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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

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 20 °C, whereas mutants impairing rol-6/cuticle or unc-54/muscles did not show the defect. Strain names and alleles are indicated. For each assay, n≥6. (b) Mutants showing developmental or functional defects in thermotaxis neurons, AFD, AWC, AIY and RIA, did not demonstrate abnormal cold tolerance. tax-6 mutants showed abnormal cold tolerance, which was partially rescued by expressing the tax-6 gene in all neurons (unc-14p::tax-6) or in sensory neurons (tax-6p(1.1 kb)::tax-6)8. The detailed information of these promoters is indicated in the Methods section. For each assay, n≥6. (c,d) Cold tolerance of mutants affecting sensory neurons. Gene products and cells expressing each gene are listed in Supplementary Fig. 2b. Both che-13 and osm-6 mutants showed abnormal increments of cold tolerance after 20 °C cultivation (c). Twenty degree centigrade-cultivated tax-4 and tax-2 mutants, encoding the cGMP-gated channel, showed significant increments in cold tolerance (d). For each assay, n≥6. (e) Cell-specific expression of tax-4 cDNA in tax-4(p678) mutants. The promoters for cell-specific expression used in this experiment were the trx-1 promoter (ASJ), str-3 promoter (ASI) and ceh-36 promoter (AWC). Abnormal cold tolerance in tax-4(p678) was rescued by specific expression of tax-4 cDNA in ASJ sensory neurons. For each assay, n≥6. (f) Laser-killing of ASJ sensory neurons affects normal cold tolerance. ASJ-ablated wild-type animals showed abnormal cold tolerance phenotypes after 20 °C cultivation. The survival rate of ASJ-ablated animals was significantly increased from that of mock-treated wild-type animals. 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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f2: 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 20 °C, whereas mutants impairing rol-6/cuticle or unc-54/muscles did not show the defect. Strain names and alleles are indicated. For each assay, n≥6. (b) Mutants showing developmental or functional defects in thermotaxis neurons, AFD, AWC, AIY and RIA, did not demonstrate abnormal cold tolerance. tax-6 mutants showed abnormal cold tolerance, which was partially rescued by expressing the tax-6 gene in all neurons (unc-14p::tax-6) or in sensory neurons (tax-6p(1.1 kb)::tax-6)8. The detailed information of these promoters is indicated in the Methods section. For each assay, n≥6. (c,d) Cold tolerance of mutants affecting sensory neurons. Gene products and cells expressing each gene are listed in Supplementary Fig. 2b. Both che-13 and osm-6 mutants showed abnormal increments of cold tolerance after 20 °C cultivation (c). Twenty degree centigrade-cultivated tax-4 and tax-2 mutants, encoding the cGMP-gated channel, showed significant increments in cold tolerance (d). For each assay, n≥6. (e) Cell-specific expression of tax-4 cDNA in tax-4(p678) mutants. The promoters for cell-specific expression used in this experiment were the trx-1 promoter (ASJ), str-3 promoter (ASI) and ceh-36 promoter (AWC). Abnormal cold tolerance in tax-4(p678) was rescued by specific expression of tax-4 cDNA in ASJ sensory neurons. For each assay, n≥6. (f) Laser-killing of ASJ sensory neurons affects normal cold tolerance. ASJ-ablated wild-type animals showed abnormal cold tolerance phenotypes after 20 °C cultivation. The survival rate of ASJ-ablated animals was significantly increased from that of mock-treated wild-type animals. 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: We next investigated which tissues were involved in temperature experience-dependent cold tolerance, by examining the phenotypes of various tissue-specific mutants. We found that a mutant with defective unc-104/kinesin in almost all neurons showed abnormal enhancement of cold tolerance after cultivation at 20 °C (Fig. 2a)34. By contrast, mutants with impairments in the cuticle or body wall muscle did not display cold tolerance abnormalities (Fig. 2a). These data suggest that temperature experience-dependent cold tolerance is regulated, at least in part, by neurons. A known-neural circuit for thermotaxis behaviour of C. elegans involves temperature sensing and processing56. We next examined the cold tolerance of mutants defective in the development or function of the temperature-sensing neurons participating in the thermotaxis neural circuit, AFD and AWC, and their downstream interneurons AIY and RIA (Fig. 2b; Supplementary Fig. 2a)567. Developmental or functional defects of these component neurons of the thermotaxis circuit did not lead to abnormal cold tolerance (Fig. 2b), suggesting that this known temperature-processing neural circuit is not essential for temperature experience-dependent cold tolerance. We found that the thermotaxis mutant, tax-6, which lacks calcineurin function in many neurons, had abnormal cold tolerance (Fig. 2b)89. This abnormality was partially rescued by the expression of the tax-6 gene in sensory neurons as well as in almost all neurons (Fig. 2b, tax-6;Ex[unc-14p:: tax-6] (almost all neurons), tax-6;Ex[tax-6p(1.1 kb)::tax-6] (many sensory neurons (amphid and phasmid))). These results imply that sensory neurons are important for cold tolerance. We therefore measured temperature experience-dependent cold tolerance in mutants with defective sensory neurons (Fig. 2c; Supplementary Fig. 2b). Mutant animals with impaired che-13 and osm-6 genes demonstrated severely abnormal cold tolerance after cultivation at 20 °C (Fig. 2c). Both che-13 and osm-6 genes encode components of an intraflagellar transport complex that is essential for cilium function in the sensory ending of sensory neurons (Supplementary Fig. 2b)10111213, suggesting that sensory input may be essential for cold tolerance.


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)

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 20 °C, whereas mutants impairing rol-6/cuticle or unc-54/muscles did not show the defect. Strain names and alleles are indicated. For each assay, n≥6. (b) Mutants showing developmental or functional defects in thermotaxis neurons, AFD, AWC, AIY and RIA, did not demonstrate abnormal cold tolerance. tax-6 mutants showed abnormal cold tolerance, which was partially rescued by expressing the tax-6 gene in all neurons (unc-14p::tax-6) or in sensory neurons (tax-6p(1.1 kb)::tax-6)8. The detailed information of these promoters is indicated in the Methods section. For each assay, n≥6. (c,d) Cold tolerance of mutants affecting sensory neurons. Gene products and cells expressing each gene are listed in Supplementary Fig. 2b. Both che-13 and osm-6 mutants showed abnormal increments of cold tolerance after 20 °C cultivation (c). Twenty degree centigrade-cultivated tax-4 and tax-2 mutants, encoding the cGMP-gated channel, showed significant increments in cold tolerance (d). For each assay, n≥6. (e) Cell-specific expression of tax-4 cDNA in tax-4(p678) mutants. The promoters for cell-specific expression used in this experiment were the trx-1 promoter (ASJ), str-3 promoter (ASI) and ceh-36 promoter (AWC). Abnormal cold tolerance in tax-4(p678) was rescued by specific expression of tax-4 cDNA in ASJ sensory neurons. For each assay, n≥6. (f) Laser-killing of ASJ sensory neurons affects normal cold tolerance. ASJ-ablated wild-type animals showed abnormal cold tolerance phenotypes after 20 °C cultivation. The survival rate of ASJ-ablated animals was significantly increased from that of mock-treated wild-type animals. 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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f2: 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 20 °C, whereas mutants impairing rol-6/cuticle or unc-54/muscles did not show the defect. Strain names and alleles are indicated. For each assay, n≥6. (b) Mutants showing developmental or functional defects in thermotaxis neurons, AFD, AWC, AIY and RIA, did not demonstrate abnormal cold tolerance. tax-6 mutants showed abnormal cold tolerance, which was partially rescued by expressing the tax-6 gene in all neurons (unc-14p::tax-6) or in sensory neurons (tax-6p(1.1 kb)::tax-6)8. The detailed information of these promoters is indicated in the Methods section. For each assay, n≥6. (c,d) Cold tolerance of mutants affecting sensory neurons. Gene products and cells expressing each gene are listed in Supplementary Fig. 2b. Both che-13 and osm-6 mutants showed abnormal increments of cold tolerance after 20 °C cultivation (c). Twenty degree centigrade-cultivated tax-4 and tax-2 mutants, encoding the cGMP-gated channel, showed significant increments in cold tolerance (d). For each assay, n≥6. (e) Cell-specific expression of tax-4 cDNA in tax-4(p678) mutants. The promoters for cell-specific expression used in this experiment were the trx-1 promoter (ASJ), str-3 promoter (ASI) and ceh-36 promoter (AWC). Abnormal cold tolerance in tax-4(p678) was rescued by specific expression of tax-4 cDNA in ASJ sensory neurons. For each assay, n≥6. (f) Laser-killing of ASJ sensory neurons affects normal cold tolerance. ASJ-ablated wild-type animals showed abnormal cold tolerance phenotypes after 20 °C cultivation. The survival rate of ASJ-ablated animals was significantly increased from that of mock-treated wild-type animals. 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: We next investigated which tissues were involved in temperature experience-dependent cold tolerance, by examining the phenotypes of various tissue-specific mutants. We found that a mutant with defective unc-104/kinesin in almost all neurons showed abnormal enhancement of cold tolerance after cultivation at 20 °C (Fig. 2a)34. By contrast, mutants with impairments in the cuticle or body wall muscle did not display cold tolerance abnormalities (Fig. 2a). These data suggest that temperature experience-dependent cold tolerance is regulated, at least in part, by neurons. A known-neural circuit for thermotaxis behaviour of C. elegans involves temperature sensing and processing56. We next examined the cold tolerance of mutants defective in the development or function of the temperature-sensing neurons participating in the thermotaxis neural circuit, AFD and AWC, and their downstream interneurons AIY and RIA (Fig. 2b; Supplementary Fig. 2a)567. Developmental or functional defects of these component neurons of the thermotaxis circuit did not lead to abnormal cold tolerance (Fig. 2b), suggesting that this known temperature-processing neural circuit is not essential for temperature experience-dependent cold tolerance. We found that the thermotaxis mutant, tax-6, which lacks calcineurin function in many neurons, had abnormal cold tolerance (Fig. 2b)89. This abnormality was partially rescued by the expression of the tax-6 gene in sensory neurons as well as in almost all neurons (Fig. 2b, tax-6;Ex[unc-14p:: tax-6] (almost all neurons), tax-6;Ex[tax-6p(1.1 kb)::tax-6] (many sensory neurons (amphid and phasmid))). These results imply that sensory neurons are important for cold tolerance. We therefore measured temperature experience-dependent cold tolerance in mutants with defective sensory neurons (Fig. 2c; Supplementary Fig. 2b). Mutant animals with impaired che-13 and osm-6 genes demonstrated severely abnormal cold tolerance after cultivation at 20 °C (Fig. 2c). Both che-13 and osm-6 genes encode components of an intraflagellar transport complex that is essential for cilium function in the sensory ending of sensory neurons (Supplementary Fig. 2b)10111213, suggesting that sensory input may be essential for cold tolerance.

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