1Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, and 2Facultad de Química y Biología, Universidad de Santiago de Chile, Santiago, Chile
Submitted 7 August 2003 ; accepted in final form 1 June 2004
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ABSTRACT |
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transduction mechanisms; P2Y receptor; calcium influx
In mammals, at least three IP3 receptor types (types 1, 2, and 3) are encoded by three distinct genes (2, 38), and the expression of the IP3 receptors has been reported in ciliated cells from both rat olfactory cilia (8) and murine oviduct (29). IP3 receptors participate in Ca2+ signaling by mediating intracellular Ca2+ release (16) and regenerative Ca2+ signals (9). Interestingly, the type 3 receptor mediates regulation of Ca2+ flux across the plasma (34, 35, 44) and nuclear (40) membranes.
IP3 receptors can be regulated in a number of ways. They contain binding sites for Ca2+, and elevation in free [Ca2+] from nanomolar to micromolar concentrations modifies receptor properties (36). Differential Ca2+ sensitivity of Ca2+ activation sites between IP3 receptor types 1 and 3 (5, 25) and a hypothetical differential subcellular localization and expression of IP3 receptor types in the same ciliated cell could evoke complex Ca2+ responses to extracellular agonist stimulation. In addition, several cytosolic factors, including Ca2+/calmodulin (CaM) (1), and phosphorylation by protein kinase A (PKA) (51), PKC (10), and CaM-dependent protein kinase II (CaMKII) (53) can modulate the activity of IP3 receptors. However, whether these factors are associated with the ATP transduction pathways in oviductal ciliated cells is an unresolved issue.
Although the activating effect of ATP on CBF has been demonstrated in ciliated cells, the presence and mechanisms of activation of IP3 receptor associated with the ATP-dependent control of CBF are still not completely understood. In the present study, we show that the participation of the extracellular and intracellular Ca2+ reservoirs in the ATP response is dependent on IP3 receptor activation and that PKC and CaMKII are involved in Ca2+ mobilization. Furthermore, we have analyzed the quantitative and temporal relationships between ATP-induced CBF increase and changes in [IP3] and [Ca2+]i. In addition, we have demonstrated the differential subcellular localization of IP3 receptor types 1 and 3 in the same oviductal ciliated cell, showing that only the type 3 receptor is present in plasma membrane. Finally, we discuss the relationship between timing and subcellular localization of IP3 receptor activity in ciliated cells and suggest that both receptor types can play specific roles in the induction of the ATP-dependent [Ca2+]i increase.
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METHODS |
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Culturing of ciliated cells from hamster oviductal epithelium. Experiments were performed in primary cultures of hamster oviductal epithelium obtained using the procedure previously described by Verdugo et al. (45). Adult (23 mo old) hamsters were anesthetized with 30% halothane and then decapitated. The oviducts were removed and placed in Hanks' solution (Sigma-Aldrich) at pH 7.4. The distal portion of the oviduct (i.e., the fimbria) was cut into small (48 mm2) pieces and placed in N-hydroxysuccinimide culture medium (in mM: 137 NaCl, 5.09 KCl, 1.14 Na2HPO4, 0.18 KH2PO4, 0.923 MgCl2, 0.91 CaCl2, 4.07 NaHCO3, 21.5 glucose, and 0.2 glutamine, supplemented with 1.0% vitamins, 1.0% essential amino acids, 1.0% nonessential amino acids, 1.0% pyruvate and antibiotics, 0.2 mg/ml neomycin, and 0.12 mg/ml penicillin, pH 7.27.4) for 3040 min at 37°C. The tissue was then transferred to sterile Hanks' solution, and the ciliated epithelium (which has >95% ciliated cells) was mechanically removed from the rest of the tissue.
Explants of ciliated epithelium were grown on glass coverslips previously coated with a solution of 0.5% gelatin. A strip of dialysis membrane was used to cover the explants and secure them on the glass coverslip before assembly into Rose chambers filled with culture medium supplemented with 10% horse serum, 1 mg/ml neomycin, and 1.21 mg/ml penicillin. Explant-containing Rose chambers were incubated at 37°C for up to 7 days until the culture formed a monolayer of ciliated cells. When this cell monolayer showed spontaneous ciliary activity, the chambers were opened and the cultures were washed three times with fresh Hanks' solution before CBF measurements were performed. All procedures were approved by the Pontifical Catholic University of Chile Animal Care and Ethics Committee.
Measurement of CBF. CBF was monitored and recorded by performing microphotodensitometry according to a procedure described previously (47). Briefly, the spectral structure of light-scattering fluctuations produced by the moving cilia of a single cell was detected with a photodiode, and the signal was processed online using a digital spectrum computer card (model R360; Rapid System, Jersey City, NJ) installed on a personal computer. The CBF was derived from the power spectrum obtained by performing fast Fourier transform of the data. The instant averaged spectrum was recorded for further analysis. CBF in individual ciliated cells was recorded.
Measurement of [Ca2+]i. [Ca2+]i was determined using a spectrofluorometric technique described previously (13). Primary cell cultures exhibiting spontaneous ciliary activity at 37°C were loaded with fura 2-AM for 30 min. Cells were excited at 349 and 380 nm in a Nikon Diaphot microscope equipped with a Photon Technology International spectrofluorometer (Lawrenceville, NJ) for ratio analysis. After 10 min of stabilization, the intensity ratio was continuously recorded and cultures were superfused with solutions containing the drugs to be tested. Fluorescence emission intensity was detected with a photomutiplier and acquired and analyzed using a fluorescence analysis program (FELIX version 1.1). To study the possible toxicity of the continuous excitation of fura 2 to ciliated cells, we determined basal CBF in individual ciliated cells (n = 15) incubated with the fluorescent indicator and either unexcited or excited at 349 and 380 nm. We did not observe a difference in the basal CBF between the two conditions. In addition, the time course of the ATP effect on CBF was similar in both protocols (n = 8).
Extraction and quantification of IP3. Oviductal ciliated cells obtained by mechanical extraction of the epithelium of fimbria were placed in Hanks' medium at 37°C in an atmosphere of 5% CO2 and incubated with ATP. The reaction was stopped with 1 M cold trichloroacetic acid (TCA). The tissue was homogenized using the XL Microson ultrasonic cell disruptor (Heat Systems Ultrasonics, Farmingdale, NY). Briefly, each homogenate was centrifuged for 10 min at 2,000 g. The supernatant was collected and the TCA was extracted using 2 volumes of a 3:1 solution of 1,1,2-trichloro-1,2,2-trifluoroethane-trioctylamine. The resulting aqueous phase, which contains IP3, was removed using a transfer pipette. Samples were maintained at 70°C until analysis. The IP3 concentration ([IP3]) in 20 µg of protein from oviductal ciliated cells was determined using a commercial radioreceptor assay kit (NEN Life Sciences, Boston, MA). The [IP3] was expressed as picomoles of IP3 per microgram of protein. Epithelial protein content was determined using the Bradford method (3). A recovery of 98% was observed after the addition of a known amount (1 pmol) of IP3 to the culture medium. The sensitivity of the assay was 0.05 pmol IP3. In all cases, cross reactivity with inositol 1,4-bisphosphate, inositol 1,3,4-trisphosphate, and inositol 1,3,4,5-tetrakisphosphate was <2%.
Extraction of PKC and quantification of PKC activity. Oviductal ciliated cells obtained by mechanical extraction of the epithelium of fimbria were placed in Hanks' medium at 37°C in an atmosphere of 5% CO2 and incubated with ATP. Samples were homogenized and centrifuged at 100,000 g for 60 min at 4°C for PKC extraction. The supernatant was collected, and the protein concentration was determined as described previously (3). The PKC activity in 20 µg of protein was determined using a commercial ELISA kit (Calbiochem). The PKC activity was expressed as milliunits of PKC per microgram of protein.
Immunocytochemical localization of IP3 receptors in cultured ciliated cells. Immunofluorescence and confocal microscopy were used to determine the cellular localization of the IP3 receptors. Cultured ciliated cells were fixed for 30 min at room temperature in 3% paraformaldehyde in PBS containing 2 mM MgCl2 and 0.2 mM CaCl2 (PBSCaMg). Samples were washed three times in PBSCaMg. Next, ciliated cells were permeabilized with 0.2% Triton X-100 in PBSCaMg for 10 min. Samples were washed four times in PBS containing 0.2% gelatin (PBS-gel) and incubated overnight at 4°C with the purified primary antibodies: anti-IP3 receptor type 1 (polyclonal; Affinity BioReagents, Golden, CO) and/or anti-IP3 receptor type 3 (monoclonal; BD Transduction Laboratories, San Diego, CA), dilution 1:50. Samples were washed four times in PBS-gel and then incubated at 37°C for 60 min either with secondary antibody Cy2-conjugated, affinity-purified goat anti-rabbit IgG (Jackson ImmunoResearch Laboratories, West Grove, PA), dilution 1:50, or with Cy3-conjugated, affinity-purified goat anti-mouse IgG (Jackson ImmunoResearch Laboratories), dilution 1:100, as appropriate. Samples were washed three times in PBS-gel and three times in PBS and then mounted in Fluoromount G (Electron Microscopy Sciences, Hatfield, PA). Fluorescence was detected using an LSM 510 laser scanning confocal microscope (Carl Zeiss, Oberkochen, Germany). Controls for the specificity of IP3 receptor immunofluorescence included 1) omitting the primary antibody, 2) analyzing the cross-reaction between primary and secondary antibodies, and 3) incubating the antibodies either with an excess of neutralizing peptide (Affinity BioReagents) that reacts with anti-IP3 receptor type 1 antibody or with HeLa lysate (BD Transduction Laboratories) for anti-IP3 receptor type 3 antibody.
Immunocytochemical subcellular localization of IP3 receptors in oviductal ciliated cells. Immunogold electron microscopy was used to determine the subcellular localization of the IP3 receptors. Tissue samples from oviductal epithelium of hamster fimbria were fixed for 4 h at room temperature in 4% paraformaldehyde containing Zamboni's fixative in 0.1 M PBS at pH 7.3. Samples were rinsed in 0.1 M PBS for 12 h at 4°C and pH 7.3, dehydrated, and embedded in LR White resin (London Resin, Reading, UK) at 50°C. Sections were placed on nickel grids and rinsed for 30 min in PBS containing 1% BSA. The grids were floated with the section side down for 1 h at room temperature on drops of primary antiserum diluted in PBS containing 1% BSA (primary antibodies were the same as those used for immunofluorescence, with dilutions of 1:30 for primary antibody anti-IP3 receptor type 1 and 1:80 for primary antibody anti-IP3 receptor type 3). The sections were then rinsed dropwise with the same buffer. The grids were treated in the same manner with goat anti-rabbit or anti-mouse antibodies conjugated to 40-nm gold particles (Kirkegaard & Perry Laboratories, Gaithersburg, MD), diluted 1:30 in the above buffer. The sections were then postfixed with 0.5% glutaraldehyde for 5 min. After a water rinse, the grids were counterstained for 5 min with 1% uranyl acetate. Electron microscopy was performed using a Siemens 101 electron microscope (Siemens, Iselin, NJ) operated at 80 keV. Controls for the specificity of IP3 receptor immunogold labeling included 1) omitting the primary antibody, 2) analyzing the cross-reaction between primary and secondary antibodies, and 3) incubating the antibodies either with an excess of neutralizing peptide (Affinity BioReagents) that reacts with anti-IP3 receptor type 1 antibody or with HeLa lysate (BD Transduction Laboratories) for anti-IP3 receptor type 3 antibody.
Data analysis. Statistical comparisons between different experimental conditions were made using ANOVA with SPSS version 8.0 software (SPSS, Chicago, IL). The criterion for a significant difference was a final value of P < 0.05. Data are expressed as means ± SE; n refers to the number of cultures or samples analyzed. The curves were fitted to logistic equations using the Inplot computer program (GraphPad Software, San Diego, CA). Analysis of regression and correlation was performed using SPSS version 8.0 with stepwise methods, with significance set at P < 0.05.
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RESULTS |
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Localization of IP3 receptors in oviductal ciliated cells. On the one hand, we report that IP3 receptors are present in ciliated cells and that they participate in the transduction pathways induced by ATP; on the other hand, it was previously suggested that multiple IP3 receptor intracellular locations could be related to the differing roles of these receptors in Ca2+ mobilization (9, 34). To determine the location of IP3 receptor types 1 and 3 in oviductal ciliated cells, immunofluorescence and confocal microscopy were performed with cultured ciliated cells using anti-IP3 receptor types 1 and 3 antibodies (Fig. 4). Figure 4A is a photomicrograph of red fluorescence indicating the localization of IP3 receptor type 3 in ciliated cells, and Fig. 4B shows the corresponding phase-contrast image. Figure 4C represents the localization of IP3 receptor type 1 in ciliated cells detected by green fluorescence, and Fig. 4D shows the corresponding phase-contrast image. In control experiments without primary antibodies, no fluorescence was detected in ciliated cells (data not shown). Interestingly, when the two receptor types were visualized in the same cell (Fig. 4, EH), the type 3 receptor (red fluorescence in Fig. 4E) was concentrated at the apical pole of the cell, whereas the type 1 receptor (green fluorescence in Fig. 4F) was homogeneously distributed. To extend our observation, we performed immunogold electron microscopy to determine the subcellular location of IP3 receptor types 1 and 3 in oviductal ciliated cells (Fig. 5). IP3 receptor type 1-reacting gold particles were found in the nucleus, endoplasmic reticulum, and intracellular vesicles, whereas practically no gold particles were found in the nuclear and plasma membranes (see Fig. 5C, solid bar). IP3 receptor type 3-reacting gold particles were also found in the nucleus and the endoplasmic reticulum of oviductal ciliated cells; however, in contrast to IP3 receptor type 1, type 3-reacting gold particles were found in the nuclear and plasma membranes (see Fig. 5C, shaded bar). Representative photomicrographs of the subcellular localization of IP3 receptor type 3-reacting gold particles in plasma membrane (Fig. 5A) and nucleus (Fig. 5B) are shown. In parallel, control experiments without primary antibody demonstrated that no gold particles were found in identical ciliated tissues (data not shown). This evidence demonstrates a diverse intracellular distribution of the IP3 receptor types 1 and 3 in ciliated cells, which could be related to the [Ca2+]i increase induced by ATP-dependent IP3 receptor activation from several Ca2+ stores, including the nucleus, the endoplasmic reticulum, and the extracellular medium.
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DISCUSSION |
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Xestospongin C almost completely blocked the first component and reduced the second component of the response to ATP. Furthermore, after treatment with both thapsigargin and xestospongin C, the second component of the [Ca2+]i increase induced by ATP was also almost completely blocked. These results indicate an interaction between these components through IP3 receptor activation-dependent Ca2+ influx. Direct activation of Ca2+ entry by plasma membrane IP3 receptors has been characterized electrophysiologically in a variety of cells, including T-lymphocytes (20), olfactory neurons (22), vascular endothelial cells (43), and a carcinoma cell line (17). Moreover, a tight functional interaction between IP3 receptors and store-operated channels can regulate capacitative Ca2+ entry (18). This result indicates the direct participation of IP3 receptors in the induction of the Ca2+ influx, an idea that is supported by our observation that the IP3 receptor type 3 is localized in the plasma membrane of the oviductal ciliated cells. Because the half-life of IP3 is 9 ± 2 s in single cells (48), and because the generation of the maximum increase in [IP3] synthesis was transient, an additional increase in [IP3] synthesis would be necessary to generate the latter Ca2+ increase because of the Ca2+ influx. Significantly, there was a good correlation between the generation of the second [IP3] peak at 60 s and the [Ca2+]i change evoked by Ca2+ influx, an observation that supports the possibility that IP3 participates directly in triggering the ATP-dependent Ca2+ influx. Electrophysiological recordings of Ca2+ channels are needed to determine the function of IP3 receptors involved in the control of Ca2+ influx in oviductal ciliated cells.
Because contamination of commercial samples of adenosine nucleotides has been reported (23), the [Ca2+]i increase could in theory be induced by ADP rather than by ATP, acting via P2Y receptors coupled to Ca2+ mobilization. Regarding this concern, we have never observed any change in CBF in the presence of ADP (28). Moreover, ADP did not change [Ca2+]i in ciliated cells. Furthermore, the EC50 and maximal effect parameters that describe the concentration-response curve of the [Ca2+]i increase induced by ATP were not affected in the presence of ADP (data not shown). Consequently, potential traces of ADP contaminating commercially available ATP should not modify the interpretation of our results.
The IP3 receptor types 1 and 3 share a subcellular distribution, with both forms being localized to the nucleus and the endoplasmic reticulum. Although we anticipate that both IP3 receptors participate in the Ca2+ response induced by ATP, at this moment there is no evidence for any selectivity of xestospongin C between the IP3 receptor types 1 and 3, supporting the possibility that these receptors could induce the [Ca2+]i increase necessary to evoke a CBF increase in oviductal ciliated cells. The IP3 receptor type 3 (which possesses 5-fold greater affinity for IP3 than the type 1 receptor) can be activated before type 1 by a small change in [IP3], which can increase the [Ca2+]i to 100200 nM (5). This hypothesis is supported by the single-channel differential Ca2+ activation properties that result in an apparent higher in vivo IP3 sensitivity of the type 3 receptor under resting levels of Ca2+ compared with type 1 (25). On the other hand, it has been reported that higher concentrations of [Ca2+]i (500 nM) cause a decrease in the IP3 binding to IP3 receptor type 1 while increasing binding to the type 3 receptor (5). In contrast to this observation, Mak et al. (25) found a similar inhibition of the activities of IP3 receptor types 1 and 3 by Ca2+ in this concentration range. Considering the subcellular distribution of the IP3 receptor types 1 and 3, it is possible that the first Ca2+ mobilization originates from the nucleus and the endoplasmic reticulum via activation of the type 3 receptor, after which IP3 receptor type 1, also localized in these organelles, participates in Ca2+ mobilization. Later, probably when [Ca2+]i has reached 400 nM, the IP3 receptors become inactivated by Ca2+ and induce the exponential decay in the response (7). It is important to emphasize that the inactivation of the IP3 receptor by IP3 can also contribute to the exponential decay in the response without changes in [Ca2+]i (24). This exponential decay was unaffected by Ca2+ influx, supporting the idea that IP3 receptor type 3 in the plasma membrane could be activated after intracellular IP3 receptor types 1 and 3 because of subsequent generation of IP3. Taken as a whole, this scenario would explain the increase in [Ca2+]i; however, experiments to control separately the activation of the two types of IP3 receptor associated with Ca2+ mobilization are required to completely understand the molecular mechanism of Ca2+ mobilization in ciliated cells.
We found that PKC activity is stimulated by ATP and is necessary to modulate Ca2+ influx induced by ATP. However, Ca2+ mobilization was not triggered in this process. Furthermore, PKC also has a role downstream of Ca2+ influx because this mediator can transiently increase CBF independently (28). On the other hand, a PKC effect upstream of the [IP3] increase can probably be excluded because the PKC activity did not modify the concentration of this mediator in any of the experiments performed in this study.
Our results suggest that the increase in CBF induced by ATP in oviductal ciliated cells requires Ca2+-dependent proteins such as CaM and CaMKII. The similarity in the time courses of the effects of CaM and CaMKII inhibitors on [Ca2+]i and CBF increases induced by ATP can be explained by the activation of CaM and the subsequent increase in CaMKII activity. CaMKII may target the IP3 receptor type 3, because these proteins have been found to be colocalized in the apical domain in gastrointestinal tissues and the IP3 receptor type 3 has potential phosphorylation sites for CaMKII (26). On the other hand, an effect upstream of the [IP3] increase induced by ATP is probably unlikely because changes in CaM and CaMKII activities did not affect the concentration of [IP3] in our experiments.
In summary, this study was focused on the elucidation of the relationship between the subcellular distribution and the functional effects of the IP3 receptors, which we postulate are associated with the ATP transduction pathway. Further experiments examining the ATP transduction pathway in oviductal ciliated cells are required to understand completely the role of IP3 receptors in the control of [Ca2+]i in these cells.
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GRANTS |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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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.
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