Hormonal gatekeeping via the blood-brain barrier governs caste-specific behavior in ants.

IF 45.5 1区生物学 Q1 BIOCHEMISTRY & MOLECULAR BIOLOGY Cell Pub Date : 2023-09-28 Epub Date: 2023-09-07 DOI:10.1016/j.cell.2023.08.002

Linyang Ju, Karl M Glastad, Lihong Sheng, Janko Gospocic, Callum J Kingwell, Shawn M Davidson, Sarah D Kocher, Roberto Bonasio, Shelley L Berger

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Abstract

Here, we reveal an unanticipated role of the blood-brain barrier (BBB) in regulating complex social behavior in ants. Using scRNA-seq, we find localization in the BBB of a key hormone-degrading enzyme called juvenile hormone esterase (Jhe), and we show that this localization governs the level of juvenile hormone (JH3) entering the brain. Manipulation of the Jhe level reprograms the brain transcriptome between ant castes. Although ant Jhe is retained and functions intracellularly within the BBB, we show that Drosophila Jhe is naturally extracellular. Heterologous expression of ant Jhe into the Drosophila BBB alters behavior in fly to mimic what is seen in ants. Most strikingly, manipulation of Jhe levels in ants reprograms complex behavior between worker castes. Our study thus uncovers a remarkable, potentially conserved role of the BBB serving as a molecular gatekeeper for a neurohormonal pathway that regulates social behavior.

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通过血脑屏障的激素门控控制蚂蚁的种姓特定行为。

在这里，我们揭示了血脑屏障（BBB）在调节蚂蚁复杂社会行为中的一个意想不到的作用。使用scRNA-seq，我们发现一种名为幼激素酯酶（Jhe）的关键激素降解酶在血脑屏障中的定位，我们表明这种定位控制着进入大脑的幼激素（JH3）的水平。Jhe水平的操作重新编程蚂蚁种姓之间的大脑转录组。尽管蚂蚁Jhe在血脑屏障内保留并在细胞内发挥作用，但我们发现果蝇Jhe是天然的细胞外生物。蚂蚁Jhe在果蝇血脑屏障中的异源表达改变了苍蝇的行为，以模仿蚂蚁的行为。最引人注目的是，蚂蚁对Jhe水平的操纵重新编程了工人种姓之间的复杂行为。因此，我们的研究揭示了血脑屏障作为调节社会行为的神经激素途径的分子守门人的显著、潜在的保守作用。

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来源期刊

Cell 生物-生化与分子生物学

CiteScore

110.00

自引率

0.80%

发文量

396

审稿时长

2 months

期刊介绍： Cells is an international, peer-reviewed, open access journal that focuses on cell biology, molecular biology, and biophysics. It is affiliated with several societies, including the Spanish Society for Biochemistry and Molecular Biology (SEBBM), Nordic Autophagy Society (NAS), Spanish Society of Hematology and Hemotherapy (SEHH), and Society for Regenerative Medicine (Russian Federation) (RPO). The journal publishes research findings of significant importance in various areas of experimental biology, such as cell biology, molecular biology, neuroscience, immunology, virology, microbiology, cancer, human genetics, systems biology, signaling, and disease mechanisms and therapeutics. The primary criterion for considering papers is whether the results contribute to significant conceptual advances or raise thought-provoking questions and hypotheses related to interesting and important biological inquiries. In addition to primary research articles presented in four formats, Cells also features review and opinion articles in its "leading edge" section, discussing recent research advancements and topics of interest to its wide readership.