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Experimental Physiology 91.6 pp 977-982
DOI: 10.1113/expphysiol.2006.034710
© The Physiological Society 2006
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Pentagastrin-induced nitric oxide-dependent protein secretion from the parotid gland of the anaesthetized rat

 Hülya Çevik Aras1 and J. Ekström1

Department of 1 Pharmacology, Institute of Neuroscience and Physiology, The Sahlgrenska Academy at Göteborg University, Medicinaregatan 15 D, 405 30 Göteborg, Sweden


   Abstract
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 Abstract
Introduction
 Methods
 Results
 Discussion
 References
 
Infusion of pentagastrin (20 µg kg–1 h–1, I.V.) for 10 min evokes protein output but no overt fluid secretion from the parotid gland of the rat, as revealed by increased protein concentration in a subsequent wash-out flow of saliva in response to a bolus injection of methacholine (5 µg kg–1, I.V.) 10 min later. Using this experimental set-up, the contribution of nitric oxide (NO) generation to the protein and amylase response evoked by pentagastrin was investigated. Neither the neuronal type NO synthase inhibitor N{omega}-propyl-L-arginine (N-PLA; 30 mg kg–1, I.V.) nor the non-selective NO synthase inhibitor L-NAME (30 mg kg–1, I.V.) as such affected the methacholine-evoked volume response or the outputs of protein and amylase. However, when preceeded by the pentagastrin infusion, the expected increases in concentrations of protein (145%) and amylase activity (127%) of the methacholine-evoked response (compared to a pre-infusion methacholine response) were reduced to 68 and 74%, respectively, in the presence of N-PLA, and to 70 and 63%, respectively, in the presence of L-NAME. Thus, NO generation resulting from the activity of the neuronal type NO synthase, most probably of parenchymal origin, plays an important role in the pentagastrin-induced protein and amylase secretion of the rat parotid gland.

(Received 13 June 2006; accepted after revision 21 July 2006; first published online 17 July 2006)
Corresponding author J. Ekström: Department of Pharmacology, Institute of Neuroscience and Physiology, The Sahlgrenska Academy at Göteborg University, Medicinaregatan 15 D, 405 30 Göteborg, Sweden. Email: jorgen.ekstrom{at}pharm.gu.se


   Introduction
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 Abstract
 Introduction
Methods
 Results
 Discussion
 References
 
The secretory activity of salivary glands is, apart from circulating catecholamines, thought to be solely under nervous control (Emmelin, 1967; Johnson & Gerwin, 2001). However, the parotid gland of the anaesthetized rat was recently found to secrete proteins without any accompanying overt fluid secretion in response to the intravenous administration of pentagastrin or cholecystokinin-8, exerting their action by stimulating cholecystokinin-A receptor (Aras & Ekström, 2006). Furthermore, pentagastrin increases the protein synthesis of the parotid gland via activation of both cholecystokinin-A and -B receptors (Çevik Aras & Ekström, 2006). The increase in protein synthesis depends on nitric oxide (NO) generation resulting from the activity of neuronal type NO synthase, most probably of parenchymal origin (Çevik Aras & Ekström, 2006). In the rat parotid gland, both the β-adrenoceptor-mediated protein synthesis in vivo and the β-adrenoceptor-mediated amylase secretion in vitro depend on neuronal type NO synthase activity (Sayardoust & Ekström, 2003, 2004). Thus, there is the possibility that the cholecystokinin-A receptor-mediated secretion of protein involves generation of NO.

In the present study, the effect of pentagastrin on parotid protein and amylase secretion in the anaesthetized rat was tested in the presence of N{omega}-propyl-L-arginine (N-PLA), a highly selective inhibitor of neuronal type NO synthase (Zhang et al. 1997), or the non-selective NO synthase inhibitor L-NAME, which inhibits, in addition, NO synthase of endothelial and inducible types (Moncada, 1992). The ‘occult’ protein and amylase secretion was revealed by a subsequent wash-out flow of saliva in response to an intravenous injection of methacholine (Aras & Ekström, 2006).


   Methods
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 Methods
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A total of 44 adult female rats, weighing 288 ± 2 g, of a Spraque–Dawley strain (B&K Universal AB, Sollentuna, Sweden) were used. The rats had free excess to a pelleted standard diet (B&K Universal AB) and tap water. The experiments were approved by the local animal welfare committee, Göteborg, Sweden.

The rats were anaesthetized with pentobarbitone (50 mg kg–1, I.P.); when required, additional pentobarbitone was given intravenously so as to maintain a deep anaesthesia. The femoral vein on both sides was cannulated; one side was used for pentagastrin or saline infusion and the other for injection of drugs. The trachea was cannulated to prevent saliva from obstructing the airways. The right parotid duct was exposed externally and cannulated with a fine polyethylene tube, the dead space being about 2 µl. The body temperature of the animal was measured with a rectal probe, and maintained at 38°C using a thermostatically controlled blanket. At the end of the experiment, the animal, still under anaesthesia, was killed by exsanguination. The right parotid gland was removed and weighed.

The experimental groups were: (1) saline +N-PLA (number of rats and observations = 5); (2) pentagastrin + N-PLA (n = 5); (3) saline +L-NAME (n = 4); (4) pentagastrin + L-NAME (n = 5); (5) saline (n = 15); and (6) pentagastrin (n = 10). Groups 5 and 6 were also used in our previous study (Aras & Ekström, 2006); for the present study, group 6 was enlarged to include observations on amylase activity. The experimental design was the same as that used by Aras & Ekström (2006). Briefly, three intravenous bolus injections of a standard dose of methacholine (5 µg kg–1, at a concentration of 5 µg per ml of saline) given with 10 min intervals were followed by a 5 min pause during which, when appropriate, N-PLA or L-NAME was injected intravenously (30 mg kg–1 of each), after which there was a 10 min long period of infusion of either saline or pentagastrin, in a volume of 0.2 ml. Ten minutes thereafter, the glands were washed out once again with the standard dose of methacholine, given three times at 10 min intervals. For statistical evaluation, the response to the fourth methacholine injection (from the start) was compared to that of the third, set to 100%. Values were normalized, since the pre-infusion methacholine-evoked secretory responses varied between the different rats (and groups) studied. Saliva secreted from the duct-cannulated gland was collected in ice-chilled preweighed tubes, and the collected saliva was frozen (–20°C) and analysed on the same day. The specific density of the saliva was taken to be 1.0 g ml–1.

The experiments were carried out in the presence of the {alpha}-adrenoreceptor blocker phentolamine and the β-adrenoceptor blocker propranolol (1 mg kg–1, I.V. of each) to avoid catecholamine influences, if any, on the glands. The blockers were given twice, 10 min before the first methacholine injection and just after the end of the infusion period.

The dose of pentagastrin (20 µg kg–1 h–1, I.V.) was that used in our previous study (Aras & Ekström, 2006). The intravenous doses of N-PLA (30 mg kg–1) and L-NAME (30 mg kg–1) were also those found effective in previous works of ours (Sayardoust & Ekström, 2004; Ekström et al. 2004; Çevik Aras & Ekström, 2006).

The protein content of saliva was determined by the method of Lowry et al. (1951) and expressed in terms of concentration (µg (µl saliva)–1), using bovine serum albumin as standard. The amylase activity of saliva was analysed by an enzymatic colourimetric test (Roche Diagnostics) using {alpha}-4- nitrophenylmaltoheptaoside (4NP-G7) as substrate (Hägele et al. 1982). One unit (U) of catalytic activity of {alpha}-amylase is defined as the hydrolysis of 1 µmol of 4NP-G7 per minute per millilitre, being equivalent to the definition of the international unit. The salivary amylase activity was expressed in units per microlitre of saliva.

Pentagastrin, methacholine hydrochloride, L-NAME and propranolol hydrochloride were from Sigma (St Louis, MO, USA). Phentolamine mesylate was from Novartis (Basel, Switzerland). N{omega}-propyl-L-arginine (N-PLA) was from Cayman Chemical Company (Ann Arbor, MI, USA).

Student's t test for paired comparisons was based on log values. Comparisons between the various groups were based on percentage values using one-way analysis of variance (ANOVA) followed by Fisher's protected least-significant difference. Probabilities of less than 5% were considered significant. Values are means and S.E.M.


   Results
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 Abstract
 Introduction
 Methods
 Results
Discussion
 References
 
Methacholine-evoked fluid response upon saline or pentagastrin infusion

The amount of saliva secreted in response to a bolus dose of methacholine (5 µg kg–1, I.V.) in response to a 10 min long period of infusion of saline or pentagastrin (20 µg kg–1, I.V.), followed by a 10 min pause, was not different from that secreted in response to methacholine before the infusion period (post/pre-infusion values as percentage: 103 and 108%, respectively: Fig. 1). Neither the neuronal type NO synthase inhibitor N-PLA nor the non-selective NO synthase inhibitor L-NAME significantly affected the methacholine response after the infusion of saline (post/pre-infusion: 99 and 93%, respectively) or pentagastrin (post/pre-infusion: 94 and 102%, respectively). Comparisons between the different groups showed no statistically significant differences.

Salivary protein and amylase concentrations upon saline or pentagastrin infusion

The protein concentration tended to be higher (11%), while the concentration of amylase activity was significantly so (22%, P < 0.001), in the methacholine-evoked saliva after saline infusion compared to the responses before infusion (Aras & Ekström, 2006; Figs 2 and 3). The pattern was the same after saline infusion in the presence of N-PLA (27%, P < 0.01, and 31%, P < 0.001, respectively) or L-NAME (30%, P < 0.001, and 35%, P < 0.001, respectively), but in these conditions, the differences between post- and pre-infusion values were significant for the protein concentration as well as the amylase concentration. The percentage figures of the groups of rats exposed to saline combined with N-PLA or L-NAME were not statistically different from those of the group of rats exposed to saline alone.

The concentrations of protein and amylase activity of the methacholine-evoked saliva were markedly elevated after pentagastrin infusion (145%, P < 0.001, and 127%, P < 0.001, respectively), in accordance with our earlier study on protein concentration alone (Aras & Ekström, 2006); compared to the corresponding values after saline infusion, the differences were significant. In the presence of N-PLA, the concentrations of protein and amylase activity after the pentagastrin infusion were still significantly higher than the pre-infusion values (68%, P < 0.001, and 74%, P < 0.001, respectively) and, furthermore, than the corresponding percentage values after saline infusion with N-PLA. The percentage values obtained were, however, significantly lower than those after pentagastrin in the absence of N-PLA. The pattern was the same when L-NAME was used instead of N-PLA. The concentrations of protein and amylase activity after pentagastrin were higher than pre-infusion values (70%, P < 0.01, and 63%, P < 0.001, respectively) and than the corresponding values after saline with L-NAME, but significantly lower than the percentage values after pentagastrin in the absence of L-NAME.

Saliva secreted in response to those methacholine injections subsequent to that methacholine injection which directly followed upon the infusion period (of saline or pentagastrin with or without the NO synthase inhibitors) contained no elevated concentrations of protein and amylase activity (compared to pre-infusion values).


   Discussion
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 Abstract
 Introduction
 Methods
 Results
 Discussion
References
 
Since the volume of saliva secreted in response to methacholine was found to be the same after the infusion period of saline or pentagastrin, with or without the inhibitors of NO synthase, as before the infusion, any change in concentrations of protein or amylase occurring represented a change in total outputs of protein and amylase. The present study showed that the major part (60–70%) of the pentagastrin-induced increase in the concentration of protein and amylase activity of the methacholine-evoked saliva resulted from NO generation and was most probably entirely dependent on the activity of neuronal type NO synthase. Though of neuronal type, the NO-synthesizing enzyme, mobilized by pentagastrin, was probably of extra-nervous origin. Such an assumption gains support from a number of observations. Both isoprenaline and vasoactive intestinal peptide evoke amylase secretion in vitro from parotid tissue as a result of neuronal type NO synthase activity regardless of whether the tissue is from an innervated or chronically denervated gland (Sayardoust & Ekström, 2003). Furthermore, isolated acinar cells from innervated rat parotid glands, loaded with a fluorescent indicator of NO, increase their fluorescence intensity strongly upon exposure to noradrenaline or isoprenaline (Looms et al. 2000; Tritsaris et al. 2000). Stimulation of the sympathetic innervation, which lacks NO synthase (Alm et al. 1995, 1997), induces β-adrenoceptor-mediated increases in protein synthesis and, in addition, mitotic activity of the parotid gland in the rat. Those responses are dependent on NO and do also result from the activity of the neuronal type of NO synthase (Sayardoust & Ekström, 2004; Ekström et al. 2004).

As in the present study, the amylase in vitro response to isoprenaline and vasoactive intestinal peptide (Sayardoust & Ekström, 2003), as well as the β-adrenoceptor-mediated increase in protein synthesis (Sayardoust & Ekström, 2004) and mitotic activity (Ekström et al. 2004), engaged both NO-dependent and non-NO-dependent mechanisms to varying extents in the parotid gland of the rat. This was also the case for the pentagastrin-induced protein synthesis in the rat parotid gland (Çevik Aras & Ekström, 2006). The increase in protein synthesis (17% above resting value) in response to an infusion of pentagastrin (at the same dose as presently used but for an infusion period of 1 h) is NO dependent, whereas the CCK receptor-mediated protein synthesis at rest (being 20% of resting value) is not.

Evidently, NO is not always involved in the glandular response. In the present study, neither the fluid response nor the output of protein and amylase in response to the muscarinic agonist methacholine was affected by N-PLA or L-NAME. Previously, bethanechol and neuropeptide Y were shown to evoke secretion of amylase from isolated parotid gland tissue without any NO dependence (Sayardoust & Ekström, 2003). Though the parasympathetic innervation of the rat parotid gland contains NO synthase (Alm et al. 1995, 1997), the parasympathetic nerve-evoked fluid secretion, amylase output, protein synthesis and mitotic activity were unaffected by N-PLA and L-NAME (Sayardoust & Ekström, 2006). In rabbit parotid acinar cells, the NO generation induced by methacholine is completely inhibited by L-NAME but the methacholine-evoked amylase secretion persists (Tsunoda et al. 2003).

In the rat pancreatic gland, activation of CCK-A receptors mobilizes Ca2+, diacylglycerol and cyclic AMP to release zymogen granules (Williams, 2001). The signalling pathways mobilized by pentagastrin in the rat parotid gland are unknown. Intracellularly, the NO/cGMP signalling system may mobilize calcium and/or prolong the action of cAMP due to the inhibition of the enzymatic degradation of cAMP by phosphodiesterases (Imai et al. 1995; Looms et al. 2000; Tritsairis et al. 2000). The ‘secretory profile’ of pentagastrin resembles that of β-adrenoceptor agonists and VIP rather than that of muscarinic agonists, {alpha}-adrenoceptor agonists and substance P. The former group of agonists, using cAMP intracellularly, produces a small flow of parotid saliva with a high protein concentration, while the latter group of agonists, using Ca2+ intracellularly, produces a large flow of saliva with a low protein concentration (Baum & Wellner, 1999). Thus, cAMP seems more likely than Ca2+ as the intracellular pathway responsible for the persisting non-NO-dependent parotid protein secretion in response to pentagastrin.

Following the period of saline infusion (and the 10 min long period of pause), the concentrations of protein and amylase activity in the methacholine-evoked saliva of those rats subjected to the NO synthase inhibitors were higher than before the infusion period. Also, in the absence of the inhibitors, the concentrations of protein and amylase activity tended to increase or were significantly increased after saline (Aras & Ekström, 2006). This phenomenon has previously been reported (in the absence of NO synhase inhibitors), and is attributed to constitutive secretion in the seemingly resting gland (Proctor et al. 2000).

It is unlikely that the decrease presently observed in the pentagastrin-evoked protein and amylase response under NO synthase blockade was, to any significant extent, secondary to circulatory events or to loss of any on-going background generation of NO, since neither the volume response nor the protein and amylase response to methacholine following the period of saline infusion was diminished by the presence of N-PLA or L-NAME.

So far, activation of cholecystokinin-A receptors has been found to evoke secretion of proteins, and activation of both cholecystokinin-A and -B receptors to induce protein synthesis in the parotid gland of the anaesthetized rat (Aras & Ekström, 2006; Çevik Aras & Ekström, 2006). Under physiological conditions, gastrin and cholecystokinin are likely to play complementary roles to the autonomic nerves in the regulation of the glandular activities. Future studies will focus on the contribution of gastrin and cholecystokinin to the gland response in the awake animal under reflex stimulation.

In conclusion, the present study showed that the major part of the pentagastrin-induced protein secretion from the rat parotid gland depends on NO generation resulting from neuronal type NO synthase activity.


Figure 1
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  		Figure 1.  Fluid secretion in response to a bolus injection of methacholine (5 µg kg–1, I.V.) after and beforeinfusion of saline or pentagastrin (‘gastrin’, 20 µg kg–1 h–1, I.V.) for 10 min (followed by a pause of 10 min), expressed as a percentage, in the absence of any NO synthase inhibitor or in the presence of either N-PLA or L-NAME
The mean ± S.E.M. pre-infusion volumes secreted were: saline, 9.5 ± 0.8 µl (gland weight, 139 ± 5 mg, n = 15); pentagastrin, 11.8 ± 1.3 µl (gland weight, 139 ± 4 mg, n = 10); saline + N-PLA, 17.6 ± 3.0 µl (gland weight, 145 ± 10 mg, n = 5); pentagastrin + N-PLA, 13.9 ± 1.6 µl (gland weight, 150 ± 8 mg, n = 5); saline + L-NAME, 14.4 ± 1.5 µl (gland weight, 126 ± 6 mg, n = 4); and pentagastrin + L-NAME, 15.6 ± 1.3 µl (gland weight, 150 ± 8 mg, n = 5). The experiments were performed under {alpha}- and β-adrenoceptor blockade. Number of observations is in parentheses. Columns represent mean values and vertical bars + S.E.M. Comparisons showed no significant differences (n.s.) in the three groups or between rats treated with pentagastrin alone and those, in addition, exposed to NO synthase inhibitors. Furthermore, there were no statistically significant differences between the volume responses after and before infusion of saline, saline + N-PLA or saline + L-NAME.

 

Figure 2
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  		Figure 2.  Concentration of protein of methacholine-evoked saliva (5 µg kg–1, I.V.) after and before infusion of saline or pentagastrin (‘gastrin’, 20 µg kg–1 h–1, I.V.) for 10 min (followed by a pause of 10 min), expressed as a percentage, in the absence of any NO synthase inhibitor or in the presence of either N-PLA or L-NAME
The mean ± S.E.M. pre-infusion concentrations were: saline, 2.6 ± 0.2 µg µl–1; pentagastrin, 1.2 ± 0.1 µg µl–1; saline + N-PLA, 1.2 ± 0.1 µl µg–1; pentagastrin + N-PLA, 1.8 ± 0.3 µg µl–1; saline + L-NAME, 1.1 ± 0.1 µg µl–1; and pentagastrin + L-NAME, 1.0 ± 0.1 µg µl–1. The experiments were performed under {alpha}- and β-adrenoceptor blockade. Number of observations is in parentheses. Columns represent mean values and vertical bars + S.E.M. *P < 0.05 and ***P < 0.001 compared with saline-treated controls of each group. #***P < 0.001 compared with rats treated with pentagastrin alone. {dagger} Statistically significant differences between protein concentration of saliva secreted after and before infusion (saline + N-PLA, P < 0.01, and saline + L-NAME, P < 0.001).

 

Figure 3
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  		Figure 3.  Concentration of amylase activity of methacholine-evoked saliva (5 µg kg–1, I.V.) after and before infusion of saline or pentagastrin (‘gastrin’, 20 µg kg–1 h–1, I.V.) for 10 min (followed by a pause of 10 min), expressed as a percentage, in the absence of any NO synthase inhibitor or in the presence of either N-PLA or L-NAME
The mean ± S.E.M. pre-infusion concentrations were: saline, 0.59 ± 0.08 U µl–1; pentagastrin, 0.28 ± 0.02 U µl–1; saline + N-PLA, 0.34 ± 0.04 U µl–1; pentagastrin + N-PLA, 0.41 ± 0.04 U µl–1; saline + L-NAME, 0.21 ± 0.04 U µl–1; and pentagastrin + L-NAME, 0.31 ± 0.04 U µl–1. The experiments were performed under {alpha}- and β-adrenoceptor blockade. Number of observations is in parentheses. Columns represent mean values and vertical bars + S.E.M. *P < 0.05, **P < 0.01 and ***P < 0.001 compared with saline-treated controls of each group. #***P < 0.001 compared with rats treated with pentagastrin alone. {dagger} Statistically significant differences between concentration of amylase activity in saliva secreted after and before infusion (saline, P < 0.001, saline + N-PLA, P < 0.001, and saline + L-NAME, P < 0.001).

 

   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
Alm P, Ekström J, Larsson B, Tobin G & Andersson K-E (1997). Nitric oxide synthase immunoreactive nerves in rat and ferret salivary glands, and effects of denervation. Histochem J 29, 669–676.[CrossRef][Medline]

Alm P, Uvelius B, Ekström J, Holmqvist B, Larsson B & Andersson K-E (1995). Nitric oxide synthase-containing neurons in rat parasympathetic, sympathetic and sensory ganglia: a comparative study. Histochem J 27, 819–831.[Medline]

Aras HC & Ekström J (2006). Cholecystokinin- and gastrin-induced protein and amylase secretion from the parotid gland of the anaesthetized rat. Regul Pept 134, 89–96.[CrossRef][Medline]

Baum BJ & Wellner RB (1999). Receptors in salivary glands. In Frontiers of Oral Biology, vol. 11, Neural Mechanisms of Salivary Gland Secretion, ed. Garrett JR, Ekström J & Anderson LC, pp. 44–58. Karger, Basel.

Çevik Aras H & Ekström J (2006). Pentagastrin-induced protein synthesis in the parotid gland of the anaesthetized rat, and its dependence on CCK-A and -B receptors and nitric oxide generation. Exp Physiol 91, 673–679.[Abstract/Free Full Text]

Ekström J, Sayardoust S & Çevik H (2004). Nitric oxide-dependent mitotic activity in salivary glands of the rat upon sympathetic stimulation. Arch Oral Biol 49, 889–894.[Medline]

Emmelin N (1967). Nervous control of salivary glands. In Handbook of Physiology, section 6, Alimentary Canal Vol. II, ed. Code CF, pp. 595–632. American Physiological Society, Washington.

Hägele EO, Schaich E, Rauscher E, Lehman P, Bürk H & Wahlefeld AW (1982). Mechanism of action of human pancreatic and salivary {alpha}-amylase on β-4-nitrophenyl maltoheptaoside substrate. Clin Chem 28, 2201–2205.[Abstract/Free Full Text]

Imai A, Nashida T & Shimomura H (1995). Regulation of cAMP phosphodiesterases by cyclic nucleotides in rat parotid glands. Biochem Mol Biol Int 37, 1029–1036.[Medline]

Johnson LR & Gerwin TA (2001). Gastrointestinal Physiology, 6th edn. Mosby, St Louis.

Looms DK, Dissing S, Tritsaris K, Pedersen AM & Nauntofte B (2000). Adrenoceptor-activated nitric oxide synthesis in salivary acinar cells. Adv Dent Res 14, 62–68.[Abstract]

Lowry OH, Rosebrough NJ, Farr AL & Randall RJ (1951). Protein measurement with the Folin phenol reagent. J Biol Chem 193, 265–275.[Free Full Text]

Moncada S (1992). The 1991 Ulf von Euler Lecture. The L-arginine: nitric oxide pathway. Acta Physiol Scand 145, 201–227.[Medline]

Proctor GB, Carpenter GH, Anderson LC & Garett JR (2000). Nerve-evoked secretion of immunoglobulin A in relation to other proteins by parotid glands in anaesthetized rat. Exp Physiol 85, 511–518.[Abstract]

Sayardoust S & Ekström J (2003). Nitric oxide-dependent in vitro secretion of amylase from innervated or chronically denervated parotid glands of the rat in response to isoprenaline and vasoactive intestinal peptide. Exp Physiol 88, 381–387.[Abstract]

Sayardoust S & Ekström J (2004). Nitric oxide-dependent protein synthesis in parotid and submandiblular glands of anaesthetized rats upon sympathetic stimulation or isoprenaline administration. Exp Physiol 89, 219–227.[Abstract/Free Full Text]

Sayardoust S & Ekström J (2006). Parasympathetic nerve-evoked protein synthesis, mitotic activity and salivary secretion in the rat parotid gland and the dependence on NO-generation. Arch Oral Biol 51, 189–197.[CrossRef][Medline]

Tritsaris K, Looms DK, Nauntofte B & Dissing S (2000). Nitric oxide synthesis causes inositol phosphate production and Ca2+ release in rat parotid acinar cells. Pflugers Arch 440, 223–228.[Medline]

Tsunoda S, Michikawa H, Furuyama S & Sugiya H (2003). Evidence that nitric oxide does not directly contribute to methacholine-induced amylase secretion in rabbit parotid acinar cells. Pflugers Arch 446, 470–474.[CrossRef][Medline]

Williams JA (2001). Intracellular signaling mechanisms activated by cholecystokinin-regulating synthesis and secretion of digestive enzymes in pancreatic acinar cells. Ann Rev Phys 63, 77–97.[CrossRef][Medline]

Zhang HQ, Fast W, Marletta MA, Martasek P & Sivermann RB (1997). Potent and selective inhibition of neuronal nitric oxide synthase by N{omega}-propyl-L-arginine. J Med Chem 40, 3869–3870.[CrossRef][Medline]


   Acknowledgements
 
This work was supported by The Swedish Science Council (project no. 05927), The Medical Society in Göteborg, Willhelm and Martina Lundgren's Foundation and The LUA/ALF agreement (ALFGBG-5262). It is a particular pleasure to acknowledge the competent technical assistance provided by Mrs Ann-Christine Reinhold.





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