Pharmacological or genetic targeting of Transient Receptor Potential (TRP) channels can disrupt the planarian escape response.
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 extr...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2019-01-01
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| Series: | PLoS ONE |
| Online Access: | https://doi.org/10.1371/journal.pone.0226104 |
| _version_ | 1818403422091608064 |
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| author | Ziad Sabry Alicia Ho Danielle Ireland Christina Rabeler Olivier Cochet-Escartin Eva-Maria S Collins |
| author_facet | Ziad Sabry Alicia Ho Danielle Ireland Christina Rabeler Olivier Cochet-Escartin Eva-Maria S Collins |
| author_sort | Ziad Sabry |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-14T08:24:00Z |
| format | Article |
| id | doaj.art-dcf030631f214fcf80a6c37ee30262db |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-12-14T08:24:00Z |
| publishDate | 2019-01-01 |
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| spelling | doaj.art-dcf030631f214fcf80a6c37ee30262db2022-12-21T23:09:41ZengPublic Library of Science (PLoS)PLoS ONE1932-62032019-01-011412e022610410.1371/journal.pone.0226104Pharmacological or genetic targeting of Transient Receptor Potential (TRP) channels can disrupt the planarian escape response.Ziad SabryAlicia HoDanielle IrelandChristina RabelerOlivier Cochet-EscartinEva-Maria S CollinsIn 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.https://doi.org/10.1371/journal.pone.0226104 |
| spellingShingle | Ziad Sabry Alicia Ho Danielle Ireland Christina Rabeler Olivier Cochet-Escartin Eva-Maria S Collins Pharmacological or genetic targeting of Transient Receptor Potential (TRP) channels can disrupt the planarian escape response. PLoS ONE |
| title | Pharmacological or genetic targeting of Transient Receptor Potential (TRP) channels can disrupt the planarian escape response. |
| title_full | Pharmacological or genetic targeting of Transient Receptor Potential (TRP) channels can disrupt the planarian escape response. |
| title_fullStr | Pharmacological or genetic targeting of Transient Receptor Potential (TRP) channels can disrupt the planarian escape response. |
| title_full_unstemmed | Pharmacological or genetic targeting of Transient Receptor Potential (TRP) channels can disrupt the planarian escape response. |
| title_short | Pharmacological or genetic targeting of Transient Receptor Potential (TRP) channels can disrupt the planarian escape response. |
| title_sort | pharmacological or genetic targeting of transient receptor potential trp channels can disrupt the planarian escape response |
| url | https://doi.org/10.1371/journal.pone.0226104 |
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