Dynamic switching between escape and avoidance regimes reduces Caenorhabditis elegans exposure to noxious heat

Schild, Lisa C.; Glauser, Dominique A.

doi:10.1038/ncomms3198

Cited by 38 publications

(52 citation statements)

References 37 publications

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“…Transient exposure to temperatures above 30°C causes an engagement of avoidance and escape locomotor behaviors[7, 8] and an inhibition of pharyngeal pumping[6], a feeding behavior that is normally continuous in the presence of food. Animals removed from a brief (<1 min) heat exposure recover normal activity within minutes (Table S1).…”

Section: Resultsmentioning

confidence: 99%

Cellular Stress Induces a Protective Sleep-like State in C. elegans

et al. 2014

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Summary Sleep is recognized to be ancient in origin, with vertebrates and invertebrates experiencing behaviorally quiescent states that are regulated by conserved genetic mechanisms[1, 2]. Despite its conservation throughout phylogeny the function of sleep remains debated. Hypotheses for the purpose of sleep include nervous system-specific functions such as modulation of synaptic strength and clearance of metabolites from the brain[3, 4], and more generalized cellular functions such as energy conservation and macromolecule biosynthesis[5]. These models are supported by the identification of synaptic and metabolic processes that are perturbed during prolonged wakefulness. It remains to be seen whether perturbations of cellular homeostasis in turn drive sleep. Here we show that under conditions of cellular stress, including noxious heat, cold, hypertonicity, and tissue damage, the nematode Caenorhabditis elegans engages a behavioral quiescence program. The stress-induced quiescent state displays properties of sleep and is dependent on the ALA neuron, which mediates the conserved soporific effect of Epidermal Growth Factor (EGF) ligand overexpression. We characterize heat-induced quiescence in detail and show that it is indeed dependent on components of EGF signaling, providing physiological relevance to the behavioral effects of EGF family ligands. We find that following noxious heat exposure, quiescence-defective animals show elevated expression of cellular stress reporter genes and are impaired for survival, demonstrating the benefit of stress-induced behavioral quiescence. These data provide evidence that cellular stress can induce a protective sleep-like state in C. elegans and suggest that a deeply conserved function of sleep is to mitigate disruptions of cellular homeostasis.

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Section: Resultsmentioning

confidence: 99%

Cellular Stress Induces a Protective Sleep-like State in C. elegans

et al. 2014

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“…In particular, C. elegans efficiently avoids noxious heat (Glauser, 2013; Schild and Glauser, 2013; Wittenburg and Baumeister, 1999) and this behavior is under the control of multiple genetic and neural circuits (Ghosh et al, 2012; Glauser et al, 2011a; Liu et al, 2012; Mohammadi et al, 2013; Wittenburg and Baumeister, 1999). Primary thermoreceptor neurons able to respond to noxious temperatures include the AFD neurons in the head amphid organs (Liu et al, 2012), the polymodal FLP nociceptors in the head (Chatzigeorgiou et al, 2010; Liu et al, 2012), the PVD nociceptors in the mid body (Mohammadi et al, 2013) and the PHC neurons in the tail (Liu et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

The Balance between Cytoplasmic and Nuclear CaM Kinase-1 Signaling Controls the Operating Range of Noxious Heat Avoidance

Schild

Zbinden

Bell

et al. 2014

Neuron

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SUMMARY Through encounters with predators, competitors, and noxious stimuli, animals have evolved defensive responses that minimize injury and are essential for survival. Physiological adaptation modulates the stimulus intensities that trigger such nocifensive behaviors, but the molecular networks that define their operating range are largely unknown. Here, we identify a novel, gain-of-function allele of the cmk-1 CaMKI gene in C. elegans and show that loss of the regulatory domain of the CaMKI enzyme produces thermal analgesia and shifts the operating range for nocifensive heat avoidance to higher temperatures. Such analgesia depends on nuclear CMK-1 signaling, while cytoplasmic CMK-1 signaling lowers the threshold for thermal avoidance. CMK-1 acts downstream of heat detection in thermal receptor neurons and controls neuropeptide release. Our results establish CaMKI as a key regulator of the operating range for nocifensive behaviors, and suggest strategies for producing thermal analgesia through the regulation of CaMKI-dependent signaling.

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“…These animals use noxious heat avoidance to limit damage, thermotaxis to find a preferred temperature in the innocuous temperature range and isothermal tracking to stay close to this preferred temperature [20,[37][38][39]. All three behaviors are modulated by previous temperature experience, implying some sort of memory.…”

Section: Thermosensory Plasticitymentioning

confidence: 99%

Molecules empowering animals to sense and respond to temperature in changing environments

Glauser

Goodman

2016

Current Opinion in Neurobiology

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Adapting behavior to thermal cues is essential for animal growth and survival. Indeed, each and every biological and biochemical process is profoundly affected by temperature and its extremes can cause irreversible damage. Hence, animals have developed thermotransduction mechanisms to detect and encode thermal information in the nervous system and acclimation mechanisms to finely tune their response over different timescales. While temperature-gated TRP channels are the best described class of temperature sensors, recent studies highlight many new candidates, including ionotropic and metabotropic receptors. Here, we review recent findings in vertebrate and invertebrate models, which highlight and substantiate the role of new candidate molecular thermometers and reveal intracellular signaling mechanisms implicated in thermal acclimation at the behavioral and cellular levels. Variations in ambient temperature have dramatic effects on animal behavior, survival, and reproduction. One dramatic example is the response of a waddle of Emperor penguins to variations in ambient temperature: the colder the temperature, the more likely penguins are to huddle and to huddle more tightly [1]. The social behavior of huddling is essential for thermoregulation, energy conservation, and to complete the breeding cycle. Thus, animals have evolved behavioral and metabolic strategies for minimizing their exposure to rapid fluctuations and for adapting to slow seasonal variations. Such thermal acclimation behaviors depend on the animal's ability to link information provided by specialized thermosensory neurons to appropriate behaviors. Laboratory studies in animals that are amenable to genetic dissection such as fruit flies, nematodes, and mice, have revealed many relevant sensory neurons and thermoreceptor proteins. In this review, we consider candidate thermoreceptor proteins and signaling pathways as well as molecular mechanisms for responding to changing thermal environments, highlighting recent key results and emerging opportunities for discovery in this area. Molecular basis of thermosensingTo function as a thermoreceptor, a protein or signaling pathway should exhibit several properties. First, the protein(s) should localize to the presumptive site of temperature-sensing within sensory neurons embedded in tissues subjected to thermal fluctuations [2 ]. Second, the proteins(s) should be required for cellular and behavioral responses to thermal cues. Third, the protein(s) should confer extraordinary temperature sensitivity on heterologous cells and, fourth, protein function should itself be exquisitely temperature-sensitive. Distinguishing ordinary from extraordinary thermal sensitivity is not easy, however. One useful rule of thumb is to focus on proteins or signaling pathways with Q 10 values that exceed those typical of biochemical reactions such as active transport of ions (ca. 3) across biological membranes [3]. Though imperfect (see Ref.[2 ]), the Q 10 metric is frequently used to assess the effect of temperature on cell func...

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Dynamic switching between escape and avoidance regimes reduces Caenorhabditis elegans exposure to noxious heat

Cited by 38 publications

References 37 publications

Cellular Stress Induces a Protective Sleep-like State in C. elegans

Cellular Stress Induces a Protective Sleep-like State in C. elegans

The Balance between Cytoplasmic and Nuclear CaM Kinase-1 Signaling Controls the Operating Range of Noxious Heat Avoidance

Molecules empowering animals to sense and respond to temperature in changing environments

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