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A2u-Globulin Mrna (Transcriptional Control/Steroid Hormone Action/Mediator Protein) CHING-LING C

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A2u-Globulin Mrna (Transcriptional Control/Steroid Hormone Action/Mediator Protein) CHING-LING C Proc. Nati. Acad. Sci. USA Vol. 76, No. 6, pp. 2669-2673, June 1979 Biochemistry Cycloheximide inhibition of hormonal induction of a2u-globulin mRNA (transcriptional control/steroid hormone action/mediator protein) CHING-LING C. CHEN AND PHILIP FEIGELSON Institute of Cancer Research and Department of Biochemistry, College of Physicians and Surgeons, Columbia University, New York, New York 10032 Communicated by Seymour Lieberman, March 19, 1979 ABSTRACT The induction of hepatic a2u-globulin synthesis methasone-induced hepatocytes comigrated in sodium dodecyl by glucocorticoids in isolated hepatocytes occurs via an increase sulfate (NaDodSO4)/polyacrylamide gels with authentic in the level of its mRNA as measured by cell-free translation and 20,000-dalton a2u-globulin. However, these dexamethasone- by hybridization to an a2u-globulin cDNA probe. To explore whether induction of this mRNA is a direct or an indirect con- induced hepatocytes, presumably through a hormonally evoked sequence of the interaction of the dexamethasone-receptor posttranslational modification, secrete into the suspension complex with the a2u-globulin genome, the requirement for medium two high molecular weight glycosylated forms of ongoing protein synthesis was examined. Concentrations of a2u-globulin (12). cycloheximide too low to prevent precursor incorporation into The induction of a2u-globulin mRNA by glucocorticoids total poly(A).containing RNA do prevent the hormonal induction manifests a lag of approximately 2 hr (12). This characteristic of a2u-globulin mRNA. Furthermore, incorporation of 3H- lag between glucocorticoid administration and a2u-globulin labeled amino acids into total protein was decreased by only mRNA induction seems longer than might be expected as a 40-50%, and the appearance of the dexamethasone-induced glycosylated forms of a2u-globulin was completely prevented consequence of a direct interaction between glucocorticoid- in these cycloheximide-treated hepatocytes. The results suggest receptor complex and chromatin. A question thus arises as to that the synthesis of a protein mediator(s) may be required for whether intervening events must precede the induction of the induction of a2u-globulin mRNA by glucocorticoids and that a2u-globulin mRNA in these cells. the steroid-receptor complex may not interact directly with the It has recently been found that glucocorticoid induction of a2u-globulin genome. rat liver tryptophan oxygenase mRNA in vivo is largely pre- vented if the rats are pretreated with protein synthesis inhibitors a2u-Globulin is present in the urine of male rats but not in the such as cycloheximide 30 min before hydrocortisone adminis- urine of female rats (1). This protein, which is synthesized in tration (13). These results suggest that the synthesis of inter- the parenchymal cells of male rat liver and represents ap- mediate protein(s) may be required for the induction of tryp- proximately 1% of hepatic protein synthesis, is secreted into the tophan oxygenase mRNA by glucocorticoids. A similar effect serum and excreted in the urine (2-4). In this laboratory, it has of protein synthesis inhibitors upon the hormonal induction of been shown that the in vivo regulation of the synthesis of this other specific mRNAs, such as ovalbumin and conalbumin, has protein by glucocorticoids (5), thyroid hormones (6), and an- been reported (14). To study whether the induction of a2u- drogens (7) occurs via modulation of the level of hepatic mRNA globulin mRNA by glucocorticoids requires a protein mediator, coding for ct2u-globulin, whereas pituitary growth hormone in vitro experiments were performed with hepatocyte sus- stimulates the synthesis of this protein translationally (8). pensions under carefully controlled experimental conditions. A hepatocyte suspension system that permits the study of hormonal control of (t2u-globulin synthesis under defined MATERIALS AND METHODS conditions in vitro has been developed (9, 10). Isolated hepa- Preparation and Incubation of Hepatocytes. Male tocytes synthesize and secrete (a2u-globulin and other hepatic Sprague-Dawley rats (280-320 g) were castrated and then, 14 proteins in vitro at an approximately linear rate throughout 30 days later, hepatocytes were prepared by a modified procedure hr of incubation. Hepatocytes isolated from animals in different of Seglen (9) involving the removal of Ca2+ from the liver fol- endocrine states synthesize a2u-globulin in vitro at rates con- lowed by recirculating perfusion with collagenase. The liver sistent with the hormonal effects upon its in vivo biosynthesis was then immediately flushed with calcium- and magne- (11). sium-free Hanks' balanced salt solution as described (11, 12). Increased synthesis of oau-globulin can be induced in vitro The liver cells were isolated, washed, and counted in a hemo- by addition of glucocorticoids to hepatocytes derived from male cytometer; viability was defined as the exclusion of trypan blue rats in which the rate of synthesis of this protein had been de- dye. The yield of cells was 7-9 X 108 cells per liver with viability pressed by adrenalectomy, castration, or estrogen pretreatment of greater than 90%. (11). The induction of (2,,-globulin synthesis by dexamethasone In a typical experiment for measuring the rate of total protein in such hepatocytes is highly specific and occurs by selective or a2u-globulin synthesis, 15 X 106 viable cells were suspended increase of aou-globulin mRNA in these cells, as measured by in 10 ml of Joklik-modified minimal essential medium (GIBCO) a wheat germ cell-free translational system and by hybridiza- containing 25 mM Hepes at pH 7.5 and 10% (vol. vol) fetal calf tion to a o2,1-globulin cDNA probe (12). The induced intra- serum (GIBCO). For mRNA studies, a large quantity of cells cellular (YoU-globulin or the translation product generated in was required to permit isolation of sufficient RNA. Cell sus- the wheat germ system using mRNA isolated from the dexa- pensions (50 ml containing 2.5-3.0 X 106 viable cells per ml) were incubated in 250-ml polypropylene flasks as described The publication costs of this article were defrayed in part by page above at 37°C under 95% 02/5% CO2 (11, 12). Hormones, in- charge payment. This article must therefore be hereby marked "ad- hibitors, or labeled precursors were added as indicated. vertisement' in accordance with 18 U. S. C. §1734 solely to indicate this fact. Abbreviation: NaDodSO4, sodium dodecdl sulfate. 2669 Downloaded by guest on October 1, 2021 2670 Biochemistry: Chen and Feigelson Proc. Natl. Acad. Sci. USA 76 (1979) Labeling of Hepatocytes. To determine the rate of synthesis and measurement of the amount of radioactivity in the aY2u- of total hepatic proteins or a2u-globulin, 15 X 106 hepatocytes globulin on the gel (6, 12). were incubated as described above. Dexamethasone or cyclo- heximide was added as indicated. After 8 hr of incubation, the RESULTS cells were washed and resuspended in leucine- and lysine-free To investigate the role of protein synthesis in a2u-globulin joklik-modified minimal essential medium containing 25 yCi mRNA induction by dexamethasone, experiments were per- (1 Ci = 3.7 X 1010becquerels) each of [3H]leucine and [3H]- formed with the protein synthesis inhibitor cycloheximide. A lysine per ml with dexamethasone and cycloheximide as indi- concentration of cycloheximide low enough to interfere only cated. The cells were chilled and harvested after 30 min of minimally with endogenous RNA synthesis was sought. precursor incorporation. Therefore, the effect of various levels of cycloheximide on total To evaluate the rate of synthesis of hepatic RNA, liver cells hepatocyte protein and RNA synthesis was studied. The degree (150 X 106) were incubated for 8 hr in the standard medium of inhibition of protein synthesis by cycloheximide increased supplemented with hormone or inhibitor as indicated. The cells as the concentration of this inhibitor was increased. Hepatocyte were collected, resuspended in fresh medium containing hor- RNA synthesis was affected to a lesser degree at each level of mone or inhibitor, and pulse-labeled with ['4C]orotic acid (2.5 cycloheximide (Fig. 1). Some decrease in total RNA synthesis ttCi/ml) for 60 min. was expected because this inhibitor is known to cause a decrease Determination of Total Hepatic Protein and a2u-Globulin in RNA polymerase I transcription of nucleolar ribosomal DNA Synthesis. Liver cells labeled with [3H]leucine and [3H]lysine (18, 19). were harvested and lysed by sonication and detergent treatment The effect of cycloheximide on intracellular ca2u-globulin (1% Triton X-100/1% sodium deoxycholate) (11, 12). The synthesis and the endogenous level of functional a2u-globulin 3H-labeled cell cytosols were prepared by centrifugation at mRNA in these cells was also studied. Increasing concentrations 105,000 X g for 60 min. Incorporation into total protein was of cycloheximide resulted in progressively decreased a2u-glo- measured by applying 1O0Ul of 3H-labeled cytosol onto What- bulin synthesis in hepatocytes. Cycloheximide caused negligible man 3MM filter paper discs that were immersed in 10% tri- loss of translatable a2u-globulin mRNA. Thus, although the chloroacetic acid containing 10 mM unlabeled amino acids and intracellular synthesis of ao2u-globulin and total protein were processed as described (11, 12). greatly inhibited as the concentration of cycloheximide in- The newly synthesized a2u-globulin was isolated by immu- creased, the translational levels of endogenous
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