NOMPC-dependent mechanotransduction shapes the dendrite of proprioceptive neurons

Chadha, Abhishek; Kaneko, Maki; Cook, Boaz

doi:10.1016/j.neulet.2015.04.033

Cited by 8 publications

(6 citation statements)

References 38 publications

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“…However, NOMPC channels and their homologs may serve multiple functions in different mechanosensors (Chadha et al, 2015; Effertz et al, 2011; Kang et al, 2010; Lehnert et al, 2013; Ramdya et al, 2015; Sidi et al, 2003; Yan et al, 2013; Zhang et al, 2013; Zhang et al, 2014), and their functions may be regulated differently in different cell types. It is conceivable that in different mechanosensors, NOMPC interacts with different sets of molecules that regulate channel opening in vivo , a possibility that warrants future investigation for better understanding of the mechanical gating machinery.…”

Section: Discussionmentioning

confidence: 99%

“…NOMPC fulfills essentially all the criteria for a bona fide mechanotransduction channel and mediates touch sensation in Drosophila larvae (Arnadottir and Chalfie, 2010; Yan et al, 2013). NOMPC is also involved in hearing of Drosophila larvae and adults (Bechstedt and Howard, 2008; Effertz et al, 2011; Kamikouchi et al, 2009; Lehnert et al, 2013; Liang et al, 2011; Zhang et al, 2013), collective behavior of adult flies (Ramdya et al, 2015), proprioception at adult leg joints (Chadha et al, 2015), as well as tension sensing in the hindgut of larvae (Zhang et al, 2014). NOMPC forms functional mechanotransduction channels in heterologous expression systems (Gong et al, 2013; Yan et al, 2013), thus facilitating structure-function studies of its mechanosensitivity (Zanini and Göpfert, 2013).…”

Section: Introductionmentioning

confidence: 99%

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Ankyrin Repeats Convey Force to Gate the NOMPC Mechanotransduction Channel

Zhang

Cheng

Kittelmann

et al. 2015

Cell

190

193

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Summary How metazoan mechanotransduction channels sense mechanical stimuli is not well understood. NOMPC channel in the transient receptor potential (TRP) family, a mechanotransduction channel for Drosophila touch sensation and hearing, contains 29 Ankyrin repeats (ARs) that associate with microtubules. These ARs have been postulated to act as a tether that conveys force to the channel. Here, we report that these N-terminal ARs form a cytoplasmic domain essential for NOMPC mechanogating in vitro, mechanosensitivity of touch receptor neurons in vivo, and touch-induced behaviors of Drosophila larvae. Duplicating the ARs elongates the filaments that tether NOMPC to microtubules in mechanosensory neurons. Moreover, microtubule association is required for NOMPC mechanogating. Importantly, transferring the NOMPC ARs to mechano-insensitive voltage-gated potassium channels confers mechanosensitivity to the chimeric channels. These experiments strongly support a tether mechanism of mechanogating for the NOMPC channel, providing insights regarding the basis of mechanosensitivity of mechanotransduction channels.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Ankyrin Repeats Convey Force to Gate the NOMPC Mechanotransduction Channel

Zhang

Cheng

Kittelmann

et al. 2015

Cell

190

193

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“…A natural question is: how much does each part of the neuronal circuit lead to recovery failure? In this context, one could consider the effect of stum, which is critical for transduction of mechanical stimuli in a subpopulation of proprioceptive neurons responsible for sensing joint angles (Desai et al, 2014), and nompC, which is required for virtually any mechanosensory signaling such as a response to changing joint angles (Chadha et al, 2015). It may also be interesting to better characterize coordination patterns (gaits) in animals after surgery.…”

Section: Discussionmentioning

confidence: 99%

Recovery of locomotion after injury inDrosophiladepends on proprioception

Isakov

Buchanan²,

Sullivan

et al. 2016

Journal of Experimental Biology

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Locomotion is necessary for survival in most animal species. However, injuries to the appendages mediating locomotion are common. We assess the recovery of walking in Drosophila melanogaster following leg amputation. Whereas flies preamputation explore open arenas in a symmetric fashion on average, foreleg amputation induces a strong turning bias away from the side of the amputation. However, we find that unbiased walking behavior returns over time in wild-type flies, while recovery is significantly impaired in proprioceptive mutants. To identify the biomechanical basis of this locomotor impairment and recovery, we then examine individual leg motion (gait) at a fine scale. A minimal mathematical model that links neurodynamics to body mechanics during walking shows that redistributing leg forces between the right and left side enables the observed recovery. Altogether, our study suggests that proprioceptive input from the intact limbs plays a crucial role in the behavioral plasticity associated with locomotor recovery after injury.

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“…() report a similar phenotype of T. castaneum , with impaired articulation in the femoral–tibial joint and severe walking disability, when treated with RNAi for the suppression of cuticular proteins analogous to peritrophins TcCPAP3‐B. Proprioceptive function of NompC for tibial‐tarsus joint is reported in D. melanogaster (Chadha et al ., ), although there is no molecular evidence for the involvement of nanchung and inactive in the femoral–tibial joint proprioception in T. castaneum . Together, the sensory setae, which consist of cuticular material, and the sensory channel Nanchung are likely involved in proprioception at the femoral–tibial joint.…”

Section: Discussionmentioning

confidence: 98%

“…Subsequently, it is reported to be a mechano‐gating channel for gentle touch in the larval stage through the class III and class IV dendritic arborization neuroenes (Gong et al ., ; Yan et al ., ). This channel is expressed in widely distributed sensory cells for sensing gentle touch, sound, proprioception and cold temperatures (Eberl et al ., ; Walker et al ., ; Gong et al ., ; Yan et al ., ; Chadha et al ., ; Turner et al ., ). A recent study describes the expression patterns of trpA5 , which is lacking in D. melanogaster , in the lepidopteran species Cydia pomonella (Cattaneo et al ., ).…”

Section: Discussionmentioning

confidence: 99%

Roles of transient receptor potential channels in eclosion and movement in the red flour beetle Tribolium castaneum

2018

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Transient receptor potential channels (TRPs) are a family of cation channels involved in various sensory mechanisms in Drosophila melanogaster, including mechanosensing. Phylogenetic analysis of mechanosensory TRPs in seven members of the TRPV, TRPN and TRPA subfamilies reveals a unique TcTrpA5 in Tribolium castaneum that is likely lost in D. melanogaster. Because mechanosensors are implicated in various key physiology, we investigate the roles of eight candidate mechanosensory TRPs in survival, walking behaviour and tonic immobility in T. castaneum using the RNA interference technique. Double-stranded RNA treatment of nompC (dsNompC) and trpA5 (dsTrpA5) results in eclosion failure, causing 93% mortality of beetles subjected to each of these treatments. The beetles that survive the dsNompC treatment show defects during sclerotization of the elytra. Adult beetles treated with dsNanchung and dsInactive show defects in the folding of the joint between the femur and tibia segments of the hind legs, resulting in abnormal walking behaviour and reduced walking speed. Regarding tonic immobility induced by mechanical stimulations on the ventral surface, knockout responses (death feignings) are significantly extended with dsNanchung, dsInactive and dsWaterwitch treatments. These data suggest that both nompC and trpA5 are required for adult eclosion. The functions of nanchung and inactive are involved in the folding the hind leg segments. In addition, nanchung, inactive, and waterwitch are likely the receptors involved in recovery from tonic immobility.

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NOMPC-dependent mechanotransduction shapes the dendrite of proprioceptive neurons

Cited by 8 publications

References 38 publications

Ankyrin Repeats Convey Force to Gate the NOMPC Mechanotransduction Channel

Ankyrin Repeats Convey Force to Gate the NOMPC Mechanotransduction Channel

Recovery of locomotion after injury inDrosophiladepends on proprioception

Roles of transient receptor potential channels in eclosion and movement in the red flour beetle Tribolium castaneum

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