Skip to main content
NCBI home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1986 Jan;6(1):209–217. doi: 10.1128/mcb.6.1.209

Polymorphism in an androgen-regulated mouse gene is the result of the insertion of a B1 repetitive element into the transcription unit.

D King, L D Snider, J B Lingrel
PMCID: PMC367500  PMID: 3023823

Abstract

The single-copy RP2 gene in mice produces three major mRNAs, the abundances of which are significantly increased in the kidneys by the administration of testosterone. S1 nuclease analysis of the kidney mRNAs indicated that they differ in the lengths of their 3' untranslated regions as a result of the use of different polyadenylation sites. When the mRNAs from different inbred mouse strains were examined by Northern blot analysis, it was observed that the largest mRNA varies in size, whereas the sizes of the other mRNAs remain the same. In DBA/LiHa and DBA/2J mice, the largest mRNA is approximately 2,150 nucleotides long, whereas the corresponding mRNA in C57BL/6J and BALB/cJ mice is only 1,950 nucleotides in length. All of these strains also have RP2 mRNAs that are 1,450 and 1,350 nucleotides long. By S1 nuclease mapping and comparison of the sequence of cDNA clones representing these mRNAs in DBA/LiHa and C57BL/6J mice, we determined that this size difference or polymorphism observed in the largest mRNA is the result of the insertion of a member of the B1 family of repeats into the 3' untranslated region of the RP2 gene in DBA mice. This particular B1 repeat is transcribed by RNA polymerase III in vitro, and its transcriptional orientation is opposite to that of the RP2 transcript. The polymorphism described here is evidence for the mobility of B1 repetitive elements within the genome.

Full text

PDF
209

Images in this article

210Image
on p.210
211Image
on p.211
212Image
on p.212
215Image
on p.215
216Image
on p.216

Selected References

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

  1. Berger F. G., Gross K. W., Watson G. Isolation and characterization of a DNA sequence complementary to an androgen-inducible messenger RNA from mouse kidney. J Biol Chem. 1981 Jul 10;256(13):7006–7013. [PubMed] [Google Scholar]
  2. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  3. Birnstiel M. L., Busslinger M., Strub K. Transcription termination and 3' processing: the end is in site! Cell. 1985 Jun;41(2):349–359. doi: 10.1016/s0092-8674(85)80007-6. [DOI] [PubMed] [Google Scholar]
  4. Bogenhagen D. F., Brown D. D. Nucleotide sequences in Xenopus 5S DNA required for transcription termination. Cell. 1981 Apr;24(1):261–270. doi: 10.1016/0092-8674(81)90522-5. [DOI] [PubMed] [Google Scholar]
  5. Dignam J. D., Lebovitz R. M., Roeder R. G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983 Mar 11;11(5):1475–1489. doi: 10.1093/nar/11.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Duncan C., Biro P. A., Choudary P. V., Elder J. T., Wang R. R., Forget B. G., de Riel J. K., Weissman S. M. RNA polymerase III transcriptional units are interspersed among human non-alpha-globin genes. Proc Natl Acad Sci U S A. 1979 Oct;76(10):5095–5099. doi: 10.1073/pnas.76.10.5095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Elliott R. W., Berger F. G. DNA sequence polymorphism in an androgen-regulated gene is associated with alteration in the encoded RNAs. Proc Natl Acad Sci U S A. 1983 Jan;80(2):501–504. doi: 10.1073/pnas.80.2.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Galli G., Hofstetter H., Birnstiel M. L. Two conserved sequence blocks within eukaryotic tRNA genes are major promoter elements. Nature. 1981 Dec 17;294(5842):626–631. doi: 10.1038/294626a0. [DOI] [PubMed] [Google Scholar]
  9. Grimaldi G., Singer M. F. A monkey Alu sequence is flanked by 13-base pair direct repeats by an interrupted alpha-satellite DNA sequence. Proc Natl Acad Sci U S A. 1982 Mar;79(5):1497–1500. doi: 10.1073/pnas.79.5.1497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Izant J. G., Weintraub H. Inhibition of thymidine kinase gene expression by anti-sense RNA: a molecular approach to genetic analysis. Cell. 1984 Apr;36(4):1007–1015. doi: 10.1016/0092-8674(84)90050-3. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Kalb V. F., Glasser S., King D., Lingrel J. B. A cluster of repetitive elements within a 700 base pair region in the mouse genome. Nucleic Acids Res. 1983 Apr 11;11(7):2177–2184. doi: 10.1093/nar/11.7.2177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kawasaki E. S. Quantitative hybridization-arrest of mRNA in Xenopus oocytes using single-stranded complementary DNA or oligonucleotide probes. Nucleic Acids Res. 1985 Jul 11;13(13):4991–5004. doi: 10.1093/nar/13.13.4991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. 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]
  18. 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]
  19. Kress M., Barra Y., Seidman J. G., Khoury G., Jay G. Functional insertion of an Alu type 2 (B2 SINE) repetitive sequence in murine class I genes. Science. 1984 Nov 23;226(4677):974–977. doi: 10.1126/science.6095445. [DOI] [PubMed] [Google Scholar]
  20. Luse D. S., Haynes J. R., VanLeeuwen D., Schon E. A., Cleary M. L., Shapiro S. G., Lingrel J. B., Roeder R. G. Transcription of the beta-like globin genes and pseudogenes of the goat in a cell-free system. Nucleic Acids Res. 1981 Sep 11;9(17):4339–4354. doi: 10.1093/nar/9.17.4339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Mizuno T., Chou M. Y., Inouye M. A unique mechanism regulating gene expression: translational inhibition by a complementary RNA transcript (micRNA). Proc Natl Acad Sci U S A. 1984 Apr;81(7):1966–1970. doi: 10.1073/pnas.81.7.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Page G. S., Smith S., Goodman H. M. DNA sequence of the rat growth hormone gene: location of the 5' terminus of the growth hormone mRNA and identification of an internal transposon-like element. Nucleic Acids Res. 1981 May 11;9(9):2087–2104. doi: 10.1093/nar/9.9.2087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Palmer R., Gallagher P. M., Boyko W. L., Ganschow R. E. Genetic control of levels of murine kidney glucuronidase mRNA in response to androgen. Proc Natl Acad Sci U S A. 1983 Dec;80(24):7596–7600. doi: 10.1073/pnas.80.24.7596. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Perez-Stable C., Ayres T. M., Shen C. K. Distinctive sequence organization and functional programming of an Alu repeat promoter. Proc Natl Acad Sci U S A. 1984 Sep;81(17):5291–5295. doi: 10.1073/pnas.81.17.5291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Proudfoot N. J., Brownlee G. G. 3' non-coding region sequences in eukaryotic messenger RNA. Nature. 1976 Sep 16;263(5574):211–214. doi: 10.1038/263211a0. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. 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]
  29. Simons R. W., Kleckner N. Translational control of IS10 transposition. Cell. 1983 Sep;34(2):683–691. doi: 10.1016/0092-8674(83)90401-4. [DOI] [PubMed] [Google Scholar]
  30. Snider L. D., King D., Lingrel J. B. Androgen regulation of MAK mRNAs in mouse kidney. J Biol Chem. 1985 Aug 15;260(17):9884–9893. [PubMed] [Google Scholar]
  31. 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]
  32. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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]
  34. Weaver R. F., Weissmann C. Mapping of RNA by a modification of the Berk-Sharp procedure: the 5' termini of 15 S beta-globin mRNA precursor and mature 10 s beta-globin mRNA have identical map coordinates. Nucleic Acids Res. 1979 Nov 10;7(5):1175–1193. doi: 10.1093/nar/7.5.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Whitelaw E., Proudfoot N. J. Transcriptional activity of the human pseudogene psi alpha globin compared with alpha globin, its functional gene counterpart. Nucleic Acids Res. 1983 Nov 25;11(22):7717–7733. doi: 10.1093/nar/11.22.7717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]

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

RESOURCES