Skip to main content
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
. 1989 Apr;86(7):2243–2247. doi: 10.1073/pnas.86.7.2243

Signal transduction pathways in the induction of 2',5'-oligoadenylate synthetase gene expression by interferon alpha/beta.

C Yan 1, P B Sehgal 1, I Tamm 1
PMCID: PMC286888  PMID: 2538838

Abstract

Treatment of quiescent BALB/c mouse 3T3 cells with murine interferon alpha/beta (IFN-alpha/beta) (1000 units/ml) leads to the appearance at 4 hr of 1.7-kilobase 2',5'-oligoadenylate (2',5'-OAS)mRNA as detected by Northern blot analysis. This mRNA accumulates for at least 18 hr. Two protein kinase C activators, 1,2-dioctanoyl glycerol and phorbol 12-myristate 13-acetate, suppress, whereas the calcium ionophore ionomycin enhances, the IFN-alpha/beta-induced expression of 2',5'-OAS mRNA. The 8-bromo and dibutyryl analogs of cAMP and the adenylate cyclase activator forskolin did not affect the induction of 2',5'-OAS mRNA by IFN-alpha/beta. In the absence of IFN-alpha/beta, the above agents used either singly or in combinations, did not induce 2',5'-OAS mRNA expression nor did platelet-derived growth factor (1-2 units/ml), fibroblast growth factor (6-100 ng/ml), or bovine serum (10-20%). Bovine serum also did not affect 2',5'-OAS mRNA induction by IFN-alpha/beta. The poly(ADP)-ribose synthetase inhibitor 3-aminobenzamide suppressed IFN-alpha/beta-induced 2',5'-OAS gene expression. These results suggest that in quiescent BALB/c 3T3 cells (i) the 2',5'-OAS gene is not responsive to the three major signal transduction pathways activated by diacylglycerol, Ca2+, and cAMP; (ii) induction of the 2',5'-OAS gene by IFN-alpha/beta is decreased by activation of the protein kinase C pathway but enhanced by elevation of intracellular [Ca2+].

Full text

PDF
2243

Images in this article

Selected References

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

  1. Aguet M. High-affinity binding of 125I-labelled mouse interferon to a specific cell surface receptor. Nature. 1980 Apr 3;284(5755):459–461. doi: 10.1038/284459a0. [DOI] [PubMed] [Google Scholar]
  2. Benech P., Vigneron M., Peretz D., Revel M., Chebath J. Interferon-responsive regulatory elements in the promoter of the human 2',5'-oligo(A) synthetase gene. Mol Cell Biol. 1987 Dec;7(12):4498–4504. doi: 10.1128/mcb.7.12.4498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berridge M. J., Heslop J. P., Irvine R. F., Brown K. D. Inositol lipids and cell proliferation. Biochem Soc Trans. 1985 Feb;13(1):67–71. doi: 10.1042/bst0130067. [DOI] [PubMed] [Google Scholar]
  4. Branca A. A., Baglioni C. Evidence that types I and II interferons have different receptors. Nature. 1981 Dec 24;294(5843):768–770. doi: 10.1038/294768a0. [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. 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]
  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. Czarniecki C. W., Sreevalsan T., Friedman R. M., Panet A. Dissociation of interferon effects on murine leukemia virus and encephalomyocarditis virus replication in mouse cells. J Virol. 1981 Feb;37(2):827–831. doi: 10.1128/jvi.37.2.827-831.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Exley R., Gordon J., Clemens M. J. Induction of B-cell differentiation antigens in interferon- or phorbol ester-treated Daudi cells is impaired by inhibitors of ADP-ribosyltransferase. Proc Natl Acad Sci U S A. 1987 Sep;84(18):6467–6470. doi: 10.1073/pnas.84.18.6467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Exton J. H. Mechanisms of action of calcium-mobilizing agonists: some variations on a young theme. FASEB J. 1988 Aug;2(11):2670–2676. doi: 10.1096/fasebj.2.11.2456243. [DOI] [PubMed] [Google Scholar]
  13. Hall D. J., Stiles C. D. Platelet-derived growth factor-inducible genes respond differentially to at least two distinct intracellular second messengers. J Biol Chem. 1987 Nov 5;262(31):15302–15308. [PubMed] [Google Scholar]
  14. Kaibuchi K., Tsuda T., Kikuchi A., Tanimoto T., Yamashita T., Takai Y. Possible involvement of protein kinase C and calcium ion in growth factor-induced expression of c-myc oncogene in Swiss 3T3 fibroblasts. J Biol Chem. 1986 Jan 25;261(3):1187–1192. [PubMed] [Google Scholar]
  15. Kelly J. M., Gilbert C. S., Stark G. R., Kerr I. M. Differential regulation of interferon-induced mRNAs and c-myc mRNA by alpha- and gamma-interferons. Eur J Biochem. 1985 Dec 2;153(2):367–371. doi: 10.1111/j.1432-1033.1985.tb09312.x. [DOI] [PubMed] [Google Scholar]
  16. Kusari J., Sen G. C. Transcriptional analyses of interferon-inducible mRNAs. Mol Cell Biol. 1987 Jan;7(1):528–531. doi: 10.1128/mcb.7.1.528. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Lin S. L., Kikuchi T., Pledger W. J., Tamm I. Interferon inhibits the establishment of competence in Go/S-phase transition. Science. 1986 Jul 18;233(4761):356–359. doi: 10.1126/science.3726533. [DOI] [PubMed] [Google Scholar]
  19. Maheshwari R. K., Husain M. M., Friedman R. M., Krishna G. The calcium ionophore A23187 evokes and potentiates antiviral activity of interferon. J Interferon Res. 1985 Fall;5(4):605–612. doi: 10.1089/jir.1985.5.605. [DOI] [PubMed] [Google Scholar]
  20. Majerus P. W., Connolly T. M., Deckmyn H., Ross T. S., Bross T. E., Ishii H., Bansal V. S., Wilson D. B. The metabolism of phosphoinositide-derived messenger molecules. Science. 1986 Dec 19;234(4783):1519–1526. doi: 10.1126/science.3024320. [DOI] [PubMed] [Google Scholar]
  21. May L. T., Sehgal P. B., LaForge K. S., Inouye M. Expression of the native alpha and beta interferon genes in human cells. Virology. 1983 Aug;129(1):116–126. doi: 10.1016/0042-6822(83)90400-2. [DOI] [PubMed] [Google Scholar]
  22. Müller R., Bravo R., Burckhardt J., Curran T. Induction of c-fos gene and protein by growth factors precedes activation of c-myc. Nature. 1984 Dec 20;312(5996):716–720. doi: 10.1038/312716a0. [DOI] [PubMed] [Google Scholar]
  23. Nishizuka Y. The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature. 1988 Aug 25;334(6184):661–665. doi: 10.1038/334661a0. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. Purnell M. R., Stone P. R., Whish W. J. ADP-ribosylation of nuclear proteins. Biochem Soc Trans. 1980 Apr;8(2):215–227. doi: 10.1042/bst0080215. [DOI] [PubMed] [Google Scholar]
  27. Rasmussen H., Barrett P. Q. Calcium messenger system: an integrated view. Physiol Rev. 1984 Jul;64(3):938–984. doi: 10.1152/physrev.1984.64.3.938. [DOI] [PubMed] [Google Scholar]
  28. Reich N., Evans B., Levy D., Fahey D., Knight E., Jr, Darnell J. E., Jr Interferon-induced transcription of a gene encoding a 15-kDa protein depends on an upstream enhancer element. Proc Natl Acad Sci U S A. 1987 Sep;84(18):6394–6398. doi: 10.1073/pnas.84.18.6394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sehgal P. B., Walther Z., Tamm I. Rapid enhancement of beta 2-interferon/B-cell differentiation factor BSF-2 gene expression in human fibroblasts by diacylglycerols and the calcium ionophore A23187. Proc Natl Acad Sci U S A. 1987 Jun;84(11):3663–3667. doi: 10.1073/pnas.84.11.3663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Stiles C. D., Capone G. T., Scher C. D., Antoniades H. N., Van Wyk J. J., Pledger W. J. Dual control of cell growth by somatomedins and platelet-derived growth factor. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1279–1283. doi: 10.1073/pnas.76.3.1279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Tamm I., Lin S. L., Pfeffer L. M., Sehgal P. B. Interferons alpha and beta as cellular regulatory molecules. Interferon. 1987;9:13–74. [PubMed] [Google Scholar]
  33. Tso J. Y., Sun X. H., Kao T. H., Reece K. S., Wu R. Isolation and characterization of rat and human glyceraldehyde-3-phosphate dehydrogenase cDNAs: genomic complexity and molecular evolution of the gene. Nucleic Acids Res. 1985 Apr 11;13(7):2485–2502. doi: 10.1093/nar/13.7.2485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Tsuda T., Hamamori Y., Yamashita T., Fukumoto Y., Takai Y. Involvement of three intracellular messenger systems, protein kinase C, calcium ion and cyclic AMP, in the regulation of c-fos gene expression in Swiss 3T3 cells. FEBS Lett. 1986 Nov 10;208(1):39–42. doi: 10.1016/0014-5793(86)81527-7. [DOI] [PubMed] [Google Scholar]
  35. Ueda K., Hayaishi O. ADP-ribosylation. Annu Rev Biochem. 1985;54:73–100. doi: 10.1146/annurev.bi.54.070185.000445. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Williams B. R., Golgher R. R., Brown R. E., Gilbert C. S., Kerr I. M. Natural occurrence of 2-5A in interferon-treated EMC virus-infected L cells. Nature. 1979 Dec 6;282(5739):582–586. doi: 10.1038/282582a0. [DOI] [PubMed] [Google Scholar]
  38. Yamashita T., Tsuda T., Hamamori Y., Takai Y. Possible involvement of cyclic AMP and calcium ion in prostaglandin E1-induced elevation of c-myc mRNA levels in Swiss 3T3 fibroblasts. J Biol Chem. 1986 Dec 25;261(36):16878–16882. [PubMed] [Google Scholar]
  39. Yap W. H., Teo T. S., McCoy E., Tan Y. H. Rapid and transient rise in diacylglycerol concentration in Daudi cells exposed to interferon. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7765–7769. doi: 10.1073/pnas.83.20.7765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Yap W. H., Teo T. S., Tan Y. H. An early event in the interferon-induced transmembrane signaling process. Science. 1986 Oct 17;234(4774):355–358. doi: 10.1126/science.2429366. [DOI] [PubMed] [Google Scholar]
  41. 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 Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES