Sfp1 regulates transcriptional networks driving cell growth and division through multiple promoter-binding modes

Albert, Benjamin; Tomassetti, Susanna; Gloor, Yvonne; Dilg, Daniel; Mattarocci, Stefano; Kubik, Slawomir; Hafner, Lukas; Shore, David

doi:10.1101/gad.322040.118

Cited by 52 publications

(86 citation statements)

References 34 publications

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“…For example, we expect to see an increase in Dot6/Tod6 binding at the Ribi genes during the initial response to glucose starvation and then a loss of Dot6/Tod6 binding over time as the factors are degraded. However, it is less clear how Sfp1 and Stb3 binding will change over time, or how these factors will influence gene expression, especially in light of a recent study showing that Sfp1 can bind promoters both directly and through a cofactor 42 .…”

Section: Discussionmentioning

confidence: 99%

Integrated TORC1 and PKA signaling control the temporal activation of glucose-induced gene expression in yeast

2019

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The growth rate of a yeast cell is controlled by the target of rapamycin kinase complex I (TORC1) and cAMP-dependent protein kinase (PKA) pathways. To determine how TORC1 and PKA cooperate to regulate cell growth, we performed temporal analysis of gene expression in yeast switched from a non-fermentable substrate, to glucose, in the presence and absence of TORC1 and PKA inhibitors. Quantitative analysis of these data reveals that PKA drives the expression of key cell growth genes during transitions into, and out of, the rapid growth state in glucose, while TORC1 is important for the steady-state expression of the same genes. This circuit design may enable yeast to set an exact growth rate based on the abundance of internal metabolites such as amino acids, via TORC1, but also adapt rapidly to changes in external nutrients, such as glucose, via PKA.

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Section: Discussionmentioning

confidence: 99%

Integrated TORC1 and PKA signaling control the temporal activation of glucose-induced gene expression in yeast

2019

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“…This clearly indicates that transcription of this locus and ribosome biogenesis must be tightly coupled and that nutrient status and availability, as well as environmental conditions (internal and external), have a profound effect on the nucleolus [44,83,84,85]. In fact, ribosome biogenesis and cell size are related through Sfp1 transcriptional regulation [86,87,88], as well as to the S6 kinase (Sch9 in budding yeast and Sck2 in fission yeast) [89]; both regulated, in turn, by the nutrient sensing TORC1 complex [90,91,92]. Moreover, cell growth and cell division are coupled through ribosome content, translation initiation rate and the G1 cyclin CLN3 expression [93].…”

Section: Key Facts About Yeast Rdna Transcription and Ribosome Promentioning

confidence: 99%

Nucleolar and Ribosomal DNA Structure under Stress: Yeast Lessons for Aging and Cancer

Matos-Perdomo

Machín

2019

Cells

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Once thought a mere ribosome factory, the nucleolus has been viewed in recent years as an extremely sensitive gauge of diverse cellular stresses. Emerging concepts in nucleolar biology include the nucleolar stress response (NSR), whereby a series of cell insults have a special impact on the nucleolus. These insults include, among others, ultra-violet radiation (UV), nutrient deprivation, hypoxia and thermal stress. While these stresses might influence nucleolar biology directly or indirectly, other perturbances whose origin resides in the nucleolar biology also trigger nucleolar and systemic stress responses. Among the latter, we find mutations in nucleolar and ribosomal proteins, ribosomal RNA (rRNA) processing inhibitors and ribosomal DNA (rDNA) transcription inhibition. The p53 protein also mediates NSR, leading ultimately to cell cycle arrest, apoptosis, senescence or differentiation. Hence, NSR is gaining importance in cancer biology. The nucleolar size and ribosome biogenesis, and how they connect with the Target of Rapamycin (TOR) signalling pathway, are also becoming important in the biology of aging and cancer. Simple model organisms like the budding yeast Saccharomyces cerevisiae, easy to manipulate genetically, are useful in order to study nucleolar and rDNA structure and their relationship with stress. In this review, we summarize the most important findings related to this topic.

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“…Compared to the other ChIP-based techniques, the ChEC procedure relies on total DNA extraction instead of chromatin solubilization and does not require protein-DNA cross-linking or sonication, thus avoiding artifacts related to epitope masking or the hyper-ChIPable euchromatic phenomenon ( 42 , 43 ). So far, ChEC has been exclusively used in the model yeast S. cerevisiae to map chromatin occupancy of general transcriptional regulators ( 44 ), chromatin remodelers ( 27 , 30 , 45 ), and histone modifiers ( 31 , 32 ) in addition to transcription factors ( 46 , 47 ). As many transcriptional regulators and chromatin remodelers are key virulence and drug resistance factors in C. albicans and other fungi ( 6 , 13 , 17 , 48 – 50 ), ChEC-seq represents an attracting tool to unbiasedly decipher transcriptional regulatory networks of fungal fitness.…”

Section: Resultsmentioning

confidence: 99%

High-Resolution Genome-Wide Occupancy in Candida spp. Using ChEC-seq

Tebbji

Khemiri

Sellam

2020

mSphere

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To persist in their dynamic human host environments, fungal pathogens must sense and adapt by modulating their gene expression to fulfill their cellular needs. Understanding transcriptional regulation on a global scale would uncover cellular processes linked to persistence and virulence mechanisms that could be targeted for antifungal therapeutics. Infections associated with the yeast Candida albicans, a highly prevalent fungal pathogen, and the multiresistant related species Candida auris are becoming a serious public health threat. To define the set of a gene regulated by a transcriptional regulator in C. albicans, chromatin immunoprecipitation (ChIP)-based techniques, including ChIP with microarray technology (ChIP-chip) or ChIP-DNA sequencing (ChIP-seq), have been widely used. Here, we describe a new set of PCR-based micrococcal nuclease (MNase)-tagging plasmids for C. albicans and other Candida spp. to determine the genome-wide location of any transcriptional regulator of interest using chromatin endogenous cleavage (ChEC) coupled to high-throughput sequencing (ChEC-seq). The ChEC procedure does not require protein-DNA cross-linking or sonication, thus avoiding artifacts related to epitope masking or the hyper-ChIPable euchromatic phenomenon. In a proof-of-concept application of ChEC-seq, we provided a high-resolution binding map of the SWI/SNF chromatin remodeling complex, a master regulator of fungal fitness in C. albicans, in addition to the transcription factor Nsi1 that is an ortholog of the DNA-binding protein Reb1 for which genome-wide occupancy was previously established in Saccharomyces cerevisiae. The ChEC-seq procedure described here will allow a high-resolution genomic location definition which will enable a better understanding of transcriptional regulatory circuits that govern fungal fitness and drug resistance in these medically important fungi. IMPORTANCE Systemic fungal infections caused by Candida albicans and the “superbug” Candida auris are becoming a serious public health threat. The ability of these yeasts to cause disease is linked to their faculty to modulate the expression of genes that mediate their escape from the immune surveillance and their persistence in the different unfavorable niches within the host. Comprehensive knowledge on gene expression control of fungal fitness is consequently an interesting framework for the identification of essential infection processes that could be hindered by chemicals as potential therapeutics. Here, we expanded the use of ChEC-seq, a technique that was initially developed in the yeast model Saccharomyces cerevisiae to identify genes that are modulated by a transcriptional regulator, in pathogenic yeasts from the genus Candida. This robust technique will allow a better characterization of key gene expression regulators and their contribution to virulence and antifungal resistance in these pathogenic yeasts.

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Sfp1 regulates transcriptional networks driving cell growth and division through multiple promoter-binding modes

Cited by 52 publications

References 34 publications

Integrated TORC1 and PKA signaling control the temporal activation of glucose-induced gene expression in yeast

Integrated TORC1 and PKA signaling control the temporal activation of glucose-induced gene expression in yeast

Nucleolar and Ribosomal DNA Structure under Stress: Yeast Lessons for Aging and Cancer

High-Resolution Genome-Wide Occupancy in Candida spp. Using ChEC-seq

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