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. 1995 Dec 25;23(24):5055–5063. doi: 10.1093/nar/23.24.5055

A novel PRD I and TG binding activity involved in virus-induced transcription of IFN-A genes.

P Génin 1, J Bragança 1, N Darracq 1, J Doly 1, A Civas 1
PMCID: PMC307513  PMID: 8559665

Abstract

Comparative analysis of the inducible elements of the mouse interferon A4 and A11 gene promoters (IE-A4 and IE-A11) by transient transfection experiments, DNase 1 footprinting and electrophoretic mobility shift assays resulted in identification of a virus-induced binding activity suggested to be involved in NDV-induced activation of transcription of these genes. The virus-induced factor, termed VIF, is activated early by contact of virions with cells. It specifically recognizes the PRD I-like domain shared by both inducible elements, as well as the TG-like domain of IE-A4. This factor, distinct from the IRF-1, IRF-2 and the alpha F1 binding proteins and presenting a different affinity pattern from that of the TG protein, is proposed as a candidate for IFN-type I gene regulation.

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Selected References

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  1. Abdollahi A., Lord K. A., Hoffman-Liebermann B., Liebermann D. A. Interferon regulatory factor 1 is a myeloid differentiation primary response gene induced by interleukin 6 and leukemia inhibitory factor: role in growth inhibition. Cell Growth Differ. 1991 Aug;2(8):401–407. [PubMed] [Google Scholar]
  2. Au W. C., Raj N. B., Pine R., Pitha P. M. Distinct activation of murine interferon-alpha promoter region by IRF-1/ISFG-2 and virus infection. Nucleic Acids Res. 1992 Jun 11;20(11):2877–2884. doi: 10.1093/nar/20.11.2877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Au W. C., Su Y., Raj N. B., Pitha P. M. Virus-mediated induction of interferon A gene requires cooperation between multiple binding factors in the interferon alpha promoter region. J Biol Chem. 1993 Nov 15;268(32):24032–24040. [PubMed] [Google Scholar]
  4. Bose H. R., Jr The Rel family: models for transcriptional regulation and oncogenic transformation. Biochim Biophys Acta. 1992 Sep 14;1114(1):1–17. doi: 10.1016/0304-419x(92)90002-g. [DOI] [PubMed] [Google Scholar]
  5. Briken V., Ruffner H., Schultz U., Schwarz A., Reis L. F., Strehlow I., Decker T., Staeheli P. Interferon regulatory factor 1 is required for mouse Gbp gene activation by gamma interferon. Mol Cell Biol. 1995 Feb;15(2):975–982. doi: 10.1128/mcb.15.2.975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Civas A., Dion M., Vodjdani G., Doly J. Repression of the murine interferon alpha 11 gene: identification of negatively acting sequences. Nucleic Acids Res. 1991 Aug 25;19(16):4497–4502. doi: 10.1093/nar/19.16.4497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Clark A. R., Docherty K. Negative regulation of transcription in eukaryotes. Biochem J. 1993 Dec 15;296(Pt 3):521–541. doi: 10.1042/bj2960521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Coulombel C., Vodjdani G., Doly J. Isolation and characterization of a novel interferon-alpha-encoding gene, IFN-alpha 11, within a murine IFN cluster. Gene. 1991 Aug 15;104(2):187–195. doi: 10.1016/0378-1119(91)90249-b. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Dion M., Vodjdani G., Doly J. Sequence and expression of a novel murine interferon alpha gene--homology with enhancer elements in the regulatory region of the gene. Biochem Biophys Res Commun. 1986 Jul 31;138(2):826–834. doi: 10.1016/s0006-291x(86)80571-x. [DOI] [PubMed] [Google Scholar]
  11. Du W., Maniatis T. An ATF/CREB binding site is required for virus induction of the human interferon beta gene [corrected]. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2150–2154. doi: 10.1073/pnas.89.6.2150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Du W., Thanos D., Maniatis T. Mechanisms of transcriptional synergism between distinct virus-inducible enhancer elements. Cell. 1993 Sep 10;74(5):887–898. doi: 10.1016/0092-8674(93)90468-6. [DOI] [PubMed] [Google Scholar]
  13. Fan C. M., Maniatis T. Two different virus-inducible elements are required for human beta-interferon gene regulation. EMBO J. 1989 Jan;8(1):101–110. doi: 10.1002/j.1460-2075.1989.tb03353.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fujita T., Kimura Y., Miyamoto M., Barsoumian E. L., Taniguchi T. Induction of endogenous IFN-alpha and IFN-beta genes by a regulatory transcription factor, IRF-1. Nature. 1989 Jan 19;337(6204):270–272. doi: 10.1038/337270a0. [DOI] [PubMed] [Google Scholar]
  15. Fujita T., Sakakibara J., Sudo Y., Miyamoto M., Kimura Y., Taniguchi T. Evidence for a nuclear factor(s), IRF-1, mediating induction and silencing properties to human IFN-beta gene regulatory elements. EMBO J. 1988 Nov;7(11):3397–3405. doi: 10.1002/j.1460-2075.1988.tb03213.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fujita T., Shibuya H., Hotta H., Yamanishi K., Taniguchi T. Interferon-beta gene regulation: tandemly repeated sequences of a synthetic 6 bp oligomer function as a virus-inducible enhancer. Cell. 1987 May 8;49(3):357–367. doi: 10.1016/0092-8674(87)90288-1. [DOI] [PubMed] [Google Scholar]
  17. Galas D. J., Schmitz A. DNAse footprinting: a simple method for the detection of protein-DNA binding specificity. Nucleic Acids Res. 1978 Sep;5(9):3157–3170. doi: 10.1093/nar/5.9.3157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Goodbourn S., Burstein H., Maniatis T. The human beta-interferon gene enhancer is under negative control. Cell. 1986 May 23;45(4):601–610. doi: 10.1016/0092-8674(86)90292-8. [DOI] [PubMed] [Google Scholar]
  19. Goodbourn S., Maniatis T. Overlapping positive and negative regulatory domains of the human beta-interferon gene. Proc Natl Acad Sci U S A. 1988 Mar;85(5):1447–1451. doi: 10.1073/pnas.85.5.1447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Harada H., Willison K., Sakakibara J., Miyamoto M., Fujita T., Taniguchi T. Absence of the type I IFN system in EC cells: transcriptional activator (IRF-1) and repressor (IRF-2) genes are developmentally regulated. Cell. 1990 Oct 19;63(2):303–312. doi: 10.1016/0092-8674(90)90163-9. [DOI] [PubMed] [Google Scholar]
  21. Hiscott J., Cantell K., Weissmann C. Differential expression of human interferon genes. Nucleic Acids Res. 1984 May 11;12(9):3727–3746. doi: 10.1093/nar/12.9.3727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hockensmith J. W., Kubasek W. L., Vorachek W. R., Evertsz E. M., von Hippel P. H. Laser cross-linking of protein-nucleic acid complexes. Methods Enzymol. 1991;208:211–236. doi: 10.1016/0076-6879(91)08015-a. [DOI] [PubMed] [Google Scholar]
  23. John S., Reeves R. B., Lin J. X., Child R., Leiden J. M., Thompson C. B., Leonard W. J. Regulation of cell-type-specific interleukin-2 receptor alpha-chain gene expression: potential role of physical interactions between Elf-1, HMG-I(Y), and NF-kappa B family proteins. Mol Cell Biol. 1995 Mar;15(3):1786–1796. doi: 10.1128/mcb.15.3.1786. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kamijo R., Harada H., Matsuyama T., Bosland M., Gerecitano J., Shapiro D., Le J., Koh S. I., Kimura T., Green S. J. Requirement for transcription factor IRF-1 in NO synthase induction in macrophages. Science. 1994 Mar 18;263(5153):1612–1615. doi: 10.1126/science.7510419. [DOI] [PubMed] [Google Scholar]
  25. Kelley K. A., Pitha P. M. Characterization of a mouse interferon gene locus II. Differential expression of alpha-interferon genes. Nucleic Acids Res. 1985 Feb 11;13(3):825–839. doi: 10.1093/nar/13.3.825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kelley K. A., Pitha P. M. Differential effect of poly rI.rC and Newcastle disease virus on the expression of interferon and cellular genes in mouse cells. Virology. 1985 Dec;147(2):382–393. doi: 10.1016/0042-6822(85)90140-0. [DOI] [PubMed] [Google Scholar]
  27. Kuhl D., de la Fuente J., Chaturvedi M., Parimoo S., Ryals J., Meyer F., Weissmann C. Reversible silencing of enhancers by sequences derived from the human IFN-alpha promoter. Cell. 1987 Sep 25;50(7):1057–1069. doi: 10.1016/0092-8674(87)90172-3. [DOI] [PubMed] [Google Scholar]
  28. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  29. Leblanc J. F., Cohen L., Rodrigues M., Hiscott J. Synergism between distinct enhanson domains in viral induction of the human beta interferon gene. Mol Cell Biol. 1990 Aug;10(8):3987–3993. doi: 10.1128/mcb.10.8.3987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lenardo M. J., Fan C. M., Maniatis T., Baltimore D. The involvement of NF-kappa B in beta-interferon gene regulation reveals its role as widely inducible mediator of signal transduction. Cell. 1989 Apr 21;57(2):287–294. doi: 10.1016/0092-8674(89)90966-5. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. MacDonald N. J., Kuhl D., Maguire D., Näf D., Gallant P., Goswamy A., Hug H., Büeler H., Chaturvedi M., de la Fuente J. Different pathways mediate virus inducibility of the human IFN-alpha 1 and IFN-beta genes. Cell. 1990 Mar 9;60(5):767–779. doi: 10.1016/0092-8674(90)90091-r. [DOI] [PubMed] [Google Scholar]
  33. Matsuyama T., Kimura T., Kitagawa M., Pfeffer K., Kawakami T., Watanabe N., Kündig T. M., Amakawa R., Kishihara K., Wakeham A. Targeted disruption of IRF-1 or IRF-2 results in abnormal type I IFN gene induction and aberrant lymphocyte development. Cell. 1993 Oct 8;75(1):83–97. [PubMed] [Google Scholar]
  34. Miyamoto M., Fujita T., Kimura Y., Maruyama M., Harada H., Sudo Y., Miyata T., Taniguchi T. Regulated expression of a gene encoding a nuclear factor, IRF-1, that specifically binds to IFN-beta gene regulatory elements. Cell. 1988 Sep 9;54(6):903–913. doi: 10.1016/s0092-8674(88)91307-4. [DOI] [PubMed] [Google Scholar]
  35. Navarro S., Dion M., Vodjdani G., Berlot-Picard F., Doly J. Isolation and characterization of a functional murine interferon alpha gene which is not expressed in fibroblasts upon virus induction. J Gen Virol. 1989 Jun;70(Pt 6):1381–1389. doi: 10.1099/0022-1317-70-6-1381. [DOI] [PubMed] [Google Scholar]
  36. Nourbakhsh M., Hoffmann K., Hauser H. Interferon-beta promoters contain a DNA element that acts as a position-independent silencer on the NF-kappa B site. EMBO J. 1993 Feb;12(2):451–459. doi: 10.1002/j.1460-2075.1993.tb05677.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Näf D., Hardin S. E., Weissmann C. Multimerization of AAGTGA and GAAAGT generates sequences that mediate virus inducibility by mimicking an interferon promoter element. Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1369–1373. doi: 10.1073/pnas.88.4.1369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Pine R., Decker T., Kessler D. S., Levy D. E., Darnell J. E., Jr Purification and cloning of interferon-stimulated gene factor 2 (ISGF2): ISGF2 (IRF-1) can bind to the promoters of both beta interferon- and interferon-stimulated genes but is not a primary transcriptional activator of either. Mol Cell Biol. 1990 Jun;10(6):2448–2457. doi: 10.1128/mcb.10.6.2448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Raj N. B., Au W. C., Pitha P. M. Identification of a novel virus-responsive sequence in the promoter of murine interferon-alpha genes. J Biol Chem. 1991 Jun 15;266(17):11360–11365. [PubMed] [Google Scholar]
  40. Raj N. B., Engelhardt J., Au W. C., Levy D. E., Pitha P. M. Virus infection and interferon can activate gene expression through a single synthetic element, but endogenous genes show distinct regulation. J Biol Chem. 1989 Oct 5;264(28):16658–16666. [PubMed] [Google Scholar]
  41. Raj N. B., Israeli R., Kellum M., Pitha P. M. Upstream regulatory elements of murine alpha 4-interferon gene confer inducibility and cell type-restricted expression. J Biol Chem. 1989 Jul 5;264(19):11149–11157. [PubMed] [Google Scholar]
  42. Raj N. B., Kellum M., Kelley K. A., Antrobus S., Pitha P. M. Differential regulation of interferon synthesis in lymphoblastoid cells. J Interferon Res. 1985 Summer;5(3):493–510. doi: 10.1089/jir.1985.5.493. [DOI] [PubMed] [Google Scholar]
  43. Reis L. F., Harada H., Wolchok J. D., Taniguchi T., Vilcek J. Critical role of a common transcription factor, IRF-1, in the regulation of IFN-beta and IFN-inducible genes. EMBO J. 1992 Jan;11(1):185–193. doi: 10.1002/j.1460-2075.1992.tb05041.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Reis L. F., Ruffner H., Stark G., Aguet M., Weissmann C. Mice devoid of interferon regulatory factor 1 (IRF-1) show normal expression of type I interferon genes. EMBO J. 1994 Oct 17;13(20):4798–4806. doi: 10.1002/j.1460-2075.1994.tb06805.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Ryals J., Dierks P., Ragg H., Weissmann C. A 46-nucleotide promoter segment from an IFN-alpha gene renders an unrelated promoter inducible by virus. Cell. 1985 Jun;41(2):497–507. doi: 10.1016/s0092-8674(85)80023-4. [DOI] [PubMed] [Google Scholar]
  46. Sedmak J. J., Grossberg S. E. A rapid, sensitive, and versatile assay for protein using Coomassie brilliant blue G250. Anal Biochem. 1977 May 1;79(1-2):544–552. doi: 10.1016/0003-2697(77)90428-6. [DOI] [PubMed] [Google Scholar]
  47. Shuttleworth J., Morser J., Burke D. C. Expression of interferon-alpha and interferon-beta genes in human lymphoblastoid (Namalwa) cells. Eur J Biochem. 1983 Jun 15;133(2):399–404. doi: 10.1111/j.1432-1033.1983.tb07476.x. [DOI] [PubMed] [Google Scholar]
  48. Sleigh M. J. A nonchromatographic assay for expression of the chloramphenicol acetyltransferase gene in eucaryotic cells. Anal Biochem. 1986 Jul;156(1):251–256. doi: 10.1016/0003-2697(86)90180-6. [DOI] [PubMed] [Google Scholar]
  49. Stevens A. M., Wang Y. F., Sieger K. A., Lu H. F., Yu-Lee L. Y. Biphasic transcriptional regulation of the interferon regulatory factor-1 gene by prolactin: involvement of gamma-interferon-activated sequence and Stat-related proteins. Mol Endocrinol. 1995 Apr;9(4):513–525. doi: 10.1210/mend.9.4.7659094. [DOI] [PubMed] [Google Scholar]
  50. Thanos D., Maniatis T. The high mobility group protein HMG I(Y) is required for NF-kappa B-dependent virus induction of the human IFN-beta gene. Cell. 1992 Nov 27;71(5):777–789. doi: 10.1016/0092-8674(92)90554-p. [DOI] [PubMed] [Google Scholar]
  51. Veals S. A., Schindler C., Leonard D., Fu X. Y., Aebersold R., Darnell J. E., Jr, Levy D. E. Subunit of an alpha-interferon-responsive transcription factor is related to interferon regulatory factor and Myb families of DNA-binding proteins. Mol Cell Biol. 1992 Aug;12(8):3315–3324. doi: 10.1128/mcb.12.8.3315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Visvanathan K. V., Goodbourn S. Double-stranded RNA activates binding of NF-kappa B to an inducible element in the human beta-interferon promoter. EMBO J. 1989 Apr;8(4):1129–1138. doi: 10.1002/j.1460-2075.1989.tb03483.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Watanabe N., Sakakibara J., Hovanessian A. G., Taniguchi T., Fujita T. Activation of IFN-beta element by IRF-1 requires a posttranslational event in addition to IRF-1 synthesis. Nucleic Acids Res. 1991 Aug 25;19(16):4421–4428. doi: 10.1093/nar/19.16.4421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Wigler M., Pellicer A., Silverstein S., Axel R. Biochemical transfer of single-copy eucaryotic genes using total cellular DNA as donor. Cell. 1978 Jul;14(3):725–731. doi: 10.1016/0092-8674(78)90254-4. [DOI] [PubMed] [Google Scholar]

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