Mechanical properties of lipid bilayers and regulation of mechanosensitive function

Balleza, Daniel

doi:10.4161/chan.21085

Cited by 23 publications

(21 citation statements)

References 153 publications

(249 reference statements)

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“…Early patch-clamping experiments resulted in the identification of stretch-activated ion channels in animal cells known to be specialized for mechanical perception 40–43 . Similar activities were soon identified in non-specialized cells 41, 44 , leading to the proposal that sensitivity to mechanical stimuli might be a basic cellular feature 26, 45 . In the decades since these first studies, many families of MS channels have been identified and characterized in bacteria, plants, animals, and archaea (reviewed in 46–48 ).…”

Section: Introductionmentioning

confidence: 75%

MscS-like Mechanosensitive Channels in Plants and Microbes

2013

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The challenge of osmotic stress is something all living organisms must face as a result of environmental dynamics. Over the past three decades, innovative research and cooperation across disciplines has irrefutably established that cells utilize mechanically gated ion channels to release osmolytes and prevent cell lysis during hypoosmotic stress. Early electrophysiological analysis of the inner membrane of Escherichia coli identified the presence of three distinct mechanosensitive activities. The subsequent discoveries of the genes responsible for two of these activities, the mechanosensitive channels of large (MscL) and small (MscS) conductance, led to the identification of two diverse families of mechanosensitive channels. The latter of these two families, the MscS family, is made up of members from bacteria, archaea, fungi, and plants. Genetic and electrophysiological analysis of these family members has provided insight into how organisms use mechanosensitive channels for osmotic regulation in response to changing environmental and developmental circumstances. Furthermore, solving the crystal structure of E. coli MscS and several homologs in several conformational states has contributed to the understanding of the gating mechanisms of these channels. Here we summarize our current knowledge of MscS homologs from all three domains of life, and address their structure, proposed physiological functions, electrophysiological behaviors, and topological diversity.

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Section: Introductionmentioning

confidence: 75%

MscS-like Mechanosensitive Channels in Plants and Microbes

2013

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“…Such hydrophobic mismatch partially prevents the channel pore from further expanding which might have detrimental effects on the cell, such as membrane rupture. Consistent with a change in thickness upon state transition in the MscL structure larger than in MscS, MscL appears to be more sensitive to thinning of the membrane . In short, it is very likely that a hydrophobic mismatch is an energetic penalty imposed upon MscL during its channel opening …”

Section: Energy Transmissionmentioning

confidence: 88%

From membrane tension to channel gating: A principal energy transfer mechanism for mechanosensitive channels

Zhang

2016

Protein Science

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Mechanosensitive (MS) channels are evolutionarily conserved membrane proteins that play essential roles in multiple cellular processes, including sensing mechanical forces and regulating osmotic pressure. Bacterial MscL and MscS are two prototypes of MS channels. Numerous structural studies, in combination with biochemical and cellular data, provide valuable insights into the mechanism of energy transfer from membrane tension to gating of the channel. We discuss these data in a unified two-state model of thermodynamics. In addition, we propose a lipid diffusion-mediated mechanism to explain the adaptation phenomenon of MscS.

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“…The lipid bilayer of the plasma membrane is also known to have viscoelasticity properties, which influence lipid‐protein or protein‐protein interaction‐induced cell signaling at the membrane surface . The mechanical properties of the lipid bilayer can change under tension, which affects mechanosensitive channels . These membrane‐mediated mechanical sensors can experience shear stress‐induced changes that, for example, expose cryptic binding sites, increase ion conductivity, produce conformational changes of membrane proteins, and increase tension in the lipid bilayer .…”

Section: Discussionmentioning

confidence: 99%

“…51 The mechanical properties of the lipid bilayer can change under tension, 52 which affects mechanosensitive channels. 53 These membrane-mediated mechanical sensors can experience shear stress-induced changes that, for example, expose cryptic binding sites, increase ion conductivity, produce conformational changes of membrane proteins, and increase tension in the lipid bilayer. 54 Membrane tension highly regulates Piezo1, a cytoskeleton-independent Ca 2+ -permeable nonselective cation channel, 55,56 which response to mechanical loading 57 within milliseconds.…”

Section: Discussionmentioning

confidence: 99%

High shear stress amplitude in combination with prolonged stimulus duration determine induction of osteoclast formation by hematopoietic progenitor cells

et al. 2020

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To date, it is unclear how fluid dynamics stimulate mechanosensory cells to induce an osteoprotective or osteodestructive response. We investigated how murine hematopoietic progenitor cells respond to 2 minutes of dynamic fluid flow stimulation with a precisely controlled sequence of fluid shear stresses. The response was quantified by measuring extracellular adenosine triphosphate (ATP), immunocytochemistry of Piezo1, and sarcoplasmic/endoplasmic Ca2+ reticulum ATPase 2 (SERCA2), and by the ability of soluble factors produced by mechanically stimulated cells to modulate osteoclast differentiation. We rejected our initial hypothesis that peak wall shear stress rate determines the response of hematopoietic progenitor cells to dynamic fluid shear stress, as it had only a minor correlation with the abovementioned parameters. Low stimulus amplitudes corresponded to activation of Piezo1, SERCA2, low concentrations of extracellular ATP, and inhibition of osteoclastogenesis and resorption area, while high amplitudes generally corresponded to osteodestructive responses. At a given amplitude (3 Pa) and waveform (square), the duration of individual stimuli (duty cycle) showed a strong correlation with the release of ATP and osteoclast number and resorption area. Collectively, our data suggest that hematopoietic progenitor cells respond in a viscoelastic manner to loading, since a combination of high shear stress amplitude and prolonged duty cycle is needed to trigger an osteodestructive response. Plain Language Summary In case of painful joints or missing teeth, the current intervention is to replace them with an implant to keep a high‐quality lifestyle. When exercising or chewing, the cells in the bone around the implant experience mechanical loading. This loading generally supports bone formation to strengthen the bone and prevent breaking, but can also stimulate bone loss when the mechanical loading becomes too high around orthopedic and dental implants. We still do not fully understand how cells in the bone can distinguish between mechanical loading that strengthens or weakens the bone. We cultured cells derived from the bone marrow in the laboratory to test whether the bone loss response depends on (i) how fast a mechanical load is applied (rate), (ii) how intense the mechanical load is (amplitude), or (iii) how long each individual loading stimulus is applied (duration). We mimicked mechanical loading as it occurs in the body, by applying very precisely controlled flow of fluid over the cells. We found that a mechanosensitive receptor Piezo1 was activated by a low amplitude stimulus, which usually strengthens the bone. The potential inhibitor of Piezo1, namely SERCA2, was only activated by a low amplitude stimulus. This happened regardless of the rate of application. At a constant high amplitude, a longer duration of the stimulus enhanced the bone‐weakening response. Based on these results we deduce that a high loading amplitude tends to be bone weakening, and the longer this high amplitude persists, the wor...

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Mechanical properties of lipid bilayers and regulation of mechanosensitive function

Cited by 23 publications

References 153 publications

MscS-like Mechanosensitive Channels in Plants and Microbes

MscS-like Mechanosensitive Channels in Plants and Microbes

From membrane tension to channel gating: A principal energy transfer mechanism for mechanosensitive channels

High shear stress amplitude in combination with prolonged stimulus duration determine induction of osteoclast formation by hematopoietic progenitor cells

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