Skip to main content
NCBI home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1985 Sep;5(9):2197–2203. doi: 10.1128/mcb.5.9.2197

Long interspersed repeated DNA (LINE) causes polymorphism at the rat insulin 1 locus.

M S Lakshmikumaran, E D'Ambrosio, L A Laimins, D T Lin, A V Furano
PMCID: PMC366944  PMID: 3016521

Abstract

The insulin 1, but not the insulin 2, locus is polymorphic (i.e., exhibits allelic variation) in rats. Restriction enzyme analysis and hybridization studies showed that the polymorphic region is 2.2 kilobases upstream of the insulin 1 coding region and is due to the presence or absence of an approximately 2.7-kilobase repeated DNA element. DNA sequence determination showed that this DNA element is a member of a long interspersed repeated DNA family (LINE) that is highly repeated (greater than 50,000 copies) and highly transcribed in the rat. Although the presence or absence of LINE sequences at the insulin 1 locus occurs in both the homozygous and heterozygous states, LINE-containing insulin 1 alleles are more prevalent in the rat population than are alleles without LINEs. Restriction enzyme analysis of the LINE-containing alleles indicated that at least two versions of the LINE sequence may be present at the insulin 1 locus in different rats. Either repeated transposition of LINE sequences or gene conversion between the resident insulin 1 LINE and other sequences in the genome are possible explanations for this.

Full text

PDF
2197

Images in this article

2198Image
on p.2198
2199Image
on p.2199
2199Image
on p.2199

Selected References

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

  1. Adams J. W., Kaufman R. E., Kretschmer P. J., Harrison M., Nienhuis A. W. A family of long reiterated DNA sequences, one copy of which is next to the human beta globin gene. Nucleic Acids Res. 1980 Dec 20;8(24):6113–6128. doi: 10.1093/nar/8.24.6113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bell G. I., Pictet R., Rutter W. J. Analysis of the regions flanking the human insulin gene and sequence of an Alu family member. Nucleic Acids Res. 1980 Sep 25;8(18):4091–4109. doi: 10.1093/nar/8.18.4091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Britten R. J., Davidson E. H. Repetitive and non-repetitive DNA sequences and a speculation on the origins of evolutionary novelty. Q Rev Biol. 1971 Jun;46(2):111–138. doi: 10.1086/406830. [DOI] [PubMed] [Google Scholar]
  4. Britten R. J., Kohne D. E. Repeated sequences in DNA. Hundreds of thousands of copies of DNA sequences have been incorporated into the genomes of higher organisms. Science. 1968 Aug 9;161(3841):529–540. doi: 10.1126/science.161.3841.529. [DOI] [PubMed] [Google Scholar]
  5. Brutlag D. L., Clayton J., Friedland P., Kedes L. H. SEQ: a nucleotide sequence analysis and recombination system. Nucleic Acids Res. 1982 Jan 11;10(1):279–294. doi: 10.1093/nar/10.1.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cordell B., Bell G., Tischer E., DeNoto F. M., Ullrich A., Pictet R., Rutter W. J., Goodman H. M. Isolation and characterization of a cloned rat insulin gene. Cell. 1979 Oct;18(2):533–543. doi: 10.1016/0092-8674(79)90070-9. [DOI] [PubMed] [Google Scholar]
  7. Davidson E. H., Hough B. R., Amenson C. S., Britten R. J. General interspersion of repetitive with non-repetitive sequence elements in the DNA of Xenopus. J Mol Biol. 1973 Jun 15;77(1):1–23. doi: 10.1016/0022-2836(73)90359-8. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. Grimaldi G., Singer M. F. Members of the KpnI family of long interspersed repeated sequences join and interrupt alpha-satellite in the monkey genome. Nucleic Acids Res. 1983 Jan 25;11(2):321–338. doi: 10.1093/nar/11.2.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. doi: 10.1016/0378-1119(84)90153-7. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. Lehrman M. A., Schneider W. J., Südhof T. C., Brown M. S., Goldstein J. L., Russell D. W. Mutation in LDL receptor: Alu-Alu recombination deletes exons encoding transmembrane and cytoplasmic domains. Science. 1985 Jan 11;227(4683):140–146. doi: 10.1126/science.3155573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lemischka I., Sharp P. A. The sequences of an expressed rat alpha-tubulin gene and a pseudogene with an inserted repetitive element. Nature. 1982 Nov 25;300(5890):330–335. doi: 10.1038/300330a0. [DOI] [PubMed] [Google Scholar]
  16. Lerman M. I., Thayer R. E., Singer M. F. Kpn I family of long interspersed repeated DNA sequences in primates: polymorphism of family members and evidence for transcription. Proc Natl Acad Sci U S A. 1983 Jul;80(13):3966–3970. doi: 10.1073/pnas.80.13.3966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lomedico P., Rosenthal N., Efstratidadis A., Gilbert W., Kolodner R., Tizard R. The structure and evolution of the two nonallelic rat preproinsulin genes. Cell. 1979 Oct;18(2):545–558. doi: 10.1016/0092-8674(79)90071-0. [DOI] [PubMed] [Google Scholar]
  18. Martin S. L., Voliva C. F., Burton F. H., Edgell M. H., Hutchison C. A., 3rd A large interspersed repeat found in mouse DNA contains a long open reading frame that evolves as if it encodes a protein. Proc Natl Acad Sci U S A. 1984 Apr;81(8):2308–2312. doi: 10.1073/pnas.81.8.2308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Meunier-Rotival M., Bernardi G. The Bam repeats of the mouse genome belong in several superfamilies the longest of which is over 9 kb in size. Nucleic Acids Res. 1984 Feb 10;12(3):1593–1608. doi: 10.1093/nar/12.3.1593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Nishioka Y., Leder A., Leder P. Unusual alpha-globin-like gene that has cleanly lost both globin intervening sequences. Proc Natl Acad Sci U S A. 1980 May;77(5):2806–2809. doi: 10.1073/pnas.77.5.2806. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nomiyama H., Tsuzuki T., Wakasugi S., Fukuda M., Shimada K. Interruption of a human nuclear sequence homologous to mitochondrial DNA by a member of the KpnI 1.8 kb family. Nucleic Acids Res. 1984 Jul 11;12(13):5225–5234. doi: 10.1093/nar/12.13.5225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Norrander J., Kempe T., Messing J. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene. 1983 Dec;26(1):101–106. doi: 10.1016/0378-1119(83)90040-9. [DOI] [PubMed] [Google Scholar]
  24. Pearson W. R., Wu J. R., Bonner J. Analysis of rat repetitive DNA sequences. Biochemistry. 1978 Jan 10;17(1):51–59. doi: 10.1021/bi00594a008. [DOI] [PubMed] [Google Scholar]
  25. Sakano H., Maki R., Kurosawa Y., Roeder W., Tonegawa S. Two types of somatic recombination are necessary for the generation of complete immunoglobulin heavy-chain genes. Nature. 1980 Aug 14;286(5774):676–683. doi: 10.1038/286676a0. [DOI] [PubMed] [Google Scholar]
  26. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Schuler L. A., Weber J. L., Gorski J. Polymorphism near the rat prolactin gene caused by insertion of an Alu-like element. Nature. 1983 Sep 8;305(5930):159–160. doi: 10.1038/305159a0. [DOI] [PubMed] [Google Scholar]
  29. Shafit-Zagardo B., Brown F. L., Maio J. J., Adams J. W. KpnI families of long, interspersed repetitive DNAs associated with the human beta-globin gene cluster. Gene. 1982 Dec;20(3):397–407. doi: 10.1016/0378-1119(82)90208-6. [DOI] [PubMed] [Google Scholar]
  30. Sharp P. A. Conversion of RNA to DNA in mammals: Alu-like elements and pseudogenes. Nature. 1983 Feb 10;301(5900):471–472. doi: 10.1038/301471a0. [DOI] [PubMed] [Google Scholar]
  31. Singer M. F. Highly repeated sequences in mammalian genomes. Int Rev Cytol. 1982;76:67–112. doi: 10.1016/s0074-7696(08)61789-1. [DOI] [PubMed] [Google Scholar]
  32. Singer M. F., Thayer R. E., Grimaldi G., Lerman M. I., Fanning T. G. Homology between the KpnI primate and BamH1 (M1F-1) rodent families of long interspersed repeated sequences. Nucleic Acids Res. 1983 Aug 25;11(16):5739–5745. doi: 10.1093/nar/11.16.5739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Singh L., Jones K. W. The use of heparin as a simple cost-effective means of controlling background in nucleic acid hybridization procedures. Nucleic Acids Res. 1984 Jul 25;12(14):5627–5638. doi: 10.1093/nar/12.14.5627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. Streeck R. E. A multicopy insertion sequence in the bovine genome with structural homology to the long terminal repeats of retroviruses. Nature. 1982 Aug 19;298(5876):767–769. doi: 10.1038/298767a0. [DOI] [PubMed] [Google Scholar]
  36. Thayer R. E., Singer M. F. Interruption of an alpha-satellite array by a short member of the KpnI family of interspersed, highly repeated monkey DNA sequences. Mol Cell Biol. 1983 Jun;3(6):967–973. doi: 10.1128/mcb.3.6.967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Tsichlis P. N., Strauss P. G., Hu L. F. A common region for proviral DNA integration in MoMuLV-induced rat thymic lymphomas. 1983 Mar 31-Apr 6Nature. 302(5907):445–449. doi: 10.1038/302445a0. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Wilbur W. J., Lipman D. J. Rapid similarity searches of nucleic acid and protein data banks. Proc Natl Acad Sci U S A. 1983 Feb;80(3):726–730. doi: 10.1073/pnas.80.3.726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Witney F. R., Furano A. V. Highly repeated DNA families in the rat. J Biol Chem. 1984 Aug 25;259(16):10481–10492. [PubMed] [Google Scholar]
  41. Witney F. R., Furano A. V. The independent evolution of two closely related satellite DNA elements in rats (Rattus). Nucleic Acids Res. 1983 Jan 25;11(2):291–304. doi: 10.1093/nar/11.2.291. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES