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Poult Sci 2007. 86:843-849
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IMMUNOLOGY, HEALTH, AND DISEASE

Effect of Mast Cell Degranulation on Chicken Ileal Ion Transport In Vitro

C. B. Collins, J. McGrath, A. W. Baird and D. P. Campion1

UCD School of Agriculture, Food Science and Veterinary Medicine and Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Belfield, Dublin 4, Ireland

1 Corresponding author: Deirdre.Campion{at}ucd.ie


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Histamine is a primary mediator of the inflammatory response in mammals. Degranulation of intestinal mast cells results in the release of mast cell mediators such as histamine. Histamine stimulates epithelial ion transport in a range of mammalian tissues via specific histamine receptors. The aim of this study was to assess a potential role of tissue mast cells and of exogenous histamine in the regulation of ion transport in avian mucosa. Broiler chicken ileal histamine release and secretory responses to mast cell degranulation were determined in vitro with the use of ELISA and Ussing chamber techniques. Pharmacological degranulation of mucosal mast cells using compound 48/80 (15 µg/mL) resulted in histamine release and an immediate-onset transient increase in transmural short-circuit current. The response to compound 48/80 was subject to tachyphylaxis and was significantly reduced in the presence of the histamine H1 antagonist mepyramine, but was unaffected by the cyclooxygenase inhibitor piroxicam. Prior incubation with the mast cell stabilizer ketotifen prevented compound 48/80-induced increase in transmural short-circuit current. In conclusion, degranulation of avian intestinal mast cells would appear to result in histamine release that stimulates epithelial ion transport via histamine H1 receptor activation. Although prostaglandin E2 is a potent secretagogue in the avian small intestine epithelium, prostanoid production appears to have little role to play in mast cell-mediated epithelial ion transport.

Key Words: broiler • mast cell • epithelium • histamine


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The intestinal mucosa acts as a defensive barrier, which selectively permits absorption of nutrients while preventing access by pathogens. This defensive barrier is organized according to the anatomical layers of the mucosa (Wallace and Granger, 1996), with different components acting in concert to resist, prevent, and, if necessary, repair injury. These components include 1) the extramucosal components such as acid, mucus, surface-active phospholipids, and bicarbonate; 2) the epithelium itself; 3) the microcirculation and sensory afferent neurons beneath the epithelium; 4) the mucosal immune system; and 5) the ability of the mucosa to undergo repair. The focus of this study is the fourth level of defense, the mucosal immune system. This consists of immunocytes such as mast cells and macrophages, normally resident within the mucosa, which act as sentinel cells (Wallace and Ma, 2001). These immunocytes can detect the entry of foreign materials such as antigens or bacteria and can respond with the release of chemical mediators, which bring about a series of physiological reactions to aid elimination of the potentially damaging substance or organism.

In response to activation, mammalian mast cells produce an array of biologically active mediators, including preformed mediators such as histamine and serotonin, proteases, and proteoglycans, as well as de novo synthesis of cytokines, growth factors, and free radicals (Galli et al., 2005). These mediators can act directly on intestinal epithelial cells, or indirectly via cross talk involving other cell types (Wang et al., 1995). Activation of mast cells in mammals is vital for a rapid response to reinfection in acquired immunity, although this process also plays a negative role in allergic disease. Although most reported studies have been performed in mammalian mast cells, many of the known mediators, and particularly histamine and serotonin, have been identified in avian mast cells (Rose et al., 1980).

Mast cell mediators have been shown to stimulate epithelial ion secretion in human intestinal epithelial cells (Barrett, 1991). Stimulation of intestinal ion transport acts as the driving force for the paracellular movement of sodium and water into the intestinal lumen, causing diarrhea, a process that may facilitate the clearance of bacteria from the gut. Furthermore, the role of mast cells in the mucosal defense mechanism against invading pathogens has been demonstrated using genetically mast cell-deficient mice. These animals showed increased mortality from bacterial infection following cecal puncture (Echtenacher et al., 1996), and in separate studies, these mice were unable to clear bacteria as efficiently as wild-type mice (Malaviya et al., 1996).

Although intestinal mast cells have proven vital in the mammalian intestine, their role in avian intestinal immunity remains unclear. However, an increase in mast cell numbers and an anaphylactic-like intestinal secretory response has been shown in Eimeria acervulina-infected broiler chickens (Morris et al., 2004), and this anaphylactic response has been attributed to epithelial chloride ion secretion (Caldwell et al., 2004).

Of the biogenic amines, histamine [2-(4-imidazolyl)-ethyl-amine] is a principal product of mast cell degranulation. In studies that have measured the quantal co-release of biogenic amines in rat peritoneal mast cells, mast cells have been shown to contain a far greater quantity (30-to 40-fold) of stored histamine than serotonin (Pihel et al., 1998).

The role of histamine as an inflammatory mediator has made it a specific target for medical therapeutics since it was first described by Dale and Laidlaw (1910) in the early part of the 20th century. Histamine is now known to act via 4 pharmacologically distinct receptors, H1 to H4, all of which are members of the G protein-coupled receptor superfamily (Akdis and Simons, 2006). Histamine-induced chloride ion secretion in human gut epithelial cell lines is mediated via the H1 receptor (Wasserman et al., 1988).

In this study, we chose to examine the physiological effects of mast cell histamine in the chicken gastrointestinal epithelium. To examine the effect of histamine, and to quantify histamine release, we stimulated degranulation of chicken intestinal mast cells pharmacologically using compound 48/80. This agent interacts with G proteins on the mast cell membrane, resulting in granule exocytosis (Mousli et al., 1990), and has previously been shown to stimulate histamine release and smooth muscle contraction in the chicken esophagus (Taneike et al., 1988). For comparison, we evaluated the effect of the mast cell-stabilizing agent ketotifen (Serna et al., 2006). Electrogenic ion transport responses to exogenous histamine, and the nonspecific cholinergic agonist carbachol (CCh) were used as controls. The release of histamine from rat and human intestinal mast cells is subject to stimulation by the neuropeptide substance P (Raithel et al., 1999; Lau et al., 2001). Substance P is a potent secretagogue in the chicken intestine (Chang et al., 1986); therefore, we investigated the possibility that the effect of substance P in the chicken may be due to stimulation of histamine release from mast cells. Finally, we investigated the role of the prostaglandins in histamine-mediated epithelial ion transport.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Experimental Birds

Male Cobb 500 broiler chickens were obtained from a local commercial hatchery on the day of hatch. All chicks were placed in straw-bedded pens and were maintained at age-appropriate temperatures and given ad libitum access to water and a commercial broiler ration. Chicks were reared in batches of 15 to 20, and were used for experimental work from d 21 until d 42. Care of the experimental birds followed institutional and international laboratory animal standards. On the experimental days, single birds were killed humanely using CO2 asphyxiation. Individual experiments were designed to provide paired (matched) tissues from each bird, which were then randomly assigned to control or to treatment groups. Thus, each experiment had an internal control. Each pharmacological treatment was used across a range of ages.

Histamine Release from Avian Intestinal Mast Cells

Ilea were excised, opened along the mesenteric border, and rinsed of luminal contents with Krebs-Henseleit bicarbonate buffer solution containing (in mmol/L) NaCl, 118; D-glucose, 11.1; NaHCO3, 24.9; MgSO4, 1.2; KCl, 4.7; KH2PO4, 1.2; and CaCl2, 2.5. From each ileum, 4 tissue samples, approximately 0.6 cm2 in size, were excised and added to 2 wells of a 6-well plate (Corning Costar cell culture plate, Corning Inc., Acton, MA), with each well containing 2 mL of Krebs-Henseleit bicarbonate buffer solution. Compound 48/80 (15 µg/mL) was added to the test well, whereas the other well served as a control. The 6-well plate was placed in a water bath maintained at 37 °C, and the well contents were gassed with 95% O2/5% CO2. The tissues were incubated for 3 min, after which the tissues were removed, placed in 0.5 mol/L of sodium hydroxide, and stored at –18°C for later analysis of protein content. The supernatant was assayed for histamine using a direct ELISA (Immuno-Biological Laboratories, Hamburg, Germany). Sample protein content was quantified using a commercially available Bradford assay (Bio-Rad protein assay, Bio-Rad Laboratories (UK) Ltd., Hemel Hempstead, Hertsfordshire, UK) following homogenization of the samples in lysis buffer (1% SDS, 1.0 mmol/L of sodium orthovanadate, 10 mmol/L of Tris at pH 7.4) and centrifugation to remove any insoluble material. Histamine content in the supernatant was expressed per milligrams of protein.

Measurement of Ion Transport in Avian Intestinal Tissue

To measure intestinal ion transport responses, ilea were excised, opened along the mesenteric border, and rinsed of luminal content with Krebs-Henseleit bicarbonate buffer solution as described previously. Tissues were stripped of overlying muscle layers by crude dissection, mounted in modified Ussing chambers (0.63 cm2 aperture), bathed in physiological buffer at 37°C, gassed with 95% O2/5% CO2 on both the apical (luminal side) and basolateral (serosal side) aspects, and voltage-clamped at 0 mV. Measurement of epithelial ion transport was carried out using a DVC 1000 voltage clamp (World Precision Instruments, Stevenage, UK). To measure this, 1 voltage-sensing and 1 current-passing silver-silver chloride agar-salt bridge electrode (3% agar in 3 mol/L of KCl) was inserted into each half-chamber, and the electrodes were connected to the DVC 1000 via a preamplifier (DC-3, World Precision Instruments). The transepithelial electrical potential difference generated by the epithelium was continuously short-circuited by passing current across the tissue with the current-passing electrodes and was adjusted by a feedback amplifier to keep the clamp voltage at 0 mV. The amount of current required was continuously recorded using a MacLab data acquisition system (AD Instruments, Hastings, UK). The change in short-circuit current ({Delta}Isc) measured under these voltage-clamp conditions was used as an indicator of active ion transport across the tissue and is expressed as microamps per square centimeter. The voltage was clamped intermittently at 1 mV and the corresponding deflection in Isc was used to calculate transepithelial electrical resistance by applying Ohm’s law (R = V/I). Transepithelial electrical resistance measurements give an indication of the ionic permeability of tight junctions and can also reflect changes in membrane conductance.

Following a 15-min equilibration period, the basal parameters were recorded, and where possible, these parameters were used to pair matched sections of ileum. Following this, antagonists were added basolaterally and allowed 15 min of contact time prior to challenge with cumulatively applied concentration response curves of agonists. Drugs were added to the basolateral bathing solution unless otherwise stated. Following each experiment, a single dose of the muscarinic agonist CCh (10 µmol/L) was added to ensure that the tissue remained viable throughout. The volume of drugs added never exceeded 1% of total reservoir volume. The tissues derived from each bird were used for at least 4 different simultaneous pharmacological experiments.

Mast Cell-Mediated Ion Transport

To examine the effect of mast cell degranulation by compound 48/80 on ion transport in the chicken ileum, 2 successive challenges of compound 48/80 (15 µg/mL) were added to the bathing solution, with 15 min between additions. This procedure was carried out either basolaterally or apically. All subsequent additions of compound 48/80 were made to the basolateral bathing solution. The effects of pretreatment with the histamine H1 receptor antagonist mepyramine (1 µmol/L), the nonselective cyclooxygenase (COX) inhibitor piroxicam (10 µmol/L), and the mast cell stabilizer ketotifen (1 µmol/L) on compound 48/80-mediated ion transport were examined to determine the mechanism underlying the changes in ion transport.

Tissue responses to single challenges (10 µmol/L) or cumulatively applied concentration ranges (1 nmol/L to 100 µmol/L) for exogenous histamine were also measured. Concentration response curves for exogenous histamine added to either the apical or basolateral bathing compartment were constructed and compared with responses of the cholinomimetic secretagogue, CCh. The selectivity of the H1 receptor antagonist mepyramine (1 µmol/L) was demonstrated by constructing concentration response curves for exogenous histamine and CCh in its presence. To examine possible mechanisms of histamine-mediated ion transport, cumulative concentration response curves to exogenous histamine were carried out in the presence or absence of piroxicam (10 µmol/L) or ketotifen (1 µmol/L). To examine the effect of the COX product prostaglandin E2 (PGE2) on chicken ileum epithelial ion transport, cumulative concentration response curves (10 pmol/L to 100 nmol/L) were carried out in the presence and absence of piroxicam (10 µmol/L). Finally, to investigate the effect of substance P on mast cell-mediated ion transport in the chicken ileum, cumulative concentration response curves to exogenous substance P (1 nmol/L to 10 µmol/L) were carried out with and without mepyramine (100 nmol/L) pretreatment.

Chemicals

Atropine, CCh, compound 48/80, histamine, PGE2, piroxicam, sodium orthovanadate, SDS, and Tris were acquired from Sigma-Aldrich Ireland Ltd. (Dublin, Ireland). Ketotifen and mepyramine were obtained from Tocris Cookson Ltd. (Bristol, UK). Substance P was purchased from Merck Biosciences Ltd. (Nottingham, UK). Stock solutions of atropine (100 mmol/L), CCh (100 mmol/L), compound 48/80 (30 mg/mL), PGE2 (1 mmol/L), histamine (100 mmol/L), and mepyramine (10 mmol/L) were made up in deionized water. Ten-millimolar stock solutions of ketotifen and piroxicam were made up in di-methyl sulfoxide. A 10-mmol/L stock solution of substance P was made up in 5% acetic acid. Stock solutions were stored at –18°C, except piroxicam, which was stored at 4°C.

Statistical Analysis

Data are presented as mean ± standard error of the mean. The population sample size (n value) refers to the number of animals used and not the number of tissue samples. Values for pD2 [–log EC50 (effective concentration 50%)] and maximal effect produced by a drug (Emax) were calculated with the statistical program GraphPad Prism (San Diego, CA). Statistically significant differences between mean values were calculated using the Student’s paired and unpaired t-test or by ANOVA. A difference was considered statistically significant if P < 0.05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Histamine Released by Compound 48/80-Induced Mast Cell Degranulation

Isolated chicken ileum tissue (n = 6) treated with compound 48/80 (15 µg/mL) released large quantities of histamine (707.0 ± 64.9 ng/mg of protein), which were significantly greater (P < 0.0005) than those of the paired control group (24.1 ± 9.5 ng/mg of protein; Table 1Go).


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  		Table 1. Histamine release from chicken ileum biopsies incubated at 37 °C with or without compound 48/801
 
Effect of Compound 48/80-Induced Mast Cell Degranulation on Ion Transport

The electrophysiological basal parameters of isolated chicken ileum demonstrated high transepithelial electrical resistance, low short-circuit current, and median potential difference values (Table 2Go). Basolateral addition of compound 48/80 (15 µg/mL) evoked a rapid, transient {Delta}Isc that was maximally expressed within 3 min (3.0 ± 0.4 µA/cm2, n = 11; Figure 1Go). This response was subject to tachyphylaxis because addition of a further 15 µg/ mL of compound 48/80 after 15 min caused no further significant change (P < 0.0005; Figure 1AGo). Apical addition of compound 48/80 (15 µg/mL) caused almost no {Delta}Isc (0.3 ± 0.4 µA/cm2) and was significantly less than basolateral addition (P < 0.05, Figure 1BGo). The mast cell stabilizer ketotifen (1 µmol/L) inhibited the effect of compound 48/80 (15 µg/mL; P < 0.0005; Table 3Go). The response of compound 48/80 was significantly reduced (P < 0.005) by prior addition of mepyramine (1 µmol/L; 1.6 ± 0.5 µA/cm2; Table 3Go) and was unaffected by pretreatment with the COX inhibitor piroxicam (10 µmol/L; Table 3Go).


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  		Table 2. Basal parameters of chicken ileum epithelium1
 

Figure 1
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  		Figure 1. The effect of compound 48/80 on ion transport responses in chicken ileal epithelium. In (A), the effect of basolateral (luminal) vs. apical (serosal) addition of compound 48/80 (15 µg/mL) in chicken ileal epithelium is shown. Each bar represents the mean change in short-circuit current ({Delta}Isc) ± SEM of n = 11 experiments; {Delta}Isc represents the difference between basal values and values obtained following addition of compound 48/80. The n values represent the number of birds from which tissues samples were derived. In (B), the {Delta}Isc evoked by initial challenge (15 µg/mL) followed by a second challenge (15 µg/mL) with basolaterally applied compound 48/80 is shown. Each bar represents the mean ± SEM of 13 paired experiments. Significant differences between means (P < 0.001) were calculated using a Student’s paired t-test and are indicated by asterisks (***).

 

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  		Table 3. Compound 48/80-mediated epithelial ion transport: Effect of prior treatment with mast cell stabilizer ketotifen, H1 antagonist mepyramine, and COX inhibitor piroxicam1
 
Effect of Exogenous Histamine and CCh on Ion Transport

Both histamine and CCh produced a concentration-dependent {Delta}Isc in isolated chicken ileum (Figure 2Go). The pD2 value for histamine was 6.2 µA/cm2 (± 0.5) and CCh was 6.0 µA/cm2 (± 0.2) with Emax values of 11.8 µA/cm2 (± 1.7) and 19.6 µA/cm2 (± 1.6), respectively. Mepyramine (1 µmol/L) virtually abolished Isc responses to histamine but had no effect on CCh-induced ion transport. Responses to histamine were of similar magnitude when challenge was made to the basolateral bathing solution, compared with addition to the apical bathing solution.


Figure 2
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  		Figure 2. The effect of exogenous histamine and carbachol on ion transport in chicken ileal epithelium. Change in short-circuit current ({Delta}Isc) was evoked in isolated chicken ileum epithelium by cumulative application of exogenous histamine (•) and carbachol ({circ}). Each data point represents the mean ± SEM of n = 7 separate experiments. The concentration-response curves were fitted using the statistical and graphing program GraphPad Prism (San Diego, CA).

 
Dependence of Histamine-Mediated Ion Transport on Postanoid Production

Histamine-mediated ion transport was markedly decreased by pretreatment with piroxicam (10 µmol/L; n = 6), with Emax values of 5.0 µA/cm2 (± 1.2) for control tissues and 1.2 µA/cm2 (± 0.6) for those treated with piroxicam. Ketotifen (1 µmol/L; n = 6) had no effect on cumulatively applied concentration response curves to exogenous histamine. Results, provided as the percentage reduction in {Delta}Isc, are shown in Table 3Go.

Effect of Mast Cell-Associated Secretagogues on Ion Transport

Prostaglandin E2 caused {Delta}Isc, with a pD2 value of 7.2 µA/cm2 (± 0.7) and an Emax of 23.6 µA/cm2 (± 7.2), which was unaffected by pretreatment with piroxicam (10 µmol/L; n = 6). Substance P caused a concentration-dependent {Delta}Isc, exhibiting a high level of potency, with a pD2 value of 8.2 µA/cm2 (± 0.8) and an Emax of 11.7 µA/cm2 (± 1.7). Mepyramine (100 nmol/L; n = 6) did not significantly alter the response of the chicken ileum to substance P (Figure 3Go).


Figure 3
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  		Figure 3. The effect of H1 receptor antagonism on ion transport responses induced by exogenous substance P in chicken ileal epithelium. Change in short-circuit current ({Delta}Isc) was evoked in isolated chicken ileum epithelium by cumulative application of exogenous substance P, both with (•) and without ({circ}) pretreatment with H1 receptor antagonist mepyramine (100 nmol/L). Each data point represents the mean ± SEM of n = 6 separate paired experiments. The concentration-response curves were fitted using the statistical and graphing program GraphPad Prism (San Diego, CA).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Mast cells have a major role in stimulating ion secretion, resulting in secretory diarrhea, as has been demonstrated in many species such as the rat (Baird et al., 1985), guinea pig (Russell, 1986), and human (Yu and Perdue, 2001). In the chicken intestine, mast cell mediators have previously been shown to increase secretion in secondary protozoan infections (Caldwell et al., 2004). In this study, compound 48/80 stimulated histamine release from chicken intestinal tissues and also stimulated epithelial ion transport. The ion transport response to compound 48/80 was inhibited by the mast cell stabilizer ketotifen (1 µmol/L), further confirming that mast cell degranulation is responsible for the ion transport induced by compound 48/80. The population of mast cells stimulated in this study was most likely located on the basolateral side of the intestinal epithelium, because compound 48/80 had a minimal effect on apical addition. Furthermore, the ion transport response was antagonized by H1 receptor antagonist mepyramine, implicating mast cell histamine release in this secretory response. Although mepyramine is reported to act as a muscarinic antagonist at high concentrations (Orzechowski et al., 2005), in this study, the ion transport responses induced by CCh were mepyramine insensitive.

Previous studies on compound 48/80-mediated histamine release in the chicken esophagus showed a dependence of histamine on COX products in the generation of a response (Kalra et al., 1993). In this study, compound 48/80-mediated ion transport was insensitive to the inhibition of COX by piroxicam.

The effect of exogenous histamine on chicken ileum smooth muscle contraction has been described previously (Chand and de Roth, 1978; Kitazawa et al., 1995). Single challenges of exogenous histamine have previously been shown to increase ion transport in the chicken ileum (Caldwell et al., 2001). Cumulatively applied exogenous histamine generated a concentration-dependent {Delta}Isc that was unaffected by ketotifen pre-treatment. When exogenous histamine, corresponding to the concentration of histamine released by compound 48/80, was added to the epithelial preparations, it generated an increase in ion transport of similar magnitude, as seen in response to compound 48/80. This further supports the role of histamine in compound 48/80-mediated ion transport. Unlike compound 48/80, exogenous histamine-mediated ion transport was sensitive to COX inhibition. One COX product that may contribute to histamine-mediated ion transport is PGE2. Exogenous PGE2 is a potent cyclic adenosine monophosphate-dependent secretagogue in the chicken ileum generating a concentration-dependent increase in epithelial ion transport that is insensitive to piroxicam. Similar effects of another cyclic adenosine monophosphate-dependent secretagogue, theophylline, on hen colon epithelial ion transport were described previously (Clauss et al., 1988). The release of histamine from rat and human intestinal mast cells is subject to stimulation by the neuropeptide substance P (Raithel et al., 1999; Lau et al., 2001). Substance P is a potent secretagogue in the chicken intestine (Chang et al., 1986), and as such, this study was extended to determine whether the effect of substance P was due to stimulation of histamine releases from mast cells. Substance P stimulated a concentration-dependent {Delta}Isc, which was mepyramine-insensitive, suggesting that it was not histamine dependent.

In summary, this study demonstrates that pharmacological stimulation of avian enteric mast cells results in a measurable increase in endogenous histamine release and a concomitant increase in intestinal ion transport. This effect was predominately H1 receptor mediated and independent of prostanoid production or interaction with the neuropeptide substance P. The occurrence of a mast cell-driven secretory event in the intestine has implications for the study of enteral pathogenic invasion of the avian system. Rose et al. (1980) demonstrated that chicken mast cells have the same biogenic amines in preformed granules with the same capacity for degranulation as mammalian mast cells. Multiple mast cell mediators may contribute to the nature and extent of the anaphylactic response (Caldwell et al., 2001).

Pharmacological stimulation of avian mast cells in this way may prove a useful model system for studying both innate and adaptive immune responses to pathogenic challenge, an area of considerable applied significance.

Received for publication September 26, 2006. Accepted for publication January 13, 2007.


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 ABSTRACT
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 RESULTS
 DISCUSSION
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