Sonogenetic control of mammalian cells using exogenous Transient Receptor Potential A1 channels

Duque, Marc; Lee-Kubli, Corinne; Tufail, Yusuf; Magaram, Uri; Patel, Janki; Chakraborty, Ahana; Lopez, Jose Mendoza; Edsinger, Eric; Vasan, Aditya; Shiao, Rani; Weiss, Connor; Friend, James; Chalasani, Sreekanth H.

doi:10.1038/s41467-022-28205-y

Cited by 77 publications

(61 citation statements)

References 85 publications

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“…Mechanosensitive ion channels allow for the direct transduction of mechanical energy (e.g., US acoustic wave) into neural signals. These neural signals could also emanate from calcium influx in hs TRPA1-expressing mammalian human embryonic kidney-293T cells, which interact with the actin cytoskeleton inducing the calcium influx (Duque et al, 2022 ). The membrane conformational states have three general frameworks of voltage-induced changes: (1) membrane tension ( Figure 2 , (2) direct flexoelectricity ( Figure 2C ), and (3) thermodynamic waves ( Figure 2B ).…”

Section: Discussionmentioning

confidence: 99%

“…In mammals, there are a family of proteins in ion channel the Homo sapiens transient receptor potential A1 ( hs TRPA1), which recently are found to have mechanosensitive properties (Duque et al, 2022 ). Duque and colleagues demonstrated that in vitro and in vivo sonication in rats and mice produced calcium influx and membrane currents in hs TRPA1-expressing mammalian human embryonic kidney-293T cells.…”

Section: Mechanisms For Neuromodulation Via Usmentioning

confidence: 99%

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Current State of Potential Mechanisms Supporting Low Intensity Focused Ultrasound for Neuromodulation

Dell’Italia¹,

Sanguinetti

Monti

et al. 2022

Front. Hum. Neurosci.

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Low intensity focused ultrasound (LIFU) has been gaining traction as a non-invasive neuromodulation technology due to its superior spatial specificity relative to transcranial electrical/magnetic stimulation. Despite a growing literature of LIFU-induced behavioral modifications, the mechanisms of action supporting LIFU's parameter-dependent excitatory and suppressive effects are not fully understood. This review provides a comprehensive introduction to the underlying mechanics of both acoustic energy and neuronal membranes, defining the primary variables for a subsequent review of the field's proposed mechanisms supporting LIFU's neuromodulatory effects. An exhaustive review of the empirical literature was also conducted and studies were grouped based on the sonication parameters used and behavioral effects observed, with the goal of linking empirical findings to the proposed theoretical mechanisms and evaluating which model best fits the existing data. A neuronal intramembrane cavitation excitation model, which accounts for differential effects as a function of cell-type, emerged as a possible explanation for the range of excitatory effects found in the literature. The suppressive and other findings need additional theoretical mechanisms and these theoretical mechanisms need to have established relationships to sonication parameters.

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Section: Discussionmentioning

confidence: 99%

Section: Mechanisms For Neuromodulation Via Usmentioning

confidence: 99%

Current State of Potential Mechanisms Supporting Low Intensity Focused Ultrasound for Neuromodulation

Dell’Italia¹,

Sanguinetti

Monti

et al. 2022

Front. Hum. Neurosci.

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show abstract

“…However, the findings of Yoo et al (2022) provide only a mechanistic explanation that ultrasound activates neurons by mechanosensitive calcium accumulation; they do not indicate the specific MS ion channels that are directly gated by ultrasound force. In contrast, Duque et al (2022) revealed that ultrasound evoking gating of hsTRPA1 specifically requires its N-terminal tip region and cholesterol interactions. The cytoskeletal elements are involved in the ultrasound sensitivity of hsTRPA1.…”

Section: Ultrasound For the Exploration Of Mechanosensitive Ion Channelsmentioning

confidence: 88%

“…The pore-forming subunits MEC-4 and MEC-10 may interact with the ECM proteins MEC-1, MEC-5, and MEC-9 and the tubulins MEC-7 and MEC-12 ( Chalfie, 2009 ). Two recently sonogenetic studies showed that ultrasonic neuromodulation is mediated by mechanical stress on the plasma membrane and relies on the intact organization of actin filaments ( Duque et al, 2022 ; Yoo et al, 2022 ). Yoo et al (2022) demonstrated ultrasound stimulation activating specific MS ion channels including TRPP1/2, TRPC1, and PIEZO1.…”

Section: Ultrasound For the Exploration Of Mechanosensitive Ion Channelsmentioning

confidence: 99%

Force From Filaments: The Role of the Cytoskeleton and Extracellular Matrix in the Gating of Mechanosensitive Channels

Chuang

Chen

2022

Front. Cell Dev. Biol.

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The senses of proprioception, touch, hearing, and blood pressure on mechanosensitive ion channels that transduce mechanical stimuli with high sensitivity and speed. This conversion process is usually called mechanotransduction. From nematode MEC-4/10 to mammalian PIEZO1/2, mechanosensitive ion channels have evolved into several protein families that use variant gating models to convert different forms of mechanical force into electrical signals. In addition to the model of channel gating by stretching from lipid bilayers, another potent model is the opening of channels by force tethering: a membrane-bound channel is elastically tethered directly or indirectly between the cytoskeleton and the extracellular molecules, and the tethering molecules convey force to change the channel structure into an activation form. In general, the mechanical stimulation forces the extracellular structure to move relative to the cytoskeleton, deforming the most compliant component in the system that serves as a gating spring. Here we review recent studies focusing on the ion channel mechanically activated by a tethering force, the mechanotransduction-involved cytoskeletal protein, and the extracellular matrix. The mechanosensitive channel PIEZO2, DEG/ENaC family proteins such as acid-sensing ion channels, and transient receptor potential family members such as NompC are discussed. State-of-the-art techniques, such as polydimethylsiloxane indentation, the pillar array, and micropipette-guided ultrasound stimulation, which are beneficial tools for exploring the tether model, are also discussed.

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“…Ultrasound has recently been used to trigger mechanosensitive K + , Ca 2+ , and Na + channels that are found in the retina and brain ( Maingret et al, 1999 ; Kubanek et al, 2016 ; Sorum et al, 2021 ). Those mechanosensitive proteins include MEC-4 ( Kubanek et al, 2018 ), TRPP1/2 ( Duque et al, 2022 ), TRPV1 ( Yang et al, 2020 ), Piezo 1 ( Qiu et al, 2019a ), MscL ( Ye et al, 2018 ), TRAAK ( Sorum et al, 2021 ), and the K2p family ( Zhao et al, 2017 ). Although it has not been fully understood, those mechanosensitive components are believed to play a critical role in neuromodulation using UST ( Ye et al, 2018 ).…”

Section: Working Principle Of Ultrasound Stimulationmentioning

confidence: 99%

Ultrasound stimulation for non-invasive visual prostheses

Badadhe

Roh²,

Lee³

et al. 2022

Front. Cell. Neurosci.

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Globally, it is estimated there are more than 2.2 billion visually impaired people. Visual diseases such as retinitis pigmentosa, age-related macular degeneration, glaucoma, and optic neuritis can cause irreversible profound vision loss. Many groups have investigated different approaches such as microelectronic prostheses, optogenetics, stem cell therapy, and gene therapy to restore vision. However, these methods have some limitations such as invasive implantation surgery and unknown long-term risk of genetic manipulation. In addition to the safety of ultrasound as a medical imaging modality, ultrasound stimulation can be a viable non-invasive alternative approach for the sight restoration because of its ability to non-invasively control neuronal activities. Indeed, recent studies have demonstrated ultrasound stimulation can successfully modulate retinal/brain neuronal activities without causing any damage to the nerve cells. Superior penetration depth and high spatial resolution of focused ultrasound can open a new avenue in neuromodulation researches. This review summarizes the latest research results about neural responses to ultrasound stimulation. Also, this work provides an overview of technical viewpoints in the future design of a miniaturized ultrasound transducer for a non-invasive acoustic visual prosthesis for non-surgical and painless restoration of vision.

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Sonogenetic control of mammalian cells using exogenous Transient Receptor Potential A1 channels

Cited by 77 publications

References 85 publications

Current State of Potential Mechanisms Supporting Low Intensity Focused Ultrasound for Neuromodulation

Current State of Potential Mechanisms Supporting Low Intensity Focused Ultrasound for Neuromodulation

Force From Filaments: The Role of the Cytoskeleton and Extracellular Matrix in the Gating of Mechanosensitive Channels

Ultrasound stimulation for non-invasive visual prostheses

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