Skip to main content
NCBI home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1989 Mar;9(3):1060–1068. doi: 10.1128/mcb.9.3.1060

Regulation of 2',5'-oligoadenylate synthetase gene expression by interferons and platelet-derived growth factor.

M A Garcia-Blanco 1, P Lengyel 1, E Morrison 1, C Brownlee 1, C D Stiles 1, M Rutherford 1, G Hannigan 1, B R Williams 1
PMCID: PMC362696  PMID: 2542764

Abstract

In murine BALB/c 3T3 cell cultures, either beta interferon or platelet-derived growth factor (PDGF) enhanced expression of the 2',5'-oligoadenylate synthetase mRNA and protein. The time course of induction in response to beta interferon was similar to that in response to PDGF. Of several growth factors known to be present in clotted blood serum (i.e., epidermal growth factor, transforming growth factor beta, and PDGF), only PDGF enhanced expression of 2',5'-oligoadenylate synthetase. The linkage of an interferon response element-containing segment from the 5'-flanking region of a human or murine 2',-5'-oligoadenylate synthetase gene made a heterologous gene responsive to interferon. The expression of such a gene construct in transfected cells was also induced by PDGF. Induction by PDGF was inhibited by mono- or polyclonal antibodies to murine interferon, which suggested that induction by PDGF requires interferon. Both PDGF and interferon induced nuclear factors that bound to this interferon response element-containing segment in vitro.

Full text

PDF
1060

Images in this article

1063Image
on p.1063
1065Image
on p.1065

Selected References

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

  1. 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]
  2. Belardelli F., Gessani S., Proietti E., Locardi C., Borghi P., Watanabe Y., Kawade Y., Gresser I. Studies on the expression of spontaneous and induced interferons in mouse peritoneal macrophages by means of monoclonal antibodies to mouse interferons. J Gen Virol. 1987 Aug;68(Pt 8):2203–2212. doi: 10.1099/0022-1317-68-8-2203. [DOI] [PubMed] [Google Scholar]
  3. Brown G. E., Lebleu B., Kawakita M., Shaila S., Sen G. C., Lengyel P. Increased endonuclease activity in an extract from mouse Ehrlich ascites tumor cells which had been treated with a partially purified interferon preparation: dependence of double-stranded RNA;. Biochem Biophys Res Commun. 1976 Mar 8;69(1):114–122. doi: 10.1016/s0006-291x(76)80280-x. [DOI] [PubMed] [Google Scholar]
  4. Carthew R. W., Chodosh L. A., Sharp P. A. An RNA polymerase II transcription factor binds to an upstream element in the adenovirus major late promoter. Cell. 1985 Dec;43(2 Pt 1):439–448. doi: 10.1016/0092-8674(85)90174-6. [DOI] [PubMed] [Google Scholar]
  5. Chebath J., Benech P., Hovanessian A., Galabru J., Revel M. Four different forms of interferon-induced 2',5'-oligo(A) synthetase identified by immunoblotting in human cells. J Biol Chem. 1987 Mar 15;262(8):3852–3857. [PubMed] [Google Scholar]
  6. Chebath J., Benech P., Revel M., Vigneron M. Constitutive expression of (2'-5') oligo A synthetase confers resistance to picornavirus infection. Nature. 1987 Dec 10;330(6148):587–588. doi: 10.1038/330587a0. [DOI] [PubMed] [Google Scholar]
  7. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Cohen B., Peretz D., Vaiman D., Benech P., Chebath J. Enhancer-like interferon responsive sequences of the human and murine (2'-5') oligoadenylate synthetase gene promoters. EMBO J. 1988 May;7(5):1411–1419. doi: 10.1002/j.1460-2075.1988.tb02958.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dignam J. D., Lebovitz R. M., Roeder R. G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983 Mar 11;11(5):1475–1489. doi: 10.1093/nar/11.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dougherty J. P., Samanta H., Farrell P. J., Lengyel P. Interferon, double-stranded RNA, and RNA degradation. Isolation of homogeneous pppA(2'p5'A)n-1 synthetase from Ehrlich ascites tumor cells. J Biol Chem. 1980 May 10;255(9):3813–3816. [PubMed] [Google Scholar]
  12. Galabru J., Robert N., Buffet-Janvresse C., Rivière Y., Hovanessian A. G. Continuous production of interferon in normal mice: effect of anti-interferon globulin, sex, age, strain and environment on the levels of 2-5A synthetase and p67K kinase. J Gen Virol. 1985 Apr;66(Pt 4):711–718. doi: 10.1099/0022-1317-66-4-711. [DOI] [PubMed] [Google Scholar]
  13. Hannigan G., Williams B. R. Transcriptional regulation of interferon-responsive genes is closely linked to interferon receptor occupancy. EMBO J. 1986 Jul;5(7):1607–1613. doi: 10.1002/j.1460-2075.1986.tb04403.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ilson D. H., Torrence P. F., Vilcek J. Two molecular weight forms of human 2',5'-oligoadenylate synthetase have different activation requirements. J Interferon Res. 1986 Feb;6(1):5–12. doi: 10.1089/jir.1986.6.5. [DOI] [PubMed] [Google Scholar]
  15. Jayaram B. M., Schmidt H., Yoshie O., Lengyel P. Simple procedure for the isolation of mouse interferon-beta. J Interferon Res. 1983;3(2):177–180. doi: 10.1089/jir.1983.3.177. [DOI] [PubMed] [Google Scholar]
  16. Johnston M. I., Hearl W. G. Purification and characterization of a 2'-phosphodiesterase from bovine spleen. J Biol Chem. 1987 Jun 15;262(17):8377–8382. [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. Kohase M., Henriksen-DeStefano D., May L. T., Vilcek J., Sehgal P. B. Induction of beta 2-interferon by tumor necrosis factor: a homeostatic mechanism in the control of cell proliferation. Cell. 1986 Jun 6;45(5):659–666. doi: 10.1016/0092-8674(86)90780-4. [DOI] [PubMed] [Google Scholar]
  19. Krishnan I., Baglioni C. Elevated levels of (2'-5')oligoadenylic acid polymerase activity in growth-arrested human lymphoblastoid Namalva cells. Mol Cell Biol. 1981 Oct;1(10):932–938. doi: 10.1128/mcb.1.10.932. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kumar R., Choubey D., Lengyel P., Sen G. C. Studies on the role of the 2'-5'-oligoadenylate synthetase-RNase L pathway in beta interferon-mediated inhibition of encephalomyocarditis virus replication. J Virol. 1988 Sep;62(9):3175–3181. doi: 10.1128/jvi.62.9.3175-3181.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lengyel P. Biochemistry of interferons and their actions. Annu Rev Biochem. 1982;51:251–282. doi: 10.1146/annurev.bi.51.070182.001343. [DOI] [PubMed] [Google Scholar]
  22. Lin S. L., Ts'o P. O., Hollenberg M. D. Epidermal growth factor-urogastrone action: induction of 2',5'-oligoadenylate synthetase activity and enhancement of the mitogenic effect by anti-interferon antibody. Life Sci. 1983 Mar 28;32(13):1479–1488. doi: 10.1016/0024-3205(83)90914-1. [DOI] [PubMed] [Google Scholar]
  23. Luckow B., Schütz G. CAT constructions with multiple unique restriction sites for the functional analysis of eukaryotic promoters and regulatory elements. Nucleic Acids Res. 1987 Jul 10;15(13):5490–5490. doi: 10.1093/nar/15.13.5490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nilsen T. W., Wood D. L., Baglioni C. Presence of 2',5'-oligo(A) and of enzymes that synthesize, bind, and degrade 2',5'-oligo(A) in HeLa cell nuclei. J Biol Chem. 1982 Feb 25;257(4):1602–1605. [PubMed] [Google Scholar]
  25. Pestka S., Langer J. A., Zoon K. C., Samuel C. E. Interferons and their actions. Annu Rev Biochem. 1987;56:727–777. doi: 10.1146/annurev.bi.56.070187.003455. [DOI] [PubMed] [Google Scholar]
  26. Pledger W. J., Stiles C. D., Antoniades H. N., Scher C. D. Induction of DNA synthesis in BALB/c 3T3 cells by serum components: reevaluation of the commitment process. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4481–4485. doi: 10.1073/pnas.74.10.4481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Porter A. C., Chernajovsky Y., Dale T. C., Gilbert C. S., Stark G. R., Kerr I. M. Interferon response element of the human gene 6-16. EMBO J. 1988 Jan;7(1):85–92. doi: 10.1002/j.1460-2075.1988.tb02786.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ratner L., Wiegand R. C., Farrell P. J., Sen G. C., Cabrer B., Lengyel P. Interferon, double-stranded RNA and RNA degradation. Fractionation of the endonucleaseINT system into two macromolecular components; role of a small molecule in nuclease activation. Biochem Biophys Res Commun. 1978 Apr 14;81(3):947–954. doi: 10.1016/0006-291x(78)91443-2. [DOI] [PubMed] [Google Scholar]
  29. Resnitzky D., Yarden A., Zipori D., Kimchi A. Autocrine beta-related interferon controls c-myc suppression and growth arrest during hematopoietic cell differentiation. Cell. 1986 Jul 4;46(1):31–40. doi: 10.1016/0092-8674(86)90857-3. [DOI] [PubMed] [Google Scholar]
  30. Revel M. F., Kimchi A. Initial characterization of a spontaneous interferon secreted during growth and differentiation of Friend erythroleukemia cells. Mol Cell Biol. 1982 Dec;2(12):1472–1480. doi: 10.1128/mcb.2.12.1472. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  32. Roberts W. K., Hovanessian A., Brown R. E., Clemens M. J., Kerr I. M. Interferon-mediated protein kinase and low-molecular-weight inhibitor of protein synthesis. Nature. 1976 Dec 2;264(5585):477–480. doi: 10.1038/264477a0. [DOI] [PubMed] [Google Scholar]
  33. Ross R., Raines E. W., Bowen-Pope D. F. The biology of platelet-derived growth factor. Cell. 1986 Jul 18;46(2):155–169. doi: 10.1016/0092-8674(86)90733-6. [DOI] [PubMed] [Google Scholar]
  34. Rutherford M. N., Hannigan G. E., Williams B. R. Interferon-induced binding of nuclear factors to promoter elements of the 2-5A synthetase gene. EMBO J. 1988 Mar;7(3):751–759. doi: 10.1002/j.1460-2075.1988.tb02872.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Saarma M., Toots U., Raukas E., Zhelkovsky A., Pivazian A., Neuman T. Nerve growth factor induces changes in (2'-5')oligo(A) synthetase and 2'-phosphodiesterase activities during differentiation of PC12 pheochromocytoma cells. Exp Cell Res. 1986 Sep;166(1):229–236. doi: 10.1016/0014-4827(86)90522-7. [DOI] [PubMed] [Google Scholar]
  36. Saunders M., Gewert D., Castelino M., Rutherford M., Flenniken A., Willard H., Williams B. R. Characterization of the small 2-5A synthetase gene in human and mouse cells. Prog Clin Biol Res. 1985;202:163–174. [PubMed] [Google Scholar]
  37. Schmidt A., Chernajovsky Y., Shulman L., Federman P., Berissi H., Revel M. An interferon-induced phosphodiesterase degrading (2'-5') oligoisoadenylate and the C-C-A terminus of tRNA. Proc Natl Acad Sci U S A. 1979 Oct;76(10):4788–4792. doi: 10.1073/pnas.76.10.4788. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Singh H., LeBowitz J. H., Baldwin A. S., Jr, Sharp P. A. Molecular cloning of an enhancer binding protein: isolation by screening of an expression library with a recognition site DNA. Cell. 1988 Feb 12;52(3):415–423. doi: 10.1016/s0092-8674(88)80034-5. [DOI] [PubMed] [Google Scholar]
  39. Singh J. P., Chaikin M. A., Stiles C. D. Phylogenetic analysis of platelet-derived growth factor by radio-receptor assay. J Cell Biol. 1982 Nov;95(2 Pt 1):667–671. doi: 10.1083/jcb.95.2.667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Smekens-Etienne M., Goldstein J., Ooms H. A., Dumont J. E. Variation of (2'-5')oligo(adenylate) synthetase activity during rat-liver regeneration. Eur J Biochem. 1983 Feb 1;130(2):269–273. doi: 10.1111/j.1432-1033.1983.tb07146.x. [DOI] [PubMed] [Google Scholar]
  41. St Laurent G., Yoshie O., Floyd-Smith G., Samanta H., Sehgal P. B., Lengyel P. Interferon action: two (2'-5')(A)n synthetases specified by distinct mRNAs in Ehrlich ascites tumor cells treated with interferon. Cell. 1983 May;33(1):95–102. doi: 10.1016/0092-8674(83)90338-0. [DOI] [PubMed] [Google Scholar]
  42. Weber H., Valenzuela D., Lujber G., Gubler M., Weissmann C. Single amino acid changes that render human IFN-alpha 2 biologically active on mouse cells. EMBO J. 1987 Mar;6(3):591–598. doi: 10.1002/j.1460-2075.1987.tb04795.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Wells J. A., Swyryd E. A., Stark G. R. An improved method for purifying 2',5'-oligoadenylate synthetases. J Biol Chem. 1984 Jan 25;259(2):1363–1370. [PubMed] [Google Scholar]
  44. Wells V., Mallucci L. Expression of the 2-5A system during the cell cycle. Exp Cell Res. 1985 Jul;159(1):27–36. doi: 10.1016/s0014-4827(85)80034-3. [DOI] [PubMed] [Google Scholar]
  45. Yang K., Samanta H., Dougherty J., Jayaram B., Broeze R., Lengyel P. Interferons, double-stranded RNA, and RNA degradation. Isolation and characterization of homogeneous human (2'-5')(a)n synthetase. J Biol Chem. 1981 Sep 10;256(17):9324–9328. [PubMed] [Google Scholar]
  46. Yarden A., Shure-Gottlieb H., Chebath J., Revel M., Kimchi A. Autogenous production of interferon-beta switches on HLA genes during differentiation of histiocytic lymphoma U937 cells. EMBO J. 1984 May;3(5):969–973. doi: 10.1002/j.1460-2075.1984.tb01915.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Zullo J. N., Cochran B. H., Huang A. S., Stiles C. D. Platelet-derived growth factor and double-stranded ribonucleic acids stimulate expression of the same genes in 3T3 cells. Cell. 1985 Dec;43(3 Pt 2):793–800. doi: 10.1016/0092-8674(85)90252-1. [DOI] [PubMed] [Google Scholar]

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

RESOURCES