Spatial organization and isotubulin composition of microtubules in epidermal tendon cells ofArtemia franciscana

Abstract

Epidermally derived tendon cells attach the exoskeleton (cuticle) of the Branchiopod crustacean, Artemia franciscana, to underlying muscle in the hindgut, while the structurally similar transalar tendon (epithelial) cells, which also arise from the epidermis and are polarized, connect dorsal and ventral exopodite surfaces. To establish these latter attachments the transalar tendon cells interact with cuticles on opposite sides of the exopodite by way of their apical surfaces and with one another via basal regions, or the cuticle attachments may be mediated through linkages with phagocytic storage cells found in the hemolymph. In some cases, phyllopod tendon cells attach directly to muscle cells. Tendon cells in the hindgut of Artemia possess microtubule bundles, as do the transalar cells, and they extend from the basal myotendinal junction to the apical domain located near the cuticle. The bundled microtubules intermingle with thin filaments reminiscent of microfilaments, but intermediate filament-like structures are absent. Microtubule bundles converging at apical cell surfaces contact structures termed apical invaginations, composed of cytoplasmic membrane infoldings associated with electron-dense material. Intracuticular rods protrude from apical invaginations, either into the cuticle during intermolt or the molting fluid in premolt. Confocal microscopy of immunofluorescently stained samples revealed tyrosinated, detyrosinated, and acetylated tubulins, the first time posttranslationally modified isoforms of this protein have been demonstrated in crustacean tendon cells. Microfilaments, as shown by staining with phalloidin, coincided spatially with microtubule bundles. Artemia tendon cells clearly represent an interesting system for study of cytoskeleton organization within the context of cytoplasmic polarity and the results in this article indicate functional cooperation of microtubules and microfilaments. These cytoskeletal elements, either acting independently or in concert, may transmit tension from muscle to cuticle in the hindgut and resist compression when connecting exopodite cuticular surfaces.

Exoskeleton anchoring to tendon cells and muscles in molting isopod crustaceans

“…The fibers extending from the tendon cells deep into the cuticular matrix in non-molting specimens are known from previous studies of arthropods ( Noble-Nesbitt 1963 , Mellon 1992 , Lai-Fook and Beaton 1998 ) and were also reported in some studies of molting insect species ( Lai-Fook 1967 , Caveney 1969 , Lai-Fook and Beaton 1998 ) and in two studies of molting crustaceans ( Buchholz and Buchholz 1989 , Yamada and Keyser 2009 ).Different authors use different names to designate these fibers, which is rather confusing. They are termed muscle attachment fibers ( Caveney 1969 ), tonofibrillae ( Buchholz and Buchholz 1989 , Lai-Fook and Beaton 1998 , Tucker et al 2004 ), tonofilaments ( Subramanian et al 2003 ), intracuticular fibers ( Mellon 1992 ) and intracuticular rods ( Criel et al 2005 ). To the best of our knowledge, the macromolecules constituting these fibers have not been identified yet, neither in insects, nor in crustaceans.…”

Small, but smart: Fine structure of an avicularium in Dendrobeania fruticosa (Bryozoa: Cheilostomata)

“…In contrast to extracellular collagen tendons of vertebrates, invertebrates have specialized epithelial cells that serve as “cellular tendons” connecting muscle cells to the exoskeleton (e.g., cuticle or shell). Among invertebrates, the ultrastructure of tendon cells has been described for different groups: crustaceans (Castejón et al, 2021; Criel et al, 2005; Freeman et al, 1995; Koulish, 1973; Nakazawa et al, 1992; Okada, 1983; Rossner & Sherman, 1976; Talbot et al, 1972; Yamada & Keyser, 2009), hexapods (Auber, 1963; Caveney, 1969; Fyrberg et al, 1990; Mogami et al, 1981; Reedy & Beall, 1993; Shafiq, 1963; Smit & Akster, 1974), chelicerates (Beadle, 1973; Kuo et al, 1971; Smith et al, 1969), pycnogonids (Fahrenbach, 1994; Totland & Kryvi, 1986), tardigrades (Greven & Grohé, 1975; Shaw, 1974), pentastomids (Banaja & Riley, 1974), mollusks (Bonar, 1978; Tompa & Watabe, 1976), annelids (Bubel, 1983; Jouin, 1978), and echinoderms (Stauber & Märkel, 1988). These cells possess a specific cytoskeleton, including numerous bundles of tonofilaments and/or microtubules, and form interdigitations with the muscle cells.…”