Mechanoreception and synaptic transmission of hydrozoan nematocytes

Thurm, Ulrich; Brinkmann, Martin; Golz, R.; Holtmann, Matthias; Oliver, Dominik; Sieger, Thiemo

doi:10.1007/978-1-4020-2762-8_12

Cited by 8 publications

(5 citation statements)

References 25 publications

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“…Similarly, the GSH response was impaired showing a slow tentacle-writhing activity, tentacle rigidity, and inhibition of mouth opening (Movie M4 in Supplementary Material). These results besides showing the feeding behavior impairment, revealed through the untangling of the prey capture from mouth opening that, as previously suggested by in vitro experiments (Thurm et al, 2004), the nematocysts discharge (the ability to catch the prey) is not sufficient to induce mouth opening. In addition, here we show that the ability of gastric region to contract must have a role in the accomplishment of feeding behavior.…”

Section: Resultssupporting

confidence: 75%

Impact of Amorphous SiO₂Nanoparticles on a Living Organism: Morphological, Behavioral, and Molecular Biology Implications

Ambrosone

Vettimo

Malvindi

et al. 2014

Front. Bioeng. Biotechnol.

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It is generally accepted that silica (SiO2) is not toxic. But the increasing use of silica nanoparticles (SiO2NPs) in many different industrial fields has prompted the careful investigation of their toxicity in biological systems. In this report, we describe the effects elicited by SiO2NPs on animal and cell physiology. Stable and monodisperse amorphous silica nanoparticles, 25 nM in diameter, were administered to living Hydra vulgaris (Cnidaria). The dose-related effects were defined by morphological and behavioral assays. The results revealed an all-or-nothing lethal toxicity with a rather high threshold (35 nM NPs) and a LT50 of 38 h. At sub lethal doses, the morphophysiological effects included: animal morphology alterations, paralysis of the gastric region, disorganization and depletion of tentacle specialized cells, increase of apoptotic and collapsed cells, and reduction of the epithelial cell proliferation rate. Transcriptome analysis (RNAseq) revealed 45 differentially expressed genes, mostly involved in stress response and cuticle renovation. Our results show that Hydra reacts to SiO2NPs, is able to rebalance the animal homeostasis up to a relatively high doses of SiO2NPs, and that the physiological modifications are transduced to gene expression modulation.

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Section: Resultssupporting

confidence: 75%

Impact of Amorphous SiO₂Nanoparticles on a Living Organism: Morphological, Behavioral, and Molecular Biology Implications

Ambrosone

Vettimo

Malvindi

et al. 2014

Front. Bioeng. Biotechnol.

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“…Nematocytes are the cnidarian‐specific stinging cells, characterized by a complex intracytoplasmic capsule (nematocyst) housing a coiled tubule, and an apical sensory ciliary cone. That nematocytes are modified nerve cells is supported by a vast array of data relating to their neurophysiological properties, ultrastructural features, and expression of neurogenic genes in nematocyte precursors . Sensory cells, ganglion cells, and some nematocytes bear neurites and establish synaptic contacts with other cells.…”

Section: The Experimental Toolkit For Cnidarian Model Systemsmentioning

confidence: 99%

The cellular and molecular basis of cnidarian neurogenesis

Rentzsch

Layden

Manuel

2016

WIREs Developmental Biology

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Neurogenesis initiates during early development and it continues through later developmental stages and in adult animals to enable expansion, remodeling, and homeostasis of the nervous system. The generation of nerve cells has been analyzed in detail in few bilaterian model organisms, leaving open many questions about the evolution of this process. As the sister group to bilaterians, cnidarians occupy an informative phylogenetic position to address the early evolution of cellular and molecular aspects of neurogenesis and to understand common principles of neural development. Here we review studies in several cnidarian model systems that have revealed significant similarities and interesting differences compared to neurogenesis in bilaterian species, and between different cnidarian taxa. Cnidarian neurogenesis is currently best understood in the sea anemone Nematostella vectensis, where it includes epithelial neural progenitor cells that express transcription factors of the soxB and atonal families. Notch signaling regulates the number of these neural progenitor cells, achaete-scute and dmrt genes are required for their further development and Wnt and BMP signaling appear to be involved in the patterning of the nervous system. In contrast to many vertebrates and Drosophila, cnidarians have a high capacity to generate neurons throughout their lifetime and during regeneration. Utilizing this feature of cnidarian biology will likely allow gaining new insights into the similarities and differences of embryonic and regenerative neurogenesis. The use of different cnidarian model systems and their expanding experimental toolkits will thus continue to provide a better understanding of evolutionary and developmental aspects of nervous system formation. © 2016 The Authors. WIREs Developmental Biology published by Wiley Periodicals, Inc. How to cite this article:WIREs Dev Biol 2017, 6:e257. doi: 10.1002/wdev.257 INTRODUCTIONC nidarians are an early offshoot in the evolution of animals, having separated from the lineage that led to the emergence of bilaterians more than 600 million years ago. 1 Their importance for understanding the evolution of nervous systems has long been recognized, based both on their phylogenetic position as an outgroup to bilaterians (Figure 1) and on the structure of their nervous system, which is predominantly organized as nerve nets. The cnidarians comprise two major clades, the anthozoans and the medusozoans (Figure 1), 2,3 which separated before 550 million years ago and thus not long after the cnidarian lineage separated from all other animals. 4 Two distinct body forms can be found in cnidarians: sessile polyps, which are tube-shaped animals with a single terminal body opening (called the mouth) surrounded by prey-catching tentacles; This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.and free-s...

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“…S1 , Supplementary Material online). Taken together, the results from the identification of group-specific residues, immunostainings, and in situ hybridizations suggest a strong functional diversification between the hydra-TRP-N paralogs which can, however, only be understood by delineating the detailed ultrastructure which underlies the function of mechanosensitive channels ( Golz and Thurm 1991b ; Brinkmann et al 1996 ; Thurm et al 2004 ). We find that the pan-TRP-N antibody signal is localized to the mechanosensory cnidocil apparatus of all types of nematocytes in the tentacles, whereas hydra-TRP-N4 is restricted to nematocyst vesicle membranes in developing nematocyte clusters in the body column of Hydra and in mature nematocytes of tentacles (see fig.…”

Section: Resultsmentioning

confidence: 99%

“…The complete loss of TRP-N at the root of Amniota has been preceded by an increase in numbers of stereovilli per cell, which occurred with a change from the originally concentric organization of hair bundles to their eccentric organization at the origin of vertebrates ( Hudspeth and Jacobs 1979 ). This could occur as stereovilli themselves are potential contributors of mechanosensation, observed already in the Cnidaria Nematostella ( Mire and Watson 1997 ) and Hydra ( Thurm et al 2004 ). Stereovilli, however, like all microvilli, are supported by an actin skeleton instead of the tubulin skeleton of cilia that supports TRP-N (see supplementary fig.…”

Section: Discussionmentioning

confidence: 96%

The Rise and Fall of TRP-N, an Ancient Family of Mechanogated Ion Channels, in Metazoa

et al. 2015

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Mechanoreception, the sensing of mechanical forces, is an ancient means of orientation and communication and tightly linked to the evolution of motile animals. In flies, the transient-receptor-potential N protein (TRP-N) was found to be a cilia-associated mechanoreceptor. TRP-N belongs to a large and diverse family of ion channels. Its unusually long N-terminal repeat of 28 ankyrin domains presumably acts as the gating spring by which mechanical energy induces channel gating. We analyzed the evolutionary origins and possible diversification of TRP-N. Using a custom-made set of highly discriminative sequence profiles we scanned a representative set of metazoan genomes and subsequently corrected several gene models. We find that, contrary to other ion channel families, TRP-N is remarkably conserved in its domain arrangements and copy number (1) in all Bilateria except for amniotes, even in the wake of several whole-genome duplications. TRP-N is absent in Porifera but present in Ctenophora and Placozoa. Exceptional multiplications of TRP-N occurred in Cnidaria, independently along the Hydra and the Nematostella lineage. Molecular signals of subfunctionalization can be attributed to different mechanisms of activation of the gating spring. In Hydra this is further supported by in situ hybridization and immune staining, suggesting that at least three paralogs adapted to nematocyte discharge, which is key for predation and defense. We propose that these new candidate proteins help explain the sensory complexity of Cnidaria which has been previously observed but so far has lacked a molecular underpinning. Also, the ancient appearance of TRP-N supports a common origin of important components of the nervous systems in Ctenophores, Cnidaria, and Bilateria.

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Mechanoreception and synaptic transmission of hydrozoan nematocytes

Cited by 8 publications

References 25 publications

Impact of Amorphous SiO₂Nanoparticles on a Living Organism: Morphological, Behavioral, and Molecular Biology Implications

Impact of Amorphous SiO₂Nanoparticles on a Living Organism: Morphological, Behavioral, and Molecular Biology Implications

The cellular and molecular basis of cnidarian neurogenesis

The Rise and Fall of TRP-N, an Ancient Family of Mechanogated Ion Channels, in Metazoa

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Mechanoreception and synaptic transmission of hydrozoan nematocytes

Cited by 8 publications

References 25 publications

Impact of Amorphous SiO2Nanoparticles on a Living Organism: Morphological, Behavioral, and Molecular Biology Implications

Impact of Amorphous SiO2Nanoparticles on a Living Organism: Morphological, Behavioral, and Molecular Biology Implications

The cellular and molecular basis of cnidarian neurogenesis

The Rise and Fall of TRP-N, an Ancient Family of Mechanogated Ion Channels, in Metazoa

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Product

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Impact of Amorphous SiO₂Nanoparticles on a Living Organism: Morphological, Behavioral, and Molecular Biology Implications

Impact of Amorphous SiO₂Nanoparticles on a Living Organism: Morphological, Behavioral, and Molecular Biology Implications