Modulation of transcriptional activation of the proliferating cell nuclear antigen promoter by the adenovirus E1A 243-residue oncoprotein depends on proximal activators

REFERENCES

• Almendral, J. M., D. Huebsch, P. A. Blundell, H. Macdonald-Bravo, and R. Bravo. 1987. Cloning and sequence of the human nuclear protein cyclin: homology with DNA-binding proteins. Proc. Natl. Acad. Sci. USA 84:1575–1579.
   PubMed Web of Science ®Google Scholar
• Bagchi, S., P. Raychaudhuri, and J. R. Nevins. 1990. Adenovirus E1A proteins can dissociate heteromeric complexes involving the E2F transcription factor: a novel mechanism for E1A trans-activation. Cell 62:659–669.
   PubMed Web of Science ®Google Scholar
• Baleja, J. D., R. Marmorstein, S. C. Harrison, and G. Wagner. 1992. Solution structure of the DNA-binding domain of Cd2-GAL4 from S. cerevisiae. Nature (London) 356:450–453.
   PubMedGoogle Scholar
• Bandara, L. R., and N. B. La Thangue. 1991. Adenovirus E1A prevents the retinoblastoma gene product from complexing with a cellular transcription factor. Nature (London) 351:494–497.
   PubMed Web of Science ®Google Scholar
• Benbrook, D. M., and N. C. Jones. 1990. Heterodimer formation between CREB and JUN proteins. Oncogene 5:295–302.
   PubMed Web of Science ®Google Scholar
• Berk, A. J. 1986. Functions of adenovirus E1A. Annu. Rev. Genet. 20:45–79.
   PubMed Web of Science ®Google Scholar
• Bravo, R., R. Frank, P. A. Blundell, and H. Macdonald-Bravo. 1987. Cyclin/PCNA is the auxiliary protein of DNA polymerase-δ. Nature (London) 326:515–517.
   PubMed Web of Science ®Google Scholar
• Brown, T. A., and S. L. McKnight. 1992. Specificities of protein-protein and protein-DNA interaction of GABPα and two newly defined ets-related proteins. Genes Dev. 6:2502–2512.
   PubMedGoogle Scholar
• Buratowski, S., S. Hahn, L. Guarente, and P. A. Sharp. 1989. Five intermediate complexes in transcription initiation by RNA polymerase II. Cell 56:549–561.
   PubMed Web of Science ®Google Scholar
• Carcamo, J., L. Buckbinder, and D. Reinberg. 1991. The initiator directs the assembly of a transcription factor IID-dependent complex. Proc. Natl. Acad. Sci. USA 88:8052–8056.
   PubMedGoogle Scholar
• Carey, M. 1991. Mechanistic advances in eukaryotic gene activation. Curr. Opin. Cell Biol. 3:452–460.
   PubMedGoogle Scholar
• Chang, C.-D., L. Ottavio, S. Travail, K. E. Lipson, and R. Baserga. 1990. Transcriptional and post-transcriptional regulation of the proliferating cell nuclear antigen gene. Mol. Cell. Biol. 10:3289–3296.
   PubMed Web of Science ®Google Scholar
• Conaway, J. W., and R. C. Conaway. 1991. Initiation of eukaryotic messenger RNA synthesis. J. Biol. Chem. 266:17721–17724.
   PubMedGoogle Scholar
• Courey, A. J., and R. Tjian. 1988. Analysis of Sp1 in vivo reveals multiple transcriptional domains, including a novel glutamine-rich activation motif. Cell 55:887–898.
   PubMed Web of Science ®Google Scholar
• Déry, C. V., C. H. Herrmann, and M. B. Mathews. 1987. Response of individual adenovirus promoters to the products of the E1A gene. Oncogene 2:15–23.
   PubMedGoogle Scholar
• Deutsch, P. J., J. P. Hoeffler, J. L. Jameson, J. C. Un, and J. F. Habener. 1988. Structural determinants for transcriptional activation by cAMP-responsive DNA elements. J. Biol. Chem. 263:18466–18472.
   PubMedGoogle Scholar
• Dynan, W. S. 1986. Promoters for housekeeping genes. Trends Genet. 2:196–197.
   Web of Science ®Google Scholar
• Dynan, W. S. 1989. Modularity in promoters and enhancers. Cell 58:1–4.
   PubMedGoogle Scholar
• Ellis, L., E. Clauser, D. O. Morgan, M. Edery, R. A. Roth, and W. J. Rutter. 1986. Replacement of insulin receptor tyrosine residues 1162 and 1163 compromises insulin-stimulated kinase activity and uptake of 2-deoxyglucose. Cell 45:721–732.
   PubMed Web of Science ®Google Scholar
• Faber, P. W., H. C. J. van Rooij, H. J. Schippert, A. O. Brinkmann, and J. Trapman. 1993. Two different, overlapping pathways of transcription initiation are active on the TATA-less human androgen receptor promoter. J. Biol. Chem. 269:9296–9301.
   Google Scholar
• Ferguson, B., B. Krippl, O. Andrisani, N. Jones, H. Westphal, and M. Rosenberg. 1985. E1A 13S and 12S mRNA products made in Escherichia coli both function as nucleus-localized transcription activators but do not directly bind DNA. Mol. Cell. Biol. 5:2653–2661.
   PubMedGoogle Scholar
• Flint, J., and T. Shenk. 1989. Adenovirus E1A protein paradigm viral transactivator. Annu. Rev. Genet. 23:141–161.
   PubMed Web of Science ®Google Scholar
• Gill, G., I. Sadowski, and M. Ptashne. 1990. Mutations that increase the activity of a transcriptional activator in yeast and mammalian cells. Proc. Natl. Acad. Sci. USA 87:2127–2131.
   PubMedGoogle Scholar
• Gingeras, T. R., D. Sciaky, R. E. Gelinas, J. Bing-Dong, C. E. Yen, M. M. Kelly, P. A. Bullock, B. L. Parsons, K. E. O'Neill, and R. J. Roberts. 1982. Nucleotide sequences from the adenovirus-2 genome. J. Biol. Chem. 257:13475–13491.
   PubMed Web of Science ®Google Scholar
• Giniger, E., and M. Ptashne. 1987. Transcription in yeast activated by a putative amphipathic a helix linked to a DNA binding unit. Nature (London) 330:670–672.
   PubMedGoogle Scholar
• Gorman, C. M., L. F. Moffat, and B. H. Howard. 1982. Recombinant genomes which express chloramphenicol acetyl-transferase in mammalian cells. Mol. Cell. Biol. 2:1044–1051.
   PubMed Web of Science ®Google Scholar
• Hai, T., F. Uu, E. A. Allegretto, M. Karin, and M. R. Green. 1988. A family of immunologically related transcription factors that includes multiple forms of ATF and AP-1. Genes Dev. 2:1216–1226.
   PubMedGoogle Scholar
• Hai, T., F. Uu, W. J. Coukos, and M. R. Green. 1989. Transcription factor ATF cDNA clones: an extensive family of leucine zipper proteins able to selectively form DNA-binding heterodimers. Genes Dev. 3:2083–2090.
   PubMed Web of Science ®Google Scholar
• Hai, T., and T. Curran. 1991. Cross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity. Proc. Natl. Acad. Sci. USA 88:3720–3724.
   PubMed Web of Science ®Google Scholar
• Herbomel, P., B. Bourachot, and M. Yaniv. 1984. Two distinct enhancers with different cell specificities coexist in the regulatory region of polyoma. Cell 39:653–662.
   PubMed Web of Science ®Google Scholar
• Herrmann, C. H., and M. B. Mathews. 1989. The adenovirus E1B 19-kilodalton protein stimulates gene expression by increasing DNA levels. Mol. Cell. Biol. 9:5412–5423.
   PubMedGoogle Scholar
• Herschlag, D., and F. B. Johnson. 1993. Synergism in transcriptional activation: a kinetic view. Genes Dev. 7:173–179.
   PubMedGoogle Scholar
• Horikoshi, M., K. Maguire, A. Kralli, E. Maldonado, D. Reinberg, and R. Weinmann. 1991. Direct interaction between adenovirus E1A protein and the TATA box binding transcription factor IID. Proc. Natl. Acad. Sci. USA 88:5124–5128.
   PubMedGoogle Scholar
• Inostroza, J. A., F. H. Mermelstein, I. Ha, W. S. Lane, and D. Reinberg. 1992. Dr1, a TATA-binding protein-associated phosphoprotein and inhibitor of class II gene transcription. Cell 70:477–489.
   PubMedGoogle Scholar
• Jaskulski, D., C. Gatti, S. Travail, B. Calabretta, and R. Baserga. 1988. Regulation of the proliferating cell nuclear antigen (cyclin) and thymidine kinase mRNA levels by growth factors. J. Biol. Chem. 263:10175–10179.
   PubMed Web of Science ®Google Scholar
• Jelsma, T. N., J. A. Howe, J. S. Mymryk, C. M. Evelegh, N. F. A. Cunniff, and S. T. Bayley. 1989. Sequences in E1A proteins of human adenovirus 5 required for cell transformation, repression of a transcriptional enhancer, and induction of proliferating cell nuclear antigen. Virology 170:120–130.
   Google Scholar
• Johnson, P. F., and S. L. McKnight. 1989. Eukaryotic transcriptional regulatory proteins. Annu. Rev. Biochem. 58:799–839.
   PubMed Web of Science ®Google Scholar
• Jones, N. C., P. W. J. Rigby, and E. B. Ziff. 1988. Trans-acting protein factors and the regulation of eukaryotic transcription: lessons from studies on DNLA tumor viruses. Genes Dev. 2:267–281.
   PubMedGoogle Scholar
• Kannabiran, C., G. F. Morris, C. Labrie, and M. B. Mathews. 1993. The adenovirus E1A 12S product displays functional redundancy in activating the human proliferating cell nuclear antigen promoter. J. Virol. 67:507–515.
   PubMedGoogle Scholar
• Keegan, L., G. Gill, and M. Ptashne. 1986. Separation of DNA binding from transcription-activating function of a eukaryotic regulatory protein. Science 231:699–704.
   PubMed Web of Science ®Google Scholar
• Labrie, C. Unpublished data.
   Google Scholar
• Labrie, C., G. F. Morris, and M. B. Mathews. 1993. A complex promoter element mediates transactivation of the human proliferating cell nuclear antigen promoter by the 243-residue adenovirus E1A oncoprotein. Mol. Cell. Biol. 13:1697–1707.
   PubMedGoogle Scholar
• Lee, W. S., C. C. Kao, G. O. Bryant, X. Liu, and A. J. Berk. 1991. Adenovirus E1A activation domain binds the basic repeat in the TATA box transcription factor. Cell 67:365–376.
   PubMedGoogle Scholar
• Leff, T., R. Elkaim, C. R. Goding, P. Jalinot, P. Sassone-Corsi, M. Perricaudet, C. Kédinger, and P. Chambon. 1984. Individual products of the adenovirus 12S and 13S E1A mRNAs stimulate viral E2A and E3 expression at the transcriptional level. Proc. Natl. Acad. Sci. USA 81:4381–4385.
   PubMedGoogle Scholar
• Lillie, J. W., and M. R. Green. 1989. Transcription activation by the adenovirus E1A protein. Nature (London) 338:39–44.
   PubMedGoogle Scholar
• Liu, F., and M. R. Green. 1990. A specific member of the ATF transcription factor family can mediate transcription activation by the adenovirus E1A protein. Cell 61:1217–1224.
   PubMed Web of Science ®Google Scholar
• Lum, L. S., S. Hsu, M. Vaewhongs, and B. Wu. 1992. The hsp70 gene CCAAT-binding factor mediates transcriptional activation by the adenovirus E1A protein. Mol. Cell. Biol. 12:2599–2605.
   PubMedGoogle Scholar
• Ma, J., and M. Ptashne. 1987. Deletion analysis of GAL4 defines two transcriptional activating segments. Cell 48:847–853.
   PubMed Web of Science ®Google Scholar
• Mack, D. H., J. Vartikar, J. M. Pipas, and L. A. Laimins. 1993. Specific repression of TATA-mediated but not initiator-mediated transcription by wild-type p53. Nature (London) 363:281–283.
   PubMed Web of Science ®Google Scholar
• Maekawa, T., S. Matsuda, J.-I. Fujisawa, M. Yoshida, and S. Ishii. 1991. Cyclic AMP response element-binding protein, CRE-BP1, mediates the E1A-induced but not the Tax-induced trans-activation. Oncogene 6:627–632.
   PubMedGoogle Scholar
• Marais, R., J. Wynne, and R. Treisman. 1993. The SRF accessory protein Elk-1 contains a growth factor-regulated transcriptional activation domain. Cell 73:381–393.
   PubMed Web of Science ®Google Scholar
• Martin, K. J., J. W. Lillie, and M. R. Green. 1990. Evidence for interaction of different eukaryotic transcriptional activators with distinct cellular targets. Nature (London) 346:147–152.
   PubMedGoogle Scholar
• Matsumoto, K., T. Moriuchi, T. Koji, and P. Nakane. 1987. Molecular cloning of cDNA coding for rat proliferating cell nuclear antigen (PCNA)/cyclin. EMBO J. 6:637–642.
   PubMed Web of Science ®Google Scholar
• Mitchell, P. J., and R. Tjian. 1989. Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science 245:371–378.
   PubMed Web of Science ®Google Scholar
• Moran, E., and M. B. Mathews. 1987. Multiple functional domains of the adenovirus E1A gene. Cell 48:177–178.
   PubMed Web of Science ®Google Scholar
• Morris, G. F., and M. B. Mathews. 1990. Analysis of the proliferating cell nuclear antigen promoter and its response to adenovirus early region 1. J. Biol. Chem. 265:16116–16125.
   PubMed Web of Science ®Google Scholar
• Morris, G. F., and M. B. Mathews. 1991. The adenovirus E1A transforming protein activates the proliferating cell nuclear antigen promoter via an activating transcription factor site. J. Virol. 65:6397–6406.
   PubMedGoogle Scholar
• Mudryj, M., S. W. Hiebert, and J. R. Nevins. 1990. A role for the adenovirus inducible E2F transcription factor in a proliferation-dependent signal transduction pathway. EMBO J. 7:2179–2184.
   Google Scholar
• Nevins, J. R. 1989. Mechanisms of viral-mediated trans-activation of transcription. Adv. Virus Res. 37:35–83.
   PubMedGoogle Scholar
• Pietrzkowski, Z., H. Alder, C.-D. Chang, D. H. Ku, and R. Baserga. 1991. Characterization of an enhancer-like structure in the promoter region of the proliferating cell nuclear antigen (PCNA) gene. Exp. Cell Res. 193:283–290.
   PubMed Web of Science ®Google Scholar
• Prelich, G., M. Kostura, D. R. Marshak, M. B. Mathews, and B. Stillman. 1987. The cell-cycle regulated proliferating cell nuclear antigen is required for SV40 DNA replication in vitro. Nature (London) 326:471–475.
   PubMed Web of Science ®Google Scholar
• Ptashne, M. 1988. How eukaryotic transcriptional activators work. Nature (London) 335:683–689.
   PubMed Web of Science ®Google Scholar
• Pugh, B. F., and R. Tjian. 1990. Mechanism of transcriptional activation by Sp1: evidence for co-activators. Cell 61:1187–1197.
   PubMed Web of Science ®Google Scholar
• Pugh, B. F., and R. Tjian. 1991. Transcription from a TATA-less promoter requires a multisubunit TFIID complex. Genes Dev. 5:1935–1945.
   PubMedGoogle Scholar
• Rochette-Egly, L., C. Fromental, and P. Chambon. 1990. General repression of enhanson activity by the adenovirus-2 E1A proteins. Genes Dev. 4:137–150.
   PubMedGoogle Scholar
• Roy, A. L., M. Meisterernst, P. Pognonec, and R. G. Roeder. 1991. Cooperative interaction of an initiator-binding transcription initiation factor and the helix-loop-helix activator USF. Nature (London) 354:245–248.
   PubMedGoogle Scholar
• Ruley, E. 1990. Transforming collaborations between ras and nuclear oncogenes. Cancer Cells 2:258–268.
   PubMed Web of Science ®Google Scholar
• Sadowski, I., J. Ma, S. Triezenberg, and M. Ptashne. 1988. GAL4-VP16 is an unusually potent transcriptional activator. Nature (London) 335:563–564.
   PubMed Web of Science ®Google Scholar
• Sambrook, J., B. Sugden, W. Keller, and P. A. Sharp. 1973. Transcription of simian virus 40. III. Mapping of “early” and “late” species of RNA. Proc. Natl. Acad. Sci. USA 70:3711–3715.
   PubMedGoogle Scholar
• Segal, R., and A. J. Berk. 1991. Promoter activity and distance constraints of one versus two Spl binding sites. J. Biol. Chem. 266:20406–20411.
   PubMedGoogle Scholar
• Seipel, K., O. Georgiev, and W. Schaffner. 1992. Different activation domains stimulate transcription from remote (‘enhancer’) and proximal (‘promoter’) positions. EMBO J. 11:4961–4968.
   PubMedGoogle Scholar
• Seto, E., Y. Shi, and T. Shenk. 1991. YY1 is an initiator sequence-binding protein that directs and activates transcription in vitro. Nature (London) 354:241–245.
   PubMed Web of Science ®Google Scholar
• Shenk, T. 1989. Oncogenesis by DNA viruses: adenoviruses, p. 239–257. In R. A. Weinberg (ed.), Oncogenes and the molecular origins of cancer. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Shi, Y., E. Seto, L.-S. Chang, and T. Shenk. 1991. Transcriptional repression by YY1, a human GLI-Krüppel-related protein, and relief of repression by adenovirus E1A protein. Cell 67:377–388.
   PubMed Web of Science ®Google Scholar
• Shipman-Appasamy, P., K. S. Cohen, and M. B. Prystowsky. 1991. Nucleotide sequence of murine PCNA: interspecies comparison of the cDNA and the 5′ flanking region of the gene. DNA Seq. 2:181–191.
   PubMedGoogle Scholar
• Shivji, M. K. K., M. K. Kenny, and R. D. Wood. 1992. Proliferating cell nuclear antigen is required for DNA excision repair. Cell 69:367–374.
   PubMed Web of Science ®Google Scholar
• Simon, M. C., T. M. Fisch, B. J. Benecke, J. R. Nevins, and N. Heintz. 1988. Definition of multiple, functionally distinct TATA elements, one of which is a target in the hsp70 promoter for E1A regulation. Cell 52:723–729.
   PubMedGoogle Scholar
• Simon, M. C., R. J. Rooney, T. M. Fisch, N. Heintz, and J. R. Nevins. 1990. E1A-dependent trans-activation of the c-fos promoter requires the TATAA sequence. Proc. Natl. Acad. Sci. USA 87:513–517.
   PubMedGoogle Scholar
• Smale, S. T., and D. Baltimore. 1989. The “initiator” as a transcription control element. Cell 57:103–113.
   PubMed Web of Science ®Google Scholar
• Smale, S. T., M. C. Schmidt, A. J. Berk, and D. Baltimore. 1990. Transcriptional activation by Sp1 as directed through TATA or initiator: specific requirement for mammalian transcription factor IID. Proc. Natl. Acad. Sci. USA 87:4509–4513.
   PubMedGoogle Scholar
• Spaete, R. R., and E. S. Mocarski. 1985. Regulation of cytomegalovirus gene expression: a and β promoters are trans activated by viral functions in permissive human fibroblasts. J. Virol. 56:135–143.
   PubMedGoogle Scholar
• Stein, R. W., M. Corrigan, P. Yaciuk, J. Whelan, and E. Moran. 1990. Analysis of E1A-mediated growth regulation functions: binding of the 300-kilodalton cellular product correlates with E1A enhancer repression function and DNA synthesis-inducing activity. J. Virol. 64:4421–4427.
   PubMedGoogle Scholar
• Stern, S., M. Tanaka, and W. Herr. 1989. The oct-1 homoeo domain directs formation of a multiprotein-DNA complex with the HSV transactivator VP16. Nature (London) 341:624–630.
   PubMed Web of Science ®Google Scholar
• Su, W., S. Jackson, R. Tjian, and H. Echols. 1991. DNA looping between sites for transcriptional activation: self-association of DNA-bound Spl. Genes Dev. 5:820–826.
   PubMed Web of Science ®Google Scholar
• Taylor, I. C. A., and R. E. Kingston. 1990. E1A transactivation of the human hsp70 gene promoter substitution mutants is independent of the composition of upstream and TATA elements. Mol. Cell. Biol. 10:176–183.
   PubMedGoogle Scholar
• Timmers, Η. T. M., and P. A. Sharp. 1991. The mammalian TFIID protein is present in two functionally distinct complexes. Genes Dev. 5:1946–1956.
   PubMedGoogle Scholar
• Vallejo, M., D. Ron, C. P. Miller, and J. F. Habener. 1993. C/ATF, a member of the activating transcription factor family of DNA-binding proteins, dimerizes with CAAT/enhancer-binding proteins and directs their binding to cAMP response elements. Proc. Natl. Acad. Sci. USA 90:4679–4683.
   PubMedGoogle Scholar
• van Dam, Η., M. Duyndam, R. Rottier, A. Bosch, L. de Vries-Smits, P. Herrlich, A. Zantema, P. Angel, and A. J. van der Eb. 1993. Heterodimer formation of cJun and ATF-2 is responsible for induction of c-jun by the 243 amino acid adenovirus E1A protein. EMBO J. 12:479–487.
   PubMed Web of Science ®Google Scholar
• Webster, L. C., and R. P. Ricciardi. 1991. trans-dominant mutant of E1A provide genetic evidence that the zinc finger of the trans-acting domain binds a transcription factor. Mol. Cell. Biol. 11:4287–4296.
   PubMedGoogle Scholar
• Wefald, F. C., B. H. Devlin, and R. S. Williams. 1990. Functional heterogeneity of mammalian TATA-box sequences revealed by interaction with a cell-specific enhancer. Nature (London) 344:260–262.
   PubMedGoogle Scholar
• Weinmann, R. 1992. The basic RNA polymerase II transcriptional machinery. Gene Expression 2:81–91.
   PubMedGoogle Scholar
• Weintraub, S. J., and D. C. Dean. 1992. Interaction of a common factor with ATF, Spl or TATAA promoter elements is required for these sequences to mediate transactivation by the adenoviral oncogene E1A. Mol. Cell. Biol. 12:512–517.
   PubMedGoogle Scholar
• Wen, P., N. Crawford, and J. Locker. 1993. A promoter-linked coupling region required for stimulation of α-fetoprotein transcription by distant enhancers. Nucleic Acids Res. 21:1911–1918.
   PubMedGoogle Scholar
• Wiley, S. R., R. J. Kraus, and J. E. Mertz. 1992. Functional binding of the “TATA” box binding component of transcription factor TFIID to the −30 region of TATA-less promoters. Proc. Natl. Acad. Sci. USA 89:5814–5818.
   PubMedGoogle Scholar
• Wu, L., D. S. E. Rosser, M. G. Schmidt, and A. J. Berk. 1987. A TATA box implicated in E1A transcriptional activation of a simple adenovirus 2 promoter. Nature (London) 326:512–515.
   PubMedGoogle Scholar
• Zawel, L., and D. Reinberg. 1993. Initiation of transcription by RNA polymerase II: a multi-step process. Prog. Nucleic Acid Res. 44:67–109.
   PubMedGoogle Scholar
• Zenke, M., T. Grundström, H. Matthes, M. Wintzerith, C. Schatz, A. Wildeman, and P. Chambon. 1986. Multiple sequence motifs are involved in SV40 enhancer function. EMBO J. 5:387–397.
   PubMed Web of Science ®Google Scholar
• Zerler, B., R. J. Roberts, M. B. Mathews, and E. Moran. 1987. Separate functional domains of the adenovirus E1A gene are involved in regulation of host cell cycle products. Mol. Cell. Biol. 7:821–829.
   PubMed Web of Science ®Google Scholar