Biology subjects

Tomioka, M.

Publications and source records attributed to Tomioka, M..

3 recordsLinked to original sources

bioRxiv2023

Multiple p38/JNK Mitogen-activated protein kinase (MAPK) signaling pathways mediate salt chemotaxis learning in C. elegans

Animals are able to adapt their behaviors to their environment. In order to achieve this, the nervous system plays integrative roles, such as perception of external signals, sensory processing, and behavioral regulations via various signal transduction pathways. Here genetic analyses of C. elegans found that mutants of components of JNK and p38 Mitogen-activated protein kinase (MAPK) signaling pathways, also known as stress-activated protein kinase (SAPK) signaling pathways, exhibit various types of defects in the learning of salt chemotaxis. C. elegans homologues of JNK MAPKKK and MAPKK, MLK-1 and MEK-1, respectively, are required to avoid salt concentrations experienced during starvation. In contrast, homologues of p38 MAPKKK and MAPKK, NSY-1 and SEK-1, respectively, are required for high-salt chemotaxis after conditioning. Genetic interaction analyses suggest that a JNK family MAPK, KGB-1, functions downstream of both signaling pathways to regulate salt chemotaxis learning. Furthermore, we found that the NSY-1/SEK-1 pathway functions in sensory neurons, ASH, ADF, and ASER, to regulate the learned high-salt chemotaxis. A neuropeptide, NLP-3, expressed in ASH, ADF, and ASER neurons, and a neuropeptide receptor, NPR-15, expressed in AIA interneurons that receive synaptic input from these sensory neurons, function in the same genetic pathway as NSY-1 / SEK-1 signaling. These findings suggest that this MAPK pathway may affect neuropeptide signaling between sensory neurons and interneurons, thus promoting high-salt chemotaxis after conditioning.

genetics↗

bioRxiv2023

Antagonistic regulation of salt and sugar chemotaxis plasticity by a single chemosensory neuron in Caenorhabditis elegans

The nematode Caenorhabditis elegans memorizes various external chemicals, such as ions and odorants, during feeding. Here we find that C. elegans is attracted to the monosaccharides glucose and fructose after exposure to these monosaccharides in the presence of food; however, it avoids them without conditioning. The attraction to glucose requires a left-sided ASE gustatory neuron called ASEL. ASEL activity increases when glucose concentration decreases. Optogenetic ASEL stimulation promotes forward movements; however, after glucose conditioning, it promotes turning, suggesting that after glucose conditioning, the behavioral output of ASEL activation switches toward glucose. We previously reported that chemotaxis toward sodium ion (Na+), which is sensed by ASEL, increases after Na+ conditioning in the presence of food. Interestingly, glucose conditioning decreases Na+ chemotaxis, and conversely, Na+ conditioning decreases glucose chemotaxis, suggesting the reciprocal inhibition of learned chemotaxis to distinct chemicals. The activation of PKC-1, an nPKC {varepsilon}/{eta} ortholog, in ASEL promotes glucose chemotaxis and decreases Na+ chemotaxis after glucose conditioning. Furthermore, genetic screening identified ENSA-1, an ortholog of the protein phosphatase inhibitor ARPP-16/19, which functions in parallel with PKC-1 in glucose-induced chemotactic learning toward distinct chemicals. These findings suggest that kinase-phosphatase signaling regulates the balance between learned behaviors based on glucose conditioning in ASEL, which might contribute to migration toward chemical compositions where the animals were previously fed. Author summaryCaenorhabditis elegans responds to compounds that taste salty, bitter, sour, etc. However, its response to sweet compounds is unclear. Here, we show that C. elegans responds to glucose through a chemosensory neuron called ASEL. C. elegans avoids high concentrations of glucose and learns to approach glucose after feeding in the presence of high glucose, dependent on the action of ASEL. The ASEL neuron has been reported to respond to salt and promotes salt attraction after feeding in the presence of high salt. We find that the feeding-associated attractive responses to glucose and salt are antagonistic. When encountered with a mixture of salt and glucose during feeding, C. elegans changes its chemotactic response toward those chemicals according to the balance of each chemical in the mixture. C. elegans may memorize the concentrations of the chemical mixture during feeding and migrates to the chemical composition previously fed, which may promote opportunities obtaining food. Furthermore, we find that kinase-phosphatase signaling, which modulates neurotransmission, in ASEL is required for chemotaxis based on information processing of salt and glucose.

neuroscience↗

bioRxiv2022

Insulin/IGF Signaling Regulates Presynaptic Glutamate Release in Aversive Olfactory Learning

Information flow through neural circuits is continuously modified by context-dependent learning. In the nematode Caenorhabditis elegans, pairing specific odors with food deprivation results in aversion to the odor. Here we identify cell-specific mechanisms of insulin/IGF receptor signaling that integrate sensory information with food context during aversive olfactory learning. Using a conditional allele of the insulin/IGF receptor DAF-2, we show that aversive learning to butanone, an odor sensed only by the AWCON olfactory neuron, requires DAF-2 in AWCON. Learning requires an axonally-localized DAF-2c isoform and the insulin receptor substrate (IRS) protein IST-1, but is partly independent of the FoxO transcription factor DAF-16. Upon food deprivation, the unconditioned stimulus for learning, DAF-2 expression increases post-transcriptionally through an insulin- and ist-1-dependent process. Aversive learning suppresses odor-regulated glutamate release from AWCON in wild-type animals but not in ist-1 mutants, suggesting that localized insulin signaling drives presynaptic depression to generate an aversive memory.

neuroscience↗