Distinct signaling of Drosophila chemoreceptors in olfactory sensory neurons

Distinct signaling of Drosophila chemoreceptors in olfactory sensory neurons
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嗅觉感觉神经元中果蝇化学感受器的独特信号传导

DOI:
10.1073/pnas.1518329113
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发表时间:
2016-02-16
影响因子:
11.1
通讯作者:
Luo, Dong-Gen
Luo, Dong-Gen
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Cao, Li-Hui;Jing, Bi-Yang;Luo, Dong-Gen

文献摘要

被引文献

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果蝇是研究嗅觉的常用模型系统。然而,其嗅觉感觉神经元的生理特性,无论是内在的还是反应性的,仍然不清楚。我们首次成功地用膜片钳记录了果蝇的嗅觉受体(Ors)和嗜离子受体(Irs)的不同信号。我们发现ir驱动的受体电流不适应,而Or反应适应强烈。令人惊讶的是,尽管气味适应在高气味背景下增加了气味敏感性,但在低气味背景下却降低了气味敏感性。适应渗透于所有感官,而在果蝇表达or的OSNs中发现的适应动态增益控制,有助于理解其他感官系统的适应。在果蝇中,嗅觉感觉神经元(OSNs)主要依赖两种化学感受器,气味感受器(Ors)和嗜离子感受器(Irs),将气味刺激转化为神经活动。由于很难从果蝇的原生osn中获得细胞内记录,这些受体在其原生osn中的细胞信号传导尚不清楚。在这里,我们开发了一种天线制备方法,通过膜片钳技术实现了对目标果蝇osn的首次记录(据我们所知)。我们发现,短暂的气味脉冲触发了梯度向内受体电流,具有不同的响应动力学和电流-电压关系,在Or和ir驱动的响应之间。当受到长距离气味刺激时,表达ir的osn的受体电流不适应。相反,表达or的osn表现出强烈的Ca2+依赖性适应。适应诱导的气味敏感性变化服从Weber-Fechner关系;然而,令人惊讶的是,增量灵敏度在低气味背景下降低,而在高气味背景下增加。我们的气味适应模型揭示了两种相反的适应作用,即脱敏和防止饱和,在动态调节气味敏感性和扩大感官操作范围方面。
Significance Drosophila is a popular model system for the study of olfaction. However, the physiological properties of its olfactory sensory neurons, both intrinsic and responsive, remain unclear. We have succeeded, for the first time, in patch-clamp recording from targeted Drosophila OSNs, revealing the distinct signaling of odorant receptors (Ors) and ionotropic receptors (Irs). We found that Ir-driven receptor currents did not adapt, whereas Or responses strongly adapted. Surprisingly, although Or adaptation increased odor sensitivity at high odor backgrounds, it reduced odor sensitivity at low backgrounds. Adaptation permeates all senses, and the finding of dynamic gain control by adaptation in Drosophila Or-expressing OSNs sheds light on the understanding of adaptation in other sensory systems. In Drosophila, olfactory sensory neurons (OSNs) rely primarily on two types of chemoreceptors, odorant receptors (Ors) and ionotropic receptors (Irs), to convert odor stimuli into neural activity. The cellular signaling of these receptors in their native OSNs remains unclear because of the difficulty of obtaining intracellular recordings from Drosophila OSNs. Here, we developed an antennal preparation that enabled the first recordings (to our knowledge) from targeted Drosophila OSNs through a patch-clamp technique. We found that brief odor pulses triggered graded inward receptor currents with distinct response kinetics and current–voltage relationships between Or- and Ir-driven responses. When stimulated with long-step odors, the receptor current of Ir-expressing OSNs did not adapt. In contrast, Or-expressing OSNs showed a strong Ca2+-dependent adaptation. The adaptation-induced changes in odor sensitivity obeyed the Weber–Fechner relation; however, surprisingly, the incremental sensitivity was reduced at low odor backgrounds but increased at high odor backgrounds. Our model for odor adaptation revealed two opposing effects of adaptation, desensitization and prevention of saturation, in dynamically adjusting odor sensitivity and extending the sensory operating range.