Channeling the Force: Piezo1 Mechanotransduction in Cancer Metastasis
Abstract
:1. Introduction
2. Piezo1 Structure
3. Angiogenesis
4. Invasion and Migration
5. Intravasation and Extravasation
6. Dissemination
7. Piezo1 in Colonization
8. Piezo1 Survival and Apoptosis
9. Piezo1 in Immune Cells
10. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Guan, X. Cancer Metastases: Challenges and Opportunities. Acta Pharm. Sin. B 2015, 5, 402–418. [Google Scholar] [CrossRef] [Green Version]
- Seyfried, T.N.; Huysentruyt, L.C. On the Origin of Cancer Metastasis. Crit. Rev. Oncog. 2013, 18, 43–73. [Google Scholar] [CrossRef] [Green Version]
- Roche, J. The Epithelial-to-Mesenchymal Transition in Cancer. Cancers 2018, 10, 52. [Google Scholar] [CrossRef] [Green Version]
- Nishida, N.; Yano, H.; Nishida, T.; Kamura, T.; Kojiro, M. Angiogenesis in Cancer. Vasc. Health Risk Manag. 2006, 2, 213–219. [Google Scholar] [CrossRef]
- Mitchell, M.J.; Denais, C.; Chan, M.F.; Wang, Z.; Lammerding, J.; King, M.R. Lamin A/C Deficiency Reduces Circulating Tumor Cell Resistance to Fluid Shear Stress. Am. J. Physiol. Cell Physiol. 2015, 309, C736–C746. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barnes, J.M.; Nauseef, J.T.; Henry, M.D. Resistance to Fluid Shear Stress Is a Conserved Biophysical Property of Malignant Cells. PLoS ONE 2012, 7, e50973. [Google Scholar] [CrossRef] [Green Version]
- Hope, J.M.; Bersi, M.R.; Dombroski, J.A.; Clinch, A.B.; Pereles, R.S.; Merryman, W.D.; King, M.R. Circulating Prostate Cancer Cells Have Differential Resistance to Fluid Shear Stress-Induced Cell Death. J. Cell Sci. 2021, 134. [Google Scholar] [CrossRef]
- Liang, S.; Hoskins, M.; Dong, C. Tumor Cell Extravasation Mediated by Leukocyte Adhesion Is Shear Rate Dependent on IL-8 Signaling. Mol. Cell Biomech. 2009, 7, 77–91. [Google Scholar]
- Cameron, M.D.; Schmidt, E.E.; Kerkvliet, N.; Nadkarni, K.V.; Morris, V.L.; Groom, A.C.; Chambers, A.F.; MacDonald, I.C. Temporal Progression of Metastasis in Lung: Cell Survival, Dormancy, and Location Dependence of Metastatic Inefficiency. Cancer Res. 2000, 60, 2541–2546. [Google Scholar] [PubMed]
- Blomberg, O.S.; Spagnuolo, L.; de Visser, K.E. Immune Regulation of Metastasis: Mechanistic Insights and Therapeutic Opportunities. Dis. Model. Mech. 2018, 11. [Google Scholar] [CrossRef] [Green Version]
- Qian, C.-N.; Mei, Y.; Zhang, J. Cancer Metastasis: Issues and Challenges. Chin. J. Cancer 2017, 36. [Google Scholar] [CrossRef] [PubMed]
- Qiu, W.-Z.; Huang, P.-Y.; Shi, J.-L.; Xia, H.-Q.; Zhao, C.; Cao, K.-J. Neoadjuvant Chemotherapy plus Intensity-Modulated Radiotherapy versus Concurrent Chemoradiotherapy plus Adjuvant Chemotherapy for the Treatment of Locoregionally Advanced Nasopharyngeal Carcinoma: A Retrospective Controlled Study. Chin. J. Cancer 2016, 35, 2. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- 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. [Google Scholar] [CrossRef] [PubMed]
- 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]
- 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] [Green Version]
- Friedrich, E.E.; Hong, Z.; Xiong, S.; Zhong, M.; Di, A.; Rehman, J.; Komarova, Y.A.; Malik, A.B. Endothelial Cell Piezo1 Mediates Pressure-Induced Lung Vascular Hyperpermeability via Disruption of Adherens Junctions. Proc. Natl. Acad. Sci. USA 2019, 116, 12980–12985. [Google Scholar] [CrossRef] [Green Version]
- Prevarskaya, N.; Skryma, R.; Shuba, Y. Calcium in Tumour Metastasis: New Roles for Known Actors. Nat. Rev. Cancer 2011, 11, 609–618. [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] [Green Version]
- 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] [Green Version]
- 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] [Green Version]
- 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] [Green Version]
- Hope, J.M.; Lopez-Cavestany, M.; Wang, W.; Reinhart-King, C.A.; King, M.R. Activation of Piezo1 Sensitizes Cells to TRAIL-Mediated Apoptosis through Mitochondrial Outer Membrane Permeability. Cell Death Dis. 2019, 10, 1–15. [Google Scholar] [CrossRef]
- 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]
- 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, 4503. [Google Scholar] [CrossRef] [Green Version]
- 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]
- Fang, X.-Z.; Zhou, T.; Xu, J.-Q.; Wang, Y.-X.; Sun, M.-M.; He, Y.-J.; Pan, S.-W.; Xiong, W.; Peng, Z.-K.; Gao, X.-H.; et al. Structure, Kinetic Properties and Biological Function of Mechanosensitive Piezo Channels. Cell Biosci. 2021, 11, 13. [Google Scholar] [CrossRef] [PubMed]
- Zetter, B.R. Angiogenesis and Tumor Metastasis. Annu. Rev. Med. 1998, 49, 407–424. [Google Scholar] [CrossRef] [Green Version]
- Rajabi, M.; Mousa, S. The Role of Angiogenesis in Cancer Treatment. Biomedicines 2017, 5, 34. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lugano, R.; Ramachandran, M.; Dimberg, A. Tumor Angiogenesis: Causes, Consequences, Challenges and Opportunities. Cell. Mol. Life Sci. 2020, 77, 1745–1770. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, S.H.; Jeong, D.; Han, Y.-S.; Baek, M.J. Pivotal Role of Vascular Endothelial Growth Factor Pathway in Tumor Angiogenesis. Ann. Surg. Treat. Res. 2015, 89, 1. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, S.; Kim, H.J.; Oh, S.C.; Lee, D.-H. Genipin Inhibits the Invasion and Migration of Colon Cancer Cells by the Suppression of HIF-1α Accumulation and VEGF Expression. Food Chem. Toxicol. 2018, 116, 70–76. [Google Scholar] [CrossRef]
- Zhu, Y.; Tan, J.; Xie, H.; Wang, J.; Meng, X.; Wang, R. HIF-1α Regulates EMT via the Snail and β-Catenin Pathways in Paraquat Poisoning-Induced Early Pulmonary Fibrosis. J. Cell. Mol. Med. 2016, 20, 688–697. [Google Scholar] [CrossRef]
- Norton, K.-A.; Popel, A.S. Effects of Endothelial Cell Proliferation and Migration Rates in a Computational Model of Sprouting Angiogenesis. Sci. Rep. 2016, 6, 36992. [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]
- 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] [PubMed] [Green Version]
- Chan, K.T.; Bennin, D.A.; Huttenlocher, A. Regulation of Adhesion Dynamics by Calpain-Mediated Proteolysis of Focal Adhesion Kinase (FAK). J. Biol. Chem. 2010, 285, 11418–11426. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Franco, S.J.; Huttenlocher, A. Regulating Cell Migration: Calpains Make the Cut. J. Cell Sci. 2005, 118, 3829–3838. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kang, H.; Hong, Z.; Zhong, M.; Klomp, J.; Bayless, K.J.; Mehta, D.; Karginov, A.V.; Hu, G.; Malik, A.B. Piezo1 Mediates Angiogenesis through Activation of MT1-MMP Signaling. Am. J. Physiol. Cell Physiol. 2019, 316, C92–C103. [Google Scholar] [CrossRef]
- Genís, L.; Gálvez, B.G.; Gonzalo, P.; Arroyo, A.G. MT1-MMP: Universal or Particular Player in Angiogenesis? Cancer Metastasis Rev. 2006, 25, 77–86. [Google Scholar] [CrossRef]
- Zhang, T.; Chi, S.; Jiang, F.; Zhao, Q.; Xiao, B. A Protein Interaction Mechanism for Suppressing the Mechanosensitive Piezo Channels. Nat. Commun. 2017, 8, 1797. [Google Scholar] [CrossRef] [Green Version]
- Friedl, P.; Wolf, K. Tumour-Cell Invasion and Migration: Diversity and Escape Mechanisms. Nat. Rev. Cancer 2003, 3, 362–374. [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]
- 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] [Green Version]
- Kuntze, A.; Goetsch, O.; Fels, B.; Najder, K.; Unger, A.; Wilhelmi, M.; Sargin, S.; Schimmelpfennig, S.; Neumann, I.; Schwab, A.; et al. Protonation of Piezo1 Impairs Cell-Matrix Interactions of Pancreatic Stellate Cells. Front. Physiol. 2020. [Google Scholar] [CrossRef] [Green Version]
- Pierobon, M.; Ramos, C.; Wong, S.; Hodge, K.A.; Aldrich, J.; Byron, S.; Anthony, S.P.; Robert, N.J.; Northfelt, D.W.; Jahanzeb, M.; et al. Enrichment of PI3K-AKT–MTOR Pathway Activation in Hepatic Metastases from Breast Cancer. Clin. Cancer Res. 2017, 23, 4919–4928. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arumugam, T.; Brandt, W.; Ramachandran, V.; Moore, T.T.; Wang, H.; May, F.E.; Westley, B.R.; Hwang, R.F.; Logsdon, C.D. Trefoil Factor 1 Stimulates Both Pancreatic Cancer and Stellate Cells and Increases Metastasis. Pancreas 2011, 40, 815–822. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kalluri, R.; Weinberg, R.A. The Basics of Epithelial-Mesenchymal Transition. J. Clin. Investig. 2009, 119, 1420–1428. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhu, B.; Qian, W.; Han, C.; Bai, T.; Hou, X. Piezo 1 Activation Facilitates Cholangiocarcinoma Metastasis via Hippo/YAP Signaling Axis. Mol. Ther. Nucleic Acids 2021, 24, 241–252. [Google Scholar] [CrossRef]
- Zhou, T.; Gao, B.; Fan, Y.; Liu, Y.; Feng, S.; Cong, Q.; Zhang, X.; Zhou, Y.; Yadav, P.S.; Lin, J.; et al. Piezo1/2 Mediate Mechanotransduction Essential for Bone Formation through Concerted Activation of NFAT-YAP1-ß-Catenin. eLife 2020, 9, e52779. [Google Scholar] [CrossRef]
- Reid, S.E.; Kay, E.J.; Neilson, L.J.; Henze, A.; 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]
- Rice, A.J.; Cortes, E.; Lachowski, D.; Cheung, B.C.H.; Karim, S.A.; Morton, J.P.; del Río Hernández, A. Matrix Stiffness Induces Epithelial–Mesenchymal Transition and Promotes Chemoresistance in Pancreatic Cancer Cells. Oncogenesis 2017, 6, e352. [Google Scholar] [CrossRef] [Green Version]
- Nourse, J.L.; Pathak, M.M. How Cells Channel Their Stress: Interplay between Piezo1 and the Cytoskeleton. Semin Cell Dev. Biol. 2017, 71, 3–12. [Google Scholar] [CrossRef] [Green Version]
- Hung, W.-C.; Yang, J.R.; Yankaskas, C.L.; Wong, B.S.; Wu, P.-H.; Pardo-Pastor, C.; Serra, S.A.; Chiang, M.-J.; Gu, Z.; Wirtz, D.; et al. Confinement Sensing and Signal Optimization via Piezo1/PKA and Myosin II Pathways. Cell Rep. 2016, 15, 1430–1441. [Google Scholar] [CrossRef] [Green Version]
- Sandrini, F.; Matyakhina, L.; Sarlis, N.J.; Kirschner, L.S.; Farmakidis, C.; Gimm, O.; Stratakis, C.A. Regulatory Subunit Type I-α of Protein Kinase A (PRKAR1A): A Tumor-Suppressor Gene for Sporadic Thyroid Cancer. Genes Chromosom. Cancer 2002, 35, 182–192. [Google Scholar] [CrossRef] [PubMed]
- Wang, S.; Cheng, Y.; Zheng, Y.; He, Z.; Chen, W.; Zhou, W.; Duan, C.; Zhang, C. PRKAR1A Is a Functional Tumor Suppressor Inhibiting ERK/Snail/E-Cadherin Pathway in Lung Adenocarcinoma. Sci. Rep. 2016, 6, 39630. [Google Scholar] [CrossRef]
- Yu, F.-X.; Zhang, Y.; Park, H.W.; Jewell, J.L.; Chen, Q.; Deng, Y.; Pan, D.; Taylor, S.S.; Lai, Z.-C.; Guan, K.-L. Protein Kinase A Activates the Hippo Pathway to Modulate Cell Proliferation and Differentiation. Genes Dev. 2013, 27, 1223–1232. [Google Scholar] [CrossRef] [Green Version]
- Ellefsen, K.L.; Holt, J.R.; Chang, A.C.; Nourse, J.L.; Arulmoli, J.; Mekhdjian, A.H.; Abuwarda, H.; Tombola, F.; Flanagan, L.A.; Dunn, A.R.; et al. Myosin-II Mediated Traction Forces Evoke Localized Piezo1-Dependent Ca2+ Flickers. Commun. Biol. 2019, 2, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Wei, C.; Wang, X.; Chen, M.; Ouyang, K.; Song, L.-S.; Cheng, H. Calcium Flickers Steer Cell Migration. Nature 2009, 457, 901–905. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- 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, gmaa112. [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] [Green Version]
- 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] [Green Version]
- 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. [Google Scholar] [CrossRef]
- Győrffy, 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] [Green Version]
- O’Callaghan, P.; Engberg, A.; Fatsis-Kavalopoulos, N.; Sanchez, G.; Idevall-Hagren, O.; Kreuger, J. Piezo1 Activation Attenuates Thrombin-Induced Blebbing in Breast Cancer Cells. bioRxiv 2020. [Google Scholar] [CrossRef]
- Emig, R.; Knodt, W.; Krussig, M.J.; Zgierski-Johnston, C.M.; Gorka, O.; Groß, O.; Kohl, P.; Ravens, U.; Peyronnet, R. Piezo1 Channels Contribute to the Regulation of Human Atrial Fibroblast Mechanical Properties and Matrix Stiffness Sensing. Cells 2021, 10, 663. [Google Scholar] [CrossRef] [PubMed]
- Reymond, N.; d’Água, B.B.; Ridley, A.J. Crossing the Endothelial Barrier during Metastasis. Nat. Rev. Cancer 2013, 13, 858–870. [Google Scholar] [CrossRef] [PubMed]
- Wei, L.; Mousawi, F.; Li, D.; Roger, S.; Li, J.; Yang, X.; Jiang, L.-H. Adenosine Triphosphate Release and P2 Receptor Signaling in Piezo1 Channel-Dependent Mechanoregulation. Front. Pharmacol. 2019, 10, 1304. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Slattery, M.J.; Dong, C. Neutrophils Influence Melanoma Adhesion and Migration under Flow Conditions. Int. J. Cancer 2003, 106, 713–722. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ma, S.; Luo, K.Q. Hemodynamic Shear Stress Stimulates Migration and Extravasation of Tumor Cells by Elevating Cellular Oxidative Stress. Breast Can. Curr Res. 2017, 02. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.; Wei, J.; Kanada, M.; Yan, L.; Zhang, Z.; Watanabe, H.; Terakawa, S. Inhibition of Store-Operated Ca2+ Entry Suppresses EGF-Induced Migration and Eliminates Extravasation from Vasculature in Nasopharyngeal Carcinoma Cell. Cancer Lett. 2013, 336, 390–397. [Google Scholar] [CrossRef]
- Yankaskas, C.L.; Bera, K.; Stoletov, K.; Serra, S.A.; Carrillo-Garcia, J.; Tuntithavornwat, S.; Mistriotis, P.; Lewis, J.D.; Valverde, M.A.; Konstantopoulos, K. The Fluid Shear Stress Sensor TRPM7 Regulates Tumor Cell Intravasation. Sci. Adv. 2021, 7, eabh3457. [Google Scholar] [CrossRef] [PubMed]
- Hope, J.M.; Greenlee, J.D.; King, M.R. Mechanosensitive Ion Channels: TRPV4 and P2X7 in Disseminating Cancer Cells. Cancer J. 2018, 24, 84–92. [Google Scholar] [CrossRef] [PubMed]
- Lee, W.H.; Choong, L.Y.; Jin, T.H.; Mon, N.N.; Chong, S.; Liew, C.S.; Putti, T.; Lu, S.Y.; Harteneck, C.; Lim, Y.P. TRPV4 Plays a Role in Breast Cancer Cell Migration via Ca2+-Dependent Activation of AKT and Downregulation of E-Cadherin Cell Cortex Protein. Oncogenesis 2017, 6, e338. [Google Scholar] [CrossRef] [PubMed]
- 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] [Green Version]
- Chen, J.; Zhou, W.; Jia, Q.; Chen, J.; Zhang, S.; Yao, W.; Wei, F.; Zhang, Y.; Yang, F.; Huang, W.; et al. Efficient Extravasation of Tumor-Repopulating Cells Depends on Cell Deformability. Sci. Rep. 2016, 6, 19304. [Google Scholar] [CrossRef] [Green Version]
- Luo, R. Silencing TRPC1 Expression Inhibits Invasion of CNE2 Nasopharyngeal Tumor Cells. Oncol. Rep. 2012. [Google Scholar] [CrossRef]
- Langley, R.R.; Fidler, I.J. The Seed and Soil Hypothesis Revisited-The Role of Tumor-Stroma Interactions in Metastasis to Different Organs. Int. J. Cancer 2011, 128, 2527–2535. [Google Scholar] [CrossRef] [Green Version]
- Tsubouchi, A.; Sakakura, J.; Yagi, R.; Mazaki, Y.; Schaefer, E.; Yano, H.; Sabe, H. Localized Suppression of RhoA Activity by Tyr31/118-Phosphorylated Paxillin in Cell Adhesion and Migration. J. Cell Biol. 2002, 159, 673–683. [Google Scholar] [CrossRef] [Green Version]
- Xia, J.; Yu, X.; Tang, L.; Li, G.; He, T. P2X7 Receptor Stimulates Breast Cancer Cell Invasion and Migration via the AKT Pathway. Oncol. Rep. 2015, 34, 103–110. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Qiu, Y.; Li, W.; Zhang, H.; Liu, Y.; Tian, X.-X.; Fang, W.-G. P2X7 Mediates ATP-Driven Invasiveness in Prostate Cancer Cells. PLoS ONE 2014, 9, e114371. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jelassi, B.; Chantôme, A.; Alcaraz-Pérez, F.; Baroja-Mazo, A.; Cayuela, M.L.; Pelegrin, P.; Surprenant, A.; Roger, S. P2X7 Receptor Activation Enhances SK3 Channels- and Cystein Cathepsin-Dependent Cancer Cells Invasiveness. Oncogene 2011, 30, 2108–2122. [Google Scholar] [CrossRef] [Green Version]
- Gu, B.J.; Wiley, J.S. Rapid ATP-Induced Release of Matrix Metalloproteinase 9 Is Mediated by the P2X7 Receptor. Blood 2006, 107, 4946–4953. [Google Scholar] [CrossRef] [Green Version]
- Kim, J.; Yu, W.; Kovalski, K.; Ossowski, L. Requirement for Specific Proteases in Cancer Cell Intravasation as Revealed by a Novel Semiquantitative PCR-Based Assay. Cell 1998, 94, 353–362. [Google Scholar] [CrossRef] [Green Version]
- Wells, A.; Yates, C.; Shepard, C.R. E-Cadherin as an Indicator of Mesenchymal to Epithelial Reverting Transitions during the Metastatic Seeding of Disseminated Carcinomas. Clin. Exp. Metastasis 2008, 25, 621–628. [Google Scholar] [CrossRef] [Green Version]
- Banyard, J.; Bielenberg, D.R. The Role of EMT and MET in Cancer Dissemination. Connect. Tissue Res. 2015, 56, 403–413. [Google Scholar] [CrossRef] [Green Version]
- Zhang, S.; Cao, S.; Gong, M.; Zhang, W.; Zhang, W.; Zhu, Z.; Wu, S.; Shi, Y.; Wang, L.; Yue, Y.; et al. The Piezo1 Mechanosensitive Ion. Channel Promotes Melanoma Malignant Progression by Activating PI3K-AKT Signaling. Res. Sq. 2021. in review. [Google Scholar]
- Lee, J.; Cabrera, A.J.H.; Nguyen, C.M.T.; Kwon, Y.V. Dissemination of RasV12-Transformed Cells Requires the Mechanosensitive Channel Piezo. Nat. Commun. 2020, 11, 3568. [Google Scholar] [CrossRef] [PubMed]
- Simanshu, D.K.; Nissley, D.V.; McCormick, F. RAS Proteins and Their Regulators in Human Disease. Cell 2017, 170, 17–33. [Google Scholar] [CrossRef] [Green Version]
- Wright, K.L.; Adams, J.R.; Liu, J.C.; Loch, A.J.; Wong, R.G.; Jo, C.E.B.; Beck, L.A.; Santhanam, D.R.; Weiss, L.; Mei, X.; et al. Ras Signaling Is a Key Determinant for Metastatic Dissemination and Poor Survival of Luminal Breast Cancer Patients. Cancer Res. 2015, 75, 4960–4972. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fernandez-Medarde, A.; Santos, E. Ras in Cancer and Developmental Diseases. Genes Cancer 2011, 2, 344–358. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Prior, I.A.; Lewis, P.D.; Mattos, C. A Comprehensive Survey of Ras Mutations in Cancer. Cancer Res. 2012, 72, 2457–2467. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Prest, S.J.; May, F.E.B.; Westley, B.R. The Estrogen-Regulated Protein, TFF1, Stimulates Migration of Human Breast Cancer Cells. FASEB J. 2002, 16, 592–594. [Google Scholar] [CrossRef] [PubMed]
- May, F.E.B.; Griffin, S.M.; Westley, B.R. The Trefoil Factor Interacting Protein TFIZ1 Binds the Trefoil Protein TFF1 Preferentially in Normal Gastric Mucosal Cells but the Co-Expression of These Proteins Is Deregulated in Gastric Cancer. Int. J. Biochem. Cell Biol. 2009, 41, 632–640. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yamaguchi, J.; Yokoyama, Y.; Kokuryo, T.; Ebata, T.; Enomoto, A.; Nagino, M. Trefoil Factor 1 Inhibits Epithelial-Mesenchymal Transition of Pancreatic Intraepithelial Neoplasm. J. Clin. Investig. 2018, 128, 3619–3629. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Buache, E.; Etique, N.; Alpy, F.; Stoll, I.; Muckensturm, M.; Reina-San-Martin, B.; Chenard, M.P.; Tomasetto, C.; Rio, M.C. Deficiency in Trefoil Factor 1 (TFF1) Increases Tumorigenicity of Human Breast Cancer Cells and Mammary Tumor Development in TFF1-Knockout Mice. Oncogene 2011, 30, 3261–3273. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ortiz-Otero, N.; Marshall, J.R.; Lash, B.W.; King, M.R. Platelet Mediated TRAIL Delivery for Efficiently Targeting Circulating Tumor Cells. Nanoscale Adv. 2020, 2, 3942–3953. [Google Scholar] [CrossRef]
- Lou, X.-L.; Sun, J.; Gong, S.-Q.; Yu, X.-F.; Gong, R.; Deng, H. Interaction between Circulating Cancer Cells and Platelets: Clinical Implication. Chin. J. Cancer Res. 2015, 27, 450–460. [Google Scholar] [CrossRef]
- Franco, A.T.; Corken, A.; Ware, J. Platelets at the Interface of Thrombosis, Inflammation, and Cancer. Blood 2015, 126, 582–588. [Google Scholar] [CrossRef] [Green Version]
- Menter, D.G.; Tucker, S.C.; Kopetz, S.; Sood, A.K.; Crissman, J.D.; Honn, K.V. Platelets and Cancer: A Casual or Causal Relationship: Revisited. Cancer Metastasis Rev. 2014, 33, 231–269. [Google Scholar] [CrossRef] [Green Version]
- Varga-Szabo, D.; Braun, A.; Nieswandt, B. Calcium Signaling in Platelets. J. Thromb. Haemost. 2009, 7, 1057–1066. [Google Scholar] [CrossRef]
- Ilkan, Z.; Wright, J.R.; Goodall, A.H.; Gibbins, J.M.; Jones, C.I.; Mahaut-Smith, M.P. Evidence for Shear-Mediated Ca2+ Entry through Mechanosensitive Cation Channels in Human Platelets and a Megakaryocytic Cell Line. J. Biol. Chem. 2017, 292, 9204–9217. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rogers, S.; Lew, V.L. Up-down Biphasic Volume Response of Human Red Blood Cells to PIEZO1 Activation during Capillary Transits. PLoS Comput. Biol. 2021, 17, e1008706. [Google Scholar] [CrossRef] [PubMed]
- Cinar, E.; Zhou, S.; DeCourcey, J.; Wang, Y.; Waugh, R.E.; Wan, J. Piezo1 Regulates Mechanotransductive Release of ATP from Human RBCs. Proc. Natl. Acad. Sci. USA 2015, 112, 11783–11788. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- 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]
- Sottnik, J.L.; Dai, J.; Zhang, H.; Campbell, B.; Keller, E.T. Tumor-Induced Pressure in the Bone Microenvironment Causes Osteocytes to Promote the Growth of Prostate Cancer Bone Metastases. Cancer Res. 2015, 75, 2151–2158. [Google Scholar] [CrossRef] [Green Version]
- Sun, W.; Chi, S.; Li, Y.; Ling, S.; Tan, Y.; Xu, Y.; Jiang, F.; Li, J.; Liu, C.; Zhong, G.; et al. The Mechanosensitive Piezo1 Channel Is Required for Bone Formation. eLife 2019, 8, e47454. [Google Scholar] [CrossRef]
- Caulier, A.; Jankovsky, N.; Demont, Y.; Ouled-Haddou, H.; Demagny, J.; Guitton, C.; Merlusca, L.; Lebon, D.; Vong, P.; Aubry, A.; et al. PIEZO1 Activation Delays Erythroid Differentiation of Normal and Hereditary Xerocytosis-Derived Human Progenitor Cells. Haematologica 2020, 105, 610–622. [Google Scholar] [CrossRef] [Green Version]
- 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]
- Zhao, T.; Zhu, Y.; Morinibu, A.; Kobayashi, M.; Shinomiya, K.; Itasaka, S.; Yoshimura, M.; Guo, G.; Hiraoka, M.; Harada, H. HIF-1-Mediated Metabolic Reprogramming Reduces ROS Levels and Facilitates the Metastatic Colonization of Cancers in Lungs. Sci. Rep. 2014, 4, 3793. [Google Scholar] [CrossRef]
- Yang, H.; Guan, L.; Li, S.; Jiang, Y.; Xiong, N.; Li, L.; Wu, C.; Zeng, H.; Liu, Y. Mechanosensitive Caveolin-1 Activation-Induced PI3K/Akt/MTOR Signaling Pathway Promotes Breast Cancer Motility, Invadopodia Formation and Metastasis in Vivo. Oncotarget 2016, 7, 16227–16247. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nwosu, Z.C.; Ebert, M.P.; Dooley, S.; Meyer, C. Caveolin-1 in the Regulation of Cell Metabolism: A Cancer Perspective. Mol. Cancer 2016, 15, 71. [Google Scholar] [CrossRef] [Green Version]
- Yang, X.-Y.; Huang, C.-C.; Kan, Q.-M.; Li, Y.; Liu, D.; Zhang, X.-C.; Sato, T.; Yamagata, S.; Yamagata, T. Calcium Regulates Caveolin-1 Expression at the Transcriptional Level. Biochem. Biophys. Res. Commun. 2012, 426, 334–341. [Google Scholar] [CrossRef]
- Caolo, V.; Debant, M.; Endesh, N.; Futers, T.S.; Lichtenstein, L.; Bartoli, F.; Parsonage, G.; Jones, E.A.; Beech, D.J. Shear Stress Activates ADAM10 Sheddase to Regulate Notch1 via the Piezo1 Force Sensor in Endothelial Cells. eLife 2020, 9, e50684. [Google Scholar] [CrossRef]
- Gagliardi, M.; Pitner, M.K.; Park, J.; Xie, X.; Saso, H.; Larson, R.A.; Sammons, R.M.; Chen, H.; Wei, C.; Masuda, H.; et al. Differential Functions of ERK1 and ERK2 in Lung Metastasis Processes in Triple-Negative Breast Cancer. Sci. Rep. 2020, 10, 8537. [Google Scholar] [CrossRef] [PubMed]
- Huang, C.; Yoon, C.; Zhou, X.-H.; Zhou, Y.-C.; Zhou, W.-W.; Liu, H.; Yang, X.; Lu, J.; Lee, S.Y.; Huang, K. ERK1/2-Nanog Signaling Pathway Enhances CD44(+) Cancer Stem-like Cell Phenotypes and Epithelial-to-Mesenchymal Transition in Head and Neck Squamous Cell Carcinomas. Cell Death Dis. 2020, 11, 1–14. [Google Scholar] [CrossRef] [PubMed]
- Yu, H.-S.; Kim, J.-J.; Kim, H.-W.; Lewis, M.P.; Wall, I. Impact of Mechanical Stretch on the Cell Behaviors of Bone and Surrounding Tissues. J. Tissue Eng. 2016, 7, 2041731415618342. [Google Scholar] [CrossRef] [Green Version]
- McHugh, B.J.; Buttery, R.; Lad, Y.; Banks, S.; Haslett, C.; Sethi, T. Integrin Activation by Fam38A Uses a Novel Mechanism of R-Ras Targeting to the Endoplasmic Reticulum. J. Cell Sci. 2010, 123, 51–61. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Paoli, P.; Giannoni, E.; Chiarugi, P. Anoikis Molecular Pathways and Its Role in Cancer Progression. Biochim. Et Biophys. Acta (BBA)—Mol. Cell Res. 2013, 1833, 3481–3498. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Eisenhoffer, G.T.; Loftus, P.D.; Yoshigi, M.; Otsuna, H.; Chien, C.-B.; Morcos, P.A.; Rosenblatt, J. Crowding Induces Live Cell Extrusion to Maintain Homeostatic Cell Numbers in Epithelia. Nature 2012, 484, 546–549. [Google Scholar] [CrossRef] [PubMed]
- Woods, N.T.; Yamaguchi, H.; Lee, F.Y.; Bhalla, K.N.; Wang, H.-G. Anoikis, Initiated by Mcl-1 Degradation and Bim Induction, Is Deregulated during Oncogenesis. Cancer Res. 2007, 67, 10744–10752. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fulda, S.; Debatin, K.-M. Extrinsic versus Intrinsic Apoptosis Pathways in Anticancer Chemotherapy. Oncogene 2006, 25, 4798–4811. [Google Scholar] [CrossRef] [Green Version]
- Um, H.-D. Bcl-2 Family Proteins as Regulators of Cancer Cell Invasion and Metastasis: A Review Focusing on Mitochondrial Respiration and Reactive Oxygen Species. Oncotarget 2015, 7, 5193–5203. [Google Scholar] [CrossRef] [Green Version]
- 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]
- 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, 147–153. [Google Scholar] [CrossRef] [PubMed]
- Friemel, T.; Grillo, S.; Stella, S.L. Activation of Piezo1 Mechanosensitive Channels in Retinal Ganglion Cells Leads to Cell Death. FASEB J. 2020, 34, 1. [Google Scholar] [CrossRef]
- Mandic, A.; Viktorsson, K.; Strandberg, L.; Heiden, T.; Hansson, J.; Linder, S.; Shoshan, M.C. Calpain-Mediated Bid Cleavage and Calpain-Independent Bak Modulation: Two Separate Pathways in Cisplatin-Induced Apoptosis. Mol. Cell Biol. 2002, 22, 3003–3013. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gil-Parrado, S.; Fernández-Montalván, A.; Assfalg-Machleidt, I.; Popp, O.; Bestvater, F.; Holloschi, A.; Knoch, T.A.; Auerswald, E.A.; Welsh, K.; Reed, J.C.; et al. Ionomycin-Activated Calpain Triggers Apoptosis: A Probable Role for Bcl-2 Family Members. J. Biol. Chem. 2002, 277, 27217–27226. [Google Scholar] [CrossRef] [Green Version]
- Sobhan, P.K.; Seervi, M.; Deb, L.; Varghese, S.; Soman, A.; Joseph, J.; Mathew, K.A.; Raghu, G.; Thomas, G. Calpain and Reactive Oxygen Species Targets Bax for Mitochondrial Permeabilisation and Caspase Activation in Zerumbone Induced Apoptosis. PLoS ONE 2013, 8, e59350. [Google Scholar] [CrossRef] [Green Version]
- Tijore, A.; Yao, M.; Wang, Y.-H.; Hariharan, A.; Nematbakhsh, Y.; Lee Doss, B.; Lim, C.T.; Sheetz, M. Selective Killing of Transformed Cells by Mechanical Stretch. Biomaterials 2021, 275, 120866. [Google Scholar] [CrossRef]
- Feske, S. Calcium Signalling in Lymphocyte Activation and Disease. Nat. Rev. Immunol. 2007, 7, 690–702. [Google Scholar] [CrossRef]
- Vig, M.; Kinet, J.-P. Calcium Signaling in Immune Cells. Nat. Immunol. 2009, 10, 21–27. [Google Scholar] [CrossRef] [Green Version]
- Huang, S.; Ingber, D.E. Cell Tension, Matrix Mechanics, and Cancer Development. Cancer Cell 2005, 8, 175–176. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cox, T.R.; Erler, J.T. Remodeling and Homeostasis of the Extracellular Matrix: Implications for Fibrotic Diseases and Cancer. Dis. Models Mech. 2011, 4, 165–178. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Handorf, A.M.; Zhou, Y.; Halanski, M.A.; Li, W.-J. Tissue Stiffness Dictates Development, Homeostasis, and Disease Progression. Organogenesis 2015, 11, 1–15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- 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]
- Atcha, H.; Jairaman, A.; Holt, J.R.; Meli, V.S.; Nagalla, R.R.; Veerasubramanian, P.K.; Brumm, K.T.; Lim, H.E.; Othy, S.; Cahalan, M.D.; et al. Mechanically Activated Ion Channel Piezo1 Modulates Macrophage Polarization and Stiffness Sensing. Nat. Commun. 2021, 12, 3256. [Google Scholar] [CrossRef]
- 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]
- Chakraborty, M.; Chu, K.; Shrestha, A.; Revelo, X.S.; Zhang, X.; Gold, M.J.; Khan, S.; Lee, M.; Huang, C.; Akbari, M.; et al. Mechanical Stiffness Controls Dendritic Cell Metabolism and Function. Cell Rep. 2021, 34, 108609. [Google Scholar] [CrossRef]
- 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]
Metastatic Stage | Promoted Cancers | Inhibited Cancers |
---|---|---|
Angiogenesis | Colon [21] | |
Invasion and migration | Breast [20], Colon [21], Gastric [42], Pancreatic [43], Prostate [44], Liver [47], Glioblastoma [18], Synovial [19] | Lung [62] |
Intravasation and Extravasation | Lung [16] | |
Dissemination | Melanoma [85] | |
Colonization | No direct links | No direct links |
Apoptosis | Colon [21], Synovial [19], Breast [129] | Colon [21], Gastric [107], Prostate [43] |
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Dombroski, J.A.; Hope, J.M.; Sarna, N.S.; King, M.R. Channeling the Force: Piezo1 Mechanotransduction in Cancer Metastasis. Cells 2021, 10, 2815. https://doi.org/10.3390/cells10112815
Dombroski JA, Hope JM, Sarna NS, King MR. Channeling the Force: Piezo1 Mechanotransduction in Cancer Metastasis. Cells. 2021; 10(11):2815. https://doi.org/10.3390/cells10112815
Chicago/Turabian StyleDombroski, Jenna A., Jacob M. Hope, Nicole S. Sarna, and Michael R. King. 2021. "Channeling the Force: Piezo1 Mechanotransduction in Cancer Metastasis" Cells 10, no. 11: 2815. https://doi.org/10.3390/cells10112815