Hexosamine biosynthetic pathway integrates circadian and metabolic signals to regulate daily rhythms in protein O-linked N-acetylglucosaminylation

Liu, Xiaoyu; Blaženović, Ivana; Aj, Contreras; Pham, T. M.; Ca, Tabuloc; Yh, Li; Ji, Junfu; Fiehn, Oliver; Chiu, Joanna C.

doi:10.1101/2020.08.18.256636

Cited by 3 publications

(5 citation statements)

References 108 publications

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“…Similar to activity, feeding occurs at slightly different times of the day in male and female flies. While males feed maximally in the early morning, females do so from the middle of the day until the evening (Seay and Thummel, 2011;Xu et al, 2011;Liu et al, 2020;Schäbler et al, 2020). In summary, general activity, mating and feeding occur at different times of the day and additionally show sex differences in timing.…”

Section: Output Rhythms In Flies and Beesmentioning

confidence: 96%

Model and Non-model Insects in Chronobiology

Beer

Helfrich‐Förster

2020

Front. Behav. Neurosci.

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The fruit fly Drosophila melanogaster is an established model organism in chronobiology, because genetic manipulation and breeding in the laboratory are easy. The circadian clock neuroanatomy in D. melanogaster is one of the best-known clock networks in insects and basic circadian behavior has been characterized in detail in this insect. Another model in chronobiology is the honey bee Apis mellifera, of which diurnal foraging behavior has been described already in the early twentieth century. A. mellifera hallmarks the research on the interplay between the clock and sociality and complex behaviors like sun compass navigation and time-place-learning. Nevertheless, there are aspects of clock structure and function, like for example the role of the clock in photoperiodism and diapause, which can be only insufficiently investigated in these two models. Unlike high-latitude flies such as Chymomyza costata or D. ezoana, cosmopolitan D. melanogaster flies do not display a photoperiodic diapause. Similarly, A. mellifera bees do not go into “real” diapause, but most solitary bee species exhibit an obligatory diapause. Furthermore, sociality evolved in different Hymenoptera independently, wherefore it might be misleading to study the social clock only in one social insect. Consequently, additional research on non-model insects is required to understand the circadian clock in Diptera and Hymenoptera. In this review, we introduce the two chronobiology model insects D. melanogaster and A. mellifera, compare them with other insects and show their advantages and limitations as general models for insect circadian clocks.

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Section: Output Rhythms In Flies and Beesmentioning

confidence: 96%

Model and Non-model Insects in Chronobiology

Beer

Helfrich‐Förster

2020

Front. Behav. Neurosci.

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“…Nevertheless, ectopic overexpression of either protein is sufficient to rescue loss of the other (47), suggesting that the nutrient access and/or responsivity of gfat1 and gfat2 expressing cells may be meaningfully distinct. Indeed, a recent study in WT flies confirms that of the two genes, only gfat2 expression is correlated with circadian eating patterns (64). By contrast, gfat1 may be more sensitive to lipid-induced stress, which is consistent with its proposed role in mediating the depressive effects of hyperlipidemia on neural O-GlcNAcylation.…”

Section: Udp-glcnac Synthesismentioning

confidence: 55%

“…However, it also potentiating OGT activity through tyrosine phosphorylation (323) and directs its translocation to cell membranes, particularly lipid rafts (92) that play a significant role in protein complex assembly and signal transduction [for review (324)]. In a detailed characterization of feeding-related O-GlcNAc regulatory patterns in the fly body, Liu et al demonstrate how both eating and circadian rhythmicity drive transient elevations in pre-prandial Ogt and fasting Oga (64). These cycles guide global O-GlcNAcylation levels to rise and fall in tandem with eating (64), evidencing the important role of this modification in the ingestion and postprandial response to food.…”

Section: Postprandial Vs Fasting Statementioning

confidence: 99%

“…In a detailed characterization of feeding-related O-GlcNAc regulatory patterns in the fly body, Liu et al demonstrate how both eating and circadian rhythmicity drive transient elevations in pre-prandial Ogt and fasting Oga (64). These cycles guide global O-GlcNAcylation levels to rise and fall in tandem with eating (64), evidencing the important role of this modification in the ingestion and postprandial response to food.…”

Section: Postprandial Vs Fasting Statementioning

confidence: 99%

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A nexus of lipid and O-Glcnac metabolism in physiology and disease

Lockridge

Hanover

2022

Front. Endocrinol.

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Although traditionally considered a glucose metabolism-associated modification, the O-linked β-N-Acetylglucosamine (O-GlcNAc) regulatory system interacts extensively with lipids and is required to maintain lipid homeostasis. The enzymes of O-GlcNAc cycling have molecular properties consistent with those expected of broad-spectrum environmental sensors. By direct protein-protein interactions and catalytic modification, O-GlcNAc cycling enzymes may provide both acute and long-term adaptation to stress and other environmental stimuli such as nutrient availability. Depending on the cell type, hyperlipidemia potentiates or depresses O-GlcNAc levels, sometimes biphasically, through a diversity of unique mechanisms that target UDP-GlcNAc synthesis and the availability, activity and substrate selectivity of the glycosylation enzymes, O-GlcNAc Transferase (OGT) and O-GlcNAcase (OGA). At the same time, OGT activity in multiple tissues has been implicated in the homeostatic regulation of systemic lipid uptake, storage and release. Hyperlipidemic patterns of O-GlcNAcylation in these cells are consistent with both transient physiological adaptation and feedback uninhibited obesogenic and metabolic dysregulation. In this review, we summarize the numerous interconnections between lipid and O-GlcNAc metabolism. These links provide insights into how the O-GlcNAc regulatory system may contribute to lipid-associated diseases including obesity and metabolic syndrome.

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“…S4). In contrast, others using variations of the CAFE assay have found prominent feeding peaks toward the beginning of the subjective day (Xu et al, 2008; Schäbler et al, 2020; Barber et al, 2021), though this appears to depend in part on sex (Liu et al, 2021). The reason for this difference in peak feeding phase is unclear, though we note that our FLIC assays also differ from other methods in that (1) we can observe strong rhythms in individual flies, whereas other methods typically report only group averages, and (2) our FLIC experiments are generally carried out for a longer time under DD conditions.…”

Section: Discussionmentioning

confidence: 84%

Central and Peripheral Clock Control of Circadian Feeding Rhythms

et al. 2021

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Many behaviors exhibit ~24-h oscillations under control of an endogenous circadian timing system that tracks time of day via a molecular circadian clock. In the fruit fly, Drosophila melanogaster, most circadian research has focused on the generation of locomotor activity rhythms, but a fundamental question is how the circadian clock orchestrates multiple distinct behavioral outputs. Here, we have investigated the cells and circuits mediating circadian control of feeding behavior. Using an array of genetic tools, we show that, as is the case for locomotor activity rhythms, the presence of feeding rhythms requires molecular clock function in the ventrolateral clock neurons of the central brain. We further demonstrate that the speed of molecular clock oscillations in these neurons dictates the free-running period length of feeding rhythms. In contrast to the effects observed with central clock cell manipulations, we show that genetic abrogation of the molecular clock in the fat body, a peripheral metabolic tissue, is without effect on feeding behavior. Interestingly, we find that molecular clocks in the brain and fat body of control flies gradually grow out of phase with one another under free-running conditions, likely due to a long endogenous period of the fat body clock. Under these conditions, the period of feeding rhythms tracks with molecular oscillations in central brain clock cells, consistent with a primary role of the brain clock in dictating the timing of feeding behavior. Finally, despite a lack of effect of fat body selective manipulations, we find that flies with simultaneous disruption of molecular clocks in multiple peripheral tissues (but with intact central clocks) exhibit decreased feeding rhythm strength and reduced overall food intake. We conclude that both central and peripheral clocks contribute to the regulation of feeding rhythms, with a particularly dominant, pacemaker role for specific populations of central brain clock cells.

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Hexosamine biosynthetic pathway integrates circadian and metabolic signals to regulate daily rhythms in protein O-linked N-acetylglucosaminylation

Cited by 3 publications

References 108 publications

Model and Non-model Insects in Chronobiology

Model and Non-model Insects in Chronobiology

A nexus of lipid and O-Glcnac metabolism in physiology and disease

Central and Peripheral Clock Control of Circadian Feeding Rhythms

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