Evolution of Thermal Response Properties in a Cold-Activated TRP Channel

Myers, Benjamin R.; Sigal, Yaron M.; Julius, David

doi:10.1371/journal.pone.0005741

Cited by 69 publications

(80 citation statements)

References 23 publications

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“…Because temperatures beyond the appropriate range have detrimental effects (32,33), the activation temperature threshold for xtTRPV1 may be lower than that of mammalian TRPV1, which is several degrees higher than the core body temperature. To support this, it is also reported that there are striking correlations between species core body temperatures and the temperature ranges that activate transient receptor potential melastatin 8 (TRPM8) (34). Therefore, thermal activation of TRPV1 may also be tuned to the most appropriate temperature ranges for respective species.…”

Section: Discussionmentioning

confidence: 96%

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

Ohkita

Saito

Imagawa

et al. 2012

Journal of Biological Chemistry

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Background: TRPV1 is a thermosensitive channel in mammalian, but little information is available on amphibian TRPV1 function. Results: Capsaicin, heat, and acid stimulated cloned and endogenous frog TRPV1 channels, and the former two stimuli evoked nocifensive behaviors. Conclusion: Frog TRPV1 functions as a capsaicin-, heat-, and acid-sensitive channel. Significance: TRPV1 may have acquired a physiological role for noxious detection soon after its evolutionary origin.

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Section: Discussionmentioning

confidence: 96%

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

Ohkita

Saito

Imagawa

et al. 2012

Journal of Biological Chemistry

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“…A similar approach revealed sites within the cold receptor, TRPM8 (35), that determine sensitivity to cooling compounds (36). Although this method has greatly facilitated the analysis of chemical sensitivity, it has met with limited success in delineating regions that account for thermal sensitivity because TRPV1 and TRPM8 from different species retain temperature sensitivity as a highly conserved function, save for differences in precise temperature activation threshold (34,37). Thus, cross-species chimeric channels cannot be used to transfer heat or cold sensitivity cleanly to a thermoinsensitive ortholog.…”

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confidence: 99%

Cytoplasmic ankyrin repeats of transient receptor potential A1 (TRPA1) dictate sensitivity to thermal and chemical stimuli

Cordero-Morales¹,

Gracheva²,

Julius

2011

Proc. Natl. Acad. Sci. U.S.A.

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195

188

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Transient receptor potential (TRP) channels are polymodal signal detectors that respond to a wide array of physical and chemical stimuli, making them important components of sensory systems in both vertebrate and invertebrate organisms. Mammalian TRPA1 channels are activated by chemically reactive irritants, whereas snake and Drosophila TRPA1 orthologs are preferentially activated by heat. By comparing human and rattlesnake TRPA1 channels, we have identified two portable heat-sensitive modules within the ankyrin repeat-rich aminoterminal cytoplasmic domain of the snake ortholog. Chimeric channel studies further demonstrate that sensitivity to chemical stimuli and modulation by intracellular calcium also localize to the N-terminal ankyrin repeat-rich domain, identifying this region as an integrator of diverse physiological signals that regulate sensory neuron excitability. These findings provide a framework for understanding how restricted changes in TRPA1 sequence account for evolution of physiologically diverse channels, also identifying portable modules that specify thermosensitivity.chemosensation | pain | thermosensation | calcium modulation | somatosensation P rimary afferent (somatosensory) neurons detect a range of physical and chemical stimuli, including temperature, pressure, and noxious irritants (1). The transient receptor potential (TRP) channel family has been shown to play a predominant role in these processes, particularly in regard to thermosensitivity and chemosensitivity (2-5). TRPA1, otherwise known as the "wasabi receptor," plays a key role in somatosensation in evolutionarily diverse phyla, including vertebrate and invertebrate species. Mammalian TRPA1 is expressed by primary afferent sensory neurons of the pain pathway, where it functions as a sensor of environmental and endogenous chemical irritants, such as allyl isothiocyanate (AITC), acrolein, and 4-hydroxynonena, and contributes to cellular mechanisms underlying inflammatory pain (6-9).TRPA1 channels show species-specific functional variation to suit their physiological roles. For example, snakes are unique among vertebrates in that their TRPA1 channels are heat-sensitive, which some species (rattlesnakes, boas, and pythons) have exploited to detect infrared radiation (10). Similarly, insect TRPA1 channels are heat-sensitive and contribute to thermal avoidance behaviors (11)(12)(13)(14). In these cases, however, thermosensitivity comes at the expense of chemosensitivity, such that AITC and other chemical irritants still activate these channels but with reduced potency compared with mammalian orthologs (10). Despite clear physiological differences between snake and mammalian TRPA1 channels, they share significant amino acid identity (56%), providing a unique opportunity to exploit sequence comparisons and domain swaps to pinpoint structural elements associated with stimulus detection and/or gating. Delineating elements that contribute to TRPA1 function will provide insights into the evolutionary process whereby structural changes lead t...

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“…Innate behavioral responses to temperature have probably evolved to match specific habitats and physiology. For example, the threshold for activation of the cold-sensitive ion channel TRPM8 correlates with core body temperature in vertebrates (Myers et al 2009). Genetic variations also modulate nociception and temperature sensation within species.…”

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confidence: 99%

Heat Avoidance Is Regulated by Transient Receptor Potential (TRP) Channels and a Neuropeptide Signaling Pathway inCaenorhabditis elegans

Glauser¹,

Chen²,

Agin³

et al. 2011

Genetics

119

135

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The ability to avoid noxious extremes of hot and cold is critical for survival and depends on thermal nociception. The TRPV subset of transient receptor potential (TRP) channels is heat activated and proposed to be responsible for heat detection in vertebrates and fruit flies. To gain insight into the genetic and neural basis of thermal nociception, we developed assays that quantify noxious heat avoidance in the nematode Caenorhabditis elegans and used them to investigate the genetic basis of this behavior. First, we screened mutants for 18 TRP channel genes (including all TRPV orthologs) and found only minor defects in heat avoidance in single and selected double and triple mutants, indicating that other genes are involved. Next, we compared two wild isolates of C. elegans that diverge in their threshold for heat avoidance and linked this phenotypic variation to a polymorphism in the neuropeptide receptor gene npr-1. Further analysis revealed that loss of either the NPR-1 receptor or its ligand, FLP-21, increases the threshold for heat avoidance. Cell-specific rescue of npr-1 implicates the interneuron RMG in the circuit regulating heat avoidance. This neuropeptide signaling pathway operates independently of the TRPV genes, osm-9 and ocr-2, since mutants lacking npr-1 and both TRPV channels had more severe defects in heat avoidance than mutants lacking only npr-1 or both osm-9 and ocr-2. Our results show that TRPV channels and the FLP-21/ NPR-1 neuropeptide signaling pathway determine the threshold for heat avoidance in C. elegans.

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Evolution of Thermal Response Properties in a Cold-Activated TRP Channel

Cited by 69 publications

References 23 publications

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

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

Cytoplasmic ankyrin repeats of transient receptor potential A1 (TRPA1) dictate sensitivity to thermal and chemical stimuli

Heat Avoidance Is Regulated by Transient Receptor Potential (TRP) Channels and a Neuropeptide Signaling Pathway inCaenorhabditis elegans

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