Changes in macromolecular organization in collagen assemblies during secretion in the nidamental gland and formation of the egg capsule wall in the dogfish Scyliorhinus canicula

Abstract

The thickest layer (L 2 ) of the egg capsule wall of the dogfish, Scyliorhinus Canicula , is constructed largely from highly ordered collagen fibrils (Knight & Hunt 1976). This collagen is stored and secreted by the nidamental gland and passes through an extraordinary series of ordered phases, m any of which have well defined liquid crystalline structure. We have examined the changes in macromolecular packing of the collagen as it moves from the cisternae of the endoplasmic reticulum to secretory granules, is secreted and then formed into the egg capsule wall. Within the endoplasmic reticulum cisternae the collagen appears anisotropic but becomes assembled into a smectic A or lamellar phase in the Golgi cisternae. This phase persists in early secretory granules, where it is found in conjunction with a micellar phase. As these granules mature, the collagen passes through a cholesteric mesophase before adopting a columnar hexagonal arrangement. On merocrine secretion the granules’ contents revert rapidly to the smectic A-lamellar and micellar phases. As it passes along the nidamental gland tubules, the collagen is first converted into a second distinct micellar phase before assembling into the final fibrils that constitute the egg capsule. These phase transitions give powerful insights into the way in which the macromolecular arrangement of collagen molecules can be modulated and are discussed in the context of a range of other related structural transitions in collagens.

The development of the oviducal gland in the Rajid thornback ray, Raja clavata

“…The larger number of transverse grooves in the baZe zone provides for a thicker egg covering (Knight et al 1993;Hamlett et al 1998). In general, oviparous species, like R. clavata (25-30 transverse grooves; present study), C. griseum (74 transverse grooves; Nalini 1940) and S. canicula (20 transverse grooves; Hamlett et al 2005) have more transverse grooves than viviparous species.…”

“…The secretory material is transformed from secretory granules into a coalescent strand within the tubular lumen and is visible in every zone of the R. clavata OG. When the coalescent strands pass through the spinneret regions of the baZe zone, they become ribbon like in form and are integrated in the network of packed Wbrils that will compose the future egg capsule (Knight et al 1993). …”

“…The material is transported to the spinneret by ciliary action and secreted around the egg jelly surface as parallel oriented Wbrils closely packed together. During the stabilization process, Wbrils experience a progressive decrease in thickness with water loss and consequent increase in resistance, improving embryo's protection (Knight et al 1993;Hamlett et al 1998). The secreted material consists of a sulphur-containing protein called prokeratine, which is chemically close to keratin (Rusaouën 1976).…”

“…The oviparous small-spotted catshark, Scyliorhinus canicula, was the Wrst to be studied (e.g. Threadgold 1957;Rusaouën 1976;Knight et al 1993), and most of the knowledge on the morphology and functionality of the OG was recorded from this species. In general, the OG is made from numerous simple gland tubules.…”

More than one way to spin a crystallite: multiple trajectories through liquid crystallinity to solid silk

“…We note that this kind of fabrication is similar to the fabrication of materials such as dogfish egg-sacks [56] and mantis ootheca [57]. In both cases, concentrated protein solutions progress through distinct mesophases before solidifying as analogues of lamellar and smectic phases.…”