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Enhancement of Malignant Transformation of C3H Mouse Fibroblasts and Growth Stimulation of Primary Rat Hepatocytes1

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Enhancement of Malignant Transformation of C3H Mouse Fibroblasts and Growth Stimulation of Primary Rat Hepatocytes1 (CANCER RESEARCH 50. 6540-6544. October 15. 1990] Hydroxyanthraquinones as Tumor Promoters: Enhancement of Malignant Transformation of C3H Mouse Fibroblasts and Growth Stimulation of Primary Rat Hepatocytes1 Detlef NVölfle,2ChristophSchmutte, Johannes Westendorf, and Hans Marquardt Department of Toxicology, L'nirersity of Hamburg Medical School, D-2001) Hamburg 13, Federal Republic of Germany ABSTRACT discrepancy has been discussed (5). Since the mouse strain used in the in vivo experiments had a relatively high incidence of Because danthron, though carcinogenic, does not seem to be genotoxic, spontaneous hepatomas, the results do not support an initiating it and 8 other hydroxyanthraquinones were comparatively investigated activity of danthron in the liver. for activities associated with tumor promotion, such as stimulation of cell Nongenotoxic carcinogens often possess tumor-promoting proliferation and enhancement of malignant transformation. The in vivo treatment of primary rat hepatocytes with danthron, aloe-emodin, chry- activity (10-13). Fundamental characteristics of promoting sophanol, and rhein resulted in a 2-3-fold increase of D.NA synthesis, agents are the modulation of growth control (14-16) and dif lucidin and purpurin were less active, and emodin, purpuroxanthin, and ferentiation (16). In experimental hepatocarcinogenesis, tumor alizarin were essentially inactive. In addition, danthron, rhein, and chry- promotion can be achieved: (a) by cytotoxins that stimulate sophanol (preliminary data), but not alizarin, enhanced transformation of regenerate growth of toxin-resistant cells (17); or (b) by chronic C3H/M2 mouse fibroblasts initiated by /V-methyl-A''-nitro-A'-nitroso- administration of mitogens without toxic effects, i.e., inducers guanidine or 3-methylcholanthrene. The results of these in vitro studies of drug-metabolizing enzymes, peroxisome proliferators, or suggest that hydroxyanthraquinones, possessing 2 hydroxy groups in the hormones (14). Therefore, stimulation of growth/DNA synthe 1,8-positions, e.g., danthron, rhein, and chrysophanol, may have tumor- sis in vivo and in vitro is widely believed to be a reliable assay promoting activities. This conclusion is in accordance with the hypothesis for tumor-promoting activity of chemicals (15). Further evi that the in vivo carcinogenic activity of danthron may be associated with dence for a tumor-promoting capacity of chemicals can be tumor promotion. obtained in vitro by assaying the capacity to enhance malignant transformation of initiated fibroblasts (18). In this report, we INTRODUCTION investigated, therefore, the ability of nongenotoxic HA to en HA3 are synthetic (i.e., danthron) or naturally occurring hance malignant transformation in vitro and to stimulate the growth of primary rat hepatocytes. The significance of the structurally related compounds that are the active principle of results with regard to HA being tumor promoters is discussed. many phytotherapeutic drugs. HA are often used chronically as laxatives (aloe, senna, frángula,and rheum; Ref. 1) or as mild sedatives (Hypericum perforatum: Ref. 2). HA are also applied MATERIALS AND METHODS for the treatment of kidney and bladder stones (Rubia tincto- Animals. Male Wistar rats (Zentralinstitut fürVersuchstierkunde, rum; Ref. 3). Previously, the mutagenic activity of various HA Hannover, Federal Republic of Germany) were fed a standard diet has been demonstrated in Salmonella typhimurium with a spe (Altromin; Lage, Federal Republic of Germany) and water ad libitum. cial sensitivity of the strain TA 1537 (4-6). Because of the They were housed under controlled conditions. unexplained particular susceptibility of this Salmonella strain, Chemicals. The following test compounds were purchased from the the significance of these findings in the bacterial assay with indicated companies: MNNG and TPA (Sigma. Munich, Federal Re respect to a human carcinogenic risk remains questionable. public of Germany): MCA (Eastman Organic Chemicals, Rochester, However, evidence for the mutagenicity of HA was also ob NY); danthron (1,8-dihydroxyanthraquinone; EGA-Chemie, Stein- tained in mammalian test systems, i.e., the V79 mutation assay heim. Federal Republic of Germany): purpurin and chrysophanic acid and the hepatocyte/DNA repair test (5-7). Recently, genotoxic (Aldrich-Chemie, Steinheim. Federal Republic of Germany); (aloe- HA were also found to transform mouse fibroblasts (5, 6). emodin. emodin, and rhein (Roth, Karlsruhe. Federal Republic of Germany); and purpuroxanthin and lucidin (synthesized in our labo Moreover, the chronic administration of danthron resulted in ratory; Ref. 6). The compounds were routinely checked for purity by the induction of intestinal tumors in rats and mice and hepa- high-performance liquid Chromatographie analysis and only accepted tocellular carcinomas in mice (8, 9). The mechanism of the for experiments if the purity was >99%. ['HjThymidine (specific activ danthron-induced tumor formation is poorly understood be ity, 40 mCi/mmol) and NTB-2 emulsion were obtained from Amersham cause this agent was found by us to be essentially negative in Buchler (Braunschweig, Federal Republic of Germany) and from East genotoxicity tests with mammalian cells (5). It should be noted man Kodak (Rochester, NY), respectively. that Mori et al. (7), in contrast to our results, reported an Malignant Transformation of C3H/M2 Mouse Fibroblasts in Vitro. induction of unscheduled DNA synthesis by danthron; this This assay was carried out as described previously (19) and adjusted to measure tumor promotion according to procedures described (20). Briefly, cells harvested from logarithmically growing stock cultures Received 4/10/90: accepted 7/13/90. (between passages 5 and 20) were plated on day 0 in basal Eagle's The costs of publication of this article were defrayed in part by the payment medium supplemented with 10% fetal calf serum into 60-mm dishes to of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. determine their plating efficiency (100 cells/dish) and the transforma 1Supported in part by the Deutsche Forschungsgemeinschaft (We 980/2-1) tion rate (1000 cells/dish). After 24 h, the cultures were treated for 24 and Roggenbuckstiftung zur Krebshilfe. h with initiating agents, i.e., MNNG (0.1 ^g/ml), MCA (1 ^g/ml), or J To whom requests for reprints should be addressed, at Department of solvent control, dimethyl sulfoxide (0.5%). Thereafter, the medium was Toxicology. University of Hamburg Medical School. Grindelallee 117. D-2000 renewed and the cells were allowed to grow in fresh medium. Beginning Hamburg 13. Federal Republic of Germany. ' The abbreviations used are: HA. hydroxyanthraquinones: MCA, 3-methyl on day 5 until the end of the experiment, with each of the (twice- cholanthrene; MNNG, A'-methyl-iV'-nitro-A'-nitrosoguanidine. weekly) medium renewals HA; the positive control, i.e., TPA (0.25 ug/ 6540 Downloaded from cancerres.aacrjournals.org on September 26, 2021. © 1990 American Association for Cancer Research. HVDROXYANTHRAQUINONES AS TUMOR PROMOTERS ml); or solvent were added. The cells were fixed and stained after 2 a slight viability loss, failed to promote the transformation of weeks (to determine their plating efficiency) or after 8 weeks (to initiated cells. determine the transformation yield). DNA Synthesis in Primary Rat Hepatocytes. The effect of DNA Synthesis in Primary Rat Hepatocytes. Rat hepatocytes were HA on DNA synthesis was studied in serum-free cultures of isolated by collagenase perfusion and plated at a final density of 10,000 cells/cm2 as described previously (21). After cell attachment, i.e., 2 h adult rat hepatocytes. As shown in Fig. 1, addition of danthron after plating, serum-free William's medium E, supplemented with in to the culture medium stimulated the incorporation of ['H] sulin (10"' M) and dexamethasone (10~7 M), was added containing HA thymidine into hepatocellular DNA by a factor of about 3 (dissolved in dimethyl sulfoxide at a final media concentration of (determined by liquid scintillation counting). Concentrations of 0.25%) or solvent. Epidermal growth factor (20 ng/ml) was added at 24 h after plating. [3H]Thymidine was added at 40 h after plating. To danthron higher than 10 ng/m\ resulted in cytotoxic effects measure DNA synthesis by liquid scintillation counting, cultures were leading to the detachment of cells. In order to distinguish allowed to grow in the presence of [3H]thymidine (0.5 ^Ci/dish) for 4 between replicative and repair synthesis, hepatocytes were cul h and were thereafter processed to determine the radioactivity of tured in the presence and absence of hydroxyurea (10 mivi). trichloroacetic acid-precipitable material as described previously (22). Hydroxyurea inhibited [3H]thymidine incorporation by 90% To determine DNA synthesis by autoradiography, cells were grown on and prevented the stimulating effect of danthron (Fig. 1). Thus, collagen-coated coverslips for 8 h in the presence of [3H]thymidine (1 the observed stimulation of DNA synthesis by danthron is not jiCi/dish), then washed and fixed with 4% buffered formalin and dipped in NTB-2 emulsion. After 12 days of exposure, the coverslips were due to the induction of DNA repair. developed (23). In further studies with hepatocyte cultures, we examined the effect of various HA on the DNA synthesis in primary rat hepatocytes (Fig. 2). Chrysophanol, aloe-emodin, danthron, and rhein were the
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