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1 Department of Physiology, College of Medicine, Yonsei University, Seoul 120-752, Republic of Korea 2 BK 21 Project for Medical Sciences, Yonsei University, Seoul 120-752, Republic of Korea
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Abstract |
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(Received 9 December 2004;
accepted after revision 18 March 2005; first published online 15 April 2005)
Corresponding author T.-S. Nam: Department of Physiology, College of Medicine, Yonsei University 134, Shinchon-Dong, Seodaemun-Gu, Seoul 120-752, Republic of Korea. Email: tsnam{at}yumc.yonsei.ac.kr
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Introduction |
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Oscillations of [Ca2+]i evoked by acetylcholine (ACh) or carbachol (CCh) were observed in a single intestinal smooth muscle cell (Pacaud & Bolton, 1991; Komori et al. 1992, 1993). According to data previously reported, activation of a G protein by muscarinic stimulation results in the opening of non-selective cationic channels, which is further potentiated by increases in [Ca2+]i (Benham et al. 1985; Inoue & Isenberg, 1990a,b). Stimulation of muscarinic receptors also causes Ca2+ release from internal stores by inositol 1,4,5-trisphosphate (IP3) formed through phosphatidylinositol breakdown (Komori & Bolton, 1990, 1991). During muscarinic stimulation, Ca2+ inhibition of IP3-induced Ca2+ release (IICR) at some critical level of [Ca2+]i allows the Ca2+ stores to refill, which leads to a fall in [Ca2+]i to a level at which IP3 can release Ca2+ from stores again. In these ways, oscillatory changes in [Ca2+]i occur in response to muscarinic stimulation (Zholos et al. 1994), which results in oscillation of the inward cationic current (Icat; Kohda et al. 1998). Although the physiological relevance of Icat oscillation remains to be elucidated, evidence has suggested that it may play a role in stimulating and maintaining intestinal contractility in response to muscarinic agonists.
Nitric oxide (NO) and NO-liberating compounds exert a relaxing effect in various smooth muscles, including those of the intestine (Lincoln, 1989; Kuriyama et al. 1995). They also cause activation of soluble guanylate cyclase with a subsequent increase in cyclic 3,5-guanosine monophosphate (cGMP) levels (Katsuki et al. 1977), in turn activating protein kinase G (PKG; Wahler & Dollinger, 1995), which results in a reduction of [Ca2+]i through poorly understood mechanisms (Lincoln et al. 1994). Kwon et al. (2000) reported that the NO donor sodium nitroprusside (SNP) inhibits the contractile response to CCh of gastrointestinal smooth muscle by decreasing [Ca2+]i through voltage-dependent inward Ca2+ current, Icat inhibition, and Ca2+-activated K+ current activation. Therefore, it is possible that SNP also affects oscillatory changes in Icat as well as oscillations in [Ca2+]i. However, this possibility remains to be tested. Therefore, in the present work, we used patch-clamp techniques to examine the effect of SNP on Icat oscillations evoked by CCh in single longitudinal smooth muscle cells from guinea-pig ileum. Furthermore, the effect of SNP on the release of Ca2+ from intracellular stores evoked by caffeine or IP3 was examined in chemically permeabilized ileal longitudinal muscle strips.
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Methods |
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All procedures were performed in accordance with protocols approved by the Institutional Animal Care and Use Committee. The longitudinal smooth muscle layer from guinea-pig ileum was isolated by a previously described method (Komori et al. 1993; Zholos et al. 1994). Briefly, guinea-pigs of both sexes, weighing about 300–350 g, were exsanguinated after being stunned. The ileum was isolated and cut into segments 3–4 cm in length and then placed in a physiological salt solution (PSS; composition given below). The longitudinal muscle layer of the intestinal segments was peeled from the underlying circular muscle and washed in PSS.
Preparation of cells
Ileal smooth muscle cells were enzymatically dissociated with some modification to the method described previously (Komori et al. 1993; Zholos et al. 1994). Briefly, the longitudinal muscle layer from the ileum was cut into small pieces and placed into Ca2+-free PSS. Ca2+-free PSS was then replaced with PSS containing 30 µM Ca2+ (low-Ca2+ PSS) and 30 min incubation at 37°C were carried out in fresh, low-Ca2+ PSS that contained collagenase (0.3 mg ml–1), papain (0.6 mg ml–1) and bovine serum albumin (1 mg ml–1). After enzyme digestion, tissue fragments were suspended in fresh 120 µM Ca2+-containing PSS and gently agitated. The resulting suspension was centrifuged at 600g for 2 min, and the cells were resuspended in 0.5 mM Ca2+-containing PSS. Aliquots (
2–3 drops) of the cell suspension were placed into 12 mm cover glasses and stored in a humidified atmosphere at 4°C. Experiments were carried out at 22–24°C within 12 h of harvesting.
Whole-cell voltage clamp
Whole-cell membrane currents were recorded at room temperature using standard patch-clamp techniques. The patch pipette had a resistance of 3–6 M
when filled with pipette solution. Membrane currents were measured with an Axoclamp 200A voltage-clamp amplifier (Axon Instruments, Foster City, CA, USA). Command pulses were applied using pCLAMP (version 6.0) software and an IBM-compatible computer. The data were filtered at 5 kHz and displayed on an oscilloscope, computer monitor and pen recorder.
In these experiments, the oscillatory inward Icat was evoked by CCh (1 µM) in cells voltage-clamped at –60 mV (Komori et al. 1993). The agonist was applied at least 3 min after the break-through.
Permeabilized longitudinal muscle cell preparation
A muscle strip, 4–6 mm in length and 0.2–0.3 mm in width, was prepared from the longitudinal muscle layer of the ileum. The strip was mounted horizontally in a 1 ml organ chamber; one of its cut ends was fixed to the chamber and the other attached to an isometric force transducer. The organ chamber was filled with PSS kept at 23°C and the muscle strip was equilibrated under a tension of 150–180 mg for 30–60 min. Permeabilization of cell membranes was then performed by incubating the muscle strip with Staphylococcus aureus
-toxin (10 µg protein ml–1) in a Ca2+-containing solution (pCa 6) for 30–60 min until the gradual rise in tension became a steady plateau. After permeabilization, the muscle strip was bathed in a relaxing solution containing 2 mM EGTA (RI solution; composition given below).
In control experiments, intracellular Ca2+ stores of the permeabilized tissue were loaded with Ca2+ by replacing the bath medium (RI solution) with Ca2+-containing solution (pCa 5) for 10 min. Then the relaxing solution (RI solution) was reintroduced for 5 min, followed by application of caffeine or IP3 for 1–1.5 min by replacing the RI solution with another relaxing solution (RII solution; composition given below) containing the drug. The series of procedures from Ca2+ loading to drug application was repeated at an interval of 20 min. However, in the second experiment, SNP was added to the RI solution during its reintroduction and the application of caffeine or IP3. GTP (100 µM) was present during the application of caffeine or IP3 (Takemura et al. 1989).
Solutions
The PSS used for cell isolation and for recording of CCh-evoked Icat had the same composition as previously described (Komori et al. 1993) and is as follows (mM): 126 NaCl, 6 KCl, 2 CaCl2, 1.2 MgCl2, 14 glucose and 10.5 Hepes (titrated to pH 7.4 with NaOH).
The Ca2+-free PSS was prepared by omitting CaCl2 from the PSS. The patch pipette solution for oscillatory Icat recording had the following composition (mM): 134 CsCl, 1.2 MgCl2, 4 MgATP, 0.3 Na2GTP, 0.05 EGTA, 10 phosphocreatine, 10 glucose and 10 Hepes (titrated to pH 7.2 with CsOH; Komori et al. 1993). In some experiments, to hold [Ca2+]i close to a resting value typical for intestinal smooth muscle and to minimize the influence of changes in [Ca2+]i on Icat, a mixture of 10 mM BAPTA and 4.6 mM Ca2+ was used instead of 0.05 mM EGTA, since BAPTA is superior to EGTA in buffering [Ca2+]i to an almost constant level (calculated [Ca2+]i
100 nM; Zholos et al. 2000). The relaxing solution for cell membrane permeabilization had the following composition (mM): 130 potassium propionate, 4 MgCl2, 5 Na2ATP, 2 creatine phosphate, 10 creatine phosphokinase, 20 Tris-maleate, and 2 EGTA (for RI solution) or 0.05 EGTA (for RII solution) (pH 6.8), to which two agents were added, i.e. the mitochodrial inhibitor carbonyl cyanide p-trifluoromethoxy phenylhydrazone (1 µM) and the protease inhibitor E-64 (1 g ml–1). Ca2+ concentrations were changed by adding an appropriate amount of CaCl2. The apparent binding constant of EGTA for Ca2+ was considered to be 1 M at pH 6.8 and 20°C.
Chemicals
Sodium nitroprusside (SNP), EGTA, carbachol (CCh), caffeine, guanosine triphosphate (sodium salt; Na2GTP), adenosine triphosphate (magnesium salt; MgATP), Hepes, BAPTA, 8-bromo-guanosine 3',5'-cyclic monophosphate (8-Br-cGMP), Rp-8-bromo-cyclic guanosine 3',5'-cyclic monophosphate (Rp-8-Br-cGMP), creatine phosphokinase, nifedipine, heparin, Staphylococcus aureus
-toxin, E-64, D-myo-inositol-1,4,5-trisphosphate (D-myo-IP3), and 1H-(1,2,4) oxadiazole [4,3-a] quinoxaline-1-one (ODQ) were purchased from Sigma. All other chemicals were of the highest grade commercially available.
Statistics
All results are expressed as means ± S.E.M. The statistical significance of differences between given sets of data was evaluated by Student's unpaired t test. A P value less than 0.05 was considered significant.
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Results |
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In most cells (32 of 35 cells), application of 1 µM CCh at –60 mV produced an oscillatory Icat response (Fig. 1). The oscillatory changes arose from a small sustained Icat component with a more or less regular frequency or without the development of a noticeable sustained current. The current oscillation persisted for the early period or the entire application of CCh (2–10 min) as previously described (Komori et al. 1993). The oscillation frequency varied among different cells from 0.05 to 0.47 Hz, giving a mean value of 0.17 ± 0.02 Hz (n = 32).
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Figure 1 demonstrates a typical example of the SNP inhibitory effect on CCh-induced Icat oscillations. Application of SNP (10 µM) during on-going oscillations in Icat resulted in their complete cessation in all cells tested (n = 6). This effect was reversible; oscillations reappeared after the wash-out of SNP with a frequency of 0.07 ± 0.01 Hz (n = 6).
Effects of ODQ and 8-Br-cGMP on the SNP-induced inhibition of Icat osillations
Treatment of cells with 1 µM ODQ, a soluble guanylate cyclase inhibitor (Kwon et al. 2000), for about 5 min did not significantly affect the CCh-evoked Icat oscillations (0.18 ± 0.03, n = 8). However, the on-going oscillations remained unchanged after application of 1 µM SNP (Fig. 2A). Intracellular application of 8-Br-cGMP (30 µM), a membrane-permeable analogue of cGMP (Rapoport et al. 1982), via patch pipettes completely prevented the generation of Icat oscillations in response to CCh (n = 6; Fig. 2B). These results suggest that the SNP-induced inhibition of Icat oscillations involves an increased intracellular level of cGMP.
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The cellular effects of cGMP are generally regarded as being mediated by PKG, which phosphorylates a variety of functional proteins, including ion channels, and thereby alters their function (McDonald & Murad, 1996). We tested the possible involvement of cGMP in the SNP-induced inhibition of Icat oscillations.
Rp-8-Br-cGMP, the Rp-diastereoisomer of cGMP, is a highly specific PKG antagonist (Butt et al. 1994; Carvajal et al. 2001). Applied intracellularly via patch pipettes, Rp-8-Br-cGMP (30 µM) had little effect on CCh-evoked Icat oscillations (0.17 ± 0.03 Hz, n = 9). In the intracellular presence of Rp-8-Br-cGMP, application of SNP caused a significant decrease in the frequency of on-going oscillations (0.08 ± 0.02 Hz), but not cessation of them (Fig. 3). Therefore, SNP-induced inhibition of Icat oscillations was suggested to involve a cGMP/PKG-dependent mechanism.
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It is possible that the cGMP/PKG-dependent mechanism responsible for the SNP-induced inhibition of Icat oscillations affects the function of muscarinic receptors, cationic channels, or their accessory proteins. To test this possibility, [Ca2+]i was held to a certain level with 10 mM BAPTA and 4.6 mM Ca2+ ([Ca2+]i
100 nM, n
= 8; Fig. 4), which prevented changes in [Ca2+]i from altering Icat. Under such conditions, CCh evoked a sustained component of Icat without any oscillations, as previously described (Komori et al. 1993; n
= 8). Application of SNP (10 µM) did not significantly affect the on-going sustained Icat, as shown in Fig. 4. Thus, some functional process other than those of muscarinic receptors, cationic channels and their accessory proteins may be targeted by the cGMP/PKG-dependent mechanism.
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IICR may play an essential role in Icat oscillations (Komori et al. 1993; Zholos et al. 1994), so it is possible that SNP stops the current oscillation by blocking IICR by reducing IP3 receptor sensitivity or IP3 generation. We investigated this possibility by applying a maximally effective concentration of IP3 (30 µM) intracellularly via patch pipettes. This concentration of IP3 is high enough to release a maximal amount of Ca2+ from stores at a maximal rate regardless of the amount of IP3 produced by 1 µM CCh (Somlyo et al. 1992). In addition, PKG is reported to inhibit IICR in competition with IP3 (Murthy & Zhou, 2003). Thus, if the inhibitory effect of SNP on Icat oscillation is due to functional modulation of the IP3 receptor by activation of PKG, SNP is less effective in preventing Icat oscillations at higher intracellular levels of IP3. In the present experiments, CCh still evoked Icat oscillations with a frequency of 0.35 ± 0.02 Hz (n = 5) in cells recorded with IP3 (30 µM) contained in the pipette. The oscillation frequency was higher than that of Icat oscillations evoked in control cells. Application of SNP (10 µM) during the on-going Icat oscillations reduced the oscillation frequency to 17 ± 0.01 Hz (n = 5), but failed to stop the oscillation (Fig. 5). When the IP3 concentration was increased to 300 µM, SNP did not change the oscillation frequency (data not shown).
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To determine whether SNP inhibits IICR, we tested its effect on IP3-induced tension developments and, for comparison, on caffeine-induced tension effects in -toxin-permeabilized muscle strips.
During the period of Ca2+ loading (see Methods), a rise in tension occurred, which reached a plateau within 3 min. The peak tension remained almost unchanged or declined gradually by less than 30%, as previously described (Komori et al. 1995). Caffeine (10 mM), applied 5 min after reintroduction of the relaxing solution (RI solution) following Ca2+ loading, produced a transient rise in tension due to the release of stored Ca2+. The caffeine responses reached a peak within 1 min and then declined to the initial tension level before caffeine application. The second application of caffeine evoked a reproducible tension increase corresponding to 96.8 ± 2.4% (n = 4) of the first response (Fig. 6A). This reproducibility held true when the second application of caffeine was made in the presence of SNP. Indeed, the tension increase evoked was 94.1 ± 3.0% (n = 4) of the first response in the absence of SNP (Fig. 6B). IP3 (30 µM), applied in the same way as the caffeine, also elicited a transient rise in tension, which was generally smaller in size and slower in time course compared with the caffeine response. This small and slow tension response to IP3 is mainly due to a rapid breakdown of IP3 by endogenous phosphatase activity during the diffusion of IP3 into the permeabilized strip (Walker et al. 1987; Ozaki et al. 2002). The second application of IP3 evoked a reproducible tension increase (93.3 ± 6.67% of the first response, n = 4; Fig. 7A). The second response to IP3 was significantly attenuated in the presence of SNP (48.9 ± 7.8% of the first control response, n = 5; Fig. 7B).
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Discussion |
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In the gastrointestinal enteric nervous system, the non-adrenergic, non-cholinergic (NANC) inhibitory nerves play a crucial role in smooth muscle regulation. Evidence indicates that NO or a related NO-donating substance are the major candidates for NANC inhibitory transmitters (Lefebvre et al. 1991; Stark et al. 1991). Because NO is an unstable gaseous agent, NO donors, such as glyceryl trinitrate, SNP and 3-morpholinosydnonimine (SIN-1), have been widely used used as a tool for studying the effects of NO (Hirata & Murad, 1994). NO is known to activate soluble guanylate cylcase with a subsequent increase in cGMP level. Increased cGMP triggers relaxation of smooth muscle by activating PKG, which in turn phosphorylates a variety of functional proteins, including ion channels, to alter their functions (Lincoln et al. 1994; McDonald & Murad, 1996). In the present study, SNP (10 µM) completely inhibited the oscillatory change in Icat induced by 1 µM CCh in all cells tested (Fig. 1), and ODQ (1 µM), a soluble guanylate cylcase inhibitor, prevented the inhibitory effect of SNP (Fig. 2A). The cGMP analogue 8-Br-cGMP (30 µM) itself blocked the generation of Icat oscillations in response to CCh (Fig. 2B). Furthermore, Rp-8-Br-cGMP, the specific PKG antagonist, significantly attenuated the inhibitory effect of SNP (Fig. 3). These results suggest that the inhibitory effect of SNP on Icat oscillations arises via PKG activation as a result of increasing intracellular cGMP levels.
In general, the smooth muscle-relaxing action of NO donors and cGMP-increasing agents is thought to result from modification of various functional proteins involved in Ca2+ homeostasis as well as those directly associated with the contractile event (Lincoln, 1989; Kuriyama et al. 1995). Increased cGMP may reduce [Ca2+]i through activation of PKG, which causes phosphorylation of some proteins and leads to activation of Ca2+-activated K+ channels (Yamakage et al. 1996; Zhou et al. 1996), inhibition of voltage-dependent Ca2+ channels (Horowitz et al. 1996; Kwon et al. 2000), inhibition of IP3 receptors (Komalavilas & Lincoln, 1994, 1996) and reduction of IP3 (Hirata et al. 1990). These result in the reduction of [Ca2+]i and relaxation of smooth muscle. In the present study, CCh-evoked Icat oscillations were measured at a holding potential of –60 mV in 130 mM Cs-filled cells, in which voltage-dependent Ca2+ channels are deactivated and various K+ channels, including those activated by Ca2+, are totally blocked. Thus the inhibitory effect of SNP on Icat oscillations is unlikely to involve inhibition of these channels.
As mentioned in the Introduction, it has been suggested that IICR plays an essential role in sustaining Icat oscillation (Komori et al. 1993; Zholos et al. 1994). IP3-gated Ca2+ release channels are under a dual regulation by [Ca2+]i; their opening is accelerated as [Ca2+]i is increased to a certain level, but inhibited when [Ca2+]i rises higher than this level. Ca2+ inhibition of IICR at some critical level of [Ca2+]i allows Ca2+ stores to refill and leads to a fall in [Ca2+]i, thus contributing to the Icat oscillations. Therefore, even in the presence of a constant level of intracellular IP3, Ca2+-dependent inhibition of the IP3-gated Ca2+-release channel can also play an important role as a negative feedback control in giving rise to Icat oscillation. These circumstances raise at least two possible mechanisms that might be responsible for the SNP-induced inhibition of Icat oscillations: (1) functional modulation of CCh-operated cationic channels, their accessory proteins, or muscarinic receptors; and (2) reduction of [Ca2+]i by inhibition of IICR. As shown in Fig. 4, CCh-evoked sustained Icat was not affected by SNP, which may exclude the first possible mechanism. Evidence suggests that phosphorylation of IP3 receptors by PKG causes a reduction in their channel activity in response to IP3, resulting in inhibition of IICR and smooth muscle relaxation (Komalavilas & Lincoln, 1994, 1996; Murthy & Zhou, 2003). Furthermore, the inhibitory effect of PKG on IICR caused by IP3 receptor phosphorylation is in competition with the intracellular level of IP3 (Murthy & Zhou, 2003); that is, the higher the intracellular concentration of IP3, the less potent is the inhibitory effect of PKG on IICR. Moreover, the maximum rate of Ca2+ release is increased as a function of IP3 concentration and is saturated at 4 µM (Somlyo et al. 1992). So it is possible that 30 µM IP3 in the patch pipette solutions can release a maximal amount of Ca2+ from the stores at a maximal rate, and may effectively prevent the PKG effect on IICR. In the present experiments, SNP (10 µM) failed to prevent Icat oscillation in the intracellular presence of 30 µM IP3, although it reduced the oscillation frequency (Fig. 5). Increasing the IP3 concentration to 300 µM prevented the oscillation frequency effect of SNP. Tension experiments on -toxin-permeabilized muscle strips showed that SNP reduces the increase in tension produced by IP3, but not by caffeine (Figs 6 and 7). Taken together, these results suggest that the inhibitory effect of SNP on Icat oscillation is brought about, at least in part, by inhibition of IICR via functional modulation of the IP3 receptor. In addition, another possibility, that SNP-induced inhibition of Icat oscillation involves reduced IP3 production, cannot be excluded.
In conclusion, this study has demonstrated that SNP may inhibit CCh-induced Ca2+ release and Icat oscillations, and suggests that the effect of SNP involves functional modulation of IP3 receptors, but not cationic channels or muscrinic receptors. SNP regulation may also arise through a cGMP/PKG-dependent mechanism. These results provide a more comprehensive mechanism for the inhibitory action of NO on the cholinergic stimulation of intestinal motility.
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Footnotes |
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