A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition

Cancer Research

Volumn 68, Issue 19, 2008, Pages 7846-7854

  Bracken, Cameron P ^a   Gregory, Philip A ^a,b   Kolesnikoff, Natasha ^a   Bert, Andrew G ^a   Wang, Jun ^c   Shannon, M Frances ^c   Goodall, Gregory J ^a,b  

^a INSTITUTE OF MEDICAL AND VETERINARY SCIENCE   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c Biology and Environment   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 200A; MICRORNA 200B; MICRORNA 429; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SIP1'; TRANSCRIPTION FACTOR ZEB1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING KINETICS; CISTRON; CONTROLLED STUDY; E BOX ELEMENT; EMBRYO DEVELOPMENT; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; GENE EXPRESSION; GENE LOCATION; GENETIC CODE; HUMAN; HUMAN CELL; MESENCHYME CELL; NEGATIVE FEEDBACK; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; TRANSCRIPTION INITIATION SITE;

ANIMALS; CELLS, CULTURED; DOGS; E-BOX ELEMENTS; EPITHELIAL CELLS; FEEDBACK, BIOCHEMICAL; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; HUMANS; MESODERM; MICE; MICRORNAS; MODELS, BIOLOGICAL; MULTIGENE FAMILY; NERVE TISSUE PROTEINS; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; RNA-BINDING PROTEINS; TRANSCRIPTION FACTORS;

EID: 54049084380     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-1942     Document Type: Article

References (43)

1. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004;116:281-97.
2. Lee Y, Kim M, Han J, et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004;23:4051-60.
3. Zhou X, Ruan J, Wang G, et al. Characterization and identification of microRNA core promoters in four model species. PLoS Comput Biol 2007;3:e37.
4. Saini HK, Griffiths-Jones S, Enright AJ. Genomic analysis of human microRNA transcripts. Proc Natl Acad Sci U S A 2007;104:17719-24.
5. Woods K, Thomson JM, Hammond SM. Direct regulation of an oncogenic micro-RNA cluster by E2F transcription factors. J Biol Chem 2007;282:2130-4.
6. Petrocca F, Visone R, Onelli MR, et al. E2F1-regulated microRNAs impair TGFh-dependent cell-cycle arrest and apoptosis in gastric cancer. Cancer Cell 2008;13:272-86.
7. Fazi F, Rosa A, Fatica A, et al. A minicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBPa regulates human granulopoiesis. Cell 2005;123:819-31.
8. Gregory PA, Bert AG, Paterson EL, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008;10:593-601.
9. Park SM, Gaur AB, Lengyel E, et al. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 2008;22:894-907.
10. Aigner K, Dampier B, Descovich L, et al. The transcription factor ZEB1 (δEF1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity. Oncogene 2007;26:6979-88.
11. Comijn J, Berx G, Vermassen P, et al. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol Cell 2001;7:1267-78.
12. Eger A, Aigner K, Sonderegger S, et al. δEF1 is a transcriptional repressor of E-cadherin and regulates epithelial plasticity in breast cancer cells. Oncogene 2005;24:2375-85.
13. Remacle JE, Kraft H, Lerchner W, et al. New mode of DNA binding of multi-zinc finger transcription factors: δEF1 family members bind with two hands to two target sites. EMBO J 1999;18:5073-84.
14. Sekido R, Murai K, Funahashi J, et al. The δ-crystallin enhancer-binding protein δ EF1 is a repressor of E2-box-mediated gene activation. Mol Cell Biol 1994;14:5692-700.
15. Spaderna S, Schmalhofer O, Wahlbuhl M, et al. The transcriptional repressor ZEB1 promotes metastasis and loss of cell polarity in cancer. Cancer Res 2008;68:537-44.
16. Vandewalle C, Comijn J, De CB, et al. SIP1/ZEB2 induces EMT by repressing genes of different epithelial cell-cell junctions. Nucleic Acids Res 2005;33:6566-78.
17. Verschueren K, Remacle JE, Collart C, et al. SIP1, a novel zinc finger/homeodomain repressor, interacts with Smad proteins and binds to 5′-CACCT sequences in candidate target genes. J Biol Chem 1999;274:20489-98.
18. Hugo H, Ackland ML, Blick T, et al. Epithelial-mesenchymal and mesenchymal-epithelial transitions in carcinoma progression. J Cell Physiol 2007;213:374-83.
19. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002;2:442-54.
20. Wyatt L, Wadham C, Crocker LA, et al. The protein tyrosine phosphatase Pez regulates TGF{β}, epithelial mesenchymal transition, and organ development. J Cell Biol 2007;178:1223-35.
21. Christoffersen NR, Silahtaroglu A, Orom UA, et al. miR-200b mediates post-transcriptional repression of ZFHX1B. RNA 2007;13:1172-8.
22. Karolchik D, Baertsch R, Diekhans M, et al. The UCSC Genome Browser Database. Nucleic Acids Res 2003;31:51-4.
23. Kimura K, Wakamatsu A, Suzuki Y, et al. Diversification of transcriptional modulation: large-scale identification and characterization of putative alternative promoters of human genes. Genome Res 2006;16:55-65.
24. Burk U, Schubert J, Wellner U, et al. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep 2008;9:582-9.
25. Hornstein E and Shomron N. Canalization of development by microRNAs. Nat Genet 2006;38 Suppl:S20-24.
26. Tsang J, Zhu J, van OA. MicroRNA-mediated feedback and feedforward loops are recurrent network motifs in mammals. Mol Cell 2007;26:753-67.
27. Chua HL, Bhat-Nakshatri P, Clare SE, et al. NF-κB represses E-cadherin expression and enhances epithelial to mesenchymal transition of mammary epithelial cells: potential involvement of ZEB-1 and ZEB-2. Oncogene 2007;26:711-24.
28. Miyoshi A, Kitajima Y, Sumi K, et al. Snail and SIP1 increase cancer invasion by upregulating MMP family in hepatocellular carcinoma cells. Br J Cancer 2004;90:1265-73.
29. Elloul S, Elstrand MB, Nesland JM, et al. Snail, Slug, and Smad-interacting protein 1 as novel parameters of disease aggressiveness in metastatic ovarian and breast carcinoma. Cancer 2005;103:1631-43.
30. Imamichi Y and Menke A. Signaling pathways involved in collagen-induced disruption of the E-cadherin complex during epithelial-mesenchymal transition. Cells Tissues Organs 2007;185:180-90.
31. Ohira T, Gemmill RM, Ferguson K, et al. WNT7a induces E-cadherin in lung cancer cells. Proc Natl Acad Sci U S A 2003;100:10429-34.
32. Rosivatz E, Becker I, Specht K, et al. Differential expression of the epithelial-mesenchymal transition regulators snail, SIP1, and twist in gastric cancer. Am J Pathol 2002;161:1881-91.
33. Spaderna S, Schmalhofer O, Hlubek F, et al. A transient, EMT-linked loss of basement membranes indicates metastasis and poor survival in colorectal cancer. Gastroenterology 2006;131:830-40.
34. Spoelstra NS, Manning NG, Higashi Y, et al. The transcription factor ZEB1 is aberrantly expressed in aggressive uterine cancers. Cancer Res 2006;66:3893-902.
35. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100:57-70.
36. Gupta GP, Massague J. Cancer metastasis: building a framework. Cell 2006;127:679-95.
37. Fodde R, Brabletz T. Wnt/β-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol 2007;19:150-8.
38. Li X, Carthew RW. A microRNA mediates EGF receptor signaling and promotes photoreceptor differentiation in the Drosophila eye. Cell 2005;123:1267-77.
39. Meulemans D, Bronner-Fraser M. Gene-regulatory interactions in neural crest evolution and development. Dev Cell 2004;7:291-9.
40. Nawshad A, LaGamba D, Hay ED. Transforming growth factor β (TGFβ) signalling in palatal growth, apoptosis and epithelial mesenchymal transformation (EMT). Arch Oral Biol 2004;49:675-89.
41. Liu Y, El-Naggar S, Darling DS, et al. Zeb1 links epithelial-mesenchymal transition and cellular senescence. Development 2008;135:579-88.
42. Krutzfeldt J, Rajewsky N, Braich R, et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature 2005;438:685-9.
43. Elmen J, Lindow M, Schutz S, et al. LNA-mediated microRNA silencing in non-human primates. Nature 2008;452:896-9.