Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1979 Oct;76(10):4788–4792. doi: 10.1073/pnas.76.10.4788

An interferon-induced phosphodiesterase degrading (2'-5') oligoisoadenylate and the C-C-A terminus of tRNA.

A Schmidt, Y Chernajovsky, L Shulman, P Federman, H Berissi, M Revel
PMCID: PMC413022  PMID: 228264

Abstract

A phosphodiesterase characterized by a generally higher activity on 2'-5' than on 3'-5' phosphodiester bonds was isolated from mouse L cells treated with interferon. A similar enzyme was purified from mouse reticulocytes. The phosphodiesterase 2'-PDi splits the 2'-phosphate bond of pppA2'p5'A2'p5'A, the oligonucleotide activator of ribonuclease F. The level of phosphodiesterase 2'-PDi is increased by interferon treatment of L cells. The phosphodiesterase was also shown to degrade the C-C-A terminus of tRNA and to reduce the amino acid acceptance of tRNA in cell-free extracts, thereby causing a tRNA-reversible inhibition of mRNA translation.

Full text

PDF
4788

Images in this article

4789Image
on p.4789
4790Image
on p.4790

Selected References

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

  1. ANDERSON E. P., HEPPEL L. A. Purification and properties of a leukemic cell phosphodiesterase. Biochim Biophys Acta. 1960 Sep 9;43:79–89. doi: 10.1016/0006-3002(60)90409-1. [DOI] [PubMed] [Google Scholar]
  2. Baglioni C. Interferon-induced enzymatic activities and their role in the antriviral state. Cell. 1979 Jun;17(2):255–264. doi: 10.1016/0092-8674(79)90151-x. [DOI] [PubMed] [Google Scholar]
  3. Baglioni C., Minks M. A., Maroney P. A. Interferon action may be mediated by activation of a nuclease by pppA2'p5'A2'p5'A. Nature. 1978 Jun 22;273(5664):684–687. doi: 10.1038/273684a0. [DOI] [PubMed] [Google Scholar]
  4. Ball L. A., White C. N. Oligonucleotide inhibitor of protein synthesis made in extracts of interferon-treated chick embryo cells: comparison with the mouse low molecular weight inhibitor. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1167–1171. doi: 10.1073/pnas.75.3.1167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bastos R. N., Volloch Z., Aviv H. Messenger RNA population analysis during erythroid differentiation: a kinetical approach. J Mol Biol. 1977 Feb 25;110(2):191–203. doi: 10.1016/s0022-2836(77)80068-5. [DOI] [PubMed] [Google Scholar]
  6. Chernajovsky Y., Kimchi A., Schmidt A., Zilberstein A., Revel M. Differential effects of two interferon-induced translational inhibitors on initiation of protein synthesis. Eur J Biochem. 1979 May 2;96(1):35–41. doi: 10.1111/j.1432-1033.1979.tb13010.x. [DOI] [PubMed] [Google Scholar]
  7. Clemens M. J., Williams B. R. Inhibition of cell-free protein synthesis by pppA2'p5'A2'p5'A: a novel oligonucleotide synthesized by interferon-treated L cell extracts. Cell. 1978 Mar;13(3):565–572. doi: 10.1016/0092-8674(78)90329-x. [DOI] [PubMed] [Google Scholar]
  8. Content J., Lebleu B., Nudel U., Zilberstein A., Berissi H., Revel M. Blocks in elongation and initiation of protein synthesis induced by interferon treatment in mouse L cells. Eur J Biochem. 1975 May;54(1):1–10. doi: 10.1111/j.1432-1033.1975.tb04106.x. [DOI] [PubMed] [Google Scholar]
  9. Cuatrecasas P. Protein purification by affinity chromatography. Derivatizations of agarose and polyacrylamide beads. J Biol Chem. 1970 Jun;245(12):3059–3065. [PubMed] [Google Scholar]
  10. DANIEL V., LITTAUER U. Z. Incorporation of terminal ribonucleotides into soluble ribonucleic acid by a purified rat liver enzyme. J Biol Chem. 1963 Jun;238:2102–2112. [PubMed] [Google Scholar]
  11. Eppstein D. A., Samuel C. E. Mechanism of interferon action. Properties of an interferon-mediated ribonucleolytic activity from mouse L929 cells. Virology. 1978 Aug;89(1):240–251. doi: 10.1016/0042-6822(78)90056-9. [DOI] [PubMed] [Google Scholar]
  12. Falcoff R., Falcoff E., Sanceau J., Lewis J. A. Influence of preincubation on the development of the inhibition of protein synthesis in extracts from interferon-treated mouse L cells. Action on tRNA. Virology. 1978 May 15;86(2):507–515. doi: 10.1016/0042-6822(78)90089-2. [DOI] [PubMed] [Google Scholar]
  13. Farrell P. J., Balkow K., Hunt T., Jackson R. J., Trachsel H. Phosphorylation of initiation factor elF-2 and the control of reticulocyte protein synthesis. Cell. 1977 May;11(1):187–200. doi: 10.1016/0092-8674(77)90330-0. [DOI] [PubMed] [Google Scholar]
  14. Farrell P. J., Sen G. C., Dubois M. F., Ratner L., Slattery E., Lengyel P. Interferon action: two distinct pathways for inhibition of protein synthesis by double-stranded RNA. Proc Natl Acad Sci U S A. 1978 Dec;75(12):5893–5897. doi: 10.1073/pnas.75.12.5893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hovanessian A. G., Kerr I. M. Synthesis of an oligonucleotide inhibitor of protein synthesis in rabbit reticulocyte lysates analogous to that formed in extracts from interferon-treated cells. Eur J Biochem. 1978 Mar;84(1):149–159. doi: 10.1111/j.1432-1033.1978.tb12151.x. [DOI] [PubMed] [Google Scholar]
  16. Kerr I. M., Brown R. E., Hovanessian A. G. Nature of inhibitor of cell-free protein synthesis formed in response to interferon and double-stranded RNA. Nature. 1977 Aug 11;268(5620):540–542. doi: 10.1038/268540a0. [DOI] [PubMed] [Google Scholar]
  17. Kerr I. M., Brown R. E. pppA2'p5'A2'p5'A: an inhibitor of protein synthesis synthesized with an enzyme fraction from interferon-treated cells. Proc Natl Acad Sci U S A. 1978 Jan;75(1):256–260. doi: 10.1073/pnas.75.1.256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kimchi A., Shulman L., Schmidt A., Chernajovsky Y., Fradin A., Revel M. Kinetics of the induction of three translation-regulatory enzymes by interferon. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3208–3212. doi: 10.1073/pnas.76.7.3208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lewis J. A., Falcoff E., Falcoff R. Dual action of double-stranded RNA inhibiting protein synthesis in extracts of interferon-treated mouse L cells. Translation is impaired at the level of initiation and by mRNA degradation. Eur J Biochem. 1978 May 16;86(2):497–509. doi: 10.1111/j.1432-1033.1978.tb12333.x. [DOI] [PubMed] [Google Scholar]
  20. Mayr U., Bermayer H. P., Weidinger G., Jungwirth C. Release of interferon-induced translation inhibition by tRNA in cell-free extracts from mouse erythroleukemia cells. Eur J Biochem. 1977 Jun 15;76(2):541–551. doi: 10.1111/j.1432-1033.1977.tb11624.x. [DOI] [PubMed] [Google Scholar]
  21. Minks M. A., Benvin S., Maroney P. A., Baglioni C. Metabolic stability of 2' 5'oligo (A) and activity of 2' 5'oligo (A)-dependent endonuclease in extracts of interferon-treated and control HeLa cells. Nucleic Acids Res. 1979 Feb;6(2):767–780. doi: 10.1093/nar/6.2.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Richards G. M., Tutas D. J., Wechter W. J., Laskowski M., Sr Hydrolysis of dinucleoside monophosphates containing arabinose in various internucleotide linkages by exonuclease from the venom of Crotalus adamanteus. Biochemistry. 1967 Sep;6(9):2908–2914. doi: 10.1021/bi00861a035. [DOI] [PubMed] [Google Scholar]
  23. Samuel C. E. Mechanism of interferon action. Studies on the mechanism of interferon-mediated inhibition of reovirus messenger RNA translation in cell-free protein synthesis systems from mouse ascites tumor cells. Virology. 1976 Nov;75(1):166–176. doi: 10.1016/0042-6822(76)90015-5. [DOI] [PubMed] [Google Scholar]
  24. Schmidt A., Zilberstein A., Shulman L., Federman P., Berissi H., Revel M. Interferon action: isolation of nuclease F, a translation inhibitor activated by interferon-induced (2'-5') oligo-isoadenylate. FEBS Lett. 1978 Nov 15;95(2):257–264. doi: 10.1016/0014-5793(78)81006-0. [DOI] [PubMed] [Google Scholar]
  25. Sela I., Grossberg S. E., Sedmak J. J., Mehler A. H. Discharge of aminoacyl-viral RNA by a factor from interferon-treated cells. Science. 1976 Oct 29;194(4264):527–529. doi: 10.1126/science.973135. [DOI] [PubMed] [Google Scholar]
  26. Sen G. C., Gupta S. L., Brown G. E., Lebleu B., Rebello M. A., Lengyel P. Interferon treatment of Ehrlich ascites tumor cells: effects on exogenous mRNA translation and tRNA inactivation in the cell extract. J Virol. 1975 Jan;17(1):191–203. doi: 10.1128/jvi.17.1.191-203.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sen G. C., Lebleu B., Brown G. E., Kawakita M., Slattery E., Lengyel P. Interferon, double-stranded RNA and mRNA degradation. Nature. 1976 Nov 25;264(5584):370–373. doi: 10.1038/264370a0. [DOI] [PubMed] [Google Scholar]
  28. Sporn M. B., Lazarus H. M., Smith J. M., Henderson W. R. Studies on nuclear exoribonucleases. 3. Isolation and properties of the enzyme from normal and malignant tissues of the mouse. Biochemistry. 1969 Apr;8(4):1698–1706. doi: 10.1021/bi00832a053. [DOI] [PubMed] [Google Scholar]
  29. Weissenbach J., Dirheimer G., Falcoff R., Sanceau J., Falcoff E. Yeast tRNALeu (anticodon U--A--G) translates all six leucine codons in extracts from interferon treated cells. FEBS Lett. 1977 Oct 1;82(1):71–76. doi: 10.1016/0014-5793(77)80888-0. [DOI] [PubMed] [Google Scholar]
  30. Williams B. R., Kerr I. M., Gilbert C. S., White C. N., Ball L. A. Synthesis and breakdown of pppA2'p5'A2'p5'A and transient inhibiton of protein synthesis in extracts from interferon-treated and control cells. Eur J Biochem. 1978 Dec;92(2):455–462. doi: 10.1111/j.1432-1033.1978.tb12767.x. [DOI] [PubMed] [Google Scholar]
  31. Zilberstein A., Dudock B., Berissi H., Revel M. Control of messenger RNA translation by minor species of leucyl-transfer RNA in extracts from interferon-treated L cells. J Mol Biol. 1976 Nov;108(1):43–54. doi: 10.1016/s0022-2836(76)80093-9. [DOI] [PubMed] [Google Scholar]
  32. Zilberstein A., Kimchi A., Schmidt A., Revel M. Isolation of two interferon-induced translational inhibitors: a protein kinase and an oligo-isoadenylate synthetase. Proc Natl Acad Sci U S A. 1978 Oct;75(10):4734–4738. doi: 10.1073/pnas.75.10.4734. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES