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Unexpected expression of heat-activated transient receptor potential (TRP) channels in winter torpid bats and cold-activated TRP channels in summer active bats

Yang-Yang Li Qing-Yun Lv Guan-Tao Zheng Di Liu Ji Ma Gui-Mei He Li-Biao Zhang Shan Zheng Hai-Peng Li Yi-Hsuan Pan

Yang-Yang Li, Qing-Yun Lv, Guan-Tao Zheng, Di Liu, Ji Ma, Gui-Mei He, Li-Biao Zhang, Shan Zheng, Hai-Peng Li, Yi-Hsuan Pan. Unexpected expression of heat-activated transient receptor potential (TRP) channels in winter torpid bats and cold-activated TRP channels in summer active bats. Zoological Research, 2022, 43(1): 52-63. doi: 10.24272/j.issn.2095-8137.2021.209
Citation: Yang-Yang Li, Qing-Yun Lv, Guan-Tao Zheng, Di Liu, Ji Ma, Gui-Mei He, Li-Biao Zhang, Shan Zheng, Hai-Peng Li, Yi-Hsuan Pan. Unexpected expression of heat-activated transient receptor potential (TRP) channels in winter torpid bats and cold-activated TRP channels in summer active bats. Zoological Research, 2022, 43(1): 52-63. doi: 10.24272/j.issn.2095-8137.2021.209

蝙蝠在冬季蛰伏期高表达热激活瞬时受体电位通道(TRPs)却在夏季活跃期高表达冷激活TRPs

doi: 10.24272/j.issn.2095-8137.2021.209

Unexpected expression of heat-activated transient receptor potential (TRP) channels in winter torpid bats and cold-activated TRP channels in summer active bats

Funds: This study was supported by the National Natural Science Foundation of China (31100273 to Y.H.P. and 91731304 to H.P.L.)
More Information
  • 摘要: 感知温度变化的能力对哺乳动物的生存至关重要。哺乳动物主要是通过温度敏感型瞬时受体电位通道(Thermosensitive transient receptor potential channels, Thermo-TRPs)感应温度变化。一些哺乳类动物为了度过寒冷的冬季并存活下来会进入冬眠状态,在此期间它们的体温有剧烈波动;然而,这些哺乳动物具有哪些潜在的温度感受(thermal response)调节机制还不清楚。我们运用实时荧光聚合酶链式反应和蛋白质免疫印记等方法,发现大足鼠耳蝠(Myotis ricketti) 在冬季蛰伏期会高表达热激活通道TRPs(例如TRPV1和TRPV4),而在夏季活跃期则高表达冷激活TRPs(例如,TRPM8和TRPC5)。我们也发现小鼠在温度相对较高的条件(40 oC)下,会高表达冷激活TRPs(例如 Trpm8Trpc5 )。这些结果提示,小型哺乳动物在温暖或较热的状况下,会上调表达冷激活TRPs。通过结合位点分析,我们发现一些同源异型盒(HOX)转录因子(Transcription factor, TF)可以调节热激活和冷激活TRPs基因的表达,而POU(Pit-Oct-Unc)家族的一些转录因子则调节温热敏感和冷激活TRPs基因的表达。双荧光素酶报告基因检测结果表明,转录因子HOXA9,POU3F1和POU5F1调节 TRPC5 的表达,可见Thermo-TRPs基因是受到HOX和POU家族中多个转录因子在不同水平上的调控。这项研究揭示蝙蝠为了在冬眠中存活下来,而采取的温度感觉适应机制。
    #Authors contributed equally to this work
  • Figure  1.  Expression of various Thermo-TRPs in bats under different physiological states

    A–C: Relative mRNA levels of Thermo-TRPs are shown: heat-activated TRPV-1, -2, -3, and -4 (A), TRPM-2, -4, and -5 (B), and cold-activated TRPM8, TRPC5, and TRPA1 (C) of bats in torpid (T), 2 h after arousal (2 h), 24 h after arousal (24 h), and active (AC) states. D: Schematic: Torpid bats with higher abundance of heat- activated TRPs and active bats with higher abundance of warm-sensitive and cold-activated TRPs. E: Relative level of UCP1 mRNA. F, G: Western blotting of Thermo-TRPs (F), and relative amount of each target protein (G) in bats under different states. kDa represents molecular weight of proteins. H: Relative mRNA and protein levels of six Thermo-TRPs in bats under different states. Difference is significant (P<0.05) for values denoted with different letters.

    Figure  2.  Transcription factors (TFs) that regulate Thermo-TRP gene expression

    A–C: Schematic of TF binding of HOX, POU, FOX, SP, E2F, JUND, and ETS families to Thermo-TRP genes. h- and c-TRPs represent heat- and cold-activated TRPs, respectively (A). Other panels show relative mRNA levels of some TFs of HOX (B) and POU (C) families of bats in torpid (T), 2 h after arousal (2 h), 24 h after arousal (24 h), and active (AC) states. D, E: Western blotting results of several TFs are shown in (D), and their relative abundance in bats under various states is shown in (E). F, G: Relative mRNA and protein levels of six TFs are shown in (F) and six TFs and 10 TRPs are shown in (G). Difference is significant (P<0.05) for values denoted with different letters.

    Figure  3.  Relative mRNA levels of Thermo-TRPs and TFs in temperature-stimulated mice

    A, B: Relative mRNA abundance of 10 Thermo-TRPs (A) and several TFs in HOX and POU families (B) of mice (n=6 per temperature group). C: Body weights of mice treated at 4 °C, 25 °C, 37 °C, and 40 °C for 6 days. Statistical significance (*: P=0.0041) of differences in body weight between 37 °C- and 40 °C-treated mice and between 4 °C- and 25 °C-treated mice was determined by two-way ANOVA. Difference is significant (P<0.05) for values denoted with different letters.

    Figure  4.  Regulation of TRPC5 expression by HOXA9, POU3F1, and POU5F1

    A: Schematic of plasmids pcDNA3.1(+) and psiCHECK-2TM. B: Relative luciferase activity of cells containing HOXA9 expression vector and reporter plasmid with Trpc5 promoter region. C, D: Relative luciferase activity of cells containing POU5F1 expression vector and reporter plasmid with Trpc5 3'-untranslated region (3'-UTR) (C) and that of cells containing POU3F1 expression vector and reporter plasmid with Trpc5 3'-UTR (D). Blank: Cells containing no plasmids. Positive control (pcheck2): Cells transfected with psiCHECK-2. pcDNA3.1NC: Cells transfected with empty vector pcDNA3.1(+). Difference is significant (P<0.05) for values denoted with different letters.

    Table  1.   List of 10 thermo-TRPs and their temperature thresholds for activation#

    H*ChannelThreshold temp for activation (°C)Expression locationPhysiological function
    Hot-sensitiveTRPV subfamily
    TRPV1>40Brain, Skin, BladderThermosensation, synaptic plasticity, pain sensation, inflammation, ischemia/reperfusion injury, body temperature regulation, metabolism (Baez et al., 2014; Castillo et al., 2018; Caterina et al., 1999; Dhaka et al., 2006; Güler et al., 2002; Huang et al., 2006; Jardín et al., 2017; Kashio, 2021; Nilius & Owsianik, 2011; Peier et al., 2002; Smith et al., 2002; Talavera et al., 2020; Vay et al., 2012)
    TRPV2>50CNS neurons, Heart, Various tissuesThermosensation (noxious heat), phagocytosis, pain sensation, osmosensation (Castillo et al., 2018; Dhaka et al., 2006; Huang et al., 2006; Kashio, 2021; Nilius & Owsianik, 2011; Palkar et al., 2015; Peier et al., 2002; Smith et al., 2002; Vay et al., 2012)
    TRPV3>30Brain, Tongue, Gut, Skin keratinocytesThermosensation, nociception, wound healing, pain sensation, skin functions (Baez et al., 2014; Castillo et al., 2018; Dhaka et al., 2006; Huang et al., 2006; Kashio, 2021; Nilius & Owsianik, 2011; Peier et al., 2002; Smith et al., 2002)
    TRPV425–42CNS neurons, Heart, Kidney, Inner ear, liver, Trachea, Fat, Salivary gland, Skin keratinocytesThermosensation, osmosensation, pain sensation, neural excitability, skin functions (Baez et al., 2014; Castillo et al., 2018; Dhaka et al., 2006; Güler et al., 2002; Huang et al., 2006; Kashio, 2021; Nilius & Owsianik, 2011; Vay et al., 2012)
    TRPM subfamily
    TRPM234–42Brain, Bone marrow, Eye, Heart, Lymph nodesThermosensation, apoptosis, pain sensation, body temperature regulation, insulin secretion (Castillo et al., 2018; Kashio, 2021; Nilius & Owsianik, 2011; Zhong et al., 2016)
    TRPM415–35Heart, Lung, CNS neurons, GutThermosensation, releasing hormone, insulin secretion, chemosensory (Baez et al., 2014; Castillo et al., 2018; Kashio, 2021; Nilius & Owsianik, 2011)
    TRPM515–35Tongue, Lung, Brain, Taste cells, GutTaste (sweet, bitter, umami), thermosensation, chemosensory, insulin secretion (Castillo et al., 2018; Kashio, 2021; Nilius & Owsianik, 2011; Talavera et al., 2005)
    Cold-sensitiveTRPM8≤25Sensory dorsal root, Trigeminal ganglia neurons, Liver, Prostate, TestisThermosensation (cold), acrosome reaction, tumor growth, body temperature regulation (Baez et al., 2014; Castillo et al., 2018; Caterina et al., 1999; Dhaka et al., 2006, 2007; Güler et al., 2002; Huang et al., 2006; Kashio, 2021; Nilius & Owsianik, 2011; Peier et al., 2002; Vay et al., 2012)
    TRPC subfamily
    TRPC525–37BrainBrain development, thermosensation (Baez et al., 2014; Castillo et al., 2018; Kashio, 2021; Nilius & Owsianik, 2011; Zimmermann et al., 2011)
    TRPA subfamily
    TRPA1$≤17Sensory dorsal root, Trigeminal ganglia neurons, Various tissuesThermosensation (noxious cold), nociception, olfactory responses, pain sensation (Baez et al., 2014; Castillo et al., 2018; Dhaka et al., 2006; Huang et al., 2006; Jardín et al., 2017; Kashio, 2021; Nilius & Owsianik, 2011; Vay et al., 2012)
    #: Features of thermo-TRPs previously characterized in other mammalian species rather than bats. H*: Classification of several TRPs in human body (Ezquerra-Romano & Ezquerra, 2017): hot- and cold-sensitive TRPs are denoted in orange and green, respectively. $: TRPA1 is a heat-activated sensor in non-mammalian species (Saito & Tominaga, 2015).
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出版历程
  • 收稿日期:  2021-10-21
  • 录用日期:  2021-11-17
  • 网络出版日期:  2021-11-17
  • 刊出日期:  2022-01-18

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