Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1984 Dec;4(12):2565–2572. doi: 10.1128/mcb.4.12.2565

Transposition of two different intracisternal A particle elements into an immunoglobulin kappa-chain gene.

R G Hawley, M J Shulman, N Hozumi
PMCID: PMC369258  PMID: 6098810

Abstract

Each of two severely defective mouse kappa-chain genes has acquired a different intracisternal A particle (IAP) element within one of its introns. One IAP element generated 6-base-pair direct repeats upon insertion. In contrast, the other IAP element was not flanked by direct repeats and was missing a single nucleotide from its 3' terminus. Sequence analysis of the latter IAP element demonstrated that its long terminal repeats were not identical. Nevertheless, the long terminal repeats were organized like proviral long terminal repeats, and this IAP element did contain two regions that were analogous to retroviral priming sites for RNA-directed DNA synthesis. The region that corresponded to a retroviral tRNA primer binding site was complementary to the 3' ends of all mammalian phenylalanine tRNAs. These findings are discussed in the context of the presumed mode of transposition of IAP elements involving the reverse transcription of IAP RNA.

Full text

PDF
2565

Images in this article

Selected References

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

  1. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baker C. C., Herisse J., Courtois G., Galibert F., Ziff E. Messenger RNA for the Ad2 DNA binding protein: DNA sequences encoding the first leader and heterogenity at the mRNA 5' end. Cell. 1979 Oct;18(2):569–580. doi: 10.1016/0092-8674(79)90073-4. [DOI] [PubMed] [Google Scholar]
  3. Biczysko W., Pienkowski M., Solter D., Koprowski H. Virus particles in early mouse embryos. J Natl Cancer Inst. 1973 Sep;51(3):1041–1050. doi: 10.1093/jnci/51.3.1041. [DOI] [PubMed] [Google Scholar]
  4. Calarco P. G., Szollosi D. Intracisternal A particles in ova and preimplantation stages of the mouse. Nat New Biol. 1973 May 16;243(124):91–93. [PubMed] [Google Scholar]
  5. Calos M. P., Miller J. H. Molecular consequences of deletion formation mediated by the transposon Tn9. Nature. 1980 May 1;285(5759):38–41. doi: 10.1038/285038a0. [DOI] [PubMed] [Google Scholar]
  6. Canaani E., Dreazen O., Klar A., Rechavi G., Ram D., Cohen J. B., Givol D. Activation of the c-mos oncogene in a mouse plasmacytoma by insertion of an endogenous intracisternal A-particle genome. Proc Natl Acad Sci U S A. 1983 Dec;80(23):7118–7122. doi: 10.1073/pnas.80.23.7118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chase D. G., Pikó L. Expression of A- and C-type particles in early mouse embryos. J Natl Cancer Inst. 1973 Dec;51(6):1971–1975. doi: 10.1093/jnci/51.6.1971. [DOI] [PubMed] [Google Scholar]
  8. Chen H. R., Barker W. C. Nucleotide sequences of the retroviral long terminal repeats and their adjacent regions. Nucleic Acids Res. 1984 Feb 24;12(4):1767–1778. doi: 10.1093/nar/12.4.1767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cohen J. B., Unger T., Rechavi G., Canaani E., Givol D. Rearrangement of the oncogene c-mos in mouse myeloma NSI and hybridomas. Nature. 1983 Dec 22;306(5945):797–799. doi: 10.1038/306797a0. [DOI] [PubMed] [Google Scholar]
  10. Cole M. D., Ono M., Huang R. C. Intracisternal A-particle genes: structure of adjacent genes and mapping of the boundaries of the transcriptional unit. J Virol. 1982 Apr;42(1):123–130. doi: 10.1128/jvi.42.1.123-130.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cole M. D., Ono M., Huang R. C. Terminally redundant sequences in cellular intracisternal A-particle genes. J Virol. 1981 May;38(2):680–687. doi: 10.1128/jvi.38.2.680-687.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Elder R. T., Loh E. Y., Davis R. W. RNA from the yeast transposable element Ty1 has both ends in the direct repeats, a structure similar to retrovirus RNA. Proc Natl Acad Sci U S A. 1983 May;80(9):2432–2436. doi: 10.1073/pnas.80.9.2432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Flavell A. J., Ish-Horowicz D. The origin of extrachromosomal circular copia elements. Cell. 1983 Sep;34(2):415–419. doi: 10.1016/0092-8674(83)90375-6. [DOI] [PubMed] [Google Scholar]
  14. Harbers K., Kuehn M., Delius H., Jaenisch R. Insertion of retrovirus into the first intron of alpha 1(I) collagen gene to embryonic lethal mutation in mice. Proc Natl Acad Sci U S A. 1984 Mar;81(5):1504–1508. doi: 10.1073/pnas.81.5.1504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hawley R. G., Shulman M. J., Murialdo H., Gibson D. M., Hozumi N. Mutant immunoglobulin genes have repetitive DNA elements inserted into their intervening sequences. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7425–7429. doi: 10.1073/pnas.79.23.7425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hawley R. G., Trimble W. S., Shulman M. J., Hozumi N. Transposition of intracisternal A-particle genes in mouse hybridomas. J Cell Physiol Suppl. 1984;3:29–38. doi: 10.1002/jcp.1041210406. [DOI] [PubMed] [Google Scholar]
  17. Hozumi N., Hawley R. G., Murialdo H. Molecular cloning of an immunoglobulin kappa constant gene from NZB mouse. Gene. 1981 Mar;13(2):163–172. doi: 10.1016/0378-1119(81)90005-6. [DOI] [PubMed] [Google Scholar]
  18. Hozumi N., Wu G. E., Murialdo H., Roberts L., Vetter D., Fife W. L., Whiteley M., Sadowski P. RNA splicing mutation in an aberrantly rearranged immunoglobulin lambda I gene. Proc Natl Acad Sci U S A. 1981 Nov;78(11):7019–7023. doi: 10.1073/pnas.78.11.7019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kelley D. E., Coleclough C., Perry R. P. Functional significance and evolutionary development of the 5'-terminal regions of immunoglobulin variable-region genes. Cell. 1982 Jun;29(2):681–689. doi: 10.1016/0092-8674(82)90184-2. [DOI] [PubMed] [Google Scholar]
  20. Kleckner N. Transposable elements in prokaryotes. Annu Rev Genet. 1981;15:341–404. doi: 10.1146/annurev.ge.15.120181.002013. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Kuff E. L., Smith L. A., Lueders K. K. Intracisternal A-particle genes in Mus musculus: a conserved family of retrovirus-like elements. Mol Cell Biol. 1981 Mar;1(3):216–227. doi: 10.1128/mcb.1.3.216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kugimiya W., Ikenaga H., Saigo K. Close relationship between the long terminal repeats of avian leukosis-sarcoma virus and copia-like movable genetic elements of Drosophila. Proc Natl Acad Sci U S A. 1983 Jun;80(11):3193–3197. doi: 10.1073/pnas.80.11.3193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lueders K. K., Kuff E. L. Intracisternal A-particle genes: identification in the genome of Mus musculus and comparison of multiple isolates from a mouse gene library. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3571–3575. doi: 10.1073/pnas.77.6.3571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Lueders K. K., Segal S., Kuff E. L. RNA sequences specifically associated with mouse intracisternal A particles. Cell. 1977 May;11(1):83–94. doi: 10.1016/0092-8674(77)90319-1. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Max E. E., Maizel J. V., Jr, Leder P. The nucleotide sequence of a 5.5-kilobase DNA segment containing the mouse kappa immunoglobulin J and C region genes. J Biol Chem. 1981 May 25;256(10):5116–5120. [PubMed] [Google Scholar]
  29. 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]
  30. McCLINTOCK B. Chromosome organization and genic expression. Cold Spring Harb Symp Quant Biol. 1951;16:13–47. doi: 10.1101/sqb.1951.016.01.004. [DOI] [PubMed] [Google Scholar]
  31. Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. doi: 10.1016/0076-6879(83)01005-8. [DOI] [PubMed] [Google Scholar]
  32. Minna J. D., Lueders K. K., Kuff E. L. Expression of genes for intracisternal A-particle antigen in somatic cell hybrids. J Natl Cancer Inst. 1974 Apr;52(4):1211–1217. doi: 10.1093/jnci/52.4.1211. [DOI] [PubMed] [Google Scholar]
  33. Mount S. M. A catalogue of splice junction sequences. Nucleic Acids Res. 1982 Jan 22;10(2):459–472. doi: 10.1093/nar/10.2.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Ono M., Cole M. D., White A. T., Huang R. C. Sequence organization of cloned intracisternal A particle genes. Cell. 1980 Sep;21(2):465–473. doi: 10.1016/0092-8674(80)90483-3. [DOI] [PubMed] [Google Scholar]
  35. Paterson B. M., Segal S., Lueders K. K., Kuff E. L. RNA associated with murine intracisternal type A particles codes for the main particle protein. J Virol. 1978 Jul;27(1):118–126. doi: 10.1128/jvi.27.1.118-126.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. 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]
  38. Schibler U., Marcu K. B., Perry R. P. The synthesis and processing of the messenger RNAs specifying heavy and light chain immunoglobulins in MPC-11 cells. Cell. 1978 Dec;15(4):1495–1509. doi: 10.1016/0092-8674(78)90072-7. [DOI] [PubMed] [Google Scholar]
  39. Shen-Ong G. L., Cole M. D. Amplification of a specific set of intracisternal A-particle genes in a mouse plasmacytoma. J Virol. 1984 Jan;49(1):171–177. doi: 10.1128/jvi.49.1.171-177.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Shen-Ong G. L., Cole M. D. Differing populations of intracisternal A-particle genes in myeloma tumors and mouse subspecies. J Virol. 1982 May;42(2):411–421. doi: 10.1128/jvi.42.2.411-421.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Shenk T. Transcriptional control regions: nucleotide sequence requirements for initiation by RNA polymerase II and III. Curr Top Microbiol Immunol. 1981;93:25–46. doi: 10.1007/978-3-642-68123-3_3. [DOI] [PubMed] [Google Scholar]
  42. Shiba T., Saigo K. Retrovirus-like particles containing RNA homologous to the transposable element copia in Drosophila melanogaster. Nature. 1983 Mar 10;302(5904):119–124. doi: 10.1038/302119a0. [DOI] [PubMed] [Google Scholar]
  43. Sprinzl M., Gauss D. H. Compilation of tRNA sequences. Nucleic Acids Res. 1982 Jan 22;10(2):r1–55. [PMC free article] [PubMed] [Google Scholar]
  44. Temin H. M. Structure, variation and synthesis of retrovirus long terminal repeat. Cell. 1981 Nov;27(1 Pt 2):1–3. doi: 10.1016/0092-8674(81)90353-6. [DOI] [PubMed] [Google Scholar]
  45. 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]
  46. Tu C. P., Cohen S. N. 3'-end labeling of DNA with [alpha-32P]cordycepin-5'-triphosphate. Gene. 1980 Jul;10(2):177–183. doi: 10.1016/0378-1119(80)90135-3. [DOI] [PubMed] [Google Scholar]
  47. Varmus H. E., Quintrell N., Ortiz S. Retroviruses as mutagens: insertion and excision of a nontransforming provirus alter expression of a resident transforming provirus. Cell. 1981 Jul;25(1):23–36. doi: 10.1016/0092-8674(81)90228-2. [DOI] [PubMed] [Google Scholar]
  48. Wilson S. H., Bohn E. W., Matsukage A., Lueders K. K., Kuff E. L. Studies on the relationship between deoxyribonucleic acid polymerase activity and intracisternal A-type particles in mouse myeloma. Biochemistry. 1974 Mar 12;13(6):1087–1094. doi: 10.1021/bi00703a005. [DOI] [PubMed] [Google Scholar]
  49. Wivel N. A., Smith G. H. Distribution of intracisternal A-particles in a variety of normal and neoplastic mouse tissues. Int J Cancer. 1971 Jan 15;7(1):167–175. doi: 10.1002/ijc.2910070119. [DOI] [PubMed] [Google Scholar]
  50. Wolf D., Rotter V. Inactivation of p53 gene expression by an insertion of Moloney murine leukemia virus-like DNA sequences. Mol Cell Biol. 1984 Jul;4(7):1402–1410. doi: 10.1128/mcb.4.7.1402. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Yang S. S., Wivel N. A. Characterization of an endogenous RNA-dependent DNA polymerase associated with murine intracisternal A particles. J Virol. 1974 Mar;13(3):712–720. doi: 10.1128/jvi.13.3.712-720.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES