Discovery and functional characterization of neuropeptides in crinoid echinoderms.

Discovery and functional characterization of neuropeptides in crinoid echinoderms.
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神经肽在红胚层中的发现和功能表征。

DOI:
10.3389/fnins.2022.1006594
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发表时间:
2022
影响因子:
4.3
通讯作者:
Elphick, Maurice R.
Elphick, Maurice R.
中科院分区:
医学2区
文献类型:
--
作者:
Aleotti, Alessandra;Wilkie, Iain C.;Yanez-Guerra, Luis A.;Gattoni, Giacomo;Rahman, Tahshin A.;Wademan, Richard F.;Ahmad, Zakaryya;Ivanova, Deyana A.;Semmens, Dean C.;Delroisse, Jerome;Cai, Weigang;Odekunle, Esther;Egertova, Michaela;Ferrario, Cinzia;Sugni, Michela;Bonasoro, Francesco;Elphick, Maurice R.

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神经肽是动物体内最大和最多样的信号分子家族之一,因此,它们调节着许多生理过程和行为。基因组和转录组测序使得能够从越来越多的分类群中识别编码神经肽前体蛋白的基因,包括双边和非双边动物。特别令人感兴趣的是后口无脊椎动物,如棘皮动物门,它在系统发育中的地位有助于重建Bilateria神经肽信号系统的进化。然而,我们对棘皮动物神经肽信号的了解很大程度上是基于对棘皮动物的生物信息学和实验分析-星虫(海星和脆星)和棘虫(海胆和海参)。海百合(羽星和海百合)是海百合的姐妹分支,目前对海百合的神经肽信号知之甚少。因此,我们分析了三个羽星物种Anneissia Japan onica、Antedon Mediterranea和Flormetra serratisima的转录组/基因组序列数据,首次全面鉴定了海百合中的神经肽前体。这些包括双侧神经肽前体家族的代表和几个预测的松果体神经肽前体。以稻纵卷叶蝉为实验模型,我们研究了特定神经肽在幼虫、变态后五环和成虫中的表达,为研究松果体神经系统的细胞结构提供了新的见解。因此,利用mRNA原位杂交技术,在位于背侧的多肽能细胞群中发现了F型SALMFamide前体转录本。此外,用免疫组织化学方法还发现,在成年大鼠的流产神经中枢、口周神经环和口腔管足以及神经系统的外胚神经室和内胚神经室都有降钙素型神经肽。此外,对一种加压素/催产素型神经肽(Crinotocin)的功能分析表明,这种肽在体外可以引起手臂制剂的机械行为随剂量的变化--这是首次报道的神经肽在松果体中的生物学作用。综上所述,我们的发现为棘皮动物神经肽信号转导提供了新的视角,并为进一步探索棘皮动物作为棘皮动物姐妹分支的神经肽表达/功能奠定了基础。
Neuropeptides are one of the largest and most diverse families of signaling molecules in animals and, accordingly, they regulate many physiological processes and behaviors. Genome and transcriptome sequencing has enabled the identification of genes encoding neuropeptide precursor proteins in species from a growing variety of taxa, including bilaterian and non-bilaterian animals. Of particular interest are deuterostome invertebrates such as the phylum Echinodermata, which occupies a phylogenetic position that has facilitated reconstruction of the evolution of neuropeptide signaling systems in Bilateria. However, our knowledge of neuropeptide signaling in echinoderms is largely based on bioinformatic and experimental analysis of eleutherozoans—Asterozoa (starfish and brittle stars) and Echinozoa (sea urchins and sea cucumbers). Little is known about neuropeptide signaling in crinoids (feather stars and sea lilies), which are a sister clade to the Eleutherozoa. Therefore, we have analyzed transcriptome/genome sequence data from three feather star species, Anneissia japonica, Antedon mediterranea, and Florometra serratissima, to produce the first comprehensive identification of neuropeptide precursors in crinoids. These include representatives of bilaterian neuropeptide precursor families and several predicted crinoid neuropeptide precursors. Using A. mediterranea as an experimental model, we have investigated the expression of selected neuropeptides in larvae (doliolaria), post-metamorphic pentacrinoids and adults, providing new insights into the cellular architecture of crinoid nervous systems. Thus, using mRNA in situ hybridization F-type SALMFamide precursor transcripts were revealed in a previously undescribed population of peptidergic cells located dorso-laterally in doliolaria. Furthermore, using immunohistochemistry a calcitonin-type neuropeptide was revealed in the aboral nerve center, circumoral nerve ring and oral tube feet in pentacrinoids and in the ectoneural and entoneural compartments of the nervous system in adults. Moreover, functional analysis of a vasopressin/oxytocin-type neuropeptide (crinotocin), which is expressed in the brachial nerve of the arms in A. mediterranea, revealed that this peptide causes a dose-dependent change in the mechanical behavior of arm preparations in vitro—the first reported biological action of a neuropeptide in a crinoid. In conclusion, our findings provide new perspectives on neuropeptide signaling in echinoderms and the foundations for further exploration of neuropeptide expression/function in crinoids as a sister clade to eleutherozoan echinoderms.
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