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First published online June 29, 2006
Journal of Experimental Biology 209, 2749-2764 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02312
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Dopamine modulation of Ca2+ dependent Cl- current regulates ciliary beat frequency controlling locomotion in Tritonia diomedea

Owen M. Woodward1,2,* and A. O. Dennis Willows1,2

1 Department of Biology, University of Washington, Seattle, WA 98195, USA
2 Friday Harbor Laboratories, University of Washington, 620 University Road, Friday Harbor, WA 98250, USA

* Author for correspondence at present address: Department of Physiology, Johns Hopkins School of Medicine, 725 N. Wolfe Street, 214 WBSB, Baltimore, MD 21205, USA (e-mail: owenw{at}jhmi.edu)

Accepted 4 May 2006

The physiological mechanisms controlling ciliary beating remain largely unknown. Evidence exists supporting both hormonal control of ciliary beating and control via direct innervation. In the present study we investigated nervous control of cilia based locomotion in the nudibranch mollusc, Tritonia diomedea. Ciliated pedal epithelial (CPE) cells acting as locomotory effectors may be electrically excitable. To explore this possibility we characterized the cells' electrical properties, and found that CPE cells have large voltage dependent whole cell currents with two components. First, there is a fast activating outward Cl- current that is both voltage and Ca2+ influx dependent (ICl(Ca)). ICl(Ca) is sensitive to DIDS and 9-AC, and resembles currents of Ca2+-activated Cl- channels (CaCC). Ca2+ dependence also suggests the presence of voltage-gated Ca2+ channels; however, we were unable to detect these currents. The second current, a voltage dependent proton current (IH), activates very slowly and is sensitive to both Zn2+ and changes in pH.

In addition we identify a new cilio-excitatory substance in Tritonia, viz., dopamine. Dopamine, in the 10 µmol l-1-1 mmol l-1 range, significantly increases ciliary beat frequency (CBF). We also found dopamine and Tritonia Pedal Peptide (TPep-NLS) selectively suppress ICl(Ca) in CPE cells, demonstrating a link between CBF excitation and ICl(Ca). It appears that dopamine and TPep-NLS inhibit ICl(Ca) not through changing [Ca2+]in, but directly by an unknown mechanism. Coupling of ICl(Ca) and CBF is further supported by our finding that DIDS and zero [Cl-]out both increase CBF, mimicking dopamine and TPep-NLS excitation. These results suggest that dopamine and TPep-NLS act to inhibit ICl(Ca), initiating and prolonging Ca2+ influx, and activating CBF excitation.

Key words: Tritonia diomedea, dopamine, ciliary beat frequency, Ca2+ activated Cl- current






© The Company of Biologists Ltd 2006