Logic of the Yeast Metabolic Cycle: Temporal Compartmentalization of Cellular Processes

Tu, Benjamin P.; Kudlicki, Andrzej; Rowicka, Maga; McKnight, Steven L.

doi:10.1126/science.1120499

Cited by 813 publications

(1,238 citation statements)

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“…The concept of a redox cycle regulating the cell cycle is further supported by a recent report from Tu et al (2005). Budding yeast exhibit a metabolic redox cycle consisting of a reductive non-respiratory phase and an oxidative respiratory phase.…”

Section: Introductionmentioning

confidence: 94%

“…Budding yeast exhibit a metabolic redox cycle consisting of a reductive non-respiratory phase and an oxidative respiratory phase. This metabolic redox cycle coordinates with periods of gene expression regulating essential cellular and metabolic events (Tu et al, 2005). Many of the genes regulating DNA replication and cell cycle progression are expressed during its reductive phase with cell cycle initiation occurring very late during the oxidative phase.…”

Section: Introductionmentioning

confidence: 99%

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A redox cycle within the cell cycle: ring in the old with the new

2006

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In recent years, the intracellular oxidation-reduction (redox) state has gained increasing attention as a critical mediator of cell signaling, gene expression changes and proliferation. This review discusses the evidence for a redox cycle (i.e., fluctuation in the cellular redox state) regulating the cell cycle. The presence of redox-sensitive motifs (cysteine residues, metal co-factors in kinases and phosphatases) in several cell cycle regulatory proteins indicate periodic oscillations in intracellular redox state could play a central role in regulating progression from G 0 /G 1 to S to G 2 and M cell cycle phases. Fluctuations in the intracellular redox state during cell cycle progression could represent a fundamental mechanism linking oxidative metabolic processes to cell cycle regulatory processes. Proliferative disorders are central to a variety of human pathophysiological conditions thought to involve oxidative stress. Therefore, a more complete understanding of redox control of the cell cycle could provide a biochemical rationale for manipulating aberrant cell proliferation.

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Section: Introductionmentioning

confidence: 94%

Section: Introductionmentioning

confidence: 99%

A redox cycle within the cell cycle: ring in the old with the new

2006

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“…In this pathway, reporter metabolite function is the rule rather than the exception ( Figure 5); a change in the flux or a metabolic transition influences multiple biological processes by changing the concentration of these metabolites. Under conditions that cause metabolic pathway oscillations, the magnitude of cellular consequences is evident: in yeast, over half of the transcriptome is expressed as a direct function of a metabolic cycle and genes with common functions have similar temporal expression patterns [53].…”

Section: Reviewmentioning

confidence: 99%

Regulatory crosstalk of the metabolic network

Grüning

Lehrach

Ralser

2010

Trends in Biochemical Sciences

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The metabolic network has a modular architecture, is robust to perturbations, and responds to biological stimuli and environmental conditions. Through monitoring by metabolite responsive macromolecules, metabolic pathways interact with the transcriptome and proteome. Whereas pathway interconnecting cofactors and substrates report on the overall state of the network, specialised intermediates measure the activity of individual functional units. Transitions in the network affect many of these regulatory metabolites, facilitating the parallel regulation of the timing and control of diverse biological processes. The metabolic network controls its own balance, chromatin structure and the biosynthesis of molecular cofactors; moreover, metabolic shifts are crucial in the response to oxidative stress and play a regulatory role in cancer.Evolution of the metabolic network and its structure Life probably began with the formation of compartmentalised autocatalytic chemical cycles. With the appearance of complex catalysts (ribonucleic acid-or protein-based enzymes), these cycles gained complexity, and evolved in their effectiveness and robustness [1]. These metabolic pathways now form the basis for life.As was the case for the first primitive life forms, the survival of today's complex organisms depends on the robustness and functionality of the metabolic framework [2]. To prevent and counteract perturbations in the flux, many biological control and sensor systems have evolved around the metabolic network. Metabolic pathways provide the cell with energy and supply macromolecular synthesis pathways with their required intermediates. They also balance metabolic systems under a variety of physiological conditions, and act as transducers and sensor systems for environmental conditions and stimuli. In addition, metabolic pathways are essential for crosstalk between metabolic regulatory components and the cellular transcriptome and proteome.As early as the 1960s, the principle that cells alter their gene expression in response to metabolic requirements has been known. The seminal work of Jacob and Monod, investigating the lac operon, uncovered one of the first examples of chemical-genetic regulation, by which bacterial cells adjust their enzyme production to the nutrient supply [3]. However, only recently have the broader implications of this principle emerged. Indeed, changes in the metabolic network not only control the metabolome, but they also have wide-ranging regulatory functions throughout biology.Most of the biochemical mechanisms that link the metabolic network to the transcriptome and proteome are incompletely understood. However, one type of regulation appears to be common: representative network intermediates bind to and modulate sensor function and activity of transcription factors, translational regulators, chromatin, enzymes, RNA molecules, and ion channels. Significant transcriptional changes around these intermediates identified them as reporter metabolites [4,5]. The use of intermediates as activity reporters ne...

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“…Conventionally, transcript level regulation has been considered to be more important during development or during long‐term adaptation (Plaxton, 1996). With an increasing number of studies utilizing advanced‐omic approaches, a deeper understanding of the significance of transcript level regulation of cellular metabolism and physiology is emerging in a variety of different organisms (Tu et al ., 2005). In eukaryotic algae, the relationship between global transcript changes and metabolic and physiological shifts has been examined only in a limited context (Nymark et al ., 2009; Chauton et al ., 2012).…”

Section: Introductionmentioning

confidence: 99%

Transcript level coordination of carbon pathways during silicon starvation‐induced lipid accumulation in the diatom Thalassiosira pseudonana

et al. 2016

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Summary Diatoms are one of the most productive and successful photosynthetic taxa on Earth and possess attributes such as rapid growth rates and production of lipids, making them candidate sources of renewable fuels. Despite their significance, few details of the mechanisms used to regulate growth and carbon metabolism are currently known, hindering metabolic engineering approaches to enhance productivity.To characterize the transcript level component of metabolic regulation, genome‐wide changes in transcript abundance were documented in the model diatom Thalassiosira pseudonana on a time‐course of silicon starvation. Growth, cell cycle progression, chloroplast replication, fatty acid composition, pigmentation, and photosynthetic parameters were characterized alongside lipid accumulation.Extensive coordination of large suites of genes was observed, highlighting the existence of clusters of coregulated genes as a key feature of global gene regulation in T. pseudonana. The identity of key enzymes for carbon metabolic pathway inputs (photosynthesis) and outputs (growth and storage) reveals these clusters are organized to synchronize these processes.Coordinated transcript level responses to silicon starvation are probably driven by signals linked to cell cycle progression and shifts in photophysiology. A mechanistic understanding of how this is accomplished will aid efforts to engineer metabolism for development of algal‐derived biofuels.

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Logic of the Yeast Metabolic Cycle: Temporal Compartmentalization of Cellular Processes

Cited by 813 publications

References 34 publications

A redox cycle within the cell cycle: ring in the old with the new

A redox cycle within the cell cycle: ring in the old with the new

Regulatory crosstalk of the metabolic network

Transcript level coordination of carbon pathways during silicon starvation‐induced lipid accumulation in the diatom Thalassiosira pseudonana

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