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. 1997 Aug;17(8):4419–4433. doi: 10.1128/mcb.17.8.4419

Isolation and characterization of a novel epithelium-specific transcription factor, ESE-1, a member of the ets family.

P Oettgen 1, R M Alani 1, M A Barcinski 1, L Brown 1, Y Akbarali 1, J Boltax 1, C Kunsch 1, K Munger 1, T A Libermann 1
PMCID: PMC232296  PMID: 9234700

Abstract

We report here the isolation of a novel, highly tissue-restricted member of the ets transcription factor/oncogene family, ESE-1 (for epithelium-specific Ets), which has features distinct from those of any other ets-related factor. ESE-1 contains two putative DNA binding domains: an ETS domain, which is unique in that the 5' half shows relatively weak homology to known ets factors, and an A/T hook domain, found in HMG proteins and various other nuclear factors. In contrast to any known ets factors, ESE-1 is expressed exclusively in epithelial cells. ESE-1 expression is induced during terminal differentiation of the epidermis and in a primary human keratinocyte differentiation system. The keratinocyte terminal differentiation marker gene, SPRR2A, is a putative target for ESE-1, since SPRR2A expression during keratinocyte differentiation correlates with induction of ESE-1 expression, and ESE-1 binds with high affinity to and transactivates the ets binding site in the SPRR2A promoter. ESE-1 also binds to and transactivates the enhancer of the Endo A gene, a potential target for ESE-1 in simple epithelia. Due to the important role that other ets factors play in cellular differentiation, ESE-1 is expected to be a critical regulator of epithelial cell differentiation.

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Selected References

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  1. Abe M., Oshima R. G. A single human keratin 18 gene is expressed in diverse epithelial cells of transgenic mice. J Cell Biol. 1990 Sep;111(3):1197–1206. doi: 10.1083/jcb.111.3.1197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ashar H. R., Fejzo M. S., Tkachenko A., Zhou X., Fletcher J. A., Weremowicz S., Morton C. C., Chada K. Disruption of the architectural factor HMGI-C: DNA-binding AT hook motifs fused in lipomas to distinct transcriptional regulatory domains. Cell. 1995 Jul 14;82(1):57–65. doi: 10.1016/0092-8674(95)90052-7. [DOI] [PubMed] [Google Scholar]
  3. Beaudette K. N., Lew J., Wang J. H. Substrate specificity characterization of a cdc2-like protein kinase purified from bovine brain. J Biol Chem. 1993 Oct 5;268(28):20825–20830. [PubMed] [Google Scholar]
  4. Bories J. C., Willerford D. M., Grévin D., Davidson L., Camus A., Martin P., Stéhelin D., Alt F. W. Increased T-cell apoptosis and terminal B-cell differentiation induced by inactivation of the Ets-1 proto-oncogene. Nature. 1995 Oct 19;377(6550):635–638. doi: 10.1038/377635a0. [DOI] [PubMed] [Google Scholar]
  5. Broeker P. L., Harden A., Rowley J. D., Zeleznik-Le N. The mixed lineage leukemia (MLL) protein involved in 11q23 translocations contains a domain that binds cruciform DNA and scaffold attachment region (SAR) DNA. Curr Top Microbiol Immunol. 1996;211:259–268. doi: 10.1007/978-3-642-85232-9_26. [DOI] [PubMed] [Google Scholar]
  6. Cheng C., Kilkenny A. E., Roop D., Yuspa S. H. The v-ras oncogene inhibits the expression of differentiation markers and facilitates expression of cytokeratins 8 and 18 in mouse keratinocytes. Mol Carcinog. 1990;3(6):363–373. doi: 10.1002/mc.2940030608. [DOI] [PubMed] [Google Scholar]
  7. Cheng C., Tennenbaum T., Dempsey P. J., Coffey R. J., Yuspa S. H., Dlugosz A. A. Epidermal growth factor receptor ligands regulate keratin 8 expression in keratinocytes, and transforming growth factor alpha mediates the induction of keratin 8 by the v-rasHa oncogene. Cell Growth Differ. 1993 Apr;4(4):317–327. [PubMed] [Google Scholar]
  8. 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]
  9. Delattre O., Zucman J., Plougastel B., Desmaze C., Melot T., Peter M., Kovar H., Joubert I., de Jong P., Rouleau G. Gene fusion with an ETS DNA-binding domain caused by chromosome translocation in human tumours. Nature. 1992 Sep 10;359(6391):162–165. doi: 10.1038/359162a0. [DOI] [PubMed] [Google Scholar]
  10. Dlugosz A. A., Cheng C., Denning M. F., Dempsey P. J., Coffey R. J., Jr, Yuspa S. H. Keratinocyte growth factor receptor ligands induce transforming growth factor alpha expression and activate the epidermal growth factor receptor signaling pathway in cultured epidermal keratinocytes. Cell Growth Differ. 1994 Dec;5(12):1283–1292. [PubMed] [Google Scholar]
  11. Farr A., Roman A. A pitfall of using a second plasmid to determine transfection efficiency. Nucleic Acids Res. 1992 Feb 25;20(4):920–920. doi: 10.1093/nar/20.4.920. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Faus I., Hsu H. J., Fuchs E. Oct-6: a regulator of keratinocyte gene expression in stratified squamous epithelia. Mol Cell Biol. 1994 May;14(5):3263–3275. doi: 10.1128/mcb.14.5.3263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ffrench-Constant C., Van de Water L., Dvorak H. F., Hynes R. O. Reappearance of an embryonic pattern of fibronectin splicing during wound healing in the adult rat. J Cell Biol. 1989 Aug;109(2):903–914. doi: 10.1083/jcb.109.2.903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fischer D. F., Gibbs S., van De Putte P., Backendorf C. Interdependent transcription control elements regulate the expression of the SPRR2A gene during keratinocyte terminal differentiation. Mol Cell Biol. 1996 Oct;16(10):5365–5374. doi: 10.1128/mcb.16.10.5365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fitzsimmons D., Hodsdon W., Wheat W., Maira S. M., Wasylyk B., Hagman J. Pax-5 (BSAP) recruits Ets proto-oncogene family proteins to form functional ternary complexes on a B-cell-specific promoter. Genes Dev. 1996 Sep 1;10(17):2198–2211. doi: 10.1101/gad.10.17.2198. [DOI] [PubMed] [Google Scholar]
  16. Fujimura Y., Yamamoto H., Hamazato F., Nozaki M. One of two Ets-binding sites in the cytokeratin EndoA enhancer is essential for enhancer activity and binds to Ets-2 related proteins. Nucleic Acids Res. 1994 Feb 25;22(4):613–618. doi: 10.1093/nar/22.4.613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gilman M. Z., Wilson R. N., Weinberg R. A. Multiple protein-binding sites in the 5'-flanking region regulate c-fos expression. Mol Cell Biol. 1986 Dec;6(12):4305–4316. doi: 10.1128/mcb.6.12.4305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Golub T. R., Barker G. F., Bohlander S. K., Hiebert S. W., Ward D. C., Bray-Ward P., Morgan E., Raimondi S. C., Rowley J. D., Gilliland D. G. Fusion of the TEL gene on 12p13 to the AML1 gene on 21q22 in acute lymphoblastic leukemia. Proc Natl Acad Sci U S A. 1995 May 23;92(11):4917–4921. doi: 10.1073/pnas.92.11.4917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Golub T. R., Barker G. F., Lovett M., Gilliland D. G. Fusion of PDGF receptor beta to a novel ets-like gene, tel, in chronic myelomonocytic leukemia with t(5;12) chromosomal translocation. Cell. 1994 Apr 22;77(2):307–316. doi: 10.1016/0092-8674(94)90322-0. [DOI] [PubMed] [Google Scholar]
  20. Guz Y., Montminy M. R., Stein R., Leonard J., Gamer L. W., Wright C. V., Teitelman G. Expression of murine STF-1, a putative insulin gene transcription factor, in beta cells of pancreas, duodenal epithelium and pancreatic exocrine and endocrine progenitors during ontogeny. Development. 1995 Jan;121(1):11–18. doi: 10.1242/dev.121.1.11. [DOI] [PubMed] [Google Scholar]
  21. Hamazato F., Fujimura Y., Tamai Y., Takemoto Y., Matsushiro A., Nozaki M. Sequence specific binding of Ets-1 to the mouse cytokeratin EndoA gene enhancer. Biochem Biophys Res Commun. 1993 Apr 30;192(2):430–438. doi: 10.1006/bbrc.1993.1433. [DOI] [PubMed] [Google Scholar]
  22. Harrison S. D., Travers A. A. The tramtrack gene encodes a Drosophila finger protein that interacts with the ftz transcriptional regulatory region and shows a novel embryonic expression pattern. EMBO J. 1990 Jan;9(1):207–216. doi: 10.1002/j.1460-2075.1990.tb08097.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hennig G., Löwrick O., Birchmeier W., Behrens J. Mechanisms identified in the transcriptional control of epithelial gene expression. J Biol Chem. 1996 Jan 5;271(1):595–602. doi: 10.1074/jbc.271.1.595. [DOI] [PubMed] [Google Scholar]
  24. Ikeda K., Shaw-White J. R., Wert S. E., Whitsett J. A. Hepatocyte nuclear factor 3 activates transcription of thyroid transcription factor 1 in respiratory epithelial cells. Mol Cell Biol. 1996 Jul;16(7):3626–3636. doi: 10.1128/mcb.16.7.3626. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Janknecht R., Nordheim A. Gene regulation by Ets proteins. Biochim Biophys Acta. 1993 Dec 23;1155(3):346–356. doi: 10.1016/0304-419x(93)90014-4. [DOI] [PubMed] [Google Scholar]
  26. Jeon I. S., Davis J. N., Braun B. S., Sublett J. E., Roussel M. F., Denny C. T., Shapiro D. N. A variant Ewing's sarcoma translocation (7;22) fuses the EWS gene to the ETS gene ETV1. Oncogene. 1995 Mar 16;10(6):1229–1234. [PubMed] [Google Scholar]
  27. 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]
  28. Jousset C., Carron C., Boureux A., Quang C. T., Oury C., Dusanter-Fourt I., Charon M., Levin J., Bernard O., Ghysdael J. A domain of TEL conserved in a subset of ETS proteins defines a specific oligomerization interface essential to the mitogenic properties of the TEL-PDGFR beta oncoprotein. EMBO J. 1997 Jan 2;16(1):69–82. doi: 10.1093/emboj/16.1.69. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Klemsz M. J., McKercher S. R., Celada A., Van Beveren C., Maki R. A. The macrophage and B cell-specific transcription factor PU.1 is related to the ets oncogene. Cell. 1990 Apr 6;61(1):113–124. doi: 10.1016/0092-8674(90)90219-5. [DOI] [PubMed] [Google Scholar]
  30. Klämbt C. The Drosophila gene pointed encodes two ETS-like proteins which are involved in the development of the midline glial cells. Development. 1993 Jan;117(1):163–176. doi: 10.1242/dev.117.1.163. [DOI] [PubMed] [Google Scholar]
  31. Kodandapani R., Pio F., Ni C. Z., Piccialli G., Klemsz M., McKercher S., Maki R. A., Ely K. R. A new pattern for helix-turn-helix recognition revealed by the PU.1 ETS-domain-DNA complex. Nature. 1996 Apr 4;380(6573):456–460. doi: 10.1038/380456a0. [DOI] [PubMed] [Google Scholar]
  32. Koizumi S., Fisher R. J., Fujiwara S., Jorcyk C., Bhat N. K., Seth A., Papas T. S. Isoforms of the human ets-1 protein: generation by alternative splicing and differential phosphorylation. Oncogene. 1990 May;5(5):675–681. [PubMed] [Google Scholar]
  33. Kozak M. At least six nucleotides preceding the AUG initiator codon enhance translation in mammalian cells. J Mol Biol. 1987 Aug 20;196(4):947–950. doi: 10.1016/0022-2836(87)90418-9. [DOI] [PubMed] [Google Scholar]
  34. Kuenzel E. A., Mulligan J. A., Sommercorn J., Krebs E. G. Substrate specificity determinants for casein kinase II as deduced from studies with synthetic peptides. J Biol Chem. 1987 Jul 5;262(19):9136–9140. [PubMed] [Google Scholar]
  35. Lazzaro D., De Simone V., De Magistris L., Lehtonen E., Cortese R. LFB1 and LFB3 homeoproteins are sequentially expressed during kidney development. Development. 1992 Feb;114(2):469–479. doi: 10.1242/dev.114.2.469. [DOI] [PubMed] [Google Scholar]
  36. Lazzaro D., Price M., de Felice M., Di Lauro R. The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis and in restricted regions of the foetal brain. Development. 1991 Dec;113(4):1093–1104. doi: 10.1242/dev.113.4.1093. [DOI] [PubMed] [Google Scholar]
  37. Lee J. H., Jang S. I., Yang J. M., Markova N. G., Steinert P. M. The proximal promoter of the human transglutaminase 3 gene. Stratified squamous epithelial-specific expression in cultured cells is mediated by binding of Sp1 and ets transcription factors to a proximal promoter element. J Biol Chem. 1996 Feb 23;271(8):4561–4568. [PubMed] [Google Scholar]
  38. Libermann T. A., Baltimore D. Pi, a pre-B-cell-specific enhancer element in the immunoglobulin heavy-chain enhancer. Mol Cell Biol. 1993 Oct;13(10):5957–5969. doi: 10.1128/mcb.13.10.5957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Libermann T. A., Friesel R., Jaye M., Lyall R. M., Westermark B., Drohan W., Schmidt A., Maciag T., Schlessinger J. An angiogenic growth factor is expressed in human glioma cells. EMBO J. 1987 Jun;6(6):1627–1632. doi: 10.1002/j.1460-2075.1987.tb02410.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Lin A., Minden A., Martinetto H., Claret F. X., Lange-Carter C., Mercurio F., Johnson G. L., Karin M. Identification of a dual specificity kinase that activates the Jun kinases and p38-Mpk2. Science. 1995 Apr 14;268(5208):286–290. doi: 10.1126/science.7716521. [DOI] [PubMed] [Google Scholar]
  41. Lopez M., Oettgen P., Akbarali Y., Dendorfer U., Libermann T. A. ERP, a new member of the ets transcription factor/oncoprotein family: cloning, characterization, and differential expression during B-lymphocyte development. Mol Cell Biol. 1994 May;14(5):3292–3309. doi: 10.1128/mcb.14.5.3292. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Magnaldo T., Vidal R. G., Ohtsuki M., Freedberg I. M., Blumenberg M. On the role of AP2 in epithelial-specific gene expression. Gene Expr. 1993;3(3):307–315. [PMC free article] [PubMed] [Google Scholar]
  43. Maher J. F., Nathans D. Multivalent DNA-binding properties of the HMG-1 proteins. Proc Natl Acad Sci U S A. 1996 Jun 25;93(13):6716–6720. doi: 10.1073/pnas.93.13.6716. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Marin O., Meggio F., Draetta G., Pinna L. A. The consensus sequences for cdc2 kinase and for casein kinase-2 are mutually incompatible. A study with peptides derived from the beta-subunit of casein kinase-2. FEBS Lett. 1992 Apr 13;301(1):111–114. doi: 10.1016/0014-5793(92)80221-2. [DOI] [PubMed] [Google Scholar]
  45. McKercher S. R., Torbett B. E., Anderson K. L., Henkel G. W., Vestal D. J., Baribault H., Klemsz M., Feeney A. J., Wu G. E., Paige C. J. Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J. 1996 Oct 15;15(20):5647–5658. [PMC free article] [PubMed] [Google Scholar]
  46. McLean T. W., Ringold S., Neuberg D., Stegmaier K., Tantravahi R., Ritz J., Koeffler H. P., Takeuchi S., Janssen J. W., Seriu T. TEL/AML-1 dimerizes and is associated with a favorable outcome in childhood acute lymphoblastic leukemia. Blood. 1996 Dec 1;88(11):4252–4258. [PubMed] [Google Scholar]
  47. Meggio F., Marin O., Pinna L. A. Substrate specificity of protein kinase CK2. Cell Mol Biol Res. 1994;40(5-6):401–409. [PubMed] [Google Scholar]
  48. Missero C., Di Cunto F., Kiyokawa H., Koff A., Dotto G. P. The absence of p21Cip1/WAF1 alters keratinocyte growth and differentiation and promotes ras-tumor progression. Genes Dev. 1996 Dec 1;10(23):3065–3075. doi: 10.1101/gad.10.23.3065. [DOI] [PubMed] [Google Scholar]
  49. Morita T., Tondella M. L., Takemoto Y., Hashido K., Ichinose Y., Nozaki M., Matsushiro A. Nucleotide sequence of mouse EndoA cytokeratin cDNA reveals polypeptide characteristics of the type-II keratin subfamily. Gene. 1988 Aug 15;68(1):109–117. doi: 10.1016/0378-1119(88)90604-x. [DOI] [PubMed] [Google Scholar]
  50. Muthusamy N., Barton K., Leiden J. M. Defective activation and survival of T cells lacking the Ets-1 transcription factor. Nature. 1995 Oct 19;377(6550):639–642. doi: 10.1038/377639a0. [DOI] [PubMed] [Google Scholar]
  51. Mélet F., Motro B., Rossi D. J., Zhang L., Bernstein A. Generation of a novel Fli-1 protein by gene targeting leads to a defect in thymus development and a delay in Friend virus-induced erythroleukemia. Mol Cell Biol. 1996 Jun;16(6):2708–2718. doi: 10.1128/mcb.16.6.2708. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Oettgen P., Akbarali Y., Boltax J., Best J., Kunsch C., Libermann T. A. Characterization of NERF, a novel transcription factor related to the Ets factor ELF-1. Mol Cell Biol. 1996 Sep;16(9):5091–5106. doi: 10.1128/mcb.16.9.5091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Pahl H. L., Scheibe R. J., Zhang D. E., Chen H. M., Galson D. L., Maki R. A., Tenen D. G. The proto-oncogene PU.1 regulates expression of the myeloid-specific CD11b promoter. J Biol Chem. 1993 Mar 5;268(7):5014–5020. [PubMed] [Google Scholar]
  54. Panagopoulos I., Aman P., Fioretos T., Höglund M., Johansson B., Mandahl N., Heim S., Behrendtz M., Mitelman F. Fusion of the FUS gene with ERG in acute myeloid leukemia with t(16;21)(p11;q22). Genes Chromosomes Cancer. 1994 Dec;11(4):256–262. doi: 10.1002/gcc.2870110408. [DOI] [PubMed] [Google Scholar]
  55. Pankov R., Neznanov N., Umezawa A., Oshima R. G. AP-1, ETS, and transcriptional silencers regulate retinoic acid-dependent induction of keratin 18 in embryonic cells. Mol Cell Biol. 1994 Dec;14(12):7744–7757. doi: 10.1128/mcb.14.12.7744. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Pio F., Kodandapani R., Ni C. Z., Shepard W., Klemsz M., McKercher S. R., Maki R. A., Ely K. R. New insights on DNA recognition by ets proteins from the crystal structure of the PU.1 ETS domain-DNA complex. J Biol Chem. 1996 Sep 20;271(38):23329–23337. doi: 10.1074/jbc.271.38.23329. [DOI] [PubMed] [Google Scholar]
  57. Pio F., Ni C. Z., Mitchell R. S., Knight J., McKercher S., Klemsz M., Lombardo A., Maki R. A., Ely K. R. Co-crystallization of an ETS domain (PU.1) in complex with DNA. Engineering the length of both protein and oligonucleotide. J Biol Chem. 1995 Oct 13;270(41):24258–24263. doi: 10.1074/jbc.270.41.24258. [DOI] [PubMed] [Google Scholar]
  58. Prasad D. D., Rao V. N., Lee L., Reddy E. S. Differentially spliced erg-3 product functions as a transcriptional activator. Oncogene. 1994 Feb;9(2):669–673. [PubMed] [Google Scholar]
  59. Prowse D. M., Bolgan L., Molnár A., Dotto G. P. Involvement of the Sp3 transcription factor in induction of p21Cip1/WAF1 in keratinocyte differentiation. J Biol Chem. 1997 Jan 10;272(2):1308–1314. doi: 10.1074/jbc.272.2.1308. [DOI] [PubMed] [Google Scholar]
  60. Rao V. N., Ohno T., Prasad D. D., Bhattacharya G., Reddy E. S. Analysis of the DNA-binding and transcriptional activation functions of human Fli-1 protein. Oncogene. 1993 Aug;8(8):2167–2173. [PubMed] [Google Scholar]
  61. Ray D., Bosselut R., Ghysdael J., Mattei M. G., Tavitian A., Moreau-Gachelin F. Characterization of Spi-B, a transcription factor related to the putative oncoprotein Spi-1/PU.1. Mol Cell Biol. 1992 Oct;12(10):4297–4304. doi: 10.1128/mcb.12.10.4297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Reeves R., Nissen M. S. The A.T-DNA-binding domain of mammalian high mobility group I chromosomal proteins. A novel peptide motif for recognizing DNA structure. J Biol Chem. 1990 May 25;265(15):8573–8582. [PubMed] [Google Scholar]
  63. Rheinwald J. G., Beckett M. A. Tumorigenic keratinocyte lines requiring anchorage and fibroblast support cultured from human squamous cell carcinomas. Cancer Res. 1981 May;41(5):1657–1663. [PubMed] [Google Scholar]
  64. Rivera R. R., Stuiver M. H., Steenbergen R., Murre C. Ets proteins: new factors that regulate immunoglobulin heavy-chain gene expression. Mol Cell Biol. 1993 Nov;13(11):7163–7169. doi: 10.1128/mcb.13.11.7163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Savant-Bhonsale S., Cleveland D. W. Evidence for instability of mRNAs containing AUUUA motifs mediated through translation-dependent assembly of a > 20S degradation complex. Genes Dev. 1992 Oct;6(10):1927–1939. doi: 10.1101/gad.6.10.1927. [DOI] [PubMed] [Google Scholar]
  66. Schallreuter K. U., Lemke K. R., Pittelkow M. R., Wood J. M., Körner C., Malik R. Catecholamines in human keratinocyte differentiation. J Invest Dermatol. 1995 Jun;104(6):953–957. doi: 10.1111/1523-1747.ep12606218. [DOI] [PubMed] [Google Scholar]
  67. Schlegel R., Phelps W. C., Zhang Y. L., Barbosa M. Quantitative keratinocyte assay detects two biological activities of human papillomavirus DNA and identifies viral types associated with cervical carcinoma. EMBO J. 1988 Oct;7(10):3181–3187. doi: 10.1002/j.1460-2075.1988.tb03185.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Scott E. W., Simon M. C., Anastasi J., Singh H. Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science. 1994 Sep 9;265(5178):1573–1577. doi: 10.1126/science.8079170. [DOI] [PubMed] [Google Scholar]
  69. Seth A., Papas T. S. The c-ets-1 proto-oncogene has oncogenic activity and is positively autoregulated. Oncogene. 1990 Dec;5(12):1761–1767. [PubMed] [Google Scholar]
  70. Seth A., Robinson L., Panayiotakis A., Thompson D. M., Hodge D. R., Zhang X. K., Watson D. K., Ozato K., Papas T. S. The EndoA enhancer contains multiple ETS binding site repeats and is regulated by ETS proteins. Oncogene. 1994 Feb;9(2):469–477. [PubMed] [Google Scholar]
  71. Sherman L., Schlegel R. Serum- and calcium-induced differentiation of human keratinocytes is inhibited by the E6 oncoprotein of human papillomavirus type 16. J Virol. 1996 May;70(5):3269–3279. doi: 10.1128/jvi.70.5.3269-3279.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Shore P., Whitmarsh A. J., Bhaskaran R., Davis R. J., Waltho J. P., Sharrocks A. D. Determinants of DNA-binding specificity of ETS-domain transcription factors. Mol Cell Biol. 1996 Jul;16(7):3338–3349. doi: 10.1128/mcb.16.7.3338. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Siddique H. R., Rao V. N., Lee L., Reddy E. S. Characterization of the DNA binding and transcriptional activation domains of the erg protein. Oncogene. 1993 Jul;8(7):1751–1755. [PubMed] [Google Scholar]
  74. Singer G. G., Yokoyama H., Bloom R. D., Jevnikar A. M., Nabavi N., Kelley V. R. Stimulated renal tubular epithelial cells induce anergy in CD4+ T cells. Kidney Int. 1993 Nov;44(5):1030–1035. doi: 10.1038/ki.1993.345. [DOI] [PubMed] [Google Scholar]
  75. Songyang Z., Blechner S., Hoagland N., Hoekstra M. F., Piwnica-Worms H., Cantley L. C. Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr Biol. 1994 Nov 1;4(11):973–982. doi: 10.1016/s0960-9822(00)00221-9. [DOI] [PubMed] [Google Scholar]
  76. Suh E., Chen L., Taylor J., Traber P. G. A homeodomain protein related to caudal regulates intestine-specific gene transcription. Mol Cell Biol. 1994 Nov;14(11):7340–7351. doi: 10.1128/mcb.14.11.7340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Tkachuk D. C., Kohler S., Cleary M. L. Involvement of a homolog of Drosophila trithorax by 11q23 chromosomal translocations in acute leukemias. Cell. 1992 Nov 13;71(4):691–700. doi: 10.1016/0092-8674(92)90602-9. [DOI] [PubMed] [Google Scholar]
  78. Wasylyk B., Hahn S. L., Giovane A. The Ets family of transcription factors. Eur J Biochem. 1993 Jan 15;211(1-2):7–18. doi: 10.1007/978-3-642-78757-7_2. [DOI] [PubMed] [Google Scholar]
  79. Wilke M. S., Hsu B. M., Wille J. J., Jr, Pittelkow M. R., Scott R. E. Biologic mechanisms for the regulation of normal human keratinocyte proliferation and differentiation. Am J Pathol. 1988 Apr;131(1):171–181. [PMC free article] [PubMed] [Google Scholar]
  80. Yukawa K., Butz K., Yasui T., Kikutani H., Hoppe-Seyler F. Regulation of human papillomavirus transcription by the differentiation-dependent epithelial factor Epoc-1/skn-1a. J Virol. 1996 Jan;70(1):10–16. doi: 10.1128/jvi.70.1.10-16.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Zeleznik-Le N. J., Harden A. M., Rowley J. D. 11q23 translocations split the "AT-hook" cruciform DNA-binding region and the transcriptional repression domain from the activation domain of the mixed-lineage leukemia (MLL) gene. Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10610–10614. doi: 10.1073/pnas.91.22.10610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Zucman J., Melot T., Desmaze C., Ghysdael J., Plougastel B., Peter M., Zucker J. M., Triche T. J., Sheer D., Turc-Carel C. Combinatorial generation of variable fusion proteins in the Ewing family of tumours. EMBO J. 1993 Dec;12(12):4481–4487. doi: 10.1002/j.1460-2075.1993.tb06137.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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