🏆 Foundational Paper

Light and pheromone-sensing neurons regulates cold habituation through insulin signalling in Caenorhabditis elegans.

Ohta Akane, Ujisawa Tomoyo, Sonoda Satoru, Kuhara Atsushi

📰 Nature communications 📅 2014 📊 101 citations

Abstract

Temperature is a critical environmental stimulus that has a strong impact on an organism's biochemistry. Animals can respond to changes in ambient temperature through behaviour or altered physiology. However, how animals habituate to temperature is poorly understood. The nematode C. elegans stores temperature experiences and can induce temperature habituation-linked cold tolerance. Here we show that light and pheromone-sensing neurons (ASJ) regulate cold habituation through insulin signalling. Calcium imaging reveals that ASJ neurons respond to temperature. Cold habituation is abnormal in a mutant with impaired cGMP signalling in ASJ neurons. Insulin released from ASJ neurons is received by the intestine and neurons regulating gene expression for cold habituation. Thus, temperature sensation in a light and pheromone-sensing neuron produces a robust effect on insulin signalling that controls experience-dependent temperature habituation.

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📋 Methods

✔ Verified methods section 1,294 words Read on PMC ↗

Statistical analysis

All error bars in the figures, including those in the Supplementary Information , indicate standard error of mean. All statistical analyses in the figures, including those in the Supplementary Information , were performed by one-way analysis of variance for multiple comparisons, which were followed by Dunnet post-hoc tests. All single asterisk (*) and double asterisk (**) in the figures indicate P

📊 Figures

Figure 1

Temperature experience-inducing cold tolerance phenotype in wild type.

N2 (Bristol) strain was used as the wild-type animal in all experiments for this figure. ( a ) Cultivation temperature-dependent cold tolerance. Twenty to twenty-five degree centigrade-cultivated anim...

Figure 2

ASJ sensory neurons are essential for cold tolerance.

( a ) Mutants impairing specific tissue functions. Mutant impairing unc-104 /kinesin expression in neurons showed abnormal cold tolerance after cultivation at 20u2009u00b0C, whereas mutants impairing ...

Figure 3

Neural activity of ASJ sensory neuron with temperature stimuli.

( a ) Wild type and mutant expressing yellow cameleon driven by trx-1 promoter, trx-1p::yc3.60 (pTOM13), were tested by calcium imaging. Representative fluorescence resonance energy transfer signal in...

Figure 4

Temperature information is processed through the cGMP pathway in ASJ neurons.

( a ) A molecular model of phototransduction in ASJ neurons, which is mediated by trimeric G-proteins and cGMP-dependent signalling 15 . ( b ) Cold tolerance of mutants with an impaired light-sensing ...

Figure 5

Insulin signalling is involved in cold tolerance.

( a ) Cold tolerance of mutants with impaired synaptic transmission containing carboxypeptidase ( egl-21 ), synaptotagmin ( snt-1 ), synaptobrevin ( snb-1 ) and syntaxin (unc-64 ). These mutants showe...

Figure 6

Insulin signalling regulates gene expression during cold tolerance.

( a ) Temperature experience-dependent cold tolerance of mutants defective in insulin signalling, TGF-u03b2 signalling or steroid hormone signalling. Mutants defective in insulin signalling showed abn...

Figure 7

Downstream molecules of insulin signalling in cold tolerance.

( a ) Cold tolerance of mutant animals with impaired genes identified from previous DNA microarray analysis were used to measure temperature change-dependent gene expression 34 . The gene and encoding...

Figure images are served from the NIH/NLM PubMed Central Open Access Subset or Europe PMC; copyright remains with the publishers and authors.

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