Nitric oxide modulates peristaltic muscle activity associated with fluid circulation in the sea pansy Renilla...

Nitric oxide (NO) is a well-known regulator of vascular activities in vertebrates and it has also been implicated as a vasodilatatory agent in a cephalopod. In the sea pansy Renilla koellikeri, an octocorallian representative of the most basal animals with a nervous system, we investigated the role of NO in peristalsis, an activity that moves body fluids through the coelenteron (gastrovascular cavity) of the polyps across the colony. NO donors increased the amplitude of peristaltic contractions and increased tonic contractions in relaxed preparations, but caused a relaxation of basal tension in contracted preparations. The NO synthase (NOS) inhibitors L-NAME (N(omega)-nitro-L-arginine methyl ester) and 7-nitroindazole reduced the amplitude of peristaltic contractions and lowered basal tension. In contrast, aminoguanidine, a specific inhibitor of inducible NOS, increased the amplitude but reduced the rate of peristalsis. Zaprinast, a cGMP-specific phosphodiesterase inhibitor, decreased the amplitude of peristaltic contractions, a decrease that was amplified by dibutyryl cGMP. In contrast, the inhibitor of soluble guanylyl cyclase ODQ (1H-(1,2,4)oxadiazolo(4,3-a)quinoxalin-1-one) enhanced peristalsis. Putative NOS-containing neurons, revealed by NADPH-diaphorase activity and citrulline immunohistochemistry, were observed in the basiectoderm at the base of the autozooid polyp tentacles and in a nerve-net around the oral disc. Their neurites ran up the tentacles and down to the polyp body wall, crossing from the ectoderm through the mesoglea and into the endoderm musculature where musculo-epithelial cells were also reactive. These data suggest that two distinct nitrergic pathways, one of which is mediated by cGMP, regulate peristalsis and muscle tone in the sea pansy and that these pathways may involve NOS-containing ectodermal neurons and musculo-epithelial cells.