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.
Original language | English (US) |
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Pages (from-to) | 4289-4309.e23 |
Journal | Cell |
Volume | 186 |
Issue number | 20 |
DOIs | |
State | Published - Sep 28 2023 |
Funding
We thank members of the Berger Lab for help in editing the manuscript, Amita Sehgal and Yongjun Li for providing fly lines and instructions, Geoffrey Dann and Benjamin Garcia for providing help on antigen purification, Duo Zhang for designing and printing fly foraging arena, Balint Kacsoh for guidance in initial optimization of DLC video analysis model fitting, Desi Alexander and Maxxum Fioriti for assisting blinding, and Cristina Brady and Tierney Gannon for ant husbandry. This work was supported by NIH training fellowship F32GM120933 (K.M.G.), NIA R01s R01AG055570 (S.L.B.), R01AG071818 (R.B.), NIMH R01 R01MH131861 (R.B.), NIMH R21 R21MH123841 (R.B.), and NSF 1DP2GM137424-01 (S.D.K.).
Keywords
- blood-brain barrier
- gene regulation
- hormones
- plasticity
- scRNA-seq
- social behavior
- social insects
ASJC Scopus subject areas
- General Biochemistry, Genetics and Molecular Biology