Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1988 Jun;85(12):4416–4420. doi: 10.1073/pnas.85.12.4416

Rat L (long interspersed repeated DNA) elements contain guanine-rich homopurine sequences that induce unpairing of contiguous duplex DNA.

K Usdin 1, A V Furano 1
PMCID: PMC280440  PMID: 2837766

Abstract

The L family (long interspersed repeated DNA) of mobile genetic elements is a persistent feature of the mammalian genome. In rats, this family contains approximately equal to 40,000 members and accounts for approximately equal to 10% of the haploid genome. We demonstrate here that the guanine-rich homopurine stretches located at the right end of L-DNA induce oligonucleotide uptake by contiguous duplex DNA. The uptake is dependent on negative supercoiling and the length of the homopurine stretch and occurs even when the L-DNA homopurine stretches are introduced into a different DNA environment. The bound oligomer primes DNA synthesis when DNA polymerase and deoxyribonucleoside triphosphates are added, resulting in a faithful copy of the template to which the oligonucleotide had bound. The implications of this property of the L-DNA guanine-rich homopurine stretches in the amplification, recombination, and dispersal of L elements is discussed.

Full text

PDF
4416

Images in this article

4418Image
on p.4418
4418Image
on p.4418
4418Image
on p.4418
4419Image
on p.4419
4419Image
on p.4419
4419Image
on p.4419

Selected References

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

  1. Burke W. D., Calalang C. C., Eickbush T. H. The site-specific ribosomal insertion element type II of Bombyx mori (R2Bm) contains the coding sequence for a reverse transcriptase-like enzyme. Mol Cell Biol. 1987 Jun;7(6):2221–2230. doi: 10.1128/mcb.7.6.2221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Burton F. H., Loeb D. D., Chao S. F., Hutchison C. A., 3rd, Edgell M. H. Transposition of a long member of the L1 major interspersed DNA family into the mouse beta globin gene locus. Nucleic Acids Res. 1985 Jul 25;13(14):5071–5084. doi: 10.1093/nar/13.14.5071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Burton F. H., Loeb D. D., Voliva C. F., Martin S. L., Edgell M. H., Hutchison C. A., 3rd Conservation throughout mammalia and extensive protein-encoding capacity of the highly repeated DNA long interspersed sequence one. J Mol Biol. 1986 Jan 20;187(2):291–304. doi: 10.1016/0022-2836(86)90235-4. [DOI] [PubMed] [Google Scholar]
  4. Cantor C. R., Efstratiadis A. Possible structures of homopurine-homopyrimidine S1-hypersensitive sites. Nucleic Acids Res. 1984 Nov 12;12(21):8059–8072. doi: 10.1093/nar/12.21.8059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Christophe D., Cabrer B., Bacolla A., Targovnik H., Pohl V., Vassart G. An unusually long poly(purine)-poly(pyrimidine) sequence is located upstream from the human thyroglobulin gene. Nucleic Acids Res. 1985 Jul 25;13(14):5127–5144. doi: 10.1093/nar/13.14.5127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cox M. M., Lehman I. R. Enzymes of general recombination. Annu Rev Biochem. 1987;56:229–262. doi: 10.1146/annurev.bi.56.070187.001305. [DOI] [PubMed] [Google Scholar]
  7. D'Ambrosio E., Waitzkin S. D., Witney F. R., Salemme A., Furano A. V. Structure of the highly repeated, long interspersed DNA family (LINE or L1Rn) of the rat. Mol Cell Biol. 1986 Feb;6(2):411–424. doi: 10.1128/mcb.6.2.411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Drew H. R., Travers A. A. DNA structural variations in the E. coli tyrT promoter. Cell. 1984 Jun;37(2):491–502. doi: 10.1016/0092-8674(84)90379-9. [DOI] [PubMed] [Google Scholar]
  9. Economou-Pachnis A., Lohse M. A., Furano A. V., Tsichlis P. N. Insertion of long interspersed repeated elements at the Igh (immunoglobulin heavy chain) and Mlvi-2 (Moloney leukemia virus integration 2) loci of rats. Proc Natl Acad Sci U S A. 1985 May;82(9):2857–2861. doi: 10.1073/pnas.82.9.2857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Elgin S. C. Anatomy of hypersensitive sites. Nature. 1984 May 17;309(5965):213–214. doi: 10.1038/309213a0. [DOI] [PubMed] [Google Scholar]
  11. Evans T., Efstratiadis A. Sequence-dependent S1 nuclease hypersensitivity of a heteronomous DNA duplex. J Biol Chem. 1986 Nov 5;261(31):14771–14780. [PubMed] [Google Scholar]
  12. Evans T., Schon E., Gora-Maslak G., Patterson J., Efstratiadis A. S1-hypersensitive sites in eukaryotic promoter regions. Nucleic Acids Res. 1984 Nov 12;12(21):8043–8058. doi: 10.1093/nar/12.21.8043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fanning T., Singer M. The LINE-1 DNA sequences in four mammalian orders predict proteins that conserve homologies to retrovirus proteins. Nucleic Acids Res. 1987 Mar 11;15(5):2251–2260. doi: 10.1093/nar/15.5.2251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fawcett D. H., Lister C. K., Kellett E., Finnegan D. J. Transposable elements controlling I-R hybrid dysgenesis in D. melanogaster are similar to mammalian LINEs. Cell. 1986 Dec 26;47(6):1007–1015. doi: 10.1016/0092-8674(86)90815-9. [DOI] [PubMed] [Google Scholar]
  15. Formosa T., Alberts B. M. DNA synthesis dependent on genetic recombination: characterization of a reaction catalyzed by purified bacteriophage T4 proteins. Cell. 1986 Dec 5;47(5):793–806. doi: 10.1016/0092-8674(86)90522-2. [DOI] [PubMed] [Google Scholar]
  16. Fujita A., Hattori M., Takenaka O., Sakaki Y. The L1 family (KpnI family) sequence near the 3' end of human beta-globin gene may have been derived from an active L1 sequence. Nucleic Acids Res. 1987 May 26;15(10):4007–4020. doi: 10.1093/nar/15.10.4007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Furano A. V., Somerville C. C., Tsichlis P. N., D'Ambrosio E. Target sites for the transposition of rat long interspersed repeated DNA elements (LINEs) are not random. Nucleic Acids Res. 1986 May 12;14(9):3717–3727. doi: 10.1093/nar/14.9.3717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gillies S. D., Folsom V., Tonegawa S. Cell type-specific enhancer element associated with a mouse MHC gene, E beta. Nature. 1984 Aug 16;310(5978):594–597. doi: 10.1038/310594a0. [DOI] [PubMed] [Google Scholar]
  19. Hattori M., Hidaka S., Sakaki Y. Sequence analysis of a KpnI family member near the 3' end of human beta-globin gene. Nucleic Acids Res. 1985 Nov 11;13(21):7813–7827. doi: 10.1093/nar/13.21.7813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hattori M., Kuhara S., Takenaka O., Sakaki Y. L1 family of repetitive DNA sequences in primates may be derived from a sequence encoding a reverse transcriptase-related protein. Nature. 1986 Jun 5;321(6070):625–628. doi: 10.1038/321625a0. [DOI] [PubMed] [Google Scholar]
  21. Hentschel C. C. Homocopolymer sequences in the spacer of a sea urchin histone gene repeat are sensitive to S1 nuclease. Nature. 1982 Feb 25;295(5851):714–716. doi: 10.1038/295714a0. [DOI] [PubMed] [Google Scholar]
  22. Hoffman-Liebermann B., Liebermann D., Troutt A., Kedes L. H., Cohen S. N. Human homologs of TU transposon sequences: polypurine/polypyrimidine sequence elements that can alter DNA conformation in vitro and in vivo. Mol Cell Biol. 1986 Nov;6(11):3632–3642. doi: 10.1128/mcb.6.11.3632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Holloman W. K., Wiegand R., Hoessli C., Radding C. M. Uptake of homologous single-stranded fragments by superhelical DNA: a possible mechanism for initiation of genetic recombination. Proc Natl Acad Sci U S A. 1975 Jun;72(6):2394–2398. doi: 10.1073/pnas.72.6.2394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Htun H., Lund E., Dahlberg J. E. Human U1 RNA genes contain an unusually sensitive nuclease S1 cleavage site within the conserved 3' flanking region. Proc Natl Acad Sci U S A. 1984 Dec;81(23):7288–7292. doi: 10.1073/pnas.81.23.7288. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ish-Horowicz D., Burke J. F. Rapid and efficient cosmid cloning. Nucleic Acids Res. 1981 Jul 10;9(13):2989–2998. doi: 10.1093/nar/9.13.2989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Katzir N., Rechavi G., Cohen J. B., Unger T., Simoni F., Segal S., Cohen D., Givol D. "Retroposon" insertion into the cellular oncogene c-myc in canine transmissible venereal tumor. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1054–1058. doi: 10.1073/pnas.82.4.1054. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kimmel B. E., ole-MoiYoi O. K., Young J. R. Ingi, a 5.2-kb dispersed sequence element from Trypanosoma brucei that carries half of a smaller mobile element at either end and has homology with mammalian LINEs. Mol Cell Biol. 1987 Apr;7(4):1465–1475. doi: 10.1128/mcb.7.4.1465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Kohwi-Shigematsu T., Gelinas R., Weintraub H. Detection of an altered DNA conformation at specific sites in chromatin and supercoiled DNA. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4389–4393. doi: 10.1073/pnas.80.14.4389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kohwi-Shigematsu T., Kohwi Y. Poly(dG)-poly(dC) sequences, under torsional stress, induce an altered DNA conformation upon neighboring DNA sequences. Cell. 1985 Nov;43(1):199–206. doi: 10.1016/0092-8674(85)90024-8. [DOI] [PubMed] [Google Scholar]
  30. Lakshmikumaran M. S., D'Ambrosio E., Laimins L. A., Lin D. T., Furano A. V. Long interspersed repeated DNA (LINE) causes polymorphism at the rat insulin 1 locus. Mol Cell Biol. 1985 Sep;5(9):2197–2203. doi: 10.1128/mcb.5.9.2197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Larsen A., Weintraub H. An altered DNA conformation detected by S1 nuclease occurs at specific regions in active chick globin chromatin. Cell. 1982 Jun;29(2):609–622. doi: 10.1016/0092-8674(82)90177-5. [DOI] [PubMed] [Google Scholar]
  32. Lechner R. L., Engler M. J., Richardson C. C. Characterization of strand displacement synthesis catalyzed by bacteriophage T7 DNA polymerase. J Biol Chem. 1983 Sep 25;258(18):11174–11184. [PubMed] [Google Scholar]
  33. Lin F. L., Sperle K., Sternberg N. Model for homologous recombination during transfer of DNA into mouse L cells: role for DNA ends in the recombination process. Mol Cell Biol. 1984 Jun;4(6):1020–1034. doi: 10.1128/mcb.4.6.1020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Loeb D. D., Padgett R. W., Hardies S. C., Shehee W. R., Comer M. B., Edgell M. H., Hutchison C. A., 3rd The sequence of a large L1Md element reveals a tandemly repeated 5' end and several features found in retrotransposons. Mol Cell Biol. 1986 Jan;6(1):168–182. doi: 10.1128/mcb.6.1.168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Meselson M. S., Radding C. M. A general model for genetic recombination. Proc Natl Acad Sci U S A. 1975 Jan;72(1):358–361. doi: 10.1073/pnas.72.1.358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Mizuuchi K., Craigie R. Mechanism of bacteriophage mu transposition. Annu Rev Genet. 1986;20:385–429. doi: 10.1146/annurev.ge.20.120186.002125. [DOI] [PubMed] [Google Scholar]
  37. Nickol J. M., Felsenfeld G. DNA conformation at the 5' end of the chicken adult beta-globin gene. Cell. 1983 Dec;35(2 Pt 1):467–477. doi: 10.1016/0092-8674(83)90180-0. [DOI] [PubMed] [Google Scholar]
  38. Okamoto T., Reitz M. S., Jr, Clarke M. F., Jagodzinski L. L., Wong-Staal F. Activation of a novel KpnI transcript by downstream integration of a human T-lymphotropic virus type I provirus. J Biol Chem. 1986 Apr 5;261(10):4615–4619. [PubMed] [Google Scholar]
  39. Orr-Weaver T. L., Szostak J. W., Rothstein R. J. Yeast transformation: a model system for the study of recombination. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6354–6358. doi: 10.1073/pnas.78.10.6354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Plesner P., Goodchild J., Kalckar H. M., Zamecnik P. C. Oligonucleotides with rapid turnover of the phosphate groups occur endogenously in eukaryotic cells. Proc Natl Acad Sci U S A. 1987 Apr;84(7):1936–1939. doi: 10.1073/pnas.84.7.1936. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Pulleyblank D. E., Haniford D. B., Morgan A. R. A structural basis for S1 nuclease sensitivity of double-stranded DNA. Cell. 1985 Aug;42(1):271–280. doi: 10.1016/s0092-8674(85)80122-7. [DOI] [PubMed] [Google Scholar]
  42. Rogers J. H. The origin and evolution of retroposons. Int Rev Cytol. 1985;93:187–279. doi: 10.1016/s0074-7696(08)61375-3. [DOI] [PubMed] [Google Scholar]
  43. Schon E., Evans T., Welsh J., Efstratiadis A. Conformation of promoter DNA: fine mapping of S1-hypersensitive sites. Cell. 1983 Dec;35(3 Pt 2):837–848. doi: 10.1016/0092-8674(83)90116-2. [DOI] [PubMed] [Google Scholar]
  44. Selleck S. B., Elgin S. C., Cartwright I. L. Supercoil-dependent features of DNA structure at Drosophila locus 67B1. J Mol Biol. 1984 Sep 5;178(1):17–33. doi: 10.1016/0022-2836(84)90228-6. [DOI] [PubMed] [Google Scholar]
  45. Shapiro J. A. Molecular model for the transposition and replication of bacteriophage Mu and other transposable elements. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1933–1937. doi: 10.1073/pnas.76.4.1933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Shyman S., Weaver S. Chromosomal rearrangements associated with LINE elements in the mouse genome. Nucleic Acids Res. 1985 Jul 25;13(14):5085–5093. doi: 10.1093/nar/13.14.5085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Siegfried E., Thomas G. H., Bond U. M., Elgin S. C. Characterization of a supercoil-dependent S1 sensitive site 5' to the Drosophila melanogaster hsp 26 gene. Nucleic Acids Res. 1986 Dec 9;14(23):9425–9444. doi: 10.1093/nar/14.23.9425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Soares M. B., Schon E., Efstratiadis A. Rat LINE1: the origin and evolution of a family of long interspersed middle repetitive DNA elements. J Mol Evol. 1985;22(2):117–133. doi: 10.1007/BF02101690. [DOI] [PubMed] [Google Scholar]
  49. Song K. Y., Chekuri L., Rauth S., Ehrlich S., Kucherlapati R. Effect of double-strand breaks on homologous recombination in mammalian cells and extracts. Mol Cell Biol. 1985 Dec;5(12):3331–3336. doi: 10.1128/mcb.5.12.3331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Tabor S., Richardson C. C. Selective oxidation of the exonuclease domain of bacteriophage T7 DNA polymerase. J Biol Chem. 1987 Nov 15;262(32):15330–15333. [PubMed] [Google Scholar]
  51. Voliva C. F., Martin S. L., Hutchison C. A., 3rd, Edgell M. H. Dispersal process associated with the L1 family of interspersed repetitive DNA sequences. J Mol Biol. 1984 Oct 5;178(4):795–813. doi: 10.1016/0022-2836(84)90312-7. [DOI] [PubMed] [Google Scholar]
  52. Yancopoulos G. D., DePinho R. A., Zimmerman K. A., Lutzker S. G., Rosenberg N., Alt F. W. Secondary genomic rearrangement events in pre-B cells: VHDJH replacement by a LINE-1 sequence and directed class switching. EMBO J. 1986 Dec 1;5(12):3259–3266. doi: 10.1002/j.1460-2075.1986.tb04637.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. d'Ambrosio E., Furano A. V. DNA synthesis arrest sites at the right terminus of rat long interspersed repeated (LINE or L1Rn) DNA family members. Nucleic Acids Res. 1987 Apr 10;15(7):3155–3175. doi: 10.1093/nar/15.7.3155. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES