A Super-Assembly of Whi3 Encodes Memory of Deceptive Encounters by Single Cells during Yeast Courtship

Caudron, Fabrice; Barral, Yves

doi:10.1016/j.cell.2013.10.046

Cited by 127 publications

(160 citation statements)

References 52 publications

(52 reference statements)

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“…Yeast mating is a carefully coordinated and complex event that may require dynamic changes in mating partner selection and thus adaptive pathway activity (35). This would necessitate highly reversible MAPK activity.…”

Section: Resultsmentioning

confidence: 99%

Single-cell dynamics and variability of MAPK activity in a yeast differentiation pathway

Conlon

Gelin-Licht

Ganesan

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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In response to pheromones, yeast cells activate a MAPK pathway to direct processes important for mating, including gene induction, cellcycle arrest, and polarized cell growth. Although a variety of assays have been able to elucidate signaling activities at multiple steps in the pathway, measurements of MAPK activity during the pheromone response have remained elusive, and our understanding of single-cell signaling behavior is incomplete. Using a yeast-optimized FRET-based mammalian Erk-activity reporter to monitor Fus3 and Kss1 activity in live yeast cells, we demonstrate that overall mating MAPK activity exhibits distinct temporal dynamics, rapid reversibility, and a graded dose dependence around the K D of the receptor, where phenotypic transitions occur. The complex dose response was found to be largely a consequence of two feedbacks involving cyclin-mediated scaffold phosphorylation and Fus3 autoregulation. Distinct cell cycle-dependent response patterns comprised a large portion of the cell-to-cell variability at each dose, constituting the major source of extrinsic noise in coupling activity to downstream gene-expression responses. Additionally, we found diverse spatial MAPK activity patterns to emerge over time in cells undergoing default, gradient, and true mating responses. Furthermore, ramping up and rapid loss of activity were closely associated with zygote formation in mating-cell pairs, supporting a role for elevated MAPK activity in successful cell fusion and morphogenic reorganization. Altogether, these findings present a detailed view of spatiotemporal MAPK activity during the pheromone response, elucidating its role in mediating complex longterm developmental fates in a unicellular differentiation system. cell signaling | MAPK dynamics | Fus3 | mating pathway | yeast

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Section: Resultsmentioning

confidence: 99%

Single-cell dynamics and variability of MAPK activity in a yeast differentiation pathway

Conlon

Gelin-Licht

Ganesan

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…If the phenotypic traits expressed by individuals depend on cellular age, this leads to phenotypic heterogeneity. Such age dependence has been demonstrated for a number of cellular traits in budding yeast (Saccharomyces cerevisiae) 26,27 as well as in bacterial systems. For example, in the alphaproteobacterium Methylobacterium extorquens, both cell size and the timing of cell division depend on cellular age 28 .…”

Section: Quorum Sensingmentioning

confidence: 89%

“…c | Cellular ageing in microorganisms that are rod-shaped or divide by budding. In such organisms, the age of cell poles and cell walls can differ between the two cells emerging from division, which can lead to phenotypic heterogeneity 27 . Here, asymmetrical segregation of protein assemblies in Saccharomyces cerevisiae is shown.…”

Section: Quorum Sensingmentioning

confidence: 99%

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A functional perspective on phenotypic heterogeneity in microorganisms

2015

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Most microbial communities consist of a genetically diverse assembly of different organisms, and the level of genetic diversity plays an important part in community properties and functions. However, biological diversity also arises at a lower level of biological organization, between genetically identical cells that reside in the same microenvironment. In this Review, I outline the molecular mechanisms responsible for phenotypic heterogeneity and discuss how phenotypic heterogeneity allows genotypes to persist in fluctuating environments. I also describe how it promotes interactions between phenotypic subpopulations in clonal groups, providing microbial groups with new functionality.

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“…In the early 1990s, the discovery of protein-based phenotypic inheritance in yeast by Reed Wickner (Wickner 1994, Wickner et al 1995 changed the way we think about prions and their biological significance. The discovery of a large number of fungal prions serving various physiological functions suggested that prions are neither rare nor always bad (Caudron & Barral 2013, Coustou et al 1997, Eaglestone et al 1999, Halfmann et al 2012, Holmes et al 2013, Jarosz et al 2014, Suzuki et al 2012, True & Lindquist 2000, True et al 2004. It also became evident that protein-based disease propagation is more prevalent than previously thought and that several disease-causing amyloids, such as Alzheimer aβ42, α-synuclein, and τ, can spread in a manner akin to prions (Cushman et al 2010, Holmes & Diamond 2014, Polymenidou & Cleveland 2012.…”

Section: A Brief History Of the Discovery Of Prion And Prion-like Promentioning

confidence: 99%

Prions: What Are They Good For?

2015

Annu. Rev. Cell Dev. Biol.

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Prions, a self-templating amyloidogenic state of normal cellular proteins such as PrP, have been identified as the basis of a number of disease states, particularly diseases of the nervous system. This finding has led to the notion that protein aggregation, namely prionogenic aggregates and amyloids, is primarily harmful for the organism. However, identification of proteins in a prion-like state that are not harmful and may even be beneficial has begun to change this perception. This review discusses when and how a prion-based protein conformational switch may be utilized to generate a sustained physiological change in response to a transient stimulus.

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A Super-Assembly of Whi3 Encodes Memory of Deceptive Encounters by Single Cells during Yeast Courtship

Cited by 127 publications

References 52 publications

Single-cell dynamics and variability of MAPK activity in a yeast differentiation pathway

Single-cell dynamics and variability of MAPK activity in a yeast differentiation pathway

A functional perspective on phenotypic heterogeneity in microorganisms

Prions: What Are They Good For?

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