Expression of a retinoic acid receptor (RAR)-like protein in the embryonic and adult nervous system of a protostome species

Carter, Christopher; Rand, Christopher D.; Mohammad, Imtiaz; Lepp, Amanda; Vesprini, Nicholas D.; Wiebe, Olivia; Carlone, Robert L.; Spencer, Gaynor E.

doi:10.1002/jez.b.22604

Cited by 35 publications

(52 citation statements)

References 52 publications

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“…We have also shown that immunoreactivity for LymRAR is present in developing neurons in the CNS and associated with the developing shell (Carter et al, 2015). We have also shown that immunoreactivity for LymRAR is present in developing neurons in the CNS and associated with the developing shell (Carter et al, 2015).…”

Section: Do Rar Agonists Mimic the Effects Of Endogenous Retinoids supporting

confidence: 53%

“…Antigen preadsorbed controls for this antibody were previously performed on Lymnaea neurons (Carter et al, 2015), so here, control experiments only omitted the primary antibody, and the regenerating PeA cells did not demonstrate any RAR immunoreactivity (0/27 cell bodies and 0/23 growth cones; data not shown). These data support our previous findings (Carter et al, 2015) that LymRAR can be found in nonsomatic compartments such as neurites and growth cones. Representative example of a PeA growth cone before (i; t = 0 min) and after responding to a gradient of atRA (ii; t = 16 min).…”

Section: Lymrar Plays a Role In Axon Guidancementioning

confidence: 96%

“…We have previously conducted preadsorption controls with this same antibody for immunostaining of LymRAR in CNS neurons (Carter et al, 2015), and as such these were not repeated again here. Samples were first washed for 10 minute in PBS and permeabilized in 0.1% Triton-X/PBS for 30 minute.…”

Section: Immunostaining Proceduresmentioning

confidence: 99%

“…Although we have previously shown in preliminary characterizations of this LymRAR, that RAR antagonists can disrupt embryonic development (Carter et al, 2015), we now provide a more thorough analysis of whether the RAR may indeed play a role in embryonic and nervous system development in an invertebrate protostome species. Although we have previously shown in preliminary characterizations of this LymRAR, that RAR antagonists can disrupt embryonic development (Carter et al, 2015), we now provide a more thorough analysis of whether the RAR may indeed play a role in embryonic and nervous system development in an invertebrate protostome species.…”

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confidence: 95%

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Pharmacological evidence for the role of RAR in axon guidance and embryonic development of a protostome species

Johnson

Hoog

Tolentino

et al. 2019

Genesis

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Summary Retinoic acid (RA), the active metabolite of vitamin A, functions through nuclear receptors, one of which is the retinoic acid receptor (RAR). Though the RAR is essential for various aspects of vertebrate development, little is known about the role of RAR in nonchordate invertebrates. Here, we examined the potential role of an invertebrate RAR in mediating chemotropic effects of retinoic acid. The RAR of the protostome Lymnaea stagnalis is present in the growth cones of regenerating cultured motorneurons, and a synthetic RAR agonist (EC23), was able to mimic the effects of retinoic acid in inducing growth cone turning. We also examined the ability of the natural retinoids, all‐trans RA and 9‐cis RA, as well as the synthetic RAR agonists, to disrupt embryonic development in Lymnaea. Developmental defects included delays in embryo hatching, arrested eye, and shell development, as well as more severe abnormalities such as halted development. Developmental defects induced by some (but not all) synthetic RAR agonists were found to mimic those induced by addition of high concentrations of the natural retinoid isomers. These pharmacological data support a possible physiological role for the RAR in axon guidance and embryonic development of an invertebrate protostome species.

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Section: Do Rar Agonists Mimic the Effects Of Endogenous Retinoids supporting

confidence: 53%

Section: Lymrar Plays a Role In Axon Guidancementioning

confidence: 96%

Section: Immunostaining Proceduresmentioning

confidence: 99%

mentioning

confidence: 95%

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Pharmacological evidence for the role of RAR in axon guidance and embryonic development of a protostome species

Johnson

Hoog

Tolentino

et al. 2019

Genesis

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“…Similarly, a specific RAR subtype, RARβ, has been shown to increase in a stage-specific manner during CNS regeneration in the adult newt [13]. As both RXR and RAR are likely critical during RA-induced regeneration [13,77], and expressed in Lymnaea PeA growth cones [19,20], it is possible that miR-124 could be targeting either mRNA sequence during specific stages of regeneration. Indeed, the 3 UTR of the Lymnaea RAR and RXR mRNAs contain potential binding sites for miR-124, though we have not yet explored whether these mRNAs are found locally in the neurites and/or growth cones.…”

Section: Role Of Mir-124 During Ra-induced Cns Regenerationmentioning

confidence: 99%

Identification and Characterization of microRNAs during Retinoic Acid-Induced Regeneration of a Molluscan Central Nervous System

Walker

Spencer

Necakov

et al. 2018

Preprint

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Retinoic acid (RA) is the biologically active metabolite of vitamin A and has become a well-established factor that induces neurite outgrowth and regeneration in both vertebrates and invertebrates. However, the underlying regulatory mechanisms that may mediate RA-induced neurite sprouting remain unclear. In the past decade, microRNAs have emerged as important regulators of nervous system development and regeneration, and have been shown to contribute to processes such as neurite sprouting. However, few studies have demonstrated the role of miRNAs in RA-induced neurite sprouting. By miRNA sequencing analysis, we identify 482 miRNAs in the regenerating central nervous system (CNS) of the mollusc Lymnaea stagnalis, 219 of which represent potentially novel miRNAs. Of the remaining conserved miRNAs, 38 show a statistically significant up-or downregulation in regenerating CNS as a result of RA treatment. We further characterized the expression of one neuronally-enriched miRNA upregulated by RA, miR-124. We demonstrate, for the first time, that miR-124 is expressed within the cell bodies and neurites of regenerating motorneurons. Moreover, we identify miR-124 expression within the growth cones of cultured ciliary motorneurons (pedal A), whereas expression in the growth cones of another class of respiratory motorneurons (right parietal A) was absent in vitro. These findings support our hypothesis that miRNAs are important regulators of retinoic acid-induced neuronal outgrowth and regeneration in regeneration-competent species.

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Retinoic acid signaling and neurogenic niche regulation in the developing peripheral nervous system of the cephalochordate amphioxus

Zieger

Garbarino

Naeije

et al. 2018

Cell. Mol. Life Sci.

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The retinoic acid (RA) signaling pathway regulates axial patterning and neurogenesis in the developing central nervous system (CNS) of chordates, but little is known about its roles during peripheral nervous system (PNS) formation and about how these roles might have evolved. This study assesses the requirement of RA signaling for establishing a functional PNS in the cephalochordate amphioxus, the best available stand-in for the ancestral chordate condition. Pharmacological manipulation of RA signaling levels during embryogenesis reduces the ability of amphioxus larvae to respond to sensory stimulation and alters the number and distribution of ectodermal sensory neurons (ESNs) in a stage- and context-dependent manner. Using gene expression assays combined with immunohistochemistry, we show that this is because RA signaling specifically acts on a small population of soxb1c-expressing ESN progenitors, which form a neurogenic niche in the trunk ectoderm, to modulate ESN production during elongation of the larval body. Our findings reveal an important role for RA signaling in regulating neurogenic niche activity in the larval amphioxus PNS. Although only few studies have addressed this issue so far, comparable RA signaling functions have been reported for neurogenic niches in the CNS and in certain neurogenic placode derivatives of vertebrates. Accordingly, the here-described mechanism is likely a conserved feature of chordate embryonic and adult neural development.

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Expression of a retinoic acid receptor (RAR)-like protein in the embryonic and adult nervous system of a protostome species

Cited by 35 publications

References 52 publications

Pharmacological evidence for the role of RAR in axon guidance and embryonic development of a protostome species

Pharmacological evidence for the role of RAR in axon guidance and embryonic development of a protostome species

Identification and Characterization of microRNAs during Retinoic Acid-Induced Regeneration of a Molluscan Central Nervous System

Retinoic acid signaling and neurogenic niche regulation in the developing peripheral nervous system of the cephalochordate amphioxus

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