The Catalytic and Non-catalytic Functions of the Brahma Chromatin-Remodeling Protein Collaborate to Fine-Tune Circadian Transcription in Drosophila

Kwok, Rosanna S.; Li, Ying H.; Lei, Anna J.; Edery, Isaac; Chiu, Joanna C.

doi:10.1371/journal.pgen.1005307

Cited by 37 publications

(89 citation statements)

References 89 publications

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“…SWI/SNF is a sophisticated and highly complex chromatin remodeler. It has a broad interaction network ( 5 and our present data), it regulates gene expression through ATP-dependent and ATP-independent mechanisms ( 7 , 50 ), and it controls both gene transcription and pre-mRNA processing ( 8 , 11–13 ). We have shown using RNA-seq that depletion of dBRM in S2 cells causes significant changes in RNA levels upstream of the TSSs and downstream of the CSs.…”

Section: Discussionmentioning

confidence: 61%

SWI/SNF interacts with cleavage and polyadenylation factors and facilitates pre-mRNA 3′ end processing

Jordán-Pla

Gañez-Zapater

et al. 2018

Nucleic Acids Research

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SWI/SNF complexes associate with genes and regulate transcription by altering the chromatin at the promoter. It has recently been shown that these complexes play a role in pre-mRNA processing by associating at alternative splice sites. Here, we show that SWI/SNF complexes are involved also in pre-mRNA 3′ end maturation by facilitating 3′ end cleavage of specific pre-mRNAs. Comparative proteomics show that SWI/SNF ATPases interact physically with subunits of the cleavage and polyadenylation complexes in fly and human cells. In Drosophila melanogaster, the SWI/SNF ATPase Brahma (dBRM) interacts with the CPSF6 subunit of cleavage factor I. We have investigated the function of dBRM in 3′ end formation in S2 cells by RNA interference, single-gene analysis and RNA sequencing. Our data show that dBRM facilitates pre-mRNA cleavage in two different ways: by promoting the association of CPSF6 to the cleavage region and by stabilizing positioned nucleosomes downstream of the cleavage site. These findings show that SWI/SNF complexes play a role also in the cleavage of specific pre-mRNAs in animal cells.

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Section: Discussionmentioning

confidence: 61%

SWI/SNF interacts with cleavage and polyadenylation factors and facilitates pre-mRNA 3′ end processing

Jordán-Pla

Gañez-Zapater

et al. 2018

Nucleic Acids Research

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“…3 × 10 6 Drosophila S2 cells were transiently transfected with pAc- eya -3XFLAG-6XHis in combination with either pAc- tim-l -3HA or pAc- tim-sc- 3HA and reciprocal coIP assays were performed as described in (8).…”

Section: Si Materials and Methodsmentioning

confidence: 99%

EYES ABSENT and TIMELESS integrate photoperiodic and temperature cues to regulate seasonal physiology inDrosophila

Abrieux

Xue

Cai

et al. 2020

Preprint

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Organisms possess photoperiodic timing mechanisms to anticipate variations in day length and temperature as the seasons progress. The nature of the molecular mechanisms interpreting and signaling these environmental changes to elicit downstream neuroendocrine and physiological responses are just starting to emerge. Here, we demonstrate that in Drosophila melanogaster, EYES ABSENT (EYA) acts as a seasonal sensor by interpreting photoperiodic and temperature changes to trigger appropriate physiological responses. We observed that tissue-specific genetic manipulation of eya expression is sufficient to disrupt the ability of flies to sense seasonal cues, thereby altering the extent of female reproductive dormancy. Specifically we observed that EYA proteins, which peak at night in short photoperiod and accumulate at higher levels in the cold, promote reproductive dormancy in female D. melanogaster. Furthermore, we provide evidence indicating that the role of EYA in photoperiodism and temperature sensing is aided by the stabilizing action of the light-sensitive circadian clock protein TIMELESS (TIM). We postulate that increased stability and level of TIM at night under short photoperiod together with the production of cold-induced and light-insensitive TIM isoforms facilitate EYA accumulation in winter conditions. This is supported by our observations that tim null mutants exhibit reduced incidence of reproductive dormancy in simulated winter conditions, while flies overexpressing tim show an increased incidence of reproductive dormancy even in long photoperiod.Significance StatementExtracting information on calendar time from seasonal changes in photoperiod and temperature is critical for organisms to maintain circannual cycles in physiology and behavior. Here we found that in flies, EYES ABSENT (EYA) protein act as a seasonal sensor by adjusting its abundance and circadian phase in response to changes in photoperiod and temperature. We show that the manipulation of EYA levels is sufficient to impair the ability of female Drosophila to regulate seasonal variation in reproductive dormancy. Finally, our results suggest an important role of the circadian clock protein TIMELESS (TIM) in modulating EYA level through its ability to measure night length, linking the circadian clock to seasonal timing.

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“…Complementary DNA synthesis and real-time quantitative PCR were performed as previously described (Kwok et al, 2015;Li et al, 2019). Expression of target genes was normalized to noncycling cbp20 (Table S2).…”

Section: Analysis Of Gene Expressionmentioning

confidence: 99%

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

Liu¹,

Blaženović²,

Aj³

et al. 2020

Preprint

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The integration of circadian and metabolic signals is essential for maintaining robust circadian rhythms and ensuring efficient metabolism and energy use. Using Drosophila as an animal model, we showed that cellular protein O-linked N-acetylglucosaminylation (O-GlcNAcylation) exhibits robust 24-hour rhythm and is a key post-translational mechanism that regulates circadian physiology. We observed strong correlation between protein O-GlcNAcylation rhythms and clock-controlled feeding-fasting cycles, suggesting that O-GlcNAcylation rhythms are primarily driven by nutrient input. Interestingly, daily O-GlcNAcylation rhythms were severely dampened when we subjected flies to time-restricted feeding (TRF) at unnatural feeding time. This suggests the presence of a clock-regulated buffering mechanism that prevents excessive O-GlcNAcylation at non-optimal times of the day-night cycle. We found that this buffering mechanism is mediated by glutamine-fructose-6-phosphate amidotransferase (GFAT) activity, which is regulated through integration of circadian and metabolic signals. Finally, we generated a mathematical model to describe the key factors that regulate daily O-GlcNAcylation rhythm.

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The Catalytic and Non-catalytic Functions of the Brahma Chromatin-Remodeling Protein Collaborate to Fine-Tune Circadian Transcription in Drosophila

Cited by 37 publications

References 89 publications

SWI/SNF interacts with cleavage and polyadenylation factors and facilitates pre-mRNA 3′ end processing

SWI/SNF interacts with cleavage and polyadenylation factors and facilitates pre-mRNA 3′ end processing

EYES ABSENT and TIMELESS integrate photoperiodic and temperature cues to regulate seasonal physiology inDrosophila

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

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