Homeoprotein Six1 increases TGF-β type I receptor and converts TGF-β signaling from suppressive to supportive for tumor growth

Cancer Research

Volumn 70, Issue 24, 2010, Pages 10371-10380

  Micalizzi, Douglas S ^a   Wang, Chu An ^a   Farabaugh, Susan M ^a   Schiemann, William P ^a   Ford, Heide L ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HOMEODOMAIN PROTEIN; HOMEOPROTEIN SIX1; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER; CANCER CELL; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EXPERIMENTAL NEOPLASM; HUMAN; HUMAN CELL; IN VIVO STUDY; METASTASIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; TUMOR GROWTH;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; MICE; MICE, INBRED NOD; MICE, NUDE; MICE, SCID; NEOPLASM METASTASIS; PROMOTER REGIONS, GENETIC; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA; UP-REGULATION;

EID: 78650359160     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-1354     Document Type: Article

References (50)

1. Brugmann SA, Pandur PD, Kenyon KL, Pignoni F, Moody SA. Six1 promotes a placodal fate within the lateral neurogenic ectoderm by functioning as both a transcriptional activator and repressor. Development 2004;131:5871-81.
2. Laclef C, Hamard G, Demignon J, Souil E, Houbron C, Maire P. Altered myogenesis in Six1-deficient mice. Development 2003;130:2239-52.
3. Xu PX, Zheng W, Huang L, Maire P, Laclef C, Silvius D. Six1 is required for the early organogenesis of mammalian kidney. Development 2003;130:3085-94.
4. Li X, Oghi KA, Zhang J, et al. Eya protein phosphatase activity regulates Six1-Dach-Eya transcriptional effects in mammalian organogenesis. Nature 2003;426:247-54. (Pubitemid 37463137)
5. Grifone R, Demignon J, Houbron C, et al. Six1 and Six4 homeoproteins are required for Pax3 and Mrf expression during myogenesis in the mouse embryo. Development 2005;132:2235-49.
6. Heanue TA, Reshef R, Davis RJ, et al. Synergistic regulation of vertebrate muscle development by Dach2, Eya2, and Six1, homologs of genes required for Drosophila eye formation. Genes Dev 1999;13:3231-43.
7. Abate-Shen C. Deregulated homeobox gene expression in cancer: cause or consequence?Nat Rev Cancer 2002;2:777-85.
8. Micalizzi DS, Ford HL. Epithelial-mesenchymal transition in development and cancer. Future Oncol 2009;5:1129-43.
9. Reichenberger KJ, Coletta RD, Schulte AP, Varella-Garcia M, Ford HL. Gene amplification is a mechanism of Six1 overexpression in breast cancer. Cancer Res 2005;65:2668-75.
10. Behbakht K, Qamar L, Aldridge CS, et al. Six1 overexpression in ovarian carcinoma causes resistance to TRAIL-mediated apoptosis and is associated with poor survival. Cancer Res 2007;67:3036-42. (Pubitemid 46724840)
11. Yu Y, Khan J, Khanna C, Helman L, Meltzer PS, Merlino G. Expression profiling identifies the cytoskeletal organizer ezrin and the developmental homeoprotein Six-1 as key metastatic regulators. Nat Med 2004;10:175-81. (Pubitemid 38524888)
12. Ng KT, Man K, Sun CK, et al. Clinicopathological significance of homeoprotein Six1 in hepatocellular carcinoma. Br J Cancer 2006;95:1050-5.
13. Coletta RD, Christensen Z, Reichenberger KJ, et al. The Six1 homeoprotein stimulates tumorigenesis by reactivation of cyclin A1. Proc Natl Acad Sci U S A 2004;101:6478-83.
14. Micalizzi DS, Christensen KL, Jedlicka P, et al. The Six1 homeoprotein induces human mammary carcinoma cells to undergo epithelial-mesenchymal transition and metastasis in mice through increasing TGF-beta signaling. J Clin Invest 2009;119:2678-90.
15. McCoy EL, Iwanaga R, Jedlicka P, et al. Six1 expands the mouse mammary epithelial stem/progenitor cell pool and induces mammary tumors that undergo epithelial-mesenchymal transition. J Clin Invest 2009;119:2663-77.
16. Coletta RD, Christensen KL, Micalizzi DS, Jedlicka P, Varella-Garcia M, Ford HL. Six1 overexpression in mammary cells induces genomic instability and is sufficient for malignant transformation. Cancer Res 2008;68:2204-13.
17. Blobe GC, Schiemann WP, Lodish HF. Role of transforming growth factor beta in human disease. N Engl J Med 2000;342:1350-8.
18. Azhar M, Runyan RB, Gard C, et al. Ligand-specific function of transforming growth factor beta in epithelial-mesenchymal transition in heart development. Dev Dyn 2009;238:431-42.
19. Nawshad A, LaGamba D, Hay ED. Transforming growth factor beta (TGFbeta) signalling in palatal growth, apoptosis and epithelial mesenchymal transformation (EMT). Arch Oral Biol 2004;49:675-89.
20. Rees JR, Onwuegbusi BA, Save VE, Alderson D, Fitzgerald RC. In vivo and in vitro evidence for transforming growth factor-beta1-mediated epithelial to mesenchymal transition in esophageal adenocarcinoma. Cancer Res 2006;66:9583-90.
21. Zavadil J, Bottinger EP. TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 2005;24:5764-74.
22. Jakowlew SB. Transforming growth factor-beta in cancer and metastasis. Cancer Metastasis Rev 2006;25:435-57.
23. Siegel PM, Massague J. Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat Rev Cancer 2003;3:807-21.
24. Chen CR, Kang Y, Massague J. Defective repression of c-myc in breast cancer cells: a loss at the core of the transforming growth factor beta growth arrest program. Proc Natl Acad Sci USA 2001;98:992-9.
25. Derynck R, Akhurst RJ, Balmain A. TGF-beta signaling in tumor suppression and cancer progression. Nat Genet 2001;29:117-29. (Pubitemid 32952643)
26. Ammanamanchi S, Brattain MG. Restoration of transforming growth factor-beta signaling through receptor RI induction by histone deacetylase activity inhibition in breast cancer cells. J Biol Chem 2004;279:32620-5.
27. Rojas A, Padidam M, Cress D, Grady WM. TGF-beta receptor levels regulate the specificity of signaling pathway activation and biological effects of TGF-beta. Biochim Biophys Acta 2009;1793:1165-73.
28. Pannu J, Gore-Hyer E, Yamanaka M, et al. An increased transforming growth factor beta receptor type I:type II ratio contributes to elevated collagen protein synthesis that is resistant to inhibition via a kinase-deficient transforming growth factor beta receptor type II in scleroderma. Arthritis Rheum 2004;50:1566-77.
29. Soufla G, Sifakis S, Baritaki S, Zafiropoulos A, Koumantakis E, Spandidos DA. VEGF, FGF2, TGFB1 and TGFBR1 mRNA expression levels correlate with the malignant transformation of the uterine cervix. Cancer Lett 2005;221:105-18.
30. Kjellman C, Olofsson SP, Hansson O, et al. Expression of TGF-beta isoforms, TGF-beta receptors, and SMAD molecules at different stages of human glioma. Int J Cancer 2000;89:251-8. (Pubitemid 30430741)
31. Takanami I, Tanaka F, Hashizume T, Kodaira S. Roles of the transforming growth factor beta 1 and its type I and II receptors in the development of a pulmonary adenocarcinoma: results of an immunohistochemical study. J Surg Oncol 1997;64:262-7.
32. Shtutman M, Levina E, Ohouo P, Baig M, Roninson IB. Cell adhesion molecule L1 disrupts E-cadherin-containing adherens junctions and increases scattering and motility of MCF7 breast carcinoma cells. Cancer Res 2006;66:11370-80.
33. Ford HL, Kabingu EN, Bump EA, Mutter GL, Pardee AB. Abrogation of the G2 cell cycle checkpoint associated with overexpression of HSIX1: a possible mechanism of breast carcinogenesis. Proc Natl Acad Sci USA 1998;95:12608-13.
34. Kalkhoven E, Roelen BA, de Winter JP, et al. Resistance to transforming growth factor beta and activin due to reduced receptor expression in human breast tumor cell lines. Cell Growth Differ 1995;6:1151-61.
35. Ko Y, Banerji SS, Liu Y, et al. Expression of transforming growth factor-beta receptor type II and tumorigenicity in human breast adenocarcinoma MCF-7 cells. J Cell Physiol 1998;176:424-34.
36. Lonn P, Moren A, Raja E, Dahl M, Moustakas A. Regulating the stability of TGFbeta receptors and Smads. Cell Res 2009;19:21-35.
37. Yu Y, Davicioni E, Triche TJ, Merlino G. The homeoprotein six1 transcriptionally activates multiple protumorigenic genes but requires ezrin to promote metastasis. Cancer Res 2006;66:1982-9.
38. Noyes MB, Christensen RG, Wakabayashi A, Stormo GD, Brodsky MH, Wolfe SA. Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell 2008;133:1277-89.
39. Spitz F, Demignon J, Porteu A, et al. Expression of myogenin during embryogenesis is controlled by Six/sine oculis homeoproteins through a conserved MEF3 binding site. Proc Natl Acad Sci USA 1998;95:14220-5.
40. Berger MF, Badis G, Gehrke AR, et al. Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 2008;133:1266-76.
41. Donepudi M, Resh MD. c-Src trafficking and co-localization with the EGF receptor promotes EGF ligand-independent EGF receptor activation and signaling. Cell Signal 2008;20:1359-67.
42. Di Fiore PP, Pierce JH, Kraus MH, Segatto O, King CR, Aaronson SA. erbB-2 is a potent oncogene when overexpressed in NIH/3T3 cells. Science 1987;237:178-82.
43. Boldin MP, Mett IL, Varfolomeev EE, et al. Self-association of the "death domains" of the p55 tumor necrosis factor (TNF) receptor and Fas/APO1 prompts signaling for TNF and Fas/APO1 effects. J Biol Chem 1995;270:387-91.
44. Nam JS, Terabe M, Mamura M, et al. An anti-transforming growth factor beta antibody suppresses metastasis via cooperative effects on multiple cell compartments. Cancer Res 2008;68:3835-43.
45. Schlingensiepen KH, Schlingensiepen R, Steinbrecher A, et al. Targeted tumor therapy with the TGF-beta 2 antisense compound AP 12009. Cytokine Growth Factor Rev 2006;17:129-39.
46. Halder SK, Beauchamp RD, Datta PK. A specific inhibitor of TGF-beta receptor kinase, SB-431542, as a potent antitumor agent for human cancers. Neoplasia 2005;7:509-21.
47. Hamada J, Omatsu T, Okada F, et al. Overexpression of homeobox gene HOXD3 induces coordinate expression of metastasis-related genes in human lung cancer cells. Int J Cancer 2001;93:516-25.
48. Wu X, Chen H, Parker B, et al. HOXB7, a homeodomain protein, is overexpressed in breast cancer and confers epithelial-mesenchymal transition. Cancer Res 2006;66:9527-34.
49. Yu M, Smolen GA, Zhang J, et al. A developmentally regulated inducer of EMT, LBX1, contributes to breast cancer progression. Genes Dev 2009;23:1737-42.
50. Hau P, Jachimczak P, Schlingensiepen R, et al. Inhibition of TGF-beta2 with AP 12009 in recurrent malignant gliomas: from preclinical to phase I/II studies. Oligonucleotides 2007;17:201-12.