Ankyrin Repeats Convey Force to Gate the NOMPC Mechanotransduction Channel

Zhang, Wei; Cheng, Li E.; Kittelmann, Maike; Li, Jiefu; Petković, Maja; Cheng, Tong; Jin, Peng; Guo, Zongyou; Göpfert, Martin C.; Jan, Yuh Nung

doi:10.1016/j.cell.2015.08.024

Cited by 197 publications

(218 citation statements)

References 58 publications

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“…2H ), suggesting that Nan functions in the Nan-Gal4 labeled neurons to mediate this kicking behavior. We also tested the involvement of NOMPC, a mechanotransduction channel involved in gentle touch of Drosophila larvae (Yan et al, 2013;Zhang et al, 2015), by using multiple RNA interference (RNAi) lines for RNAi knockdown of NOMPC in the Nanϩ neurons, and found that NOMPC channels are not required for this kicking response (Fig. 2I ).…”

Section: Resultsmentioning

confidence: 99%

A Defensive Kicking Behavior in Response to Mechanical Stimuli Mediated byDrosophilaWing Margin Bristles

Zhang

Guo

et al. 2016

J. Neurosci.

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Mechanosensation, one of the fastest sensory modalities, mediates diverse behaviors including those pertinent for survival. It is important to understand how mechanical stimuli trigger defensive behaviors. Here, we report that Drosophila melanogaster adult flies exhibit a kicking response against invading parasitic mites over their wing margin with ultrafast speed and high spatial precision. Mechanical stimuli that mimic the mites' movement evoke a similar kicking behavior. Further, we identified a TRPV channel, Nanchung, and a specific Nanchung-expressing neuron under each recurved bristle that forms an array along the wing margin as being essential sensory components for this behavior. Our electrophysiological recordings demonstrated that the mechanosensitivity of recurved bristles requires Nanchung and Nanchung-expressing neurons. Together, our results reveal a novel neural mechanism for innate defensive behavior through mechanosensation.

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Section: Resultsmentioning

confidence: 99%

A Defensive Kicking Behavior in Response to Mechanical Stimuli Mediated byDrosophilaWing Margin Bristles

Zhang

Guo

et al. 2016

J. Neurosci.

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“…Since the amount of protein per cell remains constant, it is instead likely the reduction of osmolytes for cells on stiff substrates is due to the exchange of ions with the surroundings. During cell spreading, cytoskeletal tension increases, and this has been tied to the increase of ion channel activity (28)(29)(30). To test the role of ion channel activity on cell volume variation, we inhibit chloride ion channels by 0.1 mM 5-nitro-2-(3-phenylpropylamino)-benzoic acid (NPPB) after cells fully spread.…”

Section: Ion Channels and The Actomyosin Cytoskeleton Play A Role In mentioning

confidence: 99%

Cell volume change through water efflux impacts cell stiffness and stem cell fate

Guo

Pegoraro

Mao

et al. 2017

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

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Cells alter their mechanical properties in response to their local microenvironment; this plays a role in determining cell function and can even influence stem cell fate. Here, we identify a robust and unified relationship between cell stiffness and cell volume. As a cell spreads on a substrate, its volume decreases, while its stiffness concomitantly increases. We find that both cortical and cytoplasmic cell stiffness scale with volume for numerous perturbations, including varying substrate stiffness, cell spread area, and external osmotic pressure. The reduction of cell volume is a result of water efflux, which leads to a corresponding increase in intracellular molecular crowding. Furthermore, we find that changes in cell volume, and hence stiffness, alter stem-cell differentiation, regardless of the method by which these are induced. These observations reveal a surprising, previously unidentified relationship between cell stiffness and cell volume that strongly influences cell biology.cell volume | cell mechanics | molecular crowding | gene expression | stem cell fate C ell volume is a highly regulated property that affects myriad functions (1, 2). It changes over the course of the cell life cycle, increasing as the cell plasma membrane grows and the amount of protein, DNA, and other intracellular material increases (3). However, it can also change on a much more rapid time scale, as, for example, on cell migration through confined spaces (4, 5); in this case, the volume change is a result of water transport out of the cell. This causes increased concentration of intracellular material and molecular crowding, having numerous important consequences (6, 7). Alternately, the volume of a cell can be directly changed through application of an external osmotic pressure. This forces water out of the cell, which also decreases cell volume, increases the concentration of intracellular material, and intensifies molecular crowding. Application of an external osmotic pressure to reduce cell volume also has other pronounced manifestations: For example, it leads to a significant change in cell mechanics, resulting in an increase in stiffness (8); it also impacts folding and transport of proteins (9), as well as condensation of chromatin (10). These dramatic effects of osmotic-induced volume change on cell behavior raise the question of whether cells ever change their volume through water efflux under isotonic conditions, perhaps to modulate their mechanics and behavior through changes in molecular crowding.Here, we demonstrate that when cells are cultured under the same isotonic conditions, but under stiffer extracellular environments, they reduce their cell volume through water efflux out of the cell, and this has a large and significant impact on cell mechanics and cell physiology. Specifically, as a cell spreads out on a stiff substrate, its volume decreases, and the cell behaves in a similar manner to that observed for cells under external osmotic pressure: Both the cortical and cytoplasmic stiffness increase as the vol...

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“…[9][10][11][12] Furthermore, microtubules support channel activity 13 ; for example, the coupling of the transient receptor potential family mechanotransduction channel NompC to an array of microtubules conveys force to gate channel activation. [14][15][16] Dendrite microtubule architecture differs between neuron types 15,[17][18][19][20] in order to support the specific functional requirements of each type. We illustrate that here for the specialized dendrites of class IV nociceptive 21 and class I proprioceptive 22 Drosophila body wall neurons.…”

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confidence: 99%