The ETS transcription factor ESE-1 transforms MCF-12A human mammary epithelial cells via a novel cytoplasmic mechanism

Molecular and Cellular Biology

Volumn 24, Issue 12, 2004, Pages 5548-5564

  Prescott, Jason D ^a   Koto, Karen S N ^b   Singh, Meenakshi ^a   Gutierrez Hartmann, Arthur ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b OBERLIN COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; ESTROGEN RECEPTOR; GREEN FLUORESCENT PROTEIN; PROGESTERONE RECEPTOR; SERINE; TRANSCRIPTION FACTOR ESE 1; TRANSCRIPTION FACTOR ETS 1; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CELL TRANSFORMATION; CYTOPLASM; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MUTATION; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; APOPTOSIS; BREAST; BREAST NEOPLASMS; CELL ADHESION; CELL DIVISION; CELL LINE; CELL LINE, TUMOR; CELL NUCLEUS; CELL TRANSFORMATION, NEOPLASTIC; CYTOPLASM; DNA-BINDING PROTEINS; EPITHELIAL CELLS; FEMALE; GREEN FLUORESCENT PROTEINS; HUMANS; LUMINESCENT PROTEINS; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS; RECOMBINANT FUSION PROTEINS; TRANSCRIPTION FACTORS; TRANSFECTION;

MINK CELL FOCUS-FORMING VIRUS; SIMIAE; SIMIAN VIRUS 40;

EID: 2942594555     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.12.5548-5564.2004     Document Type: Article

References (55)

1. Andreoli, J. M., S. I. Jang, E. Chung, C. M. Coticchia, P. M. Steinert, and N. G. Markova. 1997. The expression of a novel, epithelium-specific ets transcription factor is restricted to the most differentiated layers in the epidermis. Nucleic Acids Res. 25:4287-4295.
2. Asada, S., Y. Choi, and M. Uesugi. 2003. A gene-expression inhibitor that targets an alpha-helix-mediated protein interaction. J. Am. Chem. Soc. 125:4992-4993.
3. Asada, S., Y. Choi, M. Yamada, S. C. Wang, M. C. Hung, J. Qin, and M. Uesugi. 2002. External control of Her2 expression and cancer cell growth by targeting a Ras-linked coactivator. Proc. Natl. Acad. Sci. USA 99:12747-12752.
4. Boulukos, K. E., P. Pognonec, B. Rabault, A. Begue, and J. Ghysdael. 1989. Definition of an Etsl protein domain required for nuclear localization in cells and DNA-binding activity in vitro. Mol. Cell. Biol. 9:5718-5721.
5. Cabral, A., D. F. Fischer, W. P. Vermeij, and C. Backendorf. 2003. Distinct functional interactions of human Skn-1 isoforms with Ese-1 during keratinocyte terminal differentiation. J. Biol. Chem. 278:17792-17799.
6. Chang, C. H., G. K. Scott, M. A. Baldwin, and C. C. Benz. 1999. Exon 4-encoded acidic domain in the epithelium-restricted Ets factor, ESX, confers potent transactivating capacity and binds to TATA-binding protein (TBP). Oncogene 18:3682-3695.
7. Chang, C. H., G. K. Scott, W. L. Kuo, X. Xiong, Y. Suzdaltseva, J. W. Park, P. Sayre, K. Erny, C. Collins, J. W. Gray, and C. C. Benz. 1997. ESX: a structurally unique Ets overexpressed early during human breast tumorigenesis. Oncogene 14:1617-1622.
8. Chiang, S. Y., R. W. Burli, C. C. Benz, L. Gawron, G. K. Scott, P. B. Dervan, and T. A. Beerman. 2000. Targeting the ets binding site of the HER2/neu promoter with pyrrole-imidazole polyamides. J. Biol. Chem. 275:24246-24254.
9. Choi, S. G., Y. Yi, Y. S. Kim, M. Kato, J. Chang, H. W. Chung, K. B. Hahm, H. K. Yang, H. H. Rhee, Y. J. Bang, and S. J. Kim. 1998. A novel ets-related transcription factor, ERT/ESX/ESE-1, regulates expression of the transforming growth factor-beta type II receptor. J. Biol. Chem. 273:110-117.
10. Choi, Y., S. Asada, and M. Uesugi. 2000. Divergent hTAFII31-binding motifs hidden in activation domains. J. Biol. Chem. 275:15912-15916.
11. Cifone, M. A. 1982. In vitro growth characteristics associated with benign and metastatic variants of tumor cells. Cancer Metastasis Rev. 1:335-347.
12. Cohen, B. D., C. B. Siegall, S. Bacus, L. Foy, J. M. Green, I. Hellstrom, K. E. Hellstrom, and H. P. Fell. 1998. Role of epidermal growth factor receptor family members in growth and differentiation of breast carcinoma. Biochem. Soc. Symp. 63:199-210.
13. De Haro, L., and R. Janknecht. 2002. Functional analysis of the transcription factor ER71 and its activation of the matrix metalloproteinase-1 promoter. Nucleic Acids Res. 30:2972-2979.
14. Delannoy-Courdent, A., V. Mattot, V. Fafeur, W. Fauquette, I. Pollet, T. Calmels, C. Vercamer, B. Boilly, B. Vandenbunder, and X. Desbiens. 1998. The expression of an Ets1 transcription factor lacking its activation domain decreases uPA proteolytic activity and cell motility, and impairs normal tubulogenesis and cancerous scattering in mammary epithelial cells. J. Cell Sci. 111:1521-1534.
15. Delattre, O., J. Zucman, B. Plougastel, C. Desmaze, T. Melot, M. Peter, H. Kovar, I. Joubert, P. de Jong, G. Rouleau, et al. 1992. Gene fusion with an ETS DNA-binding domain caused by chromosome translocation in human tumours. Nature 359:162-165.
16. de Martin, R., J. A. Schmid, and R. Hofer-Warbinek. 1999. The NF-kappaB/Re1 family of transcription factors in oncogenic transformation and apoptosis. Mutat. Res. 437:231-243,
17. Ducret, C., S. M. Maira, A. Dierich, and B. Wasylyk. 1999. The net repressor is regulated by nuclear export in response to anisomycin, UV, and heat shock. Mol. Cell. Biol. 19:7076-7087.
18. Eckel, K. L., J. J. Tentler, G. J. Cappetta, S. E. Diamond, and A. Gutierrez-Hartmann. 2003. The epithelial-specific ETS transcription factor ESX/ESE-1/Elf-3 modulates breast cancer-associated gene expression. DNA Cell Biol. 22:79-94.
19. Feldman, R. J., V. I. Sementchenko, and D. K. Watson. 2003. The epithelial-specific Ets factors occupy a unique position in defining epithelial proliferation, differentiation and carcinogenesis. Anticancer Res. 23:2125-2131.
20. Fukuda, M., I. Gotoh, Y. Gotoh, and E. Nishida. 1996. Cytoplasmic localization of mitogen-activated protein kinase kinase directed by its NH2-terminal, leucine-rich short amino acid sequence, which acts as a nuclear export signal. J. Biol. Chem. 271:20024-20028.
21. Grall, F., X. Gu, L. Tan, J. Y. Cho, M. S. Inan, A. R. Pettit, U. Thamrongsak, B. K. Choy, C. Manning, Y. Akbarali, L. Zerbini, S. Rudders, S. R. Goldring, E. M. Gravallese, P. Oettgen, M. B. Goldring, and T. A. Libermann. 2003. Responses to the proinflammatory cytokines interleukin-1 and tumor necrosis factor alpha in cells derived from rheumatoid synovium and other joint tissues involve nuclear factor kappaB-mediated induction of the Ets transcription factor ESE-1. Arthritis Rheum. 48:1249-1260.
22. Janknecht, R., R. Zinck, W. H. Ernst, and A. Nordheim. 1994. Functional dissection of the transcription factor Elk-1. Oncogene 9:1273-1278.
23. Jobling, A. I., Z. Fang, D. Koleski, and M. J. Tymms. 2002. Expression of the ETS transcription factor ELF3 in the retinal pigment epithelium. Investig. Ophthalmol. Vis. Sci. 43:3530-3537.
24. Kapuscinski, J. 1995. DAPI: a DNA-specific fluorescent probe. Biotechnol. Histochem. 70:220-233.
25. Kas, K., E. Finger, F. Grall, X. Gu, Y. Akbarali, J. Boltax, A. Weiss, P. Oettgen, R. Kapeller, and T. A. Libermann. 2000. ESE-3, a novel member of an epithelium-specific ets transcription factor subfamily, demonstrates different target gene specificity from ESE-1. J. Biol. Chem. 275:2986-2998.
26. Le Gallic, L., D. Sgouras, G. Beal, Jr., and G. Mavrothalassitis. 1999. Transcriptional repressor ERF is a Ras/mitogen-activated protein kinase target that regulates cellular proliferation. Mol. Cell. Biol. 19:4121-4133.
27. Leprince, D., A. Gegonne, J. Coll, C. de Taisne, A. Schneeberger, C. Lagrou, and D. Stehelin. 1983. A putative second cell-derived oncogene of the avian leukaemia retrovirus E26. Nature 306:395-397.
28. Lopez, R. G., C. Carron, and J. Ghysdael. 2003. v-SRC specifically regulates the nucleo-cytoplasmic delocalization of the major isoform of TEL (ETV6). J. Biol. Chem. 278:41316-41325.
29. Neve, R., C. H. Chang, G. K. Scott, A. Wong, R. R. Friis, N. E. Hynes, and C. C. Benz. 1998. The epithelium-specific ets transcription factor ESX is associated with mammary gland development and involution. FASEB J. 12:1541-1550.
30. Neve, R. M., B. Ylstra, C. H. Chang, D. G. Albertson, and C. C. Benz. 2002, ErbB2 activation of ESX gene expression. Oncogene 21:3934-3938.
31. Neznanov, N., A. K. Man, H. Yamamoto, C. A. Hauser, R. D. Cardiff, and R. G. Oshima. 1999. A single targeted Ets2 allele restricts development of mammary tumors in transgenic mice. Cancer Res. 59:4242-4246.
32. Ng, A. Y., P. Waring, S. Ristevski, C. Wang, T. Wilson, M. Pritchard, P. Hertzog, and I. Kola. 2002. Inactivation of the transcription factor Elf3 in mice results in dysmorphogenesis and altered differentiation of intestinal epithelium. Gastroenterology 122:1455-1466.
33. Niswender, K. D., S. M. Blackman, L. Rohde, M. A. Magnuson, and D. W. Piston. 1995. Quantitative imaging of green fluorescent protein in cultured cells: comparison of microscopic techniques, use in fusion proteins and detection limits. J. Microsc. 180:109-116.
34. Oettgen, P., R. M. Alani, M. A. Barcinski, L. Brown, Y. Akbarali, J. Boltax, C. Kunsch, K. Munger, and T. A. Libermann. 1997. Isolation and characterization of a novel epithelium-specific transcription factor, ESE-1, a member of the ets family. Mol. Cell. Biol. 17:4419-4433.
35. Oettgen, P., K. Kas, A. Dube, X. Gu, F. Grall, U. Thamrongsak, Y. Akbarali, E. Finger, J. Boltax, G. Endress, K. Munger, C. Kunsch, and T. A. Libermann. 1999. Characterization of ESE-2, a novel ESE-1-related Ets transcription factor that is restricted to glandular epithelium and differentiated keratinocytes. J. Biol. Chem. 274:29439-29452.
36. Oikawa, T., and T. Yamada. 2003. Molecular biology of the Ets family of transcription factors. Gene 303:11-34.
37. Oren, M. 2003. Decision making by p53: life, death and cancer. Cell Death Differ. 10:431-442.
38. Reddy, S. P., H. Vuong, and P. Adiseshaiah. 2003. Interplay between proximal and distal promoter elements is required for squamous differentiation marker induction in the bronchial epithelium: role for ESE-1, Sp1, and AP-1 proteins. J. Biol. Chem. 278:21378-21387.
39. Rhim, J. S. 2001. Molecular and genetic mechanisms of prostate cancer. Radiat. Res. 155:128-132.
40. Sapi, E., M. B. Flick, S. Rodov, and B. M. Kacinski. 1998. Ets-2 transdominant mutant abolishes anchorage-independent growth and macrophage colony-stimulating factor-stimulated invasion by BT20 breast carcinoma cells. Cancer Res. 58:1027-1033.
41. Schedin, P. J., K. L. Eckel-Mahan, S. M. McDaniel, J. D. Prescott, K. S. Brodsky, J. J. Tentler, and A. Gutierrez-Hartmann. 2004. ESX induces transformation and functional epithelial to mesenchymal transition in MCF-12A mammary epithelial cells. Oncogene 9:1766-1779.
42. Sharrocks, A. D. 2001. The ETS-domain transcription factor family. Nat. Rev. Mol. Cell. Biol. 2:827-837.
43. Soule, H. D., T. M. Maloney, S. R. Wolman, W. D. Peterson, Jr., R. Brenz, C. M. McGrath, J. Russo, R. J. Pauley, R. F. Jones, and S. C. Brooks. 1990. Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res. 50:6075-6086.
44. Teruyama, K., M. Abe, T. Nakano, C. Iwasaka-Yagi, S. Takahashi, S. Yamada, and Y. Sato. 2001. Role of transcription factor Ets-1 in the apoptosis of human vascular endothelial cells. J. Cell. Physiol. 188:243-252.
45. Tootle, T. L., P. S. Lee, and I. Rebay. 2003. CRM1-mediated nuclear export and regulated activity of the Receptor Tyrosine Kinase antagonist YAN require specific interactions with MAE. Development 130:845-857.
46. Trempe, G. L. 1976. Human breast cancer in culture. Recent Results Cancer Res. 57:33-41.
47. Tugores, A., J. Le, I. Sorokina, A. J. Snijders, M. Duyao, P. S. Reddy, L. Carlee, M. Ronshaugen, A. Mushegian, T. Watanaskul, S. Chu, A. Buckler, S. Emtage, and M. K. McCormick. 2001. The epithelium-specific ETS protein EHF/ ESE-3 is a context-dependent transcriptional repressor downstream of MAPK signaling cascades. J. Biol. Chem. 276:20397-20406.
48. Tymms, M. J., A. Y. Ng, R. S. Thomas, B. C. Schutte, J. Zhou, H. J. Eyre, G. R. Sutherland, A. Seth, M. Rosenberg, T. Papas, C. Debouck, and I. Kola. 1997. A novel epithelial-expressed ETS gene, ELF3: human and murine cDNA sequences, murine genomic organization, human mapping to 1q32.2 and expression in tissues and cancer. Oncogene 15:2449-2462.
49. Vermes, I., C. Haanen, H. Steffens-Nakken, and C. Reutelingsperger. 1995. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V, J. Immunol. Methods 184:39-51.
50. Vida, T. A., and S. D. Emr. 1995. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J. Cell Biol. 128:779-792.
51. Wasylyk, B., J. Hagman, and A. Gutierrez-Hartmann. 1998. Ets transcription factors: nuclear effectors of the Ras-MAP-kinase signaling pathway. Trends Biochem. Sci. 23:213-216.
52. Wolvetang, E. J., T. J. Wilson, E. Sanij, J. Busciglio, T. Hatzistavrou, A. Seth, P. J. Hertzog, and I. Kola. 2003. ETS2 overexpression in transgenic models and in Down syndrome predisposes to apoptosis via the p53 pathway. Hum. Mol. Genet. 12:247-255.
53. Yamada, T., and T. Oikawa. 1997. Induction of apoptosis by overexpression of the PU.1/Spi-1 gene in murine erythroleukemia cells. Leukemia 11(Suppl. 3):480-481.
54. Yoneda, Y. 1997. How proteins are transported from cytoplasm to the nucleus. J. Biochem. (Tokyo) 121:811-817.
55. Yoshida, N., S. Yoshida, M. Araie, H. Handa, and Y. Nabeshima. 2000. Ets family transcription factor ESE-1 is expressed in corneal epithelial cells and is involved in their differentiation. Mech. Dev. 97:27-34.