SOX4 induces epithelial-mesenchymal transition and contributes to breast cancer progression

Cancer Research

Volumn 72, Issue 17, 2012, Pages 4597-4608

  Zhang, Jianchao ^a   Liang, Qian ^a   Lei, Yang ^a   Yao, Min ^b   Li, Lili ^a   Gao, Xiaoge ^a   Feng, Jingxin ^a   Zhang, Yu ^a   Gao, Hongwen ^b   Liu, Dong Xu ^c   Lu, Jun ^a   Huang, Baiqu ^a  

^a NORTHEAST NORMAL UNIVERSITY   (China)

^b THE SECOND HOSPITAL OF JILIN UNIVERSITY   (China)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; PROGESTERONE RECEPTOR; TRANSCRIPTION FACTOR SOX4; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CANCER GROWTH; CARCINOGENESIS; CELL INVASION; CELL MIGRATION; CELL SUBPOPULATION; CONTROLLED STUDY; DISEASE ASSOCIATION; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIAL STEM CELL; FEMALE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; MARKER GENE; MOUSE; NONHUMAN; ONCOGENE RAS; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STEM CELL; TUMOR XENOGRAFT;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL TRANSFORMATION, NEOPLASTIC; DISEASE PROGRESSION; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, RAS; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM INVASIVENESS; NEOPLASTIC STEM CELLS; PROGNOSIS; SOXC TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84865767219     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-1045     Document Type: Article

References (48)

1. Bray F, McCarron P, Parkin DM. The changing global patterns of female breast cancer incidence and mortality. Breast Cancer Res 2004;6:229-39.
2. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
3. Gupta GP, Massague J. Cancer metastasis: building a framework. Cell 2006;127:679-95.
4. Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 2009;9:265-73.
5. Acloque H, Adams MS, Fishwick K, Bronner-Fraser M, Nieto MA. Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. J Clin Invest 2009;119:1438-49.
6. Yu M, Smolen GA, Zhang J, Wittner B, Schott BJ, Brachtel E, et al. A developmentally regulated inducer of EMT, LBX1, contributes to breast cancer progression. Genes Dev 2009;23:1737-42.
7. Huber MA, Kraut N, Beug H. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol 2005;17:548-58.
8. Xu J, Lamouille S, Derynck R. TGF-beta-induced epithelial to mesenchymal transition. Cell Res 2009;19:156-72.
9. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008;133:704-15.
10. Sarrio D, Rodriguez-Pinilla SM, Hardisson D, Cano A, Moreno-Bueno G, Palacios J. Epithelial-mesenchymal transition in breast cancer relates to the basal-like phenotype. Cancer Res 2008;68:989-97.
11. Schepers GE, Teasdale RD, Koopman P. Twenty pairs of sox: extent, homology, and nomenclature of the mouse and human sox transcription factor gene families. Dev Cell 2002;3:167-70.
12. Wegner M. From head to toes: the multiple facets of Sox proteins. Nucleic Acids Res 1999;27:1409-20.
13. van Houte L, van Oers A, van de Wetering M, Dooijes D, Kaptein R, Clevers H. The sequence-specific high mobility group 1 box of TCF-1 adopts a predominantly alpha-helical conformation in solution. J Biol Chem 1993;268:18083-7.
14. Schilham MW, Oosterwegel MA, Moerer P, Ya J, de Boer PA, van de Wetering M, et al. Defects in cardiac outflow tract formation and pro-Blymphocyte expansion in mice lacking Sox-4. Nature 1996;380:711-4.
15. Cheung M, Abu-Elmagd M, Clevers H, Scotting PJ. Roles of Sox4 in central nervous system development. Brain Res Mol Brain Res 2000;79:180-91.
16. van de Wetering M, Oosterwegel M, van Norren K, Clevers H. Sox-4, an Sry-like HMG box protein, is a transcriptional activator in lymphocytes. EMBO J 1993;12:3847-54.
17. Penzo-Mendez AI. Critical roles for Sox C transcription factors in development and cancer. Int J Biochem Cell Biol 2010;42:425-8.
18. Lee CJ, Appleby VJ, Orme AT, Chan WI, Scotting PJ. Differential expression of SOX4 and SOX11 in medulloblastoma. J Neurooncol 2002;57:201-14.
19. Castillo SD, Matheu A, Mariani N, Carretero J, Lopez-Rios F, Lovell-Badge R, et al. Novel transcriptional targets of the SRY-HMG box transcription factor SOX4 link its expression to the development of small cell lung cancer. Cancer Res 2012;72:176-86.
20. Liu P, Ramachandran S, Ali Seyed M, Scharer CD, Laycock N, Dalton WB, et al. Sex-determining region Y box 4 is a transforming oncogene in human prostate cancer cells. Cancer Res 2006;66:4011-9.
21. Graham JD, Hunt SM, Tran N, Clarke CL. Regulation of the expression and activity by progestins of a member of the SOX gene family of transcriptional modulators. J Mol Endocrinol 1999;22:295-304.
22. Ikushima H, Todo T, Ino Y, Takahashi M, Miyazawa K, Miyazono K. Autocrine TGF-beta signaling maintains tumorigenicity of glioma-initiating cells through Sry-related HMG-box factors. Cell Stem Cell 2009;5:504-14.
23. Lin B, Madan A, Yoon JG, Fang X, Yan X, Kim TK, et al. Massively parallel signature sequencing and bioinformatics analysis identifies up-regulation of TGFBI and SOX4 in human glioblastoma. PloS One 2010;5:e10210.
24. Sinner D, Kordich JJ, Spence JR, Opoka R, Rankin S, Lin SC, et al. Sox17 and Sox4 differentially regulate beta-catenin/T-cell factor activity and proliferation of colon carcinoma cells. Mol Cell Biol 2007;27:7802-15.
25. Lee AK, Ahn SG, Yoon JH, Kim SA. Sox4 stimulates b-catenin activity through induction of CK2. Oncology Rep 2011;25:559-65.
26. Debnath J, Muthuswamy SK, Brugge JS. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 2003;30:256-68.
27. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003;17:1253-70.
28. Zeng Q, Li W, Lu D, Wu Z, Duan H, Luo Y, et al. CD146, an epithelial-mesenchymal transition inducer, is associated with triple-negative breast cancer. Proc Natl Acad Sci U S A 2012;109:1127-32.
29. Ansieau S, Bastid J, Doreau A, Morel AP, Bouchet BP, Thomas C, et al. Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence. Cancer Cell 2008;14:79-89.
30. Miyazono K. Transforming growth factor-beta signaling in epithelial-mesenchymal transition and progression of cancer. Proc Jpn Acad Ser B Phys Biol Sci 2009;85:314-23.
31. Maeda M, Johnson KR, Wheelock MJ. Cadherin switching: essential for behavioral but not morphological changes during an epithelium-to-mesenchyme transition. J Cell Sci 2005;118:873-87.
32. Vincent T, Neve EP, Johnson JR, Kukalev A, Rojo F, Albanell J, et al. A SNAIL1-SMAD3/4 transcriptional repressor complex promotes TGF-beta mediated epithelial-mesenchymal transition. Nat Cell Biol 2009;11:943-50.
33. Tavazoie SF, Alarcon C, Oskarsson T, Padua D, Wang Q, Bos PD, et al. Endogenous human microRNAs that suppress breast cancer metastasis. Nature 2008;451:147-52.
34. Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, et al. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 2010;140:62-73.
35. Hur W, Rhim H, Jung CK, Kim JD, Bae SH, Jang JW, et al. SOX4 overexpression regulates the p53-mediated apoptosis in hepatocellular carcinoma: clinical implication and functional analysis in vitro. Carcinogenesis 2010;31:1298-307.
36. Huang YW, Liu JC, Deatherage DE, Luo J, Mutch DG, Goodfellow PJ, et al. Epigenetic repression of microRNA-129-2 leads to overexpression of SOX4 oncogene in endometrial cancer. Cancer Res 2009;69:9038-46.
37. Foubert E, De Craene B, Berx G. Key signalling nodes in mammary gland development and cancer. The Snail1-Twist1 conspiracy in malignant breast cancer progression. Breast Cancer Res 2010;12:206.
38. Pan X, Zhao J, Zhang WN, Li HY, Mu R, Zhou T, et al. Induction of SOX4 by DNA damage is critical for p53 stabilization and function. Proc Natl Acad Sci U S A 2009;106:3788-93.
39. Taube JH, Herschkowitz JI, Komurov K, Zhou AY, Gupta S, Yang J, et al. Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes. Proc Natl Acad Sci U S A 2010;107:15449-54.
40. Casas E, Kim J, Bendesky A, Ohno-Machado L, Wolfe CJ, Yang J. Snail2 is an essential mediator of Twist1-induced epithelial mesenchymal transition and metastasis. Cancer Res 2011;71:245-54.
41. Scheel C, Eaton EN, Li SH, Chaffer CL, Reinhardt F, Kah KJ, et al. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell 2011;145:926-40.
42. Cai H, Ni A, Li W, Li J. Inhibition of melanoma cell proliferation by targeting Wnt/b-catenin pathway through Sox4 RNA interference. J Huazhong U Sci-Med 2011;31:565-9.
43. Chen L, Xiao Z, Meng Y, Zhao Y, Han J, Su G, et al. The enhancement of cancer stem cell properties of MCF-7 cells in 3D collagen scaffolds for modeling of cancer and anti-cancer drugs. Biomaterials 2012;33:1437-44.
44. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 2003;100:3983-8.
45. Medina PP, Castillo SD, Blanco S, Sanz-Garcia M, Largo C, Alvarez S, et al. The SRY-HMG box gene, SOX4, is a target of gene amplification at chromosome 6p in lung cancer. Hum Mol Genet 2009;18:1343-52.
46. Liu M, Casimiro MC, Wang C, Shirley LA, Jiao X, Katiyar S, et al. p21CIP1 attenuates Ras- and c-Myc-dependent breast tumor epithelial mesenchymal transition and cancer stem cell-like gene expression in vivo. Proc Natl Acad Sci U S A 2009;106:19035-9.
47. Carey L, Winer E, Viale G, Cameron D, Gianni L. Triple-negative breast cancer: disease entity or title of convenience? Nat Rev Clin Oncol 2010;7:683-92.
48. Peddi PF, Ellis MJ, Ma C. Molecular basis of triple negative breast cancer and implications for therapy. Int J Breast Cancer 2012;2012:217185.