Abstract
In response to noxious stimuli, planarians cease their typical ciliary gliding and exhibit an oscillatory type of locomotion called scrunching. We have previously characterized the biomechanics of scrunching and shown that it is induced by specific stimuli, such as amputation, noxious heat, and extreme pH. Because these specific inducers are known to activate Transient Receptor Potential (TRP) channels in other systems, we hypothesized that TRP channels control scrunching. We found that chemicals known to activate TRPA1 (allyl isothiocyanate (AITC) and hydrogen peroxide) and TRPV (capsaicin and anandamide) in other systems induce scrunching in the planarian species Dugesia japonica and, except for anandamide, in Schmidtea mediterranea. To confirm that these responses were specific to either TRPA1 or TRPV, respectively, we tried to block scrunching using selective TRPA1 or TRPV antagonists and RNA interference (RNAi) mediated knockdown. Unexpectedly, co-treatment with a mammalian TRPA1 antagonist, HC-030031, enhanced AITC-induced scrunching by decreasing the latency time, suggesting an agonistic relationship in planarians. We further confirmed that TRPA1 in both planarian species is necessary for AITC-induced scrunching using RNAi. Conversely, while co-treatment of a mammalian TRPV antagonist, SB-366791, also enhanced capsaicin-induced reactions in D. japonica, combined knockdown of two previously identified D. japonica TRPV genes (DjTRPVa and DjTRPVb) did not inhibit capsaicin-induced scrunching. RNAi of DjTRPVa/DjTRPVb attenuated scrunching induced by the endocannabinoid and TRPV agonist, anandamide. Overall, our results show that although scrunching induction can involve different initial pathways for sensing stimuli, this behavior’s signature dynamical features are independent of the inducer, implying that scrunching is a stereotypical planarian escape behavior in response to various noxious stimuli that converge on a single downstream pathway. Understanding which aspects of nociception are conserved or not across different organisms can provide insight into the underlying regulatory mechanisms to better understand pain sensation.
Highlights
Normal locomotion of freshwater planarians, termed gliding, is achieved through synchronous beating of cilia in a layer of secreted mucus [1,2,3]
Based on the known inducers of scrunching in D. japonica and S. mediterranea ([4] and S2 Fig), and the recent work by Arenas et al suggesting that TRP ankyrin 1 (TRPA1) mediates scrunching in response to amputation in S. mediterranea [10], we tested known chemical agonists of planarian and/or other species’ TRPA1 and TRP vanilloid (TRPV) (Table 1) for their ability to trigger scrunching in D. japonica and S. mediterranea
We previously found that each planarian species exhibits a characteristic scrunching frequency and speed, with D. japonica scrunching at higher speeds and with almost double the frequency of S. mediterranea planarians [4]
Summary
Normal locomotion of freshwater planarians, termed gliding, is achieved through synchronous beating of cilia in a layer of secreted mucus [1,2,3]. When exposed to certain noxious stimuli (e.g. low pH, high temperature, or amputation), planarians switch to a muscular-based escape gait that is characterized by oscillatory body length changes [4] We termed this gait scrunching and showed that it has a characteristic set of 4 quantifiable parameters: 1. Scrunching shares similarities with peristalsis, another muscle-based oscillatory gait that occurs when cilia beating is disrupted [2,5,6,7], scrunching is cilia-independent, can be induced in animals performing peristalsis, and is distinguishable from peristalsis based on the 4 parameters listed above [4], demonstrating that scrunching and peristalsis are distinct gaits Because scrunching is such a stereotypical response involving many steps of neuronal communication (sensation, processing, neuromuscular communication), scrunching in response to noxious heat has proven to be a useful and sensitive readout of neuronal function in planarian toxicological studies [8,9]. Which molecular targets and neuronal circuits regulate scrunching remain an open question
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