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The Journal of Experimental Biology 205, 3143-3152 (2002)
Copyright © 2002 The Company of Biologists Limited

Regulation of early embryonic behavior by nitric oxide in the pond snail Helisoma trivolvis

Alison G. Cole, Aniseh Mashkournia, Shawn C. Parries and Jeffrey I. Goldberg^*

Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada T6G 2E9

^* Author for correspondence (e-mail: jeff.goldberg{at}ualberta.ca)

Accepted 22 July 2002

Helisoma trivolvis embryos display a cilia-driven rotational behavior that is regulated by a pair of serotonergic neurons named ENC1s. As these cilio-excitatory motor neurons contain an apical dendrite ending in a chemosensory dendritic knob at the embryonic surface, they probably function as sensorimotor neurons. Given that nitric oxide (NO) is often associated with sensory neurons in invertebrates, and has also been implicated in the control of ciliary activity, we examined the expression of NO synthase (NOS) activity and possible function of NO in regulating the rotational behavior in H. trivolvis embryos. NADPH diaphorase histochemistry on stage E25-E30 embryos revealed NOS expression in the protonephridia, buccal mass, dorsolateral ciliary cells and the sensory dendritic knobs of ENC1. At stages E35-40, the pedal ciliary cells and ENC1's soma, apical dendrite and proximal descending axon were also stained. In stage E25 embryos, optimal doses of the NO donors SNAP and SNP increased the rate of embryonic rotation by twofold, in contrast to the fourfold increase caused by 100 µmol l^-1 serotonin. The NOS inhibitors L-NAME (10 mmol l^-1) and 7-NI (100 µmol l^-1) decreased the rotation rate by approximately 50%, whereas co-addition of L-NAME and SNAP caused a twofold increase. In an analysis of the surge and inter-surge subcomponents of the rotational behavior, the NO donors increased the inter-surge rotation rate and the surge amplitude. In contrast, the NO inhibitors decreased the inter-surge rotation rate and the frequency of surges. These data suggest that the embryonic rotational behavior depends in part on the constitutive excitatory actions of NO on ENC1 and ciliary cells.

Key words: Embryonic behavior, nitric oxide, pond snail, Helisoma trivolvis, serotonin, ciliary beating, gastropods, NADPH diaphorase

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