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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 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 signalling15. (b) Cold tolerance of mutants with an impaired light-sensing pathway in ASJ neurons, which contains photoreceptor (lite-1), trimeric G protein alpha subunits (goa-1, gpa-1 and gpa-3), guanylyl cyclase (daf-11 and odr-1) and phosphodiesterase (pde-1 to 5). Allele names of double or triple mutants are the same for each single mutant. 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<0.05; **P<0.01. Abbreviations: cGMP, cyclic guanosine monophosphate; Gα, trimeric G protein alpha subunit; GC, guanylyl cyclase; PDE, phosphodiesterase.
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f4: 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 signalling15. (b) Cold tolerance of mutants with an impaired light-sensing pathway in ASJ neurons, which contains photoreceptor (lite-1), trimeric G protein alpha subunits (goa-1, gpa-1 and gpa-3), guanylyl cyclase (daf-11 and odr-1) and phosphodiesterase (pde-1 to 5). Allele names of double or triple mutants are the same for each single mutant. 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<0.05; **P<0.01. Abbreviations: cGMP, cyclic guanosine monophosphate; Gα, trimeric G protein alpha subunit; GC, guanylyl cyclase; PDE, phosphodiesterase.

Mentions: To determine what molecules are involved in temperature signalling in ASJ neurons, we tested mutants defective in phototransduction in ASJ neurons15. We found that mutants of proteins involved in phototransduction in ASJ neurons, including trimeric G protein alpha subunits (gpa-1, gpa-3 or goa-1), guanylyl cyclase (daf-11; odr-1) or phosphodiesterase (pde-1; pde-2), showed abnormalities in cold tolerance (Fig. 4a,b). Although the specific neuron responsible for these abnormalities in cold tolerance was not determined, these results are consistent with a hypothesis that two sensory modalities, light and temperature, are transduced by shared signalling molecules. A lite-1 mutant, lacking a photoreceptor protein expressed in ASJ neurons, showed normal cold tolerance (Fig. 4a,b) and normal calcium concentration changes in ASJ neurons in response to temperature changes (Fig. 3c)15. Therefore, temperature is probably received in ASJ neurons by other receptors.


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 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 signalling15. (b) Cold tolerance of mutants with an impaired light-sensing pathway in ASJ neurons, which contains photoreceptor (lite-1), trimeric G protein alpha subunits (goa-1, gpa-1 and gpa-3), guanylyl cyclase (daf-11 and odr-1) and phosphodiesterase (pde-1 to 5). Allele names of double or triple mutants are the same for each single mutant. 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<0.05; **P<0.01. Abbreviations: cGMP, cyclic guanosine monophosphate; Gα, trimeric G protein alpha subunit; GC, guanylyl cyclase; PDE, phosphodiesterase.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4109018&req=5

f4: 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 signalling15. (b) Cold tolerance of mutants with an impaired light-sensing pathway in ASJ neurons, which contains photoreceptor (lite-1), trimeric G protein alpha subunits (goa-1, gpa-1 and gpa-3), guanylyl cyclase (daf-11 and odr-1) and phosphodiesterase (pde-1 to 5). Allele names of double or triple mutants are the same for each single mutant. 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<0.05; **P<0.01. Abbreviations: cGMP, cyclic guanosine monophosphate; Gα, trimeric G protein alpha subunit; GC, guanylyl cyclase; PDE, phosphodiesterase.
Mentions: To determine what molecules are involved in temperature signalling in ASJ neurons, we tested mutants defective in phototransduction in ASJ neurons15. We found that mutants of proteins involved in phototransduction in ASJ neurons, including trimeric G protein alpha subunits (gpa-1, gpa-3 or goa-1), guanylyl cyclase (daf-11; odr-1) or phosphodiesterase (pde-1; pde-2), showed abnormalities in cold tolerance (Fig. 4a,b). Although the specific neuron responsible for these abnormalities in cold tolerance was not determined, these results are consistent with a hypothesis that two sensory modalities, light and temperature, are transduced by shared signalling molecules. A lite-1 mutant, lacking a photoreceptor protein expressed in ASJ neurons, showed normal cold tolerance (Fig. 4a,b) and normal calcium concentration changes in ASJ neurons in response to temperature changes (Fig. 3c)15. Therefore, temperature is probably received in ASJ neurons by other receptors.

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