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. 1997 Jan;71(1):362–370. doi: 10.1128/jvi.71.1.362-370.1997

Antioxidant-induced changes of the AP-1 transcription complex are paralleled by a selective suppression of human papillomavirus transcription.

F Rösl 1, B C Das 1, M Lengert 1, K Geletneky 1, H zur Hausen 1
PMCID: PMC191059  PMID: 8985358

Abstract

Considering the involvement of a redox-regulatory pathway in the expression of human papillomaviruses (HPVs), HPV type 16 (HPV-16)-immortalized human keratinocytes were treated with the antioxidant pyrrolidine-dithiocarbamate (PDTC). PDTC induces elevated binding of the transcription factor AP-1 to its cognate recognition site within the viral regulatory region. Despite of increased AP-1 binding, normally indispensable for efficient HPV-16 transcription, viral gene expression was selectively suppressed at the level of initiation of transcription. Electrophoretic mobility supershift assays showed that the composition of the AP-1 complex, predominantly consisting of Jun homodimers in untreated cells, was altered. Irrespective of enhanced c-fos expression, c-jun was phosphorylated and became primarily heterodimerized with fra-1, which was also induced after PDTC incubation. Additionally, there was also an increased complex formation between c-jun and junB. Because both fra-1 and junB overexpression negatively interferes with c-jun/c-fos trans-activation of AP-1-responsive genes, our results suggest that the observed block in viral transcription is mainly the consequence of an antioxidant-induced reconstitution of the AP-1 transcription complex. Since expression of the c-jun/c-fos gene family is tightly regulated during cellular differentiation, defined reorganization of a central viral transcription factor may represent a novel mechanism controlling the transcription of pathogenic HPVs during keratinocyte differentiation and in the progression to cervical cancer.

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Selected References

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

  1. Abate C., Patel L., Rauscher F. J., 3rd, Curran T. Redox regulation of fos and jun DNA-binding activity in vitro. Science. 1990 Sep 7;249(4973):1157–1161. doi: 10.1126/science.2118682. [DOI] [PubMed] [Google Scholar]
  2. Angel P., Allegretto E. A., Okino S. T., Hattori K., Boyle W. J., Hunter T., Karin M. Oncogene jun encodes a sequence-specific trans-activator similar to AP-1. Nature. 1988 Mar 10;332(6160):166–171. doi: 10.1038/332166a0. [DOI] [PubMed] [Google Scholar]
  3. Angel P., Hattori K., Smeal T., Karin M. The jun proto-oncogene is positively autoregulated by its product, Jun/AP-1. Cell. 1988 Dec 2;55(5):875–885. doi: 10.1016/0092-8674(88)90143-2. [DOI] [PubMed] [Google Scholar]
  4. Angel P., Karin M. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochim Biophys Acta. 1991 Dec 10;1072(2-3):129–157. doi: 10.1016/0304-419x(91)90011-9. [DOI] [PubMed] [Google Scholar]
  5. Bohmann D., Bos T. J., Admon A., Nishimura T., Vogt P. K., Tjian R. Human proto-oncogene c-jun encodes a DNA binding protein with structural and functional properties of transcription factor AP-1. Science. 1987 Dec 4;238(4832):1386–1392. doi: 10.1126/science.2825349. [DOI] [PubMed] [Google Scholar]
  6. Boshart M., Gissmann L., Ikenberg H., Kleinheinz A., Scheurlen W., zur Hausen H. A new type of papillomavirus DNA, its presence in genital cancer biopsies and in cell lines derived from cervical cancer. EMBO J. 1984 May;3(5):1151–1157. doi: 10.1002/j.1460-2075.1984.tb01944.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Butz K., Hoppe-Seyler F. Transcriptional control of human papillomavirus (HPV) oncogene expression: composition of the HPV type 18 upstream regulatory region. J Virol. 1993 Nov;67(11):6476–6486. doi: 10.1128/jvi.67.11.6476-6486.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Butz K., Shahabeddin L., Geisen C., Spitkovsky D., Ullmann A., Hoppe-Seyler F. Functional p53 protein in human papillomavirus-positive cancer cells. Oncogene. 1995 Mar 2;10(5):927–936. [PubMed] [Google Scholar]
  9. Chiu R., Angel P., Karin M. Jun-B differs in its biological properties from, and is a negative regulator of, c-Jun. Cell. 1989 Dec 22;59(6):979–986. doi: 10.1016/0092-8674(89)90754-x. [DOI] [PubMed] [Google Scholar]
  10. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  11. Choo K. B., Huang C. J., Chen C. M., Han C. P., Au L. C. Jun-B oncogene aberrations in cervical cancer cell lines. Cancer Lett. 1995 Jul 13;93(2):249–253. doi: 10.1016/0304-3835(95)03817-g. [DOI] [PubMed] [Google Scholar]
  12. Cripe T. P., Alderborn A., Anderson R. D., Parkkinen S., Bergman P., Haugen T. H., Pettersson U., Turek L. P. Transcriptional activation of the human papillomavirus-16 P97 promoter by an 88-nucleotide enhancer containing distinct cell-dependent and AP-1-responsive modules. New Biol. 1990 May;2(5):450–463. [PubMed] [Google Scholar]
  13. Dani C., Blanchard J. M., Piechaczyk M., El Sabouty S., Marty L., Jeanteur P. Extreme instability of myc mRNA in normal and transformed human cells. Proc Natl Acad Sci U S A. 1984 Nov;81(22):7046–7050. doi: 10.1073/pnas.81.22.7046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Desaintes C., Hallez S., Detremmerie O., Burny A. Wild-type p53 down-regulates transcription from oncogenic human papillomavirus promoters through the epithelial specific enhancer. Oncogene. 1995 Jun 1;10(11):2155–2161. [PubMed] [Google Scholar]
  15. Desaintes C., Hallez S., Van Alphen P., Burny A. Transcriptional activation of several heterologous promoters by the E6 protein of human papillomavirus type 16. J Virol. 1992 Jan;66(1):325–333. doi: 10.1128/jvi.66.1.325-333.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Dyson N., Howley P. M., Münger K., Harlow E. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science. 1989 Feb 17;243(4893):934–937. doi: 10.1126/science.2537532. [DOI] [PubMed] [Google Scholar]
  18. Dürst M., Dzarlieva-Petrusevska R. T., Boukamp P., Fusenig N. E., Gissmann L. Molecular and cytogenetic analysis of immortalized human primary keratinocytes obtained after transfection with human papillomavirus type 16 DNA. Oncogene. 1987;1(3):251–256. [PubMed] [Google Scholar]
  19. Dürst M., Gissmann L., Ikenberg H., zur Hausen H. A papillomavirus DNA from a cervical carcinoma and its prevalence in cancer biopsy samples from different geographic regions. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3812–3815. doi: 10.1073/pnas.80.12.3812. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. East C. J., Abboud C. N., Borch R. F. Diethyldithiocarbamate induction of cytokine release in human long-term bone marrow cultures. Blood. 1992 Sep 1;80(5):1172–1177. [PubMed] [Google Scholar]
  21. Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
  22. Frank N., Christmann A., Frei E. Comparative studies on the pharmacokinetics of hydrophilic prolinedithiocarbamate, sarcosinedithiocarbamate and the less hydrophilic diethyldithiocarbamate. Toxicology. 1995 Jan 6;95(1-3):113–122. doi: 10.1016/0300-483x(94)02890-7. [DOI] [PubMed] [Google Scholar]
  23. Fujii M., Niki T., Mori T., Matsuda T., Matsui M., Nomura N., Seiki M. HTLV-1 Tax induces expression of various immediate early serum responsive genes. Oncogene. 1991 Jun;6(6):1023–1029. [PubMed] [Google Scholar]
  24. Goossens V., Grooten J., De Vos K., Fiers W. Direct evidence for tumor necrosis factor-induced mitochondrial reactive oxygen intermediates and their involvement in cytotoxicity. Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8115–8119. doi: 10.1073/pnas.92.18.8115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Gunning P., Ponte P., Okayama H., Engel J., Blau H., Kedes L. Isolation and characterization of full-length cDNA clones for human alpha-, beta-, and gamma-actin mRNAs: skeletal but not cytoplasmic actins have an amino-terminal cysteine that is subsequently removed. Mol Cell Biol. 1983 May;3(5):787–795. doi: 10.1128/mcb.3.5.787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hainaut P., Milner J. Redox modulation of p53 conformation and sequence-specific DNA binding in vitro. Cancer Res. 1993 Oct 1;53(19):4469–4473. [PubMed] [Google Scholar]
  27. Holmgren A. Thioredoxin. Annu Rev Biochem. 1985;54:237–271. doi: 10.1146/annurev.bi.54.070185.001321. [DOI] [PubMed] [Google Scholar]
  28. Hunter T., Karin M. The regulation of transcription by phosphorylation. Cell. 1992 Aug 7;70(3):375–387. doi: 10.1016/0092-8674(92)90162-6. [DOI] [PubMed] [Google Scholar]
  29. Jesudasan R. A., Rahman R. A., Chandrashekharappa S., Evans G. A., Srivatsan E. S. Deletion and translocation of chromosome 11q13 sequences in cervical carcinoma cell lines. Am J Hum Genet. 1995 Mar;56(3):705–715. [PMC free article] [PubMed] [Google Scholar]
  30. Khandjian E. W., Méric C. A procedure for Northern blot analysis of native RNA. Anal Biochem. 1986 Nov 15;159(1):227–232. doi: 10.1016/0003-2697(86)90332-5. [DOI] [PubMed] [Google Scholar]
  31. Koi M., Morita H., Yamada H., Satoh H., Barrett J. C., Oshimura M. Normal human chromosome 11 suppresses tumorigenicity of human cervical tumor cell line SiHa. Mol Carcinog. 1989;2(1):12–21. doi: 10.1002/mc.2940020103. [DOI] [PubMed] [Google Scholar]
  32. Kunze N., Klein M., Richter A., Knippers R. Structural characterization of the human DNA topoisomerase I gene promoter. Eur J Biochem. 1990 Dec 12;194(2):323–330. doi: 10.1111/j.1432-1033.1990.tb15620.x. [DOI] [PubMed] [Google Scholar]
  33. Kyo S., Tam A., Laimins L. A. Transcriptional activity of human papillomavirus type 31b enhancer is regulated through synergistic interaction of AP1 with two novel cellular factors. Virology. 1995 Aug 1;211(1):184–197. doi: 10.1006/viro.1995.1390. [DOI] [PubMed] [Google Scholar]
  34. Lechner M. S., Mack D. H., Finicle A. B., Crook T., Vousden K. H., Laimins L. A. Human papillomavirus E6 proteins bind p53 in vivo and abrogate p53-mediated repression of transcription. EMBO J. 1992 Aug;11(8):3045–3052. doi: 10.1002/j.1460-2075.1992.tb05375.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Lee W., Mitchell P., Tjian R. Purified transcription factor AP-1 interacts with TPA-inducible enhancer elements. Cell. 1987 Jun 19;49(6):741–752. doi: 10.1016/0092-8674(87)90612-x. [DOI] [PubMed] [Google Scholar]
  36. Linial M., Gunderson N., Groudine M. Enhanced transcription of c-myc in bursal lymphoma cells requires continuous protein synthesis. Science. 1985 Dec 6;230(4730):1126–1132. doi: 10.1126/science.2999973. [DOI] [PubMed] [Google Scholar]
  37. Los M., Dröge W., Stricker K., Baeuerle P. A., Schulze-Osthoff K. Hydrogen peroxide as a potent activator of T lymphocyte functions. Eur J Immunol. 1995 Jan;25(1):159–165. doi: 10.1002/eji.1830250127. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Matsuda M., Masutani H., Nakamura H., Miyajima S., Yamauchi A., Yonehara S., Uchida A., Irimajiri K., Horiuchi A., Yodoi J. Protective activity of adult T cell leukemia-derived factor (ADF) against tumor necrosis factor-dependent cytotoxicity on U937 cells. J Immunol. 1991 Dec 1;147(11):3837–3841. [PubMed] [Google Scholar]
  40. Matthews J. R., Wakasugi N., Virelizier J. L., Yodoi J., Hay R. T. Thioredoxin regulates the DNA binding activity of NF-kappa B by reduction of a disulphide bond involving cysteine 62. Nucleic Acids Res. 1992 Aug 11;20(15):3821–3830. doi: 10.1093/nar/20.15.3821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Meyer M., Schreck R., Baeuerle P. A. H2O2 and antioxidants have opposite effects on activation of NF-kappa B and AP-1 in intact cells: AP-1 as secondary antioxidant-responsive factor. EMBO J. 1993 May;12(5):2005–2015. doi: 10.1002/j.1460-2075.1993.tb05850.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Mincheva A., Gissmann L., zur Hausen H. Chromosomal integration sites of human papillomavirus DNA in three cervical cancer cell lines mapped by in situ hybridization. Med Microbiol Immunol. 1987;176(5):245–256. doi: 10.1007/BF00190531. [DOI] [PubMed] [Google Scholar]
  43. Müller R., Tremblay J. M., Adamson E. D., Verma I. M. Tissue and cell type-specific expression of two human c-onc genes. Nature. 1983 Aug 4;304(5925):454–456. doi: 10.1038/304454a0. [DOI] [PubMed] [Google Scholar]
  44. Münger K., Phelps W. C., Bubb V., Howley P. M., Schlegel R. The E6 and E7 genes of the human papillomavirus type 16 together are necessary and sufficient for transformation of primary human keratinocytes. J Virol. 1989 Oct;63(10):4417–4421. doi: 10.1128/jvi.63.10.4417-4421.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Nakabeppu Y., Ryder K., Nathans D. DNA binding activities of three murine Jun proteins: stimulation by Fos. Cell. 1988 Dec 2;55(5):907–915. doi: 10.1016/0092-8674(88)90146-8. [DOI] [PubMed] [Google Scholar]
  46. Oberley T. D., Schultz J. L., Li N., Oberley L. W. Antioxidant enzyme levels as a function of growth state in cell culture. Free Radic Biol Med. 1995 Jul;19(1):53–65. doi: 10.1016/0891-5849(95)00012-m. [DOI] [PubMed] [Google Scholar]
  47. Offord E. A., Beard P. A member of the activator protein 1 family found in keratinocytes but not in fibroblasts required for transcription from a human papillomavirus type 18 promoter. J Virol. 1990 Oct;64(10):4792–4798. doi: 10.1128/jvi.64.10.4792-4798.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Papavassiliou A. G., Treier M., Bohmann D. Intramolecular signal transduction in c-Jun. EMBO J. 1995 May 1;14(9):2014–2019. doi: 10.1002/j.1460-2075.1995.tb07193.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Papavassiliou A. G., Treier M., Chavrier C., Bohmann D. Targeted degradation of c-Fos, but not v-Fos, by a phosphorylation-dependent signal on c-Jun. Science. 1992 Dec 18;258(5090):1941–1944. doi: 10.1126/science.1470918. [DOI] [PubMed] [Google Scholar]
  50. Phelps W. C., Yee C. L., Münger K., Howley P. M. The human papillomavirus type 16 E7 gene encodes transactivation and transformation functions similar to those of adenovirus E1A. Cell. 1988 May 20;53(4):539–547. doi: 10.1016/0092-8674(88)90570-3. [DOI] [PubMed] [Google Scholar]
  51. Polack A., Eick D., Koch E., Bornkamm G. W. Truncation does not abrogate transcriptional downregulation of the c-myc gene by sodium butyrate in Burkitt's lymphoma cells. EMBO J. 1987 Oct;6(10):2959–2964. doi: 10.1002/j.1460-2075.1987.tb02601.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Rainwater R., Parks D., Anderson M. E., Tegtmeyer P., Mann K. Role of cysteine residues in regulation of p53 function. Mol Cell Biol. 1995 Jul;15(7):3892–3903. doi: 10.1128/mcb.15.7.3892. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Ross J. mRNA stability in mammalian cells. Microbiol Rev. 1995 Sep;59(3):423–450. doi: 10.1128/mr.59.3.423-450.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Rösl F., Achtstätter T., Bauknecht T., Hutter K. J., Futterman G., zur Hausen H. Extinction of the HPV18 upstream regulatory region in cervical carcinoma cells after fusion with non-tumorigenic human keratinocytes under non-selective conditions. EMBO J. 1991 Jun;10(6):1337–1345. doi: 10.1002/j.1460-2075.1991.tb07653.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Rösl F., Dürst M., zur Hausen H. Selective suppression of human papillomavirus transcription in non-tumorigenic cells by 5-azacytidine. EMBO J. 1988 May;7(5):1321–1328. doi: 10.1002/j.1460-2075.1988.tb02947.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Rösl F., Lengert M., Albrecht J., Kleine K., Zawatzky R., Schraven B., zur Hausen H. Differential regulation of the JE gene encoding the monocyte chemoattractant protein (MCP-1) in cervical carcinoma cells and derived hybrids. J Virol. 1994 Apr;68(4):2142–2150. doi: 10.1128/jvi.68.4.2142-2150.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Sato K., Taguchi H., Maeda T., Minami H., Asada Y., Watanabe Y., Yoshikawa K. The primary cytotoxicity in ultraviolet-a-irradiated riboflavin solution is derived from hydrogen peroxide. J Invest Dermatol. 1995 Oct;105(4):608–612. doi: 10.1111/1523-1747.ep12323724. [DOI] [PubMed] [Google Scholar]
  58. Saxon P. J., Srivatsan E. S., Stanbridge E. J. Introduction of human chromosome 11 via microcell transfer controls tumorigenic expression of HeLa cells. EMBO J. 1986 Dec 20;5(13):3461–3466. doi: 10.1002/j.1460-2075.1986.tb04670.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Scheffner M., Werness B. A., Huibregtse J. M., Levine A. J., Howley P. M. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell. 1990 Dec 21;63(6):1129–1136. doi: 10.1016/0092-8674(90)90409-8. [DOI] [PubMed] [Google Scholar]
  60. Scheidereit C., Cromlish J. A., Gerster T., Kawakami K., Balmaceda C. G., Currie R. A., Roeder R. G. A human lymphoid-specific transcription factor that activates immunoglobulin genes is a homoeobox protein. Nature. 1988 Dec 8;336(6199):551–557. doi: 10.1038/336551a0. [DOI] [PubMed] [Google Scholar]
  61. Schenk H., Klein M., Erdbrügger W., Dröge W., Schulze-Osthoff K. Distinct effects of thioredoxin and antioxidants on the activation of transcription factors NF-kappa B and AP-1. Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1672–1676. doi: 10.1073/pnas.91.5.1672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Schreck R., Grassmann R., Fleckenstein B., Baeuerle P. A. Antioxidants selectively suppress activation of NF-kappa B by human T-cell leukemia virus type I Tax protein. J Virol. 1992 Nov;66(11):6288–6293. doi: 10.1128/jvi.66.11.6288-6293.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Schreck R., Meier B., Männel D. N., Dröge W., Baeuerle P. A. Dithiocarbamates as potent inhibitors of nuclear factor kappa B activation in intact cells. J Exp Med. 1992 May 1;175(5):1181–1194. doi: 10.1084/jem.175.5.1181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Schreck R., Rieber P., Baeuerle P. A. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J. 1991 Aug;10(8):2247–2258. doi: 10.1002/j.1460-2075.1991.tb07761.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Schulze-Osthoff K., Los M., Baeuerle P. A. Redox signalling by transcription factors NF-kappa B and AP-1 in lymphocytes. Biochem Pharmacol. 1995 Sep 7;50(6):735–741. doi: 10.1016/0006-2952(95)02011-z. [DOI] [PubMed] [Google Scholar]
  66. Schütte J., Viallet J., Nau M., Segal S., Fedorko J., Minna J. jun-B inhibits and c-fos stimulates the transforming and trans-activating activities of c-jun. Cell. 1989 Dec 22;59(6):987–997. doi: 10.1016/0092-8674(89)90755-1. [DOI] [PubMed] [Google Scholar]
  67. Shyy J. Y., Lin M. C., Han J., Lu Y., Petrime M., Chien S. The cis-acting phorbol ester "12-O-tetradecanoylphorbol 13-acetate"-responsive element is involved in shear stress-induced monocyte chemotactic protein 1 gene expression. Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):8069–8073. doi: 10.1073/pnas.92.17.8069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Sinke R. J., Tanigami A., Nakamura Y., Geurts van Kessel A. Reverse mapping of the gene encoding the human fos-related antigen-1 (fra-1) within chromosome band 11q13. Genomics. 1993 Oct;18(1):165–165. doi: 10.1006/geno.1993.1447. [DOI] [PubMed] [Google Scholar]
  69. Srivatsan E. S., Misra B. C., Venugopalan M., Wilczynski S. P. Loss of heterozygosity for alleles on chromosome II in cervical carcinoma. Am J Hum Genet. 1991 Oct;49(4):868–877. [PMC free article] [PubMed] [Google Scholar]
  70. Stanbridge E. J., Der C. J., Doersen C. J., Nishimi R. Y., Peehl D. M., Weissman B. E., Wilkinson J. E. Human cell hybrids: analysis of transformation and tumorigenicity. Science. 1982 Jan 15;215(4530):252–259. doi: 10.1126/science.7053574. [DOI] [PubMed] [Google Scholar]
  71. Stein B., Rahmsdorf H. J., Steffen A., Litfin M., Herrlich P. UV-induced DNA damage is an intermediate step in UV-induced expression of human immunodeficiency virus type 1, collagenase, c-fos, and metallothionein. Mol Cell Biol. 1989 Nov;9(11):5169–5181. doi: 10.1128/mcb.9.11.5169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Suzuki T., Okuno H., Yoshida T., Endo T., Nishina H., Iba H. Difference in transcriptional regulatory function between c-Fos and Fra-2. Nucleic Acids Res. 1991 Oct 25;19(20):5537–5542. doi: 10.1093/nar/19.20.5537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Takimoto M., Quinn J. P., Farina A. R., Staudt L. M., Levens D. fos/jun and octamer-binding protein interact with a common site in a negative element of the human c-myc gene. J Biol Chem. 1989 May 25;264(15):8992–8999. [PubMed] [Google Scholar]
  74. Thierry F., Spyrou G., Yaniv M., Howley P. Two AP1 sites binding JunB are essential for human papillomavirus type 18 transcription in keratinocytes. J Virol. 1992 Jun;66(6):3740–3748. doi: 10.1128/jvi.66.6.3740-3748.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Toledano M. B., Leonard W. J. Modulation of transcription factor NF-kappa B binding activity by oxidation-reduction in vitro. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4328–4332. doi: 10.1073/pnas.88.10.4328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Tsurumi C., Ishida N., Tamura T., Kakizuka A., Nishida E., Okumura E., Kishimoto T., Inagaki M., Okazaki K., Sagata N. Degradation of c-Fos by the 26S proteasome is accelerated by c-Jun and multiple protein kinases. Mol Cell Biol. 1995 Oct;15(10):5682–5687. doi: 10.1128/mcb.15.10.5682. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Ueda A., Okuda K., Ohno S., Shirai A., Igarashi T., Matsunaga K., Fukushima J., Kawamoto S., Ishigatsubo Y., Okubo T. NF-kappa B and Sp1 regulate transcription of the human monocyte chemoattractant protein-1 gene. J Immunol. 1994 Sep 1;153(5):2052–2063. [PubMed] [Google Scholar]
  78. Wakasugi N., Tagaya Y., Wakasugi H., Mitsui A., Maeda M., Yodoi J., Tursz T. Adult T-cell leukemia-derived factor/thioredoxin, produced by both human T-lymphotropic virus type I- and Epstein-Barr virus-transformed lymphocytes, acts as an autocrine growth factor and synergizes with interleukin 1 and interleukin 2. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8282–8286. doi: 10.1073/pnas.87.21.8282. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Werness B. A., Levine A. J., Howley P. M. Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science. 1990 Apr 6;248(4951):76–79. doi: 10.1126/science.2157286. [DOI] [PubMed] [Google Scholar]
  80. Yoshioka K., Deng T., Cavigelli M., Karin M. Antitumor promotion by phenolic antioxidants: inhibition of AP-1 activity through induction of Fra expression. Proc Natl Acad Sci U S A. 1995 May 23;92(11):4972–4976. doi: 10.1073/pnas.92.11.4972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. de Wet J. R., Wood K. V., DeLuca M., Helinski D. R., Subramani S. Firefly luciferase gene: structure and expression in mammalian cells. Mol Cell Biol. 1987 Feb;7(2):725–737. doi: 10.1128/mcb.7.2.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. el-Deiry W. S., Tokino T., Velculescu V. E., Levy D. B., Parsons R., Trent J. M., Lin D., Mercer W. E., Kinzler K. W., Vogelstein B. WAF1, a potential mediator of p53 tumor suppression. Cell. 1993 Nov 19;75(4):817–825. doi: 10.1016/0092-8674(93)90500-p. [DOI] [PubMed] [Google Scholar]
  83. zur Hausen H. Disrupted dichotomous intracellular control of human papillomavirus infection in cancer of the cervix. Lancet. 1994 Apr 16;343(8903):955–957. doi: 10.1016/s0140-6736(94)90070-1. [DOI] [PubMed] [Google Scholar]
  84. zur Hausen H. Human papillomaviruses in the pathogenesis of anogenital cancer. Virology. 1991 Sep;184(1):9–13. doi: 10.1016/0042-6822(91)90816-t. [DOI] [PubMed] [Google Scholar]

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