Membrane Fluidity Changes Are Associated with Benzo[a]Pyrene-Induced Apoptosis in F258 Cells
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1 Membrane Fluidity Changes Are Associated with Benzo[a]Pyrene-Induced Apoptosis in F258 Cells Protection by Exogenous Cholesterol MORGANE GORRIA, a XAVIER TEKPLI, a ODILE SERGENT, b LAURENCE HUC, a FRANÇOIS GABORIAU, c MARY RISSEL, a MARTINE CHEVANNE, b MARIE-THÉRÈSE DIMANCHE-BOITREL, a AND DOMINIQUE LAGADIC-GOSSMANN a a INSERM U620, UniversitédeRennes 1, Rennes, France b UPRES EA 3891, UniversitédeRennes 1, Rennes, France c INSERM U522, Hôpital Ponchaillou, Rennes, France ABSTRACT: Polycyclic aromatic hydrocarbons (PAHs) such as benzo[a]yrene (B[a]P) constitute a widely distributed class of environmental pollutants, responsible for highly toxic effects. Elucidating the intracellular mechanisms of this cytotoxicity thus remains a major challenge. Besides the activation of the p53 apoptotic pathway, we have previously found in F258 hepatic cells that the B[a]P (50 nm)-induced apoptosis was also dependent upon the transmembrane transporter NHE1, whose activation might result from membrane alterations in our model. We here demonstrate that: (1) B[a]P induces a membrane fluidization surprisingly linked to NHE1 activation; (2) membrane stabilization by exogenous cholesterol protects cells from B[a]P-induced apoptosis, via an effect on late acidification and iron uptake. KEYWORDS: benzo[a]pyrene; apoptosis; membrane fluidity; NHE1; cholesterol INTRODUCTION Polycyclic aromatic hydrocarbons (PAHs) are important environmental pollutants to which humans are largely exposed. Besides their well-known carcinogenic effects, PAHs also induce apoptosis in different cell types, for example, hepatic cells. 1,2 Although activation of p53 plays a primordial role in this Address for correspondence: Dominique Lagadic-Gossmann, INSERM U620, Faculté de Pharmacie, Université de Rennes 1, 2 Av. Du. Prof Léon Bernard, Rennes cedex, France. Voice: ; fax: dominique.lagadic@rennes.inserm.fr Ann. N.Y. Acad. Sci. 1090: (2006). C 2006 New York Academy of Sciences. doi: /annals
2 GORRIA et al.: MEMBRANE FLUIDITY CHANGES IN APOPTOSIS 109 apoptosis, permissive pathways might also occur; indeed, we have recently evidenced a parallel activation of Na + /H + exchanger (NHE1) with consequences on apoptosis occurrence. 1 Such an activation might result from changes in membrane characteristics, especially as PAHs are highly lipophilic molecules capable of interacting with biological membranes. 3 Increases in membrane fluidity can be involved in apoptosis, since inhibition of membrane fluidization has been shown to be protective in different apoptotic models. 4 An important role for reactive oxygen species (ROS) production has also been demonstrated in cell death induced by various chemicals. 5 As we recently demonstrated strong interactions between changes in membrane fluidity and ROS production in hepatocytes exposed to ethanol 4 and as PAHs induce ROS production, 1 we wanted to test here the possible involvement of membrane fluidity changes in B[a]P-induced apoptosis. MATERIALS AND METHODS Rat hepatic F258 epithelial cells were cultured and treated as previously described. 1 Membrane fluidity was measured either by quantification of the polarization fluorescent ratio of 1,6-diphenyl-1,3,5-hexatriene (DPH, 5 M) or by analysis of electron paramagnetic resonance of 12-doxyl stearic acid (12-DSA, 50 g/ml) spin label. Apoptosis was evaluated either by Hoechst staining of chromatin or measurement of caspase 3/7 activity, and the intracellular ph (ph i )was monitored by microspectrofluorimetry using the ph-sensitive fluorescent probe, carboxy-snarf-1. 1 Iron uptake was measured from cell lysates following a 6-h incubation with [ 55 Fe]-iron chloride (10 mm) performed during the late hours of each cell treatment. Lipid peroxidation was measured using the fluoroprobe C 11 - BODIPY 581/591 (10 M). 4 RESULTS AND DISCUSSION Using the fluorescence polarization technique and DPH, we first demonstrated that B[a]P (50 nm) induces a significant increase in bulk membrane fluidity following 48 h of exposure, as pointed out by the decrease of polarization ratio (FIG. 1A). Under our experimental conditions, we have previously found that B[a]P is metabolized by cytochromes of the CYP1 family within the first 24 h, indicating that B[a]P has already entered the cells through the plasma membrane at this time. We showed here that the B[a]Pinduced membrane fluidization remained undetectable after a 24-h treatment, thus suggesting an indirect action of B[a]P on the membrane s physical state. After a 72-h treatment, an increase in fluidity was still detected. This latter
3 110 ANNALS NEW YORK ACADEMY OF SCIENCES FIGURE 1. Effects of B[a]P (50 nm) on membrane fluidity in F258 cells. (A) Kinetics of B[a]P-induced bulk membrane fluidization. The fluorescence polarization ratio measured from DPH-labeled cells is conversely proportional to membrane fluidity. (B) Effects of cariporide (30 M; B) and exogenous cholesterol (30 g/ml;b) on B[a]P (48 h)-induced membrane fluidization, measured using EPR and 12-DSA spin label. S order parameter is conversely proportional to membrane fluidity. Data are given as mean ± SEM of at least three independent experiments ( P < 0.05; P < 0.01, t-test). result further reinforces the idea that a direct interaction of B[a]P with plasma membrane was likely not responsible for this sustained increase of membrane fluidity. As we previously demonstrated that the transmembrane protein NHE1 was involved in our model of apoptosis, we then tested the possible involvement of this exchanger in the B[a]P-induced increase of membrane fluidity. Using cariporide (30 M) to inhibit NHE1 activation observed at 48 h, 1 we then showed that the B[a]P-induced change in fluidity was partly related to this transporter, as pointed out by the absence of a significant decrease of the membrane order parameter estimated using 12-DSA and RPE (FIG. 1B).
4 GORRIA et al.: MEMBRANE FLUIDITY CHANGES IN APOPTOSIS 111 FIGURE 2. (A, B) Cotreatment with exogenous cholesterol affects B[a]P-induced apoptosis. Apoptosis was analyzed following a 72-h treatment with B[a]P by (A) counting the percentage of cells with apoptotic nuclei after Hoechst staining, and by (B) estimating caspase 3/7 activity. (C) Oxidative stress was analyzed by lipid peroxidation measurements after a 72-h treatment. (D) Iron uptake in F258 cells was analyzed using 55 Fe after a 72-h treatment. Results are representative of at least three independent experiments in each case ( P < 0.05; P < 0.001, t-test). Exogenous application of cholesterol (30 g/ml), a well-known membrane stabilizer, was then used to test the involvement of membrane fluidization in B[a]P-induced apoptosis. Our data demonstrated that cotreatment with this compound, besides inhibiting any membrane fluidization (FIG. 1B), significantly reduced apoptosis, as evidenced by a decrease of cell population exhibiting nuclear fragmentation (FIG. 2A) and of caspase 3/7 activity (FIG. 2B). The inhibition by 30% of B[a]P-induced apoptosis by cholesterol was in the range of inhibitions observed when the permissive apoptotic pathway relying upon NHE1 activation was targeted. 1 In order to find out which event in the B[a]P-induced apoptotic cascade was related to membrane fluidization, we decided to test the effects of exogenous cholesterol application on the apoptosis-related intracellular acidification and the oxidative stress previously shown to be associated with B[a]P-induced apoptosis. Our results clearly demonstrated that cotreatment of F258 cells with cholesterol led to a significant reduction of B[a]P-induced acidification ( ph i = 0.08 ± 0.04 [+ cholesterol] vs. ph i = 0.17 ± 0.04 ph units [ cholesterol], n = 10, P < 0.01, t-test), thus suggesting an inhibition of
5 112 ANNALS NEW YORK ACADEMY OF SCIENCES B[a]P-induced mitochondrial damages; indeed, the observed acidification has been shown to be due to mitochondrial dysfunction. 1 We then focused on the possible involvement of membrane fluidization in B[a]P-induced oxidative stress. To do so, oxidative stress was evaluated by measuring lipid peroxidation. As shown in FIGURE 2C, cholesterol treatment remained ineffective on B[a]P-induced lipid peroxidation. On the basis of our recent observation showing that ethanol-induced membrane fluidization enhanced oxidative stress in rat hepatocytes via interactions with iron metabolism 4 and knowing that iron was involved in caspase 3/7 activation in our model (unpublished data), we finally investigated the possible action of cholesterol on B[a]P-elicited iron uptake. Analyzing 55 Fe uptake under our experimental conditions, we showed that the protective effect of cholesterol was likely through an inhibition of B[a]P-induced iron uptake (FIG. 2D). Altogether, our results indicate that cholesterol might reduce B[a]P-induced apoptosis by inhibiting both iron uptake and mitochondria-dependent acidification, thereby possibly interfering with caspase 3/7 activation. In conclusion, this work suggests a role for NHE1 activation in B[a]Pinduced membrane fluidization and an involvement of fluidization in the early events of B[a]P-induced apoptotic cascade. This, along with our previous work, 4 also points to a role for membrane fluidization in chemically induced cell death likely through interactions with iron transport. REFERENCES 1. HUC, L.et al Identification of Na + /H + exchange as a new target for toxic polycyclic aromatic hydrocarbons. FASEB J. 18: SOLHAUG,A. et al Polycyclic aromatic hydrocarbons induce both apoptotic and anti-apoptotic signals in Hepa1c1c7 cells. Carcinogenesis 25: JIMENEZ,M. et al The chemical toxic benzo[a]pyrene perturbs the physical organization of phosphatidylcholine membranes. Environ. Toxicol. Chem. 21: SERGENT, O. et al Role for membrane fluidity in ethanol-induced oxidative stress of primary rat hepatocytes. J. Pharmacol. Exp. Ther. 313: FLEURY, C., B. MIGNOTTE & J.L. VAYSSIERE Mitochondrial reactive oxygen species in cell death signaling. Biochimie 84:
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