Literature DB >> 23516290

The zebrafish ortholog of TRPV1 is required for heat-induced locomotion.

Philia Gau1, Jason Poon, Carmen Ufret-Vincenty, Corey D Snelson, Sharona E Gordon, David W Raible, Ajay Dhaka.   

Abstract

The ability to detect hot temperatures is critical to maintaining body temperature and avoiding injury in diverse animals from insects to mammals. Zebrafish embryos, when given a choice, actively avoid hot temperatures and display an increase in locomotion similar to that seen when they are exposed to noxious compounds such as mustard oil. Phylogenetic analysis suggests that the single zebrafish ortholog of TRPV1/2 may have arisen from an evolutionary precursor of the mammalian TRPV1 and TRPV2. As opposed to TRPV2, mammalian TRPV1 is essential for environmentally relevant heat sensation. In the present study, we provide evidence that the zebrafish TRPV1 ion channel is also required for the sensation of heat. Contrary to development in mammals, zebrafish TRPV1(+) neurons arise during the first wave of somatosensory neuron development, suggesting a vital importance of thermal sensation in early larval survival. In vitro analysis showed that zebrafish TRPV1 acts as a molecular sensor of environmental heat (≥25°C) that is distinctly lower than the sensitivity of the mammalian form (≥42°C) but consistent with thresholds measured in behavioral assays. Using in vivo calcium imaging with the genetically encoded calcium sensor GCaMP3, we show that TRPV1-expressing trigeminal neurons are activated by heat at behaviorally relevant temperatures. Using knock-down studies, we also show that TRPV1 is required for normal heat-induced locomotion. Our results demonstrate for the first time an ancient role for TRPV1 in the direct sensation of environmental heat and show that heat sensation is adapted to reflect species-dependent requirements in response to environmental stimuli.

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Year:  2013        PMID: 23516290      PMCID: PMC3893356          DOI: 10.1523/JNEUROSCI.5403-12.2013

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  47 in total

1.  The metalloproteinase inhibitor Reck is essential for zebrafish DRG development.

Authors:  Andrew Prendergast; Tor H Linbo; Tanya Swarts; Josette M Ungos; Hillary F McGraw; Shlomo Krispin; Brant M Weinstein; David W Raible
Journal:  Development       Date:  2012-02-01       Impact factor: 6.868

2.  TRP vanilloid 2 knock-out mice are susceptible to perinatal lethality but display normal thermal and mechanical nociception.

Authors:  Una Park; Nisha Vastani; Yun Guan; Srinivasa N Raja; Martin Koltzenburg; Michael J Caterina
Journal:  J Neurosci       Date:  2011-08-10       Impact factor: 6.167

3.  Multichannel wholemount fluorescent and fluorescent/chromogenic in situ hybridization in Xenopus embryos.

Authors:  Peter D Vize; Kyle E McCoy; Xiaolan Zhou
Journal:  Nat Protoc       Date:  2009       Impact factor: 13.491

4.  Rapid BAC selection for tol2-mediated transgenesis in zebrafish.

Authors:  Jeroen Bussmann; Stefan Schulte-Merker
Journal:  Development       Date:  2011-08-24       Impact factor: 6.868

5.  Molecular cloning and functional characterization of Xenopus tropicalis frog transient receptor potential vanilloid 1 reveal its functional evolution for heat, acid, and capsaicin sensitivities in terrestrial vertebrates.

Authors:  Masashi Ohkita; Shigeru Saito; Toshiaki Imagawa; Kenji Takahashi; Makoto Tominaga; Toshio Ohta
Journal:  J Biol Chem       Date:  2011-11-30       Impact factor: 5.157

6.  Robo2 determines subtype-specific axonal projections of trigeminal sensory neurons.

Authors:  Y Albert Pan; Margaret Choy; David A Prober; Alexander F Schier
Journal:  Development       Date:  2011-12-21       Impact factor: 6.868

7.  TRPM3 is a nociceptor channel involved in the detection of noxious heat.

Authors:  Joris Vriens; Grzegorz Owsianik; Thomas Hofmann; Stephan E Philipp; Julia Stab; Xiaodi Chen; Melissa Benoit; Fenqin Xue; Annelies Janssens; Sara Kerselaers; Johannes Oberwinkler; Rudi Vennekens; Thomas Gudermann; Bernd Nilius; Thomas Voets
Journal:  Neuron       Date:  2011-05-12       Impact factor: 17.173

8.  Molecular basis of infrared detection by snakes.

Authors:  Elena O Gracheva; Nicholas T Ingolia; Yvonne M Kelly; Julio F Cordero-Morales; Gunther Hollopeter; Alexander T Chesler; Elda E Sánchez; John C Perez; Jonathan S Weissman; David Julius
Journal:  Nature       Date:  2010-03-14       Impact factor: 49.962

9.  Ganglion-specific splicing of TRPV1 underlies infrared sensation in vampire bats.

Authors:  Elena O Gracheva; Julio F Cordero-Morales; José A González-Carcacía; Nicholas T Ingolia; Carlo Manno; Carla I Aranguren; Jonathan S Weissman; David Julius
Journal:  Nature       Date:  2011-08-03       Impact factor: 49.962

10.  Evolution of vertebrate transient receptor potential vanilloid 3 channels: opposite temperature sensitivity between mammals and western clawed frogs.

Authors:  Shigeru Saito; Naomi Fukuta; Ryuzo Shingai; Makoto Tominaga
Journal:  PLoS Genet       Date:  2011-04-07       Impact factor: 5.917

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  32 in total

Review 1.  Evolutionary tuning of TRPA1 and TRPV1 thermal and chemical sensitivity in vertebrates.

Authors:  Shigeru Saito; Makoto Tominaga
Journal:  Temperature (Austin)       Date:  2017-04-07

2.  Osteoblasts pattern endothelium and somatosensory axons during zebrafish caudal fin organogenesis.

Authors:  Rosalind G Bump; Camille E A Goo; Emma C Horton; Jeffrey P Rasmussen
Journal:  Development       Date:  2022-02-07       Impact factor: 6.868

3.  The MAP3Ks DLK and LZK Direct Diverse Responses to Axon Damage in Zebrafish Peripheral Neurons.

Authors:  Kadidia Pemba Adula; Matthew Shorey; Vasudha Chauhan; Khaled Nassman; Shu-Fan Chen; Melissa M Rolls; Alvaro Sagasti
Journal:  J Neurosci       Date:  2022-07-15       Impact factor: 6.709

4.  Convergent Temperature Representations in Artificial and Biological Neural Networks.

Authors:  Martin Haesemeyer; Alexander F Schier; Florian Engert
Journal:  Neuron       Date:  2019-07-31       Impact factor: 17.173

5.  Evolution of Heat Sensors Drove Shifts in Thermosensation between Xenopus Species Adapted to Different Thermal Niches.

Authors:  Shigeru Saito; Masashi Ohkita; Claire T Saito; Kenji Takahashi; Makoto Tominaga; Toshio Ohta
Journal:  J Biol Chem       Date:  2016-03-28       Impact factor: 5.157

6.  The structure and timescales of heat perception in larval zebrafish.

Authors:  Martin Haesemeyer; Drew N Robson; Jennifer M Li; Alexander F Schier; Florian Engert
Journal:  Cell Syst       Date:  2015-11-25       Impact factor: 10.304

Review 7.  TRPs et al.: a molecular toolkit for thermosensory adaptations.

Authors:  Lydia J Hoffstaetter; Sviatoslav N Bagriantsev; Elena O Gracheva
Journal:  Pflugers Arch       Date:  2018-02-27       Impact factor: 3.657

Review 8.  Transient receptor potential ankyrin 1 channel: An evolutionarily tuned thermosensor.

Authors:  V Sinica; V Vlachová
Journal:  Physiol Res       Date:  2021-05-12       Impact factor: 1.881

9.  Sub-lethal Camphor Exposure Triggers Oxidative Stress, Cardiotoxicity, and Cardiac Physiology Alterations in Zebrafish Embryos.

Authors:  Zheng-Cai Du; Zhong-Shang Xia; Ming-Zhe Zhang; Yan-Ting Wei; Nemi Malhotra; Ferry Saputra; Gilbert Audira; Marri Jmelou M Roldan; Chung-Der Hsiao; Er-Wei Hao; Xiao-Tao Hou; Jia-Gang Deng
Journal:  Cardiovasc Toxicol       Date:  2021-08-02       Impact factor: 3.231

10.  FAM19A5l Affects Mustard Oil-Induced Peripheral Nociception in Zebrafish.

Authors:  Inyoung Jeong; Seongsik Yun; Anu Shahapal; Eun Bee Cho; Sun Wook Hwang; Jae Young Seong; Hae-Chul Park
Journal:  Mol Neurobiol       Date:  2021-06-26       Impact factor: 5.590

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