Massive actin bundle couples macrocilia to muscles in the ctenophore <i>Beroë</i>

Tarmm, Sidney L.; Tamm, Sidney L.

doi:10.1002/cm.970070204

Cited by 30 publications

(25 citation statements)

References 46 publications

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“…Each group was weakly stained by tubulin antibody and was attached to a bundle of noncontractile actin filaments brightly stained by phalloidin (Figures b and c). Similar bundles of phalloidin‐labeled actin filaments have been previously described at the base of the macrocilia in Beroe and suggested to “serve as intracellular tendons” (Tamm and Tamm, ; Tamm, ). A large group of muscles encircled the mouth (Figure a,b) and mediated its closure.…”

Section: Resultssupporting

confidence: 71%

Neuromuscular organization of the Ctenophore Pleurobrachia bachei

Norekian

Moroz

2018

J of Comparative Neurology

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Ctenophores are descendants of one of the earliest branching metazoan lineage with enigmatic nervous systems. The lack of convenient neurogenic molecules and neurotransmitters suggests an extensive parallel evolution and independent origins of neurons and synapses. However, the field lags due to the lack of microanatomical data about the neuro‐muscular systems in this group of animals. Here, using immunohistochemistry and scanning electron microscopy, we describe the organization of both muscular and nervous systems in the sea gooseberry, Pleurobrachia bachei, from North Pacific. The diffuse neural system of Pleurobrachia consists of two subsystems: the subepithelial neural network and the mesogleal net with about 5,000–7,000 neurons combined. Our data revealed the unexpected complexity of neuromuscular organization in this basal metazoan lineage. The anatomical diversity of cell types includes at least nine broad categories of neurons, five families of surface receptors and more than two dozen types of muscle cells as well as regional concentrations of neuronal elements to support ctenophore feeding, complex swimming, escape, and prey capture behaviors. In summary, we recognize more than 80 total morphological cell types. Thus, in terms of cell‐type specification and diversity, ctenophores significantly exceed what we currently know about other prebilaterian groups (placozoan, sponges, and cnidarians), and some basal bilaterians.

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Section: Resultssupporting

confidence: 71%

Neuromuscular organization of the Ctenophore Pleurobrachia bachei

Norekian

Moroz

2018

J of Comparative Neurology

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“…Detergent-treated macrocilia freed from the tissue typically remain anchored to their large actin bundles (20,21). Macrocilia of B. mitrata are 80-100 Im long and 12-15 ,um in diameter, considerably larger than those of other beroids (Fig.…”

Section: Resultsmentioning

confidence: 99%

Calcium sensitivity extends the length of ATP-reactivated ciliary axonemes.

Tamm

1989

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

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We use the Ca-dependent activation response of macrocilia of the ctenophore Beroe to map the distribution of Ca sensitivity along axonemes of detergent-extracted ATPreactivated models. Local iontophoretic application of Ca (or Sr or Ba) to any site along the length of demembranated macrocilia in ATP-Mg solution elicits oscillatory bending. Bending responses are localized to the site of application of these cations and do not propagate. Ca sensitivity for initiating bends is, therefore, distributed along the entire length of the axonemes. Since Ca triggers ATP-dependent microtubule sliding disintegration of macrociliary axonemes, a Ca-sensitive mechanism for activating microtubule sliding extends the length of the axonemes. In contrast, local application of Ca to living dissociated macrociliary cells elicits beating only when applied to the base of the macrocilium, indicating that the effective site of Ca entry is localized to the membrane at the ciliary base. Therefore, the spatial distributions of membrane Ca permeability and axonemal Ca sensors do not coincide.Calcium ions (Ca) play a key role in signaling various modifications of ciliary and flagellar motility in response to environmental stimuli. Ca-triggered behavioral responses include: reorientation of ciliary beat direction (1-3), reversal of flagellar wave direction (4), alteration of flagellar waveform (5-8), arrest of beating (9-11), and activation of beating (12,13).Stimulus-evoked increase in intraciliary Ca concentration is mediated by voltage-gated Ca channels in the ciliary membrane (14-16). Electrophysiological recording from ctenophore comb plate cilia showed that the Ca conductance controlling reversal of beat direction is distributed over most of the length of the ciliary membrane (17).Macrocilia of the ctenophore Beroe are compound organelles containing hundreds (or thousands, depending on species) of "9+2" ciliary axonemes enclosed by a single common membrane (18), except at the base (19). Macrocilia are usually quiescent but are activated to beat rapidly and continuously by depolarization-gated Ca influx (13). Extracellular application of Ca to various sites along macrocilia of heat-dissociated cells indicated that Ca permeability for triggering beating is localized to the basal region of the macrociliary membrane, corresponding to a rete of unfused ciliary membranes (19).Little is known about the site(s) and mechanism(s) ofaction of Ca within the axoneme. Detergent-permeabilized models of macrocilia that require micromolar levels of free Ca, Ba, or Sr for ATP reactivation of beating and/or microtubule sliding disintegration have been devised (20). In this report we iontophoretically apply these cations at various regions along demembranated macrocilia in ATP to map the distri- (Fig. 1). MATERIALS AND METHODSPermeabilized Models. Lip pieces bearing macrocilia were washed in Ca-free artificial seawater for 30 min. Tissue was then extracted in 0.05% or 0.1% saponin (B. ovata) or 0.05%

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“…Earlier work on the neurobiology of ctenophores performed by Horridge (Bullock and Horridge, 1965;Horridge, 1965c;Horridge, 1974), Tamm (Moss and Tamm, 1986;Moss and Tamm, 1987;Tamm, 1982;Tamm, 1984;Tamm and Moss, 1985;Tamm and Tamm, 1981;Tamm and Tamm, 1987) and others (Haddock, 2007;Satterlie and Case, 1978) revealed a very complex behavioral repertoire in these marine predators. Nevertheless, we know little about ctenophore neurons because classical nerve stains are particularly unreliable in these animals.…”

Section: Enigmatic Ctenophore Neuronsmentioning

confidence: 99%

Convergent evolution of neural systems in ctenophores

Moroz

2015

Journal of Experimental Biology

116

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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Massive actin bundle couples macrocilia to muscles in the ctenophore Beroë

Cited by 30 publications

References 46 publications

Neuromuscular organization of the Ctenophore Pleurobrachia bachei

Neuromuscular organization of the Ctenophore Pleurobrachia bachei

Calcium sensitivity extends the length of ATP-reactivated ciliary axonemes.

Convergent evolution of neural systems in ctenophores

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