Skip to main content
PMC home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1996 Mar 1;24(5):970–976. doi: 10.1093/nar/24.5.970

A binding factor for interleukin 2 mRNA.

J Hua 1, V Paetkau 1
PMCID: PMC145722  PMID: 8600467

Abstract

Jurkat cells, a human T lymphocyte line that can be induced to synthesize and secrete interleukin 2, contain a factor that binds interleukin 2 mRNA. Binding can be demonstrated by formation of a complex detectable by gel electrophoresis. The binding is sequence specific and occurs in the 3'-non-coding region, within 160 nt of the end of the coding region, at or near a site on the mRNA that is rich in A and U residues. However, it appears not to be due to known AU binding factors. The factor is protease sensitive and binds non-covalently to interleukin 2 mRNA. It behaves like a protein of molecular weight 50 000-60 000 after UV-induced cross-linking to the mRNA. Preparations of the binding factor also protect interleukin 2 mRNA against degradation by a recently described RNasin-resistant endoribonuclease activity in Jurkat cells. Protection occurs under the same conditions required to generate the gel-retarded complex.

Full Text

The Full Text of this article is available as a PDF (141.6 KB).

Selected References

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

  1. Alberta J. A., Rundell K., Stiles C. D. Identification of an activity that interacts with the 3'-untranslated region of c-myc mRNA and the role of its target sequence in mediating rapid mRNA degradation. J Biol Chem. 1994 Feb 11;269(6):4532–4538. [PubMed] [Google Scholar]
  2. Amara F. M., Chen F. Y., Wright J. A. A novel transforming growth factor-beta 1 responsive cytoplasmic trans-acting factor binds selectively to the 3'-untranslated region of mammalian ribonucleotide reductase R2 mRNA: role in message stability. Nucleic Acids Res. 1993 Oct 11;21(20):4803–4809. doi: 10.1093/nar/21.20.4803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Anderson J. T., Paddy M. R., Swanson M. S. PUB1 is a major nuclear and cytoplasmic polyadenylated RNA-binding protein in Saccharomyces cerevisiae. Mol Cell Biol. 1993 Oct;13(10):6102–6113. doi: 10.1128/mcb.13.10.6102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bernstein P. L., Herrick D. J., Prokipcak R. D., Ross J. Control of c-myc mRNA half-life in vitro by a protein capable of binding to a coding region stability determinant. Genes Dev. 1992 Apr;6(4):642–654. doi: 10.1101/gad.6.4.642. [DOI] [PubMed] [Google Scholar]
  5. Bickel M., Cohen R. B., Pluznik D. H. Post-transcriptional regulation of granulocyte-macrophage colony-stimulating factor synthesis in murine T cells. J Immunol. 1990 Aug 1;145(3):840–845. [PubMed] [Google Scholar]
  6. Bickel M., Iwai Y., Pluznik D. H., Cohen R. B. Binding of sequence-specific proteins to the adenosine- plus uridine-rich sequences of the murine granulocyte/macrophage colony-stimulating factor mRNA. Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10001–10005. doi: 10.1073/pnas.89.21.10001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Blobel G., Potter V. R. Relation of ribonuclease and ribonuclease inhibitor to the isolation of polysomes from rat liver. Proc Natl Acad Sci U S A. 1966 May;55(5):1283–1288. doi: 10.1073/pnas.55.5.1283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bohjanen P. R., Petryniak B., June C. H., Thompson C. B., Lindsten T. AU RNA-binding factors differ in their binding specificities and affinities. J Biol Chem. 1992 Mar 25;267(9):6302–6309. [PubMed] [Google Scholar]
  9. Bohjanen P. R., Petryniak B., June C. H., Thompson C. B., Lindsten T. An inducible cytoplasmic factor (AU-B) binds selectively to AUUUA multimers in the 3' untranslated region of lymphokine mRNA. Mol Cell Biol. 1991 Jun;11(6):3288–3295. doi: 10.1128/mcb.11.6.3288. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Brewer G., Ross J. Poly(A) shortening and degradation of the 3' A+U-rich sequences of human c-myc mRNA in a cell-free system. Mol Cell Biol. 1988 Apr;8(4):1697–1708. doi: 10.1128/mcb.8.4.1697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Brown B. D., Zipkin I. D., Harland R. M. Sequence-specific endonucleolytic cleavage and protection of mRNA in Xenopus and Drosophila. Genes Dev. 1993 Aug;7(8):1620–1631. doi: 10.1101/gad.7.8.1620. [DOI] [PubMed] [Google Scholar]
  12. Caput D., Beutler B., Hartog K., Thayer R., Brown-Shimer S., Cerami A. Identification of a common nucleotide sequence in the 3'-untranslated region of mRNA molecules specifying inflammatory mediators. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1670–1674. doi: 10.1073/pnas.83.6.1670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cerdan C., Martin Y., Courcoul M., Mawas C., Birg F., Olive D. CD28 costimulation up-regulates long-term IL-2R beta expression in human T cells through combined transcriptional and post-transcriptional regulation. J Immunol. 1995 Feb 1;154(3):1007–1013. [PubMed] [Google Scholar]
  14. Chen C. Y., You Y., Shyu A. B. Two cellular proteins bind specifically to a purine-rich sequence necessary for the destabilization function of a c-fos protein-coding region determinant of mRNA instability. Mol Cell Biol. 1992 Dec;12(12):5748–5757. doi: 10.1128/mcb.12.12.5748. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Chen F. Y., Amara F. M., Wright J. A. Regulation of mammalian ribonucleotide reductase R1 mRNA stability is mediated by a ribonucleotide reductase R1 mRNA 3'-untranslated region cis-trans interaction through a protein kinase C-controlled pathway. Biochem J. 1994 Aug 15;302(Pt 1):125–132. doi: 10.1042/bj3020125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Cormack R. S., Genereaux J. L., Mackie G. A. RNase E activity is conferred by a single polypeptide: overexpression, purification, and properties of the ams/rne/hmp1 gene product. Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):9006–9010. doi: 10.1073/pnas.90.19.9006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Czyzyk-Krzeska M. F., Dominski Z., Kole R., Millhorn D. E. Hypoxia stimulates binding of a cytoplasmic protein to a pyrimidine-rich sequence in the 3'-untranslated region of rat tyrosine hydroxylase mRNA. J Biol Chem. 1994 Apr 1;269(13):9940–9945. [PubMed] [Google Scholar]
  18. Deutscher M. P. Ribonuclease multiplicity, diversity, and complexity. J Biol Chem. 1993 Jun 25;268(18):13011–13014. [PubMed] [Google Scholar]
  19. Dodson R. E., Shapiro D. J. An estrogen-inducible protein binds specifically to a sequence in the 3' untranslated region of estrogen-stabilized vitellogenin mRNA. Mol Cell Biol. 1994 May;14(5):3130–3138. doi: 10.1128/mcb.14.5.3130. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gillis S., Watson J. Biochemical and biological characterization of lymphocyte regulatory molecules. V. Identification of an interleukin 2-producing human leukemia T cell line. J Exp Med. 1980 Dec 1;152(6):1709–1719. doi: 10.1084/jem.152.6.1709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hargrove J. L., Schmidt F. H. The role of mRNA and protein stability in gene expression. FASEB J. 1989 Oct;3(12):2360–2370. doi: 10.1096/fasebj.3.12.2676679. [DOI] [PubMed] [Google Scholar]
  22. Hua J., Garner R., Paetkau V. An RNasin-resistant ribonuclease selective for interleukin 2 mRNA. Nucleic Acids Res. 1993 Jan 11;21(1):155–162. doi: 10.1093/nar/21.1.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Krikorian C. R., Read G. S. In vitro mRNA degradation system to study the virion host shutoff function of herpes simplex virus. J Virol. 1991 Jan;65(1):112–122. doi: 10.1128/jvi.65.1.112-122.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lindstein T., June C. H., Ledbetter J. A., Stella G., Thompson C. B. Regulation of lymphokine messenger RNA stability by a surface-mediated T cell activation pathway. Science. 1989 Apr 21;244(4902):339–343. doi: 10.1126/science.2540528. [DOI] [PubMed] [Google Scholar]
  25. Malter J. S. Identification of an AUUUA-specific messenger RNA binding protein. Science. 1989 Nov 3;246(4930):664–666. doi: 10.1126/science.2814487. [DOI] [PubMed] [Google Scholar]
  26. Mudd E. A., Higgins C. F. Escherichia coli endoribonuclease RNase E: autoregulation of expression and site-specific cleavage of mRNA. Mol Microbiol. 1993 Aug;9(3):557–568. doi: 10.1111/j.1365-2958.1993.tb01716.x. [DOI] [PubMed] [Google Scholar]
  27. Pei R., Calame K. Differential stability of c-myc mRNAS in a cell-free system. Mol Cell Biol. 1988 Jul;8(7):2860–2868. doi: 10.1128/mcb.8.7.2860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Prokipcak R. D., Herrick D. J., Ross J. Purification and properties of a protein that binds to the C-terminal coding region of human c-myc mRNA. J Biol Chem. 1994 Mar 25;269(12):9261–9269. [PubMed] [Google Scholar]
  29. Raj N. B., Pitha P. M. 65-kDa protein binds to destabilizing sequences in the IFN-beta mRNA coding and 3' UTR. FASEB J. 1993 May;7(8):702–710. doi: 10.1096/fasebj.7.8.8500695. [DOI] [PubMed] [Google Scholar]
  30. Rajagopalan L. E., Malter J. S. Modulation of granulocyte-macrophage colony-stimulating factor mRNA stability in vitro by the adenosine-uridine binding factor. J Biol Chem. 1994 Sep 30;269(39):23882–23888. [PubMed] [Google Scholar]
  31. Rodgers J. R., Johnson M. L., Rosen J. M. Measurement of mRNA concentration and mRNA half-life as a function of hormonal treatment. Methods Enzymol. 1985;109:572–592. doi: 10.1016/0076-6879(85)09116-9. [DOI] [PubMed] [Google Scholar]
  32. Ross J., Kobs G., Brewer G., Peltz S. W. Properties of the exonuclease activity that degrades H4 histone mRNA. J Biol Chem. 1987 Jul 5;262(19):9374–9381. [PubMed] [Google Scholar]
  33. Shapiro R., Vallee B. L. Interaction of human placental ribonuclease with placental ribonuclease inhibitor. Biochemistry. 1991 Feb 26;30(8):2246–2255. doi: 10.1021/bi00222a030. [DOI] [PubMed] [Google Scholar]
  34. Shaw G., Kamen R. A conserved AU sequence from the 3' untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell. 1986 Aug 29;46(5):659–667. doi: 10.1016/0092-8674(86)90341-7. [DOI] [PubMed] [Google Scholar]
  35. Shaw J., Meerovitch K., Bleackley R. C., Paetkau V. Mechanisms regulating the level of IL-2 mRNA in T lymphocytes. J Immunol. 1988 Apr 1;140(7):2243–2248. [PubMed] [Google Scholar]
  36. Taniguchi T., Matsui H., Fujita T., Takaoka C., Kashima N., Yoshimoto R., Hamuro J. Structure and expression of a cloned cDNA for human interleukin-2. Nature. 1983 Mar 24;302(5906):305–310. doi: 10.1038/302305a0. [DOI] [PubMed] [Google Scholar]
  37. Vicentini A. M., Kieffer B., Matthies R., Meyhack B., Hemmings B. A., Stone S. R., Hofsteenge J. Protein chemical and kinetic characterization of recombinant porcine ribonuclease inhibitor expressed in Saccharomyces cerevisiae. Biochemistry. 1990 Sep 18;29(37):8827–8834. doi: 10.1021/bi00489a046. [DOI] [PubMed] [Google Scholar]
  38. Wager R. E., Assoian R. K. A phorbol ester-regulated ribonuclease system controlling transforming growth factor beta 1 gene expression in hematopoietic cells. Mol Cell Biol. 1990 Nov;10(11):5983–5990. doi: 10.1128/mcb.10.11.5983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Wager R. E., Scotto L., Assoian R. K. Analysis of transforming growth factor beta 1 messenger RNA degradation by the transcript-selective, 12-O-tetradecanoylphorbol-13-acetate-regulated ribonuclease system from U937 promonocytes. Cell Growth Differ. 1994 Feb;5(2):117–124. [PubMed] [Google Scholar]
  40. Wisdom R., Lee W. The protein-coding region of c-myc mRNA contains a sequence that specifies rapid mRNA turnover and induction by protein synthesis inhibitors. Genes Dev. 1991 Feb;5(2):232–243. doi: 10.1101/gad.5.2.232. [DOI] [PubMed] [Google Scholar]
  41. Wodnar-Filipowicz A., Moroni C. Regulation of interleukin 3 mRNA expression in mast cells occurs at the posttranscriptional level and is mediated by calcium ions. Proc Natl Acad Sci U S A. 1990 Jan;87(2):777–781. doi: 10.1073/pnas.87.2.777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Zaidi S. H., Malter J. S. Amyloid precursor protein mRNA stability is controlled by a 29-base element in the 3'-untranslated region. J Biol Chem. 1994 Sep 30;269(39):24007–24013. [PubMed] [Google Scholar]
  43. Zhang W., Wagner B. J., Ehrenman K., Schaefer A. W., DeMaria C. T., Crater D., DeHaven K., Long L., Brewer G. Purification, characterization, and cDNA cloning of an AU-rich element RNA-binding protein, AUF1. Mol Cell Biol. 1993 Dec;13(12):7652–7665. doi: 10.1128/mcb.13.12.7652. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES