Interneuron control of C. elegans developmental decision-making

Chai, Cynthia M.; Torkashvand, Mahdi; Seyedolmohadesin, Maedeh; Park, Heenam; Venkatachalam, Vivek; Sternberg, Paul W.

doi:10.1016/j.cub.2022.03.077

Cited by 22 publications

(11 citation statements)

References 83 publications

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“…The AIA is one of the first-layer amphid interneurons, receiving extensive synaptic inputs from sensory amphid neurons [ 43 ] and regulating various behavioral responses such as locomotion, chemotaxis, and learning [ 44 , 45 , 46 , 47 , 48 , 49 ]. A recent report revealed that AIA interneurons integrate external sensory cues into effector tissue signaling pathways via neuropeptidergic propagation to determine larval developmental fate [ 33 ]. In other words, AIA interneuron-derived FLP-2 neuropeptide signaling is found to promote reproductive growth and AIA activity is inhibited by pheromones to induce diapause entry [ 33 ].…”

Section: Discussionmentioning

confidence: 99%

“…A recent report revealed that AIA interneurons integrate external sensory cues into effector tissue signaling pathways via neuropeptidergic propagation to determine larval developmental fate [ 33 ]. In other words, AIA interneuron-derived FLP-2 neuropeptide signaling is found to promote reproductive growth and AIA activity is inhibited by pheromones to induce diapause entry [ 33 ]. Thus, this provides the possibility that calu-1 may be involved in this process, as calu-1 is expressed in AIA interneurons and large precursors of neuropeptides are processed by multiple proteolytic enzymes in the ER where CALU-1—a Ca 2+ binding protein—usually functions [ 50 ].…”

Section: Discussionmentioning

confidence: 99%

“…This cultivation induces the worms to produce many dauer pheromones. The crude pheromone dose that yielded 50% dauer formation was determined by generating a pheromone dose response curve [ 33 ]. The assay was performed based on a previous study, with modifications [ 31 ].…”

Section: Methodsmentioning

confidence: 99%

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Calumenin, a Ca2+ Binding Protein, Is Required for Dauer Formation in Caenorhabditis elegans

Lee

Cho

Song

2023

Biology

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Caenorhabditis elegans can adapt and survive in dynamically changing environments by the smart and delicate switching of molecular plasticity. C. elegans dauer diapause is a form of phenotypic and developmental plasticity that induces reversible developmental arrest upon environmental cues. An ER (endoplasmic reticulum)-resident Ca2+ binding protein, calumenin has been reported to function in a variety of malignant diseases in vertebrates and in the process of muscle contraction–relaxation. In C. elegans, CALU-1 is known to function in Ca2+-regulated behaviors (pharyngeal pumping and defecation) and cuticle formation. The cuticles of dauer larvae are morphologically distinct from those of larvae that develop in favorable conditions. The structure of the dauer cuticle is thicker and more highly reinforced than that of other larval stages to protect dauer larvae from various environmental insults. Since the calu-1(tm1783) mutant exhibited abnormal cuticle structures such as highly deformed annuli and alae, we investigated whether CALU-1 is involved in dauer formation or not. Ascaroside pheromone (ascr#2) and crude daumone were used under starvation conditions to analyze the rate of dauer formation in the calu-1(tm1783) mutant. Surprisingly, the dauer ratio of the calu-1(tm1783) mutant was extremely low compared to that of the wild type. In fact, the calu-1(tm1783) mutants were mostly unable to enter diapause. We also found that calu-1 is expressed in body-wall muscle and AIA interneurons at the dauer stage. Taken together, our results suggest that CALU-1 is required for normal entry into diapause in C. elegans.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Calumenin, a Ca2+ Binding Protein, Is Required for Dauer Formation in Caenorhabditis elegans

Lee

Cho

Song

2023

Biology

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“…mating (56), feeding (38), sleep (57) and others (47). More specifically, in the context of dauer larvae, previous work has identified increased neuropeptide signaling as an important neuromodulatory event for promoting the dauer entry decision (58, 59). Hence, adjusting the neural transcriptome at the level of diffusible signaling-molecules, i. e. neuropeptides, increases the larva’s behavioral repertoire.…”

Section: Discussionmentioning

confidence: 99%

Long-term imaging reveals behavioral plasticity during C. elegans dauer exit

Preußer

Neuschulz

Junker

et al. 2022

Preprint

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During their lifetime, animals must adapt their behavior to survive in changing environments. This ability requires the nervous system to adjust through dynamic expression of neurotransmitters and receptors but also through growth, spatial reorganization and connectivity while integrating external stimuli. For instance, despite having a fixed neuronal cell lineage, the nematode Caenorhabditis elegans’ nervous system remains plastic throughout its development. Here, we focus on a specific example of nervous system plasticity, the C. elegans dauer exit decision. Under unfavorable conditions, larvae will enter the non-feeding and non-reproductive dauer stage and adapt their behavior to cope with a new environment. Upon improved conditions, this stress resistant developmental stage is actively reversed to resume reproductive development. However, how different environmental stimuli regulate the exit decision mechanism and thereby drive the larva’s behavioral change is unknown. To fill this gap, we developed a new open hardware method for long-term imaging (12h) of C. elegans larvae. We identified dauer-specific behavioral motifs and characterized the behavioral trajectory of dauer exit in different environments to identify key decision points. Combining long-term behavioral imaging with transcriptomics, we find that bacterial ingestion triggers a change in neuropeptide gene expression to establish post-dauer behavior. Taken together, we show how a developing nervous system can robustly integrate environmental changes, activate a developmental switch and adapt the organism’s behavior to a new environment.

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“…In C. elegans, the dynamic expression of neuropeptides has been described to control several fundamental behavioral programs, e.g., mating [61], feeding [38], sleep [62], and others [49]. More specifically, in the context of dauer larvae, previous work has identified increased neuropeptide signaling as an important neuromodulatory event for promoting the dauer entry decision [63,64]. Hence, adjusting the neural transcriptome at the level of diffusible signaling-molecules, i.e., neuropeptides, increases the larva's behavioral repertoire.…”

Section: Discussionmentioning

confidence: 99%

Long-term imaging reveals behavioral plasticity during C. elegans dauer exit

et al. 2022

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Background During their lifetime, animals must adapt their behavior to survive in changing environments. This ability requires the nervous system to undergo adjustments at distinct temporal scales, from short-term dynamic changes in expression of neurotransmitters and receptors to longer-term growth, spatial and connectivity reorganization, while integrating external stimuli. The nematode Caenorhabditis elegans provides a model of nervous system plasticity, in particular its dauer exit decision. Under unfavorable conditions, larvae will enter the non-feeding and non-reproductive stress-resistant dauer stage and adapt their behavior to cope with the harsh new environment, with active reversal under improved conditions leading to resumption of reproductive development. However, how different environmental stimuli regulate the exit decision mechanism and thereby drive the larva’s behavioral change is unknown. To fill this gap and provide insights on behavioral changes over extended periods of time, we developed a new open hardware method for long-term imaging (12h) of C. elegans larvae. Results Our WormObserver platform comprises open hardware and software components for video acquisition, automated processing of large image data (> 80k images/experiment) and data analysis. We identified dauer-specific behavioral motifs and characterized the behavioral trajectory of dauer exit in different environments and genetic backgrounds to identify key decision points and stimuli promoting dauer exit. Combining long-term behavioral imaging with transcriptomics data, we find that bacterial ingestion triggers a change in neuropeptide gene expression to establish post-dauer behavior. Conclusions Taken together, we show how a developing nervous system can robustly integrate environmental changes activate a developmental switch and adapt the organism’s behavior to a new environment. WormObserver is generally applicable to other research questions within and beyond the C. elegans field, having a modular and customizable character and allowing assessment of behavioral plasticity over longer periods.

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Interneuron control of C. elegans developmental decision-making

Cited by 22 publications

References 83 publications

Calumenin, a Ca2+ Binding Protein, Is Required for Dauer Formation in Caenorhabditis elegans

Calumenin, a Ca2+ Binding Protein, Is Required for Dauer Formation in Caenorhabditis elegans

Long-term imaging reveals behavioral plasticity during C. elegans dauer exit

Long-term imaging reveals behavioral plasticity during C. elegans dauer exit

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