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. 1996 Apr;16(4):1659–1667. doi: 10.1128/mcb.16.4.1659

Interaction of Sp1 with the growth- and cell cycle-regulated transcription factor E2F.

J Karlseder 1, H Rotheneder 1, E Wintersberger 1
PMCID: PMC231152  PMID: 8657141

Abstract

Within the region around 150 bp upstream of the initiation codon, which was previously shown to suffice for growth-regulated expression, the murine thymidine kinase gene carries a single binding site for transcription factor Sp1; about 10 bp downstream of this site, there is a binding motif for transcription factor E2F. The latter protein appears to be responsible for growth regulation of the promoter. Mutational inactivation of either the Sp1 or the E2F site almost completely abolishes promoter activity, suggesting that the two transcription factors interact directly in delivering an activation signal to the basic transcription machinery. This was verified by demonstrating with the use of glutathione S-transferase fusion proteins that E2F and Sp1 bind to each other in vitro. For this interaction, the C-terminal part of Sp1 and the N terminus of E2F1, a domain also present in E2F2 and E2F3 but absent in E2F4 and E2F5, were essential. Accordingly, E2F1 to E2F3 but not E2F4 and E2F5 were found to bind sp1 in vitro. Coimmunoprecipitation experiments showed that complexes exist in vivo, and it was estabilished that the distance between the binding sites for the two transcription factors was critical for optimal promoter activity. Finally, in vivo footprinting experiments indicated that both the sp1 and E2F binding sites are occupied throughout the cell cycle. Mutation of either binding motif abolished binding of both transcription factors in vivo, which may indicate cooperative binding of the two proteins to chromatin-organized DNA. Our data are in line with the hypothesis that E2F functions as a growth- and cell cycle regulated tethering factor between Sp1 and the basic transcription machinery.

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Selected References

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  1. Adams C. C., Workman J. L. Binding of disparate transcriptional activators to nucleosomal DNA is inherently cooperative. Mol Cell Biol. 1995 Mar;15(3):1405–1421. doi: 10.1128/mcb.15.3.1405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aubin R. J., Weinfeld M., Paterson M. C. Factors influencing efficiency and reproducibility of polybrene-assisted gene transfer. Somat Cell Mol Genet. 1988 Mar;14(2):155–167. doi: 10.1007/BF01534401. [DOI] [PubMed] [Google Scholar]
  3. Bandara L. R., Buck V. M., Zamanian M., Johnston L. H., La Thangue N. B. Functional synergy between DP-1 and E2F-1 in the cell cycle-regulating transcription factor DRTF1/E2F. EMBO J. 1993 Nov;12(11):4317–4324. doi: 10.1002/j.1460-2075.1993.tb06116.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bandara L. R., Lam E. W., Sørensen T. S., Zamanian M., Girling R., La Thangue N. B. DP-1: a cell cycle-regulated and phosphorylated component of transcription factor DRTF1/E2F which is functionally important for recognition by pRb and the adenovirus E4 orf 6/7 protein. EMBO J. 1994 Jul 1;13(13):3104–3114. doi: 10.1002/j.1460-2075.1994.tb06609.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beijersbergen R. L., Kerkhoven R. M., Zhu L., Carlée L., Voorhoeve P. M., Bernards R. E2F-4, a new member of the E2F gene family, has oncogenic activity and associates with p107 in vivo. Genes Dev. 1994 Nov 15;8(22):2680–2690. doi: 10.1101/gad.8.22.2680. [DOI] [PubMed] [Google Scholar]
  6. Blake M. C., Azizkhan J. C. Transcription factor E2F is required for efficient expression of the hamster dihydrofolate reductase gene in vitro and in vivo. Mol Cell Biol. 1989 Nov;9(11):4994–5002. doi: 10.1128/mcb.9.11.4994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Blake M. C., Jambou R. C., Swick A. G., Kahn J. W., Azizkhan J. C. Transcriptional initiation is controlled by upstream GC-box interactions in a TATAA-less promoter. Mol Cell Biol. 1990 Dec;10(12):6632–6641. doi: 10.1128/mcb.10.12.6632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dou Q. P., Zhao S., Levin A. H., Wang J., Helin K., Pardee A. B. G1/S-regulated E2F-containing protein complexes bind to the mouse thymidine kinase gene promoter. J Biol Chem. 1994 Jan 14;269(2):1306–1313. [PubMed] [Google Scholar]
  9. Dyson N., Dembski M., Fattaey A., Ngwu C., Ewen M., Helin K. Analysis of p107-associated proteins: p107 associates with a form of E2F that differs from pRB-associated E2F-1. J Virol. 1993 Dec;67(12):7641–7647. doi: 10.1128/jvi.67.12.7641-7647.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fetzer J., Michael M., Bohner T., Hofbauer R., Folkers G. A fast method for obtaining highly pure recombinant herpes simplex virus type 1 thymidine kinase. Protein Expr Purif. 1994 Oct;5(5):432–441. doi: 10.1006/prep.1994.1062. [DOI] [PubMed] [Google Scholar]
  11. Fridovich-Keil J. L., Markell P. J., Gudas J. M., Pardee A. B. DNA sequences required for serum-responsive regulation of expression from the mouse thymidine kinase promoter. Cell Growth Differ. 1993 Aug;4(8):679–687. [PubMed] [Google Scholar]
  12. Ginsberg D., Vairo G., Chittenden T., Xiao Z. X., Xu G., Wydner K. L., DeCaprio J. A., Lawrence J. B., Livingston D. M. E2F-4, a new member of the E2F transcription factor family, interacts with p107. Genes Dev. 1994 Nov 15;8(22):2665–2679. doi: 10.1101/gad.8.22.2665. [DOI] [PubMed] [Google Scholar]
  13. Girling R., Partridge J. F., Bandara L. R., Burden N., Totty N. F., Hsuan J. J., La Thangue N. B. A new component of the transcription factor DRTF1/E2F. Nature. 1993 Mar 4;362(6415):83–87. doi: 10.1038/362083a0. [DOI] [PubMed] [Google Scholar]
  14. Gudas J. M., Fridovich-Keil J. L., Datta M. W., Bryan J., Pardee A. B. Characterization of the murine thymidine kinase-encoding gene and analysis of transcription start point heterogeneity. Gene. 1992 Sep 10;118(2):205–216. doi: 10.1016/0378-1119(92)90190-z. [DOI] [PubMed] [Google Scholar]
  15. Hagemeier C., Cook A., Kouzarides T. The retinoblastoma protein binds E2F residues required for activation in vivo and TBP binding in vitro. Nucleic Acids Res. 1993 Nov 11;21(22):4998–5004. doi: 10.1093/nar/21.22.4998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hamel P. A., Gallie B. L., Phillips R. A. The retinoblastoma protein and cell cycle regulation. Trends Genet. 1992 May;8(5):180–185. doi: 10.1016/0168-9525(92)90221-o. [DOI] [PubMed] [Google Scholar]
  17. Helin K., Lees J. A., Vidal M., Dyson N., Harlow E., Fattaey A. A cDNA encoding a pRB-binding protein with properties of the transcription factor E2F. Cell. 1992 Jul 24;70(2):337–350. doi: 10.1016/0092-8674(92)90107-n. [DOI] [PubMed] [Google Scholar]
  18. Helin K., Wu C. L., Fattaey A. R., Lees J. A., Dynlacht B. D., Ngwu C., Harlow E. Heterodimerization of the transcription factors E2F-1 and DP-1 leads to cooperative trans-activation. Genes Dev. 1993 Oct;7(10):1850–1861. doi: 10.1101/gad.7.10.1850. [DOI] [PubMed] [Google Scholar]
  19. Hiebert S. W., Blake M., Azizkhan J., Nevins J. R. Role of E2F transcription factor in E1A-mediated trans activation of cellular genes. J Virol. 1991 Jul;65(7):3547–3552. doi: 10.1128/jvi.65.7.3547-3552.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hiebert S. W., Chellappan S. P., Horowitz J. M., Nevins J. R. The interaction of RB with E2F coincides with an inhibition of the transcriptional activity of E2F. Genes Dev. 1992 Feb;6(2):177–185. doi: 10.1101/gad.6.2.177. [DOI] [PubMed] [Google Scholar]
  21. Hijmans E. M., Voorhoeve P. M., Beijersbergen R. L., van 't Veer L. J., Bernards R. E2F-5, a new E2F family member that interacts with p130 in vivo. Mol Cell Biol. 1995 Jun;15(6):3082–3089. doi: 10.1128/mcb.15.6.3082. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hoey T., Weinzierl R. O., Gill G., Chen J. L., Dynlacht B. D., Tjian R. Molecular cloning and functional analysis of Drosophila TAF110 reveal properties expected of coactivators. Cell. 1993 Jan 29;72(2):247–260. doi: 10.1016/0092-8674(93)90664-c. [DOI] [PubMed] [Google Scholar]
  23. Huber H. E., Edwards G., Goodhart P. J., Patrick D. R., Huang P. S., Ivey-Hoyle M., Barnett S. F., Oliff A., Heimbrook D. C. Transcription factor E2F binds DNA as a heterodimer. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3525–3529. doi: 10.1073/pnas.90.8.3525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Imataka H., Sogawa K., Yasumoto K., Kikuchi Y., Sasano K., Kobayashi A., Hayami M., Fujii-Kuriyama Y. Two regulatory proteins that bind to the basic transcription element (BTE), a GC box sequence in the promoter region of the rat P-4501A1 gene. EMBO J. 1992 Oct;11(10):3663–3671. doi: 10.1002/j.1460-2075.1992.tb05451.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ivey-Hoyle M., Conroy R., Huber H. E., Goodhart P. J., Oliff A., Heimbrook D. C. Cloning and characterization of E2F-2, a novel protein with the biochemical properties of transcription factor E2F. Mol Cell Biol. 1993 Dec;13(12):7802–7812. doi: 10.1128/mcb.13.12.7802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Janson L., Pettersson U. Cooperative interactions between transcription factors Sp1 and OTF-1. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4732–4736. doi: 10.1073/pnas.87.12.4732. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Jordan K. L., Haas A. R., Logan T. J., Hall D. J. Detailed analysis of the basic domain of the E2F1 transcription factor indicates that it is unique among bHLH proteins. Oncogene. 1994 Apr;9(4):1177–1185. [PubMed] [Google Scholar]
  28. Kadonaga J. T., Carner K. R., Masiarz F. R., Tjian R. Isolation of cDNA encoding transcription factor Sp1 and functional analysis of the DNA binding domain. Cell. 1987 Dec 24;51(6):1079–1090. doi: 10.1016/0092-8674(87)90594-0. [DOI] [PubMed] [Google Scholar]
  29. Kaelin W. G., Jr, Krek W., Sellers W. R., DeCaprio J. A., Ajchenbaum F., Fuchs C. S., Chittenden T., Li Y., Farnham P. J., Blanar M. A. Expression cloning of a cDNA encoding a retinoblastoma-binding protein with E2F-like properties. Cell. 1992 Jul 24;70(2):351–364. doi: 10.1016/0092-8674(92)90108-o. [DOI] [PubMed] [Google Scholar]
  30. Kaelin W. G., Jr, Pallas D. C., DeCaprio J. A., Kaye F. J., Livingston D. M. Identification of cellular proteins that can interact specifically with the T/E1A-binding region of the retinoblastoma gene product. Cell. 1991 Feb 8;64(3):521–532. doi: 10.1016/0092-8674(91)90236-r. [DOI] [PubMed] [Google Scholar]
  31. Kitagawa M., Higashi H., Suzuki-Takahashi I., Segawa K., Hanks S. K., Taya Y., Nishimura S., Okuyama A. Phosphorylation of E2F-1 by cyclin A-cdk2. Oncogene. 1995 Jan 19;10(2):229–236. [PubMed] [Google Scholar]
  32. Kouzarides T. Transcriptional regulation by the retinoblastoma protein. Trends Cell Biol. 1993 Jul;3(7):211–213. doi: 10.1016/0962-8924(93)90113-f. [DOI] [PubMed] [Google Scholar]
  33. Krek W., Ewen M. E., Shirodkar S., Arany Z., Kaelin W. G., Jr, Livingston D. M. Negative regulation of the growth-promoting transcription factor E2F-1 by a stably bound cyclin A-dependent protein kinase. Cell. 1994 Jul 15;78(1):161–172. doi: 10.1016/0092-8674(94)90582-7. [DOI] [PubMed] [Google Scholar]
  34. La Thangue N. B. DRTF1/E2F: an expanding family of heterodimeric transcription factors implicated in cell-cycle control. Trends Biochem Sci. 1994 Mar;19(3):108–114. doi: 10.1016/0968-0004(94)90202-x. [DOI] [PubMed] [Google Scholar]
  35. Lai J. S., Herr W. Ethidium bromide provides a simple tool for identifying genuine DNA-independent protein associations. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6958–6962. doi: 10.1073/pnas.89.15.6958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Lam E. W., La Thangue N. B. DP and E2F proteins: coordinating transcription with cell cycle progression. Curr Opin Cell Biol. 1994 Dec;6(6):859–866. doi: 10.1016/0955-0674(94)90057-4. [DOI] [PubMed] [Google Scholar]
  37. Lees J. A., Saito M., Vidal M., Valentine M., Look T., Harlow E., Dyson N., Helin K. The retinoblastoma protein binds to a family of E2F transcription factors. Mol Cell Biol. 1993 Dec;13(12):7813–7825. doi: 10.1128/mcb.13.12.7813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Li R., Knight J. D., Jackson S. P., Tjian R., Botchan M. R. Direct interaction between Sp1 and the BPV enhancer E2 protein mediates synergistic activation of transcription. Cell. 1991 May 3;65(3):493–505. doi: 10.1016/0092-8674(91)90467-d. [DOI] [PubMed] [Google Scholar]
  39. Li Y., Slansky J. E., Myers D. J., Drinkwater N. R., Kaelin W. G., Farnham P. J. Cloning, chromosomal location, and characterization of mouse E2F1. Mol Cell Biol. 1994 Mar;14(3):1861–1869. doi: 10.1128/mcb.14.3.1861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Lieberman H. B., Lin P. F., Yeh D. B., Ruddle F. H. Transcriptional and posttranscriptional mechanisms regulate murine thymidine kinase gene expression in serum-stimulated cells. Mol Cell Biol. 1988 Dec;8(12):5280–5291. doi: 10.1128/mcb.8.12.5280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Lin S. Y., Black A. R., Kostic D., Pajovic S., Hoover C. N., Azizkhan J. C. Cell cycle-regulated association of E2F1 and Sp1 is related to their functional interaction. Mol Cell Biol. 1996 Apr;16(4):1668–1675. doi: 10.1128/mcb.16.4.1668. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Merika M., Orkin S. H. Functional synergy and physical interactions of the erythroid transcription factor GATA-1 with the Krüppel family proteins Sp1 and EKLF. Mol Cell Biol. 1995 May;15(5):2437–2447. doi: 10.1128/mcb.15.5.2437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Moran E. DNA tumor virus transforming proteins and the cell cycle. Curr Opin Genet Dev. 1993 Feb;3(1):63–70. doi: 10.1016/s0959-437x(05)80342-9. [DOI] [PubMed] [Google Scholar]
  44. Mueller P. R., Salser S. J., Wold B. Constitutive and metal-inducible protein:DNA interactions at the mouse metallothionein I promoter examined by in vivo and in vitro footprinting. Genes Dev. 1988 Apr;2(4):412–427. doi: 10.1101/gad.2.4.412. [DOI] [PubMed] [Google Scholar]
  45. Mueller P. R., Wold B. In vivo footprinting of a muscle specific enhancer by ligation mediated PCR. Science. 1989 Nov 10;246(4931):780–786. doi: 10.1126/science.2814500. [DOI] [PubMed] [Google Scholar]
  46. Murata Y., Kim H. G., Rogers K. T., Udvadia A. J., Horowitz J. M. Negative regulation of Sp1 trans-activation is correlated with the binding of cellular proteins to the amino terminus of the Sp1 trans-activation domain. J Biol Chem. 1994 Aug 12;269(32):20674–20681. [PubMed] [Google Scholar]
  47. Naeve G. S., Sharma A., Lee A. S. Temporal events regulating the early phases of the mammalian cell cycle. Curr Opin Cell Biol. 1991 Apr;3(2):261–268. doi: 10.1016/0955-0674(91)90150-w. [DOI] [PubMed] [Google Scholar]
  48. Nevins J. R. Cell cycle targets of the DNA tumor viruses. Curr Opin Genet Dev. 1994 Feb;4(1):130–134. doi: 10.1016/0959-437x(94)90101-5. [DOI] [PubMed] [Google Scholar]
  49. Nevins J. R. E2F: a link between the Rb tumor suppressor protein and viral oncoproteins. Science. 1992 Oct 16;258(5081):424–429. doi: 10.1126/science.1411535. [DOI] [PubMed] [Google Scholar]
  50. Ogris E., Rotheneder H., Mudrak I., Pichler A., Wintersberger E. A binding site for transcription factor E2F is a target for trans activation of murine thymidine kinase by polyomavirus large T antigen and plays an important role in growth regulation of the gene. J Virol. 1993 Apr;67(4):1765–1771. doi: 10.1128/jvi.67.4.1765-1771.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Pagano M., Draetta G., Jansen-Dürr P. Association of cdk2 kinase with the transcription factor E2F during S phase. Science. 1992 Feb 28;255(5048):1144–1147. doi: 10.1126/science.1312258. [DOI] [PubMed] [Google Scholar]
  52. Pardee A. B. G1 events and regulation of cell proliferation. Science. 1989 Nov 3;246(4930):603–608. doi: 10.1126/science.2683075. [DOI] [PubMed] [Google Scholar]
  53. Pascal E., Tjian R. Different activation domains of Sp1 govern formation of multimers and mediate transcriptional synergism. Genes Dev. 1991 Sep;5(9):1646–1656. doi: 10.1101/gad.5.9.1646. [DOI] [PubMed] [Google Scholar]
  54. Plet A., Tourkine N., Mechti N., Jeanteur P., Blanchard J. M. In vivo footprints between the murine c-myc P1 and P2 promoters. Oncogene. 1992 Sep;7(9):1847–1851. [PubMed] [Google Scholar]
  55. Pugh B. F., Tjian R. Mechanism of transcriptional activation by Sp1: evidence for coactivators. Cell. 1990 Jun 29;61(7):1187–1197. doi: 10.1016/0092-8674(90)90683-6. [DOI] [PubMed] [Google Scholar]
  56. Pugh B. F., Tjian R. Transcription from a TATA-less promoter requires a multisubunit TFIID complex. Genes Dev. 1991 Nov;5(11):1935–1945. doi: 10.1101/gad.5.11.1935. [DOI] [PubMed] [Google Scholar]
  57. Rotheneder H., Grabner M., Wintersberger E. Presence of regulatory sequences within intron 2 of the mouse thymidine kinase gene. Nucleic Acids Res. 1991 Dec 25;19(24):6805–6809. doi: 10.1093/nar/19.24.6805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Sardet C., Vidal M., Cobrinik D., Geng Y., Onufryk C., Chen A., Weinberg R. A. E2F-4 and E2F-5, two members of the E2F family, are expressed in the early phases of the cell cycle. Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):2403–2407. doi: 10.1073/pnas.92.6.2403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Seiser C., Knöfler M., Rudelstorfer I., Haas R., Wintersberger E. Mouse thymidine kinase: the promoter sequence and the gene and pseudogene structures in normal cells and in thymidine kinase deficient mutants. Nucleic Acids Res. 1989 Jan 11;17(1):185–195. doi: 10.1093/nar/17.1.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Seto E., Lewis B., Shenk T. Interaction between transcription factors Sp1 and YY1. Nature. 1993 Sep 30;365(6445):462–464. doi: 10.1038/365462a0. [DOI] [PubMed] [Google Scholar]
  61. Shan B., Zhu X., Chen P. L., Durfee T., Yang Y., Sharp D., Lee W. H. Molecular cloning of cellular genes encoding retinoblastoma-associated proteins: identification of a gene with properties of the transcription factor E2F. Mol Cell Biol. 1992 Dec;12(12):5620–5631. doi: 10.1128/mcb.12.12.5620. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Sherr C. J. The ins and outs of RB: coupling gene expression to the cell cycle clock. Trends Cell Biol. 1994 Jan;4(1):15–18. doi: 10.1016/0962-8924(94)90033-7. [DOI] [PubMed] [Google Scholar]
  63. Slansky J. E., Li Y., Kaelin W. G., Farnham P. J. A protein synthesis-dependent increase in E2F1 mRNA correlates with growth regulation of the dihydrofolate reductase promoter. Mol Cell Biol. 1993 Mar;13(3):1610–1618. doi: 10.1128/mcb.13.3.1610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Vairo G., Livingston D. M., Ginsberg D. Functional interaction between E2F-4 and p130: evidence for distinct mechanisms underlying growth suppression by different retinoblastoma protein family members. Genes Dev. 1995 Apr 1;9(7):869–881. doi: 10.1101/gad.9.7.869. [DOI] [PubMed] [Google Scholar]
  65. Wade M., Blake M. C., Jambou R. C., Helin K., Harlow E., Azizkhan J. C. An inverted repeat motif stabilizes binding of E2F and enhances transcription of the dihydrofolate reductase gene. J Biol Chem. 1995 Apr 28;270(17):9783–9791. doi: 10.1074/jbc.270.17.9783. [DOI] [PubMed] [Google Scholar]
  66. Weichselbraun I., Ogris E., Wintersberger E. Bidirectional promoter activity of the 5' flanking region of the mouse thymidine kinase gene. FEBS Lett. 1990 Nov 26;275(1-2):49–52. doi: 10.1016/0014-5793(90)81436-r. [DOI] [PubMed] [Google Scholar]
  67. Weinberg R. A. The retinoblastoma protein and cell cycle control. Cell. 1995 May 5;81(3):323–330. doi: 10.1016/0092-8674(95)90385-2. [DOI] [PubMed] [Google Scholar]
  68. Weinzierl R. O., Dynlacht B. D., Tjian R. Largest subunit of Drosophila transcription factor IID directs assembly of a complex containing TBP and a coactivator. Nature. 1993 Apr 8;362(6420):511–517. doi: 10.1038/362511a0. [DOI] [PubMed] [Google Scholar]
  69. Wintersberger E. Biochemical events controlling initiation and propagation of the S phase of the cell cycle. Rev Physiol Biochem Pharmacol. 1991;118:49–95. doi: 10.1007/BFb0031481. [DOI] [PubMed] [Google Scholar]
  70. Wintersberger E., Rotheneder H., Grabner M., Beck G., Seiser C. Regulation of thymidine kinase during growth, cell cycle and differentiation. Adv Enzyme Regul. 1992;32:241–254. doi: 10.1016/0065-2571(92)90020-z. [DOI] [PubMed] [Google Scholar]
  71. Wu C. L., Zukerberg L. R., Ngwu C., Harlow E., Lees J. A. In vivo association of E2F and DP family proteins. Mol Cell Biol. 1995 May;15(5):2536–2546. doi: 10.1128/mcb.15.5.2536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Xu M., Sheppard K. A., Peng C. Y., Yee A. S., Piwnica-Worms H. Cyclin A/CDK2 binds directly to E2F-1 and inhibits the DNA-binding activity of E2F-1/DP-1 by phosphorylation. Mol Cell Biol. 1994 Dec;14(12):8420–8431. doi: 10.1128/mcb.14.12.8420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Zhang Y., Chellappan S. P. Cloning and characterization of human DP2, a novel dimerization partner of E2F. Oncogene. 1995 Jun 1;10(11):2085–2093. [PubMed] [Google Scholar]

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