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. 1986 May;83(10):3106–3110. doi: 10.1073/pnas.83.10.3106

Stable accumulation of a rat truncated repeat transcript in Xenopus oocytes.

A Gutierrez-Hartmann, J D Baxter
PMCID: PMC323461  PMID: 2422646

Abstract

To define potential mechanisms of expression of middle-repetitive DNA, Xenopus oocytes were employed to examine the rat type 2 and truncated repeat (TR) elements contained in an intron and in the 3'-flanking region of the rat growth hormone gene. These repeats contain significant sequence and structural homology to tRNA genes and, thus, may represent tRNA pseudogenes. Transcripts from the type 2 elements do not accumulate in the cytosol and are found predominantly in the nucleus, whereas those from TR DNA are expressed in the cytosol of neural and pituitary tissues. In HeLa cell extracts, the rat growth hormone type 2 sequences initiate RNA polymerase III transcription resulting in multiple transcripts of 175-970 nucleotides; some of these also contain TR sequences that are present only as downstream structures since the rat growth hormone-TR DNA lacks promoter activity. In Xenopus oocytes the same template also results in multiple transcripts, but with time a single, homogeneous 73-base RNA preferentially accumulates. This RNA probably arises from larger repetitive DNA transcripts as assessed by the kinetics of its formation, its 5' terminus, and the injection of transcripts generated in HeLa cell-free extracts into the oocytes. Sequence analysis of the 73-base RNA suggests that it is a TR transcripts derived from the TR region with tRNA homology. Stable type 2 transcripts were not detected. Thus, type 2 elements are transcribed in the oocytes, but RNAs from them are degraded whereas discrete TR DNA transcripts can be derived from larger RNA molecules and can accumulate in the cytosol due to their preferential stability. These findings indicate that posttranscriptional control mechanisms can operate to direct differential expression of closely related repetitive DNAs and suggest that structures similar to tRNA contained within the TR sequences may allow them to accumulate preferentially in the cytoplasm.

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Selected References

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

  1. Adeniyi-Jones S., Zasloff M. Transcription, processing and nuclear transport of a B1 Alu RNA species complementary to an intron of the murine alpha-fetoprotein gene. Nature. 1985 Sep 5;317(6032):81–84. doi: 10.1038/317081a0. [DOI] [PubMed] [Google Scholar]
  2. Anderson D. M., Richter J. D., Chamberlin M. E., Price D. H., Britten R. J., Smith L. D., Davidson E. H. Sequence organization of the poly(A) RNA synthesized and accumulated in lampbrush chromosome stage Xenopus laevis oocytes. J Mol Biol. 1982 Mar 5;155(3):281–309. doi: 10.1016/0022-2836(82)90006-7. [DOI] [PubMed] [Google Scholar]
  3. Barta A., Richards R. I., Baxter J. D., Shine J. Primary structure and evolution of rat growth hormone gene. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4867–4871. doi: 10.1073/pnas.78.8.4867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Costantini F. D., Britten R. J., Davidson E. H. Message sequences and short repetitive sequences are interspersed in sea urchin egg poly(A)+ RNAs. Nature. 1980 Sep 11;287(5778):111–117. doi: 10.1038/287111a0. [DOI] [PubMed] [Google Scholar]
  5. Daniels G. R., Deininger P. L. Repeat sequence families derived from mammalian tRNA genes. 1985 Oct 31-Nov 6Nature. 317(6040):819–822. doi: 10.1038/317819a0. [DOI] [PubMed] [Google Scholar]
  6. Dhar R., Ellis R. W., Shih T. Y., Oroszlan S., Shapiro B., Maizel J., Lowy D., Scolnick E. Nucleotide sequence of the p21 transforming protein of Harvey murine sarcoma virus. Science. 1982 Sep 3;217(4563):934–936. doi: 10.1126/science.6287572. [DOI] [PubMed] [Google Scholar]
  7. Gurdon J. B., Brown D. D. The transcription of 5 S DNA injected into Xenopus oocytes. Dev Biol. 1978 Dec;67(2):346–356. doi: 10.1016/0012-1606(78)90205-1. [DOI] [PubMed] [Google Scholar]
  8. Gutierrez-Hartmann A., Lieberburg I., Gardner D., Baxter J. D., Cathala G. G. Transcription of two classes of rat growth hormone gene-associated repetitive DNA: differences in activity and effects of tandem repeat structure. Nucleic Acids Res. 1984 Sep 25;12(18):7153–7173. doi: 10.1093/nar/12.18.7153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Hofstetter H., Kressman A., Birnstiel M. L. A split promoter for a eucaryotic tRNA gene. Cell. 1981 May;24(2):573–585. doi: 10.1016/0092-8674(81)90348-2. [DOI] [PubMed] [Google Scholar]
  11. Hurst H. C., Parker M. G. Rat prostatic steroid binding protein: characterisation of the Alu element upstream of the C3 genes. Nucleic Acids Res. 1984 May 25;12(10):4313–4322. doi: 10.1093/nar/12.10.4313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jelinek W. R., Schmid C. W. Repetitive sequences in eukaryotic DNA and their expression. Annu Rev Biochem. 1982;51:813–844. doi: 10.1146/annurev.bi.51.070182.004121. [DOI] [PubMed] [Google Scholar]
  13. Jelinek W. R. Specific nucleotide sequences in HeLa cell inverted repeated DNA: enrichment for sequences found in double-stranded regions of heterogeneous nuclear RNA. J Mol Biol. 1977 Oct 5;115(4):591–601. doi: 10.1016/0022-2836(77)90104-8. [DOI] [PubMed] [Google Scholar]
  14. Jelinek W., Evans R., Wilson M., Salditt-Georgieff M., Darnell J. E. Oligonucleotides in heterogeneous nuclear RNA: similarity of inverted repeats and RNA from repetitious DNA sites. Biochemistry. 1978 Jul 11;17(14):2776–2783. doi: 10.1021/bi00607a012. [DOI] [PubMed] [Google Scholar]
  15. Lawrence C. B., McDonnell D. P., Ramsey W. J. Analysis of repetitive sequence elements containing tRNA-like sequences. Nucleic Acids Res. 1985 Jun 25;13(12):4239–4252. doi: 10.1093/nar/13.12.4239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Miller W. L., Eberhardt N. L. Structure and evolution of the growth hormone gene family. Endocr Rev. 1983 Spring;4(2):97–130. doi: 10.1210/edrv-4-2-97. [DOI] [PubMed] [Google Scholar]
  18. Milner R. J., Bloom F. E., Lai C., Lerner R. A., Sutcliffe J. G. Brain-specific genes have identifier sequences in their introns. Proc Natl Acad Sci U S A. 1984 Feb;81(3):713–717. doi: 10.1073/pnas.81.3.713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell. 1982 Oct;30(3):687–696. doi: 10.1016/0092-8674(82)90273-2. [DOI] [PubMed] [Google Scholar]
  20. Owens G. P., Chaudhari N., Hahn W. E. Brain "identifier sequence" is not restricted to brain: similar abundance in nuclear RNA of other organs. Science. 1985 Sep 20;229(4719):1263–1265. doi: 10.1126/science.2412293. [DOI] [PubMed] [Google Scholar]
  21. Raymond G. J., Johnson J. D. The role of non-coding DNA sequences in transcription and processing of a yeast tRNA. Nucleic Acids Res. 1983 Sep 10;11(17):5969–5988. doi: 10.1093/nar/11.17.5969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Sakamoto K., Okada N. 5-Methylcytidylic modification of in vitro transcript from the rat identifier sequence; evidence that the transcript forms a tRNA-like structure. Nucleic Acids Res. 1985 Oct 25;13(20):7195–7206. doi: 10.1093/nar/13.20.7195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. Sutcliffe J. G., Milner R. J., Bloom F. E., Lerner R. A. Common 82-nucleotide sequence unique to brain RNA. Proc Natl Acad Sci U S A. 1982 Aug;79(16):4942–4946. doi: 10.1073/pnas.79.16.4942. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sutcliffe J. G., Milner R. J., Gottesfeld J. M., Lerner R. A. Identifier sequences are transcribed specifically in brain. Nature. 1984 Mar 15;308(5956):237–241. doi: 10.1038/308237a0. [DOI] [PubMed] [Google Scholar]
  28. Sutcliffe J. G., Milner R. J., Gottesfeld J. M., Reynolds W. Control of neuronal gene expression. Science. 1984 Sep 21;225(4668):1308–1315. doi: 10.1126/science.6474179. [DOI] [PubMed] [Google Scholar]
  29. Walter P., Blobel G. Signal recognition particle contains a 7S RNA essential for protein translocation across the endoplasmic reticulum. Nature. 1982 Oct 21;299(5885):691–698. doi: 10.1038/299691a0. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. 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]

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