TY - JOUR
T1 - EGL-4/PKG regulates the role of an interneuron in a chemotaxis circuit of C. elegans through mediating integration of sensory signals
AU - Hino, Takahiro
AU - Hirai, Shota
AU - Ishihara, Takeshi
AU - Fujiwara, Manabi
N1 - Funding Information:
This work was supported by a Japan Society for the Promotion of Science (JSPS) Research Fellows (JP18J11948 to T.H.) and by JSPS KAKENHI (JP23370002, JP25115009, JP18H05135, JP17H06113, and JP19H03326 to T.I. and JP17K07503 to M.F.). We thank Yuichi Iino for JN578 (AIB ablated strain) and JN580 (AIA ablated strain), Tokumitsu Wakabayashi for the AWB and AWC ablated strain, Oliver Hobert for pOH22 and pOH443 plasmids, the Caenorhabditis Genetics Center for strains, and Noriko Sato for technical assistance. We thank Jeremy Allen, PhD, from Edanz Group (https://en-author-services.edanz.com/ac) for editing a draft of this manuscript.
Funding Information:
This work was supported by a Japan Society for the Promotion of Science (JSPS) Research Fellows (JP18J11948 to T.H.) and by JSPS KAKENHI (JP23370002, JP25115009, JP18H05135, JP17H06113, and JP19H03326 to T.I. and JP17K07503 to M.F.). We thank Yuichi Iino for JN578 (AIB ablated strain) and JN580 (AIA ablated strain), Tokumitsu Wakabayashi for the AWB and AWC ablated strain, Oliver Hobert for pOH22 and pOH443 plasmids, the Caenorhabditis Genetics Center for strains, and Noriko Sato for technical assistance. We thank Jeremy Allen, PhD, from Edanz Group ( https://en‐author‐services.edanz.com/ac ) for editing a draft of this manuscript.
Publisher Copyright:
© 2021 Molecular Biology Society of Japan and John Wiley & Sons Australia, Ltd
PY - 2021/6
Y1 - 2021/6
N2 - Interneurons, innervated by multiple sensory neurons, need to integrate information from these sensory neurons and respond to sensory stimuli adequately. Mechanisms how sensory information is integrated to form responses of interneurons are not fully understood. In Caenorhabditis elegans, loss-of-function mutations of egl-4, which encodes a cGMP-dependent protein kinase (PKG), cause a defect in chemotaxis to odorants. Our genetic and imaging analyses revealed that the response property of AIY interneuron to an odorant is reversed in the egl-4 mutant, while the responses of two upstream olfactory neurons, AWA and AWC, are largely unchanged. Cell- ablation experiments show that AIY in the egl-4 mutant functions to suppress chemotaxis. Furthermore, the reversal of AIY response occurs only in the presence of sensory signals from both AWA and AWC. These results suggest that sensory signals are inadequately integrated in the egl-4 mutant. We also show that egl-4 expression in AWA and another sensory neuron prevents the reversed AIY response and restores chemotaxis in the egl-4 mutants. We propose that EGL-4/PKG, by suppressing aberrant integration of signals from olfactory neurons, converts the response property of an interneuron to olfactory stimuli and maintains the role of the interneuron in the circuit to execute chemotactic behavior.
AB - Interneurons, innervated by multiple sensory neurons, need to integrate information from these sensory neurons and respond to sensory stimuli adequately. Mechanisms how sensory information is integrated to form responses of interneurons are not fully understood. In Caenorhabditis elegans, loss-of-function mutations of egl-4, which encodes a cGMP-dependent protein kinase (PKG), cause a defect in chemotaxis to odorants. Our genetic and imaging analyses revealed that the response property of AIY interneuron to an odorant is reversed in the egl-4 mutant, while the responses of two upstream olfactory neurons, AWA and AWC, are largely unchanged. Cell- ablation experiments show that AIY in the egl-4 mutant functions to suppress chemotaxis. Furthermore, the reversal of AIY response occurs only in the presence of sensory signals from both AWA and AWC. These results suggest that sensory signals are inadequately integrated in the egl-4 mutant. We also show that egl-4 expression in AWA and another sensory neuron prevents the reversed AIY response and restores chemotaxis in the egl-4 mutants. We propose that EGL-4/PKG, by suppressing aberrant integration of signals from olfactory neurons, converts the response property of an interneuron to olfactory stimuli and maintains the role of the interneuron in the circuit to execute chemotactic behavior.
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U2 - 10.1111/gtc.12849
DO - 10.1111/gtc.12849
M3 - Article
C2 - 33817914
AN - SCOPUS:85104320206
VL - 26
SP - 411
EP - 425
JO - Genes to Cells
JF - Genes to Cells
SN - 1356-9597
IS - 6
ER -