Diurnal regulation of RNA polymerase III transcription is under the control of both the feeding–fasting response and the circadian clock

Mange, François; Praz, Viviane; Migliavacca, Eugenia; Willis, Ian M.; Schütz, Frédéric; Hernandez, Nouria

doi:10.1101/gr.217521.116

Cited by 28 publications

(31 citation statements)

References 78 publications

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“…The liver‐regeneration response to PH in rats and to a lesser extent in mice has been extensively studied . Consistent with prior studies, (i) sham‐operated mice displayed a transient decrease in liver‐to‐body ratio; (ii) PH mice reconstituted the original liver‐to‐body weight ratio by 4 weeks (http://onlinelibrary.wiley.com/doi/10.1002/hep4.1102/suppinfo); (iii) H&E staining (http://onlinelibrary.wiley.com/doi/10.1002/hep4.1102/suppinfo) revealed little cell death but did reveal periodic increases in a staining pattern that probably reflects fat droplets, as described in detail; (iv) by 4 weeks, a normal tissue morphology was evident; and (v) the ratio of mononucleated‐to‐binucleated hepatocytes changed 3‐fold (from 2:1 to 6:1) during the course of regeneration (http://onlinelibrary.wiley.com/doi/10.1002/hep4.1102/suppinfo).…”

Section: Resultssupporting

confidence: 69%

“…We initiated these studies of cell proliferation in response to PH in the context of a multifaceted program project study of three cycles of gene expression (circadian, nutrient response, and cell division) in the mouse liver. (19)(20)(21)(22) To combine the cell-division studies using PH with the circadian and nutrient-response studies, all mice were entrained with 12-hour-light fasting and 12hour-dark feeding cycles. Thus, prior to PH, 12-14week-old mice had been first entrained for 2 weeks on 12-hour ZT0-ZT12-light/12-hour ZT12-ZT24-dark cycles to fix the circadian clock, followed by a further 2week entrainment with ZT0-ZT12-light fasting/ZT12-ZT24-dark feeding cycles, to entrain both the circadian and nutrient-response cycles.…”

Section: Resultsmentioning

confidence: 99%

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Segregated hepatocyte proliferation and metabolic states within the regenerating mouse liver

Minocha

Villeneuve

Rib

et al. 2017

Hepatology Communications

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Mammalian partial hepatectomy (PH) induces an orchestrated compensatory hyperplasia, or regeneration, in remaining tissue to restore liver mass; during this process, liver functions are maintained. We probed this process in mice with feeding‐ and light/dark‐entrained animals subjected to sham or PH surgery. Early on (i.e., 10 hours), irrespective of sham or PH surgery, hepatocytes equidistant from the portal and central veins (i.e., midlobular) accumulated the G1‐phase cell‐division‐cycle marker cyclin D1. By 24 hours, however, cyclin D1 disappeared absent PH but was reinforced in midlobular hepatocytes after PH. At 48 hours after PH and 2 hours fasting, synchronously mitotic hepatocytes possessed less glycogen than surrounding nonproliferating hepatocytes. The differential glycogen content generated a conspicuous entangled pattern of proliferating midlobular and nonproliferating periportal and pericentral hepatocytes. The nonproliferating hepatocytes maintained aspects of normal liver properties. Conclusion: In the post‐PH regenerating mouse liver, a binary switch segregates midlobular cells to proliferate side‐by‐side with nonproliferating periportal and pericentral cells, which maintain metabolic functions. Our results also indicate that mechanisms of liver regeneration display evolutionary flexibility. (Hepatology Communications 2017;1:871–885)

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Section: Resultssupporting

confidence: 69%

Section: Resultsmentioning

confidence: 99%

Segregated hepatocyte proliferation and metabolic states within the regenerating mouse liver

Minocha

Villeneuve

Rib

et al. 2017

Hepatology Communications

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“…Two recent studies 340 have reported on the inverse experiment, i.e. the application of an arrhythmic feeding protocol in wild-type animals with an intact clock [67,68]. Greenwell et al [68] observed that about 70% of mRNA rhythms were lost under these conditions, further underlining the exceptional importance of feeding-fasting cycles for hepatic gene expression rhythms.…”

Section: Interplay Between Circadian Clocks and Feeding/fasting Cyclementioning

confidence: 99%

Emerging Roles of Translational Control in Circadian Timekeeping

Castelo-Szekely

Gatfield

2020

Journal of Molecular Biology

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A large part of mammalian physiology and behaviour shows regular daily variations. This temporal organisation is driven by the activity of an endogenous circadian clock, whose molecular basis consists of diurnal waves in gene expression. Circadian transcription is the major driver of these rhythms, yet post-transcriptional mechanisms, some of which occur in response to systemic cues and in a tissue-specific fashion, have central roles in ultimately establishing the oscillatory gene expression programme as well. Regulatory control that occurs at the level of translation is emerging as an important player in the generation and modulation of protein accumulation rhythms. As a mechanism, translation lies at a privileged position to integrate genetically encoded rhythmic signals with other, external and internal stimuli, including nutrient-derived cues. In this review, we summarise our current knowledge of how diurnal control of translation affects both bulk protein levels and gene-specific protein biosynthesis. We discuss mechanisms of regulation, in particular with regard to the complex interplay between circadian cycles and feeding/fasting cycles, as well as emerging roles for upstream open reading frames (uORFs) in clock control. cyanobacterial clocks can operate in the absence of any transcription at all and that self-sustained rhythmic phosphorylation of the essential clock component KaiC even occurs in vitro using recom-2 binant clock proteins and ATP [4]. Transcription-independent molecular rhythms have also been observed in human erythrocytes. In these naturally nucleus-free cells, antioxidant proteins known as peroxiredoxins undergo changes in their redox status, which show self-sustained, entrainable, and 35 temperature-compensated 24-hour periodicity in the absence of transcription and translation [5]. In the wake of such surprising discoveries (and as a consequence of the technical advances made in the fields of high-throughput nucleic acid sequencing and proteomics), the longstanding concept which places daily changes in transcriptional activity at the heart of rhythmic gene expression was revisited as well. A more nuanced picture has arisen that accords a significant role to post-transcriptional 40 mechanisms in the generation of rhythmic clock outputs in mammals. Furthermore, it has become clear that a significant proportion of RNA and protein oscillations is not necessarily a direct output of the local, cellular clock, but rather driven by systemic cues, in particular by signals related to feeding.This review aims at presenting and discussing our current knowledge of how one of the implicated 45 post-transcriptional mechanism, i.e. translation, can generate, modulate, and sustain circadian rhythms. Our main focus will lie on the mammalian circadian system. Before we delve into the details, however, we shall take this opportunity for a brief digression into findings from two of the more exotic organisms that have been used in circadian clock research, namely green algae and marine dinoflagellates. It i...

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“…We thank the CycliX Consortium: Nouria Hernandez, 1 Mauro Delorenzi, 2,3,4 Bart Deplancke, 5 Béatrice Desvergne, 1 Nicolas Guex, 6 Winship Herr, 1 Felix Naef, 5 Jacques Rougemont, 7 Ueli Schibler, 8 Teemu Andersin, 8 Pascal Cousin, 1 Federica Gilardi, 1 Pascal Gos, 8…”

Section: Acknowledgementsmentioning

confidence: 99%

“…In eukaryotes, both active and repressed genes are packaged in nucleosome-containing chromatin in which histones are reversibly modified -often reflecting the underlying gene transcription status. In this chromatin context, we study how cyclical programs of gene expression -i.e., circadian, nutrition and cell division -are regulated in differentiated cells using the mouse liver as model [1,2,3,4]. We focus on gene expression as measured by RNA-transcript levels and study the relationship between gene occupancy by RNA polymerase II (Pol II) and two specific histone modifications: histone H3 lysine 4 trimethylation (H3K4me3) observed at active promoters and histone H3 lysine 36 trimethylation (H3K36me3) associated with the body of actively transcribed genes (reviewed in [5]).…”

Section: Introductionmentioning

confidence: 99%

Cycles of gene expression and genome response during mammalian tissue regeneration

Rib

Villeneuve

Praz

et al. 2018

Preprint

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Background: Compensatory liver hyperplasia -or regeneration -induced by two-thirds partial hepatectomy (PH) permits the study of synchronized activation of mammalian gene expression, particularly in relation to cell proliferation. Here, we measured genomic transcriptional responses and mRNA accumulation changes after PH and sham surgeries. Results:During the first 10-20 hours, the PH-and sham-surgery responses were very similar, including parallel early activation of cell-division-cycle genes. After 20 hours, however, whereas post-PH livers continued with a robust and coordinate cell-division-cycle gene-expression response before returning to the resting state by one week, sham-surgery livers returned directly to a resting gene-expression state. Localization of RNA polymerase II (Pol II), and trimethylated histone H3 lysine 4 (H3K4me3) and 36 (H3K36me3) on genes dormant in the resting liver and activated during the PH response revealed a general de novo promoter Pol II recruitment and H3K4me3 increase during the early 10-20 hour phase followed by Pol II elongation and H3K36me3 accumulation in gene bodies during the later proliferation phase. H3K36me3, generally appearing at the first-internal exon, was preceded 5' by H3K36me2; 3' of the first-internal exon, in about half of genes H3K36me3 predominated and in the other half H3K36me2 and H3K36me3 co-existed. Further, we observed some unusual gene profiles with abundant Pol II but little evident H3K4me3 or H3K36me3 modification, indicating that these modifications are neither universal nor essential partners to Pol II transcription.Conclusions: PH and sham surgical procedures on mice reveal striking early post-operatory gene expression similarities followed by synchronized mRNA accumulation and epigenetic histone mark changes specific to PH.

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Diurnal regulation of RNA polymerase III transcription is under the control of both the feeding–fasting response and the circadian clock

Cited by 28 publications

References 78 publications

Segregated hepatocyte proliferation and metabolic states within the regenerating mouse liver

Segregated hepatocyte proliferation and metabolic states within the regenerating mouse liver

Emerging Roles of Translational Control in Circadian Timekeeping

Cycles of gene expression and genome response during mammalian tissue regeneration

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