Sea urchin larvae utilize light for regulating the pyloric opening

Yaguchi, Junko; Yaguchi, Shunsuke

doi:10.1186/s12915-021-00999-1

Cited by 22 publications

(27 citation statements)

References 54 publications

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“…Because it is reasonable to speculate that the cessation of forward swimming and/or the reversal of swimming direction after photoirradiation is mediated by a complex system including photoreceptors, neurons, and ciliary cells, we attempted to identify the most important body parts for this response by removing the larval anterior neuroectoderm (ANE) and/or postoral arms and then observing larval swimming behaviors. It has already been shown that this microdissection method is useful for investigating the essential parts of the body for a targeted phenomenon [ 12 ]. The cessation of forward swimming or reversal of swimming direction after photoirradiation was observed in 80% of the normal H .…”

Section: Resultsmentioning

confidence: 99%

Planktonic sea urchin larvae change their swimming direction in response to strong photoirradiation

et al. 2022

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To survive, organisms need to precisely respond to various environmental factors, such as light and gravity. Among these, light is so important for most life on Earth that light-response systems have become extraordinarily developed during evolution, especially in multicellular animals. A combination of photoreceptors, nervous system components, and effectors allows these animals to respond to light stimuli. In most macroscopic animals, muscles function as effectors responding to light, and in some microscopic aquatic animals, cilia play a role. It is likely that the cilia-based response was the first to develop and that it has been substituted by the muscle-based response along with increases in body size. However, although the function of muscle appears prominent, it is poorly understood whether ciliary responses to light are present and/or functional, especially in deuterostomes, because it is possible that these responses are too subtle to be observed, unlike muscle responses. Here, we show that planktonic sea urchin larvae reverse their swimming direction due to the inhibitory effect of light on the cholinergic neuron signaling>forward swimming pathway. We found that strong photoirradiation of larvae that stay on the surface of seawater immediately drives the larvae away from the surface due to backward swimming. When Opsin2, which is expressed in mesenchymal cells in larval arms, is knocked down, the larvae do not show backward swimming under photoirradiation. Although Opsin2-expressing cells are not neuronal cells, immunohistochemical analysis revealed that they directly attach to cholinergic neurons, which are thought to regulate forward swimming. These data indicate that light, through Opsin2, inhibits the activity of cholinergic signaling, which normally promotes larval forward swimming, and that the light-dependent ciliary response is present in deuterostomes. These findings shed light on how light-responsive tissues/organelles have been conserved and diversified during evolution.

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Section: Resultsmentioning

confidence: 99%

Planktonic sea urchin larvae change their swimming direction in response to strong photoirradiation

et al. 2022

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“…The association of these photoreceptors with pigment cells suggests that sea urchin larvae might be capable of directional light perception [ 4 ]. Indeed, the activity of the digestive tract in sea urchin larvae is regulated in response to light, by a mechanism depending on opsin3.2, which indicates that the photoreceptors are capable of initiating a behavioral response upon stimulation with light [ 34 ].…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, the c-opsin opsin1 is expressed in several tissues of adult sea urchins and in other echinoderms [ 32 ]. In sea urchin larvae, the expression of the Go-opsin opsin3.2 was detected in cells that were described as non-directional photoreceptors [ 33 ], and opsin3.2 was shown to be involved in the behavioral response to light [ 34 ]. These studies suggest that functional photoreceptor cells are present in sea urchin larvae, although the cell type identity of these photoreceptors has not been established.…”

Section: Introductionmentioning

confidence: 99%

Ciliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation

et al. 2021

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Background The evolutionary history of cell types provides insights into how morphological and functional complexity arose during animal evolution. Photoreceptor cell types are particularly broadly distributed throughout Bilateria; however, their evolutionary relationship is so far unresolved. Previous studies indicate that ciliary photoreceptors are homologous at least within chordates, and here, we present evidence that a related form of this cell type is also present in echinoderm larvae. Results Larvae of the purple sea urchin Strongylocentrotus purpuratus have photoreceptors that are positioned bilaterally in the oral/anterior apical neurogenic ectoderm. Here, we show that these photoreceptors express the transcription factor Rx, which is commonly expressed in ciliary photoreceptors, together with an atypical opsin of the GO family, opsin3.2, which localizes in particular to the cilia on the cell surface of photoreceptors. We show that these ciliary photoreceptors express the neuronal marker synaptotagmin and are located in proximity to pigment cells. Furthermore, we systematically identified additional transcription factors expressed in these larval photoreceptors and found that a majority are orthologous to transcription factors expressed in vertebrate ciliary photoreceptors, including Otx, Six3, Tbx2/3, and Rx. Based on the developmental expression of rx, these photoreceptors derive from the anterior apical neurogenic ectoderm. However, genes typically involved in eye development in bilateria, including pax6, six1/2, eya, and dac, are not expressed in sea urchin larval photoreceptors but are instead co-expressed in the hydropore canal. Conclusions Based on transcription factor expression, location, and developmental origin, we conclude that the sea urchin larval photoreceptors constitute a cell type that is likely homologous to the ciliary photoreceptors present in chordates.

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“…A potential explanation may be due to decreased level of serotonin (Fig. 6A), as it has been shown that serotonin binds to the receptors near the pyloric sphincter to allow for sphincter opening 42 . Since we observe a trend in decreased gut contractions in the NeuroD1 TP injected larvae, whereas miR-124 inhibition and NeuroD1 overexpression resulted in significant decrease in gut contractions compared to the control, this suggests that miR-124 is likely to regulate NeuroD1 and an additional unknown factor to impact gut contractions (Figs.…”

Section: Discussionmentioning

confidence: 99%

“…SoxB1, Six3, and Nkx2-3 expression in the endomesoderm could specify the foregut as neuroenderm but this had not been proven 40 . Recently, it has been shown that the opening of the pyloric sphincter is responsive to light, as a result of released serotonin that bind to the receptors in the midgut to mediate contraction 42 . During the larval stage, in response to calcium influx and release of different neurotransmitters, neurons in these three neuronal domains mediate swimming and feeding behavior which is vital for proper development.…”

Section: Introductionmentioning

confidence: 99%

miR-124 regulates Notch and NeuroD1 and to mediate transition states of neuronal development

Konrad

Song

2021

Preprint

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MicroRNAs (miRNAs) regulate gene expression by destabilizing target mRNA and/or inhibiting translation in animal cells. The ability to mechanistically dissect the function of miR-124 during specification, differentiation, and maturation of neurons during development within a single system has not been accomplished. Using the sea urchin (Strongylocentrotus purpuratus) embryo, we take advantage of the manipulability of the embryo and its well-documented gene regulatory networks (GRNs). We incorporated NeuroD1 as part of the sea urchin neuronal GRN and determined that miR-124 inhibition resulted in decreased gut contractions, swimming velocity, and neuronal development. We further integrated post-transcriptional regulation of miR-124 into the neuronal GRN. Inhibition of miR-124 resulted in increased number of cells expressing transcription factors associated with progenitor neurons and a concurrent decrease of mature and functional neurons. Results revealed that miR-124 regulates undefined factors early in neurogenesis during neuronal specification and differentiation in the early blastula and gastrula stages. In the late gastrula and larval stages, miR-124 regulates Notch and NeuroD1. Specifically, miR-124 regulates the transition between neuronal differentiation and maturation, by directly suppressing NeuroD1. Removal of miR-124 ″s suppression of NeuroD1 results in increased mature neurons with decreased Synaptagmin B-positive mature, functional neurons. By removing both miR-124 suppression of NeuroD1 and Notch, we were able to phenocopy miR-124 inhibitor induced defects. Overall, we have improved the neuronal GRN and identified miR-124 to play a prolific role in regulating various transitions of neuronal development.

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Sea urchin larvae utilize light for regulating the pyloric opening

Cited by 22 publications

References 54 publications

Planktonic sea urchin larvae change their swimming direction in response to strong photoirradiation

Planktonic sea urchin larvae change their swimming direction in response to strong photoirradiation

Ciliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation

miR-124 regulates Notch and NeuroD1 and to mediate transition states of neuronal development

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