Abstract
The central nervous system (CNS) of a metamorphically competent larva of the caenogastropod Ilyanassa obsoleta contains a medial, unpaired apical ganglion (AG) of approximately 25 neurons that lies above the commissure connecting the paired cerebral ganglia. The AG, also known as the cephalic or apical sensory organ (ASO), contains numerous sensory neurons and innervates the ciliated velar lobes, the larval swimming and feeding structures. Before metamorphosis, the AG contains 5 serotonergic neurons and exogenous serotonin can induce metamorphosis in competent larvae. The AG appears to be a purely larval structure as it disappears within 3 days of metamorphic induction. In competent larvae, most neurons of the AG display nitric oxide synthase (NOS)-like immunoreactivity and inhibition of NOS activity can induce larval metamorphose. Because nitric oxide (NO) can prevent cells from undergoing apoptosis, a form of programmed cell death (PCD), we hypothesize that inhibition of NOS activity triggers the loss of the AG at the beginning of the metamorphic process. Within 24 hours of metamorphic induction, cellular changes that are typical of the early stages of PCD are visible in histological sections and results of a terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL) assay in metamorphosing larvae show AG nuclei containing fragmented DNA, supporting our hypothesis.
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Barlow, L. A., Truman, J. W. (1992) Patterns of serotonin and SCP immunoreactivity during metamorphosis of the nervous system of the red abalone, Haliotis rufescens. J. Neurobiology 23, 829–844.
Beiras, R., Widdows, J. (1995) Effect of the neurotransmitters dopamine, serotonin and norepinephrine on the ciliary activity of mussel (Mytilus edulis) larvae. Mar. Biol. 122, 597–603.
Bishop, C., Bates, W., Brandhorst, B. (2001) Regulation of metamorphosis in ascidians involves NO/cGMP signaling and HSP90. J. Exp. Zool. 289, 374–384.
Bishop, C., Brandhorst, B. (2001) NO/cGMP Signaling and HSP90 activity represses metamorphosis in the Sea Urchin Lytechinus pictus. Biol. Bull. 201, 394–404.
Boettcher, A. A., Targett, N. M. (1996) Induction of metamorphosis in queen conch, Strombus gigas Linnaeus, larvae by cues associated with red algae from their nursery grounds. J. Exp. Mar. Biol. Ecol. 196, 29–52.
Bonar, D. B. (1978) Ultrastructure of a cephalic sensory organ in larvae of the gastropod Phestilla sibogae (Aeolidacea, Nudibranchia). Tissue and Cell 10, 153–165.
Boyd, C., Cadenas, E. (2002) Nitric oxide and cell signaling pathways in mitochondrial-dependent apoptosis. Biol. Chem. 383, 411–423.
Brenchley, G. A. (1987) Herbivory in juvenile Ilyanassa obsoleta (Neogastropoda). Veliger 30, 167–172.
Broillet, M.-C., Firestein, S. (1996) Direct activation of the olfactory cyclic nucleotide-gated channel through modification of sulfhydryl groups by NO compounds. Neuron 16, 377–385.
Cooke, I. R. C., Edwards, S. L., Anderson, C. R. (1994) The distribution of NADPH diaphorase activity and immunoreactivity to nitric oxide synthase in the nervous system of the pulmonate mollusc Helix aspersa. Cell Tiss. Res. 277, 565–572.
Couper, J., Leise, E. (1996) Serotonin injections induce metamorphosis in larvae of the gastropod mollusc Ilyanassa obsoleta. Biol. Bull. 191, 178–186.
Durham, N. R. (2002) An investigation of cGMP signaling in the metamorphic neuronal circuitry of the marine gastropod Ilyanassa obsoleta. M.S. Biology, University of North Carolina Greensboro, p. 61.
Fretter, V. (1972) Metamorphic changes in the velar musculature, head and shell of some prosobranch veligers. Journal of the Marine Biological Association of the United Kingdom 52, 161–177.
Fretter, V., Graham, A. (1962) British Prosobranch Molluscs. Ray Society, London.
Froggett, S., Leise, E. (1999) Metamorphosis in the marine snail Ilyanassa obsoleta, yes or NO? Biol. Bull. 196, 57–62.
Gifondorwa, D. J. (2002) Programmed cell death in the apical ganglion during the metamorphosis of the marine mollusc Ilyanassa obsoleta. M.S. Biology, University of North Carolina Greensboro.
Hadfield, M. G., Meleshkevitch, E. A., Boudko, D. Y. (2000) The apical sensory organ of a gastropod veliger is a receptor for settlement cues. Biol. Bull. 198, 67–76.
Hope, B. T., Michael, G. J., Knigge, K. M., Vincent, S. R. (1991) Neuronal NADPH diaphorase is a nitric oxide synthase. Proceedings of the National Academy of Science 88, 2811–2814.
Hurd, L. E. (1985) On the importance of carrion to reproduction in an omnivorous estuarine neogastropod, Ilyanassa obsoleta (Say). Oecologia 65, 513–515.
Kempf, S. C., Page, L. R., Pires, A. (1997) Development of serotonin-like immunoreactivity in the embryos and larvae of nudibranch mollusks with emphasis on the structure and possible function of the apical sensory organ. J. Comp. Neurol. 386, 507–528.
Kriegstein, A. R. (1974) Metamorphosis of Aplysia californica in laboratory culture. Proceedings of the National Academy of Science 71, 3654–3658.
Lacalli, T. (1994) Apical organs, epithelial domains, and the origin of the chordate central nervous system. American Zoologist 34, 533–541.
Leise, E. (1996) Selective retention of the fluorescent dye DASPEI in a larval gastropod mollusc after paraformaldehyde fixation. Microscopy Research and Technique 33, 496–500.
Leise, E., Nearhoof, J., Froggett, S., Cahoon, L. (1996) Benthic diatoms induce metamorphosis in larvae of the caenogastropod mollusc Ilyanassa obsoleta. American Zoologist 36, 107A.
Leise, E., Thavaradhara, K., Durham, N., Turner, B. (2001) Serotonin and nitric oxide regulate metamorphosis in the marine snail Ilyanassa obsoleta. American Zoologist 41, 122–131.
Levantine, P., Bonar, D. (1986) Metamorphosis of Ilyanassa obsoleta: Natural and artificial inducers. American Zoologist 26, 14A.
Lin, M.-F., Leise, E. M. (1996) Gangliogenesis in the prosobranch gastropod Ilyanassa obsoleta. J. Comp. Neurol. 374, 180–193.
Lin, M.-F., Leise, E. M. (1996) NADPH-diaphorase activity changes during gangliogenesis and metamorphosis in the gastropod mollusc Ilyanassa obsoleta. J. Comp. Neurol. 374, 194–203.
Marois, R., Carew, T. J. (1997) Fine structure of the apical ganglion and its serotonergic cells in the larva of Aplysia californica. Biol. Bull. 192, 388–398.
Marois, R., Carew, T. J. (1997) Ontogeny of serotonergic neurons in Aplysia californica. J. Comp. Neurol. 386, 477–490.
Marois, R., Carew, T. J. (1997) Projection patterns and target tissues of the serotonergic cells in larval Aplysia californica. J. Comp. Neurol. 386, 491–506.
Morse, D. E. (1985) Neurotransmitter-mimetic inducers of larval settlement and metamorphosis. Bulletin of Marine Science 37, 697–706.
Page, L. (2002) Apical sensory organ in larvae of the patellogastropod Tectura scutum. Biol. Bull. 202, 6–22.
Page, L. (2002) Comparative structure of the larval apical sensory organ in gastropods and hypotheses about function and developmental evolution. Invertebrate Reproduction and Development 41, 193–200.
Page, L., Parries, S. (2000) Comparative study of the apical ganglion in planktotrophic caenogastropod larvae: ultrastructure and immunoreactivity to serotonin. J. Comp. Neurol. 418, 383–401.
Pechenik, J., Li, W., Cochrane, D. (2002) Timing is everything: the effects of putative dopamine antagonists on metamorphosis vary with larval age and experimental duration in the prosobranch gastropod Crepidula fornicata. Biol. Bull. 202, 137–147.
Peunova, N., Scheinker, V., Cline, H., Enikolopov, G. (2001) Nitric oxide is an essential negative regulator of cell proliferation in xenopus brain. J. Neurosci. 21, 8809–8818.
Raven, C. (1966) Morphogenesis. The analysis of Molluscan Development. Pergamon Press, Oxford.
Scheltema, R. S. (1962) Pelagic larvae of New England intertidal gastropods I. Nassarius obsoletus Say and Nassarius vibex Say. Transactions of the American Microscopical Society 81, 1–11.
Schwartz, L., Osborne, B. (1995) Cell Death. Academic Press, Inc., San Diego.
Switzer-Dunlap, M., Hadfield, M. (1977) Observations on development, larval growth and metamorphosis of four species of Aplysiidae (Gastropod: Opishtobranchia) in laboratory culture. J. Exp. Mar. Biol. Ecol. 29, 245–261.
Thavaradhara, K., Leise, E. M. (2001) Localization of nitric oxide synthase-like immunoreactivity in the developing nervous system of the snail Ilyanassa obsoleta. J. Neurocytology 30, 449–456.
Vincent, S. (1995) Nitric Oxide in the Nervous System. Academic Press, San Diego.
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Presented at the 10th ISIN Symposium on Invertebrate Neurobiology, July 5–9, 2003, Tihany, Hungary.
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Leise, E.M., Kempf, S.C., Durham, N.R. et al. Induction of Metamorphosis in the Marine Gastropod Ilyanassa Obsoleta: 5HT, No and Programmed Cell Death. BIOLOGIA FUTURA 55, 293–300 (2004). https://doi.org/10.1556/ABiol.55.2004.1-4.35
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DOI: https://doi.org/10.1556/ABiol.55.2004.1-4.35