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

Ohta A, Ujisawa T, Sonoda S, Kuhara A - Nat Commun (2014)

Bottom Line: However, how animals habituate to temperature is poorly understood.Calcium imaging reveals that ASJ neurons respond to temperature.Thus, temperature sensation in a light and pheromone-sensing neuron produces a robust effect on insulin signalling that controls experience-dependent temperature habituation.

View Article: PubMed Central - PubMed

Affiliation: 1] Laboratory of Molecular and Cellular Regulation, Faculty of Science and Engineering, Institute for Integrative Neurobiology, Konan University, 8-9-1 Okamoto, Higashinada-ku, Kobe 658-8501, Japan [2].

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.

No MeSH data available.


Related in: MedlinePlus

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 animals cannot live after cultivation at 2 °C for 48 h, while 13–17 °C-cultivated animals can live after 48 h at 2 °C. (b) Effect of cold-shock temperatures (0, 1, 2 and 4 °C). Fifteen degree centigrade-cultivated animals can survive at 2 and 4 °C. Twenty degree centigrade-cultivated animals can survive at 4 °C. Twenty-five degree centigrade-cultivated animals cannot survive at 0–4 °C. For each assay, n≥6. (c) Effect of cultivation temperatures (from 13–27 °C). Thirteen to fifteen degree centigrade-cultivated animals can survive at 2 °C, while 20–27 °C-cultivated animals cannot survive at 2 °C. For each assay, n≥6. (d,e) Temperature shift experiments using L1 to L4 stage larvae (15–25 °C (d) or 25–15 °C (e)). Worms are initially cultivated at the first temperature (15 °C (d) or 25 °C (e)) from egg to each larval stage, and then worms were transferred to the second temperature (25 °C (d) or 15 °C (e)) and cultivated until they reached adult stage. After the adult worms were subjected to cold shock (2 °C, 48 h), survival rate was calculated. Cold tolerance is not dependent on the temperature experience at the larval stage. For each assay, n≥6. (f,g) Temperature shift experiments at the adult stage (25–15 °C (f) or 20–15 °C (g)). Worms were cultivated at the first temperature (25 °C (f) or 20 °C (g)) until they reached the adult stage, and then worms were transferred to the second temperature (15 °C (f,g)) and cultivated for specific times (0–12 h indicated on the horizontal axis). After the temperature shifted-adult worms were subjected to cold shock (2 °C, 48 h), survival rate was calculated. About 3 h after the cultivation temperature was changed, cold tolerance was acquired. For each assay, n≥6. Error bars indicate standard error of the mean. analysis of variance followed by Dunnet post-hoc test was used for multiple comparisons. **P<0.01.
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f1: 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 animals cannot live after cultivation at 2 °C for 48 h, while 13–17 °C-cultivated animals can live after 48 h at 2 °C. (b) Effect of cold-shock temperatures (0, 1, 2 and 4 °C). Fifteen degree centigrade-cultivated animals can survive at 2 and 4 °C. Twenty degree centigrade-cultivated animals can survive at 4 °C. Twenty-five degree centigrade-cultivated animals cannot survive at 0–4 °C. For each assay, n≥6. (c) Effect of cultivation temperatures (from 13–27 °C). Thirteen to fifteen degree centigrade-cultivated animals can survive at 2 °C, while 20–27 °C-cultivated animals cannot survive at 2 °C. For each assay, n≥6. (d,e) Temperature shift experiments using L1 to L4 stage larvae (15–25 °C (d) or 25–15 °C (e)). Worms are initially cultivated at the first temperature (15 °C (d) or 25 °C (e)) from egg to each larval stage, and then worms were transferred to the second temperature (25 °C (d) or 15 °C (e)) and cultivated until they reached adult stage. After the adult worms were subjected to cold shock (2 °C, 48 h), survival rate was calculated. Cold tolerance is not dependent on the temperature experience at the larval stage. For each assay, n≥6. (f,g) Temperature shift experiments at the adult stage (25–15 °C (f) or 20–15 °C (g)). Worms were cultivated at the first temperature (25 °C (f) or 20 °C (g)) until they reached the adult stage, and then worms were transferred to the second temperature (15 °C (f,g)) and cultivated for specific times (0–12 h indicated on the horizontal axis). After the temperature shifted-adult worms were subjected to cold shock (2 °C, 48 h), survival rate was calculated. About 3 h after the cultivation temperature was changed, cold tolerance was acquired. For each assay, n≥6. Error bars indicate standard error of the mean. analysis of variance followed by Dunnet post-hoc test was used for multiple comparisons. **P<0.01.

Mentions: As previously reported by Murray et al.1 and Savory et al.2, C. elegans has a cultivation temperature-dependent cold tolerance. Wild-type animals cultivated at 20 or 25 °C were killed by cold shock. In contrast, most wild-type animals cultivated at 15 °C survived after cold shock (Fig. 1a). To examine the conditions of temperature experience-dependent cold tolerance in detail, we used varying cold-shock temperatures (0–4 °C) (Fig. 1b), cultivation temperatures (13–27 °C) (Fig. 1c) and cold-shock times (6–240 h) (Supplementary Fig. 1a–c). Cold tolerance decreased when cultivation temperature was higher, when cold-shock temperature was lower and when cold-shock time was longer. We used 2 °C for 48 h as a typical cold-shock treatment for the majority of the following experiments. To determine whether cold tolerance was established at a specific developmental stage, we performed temperature shift experiments using larvae between the L1 and L4 stages (Fig. 1d,e). We found that a shift of cultivation temperature at larval stages did not severely affect the cold tolerance of adult animals (Fig. 1d,e). To understand how long it takes for cold tolerance to be established in adult animals, we shifted the temperature of adult animals (Fig. 1f,g). Unexpectedly, cold tolerance was established only 2–3 h after the cultivation temperature was changed from 25 to 15 °C (Fig. 1f) or from 20 to 15 °C (Fig. 1g). Furthermore, cold tolerance was diminished 2–3 h after the cultivation temperature was changed from 15 to 25 °C (Supplementary Fig. 1d) or 20 to 25 °C (Supplementary Fig. 1e). Detailed-phenotypic analyses indicated that temperature experience for the formation of cold tolerance can be overwritten within 2–3 h.


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

Ohta A, Ujisawa T, Sonoda S, Kuhara A - Nat Commun (2014)

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 animals cannot live after cultivation at 2 °C for 48 h, while 13–17 °C-cultivated animals can live after 48 h at 2 °C. (b) Effect of cold-shock temperatures (0, 1, 2 and 4 °C). Fifteen degree centigrade-cultivated animals can survive at 2 and 4 °C. Twenty degree centigrade-cultivated animals can survive at 4 °C. Twenty-five degree centigrade-cultivated animals cannot survive at 0–4 °C. For each assay, n≥6. (c) Effect of cultivation temperatures (from 13–27 °C). Thirteen to fifteen degree centigrade-cultivated animals can survive at 2 °C, while 20–27 °C-cultivated animals cannot survive at 2 °C. For each assay, n≥6. (d,e) Temperature shift experiments using L1 to L4 stage larvae (15–25 °C (d) or 25–15 °C (e)). Worms are initially cultivated at the first temperature (15 °C (d) or 25 °C (e)) from egg to each larval stage, and then worms were transferred to the second temperature (25 °C (d) or 15 °C (e)) and cultivated until they reached adult stage. After the adult worms were subjected to cold shock (2 °C, 48 h), survival rate was calculated. Cold tolerance is not dependent on the temperature experience at the larval stage. For each assay, n≥6. (f,g) Temperature shift experiments at the adult stage (25–15 °C (f) or 20–15 °C (g)). Worms were cultivated at the first temperature (25 °C (f) or 20 °C (g)) until they reached the adult stage, and then worms were transferred to the second temperature (15 °C (f,g)) and cultivated for specific times (0–12 h indicated on the horizontal axis). After the temperature shifted-adult worms were subjected to cold shock (2 °C, 48 h), survival rate was calculated. About 3 h after the cultivation temperature was changed, cold tolerance was acquired. For each assay, n≥6. Error bars indicate standard error of the mean. analysis of variance followed by Dunnet post-hoc test was used for multiple comparisons. **P<0.01.
© Copyright Policy - open-access
Related In: Results  -  Collection

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f1: 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 animals cannot live after cultivation at 2 °C for 48 h, while 13–17 °C-cultivated animals can live after 48 h at 2 °C. (b) Effect of cold-shock temperatures (0, 1, 2 and 4 °C). Fifteen degree centigrade-cultivated animals can survive at 2 and 4 °C. Twenty degree centigrade-cultivated animals can survive at 4 °C. Twenty-five degree centigrade-cultivated animals cannot survive at 0–4 °C. For each assay, n≥6. (c) Effect of cultivation temperatures (from 13–27 °C). Thirteen to fifteen degree centigrade-cultivated animals can survive at 2 °C, while 20–27 °C-cultivated animals cannot survive at 2 °C. For each assay, n≥6. (d,e) Temperature shift experiments using L1 to L4 stage larvae (15–25 °C (d) or 25–15 °C (e)). Worms are initially cultivated at the first temperature (15 °C (d) or 25 °C (e)) from egg to each larval stage, and then worms were transferred to the second temperature (25 °C (d) or 15 °C (e)) and cultivated until they reached adult stage. After the adult worms were subjected to cold shock (2 °C, 48 h), survival rate was calculated. Cold tolerance is not dependent on the temperature experience at the larval stage. For each assay, n≥6. (f,g) Temperature shift experiments at the adult stage (25–15 °C (f) or 20–15 °C (g)). Worms were cultivated at the first temperature (25 °C (f) or 20 °C (g)) until they reached the adult stage, and then worms were transferred to the second temperature (15 °C (f,g)) and cultivated for specific times (0–12 h indicated on the horizontal axis). After the temperature shifted-adult worms were subjected to cold shock (2 °C, 48 h), survival rate was calculated. About 3 h after the cultivation temperature was changed, cold tolerance was acquired. For each assay, n≥6. Error bars indicate standard error of the mean. analysis of variance followed by Dunnet post-hoc test was used for multiple comparisons. **P<0.01.
Mentions: As previously reported by Murray et al.1 and Savory et al.2, C. elegans has a cultivation temperature-dependent cold tolerance. Wild-type animals cultivated at 20 or 25 °C were killed by cold shock. In contrast, most wild-type animals cultivated at 15 °C survived after cold shock (Fig. 1a). To examine the conditions of temperature experience-dependent cold tolerance in detail, we used varying cold-shock temperatures (0–4 °C) (Fig. 1b), cultivation temperatures (13–27 °C) (Fig. 1c) and cold-shock times (6–240 h) (Supplementary Fig. 1a–c). Cold tolerance decreased when cultivation temperature was higher, when cold-shock temperature was lower and when cold-shock time was longer. We used 2 °C for 48 h as a typical cold-shock treatment for the majority of the following experiments. To determine whether cold tolerance was established at a specific developmental stage, we performed temperature shift experiments using larvae between the L1 and L4 stages (Fig. 1d,e). We found that a shift of cultivation temperature at larval stages did not severely affect the cold tolerance of adult animals (Fig. 1d,e). To understand how long it takes for cold tolerance to be established in adult animals, we shifted the temperature of adult animals (Fig. 1f,g). Unexpectedly, cold tolerance was established only 2–3 h after the cultivation temperature was changed from 25 to 15 °C (Fig. 1f) or from 20 to 15 °C (Fig. 1g). Furthermore, cold tolerance was diminished 2–3 h after the cultivation temperature was changed from 15 to 25 °C (Supplementary Fig. 1d) or 20 to 25 °C (Supplementary Fig. 1e). Detailed-phenotypic analyses indicated that temperature experience for the formation of cold tolerance can be overwritten within 2–3 h.

Bottom Line: However, how animals habituate to temperature is poorly understood.Calcium imaging reveals that ASJ neurons respond to temperature.Thus, temperature sensation in a light and pheromone-sensing neuron produces a robust effect on insulin signalling that controls experience-dependent temperature habituation.

View Article: PubMed Central - PubMed

Affiliation: 1] Laboratory of Molecular and Cellular Regulation, Faculty of Science and Engineering, Institute for Integrative Neurobiology, Konan University, 8-9-1 Okamoto, Higashinada-ku, Kobe 658-8501, Japan [2].

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.

No MeSH data available.


Related in: MedlinePlus