Dataset Information

Ribosome profiling the cell cycle: lessons and challenges.

ABSTRACT: Understanding the causes and consequences of dynamic changes in the abundance and activity of cellular components during cell division is what most cell cycle studies are about. Here we focus on control of gene expression in the cell cycle at the level of translation. The advent of deep sequencing methodologies led to technologies that quantify the levels of all mRNAs that are bound by ribosomes and engaged in translation in the cell (Ingolia et al. Science 324:218-223, 2009). This approach has been applied recently to synchronous cell populations to find transcripts under translational control at different cell cycle phases (Blank et al. EMBO J 36:487-502, 2017; Stumpf et al. Mol Cell 52:574-582, 2013; Tanenbaum et al. Elife 4:e07957, 2015). These studies revealed new biology, but they also have limitations, pointing to challenges that need to be addressed in the future.

SUBMITTER: Aramayo R

PROVIDER: S-EPMC5790165 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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Ribosome profiling the cell cycle: lessons and challenges.

Aramayo Rodolfo R Polymenis Michael M

Current genetics 20170427 6

Understanding the causes and consequences of dynamic changes in the abundance and activity of cellular components during cell division is what most cell cycle studies are about. Here we focus on control of gene expression in the cell cycle at the level of translation. The advent of deep sequencing methodologies led to technologies that quantify the levels of all mRNAs that are bound by ribosomes and engaged in translation in the cell (Ingolia et al. Science 324:218-223, 2009). This approach has ...[more]

PMID: 28451847

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Project description:The fundamental dynamics of the cell cycle, underlying cell growth and reproduction, were previously found to be robust under a wide range of environmental and internal perturbations. This property was commonly attributed to its network structure, which enables the coordinated interactions among hundreds of proteins. Despite significant advances in deciphering the components and autonomous interactions of this network, understanding the interfaces of the cell cycle with other major cellular processes is still lacking. To gain insight into these interfaces, we used the process of genome-rewiring in yeast by placing an essential metabolic gene HIS3 from the histidine biosynthesis pathway, under the exclusive regulation of different cell-cycle promoters. In a medium lacking histidine and under partial inhibition of the HIS3p, the rewired cells encountered an unforeseen multitasking challenge; the cell-cycle regulatory genes were required to regulate the essential histidine-pathway gene in concert with the other metabolic demands, while simultaneously driving the cell cycle through its proper temporal phases. We show here that chemostat cell populations with rewired cell-cycle promoters adapted within a short time to accommodate the inhibition of HIS3p and stabilized a new phenotypic state. Furthermore, a significant fraction of the population was able to adapt and grow into mature colonies on plates under such inhibiting conditions. The adapted state was shown to be stably inherited across generations. These adaptation dynamics were accompanied by a non-specific and irreproducible genome-wide transcriptional response. Adaptation of the cell-cycle attests to its multitasking capabilities and flexible interface with cellular metabolic processes and requirements. Similar adaptation features were found in our previous work when rewiring HIS3 to the GAL system and switching cells from galactose to glucose. Thus, at the basis of cellular plasticity is the emergence of a yet-unknown general, non-specific mechanism allowing fast inherited adaptation to unforeseen challenges.

Dataset Information

Ribosome profiling the cell cycle: lessons and challenges.

Publications

Ribosome profiling the cell cycle: lessons and challenges.

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