Membrane currents that govern smooth muscle contraction in a ctenophore

Bilbaut, André; Hernandez‐Nicaise, Mari‐Luz; Leech, Colin A.; Meech, Robert W

doi:10.1038/331533a0

Cited by 32 publications

(17 citation statements)

References 15 publications

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“…Secondly, the IA-like current is largely inactivated within 50 ms at plateau potential (about 90 % inactivated as steady state at -20 mV, K. Muraki, Y. Imaizumi & M. Watanabe, unpublished observation). Quite recently, it has been suggested that IA-like current in smooth muscle cells has a role in reducing the rate of decay of the afterhyperpolarization (Beech & Bolton, 1988;Bilbaut, Hernandez-Nicaise, Leech & Meech, 1988) as has been originally reported in molluscan neurones (Connor & Stevens, 1971). This mechanism was not examined in the present study.…”

Section: Y Imaizumi K Muraki and M Watanabecontrasting

confidence: 39%

Ionic currents in single smooth muscle cells from the ureter of the guinea‐pig.

Imaizumi

Muraki

Watanabe

1989

The Journal of Physiology

112

121

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SUMMARY1. Ionic currents underlying the action potential were recorded from enzymatically isolated smooth muscle cells of guinea-pig ureter.2. The action potential recorded from a single cell was similar to that from a multicellular preparation. It showed repetitive spikes on a plateau potential which followed the first spike. Treatment with 10 mM-tetraethylammonium (TEA) increased the amplitude and duration of the plateau phase and abolished the repetitive spikes.3. Under voltage clamp mode, at least two (maybe three) kinds of outward currents were activated during depolarizing pulses. The main outward current was Ca2"-dependent K+ current (IK(ca)), which was mostly blocked in Ca2`-free solution, or by application of 1 mM-cadmium (Cd2+) or 2 mM-tetraethylammonium (TEA).IK(ca) was greatly decreased by treatment with 5 mM-caffeine or an addition of 10 mM-EGTA in a pipette solution.4. In the presence of 1 mM-Cd2' and 2 mM-TEA, a small transient outward current remained. 4-Aminopyridine (1 mM) suppressed the transient outward current by about 40 %. Time-and voltage-dependent delayed rectifier outward currents were small in ureter cells. An inwardly rectifying K+ current was not detected.5. An application of 1 mM-Cd2+, 5 mM-cobalt (Co2+), 1 mM-lanthanum (La3+) or 0-1 IuM-nifedipine completely blocked the action potential. Replacement of 80-90 % of extracellular Na+ with Li+ or Tris almost abolished the plateau potential and repetitive spikes but did not change significantly the first spike. 6. In the presence of 30 mM-TEA, the inward current elicited by depolarization was monophasic and lasted for more than 1 s. Application of 1 mM-Cd2+, 1 mM-La3 , 0-1 /LM-nifedipine, or 5 mM-Co2+ completely blocked inward current. The replacement (87 %) of extracellular Na+ ions with Li+, Tris, sucrose or TEA speeded up the decay of inward current; the inward current decreased by 10-60 % at the end of a 500 ms pulse.7. Even in low-Na+ solution (120 mM-TEA), the inactivation of ICa had a quite slow component (T = 1 S), in addition to another faster component (T = 100 ms) at 0 mV. When short depolarizing clamp pulses (50 ms) were repetitively applied at short intervals (50 ms) and with interpulse voltage of -10 or -20 mV to mimic the repetitive spikes on the plateau of the action potential, the decline of peak Ca2+ 5-2 Y. IMAIZUMI, K. MURAKI AND M. WATANABE current during the train of pulses was smaller than the decay of Ca2+ current during a long pulse.8. These results indicate that (1) the repetitive spikes on the plateau phase of the action potential are attributable to the slow inactivation and rapid reactivation of I4a and repetitive activation of IK(Ca) due to Ca2+-induced Ca2+ release from stores, and (2) the long plateau phase in the action potential may be due to a slowly inactivating Iba, a Na+-dependent late inward current, and a small delayed rectifier outward current.

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Section: Y Imaizumi K Muraki and M Watanabecontrasting

confidence: 39%

Ionic currents in single smooth muscle cells from the ureter of the guinea‐pig.

Imaizumi

Muraki

Watanabe

1989

The Journal of Physiology

112

121

View full text Add to dashboard Cite

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“…Electrical signaling in ctenophores is well developed, especially in non-neuronal conductive and locomotory systems (Bilbaut et al, 1988;Dubas et al, 1988;Horridge, 1965a). Ctenophores have more genes encoding ion channels than sponges and placozoans .…”

Section: Reviewmentioning

confidence: 99%

“…The muscle cells are supposedly derived from a type of mesenchyme cell in the mesoglea; they are segregated early in embryonic development and therefore can be considered as true mesodermal derivatives [separate from epidermis and gastrodermis (Burton, 2008;Derelle and Manuel, 2007)]. Some of them are giant and well characterized electrophysiologically (Anderson, 1984;Bilbaut et al, 1988;Dubas et al, 1988;Stein and Anderson, 1984). These muscles are used to control hydroskeleton tone, body shape and feeding, which might be original functions of muscle elements in animal ancestors.…”

Section: Ctenophores As Basal Metazoans Sister To Other Animalsmentioning

confidence: 99%

Convergent evolution of neural systems in ctenophores

Moroz

2015

Journal of Experimental Biology

120

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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“…Although typical in hydromedusae, ring muscles are not known in other orders of ctenophores. Lobate ctenophores have muscular lobes, but they are unlike the muscle discovered in Thalassocalycida (Bilbaut et al 1988;Tamm and Tamm 1989;Seipel and Schmid 2005). This remarkable adaptation allowed thalassocalycids to evolve a much diVerent body plan from ctenophores in the Order Lobata, one that permits it to quickly engulf relatively large volumes of water and capture fast prey.…”

Section: Discussionmentioning

confidence: 99%

Feeding behavior of the ctenophore Thalassocalyce inconstans: revision of anatomy of the order Thalassocalycida

et al. 2009

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Behavioral observations using a remotely operated vehicle (ROV) in the Gulf of California in March, 2003, provided insights into the vertical distribution, feeding and anatomy of the rare and delicate ctenophore Thalassocalyce inconstans. Additional archived ROV video records from the Monterey Bay Aquarium Research Institute of 288 sightings of T. inconstans and 2,437 individual observations of euphausiids in the Gulf of California and Monterey Canyon between 1989 and 2005 were examined to determine ctenophore and euphausiid prey depth distributions with respect to temperature and dissolved oxygen concentration [dO]. In the Gulf of California most ctenophores (96.9%) were above 350 m, the top of the oxygen minimum layer. In Monterey Canyon the ctenophores were more widely distributed throughout the water column, including the hypoxic zone, to depths as great as 3,500 m. Computer-aided behavioral analysis of two video records of the capture of euphausiids by T. inconstans showed that the ctenophore contracted its bell almost instantly (0.5 s), transforming its Xattened, hemispherical resting shape into a closed bi-lobed globe in which seawater and prey were engulfed. Euphausiids entrapped within the globe displayed a previously undescribed escape response for krill ('probing behavior'), in which they hovered and gently probed the inner surfaces of the globe with antennae without stimulating further contraction by the ctenophore. Such rapid bell contraction could be eVected only by a peripheral sphincter muscle even though the presence of circumferential ring musculature was unknown for the Phylum Ctenophora. Thereafter, several live T. inconstans were collected by hand oV Barbados and microscopic observations conWrmed that assumption.

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Membrane currents that govern smooth muscle contraction in a ctenophore

Cited by 32 publications

References 15 publications

Ionic currents in single smooth muscle cells from the ureter of the guinea‐pig.

Ionic currents in single smooth muscle cells from the ureter of the guinea‐pig.

Convergent evolution of neural systems in ctenophores

Feeding behavior of the ctenophore Thalassocalyce inconstans: revision of anatomy of the order Thalassocalycida

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