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Detection and Analysis of Cancer Genes Amplified from Bone Material of a Scythian Royal Burial in Arzhan Near Tuva, Siberia

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Detection and Analysis of Cancer Genes Amplified from Bone Material of a Scythian Royal Burial in Arzhan Near Tuva, Siberia ANTICANCER RESEARCH 27: 4117-4120 (2007) Detection and Analysis of Cancer Genes Amplified from Bone Material of a Scythian Royal Burial in Arzhan Near Tuva, Siberia THILO SCHLOTT1, HELMUT EIFFERT2, TYEDE SCHMIDT-SCHULTZ3, MELANIE GEBHARDT4, HERMANN PARZINGER5 and MICHAEL SCHULTZ6 1Department of Pathology, 2Department of Medical Microbiology, 3Department of Biochemistry, 4Department of Gastroenteropathology, 6Department of Anatomy; Georg August Universitaet, Goettingen; 5German Archaeological Institute (DAI), Berlin, Germany Abstract. Molecular paleopathology has become an emerging be suitable for investigation using complex and comprehensive field that helps to characterize molecular markers of past genotyping techniques (3). Encouraged by all these facts, a pilot disease. Especially highly sensitive genetic techniques such as study with bone material from a Scythian burial (4) was PCR are an important means of unraveling changes in ancient performed, in order to test whether ancient DNA is suited to DNA extracted from bone tissue, teeth and mummified soft characterization of the genes involved in carcinogenesis and to tissue. In the present study, excavated bone material from the tumoripathological problems analysis. skeleton of a Scythian sovereign, morphologically and immunohistochemically suspicious of a metastatic prostate Materials and Methods carcinoma, was analyzed by PCR for amplifiable human gene sequences. Short sequences of the human GADD153 DNA Bone material. A compact bone sample was taken from the left femur of the male of burial no. 5 from the royal tumulus (kurgan) repair gene and p53 tumor suppressor gene were detectable of Arzhan II near Tuva, Siberia (Russia). which revealed the absence of mutations according to the data of automatic sequencing. Using bisulfite-treated DNA from the DNA extraction. DNA was extracted from 2 g of pulverized bone bone, methylation-specific PCR detected hypermethylated material with the QIAamp DNA Mini Kit (Qiagen, Hilden, promoter sequences of the p14ARF tumor suppressor gene. In Germany) according to the manufacturer’s instructions with the summary, these data show that it is possible: a) to amply short following modifications. The specimen was incubated in 5 ml buffer human DNA stretches from 2,500-year-old bone material, b) to for 4 days at 55ÆC, with the addition of fresh protease every day to increase the DNA yield. The DNA eluted with 400 Ìl double- detect tumorigenetically important genes within this DNA, c) to distilled H2O was mixed with 400 Ìl isopropanol and incubated for detect epigenetically modified DNA in ancient bone material. 60 min at room temperature (RT). The precipitated DNA was The finding of hypermethylated p14ARF sequences merits collected by centrifuging the solution for 60 min at 14,000 xg attention because this may indicate an intraosseal neoplastic (Heraeus Biofuge 15, Germany) and washed with 100 Ìl ethanol process and may corroborate the hypothesis of prostate cancer. (96%). The tubes were incubated at RT for 10 min with the lids open. Afterwards the DNA pellet was carefully dissolved in 40 Ìl In paleopathology and anthropology, analysis of ancient DNA double-distilled H2O at 50ÆC for 10 min. has become an intriguing approach that not only focuses on Detection and sequencing of p53 and GADD153 gene sequences. The human samples but also on samples from animals such as primers used for amplification of p53 exon 7 were 5’-AGG GGT horses and bears (1, 2). Despite all the technical limitations in CAG CGG CAA GCA GA-3’ (antisense primer) and 5’-CTT GCC this field of research, the increasing number of publications ACA GGT CTC CCC AA-3’ (sense primer). These primers yielded emphasizes the scientific value of ancient DNA which seems to a 237 bp fragment. The primers used for amplification of GADD153 sequences were 5’-AGATGTGCTTTTCCAGACTG-3’ (sense primer) and 5’-TCCAGGAGGTGAAACATAG-3’ (antisense primer). The primer combination yielded a 163 bp Correspondence to: Dr. Thilo Schlott, Buerger Street 20, 37073 fragment. Both kinds of products were amplified using the Goettingen, Germany. Tel: +40 551 3077244, e-mail: thiloschlott@ following PCR conditions. Following an initial denaturing step at web.de 95ÆC for 15 min to activate HotStar Taq DNA polymerase, DNA was amplified 45 times in 3 temperature cycles. In each Key Words: Ancient DNA, bone, cancer genes, paleopathology. amplification series a 60-sec melting cycle at 95ÆC was followed by 0250-7005/2007 $2.00+.40 4117 ANTICANCER RESEARCH 27: 4117-4120 (2007) Figure 1. Detection of DNA sequences of the DNA repair gene GADD153 and tumor suppressor gene p53 in ancient bone material (inverse black- white presentation). The PCR fragments were not mutated according to Figure 2. Detection of hypermethylated sequences of tumor suppressor the data of automatic sequencing (data not shown). Lane A: size gene p14ARF in ancient bone material histologically and biochemically standard, lane B: GADD153 sequence, lane E: p53 exon 7 sequence. diagnosed as metastatic prostate carcinoma (arrow). Since hypermethylated p14ARF sequences usually indicate neoplastic processes, the data may support the histological diagnosis. Lane A: size standard, lane B: negative control, lane C: PCR with p14ARF primers specific for a combined annealing cycle for 60 sec at 58ÆC, and an extension nonmethylated promoter sequence, lane D: PCR with p14ARF primers cycle for 60 sec at 72ÆC. The final round was completed with a specific for methylated promoter sequence. primer extension for 7 min at 72ÆC. For visualization, 5 Ìl of each PCR assay (final volume 100 Ìl) was separated on a 3% (w/v) agarose gel containing 0.5 Ìg ethidium bromide per ml. The gel was photographed with a CCD camera (Biometra, Goettingen, absence of gene mutations in all fragments obtained (data Germany). p53 and GADD153 PCR products were separated on not shown). Furthermore, methylation-specific PCR 3% low-melting agarose (Biozym, Hameln, Germany) and cut from detected a hypermethylated p14ARF sequence in the the gel. The QIAEX II Gel Extraction Kit (QIAGEN, Hilden, sample (Figure 2). Germany) was used to purify the DNA. A total of 50 ng of isolated DNA was labeled with the PRISM Ready Dye Deoxy Terminator Discussion Cycle Sequencing Kit (Applied Biosystems, Weiterstadt, Germany) according to the manufacturer’s instructions, and analyzed in an Applied Biosystems DNA sequencer (model 310). The To our knowledge, this is the first study to analyze human oligonucleotides previously used for the amplification of fragments cancer genes in DNA extracted from ancient bones. The served as sequencing primers. Each p53 and GADD153 analysis data obtained are promising because they indicate that was repeated 3 times to guarantee reproducibility of data. ancient DNA is suitable for amplifying nucleotide sequences of genes (p53, GADD153) often involved in tumorigenesis Analysis of p14 promoter methylation. The DNA isolated from the and for detecting hypermethylated promoter sequences of bone was treated with sodium bisulfite using a CpGenome DNA tumor suppressor genes (p14ARF). Therefore, the findings Modification Kit (Intergen Company, Oxford, UK) according to the manufacturer’s instructions. Samples of 2 Ìl of modified DNA may open another door to the new field of (1/5 volume) were used for PCR amplification. ∆he primers were "tumorpaleopathology", especially since the bone samples p14ARF sense 5’-GTG TTA AAG GGC GGC GTA GC-3’ and analyzed were histologically and biochemically diagnosed as p14ARF antisense 5’-AAA ACC CTC ACT CGC GAC GA-3’ for metastatic prostate cancer (4). For the evaluation of the methylated sequences, p14ARF sense 5’-TTT TTG GTG TTA potential tumorigenic effects of the genetic features, it has AAG GGT GTA GT-3’ and p14ARF antisense 5’-CAC AAA AAC become clear that the role of the p53 and GADD153 CCT CAC TCA CAA CAA-3’ for non-methylated sequences. The sequences analyzed can be neglected because they were not PCR conditions for analysis of methylation status were described previously (5). The PCR fragments were separated on a 3 % mutated. In fact, even if mutations had been found, it would agarose gel. Each p14 methylation analysis was repeated 3 times to still have been unclear whether they had influenced the guarantee reproducibility of data. neoplastic change because other working groups have described "artifical" mutations induced in the PCR Results fragments by the enzyme itself during amplification (6) or by pre-existing miscoding lesions and damage to the DNA The data showed that sequences of the DNA repair gene (7). However, the finding of a hypermethylated p14ARF GADD153 and of the tumor suppressor p53 (exon 7) could promoter sequence proves that epigenetic changes of be amplified (Figure 1). Automatic sequencing revealed human DNA are preserved over long periods of time, if 4118 Schlott et al: Analysis of Cancer Genes in Excavated Bone there is no severe damage due to diagenesis, and may be 4 Schultz M, Parzinger H, Posdnjakov DV, Chikisheva TA and directly linked to the promotion of a neoplastic metastatic Schmidt-Schultz T: Oldest known case of metastasizing prostate process since a recent study indicated hypermethylated carcinoma diagnosed in the skeleton of a 2,700-year-old Scythioan king of Arzhan (Siberia, Russia). Int J Cancer 121: p14ARF in primary and metastatic prostate cancer (8). 2591-2595, 2007. The amplification of gene sequences from ancient DNA 5 Esteller M, Cordon-Cardo C, Corn PG, Meltzer SJ, Pohar KS, is still difficult to achieve and was
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