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

Evolution of vertebrate transient receptor potential vanilloid 3 channels: opposite temperature sensitivity between mammals and western clawed frogs.
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DOI:
10.1371/journal.pgen.1002041
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发表时间:
2011-04
期刊:
影响因子:
4.5
通讯作者:
Tominaga M
Tominaga M
中科院分区:
生物学2区
文献类型:
--
作者:
Saito S;Fukuta N;Shingai R;Tominaga M

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瞬时受体电位(Trp)通道在多种动物中作为温度受体,在热适应中起着至关重要的作用。色氨酸香草酸(Trp vanilloid,TRPV)亚家族含有多种温度感受器,具有不同的温度敏感性。已知的是,TRPV3通道在皮肤中高度表达,它在温暖的温度下被激活,并作为传感器检测哺乳动物等恒温动物体温附近的环境温度。在这里,我们对TRPV亚家族进行了全面的比较分析,以了解其进化过程;我们发现了新的TRPV基因,并表征了TRPV3在脊椎动物进化过程中的进化灵活性。为了了解热带爪蛙TRPV3通道的功能进化,我们克隆了热带爪蛙的TRPV3通道。与其他陆生脊椎动物的TRPV3通道相比,TRPV3通道N-末端和C-末端的氨基酸序列高度多样化,尽管中央部分保守得很好。在异源表达系统中,几种哺乳动物的TRPV3激动剂不能激活西爪蛙的TRPV3通道。此外,蛙类的TRPV3通道对热刺激没有反应,而是被低温激活。激活的温度阈值约为16℃,略低于西爪蛙的下限温度。鉴于TRPV3通道是在皮肤中表达的,它可能的作用是检测有害的寒冷温度。因此,西方爪蛙和哺乳动物获得了与TRPV3通道相反的温度敏感性,以检测适合它们各自物种的环境温度,这表明温度受体在进化过程中可以动态改变特性,以适应不同的热环境。温度感知的进化对于适应热环境至关重要;然而,人们对这一过程知之甚少。在这里,我们研究了脊椎动物TRPV亚家族的进化,该家族包含几个哺乳动物的温度受体。我们鉴定了几个以前没有发现的新的TRPV基因,并发现了TRPV3基因在脊椎动物进化过程中的进化灵活性。TRPV3通道感知温暖的温度,并作为传感器来检测哺乳动物等恒温动物体温附近的环境温度。为了研究TRPV3通道在脊椎动物进化中的功能进化,我们克隆了西爪蛙的TRPV3通道基因,发现其N-末端和C-末端区域与其他陆生脊椎动物的TRPV3通道基因高度多样化。对西爪蛙TRPV3通道特性的研究表明,它不是被热刺激激活的,而是被冷刺激激活的。激活的温度阈值约为16℃,略低于西爪蛙的下限温度。因此,西方爪蛙和哺乳动物获得了与TRPV3通道相反的温度敏感性,以检测适合各自物种的环境温度,表明温度受体可以在进化过程中动态改变特性以适应热环境。
Transient Receptor Potential (TRP) channels serve as temperature receptors in a wide variety of animals and must have played crucial roles in thermal adaptation. The TRP vanilloid (TRPV) subfamily contains several temperature receptors with different temperature sensitivities. The TRPV3 channel is known to be highly expressed in skin, where it is activated by warm temperatures and serves as a sensor to detect ambient temperatures near the body temperature of homeothermic animals such as mammals. Here we performed comprehensive comparative analyses of the TRPV subfamily in order to understand the evolutionary process; we identified novel TRPV genes and also characterized the evolutionary flexibility of TRPV3 during vertebrate evolution. We cloned the TRPV3 channel from the western clawed frog Xenopus tropicalis to understand the functional evolution of the TRPV3 channel. The amino acid sequences of the N- and C-terminal regions of the TRPV3 channel were highly diversified from those of other terrestrial vertebrate TRPV3 channels, although central portions were well conserved. In a heterologous expression system, several mammalian TRPV3 agonists did not activate the TRPV3 channel of the western clawed frog. Moreover, the frog TRPV3 channel did not respond to heat stimuli, instead it was activated by cold temperatures. Temperature thresholds for activation were about 16 °C, slightly below the lower temperature limit for the western clawed frog. Given that the TRPV3 channel is expressed in skin, its likely role is to detect noxious cold temperatures. Thus, the western clawed frog and mammals acquired opposite temperature sensitivity of the TRPV3 channel in order to detect environmental temperatures suitable for their respective species, indicating that temperature receptors can dynamically change properties to adapt to different thermal environments during evolution. Evolution of temperature perception is crucial for adaptation to thermal environments; however, this process is poorly understood. Here we investigated the evolution of the vertebrate TRPV subfamily which contains several mammalian temperature receptors. We identified several novel TRPV genes that have not been found previously and discovered evolutionary flexibility of the TRPV3 gene during vertebrate evolution. TRPV3 channels perceive warm temperature and serve as sensors to detect ambient temperatures near the body temperature of homeothermic animals such as mammals. To examine the functional evolution of TRPV3 channels in vertebrate evolution, we cloned the gene from the western clawed frog and found that its N- and C-terminal regions were highly diversified from those of other terrestrial vertebrate TRPV3 channels. Characterization of the channel properties of western clawed frog TRPV3 revealed that it was not activated by heat stimuli, but instead was activated by cold stimuli. Temperature thresholds for activation were about 16 °C, slightly below the lower temperature limit for the western clawed frog. Thus, the western clawed frog and mammals acquired opposite temperature sensitivity of TRPV3 channels to detect environmental temperatures suitable for their respective species, indicating that temperature receptors can dynamically change properties to adapt to thermal environments during evolution.
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影响因子: --
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