Abstract
The blood brain barrier (BBB) forms a stringent barrier that protects the brain from components in the circulation that could interfere with neuronal function. At the same time, the BBB enables selective transport of critical nutrients and other chemicals to the brain. Beyond these functions, another recently recognized function is even less characterized, specifically the role of the BBB in modulating behavior by affecting neuronal function in a sex-dependent manner. Notably, signaling in the adult Drosophila BBB is required for normal male courtship behavior. Courtship regulation also relies on male-specific molecules in the BBB. Our previous studies have demonstrated that adult feminization of these cells in males significantly lowered courtship. Here, we conducted microarray analysis of BBB cells isolated from males and females. Findings revealed that these cells contain male- and female-enriched transcripts, respectively. Among these transcripts, nuclear receptor Hr46/Hr3 was identified as a male-enriched BBB transcript. Hr46/Hr3 is best known for its essential roles in the ecdysone response during development and metamorphosis. In this study, we demonstrate that Hr46/Hr3 is specifically required in the BBB cells for courtship behavior in mature males. The protein is localized in the nuclei of sub-perineurial glial cells (SPG), indicating that it might act as a transcriptional regulator. These data provide a catalogue of sexually dimorphic BBB transcripts and demonstrate a physiological adult role for the nuclear receptor Hr46/Hr3 in the regulation of male courtship, a novel function that is independent of its developmental role.
Highlights
It is well established that the two layers of glial cells that tightly surround the nervous system form the Drosophila blood brain barrier (BBB) [1,2]
The neuronal circuits that control the behavior are inside the brain, separated from these molecules by the blood brain barrier
The BBB forms the tight exclusion barrier that is essential to protecting neurons from hemolymph components that could interfere with neuronal function [1,3]
Summary
It is well established that the two layers of glial cells that tightly surround the nervous system form the Drosophila blood brain barrier (BBB) [1,2]. The inner layer, the subperineurial glia (SPG), is adjacent to the neuronal cell bodies and contains the tight junctions that form the physical barrier (Fig 1A) It has been shown in a number of genetic and functional studies that the barriers in flies and vertebrates share structure and function, and many homologous proteins that ensure their function, as shown in [6]. This would be in agreement with the finding that feminization of the BBB by expression of the feminizing TRA protein in the BBB of adult males results in a significant reduction in male courtship [10] In these experiments, the tightness of the barrier was unaffected, suggesting that specific male transcripts are physiologically participating in courtship control. We identify sex-preferentially expressed transcripts in the BBB of males and females and demonstrate that the nuclear receptor Hr46/Hr3, best known for its roles in larval development [12,13,14], is physiologically required in the BBB of adult mature males to ensure normal male courtship behavior
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