Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1996 Oct 15;24(20):4078–4083. doi: 10.1093/nar/24.20.4078

Regulated nuclear polyadenylation of Xenopus albumin pre-mRNA.

M N Rao 1, E Chernokalskaya 1, D R Schoenberg 1
PMCID: PMC146192  PMID: 8918815

Abstract

Cytoplasmic regulation of the length of poly(A) on mRNA is a well-characterized process involved in translational control during development. In contrast, there is no direct in vivo evidence for regulation of the length of poly(A) added during nuclear pre-mRNA processing in somatic cells. We previously reported that Xenopus serum albumin [Schoenberg et al. (1989) Mol. Endocrinol. 3, 805-815] and transferrin [Pastori et al. (1992) J. Steroid Biochem. Mol. Biol. 42, 649-657], mRNA have exceptionally short poly(A) tails ranging from 12 to 17 residues, whereas vitellogenin mRNA has long poly(A). An RT-PCR protocol was adapted to determine the length of poly(A) added onto pre-mRNA, defined here as that species bearing the terminal intron. Using this assay we show that vitellogenin pre-mRNA has the same long poly(A) tail as mature vitellogenin mRNA. In contrast, albumin pre-mRNA has the same short poly(A) as found on fully-processed albumin mRNA. These results indicate that the short poly(A) tail on albumin mRNA results from regulation of poly(A) addition during nuclear 3' processing.

Full Text

The Full Text of this article is available as a PDF (105.2 KB).

Selected References

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

  1. Baurén G., Wieslander L. Splicing of Balbiani ring 1 gene pre-mRNA occurs simultaneously with transcription. Cell. 1994 Jan 14;76(1):183–192. doi: 10.1016/0092-8674(94)90182-1. [DOI] [PubMed] [Google Scholar]
  2. Bienroth S., Keller W., Wahle E. Assembly of a processive messenger RNA polyadenylation complex. EMBO J. 1993 Feb;12(2):585–594. doi: 10.1002/j.1460-2075.1993.tb05690.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Carrazana E. J., Pasieka K. B., Majzoub J. A. The vasopressin mRNA poly(A) tract is unusually long and increases during stimulation of vasopressin gene expression in vivo. Mol Cell Biol. 1988 Jun;8(6):2267–2274. doi: 10.1128/mcb.8.6.2267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Decker C. J., Parker R. A turnover pathway for both stable and unstable mRNAs in yeast: evidence for a requirement for deadenylation. Genes Dev. 1993 Aug;7(8):1632–1643. doi: 10.1101/gad.7.8.1632. [DOI] [PubMed] [Google Scholar]
  5. Dompenciel R. E., Garnepudi V. R., Schoenberg D. R. Purification and characterization of an estrogen-regulated Xenopus liver polysomal nuclease involved in the selective destabilization of albumin mRNA. J Biol Chem. 1995 Mar 17;270(11):6108–6118. doi: 10.1074/jbc.270.11.6108. [DOI] [PubMed] [Google Scholar]
  6. Greenberg M. E., Shyu A. B., Belasco J. G. Deadenylylation: a mechanism controlling c-fos mRNA decay. Enzyme. 1990;44(1-4):181–192. doi: 10.1159/000468756. [DOI] [PubMed] [Google Scholar]
  7. Huarte J., Stutz A., O'Connell M. L., Gubler P., Belin D., Darrow A. L., Strickland S., Vassalli J. D. Transient translational silencing by reversible mRNA deadenylation. Cell. 1992 Jun 12;69(6):1021–1030. doi: 10.1016/0092-8674(92)90620-r. [DOI] [PubMed] [Google Scholar]
  8. Krizman D. B., Berget S. M. Efficient selection of 3'-terminal exons from vertebrate DNA. Nucleic Acids Res. 1993 Nov 11;21(22):5198–5202. doi: 10.1093/nar/21.22.5198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. MacDonald C. C., Wilusz J., Shenk T. The 64-kilodalton subunit of the CstF polyadenylation factor binds to pre-mRNAs downstream of the cleavage site and influences cleavage site location. Mol Cell Biol. 1994 Oct;14(10):6647–6654. doi: 10.1128/mcb.14.10.6647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Manley J. L. A complex protein assembly catalyzes polyadenylation of mRNA precursors. Curr Opin Genet Dev. 1995 Apr;5(2):222–228. doi: 10.1016/0959-437x(95)80012-3. [DOI] [PubMed] [Google Scholar]
  11. Moskaitis J. E., Sargent T. D., Smith L. H., Jr, Pastori R. L., Schoenberg D. R. Xenopus laevis serum albumin: sequence of the complementary deoxyribonucleic acids encoding the 68- and 74-kilodalton peptides and the regulation of albumin gene expression by thyroid hormone during development. Mol Endocrinol. 1989 Mar;3(3):464–473. doi: 10.1210/mend-3-3-464. [DOI] [PubMed] [Google Scholar]
  12. Muhlrad D., Decker C. J., Parker R. Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 5'-->3' digestion of the transcript. Genes Dev. 1994 Apr 1;8(7):855–866. doi: 10.1101/gad.8.7.855. [DOI] [PubMed] [Google Scholar]
  13. Murthy K. G., Manley J. L. Characterization of the multisubunit cleavage-polyadenylation specificity factor from calf thymus. J Biol Chem. 1992 Jul 25;267(21):14804–14811. [PubMed] [Google Scholar]
  14. Nesic D., Zhang J., Maquat L. E. Lack of an effect of the efficiency of RNA 3'-end formation on the efficiency of removal of either the final or the penultimate intron in intact cells. Mol Cell Biol. 1995 Jan;15(1):488–496. doi: 10.1128/mcb.15.1.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Pastori R. L., Moskaitis J. E., Buzek S. W., Schoenberg D. R. Coordinate estrogen-regulated instability of serum protein-coding messenger RNAs in Xenopus laevis. Mol Endocrinol. 1991 Apr;5(4):461–468. doi: 10.1210/mend-5-4-461. [DOI] [PubMed] [Google Scholar]
  16. Pastori R. L., Moskaitis J. E., Buzek S. W., Schoenberg D. R. Differential regulation and polyadenylation of transferrin mRNA in Xenopus liver and oviduct. J Steroid Biochem Mol Biol. 1992 Aug;42(7):649–657. doi: 10.1016/0960-0760(92)90105-r. [DOI] [PubMed] [Google Scholar]
  17. Pastori R. L., Moskaitis J. E., Schoenberg D. R. Estrogen-induced ribonuclease activity in Xenopus liver. Biochemistry. 1991 Oct 29;30(43):10490–10498. doi: 10.1021/bi00107a018. [DOI] [PubMed] [Google Scholar]
  18. Riegel A. T., Martin M. B., Schoenberg D. R. Transcriptional and post-transcriptional inhibition of albumin gene expression by estrogen in Xenopus liver. Mol Cell Endocrinol. 1986 Mar;44(3):201–209. doi: 10.1016/0303-7207(86)90125-5. [DOI] [PubMed] [Google Scholar]
  19. Sachs A. B., Kornberg R. D. Nuclear polyadenylate-binding protein. Mol Cell Biol. 1985 Aug;5(8):1993–1996. doi: 10.1128/mcb.5.8.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sachs A., Wahle E. Poly(A) tail metabolism and function in eucaryotes. J Biol Chem. 1993 Nov 5;268(31):22955–22958. [PubMed] [Google Scholar]
  21. Sallés F. J., Strickland S. Rapid and sensitive analysis of mRNA polyadenylation states by PCR. PCR Methods Appl. 1995 Jun;4(6):317–321. doi: 10.1101/gr.4.6.317. [DOI] [PubMed] [Google Scholar]
  22. Schoenberg D. R., Moskaitis J. E., Smith L. H., Jr, Pastori R. L. Extranuclear estrogen-regulated destabilization of Xenopus laevis serum albumin mRNA. Mol Endocrinol. 1989 May;3(5):805–814. doi: 10.1210/mend-3-5-805. [DOI] [PubMed] [Google Scholar]
  23. Sheets M. D., Wickens M. Two phases in the addition of a poly(A) tail. Genes Dev. 1989 Sep;3(9):1401–1412. doi: 10.1101/gad.3.9.1401. [DOI] [PubMed] [Google Scholar]
  24. Sheflin L. G., Brooks E. M., Spaulding S. W. Assessment of transcript polyadenylation by 3' RACE: the response of epidermal growth factor messenger ribonucleic acid to thyroid hormone in the thyroid and submaxillary glands. Endocrinology. 1995 Dec;136(12):5666–5676. doi: 10.1210/endo.136.12.7588322. [DOI] [PubMed] [Google Scholar]
  25. Shyu A. B., Belasco J. G., Greenberg M. E. Two distinct destabilizing elements in the c-fos message trigger deadenylation as a first step in rapid mRNA decay. Genes Dev. 1991 Feb;5(2):221–231. doi: 10.1101/gad.5.2.221. [DOI] [PubMed] [Google Scholar]
  26. Takagaki Y., MacDonald C. C., Shenk T., Manley J. L. The human 64-kDa polyadenylylation factor contains a ribonucleoprotein-type RNA binding domain and unusual auxiliary motifs. Proc Natl Acad Sci U S A. 1992 Feb 15;89(4):1403–1407. doi: 10.1073/pnas.89.4.1403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Varnum S. M., Wormington W. M. Deadenylation of maternal mRNAs during Xenopus oocyte maturation does not require specific cis-sequences: a default mechanism for translational control. Genes Dev. 1990 Dec;4(12B):2278–2286. doi: 10.1101/gad.4.12b.2278. [DOI] [PubMed] [Google Scholar]
  28. Wahle E. A novel poly(A)-binding protein acts as a specificity factor in the second phase of messenger RNA polyadenylation. Cell. 1991 Aug 23;66(4):759–768. doi: 10.1016/0092-8674(91)90119-j. [DOI] [PubMed] [Google Scholar]
  29. Wahle E., Keller W. The biochemistry of 3'-end cleavage and polyadenylation of messenger RNA precursors. Annu Rev Biochem. 1992;61:419–440. doi: 10.1146/annurev.bi.61.070192.002223. [DOI] [PubMed] [Google Scholar]
  30. Wahle E. Poly(A) tail length control is caused by termination of processive synthesis. J Biol Chem. 1995 Feb 10;270(6):2800–2808. doi: 10.1074/jbc.270.6.2800. [DOI] [PubMed] [Google Scholar]
  31. Wilson T., Treisman R. Removal of poly(A) and consequent degradation of c-fos mRNA facilitated by 3' AU-rich sequences. Nature. 1988 Nov 24;336(6197):396–399. doi: 10.1038/336396a0. [DOI] [PubMed] [Google Scholar]
  32. Wormington M., Searfoss A. M., Hurney C. A. Overexpression of poly(A) binding protein prevents maturation-specific deadenylation and translational inactivation in Xenopus oocytes. EMBO J. 1996 Feb 15;15(4):900–909. [PMC free article] [PubMed] [Google Scholar]
  33. Zingg H. H., Lefebvre D. L., Almazan G. Regulation of poly(A) tail size of vasopressin mRNA. J Biol Chem. 1988 Aug 15;263(23):11041–11043. [PubMed] [Google Scholar]

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

RESOURCES