Signal Decoding for Glutamate Modulating Egg Laying Oppositely in Caenorhabditis elegans under Varied Environmental Conditions

Abstract

Summary Animals' ability to sense environmental cues and to integrate this information to control fecundity is vital for continuing the species lineage. In this study, we observed that the sensory neurons Amphid neuron (ASHs and ADLs) differentially regulate egg-laying behavior in Caenorhabditis elegans under varied environmental conditions via distinct neuronal circuits. Under standard culture conditions, ASHs tonically release a small amount of glutamate and inhibit Hermaphrodite specific motor neuron (HSN) activities and egg laying via a highly sensitive Glutamate receptor (GLR)-5 receptor. In contrast, under Cu 2+ stimulation, ASHs and ADLs may release a large amount of glutamate and inhibit Amphid interneuron (AIA) interneurons via low-sensitivity Glutamate-gated chloride channel (GLC)-3 receptor, thus removing the inhibitory roles of AIAs on HSN activity and egg laying. However, directly measuring the amount of glutamate released by sensory neurons under different conditions and assaying the binding kinetics of receptors with the neurotransmitter are still required to support this study directly.

Positive interaction between ASH and ASK sensory neurons accelerates nociception and inhibits behavioral adaptation

“…It sounds reasonable that eat-4 reconstitution in ASH alone cannot restore WT Cu 2+ avoidance behavior. However, our previous study shows that eat-4 reconstitution in ASH alone is sufficient to restore the WT phenotype of egg laying ( Wen et al., 2020 ). We next checked the Cu 2+ -evoked Ca 2+ transients of ASK soma in the eat-4 mutant, gene rescued, and knocked down transgenic animals.…”

“…Because ASK is involved in regulating animals’ Cu 2+ avoidance, it should display responses to Cu 2+ . To examine whether ASK senses Cu 2+ , we employed fluorescent Ca 2+ imaging with GCaMP6s ( Chen et al., 2013 ) and combined it with microfluidic control of stimulation and animal movement ( Chronis et al., 2007 ; Ge et al., 2020 ; Guo et al., 2015 ; Liu et al., 2019 ; Wang et al., 2016 ; Wen et al., 2020 ). ASK sensory neurons in WT N2 worm displayed a robust Ca 2+ response to 3 mM CuSO 4 stimulation ( Figure 1 D).…”

“…What is the source of AIA excitation: ASH or other Cu 2+ -sensitive neurons? Our previous report shows that C. elegans is very sensitive to Cu 2+ , with an EC 50 (the concentration for 50% of maximal effect) of 4.68 μM for Cu 2+ enhancing egg laying ( Wen et al., 2020 ). The Cu 2+ concentration of 3 mM used in this study is relatively high.…”

“…They express the vesicular glutamate transporter (VGlut) EAT-4, which is required for ASH nociceptive responses ( Berger et al., 1998 ; Lee et al., 1999 ). ASH releases glutamate in a graded manner to elicit and modulate different models of nociceptive escape responses ( deBono and Maricq, 2005 ) and to regulate eating ( Zou et al., 2018 ) and egg laying ( Wen et al., 2020 ). ASH receives elaborate modulations from central and peripheral neurons by various signals of monoamines and peptides ( Ezcurra et al., 2016 ; Ghosh et al., 2016 ; Guo et al., 2015 ; Hapiak et al., 2013 ; Harris et al., 2010 ; Mills et al., 2012 ; Voelker et al., 2019 ; Zahratka et al., 2015 ).…”

Dietary vitamin B12 regulates chemosensory receptor gene expression via the MEF2 transcription factor in Caenorhabditis elegans

“…The nociceptive ADL neuron where srh-234 is specifically expressed mediates avoidance responses to a wide variety of environmental signals such as odors (Chao et al 2004; Troemel et al 1995; Troemel et al 1997), pheromones (Jang et al 2012), and heavy metals (Sambongi et al 1999; Wen et al 2020). Since chemoreceptor genes expressed in a specific chemosensory neuron type are generally linked to a common chemical response determined by the identity of the neuron in C. elegans , with a few exceptions in which neurons switch their preference towards odors (Tsunozaki et al 2008), it is probable that the srh-234 chemoreceptor may detect aversive chemical stimuli perceived by ADL.…”