Codon usage affects the structure and function of the <i>Drosophila</i> circadian clock protein PERIOD

Fu, Jingjing; Murphy, Katherine A.; Zhou, Mian; Li, Ying H.; Lam, Vu H.; Tabuloc, Christine A.; Chiu, Joanna C.; Liu, Yi

doi:10.1101/gad.281030.116

Cited by 65 publications

(74 citation statements)

References 83 publications

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“…One example that this review did not cover, is the finding that it matters to circadian clock proteins from which codons they are translated. This phenomenon has 520 been described in cyanobacteria [99], Neurospora crassa [100] and more recently also in flies [101]).…”

Section: Final Considerationsmentioning

confidence: 62%

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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Section: Final Considerationsmentioning

confidence: 62%

Emerging Roles of Translational Control in Circadian Timekeeping

Castelo-Szekely

Gatfield

2020

Journal of Molecular Biology

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“…Furthermore, insights into the physiological role of ultradian oscillating genes have been published, suggesting the importance of the ultradian expression of genes involved in metabolism regulation, feeding behavior and response to dawn/dusk transition-related stress situations (Hughes et al2009 PMID:19343201 ).. Another intriguing aspect of oscillating gene regulation regards codon usage and translation: recent experimental evidences found that key circadian genes within simple organisms (i.e., Neurospora crassa, Synechococcus elongatus, Drosophila melanogaster) exhibit an unexpected non-optimized codon usage (Zhou et al, 2013; Zhou et al, 2015; Xu et al, 2013; Fu et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Systematic analysis of mouse genome reveals distinct evolutionary and functional properties among circadian and ultradian genes

Castellana

Mazza

Capocefalo

et al. 2018

Preprint

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In living organisms, biological clocks regulate 24 h (circadian) molecular, physiological, and behavioral rhythms to maintain homeostasis and synchrony with predictable environmental changes. Harmonics of these circadian rhythms having periods of 8 hours and 12 hours (ultradian) have been documented in several species. In mouse liver, harmonics of the 24-hour period of gene transcription hallmarked genes oscillating with a frequency two or three times faster than the circadian circuitry. Many of these harmonic transcripts enriched pathways regulating responses to environmental stress and coinciding preferentially with subjective dawn and dusk. We hypothesized that these stress anticipatory genes would be more evolutionarily conserved than background circadian and non-circadian genes. To investigate this issue, we performed broad computational analyses of genes/proteins oscillating at different frequency ranges across several species and showed that ultradian genes/proteins, especially those oscillating with a 12-hour periodicity, are more likely to be of ancient origin and essential in mice. In summary, our results show that genes with ultradian transcriptional patterns are more likely to be phylogenetically conserved and associated with the primeval and inevitable dawn/dusk transitions.

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“…具体原因是源于优化frq基因的密码子改变了FRQ蛋白的构象及磷酸化修饰, 从而影响蛋白的功能和稳定性 [52] . 同样的现象也可在调控果蝇生物钟的period基因和哺乳动物视觉晶体蛋白gamma-B crystalli的编码基因中观测到 [53,54] .…”

Section: 与Rna转录相比蛋白质的翻译过程不仅耗能而unclassified