Cellular expression and functional roles of all 26 neurotransmitter GPCRs in the<i>C. elegans</i>egg-laying circuit

Fernandez, Robert W.; Wei, Kimberly; Wang, Erin Y.; Mikalauskaite, Deimante; Olson, Andrew; Pepper, Judy S; Christie, Nakeirah T.M.; Kim, Seongseop; Koelle, Michael R.

doi:10.1101/2020.04.23.037242

Cited by 5 publications

(6 citation statements)

References 68 publications

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“…First, it can act to feedback inhibit the circuit to signal when the behavior has been executed. We find that vulval muscle contraction activates the VCs, which may inhibit the egg-laying circuit through release of acetylcholine acting on metabotropic receptors such as GAR-2 on the HSNs, vulval muscles, and uv1 cells (Bany et al, 2003;Fernandez et al, 2020;Zhang et al, 2008Zhang et al, , 2010. GAR-2 has been shown to act in parallel with ionotropic receptors to differentially modulate locomotion behavior, providing both short-and longer-term effects in response to cholinergic signaling (Dittman & Kaplan, 2008).…”

Section: Locomotion 535mentioning

confidence: 74%

“…Serotonin acting through SER-7 has 544 previously been shown to initiate neural circuit activity, such as in feeding behavior (Song et al, 545 2013). SER-7 is also expressed in the VC neurons (Fernandez et al, 2020), and serotonin 546 stimulates VC Ca 2+ activity (Zhang et al, 2008). Similar to animals where VC neurotransmitter 547 release is blocked, ser-7 mutants also fail to respond to exogenous serotonin (Hobson et al, 548 2006).…”

Section: Locomotion 535mentioning

confidence: 99%

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The sex-specific VC neurons are mechanically activated motor neurons that facilitate serotonin-induced egg laying inC. elegans

Kopchock

Ravi

Bode

et al. 2020

Preprint

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Successful execution of behavior requires the coordinated activity and communication between multiple cell types. Studies using the relatively simple neural circuits of invertebrates have helped to uncover how conserved molecular and cellular signaling events shape animal behavior. To understand the mechanisms underlying neural circuit activity and behavior, we have been studying a simple circuit that drives egg-laying behavior in the nematode worm C. elegans. Here we show that the female-specific, Ventral C (VC) motoneurons are required for vulval muscle contractility and egg laying in response to serotonin. Ca2+ imaging experiments show the VCs are active during times of vulval muscle contraction and vulval opening, and optogenetic stimulation of the VCs promotes vulval muscle Ca2+ activity. However, while silencing of the VCs does not grossly affect steady-state egg-laying behavior, VC silencing does block egg laying in response to serotonin and increases the failure rate of egg-laying attempts. Signaling from the VCs facilitates full vulval muscle contraction and opening of the vulva for efficient egg laying. We also find the VCs are mechanically activated in response to vulval opening. Optogenetic stimulation of the vulval muscles is sufficient to drive VC Ca2+ activity and requires muscle contractility, showing the presynaptic VCs and the postsynaptic vulval muscles can mutually excite each other. Together, our results demonstrate that the VC neurons facilitate efficient execution of egg-laying behavior by coordinating postsynaptic muscle contractility in response to serotonin and mechanosensory feedback.

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Section: Locomotion 535mentioning

confidence: 74%

Section: Locomotion 535mentioning

confidence: 99%

The sex-specific VC neurons are mechanically activated motor neurons that facilitate serotonin-induced egg laying inC. elegans

Kopchock

Ravi

Bode

et al. 2020

Preprint

View full text Add to dashboard Cite

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“…These results underscore the need for unbiased and brainwide analysis of how functional activity is shaped by neurotransmitters and receptors. We envision future work, using NeuroPAL, to map expression of the remaining aminergic and ionotropic neurotransmitter receptors (Fernandez et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

“…Cell 184, 272-288.e1-e7, January 7, 2021 e5 previously reported (Fernandez et al, 2020;Zhong et al, 2010). The gar-1, gar-2, gbb-1, mgl-1, and mgl-3 fosmid reporters were generated by modENCODE (Sarov et al, 2012).…”

Section: Identifying Neuronal Sites Of Gene Expressionmentioning

confidence: 99%

NeuroPAL: A Multicolor Atlas for Whole-Brain Neuronal Identification in C. elegans

Yemini

Lin

Nejatbakhsh

et al. 2021

Cell

182

285

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“…elegans expresses numerous GPCRs [ 63 ], which has hampered our efforts to identify the upstream activator of Gα. A set of GPCRs expressed in the spermatheca has recently been published [ 64 ], which may facilitate the identification of a receptor that acts upstream of GSA-1. Alternatively, GPRs can facilitate the activation of G proteins via GPCR-independent mechanisms [ 20 , 28 ].…”

Section: Discussionmentioning

confidence: 99%

Gα/GSA-1 works upstream of PKA/KIN-1 to regulate calcium signaling and contractility in the Caenorhabditis elegans spermatheca

et al. 2020

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Correct regulation of cell contractility is critical for the function of many biological systems. The reproductive system of the hermaphroditic nematode C. elegans contains a contractile tube of myoepithelial cells known as the spermatheca, which stores sperm and is the site of oocyte fertilization. Regulated contraction of the spermatheca pushes the embryo into the uterus. Cell contractility in the spermatheca is dependent on actin and myosin and is regulated, in part, by Ca 2+ signaling through the phospholipase PLC-1, which mediates Ca 2+ release from the endoplasmic reticulum. Here, we describe a novel role for GSA-1/Gα s, and protein kinase A, composed of the catalytic subunit KIN-1/PKA-C and the regulatory subunit KIN-2/PKA-R, in the regulation of Ca 2+ release and contractility in the C. elegans spermatheca. Without GSA-1/Gα s or KIN-1/PKA-C, Ca 2+ is not released, and oocytes become trapped in the spermatheca. Conversely, when PKA is activated through either a gain of function allele in GSA-1 (GSA-1(GF)) or by depletion of KIN-2/PKA-R, the transit times and total numbers, although not frequencies, of Ca 2+ pulses are increased, and Ca 2+ propagates across the spermatheca even in the absence of oocyte entry. In the spermathecal-uterine valve, loss of GSA-1/Gα s or KIN-1/PKA-C results in sustained, high levels of Ca 2+ and a loss of coordination between the spermathecal bag and sp-ut valve. Additionally, we show that depleting phosphodiesterase PDE-6 levels alters contractility and Ca 2+ dynamics in the spermatheca, and that the GPB-1 and GPB-2 G β subunits play a central role in regulating spermathecal contractility and Ca 2+ signaling. This work identifies a signaling network in which Ca 2+ and cAMP pathways work together to coordinate spermathecal contractions for successful ovulations.

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Cellular expression and functional roles of all 26 neurotransmitter GPCRs in theC. elegansegg-laying circuit

Cited by 5 publications

References 68 publications

The sex-specific VC neurons are mechanically activated motor neurons that facilitate serotonin-induced egg laying inC. elegans

The sex-specific VC neurons are mechanically activated motor neurons that facilitate serotonin-induced egg laying inC. elegans

NeuroPAL: A Multicolor Atlas for Whole-Brain Neuronal Identification in C. elegans

Gα/GSA-1 works upstream of PKA/KIN-1 to regulate calcium signaling and contractility in the Caenorhabditis elegans spermatheca

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