Piezo1 mediates neuron oxygen-glucose deprivation/reoxygenation injury via Ca2+/calpain signaling

Wang, Yingying; Zhang, Hao; Ma, Tran; Liu, Yan; Xie, Hou-Yun; Wang, Wei; Ma, Yong; Li, Guanhua; Li, Yongwang

doi:10.1016/j.bbrc.2019.03.163

Cited by 37 publications

(36 citation statements)

References 22 publications

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“…Therefore, we cannot rule out the possibility that GsMTx4 may also directly protect oligodendrocytes through several mechanisms that are independent of Piezo1. More recently, Wang et al () have shown that Yoda‐1 induces Ca 2+ influx and calpain activation in the PC12 neuronal cell line and enhances oxygen/glucose deprivation‐induced apoptosis. This may help to explain the data presented here, which show that Yoda‐1 triggers axonal damage and demyelination and that GsMTx4 peptide attenuates both psychosine and LPC‐induced demyelination.…”

Section: Discussionmentioning

confidence: 99%

“…This may promote the influx of extracellular Ca 2+ into the neuron which, in turn, could trigger calcium‐induced calcium release (CICR) from intracellular stores. Yoda1 has also been shown to activate calpain signaling in neurons leading to neurodegeneration (Wang et al, ). This may explain how Yoda1 causes demyelination of CNS axons, that is, partly mediated through excitotoxicity and neuronal damage.…”

Section: Discussionmentioning

confidence: 99%

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Inhibition of Piezo1 attenuates demyelination in the central nervous system

Velasco‐Estevez

Gadalla

Liñan-Barba

et al. 2019

Glia

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Piezo1 is a mechanosensitive ion channel that facilitates the translation of extracellular mechanical cues to intracellular molecular signaling cascades through a process termed, mechanotransduction. In the central nervous system (CNS), mechanically gated ion channels are important regulators of neurodevelopmental processes such as axon guidance, neural stem cell differentiation, and myelination of axons by oligodendrocytes. Here, we present evidence that pharmacologically mediated overactivation of Piezo1 channels negatively regulates CNS myelination. Moreover, we found that the peptide GsMTx4, an antagonist of mechanosensitive cation channels such as Piezo1, is neuroprotective and prevents chemically induced demyelination. In contrast, the positive modulator of Piezo1 channel opening, Yoda‐1, induces demyelination and neuronal damage. Using an ex vivo murine‐derived organotypic cerebellar slice culture model, we demonstrate that GsMTx4 attenuates demyelination induced by the cytotoxic lipid, psychosine. Importantly, we confirmed the potential therapeutic effects of GsMTx4 peptide in vivo by co‐administering it with lysophosphatidylcholine (LPC), via stereotactic injection, into the cerebral cortex of adult mice. GsMTx4 prevented both demyelination and neuronal damage usually caused by the intracortical injection of LPC in vivo; a well‐characterized model of focal demyelination. GsMTx4 also attenuated both LPC‐induced astrocyte toxicity and microglial reactivity within the lesion core. Overall, our data suggest that pharmacological activation of Piezo1 channels induces demyelination and that inhibition of mechanosensitive channels, using GsMTx4, may alleviate the secondary progressive neurodegeneration often present in the latter stages of demyelinating diseases.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Inhibition of Piezo1 attenuates demyelination in the central nervous system

Velasco‐Estevez

Gadalla

Liñan-Barba

et al. 2019

Glia

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“…Western blots were performed as previously described [19]. Antibodies included Piezo1 (Santa Cruz Biotechnology, Dallas, TX, USA; sc-164,319),dilution ratio 1:1000),Bcl-2(Abgent, San Diego, CA, USA, dilution ratio 1:1000),caspase3 + cleaved caspase3(Cell Signaling Technology, Danvers, MA, USA; 9664 t, dilution ratio 1:2000) and GAPDH (Abcam, Cambridge, UK; Ab8245; dilution ratio 1:1000).…”

Section: Methodsmentioning

confidence: 99%

Piezo1 induced apoptosis of type II pneumocytes during ARDS

Liang

Cao

et al. 2019

Respir Res

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Objective The mechanisms of lung injury in acute respiratory distress syndrome (ARDS) are not well understood.Piezo1 was recently identified as a mechanotransduction protein. The present study found the expression of Piezo1 in type II pneumocytes and investigated its role in mediating ARDS-related lung injury. Methods Sprague-Dawley rats were used to establish an ARDS model, the expression of Piezo1,lung injuries, apoptosis as well as calcium influx were assessed. Results Piezo1 was expressed in type II pneumocytes as shown by immunofluorescence staining and expression was increased in the ARDS model. Knockdown of Piezo1 reduced apoptosis which was related to the elevation of Bcl-2.Calcium influx played a vital role in Piezo1-induced apoptosis. Conclusion Piezo1 was expressed in type II pneumocytes. Mechanical stretch of alveoli during ARDS induced activation of the Piezo1 channel,which resulted in calcium influx. The increased intracellular Ca2+ induced the apoptosis of type II pneumocytes, which may be related to the Bcl-2 pathway. Electronic supplementary material The online version of this article (10.1186/s12931-019-1083-1) contains supplementary material, which is available to authorized users.

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“…Most notably, in mouse DRG neurons Piezo2 was very highly expressed compared with Piezo1, whereas in mouse brain Piezo1 and Piezo2 were expressed in equally low, but quantifiable levels (Coste et al, 2010) as one might expect if Piezo1 and Piezo2 were only expressed in very select brain neurons (Satoh et al, 2006). In the case of Piezo1, subsequent studies have confirmed Piezo1 expression in the brain (Blumenthal et al, 2014;Pathak et al, et al, 2014;Zhang et al, 2014;Zeisel et al, 2015;Habib et al, 2016;Wang et al, 2019c). Most significantly, Blumenthal et al, (2014) studying rat hippocampal neuron-astrocyte interactions, proposed that the Piezo1 channel in neurons is able to sense and transduce the surface nanoroughness of astrocytes into trophic signals that maintain neuronal survival.…”

Section: Introductionmentioning

confidence: 96%

“…Interestingly, other stressful conditions increase Piezo1 expression, including those occurring with normal aging, bacterial infection, brain ischemia or exposure to demyelinating agents. Furthermore, experimental over activation of Piezo1 channels using Yoda1, a Piezo1 specific agonist (Syeda et al, 2015) directly disrupts normal neuronal function and/or survival (Wang et al, 2019c;Velasco-Esterervez et al, 2019a, b).…”

Section: Introductionmentioning

confidence: 99%

Piezo2, a pressure sensitive channel is expressed in select neurons of the mouse brain: a putative mechanism for synchronizing neural networks by transducing intracranial pressure pulses

Wang

Hamill

2020

Preprint

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Piezo2 expression in the normal, young adult mouse brain was examined using an anti-PIEZO2 Ab generated against a C-terminal fragment of the human PIEZO2 protein. As a positive control for Ab staining of mouse neurons, the Ab was shown to stain the majority (~90%) of mouse dorsal root ganglia (DRG) neurons, consistent with recent in situ hybridization and transcriptomic studies that also indicate Piezo2 gene expression in ~90% mouse DRG neurons.As a negative control and stringent test for specificity, the Ab failed to stain DRG satellite glial cells, which do not express Piezo2 but rather its paralog, Piezo1. In slices of brains isolated from the same mice as the DRG, the Ab displayed high selectivity in staining only specific neuron types, including some pyramidal neurons in the neocortex and hippocampus, Purkinje cells in the cerebellar cortex, and most notably mitral cells within the olfactory bulb. Given the demonstrated role of Piezo2 channels in peripheral neurons as a low-threshold pressure sensor (i.e., ≤ 5 mm Hg) critical for gentle touch, proprioception, and the regulation of breathing and blood pressure, its expression in select brain neurons has interesting implications. In particular, we propose that the pressure sensitive channel may provide specific brain neurons with an intrinsic resonance that acts to synchronize their firing with the normal pulsatile changes in intracranial pressure (ICP) associated with breathing and cardiac cycles. This novel mechanism could serve to increase the robustness of the respiration entrained oscillations that have been recorded in both rodent and human brains across widely distributed neuronal networks. The idea of a "global rhythm" within the brain has been mainly related to the effect of nasal airflow activating mechanosensitive neurons within the olfactory epithelium, which in turn synchronize, through direct synaptic connections, mitral neurons within the olfactory bulb and then through their projections, the activity of neural networks in other brain regions, including the hippocampus and neocortex. Our proposed, non-synaptic, intrinsic resonance mechanism for tracking pulsatile ICP changes would have the advantage that spatially separated brain networks could be globally synchronized effectively at the speed of sound.

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Piezo1 mediates neuron oxygen-glucose deprivation/reoxygenation injury via Ca2+/calpain signaling

Cited by 37 publications

References 22 publications

Inhibition of Piezo1 attenuates demyelination in the central nervous system

Inhibition of Piezo1 attenuates demyelination in the central nervous system

Piezo1 induced apoptosis of type II pneumocytes during ARDS

Piezo2, a pressure sensitive channel is expressed in select neurons of the mouse brain: a putative mechanism for synchronizing neural networks by transducing intracranial pressure pulses

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