A role for glia in cellular and systemic metabolism: insights from the fly

Backer, Jean-François De; Kadow, Ilona C. Grunwald

doi:10.1016/j.cois.2022.100947

Cited by 13 publications

(9 citation statements)

References 88 publications

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“…The action of ensheathing glia could include the regulation of glutamate in the enclosed circuits 15,66 . Fly glia are also important for supplying energy to neurons and the underlying mechanism could also rely on glutamate 12,67 .…”

Section: Discussionmentioning

confidence: 99%

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Dynamics of sleep, feeding, and metabolic homeostasis inDrosophilaensheathing glia, astrocytes, and neurons

Flores-Valle

Seelig

2022

Preprint

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An animal's need to sleep grows with time spent awake and decays again during sleep. In the brain, a homeostatic process or signal has been proposed to represent sleep need, steadily increasing during wakefulness and gradually decreasing during sleep. However, such dynamics of a sleep homeostat, capturing the changing need to sleep in real time depending on behavior, has so far not been observed in identified cells. Here, using a system that we developed for monitoring calcium activity over multiple days in head-fixed, walking fruit flies, we find that a class of glia in the fly brain, called ensheathing glia, shows dynamics expected of a sleep homeostat. Calcium levels in these cells - monitored in a central brain area important for memory, navigation and sleep - integrate activity during wakefulness, reset during sleep, and saturate under sleep deprivation. Optogenetic activation of ensheathing glia induces sleep consistent with charging of the homeostat. The dynamics of the sleep homeostat, observed in glia of different brain compartments with similar but distinct dynamics, agree with conceptual model expectations. Ensheathing glia therefore act as a system for sleep control distributed across brain areas. The structural arrangement of these glia suggests that sleep homeostasis differentially impacts large ensembles of cells at the same time.

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Section: Discussionmentioning

confidence: 99%

“…Glia are also important for sleep regulation in Drosophila 11,12 . Glia constitute about 10 percent of the cells in the fly brain and about a third of these are ensheathing glia 13 .…”

Section: Introductionmentioning

confidence: 99%

Dynamics of sleep, feeding, and metabolic homeostasis inDrosophilaensheathing glia, astrocytes, and neurons

Flores-Valle

Seelig

2022

Preprint

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“…Similar to the human brain, Drosophila glia may well be divided into several subtypes that each carry out specific functions, such as CNS pruning, controlling synaptic signals, forming the blood–brain barrier, and providing neuroprotection. Recent studies in Drosophila suggest that glia supports the systemic metabolism for brain health (Backer & Kadow, 2022; Logan, 2017). For instance, glial glycolysis, which is mediated by glycolytic enzymes mostly produced by blood–brain barrier (BBB) glia, is crucial for neuronal survival and is involved in mediating sugar import into the Drosophila brain (Volkenhoff et al., 2015).…”

Section: Introductionmentioning

confidence: 99%

Glia‐specific expression of neuropeptide receptor Lgr4 regulates development and adult physiology in Drosophila

Miao,

Wei,

Lee

et al. 2023

J of Neuroscience Research

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Similar to the human brain, Drosophila glia may well be divided into several subtypes that each carries out specific functions. Glial GPCRs play key roles in crosstalk between neurons and glia. Drosophila Lgr4 (dLgr4) is a human relaxin receptor homolog involved in angiogenesis, cardiovascular regulation, collagen remodeling, and wound healing. A recent study suggests that ilp7 might be the ligand for Lgr4 and regulates escape behavior of Drosophila larvae. Here we demonstrate that Drosophila Lgr4 expression in glial cells, not neurons, is necessary for early development, adult behavior, and lifespan. Reducing the Lgr4 level in glial cells disrupts Drosophila development, while knocking down other LGR family members in glia has no impact. Adult‐specific knockdown of Lgr4 in glia but not neurons reduce locomotion, male reproductive success, and animal longevity. The investigation of how glial expression of Lgr4 contributes to this behavioral alteration will increase our understanding of how insulin signaling via glia selectively modulates neuronal activity and behavior.

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“…The sleep phenotype induced by Appl inhibition could be rescued by increasing the expression of the glutamate transporter dEaat1 ( Farca Luna et al, 2017 ) and, interestingly, Eaat1 is required for the consolidation of long-term memories ( Matsuno et al, 2019 ). Glia has an established role in neural metabolism, providing neurons with energy during times of high energy demand, such as long-term memory formation ( de Tredern et al, 2021 ; De Backer and Grunwald Kadow, 2022 ; Silva et al, 2022 ). Although it is likely that the roles of glia in sleep and memory are intertwined, this relationship is currently largely unexplored.…”

Section: Introductionmentioning

confidence: 99%

Sleep benefits different stages of memory in Drosophila

et al. 2023

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Understanding the physiological mechanisms that modulate memory acquisition and consolidation remains among the most ambitious questions in neuroscience. Massive efforts have been dedicated to deciphering how experience affects behavior, and how different physiological and sensory phenomena modulate memory. Our ability to encode, consolidate and retrieve memories depends on internal drives, and sleep stands out among the physiological processes that affect memory: one of the most relatable benefits of sleep is the aiding of memory that occurs in order to both prepare the brain to learn new information, and after a learning task, to consolidate those new memories. Drosophila lends itself to the study of the interactions between memory and sleep. The fruit fly provides incomparable genetic resources, a mapped connectome, and an existing framework of knowledge on the molecular, cellular, and circuit mechanisms of memory and sleep, making the fruit fly a remarkable model to decipher the sophisticated regulation of learning and memory by the quantity and quality of sleep. Research in Drosophila has stablished not only that sleep facilitates learning in wild-type and memory-impaired animals, but that sleep deprivation interferes with the acquisition of new memories. In addition, it is well-accepted that sleep is paramount in memory consolidation processes. Finally, studies in Drosophila have shown that that learning itself can promote sleep drive. Nevertheless, the molecular and network mechanisms underlying this intertwined relationship are still evasive. Recent remarkable work has shed light on the neural substrates that mediate sleep-dependent memory consolidation. In a similar way, the mechanistic insights of the neural switch control between sleep-dependent and sleep-independent consolidation strategies were recently described. This review will discuss the regulation of memory by sleep in Drosophila, focusing on the most recent advances in the field and pointing out questions awaiting to be investigated.

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A role for glia in cellular and systemic metabolism: insights from the fly

Cited by 13 publications

References 88 publications

Dynamics of sleep, feeding, and metabolic homeostasis inDrosophilaensheathing glia, astrocytes, and neurons

Dynamics of sleep, feeding, and metabolic homeostasis inDrosophilaensheathing glia, astrocytes, and neurons

Glia‐specific expression of neuropeptide receptor Lgr4 regulates development and adult physiology in Drosophila

Sleep benefits different stages of memory in Drosophila

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