Temperature- and Touch-Sensitive Neurons Couple CNG and TRPV Channel Activities to Control Heat Avoidance in Caenorhabditis elegans

Liu, Shu; Schulze, Ekkehard; Baumeister, Ralf

doi:10.1371/journal.pone.0032360

Cited by 69 publications

(97 citation statements)

References 52 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Given that C. elegans displays isothermal tracking by detecting temperature differences of 0.01°C mm −1 via AFD, humidity gradients probably produce salient temperature cues (12). Alternatively, the FLP neurons may also convey thermal information (although FLP may respond only to noxious heat) (23,35,36). The strategy of assessing thermal cues in parallel to mechanical cues may further disambiguate hygrosensory signals from either single modality.…”

Section: Discussionmentioning

confidence: 99%

Humidity sensation requires both mechanosensory and thermosensory pathways in Caenorhabditis elegans

Russell

Vidal-Gadea

Makay

et al. 2014

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

View full text Add to dashboard Cite

All terrestrial animals must find a proper level of moisture to ensure their health and survival. The cellular-molecular basis for sensing humidity is unknown in most animals, however. We used the model nematode Caenorhabditis elegans to uncover a mechanism for sensing humidity. We found that whereas C. elegans showed no obvious preference for humidity levels under standard culture conditions, worms displayed a strong preference after pairing starvation with different humidity levels, orienting to gradients as shallow as 0.03% relative humidity per millimeter. Cell-specific ablation and rescue experiments demonstrate that orientation to humidity in C. elegans requires the obligatory combination of distinct mechanosensitive and thermosensitive pathways. The mechanosensitive pathway requires a conserved DEG/ENaC/ ASIC mechanoreceptor complex in the FLP neuron pair. Because humidity levels influence the hydration of the worm's cuticle, our results suggest that FLP may convey humidity information by reporting the degree that subcuticular dendritic sensory branches of FLP neurons are stretched by hydration. The thermosensitive pathway requires cGMP-gated channels in the AFD neuron pair. Because humidity levels affect evaporative cooling, AFD may convey humidity information by reporting thermal flux. Thus, humidity sensation arises as a metamodality in C. elegans that requires the integration of parallel mechanosensory and thermosensory pathways. This hygrosensation strategy, first proposed by Thunberg more than 100 y ago, may be conserved because the underlying pathways have cellular and molecular equivalents across a wide range of species, including insects and humans. mechanosensation | thermosensation M oisture is essential for life. As such, many animals have adapted different behavioral mechanisms to migrate toward their preferred moisture level (hygrotaxis) (1-6). For instance, Drosophila avoid high humidity that impedes flight, whereas green frogs orient toward high humidity to maintain hydration (5, 6). Animals also sense moisture levels to determine important information about their environment; for example, moths detect humidity levels around flowers to deduce which ones might be damaged and contain less nectar (7). These behaviors are often critical to keep an animal within its niche and regulate essential processes such as growth and reproduction. Thus, it is surprising that the molecular basis for how different humidity levels are detected and encoded by the nervous system (hygrosensation) remains unknown in most animals.The search for humidity receptors has achieved the most progress in insects. For instance, distinct sets of hygrosensitive neurons have been found in dome-shaped organs on the antenna of the giant cockroach (8). One set activates with moist air, and the other set responds to dry air. Similar moist and dry receptive neurons have been detected in the branched arista subsegment of the antennae in adult Drosophila (9). Removal of the arista or deletion of any one of three TRP channels expres...

show abstract

Section: Discussionmentioning

confidence: 99%

Humidity sensation requires both mechanosensory and thermosensory pathways in Caenorhabditis elegans

Russell

Vidal-Gadea

Makay

et al. 2014

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

View full text Add to dashboard Cite

show abstract

“…AFD neuron is the best studied heat-sensitive neuron in C. elegans (Garrity et al 2010; Mori et al 2007). In addition, AWC, ASI, FLP and PHC neurons may also play a role in sensing heat (Chatzigeorgiou et al 2010; Liu et al 2012; Mohammadi et al 2013; Mori et al 2007). Interestingly, PVD neuron can respond to both heat and cold in C. elegans (Chatzigeorgiou et al 2010; Mohammadi et al 2013; Xiao et al 2013).…”

Section: Molecular Sensors Of Temperaturementioning

confidence: 99%

Thermosensation and longevity

Xiao

Liu

2015

J Comp Physiol A

View full text Add to dashboard Cite

Temperature has profound effects on behavior and aging in both poikilotherms and homeotherms. To thrive under the ever fluctuating environmental temperatures, animals have evolved sophisticated mechanisms to sense and adapt to temperature changes. Animals sense temperature through various molecular thermosensors, such as thermosensitive TRP channels expressed in neurons, keratinocytes, and intestine. These evolutionarily conserved thermosensitive TRP channels feature distinct activation thresholds, thereby covering a wide spectrum of ambient temperature. Temperature changes trigger complex thermosensory behaviors. Due to the simplicity of the nervous system in model organisms such as C. elegans and Drosophila, the mechanisms of thermosensory behaviors in these species have been extensively studied at the circuit and molecular levels. While much is known about temperature regulation of behavior, it remains largely unclear how temperature affects aging. Recent studies in C. elegans demonstrate that temperature modulation of longevity is not simply a passive thermodynamic phenomenon as suggested by the rate-of-living theory, but rather a process that is actively regulated by genes, including those encoding thermosensitive TRP channels. In this review, we discuss our current understanding of thermosensation and its role in aging.

show abstract

“…However, the role of a CNGC in these pathways has not been established, and it should be noted that animals (and plants) have other potential cNMP-activated enzymes (Bridges et al, 2005). Nevertheless, a genetic knockout of a CNGC in Caenorhabditis elegans provides evidence for an animal CNGC pathway being involved in thermosensing (Cho et al, 2004;Hellman and Shen, 2011;Liu et al, 2012).…”

Section: A General Model For a Cnmp-triggered Heat Stress Responsementioning

confidence: 99%

A Cyclic Nucleotide-Gated Channel (CNGC16) in Pollen Is Critical for Stress Tolerance in Pollen Reproductive Development

et al. 2012

View full text Add to dashboard Cite

Cyclic nucleotide-gated channels (CNGCs) have been implicated in diverse aspects of plant growth and development, including responses to biotic and abiotic stress, as well as pollen tube growth and fertility. Here, genetic evidence identifies CNGC16 in Arabidopsis (Arabidopsis thaliana) as critical for pollen fertility under conditions of heat stress and drought. Two independent transfer DNA disruptions of cngc16 resulted in a greater than 10-fold stress-dependent reduction in pollen fitness and seed set. This phenotype was fully rescued through pollen expression of a CNGC16 transgene, indicating that cngc16-1 and 16-2 were both loss-of-function null alleles. The most stress-sensitive period for cngc16 pollen was during germination and the initiation of pollen tube tip growth. Pollen viability assays indicate that mutant pollen are also hypersensitive to external calcium chloride, a phenomenon analogous to calcium chloride hypersensitivities observed in other cngc mutants. A heat stress was found to increase concentrations of 39,59-cyclic guanyl monophosphate in both pollen and leaves, as detected using an antibody-binding assay. A quantitative PCR analysis indicates that cngc16 mutant pollen have attenuated expression of several heat-stress response genes, including two heat shock transcription factor genes, HsfA2 and HsfB1. Together, these results provide evidence for a heat stress response pathway in pollen that connects a cyclic nucleotide signal, a Ca 2+ -permeable ion channel, and a signaling network that activates a downstream transcriptional heat shock response.

show abstract

Temperature- and Touch-Sensitive Neurons Couple CNG and TRPV Channel Activities to Control Heat Avoidance in Caenorhabditis elegans

Cited by 69 publications

References 52 publications

Humidity sensation requires both mechanosensory and thermosensory pathways in Caenorhabditis elegans

Humidity sensation requires both mechanosensory and thermosensory pathways in Caenorhabditis elegans

Thermosensation and longevity

A Cyclic Nucleotide-Gated Channel (CNGC16) in Pollen Is Critical for Stress Tolerance in Pollen Reproductive Development

Contact Info

Product

Resources

About