Dynamical modelling of the heat shock response inChlamydomonas reinhardtii

AbstractGlobal warming is exposing plants to more frequent heat stress, with consequent crop yield reduction. Organisms exposed to large temperature increases protect themselves typically with a heat shock response (HSR). To study the HSR in photosynthetic organisms we present here a data driven mathematical model describing the dynamics of the HSR in the model organismChlamydomonas reinhartii. Temperature variations are sensed by the accumulation of unfolded proteins, which activates the synthesis of heat shock proteins (HSP) mediated by the heat shock transcription factor HSF1. Our dynamical model employs a system of ordinary differential equations mostly based on mass-action kinetics to study the time evolution of the involved species. The signalling network is inferred from data in the literature, and the multiple experimental data-sets available are used to calibrate the model, which allows to reproduce their qualitative behaviour. With this model we show the ability of the system to adapt to temperatures higher than usual during heat shocks longer than three hours by shifting to a new steady state. We study how the steady state concentrations depend on the temperature at which the steady state is reached. We systematically investigate how the accumulation of HSPs depends on the combination of temperature and duration of the heat shock. We finally investigate the system response to a smooth variation in temperature simulating a hot day.

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Data-driven dynamical model indicates that the heat shock response in Chlamydomonas reinhardtii is tailored to handle natural temperature variation

Journal of The Royal Society Interface ◽

10.1098/rsif.2017.0965 ◽

2018 ◽

Vol 15 (142) ◽

pp. 20170965 ◽

Cited By ~ 1

Author(s):

Stefano Magni ◽

Antonella Succurro ◽

Alexander Skupin ◽

Oliver Ebenhöh

Keyword(s):

Mathematical Model ◽

Heat Shock ◽

Chlamydomonas Reinhardtii ◽

Heat Shock Response ◽

Mass Action ◽

Data Driven ◽

Dynamical Model ◽

Misfolded Proteins ◽

Mass Action Kinetics ◽

Shock Response

Global warming exposes plants to severe heat stress, with consequent crop yield reduction. Organisms exposed to high temperature stresses typically protect themselves with a heat shock response (HSR), where accumulation of unfolded proteins initiates the synthesis of heat shock proteins through the heat shock transcription factor HSF1. While the molecular mechanisms are qualitatively well characterized, our quantitative understanding of the underlying dynamics is still very limited. Here, we study the dynamics of HSR in the photosynthetic model organism Chlamydomonas reinhardtii with a data-driven mathematical model of HSR. We based our dynamical model mostly on mass action kinetics, with a few nonlinear terms. The model was parametrized and validated by several independent datasets obtained from the literature. We demonstrate that HSR quantitatively and significantly differs if an increase in temperature of the same magnitude occurs abruptly, as often applied under laboratory conditions, or gradually, which would rather be expected under natural conditions. In contrast to rapid temperature increases, under gradual changes only negligible amounts of misfolded proteins accumulate, indicating that the HSR of C. reinhardtii efficiently avoids the accumulation of misfolded proteins under conditions most likely to prevail in nature. The mathematical model we developed is a flexible tool to simulate the HSR to different conditions and complements the current experimental approaches.

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Convergence of Molecular, Modeling, and Systems Approaches for an Understanding of the Escherichia coli Heat Shock Response

Microbiology and Molecular Biology Reviews ◽

10.1128/mmbr.00007-08 ◽

2008 ◽

Vol 72 (3) ◽

pp. 545-554 ◽

Cited By ~ 175

Author(s):

Eric Guisbert ◽

Takashi Yura ◽

Virgil A. Rhodius ◽

Carol A. Gross

Keyword(s):

Escherichia Coli ◽

Heat Shock ◽

Heat Shock Response ◽

Feedback Loop ◽

Model Organism ◽

Central Component ◽

E Coli ◽

Functional Aspects ◽

Shock Response ◽

Homeostatic Response

SUMMARY The heat shock response (HSR) is a homeostatic response that maintains the proper protein-folding environment in the cell. This response is universal, and many of its components are well conserved from bacteria to humans. In this review, we focus on the regulation of one of the most well-characterized HSRs, that of Escherichia coli. We show that even for this simple model organism, we still do not fully understand the central component of heat shock regulation, a chaperone-mediated negative feedback loop. In addition, we review other components that contribute to the regulation of the HSR in E. coli and discuss how these additional components contribute to regulation. Finally, we discuss recent genomic experiments that reveal additional functional aspects of the HSR.

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Influence of temperature on the development, reproduction and regeneration in the flatworm model organism Macrostomum lignano

10.1101/389478 ◽

2018 ◽

Cited By ~ 1

Author(s):

Jakub Wudarski ◽

Kirill Ustyantsev ◽

Lisa Glazenburg ◽

Eugene Berezikov

Keyword(s):

Heat Shock ◽

Heat Shock Response ◽

Elevated Temperatures ◽

Model Organism ◽

Response Threshold ◽

Reproduction Rate ◽

Negative Consequences ◽

Time Reproduction ◽

Shock Response ◽

Macrostomum Lignano

AbstractThe free-living marine flatworm Macrostomum lignano is a powerful model organism to study mechanisms of regeneration and stem cell regulation due to its convenient combination of biological and experimental properties, including the availability of transgenesis methods, which is unique among flatworm models. However, due to its relatively recent introduction in research, there are still many biological aspects of the animal that are not known. One of such questions is the influence of the culturing temperature on Macrostomum biology. Here we systematically investigated how different culturing temperatures affect the development time, reproduction rate, regeneration, heat shock response, and gene knockdown efficiency by RNA interference in M. lignano. We used marker transgenic lines of the flatworm to accurately measure the regeneration endpoint and to establish the stress response threshold for temperature shock. We found that compared to the culturing temperature of 20°C commonly used for M. lignano, elevated temperatures of 25°C-30°C substantially speed-up the development and regeneration time and increase reproduction rate without detectable negative consequences for the animal, while temperatures above 30°C elicit a heat shock response.We show that altering the temperature conditions can be used to shorten the time required to establish M. lignano cultures, store important lines and optimize the microinjection procedures for transgenesis. Our findings will help to optimize the design of experiments in M. lignano and thus facilitate future research in this model organism.

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A simple mass-action model for the eukaryotic heat shock response and its mathematical validation

Natural Computing ◽

10.1007/s11047-010-9216-y ◽

2010 ◽

Vol 10 (1) ◽

pp. 595-612 ◽

Cited By ~ 34

Author(s):

Ion Petre ◽

Andrzej Mizera ◽

Claire L. Hyder ◽

Annika Meinander ◽

Andrey Mikhailov ◽

...

Keyword(s):

Heat Shock ◽

Heat Shock Response ◽

Mass Action ◽

Mass Action Model ◽

Shock Response ◽

Action Model ◽

Simple Mass

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Proteome analysis of the Escherichia coli heat shock response under steady-state conditions

Proteome Science ◽

10.1186/1477-5956-7-36 ◽

2009 ◽

Vol 7 (1) ◽

pp. 36 ◽

Cited By ~ 29

Author(s):

Svenja Lüders ◽

Claas Fallet ◽

Ezequiel Franco-Lara

Keyword(s):

Escherichia Coli ◽

Steady State ◽

Heat Shock ◽

Heat Shock Response ◽

Proteome Analysis ◽

Shock Response

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Heat shock response in archaea

Emerging Topics in Life Sciences ◽

10.1042/etls20180024 ◽

2018 ◽

Vol 2 (4) ◽

pp. 581-593 ◽

Cited By ~ 2

Author(s):

Liesbeth Lemmens ◽

Rani Baes ◽

Eveline Peeters

Keyword(s):

Heat Shock ◽

Heat Shock Response ◽

Molecular Mechanisms ◽

Structural Response ◽

Large Temperature ◽

Cell Factories ◽

Shock Response ◽

Molecular Aspects ◽

Shock Proteins ◽

Response To Temperature

An adequate response to a sudden temperature rise is crucial for cellular fitness and survival. While heat shock response (HSR) is well described in bacteria and eukaryotes, much less information is available for archaea, of which many characterized species are extremophiles thriving in habitats typified by large temperature gradients. Here, we describe known molecular aspects of archaeal heat shock proteins (HSPs) as key components of the protein homeostasis machinery and place this in a phylogenetic perspective with respect to bacterial and eukaryotic HSPs. Particular emphasis is placed on structure–function details of the archaeal thermosome, which is a major element of the HSR and of which subunit composition is altered in response to temperature changes. In contrast with the structural response, it is largely unclear how archaeal cells sense temperature fluctuations and which molecular mechanisms underlie the corresponding regulation. We frame this gap in knowledge by discussing emerging questions related to archaeal HSR and by proposing methodologies to address them. Additionally, as has been shown in bacteria and eukaryotes, HSR is expected to be relevant for the control of physiology and growth in various stress conditions beyond temperature stress. A better understanding of this essential cellular process in archaea will not only provide insights into the evolution of HSR and of its sensing and regulation, but also inspire the development of biotechnological applications, by enabling transfer of archaeal heat shock components to other biological systems and for the engineering of archaea as robust cell factories.

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