Ultrastructural changes of posterior lingual glands after hypoglossal denervation in hamsters

Abstract

Posterior lingual glands consist of two sets of minor salivary glands that serve important functions in oral physiology. To investigate the hypothesis that the hypoglossal nerve provides sympathetic innervation to the posterior lingual glands, we examined ultrastructural changes in the glands following hypoglossal denervation. In the posterior deep lingual glands (of von Ebner), the serous acinar cells showed a decrease in the number of secretory granules and an increase in lipofuscin accumulation. The ratios of cells containing lipofuscin granules were 11.39, 36.49 and 50.46%, respectively, of the control, 3- and 7-day post-axotomy glands (P < 0.001). Intraepithelial phagocytotic activity was increased. The mucous acinar cells in the posterior superficial lingual glands (of Weber) also showed degenerative changes after hypoglossal denervation. One week after nerve transection, marked cytoplasmic vacuolation and fragmentation of organelles were frequently observed. Degenerative changes were also found in unmyelinated axons associated with the glands. We provide the first evidence of the structural and functional connections between the sympathetic component of the hypoglossal nerve and posterior lingual glands.

Fig. 1

Light microscopy showed no significant morphological changes in posterior deep and superficial lingual glands after hypoglossal denervation. (A) Normal serous and mucous glands beneath the circumvallate papilla between striated muscle fibers on the control side. No significant morphological alteration in the glands 3 (B) or 7 days (C) after hypoglossal denervation. S, serous glands; M, mucous glands. Toluidine blue. Bars = 150 µm.

Fig. 2

Ultrastructures of normal acinar cells in posterior deep lingual glands. (A) Normal acinar cells filled with electron-dense secretory granules. Lipid droplets (asterisk) are occasionally found. Intercellular canaliculi and acinar lumen (L) are evident. Bar = 10 µm. (B) Higher magnification of normal acinar cells showing parallel arrays of endoplasmic reticulum and well-developed Golgi complexes (G) in perinuclear regions. Arrowheads: macula adherens. Bar = 3.4 µm.

Fig. 3

Ultrastructural changes of posterior deep lingual glands after hypoglossal denervation. (A) Three days after hypoglossal denervation, lipid droplets (asterisk) increased dramatically at the expense of secretory granules. Bar = 3.4 µm. (B) Seven days following axotomy, large bodies containing dense materials and numerous vesicles (arrowheads) are prominent. Bar = 4.0 µm. (C) Lipofuscin granules (arrowhead) are frequently found. Also note chromatin condensation and nuclear vacuolation (arrows). Bar = 2.5 µm. (D) The intercellular spaces (IS) around some acinar cells are dramatically enlarged. A: acinar cell; C: intercellular canaliculi; M: myoepithelial cell. Bar = 2.5 µm. (E) Numerous lipofuscin granules (arrowhead) are scattered in myoepithelial cells. M: myoepithelial cell nucleus. Bar = 2.0 µm. (F) Active phagocytes invading the acini. Note the lipofuscin granules (arrow) and large bodies containing dense materials and numerous vesicles (arrowhead) in the cell. A: acinar cell; N: nucleus of phagocyte. Bar = 6.5 µm.

Fig. 4

Normal ultrastructure and changes following hypoglossal denervation in posterior superficial lingual glands. (A) Normal mucous acinar cells. Note the flattened nuclei and prominent mucigen droplets. S: intercellular spaces. Bar = 4.0 µm. (B) Degenerating mucous acinar cells three days after denervation. Note the enlarged intercellular spaces (double arrowheads), dilated cisternae of endoplasmic reticulum (arrowhead), edematous mitochondria (arrows) and autophagic bodies (asterisk) containing secretory granules and cytoplasmic debris. Bar = 3.4 µm. (C and D) Degenerated mucous acinar cells 1 week after denervation. Note the obvious cytoplasmic vacuolation and fragmentation of organelles. Bars = 3.4 µm.

Fig. 5

Ultrastructural changes of axonal terminals associated with posterior lingual glands following hypoglossal denervation. (A) Three days after axotomy, a degenerating intraparenchymal terminal (asterisk) shows mitochondrial disruption and accumulation of glycogen granules. A: acinar cell; S: skeletal muscle cell; Arrowhead: basement membrane. Bar = 2.0 µm. (B–D) Degenerating extraparenchymal terminals observed 3 days after denervation, showing swollen mitochondria and vesicles (B), accumulation of glycogen granules (C) and lamellar body (D). Bars = 2.0 µm.