Ultrastructure of the giant smooth muscle fiber of the ctenophore Beroe ovata

Hernandez‐Nicaise, Mari‐Luz; Amsellem, Jacqueline

doi:10.1016/s0022-5320(80)90053-2

Cited by 58 publications

(22 citation statements)

References 31 publications

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“…The cell organelles and the membrane systems were well preserved (Fig. 2), and the general organization of the cells did not differ markedly from that of cells in intact tissue (2).…”

Section: Resultsmentioning

confidence: 88%

“…Similar features have been described for in situ Beroe muscle cells (2), but in that situation the state of contraction could not be assessed. In the latter study, it was proposed that the actin-like filaments attach directly upon the cell membrane and that the "attachment sites could be located along several longitudinal strands."…”

Section: Discussionmentioning

confidence: 92%

“…Their ultrastructural features and basic electrophysiological properties have been described (1,2). However, the anatomical organization ofBeroe has hindered our understanding of these muscle cells when studied in situ.…”

mentioning

confidence: 99%

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Isolation of functional giant smooth muscle cells from an invertebrate: structural features of relaxed and contracted fibers.

Hernandez‐Nicaise¹,

Bilbaut²,

Malaval³

et al. 1982

Proc. Natl. Acad. Sci. U.S.A.

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The giant smooth muscle fibers of a ctenophore were isolated by enzymatic digestion. These fibers are multinucleated cells, up to 50 ,um in diameter and 2 cm in length. Their ultrastructure and membrane electrical properties are similar to those of in situ fibers. Relaxed, coiled (partially contracted), and fully shortened states were distinguished in isolated cells and studied by scanning and transmission electron microscopy. Calciumcontaining mitochondrial granules were found in the coiled cells but not in either the relaxed or the fully shortened cells. The relaxed cell is characterized in cross section by the density of myosin filaments (457 ± 15 per jpm2) and the thin-to-thick filament ratio (5.2 ± 0.2). In the coiled cell, the muscle lattice does not expand uniformly, as shown by the variability of myosin spacing, and the thin-to-thick filament ratio decreases. Both clockwise and counterclockwise coiling occur along the same fiber. The implications of these findings with respect to the structure of the contractile apparatus are discussed.Giant smooth muscle fibers up to 50 Am in diameter and from 0.5 mm to several cm in length occur in the marine planktonic invertebrate Beroe ovata. Their ultrastructural features and basic electrophysiological properties have been described (1,2). However, the anatomical organization ofBeroe has hindered our understanding of these muscle cells when studied in situ. An unequivocal characterization ofthe contracted muscle at the ultrastructural level has yet to be done, and the electrophysiological study could not take full advantage of the extreme length of the longitudinal muscles due to complex overlapping of the cells. In addition, the biophysical properties of the intercellular matrix may interfere either by limiting the diffusion of various substances or by restricting the access of electrodes to deeply situated fibers. These latter difficulties were partly overcome by incomplete enzymatic digestion of the mesoglea (1).A new insight into the properties ofsmooth muscle has arisen from the use of cells isolated from various vertebrates (3-5). In this report, we describe a simple technique for isolating the giant muscle fibers of Beroe in viable form and for processing them for ultrastructural studies. A description of the isolated cell in relaxed, coiled, and fully shortened states is given. The comparison of these states leads us to propose a possible arrangement of the myofilaments in this particular muscle cell. MATERIAL AND METHODSSpecimens of Beroe ovata were collected at the Station Zoologique, Villefranche-sur-Mer, France. Cell Preparation. The procedure adopted takes advantage ofthe resealing properties ofthe muscle fiber ofBeroe (1). Thin slices of the body wall (2-4 cm long) from any level of the organism were dissected out. The length of the strip was parallel to the longitudinal axis of the animal so as to include intact longitudinal muscle fibers. The tissues were kept for 15 min in cooled artificial sea water (ASW; 500 mM NaCl/10 mM KCl/ 58 mM M...

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“…The cell organelles and the membrane systems were well preserved (Fig. 2), and the general organization of the cells did not differ markedly from that of cells in intact tissue (2).…”

Section: Resultsmentioning

confidence: 88%

Section: Discussionmentioning

confidence: 92%

See 1 more Smart Citation

Isolation of functional giant smooth muscle cells from an invertebrate: structural features of relaxed and contracted fibers.

Hernandez‐Nicaise¹,

Bilbaut²,

Malaval³

et al. 1982

Proc. Natl. Acad. Sci. U.S.A.

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“…Different comb rows can beat synchronously or asynchronously, controlling various behaviors during prey capture or escape responses. Ciliated cells are under neuronal (primarily inhibitory) controls, with multiple different types of synapses described by electron microscopy (Hernandez-Nicaise, 1968;Hernandez-Nicaise, 1973a;HernandezNicaise, 1973b;Hernandez-Nicaise, 1973c;Hernandez-Nicaise, 1974;Hernandez-Nicaise and Amsellem, 1980;Hernandez-Nicaise et al, 1982;Horridge, 1965c;Horridge et al, 1962;Horridge and Mackay, 1964). The frequency of beating can be accelerated, decreased, arrested or even completely reversed, presumably by neuronal-mediated stimuli; high Mg 2+ , which suppresses synaptic transmission, eliminates these regulatory inputs (Horridge, 1974;Tamm, 1982).…”

Section: Neural Systems In Ctenophoresmentioning

confidence: 99%

Convergent evolution of neural systems in ctenophores

Moroz

2015

Journal of Experimental Biology

117

139

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Neurons are defined as polarized secretory cells specializing in directional propagation of electrical signals leading to the release of extracellular messengers -features that enable them to transmit information, primarily chemical in nature, beyond their immediate neighbors without affecting all intervening cells en route. Multiple origins of neurons and synapses from different classes of ancestral secretory cells might have occurred more than once during ~600 million years of animal evolution with independent events of nervous system centralization from a common bilaterian/cnidarian ancestor without the bona fide central nervous system. Ctenophores, or comb jellies, represent an example of extensive parallel evolution in neural systems. First, recent genome analyses place ctenophores as a sister group to other animals. Second, ctenophores have a smaller complement of pan-animal genes controlling canonical neurogenic, synaptic, muscle and immune systems, and developmental pathways than most other metazoans. However, comb jellies are carnivorous marine animals with a complex neuromuscular organization and sophisticated patterns of behavior. To sustain these functions, they have evolved a number of unique molecular innovations supporting the hypothesis of massive homoplasies in the organization of integrative and locomotory systems. Third, many bilaterian/cnidarian neuron-specific genes and 'classical' neurotransmitter pathways are either absent or, if present, not expressed in ctenophore neurons (e.g. the bilaterian/cnidarian neurotransmitter, γ-amino butyric acid or GABA, is localized in muscles and presumed bilaterian neuronspecific RNA-binding protein Elav is found in non-neuronal cells). Finally, metabolomic and pharmacological data failed to detect either the presence or any physiological action of serotonin, dopamine, noradrenaline, adrenaline, octopamine, acetylcholine or histamineconsistent with the hypothesis that ctenophore neural systems evolved independently from those in other animals. Glutamate and a diverse range of secretory peptides are first candidates for ctenophore neurotransmitters. Nevertheless, it is expected that other classes of signal and neurogenic molecules would be discovered in ctenophores as the next step to decipher one of the most distinct types of neural organization in the animal kingdom.

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“…Despite the absence of a distinct mesodermal germ layer, ctenophore-specific giant smooth muscle cells (Dayraud et al, 2012;Hernandez-Nicaise and Amsellem, 1980;Hernandez-Nicaise et al, 1984) are distributed throughout the mesoglea, and striated muscle cells have been documented in one species (Mackie et al, 1988). The ctenophore nervous system is composed of a subepithelial nerve net, mesogleal nerves and tentacular nerves (Jager et al, 2011;Moroz et al, 2014;Norekian and Moroz, 2016).…”

Section: Introductionmentioning

confidence: 99%

Establishing and maintaining primary cell cultures derived from the ctenophore Mnemiopsis leidyi

Vandepas

Warren

Amemiya

et al. 2017

Journal of Experimental Biology

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We have developed an efficient method for the preparation and maintenance of primary cell cultures isolated from adult Mnemiopsis leidyi, a lobate ctenophore. Our primary cell cultures are derived from tissue explants or enzymatically dissociated cells, and maintained in a complex undefined ctenophore mesogleal serum. These methods can be used to isolate, maintain and visually monitor ctenophore cells to assess proliferation, cellular morphology and cell differentiation in future studies. Exemplar cell types that can be easily isolated from primary cultures include proliferative ectodermal and endodermal cells, motile amebocyte-like cells, and giant smooth muscle cells that exhibit inducible contractile properties. We have also derived 'tissue envelopes' containing sections of endodermal canal surrounded by mesoglea and ectoderm that can be used to monitor targeted cell types in an in vivo context. Access to efficient and reliably generated primary cell cultures will facilitate the analysis of ctenophore development, physiology and morphology from a cell biological perspective.

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Ultrastructure of the giant smooth muscle fiber of the ctenophore Beroe ovata

Cited by 58 publications

References 31 publications

Isolation of functional giant smooth muscle cells from an invertebrate: structural features of relaxed and contracted fibers.

Isolation of functional giant smooth muscle cells from an invertebrate: structural features of relaxed and contracted fibers.

Convergent evolution of neural systems in ctenophores

Establishing and maintaining primary cell cultures derived from the ctenophore Mnemiopsis leidyi

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