Sex-Specific Signaling in the Blood–Brain Barrier Is Required for Male Courtship in Drosophila

Hoxha, Valbona; Lama, Chamala; Chang, Peter L.; Saurabh, Sumit; Patel, Naiya; Olate, Nicole; Dauwalder, Brigitte

doi:10.1371/journal.pgen.1003217

Cited by 19 publications

(26 citation statements)

References 54 publications

(71 reference statements)

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“…Given that sex differences exist in many tissues throughout the fly [45][46][47][48][49][50][51][52][53][54][55], we wanted to determine the anatomical focus of bmm's effects on the male-female differences in triglyceride homeostasis. bmm is highly expressed in the fat body, and previous studies have demonstrated a central role for this tissue in the regulation of triglyceride storage and breakdown in males [29,32].…”

Section: Bmm Function In the Somatic Cells Of The Gonad Plays A Role mentioning

confidence: 99%

A role for triglyceride lipase brummer in the regulation of sex differences in Drosophila fat storage and breakdown

et al. 2020

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Triglycerides are the major form of stored fat in all animals. One important determinant of whole-body fat storage is whether an animal is male or female. Here, we use Drosophila, an established model for studies on triglyceride metabolism, to gain insight into the genes and physiological mechanisms that contribute to sex differences in fat storage. Our analysis of triglyceride storage and breakdown in both sexes identified a role for triglyceride lipase brummer (bmm) in the regulation of sex differences in triglyceride homeostasis. Normally, male flies have higher levels of bmm mRNA both under normal culture conditions and in response to starvation, a lipolytic stimulus. We find that loss of bmm largely eliminates the sex difference in triglyceride storage and abolishes the sex difference in triglyceride breakdown via strongly male-biased effects. Although we show that bmm function in the fat body affects whole-body triglyceride levels in both sexes, in males, we identify an additional role for bmm function in the somatic cells of the gonad and in neurons in the regulation of whole-body triglyceride homeostasis. Furthermore, we demonstrate that lipid droplets are normally present in both the somatic cells of the male gonad and in neurons, revealing a previously unrecognized role for bmm function, and possibly lipid droplets, in these cell types in the regulation of whole-body triglyceride homeostasis. Taken together, our data reveal a role for bmm function in the somatic cells of the gonad and in neurons in the regulation of male-female differences in fat storage and breakdown and identify bmm as a link between the regulation of triglyceride homeostasis and biological sex.

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Section: Bmm Function In the Somatic Cells Of The Gonad Plays A Role mentioning

confidence: 99%

A role for triglyceride lipase brummer in the regulation of sex differences in Drosophila fat storage and breakdown

et al. 2020

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“…This has been shown for the Drosophila liver and adipose tissue equivalent (the fat body), showing that male courtship behavior can be altered by changing the sex identity of the fat body cells (Lazareva et al, 2007 ). This technique was recently applied to the BBB, showing a behavioral impact of sex-specificity in the BBB (Hoxha et al, 2013 ). BBB-specific, ectopic expression of a gene that feminizes cells ( TraF ) led to reduced courtship behavior in males.…”

Section: Future Questions and Emerging Areas Of Bbb Researchmentioning

confidence: 99%

“…BBB-specific, ectopic expression of a gene that feminizes cells ( TraF ) led to reduced courtship behavior in males. Hoxha et al ( 2013 ) showed that this was not solely a developmental effect, as BBB-specific expression of TraF only during the adult stages of the fly still reduced courtship in males. The authors also showed that this reduction in courtship behavior required the GPCR Moody, which Bainton et al ( 2005 ) previously showed to have separable roles in maintaining BBB integrity (a structural role) and behavioral drug responses (a signaling role).…”

Section: Future Questions and Emerging Areas Of Bbb Researchmentioning

confidence: 99%

Barrier mechanisms in the Drosophila blood-brain barrier

2014

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The invertebrate blood-brain barrier (BBB) field is growing at a rapid pace and, in recent years, studies have shown a physiologic and molecular complexity that has begun to rival its vertebrate counterpart. Novel mechanisms of paracellular barrier maintenance through G-protein coupled receptor signaling were the first demonstrations of the complex adaptive mechanisms of barrier physiology. Building upon this work, the integrity of the invertebrate BBB has recently been shown to require coordinated function of all layers of the compound barrier structure, analogous to signaling between the layers of the vertebrate neurovascular unit. These findings strengthen the notion that many BBB mechanisms are conserved between vertebrates and invertebrates, and suggest that novel findings in invertebrate model organisms will have a significant impact on the understanding of vertebrate BBB functions. In this vein, important roles in coordinating localized and systemic signaling to dictate organism development and growth are beginning to show how the BBB can govern whole animal physiologies. This includes novel functions of BBB gap junctions in orchestrating synchronized neuroblast proliferation, and of BBB secreted antagonists of insulin receptor signaling. These advancements and others are pushing the field forward in exciting new directions. In this review, we provide a synopsis of invertebrate BBB anatomy and physiology, with a focus on insights from the past 5 years, and highlight important areas for future study.

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“…Factors that mediate these sex-dependent differences in hypothalamic neurogenesis have not yet been identified but could involve numerous levels of regulation, such as hormone-dependent plasticity (de Seranno et al 2010), differences in blood-barrier access between the sexes (Hoxha et al 2013), and hormonespecific induction of feeding behavior (Sieck et al 1978). Lastly, it is possible that it is the survival of newborn neurons, rather than (or in addition to) their proliferation, that is sexually dimorphic, as has been previously demonstrated for prenatally generated hypothalamic neurons (Waters and Simerly 2009;Forger et al 2004;Tobet and Hanna 1997;Park et al 1998).…”

Section: Discussionmentioning

confidence: 99%

Regulation of Body Weight and Metabolism by Tanycyte-Derived Neurogenesis in Young Adult Mice

Blackshaw

Lee

Pak

et al. 2016

Research and Perspectives in Endocrine Interactions

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The hypothalamus controls many homeostatic and instinctive physiological processes, including the sleep-wake cycle, food intake, and sexually dimorphic behaviors. These behaviors are regulated by environmental and physiological cues, although the molecular and cellular mechanisms that underlie these effects are still poorly understood. Recently, it has become clear that both the juvenile and adult hypothalamus exhibit neurogenesis, which modifies homeostatic neural circuitry. In this manuscript, we report data addressing the role of sex-specific and dietary factors in controlling neurogenesis in the mediobasal hypothalamus. We report that a high fat diet (HFD) activates neurogenesis in the median eminence (ME) of young adult female, but not male mice, and that focal irradiation of the ME in HFD-fed mice reduces weight gain in females, but not males. These results suggest that some physiological effects of HFD are mediated by sexually dimorphic neurogenesis in the ME. We present these findings in the context of other studies on

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Sex-Specific Signaling in the Blood–Brain Barrier Is Required for Male Courtship in Drosophila

Cited by 19 publications

References 54 publications

A role for triglyceride lipase brummer in the regulation of sex differences in Drosophila fat storage and breakdown

A role for triglyceride lipase brummer in the regulation of sex differences in Drosophila fat storage and breakdown

Barrier mechanisms in the Drosophila blood-brain barrier

Regulation of Body Weight and Metabolism by Tanycyte-Derived Neurogenesis in Young Adult Mice

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