Temperature- and Touch-Sensitive Neurons Couple CNG and TRPV Channel Activities to Control Heat Avoidance in Caenorhabditis elegans
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{"title"=>"Temperature- and touch-sensitive neurons couple cng and trpv channel activities to control heat avoidance in caenorhabditis elegans", "type"=>"journal", "authors"=>[{"first_name"=>"Shu", "last_name"=>"Liu", "scopus_author_id"=>"55286375400"}, {"first_name"=>"Ekkehard", "last_name"=>"Schulze", "scopus_author_id"=>"7103397703"}, {"first_name"=>"Ralf", "last_name"=>"Baumeister", "scopus_author_id"=>"7102470615"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "pui"=>"364479942", "doi"=>"10.1371/journal.pone.0032360", "sgr"=>"84863373210", "scopus"=>"2-s2.0-84863373210", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"22448218"}, "id"=>"23d92726-d2fd-319a-b6d5-bc41b52637d7", "abstract"=>"BACKGROUND: Any organism depends on its ability to sense temperature and avoid noxious heat. The nematode Caenorhabditis elegans responds to noxious temperatures exceeding ∼35°C and also senses changes in its environmental temperature in the range between 15 and 25°C. The neural circuits and molecular mechanisms involved in thermotaxis have been successfully studied, whereas details of the thermal avoidance behavior remain elusive. In this work, we investigate neurological and molecular aspects of thermonociception using genetic, cell biological and physiological approaches.\\n\\nMETHODOLOGY/PRINCIPAL FINDINGS: We show here that the thermosensory neurons AFD, in addition to sensing temperature within the range within which the animals can thrive, also contribute to the sensation of noxious temperatures resulting in a reflex-like escape reaction. Distinct sets of interneurons are involved in transmitting thermonociception and thermotaxis, respectively. Loss of AFD is partially compensated by the activity of a pair of multidendritic, polymodal neurons, FLP, whereas laser ablation of both types of neurons abrogated the heat response in the head of the animals almost completely. A third pair of heat sensory neurons, PHC, is situated in the tail. We find that the thermal avoidance response requires the cell autonomous function of cGMP dependent Cyclic Nucleotide-Gated (CNG) channels in AFD, and the heat- and capsaicin-sensitive Transient Receptor Potential Vanilloid (TRPV) channels in the FLP and PHC sensory neurons.\\n\\nCONCLUSIONS/SIGNIFICANCE: Our results identify distinct thermal responses mediated by a single neuron, but also show that parallel nociceptor circuits and molecules may be used as back-up strategies to guarantee fast and efficient responses to potentially detrimental stimuli.", "link"=>"http://www.mendeley.com/research/temperature-touchsensitive-neurons-couple-cng-trpv-channel-activities-control-heat-avoidance-caenorh", "reader_count"=>48, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>4, "Librarian"=>1, "Researcher"=>11, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>16, "Student > Postgraduate"=>1, "Student > Master"=>4, "Other"=>2, "Student > Bachelor"=>5, "Professor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>4, "Librarian"=>1, "Researcher"=>11, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>16, "Student > Postgraduate"=>1, "Student > Master"=>4, "Other"=>2, "Student > Bachelor"=>5, "Professor"=>2}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>6, "Agricultural and Biological Sciences"=>28, "Medicine and Dentistry"=>1, "Neuroscience"=>6, "Arts and Humanities"=>1, "Physics and Astronomy"=>1, "Psychology"=>2, "Social Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Neuroscience"=>{"Neuroscience"=>6}, "Social Sciences"=>{"Social Sciences"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Psychology"=>{"Psychology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>28}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Unspecified"=>{"Unspecified"=>1}, "Arts and Humanities"=>{"Arts and Humanities"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "United States"=>5}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/665071"], "description"=>"<p>(A) Laser ablation of AFD, FLP and AIB led to severe defects in the head Tav response compared to mock-ablated animals (n>8). Individual neurons were identified by GFP-labeling and the success of the ablations was visualized by the disappearance of the GFP label in these neurons. Tav responses of the mock-ablated animals slightly differed, which is perhaps due to different GFP transgenes (see Methods). (B) AFD-laser-ablated and two transgenic lines [expressing <i>Diphtheria</i> Toxin A (DT-A) under the control of the <i>gcy-8</i> promoter] in which AFD was genetically ablated showed defective head Tav response, whereas DT-A killing of five pairs of sensory neurons (from the <i>odr-3</i> promoter), but not AFD, behaved like wild-type (n>80). (**P<0.001). Error bars indicate SD.</p>", "links"=>[], "tags"=>["afd", "flp", "sensory", "neurons", "mediate", "tav"], "article_id"=>335561, "categories"=>["Neuroscience"], "users"=>["Shu Liu", "Ekkehard Schulze", "Ralf Baumeister"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032360.g001", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_AFD_and_FLP_sensory_neurons_mediate_Tav_response_in_the_head_/335561", "title"=>"The AFD and FLP sensory neurons mediate Tav response in the head.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-20 01:32:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/665489"], "description"=>"<p>(A) The head Tav responses of mutants in CNG channel genes are shown. (B) Genetic-ablation of AFD did not further decrease the head Tav response in <i>tax-2</i>;<i>tax-4</i> double mutant. (C), (D) The defective Tav phenotype of both <i>tax-2</i> and <i>tax-4</i> single mutant was rescued by expressing a wild-type copy of the respective gene (<i>tax-2</i> or <i>tax-4</i>). Expression of <i>tax-4</i> or <i>tax-2</i> cDNA under the control of the AFD-specific <i>gcy-8</i> promoter rescued the respective mutant phenotype. No rescue was obtained when the <i>tax-4</i> or <i>tax-2</i> cDNA was expressed from the <i>odr-4</i> promoter (expressed in 12 neurons, but not in AFD). (E) The head Tav responses of the <i>gcy</i> mutants are shown. (*P<0.01; **P<0.001, n>50). Error bars indicate SD.</p>", "links"=>[], "tags"=>["cgmp", "signaling", "contributes", "tav", "afd"], "article_id"=>335975, "categories"=>["Neuroscience"], "users"=>["Shu Liu", "Ekkehard Schulze", "Ralf Baumeister"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032360.g005", "stats"=>{"downloads"=>3, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_cGMP_signaling_contributes_to_the_Tav_response_in_the_AFD_neurons_/335975", "title"=>"A cGMP signaling contributes to the Tav response in the AFD neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-20 01:39:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/665358"], "description"=>"<p>(A), (B) The head and tail Tav of <i>osm-9</i> and <i>ocr</i> single and double mutants are shown. (C) The defective Tav response in the head of the <i>ocr-2 osm-9</i> double mutant was rescued by the expression of <i>ocr-2</i> and/or <i>osm-9</i> full length genomic DNA as well as by expression of their respective cDNAs under the control of the <i>mec-3</i> promoter. (D) The expression of either <i>ocr-2</i> or <i>osm-9</i> full-length genomic DNA was sufficient for at least partial rescue of the defective Tav response in the tail of the <i>ocr-2 osm-9</i> double mutant. (*P<0.01; **P<0.001, n>80). Error bars indicate SD.</p>", "links"=>[], "tags"=>["osm-9", "tav", "flp", "neurons", "phc"], "article_id"=>335846, "categories"=>["Neuroscience"], "users"=>["Shu Liu", "Ekkehard Schulze", "Ralf Baumeister"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032360.g004", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_OCR_2_and_OSM_9_contribute_to_the_Tav_response_in_the_FLP_neurons_in_the_head_and_in_the_PHC_neurons_in_the_tail_of_C_elegans_/335846", "title"=>"OCR-2 and OSM-9 contribute to the Tav response in the FLP neurons in the head and in the PHC neurons in the tail of <i>C. elegans</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-20 01:37:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/340737", "https://ndownloader.figshare.com/files/340766", "https://ndownloader.figshare.com/files/340826", "https://ndownloader.figshare.com/files/340870", "https://ndownloader.figshare.com/files/340934", "https://ndownloader.figshare.com/files/340978", "https://ndownloader.figshare.com/files/341028", "https://ndownloader.figshare.com/files/341074", "https://ndownloader.figshare.com/files/341127", "https://ndownloader.figshare.com/files/341197", "https://ndownloader.figshare.com/files/341234", "https://ndownloader.figshare.com/files/341277", "https://ndownloader.figshare.com/files/341330"], "description"=>"<div><h3>Background</h3><p>Any organism depends on its ability to sense temperature and avoid noxious heat. The nematode <em>Caenorhabditis elegans</em> responds to noxious temperatures exceeding ∼35°C and also senses changes in its environmental temperature in the range between 15 and 25°C. The neural circuits and molecular mechanisms involved in thermotaxis have been successfully studied, whereas details of the thermal avoidance behavior remain elusive. In this work, we investigate neurological and molecular aspects of thermonociception using genetic, cell biological and physiological approaches.</p> <h3>Methodology/Principal Findings</h3><p>We show here that the thermosensory neurons AFD, in addition to sensing temperature within the range within which the animals can thrive, also contribute to the sensation of noxious temperatures resulting in a reflex-like escape reaction. Distinct sets of interneurons are involved in transmitting thermonociception and thermotaxis, respectively. Loss of AFD is partially compensated by the activity of a pair of multidendritic, polymodal neurons, FLP, whereas laser ablation of both types of neurons abrogated the heat response in the head of the animals almost completely. A third pair of heat sensory neurons, PHC, is situated in the tail. We find that the thermal avoidance response requires the cell autonomous function of cGMP dependent Cyclic Nucleotide-Gated (CNG) channels in AFD, and the heat- and capsaicin-sensitive Transient Receptor Potential Vanilloid (TRPV) channels in the FLP and PHC sensory neurons.</p> <h3>Conclusions/Significance</h3><p>Our results identify distinct thermal responses mediated by a single neuron, but also show that parallel nociceptor circuits and molecules may be used as back-up strategies to guarantee fast and efficient responses to potentially detrimental stimuli.</p> </div>", "links"=>[], "tags"=>["temperature-", "touch-sensitive", "neurons", "cng", "trpv", "activities", "avoidance"], "article_id"=>127362, "categories"=>["Neuroscience"], "users"=>["Shu Liu", "Ekkehard Schulze", "Ralf Baumeister"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0032360.s001", "https://dx.doi.org/10.1371/journal.pone.0032360.s002", "https://dx.doi.org/10.1371/journal.pone.0032360.s003", "https://dx.doi.org/10.1371/journal.pone.0032360.s004", "https://dx.doi.org/10.1371/journal.pone.0032360.s005", "https://dx.doi.org/10.1371/journal.pone.0032360.s006", "https://dx.doi.org/10.1371/journal.pone.0032360.s007", "https://dx.doi.org/10.1371/journal.pone.0032360.s008", "https://dx.doi.org/10.1371/journal.pone.0032360.s009", "https://dx.doi.org/10.1371/journal.pone.0032360.s010", "https://dx.doi.org/10.1371/journal.pone.0032360.s011", "https://dx.doi.org/10.1371/journal.pone.0032360.s012", "https://dx.doi.org/10.1371/journal.pone.0032360.s013"], "stats"=>{"downloads"=>38, "page_views"=>43, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Temperature_and_Touch_Sensitive_Neurons_Couple_CNG_and_TRPV_Channel_Activities_to_Control_Heat_Avoidance_in_Caenorhabditis_elegans_/127362", "title"=>"Temperature- and Touch-Sensitive Neurons Couple CNG and TRPV Channel Activities to Control Heat Avoidance in <em>Caenorhabditis elegans</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-03-20 02:02:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/665701"], "description"=>"<p>Five seconds after recording, the animals were exposed to the noxious heat stimuli which reached 38°C maximal temperature after seven seconds. Values reported are mean % ± SD % (sample size) of the average maximal FRET ratio change amplitude in each population post stimuli. ND: not determined.</p>", "links"=>[], "tags"=>["noxious", "stimuli", "sensory"], "article_id"=>336189, "categories"=>["Neuroscience"], "users"=>["Shu Liu", "Ekkehard Schulze", "Ralf Baumeister"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032360.t002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_YFP_CFP_ratio_change_calcium_influx_after_noxious_heat_stimuli_in_different_sensory_neurons_/336189", "title"=>"YFP/CFP ratio change (calcium influx) after noxious heat stimuli in different sensory neurons.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-03-20 01:43:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/665263"], "description"=>"<p>(A) Average ratio changes in AFD, PLM, PVD and ALM upon noxious heat. (**P<0.001 different from ratio changes in AFD in wild-type). (B), (C) Average ratio changes in FLP and PHC upon heat stimuli in wild-type, <i>unc-13</i> and <i>unc-31</i> mutant backgrounds. Data are shown in box plot (n>4). Error bars indicate SD.</p>", "links"=>[], "tags"=>["phc", "sensory", "neurons", "tav"], "article_id"=>335754, "categories"=>["Neuroscience"], "users"=>["Shu Liu", "Ekkehard Schulze", "Ralf Baumeister"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032360.g003", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_AFD_FLP_and_PHC_function_as_primary_sensory_neurons_in_the_Tav_response_/335754", "title"=>"AFD, FLP, and PHC function as primary sensory neurons in the Tav response.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-20 01:35:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/665664"], "description"=>"<p>The PVC and DVA interneurons mediate thermonociception in the tail of <i>C. elegans</i>.</p>", "links"=>[], "tags"=>["pvc", "dva", "interneurons", "mediate", "thermonociception"], "article_id"=>336152, "categories"=>["Neuroscience"], "users"=>["Shu Liu", "Ekkehard Schulze", "Ralf Baumeister"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032360.t001", "stats"=>{"downloads"=>4, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_PVC_and_DVA_interneurons_mediate_thermonociception_in_the_tail_of_C_elegans_/336152", "title"=>"The PVC and DVA interneurons mediate thermonociception in the tail of <i>C. elegans</i>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-03-20 01:42:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/665169"], "description"=>"<p>(A) <i>sem-4</i> and <i>unc-86</i> mutants showed strongly reduced tail Tav response (n>100). (B) Laser-ablation of the PHC neurons almost abrogated the tail Tav response, while ablation of PHA, PHB, PVD and the six touch neurons had no significant defects. (**P<0.001, n>8). Error bars indicate SD.</p>", "links"=>[], "tags"=>["phc", "sensory", "neurons", "mediate", "tav"], "article_id"=>335653, "categories"=>["Neuroscience"], "users"=>["Shu Liu", "Ekkehard Schulze", "Ralf Baumeister"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032360.g002", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_PHC_sensory_neurons_mediate_Tav_response_in_the_tail_of_C_elegans_/335653", "title"=>"The PHC sensory neurons mediate Tav response in the tail of <i>C. elegans</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-20 01:34:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/665577"], "description"=>"<p>(A) Circuit diagram of head Tav response. AFD forms gap junction with AIB. (B) Circuit diagram of tail Tav response. (C) Genetic pathways contributing to Tav response. Head Tav response is mediated by a cGMP signaling pathway within the AFD neurons and a TRPV1 pathway in FLP, whereas the tail Tav response is mediated via TRPV1 in the PHC neurons.</p>", "links"=>[], "tags"=>["noxious", "sensory", "neuron"], "article_id"=>336063, "categories"=>["Neuroscience"], "users"=>["Shu Liu", "Ekkehard Schulze", "Ralf Baumeister"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032360.g006", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Models_of_noxious_heat_sensory_neuron_function_/336063", "title"=>"Models of noxious heat sensory neuron function.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-20 01:41:03"}

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Relative Metric

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