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

Molecular and Cellular Biology

Volumn 17, Issue 8, 1997, Pages 4419-4433

  Oettgen, Peter ^a   Alani, Rhoda M ^a   Barcinski, Marcello A ^b   Brown, Lawrence ^a   Akbarali, Yasmin ^a   Boltax, Jay ^a   Kunsch, Charles ^c   Munger, Karl ^a   Libermann, Towia A ^a,d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c GLAXOSMITHKLINE   (United States)

^d BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ESE 1; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DNA BINDING; EPITHELIUM CELL; FETUS; GENE ISOLATION; HUMAN; HUMAN CELL; KERATINOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN ISOLATION; REGULATOR GENE; TRANSCRIPTION REGULATION;

EID: 0030839767     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.8.4419     Document Type: Article

References (85)

1. Abe, M., and R. G. Oshima. 1990. A single human keratin 18 gene is expressed in diverse epithelial cells of transgenic mice. J. Cell Biol. 111:1197-1206.
2. Akbarali, Y., P. Oettgen, and T. A. Libermann. 1997. Unpublished data.
3. Ashar, H. R., M. S. Fejzo, A. Tkachenko, X. Zhou, J. A. Fletcher, S. Weremowicz, C. C. Morton, and K. Chada. 1995. Disruption of the architectural factor HMGI-C: DNA-binding AT hook motifs fused in lipomas to distinct transcriptional regulatory domains. Cell 82:57-65.
4. Beaudette, K. N., J. Lew, and J. H. Wang. 1993. Substrate specificity characterization of a cdc2-like protein kinase purified from bovine brain. J. Biol. Chem. 268:20825-20830.
5. Borles, J. C., D. M. Willerford, D. Grevin, L. Davidson, A. Camus, P. Martin, D. Stehelin, and F. W. Alt. 1995. Increased T-cell apoptosis and terminal B-cell differentiation induced by inactivation of the Ets-1 proto-oncogene. Nature 377:635-638.
6. Broeker, P. L., A. Harden, J. D. Rowley, and L. N. Zeleznik. 1996. 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. 211:259-268.
7. Cheng, C., A. E. Kilkenny, D. Roop, and S. H. Yuspa. 1990. The v-ras oncogene inhibits the expression of differentiation markers and facilitates expression of cytokeratins 8 and 18 in mouse keratinocytes. Mol. Carcinog. 3:363-373.
8. Cheng, C., T. Tennenbaum, P. J. Dempsey R. J. Coffey, S. H. Yuspa, and A. A. Dlugosz. 1993. 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. 4:317-327.
9. Chirgwin, J. M., A. E. Przybyla, R. J. MacDonald, and W. J. Rutter. 1979. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18:5294-5299.
10. Delattre, O., J. Zucman, B. Plougastel, C. Desmaze, T. Melot, M. Peter, H. Kovar, I. Joubert, J. P. de Dong, G. Rouleau, et al. 1992. Gene fusion with an ETS DNA-binding domain caused by chromosome translocation in human tumours. Nature 359:162-165.
11. Dlugosz, A. A., C. Cheng, M. F. Denning, P. J. Dempsey, R. J. Coffey, and S. H. Yuspa. 1994. 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. 5:1283-1292.
12. Farr, A., and A. Roman. 1992. A pitfall of using a second plasmid to determine transfection efficiency. Nucleic Acids Res. 20:920.
13. Faus, I., H. J. Hsu, and E. Fuchs. 1994. Oct-6: a regulator of keratinocyte gene expression in stratified squamous epithelia. Mol. Cell. Biol. 14:3263-3275.
14. Ffrench, C. C., L. Van de Water, H. F. Dvorak, and R. O. Hynes. 1989. Reappearance of an embryonic pattern of fibronectin splicing during wound healing in the adult rat. J. Cell Biol. 109:903-914.
15. Fischer, D. F., S. Gibbs, P. van de Putte, and C. Backendorf. 1996. Interdependent transcription control elements regulate the expression of the SPRR2A gene during keratinocyte terminal differentiation. Mol. Cell. Biol. 16:5365-5374.
16. Fitzsimmons, D., W. Hodsdon, W. Wheat, S.-M. Maira, B. Wasylyk, and J. Hagman. 1996. Pax-5 (BSAP) recruits Ets proto-oncogene family proteins to form functional ternary complexes on a B cell-specific promoter. Genes Dev. 10:2198-2211.
17. Fujimura, Y., H. Yamamoto, F. Hamazato, and M. Nozaki. 1994. 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. 22: 613-618.
18. Gilman, M. Z., R. N. Wilson, and R. A. Weinberg. 1986. Multiple protein-binding sites in the 5′-flanking region regulate c-fos expression. Mol. Cell. Biol. 6:4305-4316.
19. Golub, T. R., G. F. Barker, S. K. Bohlander, S. W. Hiebert, D. C. Ward, W. P. Bray, E. Morgan, S. C. Raimondi, J. D. Rowley, and D. G. Gilliland. 1995. Fusion of the TEL gene on 12p13 to the AML1 gene on 21q22 in acute lymphoblastic leukemia. Proc. Natl. Acad. Sci. USA 92:4917-4921.
20. Golub, T. R., G. F. Barker, M. Lovett, and D. G. Gilliland. 1994. Fusion of PDGF receptor beta to a novel ets-like gene, tel, in chronic myelomonocytic leukemia with t(5;12) chromosomal translocation. Cell 77:307-316.
21. Guz., Y., M. R. Montminy, R. Stein, J. Leonard, L. W. Gamer, C. V. Wright, and G. Teitelman. 1995. 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 121:11-18.
22. Hamazato, F., Y. Fujimura, Y. Tamai, Y. Takemoto, A. Matsushiro, and M. Nozaki. 1993. Sequence specific binding of Ets-1 to the mouse cytokeratin EndoA gene enhancer. Biochem. Biophys. Res. Commun. 192:430-438.
23. Harrison, S. D., and A. A. Travers. 1990. 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. 9:207-216.
24. Hennig, G., O. Lowrick, W. Birchmeier, and J. Behrens. 1996. Mechanisms identified in the transcriptional control of epithelial gene expression. J. Biol. Chem. 271:595-602.
25. Ikeda, K., W. J. Shaw, S. E. Wert, and J. A. Whitsett. 1996. Hepatocyte nuclear factor 3 activates transcription of thyroid transcription factor 1 in respiratory epithelial cells. Mol. Cell. Biol. 16:3626-3636.
26. Janknecht, R., and A. Nordheim. 1993. Gene regulation by Ets proteins. Biochim Biophys. Acta 1155:346-356.
27. Jeon, I. S., J. N. Davis, B. S. Braun, J. E. Sublett, M. F. Roussel, C. T. Denny, and D. N. Shapiro. 1995. A variant Ewing's sarcoma translocation (7;22) fuses the EWS gene to the ETS gene ETV1. Oncogene 10:1229-1234.
28. John, S., R. B. Reeves, J. X. Lin, R. Child, J. M. Leiden, C. B. Thompson, and W. J. Leonard. 1995. Regulation of cell-type-specific interleukin-2 receptor alpha-chain gene expression: potential role of physical interactions between Elf-1, HMG-1(Y), and NF-kappa B family proteins. Mol. Cell. Biol. 15:1786-1796.
29. Jousset, C., C. Carron, A. Boureux, C. T. Quang, C. Oury, F. I. Dusanter, M. Charon, J. Levin, O. Bernard, and J. Ghysdael. 1997. 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 oncoprolein. EMBO J. 16:69-82.
30. Klambt, C. 1993. The Drosophila gene pointed encodes two ETS-like proteins which are involved in the development of the midline glial cells. Development 117:163-176.
31. Klemsz, M. J., S. R. McKercher, A. Celada, C. Van Beveren, and R. A. Maki. 1990. The macrophage and B cell-specific transcription factor PU.1 is related to the ets oncogene. Cell 61:113-124.
32. Kodandapani, R., F. Pio, C. Z. Ni, G. Piccialli, M. Klemsz, S. McKercher, R. A. Maki, and K. R. Ely. 1996. A new pattern for helix-turn-helix recognition revealed by the PU.1 ETS-domain-DNA complex. Nature 380:456-460.
33. Koizumi, S., R. J. Fisher, S. Fujiwara, C. Jorcyk, N. K. Bhat, A. Seth, and T. S. Papas. 1990. Isoforms of the human ets-1 protein: generation by alternative splicing and differential phosphorylation. Oncogene 5:675-681.
34. Kozak, M. 1987. At least six nucleotides preceding the AUG initiator codon enhance translation in mammalian cells, J. Mol. Biol. 196:947-950.
35. Kuenzel, E. A., J. A. Mulligan, J. Sommercorn, and E. G. Krebs. 1987. Substrate specificity determinants for casein kinase II as deduced from studies with synthetic peptides. J. Biol. Chem. 262:9136-9140.
36. Lazzaro, D., V. De Simone, L, De Magistris, E. Lehtonen, and R. Cortese. 1992. LFB1 and LFB3 homeoproteins are sequentially expressed during kidney development. Development 114:469-479.
37. Lazzaro, D., M. Price, M. de Felice, and R. Di Lauro. 1991. The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis and in restricted regions of the foetal brain. Development 113:1093-1104.
38. Lee, J. H., S. I. Jang, J. M. Yang, N. G. Markova, and P. M. Steinert. 1996. 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. 271:4561-4568.
39. Libermann, T. A., R. Friesel, M. Jaye, R. M. Lyall, B. Westermark, W. Drohan, A. Schmidt, T. Maciag, and J. Schlessinger. 1987. An angiogenic growth factor is expressed in human glioma cells. EMBO J. 6:1627-1632.
40. Libermann, T. A., and D. Baltimore. 1993. Pi, a pre-B-cell-specific enhancer element in the immunoglobulin heavy-chain enhancer. Mol. Cell. Biol. 13: 5957-5969.
41. Lin, A., A. Minden, H. Martinetto, F. X. Claret, C. C. Lange, F. Mercurio, G. L. Johnson, and M. Karin. 1995. Identification of a dual specificity kinase that activates the Jun kinases and p38-Mpk2. Science 268:286-290.
42. Lopez, M., P. Oettgen, Y. Akbarali, U. Dendorfer, and T. A. Libermann. 1994. ERP, a new member of the ets transcription factor/oncoprotein family: cloning, characterization, and differential expression during B-lymphocyte development. Mol. Cell. Biol. 14:3292-3309.
43. Magnaldo, T., R. G. Vidal, M. Ohtsuki, I. M. Freedberg, and M. Blumenberg. 1993. On the role of AP2 in epithelial-specific gene expression. Gene Exp. 3:307-315.
44. Maher, J. F., and D. Nathans. 1996. Multivalent DNA-binding properties of the HMG-1 proteins. Proc. Natl. Acad. Sci. USA 93:6716-6720.
45. Marin, O., F. Meggio, G. Draetta, and L. A. Pinna. 1992. 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. 301:111-114.
46. McKercher, S. R.., B. E. Torbett, K. L. Anderson, G. W. Henkel, D. J. Vestal, H. Baribault, M. Klemsz, A. J. Feeney, G. E. Wu, C. J. Paige, and R. A. Maki. 1996. Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J. 15:5647-5658.
47. McLean, T. W., S. Ringold, D. Neuberg, K. Stegmaier, R. Tantravahi, J. Ritz, H. P. Koeffler, S. Takeuchi, J. W. G. Janssen, T. Seriu, C. R. Bartram, S. E. Sallan, D. G. Gilliland, and T. R. Golub. 1996. Tel/AML-1 dimerizes and is associated with a favorable outcome in childhood acute lymphoblastic leukemia. Blood 88:4252-4258.
48. Meggio, F., O. Marin, and L. A. Pinna. 1994. Substrate specificity of protein kinase CK2. Cell. Mol. Biol. Res. 40:401-409.
49. Melet, F., B. Motro, D. J. Rossi, L. Zhang, and A. Bernstein. 1996. Generation of a novel Fli-1 protein by gene targeting leads to a defect in thymus development and a delay in Friend virus-induced crythroleukemia. Mol. Cell. Biol. 16:2708-2718.
50. Missero, C., F. Di Cunto, H. Kiyokawa, A. Koff, and G. P. Dotto. 1990 The absence of p21Cip1/WAF1 alters keratinocyte growth and differentiation and promotes ras-tumor progression. Genes Dev. 10:3065-3075.
51. Morita, T., M. L. Tondella, Y. Takemoto, K. Hashido, Y. Ichinose, M. Nozaki, and A. Matsushiro. 1988. Nucleotide sequence of mouse EndoA cytokeratin cDNA reveals polypeptide characteristics of the type-II keratin subfamily. Gene 68:109-117.
52. Muthusamy, N., K. Barton, and J. M. Leiden. 1995. Defective activation and survival of Tcells lacking the Ets-1 transcription factor. Nature 377:639-642.
53. Oettgen, J. P., Y. Akbarali, M. Barcinski, J. Boltax, and T. A. Libermann. 1997. Unpublished data.
54. Oettgen, P., Y. Akbarali, J. Boltax, J. Best, C. Kunsch, and T. A. Libermann. 1996. Characterization of NERF, a novel transcription factor related to the Ets factor ELF-1. Mol. Cell. Biol. 16:5091-5106.
55. Oettgen, P., L. Brown, R. M. Aiani, M. A. Barcinski, K. C. Carter, M. Augustus, J. Boltax, C. Kunsch, K. Munger, and T. A. Libermann. Aberrant expression of a novel epithelial-specific Ets transcription factor, ESE-1, in human cancers. Submitted for publication.
56. Pahl, H. L., R. J. Scheibe, D. E. Zhang, H. M. Chen, D. L. Galson, R. A. Maki, and D. G. Tenen. 1993. The proto-oncogene PU.1 regulates expression of the myeloid-specific CD11b promoter. J. Biol. Chem. 268:5014-5020.
57. Panagopoulos, I, P. Aman, T. Fioretos, M. Hoglund, B. Johansson, N. Mandahl, S. Heim, M. Behrendtz, and F. Mitelman. 1994. Fusion of the FUS gene with ERG in acute myeloid leukemia with t(16;21)(p11;q22). Genes Chromosome Cancer 11:256-262.
58. Pankov, R., N. Neznanov, A. Umezawa, and R. G. Oshima. 1994. AP-1, ETS, and transcriptional silencers regulate retinoic acid-dependent induction of keratin 18 in embryonic cells. Mol. Cell. Biol. 14:7744-7757.
59. Pio, F., R. Kodandapani, C.-Z. Ni, W. Shepard, M. Klemsz, S. R. McKercher, R. A. Maki, and K. R. Ely. 1996. New insight on DNA recognition by ets proteins from the crystal structure of the PU.1 ETS domain-DNA complex. J. Biol. Chem. 271:23329-23337.
60. Pio, F., C. Z. Ni, R. S. Mitchell, J. Knight, S. McKercher, M. Klemsz, A. Lombardo, R. A. Maki, and K. R. Ely. 1995. Co-crystallization of an ETS domain (PU.1) in complex with DNA. Engineering the length of both protein and oligonucleotide. J. Biol. Chem. 270:24258-24263.
61. Prasad, D. D., V. N. Rao, L. Lee, and E. S. Reddy. 1994. Differentially spliced ere-3 product functions as a transcriptional activator. Oncogene 9:669-673.
62. Prowse, D. M., L. Bolgan, A. Molnar, and G. P. Dotto. 1997. Involvement of the Sp3 transcription factor in induction of p21Cip1/WAF1 in keratinocyte differentiation. J. Biol. Chem. 272:1308-1314.
63. Rao, V. N., T. Ohno, D. D. Prasad, G. Bhattacharya, and E. S. Reddy. 1993. Analysis of the DNA-binding and transcriptional activation functions of human Fli-1 protein. Oncogene 8:2167-2173.
64. Ray, D., R. Bosselut, J. Ghysdael, M. G. Mattei, A. Tavitian, and G. F. Moreau. 1992. Characterization of Spi-B, a transcription factor related to the putative oncoprotein Spi-1/PU.1. Mol. Cell. Biol. 12:4297-4304.
65. Reeves, R., and M. S. Nissen. 1990. 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. 265:8573-8582.
66. Rheinwald, J. G., and M. A. Beckett. 1981. Tumorigenic keratinocyte lines requiring anchorage and fibroblast support cultures from human squamous cell carcinomas. Cancer Res. 41:1657-1663.
67. Rivera, R. R., M. H. Stuiver, R. Steenbergen, and C. Murre. 1993. Ets proteins: new factors that regulate immunoglobulin heavy-chain gene expression. Mol. Cell. Biol. 13:7163-7169.
68. Savant, B. S., and D. W. Cleveland. 1992. Evidence for instability of mRNAs containing AUUUA motifs mediated through translation-dependent assembly of a > 20S degradation complex. Genes Dev. 6:1927-39.
69. Schallreuter, K. U., K. R. Lemke, M. R. Pittelkow, J. M. Wood, C. Korner, and R. Malik. 1995. Catecholamines in human keratinocyte differentiation. J. Invest. Dermatol. 104:953-957.
70. Schlegel, R., W. C. Phelps, Y. L. Zhang, and M. Barbosa. 1988. Quantitative keratinocyte assay detects two biological activities of human papillomavirus DNA and identifies viral types associated with cervical carcinoma. EMBO J. 7:3181-3187.
71. Scott, E. W., M. C. Simon, J. Anastasi, and H. Singh. 1994. Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science 265:1573-1577.
72. Seth, A., and T. S. Papas. 1990. The c-ets-1 proto-oncogene has oncogenic activity and is positively autoregulated. Oncogene 5:1761-1767.
73. Seth, A., L. Robinson, A. Panayiotakis, D. M. Thompson, D. R. Hodge, X. K. Zhang, D. K. Watson, K. Ozato, and T. S. Papas. 1994 The EndoA enhancer contains multiple ETS binding site repeats and is regulated by ETS proteins. Oncogene 9:469-477.
74. Sherman, L., and R. Schlegel. 1996. Serum- and calcium-induced differentiation of human keratinocytes is inhibited by the E6 oncoprotein of human papillomavirus type 16. J. Virol. 70:3269-3279.
75. Shore, P., A. J. Whitmarsh, R. Bhaskaran, R. J. Davis, J. P. Waltho, and A. D. Sharrocks. 1996. Determinants of DNA-binding specificity of ETS-domain transcription factors. Mol. Cell. Biol. 16:3338-3349.
76. Siddique, H. R., V. N. Rao, L. Lee, and E. S. Reddy. 1993. Characterization of the DNA binding and transcriptional activation domains of the erg protein. Oncogene 8:1751-1755.
77. Singer, G. G., H. Yokoyama, R. D. Bloom, A. M. Jevnikar, N. Nabavi, and V. R. Kelley. 1993. Stimulated renal tubular epithelial cells induce anergy in CD4+ T cells. Kidney Int. 44:1030-1035.
78. Songyang, Z., S. Blechner, N. Hoagland, M. F. Hoekstra, W. H. Piwnica, and L. C. Cantley. 1994. Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr. Biol. 4:973-982.
79. Suh, E., L. Chen, J. Taylor, and P. G. Traber. 1994. A homeodomain protein related to caudal regulates intestine-specific gene transcription. Mol. Cell. Biol. 14:7340-7351.
80. Tkachuk, D. C., S. Kohler, and M. L. Cleary. 1992. Involvement of a homolog of Drosophila trithorax by 11q23 chromosomal translocations in acute leukemias. Cell 71:691-700.
81. Wasylyk, B., S. L. Hahn, and A. Giovane. 1993. The Ets family of transcription factors. Eur. J. Biochem. 211:7-18.
82. Wilke, M. S., B. M. Hsu, J. J. Wille, M. R. Pittelkow, and R. E. Scott. 1988. Biologic mechanisms for the regulation of normal human keratinocyte proliferation and differentiation. Am. J. Pathol. 131:171-181.
83. Yukawa, K., K. Butz, T. Yasui, H. Kikutani, and S. F. Hoppe. 1996. Regulation of human papillomavirus transcription by the differentiation-dependent epithelial factor Epoc-1/skn-1a. J. Virol. 70:10-16.
84. Zeleznik, L. N., A. M. Harden, and J. D. Rowley. 1994. 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. USA 91:10610-10614.
85. Zucman, J., T. Melot, C. Desmaze, J. Ghysdael, B. Plougastel, M. Peter, J. M. Zucker, T. J. Triche, D. Sheer, C. C. Turc, et al. 1993. Combinatorial generation of variable fusion proteins in the Ewing family of tumours. EMBO J. 12:4481-4487.