Abstract
Resting secretion of salivary proteins by the parotid gland is sustained in situ between periods of eating by parasympathetic stimulation and has been assumed to involve low level granule exocytosis. By using parotid lobules from ad libitum fed rats stimulated with low doses of carbachol as an in vitro analog of resting secretion, we deduce from the composition of discharged proteins that secretion does not involve granule exocytosis. Rather, it derives from two other acinar export routes, the constitutive-like (stimulus-independent) pathway and the minor regulated pathway, which responds to low doses of cholinergic or beta-adrenergic agonists (Castle, J. D., and Castle, A. M. (1996) J. Cell Sci. 109, 2591-2599). The protein composition collected in vitro mimics that collected from cannulated ducts of glands given low level stimulation in situ. Analysis of secretory trafficking along the two pathways of resting secretion has indicated that the constitutive-like pathway may pass through endosomes after diverging from the minor regulated pathway at a brefeldin A-sensitive branch point. The branch point is deduced to be distal to a common vesicular budding event by which both pathways originate from immature granules. Detectable perturbation of neither pathway in lobules was observed by wortmannin addition, and neither serves as a significant export route for lysosomal procathepsin B. These findings show that parotid acinar cells use low capacity, high sensitivity secretory pathways for resting secretion and reserve granule exocytosis, a high capacity, low sensitivity pathway, for massive salivary protein export during meals. An analogous strategy may be employed in other secretory cell types.
Highlights
Salivary acinar cells are highly polarized epithelial cells that are specialized for the secretion of the macromolecular, electrolyte, and fluid components of saliva
These findings show that parotid acinar cells use low capacity, high sensitivity secretory pathways for resting secretion and reserve granule exocytosis, a high capacity, low sensitivity pathway, for massive salivary protein export during meals
Major Secretory Products in the Parotid Are Expressed in All Acinar Cells—In analyzing the secretory pathways that are present in parotid acinar cells, we have focused our attention on some of the major secretory products
Summary
Salivary acinar cells are highly polarized epithelial cells that are specialized for the secretion of the macromolecular, electrolyte, and fluid components of saliva. Parasympathetically and sympathetically controlled signaling pathways are synergistic in enhancing the rates of protein export and fluid and electrolyte transport [4, 7,8,9,10]. The best characterized unstimulated pathway is the constitutive-like pathway, which has been observed in various exocrine and endocrine cells and has been distinguished from the constitutive secretory pathway It preferentially exports newly synthesized proteins, beginning soon after transit through the Golgi, and has been deduced to originate by vesicular budding that is linked to the maturation of newly formed secretory granules [11]. A second unstimulated pathway occurring at Ͼ3-h chase times (after the bulk of constitutive-like secretion) exports proteins having a radiochemical composition resembling the content stored in mature secretory granules, and it may represent unstimulated granule exocytosis. The magnitude of this type of release, which has been variable in previous studies [12,13,14], is of significant interest with respect to its potential contribution to resting secretion
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