Comparison of nonciliated tracheal epithelial cells in six mammalian species: ultrastructure and population densities.

Abstract

Three types of nonciliated epithelial cells in mammalian conducting respiratory airways are thought to be secretory: mucous (goblet) cells, serous epithelial cells, and Clara cells. Mucous and serous cells are considered to be the secretory cells of the trachea. Clara cells are considered to be the secretory cells of the most distal conducting airways or bronchioles. To ascertain if mucous and serous epithelial cells are common to the tracheal epithelium of mammalian species, we characterized the ultrastructure and population densities of tracheal epithelial cells in six species: hamster (H), rat (Rt), rabbit (Rb), cat (C), Bonnet monkey (M. radiata) (B), and sheep (S). Following fixation by airway infusion with glutaraldehyde/paraformaldehyde, tracheal tissue was processed for light and electron microscopy (EM) by a selective embedding technique. Tracheal epithelium over cartilage was quantitated by light microscopy and characterized by transmission EM. Mucous cells were defined by abundant large nonhomogeneous granules, numerous Golgi complexes, basally located nuclei and granular endoplasmic reticulum (GER). The percentage of mucous cells in the tracheal epithelium was: H (0%), Rt (0.5%), Rb (1.3%), C (20.2%), B (8%), S (5.1%). Serous cells had homogeneous, electron-dense granules and extensive GER. Serous cells were present only in rats (39.2%). Clara cells had homogeneous electron-dense granules, abundant agranular endoplasmic reticulum (AER) and basal GER. Clara cells were found in hamsters (41.4%) and rabbits (17.6%). In sheep trachea, 35.9% of the epithelial cells had small electron-lucent granules, abundant AER and numerous Golgi complexes. In Bonnet monkey trachea, 16% of the epithelial cells had small electron-lucent granules, numerous polyribosomes, perinuclear Golgi apparatus and moderate GER. In cat trachea, 5.4% of the epithelial cells lacked granules, and had moderate numbers of mitochondria, moderate amounts of polyribosomes, a central nucleus, and long luminal microvilli. The percentage of the tracheal epithelial population occupied by basal, ciliated and nonciliated cells was: H (5.6%, 47.5%, 46.7%), Rt (13.4%, 40.6%, 45.9%), Rb (28.2%, 43.0%, 28.3%), C (37.3%, 36.1%, 26.7%), B (31%, 41%, 28%), S (28.5%, 30.6%, 41%). We conclude: 1) mucous and serous cells are not common to the tracheal epithelial lining of all mammalian species; 2) there is significant interspecies heterogeneity in the abundance, distribution and ultrastructure of tracheal secretory cells; 3) potential differences in the roles of nonciliated cells in tracheal function exists within tracheal epithelial populations and between species.