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. 1984 Aug;4(8):1561–1571. doi: 10.1128/mcb.4.8.1561

Most highly repeated dispersed DNA families in the mouse genome.

K L Bennett, R E Hill, D F Pietras, M Woodworth-Gutai, C Kane-Haas, J M Houston, J K Heath, N D Hastie
PMCID: PMC368948  PMID: 6208477

Abstract

The construction of a small library of mouse repetitive DNA has been previously reported (Pietras et al., Nucleic Acids Res. 11:6965-6983, 1983). Here we report that the 35 plasmids in this library corresponding to highly repeated (greater than 30,000 copies per genome) dispersed DNA sequences can be grouped into no more than 5 distinct families. These families together comprise 8 to 10% of the mouse genome. They include the previously described small elements B1, B2, and R and the large MIF-1 element. Twelve of the 35 clones contain evolutionarily conserved (EC) sequences. One EC clone in our library mostly consists of alternating dCdT residues; another consists of tandem repeats of the sequence CCTCT. The majority of B1s and B2s in the genome appear to be homogeneous, whereas R sequences, ECs, and MIF-1s are heterogeneous. Two earlier reports showed highly repeated mammalian DNA sequences in the herpesvirus genome (Peden et al., Cell 31:71-80, 1982; Puga et al., Cell 31:81-87, 1982). We show that sequences homologous to our EC clones are present in the herpesvirus genome, although these polypyrimidine stretches are not detected in poxvirus, adenovirus, and simian virus 40 genomes. We detect transcripts containing homology to all of these sequences in a nuclear transcription assay. Also, we show that small, polyadenylated RNA molecules homologous to B2 sequences are expressed in undifferentiated embryonal carcinoma cells but not in their differentiated derivatives. The significance of these findings is discussed.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adamson E. D., Gaunt S. J., Graham C. F. The differentiation of teratocarcinoma stem cells is marked by the types of collagen which are synthesized. Cell. 1979 Jul;17(3):469–476. doi: 10.1016/0092-8674(79)90254-x. [DOI] [PubMed] [Google Scholar]
  2. Arnheim N., Seperack P., Banerji J., Lang R. B., Miesfeld R., Marcu K. B. Mouse rDNA nontranscribed spacer sequences are found flanking immunoglobulin CH genes and elsewhere throughout the genome. Cell. 1980 Nov;22(1 Pt 1):179–185. doi: 10.1016/0092-8674(80)90166-x. [DOI] [PubMed] [Google Scholar]
  3. Barta A., Richards R. I., Baxter J. D., Shine J. Primary structure and evolution of rat growth hormone gene. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4867–4871. doi: 10.1073/pnas.78.8.4867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barth R. K., Gross K. W., Gremke L. C., Hastie N. D. Developmentally regulated mRNAs in mouse liver. Proc Natl Acad Sci U S A. 1982 Jan;79(2):500–504. doi: 10.1073/pnas.79.2.500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bennett K. L., Hastie N. D. Looking for relationships between the most repeated dispersed DNA sequences in the mouse: small R elements are found associated consistently with long MIF repeats. EMBO J. 1984 Feb;3(2):467–472. doi: 10.1002/j.1460-2075.1984.tb01829.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bennett K. L., Lalley P. A., Barth R. K., Hastie N. D. Mapping the structural genes coding for the major urinary proteins in the mouse: combined use of recombinant inbred strains and somatic cell hybrids. Proc Natl Acad Sci U S A. 1982 Feb;79(4):1220–1224. doi: 10.1073/pnas.79.4.1220. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Benton W. D., Davis R. W. Screening lambdagt recombinant clones by hybridization to single plaques in situ. Science. 1977 Apr 8;196(4286):180–182. doi: 10.1126/science.322279. [DOI] [PubMed] [Google Scholar]
  8. Bernstein L. B., Mount S. M., Weiner A. M. Pseudogenes for human small nuclear RNA U3 appear to arise by integration of self-primed reverse transcripts of the RNA into new chromosomal sites. Cell. 1983 Feb;32(2):461–472. doi: 10.1016/0092-8674(83)90466-x. [DOI] [PubMed] [Google Scholar]
  9. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Birnboim H. C. Polypyrimidine segments in Drosophila melanogaster DNA: I. Detection of a cryptic satellite containing polypyrimidine/polypurine DNA. Cell. 1975 Jun;5(2):173–181. doi: 10.1016/0092-8674(75)90025-2. [DOI] [PubMed] [Google Scholar]
  11. Birnboim H. C. Spacing of polypyrimidine regions in mouse DNA as determined by poly(adenylate, guanylate) binding. J Mol Biol. 1978 Jun 5;121(4):541–559. doi: 10.1016/0022-2836(78)90399-6. [DOI] [PubMed] [Google Scholar]
  12. Bonner J. J., Pardue M. L. Ecdysone-stimulated RNA synthesis in imaginal discs of Drosophila melanogaster. Assay by in situ hybridization. Chromosoma. 1976 Oct 12;58(1):87–99. doi: 10.1007/BF00293443. [DOI] [PubMed] [Google Scholar]
  13. Brown S. D., Dover G. Organization and evolutionary progress of a dispersed repetitive family of sequences in widely separated rodent genomes. J Mol Biol. 1981 Aug 25;150(4):441–466. doi: 10.1016/0022-2836(81)90374-0. [DOI] [PubMed] [Google Scholar]
  14. Cheng S. M., Schildkraut C. L. A family of moderately repetitive sequences in mouse DNA. Nucleic Acids Res. 1980 Sep 25;8(18):4075–4090. doi: 10.1093/nar/8.18.4075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Denhardt D. T. A membrane-filter technique for the detection of complementary DNA. Biochem Biophys Res Commun. 1966 Jun 13;23(5):641–646. doi: 10.1016/0006-291x(66)90447-5. [DOI] [PubMed] [Google Scholar]
  16. Derman E., Krauter K., Walling L., Weinberger C., Ray M., Darnell J. E., Jr Transcriptional control in the production of liver-specific mRNAs. Cell. 1981 Mar;23(3):731–739. doi: 10.1016/0092-8674(81)90436-0. [DOI] [PubMed] [Google Scholar]
  17. Doolittle W. F., Sapienza C. Selfish genes, the phenotype paradigm and genome evolution. Nature. 1980 Apr 17;284(5757):601–603. doi: 10.1038/284601a0. [DOI] [PubMed] [Google Scholar]
  18. Elder J. T., Pan J., Duncan C. H., Weissman S. M. Transcriptional analysis of interspersed repetitive polymerase III transcription units in human DNA. Nucleic Acids Res. 1981 Mar 11;9(5):1171–1189. doi: 10.1093/nar/9.5.1171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Fanning T. G. Size and structure of the highly repetitive BAM HI element in mice. Nucleic Acids Res. 1983 Aug 11;11(15):5073–5091. doi: 10.1093/nar/11.15.5073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gebhard W., Meitinger T., Höchtl J., Zachau H. G. A new family of interspersed repetitive DNA sequences in the mouse genome. J Mol Biol. 1982 May 25;157(3):453–471. doi: 10.1016/0022-2836(82)90471-5. [DOI] [PubMed] [Google Scholar]
  21. Gebhard W., Zachau H. G. Organization of the R family and other interspersed repetitive DNA sequences in the mouse genome. J Mol Biol. 1983 Oct 25;170(2):255–270. doi: 10.1016/s0022-2836(83)80147-8. [DOI] [PubMed] [Google Scholar]
  22. Grunstein M., Hogness D. S. Colony hybridization: a method for the isolation of cloned DNAs that contain a specific gene. Proc Natl Acad Sci U S A. 1975 Oct;72(10):3961–3965. doi: 10.1073/pnas.72.10.3961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Haigwood N. L., Jahn C. L., Hutchison C. A., 3rd, Edgell M. H. Locations of three repetitive sequence families found in BALB/c adult beta-globin clones. Nucleic Acids Res. 1981 Mar 11;9(5):1133–1150. doi: 10.1093/nar/9.5.1133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Haynes S. R., Jelinek W. R. Low molecular weight RNAs transcribed in vitro by RNA polymerase III from Alu-type dispersed repeats in Chinese hamster DNA are also found in vivo. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6130–6134. doi: 10.1073/pnas.78.10.6130. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Heath J. K., Deller M. J. Serum-free culture of PC13 murine embryonal carcinoma cells. J Cell Physiol. 1983 Jun;115(3):225–230. doi: 10.1002/jcp.1041150302. [DOI] [PubMed] [Google Scholar]
  26. Heller R., Arnheim N. Structure and organization of the highly repeated and interspersed 1.3 kb EcoRI-Bg1II sequence family in mice. Nucleic Acids Res. 1980 Nov 11;8(21):5031–5042. doi: 10.1093/nar/8.21.5031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Honjo T., Nakai S., Nishida Y., Kataoka T., Yamawaki-Kataoka Y., Takahashi N., Obata M., Shimizu A., Yaoita Y., Nikaido T. Rearrangements of immunoglobulin genes during differentiation and evolution. Immunol Rev. 1981;59:33–67. doi: 10.1111/j.1600-065x.1981.tb00455.x. [DOI] [PubMed] [Google Scholar]
  28. Iatrou K., Tsitilou S. G., Goldsmith M. R., Kafatos F. C. Molecular analysis of the GrB mutation in Bombyx mori through the use of chorion cDNA library. Cell. 1980 Jul;20(3):659–669. doi: 10.1016/0092-8674(80)90312-8. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Jelinek W. R., Schmid C. W. Repetitive sequences in eukaryotic DNA and their expression. Annu Rev Biochem. 1982;51:813–844. doi: 10.1146/annurev.bi.51.070182.004121. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Krayev A. S., Kramerov D. A., Skryabin K. G., Ryskov A. P., Bayev A. A., Georgiev G. P. The nucleotide sequence of the ubiquitous repetitive DNA sequence B1 complementary to the most abundant class of mouse fold-back RNA. Nucleic Acids Res. 1980 Mar 25;8(6):1201–1215. doi: 10.1093/nar/8.6.1201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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]
  34. 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]
  35. Lueders K. K., Paterson B. M. A short interspersed repetitive element found near some mouse structural genes. Nucleic Acids Res. 1982 Dec 11;10(23):7715–7729. doi: 10.1093/nar/10.23.7715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Maroteaux L., Heilig R., Dupret D., Mandel J. L. Repetitive satellite-like sequences are present within or upstream from 3 avian protein-coding genes. Nucleic Acids Res. 1983 Mar 11;11(5):1227–1243. doi: 10.1093/nar/11.5.1227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  38. McKnight G. S., Palmiter R. D. Transcriptional regulation of the ovalbumin and conalbumin genes by steroid hormones in chick oviduct. J Biol Chem. 1979 Sep 25;254(18):9050–9058. [PubMed] [Google Scholar]
  39. Meunier-Rotival M., Soriano P., Cuny G., Strauss F., Bernardi G. Sequence organization and genomic distribution of the major family of interspersed repeats of mouse DNA. Proc Natl Acad Sci U S A. 1982 Jan;79(2):355–359. doi: 10.1073/pnas.79.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Miesfeld R., Krystal M., Arnheim N. A member of a new repeated sequence family which is conserved throughout eucaryotic evolution is found between the human delta and beta globin genes. Nucleic Acids Res. 1981 Nov 25;9(22):5931–5947. doi: 10.1093/nar/9.22.5931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Orgel L. E., Crick F. H. Selfish DNA: the ultimate parasite. Nature. 1980 Apr 17;284(5757):604–607. doi: 10.1038/284604a0. [DOI] [PubMed] [Google Scholar]
  42. Pardue M. L., Gall J. G. Nucleic acid hybridization to the DNA of cytological preparations. Methods Cell Biol. 1975;10:1–16. doi: 10.1016/s0091-679x(08)60727-x. [DOI] [PubMed] [Google Scholar]
  43. Pearson W. R., Morrow J. F. Discrete-length repeated sequences in eukaryotic genomes. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4016–4020. doi: 10.1073/pnas.78.7.4016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Peden K., Mounts P., Hayward G. S. Homology between mammalian cell DNA sequences and human herpesvirus genomes detected by a hybridization procedure with high-complexity probe. Cell. 1982 Nov;31(1):71–80. doi: 10.1016/0092-8674(82)90406-8. [DOI] [PubMed] [Google Scholar]
  45. Piccini N., Knopf J. L., Gross K. W. A DNA polymorphism, consistent with gene duplication, correlates with high renin levels in the mouse submaxillary gland. Cell. 1982 Aug;30(1):205–213. doi: 10.1016/0092-8674(82)90026-5. [DOI] [PubMed] [Google Scholar]
  46. Pietras D. F., Bennett K. L., Siracusa L. D., Woodworth-Gutai M., Chapman V. M., Gross K. W., Kane-Haas C., Hastie N. D. Construction of a small Mus musculus repetitive DNA library: identification of a new satellite sequence in Mus musculus. Nucleic Acids Res. 1983 Oct 25;11(20):6965–6983. doi: 10.1093/nar/11.20.6965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Puga A., Cantin E. M., Notkins A. L. Homology between murine and human cellular DNA sequences and the terminal repetition of the S component of herpes simplex virus type 1 DNA. Cell. 1982 Nov;31(1):81–87. doi: 10.1016/0092-8674(82)90407-x. [DOI] [PubMed] [Google Scholar]
  48. Scheller R. H., Thomas T. L., Lee A. S., Klein W. H., Niles W. D., Britten R. J., Davidson E. H. Clones of individual repetitive sequences from sea urchin DNA constructed with synthetic Eco RI sites. Science. 1977 Apr 8;196(4286):197–200. doi: 10.1126/science.847467. [DOI] [PubMed] [Google Scholar]
  49. Schmid C. W., Jelinek W. R. The Alu family of dispersed repetitive sequences. Science. 1982 Jun 4;216(4550):1065–1070. doi: 10.1126/science.6281889. [DOI] [PubMed] [Google Scholar]
  50. Singer M. F. SINEs and LINEs: highly repeated short and long interspersed sequences in mammalian genomes. Cell. 1982 Mar;28(3):433–434. doi: 10.1016/0092-8674(82)90194-5. [DOI] [PubMed] [Google Scholar]
  51. Siracusa L. D., Chapman V. M., Bennett K. L., Hastie N. D., Pietras D. F., Rossant J. Use of repetitive DNA sequences to distinguish Mus musculus and Mus caroli cells by in situ hybridization. J Embryol Exp Morphol. 1983 Feb;73:163–178. [PubMed] [Google Scholar]
  52. 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]
  53. Steinmetz M., Frelinger J. G., Fisher D., Hunkapiller T., Pereira D., Weissman S. M., Uehara H., Nathenson S., Hood L. Three cDNA clones encoding mouse transplantation antigens: homology to immunoglobulin genes. Cell. 1981 Apr;24(1):125–134. doi: 10.1016/0092-8674(81)90508-0. [DOI] [PubMed] [Google Scholar]
  54. Sutcliffe J. G., Milner R. J., Bloom F. E., Lerner R. A. Common 82-nucleotide sequence unique to brain RNA. Proc Natl Acad Sci U S A. 1982 Aug;79(16):4942–4946. doi: 10.1073/pnas.79.16.4942. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Tata J. R. Isolation of nuclei from liver and other tissues. Methods Enzymol. 1974;31:253–262. doi: 10.1016/0076-6879(74)31027-0. [DOI] [PubMed] [Google Scholar]
  56. Van Arsdell S. W., Denison R. A., Bernstein L. B., Weiner A. M., Manser T., Gesteland R. F. Direct repeats flank three small nuclear RNA pseudogenes in the human genome. Cell. 1981 Oct;26(1 Pt 1):11–17. doi: 10.1016/0092-8674(81)90028-3. [DOI] [PubMed] [Google Scholar]
  57. Wahl G. M., Stern M., Stark G. R. Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl-paper and rapid hybridization by using dextran sulfate. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3683–3687. doi: 10.1073/pnas.76.8.3683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Young P. R., Scott R. W., Hamer D. H., Tilghman S. M. Construction and expression in vivo of an internally deleted mouse alpha-fetoprotein gene: presence of a transcribed Alu-like repeat within the first intervening sequence. Nucleic Acids Res. 1982 May 25;10(10):3099–3116. doi: 10.1093/nar/10.10.3099. [DOI] [PMC free article] [PubMed] [Google Scholar]

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