Sympathetic stimulation of amylase secretion during a parasympathetic background activity in the rat parotid gland

Asking, B.

doi:10.1111/j.1748-1716.1985.tb00045.x

Cited by 41 publications

(22 citation statements)

References 23 publications

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“…Furthermore, none of the proteins accumulates in the acinar extracellular space under the unstimulated or carbachol-stimulated conditions used in this study. 2 Consequently, compositional differences involving these three proteins among different secretory pathways are almost certainly the consequence of intracellular sorting events occurring generally in acinar cells and also do not reflect different cellular origins for distinct secretory pathways.…”

Section: Major Secretory Products In the Parotid Are Expressed In Allmentioning

confidence: 99%

Resting (Basal) Secretion of Proteins Is Provided by the Minor Regulated and Constitutive-like Pathways and Not Granule Exocytosis in Parotid Acinar Cells

Huang

Castle

Hinton

et al. 2001

Journal of Biological Chemistry

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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 ␤-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.Salivary acinar cells are highly polarized epithelial cells that are specialized for the secretion of the macromolecular, electrolyte, and fluid components of saliva. Macromolecular secretion is achieved by the intracellular transport pathway, culminating in exocytosis of post-Golgi carriers at the apical plasma membrane. In contrast, export of electrolytes and fluid is achieved by a transepithelial flux of ions and passive flow of water mediated by specific membrane-associated pumps and channels. Secretion is mostly neurally regulated with the discharge of macromolecules and of electrolytes and fluid being controlled differentially (1). In the parotid gland, the rate of macromolecular (mostly protein) secretion is mainly controlled by sympathetic stimulation through ␤-adrenergic receptors. Rates of fluid and electrolyte secretion are mainly controlled by parasympathetic stimulation through muscarinic acetylcholine receptors and, to a lesser extent, sympathetic stimulation through ␣-adrenergic receptors (see Refs. 2-4 and reviewed in Refs. 5 and 6). Although these are the primary divisions in secretory signaling, they are not absolute. Indeed, the dilute secretion elicited by parasympathetic stimulation in situ (or muscarinic cholinergic agonists in vitro) contains a protein content, whereas the protein-rich, low volume secretion...

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Section: Major Secretory Products In the Parotid Are Expressed In Allmentioning

confidence: 99%

Resting (Basal) Secretion of Proteins Is Provided by the Minor Regulated and Constitutive-like Pathways and Not Granule Exocytosis in Parotid Acinar Cells

Huang

Castle

Hinton

et al. 2001

Journal of Biological Chemistry

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“…At higher frequencies of parasympathetic stimulation, at which the cholinergic drive to protein secretion predominates, that effect is somehow reduced by simultaneous stimulation of the sympathetic innervation. The precise mechanism upon which this inhibition depends has yet to be identified but does not appear to relate to any restriction of the flow of blood through the gland, which is not compromised by this pattern of sympathetic stimulation (20 Hz in bursts; Figs 3 and 4; Edwards & Garrett, 1992, 1993 (Edwards & Titchen, 1990), rat (Asking, 1985) and probably the cat (Proctor, Emmelin & Garrett, 1989). Submandibular peroxidase output followed a similar pattern, except that parasympathetic was less effective than sympathetic stimulation in releasing the enzyme over the whole range of frequencies tested.…”

Section: Discussionmentioning

confidence: 99%

Secretory interactions between the sympathetic and parasympathetic innervations of the submandibular gland in the anaesthetized cat

Edwards

Garrett²,

Proctor³

1997

Experimental Physiology

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SUMMARYInteractions between the sympathetic and parasympathetic innervations of the submandibular gland have been investigated in the anaesthetized cat. At low frequencies of chorda lingual (parasympathetic) stimulation, simultaneous stimulation of the ascending cervical sympathetic nerve in bursts (20 Hz for 1 s at 10 s intervals) increased the flow of submandibular saliva, but the effect was never more than additive. The output of protein was consistently reduced by simultaneous stimulation of both the sympathetic and parasympathetic innervations, below that evoked by stimulation of either alone. Sympathetic stimulation was more effective than parasympathetic stimulation in promoting the secretion of tissue kallikrein and peroxidase in the submandibular saliva. The output of the latter enzyme, in response to sympathetic stimulation, was significantly reduced by simultaneous stimulation of the parasympathetic innervation at frequencies greater than 1 Hz, but nevertheless exceeded the amount secreted during chorda stimulation alone. Thus, this protocol provided no evidence of synergy between the two divisions of the autonomic nervous system with respect to any submandibular secretory function that was recorded. However, following the administration of a small dose of atropine (2-15 jug kg-' I.V.), sufficient to block secretion during chorda stimulation alone, the flow of saliva, in response to sympathetic stimulation, was potentiated when superimposed on a background of parasympathetic stimulation at all frequencies that were employed. This effect was abolished by larger doses of atropine, indicating that it was dependent upon activation of muscarinic receptors, only some of which could have been blocked by the initial dose.

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“…VIP is also implicated in the production of protein in the saliva in all species which have so far been studied, including the rat, sheep, pig, ferret, cat, dog and mink (Ekstrom, Mansson & Tobin, 1983;Reid & Titchen, 1985;Reid & Heywood, 1988;Ekstrom & Tobin, 1989Tobin & Ekstriom, 1992), which explains why intermittent, high-frequency stimulation, which favours the release of VIP from these nerve terminals (Andersson, Bloom Edwards & Jarhult, 1982), also promotes secretion of protein in the saliva (Buckle, Parker, Bloom & Edwards, 1995). Secretion of protein in saliva may also be enhanced when parasympathetic stimulation is combined with sympathetic stimulation, as has been shown to occur in the parotid gland of the sheep (Edwards & Titchen, 1992) and, in respect of amylase, in the parotid glands of rabbits and rats and cats (Gjorstrup, 1979;Asking, 1985;Asking & Gjorstrup 1987; Proctor, Emmelin & Garrett, 1989), although not in the submandibular gland of the cat (Edwards, Garrett & Proctor, 1997). In addition to VIP, other neuropeptides, including pituitary adenylate cyclase-activating peptide (PACAP), calcitonin gene-related peptide (CGRP) and substance P have been implicated in the control of salivary function in certain species (Ekstrom, 1987;Edwards, Reid & Titchen, 1988;Tobin, Ekstrom, Bloom & Edwards, 1991;Tobin, Asztely, Edwards, Ekstrom, HAkanson & Sundler, 1995;Tobin, Edwards, Bloom & Ekstrom, 1997 (Bloom, Edwards & Garrett, 1987) peptides were administered in the form of a bolus injection into the carotid artery at a dose of 1-25 nmol in a volume of 1-0-1 3 ml injected over a 30 s period.…”

Section: Introductionmentioning

confidence: 99%

Autonomic control of submandibular protein secretion in the anaesthetized calf

Pa¹,

Pm²,

Edwards³

1998

Experimental Physiology

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SUMMARYThe autonomic control of submandibular secretion has been investigated in fully weaned, anaesthetized calves 7 weeks after birth. Stimulation of the parasympathetic (chorda-lingual) innervation invariably produced a flow of saliva, the rate of which was frequency dependent over the range 2-8 Hz continuously. Neither the rate of flow nor the output of protein was enhanced by stimulating in bursts at relatively high frequencies. Stimulation of the sympathetic innervation (20 Hz for 1 s at 10 s intervals) alone produced a much slower flow of saliva but with a considerably higher protein content. Stimulation of both together produced no greater flow of saliva than occurred with either alone at the lower frequencies (2 and 4 Hz) but there was a pronounced synergy in respect of the secretion of protein. Following pre-treatment with propranolol (1.0 mg kg-1 I.V.), during on-going chorda-lingual stimulation at 4 Hz, intra-arterial injections of 1 nmol of either vasoactive intestinal peptide (VIP) or pituitary adenylate cyclase activating peptide (PACAP) elicited an increase in the flow and protein output of about the same order of magnitude. Calcitonin gene-related peptide (CGRP) also produced these same effects with roughly half the efficacy of VIP and PACAP but substance P had no detectable effect. It is concluded that VIP, PACAP and possibly CGRP are candidates for neurotransmitters with a role in the control of secretion in this gland.

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Sympathetic stimulation of amylase secretion during a parasympathetic background activity in the rat parotid gland

Cited by 41 publications

References 23 publications

Resting (Basal) Secretion of Proteins Is Provided by the Minor Regulated and Constitutive-like Pathways and Not Granule Exocytosis in Parotid Acinar Cells

Resting (Basal) Secretion of Proteins Is Provided by the Minor Regulated and Constitutive-like Pathways and Not Granule Exocytosis in Parotid Acinar Cells

Secretory interactions between the sympathetic and parasympathetic innervations of the submandibular gland in the anaesthetized cat

Autonomic control of submandibular protein secretion in the anaesthetized calf

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