The pulmonary neuroepithelial endocrine system in the quail, Coturnix coturnix. Light‐ and electron‐microscopical immunocytochemistry and morphology

Abstract

Despite extensive knowledge of the neuroepithelial endocrine (NEE) system in the lungs of species of various vertebrate classes, data on avians are limited. The present investigation deals with the light- and electron-microscopical immunocytochemistry and morphology of pulmonary NEE cells in the quail, Coturnix coturnix. Light-microscopically, serotonin immunoreactivity was detected in numerous solitary and clustered NEE cells located in the cilio-mucous epithelium of primary and secondary bronchi in adult as well as in newly hatched quails. Only in newly hatched quails could a small number of bombesin- and somatostatin-like immunoreactive NEE cells be demonstrated. Electron-microscopical morphology revealed that NEE cells contained dense-cored vesicles of a wide range of diameters and electron densities. Nearly all of the NEE cells were seen to rest on the basement membrane of the cilio-mucous epithelium, lacking direct contact with the luminal surface. Nerve varicosities or nerve endings, of both afferent and efferent morphological appearance, were found directly apposed to the basal portion of NEE cells, invaginating between NEE cells or between NEE cells and adjacent epithelial cells. Often, synaptic specializations could be recognized between NEE cells and nerve terminals. Electron-microscopical immunocytochemistry confirmed that the intraepithelial serotonin-containing cells correspond to the cells with NEE characteristics. Moreover, two types of NEE cells could be distinguished in newly hatched quail lungs. Both types showed serotonin immunoreactivity selectively distributed over the dense-cored vesicles, but somatostatin- and bombesin-like immunoreactivities were only noted in one of the NEE cell types and were never seen colocalized. Thus, the avian NEE system too, harbors at least three different bioactive substances and has a morphology comparable to that of mammals, reptiles and amphibians.

Functional morphology of pulmonary neuroepithelial bodies: Extremely complex airway receptors

“…Direct innervation of pulmonary NEBs was observed in humans (Lauweryns et al, 1970) and many mammalian species, such as mice (Wasano, 1977; Wasano and Yamamoto, 1981), rats (Van Lommel and Lauweryns, 1993a), hamsters (Sorokin and Hoyt, 1989), rabbits (Lauweryns et al, 1972; Lauweryns and Van Lommel, 1987; Sorokin and Hoyt, 1989; Adriaensen and Scheuermann, 1993), and cats (Van Lommel and Lauweryns, 1993b). In birds, similar NEB/nerve contacts were reported in the lungs of chickens (Cook and King, 1969; Walsh and McLelland, 1978; Wasano and Yamamoto, 1979; López et al, 1983), pigeons (McLelland and MacFarlane, 1986), and quails (Adriaensen et al, 1994). In lower vertebrates, direct innervation was shown in reptiles, such as turtles (Scheuermann et al, 1983), lizards (Ravazzola and Orci, 1981), and snakes (Wasano and Yamamoto, 1976); in amphibia, such as newts (Scheuermann et al, 1989; Goniakowska‐Witalinska et al, 1992; Adriaensen and Scheuermann, 1993), frogs (Wasano and Yamamoto, 1978; Goniakowska‐Witalinska, 1981), and toads (Rogers and Haller, 1980; Goniakowska‐Witalinska et al, 1990); and in lungfish (Dipnoi) (Adriaensen et al, 1990).…”

Vagal innervation of the air sacs in a songbird, Taenopygia guttata

“…2J–L), a characteristic feature of neuroendocrine cells in birds as well as in mammals (Salvi & Renda, 1992; Lopez et al. 1993; Adriaensen et al. 1994).…”

“…In addition, to identify cellular and subcellular components of the vagally innervated structures in the air sac, we used antibodies against a synaptic vesicle protein SV2 (Buckley & Kelly, 1985), which labels both synaptic and neurosecretory vesicles; serotonin, which is characteristically found in avian neuroendocrine cells (Salvi & Renda, 1992; Lopez et al. 1993; Adriaensen et al. 1994); and neurofilament protein, to determine the neuronal nature of labelled structures.…”

Immunoreactive luteinizing hormone (ir-LH) cells in the lung and stomach of chick embryos

“…On the basis of the fine structural characteristics of secretory granules, a few types of endocrine cells have been identified in chicken lung (Cook and King 1969;Walsh and McLelland 1978;López et al 1983;Cook et al 1986). The existence of immunoreactive bombesin, somatostatin, or serotonin cells in the epithelial layer of avian lung was reported by Adriaensen et al (1994), and the majority of the neuroepithelial endocrine cells was distributed on the BM of the epithelium, lacking direct contact with the luminal surface. Considering the location, ir-LH cells may be different from the neuroepithelial endocrine cells already reported.…”