The high mobility group A2 protein epigenetically silences the Cdh1 gene during epithelial-to-mesenchymal transition

Nucleic Acids Research

Volumn 43, Issue 1, 2015, Pages 162-178

  Tan, E Jean ^a   Kahata, Kaoru ^a   Idås, Oskar ^a   Thuault, Sylvie ^a,b   Heldin, Carl Henrik ^a   Moustakas, Aristidis ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b University of the Mediterranean Aix Marseille II   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AZACITIDINE; CADHERIN; CCCTC-BINDING FACTOR; CDH1 PROTEIN, HUMAN; DECITABINE; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA METHYLTRANSFERASE 3A; HIGH MOBILITY GROUP A2 PROTEIN; REPRESSOR PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANALOGS AND DERIVATIVES; BIOSYNTHESIS; BREAST TUMOR; CELL CULTURE; CELL MOTION; CPG ISLAND; DNA METHYLATION; DRUG EFFECTS; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE SILENCING; GENETICS; HUMAN; METABOLISM; PROMOTER REGION; TUMOR CELL LINE;

AZACITIDINE; BREAST NEOPLASMS; CADHERINS; CELL LINE, TUMOR; CELL MOVEMENT; CELLS, CULTURED; CPG ISLANDS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE SILENCING; HMGA2 PROTEIN; HUMANS; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84945188848     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1293     Document Type: Article

References (49)

1. Nieto,M.A. (2013) Epithelial plasticity: a common theme in embryonic and cancer cells. Science, 342, 1234850.
2. Gunasinghe,N.P.A.D.,Wells,A., Thompson,E.W. and Hugo,H.J. (2012) Mesenchymal-epithelial transition (MET) as a mechanism for metastatic colonisation in breast cancer. Cancer Metast. Rev., 31, 469-478.
3. Thiery,J.P., Acloque,H., Huang,R.Y.J. and Nieto,M.A. (2009) Epithelial-mesenchymal transitions in development and disease. Cell, 139, 871-890.
4. Craene,B.D. and Berx,G. (2012) Regulatory networks defining EMT during cancer initiation and progression. Nat. Rev. Cancer, 13, 97-110.
5. Tam,W.L. and Weinberg,R.A. (2013) The epigenetics of epithelial-mesenchymal plasticity in cancer. Nat. Med., 19, 1438-1449.
6. van Roy,F. and Berx,G. (2008) The cell-cell adhesion molecule E-cadherin. Cell. Mol. Life Sci., 65, 3756-3788.
7. Cedar,H. and Bergman,Y. (2009) Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet., 10, 295-304.
8. Graff,J.R., Herman,J.G., Lapidus,R.G., Chopra,H., Xu,R., Jarrard,D.F., Isaacs,W.B., Pitha,P.M., Davidson,N.E. and Baylin,S.B. (1995) E-cadherin expression is silenced by DNA hypermethylation in human breast and prostate carcinomas. Cancer Res., 55, 5195-5199.
9. Lombaerts,M., van Wezel,T., Philippo,K., Dierssen,J.W.F., Zimmerman,R.M.E., Oosting,J., van Eijk,R., Eilers,P.H., van de Water,B., Cornelisse,C.J. et al. (2006) E-cadherin transcriptional downregulation by promoter methylation but not mutation is related to epithelial-to-mesenchymal transition in breast cancer cell lines. Br. J. Cancer, 94, 661-671.
10. Yoshiura,K., Kanai,Y., Ochiai,A., Shimoyama,Y., Sugimura,T. and Hirohashi,S. (1995) Silencing of the E-cadherin invasion-suppressor gene by CpG methylation in human carcinomas. Proc. Natl. Acad. Sci. U.S.A., 92, 7416-7419.
11. Moustakas,A. and Heldin,C.-H. (2012) Induction of epithelial-mesenchymal transition by transforming growth factor. Sem. Cancer Biol., 22, 446-454.
12. Thuault,S., Valcourt,U., Petersen,M., Manfioletti,G., Heldin,C.-H. and Moustakas,A. (2006) Transforming growth factor-employs HMGA2 to elicit epithelial-mesenchymal transition. J. Cell Biol., 174, 175-183.
13. Pfannkuche,K., Summer,H., Li,O., Hescheler,J. and Dröge,P. (2009) The high mobility group protein HMGA2: a co-regulator of chromatin structure and pluripotency in stem cells? Stem Cell Rev., 5, 224-230.
14. Kumar,M.S., Armenteros-Monterroso,E., East,P., Chakravorty,P., Matthews,N., Winslow,M.M. and Downward,J. (2013) HMGA2 functions as a competing endogenous RNA to promote lung cancer progression. Nature, 505, 212-217.
15. Morishita,A., Zaidi,M.R., Mitoro,A., Sankarasharma,D., Szabolcs,M., Okada,Y., D'Armiento,J. and Chada,K. (2013) HMGA2 is a driver of tumor metastasis. Cancer Res., 73, 4289-4299.
16. Sun,M., Song,C.X., Huang,H., Frankenberger,C.A., Sankarasharma,D., Gomes,S., Chen,P., Chen,J., Chada,K.K., He,C. et al. (2013) HMGA2/TET1/HOXA9 signaling pathway regulates breast cancer growth and metastasis. Proc. Natl. Acad. Sci. U.S.A., 110, 9920-9925.
17. Thuault,S., Tan,E.-J., Peinado,H., Cano,A., Heldin,C.-H. and Moustakas,A. (2008) HMGA2 and Smads co-regulate SNAIL1 expression during induction of epithelial-to-mesenchymal transition. J. Biol. Chem., 283, 33437-33446.
18. Tan,E.-J., Thuault,S., Caja,L., Carletti,T., Heldin,C.-H. and Moustakas,A. (2012) Regulation of transcription factor Twist expression by the DNA architectural protein high mobility group A2 during epithelial-to-mesenchymal transition. J. Biol. Chem., 287, 7134-7145.
19. Santner,S.J., Dawson,P.J., Tait,L., Soule,H.D., Eliason,J., Mohamed,A.N.,Wolman,S.R., Heppner,G.H. and Miller,F.R. (2001) Malignant MCF10CA1 cell lines derived from premalignant human breast epithelial MCF10AT cells. Breast Cancer Res. Treat., 65, 101-110.
20. Deckers,M., van Dinther,M., Buijs,J., Que,I., Löwik,C., van der Pluijm,G. and ten Dijke,P. (2006) The tumor suppressor Smad4 is required for transforming growth factor-induced epithelial to mesenchymal transition and bone metastasis of breast cancer cells. Cancer Res., 66, 2202-2209.
21. Ringnér,M., Fredlund,E., Hakkinen,J., Borg,A. and Staaf,J. (2011) GOBO: gene expression-based outcome for breast cancer online. PLoS One, 6, e17911.
22. Ji,X., Woodard,A.S., Rimm,D.L. and Fearon,E.R. (1997) Transcriptional defects underlie loss of E-cadherin expression in breast cancer. Cell Growth Differ., 8, 773-778.
23. Bergstr öm,R., Savary,K., Morén,A., Guibert,S., Heldin,C.-H., Ohlsson,R. and Moustakas,A. (2010) Transforming growth factor promotes complexes between Smad proteins and the CCCTC-binding factor on the H19 imprinting control region chromatin. J. Biol. Chem., 285, 19727-19737.
24. McDonald,O.G.,Wu,H., Timp,W., Doi,A. and Feinberg,A.P. (2011) Genome-scale epigenetic reprogramming during epithelial-to-mesenchymal transition. Nat. Struct. Mol. Biol., 18, 867-874.
25. Suva,M.L., Riggi,N. and Bernstein,B.E. (2013) Epigenetic Reprogramming in Cancer. Science, 339, 1567-1570.
26. Peinado,H., Ballestar,E., Esteller,M. and Cano,A. (2003) Snail mediates E-cadherin repression by the recruitment of the Sin3A/histone deacetylase 1 (HDAC1)/HDAC2 complex. Mol. Cell. Biol., 24, 306-319.
27. Neve,R.M., Chin,K., Fridlyand,J., Yeh,J., Baehner,F.L., Fevr,T., Clark,L., Bayani,N., Coppe,J.P., Tong,F. et al. (2006) A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell, 10, 515-527.
28. Kelly,T.K., De Carvalho,D.D. and Jones,P.A. (2010) Epigenetic modifications as therapeutic targets. Nat. Biotechnol., 28, 1069-1078.
29. Berx,G., Cleton-Jansen,A.M., Nollet,F., de Leeuw,W.J., van de Vijver,M., Cornelisse,C. and van Roy,F. (1995) E-cadherin is a tumour/invasion suppressor gene mutated in human lobular breast cancers. EMBO J., 14, 6107-6115.
30. Frixen,U.H., Behrens,J., Sachs,M., Eberle,G., Voss,B., Warda,A., Löchner,D. and Birchmeier,W. (1991) E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J. Cell Biol., 113, 173-185.
31. Tessari,M.A., Gostissa,M., Altamura,S., Sgarra,R., Rustighi,A., Salvagno,C., Caretti,G., Imbriano,C.,Mantovani,R., Del Sal,G. et al. (2003) Transcriptional activation of the cyclin A gene by the architectural transcription factor HMGA2. Mol. Cell. Biol., 23, 9104-9116.
32. Oskarsson,T., Acharyya,S., Zhang,X.H.-F., Vanharanta,S., Tavazoie,S.F., Morris,P.G., Downey,R.J., Manova-Todorova,K., Brogi,E. and Massagué,J. (2011) Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat. Med., 17, 867-874.
33. Gal,A., Sj öblom,T., Fedorova,L., Imreh,S., Beug,H. and Moustakas,A. (2008) Sustained TGF exposure suppresses Smad and non-Smad signalling in mammary epithelial cells, leading to EMT and inhibition of growth arrest and apoptosis. Oncogene, 27, 1218-1230.
34. McGarvey,K.M., Fahrner,J.A., Greene,E., Martens,J., Jenuwein,T. and Baylin,S.B. (2006) Silenced tumor suppressor genes reactivated by DNA demethylation do not return to a fully euchromatic chromatin state. Cancer Res., 66, 3541-3549.
35. Witcher,M. and Emerson,B.M. (2009) Epigenetic silencing of the p16INK4a tumor suppressor is associated with loss of CTCF binding and a chromatin boundary. Mol. Cell, 34, 271-284.
36. Wang,H., Maurano,M.T., Qu,H., Varley,K.E., Gertz,J., Pauli,F., Lee,K., Canfield,T.,Weaver,M., Sandstrom,R. et al. (2012) Widespread plasticity in CTCF occupancy linked to DNA methylation. Genome Res., 22, 1680-1688.
37. Dong,C., Wu,Y., Yao,J., Wang,Y., Yu,Y., Rychahou,P.G., Evers,B.M. and Zhou,B.P. (2012) G9a interacts with Snail and is critical for Snail-mediated E-cadherin repression in human breast cancer. J. Clin. Invest., 122, 1469-1486.
38. Dumont,N., Wilson,M.B., Crawford,Y.G., Reynolds,P.A., Sigaroudinia,M. and Tlsty,T.D. (2008) Sustained induction of epithelial to mesenchymal transition activates DNA methylation of genes silenced in basal-like breast cancers. Proc. Natl. Acad. Sci. U.S.A., 105, 14867-14872.
39. Perl,A.K., Wilgenbus,P., Dahl,U., Semb,H. and Christofori,G. (1998) A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature, 392, 190-193.
40. Papageorgis,P., Lambert,A.W., Ozturk,S., Gao,F., Pan,H., Manne,U., Alekseyev,Y.O., Thiagalingam,A., Abdolmaleky,H.M., Lenburg,M. et al. (2010) Smad signaling is required to maintain epigenetic silencing during breast cancer progression. Cancer Res., 70, 968-978.
41. Zhang,Q., Chen,L., Helfand,B.T., Jang,T.L., Sharma,V., Kozlowski,J., Kuzel,T.M., Zhu,L.J., Yang,X.J., Javonovic,B. et al. (2011) TGF-regulates DNA methyltransferase expression in prostate cancer, correlates with aggressive capabilities, and predicts disease recurrence. PLoS One, 6, e25168.
42. Janda,E., Lehmann,K., Killisch,I., Jechlinger,M., Herzig,M., Downward,J., Beug,H. and Grünert,S. (2002) Ras and TGFcooperatively regulate epithelial cell plasticity and metastasis: dissection of Ras signaling pathways. J. Cell Biol., 156, 299-313.
43. Fusco,A. and Fedele,M. (2007) Roles of HMGA proteins in cancer. Nat. Rev. Cancer, 7, 899-910.
44. Kishi,Y., Fujii,Y., Hirabayashi,Y. and Gotoh,Y. (2012) HMGA regulates the global chromatin state and neurogenic potential in neocortical precursor cells. Nat. Neurosci., 15, 1127-1133.
45. Ooi,S.K.T., Qiu,C., Bernstein,E., Li,K., Jia,D., Yang,Z., Erdjument-Bromage,H., Tempst,P., Lin,S.-P., Allis,C.D. et al. (2007) DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature, 448, 714-717.
46. Herold,M., Bartkuhn,M. and Renkawitz,R. (2012) CTCF: insights into insulator function during development. Development, 139, 1045-1057.
47. Yilmaz,M. and Christofori,G. (2010) Mechanisms of motility in metastasizing cells. Mol. Cancer Res., 8, 629-642.
48. Winter,N., Nimzyk,R., Bösche,C., Meyer,A. and Bullerdiek,J. (2011) Chromatin immunoprecipitation to analyze DNA binding sites of HMGA2. PLoS One, 6, e18837.
49. Zha,L., Wang,Z., Tang,W., Zhang,N., Liao,G. and Huang,Z. (2012) Genome-wide analysis of HMGA2 transcription factor binding sites by ChIP on chip in gastric carcinoma cells. Mol. Cell. Biochem., 364, 243-251.