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1 CNRS UMR 6187, Institut de Physiologie et Biologie Cellulaires, Université de Poitiers, 40, Avenue du Recteur Pineau, 86022 Poitiers Cedex, France
2 INSERM U427, Développement, humain et différenciation, Faculté de pharmacie, 75270 Paris cedex 6, France
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(Received 30 July 2004;
accepted after revision 1 September 2004;
first published online 9 September 2004)
Corresponding author L. Cronier: CNRS UMR 6187, Institut de Physiologie et Biologie Cellulaires, 40 Avenue du Recteur Pineau, 86022 Poitiers Cedex, France. Email: laurent.cronier{at}univ-poitiers.fr
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Introduction |
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Ca2+ ion transfer across the ST is essential for normal fetal development. Its transport takes place in an active manner against a concentration gradient, as the Ca2+ concentration in the fetal circulation is considerably higher than that of the mother. This active transfer is carried out by the ST, for which the first step is that of membrane-gated Ca2+ entry. It has been suggested that the influx of Ca2+ across the ST microvillous membrane is performed by a facilitated diffusion process (Kamath et al. 1992). Recently, the presence of Ca2+ transporter types 1 and 2 was demonstrated in cultured trophoblastic cells (Moreau et al. 2002a). Furthermore, Ca2+ is required in multiple cellular functions that include secretion, ionic conductance, cell-cycle regulation and programmed cell death (Berridge et al. 2000). However, the nature of Ca2+ conductance in the ST, and the mechanisms by which it is regulated, are poorly understood. Previous studies have demonstrated an increase in intracellular Ca2+ in the ST following exposure to various biologically active substances acting in both autocrine and paracrine fashions: GnRH (Currie et al. 1993), ATP and UTP (Petit & Belisle, 1995), ATP and angiotensin II (Karl et al. 1997), endothelin (Cronier et al. 1999), ATP (Clarson et al. 2002). However, the nature of Ca2+ channel activation in the ST remains controversial, with voltage-operated Ca2+ channels (VOCC; Meuris et al. 1994; Petit & Belisle, 1995; Robidoux et al. 2000), non-selective cationic channels (NSCC; Grosman and Reisin, 2000; Llanos et al. 2002; Long & Clarson, 2002), store-operated Ca2+ channels (SOCCs; Clarson et al. 2003) and receptor-operated Ca2+ channels (ROCCs; Bax et al. 1994) all having been described.
We previously demonstrated the presence of endothelin (ET) receptors A and B on the human trophoblastic membrane (Malassiné et al. 1993b). With the major signal transduction pathway of endothelin-1 (ET1) acting via phospholipase C (PLC) and the mobilization of intracellular Ca2+, we have thus used cytofluorimetry and pharmacological analysis to determine the nature of ET1-mediated Ca2+ entry into ST cells in primary culture.
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Methods |
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ET1, trypsin, DNase I, NiCl2, Indo-1 AM and nifedipine were purchased from Sigma (St Louis, MO, USA), BQ123 and BQ788 were from Neosystem (Strasbourg, France), monoclonal anti-human leucocytic antigen-A, B and C antibody (W6-32HL) was from Sera Laboratory (Crawley Down, UK) and SK&F96365 was from Calbiochem (VWR International, Fontenay-sous-bois, France). LOE 908 was kindly provided by Boehringer Ingelheim (Ingelheim, Germany). All other reagents were from standard suppliers.
Trophoblastic cell culture
Human placentas were obtained after caesarean section from mothers with uncomplicated pregnancies. The use of human placentas for this study was approved by the ethics committee of the Clinique du Fief de Grimoire (Poitiers, France). CT cells were isolated using a previously described method (Malassiné et al. 1993a), which was adapted from that of Kliman et al. (1986). Briefly, after several sequential trypsin/DNase digestions followed by Percoll gradient centrifugation, cells were further purified by means of W6-32HL. CT cells were diluted to a final concentration of 0.5 x 106 ml–1 in minimum essential medium (MEM) containing 10% fetal calf serum (FCS), 25 mM glucose and 50 µg ml–1 gentamicin. Cells were plated onto glass coverslips in 35 mm plastic dishes (Nunclon, Nunc, Roskilde, Denmark) and incubated for 2 days at 37 °C in 5% CO2. The culture medium was renewed daily. Cytokeratin 07 immunocytochemistry (clone OV.TL12/30, Dako, Denmark) was performed to confirm the cytotrophoblastic nature of the attached cells. After the purification procedure, 95% of the cells stained positively for cytokeratin.
Recording of [Ca2+]i transients
Intracellular free Ca2+ concentrations ([Ca2+]i) were measured by means of the ratiometric method with an inverted epifluorescence microscope (Olympus IX 70). Briefly, the Ca2+ indicator Indo-1 was used, for which fluorescence emissions of the Ca2+-free (485 nm) and Ca2+-bound (405 nm) forms of the indicator were collected using a dichroic filter and two photomultiplier tubes (excitation wavelength 355 nm). The Ca2+ activity was estimated as the ratio of the 405/485 nm fluorescence emission intensities. For loading of the probe, trophoblastic cells were incubated for 45 min in the dark in Tyrode solution (mM: 144 NaCl, 5.4 KCl, 2.5 CaCl2, 1 MgCl2, 0.3 NaH2PO4, 5 Hepes, 5.6 glucose, pH 7.4) containing the lipophilic form of the dye (Indo-1 AM dissolved in DMSO 0.3%) at a concentration of 3 µM. After carefully washing off the unincorporated fluorogenic dye, cells were incubated in Tyrode solution for a further 15 min in the dark to obtain complete de-esterification of the dye. STs with between six and eight nuclei accumulated in a central nuclei mount were identified with the aid of the inverted epifluorescence microscope. Variations of [Ca2+]i with time were measured in a defined area located approximately in the centre of the trophoblastic cells. By means of a home-made gravity-based microperfusion system, test solutions were applied rapidly onto the ST under investigation by using a streamline flow directed from the opening of a stainless steel capillary tube (internal diameter 50 µm) positioned in the bath. Switching between different solutions was performed with electrovalves controlling different juxtaposed capillaries. Treatments were performed by perfusion of Tyrode solution containing ET1 or pharmacological agents. All experiments were conducted at room temperature (20 ± 1 °C).
Ratio analyses and statistics
Indo-1 signals were not calibrated in terms of absolute values since this was not necessary for the monitoring of variations of Ca2+ levels. Intracellular Ca2+ concentration changes were expressed as changes in the ratio of the 405/485 nm fluorescence emissions of the dye. Reported data represent the mean ± S.E.M. of the percentage difference in ratio between the basal level and peak or plateau levels, with n being the number of STs tested. One-way analysis of variance followed by a Dunnett's post hoc test was used to compare peak ratio values, while paired Student's t tests were used for statistical comparisons of baseline and plateau Ca2+ levels for different treatments.
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Results |
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When purified CT cells are cultured in the presence of 10% FCS, after adhesion and flattening, cells make initial contacts by pseudopodia with neighbouring cells, transform into cellular aggregates and fuse to form STs. This differentiation process was monitored by the immunostaining of cells for desmoplakin and ßhCG secretion as previously described (Cronier et al. 1994, 2003; Frendo et al. 2003). Under the experimental conditions used here, a large proportion of mononuclear cells had differentiated into ST after 48 h of culture. Only STs with between six and eight nuclei amassed in a central mount were selected for further study.
Effect of ET1 on [Ca2+]i in STs
Previous studies have demonstrated that, in our experimental conditions, ET1 (100 nM) is effective in inducing a Ca2+ response in around 75% of investigated cells (Cronier et al. 1999). As shown in Fig. 1, a stable resting [Ca2+]i level is followed by a rapid increase in fluorescence ratio upon the addition of 100 nM ET1. This was followed by a sustained prolongation of [Ca2+]i in 41% of ET1-responding cells. The effect of ET3 on Ca2+ activity presented an identical profile (data not shown).
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Coupling of the ETB receptor to PLC was examined pharmacologically using U73122, a membrane-permeable inhibitor which inhibits PLC by disrupting its coupling to G protein. As shown in Figs 2D and 4, pre-incubation of cells with 2 µM U73122 completely abolished the ET1-induced [Ca2+]i increase (spike and plateau; n = 12) indicating that the mobilization of Ca2+ from inositol 1,4,5-trisphosphate (IP3)-sensitive intracellular Ca2+ stores is a pre-requisite for the ET1-induced Ca2+ response.
Characterization of channels involved in Ca2+ entry
To characterize the nature of Ca2+ channels involved in ET1-evoked Ca2+ entry in STs, a panel of Ca2+ channel inhibitors was tested. Ni2+ is an inorganic, non-specific inhibitor of Ca2+ channels, and it has been demonstrated to block Ca2+ entry in other cell types. As illustrated in Fig. 3A and Fig. 4, 1 mM Ni2+ significantly reduced the ET1-evoked initial Ca2+ entry by 70% and inhibited the plateau phase (n = 13). The inhibitory effects of Ni2+ were reversible.
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It is possible, therefore, that the ET-induced Ca2+ entry occurs via voltage-insensitive Ca2+ channels. Recently, two types of organic compounds have been used as pharmacological tools to block L-type Ca2+ channel blocker-insensitive Ca2+ influx mechanisms, they are the imidazole derivatives SK&F96365 and LOE 908. Importantly, NSCCs and SOCCs can be distinguished in terms of their sensitivities to these compounds (Kawanabe et al. 2001, 2002). NSCCs are sensitive to LOE 908, whereas SOCCs are resistant to LOE 908 and sensitive to SK&F96365. As shown in Fig. 5A and B, perfusion of STs with 30 µM SK&F96365 during the plateau phase decreased the ET1-evoked Ca2+ entry by 80% (n = 10). However, SK&F96365 did not totally abolished the plateau phase. Perfusion of STs with LOE 908 during the plateau phase induced a dose-dependent decrease of the ET1-evoked Ca2+ entry without totally abolishing the ET1 response (Fig. 5C and D).
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Discussion |
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The results presented here indicate that ET1 stimulated a biphasic (transient and sustained) increase in [Ca2+]i in trophoblastic cells. This Ca2+ response is mediated by the ETB receptor, since BQ788 totally abolished the response. ETB receptors were previously demonstrated in the term trophoblastic microvillous membrane (Malassiné et al. 1993b), in first trimester trophoblastic cells (Cervar et al. 1997) and in a human extravillous trophoblast cell line (Chakraborty et al. 2003). In various cell types, ETB receptors are protein Gq-coupled receptors activating PLC to produce IP3 as well as 1,2-diacylglycerol (DAG). IP3 stimulates the release of Ca2+ from IP3-sensitive stores and subsequently the activation of SOCCs. Furthermore, it was recently demonstrated that a non-metabolizable analogue of DAG (OAG) could directly activate members of the transient receptor potential (TRP) superfamily, thereby inducing an increase of intracellular Ca2+ in placental explants (Clarson et al. 2003). Abrogation of the ET1-mediated Ca2+ response after pre-treatment with U73122, a PLC inhibitor, indicates firstly that in human trophoblastic cells ETB receptors are coupled to PLC via Gq protein. The abrogation of both the spike and plateau phases indicates that the inhibition of PLC could also induce inhibition of other functional Ca2+ channels such as SOCC, NSCC or other members of the TRP superfamily. The persistence of the rapid transient rise in [Ca2+]i in Ca2+-free extracellular medium confirms the release of Ca2+ from intracellular Ca2+ stores in response to ET1 stimulation. Furthermore, abolition of the sustained increase in [Ca2+]i in Ca2+-free extracellular medium argues for the entry of extracellular Ca2+ during the plateau phase. Inhibition of the plateau phase by Ni2+ confirms the existence of an ET1-induced Ca2+ entry.
Based on the findings presented here, several candidate Ca2+ channel types could mediate Ca2+ entry. These include voltage-operated channels, store-operated Ca2+ channels, receptor-operated channels and non-selective cationic channels. Abrogation of the Ca2+ response in the presence of U73122 argues for the absence of a receptor-operated channel stimulation induced by ET1. No evidence for the presence of voltage-operated channels was demonstrated during ET1 stimulation, since nifedipine did not reduce the ET1-induced Ca2+ response, and depolarization with a hyper-potassium solution had no effect. These results confirm findings from a previous electrophysiological study by this group (Cronier et al. 1999). Other studies have suggested the presence of nifedipine-sensitive channels in the ST of term placenta (Polliotti et al. 1994; Meuris et al. 1994; Cemerikic et al. 1998; Robidoux et al. 2000). However, Bax et al. (1994) using Ca2+ measurements could not demonstrate the presence of these voltage-operated channels in cultured trophoblastic cells. Furthermore, it was reported that in a trophoblastic cell line (BeWo cells), Ca2+ uptake was not influenced by L-type Ca2+ channel modulators (Moreau et al. 2001). This insensitivity towards blockers of voltage-operated Ca2+ channels was also observed with other experimental models including placental perfusion (Stulc et al. 1994), ST membrane vesicles (Kamath et al. 1992) and placental explants (Long & Clarson, 2002; Clarson et al. 2003). It should be pointed out that physiological studies require a clear identification of the investigated cells. Under the experimental conditions employed here, the procedure for trophoblast isolation prevents contamination by other placental cells such as macrophages, fibroblasts, endothelial or smooth muscle cells.
Recently, SK&F96365 (Merrit et al. 1990) and LOE 908 (Encabo et al. 1996) have been used as pharmacological tools to analyse L-type Ca2+ channel blocker-insensitive Ca2+ influx mechanisms. These compounds have permitted characterization of Ca2+ entry routes in excitable and non-excitable cells. Indeed, NSCCs are sensitive to LOE 908, whereas SOCCs are resistant to LOE 908 and sensitive to SK&F96365 (Kawanabe et al. 2001, 2002). From the pharmacological experiments reported here, the presence of both SOCC and NSCC activation during the ET1-induced Ca2+ response in cultured ST cells has been demonstrated.
SOCCs serve as an important class of Ca2+ entry channel which are activated by depletion of intracellular Ca2+ stores upon stimulation of G-protein-coupled receptors (Berridge et al. 2000; Peng et al. 2003). In electrically non-excitable cells, SOCCs serve as one of the main routes for the entry of extracellular Ca2+. The presence of SOCCs in cultured cytotrophoblastic cells was previously suggested in response to stimulation by various ligands (Petit & Belisle, 1995; Karl et al. 1997; Cronier et al. 1999; Clarson et al. 2002). Recently, using placental explants, Clarson et al. (2003) demonstrated pharmacologically the presence of SOCC in term placenta, the expression of transient receptor potential canonical (TRPC) mRNA in first trimester and term placentas, and the immunolocalization of TRPC3, 4 and 6 in term ST cells. They concluded that store-operated Ca2+ entry occurs in human term placenta and that it may be gestationally regulated. Here we have demonstrated the activation of SOCCs by ET1 in cultured human term trophoblastic cells. The molecular identity of this SOCC needs to be identified, but based on previous studies, CaT1 (Moreau et al. 2002a), TRPC (Clarson et al. 2003) and polycystin-2 (Ong et al. 1999) could be candidates for this function. In situ hybridization studies have demonstrated the presence of CaT1 in STs (Peng et al. 2001; Wissenbach et al. 2001). Its expression seems to be correlated to Ca2+ uptake activity and hCG secretion (Moreau et al. 2002a). Moreover, another member of the TRP superfamily, polycystin-2, is present in term human STs (Gonzalez-Perret et al. 2001) .
NSCC form a mixed group of ion channels that include ligand-gated, mechanosensitive and hyperpolarization- or stress-activated channels. NSCCs are widely distributed in numerous tissue types and could be permeable to Ca2+ ions. Many of their biophysical and regulatory properties have been described (for review, see Nilius, 2003; Clapham, 2003), but channel functions remain unknown in many cases. The presence of NSCCs in the human placenta has been previously considered by means of electrophysiological studies on placental CT cells (Clarson et al. 1999), after fusion of microvillous membranes with planar lipid bilayers (Grosman & Reisin, 2000) or after reconstitution of brush border membranes into giant liposomes (Riquelme et al. 1995; Llanos et al. 2002). Moreover, in excitable (Van Renterghem et al. 1988; Enoki et al. 1995; Minowa et al. 1997) and non-excitable cells (Enoki et al. 1995; Lee et al. 1999), ET1 was able to activate NSCCs.
SOCCs and NSCCs appear to be essential in replenishing ST Ca2+ stores (Putney, 1999, 2001) and serve as an important means of Ca2+ entry in trophoblastic cells (Shennan & Boyd, 1987; Illsley & Sellers, 1992). Moreover, in non-excitable cell types, activation of NSCCs and SOCCs leading to Ca2+ influx seems to play a role in processes that include secretion, cell proliferation, gene transcription and cell death (Berridge et al. 2000). In the human trophoblast, transient intracellular Ca2+ variations could affect these processes. It has been demonstrated that in purified human trophoblastic cells, raising [Ca2+]i induces an increase of K+ and Cl– efflux (Kibble et al. 1996; Turner et al. 1999; Clarson et al. 2002). As the placental transfer of maternal calcium is carried out in vivo by the ST, SOCCs and Ca2+-permeable NSCCs could also represent regulated modes of Ca2+ entry. Furthermore, Ca2+ ions could serve as mediators implicated in gap junctional intercellular communication during trophoblastic fusion (Cronier et al. 1994, 1999, 2003).
Various bioactive substances have been demonstrated to induce an increase in intracellular Ca2+ in isolated trophoblastic cells. These include GnRH (Currie et al. 1993), ATP and UTP (Petit & Belisle, 1995), ATP and angiotensin II (Karl et al. 1997), ET (Cronier et al. 1999) and ATP (Clarson et al. 2002). The human placenta appears to be an important source of ETs; cultured trophoblastic cells have been shown to release ET1 and to express pre-pro-ET1 and pre-pro-ET3 mRNA (Malassiné et al. 1993a; Robert et al. 1996). Since the first description of ETs, it is evident that these peptides display a multitude of biological functions controlling cellular ion fluxes, cell-to-cell communication, hormone release, cell chemokinesis, cell proliferation, cell differentiation, and the growth and progression of various tumours (Nelson et al. 2003). We have previously demonstrated that ET1 impairs trophoblast differentiation (Cronier et al. 1999). Furthermore, ET1 stimulates the invasion of first trimester trophoblastic cells (Cervar et al. 1997) and the migration of a human extravillous trophoblast cell line (Chakraborty et al. 2003). Further studies are required to determine the implications of ET1-induced Ca2+ increases in the human trophoblast.
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