1 Department of Veterinary PathoBiology, College of Veterinary Medicine, University of Minnesota, St. Paul 55108; and 2 Department of Pharmacology, University of Minnesota, Minneapolis, Minnesota 55455
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ABSTRACT |
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There is evidence for a role of cyclic ADP-ribose (cADPR) in intracellular Ca2+ regulation in smooth muscle. cADPR is synthesized and degraded by ADP-ribosyl cyclase and cADPR hydrolase, respectively, by a bifunctional protein, CD38. Nitric oxide (NO) inhibits intracellular Ca2+ mobilization in airway smooth muscle. The present study was designed to determine whether this inhibition is due to regulation of ADP-ribosyl cyclase and/or cADPR hydrolase activity. Sodium nitroprusside (SNP) and S-nitroso-N-acetylpenicillamine, NO donors, produced a concentration-dependent decrease in ADP-ribosyl cyclase, but not cADPR hydrolase, activity. The NO scavenger carboxy-PTIO prevented and reversed, and reduced glutathione prevented, the inhibition of ADP-ribosyl cyclase by SNP, suggesting S-nitrosylation by NO as a mechanism. N-ethylmaleimide, which covalently modifies protein sulfhydryl groups, making them incapable of nitrosylation, produced a marked inhibition of ADP-ribosyl cyclase, but not cADPR hydrolase, activity. SNP and N-ethylmaleimide significantly inhibited the ADP-ribosyl cyclase activity in recombinant human CD38 without affecting the cADPR hydrolase activity. These results provide a novel mechanism for differential regulation of CD38 by NO through a cGMP-independent pathway involving S-nitrosylation of thiols.
intracellular calcium; tracheal smooth muscle; S-nitrosylation
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INTRODUCTION |
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IT HAS BEEN SHOWN THAT cyclic ADP-ribose (cADPR) plays a role in the regulation of intracellular Ca2+ ([Ca2+]i) in smooth muscles of the airways (35), intestine (25), and blood vessels (20). cADPR is produced in a wide variety of mammalian tissues, including heart, liver, and brain (39). As in smooth muscle, cADPR also causes Ca2+ mobilization in these tissues. It has therefore been proposed that cADPR acts as a second messenger similar to that of inositol 1,4,5-trisphosphate (IP3). The mechanism of cADPR-induced Ca2+ mobilization is completely independent of IP3, because heparin, an IP3 receptor antagonist, does not inhibit cADPR-induced Ca2+ release from the sarcoplasmic reticulum (SR) (20, 35). cADPR has been demonstrated to mediate a variety of cellular responses, including secretion (28, 30, 38), immune cell regulation (15), cardiac function (16, 17), and myometrial contraction (7). Recent studies in our laboratory demonstrated the presence of the metabolic machinery for the synthesis and degradation of cADPR, ADP-ribosyl cyclase and cADPR hydrolase, respectively, in airway smooth muscle (40). No information is available concerning the regulation of ADP-ribosyl cyclase or cADPR hydrolase in airway smooth muscle, which will have implications for [Ca2+]i regulation and, therefore, contractility. Regulation of ADP-ribosyl cyclase activity has been described in smooth muscle of the intestine (25) as well as in coronary arterial smooth muscle (42).
Several recent studies have shown that nitric oxide (NO) inhibits the [Ca2+]i response to agonists in airway smooth muscle (18, 24, 34). NO is the predominant inhibitory neurotransmitter released from nonadrenergic, noncholinergic nerves within airways of many species (3, 4, 21). The mechanisms underlying NO-mediated airway smooth muscle relaxation have been described and include activation of soluble guanylyl cyclase, leading to the production of cGMP (22, 43), inhibition of [Ca2+]i responses to agonists (18, 24, 34), and activation of Ca2+-activated K+ (KCa) channels (1, 22). cGMP activates a cGMP-dependent kinase (10), which results in smooth muscle relaxation through phosphorylation of specific substrates, leading to a decrease in [Ca2+]i as well as a reduction in the Ca2+ sensitivity of the contractile apparatus (18, 27, 37). There is growing evidence that a variety of ion channels (1, 5, 26, 41), enzymes (2, 36), G proteins (6), and transcription factors (8) can also be regulated directly by NO, independent of the activation of soluble guanylyl cyclase and subsequent production of cGMP. The evidence presented in these reports suggests S-nitrosylation of proteins as a mechanism for the direct effects of NO.
In porcine airway smooth muscle cells, muscarinic receptor activation by acetylcholine results in [Ca2+]i oscillations (33), which reflect Ca2+ release through IP3 and ryanodine receptors in the SR (23). The steady-state phase of these oscillations principally reflects activation of ryanodine receptors and is mediated by cADPR (35). Exposure to NO donors leads to inhibition of these [Ca2+]i oscillations primarily because of inhibition of SR Ca2+ release (24, 34). cGMP-dependent and -independent mechanisms appear to be involved in the actions of NO (34). cGMP-independent mechanisms of airway smooth muscle relaxation and [Ca2+]i regulation have also been described in airway smooth muscle of other species (11, 31). However, it is not known whether NO donors have any direct effects on the enzymes involved in the synthesis and degradation of cADPR in airway smooth muscle. The purpose of the present study was therefore to examine the effects of NO on ADP-ribosyl cyclase and cADPR hydrolase activities in membranes from airway smooth muscle. Any effects of NO on these enzyme activities may, at least in part, explain the cGMP-independent effects of NO on [Ca2+]i regulation in airway smooth muscle.
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METHODS |
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Airway smooth muscle isolation and membrane preparation.
Pig tracheas were obtained from a local abattoir and transported on ice
in Hanks' balanced salt solution (pH 7.4) containing (in mM) 2.5 CaCl2, 1.2 MgCl2, 10 HEPES, and 11 glucose.
Smooth muscle was isolated as previously described (23).
Muscle pooled from two or three animals was homogenized in 8% sucrose
and 20 mM MOPS (pH 7.0) containing a protease inhibitor cocktail. Crude homogenates were centrifuged at 10,000 g for 15 min to
remove cell debris, nuclei, and mitochondria. Resulting supernatants were further centrifuged at 100,000 g for 60 min. The
pellets (crude membrane fractions) were resuspended in 8% sucrose and 20 mM MOPS (pH 7.0) and frozen at 80°C until used. Protein
concentrations were determined using a Bio-Rad protein assay kit with
bovine serum albumin as standard.
Measurement of ADP-ribosyl cyclase activity. To measure ADP-ribosyl cyclase activity, crude membranes were diluted ~1:10 in HEPES buffer (pH 7.0) containing (in mM) 10 HEPES, 148 NaCl, 5 KCl, 1.8 CaCl2, 0.3 MgCl2, and 5.5 glucose. Recombinant human CD38 (1.5 mg/ml) was treated similarly, with the exception of a 1:50 dilution in HEPES buffer. The diluted samples were then incubated in the presence of 400 µM nicotinamide guanine dinucleotide (NGD), and conversion of NGD to the fluorescent cADPR analog cyclic GDP-ribose (cGDPR) was followed in a fluorescence plate reader for 15 min (13, 14). cGDPR formation was monitored at an excitation wavelength of 305 nm and an emission wavelength of 410 nm. cGDPR is resistant to hydrolysis, unlike cADPR, making the NGD assay a useful tool to measure ADP-ribosyl cyclase activity without the confounding effects of cADPR hydrolase activity.
Measurement of cADPR hydrolase activity. cADPR hydrolase activity was measured in membrane fractions using [32P]cADPR as substrate (12). Membranes were incubated in HEPES buffer (pH 7.0), [32P]cADPR (2,000 cpm/µl), and 250 µM cADPR at 37°C for 30 min. Products were separated by thin-layer chromatography (TLC) as previously described (12). Briefly, 1 µl of reaction mixture was spotted on a PEI cellulose plate. The plate was developed in 0.2 M NaCl in 30% ethanol, dried, and exposed to a phosphor image screen for 3 h. The phosphor image was then developed using a Packard Instruments Cyclone phosphor imager. The densities of spots corresponding to cADPR and ADPR were quantified, and the amount of cADPR hydrolyzed was calculated. cADPR hydrolase activity was also determined in recombinant human CD38 and tracheal smooth muscle (TSM) membranes using a method in which the labeled ADPR formed was converted to adenosine and [32P]Pi by alkaline phosphatase and nucleotide pyrophosphatase. Separation of [32P]Pi from remaining [32P]cADPR was achieved by adding 1 ml of a slurry of 25 mg/ml Norit A in 0.1 M phosphoric acid. Remaining labeled cADPR was adsorbed by Norit A, and [32P]Pi was not. Reaction mixtures were centrifuged for 10 min at 2,000 g, an aliquot (0.7 ml) of the supernatant was quantitated in a scintillation counter, and the amount of cADPR hydrolyzed was calculated. Similar results were obtained by both methods.
Effects of NO donors on ADP-ribosyl cyclase and cADPR hydrolase activities. To determine the effect of NO donors on ADP-ribosyl cyclase and cADPR hydrolase activities, the membrane fractions were first incubated with 10-1,000 µM sodium nitroprusside (SNP) or 10-1,000 µM S-nitroso-N-acetylpenicillamine (SNAP) for 3 min. ADP-ribosyl cyclase activity was then followed after the addition of NGD as described above. cADPR hydrolase activity was measured by TLC after an additional 20-min incubation with [32P]cADPR as described above. To confirm whether the effect of SNP on ADP-ribosyl cyclase is due to the release of NO, 100 µM carboxy-PTIO (c-PTIO), an NO scavenger, was added to reaction mixtures before the addition of 100 µM SNP. In another experimental group, 100 µM c-PTIO was added after the 3-min incubation with SNP to determine whether the effect of SNP on ADP-ribosyl cyclase was reversible. To determine whether S-nitrosylation of ADP-ribosyl cyclase was a possible mechanism for NO inhibition, 2 mM reduced glutathione (GSH) was added to the reaction mixtures before the addition of SNP. To further demonstrate the role of S-nitrosylation underlying the effects of NO, TSM membranes were preincubated with N-ethylmaleimide (NEM), an alkylating agent known to covalently modify protein sulfhydryl groups, making them incapable of nitrosylation. Membranes were incubated for 5 min with 5 mM NEM and for 3 min in the presence of SNP or buffer (control) before measurement of ADP-ribosyl cyclase or cADPR hydrolase activity.
Statistical analysis. Values are means ± SE; n indicates the number of membrane preparations. The effects of various treatments, except NEM on cADPR hydrolase activity in the TSM membranes, were assessed by analysis of variance with a post hoc multiple comparison test. The effects of NEM on cADPR hydrolase activities in TSM membranes were determined by unpaired Student's t-test. P < 0.05 was considered statistically significant.
Chemicals and supplies. Cellulose PEI TLC plates were purchased from Fisher Scientific (Pittsburgh, PA); NGD, SNP, GSH, ADP-ribosyl cyclase (from Aplysia californica), and all other fine chemicals from Sigma Chemical (St. Louis, MO); Hanks' balanced salt solution from GIBCO BRL (Grand Island, NY); and c-PTIO, NEM, SNAP, and protease inhibitor cocktail from Calbiochem (La Jolla, CA). NO donors were dissolved in HEPES buffer and kept on ice before use. Bio-Rad protein assay kit was purchased from Bio-Rad Laboratories (Hercules, CA). Recombinant human CD38 expressed in a yeast expression system (29) was a generous gift from Cyrus Munshi and Hon Cheung Lee.
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RESULTS |
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Effect of NO donors on ADP-ribosyl cyclase and cADPR hydrolase
activities.
To determine whether NO has a direct, cGMP-independent effect on
ADP-ribosyl cyclase or cADPR hydrolase activity, TSM membranes were
incubated with SNP or SNAP. Exposure to 0-1,000 µM SNP led to a
concentration-dependent decrease in ADP-ribosyl cyclase activity (Fig.
1A). To eliminate the
possibility that cGMP generation in response to NO was responsible for
the observed inhibition, ADP-ribosyl cyclase activities were measured
in TSM membranes preexposed to 100 µM cGMP for 3 min. No change in
ADP-ribosyl cyclase was observed (data not shown). At 10, 100, and
1,000 µM, SNP reduced the ADP-ribosyl cyclase activities to 88, 78, and 67% of control, respectively. Activity decreased from 0.60 ± 0.08 to 0.44 ± 0.07 nmol · min1 · mg protein
1
at 1 mM SNP. SNP had no effect on cADPR hydrolase activity at any of the concentrations used (Fig. 1B). Similar
concentration-dependent inhibition of ADP-ribosyl cyclase activity was
obtained in the presence of 0-1,000 µM SNAP (Fig.
2).
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NO scavenger effects on inhibition of ADP-ribosyl cyclase by SNP.
To determine whether the effects of SNP on ADP-ribosyl cyclase activity
are due to the release of NO, the NO scavenger c-PTIO (32)
was added to reaction mixtures. Preincubation of TSM membranes with 100 µM c-PTIO prevented the inhibition caused by subsequent incubation
with 100 µM SNP (Fig. 3A).
To determine whether the inhibitory effect of SNP on ADP-ribosyl
cyclase activity was reversible, TSM membranes were incubated with 100 µM SNP for 3 min and then with 100 µM c-PTIO. c-PTIO reversed the
inhibition of ADP-ribosyl cyclase activity caused by 100 µM SNP (Fig.
3B). c-PTIO by itself had no significant effect on
ADP-ribosyl cyclase activity.
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S-nitrosylation of ADP-ribosyl cyclase as a mechanism of
inhibition.
Evidence for S-nitrosylation of sulfhydryl groups by NO on
numerous proteins, including ion channels and enzymes, has been described through a cGMP-independent mechanism. To determine
whether inhibition of ADP-ribosyl cyclase activity by NO also
involves a similar mechanism, the effects of GSH were studied. TSM
membranes were first incubated in the presence of 2 mM GSH before
addition of 100 µM SNP. GSH completely prevented the inhibition of
ADP-ribosyl cyclase activity in response to SNP (Fig.
4). GSH had no significant effect on
ADP-ribosyl cyclase activity by itself. These results suggest
S-nitrosylation of ADP-ribosyl cyclase by NO as a plausible mechanism underlying its direct effects.
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DISCUSSION |
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In the present study, we have provided evidence for cGMP-independent inhibition of ADP-ribosyl cyclase activity by NO in porcine TSM. Although membrane preparations may contain many elements, addition of cGMP to the membranes did not alter the ADP-ribosyl cyclase activities. This finding supports the conclusion that the inhibition of ADP-ribosyl cyclase by NO is not due to formation of cGMP in these crude membrane preparations. This finding is further supported by the inhibition of ADP-ribosyl cyclase activity observed in preparations of recombinant human CD38, which are unlikely to contain guanylyl cyclase/GTP/cGMP. No significant inhibition of cADPR hydrolase activity was observed in the presence of NO donors. The effects of NO were clearly concentration dependent and involved S-nitrosylation of sulfhydryl groups in the enzyme. The inhibitory effects of NO on ADP-ribosyl cyclase activity were not only prevented, but also reversed, by the NO scavenger c-PTIO. Furthermore, covalent modification of sulfhydryl groups in the enzyme by NEM also resulted in significant inhibition of ADP-ribosyl cyclase activity without any effect on cADPR hydrolase activity. The reduction of ADP-ribosyl cyclase activity in the presence of NEM was much greater than that induced by NO. Inhibition of ADP-ribosyl cyclase activity in recombinant human CD38 by SNP and NEM, with no significant effect on cADPR hydrolase activity, further supports the conclusion that the effects of NO are due to direct modification of CD38 in TSM membranes.
Sulfhydryl modification of thiol residues by NO or NEM causes selective inhibition of ADP-ribosyl cyclase, but not cADPR hydrolase, activity in TSM membranes. In many cell types, the activities of ADP-ribosyl cyclase and cADPR hydrolase are associated with a single bifunctional protein, CD38. Results of a recently published study from our laboratory in porcine TSM suggest that these enzyme activities are associated with a single protein that is localized to the plasma membrane (40). The CD38 gene has been cloned, and the nucleotide and amino acid sequences have been described for human, mouse, and rat (9). The amino acid sequence reveals 12 conserved cysteine residues, which are potential sites for thiol modification. The deduced amino acid sequence of porcine CD38 also contains these cysteine residues (unpublished observations). The selective effects of inhibition by S-nitrosylation of thiol groups on ADP-ribosyl cyclase, but not cADPR hydrolase, activity suggest that these residues are critical for ADP-ribosyl cyclase activity or are involved in its regulation. Evidence for differential regulation of ADP-ribosyl cyclase and cADPR hydrolase activities resulting from modification of specific amino acid residues in CD38 has been reported. For example, ADP-ribosylation of arginine residues in CD38 by ecto-mono-ADP-ribosyltransferases leads to inactivation of ADP-ribosyl cyclase and cADPR hydrolase activities, whereas mono-ADP-ribosylation of cysteine residues results in inhibition of cADPR hydrolase, but not ADP-ribosyl cyclase, activity (15). These findings were further confirmed by site-directed mutagenesis of arginine or cysteine residues in the CD38 and measurement of the functional consequence of such changes. Results of the present study suggest another possible mechanism for differential regulation of CD38 involving S-nitrosylation.
In smooth muscle, little information is available regarding the regulation of CD38. However, some recent studies in smooth muscles of the intestine (25) and vasculature (42) provide some evidence for such regulation. In longitudinal smooth muscle from the intestine, cholecystokinin stimulation leads to increased production of cADPR (25). This increase in cADPR levels is concentration dependent and could be suppressed by receptor antagonist or nifedipine, which blocks Ca2+ influx through voltage-gated Ca2+ channels. This study suggests that Ca2+ influx upon agonist stimulation is required for increased cADPR levels, although the mechanism by which Ca2+ influx leads to this increase was not elucidated. In a more recent study in coronary artery smooth muscle cells, Yu et al. (42) reported that NO inhibits Ca2+ mobilization through the cADPR-mediated signaling pathway. They concluded that NO led to inhibition of ADP-ribosyl cyclase activity, resulting in reduced production of cADPR and reduced [Ca2+]i. No conclusions were drawn about the mechanism by which NO produced this inhibition.
Previous studies from our laboratory indicate that NO inhibits Ca2+ release from SR of porcine TSM cells (24, 34). The membrane-permeant analog of cGMP, 8-bromo-cGMP, mimicked the effects of NO, suggesting a cGMP-dependent mechanism of [Ca2+]i regulation. However, the effects of NO on acetylcholine-induced [Ca2+]i oscillations, reflected by cADPR-induced SR Ca2+ release through ryanodine receptor channels, revealed an additional cGMP-independent [Ca2+]i regulation. The results from the present study on the selective inhibition of ADP-ribosyl cyclase offer a possible mechanism underlying this cGMP-independent component in the regulation of [Ca2+]i oscillations.
The mechanisms by which NO causes relaxation of smooth muscle are complex and involve cGMP-dependent phosphorylation of contractile proteins (19) and cGMP-independent effects on ion channels (1, 5) and oxidation of protein thiols (31). Evidence for direct activation of KCa channels by NO in airway smooth muscle has also been obtained and involves modulation of the gating characteristics of this channel (1). Activation of KCa channels leads to membrane hyperpolarization and relaxation of smooth muscle, and this effect is inhibited specifically by the KCa channel inhibitors charybdotoxin and iberiotoxin (22). We demonstrate another possible mechanism by which the direct actions of NO in airway smooth muscle can lead to reduction of [Ca2+]i and thereby contribute to relaxation. This direct effect of NO involves S-nitrosylation of CD38 and a selective inhibition of the pathway involved in the production of the Ca2+ second messenger cADPR, without any significant effect on cADPR hydrolysis. This is the first report of such a novel mechanism of CD38 regulation in airway smooth muscle.
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ACKNOWLEDGEMENTS |
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This study was supported by National Institutes of Health Grants HL-057498 (to M. S. Kannan) and DA-11806 (to T. F. Walseth) and a University of Minnesota Academic Health Center Faculty Development Grant (to M. S. Kannan and T. F. Walseth).
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FOOTNOTES |
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Address for reprint requests and other correspondence: M. S. Kannan, Dept. of Veterinary PathoBiology, College of Veterinary Medicine, University of Minnesota, 1971 Commonwealth Ave., St. Paul, MN 55108 (E-mail: kanna001{at}tc.umn.edu).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
June 21, 2002;10.1152/ajplung.00064.2002
Received 18 March 2002; accepted in final form 10 June 2002.
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