Structure of Neuropeptide Precursors in Cnidaria

Gajewski, Martin; Schmutzler, Cornelia; Plickert, Günter

doi:10.1111/j.1749-6632.1998.tb10782.x

Cited by 17 publications

(12 citation statements)

References 14 publications

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“…They are also present in terrestrial invertebrates, such as nematodes and insects (Figure 1E). In cnidarians, platyhelminthes and nematodes, RYa peptides co-occur with RFa peptides on the same precursor [33,34,41], whereas in most other phyla they originate from a distinct precursor. Given the broad phyletic distribution of RYa peptides and the observation that they often derive from distinct precursors expressed in different cells than RFa [23], the RYa antibody could have a great value for comparative neuroanatomical studies.…”

Section: Resultsmentioning

confidence: 99%

Antibodies against conserved amidated neuropeptide epitopes enrich the comparative neurobiology toolbox

Conzelmann

Jékely

2012

EvoDevo

103

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BackgroundNeuronal antibodies that show immunoreactivity across a broad range of species are important tools for comparative neuroanatomy. Nonetheless, the current antibody repertoire for non-model invertebrates is limited. Currently, only antibodies against the neuropeptide RFamide and the monoamine transmitter serotonin are extensively used. These antibodies label respective neuron-populations and their axons and dendrites in a large number of species across various animal phyla.ResultsSeveral other neuropeptides also have a broad phyletic distribution among invertebrates, including DLamides, FVamides, FLamides, GWamides and RYamides. These neuropeptides show strong conservation of the two carboxy-terminal amino acids and are α-amidated at their C-termini. We generated and affinity-purified specific polyclonal antibodies against each of these conserved amidated dipeptide motifs. We thoroughly tested antibody reactivity and specificity both by peptide pre-incubation experiments and by showing a close correlation between the immunostaining signals and mRNA expression patterns of the respective precursor genes in the annelid Platynereis. We also demonstrated the usefulness of these antibodies by performing immunostainings on a broad range of invertebrate species, including cnidarians, annelids, molluscs, a bryozoan, and a crustacean. In all species, the antibodies label distinct neuronal populations and their axonal projections. In the ciliated larvae of cnidarians, annelids, molluscs and bryozoans, a subset of antibodies reveal peptidergic innervation of locomotor cilia.ConclusionsWe developed five specific cross-species-reactive antibodies recognizing conserved two-amino-acid amidated neuropeptide epitopes. These antibodies allow specific labelling of peptidergic neurons and their projections in a broad range of invertebrates. Our comparative survey across several marine phyla demonstrates a broad occurrence of peptidergic innervation of larval ciliary bands, suggesting a general role of these neuropeptides in the regulation of ciliary swimming.

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Section: Resultsmentioning

confidence: 99%

Antibodies against conserved amidated neuropeptide epitopes enrich the comparative neurobiology toolbox

Conzelmann

Jékely

2012

EvoDevo

103

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“…Hence, RFamide-positive neuronal cells may either be removed later during metamorphosis, or may be conserved to acquire a novel role in the adult polyp. In this stage, two further neuropeptides encoded by the RFamide preproprotein and terminating as RNamide or RYamide (Gajewski et al 1998) could become functional. Some RFamidepositive ganglionic cells, however, entered PCD early and rapidly reached final apoptotis with visible nuclear blebbing, while functional neuropeptide was still detectable in them.…”

Section: Discussionmentioning

confidence: 99%

“…For performance of the runoff in vitro transcription, a cloned multiple neuropeptide RFamide/RNamide/RYamide precursor was used (Gajewski et al 1998;accession number X97413). This common precursor gives rise to several copies of the Hydractinia RFamide neuropeptide.…”

Section: Whole-mount In Situ Hybridisationmentioning

confidence: 99%

Neuronal cell death during metamorphosis of Hydractina echinata (Cnidaria, Hydrozoa)

et al. 2010

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In planula larvae of the invertebrate Hydractinia echinata (Cnidaria, Hydrozoa), peptides of the GLWamide and the RFamide families are expressed in distinct subpopulations of neurons, distributed in a typical spatial pattern through the larval body. However, in the adult polyp GLWamide or RFamide-expressing cells are located at body parts that do not correspond to the prior larval regions. Since we had shown previously that during metamorphosis a large number of cells are removed by programmed cell death (PCD), we aimed to analyze whether cells of the neuropeptide-expressing larval nerve net are among those sacrificed. By immunohistochemical staining and in situ hybridization, we labeled GLWamide- and RFamide-expressing cells. Double staining of neuropeptides and degraded DNA (TUNEL analysis) identified some neurosensory cells as being apoptotic. Derangement of the cytoplasm and rapid destruction of neuropeptide precursor RNA indicated complete death of these particular sensory cells in the course of metamorphosis. Additionally, a small group of RFamide-positive sensory cells in the developing mouth region of the primary polyp could be shown to emerge by proliferation. Our results support the idea that during metamorphosis, specific parts of the larval neuronal network are subject to neurodegeneration and therefore not used for construction of the adult nerve net. Most neuronal cells of the primary polyp arise by de novo differentiation of stem cells commited to neural differentiation in embryogenesis. At least some nerve cells derive from proliferation of progenitor cells. Clarification of how the nerve net of these basal eumetazoans degenerates may add information to the understanding of neurodegeneration by apoptosis as a whole in the animal kingdom.

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“…The other peptide was Hydra-RFamide I (pGlu-Trp-LeuGly-Gly-Arg-Phe-NH 2 ) which was isolated from the freshwater hydroid, Hydra magnipapillata, closely related to Hydractinia (Moosler et al 1996). The latter peptide and the RFamide peptide from Hydractinia (pGlu-Trp-Leu-Lys-Gly-Arg-Phe-NH 2 ; Gajewski et al 1998) have nearly identical structures with only one amino acid replacement at position 4. These two peptides and all other RFamide family members sharing the common C-terminal sequence Gly-Arg-Phe-NH 2 presumably have the same basic functions in cnidarians as described earlier for the LWamides (also see Results).…”

Section: Peptidesmentioning

confidence: 98%

Inhibition of metamorphosis by RFamide neuropeptides in planula larvae of Hydractinia echinata

Katsukura

David

Grimmelikhuijzen

et al. 2003

Development Genes and Evolution

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The primitive nervous system in planula larvae of Hydractinia echinata (Cnidaria) has sensory neurons containing LWamide or RFamide neuropeptides. LWamides have been shown to induce metamorphosis of planula larvae into adult polyps. We report here that RFamides act antagonistically to LWamides. RFamides inhibit metamorphosis when applied to planula larvae during metamorphosis induction by treatment with LWamides (or other inducing agents such as CsCl ions, diacylglycerol and bacterial inducers). Our results show further that RFamides act downstream of LWamide release, presumably directly on target cells mediating metamorphosis. These observations support a model in which metamorphosis in H. echinata is regulated by sensory neurons secreting LWamides and RFamides in response to environmental cues.

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Structure of Neuropeptide Precursors in Cnidaria

Cited by 17 publications

References 14 publications

Antibodies against conserved amidated neuropeptide epitopes enrich the comparative neurobiology toolbox

Antibodies against conserved amidated neuropeptide epitopes enrich the comparative neurobiology toolbox

Neuronal cell death during metamorphosis of Hydractina echinata (Cnidaria, Hydrozoa)

Inhibition of metamorphosis by RFamide neuropeptides in planula larvae of Hydractinia echinata

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