Functional diversity and evolutionary dynamics of thermoTRP channels

doi:10.1016/j.ceca.2014.12.001

Cell Calcium

Volume 57, Issue 3, March 2015, Pages 214-221

https://doi.org/10.1016/j.ceca.2014.12.001 Get rights and content

Highlights

•
ThermoTRP channels perceive temperature and chemical stimuli.
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Functional properties of thermoTRP channels vary among animal species.
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We describe the current understanding of evolutionary aspects of thermoTRP channels.

Abstract

Animals have evolved sophisticated physiological systems for sensing ambient temperature since changes in environmental temperatures affect various biological processes. Thermosensitive transient receptor potential (thermoTRP) channels serve as thermal sensors in diverse animal species. They are multimodal receptors that are activated by temperature as well as other physical and chemical stimuli. Since thermoTRP channels are calcium permeable non-selective cation channels, their activation leads to an influx of calcium and sodium ions into the cell and triggers downstream signal transduction. ThermoTRP channels have been characterized in diverse animal species over the past several years, illuminating the diversification of thermoTRP channels in the course of evolution. The gene repertoires of thermoTRP channels differ among animal species. Additionally, in some cases, the temperature and chemical sensitivities among orthologous thermoTRP channels vary among species. The evolutionary flexibility of thermoTRP channels enabled them to contribute to unique physiological systems such as infrared sensation in snakes and bats and seasonal adaptation in silk moth. On the other hand, the functional differences of thermoTRP channels among species have been utilized for understanding the molecular basis for their activation (or inhibition) mechanisms, and amino acid residues (or domains) responsible for the respective channel properties have been identified in various thermoTRP channels. Here we summarize the current understanding of the functional diversity and evolutionary dynamics of thermoTRP channels.

Graphical abstract

Introduction

Animals have evolved sophisticated physiological systems for sensing ambient temperatures (thermosensation) since changes in environmental temperature affect various biological processes. During the initiation of signal transduction for thermosensation, a subset of temperature sensitive ion channels belonging to the transient receptor potential (TRP) superfamily play crucial roles. Among the members of the TRP superfamily, several channels possess temperature sensitivity and are called thermoTRP channels. Many of the thermoTRP channels are calcium-permeable non-selective cation channels expressed in plasma membranes, thus their activation triggers depolarization upon cation influx followed by action potential generation in sensory neurons, which initiates signal transduction for thermosensation [1], [2], [3], [4]. A peculiar feature of thermoTRP channels is that they are multimodal receptors that are also activated by chemical as well as physical stimuli other than temperature. In addition, expression of thermoTRP channels is not just confined to sensory neurons but is also distributed in various kinds of tissues [1], [2], [3], [4], [5], [6]. Since many of the thermoTRP channels are calcium-permeable channels, their activation leads to the elevation of intracellular calcium concentrations within the cells and trigger the downstream calcium-dependent signaling cascades related to various physiological processes.

Identification of the thermoTRP channels as thermal sensors provided us the opportunity to examine the evolutionary changes of thermosensation by comparing the functional properties of thermoTRP channels among diverse species. However, thermoTRP channels had mainly been analyzed in a few model organisms such as mice and Drosophila, thus evolutionary aspects of thermoTRP channels were not well understood. Over the past several years, thermoTRP channels from diverse non-model organisms have been cloned and characterized and comparative studies illuminated their functional flexibility during the evolutionary process. The functional diversity of thermoTRP channels is also useful for understanding the structural basis of the channel function and various key amino acid residues responsible for activation (or inhibition) of thermoTRP channels have been identified. In this review, we will focus on recent understandings of the evolutionary aspects of thermoTRP channels.

Section snippets

Functional properties of thermoTRP channels in mammals

After the discovery of the first thermoTRP channel (TRPV1) in rats [7], research into other thermosensitive ion channels was conducted resulting in the identification of nine main thermoTRP channels in rodents and humans [1], [2], [3], [4], [5], [6]. In rodents, the TRP superfamily is composed of about 28 members divided into six different subfamilies. Mammalian thermoTRP channels belong to three different subfamilies: TRPV (TRPV1-TRPV4), TRPM (TRPM2, TRPM4, TRPM5, TRPM8), and TRPA (TRPA1).

Diversity of thermoTRP channel repertoires among vertebrate species

Mammalian species such as rodents and humans possess thermoTRP channels belonging to three different subfamilies: TRPV, TRPM, and TRPA. Analysis of the genome sequence of sea squirts, non-vertebrate species closely related to vertebrates, revealed that most orthologous genes for mammalian thermoTRP channels are absent except for TRPA1 (although sea squirts do possess multiple genes that belongs to the TRPV, TRPM, and TRPA subfamilies) [31]. To infer the origin and evolutionary trajectory of

Amino acid changes underlying species differences in TRPV1 sensitivity to capsaicin

Species diversity of thermoTRP channels has been utilized for understanding the molecular basis of activation (or inhibition) mechanisms. Channel properties of TRPV1 have been compared across a wide variety of vertebrate species, and species diversity in TRPV1 sensitivity to capsaicin has been reported [7], [34], [35], [36], [59]. Comparison of TRPV1 between chickens and rats revealed that sensitivity of chicken TRPV1 to capsaicin is considerably lower than that of rat TRPV1 [35]. Analysis of

Future perspectives

Characterization of thermoTRP channels among a wide variety of animal species has facilitated our understanding of the evolution of thermoTRP channels. ThermoTRP channels have changed their gene repertoires and functional properties throughout the course of evolution, which resulted in diversity among animal species. The functional diversity of thermoTRP channels can be utilized for understanding the molecular basis of the species differences in channel properties. Over the past few years, the

Conflict of interest

The authors confirm that there is no conflict of interest.

Funding

There has been no significant financial support for this work that could have influenced its outcome.

Acknowledgments

We thank our collaborators Dr. T. Ohta, Dr. R. Shingai, M. Ohkita, K. Nakatsuka, N. Banzawa, N. Fukuta, and C.T. Saito. We also thank the National Bio-resource Project (NBRP) of the Ministry of Education, Science, Sports and Culture of Japan for providing us with western clawed frogs. This work was supported by the Grant-in-aid from Ministry of Education, Culture, Sports, Science and Technology in Japan (23249012 to MT and 20770191 to SS).

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In this study, we focused on TRPV1 of African lungfish, Protopterus annectens. During drought at high temperature, African lungfish can survive by undergoing into aestivation in mud cocoons. Therefore, lungfish is considered to have some specialized heat-sensor, TRPV1, for heat tolerance. Further, lungfish which shares similarities with fishes and amphibians, is one of important species for investigating the fish-tetrapod transition. Since fish TRPV1 and tetrapod TRPV1 have some differences, character of lungfish TRPV1 attracts attention. Here, we first cloned TRPV1 paralogue from lungfish, Protopterus annectens (lfTRPV1) and determined the chemical and thermal sensitivities of lfTRPV1 by two-electrode voltage clamp method using frog oocytes. We detected activation of lfTRPV1 by acid and 2-APB, but capsaicin-induced activation was not observed. The sensitivity to acid of lfTRPV1 was similar to that of rat TRPV1 (rTRPV1), but the 2-APB sensitivity of lfTRPV1 was relatively weaker than rTRPV1. Heat stimulation up to 44 °C did not activate lfTRPV1 and the heat-activation was not detected even on acid condition of pH6. This dramatically decreased heat-sensitivity of TRPV1 may contribute the heat tolerance of African lungfish. Moreover, this might be the property of ancient tetrapod-type TRPV1 gene.
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Citation Excerpt :
They are multimodal receptors that are activated by temperature as well as other physical and chemical stimuli [3]. ThermoTRPs have been characterized in diverse animal species over the past two decades, which has illuminated their functional diversification in the course of evolution [4,5]. Among thermoTRP channels, TRP vanilloid 1 (TRPV1) is well conserved among vertebrate species and serves as a sensor for noxious stimuli.
Transient receptor potential vanilloid 1 (TRPV1) is mainly expressed in nociceptive primary sensory neurons and acts as a sensor for heat and capsaicin. The functional properties of TRPV1 have been reported to vary among species and, in some cases, the species difference in its thermal sensitivity is likely to be associated with thermal habitat conditions. To clarify the functional properties and physiological roles of TRPV1 in aquatic vertebrates, we examined the temperature and chemical sensitivities of TRPV1 in masu salmon (Oncorhynchus masou ishikawae, Om) belonging to a family of salmonids that generally prefer cool environments. First, behavioral experiments were conducted using a video tracking system. Application of capsaicin, a TRPV1 agonist, induced locomotor activities in juvenile Om. Increasing the ambient temperature also elicited locomotor activity potentiated by capsaicin. RT-PCR revealed TRPV1 expression in gills as well as spinal cord. Next, electrophysiological analyses of OmTRPV1 were performed using a two-electrode voltage-clamp technique with a Xenopus oocyte expression system. Heat stimulation evoked an inward current in heterologously expressed OmTRPV1. In addition, capsaicin produced current responses in OmTRPV1-expressing oocytes, but higher concentrations were needed for its activation compared to the mammalian orthologues. These results indicate that Om senses environmental stimuli (heat and capsaicin) through the activation of TRPV1, and this channel may play important roles in avoiding environments disadvantageous for survival in aquatic vertebrates.
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ReviewFunctional diversity and evolutionary dynamics of thermoTRP channels

Highlights

Abstract

Graphical abstract

Introduction

Section snippets

Functional properties of thermoTRP channels in mammals

Diversity of thermoTRP channel repertoires among vertebrate species

Amino acid changes underlying species differences in TRPV1 sensitivity to capsaicin

Future perspectives

Conflict of interest

Funding

Acknowledgments

Curr. Opin. Neurobiol.

Cell

Cell

Neuron

Neuron

J. Biol. Chem.

J. Biol. Chem.

Cell

J. Biol. Chem.

Cell

Neuron

J. Biol. Chem.

Cell

Cell

J. Biol. Chem.

TRP ion channels and temperature sensation

Annu. Rev. Neurosci.

ThermoTRP channels and beyond: mechanisms of temperature sensation

Nat. Rev. Neurosci.

Thermosensation and pain

J. Neurobiol.

TRPV channels as thermosensory receptors in epithelial cells

Pflugers Arch.

The role of thermosensitive TRP (transient receptor potential) channels in insulin secretion

Endocr. J.

The capsaicin receptor: a heat-activated ion channel in the pain pathway

Nature

TRPV3 in keratinocytes transmits temperature information to sensory neurons via ATP

Pflugers Arch.

Heat activation of TRPM5 underlies thermal sensitivity of sweet taste

Nature

Loss of high-frequency glucose-induced Ca2+ oscillations in pancreatic islets correlates with impaired glucose tolerance in Trpm5−/− mice

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

Identification of a cold receptor reveals a general role for TRP channels in thermosensation

Nature

Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1

Nature

OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity

Nat. Cell Biol.

Lack of TRPM2 impaired insulin secretion and glucose metabolisms in mice

Diabetes

TRPM2 modulates insulin secretion in pancreatic beta-cells

Islets

Redox signal-mediated sensitization of transient receptor potential melastatin 2 (TRPM2) to temperature affects macrophage functions

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

Modulation of water efflux through functional interaction between TRPV4 and TMEM16A/anoctamin 1

FASEB J.

PI(4 5)P2 regulates the activation and desensitization of TRPM8 channels through the TRP domain

Nat. Neurosci.

Review
Functional diversity and evolutionary dynamics of thermoTRP channels

Loss of high-frequency glucose-induced Ca²⁺ oscillations in pancreatic islets correlates with impaired glucose tolerance in Trpm5^−/− mice