KLF17 is a negative regulator of epithelial-mesenchymal transition and metastasis in breast cancer

Nature Cell Biology

Volumn 11, Issue 11, 2009, Pages 1297-1304

  Gumireddy, Kiranmai ^a   Li, Anping ^a   Gimotty, Phyllis A ^b   Klein Szanto, Andres J ^c   Showe, Louise C ^a   Katsaros, Dionyssios ^d   Coukos, George ^b,e   Zhang, Lin ^b   Huang, Qihong ^a  

^a WISTAR INSTITUTE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c FOX CHASE CANCER CENTER   (United States)

^d UNIVERSITY OF TURIN   (Italy)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KRUPPEL LIKE FACTOR 17; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER INVASION; CELL SELECTION; CELL TRANSFORMATION; CONTROLLED STUDY; DOWN REGULATION; EPITHELIUM CELL; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG METASTASIS; MALIGNANT TRANSFORMATION; MESENCHYME CELL; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; RNA INTERFERENCE; TRANSCRIPTION REGULATION;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DOWN-REGULATION; EPITHELIAL CELLS; FEMALE; GENES, TUMOR SUPPRESSOR; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEIN 1; MESODERM; MICE; NEOPLASM METASTASIS; RNA INTERFERENCE; TRANSCRIPTION FACTORS;

EID: 70449529854     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1974     Document Type: Article

References (56)

1. Gupta, G. P. & Massague, J. Cancer Metastasis: Building a framework. Cell 127, 679 (2006).
2. Steeg, P. S. Tumor metastasis: Mechanistic insights and clinical challenges. Nature Rev. Med. 12, 895-904 (2006).
3. Fidler, I. J. The pathogenesis of cancer metastasis: The "seed and soil" hypothesis revisited. Nature Rev. Cancer 3, 1-6 (2003).
4. Steeg, P. S. Metastasis suppressors alter the signal transduction of cancer cells. Nature Rev. Cancer 3, 55-63 (2003).
5. Yang, J. et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117, 927-939 (2004).
6. Kang, Y. et al. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3, 537-549 (2003).
7. Muller, A. et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 410, 50-56 (2001).
8. Eccles, S. A. & Welch, D. R. Metastasis: Recent discoveries and novel treatment. strategies. Lancet 369, 1742-1757 (2007).
9. Chambers, A. F., Groom, A. C. & MacDonald, I. C. Dissemination and growth of cancer cells in metastatic sites. Nature Rev. Cancer 2, 563-572 (2002).
10. Stafford, L. J., Vaidya, K. S. & Welch, D. R. Metastasis suppressor genes in cancer. Int. J. Biochem. Cell Biol. 40, 874-891 (2008).
11. Yoshida, B. A., Sokoloff, M. M., Welch, D. R. & Rinker-Schaeffer, C. W. Metastasissuppressor genes: A review and perspective on an emerging field. J. Natl Cancer Inst. 92, 1717-1730 (2000).
12. Grimm, S. The art and design of genetic screens: Mammalian culture cells. Nature Rev. Genet. 5, 179-189 (2004).
13. Schlabach, M. et al. Cancer proliferation gene discovery through functional genomics. Science 319, 620-624 (2008).
14. Dasgupta, R., Kaykas, A., Moon, R. T. & Perrimon, N. Functional genomic analysis of the Wnt-Wingless signaling pathway. Science 308, 826-832 (2005).
15. Fraser, A. G. et al. Functional genomic analysis of C. elegans chromosome I by systemic RNA interference. Nature 408, 325-330 (2000).
16. Paddison, P. J. et al. A resource for large-scale RNA-interference-based screens in mammals. Nature 428, 427-431 (2004).
17. Berns K et al. A large-scale RNAi screen in human cells identifies new components of the p53 pathway. Nature 428, 431-7 (2004).
18. Kolfschoten, I. G. et al. A genetic screen identifies PITX1 as a suppressor of RAS activity and tumorigenicity Cell 121, 849-58 (2005).
19. Aslakson, C. J. & Miller, F. R. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res. 52, 1399-1405 (1992).
20. Aslakson, C. J., Rak, J. W., Miller, B. E. & Miller, F. R. Differential influence of organ site on three subpopulations of a single mouse mammary tumor at two distinct steps in metastasis. Int. J. Cancer 47, 466-472 (1991).
21. Miller, F., Jones, R. F., Jacob, J., Kong, Y. C., Wei, Y. Z. From breast cancer immunology to her-2 DNA vaccine and autoimmune sequelae. Breast Dis. 20, 43-51 (2004).
22. Dexter, D. L. et al. Heterogeneity of tumor cells from a single mouse mammary tumor. Cancer Res. 38, 3174-3181 (1978).
23. Gumireddy, K. et al. An in vivo selection for metastasis promoting genes in the mouse. Proc. Natl Acad. Sci. USA 104, 6696-6701 (2007).
24. Lomberk, G., Urrutia, R. The family feud: Turning off Sp1 by Sp1-like KLF proteins. Biochem. J. 392, 1-11 (2005).
25. Kaczynski, J., Cook, T., Urrutia, R. Sp1- and Krüppel-like transcription factors. Genome Biol. 4, 206 (2003).
26. Vliet, J. V. et al. Human KLF17 is a new member of the Sp/KLF family of transcription factors. Genomics 87, 474-482 (2005).
27. Takahashi, K. et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872 (2007).
28. Nuez, B., Michalovich, D., Bygrave, A., Ploemacher, R., Grosveld, F. Defective haematopoiesis in fetal liver resulting from inactivation of the EKLF gene. Nature 375, 316-318 (1995).
29. Perkins, A. C., Sharpe, A. H. & Orkin, S. H. Lethal -thalassaemia in mice lacking the erythroid CACCC-transcription factor EKLF. Nature 375, 318-322 (1995).
30. Kuo, C. T., Veselits, M. L., Leiden, J. M. LKLF: A transcriptional regulator of singlepositive T cell quiescence and survival. Science 277, 1986-1990 (1997).
31. Foster, K. W. et al. Increase of GKLF messenger RNA and protein expression during progression of breast cancer. Cancer Res. 60, 6488-6495 (2000).
32. Narla, G. et al. KLF6, a candidate tumor suppressor gene mutated in prostate cancer. Science 294, 2563-2566 (2001).
33. Ghaleb, A. M. et al. Krüppel-like factors 4 and 5: The yin and yang regulators of cellular proliferation. Cell Res. 15, 92-96 (2005).
34. Yan, W., Burns, K. H., Ma, L., Matzuk, M. M. Identification of Zfp393 a germ-cell specific gene encoding a novel zinc finger protein. Mech. of Dev. 118, 233-239 (2002).
35. Hugo, H. et al. Epithelial-mesenchymal and mesenchymal-epithelial transition in carcinoma progression. J. Cell. Physiol. 213, 374-383 (2007).
36. Huber, M. A., Kraut, N. & Beug, H. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr. Opin. Cell Biol. 17, 548-558 (2005).
37. Zavadil, J., Cermak, L., Soto-Nieves, N., Bottinger, E. P. Integration of TGF-β/Smad and Jagged1/Notch signaling in endothelial to mesenchymal transition. EMBO J. 23, 1155-1165 (2004).
38. Liebner, S. et al. β-catinin is required for endothelial-mesenchymal transformation furing heart cushion development in the mouse. J. Cell. Biol. 166, 359-367 (2004).
39. Moody, S. E. et al. The transcriptional repressor Snail promotes mammary tumor recurrence. Cancer Cell 8, 197-209 (2005).
40. Hartwell, K. A. et al. The spemann organizer gene, goosecoid promotes tumor metastasis. Proc. Natl. Acad. Sci. USA 103 18969-18974 (2006).
41. Ruzinova, M. B. & Benezra, R. Id proteins in development, cell cycle and cancer. Trends in Cell Biol. 13, 410-418 (2003).
42. Sikder, H. A., Devlin, M. K., Dunlap, S., Ryu, B. & Alani, R. Id proteins in cell growth and tumorigenesis Cancer Cell 3, 525-530 (2003).
43. Ivarone, A. & Lasorella, A. ID proteins as targets in cancer and tools in neurobiology. Trends in Mol. Med. 12, 588-594 (2006).
44. Ying, Q., Nichols, J., Chambers, I. & Smith, A. BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115, 281-292 (2003).
45. Li, Y., Yang, J., Luo, J., Dedhar, S., Liu, Y. Tubular epithelial cell dedifferentiation is driven by the helix-loop-helix transcriptional inhibitor Id1. J. Am. Soc. Nephrol. 18, 449-460 (2007).
46. Lyden, D. et al. Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumor xenograft. Nature 401 670-677 (1999).
47. Minn, A. J. et al. Genes that mediate breast cancer metastasis to lung. Nature 436, 518-524 (2005).
48. Swarbrick, A., Roy, E., Allen, T. & Bishop, J. M. Id1 cooperates with oncogenic Ras to induce metastastic mammary carcinoma by subversion of the cellular senescence response. Proc. Natl. Acad. Sci. USA 105, 5402-5407 (2008).
49. Schoppmann, S. F. et al. Overexpression of Id-1 is associated with poor clinical outcome in node negative breast cancer. Int. J. Cancer 104, 677-682 (2003).
50. Lin, C. Q. et al. A role for Id-1 in the aggressive phenotype and steroid hormone response of human breast cancer cells. Cancer Res. 60, 1332-1340 (2000).
51. Gupta, G. P. et al. ID genes mediate tumor reinitiation during breast cancer lung metastasis. Proc. Natl. Acad. Sci. USA 104 19506-19511 (2007).
52. Henke, E. et al. Peptide-conjugated antise oligonucleotides for targeted inhibition of a transcription regulator in vivo. Nature Biotechnol. 26, 91-100 (2008).
53. McAllister, S. D., Christian, R. T., Horowitz, M. P., Garcia, A. & Desprez, P. Cannabidiol as a novel inhibitor of Id-1 gene expression in aggressive breast cancer cells. Mol. Cancer Ther. 6, 2921-2927 (2007).
54. Kataoka, M. et al. An agent that increases tumor suppressor transgene product coupled with systemic transgene delivery inhibits growth of metastatic lung cancer in vivo. Cancer Res. 58, 4761-4765 (1998).
55. Huang, Q. et al. The microRNAs miR-373 and miR-520c promote tumor invasion and metastasis. Nature Cell Biol. 10, 202-210 (2008).
56. Mukhopadhyay, A., Deplancke, B., Walhout, A. J. M., Tissenbaum, H. A. Chromatin immunoprecipitation (ChIP) coupled to detection by quantitative real- time PCR to study transcription factors binding to DNA in Caenorhabditis elegans. Nature Protoc. 3, 698-709 (2008).