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Department of Medicine, University of Illinois at Chicago, Chicago, Illinois 60612
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ABSTRACT |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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The purpose of this study was to determine whether tannic acid elicits neurogenic plasma exudation from the oral mucosa in vivo and, if so, whether this response is transduced in part by the L-arginine-nitric oxide (NO) biosynthetic pathway. Using intravital microscopy, we found that suffusion of tannic acid elicits significant concentration-dependent leaky site formation and increase in clearance of fluorescein isothiocyanate-dextran (molecular mass 70 kDa) from the in situ hamster cheek pouch (P < 0.05). These effects are significantly attenuated by two selective, but structurally distinct, nonpeptide neurokinin-1 (NK1) receptor antagonists, CP-96,345 and RP-67580, but not by CP-96,344, the 2R,3R enantiomer of CP-96,345. NG-nitrol-arginine methyl ester (L-NAME), an NO synthase inhibitor, but not D-NAME, significantly attenuates tannic acid-induced responses. L-Arginine, but not D-arginine, reverses the attenuating effects of L-NAME. We conclude that tannic acid elicits L-arginine-NO biosynthetic pathway-dependent neurogenic plasma exudation from the in situ hamster cheek pouch.
microcirculation; tachykinins; neurokinin-1 receptor antagonist; nitric oxide; byssinosis
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INTRODUCTION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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TANNINS, A MAJOR COMPONENT of plant polyphenols (2, 4, 5, 25, 28), have been implicated in the pathophysiology of byssinosis in cotton and textile workers (34). The acute, intermittent phase of this disorder is characterized by coughing, wheezing, chest tightness, and shortness of breath (34). These manifestations are thought to be related, in part, to airway mucosa inflammation elicited by tannins (4, 5, 15, 29, 32). However, the mechanisms underlying this process are uncertain.
To this end, the airway mucosa is densely innervated with perivascular sensory nerves that also extend into the surface epithelium (8, 12, 18, 27, 30). Various environmental toxicants have been shown to stimulate these nerves to release tachykinins, the best known of which is substance P (7, 11, 18, 22, 30). On its release, substance P activates a cascade of biological responses in the tissue collectively termed neurogenic inflammation (8, 11, 12, 27, 30). A characteristic feature of this process is plasma exudation from postcapillary venules mediated by stimulation of neurokinin-1 (NK1) receptors that, if persistent, could lead to pronounced interstitial edema and tissue dysfunction (8, 10-12, 27, 30). Current concepts suggest that substance P-induced plasma exudation from the airway mucosa is transduced, in part, by the L-arginine-nitric oxide (NO) biosynthetic pathway (1, 13, 17).
We reasoned that because byssinosis is associated with acute, intermittent symptoms of airway dysfunction, tannins, a major component of cotton bracts, could play a role in the pathophysiology of this disorder by stimulating sensory nerves in the airway mucosa to elicit neurogenic plasma exudation (7, 11, 18, 22, 30). The purpose of this study was to begin to address this issue by determining whether tannic acid elicits neurogenic plasma exudation from the in situ hamster cheek pouch and, if so, whether this response is transduced, in part, by the L-arginine-NO biosynthetic pathway.
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METHODS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Preparation of Animals
Adult, male, golden Syrian hamsters weighing 135 ± 2 g (n = 26) were anesthetized with pentobarbital sodium (6 mg/100 g body wt ip). A tracheotomy was performed to facilitate spontaneous breathing. A femoral vein was cannulated to inject the intravascular tracer, fluorescein isothiocyanate-labeled dextran (FITC-dextran; molecular mass 70 kDa; 40 mg/100 g body wt dissolved in 1.0 ml normal saline and administered over 1 min) and supplemental anesthesia (2-4 mg · 100 g body wt
1 · h1). A femoral artery
was cannulated to obtain arterial blood samples and monitor arterial
blood pressure. Body temperature was kept constant (37-38°C)
throughout the experiment with the use of a heating pad.
To visualize the microcirculation of the cheek pouch, we used a method previously described in our laboratory (9-11). Briefly, the left cheek pouch was spread gently over a small plastic baseplate, and an incision was made in the outer skin to expose the cheek pouch membrane. The avascular connective tissue layer was removed, and a plastic chamber was positioned over the baseplate and secured in place by suturing the skin around the upper chamber. This chamber contained the suffusion fluid. This arrangement forms a triple-layered complex: the baseplate, the upper chamber, and the cheek pouch membrane exposed between the two plates. After these initial procedures, the hamster was transferred to a heated microscope stage. The chamber was connected to a reservoir containing warmed bicarbonate buffer (37-38°C) composed (in mM) of 131.9 NaCl, 2.95 KCl, 1.48 CaCl2, 0.76 MgCl2, and 11.87 NaHCO3, which allowed continuous suffusion of the cheek pouch. The buffer was bubbled continuously with 95% N2-5% CO2 (pH 7.4). The chamber was also connected via a three-way valve to an infusion pump (Sage Instruments, Boston, MA) that allowed for the constant administration of drugs into the suffusate.
Determination of Clearance of Macromolecules
The cheek pouch microcirculation was visualized with an Olympus microscope (Jacobs Instruments, Shawnee Mission, KS) coupled to a 100-W mercury light source at a magnification of ×40. Fluorescence microscopy was accomplished with the aid of filters that matched the spectral characteristics of FITC-dextran as previously described (9-11, 19, 21, 23, 30, 31). Macromolecular leakage was determined by extravasation of FITC-dextran, which appeared as fluorescent "spots" or leaky sites around postcapillary venules. The number of leaky sites was determined by counting three random microscopic fields every minute for the first 7 min and then at 5-min intervals for 30-60 min after each intervention (see below). The total number of leaky sites was averaged and expressed as the number of leaky sites per 0.11 cm2 of cheek pouch, corresponding to the area of one microscopic field (10, 11).To calculate clearance of FITC-dextran from the cheek pouch, the suffusate was collected at 5-min intervals during the experiment using a fraction collector (Cygnet, ISCO, Lincoln, NE). Samples were collected in glass test tubes, and the concentration of FITC-dextran was determined. Arterial blood samples were collected in heparinized capillary tubes (70-µl volume; Scientific Products, McGraw Park, IL), beginning 5 min before and 5, 30, 60, 120, 180, and 240 min after injection of FITC-dextran. The concentration of FITC-dextran was determined in all plasma samples. To quantitate the concentration of FITC-dextran in plasma and suffusate, a standard curve for FITC-dextran concentrations versus percent emission was performed on a spectrophotofluorometer (Photon Technology International, Princeton, NJ). The standard was FITC-dextran that was prepared on a weight per volume basis. With the bicarbonate buffer used as background, a standard curve was generated for each experiment and each curve was subjected to linear regression analysis. The percent emission for unknown samples (plasma and suffusate) was measured on the spectrophotofluorometer, and the concentration of FITC-dextran was calculated from the standard curve. In preliminary experiments, minimal fluorescence signal (<2% above background) was detected when drugs were added to the buffer and when plasma and suffusate samples were examined before addition of FITC-dextran. Clearance of FITC-dextran was determined by calculating the ratio of suffusate (ng/ml) to plasma (mg/ml) concentration of FITC-dextran and multiplying this ratio by the suffusate flow rate (2 ml/min).
Experimental Protocols
Effects of NK1 receptor antagonists on tannic acid-induced responses. The purpose of these studies was to determine whether suffusion of tannic acid on the cheek pouch increases macromolecular efflux and, if so, whether this response is mediated in part by substance P. After suffusing buffer for 30 min (equilibration period), FITC-dextran was injected intravenously and the number of leaky sites and clearance of FITC-dextran were determined for 30 min. Then, two concentrations of tannic acid (200 and 300 µg/ml) were suffused onto the cheek pouch in an arbitrary fashion. Each concentration was suffused for 20 min. At least 60 min elapsed between subsequent suffusions of tannic acid. The number of leaky sites was determined every min for 10 min and at 5-min intervals for 60 min thereafter. Clearance of FITC-dextran was determined before and every 5 min for 60 min. After suffusion of tannic acid was stopped and the number of leaky sites returned to baseline, CP-96,345 (5 mg/kg) or RP-67580 (1 mg/kg), two selective, but structurally distinct, nonpeptide NK1 receptor antagonists (10, 11), was infused intravenously for 30 min with the use of an infusion pump and suffusion of tannic acid was repeated. In another group of animals, the 2R,3R enantiomer CP-96,344 (5 mg/kg) rather than CP-96,345 was infused intravenously. The number of leaky sites and clearance of FITC-dextran were determined during each intervention.In preliminary studies, we determined that repeated suffusions of tannic acid (200 and 300 µg/ml) were associated with reproducible results. In addition, suffusion of saline (vehicle) for the entire duration of the experiment and intravenous infusion of CP-96,345 and CP-96,344 (each 5 mg/kg) alone for 30 min were not associated with leaky site formation or significant increases in clearance of FITC-dextran from baseline. The concentrations of tannic acid, CP-96,345, RP-67580, and CP-96,344 used in these studies were based on previous and preliminary studies in our laboratory and reports in the literature (4, 5, 10, 11, 25, 26, 29, 32).
Effects of NG-nitro-L-arginine methyl ester on tannic acid-induced responses. The purpose of these experiments was to determine whether NG-nitro-L-arginine methyl ester (L-NAME), an NO synthase inhibitor that attenuates substance P-induced increase in macromolecular efflux from the cheek pouch (6, 9), attenuates tannic acid-induced leaky site formation and increase in clearance of FITC-dextran from the cheek pouch. After suffusing buffer for 30 min (equilibration period), FITC-dextran was injected intravenously and the number of leaky sites and clearance of FITC-dextran were determined for 30 min. Then, tannic acid (200 µg/ml) was suffused for 20 min. After suffusion of tannic acid was stopped and the number of leaky sites returned to baseline, L-NAME or D-NAME (each 100 µM) was suffused for 30 min and suffusion of tannic acid was repeated. The number of leaky sites and clearance of FITC-dextran were determined during each intervention.
In another group of animals, we determined whether L-arginine, the substrate for NO synthase, or D-arginine reverses L-NAME attenuation of tannic acid-induced leaky site formation and increase in clearance of FITC-dextran. The experimental design was similar to that outlined above, except that L-arginine or D-arginine (each 1.0 mM) was now suffused with L-NAME (100 µM) for 30 min before suffusion of tannic acid (200 µg/ml) for 20 min. The number of leaky sites and clearance of FITC-dextran were determined during each intervention. In preliminary experiments, we determined that suffusion of L-NAME, D-NAME (each 100 µM), L-arginine, and D-arginine (each 1 mM) alone was not associated with leaky site formation and significant increases in clearance of FITC-dextran above baseline. The concentrations of L-NAME, D-NAME, L-arginine, and D-arginine used in these studies were based on a previous study in our laboratory (9).
Drugs. FITC-dextran, tannic acid, L-NAME, D-NAME, L-arginine, and D-arginine were obtained from Sigma Chemical (St. Louis, MO). CP-96,345 and CP-96,344 were gifts from Pfizer (New York, NY). RP-67580 was a gift from Rhône-Poulenc Rorer (Vitry sur Seine, France). All drugs were prepared on the day of the experiment and diluted in saline to the desired concentrations.
Data and statistical analyses. When a test compound was suffused onto the cheek pouch, we determined the maximal change in the number of leaky sites and clearance of FITC-dextran and used it as the response to that compound. Data are expressed as means ± SE. Because the number of leaky sites and clearance of FITC-dextran returned to baseline between successive suffusions of test compounds, all vehicle (saline) control data are expressed as a single value for each experimental condition. Statistical analysis was performed using two-way analysis of variance and the Newman-Keuls test for multiple comparisons; n is given as the number of experiments, with each experiment representing a separate animal. P < 0.05 was considered significant.
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RESULTS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Mean arterial pressure was 105 ± 5 mmHg at the start and 97 ± 4 mmHg at the conclusion of the experiments (n = 26; P > 0.5).
Effects of NK1 Receptor Antagonists on Tannic Acid-Induced Responses
Suffusion of tannic acid for 20 min elicited a significant, concentration-dependent leaky site formation and increase in clearance of FITC-dextran from the cheek pouch (Figs. 1 and 2; each group, n = 6; P < 0.05). These effects were maximal within 10 min after the start of suffusion and returned to baseline within 40 min after suffusion of tannic acid was stopped. CP-96,345 (5 mg/kg iv) significantly attenuated tannic acid-induced responses (Fig. 1; each group, n = 6; P < 0.05). The number of leaky sites decreased from 13 ± 3/0.11 cm2 during suffusion of tannic acid (300 µg/ml) alone to 2 ± 1/0.11 cm2 during suffusion of tannic acid (300 µg/ml) in the presence of CP-96,345 (95 mg/kg iv; Fig. 1, top). Likewise, clearance of FITC-dextran decreased from 31.1 ± 6.2 ml/min × 106 during suffusion of
tannic acid (300 µg/ml) alone to 9.1 ± 2.9 ml/min × 106 during suffusion of
tannic acid (300 µg/ml) in the presence of CP-96,345 (5 mg/kg iv;
Fig. 1, bottom). CP-96,344 (5 mg/kg
iv) had no significant effects on tannic acid-induced responses (Fig. 2; each group, n = 4;
P > 0.5). RP-67580 (1 mg/kg iv)
significantly attenuated tannic acid-induced leaky site formation and
increase in clearance of FITC-dextran (Fig.
3; each group,
n = 5;
P < 0.05). The number of leaky sites
decreased from 15 ± 2/0.11 cm2
during suffusion of tannic acid (300 µg/ml) alone to 1 ± 1/0.11 cm2 during suffusion of tannic
acid (300 µg/ml) in the presence of RP-67580 (1 mg/kg iv; Fig. 3,
top). Clearance of FITC-dextran decreased from 28.3 ± 5.6 ml/min × 106 during suffusion of
tannic acid (300 µg/ml) alone to 10.8 ± 3.9 ml/min × 106 during
suffusion of tannic acid (300 µg/ml) in the presence of RP-67580 (1 mg/kg iv; Fig. 3, bottom).
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Effects of NG-Nitro-L-Arginine Methyl Ester on Tannic Acid-Induced Responses
L-NAME, but not D-NAME (each 100 µM), significantly attenuated tannic acid (200 µg/ml)-induced leaky site formation and increase in clearance of FITC-dextran (Fig. 4; each group, n = 4; P < 0.05). The number of leaky sites decreased from 7 ± 1/0.11 cm2 during suffusion of tannic acid (200 µg/ml) alone to 2 ± 1/0.11 cm2 during suffusion of tannic acid (200 µg/ml) and L-NAME (100 µM; Fig. 4, top). Likewise, clearance of FITC-dextran decreased from 30.3 ± 5.1 ml/min × 106 during suffusion of
tannic acid (200 µg/ml) alone to 10.1 ± 3.0 ml/min × 106 during suffusion of
tannic acid (200 µg/ml) and
L-NAME (100 µM; Fig. 4,
bottom).
L-Arginine, but not
D-arginine (each 1 mM), reversed the attenuating effects of
L-NAME (100 µM) on tannic acid
(200 µg/ml)-induced leaky site formation and increase in clearance of
FITC-dextran (Fig. 4; each group, n = 4). The number of leaky sites increased significantly from 2 ± 1/0.11 cm2 during suffusion of
tannic acid (200 µg/ml) and
L-NAME (100 µM) to 7 ± 1/0.11 cm2 during suffusion of
tannic acid (200 µg/ml) and
L-NAME and
L-arginine (1 mM; Fig. 4,
top;
P < 0.05). Clearance of FITC-dextran
increased significantly from 10.1 ± 3.0 ml/min × 106 during suffusion of
tannic acid (200 µg/ml) and
L-NAME (100 µM) to 24.3 ± 3.9 ml/min × 106 during suffusion of
tannic acid (200 µg/ml),
L-NAME (100 µM), and
L-arginine (1 mM; Fig. 4,
bottom).
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DISCUSSION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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The are three new findings of this study. Suffusion of tannic acid, a major component of cotton bracts (4, 5, 14, 15, 25, 26, 29, 32), increases macromolecular efflux from the in situ hamster cheek pouch in a concentration-dependent fashion. The magnitude of this response is similar to that elicited by histamine (1.0 µM), a potent phlogistic mediator, in the cheek pouch (20). Moreover, tannic acid-induced leaky site formation and increase in clearance of FITC-dextran are not related to nonspecific damage to microvascular endothelium, because both parameters return to baseline values once suffusion of tannic acid is stopped (14).
Importantly, tannic acid-induced responses are mediated by local release of substance P from sensory nerves because CP-96,345 and RP-67580, two selective, but structurally distinct NK1 receptor antagonists (10, 11), but not CP-96,344, the 2R,3R enantiomer of CP-96,345, significantly attenuate these responses. On its release, substance P activates the L-arginine-NO biosynthetic pathway in the cheek pouch microcirculation, because L-NAME, an NO synthase inhibitor, but not D-NAME, significantly attenuates tannic acid-induced increase in macromolecular efflux and because L-arginine, the substrate for NO synthase, but not D-arginine, reverses the attenuating effects of L-NAME. Taken together, these data suggest that tannic acid elicits reversible L-arginine-NO biosynthetic pathway-dependent neurogenic plasma exudation from the in situ hamster cheek pouch. This process may contribute to acute, intermittent airway dysfunction observed in patients with byssinosis.
The hamster is an established model to elucidate mechanisms underlying plasma exudation elicited by environmental toxicants in situ (9-11, 15, 19, 23, 24, 30, 31). For instance, Kilburn et al. (15) showed that exposure of normal hamsters to an aqueous extract of cotton mill dust is associated with leukocyte recruitment into the airway mucosa. Whether this exposure is also associated with plasma exudation was not determined in this study. To this end, Gao et al. (11) showed recently that an aqueous extract of grain sorghum dust, which contains tannins (2, 15), elicits neurogenic plasma exudation from the in situ hamster cheek pouch through stimulation of NK1 receptors. Gao et al. (9) also showed that substance P-induced increase in macromolecular efflux from the cheek pouch is mediated, in part, by the L-arginine-NO biosynthetic pathway. The results of the present study support and extend these observations by showing that tannic acid, a major component of cotton bracts, elicits neurogenic plasma exudation from the in situ hamster cheek pouch, which is transduced, in part, by the L-arginine-NO biosynthetic pathway. Overall, these data indicate that the hamster cheek pouch is a suitable model to investigate the mechanisms underlying the injurious effects of tannins in vivo.
Changes in vasomotor tone and/or venular driving pressure in the cheek pouch may have mediated, in part, the effects of tannic acid, NK1 receptor antagonists, and L-NAME on macromolecular efflux from this organ. However, this possibility seems unlikely, because we have previously shown that CP-96,345 and RP-67580 have no significant effects on adenosine-induced increase in macromolecular efflux from the cheek pouch (9, 11). Moreover, L-NAME has no significant effects on leaky site formation and increase in clearance of FITC-dextran from the cheek pouch elicited by the calcium ionophore A-23187, which activates the L-arginine-NO biosynthetic pathway in a nonreceptor-mediated endothelium-dependent fashion (9). Studies in other vascular beds and species have also dissociated changes in vasomotor tone from macromolecular transport (21, 23, 31, 33). On balance, these data suggest that the effects of tannic acid, NK1 receptor antagonists, and L-NAME on macromolecular efflux from the in situ cheek pouch could not be attributed to local changes in vasomotor tone and/or venular driving pressure.
Current concepts suggest that, in certain species under physiological conditions, NO or NO-related compound(s) tonically suppresses plasma exudation from postcapillary venules (1, 6, 16). However, Gao et al. (9) and Mayhan (19, 20) showed that NO synthase inhibitors have no significant effects on baseline macromolecular efflux from the in situ hamster cheek pouch. Importantly, activation of the L-arginine-NO biosynthetic pathway in the upper and lower airway mucosa by various phlogistic mediators, including substance P, has been shown to disrupt the barrier function of postcapillary venules, leading to plasma exudation, interstitial edema, and tissue dysfunction (1, 9, 13, 17, 19).
The results of this study support these observations by showing that tannic acid-induced increase in macromolecular efflux from the in situ cheek pouch is transduced, in part, by the L-arginine-NO biosynthetic pathway and that this process is reversible. By contrast, Chiesi and Schwaller (3) showed that tannin inhibits constitutive endothelial NO synthase activity in cultured bovine aortic endothelial cells. In addition, Johnson et al. (14) showed that exposure of cultured endothelial cells to tannin is associated with morphological and cytotoxic changes. Although the reasons underlying these discrepant results are uncertain, they may be related, in part, to differences in methods, species, and tannin preparations used in these studies. Further studies are indicated to elucidate the mechanisms whereby tannic acid modulates NO synthase expression and activity in the microcirculation.
The effects of tannins on barrier function of postcapillary venules in the lower airway mucosa in vivo are uncertain (14, 15, 25). Russell and Rohrbach (26) showed that cotton bract tannin relaxes isolated rabbit pulmonary artery by producing NO or an NO-related compound(s). Other investigators showed that tannins stimulate resident and migrant cells in the airway mucosa to produce and release potent phlogistic mediators, such as arachidonic acid, 5-hydroxytryptamine, and hydrogen peroxide (4, 25, 29, 32). Conceivably, these mediators could stimulate sensory nerves in airway mucosa to elicit L-arginine-NO biosynthetic pathway-dependent neurogenic plasma exudation, leading to interstitial edema and airway narrowing. This process may be manifested clinically as acute, intermittent coughing, wheezing, chest tightness, and shortness of breath in patients with byssinosis (2, 34). Clearly, additional studies are warranted to support or refute this hypothesis.
Perspectives
This study unravels a novel mechanism whereby tannic acid, a plant toxicant implicated in the pathogenesis of byssinosis (34), adversely affects upper airway mucosa function, namely stimulation of sensory nerves to elicit neurogenic plasma exudation. I propose that this process may contribute to acute, intermittent symptoms of airway dysfunction observed in patients with byssinosis.In summary, I found that tannic acid elicits reversible L-arginine-NO biosynthetic pathway-dependent neurogenic plasma exudation from the in situ hamster cheek pouch.
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ACKNOWLEDGEMENTS |
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I thank Drs. R. M. Snider and C. Garret for providing CP-96,345 and CP-96,344, and RP-67580 and Dr. I. Rubinstein for reviewing the manuscript.
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FOOTNOTES |
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This study was supported in part by a grant from the American Heart Association of Metropolitan Chicago.
Address for reprint requests: X.-p. Gao, Dept. of Medicine (M/C 787), Univ. of Illinois at Chicago, 840 South Wood St., Chicago, IL 60612-7323.
Received 1 July 1997; accepted in final form 9 October 1997.
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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P < 0.05 compared with tannic acid alone.
