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. 1985 Sep;4(9):2209–2215. doi: 10.1002/j.1460-2075.1985.tb03916.x

Activation of putative transposition intermediate formation in tumor cells.

M S Grigoryan, D A Kramerov, E M Tulchinsky, E S Revasova, E M Lukanidin
PMCID: PMC554487  PMID: 2416560

Abstract

The transcription levels of two families of mouse repetitive elements namely intracisternal A particle (IAP) genes, and B2 sequences were analyzed in different tumor cells and normal tissues. These sequences belong to two major classes of mobile elements present in the mouse genome. The Northern blots containing poly(A) + RNAs from tumor cells and normal tissues were hybridized to the cloned IAP gene and B2 sequence. The content of IAP gene transcripts in tumor cells is much higher than in normal cells. A 10- to 100-fold difference was found. The predominant IAP-gene specific RNAs in all investigated tumor cells were 9.5, 6.8 and 5.3 kb long. Additional RNA species were found in some of the tumors. The active synthesis of small cytoplasmic B2 RNA transcribed by RNA polymerase III was also detected in most tumor cells tested. Usually it was higher than in normal cells. Free closed circular DNAs hybridizing to IAP gene probes were cloned from Ehrlich ascites carcinoma cells. We speculate that the data obtained indicate the enhanced transposition of mobile elements in tumor cells which may be an important factor of tumor progression.

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  1. Alwine J. C., Kemp D. J., Parker B. A., Reiser J., Renart J., Stark G. R., Wahl G. M. Detection of specific RNAs or specific fragments of DNA by fractionation in gels and transfer to diazobenzyloxymethyl paper. Methods Enzymol. 1979;68:220–242. doi: 10.1016/0076-6879(79)68017-5. [DOI] [PubMed] [Google Scholar]
  2. Alwine J. C., Kemp D. J., Stark G. R. Method for detection of specific RNAs in agarose gels by transfer to diazobenzyloxymethyl-paper and hybridization with DNA probes. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5350–5354. doi: 10.1073/pnas.74.12.5350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Arkhipova I. R., Gorelova T. V., Ilyin Y. V., Schuppe N. G. Reverse transcription of Drosophila mobile dispersed genetic element RNAs: detection of intermediate forms. Nucleic Acids Res. 1984 Oct 11;12(19):7533–7548. doi: 10.1093/nar/12.19.7533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Biczysko W., Pienkowski M., Solter D., Koprowski H. Virus particles in early mouse embryos. J Natl Cancer Inst. 1973 Sep;51(3):1041–1050. doi: 10.1093/jnci/51.3.1041. [DOI] [PubMed] [Google Scholar]
  5. Calarco P. G., Szollosi D. Intracisternal A particles in ova and preimplantation stages of the mouse. Nat New Biol. 1973 May 16;243(124):91–93. [PubMed] [Google Scholar]
  6. Cameron J. R., Loh E. Y., Davis R. W. Evidence for transposition of dispersed repetitive DNA families in yeast. Cell. 1979 Apr;16(4):739–751. doi: 10.1016/0092-8674(79)90090-4. [DOI] [PubMed] [Google Scholar]
  7. Canivet M., Lasneret J., Dianoux L., Roseto A., Peries J. Distribution of intracisternal A particles in mouse teratocarcinoma-derived cell lines. Eur J Cancer. 1980 May;16(5):609–615. doi: 10.1016/0014-2964(80)90200-5. [DOI] [PubMed] [Google Scholar]
  8. Cole M. D., Ono M., Huang R. C. Intracisternal A-particle genes: structure of adjacent genes and mapping of the boundaries of the transcriptional unit. J Virol. 1982 Apr;42(1):123–130. doi: 10.1128/jvi.42.1.123-130.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cole M. D., Ono M., Huang R. C. Terminally redundant sequences in cellular intracisternal A-particle genes. J Virol. 1981 May;38(2):680–687. doi: 10.1128/jvi.38.2.680-687.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Doerfler W. DNA methylation--a regulatory signal in eukaryotic gene expression. J Gen Virol. 1981 Nov;57(Pt 1):1–20. doi: 10.1099/0022-1317-57-1-1. [DOI] [PubMed] [Google Scholar]
  11. Finnegan D. J., Rubin G. M., Young M. W., Hogness D. S. Repeated gene families in Drosophila melanogaster. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):1053–1063. doi: 10.1101/sqb.1978.042.01.106. [DOI] [PubMed] [Google Scholar]
  12. Georgiev G. P., Ilyin Y. V., Chmeliauskaite V. G., Ryskov A. P., Kramerov D. A., Skryabin K. G., Krayev A. S., Lukanidin E. M., Grigoryan M. S. Mobile dispersed genetic elements and other middle repetitive DNA sequences in the genomes of Drosophila and mouse: transcription and biological significance. Cold Spring Harb Symp Quant Biol. 1981;45(Pt 2):641–654. doi: 10.1101/sqb.1981.045.01.082. [DOI] [PubMed] [Google Scholar]
  13. Georgiev G. P. Mobile genetic elements in animal cells and their biological significance. Eur J Biochem. 1984 Dec 3;145(2):203–220. doi: 10.1111/j.1432-1033.1984.tb08541.x. [DOI] [PubMed] [Google Scholar]
  14. Hirt B. Selective extraction of polyoma DNA from infected mouse cell cultures. J Mol Biol. 1967 Jun 14;26(2):365–369. doi: 10.1016/0022-2836(67)90307-5. [DOI] [PubMed] [Google Scholar]
  15. Hojman-Montes de Oca F., Dianoux L., Peries J., Emanoil-Ravicovitch R. Intracisternal A particles: RNA expression and DNA methylation in murine teratocarcinoma cell lines. J Virol. 1983 Apr;46(1):307–310. doi: 10.1128/jvi.46.1.307-310.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ilyin Y. V., Tchurikov N. A., Ananiev E. V., Ryskov A. P., Yenikolopov G. N., Limborska S. A., Maleeva N. E., Gvozdev V. A., Georgiev G. P. Studies on the DNA fragments of mammals and Drosophila containing structural genes and adjacent sequences. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):959–969. doi: 10.1101/sqb.1978.042.01.097. [DOI] [PubMed] [Google Scholar]
  17. Jagadeeswaran P., Forget B. G., Weissman S. M. Short interspersed repetitive DNA elements in eucaryotes: transposable DNA elements generated by reverse transcription of RNA pol III transcripts? Cell. 1981 Oct;26(2 Pt 2):141–142. doi: 10.1016/0092-8674(81)90296-8. [DOI] [PubMed] [Google Scholar]
  18. Kominami R., Muramatsu M., Moriwaki K. A mouse type 2 Alu sequence (M2) is mobile in the genome. Nature. 1983 Jan 6;301(5895):87–89. doi: 10.1038/301087a0. [DOI] [PubMed] [Google Scholar]
  19. Kramerov D. A., Grigoryan A. A., Ryskov A. P., Georgiev G. P. Long double-stranded sequences (dsRNA-B) of nuclear pre-mRNA consist of a few highly abundant classes of sequences: evidence from DNA cloning experiments. Nucleic Acids Res. 1979 Feb;6(2):697–713. doi: 10.1093/nar/6.2.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kramerov D. A., Lekakh I. V., Samarina O. P., Ryskov A. P. The sequences homologous to major interspersed repeats B1 and B2 of mouse genome are present in mRNA and small cytoplasmic poly(A) + RNA. Nucleic Acids Res. 1982 Dec 11;10(23):7477–7491. doi: 10.1093/nar/10.23.7477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kramerov D. A., Tillib S. V., Lekakh I. V., Ryskov A. P., Georgiev G. P. Biosynthesis and cytoplasmic distribution of small poly(A)-containing B2 RNA. Biochim Biophys Acta. 1985 Feb 20;824(2):85–98. doi: 10.1016/0167-4781(85)90084-3. [DOI] [PubMed] [Google Scholar]
  22. Krayev A. S., Markusheva T. V., Kramerov D. A., Ryskov A. P., Skryabin K. G., Bayev A. A., Georgiev G. P. Ubiquitous transposon-like repeats B1 and B2 of the mouse genome: B2 sequencing. Nucleic Acids Res. 1982 Dec 11;10(23):7461–7475. doi: 10.1093/nar/10.23.7461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kuff E. L., Feenstra A., Lueders K., Rechavi G., Givol D., Canaani E. Homology between an endogenous viral LTR and sequences inserted in an activated cellular oncogene. Nature. 1983 Apr 7;302(5908):547–548. doi: 10.1038/302547a0. [DOI] [PubMed] [Google Scholar]
  24. Kuff E. L., Feenstra A., Lueders K., Smith L., Hawley R., Hozumi N., Shulman M. Intracisternal A-particle genes as movable elements in the mouse genome. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1992–1996. doi: 10.1073/pnas.80.7.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kuff E. L., Leuders K. K., Ozer H. L., Wivel N. A. Some structural and antigenic properties of intracisternal A particles occurring in mouse tumors (complement fixation-immunodiffusion-neuroblastoma-plasma-cell tumor). Proc Natl Acad Sci U S A. 1972 Jan;69(1):218–222. doi: 10.1073/pnas.69.1.218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kuff E. L., Smith L. A., Lueders K. K. Intracisternal A-particle genes in Mus musculus: a conserved family of retrovirus-like elements. Mol Cell Biol. 1981 Mar;1(3):216–227. doi: 10.1128/mcb.1.3.216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lasneret J., Canivet M., Hojman-Montes de Oca F., Tobaly J., Emanoil-Ravicovitch R., Peries J. Activation of intracisternal a particles by 5-azacytidine in mouse Ki-BALB cell line. Virology. 1983 Jul 30;128(2):485–489. doi: 10.1016/0042-6822(83)90275-1. [DOI] [PubMed] [Google Scholar]
  28. Lehrach H., Diamond D., Wozney J. M., Boedtker H. RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical reexamination. Biochemistry. 1977 Oct 18;16(21):4743–4751. doi: 10.1021/bi00640a033. [DOI] [PubMed] [Google Scholar]
  29. Lueders K. K., Kuff E. L. Intracisternal A-particle genes: identification in the genome of Mus musculus and comparison of multiple isolates from a mouse gene library. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3571–3575. doi: 10.1073/pnas.77.6.3571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lueders K. K., Kuff E. L. Sequences associated with intracisternal A particles are reiterated in the mouse genome. Cell. 1977 Dec;12(4):963–972. doi: 10.1016/0092-8674(77)90161-1. [DOI] [PubMed] [Google Scholar]
  31. Maxam A. M., Gilbert W. A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977 Feb;74(2):560–564. doi: 10.1073/pnas.74.2.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Ono M., Ohishi H. Long terminal repeat sequences of intracisternal A particle genes in the Syrian hamster genome: identification of tRNAPhe as a putative primer tRNA. Nucleic Acids Res. 1983 Oct 25;11(20):7169–7179. doi: 10.1093/nar/11.20.7169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Razin A., Riggs A. D. DNA methylation and gene function. Science. 1980 Nov 7;210(4470):604–610. doi: 10.1126/science.6254144. [DOI] [PubMed] [Google Scholar]
  34. Robertson D. L., Baenziger N. L., Dobbertin D. C., Thach R. E. Characterization of DNA polymerase and RNA associated with A-type particles from murine myeloma cells. J Virol. 1975 Feb;15(2):407–415. doi: 10.1128/jvi.15.2.407-415.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rosen J. M., Woo S. L., Holder J. W., Means A. R., O'Malley B. W. Preparation and preliminary characterization of purified ovalbumin messenger RNA from the hen oviduct. Biochemistry. 1975 Jan 14;14(1):69–78. doi: 10.1021/bi00672a012. [DOI] [PubMed] [Google Scholar]
  36. Ryskov A. P., Ivanov P. L., Kramerov D. A., Georgiev G. P. Mouse ubiquitous B2 repeat in polysomal and cytoplasmic poly(A)+RNAs: uniderectional orientation and 3'-end localization. Nucleic Acids Res. 1983 Sep 24;11(18):6541–6558. doi: 10.1093/nar/11.18.6541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Shen-Ong G. L., Cole M. D. Differing populations of intracisternal A-particle genes in myeloma tumors and mouse subspecies. J Virol. 1982 May;42(2):411–421. doi: 10.1128/jvi.42.2.411-421.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  39. Williams J. G., Hoffman R., Penman S. The extensive homology between mRNA sequences of normal and SV40-transformed human fibroblasts. Cell. 1977 Aug;11(4):901–907. doi: 10.1016/0092-8674(77)90301-4. [DOI] [PubMed] [Google Scholar]
  40. Wivel N. A., Smith G. H. Distribution of intracisternal A-particles in a variety of normal and neoplastic mouse tissues. Int J Cancer. 1971 Jan 15;7(1):167–175. doi: 10.1002/ijc.2910070119. [DOI] [PubMed] [Google Scholar]
  41. Wong-Staal F., Reitz M. S., Jr, Trainor C. D., Gallo R. C. Murine intracisternal type A particles: a biochemical characterization. J Virol. 1975 Oct;16(4):887–896. doi: 10.1128/jvi.16.4.887-896.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]

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