A.; van Leeuwen, F.N.; Jalink, K. TRPM7 triggers Ca2+ sparks and invadosome formation in neuroblastoma cells. Cell Calcium 2013, 54, 404–415. [Google Scholar] [CrossRef] [PubMed]
- Chen, L.; Cao, R.; Wang, G.; Yuan, L.; Qian, G.; Guo, Z.; Wu, C.-L.; Wang, X.; Xiao, Y. Downregulation of TRPM7 suppressed migration and invasion by regulating epithelial–mesenchymal transition in prostate cancer cells. Med. Oncol. 2017, 34, 127. [Google Scholar] [CrossRef]
- Sun, Y.; Sukumaran, P.; Varma, A.; Derry, S.; Sahmoun, A.E.; Singh, B.B. Cholesterol-induced activation of TRPM7 regulates cell proliferation, migration, and viability of human prostate cells. Biochim. Biophys. Acta (BBA)-Mol. Cell Res. 2014, 1843, 1839–1850. [Google Scholar] [CrossRef]
- Yang, F.; Cai, J.; Zhan, H.; Situ, J.; Li, W.; Mao, Y.; Luo, Y. Suppression of TRPM7 Inhibited Hypoxia-Induced Migration and Invasion of Androgen-Independent Prostate Cancer Cells by Enhancing RACK1-Mediated Degradation of HIF-1α. Oxidative Med. Cell. Longev. 2020, 2020, 6724810. [Google Scholar] [CrossRef]
- Sun, Y.; Schaar, A.; Sukumaran, P.; Dhasarathy, A.; Singh, B.B. TGFβ-induced epithelial-to-mesenchymal transition in prostate cancer cells is mediated via TRPM7 expression. Mol. Carcinog. 2018, 57, 752–761. [Google Scholar] [CrossRef]
- Pugliese, D.; Armuzzi, A.; Castri, F.; Benvenuto, R.; Mangoni, A.; Guidi, L.; Gasbarrini, A.; Rapaccini, G.L.; Wolf, F.I.; Trapani, V. TRPM7 is overexpressed in human IBD-related and sporadic colorectal cancer and correlates with tumor grade. Dig. Liver Dis. 2020, 52, 1188–1194. [Google Scholar] [CrossRef]
- Kim, B.J.; Park, E.J.; Lee, J.H.; Jeon, J.-H.; Kim, S.J.; So, I. Suppression of transient receptor potential melastatin 7 channel induces cell death in gastric cancer. Cancer Sci. 2008, 99, 2502–2509. [Google Scholar] [CrossRef]
- Lefebvre, T.; Rybarczyk, P.; Bretaudeau, C.; Vanlaeys, A.; Cousin, R.; Brassart-Pasco, S.; Chatelain, D.; Dhennin-Duthille, I.; Ouadid-Ahidouch, H.; Brassart, B.; et al. TRPM7/RPSA Complex Regulates Pancreatic Cancer Cell Migration. Front. Cell Dev. Biol. 2020, 8, 549. [Google Scholar] [CrossRef]
- Luanpitpong, S.; Rodboon, N.; Samart, P.; Vinayanuwattikun, C.; Klamkhlai, S.; Chanvorachote, P.; Rojanasakul, Y.; Issaragrisil, S. A novel TRPM7/O-GlcNAc axis mediates tumour cell motility and metastasis by stabilising c-Myc and caveolin-1 in lung carcinoma. Br. J. Cancer 2020, 123, 1289–1301. [Google Scholar] [CrossRef] [PubMed]
- Takahashi, K.; Umebayashi, C.; Numata, T.; Honda, A.; Ichikawa, J.; Hu, Y.; Yamaura, K.; Inoue, R. TRPM7-mediated spontaneous Ca2+ entry regulates the proliferation and differentiation of human leukemia cell line K562. Physiol. Rep. 2018, 6, e13796. [Google Scholar] [CrossRef] [PubMed]
- Qiao, W.; Lan, X.; Ma, H.; Chan, J.; Lui, V.; Yeung, K.; Kwong, D.; Hu, Z.; Tsoi, J.; Matinlinna, J.; et al. Effects of Salivary Mg on Head and Neck Carcinoma via TRPM7. J. Dent. Res. 2019, 98, 304–312. [Google Scholar] [CrossRef]
- Luo, Y.; Wu, J.-Y.; Lu, M.-H.; Shi, Z.; Na, N.; Di, J.-M. Carvacrol Alleviates Prostate Cancer Cell Proliferation, Migration, and Invasion through Regulation of PI3K/Akt and MAPK Signaling Pathways. Oxidative Med. Cell. Longev. 2016, 2016, 1469693. [Google Scholar] [CrossRef] [PubMed]
- Sun, Y.; Selvaraj, S.; Varma, A.; Derry, S.; Sahmoun, A.E.; Singh, B.B. Increase in serum Ca2+/Mg2+ ratio promotes proliferation of prostate cancer cells by activating TRPM7 channels. J. Biol. Chem. 2013, 288, 255–263. [Google Scholar] [CrossRef] [PubMed]
- Toft-Bertelsen, T.L.; MacAulay, N. TRPing to the Point of Clarity: Understanding the Function of the Complex TRPV4 Ion Channel. Cells 2021, 10, 165. [Google Scholar] [CrossRef] [PubMed]
- Peters, A.A.; Jamaludin, S.Y.N.; Yapa, K.T.D.S.; Chalmers, S.; Wiegmans, A.P.; Lim, H.F.; Milevskiy, M.J.G.; Azimi, I.; Davis, F.M.; Northwood, K.S.; et al. Oncosis and apoptosis induction by activation of an overexpressed ion channel in breast cancer cells. Oncogene 2017, 36, 6490–6500. [Google Scholar] [CrossRef]
- Lee, W.H.; Choong, L.Y.; Mon, N.N.; Lu, S.; Lin, Q.; Pang, B.; Yan, B.; Krishna, V.S.R.; Singh, H.; Tan, T.Z.; et al. TRPV4 Regulates Breast Cancer Cell Extravasation, Stiffness and Actin Cortex. Sci. Rep. 2016, 6, 27903. [Google Scholar] [CrossRef]
- Fang, Y.; Liu, G.; Xie, C.; Qian, K.; Lei, X.; Liu, Q.; Liu, G.; Cao, Z.; Fu, J.; Du, H.; et al. Pharmacological inhibition of TRPV4 channel suppresses malignant biological behavior of hepatocellular carcinoma via modulation of ERK signaling pathway. Biomed. Pharmacother. 2018, 101, 910–919. [Google Scholar] [CrossRef]
- Liu, X.; Zhang, P.; Xie, C.; Sham, K.W.Y.; Ng, S.S.M.; Chen, Y.; Cheng, C.H.K. Activation of PTEN by inhibition of TRPV4 suppresses colon cancer development. Cell Death Dis. 2019, 10, 460. [Google Scholar] [CrossRef]
- Zhang, P.; Xu, J.; Zhang, H.; Liu, X.-Y. Identification of TRPV4 as a novel target in invasiveness of colorectal cancer. BMC Cancer 2021, 21, 1264. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.; Zhang, B.; Wang, X.; Mao, J.; Li, W.; Sun, Y.; Yuan, Y.; Ben, Q.; Hua, L.; Qian, A. TRPV4 Overexpression Promotes Metastasis Through Epithelial–Mesenchymal Transition in Gastric Cancer and Correlates with Poor Prognosis. OncoTargets Ther. 2020, 13, 8383–8394. [Google Scholar] [CrossRef] [PubMed]
- Xie, R.; Xu, J.; Xiao, Y.; Wu, J.; Wan, H.; Tang, B.; Liu, J.; Fan, Y.; Wang, S.; Wu, Y.; et al. Calcium Promotes Human Gastric Cancer via a Novel Coupling of Calcium-Sensing Receptor and TRPV4 Channel. Cancer Res 2017, 77, 6499–6512. [Google Scholar] [CrossRef] [PubMed]
- Tang, B.; Wu, J.; Zhu, M.X.; Sun, X.; Liu, J.; Xie, R.; Dong, T.X.; Xiao, Y.; Carethers, J.M.; Yang, S.; et al. VPAC1 couples with TRPV4 channel to promote calcium-dependent gastric cancer progression via a novel autocrine mechanism. Oncogene 2019, 38, 3946–3961. [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, srep08364. [Google Scholar] [CrossRef]
- Yu, Y.; Wu, X.; Liu, S.; Zhao, H.; Li, B.; Zhao, H.; Feng, X. Piezo1 regulates migration and invasion of breast cancer cells via modulating cell mechanobiological properties. Acta Biochim. Biophys. Sin. 2020, 53, 10–18. [Google Scholar] [CrossRef]
- Luo, M.; Cai, G.; Ho, K.K.Y.; Wen, K.; Tong, Z.; Deng, L.; Liu, A.P. Compression enhances invasive phenotype and matrix degradation of breast cancer cells via Piezo1 activation. BMC Mol. Cell Biol. 2022, 23, 1. [Google Scholar] [CrossRef]
- O’Callaghan, P.; Engberg, A.; Eriksson, O.; Fatsis-Kavalopoulos, N.; Stelzl, C.; Sanchez, G.; Idevall-Hagren, O.; Kreuger, J. Piezo1 activation attenuates thrombin-induced blebbing in breast cancer cells. J. Cell Sci. 2022, 135, jcs258809. [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.e7. [Google Scholar] [CrossRef]
- Qu, S.; Hu, T.; Qiu, O.; Su, Y.; Gu, J.; Xia, Z. Effect of Piezo1 Overexpression on Peritumoral Brain Edema in Glioblastomas. Am. J. Neuroradiol. 2020, 41, 1423–1429. [Google Scholar] [CrossRef]
- 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. Rep. 2020, 10, 16121. [Google Scholar] [CrossRef] [PubMed]
- 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/mTOR pathway and acceleration of cell cycle. Int. J. Oncol. 2019, 55, 629–644. [Google Scholar] [CrossRef] [PubMed]
- Kim, O.-H.; Choi, Y.W.; Park, J.H.; Hong, S.A.; Hong, M.; Chang, I.H.; Lee, H.J. Fluid shear stress facilitates prostate cancer metastasis through Piezo1-Src-YAP axis. Life Sci. 2022, 308, 120936. [Google Scholar] [CrossRef]
- Wang, X.; Cheng, G.; Miao, Y.; Qiu, F.; Bai, L.; Gao, Z.; Huang, Y.; Dong, L.; Niu, X.; Wang, X.; et al. Piezo type mechanosensitive ion channel component 1 facilitates gastric cancer omentum metastasis. J. Cell. Mol. Med. 2021, 25, 2238–2253. [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]
- 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] [PubMed]
- Li, Y.-M.; Xu, C.; Sun, B.; Zhong, F.-J.; Cao, M.; Yang, L.-Y. Piezo1 promoted hepatocellular carcinoma progression and EMT through activating TGF-β signaling by recruiting Rab5c. Cancer Cell Int. 2022, 22, 162. [Google Scholar] [CrossRef]
- Liu, S.; Xu, X.; Fang, Z.; Ning, Y.; Deng, B.; Pan, X.; He, Y.; Yang, Z.; Huang, K.; Li, J. Piezo1 impairs hepatocellular tumor growth via deregulation of the MAPK-mediated YAP signaling pathway. Cell Calcium 2021, 95, 102367. [Google Scholar] [CrossRef]
- Li, M.; Zhang, X.; Wang, M.; Wang, Y.; Qian, J.; Xing, X.; Wang, Z.; You, Y.; Guo, K.; Chen, J.; et al. Activation of Piezo1 contributes to matrix stiffness-induced angiogenesis in hepatocellular carcinoma. Cancer Commun. 2022, 42, 1162–1184. [Google Scholar] [CrossRef]
- Xiong, Y.; Dong, L.; Bai, Y.; Tang, H.; Li, S.; Luo, D.; Liu, F.; Bai, J.; Yang, S.; Song, X. Piezo1 activation facilitates ovarian cancer metastasis via Hippo/YAP signaling axis. Channels 2022, 16, 159–166. [Google Scholar] [CrossRef]
- Etem, E.; 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] [PubMed]
- Sun, Y.; Li, M.; Liu, G.; Zhang, X.; Zhi, L.; Zhao, J.; Wang, G. The function of Piezo1 in colon cancer metastasis and its potential regulatory mechanism. J. Cancer Res. Clin. Oncol. 2020, 146, 1139–1152. [Google Scholar] [CrossRef]
- Song, Y.; Chen, J.; Zhang, C.; Xin, L.; Li, Q.; Liu, Y.; Zhang, C.; Li, S.; Huang, P. Mechanosensitive channel Piezo1 induces cell apoptosis in pancreatic cancer by ultrasound with microbubbles. iScience 2022, 25, 103733. [Google Scholar] [CrossRef] [PubMed]
- 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]
- Szczot, M.; Nickolls, A.R.; Lam, R.M.; Chesler, A.T. The Form and Function of PIEZO2. Annu. Rev. Biochem. 2021, 90, 507–534. [Google Scholar] [CrossRef]
- Chen, X.; Momin, A.; Wanggou, S.; Wang, X.; Min, H.-K.; Dou, W.; Gong, Z.; Chan, J.; Dong, W.; Fan, J.J.; et al. Mechanosensitive brain tumor cells construct blood-tumor barrier to mask chemosensitivity. Neuron 2023, 111, 30–48.e14. [Google Scholar] [CrossRef]
- 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]
- 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, jcs258809. [Google Scholar] [CrossRef]
- 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]
- 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]
- Katsuta, E.; Takabe, K.; Vujcic, M.; Gottlieb, P.A.; Dai, T.; Mercado-Perez, A.; Beyder, A.; Wang, Q.; Opyrchal, M. Mechano-Sensing Channel PIEZO2 Enhances Invasive Phenotype in Triple-Negative Breast Cancer. Int. J. Mol. Sci. 2022, 23, 9909. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.; Jia, Y.; Wang, Z.; Zhang, Z.; Fu, W. A pan-cancer analysis reveals the genetic alterations and immunotherapy of Piezo2 in human cancer. Front. Genet. 2022, 13, 918977. [Google Scholar] [CrossRef] [PubMed]
- Pageon, S.V.; Govendir, M.A.; Kempe, D.; Biro, M.; Sawicka, A.; Babataheri, A.; Dogniaux, S.; Barakat, A.I.; Gonzalez-Rodriguez, D.; Hivroz, C.; et al. Mechanoimmunology: Molecular-scale forces govern immune cell functions. Mol. Biol. Cell 2018, 29, 1919–1926. [Google Scholar] [CrossRef]
- Mihăilă, R.-G. Liver stiffness in chronic hepatitis C virus infection. Rom. J. Intern. Med. 2019, 57, 85–98. [Google Scholar] [CrossRef] [PubMed]
- Miyazawa, A.; Ito, S.; Asano, S.; Tanaka, I.; Sato, M.; Kondo, M.; Hasegawa, Y. Regulation of PD-L1 expression by matrix stiffness in lung cancer cells. Biochem. Biophys. Res. Commun. 2018, 495, 2344–2349. [Google Scholar] [CrossRef] [PubMed]
- 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.; York, A.G.; et al. Mechanosensation of cyclical force by PIEZO1 is essential for innate immunity. Nature 2019, 573, 69–74. [Google Scholar] [CrossRef]
- Sahoo, S.S.; Majhi, R.K.; Tiwari, A.; Acharya, T.; Kumar, P.S.; Saha, S.; Kumar, A.; Goswami, C.; Chattopadhyay, S. Transient receptor potential ankyrin1 channel is endogenously expressed in T cells and is involved in immune functions. Biosci. Rep. 2019, 39, BSR20191437. [Google Scholar] [CrossRef] [PubMed]
- Yin, J.; Michalick, L.; Tang, C.; Tabuchi, A.; Goldenberg, N.; Dan, Q.; Awwad, K.; Wang, L.; Erfinanda, L.; Nouailles, G.; et al. Role of Transient Receptor Potential Vanilloid 4 in Neutrophil Activation and Acute Lung Injury. Am. J. Respir. Cell Mol. Biol. 2016, 54, 370–383. [Google Scholar] [CrossRef] [PubMed]
- Talavera, K.; Startek, J.B.; Alvarez-Collazo, J.; Boonen, B.; Alpizar, Y.A.; Sanchez, A.; Naert, R.; Nilius, B. Mammalian Transient Receptor Potential TRPA1 Channels: From Structure to Disease. Physiol. Rev. 2020, 100, 725–803. [Google Scholar] [CrossRef]
- Jordt, S.-E.; Bautista, D.M.; Chuang, H.-H.; McKemy, D.D.; Zygmunt, P.M.; Högestätt, E.D.; Meng, I.D.; Julius, D. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 2004, 427, 260–265. [Google Scholar] [CrossRef]
- Bautista, D.M.; Movahed, P.; Hinman, A.; Axelsson, H.E.; Sterner, O.; Högestätt, E.D.; Julius, D.; Jordt, S.-E.; Zygmunt, P.M. Pungent products from garlic activate the sensory ion channel TRPA1. Proc. Natl. Acad. Sci. USA 2005, 102, 12248–12252. [Google Scholar] [CrossRef] [PubMed]
- Sawada, Y.; Hosokawa, H.; Hori, A.; Matsumura, K.; Kobayashi, S. Cold sensitivity of recombinant TRPA1 channels. Brain Res. 2007, 1160, 39–46. [Google Scholar] [CrossRef] [PubMed]
- Moparthi, L.; Kichko, T.I.; Eberhardt, M.; Högestätt, E.D.; Kjellbom, P.; Johanson, U.; Reeh, P.W.; Leffler, A.; Filipovic, M.R.; Zygmunt, P.M. Human TRPA1 is a heat sensor displaying intrinsic U-shaped thermosensitivity. Sci. Rep. 2016, 6, 28763. [Google Scholar] [CrossRef]
- Startek, J.B.; Talavera, K.; Voets, T.; Alpizar, Y.A. Differential interactions of bacterial lipopolysaccharides with lipid membranes: Implications for TRPA1-mediated chemosensation. Sci. Rep. 2018, 8, 12010. [Google Scholar] [CrossRef]
- Shimizu, S.; Takahashi, N.; Mori, Y. TRPs as Chemosensors (ROS, RNS, RCS, Gasotransmitters). Handb. Exp. Pharmacol. 2014, 223, 767–794. [Google Scholar] [CrossRef]
- Horváth, Á.; Tékus, V.; Boros, M.; Pozsgai, G.; Botz, B.; Borbély, É.; Szolcsányi, J.; Pintér, E.; Helyes, Z. Transient receptor potential ankyrin 1 (TRPA1) receptor is involved in chronic arthritis: In vivo study using TRPA1-deficient mice. Arthritis Res. Ther. 2016, 18, 6. [Google Scholar] [CrossRef] [PubMed]
- Wechsler, J.B.; Hsu, C.-L.; Bryce, P.J. IgE-mediated mast cell responses are inhibited by thymol-mediated, activation-induced cell death in skin inflammation. J. Allergy Clin. Immunol. 2014, 133, 1735–1743. [Google Scholar] [CrossRef]
- Matsuda, K.; Arkwright, P.D.; Mori, Y.; Oikawa, M.-A.; Muko, R.; Tanaka, A.; Matsuda, H. A Rapid Shift from Chronic Hyperoxia to Normoxia Induces Systemic Anaphylaxis via Transient Receptor Potential Ankyrin 1 Channels on Mast Cells. J. Immunol. 2020, 205, 2959–2967. [Google Scholar] [CrossRef]
- Ma, S.; Wang, D.H. Knockout of Trpa1 Exacerbates Renal Ischemia–Reperfusion Injury with Classical Activation of Macrophages. Am. J. Hypertens. 2021, 34, 110–116. [Google Scholar] [CrossRef]
- Wang, Q.; Chen, K.; Zhang, F.; Peng, K.; Wang, Z.; Yang, D.; Yang, Y. TRPA1 regulates macrophages phenotype plasticity and atherosclerosis progression. Atherosclerosis 2020, 301, 44–53. [Google Scholar] [CrossRef]
- Huang, W.; August, A. The signaling symphony: T cell receptor tunes cytokine-mediated T cell differentiation. J. Leukoc. Biol. 2015, 97, 477–485. [Google Scholar] [CrossRef] [PubMed]
- Forni, M.F.; Domínguez-Amorocho, O.A.; de Assis, L.V.M.; Kinker, G.S.; Moraes, M.N.; de Lauro Castrucci, A.M.; Câmara, N.O.S. An Immunometabolic Shift Modulates Cytotoxic Lymphocyte Activation During Melanoma Progression in TRPA1 Channel Null Mice. Front. Oncol. 2021, 11, 667715. [Google Scholar] [CrossRef] [PubMed]
- Szabó, K.; Kemény, Á.; Balázs, N.; Khanfar, E.; Sándor, Z.; Boldizsár, F.; Gyulai, R.; Najbauer, J.; Pintér, E.; Berki, T. Presence of TRPA1 Modifies CD4+/CD8+ T Lymphocyte Ratio and Activation. Pharmaceuticals 2022, 15, 57. [Google Scholar] [CrossRef] [PubMed]
- Bertin, S.; Aoki-Nonaka, Y.; Lee, J.; de Jong, P.R.; Kim, P.; Han, T.; Yu, T.; To, K.; Takahashi, N.; Boland, B.S.; et al. The TRPA1 ion channel is expressed in CD4+ T cells and restrains T-cell-mediated colitis through inhibition of TRPV1. Gut 2016, 66, 1584–1596. [Google Scholar] [CrossRef]
- Morty, R.E.; Kuebler, W.M. TRPV4: An exciting new target to promote alveolocapillary barrier function. Am. J. Physiol.-Lung Cell. Mol. Physiol. 2014, 307, L817–L821. [Google Scholar] [CrossRef]
- Michalick, L.; Erfinanda, L.; Weichelt, U.; van der Giet, M.; Liedtke, W.; Kuebler, W.M. Transient Receptor Potential Vanilloid 4 and Serum Glucocorticoid–regulated Kinase 1 Are Critical Mediators of Lung Injury in Overventilated Mice In Vivo. Anesthesiology 2017, 126, 300–311. [Google Scholar] [CrossRef]
- Scheraga, R.G.; Abraham, S.; Niese, K.A.; Southern, B.D.; Grove, L.M.; Hite, R.D.; McDonald, C.; Hamilton, T.A.; Olman, M.A. TRPV4 Mechanosensitive Ion Channel Regulates Lipopolysaccharide-Stimulated Macrophage Phagocytosis. J. Immunol. 2016, 196, 428–436. [Google Scholar] [CrossRef]
- Meli, V.S.; Atcha, H.; Veerasubramanian, P.K.; Nagalla, R.R.; Luu, T.U.; Chen, E.Y.; Guerrero-Juarez, C.F.; Yamaga, K.; Pandori, W.; Hsieh, J.Y.; et al. YAP-mediated mechanotransduction tunes the macrophage inflammatory response. Sci. Adv. 2020, 6, eabb8471. [Google Scholar] [CrossRef]
- Scheraga, R.G.; Abraham, S.; Grove, L.M.; Southern, B.D.; Crish, J.F.; Perelas, A.; McDonald, C.; Asosingh, K.; Hasday, J.D.; Olman, M.A. TRPV4 Protects the Lung from Bacterial Pneumonia via MAPK Molecular Pathway Switching. J. Immunol. 2020, 204, 1310–1321. [Google Scholar] [CrossRef]
- Geng, J.; Shi, Y.; Zhang, J.; Yang, B.; Wang, P.; Yuan, W.; Zhao, H.; Li, J.; Qin, F.; Hong, L.; et al. TLR4 signalling via Piezo1 engages and enhances the macrophage mediated host response during bacterial infection. Nat. Commun. 2021, 12, 3519. [Google Scholar] [CrossRef]
- Atcha, H.; Meli, V.S.; Davis, C.T.; Brumm, K.T.; Anis, S.; Chin, J.; Jiang, K.; Pathak, M.M.; Liu, W.F. Crosstalk Between CD11b and Piezo1 Mediates Macrophage Responses to Mechanical Cues. Front. Immunol. 2021, 12, 689397. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Zhang, Z.; Yang, Q.; Cao, Y.; Dong, Y.; Bi, Y.; Liu, G. Immunoregulatory Role of the Mechanosensitive Ion Channel Piezo1 in Inflammation and Cancer. Molecules 2022, 28, 213. [Google Scholar] [CrossRef] [PubMed]
- Liu, C.S.C.; Raychaudhuri, D.; Paul, B.; Chakrabarty, Y.; Ghosh, A.R.; Rahaman, O.; Talukdar, A.; Ganguly, D. Cutting Edge: Piezo1 Mechanosensors Optimize Human T Cell Activation. J. Immunol. 2018, 200, 1255–1260. [Google Scholar] [CrossRef]
- Jairaman, A.; Othy, S.; Dynes, J.L.; Yeromin, A.V.; Zavala, A.; Greenberg, M.L.; Nourse, J.L.; Holt, J.R.; Cahalan, S.M.; Marangoni, F.; et al. Piezo1 channels restrain regulatory T cells but are dispensable for effector CD4+ T cell responses. Sci. Adv. 2021, 7, eabg5859. [Google Scholar] [CrossRef]
- Wang, Y.; Yang, H.; Jia, A.; Wang, Y.; Yang, Q.; Dong, Y.; Hou, Y.; Cao, Y.; Dong, L.; Bi, Y.; et al. Dendritic cell Piezo1 directs the differentiation of TH1 and Treg cells in cancer. eLife 2022, 11, e79957. [Google Scholar] [CrossRef] [PubMed]
- Aykut, B.; Chen, R.; Kim, J.I.; Wu, D.; Shadaloey, S.A.A.; Abengozar, R.; Preiss, P.; Saxena, A.; Pushalkar, S.; Leinwand, J.; et al. Targeting Piezo1 unleashes innate immunity against cancer and infectious disease. Sci. Immunol. 2020, 5, eabb5168. [Google Scholar] [CrossRef]
- Mueller, S.; Sandrin, L. Liver stiffness: A novel parameter for the diagnosis of liver disease. Hepatic Med. Evid. Res. 2010, 2, 49–67. [Google Scholar] [CrossRef]
- Huse, M. Mechanical forces in the immune system. Nat. Rev. Immunol. 2017, 17, 679–690. [Google Scholar] [CrossRef]
Cancer Type | Expression | Function | Clinical Features | Molecular Mechanism | References |
---|---|---|---|---|---|
Breast | Upregulated | Migration, invasion. | Poor overall survival. | Mechanical stress sensor. Actin protrusion formation via Src. Bleb-driven cell migration attenuation. | [101,102,103,104] |
Glioma | Upregulated | Proliferation, migration, invasion, angiogenesis. | Glioblastoma aggravation, poor prognosis. | ECM remodeling. | [105,106,107] |
Prostate | Upregulated | Proliferation, migration, invasion. | Poor overall survival. | Akt/mTOR signaling activation. Src/YAP signaling activation. | [108,109] |
Gastric | Upregulated | Proliferation, migration, invasion, angiogenesis. | Poor overall survival. | TFF1 inhibition. RhoA and Rac1 activation Calpain1/2 activation via HIF-1α upregulation. | [110,111,112] |
Liver | Upregulated | Migration, invasion, angiogenesis. | Poor clinical outcomes. | TGF-β activation via Rac5c. YAP activation in a Hippo-independent signaling mechanism. Mechanical stress sensor. | [113,114] |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 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 (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Otero-Sobrino, Á.; Blanco-Carlón, P.; Navarro-Aguadero, M.Á.; Gallardo, M.; Martínez-López, J.; Velasco-Estévez, M. Mechanosensitive Ion Channels: Their Physiological Importance and Potential Key Role in Cancer. Int. J. Mol. Sci. 2023, 24, 13710. https://doi.org/10.3390/ijms241813710
Otero-Sobrino Á, Blanco-Carlón P, Navarro-Aguadero MÁ, Gallardo M, Martínez-López J, Velasco-Estévez M. Mechanosensitive Ion Channels: Their Physiological Importance and Potential Key Role in Cancer. International Journal of Molecular Sciences. 2023; 24(18):13710. https://doi.org/10.3390/ijms241813710
Chicago/Turabian StyleOtero-Sobrino, Álvaro, Pablo Blanco-Carlón, Miguel Ángel Navarro-Aguadero, Miguel Gallardo, Joaquín Martínez-López, and María Velasco-Estévez. 2023. "Mechanosensitive Ion Channels: Their Physiological Importance and Potential Key Role in Cancer" International Journal of Molecular Sciences 24, no. 18: 13710. https://doi.org/10.3390/ijms241813710