The microvilli and hyaline layer of embryonic asteroid epithelial collar cells: A sensory structure to determine the position of locomotory cilia?

Abstract

Early stage embryos of the starfish Pisaster ochraceus exhibit one cilium per cell which is primarily involved in locomotion. SEM observations have demonstrated two types of microvilli "stage horn"-like and "finger-like" microvilli (CMs), both of which probably serve to anchor and support the hyaline layer (HL). The CMs arise from the cellular membrane a short distance from the base of the ciliary shaft and form a circle around the base of each cilium. This arrangement is found in embryos and larvae as well as in adult tissues of many other marine organisms. TEM observations of material prepared by freeze substitution has demonstrated that the HL unites the circle of CMs and forms two collars. The outer ECM collar is single and attached directly to the CMs, while the inner collar consists of multiple rings of ECM located between the cilium and the CMs. The inner collar elements are not attached to the cilium but are attached to the inner aspects of the CMs by a complex arrangement consisting of a loop of ECM and two short ECM fibers. The arrangement of the ECM of the collars could provide an excellent way to transmit the movements of the cilium to the surrounding microvilli. Although the bases of the CMs always encircle the ciliary shaft, the shafts of the CMs are seen in different positions. This suggests that the CM/ECM collar may be able to change position relative to the cilium. Confocal laser scanning microscopy demonstrates that the CMs contain phalloidin positive material which extends into a phalloidin positive region located in the apex of the cells. The CMs and apical web contain microfilaments which are probably actin and could be involved in movement of the CMs. A movable circle of CMs with their associated ECM could represent a mechanism to sense the position of the cilium and/or to define the direction and extent of the stroke.

Chloral hydrate alters the organization of the ciliary basal apparatus and cell organelles in sea urchin embryos

“…Striated rootlets which are composed of numerous fibers forming horizontal bands (Anstrom 1992;Hagiwara et al 1997) do not appear to be affected by chloral hydrate. The ten microvilli surrounding each cilium in a circle (Anstrom 1992;Crawford and Campbell 1993) also do not appear to be affected by chloral hydrate.…”

“…However, very little work has been undertaken on echinoderms (Gibbins et al 1969;Anstrom 1992;Crawford and Campbell 1993). The structure and organization of the basal apparatus varies considerably in those above-mentioned genera.…”

Synthesis and secretion of molecules exhibiting the HL1 epitope during development of the hyaline layer of the asteroid pisaster ochraceus

“…If they are then transferred to fresh seawater without the antibody for 12-24 h they appear to regain some of the HL and some swimming ability. Previous studies have shown that each cilium is surrounded by a complex structure composed of a circle of microvilli and the HL that may be involved in sensing and/or coordinating ciliary movement (Crawford and Campbell, 1993). These observations suggest a possible further role for the HL, i.e., that it is necessary for normal swimming activity.…”

Ultrastructure of the abdominal sense organ of the scallop Mizuchopecten yessoensis (Jay)

“…Water flow velocity is 1.5 mm/s. Scale bar: 40 μm microvilli were found in sensory cells of sea stars (Crawford and Campbell 1993), molluscs (Frenkiel and Moueza 1980;Haszprunar 1985b), marine anemones (Golz 1994;Watson et al 1997), and nemertins (Montalvo et al 1996).…”

“…These stereovilli are also interconnected by fibrillar material (Frenkiel 1980;Haszprunar 1985b;Crawford and Campbell 1993;Montalvo et al 1996;Watson et al 1997). It was supposed that in invertebrate mechanosensitive cells, these interconnections participate in mechanotransduction (Golz and Thurm 1991;Watson et al 1998).…”