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Bidirectional regulation of thermotaxis by glutamate transmissions in Caenorhabditis elegans.

Ohnishi N, Kuhara A, Nakamura F, Okochi Y, Mori I - EMBO J. (2011)

Bottom Line: EAT-4/VGLUT (vesicular glutamate transporter)-dependent glutamate signals from AFD thermosensory neurons inhibit the postsynaptic AIY interneurons through activation of GLC-3/GluCl inhibitory glutamate receptor and behaviourally drive migration towards colder temperature.By contrast, EAT-4-dependent glutamate signals from AWC thermosensory neurons stimulate the AIY neurons to induce migration towards warmer temperature.Alteration of the strength of AFD and AWC signals led to significant changes of AIY activity, resulting in drastic modulation of behaviour.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Molecular Neurobiology, Division of Biological Science, Department of Molecular Biology, Graduate School of Science, Nagoya University, Nagoya, Aichi, Japan.

ABSTRACT
In complex neural circuits of the brain, massive information is processed with neuronal communication through synaptic transmissions. It is thus fundamental to delineate information flows encoded by various kinds of transmissions. Here, we show that glutamate signals from two distinct sensory neurons bidirectionally affect the same postsynaptic interneuron, thereby producing the opposite behaviours. EAT-4/VGLUT (vesicular glutamate transporter)-dependent glutamate signals from AFD thermosensory neurons inhibit the postsynaptic AIY interneurons through activation of GLC-3/GluCl inhibitory glutamate receptor and behaviourally drive migration towards colder temperature. By contrast, EAT-4-dependent glutamate signals from AWC thermosensory neurons stimulate the AIY neurons to induce migration towards warmer temperature. Alteration of the strength of AFD and AWC signals led to significant changes of AIY activity, resulting in drastic modulation of behaviour. We thus provide an important insight on information processing, in which two glutamate transmissions encoding opposite information flows regulate neural activities to produce a large spectrum of behavioural outputs.

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Related in: MedlinePlus

Cell-specific rescue experiments for thermotaxis defects of eat-4(ky5) mutants. (A) Rescue experiments for defective isothermal tracking (IT behaviour) of eat-4(ky5) mutants by introducing cell-specific promoters∷eat-4 cDNA at 5 ng/μl; n=58 or more animals. Error bar indicates s.e.m. Single and double asterisk indicate P<0.05 and 0.01, respectively, in ANOVA for a comparison with eat-4(ky5) mutants. (B, C) Rescue experiments for defective migration to cultivation temperature of eat-4(ky5) mutants by introducing individual cell-specific promoters∷eat-4 cDNA at 5 ng/μl (B) or by introducing AFDp∷eat-4 cDNA, AWCp∷eat-4 cDNA, and RIAp∷eat-4 cDNA simultaneously at several doses (C); n=3 or more assays. Error bars indicate s.e.m. Single asterisk, double asterisk, and NS indicate P<0.05, P<0.01, and P>0.05 respectively, in post hoc Tukey–Kramer tests for a comparison with eat-4(ky5) mutants (B) and for a comparison of each genotype (C). (D) The population thermotaxis assays of eat-4 transgenic mutants carrying genetically abnormal function in RIA. eat-4 (AFD+) represents the transgenic eat-4(ky5) mutants expressing EAT-4 in AFD; n=⩾3 assays. Error bars indicate s.e.m. Double asterisk and NS indicate P<0.01 and P>0.05, respectively, in post hoc Tukey–Kramer tests for a comparison of each genotype.
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f3: Cell-specific rescue experiments for thermotaxis defects of eat-4(ky5) mutants. (A) Rescue experiments for defective isothermal tracking (IT behaviour) of eat-4(ky5) mutants by introducing cell-specific promoters∷eat-4 cDNA at 5 ng/μl; n=58 or more animals. Error bar indicates s.e.m. Single and double asterisk indicate P<0.05 and 0.01, respectively, in ANOVA for a comparison with eat-4(ky5) mutants. (B, C) Rescue experiments for defective migration to cultivation temperature of eat-4(ky5) mutants by introducing individual cell-specific promoters∷eat-4 cDNA at 5 ng/μl (B) or by introducing AFDp∷eat-4 cDNA, AWCp∷eat-4 cDNA, and RIAp∷eat-4 cDNA simultaneously at several doses (C); n=3 or more assays. Error bars indicate s.e.m. Single asterisk, double asterisk, and NS indicate P<0.05, P<0.01, and P>0.05 respectively, in post hoc Tukey–Kramer tests for a comparison with eat-4(ky5) mutants (B) and for a comparison of each genotype (C). (D) The population thermotaxis assays of eat-4 transgenic mutants carrying genetically abnormal function in RIA. eat-4 (AFD+) represents the transgenic eat-4(ky5) mutants expressing EAT-4 in AFD; n=⩾3 assays. Error bars indicate s.e.m. Double asterisk and NS indicate P<0.01 and P>0.05, respectively, in post hoc Tukey–Kramer tests for a comparison of each genotype.

Mentions: Consistent with the important neural function of EAT-4, expression of eat-4 cDNA from its own promoter (5.5 kb) and in all neurons strongly rescued the IT behaviour defect of eat-4(ky5) mutants (50±2% and 31±2%, respectively, Figure 3A) and restored normal migrations to cultivation temperature (P>0.05 compared with wild-type animals at every cultivation temperature; Figure 3B). To identify the neurons in which EAT-4 functions for thermotaxis, we introduced eat-4 cDNA under the control of various cell-specific promoters into eat-4(ky5) mutants. Expression of EAT-4 in AFD, AWC, or AIZ did not rescue IT behaviour defect of eat-4(ky5) mutants (0%), whereas expression of EAT-4 in RIA weakly did (10±2%; Figure 3A). Remarkably, simultaneous expression of EAT-4 in AFD and RIA rescued the defect (39±1%) as strongly as the transgenic animals expressing EAT-4 from the eat-4 promoter (P>0.05; Figure 3A). The rescue efficiency of the animals expressing EAT-4 in AFD and RIA was not increased by additional expression of EAT-4 in other neurons (Figure 3A). These results suggest that EAT-4-dependent glutamate transmission from RIA to downstream motor neurons is critical for conveying thermal information from AFD.


Bidirectional regulation of thermotaxis by glutamate transmissions in Caenorhabditis elegans.

Ohnishi N, Kuhara A, Nakamura F, Okochi Y, Mori I - EMBO J. (2011)

Cell-specific rescue experiments for thermotaxis defects of eat-4(ky5) mutants. (A) Rescue experiments for defective isothermal tracking (IT behaviour) of eat-4(ky5) mutants by introducing cell-specific promoters∷eat-4 cDNA at 5 ng/μl; n=58 or more animals. Error bar indicates s.e.m. Single and double asterisk indicate P<0.05 and 0.01, respectively, in ANOVA for a comparison with eat-4(ky5) mutants. (B, C) Rescue experiments for defective migration to cultivation temperature of eat-4(ky5) mutants by introducing individual cell-specific promoters∷eat-4 cDNA at 5 ng/μl (B) or by introducing AFDp∷eat-4 cDNA, AWCp∷eat-4 cDNA, and RIAp∷eat-4 cDNA simultaneously at several doses (C); n=3 or more assays. Error bars indicate s.e.m. Single asterisk, double asterisk, and NS indicate P<0.05, P<0.01, and P>0.05 respectively, in post hoc Tukey–Kramer tests for a comparison with eat-4(ky5) mutants (B) and for a comparison of each genotype (C). (D) The population thermotaxis assays of eat-4 transgenic mutants carrying genetically abnormal function in RIA. eat-4 (AFD+) represents the transgenic eat-4(ky5) mutants expressing EAT-4 in AFD; n=⩾3 assays. Error bars indicate s.e.m. Double asterisk and NS indicate P<0.01 and P>0.05, respectively, in post hoc Tukey–Kramer tests for a comparison of each genotype.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC3094115&req=5

f3: Cell-specific rescue experiments for thermotaxis defects of eat-4(ky5) mutants. (A) Rescue experiments for defective isothermal tracking (IT behaviour) of eat-4(ky5) mutants by introducing cell-specific promoters∷eat-4 cDNA at 5 ng/μl; n=58 or more animals. Error bar indicates s.e.m. Single and double asterisk indicate P<0.05 and 0.01, respectively, in ANOVA for a comparison with eat-4(ky5) mutants. (B, C) Rescue experiments for defective migration to cultivation temperature of eat-4(ky5) mutants by introducing individual cell-specific promoters∷eat-4 cDNA at 5 ng/μl (B) or by introducing AFDp∷eat-4 cDNA, AWCp∷eat-4 cDNA, and RIAp∷eat-4 cDNA simultaneously at several doses (C); n=3 or more assays. Error bars indicate s.e.m. Single asterisk, double asterisk, and NS indicate P<0.05, P<0.01, and P>0.05 respectively, in post hoc Tukey–Kramer tests for a comparison with eat-4(ky5) mutants (B) and for a comparison of each genotype (C). (D) The population thermotaxis assays of eat-4 transgenic mutants carrying genetically abnormal function in RIA. eat-4 (AFD+) represents the transgenic eat-4(ky5) mutants expressing EAT-4 in AFD; n=⩾3 assays. Error bars indicate s.e.m. Double asterisk and NS indicate P<0.01 and P>0.05, respectively, in post hoc Tukey–Kramer tests for a comparison of each genotype.
Mentions: Consistent with the important neural function of EAT-4, expression of eat-4 cDNA from its own promoter (5.5 kb) and in all neurons strongly rescued the IT behaviour defect of eat-4(ky5) mutants (50±2% and 31±2%, respectively, Figure 3A) and restored normal migrations to cultivation temperature (P>0.05 compared with wild-type animals at every cultivation temperature; Figure 3B). To identify the neurons in which EAT-4 functions for thermotaxis, we introduced eat-4 cDNA under the control of various cell-specific promoters into eat-4(ky5) mutants. Expression of EAT-4 in AFD, AWC, or AIZ did not rescue IT behaviour defect of eat-4(ky5) mutants (0%), whereas expression of EAT-4 in RIA weakly did (10±2%; Figure 3A). Remarkably, simultaneous expression of EAT-4 in AFD and RIA rescued the defect (39±1%) as strongly as the transgenic animals expressing EAT-4 from the eat-4 promoter (P>0.05; Figure 3A). The rescue efficiency of the animals expressing EAT-4 in AFD and RIA was not increased by additional expression of EAT-4 in other neurons (Figure 3A). These results suggest that EAT-4-dependent glutamate transmission from RIA to downstream motor neurons is critical for conveying thermal information from AFD.

Bottom Line: EAT-4/VGLUT (vesicular glutamate transporter)-dependent glutamate signals from AFD thermosensory neurons inhibit the postsynaptic AIY interneurons through activation of GLC-3/GluCl inhibitory glutamate receptor and behaviourally drive migration towards colder temperature.By contrast, EAT-4-dependent glutamate signals from AWC thermosensory neurons stimulate the AIY neurons to induce migration towards warmer temperature.Alteration of the strength of AFD and AWC signals led to significant changes of AIY activity, resulting in drastic modulation of behaviour.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Molecular Neurobiology, Division of Biological Science, Department of Molecular Biology, Graduate School of Science, Nagoya University, Nagoya, Aichi, Japan.

ABSTRACT
In complex neural circuits of the brain, massive information is processed with neuronal communication through synaptic transmissions. It is thus fundamental to delineate information flows encoded by various kinds of transmissions. Here, we show that glutamate signals from two distinct sensory neurons bidirectionally affect the same postsynaptic interneuron, thereby producing the opposite behaviours. EAT-4/VGLUT (vesicular glutamate transporter)-dependent glutamate signals from AFD thermosensory neurons inhibit the postsynaptic AIY interneurons through activation of GLC-3/GluCl inhibitory glutamate receptor and behaviourally drive migration towards colder temperature. By contrast, EAT-4-dependent glutamate signals from AWC thermosensory neurons stimulate the AIY neurons to induce migration towards warmer temperature. Alteration of the strength of AFD and AWC signals led to significant changes of AIY activity, resulting in drastic modulation of behaviour. We thus provide an important insight on information processing, in which two glutamate transmissions encoding opposite information flows regulate neural activities to produce a large spectrum of behavioural outputs.

Show MeSH
Related in: MedlinePlus