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Pyrene at Nanomolar Concentrations by Intact Murine Hepatoma Cells1

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Pyrene at Nanomolar Concentrations by Intact Murine Hepatoma Cells1 [CANCER RESEARCH 42, 4473-4478, November 1982] 0008-5472/82/0042-OOOOS02.00 Efficient Metabolism of Benzo(a)pyrene at Nanomolar Concentrations by Intact Murine Hepatoma Cells1 Arthur G. Miller2 and James P. Whitlock, Jr.3 Department of Pharmacology, Stanford University School of Medicine, Stanford, California 94305 ABSTRACT We have shown previously that the disappearance of BP fluo rescence is due to metabolism of BP (24). Using this assay, we We have studied the metabolism of benzo(a)pyrene (BP) by found rapid metabolism of BP at nM levels, similar to those in intact mouse hepatoma cells, at nM concentrations of the the environment. These results seemed incompatible with pre carcinogen, using an assay in which we directly measure the vious studies of BP metabolism using the standard AHH assay, rate of BP fluorescence disappearance. The rate of BP metab in which the apparent Kmfor BP metabolism was found to be in olism is half-maximal, at limiting cell dilution, when the concen the ¡IMrange (20, 27, 38). In fact, we were unable to detect tration of BP is about 4 nM. This apparent Kmfor BP metabolism metabolism, using the AHH assay, at a BP concentration at is much lower than those reported previously for several rea which the rate of metabolism was half-maximal, as measured sons, (a) Partitioning of BP into cells markedly influences by the BP disappearance assay. Therefore, we performed kinetic measurements, and we account for these effects, (b) experiments to further characterize BP metabolism at low con Enzyme inducers can competitively inhibit BP metabolism and centrations and to determine the relation between the BP thus may introduce artifacts into kinetic measurements, (c) disappearance assay and the AHH assay. Under the conditions of this assay, phenolic BP metabolites are Using the BP disappearance assay, we find that the apparent produced but do not accumulate, due to their further metabo Km for BP metabolism is 3 to 5 nM, when measured at limiting lism; therefore, assays of BP metabolism which measure the cell dilution. This apparent Kmis equal to an apparent Kmbased production of phenols, such as the commonly used aryl hydro on the aqueous concentration of BP. Cell concentration has a carbon hydroxylase assay, may markedly underestimate the strong effect on the kinetics of BP metabolism; we can account rate of BP metabolism when intact cells and low substrate for this effect by considering the partitioning of BP between concentrations are used. Our results show that cells can effi cells and the medium in which they are suspended. Another ciently metabolize BP when exposed to BP concentrations important factor influencing BP metabolism at low substrate similar to those present in the environment. concentrations is the presence of enzyme inducers, which may competitively inhibit BP metabolism. In addition, the AHH assay INTRODUCTION does not detect BP metabolism in intact cells at low substrate PAHs,4 such as the carcinogen BP, are ubiquitous pollutants concentrations, due to the rapid further metabolism of the phenolic metabolites measured in the AHH assay. and are present in the environment at PM to nM concentrations (2, 3, 7, 12, 16, 34). These compounds, like other lipophilic MATERIALS AND METHODS substances, are metabolized to more polar derivatives by sub- strate-inducible, microsomal, cytochrome P-450-containing Materials. Materials were obtained as follows: cell culture media, enzyme systems (8,11,14,15). The metabolism of PAHs can PBS, and trypsin/EDTA from Grand Island Biological Co.; fetal bovine also convert them to chemically reactive, electrophilic inter serum from Irvine Scientific; cell culture plasticware from Falcon Plas tics; BA from Eastman Organic Chemicals; BP, 5,6-benzoflavone (ß- mediates which bind covalently to cellular macromolecules; such metabolic activation appears to be a key step in PAH- naphthoflavone), and 7,8-benzoflavone (o-naphthoflavone) from Aid- rich Chemical Co.; NADPH from Calbiochem/Behring Corp.; UDPGA induced neoplasia and toxicity (8, 15, 19, 25, 26, 36). Thus, (sodium salt) and /8-glucuronidase (type H-1 ) from Sigma Chemical Co. knowledge of the metabolism of PAHs at low concentrations is Cell Culture. Hepa-1c1c7 mouse hepatoma cells (17) were main required in order to better understand the effects on animals of tained as monolayer cultures at 37°and 5% CO2 in «-minimal essential PAHs present in the environment. medium without nucleosides, supplemented with 10% fetal calf serum. We have studied BP metabolism using low (nM) concentra Trypsin/EDTA (0.05%/0.02%) was used to detach cells from dishes tions of the carcinogen and intact cells. BP metabolism was for subculture or fluorescence measurements. Cells were plated at 2 quantitated by direct measurement of BP fluorescence loss. x 106 cells/100-mm dish in 10 ml medium 2 days before use. BP- metabolizing enzyme activity was induced by addition of 120 nmol of 1 Supported by Research Grants CA 24580 and GM 17367 and Training BA in acetone per dish 16 hr before use. The final concentration of Grant GM 07149 from the NIH and Institutional Grant IN 32S from the American acetone in the medium was 0.1 %; this had no detectable effect on cell Cancer Society. viability or enzyme activity. Monolayers were trypsinized, diluted 10- 2 Present address: Tumor Virology Laboratory. The Salk Institute, P.O. Box fold with PBS, centrifuged at 500 x g for 4 min, and resuspended in 85800, San Diego, Calif. 92138. 3 Recipient of a faculty research award from the American Cancer Society. fresh PBS. After trypsinization, cells were kept on ice until assayed. ' The abbreviations used are: PAH, polycyclic aromatic hydrocarbon; BP, Cell Sonication. Cells were sonicated using a Model W-225R cell benzo(a)pyrene; AHH. aryl hydrocarbon hydroxylase; PBS, calcium- and mag disruptor equipped with a stepped microtip (Heat Systems-Ultrasonics, nesium-free Dulbecco's phosphate-buffered saline [containing (in g/liter): Inc., Plainview, N. Y.). Aliquots (5 ml) of cells suspended in PBS were KHîPO..,0.2; Na2HPCv7H2O, 2.16; and NaCI. 8.0]; BA, benz(a)anthracene; sonicated at 0°in plastic tubes for 15 sec, using the highest power UDPGA, uridine diphosphoglucuronic acid; FACS, fluorescence-activated cell sorter; 3-OHBP, 3-hydroxybenzo(a)pyrene. setting possible without producing foaming. Microscopic examination Received March 8, 1982; accepted July 26. 1982. revealed total cellular disruption. NOVEMBER 1982 4473 Downloaded from cancerres.aacrjournals.org on September 25, 2021. © 1982 American Association for Cancer Research. A. G. Miller and J. P. Whitlock, Jr. Cell Sorter Analysis. Single-cell BP fluorescence was measured on disappearance assay, we measured the initial rate of BP fluo a Becton-Dickinson FACS as described previously (24). An argon laser rescence loss as a function of the overall concentration of BP provided mixed 350-nm/360-nm excitation to the cell stream. BP in the system, at several different cell densities. Lineweaver- fluorescence was measured using a 10-nm bandpass filter with center Burk plots of the data (Chart 1,4) reveal that the cell density frequency of 405 nm (Ditric Optics, Hudson, Mass.). strongly influences both the Vmaxand the apparent Km of the Measurement of Cell Size. Cell size was determined (32) using a reaction. For example, at a cell density of 8 x 10" cells/ml, Model ZBI Coulter Counter (Coulter Electronics, Inc., Hialeah, Fla.). The instrument was calibrated using 19.72-fim polystyrene micro- these measurements indicate a Vmaxof 2.7 pmol/ml/min and spheres, which have a diameter similar to that of the cells analyzed. an apparent Km of 7.8 nw; in contrast, experiments performed at a higher cell density (2 x 105 cells/ml) reveal a Vma)lof 6.3 Fluorescence Measurements. Fluorescence was measured on a Perkin-Elmer Model 512 fluorescence spectrophotometer in a pmol/ml/min and an apparent Km of 14 nM. Thus, not only darkened room. The cuvet holder was maintained at 37°, and cell does the Vmaxfor BP disappearance increase with increasing suspensions were mixed periodically by gentle pipeting. PAHs were cell density, as expected, but so does the apparent Km. dissolved in acetone for addition to cell suspensions; the final concen BP is very lipophilic, and it seemed likely that the partitioning tration of acetone never exceeded 0.5%. At this concentration, acetone of BP into cells from the aqueous medium could influence these did not affect enzyme activity. BP fluorescence was measured using kinetic measurements. In studies involving membrane-bound the 406-nm emission peak and a 360-nm excitation frequency. The enzymes and lipophilic substrates, other investigators have excitation frequency was chosen to coincide with the UV excitation frequency of the FACS laser. BP fluorescence, measured in this way, found that binding and kinetic parameters are affected by the was not affected by the change in environment associated with passive amount of membrane in the assay (10, 22). Such effects can uptake of BP by cells. BP fluorescence was linearly related to concen be explained by a model which accounts for partitioning of the tration in all studies described here. Cells were assayed in PBS to substrate between membranes and the aqueous phase (31 ). minimize background fluorescence. At the wavelengths used to mea We have analyzed our data in a similar fashion, by considering sure BP fluorescence, the background fluorescence of cells suspended the partitioning of BP between cells and the aqueous extracel in PBS was equal to the fluorescence of 1.5 nM BP in PBS. This lular phase. The effect of cell density on the apparent Km for background fluorescence did not change with time at either 0 or 37°. BP metabolism can be eliminated by extrapolation to zero cell BP Disappearance Assay. BP fluorescence in cell suspensions or density.
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