Institut für Klinische Physiologie / Inst. of Clinical Physiology
Charité  > Campus Benjamin Franklin  > Inst. Clin. Physiology  > Gitter  > Nematocysts

Alfred H. Gitter
The discharge of nematocysts:
an extraordinary and fast exocytotic process

Nematocytes are the stinging cells in the ectoderm of cnidarians. They contain a unique, very large secretory vesicle (e.g., in Hydra vulgaris the diameter is up to 10 mm), the capsular nematocyst, which can eject its content (in stenotele-typ nematocysts a coiled, inverted tubule) in a spectacular discharge process. Nematocyst discharge is initiated by voltage- and Ca2+-dependent exocytosis (Gitter et al., 1994), which is triggered by mechanoreception that can be blocked by streptomycin (Gitter and Thurm, 1993a).

Revisiting the history of the recognition of cnidarians as animals and the discovery of nematocysts, Lenhoff and Lenhoff (1988) relate that overall function and morphology of the nematocysts were detected not until the mid-nineteenth century when the necessary techniques of histology had been developed. The early literature on nematocysts has been reviewed by Weill (1934), and thereafter Mariscal (1974) outlined the topic. Following the suggestions of a colloquium on terminology held in 1986 (Watson and Wood, 1988), the intracellular secretory product diagnostic of all members of the phylum Cnidaria shall be called cnida and the three major categories of cnidae are nematocysts, spirocysts and ptychocysts. The nematocyst is an organelle of the nematocyte, which developes from the (immature) nematoblast.

As shown by transmission electron microscopy (Golz, 1994), the nematocyst is completely enclosed by a vesicular membrane. In its basolateral portion, this membrane is separated from the cell membrane by a more than 0.5 mm thick cytoplasmic layer containing other intracellular membranes and a complex cytoskeleton. At its apical part, however, the nematocyst membrane is closely apposed to the cell membrane of the opercular region, forming a putative contact region of up to 1 mm2. Here are vesicular and cell membranes separated by a thin cytoplasmic lamella of less than 50 nm.

Anderson and McKay (1987) report that depolarization of nematocytes' cell membrane with intracellular current injection does not trigger cyst discharge in nematocytes in situ or isolated from various Hydrozoa and Scyphozoa. By contrast, stenotele-type nematocysts of Hydra vulgaris discharge upon extracellular electrical stimulation that depolarizes the apical membrane of nematocytes by about 25 mV (threshold) or more (Gitter et al., 1994). Starvation increases the electrically induced exocytosis of nematocysts (Gitter and Thurm, 1993b).

The time course of the rapid process of nematocyst discharge has been visualized in Hydra vulgaris by Holstein and Tardent (1984). Discharge was triggered by an extracellular electrical stimulus. Using high-speed microcinematography, an initial increase of the stenotele volume (phase a) can be demonstrated during the interval between the onset of the electrical stimulus and the opening of the operculum. After about 100 ms the capsule's cover is opened and the stylets are ejected in less than 10 ms (phase b). Discharge is then arrested for approximately 150 ms (phase c), presumably in order to allow withdrawal of the stylets from the opening created in the prey's integument. Then the long (0.5 mm) and slender (0.8 mm) tubule evaginates at a velocity of about 0.3 m/s into the prey's body.

The volume of the capsule of in situ nematocysts (Robson, 1973; Holstein and Tardent, 1984) and of isolated capsules (Salleo et al., 1986) increases immediately before evagination of their tubular contents. After discharge, however, the volume of the capsule decreases by 40 - 50 % (Tardent and Holstein, 1982; Holstein and Tardent, 1984; Salleo et al., 1986).

Due to technical difficulties Holstein and Tardent (1984) did not determine precisely the delay between electrical stimulus and the first visible sign of discharge. Using a new technique, light microscopic images of stenotele discharge have been produced with an electrical pulse that stimulated discharge and, with a variable delay, triggered a flash of light (Gitter, 1995). The time between depolarization of the nematocyte's apical membrane and visible discharge (i.e., projection of the stylets and appearance of the tubular content oft the nematocyst) is between 1/3 and 1 ms (Gitter, 1994; Gitter and Thurm, 1996).

series 1:

3 consecutive video micrographs (20 ms apart)

  

series 2:

3 consecutive video micrographs (20 ms apart)

a: before discharge, bar 20 m m, 15 m s illumination

  

a: before discharge, bar 20 m m, arrow: stenotele

 

b: during discharge (350 m s after depolarization)

  

b: during discharge (400 m s after depolarization)

 

c: after discharge (insert: stenotele and desmoneme)

  

c: after discharge, arrow: stenotele tubule ejected

 

 

The delay between membrane depolarization and first signs of discharge, measured at 24 °C, is similar to the delay between pre-synaptic action potential and exocytosis of synaptic vesicles (as assayed by the post-synaptic potential change) in frog motor neurons, 0.5 ms at 19 °C (Katz and Miledi, 1965), and cat afferent neurons, 0.2 ms at 38 °C (Munson and Sypert, 1979; Cope and Mendell, 1982).

References