Filament organization and formation of microridges at the surface of fish epidermis

Abstract

The surface of fish epidermis cells is characterized by a varying pattern of microridges. Their width is about 0.3 μm and the height may reach values up to 1 μm. Under certain conditions these microridges can be maintained in cultures of epidermis derived from guppy embryos after outgrowth on glass coverslips. In such preparations indirect immunofluorescence microscopy allows the identification of actin and α-actinin as characteristic components of the microridges. The distribution of prekeratin-related tonofilaments (7- to 10-nm filaments) was visualized by the same method. A good correlation between the display of the microridges and accumulations of tonofilaments was observed, while the organization of microtubules seemed to be without any direct relation to the surface structures. The highly dynamic activity of microridges and their changing length is demonstrated by time-lapse cinemicrography. Ridges and their precursors, which are small zones of increased optical density, display in histochemical procedures a strong ATPase activity. The course of filaments in the ridges and in the subjacent terminal web has been studied also by electron microscopy. Epidermis cells of the midbody region of female guppies (Poecilia reticulata, Peters), the sea horse (Hippocampus kuda, Bleeker), and embryonic guppy epidermis in culture have been used. Treatment of adult guppy epidermis with Triton X-100 prior to fixation facilitated the interpretation of the organization of filaments in the microridges and the terminal web. From these observations a similarity between microridges and microvilli is discussed. The major similarities involve a core of actin filaments attached to the plasma membrane and a thickened glycocalyx. Filaments are arranged as bundles along the length of the ridges, a behavior which is most pronounced in the concentric ridges of the flame cone cells of sea horse epidermis. A model for the formation of the microridges is proposed which explains the strong interdependence of the development of surface protrusions and the organization of a terminal web. Folding up of the plasmalemma is thought to be brought about by the force generated by filaments inserting at the prospective flank region of the developing microridge. These filaments are supposed to stick in the subjacent terminal web and intermingle with tonofilaments. The course of filaments from opposite flanks is marked by a crossover under the center of the ridge. The relation of these findings to observations on the reformation of microvilli is briefly discussed.