Variations of concentric hair cells in a Cnidarian sensory epithelium (Coryne tubulosa)

Abstract

In capitate hydropolyps, the spherical end-knobs of the short tentacles present an exceptional concentration of sensory functions in one of the evolutionarily oldest nervous systems. The tentacular spheres are the basis of sensation and discrimination of objects and of capturing of prey-objects by the discharge of nematocytes (stinging cells). Recent electrophysiological studies of the spheres revealed combined chemo/mechanosensory functioning of the nematocytes and mechanosensitivity of further types of cells. The present electron microscopical study made use of the small size of the spheres of Coryne tubulosa to characterize all cells of some spheres. Five types of ectodermal cells were found to have sensory structural features and to be separated by or enclosed in supporting cells: 1) nematocytes of the stenotele type; 2) short and 3) long ciliated concentric hair cells, which carry a cilium-stereovilli bundle, similar to the cnidocil apparatus of nematocytes; 4) cells having a recessed cilium-microvilli complex equipped with a thick cell-traversing rootlet (rootlet cells); and 5) cells having a recessed short cilium with no microvilli and only a short rootlet and containing, apically as well as basally, aggregations of dense-core vesicles (vesicle-rich cells). Types 1-4 vary the configuration of a concentric cilium-microvilli complex (variations of a concentric hair bundle) and were demonstrated or inferred to be mechanosensitive. Apical exocytotic activity, which is well known for the nematocytes (discharge of their cnidocyst), is indicated by ultrastructure for the nematocyte-resembling concentric hair cells and for the vesicle-rich cells. The tentacular spheres are considered an early paradigm of a sensory epithelium. Its synaptic structures and extensive connectivity are the subject of a subsequent paper.

Stem/Progenitor Cells Derived from the Cochlear Sensory Epithelium Give Rise to Spheres with Distinct Morphologies and Features

“…Hair cell-bearing sensory organs are used by virtually all metazoan life forms for the detection of mechanical stimuli (Holtmann and Thurm 2001;Watson and Mire 1999). Throughout the animal kingdom, these organs have maintained bona fide stem cell niches, which provide regenerative capacity to replace lost sensory hair cells throughout the life of the individual animal (Corwin 1981(Corwin , 1985Corwin and Cotanche 1988;Cruz et al 1987;Lopez-Schier and Hudspeth 2006;Ryals and Rubel 1988).…”

Hydrozoan nematocytes send and receive synaptic signals induced by mechano-chemical stimuli

“…1). Besides the nematocytes, which are exclusively of the stenotele type, the spheres comprise four types of sensory cells: mechanosensory hair cells with a long or short cilium, rootlet cells and vesicle-rich, probably chemosensory, cells (Holtmann and Thurm, 2001b). Somata of ganglion cells are absent in the spheres.…”

“…The probe was hooked behind one of the stylets of the tubule and displaced the tubule by about 1 μm. We assume that in this setting a sensory rootlet cell close to the discharged nematocyte was stimulated (Holtmann and Thurm, 2001b) instead of the injured cell itself.…”

“…Additionally, we chose to study Coryne tubulosa as the smaller size of their tentacular spheres allowed for an electron-microscopical characterization of all cells and their connectivity within complete spheres (Holtmann and Thurm, 2001a;Holtmann and Thurm, 2001b). We show that hydrozoan stenotele nematocytes receive sensory signals from other nematocytes as well as from sensory cells.…”

“…The mechanosensory organelle of hydrozoan nematocytes is the cnidocil apparatus, a concentric hair bundle composed of a cilium and stereovilli originating from the same cell (in contrast to multicellular hair bundles of sea anemones). The cnidocil apparatus can be considered a prototype, as similar concentric hair bundles are found in mechanosensory hair cells of most invertebrate phyla, from cnidarians to lower chordates (Slautterback, 1967;Golz and Thurm, 1991;Golz, 1994;Thurm et al, 1998a;Holtmann and Thurm, 2001b). Sensory transduction in hydrozoan nematocytes shows mechanically controlled conductance changes similar to those of vertebrate hair cells but without directional selectivity (Brinkmann et al, 1996).…”