Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1984 Dec 11;12(23):8835–8846. doi: 10.1093/nar/12.23.8835

A complete and a truncated U1 snRNA gene of Drosophila melanogaster are found as inverted repeats at region 82E of the polytene chromosomes.

J Kejzlarová-Lepesant, H W Brock, J Moreau, M L Dubertret, A Billault, J A Lepesant
PMCID: PMC320422  PMID: 6083546

Abstract

A phage containing two sequences homologous to U1 snRNA was isolated from a Drosophila melanogaster genomic library, and identified with a previously cloned D. melanogaster U1 snRNA gene. DNA sequence analysis showed that complete and truncated U1 snRNA genes are present, both of which have base substitutions relative to U1 snRNA. These genes show conservation of 5' and 3' flanking regions relative to other U1 and U2 snRNA genes of Drosophila. Intramolecular renaturation experiments and electron microscope mapping demonstrates that the two U1 snRNA sequences are present as inverted repeats about 2.7kb apart, separated by a smaller pair of inverted repeats of an unrelated sequence. These U1 snRNA sequences were located by in situ hybridization at 82E, and related sequences were found at 21D and 95C on the polytene chromosome map. The results are discussed with reference to the origin and function of snRNAs.

Full text

PDF
8836

Images in this article

Selected References

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

  1. Alonso A., Jorcano J. L., Beck E., Spiess E. Isolation and characterization of Drosophila melanogaster U2 small nuclear RNA genes. J Mol Biol. 1983 Sep 25;169(3):691–705. doi: 10.1016/s0022-2836(83)80165-x. [DOI] [PubMed] [Google Scholar]
  2. Beck E., Jorcano J. L., Alonso A. Drosophila melanogaster U1 and U2 small nuclear RNA genes contain common flanking sequences. J Mol Biol. 1984 Mar 15;173(4):539–542. doi: 10.1016/0022-2836(84)90397-8. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Branlant C., Krol A., Ebel J. P., Lazar E., Gallinaro H., Jacob M., Sri-Widada J., Jeanteur P. Nucleotide sequences of nuclear U1A RNAs from chicken, rat and man. Nucleic Acids Res. 1980 Sep 25;8(18):4143–4154. doi: 10.1093/nar/8.18.4143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bringmann P., Appel B., Rinke J., Reuter R., Theissen H., Lührmann R. Evidence for the existence of snRNAs U4 and U6 in a single ribonucleoprotein complex and for their association by intermolecular base pairing. EMBO J. 1984 Jun;3(6):1357–1363. doi: 10.1002/j.1460-2075.1984.tb01977.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brock H. W., Roberts D. B. Location of the LSP-1 Genes in Drosophila Species by IN SITU Hybridization. Genetics. 1983 Jan;103(1):75–92. doi: 10.1093/genetics/103.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Busch H., Reddy R., Rothblum L., Choi Y. C. SnRNAs, SnRNPs, and RNA processing. Annu Rev Biochem. 1982;51:617–654. doi: 10.1146/annurev.bi.51.070182.003153. [DOI] [PubMed] [Google Scholar]
  8. Calvet J. P., Pederson T. Base-pairing interactions between small nuclear RNAs and nuclear RNA precursors as revealed by psoralen cross-linking in vivo. Cell. 1981 Nov;26(3 Pt 1):363–370. doi: 10.1016/0092-8674(81)90205-1. [DOI] [PubMed] [Google Scholar]
  9. Card C. O., Morris G. F., Brown D. T., Marzluff W. F. Sea urchin small nuclear RNA genes are organized in distinct tandemly repeating units. Nucleic Acids Res. 1982 Dec 11;10(23):7677–7688. doi: 10.1093/nar/10.23.7677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Denison R. A., Van Arsdell S. W., Bernstein L. B., Weiner A. M. Abundant pseudogenes for small nuclear RNAs are dispersed in the human genome. Proc Natl Acad Sci U S A. 1981 Feb;78(2):810–814. doi: 10.1073/pnas.78.2.810. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Denison R. A., Weiner A. M. Human U1 RNA pseudogenes may be generated by both DNA- and RNA-mediated mechanisms. Mol Cell Biol. 1982 Jul;2(7):815–828. doi: 10.1128/mcb.2.7.815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Flytzanis C., Alonso A., Louis C., Krieg L., Sekeris C. E. Association of small nuclear RNA with HnRNA isolated from nuclear RNP complexes carrying HnRNA. FEBS Lett. 1978 Dec 1;96(1):201–206. doi: 10.1016/0014-5793(78)81094-1. [DOI] [PubMed] [Google Scholar]
  14. Forbes D. J., Kirschner M. W., Caput D., Dahlberg J. E., Lund E. Differential expression of multiple U1 small nuclear RNAs in oocytes and embryos of Xenopus laevis. Cell. 1984 Oct;38(3):681–689. doi: 10.1016/0092-8674(84)90263-0. [DOI] [PubMed] [Google Scholar]
  15. Fradin A., Jove R., Hemenway C., Keiser H. D., Manley J. L., Prives C. Splicing pathways of SV40 mRNAs in X. laevis oocytes differ in their requirements for snRNPs. Cell. 1984 Jul;37(3):927–936. doi: 10.1016/0092-8674(84)90427-6. [DOI] [PubMed] [Google Scholar]
  16. Krol A., Gallinaro H., Lazar E., Jacob M., Branlant C. The nuclear 5S RNAs from chicken, rat and man. U5 RNAs are encoded by multiple genes. Nucleic Acids Res. 1981 Feb 25;9(4):769–787. doi: 10.1093/nar/9.4.769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Krämer A., Keller W., Appel B., Lührmann R. The 5' terminus of the RNA moiety of U1 small nuclear ribonucleoprotein particles is required for the splicing of messenger RNA precursors. Cell. 1984 Aug;38(1):299–307. doi: 10.1016/0092-8674(84)90551-8. [DOI] [PubMed] [Google Scholar]
  18. Lepesant J. A., Levine M., Garen A., Lepesant-Kejzlarvoa J., Rat L., Somme-Martin G. Developmentally regulated gene expression in Drosophila larval fat bodies. J Mol Appl Genet. 1982;1(5):371–383. [PubMed] [Google Scholar]
  19. Lerner M. R., Boyle J. A., Mount S. M., Wolin S. L., Steitz J. A. Are snRNPs involved in splicing? Nature. 1980 Jan 10;283(5743):220–224. doi: 10.1038/283220a0. [DOI] [PubMed] [Google Scholar]
  20. Lerner M. R., Steitz J. A. Antibodies to small nuclear RNAs complexed with proteins are produced by patients with systemic lupus erythematosus. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5495–5499. doi: 10.1073/pnas.76.11.5495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lund E., Dahlberg J. E. True genes for human U1 small nuclear RNA. Copy number, polymorphism, and methylation. J Biol Chem. 1984 Feb 10;259(3):2013–2021. [PubMed] [Google Scholar]
  22. Maniatis T., Hardison R. C., Lacy E., Lauer J., O'Connell C., Quon D., Sim G. K., Efstratiadis A. The isolation of structural genes from libraries of eucaryotic DNA. Cell. 1978 Oct;15(2):687–701. doi: 10.1016/0092-8674(78)90036-3. [DOI] [PubMed] [Google Scholar]
  23. Manser T., Gesteland R. F. Human U1 loci: genes for human U1 RNA have dramatically similar genomic environments. Cell. 1982 May;29(1):257–264. doi: 10.1016/0092-8674(82)90110-6. [DOI] [PubMed] [Google Scholar]
  24. Mattaj I. W., Zeller R. Xenopus laevis U2 snRNA genes: tandemly repeated transcription units sharing 5' and 3' flanking homology with other RNA polymerase II transcribed genes. EMBO J. 1983;2(11):1883–1891. doi: 10.1002/j.1460-2075.1983.tb01675.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Monstein H. J., Hammarström K., Westin G., Zabielski J., Philipson L., Pettersson U. Loci for human U1 RNA: structural and evolutionary implications. J Mol Biol. 1983 Jun 25;167(2):245–257. doi: 10.1016/s0022-2836(83)80334-9. [DOI] [PubMed] [Google Scholar]
  27. Mount S. M., Pettersson I., Hinterberger M., Karmas A., Steitz J. A. The U1 small nuclear RNA-protein complex selectively binds a 5' splice site in vitro. Cell. 1983 Jun;33(2):509–518. doi: 10.1016/0092-8674(83)90432-4. [DOI] [PubMed] [Google Scholar]
  28. Mount S. M., Steitz J. A. Sequence of U1 RNA from Drosophila melanogaster: implications for U1 secondary structure and possible involvement in splicing. Nucleic Acids Res. 1981 Dec 11;9(23):6351–6368. doi: 10.1093/nar/9.23.6351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ohshima Y., Okada N., Tani T., Itoh Y., Itoh M. Nucleotide sequences of mouse genomic loci including a gene or pseudogene for U6 (4.8S) nuclear RNA. Nucleic Acids Res. 1981 Oct 10;9(19):5145–5158. doi: 10.1093/nar/9.19.5145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Padgett R. A., Mount S. M., Steitz J. A., Sharp P. A. Splicing of messenger RNA precursors is inhibited by antisera to small nuclear ribonucleoprotein. Cell. 1983 Nov;35(1):101–107. doi: 10.1016/0092-8674(83)90212-x. [DOI] [PubMed] [Google Scholar]
  31. Reddy R., Spector D., Henning D., Liu M. H., Busch H. Isolation and partial characterization of dinoflagellate U1-U6 small RNAs homologous to rat U small nuclear RNAs. J Biol Chem. 1983 Nov 25;258(22):13965–13969. [PubMed] [Google Scholar]
  32. Rogers J., Wall R. A mechanism for RNA splicing. Proc Natl Acad Sci U S A. 1980 Apr;77(4):1877–1879. doi: 10.1073/pnas.77.4.1877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Roop D. R., Kristo P., Stumph W. E., Tsai M. J., O'Malley B. W. Structure and expression of a chicken gene coding for U1 RNA. Cell. 1981 Mar;23(3):671–680. doi: 10.1016/0092-8674(81)90430-x. [DOI] [PubMed] [Google Scholar]
  34. Saluz H. P., Schmidt T., Dudler R., Altwegg M., Stumm-Zollinger E., Kubli E., Chen P. S. The genes coding for 4 snRNAs of Drosophila melanogaster: localization and determination of gene numbers. Nucleic Acids Res. 1983 Jan 11;11(1):77–90. doi: 10.1093/nar/11.1.77. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Smith D. F., McClelland A., White B. N., Addison C. F., Glover D. M. The molecular cloning of a dispersed set of developmentally regulated genes which encode the major larval serum protein of D. melanogaster. Cell. 1981 Feb;23(2):441–449. doi: 10.1016/0092-8674(81)90139-2. [DOI] [PubMed] [Google Scholar]
  36. Tani T., Watanabe-Nagasu N., Okada N., Ohshima Y. Molecular cloning and characterization of a gene for rat U2 small nuclear RNA. J Mol Biol. 1983 Aug 15;168(3):579–594. doi: 10.1016/s0022-2836(83)80303-9. [DOI] [PubMed] [Google Scholar]
  37. Truett M. A., Jones R. S., Potter S. S. Unusual structure of the FB family of transposable elements in Drosophila. Cell. 1981 Jun;24(3):753–763. doi: 10.1016/0092-8674(81)90101-x. [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. Watanabe-Nagasu N., Itoh Y., Tani T., Okano K., Koga N., Okada N., Ohshima Y. Structural analysis of gene loci for rat U1 small nuclear RNA. Nucleic Acids Res. 1983 Mar 25;11(6):1791–1801. doi: 10.1093/nar/11.6.1791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wieben E. D., Madore S. J., Pederson T. Protein binding sites are conserved in U1 small nuclear RNA from insects and mammals. Proc Natl Acad Sci U S A. 1983 Mar;80(5):1217–1220. doi: 10.1073/pnas.80.5.1217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wieben E. D., Pederson T. Small nuclear ribonucleoproteins of Drosophila: identification of U1 RNA-associated proteins and their behavior during heat shock. Mol Cell Biol. 1982 Aug;2(8):914–920. doi: 10.1128/mcb.2.8.914. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wise J. A., Tollervey D., Maloney D., Swerdlow H., Dunn E. J., Guthrie C. Yeast contains small nuclear RNAs encoded by single copy genes. Cell. 1983 Dec;35(3 Pt 2):743–751. doi: 10.1016/0092-8674(83)90107-1. [DOI] [PubMed] [Google Scholar]
  43. Wooley J. C., Cone R. D., Tartof D., Chung S. Y. Small nuclear ribonucleoprotein complexes of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6762–6766. doi: 10.1073/pnas.79.22.6762. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Zieve G., Penman S. Subnuclear particles containing a small nuclear RNA and heterogeneous nuclear RNA. J Mol Biol. 1981 Jan 25;145(3):501–523. doi: 10.1016/0022-2836(81)90542-8. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES