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First published online December 2, 2005
Journal of Experimental Biology 208, 4577-4584 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01930
Long-lasting potassium channel inactivation in myoepithelial fibres is related to characteristics of swimming in diphyid siphonophores
1 Ine Marine Laboratory of National Institute for Physiological Sciences,
Ine, Kyoto 626-0424, Japan
2 Institute for Enzyme Research, Tokushima University, Tokushima 770-8503,
Japan
3 Laboratory of Biology, Graduate School of Commerce and Management,
Hitotsubashi University, Kunitachi, Tokyo 186-8601, Japan
4 Marine Biological Association of UK, Plymouth, PL1 2PB, UK
* Author for correspondence (e-mail: iinoue{at}ier.tokushima-u.ac.jp)
Accepted 13 October 2005
Diphyid siphonophores swim using bursts of propulsive jets, which are
produced by contractions of a monolayer of subumbrellar myoepithelial fibres
lining the nectophore. This swimming behaviour is characterised by successive
increases in the force generating the jets during the initial jets of the
burst. Action potentials that generate the contractions propagate throughout
the myoepithelial layer: both their amplitude and duration successively
increase during the first part of the burst. To investigate the ionic
mechanism of this action potential augmentation, single myoepithelial cells
were enzymatically dissociated and whole-cell voltage clamped. Na+,
Ca2+ and K+ currents were recorded under different
internal and external salt compositions. The Na+ current was
blocked by a relatively high concentration (4 µmol l1 or
higher) of tetrodotoxin (TTX), indicating that the Na+ channel
belongs to a group of TTX-resistant Na+ channels. The
Ca2+ current was blocked by nifedipine (10 µmol
l1) and Co2+ (5 mmol l1),
indicating that the Ca2+ channel is L-type. The K+
current possessed a unique property of long-lasting inactivation. The
K+ current fully inactivated during a depolarisation to +30 mV with
a time-constant of
9 ms, and the time constant of recovery from
inactivation at 70 mV was 13.2 s. This long-lasting inactivation of the
K+ channel was the major factor in the augmentation of both action
potentials and contractions of the myoepithelial sheet during the initial part
of the burst.
Key words: diphyid, behaviour, striated muscle, K+ channel, inactivation, Diphyes chamissonis