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Institute
The honeybee hypopharyngeal gland consists in numerous units, each comprising a secretory cell and a canal cell. The secretory cell discharges its products into a convoluted tubular membrane system, the canaliculus, which is surrounded at regular intervals by rings of actin filaments. Using probes for various membrane components, we analyze the organization of the secretory cells relative to the apicobasal configuration of epithelial cells. The canaliculus was defined by labeling with an antibody against phosphorylated ezrin/radixin/moesin (pERM), a marker protein for the apical membrane domain of epithelial cells. Anti-phosphotyrosine visualizes the canalicular system, possibly by staining the microvillar tips. The open end of the canaliculus leads to a region in which the secretory cell is attached to the canal cell by adherens and septate junctions. The remaining plasma membrane stains for Na,K-ATPase and spectrin and represents the basolateral domain. We also used fluorophore-tagged phalloidin, anti-phosphotyrosine and anti-pERM as probes for the canaliculus in order to describe fine-structural changes in the organization of the canalicular system during the adult life cycle. These probes in conjunction with fluorescence microscopy allow the fast and detailed three-dimensional analysis of the canalicular membrane system and its structural changes in a developmental mode or in response to environmental factors.
Background
The hypopharyngeal gland of worker bees contributes to the production of the royal jelly fed to queens and larvae. The gland consists of thousands of two-cell units that are composed of a secretory cell and a duct cell and that are arranged in sets of about 12 around a long collecting duct.
Results
By fluorescent staining, we have examined the morphogenesis of the hypopharyngeal gland during pupal life, from a saccule lined by a pseudostratified epithelium to the elaborate organ of adult worker bees. The hypopharyngeal gland develops as follows. (1) Cell proliferation occurs during the first day of pupal life in the hypopharyngeal gland primordium. (2) Subsequently, the epithelium becomes organized into rosette-like units of three cells. Two of these will become the secretory cell and the duct cell of the adult secretory units; the third cell contributes only temporarily to the development of the secretory units and is eliminated by apoptosis in the second half of pupal life. (3) The three-cell units of flask-shaped cells undergo complex changes in cell morphology. Thus, by mid-pupal stage, the gland is structurally similar to the adult hypopharyngeal gland. (4) Concomitantly, the prospective secretory cell attains its characteristic subcellular organization by the invagination of a small patch of apical membrane domain, its extension to a tube of about 100 μm in length (termed a canaliculus), and the expansion of the tube to a diameter of about 3 μm. (6) Finally, the canaliculus-associated F-actin system becomes reorganized into rings of bundled actin filaments that are positioned at regular distances along the membrane tube.
Conclusions
The morphogenesis of the secretory units in the hypopharyngeal gland of the worker bee seems to be based on a developmental program that is conserved, with slight modification, among insects for the production of dermal glands. Elaboration of the secretory cell as a unicellular seamless epithelial tube occurs by invagination of the apical membrane, its extension likely by targeted exocytosis and its expansion, and finally the reorganisation of the membrane-associated F-actin system. Our work is fundamental for future studies of environmental effects on hypopharyngeal gland morphology and development.
Background
The hypopharyngeal gland of worker bees contributes to the production of the royal jelly fed to queens and larvae. The gland consists of thousands of two-cell units that are composed of a secretory cell and a duct cell and that are arranged in sets of about 12 around a long collecting duct.
Results
By fluorescent staining, we have examined the morphogenesis of the hypopharyngeal gland during pupal life, from a saccule lined by a pseudostratified epithelium to the elaborate organ of adult worker bees. The hypopharyngeal gland develops as follows. (1) Cell proliferation occurs during the first day of pupal life in the hypopharyngeal gland primordium. (2) Subsequently, the epithelium becomes organized into rosette-like units of three cells. Two of these will become the secretory cell and the duct cell of the adult secretory units; the third cell contributes only temporarily to the development of the secretory units and is eliminated by apoptosis in the second half of pupal life. (3) The three-cell units of flask-shaped cells undergo complex changes in cell morphology. Thus, by mid-pupal stage, the gland is structurally similar to the adult hypopharyngeal gland. (4) Concomitantly, the prospective secretory cell attains its characteristic subcellular organization by the invagination of a small patch of apical membrane domain, its extension to a tube of about 100 μm in length (termed a canaliculus), and the expansion of the tube to a diameter of about 3 μm. (6) Finally, the canaliculus-associated F-actin system becomes reorganized into rings of bundled actin filaments that are positioned at regular distances along the membrane tube.
Conclusions
The morphogenesis of the secretory units in the hypopharyngeal gland of the worker bee seems to be based on a developmental program that is conserved, with slight modification, among insects for the production of dermal glands. Elaboration of the secretory cell as a unicellular seamless epithelial tube occurs by invagination of the apical membrane, its extension likely by targeted exocytosis and its expansion, and finally the reorganisation of the membrane-associated F-actin system. Our work is fundamental for future studies of environmental effects on hypopharyngeal gland morphology and development.
Drosophila melanogaster photoreceptors are highly polarized cells and their plasma membrane is organized into distinct domains. Zonula adherens junctions separate a smooth peripheral surface, the equivalent of the basolateral surface in other epithelial cells, from the central surface (cong apical surface). The latter consists of the microvillar rhabdomere and the juxtarhabdomeric domain, a nonmicrovillar area between the rhabdomere and the zonulae adherens. The distribution of Na/K-ATPase over these domains was examined by immunocytochemical, developmental, and genetic approaches. Immunofluorescence and immunogold labeling of adult compound eyes reveal that the distribution of Na/ K-ATPase is concentrated at the peripheral surface in the photoreceptors R1-R6, but extends over the juxtarhabdomeric domain to the rhabdomere in the photoreceptors R7/R8. Developmental analysis demonstrates further that Na/K-ATPase is localized over the entire plasma membrane in all photoreceptors in early pupal eyes. Redistribution of Na/K-ATPase in R1- R6 occurs at about 78% of pupal life, coinciding with the onset of Rh1-rhodopsin expression on the central surface of these cells. Despite the essential role of Rh1 in structural development and intracellular trafficking, Rh1 mutations do not affect the distribution of Na/K-ATPase. These results suggest that Na/K-ATPase and rhodopsin are involved in distinct intracellular localization mechanisms, which are maintained independent of each other.