Abstract
Sea anemones are predominately sessile marine invertebrates that detect prey using a combination of receptors. Chemoreceptors detect prey derived compounds including N-acetylated sugars and amino compounds. Activated chemoreceptors tune hair bundle mechanoreceptors to frequencies and amplitudes corresponding to prey movements. Chemoreceptor-mediated adjustments to vibration sensitivity require modifications to the actin-based cytoskeleton within stereocilia of the hair bundles. Such modifications are initiated by classical second messenger cascades. Hair bundles of sea anemones arise from a multicellular complex comprising a centrally located sensory neuron surrounded by several supporting cells. Stereocilia from the supporting cells converge onto longer stereocilia from the sensory neuron. Electrophysiological recordings from supporting cells indicate that current transients accompany deflections of the hair bundle. Current transients are graded in relation to stimulus strength, saturate at strong stimuli, and are reversibly inhibited by aminoglycoside antibiotics. During prolonged stimulation, the currents completely adapt. These data suggest that individual supporting cells on opposite sides of the hair bundle function in an analogous fashion to oppositely directed hair cells of the acousticolateralis system. Hair bundles of sea anemones possess tip links among other linkages. Agents thought to attack tip links in hair bundles of vertebrate systems, including elastase and calcium free buffers, abolish vibration sensitivity in anemones. In anemones, vibration sensitivity is reversibly abolished by aminoglycoside antibiotics, but is unaffected by amiloride.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Assad, J.A., Shepherd, G.M.G., and Corey, D.P. (1991) Tip link integrity and mechanotransduction in vertebrate hair cells. Neuron 7: 985–994.
Barnes, R.D. (1987) Invertebrate Zoology. CBS College Publishing, New York, 893 pp.
Berridge, M.J., Cheek, T.R., Bennett, D.L., and Bootman, M.D. (1996) Ryanodine receptors and intracellular calcium signaling. In: Ryanodine Receptors. Sorrentino, V., ed. CRC Press, Boca Raton/New York, pp. 119–153.
Bleckmann, H. (1988) Prey identification and prey localization in surface-feeding fish and fishing spiders. In Sensory Biology of Aquatic Animals. Atema, J., Fay, R.R., Popper, A.N., and Tavolga, W.N., eds., Springer-Verlag, New York, pp. 619–641.
Cooper, J.A. (1987) Effects of cytochalasin and phalloidin on actin. J. Cell Biol. 105: 1473–1478.
Corey, D.P., and Hudspeth, A.J. (1983) Kinetics and the receptor current in bullfrog saccular hair cells. J. Neurosci. 3: 962–976.
Crawford, A.C., Evans, M.G., and Fettiplace, R. (1991) The actions of calcium on the mechano-electrical transducer current of turtle hair cells. J. Physiol. 434: 369–398.
Csukas, S.R., Rosenquist, T.H., and Mulroy, M.J. (1987) Connections between stereocilia in auditory hair cells of the alligator lizard. Hear. Res. 30: 147–156.
Holstein, T., and Tardent, P. (1984) An ultrahigh-speed analysis of exocytosis: Nematocyst discharge. Science 223: 830–833.
Kroese, A.B.A., Das, A., and Hudspeth, A.J. (1989) Blockage of the transduction channels of hair cells in the bullfrog’s sacculus by aminoglycoside antibiotics. Hear. Res. 37: 203–218.
Mariscal, R.N. (1974) Nematocysts. In: Coelenterate Biology: Reviews and New Perspectives. Muscatine, L., and Lenhoff, H.M., eds. Academic Press, New York, pp. 129–178.
Mariscal, R.N. (1984) Cnidaria: Cnidae. In: Biology of the Integument, vol. I, Invertebrates. Bereiter-Hahn, J., Maltoltsy, A.G., and Richards, K.S., eds. Springer-Verlag, Berlin/New York, pp. 57–67.
Mariscal, R.N., Conklin, E.J., and Bigger, C.H. (1978) The putative sensory receptors associated with the cnidae of cnidarians. Scanning Electron Microsc. 2: 959–966.
Mire, P., and Watson, G.M. (1997) Mechanotransduction of hair bundles arising from multicellular complexes in anemones. Hear. Res. 113: 224–234.
Mire-Thibodeaux, P., and Watson, G.M. (1993) Direct monitoring of intracellular calcium ions in sea anemone tentacles suggests regulation of nematocyst discharge by remote, rare epidermal cells. Biol. Bull. 185: 335–345.
Mire-Thibodeaux, R, and Watson, G.M. (1994a) Morphodynamic hair bundles arising from sensory cell/ supporting cell complexes frequency-tune nematocyst discharge in sea anemones. J. Exp. Zool. 268: 282–292.
Mire-Thibodeaux, R, and Watson, G.M. (1994b) Cyclical morphodynamics of hair bundles in sea anemones: Second messenger pathways. J. Exp. Zool. 270: 517–526.
Montgomery, J.C., and MacDonald, J.A. (1987) Sensory tuning of lateral line receptors in antarctic fish to the movements of planktonic prey. Science 235: 195–196.
Pantin, C.F.A. (1942) The excitation of nematocysts. J. Exp. Biol. 19: 294–310.
Parker, G.H. (1916) The effector system of actinians. J. Exp. Zool. 21: 461–484.
Parker, G.H. (1919) The Elementary Nervous System, Lippincott, Philadelphia.
Parker, G.H., and VanAlstyne, M.A. (1932) The control and discharge of nematocysts, especially in Metridium and Physalia. J. Exp. Biol. 63: 329–344.
Peteya, D.J. (1975) The ciliary-cone sensory cell of anemones and cerianthids. Tissue Cell 7: 243–252.
Pickles, J.O., Comis, S.D., and Osborne, M.P. (1984) Cross-links between stereocilia in the guinea pig organ of Corti, and their possible relation to sensory transduction. Hear. Res. 15: 103–112.
Preyer, S., Hemmert, W., Zenner, H.P., and Gummer, A.W. (1995) Abolition of the receptor potential response of isolated mammalian outer hair cells by hair-bundle treatment with elastase: a test of the tip-link hypothesis. Hear. Res. 89, 187–193.
Rusch, A., Kros, C.J., and Richardson, G.P. (1994) Block by amiloride and its derivatives of mechano electrical transduction in outer hair cells of mouse cochlear cultures. J. Physiol. 474.1: 75–86.
Russell, T.J., and Watson, G.M. (1995) Evidence for intracellular stores of calcium ions involved in regulating nematocyst discharge. J. Exp. Zool. 273: 175–185.
Shick, J.M. (1991) A Functional Biology of Sea Anemones. Chapman and Hall, New York.
Skaer, R.J., and Picken, L.E.R. (1965) The structure of the nematocyst thread and the geometry of discharge in Corynactis viridis (Allman). Phil. Trans. R. Soc. Lond., Ser. B. 250: 131–164.
Slepecky, N., and Chamberlain, S.C. (1985) The cell coat of the inner ear sensory and supporting cells as demonstrated by ruthenium red. Hear. Res. 17: 281–288.
Thorington, G.U., and Hessinger, D.A. (1988) Control of cnida discharge: I. Evidence for two classes of chemoreceptor. Biol. Bull. 174: 163–171.
Watson, G.M. (1988) Ultrastructure and cytochemistry of developing nematocysts. In The Biology of Nematocysts. (Hessinger, D.A., and Lenhoff, H.M., eds.), Academic Press, Orlando, pp. 143–164.
Watson, G.M., and Hessinger, D.A. (1987) Receptor-mediated endocytosis of a chemoreceptor involved in triggering the discharge of cnidae in a sea anemone tentacle. Tissue Cell 19: 747–755.
Watson, G.M., and Hessinger, D.A. (1989a) Cnidocytes and adjacent supporting cells form receptor-effector complexes in anemone tentacles. Tissue Cell 21: 17–24.
Watson, G.M., and Hessinger, D.A. (1989b) Cnidocyte mechanoreceptors are tuned to the movements of swimming prey by chemoreceptors. Science 243: 1589–1591.
Watson, G.M., and Hessinger, D.A. (1991) Chemoreceptor-mediated elongation of stereocilium bundles tunes vibration-sensitive mechanoreceptors on cnidocyte-supporting cell complexes to lower frequencies. J. Cell Sci. 99: 307–316.
Watson, G.M., and Hessinger, D.A. (1992) Receptors for N-acetylated sugars may stimulate adenylate cyclase to sensitize and tune mechanoreceptors involved in triggering nematocyst discharge. Exp. Cell Res. 198: 8–16.
Watson, G.M., and Hessinger, D.A. (1994a) Evidence for calcium channels involved in regulating nematocyst discharge. Comp. Biochem. Physiol. 107A: 473–481.
Watson, G.M., and Hessinger, D.A. (1994b) Antagonistic frequency tuning of hair bundles by different chemoreceptors regulates nematocyst discharge. J. Exp. Biol. 187: 57–73.
Watson, G.M., and Hudson, R.R. (1994) Frequency and amplitude tuning of nematocyst discharge by proline. J. Exp. Zool. 268: 177–185.
Watson, G.M., and Mire-Thibodeaux, P. (1994) The cell biology of nematocysts. Int. Rev. Cytol. 156: 275–300.
Watson, G.M., Mire, P., and Hudson, R.R. (1997) Hair bundles of sea anemones as a model system for vertebrate hair bundles. Hear. Res. 107: 53–66.
Watson, G.M., Mire, P., and Hudson, R.R. (1998a) Frequency specificity of vibration dependent discharge of nematocysts in sea anemones. J. Exp. Zool. 281: 582–593.
Watson, G.M., Mire, P., and Hudson, R.R. (1998b) Repair of hair bundles in sea anemones by secreted proteins. Hear. Res. 115: 119–128.
Watson, G.M., and Roberts, J. (1994) Localization of proline receptors involved in regulating nematocyst discharge. J. Exp. Zool. 270: 527–537.
Watson, G.M., and Roberts, J. (1995) Chemoreceptor-mediated polymerization and depolymerization of actin in hair bundles of sea anemones. Cell Motil. Cytoskel. 30: 208–220.
Zhao, Y., Yamoah, E.N., and Gillespie, P.G. (1996) Regeneration of broken tip links and restoration of mechanical transduction in hair cells. Proc. Natl. Acad. Sci. USA, 94: 15469–15474.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2000 Kluwer Academic/Plenum Publishers, New York
About this chapter
Cite this chapter
Watson, G.M., Mire, P. (2000). Stereocilia Based Mechanoreceptors of Sea Anemones. In: Lim, D.J. (eds) Cell and Molecular Biology of the Ear. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-4223-0_2
Download citation
DOI: https://doi.org/10.1007/978-1-4615-4223-0_2
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4613-6896-0
Online ISBN: 978-1-4615-4223-0
eBook Packages: Springer Book Archive