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

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

doi:10.1016/j.cell.2023.08.002

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

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

Research output: Contribution to journal › Article › peer-review

5 Scopus citations

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)
Pages (from-to)	4289-4309.e23
Journal	Cell
Volume	186
Issue number	20
DOIs	https://doi.org/10.1016/j.cell.2023.08.002
State	Published - Sep 28 2023
Externally published	Yes

Keywords

blood-brain barrier
gene regulation
hormones
plasticity
scRNA-seq
social behavior
social insects

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.cell.2023.08.002

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title = "Hormonal gatekeeping via the blood-brain barrier governs caste-specific behavior in ants",

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.",

keywords = "blood-brain barrier, gene regulation, hormones, plasticity, scRNA-seq, social behavior, social insects",

author = "Linyang Ju and Glastad, {Karl M.} and Lihong Sheng and Janko Gospocic and Kingwell, {Callum J.} and Davidson, {Shawn M.} and Kocher, {Sarah D.} and Roberto Bonasio and Berger, {Shelley L.}",

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doi = "10.1016/j.cell.2023.08.002",

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AU - Ju, Linyang

AU - Glastad, Karl M.

AU - Sheng, Lihong

AU - Gospocic, Janko

AU - Kingwell, Callum J.

AU - Davidson, Shawn M.

AU - Kocher, Sarah D.

AU - Bonasio, Roberto

AU - Berger, Shelley L.

PY - 2023/9/28

Y1 - 2023/9/28

N2 - 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.

AB - 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.

KW - blood-brain barrier

KW - gene regulation

KW - hormones

KW - plasticity

KW - scRNA-seq

KW - social behavior

KW - social insects

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ER -

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

Abstract

Keywords

ASJC Scopus subject areas

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