Functional Role for Piezo1 in Stretch-evoked Ca2+ Influx and ATP Release in Urothelial Cell Cultures

Miyamoto, Tatsuya; Mochizuki, Takashi; Nakagomi, Hiroshi; Kira, Satoru; Watanabe, Masaki; Takayama, Yasunori; Suzuki, Yoshiro; Koizumi, Schuichi; Takeda, Masayuki; Tominaga, Makoto

doi:10.1074/jbc.m113.528638

Cited by 263 publications

(301 citation statements)

References 61 publications

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“…Piezo1 has been implicated in cellular processes in which cells respond to an external mechanical force, e.g., a stretch stimulus, osmotic pressure, or shear stress (31,33,34,(36)(37)(38). We asked whether cell-generated forces, such as traction forces, also can activate Piezo1.…”

Section: Resultsmentioning

confidence: 99%

Stretch-activated ion channel Piezo1 directs lineage choice in human neural stem cells

Pathak¹,

Nourse

Tran³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

499

509

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Neural stem cells are multipotent cells with the ability to differentiate into neurons, astrocytes, and oligodendrocytes. Lineage specification is strongly sensitive to the mechanical properties of the cellular environment. However, molecular pathways transducing matrix mechanical cues to intracellular signaling pathways linked to lineage specification remain unclear. We found that the mechanically gated ion channel Piezo1 is expressed by brainderived human neural stem/progenitor cells and is responsible for a mechanically induced ionic current. Piezo1 activity triggered by traction forces elicited influx of Ca 2+ , a known modulator of differentiation, in a substrate-stiffness-dependent manner. Inhibition of channel activity by the pharmacological inhibitor GsMTx-4 or by siRNA-mediated Piezo1 knockdown suppressed neurogenesis and enhanced astrogenesis. Piezo1 knockdown also reduced the nuclear localization of the mechanoreactive transcriptional coactivator Yes-associated protein. We propose that the mechanically gated ion channel Piezo1 is an important determinant of mechanosensitive lineage choice in neural stem cells and may play similar roles in other multipotent stem cells. (5) and that the mechanical properties of the culturing environment before transplantation can influence the outcome of in vivo stem cell transplants (6). Hence, a molecular and mechanistic understanding of how stem cells process mechanical cues and how this processing results in downstream signaling events and ultimately in fate decisions is needed for greater control over the fate of transplanted cells.Studies in mesenchymal and neural stem cells have revealed the involvement of focal adhesion zones and cytoskeletal proteins, such as integrins, nonmuscle myosin II (7), Rho GTPases (8-10), and vinculin (11), that participate in the generation of cellular traction forces. Recent work also has identified the nucleoskeletal protein lamin-A (12) and the transcriptional coactivators Yap (Yesassociated protein) and Taz (transcriptional coactivator with PDZbinding motif) (13) in mechanotransduction in mesenchymal stem cells. However, the mechanisms by which mechanical cues detected by cellular traction forces are transduced to downstream intracellular pathways of differentiation remain unclear.Ion channels are involved, directly or indirectly, in the transduction of all forms of physical stimuli-including sound, light, temperature, mechanical force, and even gravity-into intracellular signaling pathways. Hence, we wondered whether ion channels could be involved in transducing matrix mechanical cues to intracellular signaling pathways linked to lineage specification. In particular, we focused here on cationic stretch-activated channels (SACs) because they are known to detect mechanical forces with high sensitivity and broad dynamic range and because they are permeable to Ca 2+ , an important second messenger implicated in cell fate (14,15). We examined the role of SACs in neural stem cells, for which mechanical cues influence specification alo...

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Section: Resultsmentioning

confidence: 99%

Stretch-activated ion channel Piezo1 directs lineage choice in human neural stem cells

Pathak¹,

Nourse

Tran³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

499

509

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“…Volume 126 Number 12 December 2016 studies using urothelial cells and red blood cells have also shown a PIEZO1-mediated mechanotransductive release of ATP, indicating that this is a cellular mechanism not restricted to endothelial cells (48,49). However, the process of PIEZO1-mediated ATP release from endothelial cells appears to involve additional mechanisms that still need to be fully explored.…”

Section: +mentioning

confidence: 99%

Endothelial cation channel PIEZO1 controls blood pressure by mediating flow-induced ATP release

Wang

Chennupati

Kaur

et al. 2016

Journal of Clinical Investigation

467

454

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“…Primary Culture of Mouse Urothelial Cells-Following anesthesia, whole bladders were separated, and urothelial cells were prepared by the methods described previously with slight mod-ifications (17,18). The everted bladder was incubated with papain (6 l/ml) for 25 min at 37°C with just one tapping for 15 min after incubation.…”

Section: Methodsmentioning

confidence: 99%

Trpm7 Protein Contributes to Intercellular Junction Formation in Mouse Urothelium

Watanabe

Suzuki

Uchida

et al. 2015

Journal of Biological Chemistry

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Background: Transient receptor potential melastatin 7 (Trpm7) is a Ca 2ϩ -permeable channel with a kinase domain that is implicated in cell migration and adhesion. Results: Urothelium-specific Trpm7 knock-out caused immature intercellular junctions, inflammation, and smaller voided volume. Conclusion: Trpm7 contributes to the intercellular junction formation in the urothelium. Significance: These findings might provide the first evidence for the significance of Trpm7 in bladder function in vivo.

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Functional Role for Piezo1 in Stretch-evoked Ca2+ Influx and ATP Release in Urothelial Cell Cultures

Cited by 263 publications

References 61 publications

Stretch-activated ion channel Piezo1 directs lineage choice in human neural stem cells

Stretch-activated ion channel Piezo1 directs lineage choice in human neural stem cells

Endothelial cation channel PIEZO1 controls blood pressure by mediating flow-induced ATP release

Trpm7 Protein Contributes to Intercellular Junction Formation in Mouse Urothelium

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