Oncogenic RAS alters the global and gene-specific histone modification pattern during epithelial-mesenchymal transition in colorectal carcinoma cells

International Journal of Biochemistry and Cell Biology

Volumn 42, Issue 6, 2010, Pages 911-920

  Mazón Peláez, Ignacio ^a   Kalogeropoulou, Margarita ^a   Ferraro, Angelo ^a   Voulgari, Angeliki ^a   Pankotai, Tibor ^b   Boros, Imre ^c   Pintzas, Alexander ^a  

^a INSTITUTE OF BIOLOGY   (Greece)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^c UNIVERSITY OF SZEGED   (Hungary)

Author keywords

Colon cancer; EMT; Histone modifications; MSK1; RAS

Indexed keywords

CYCLIN D1; HISTONE H3; LYSINE; METHYLTRANSFERASE; MITOGEN ACTIVATED PROTEIN KINASE; UVOMORULIN;

ARTICLE; CARCINOMA CELL; CELL LINE; CELL PROLIFERATION; CELL TRANSFORMATION; COLORECTAL CARCINOMA; CONTROLLED STUDY; DNA MODIFICATION; EPIGENETICS; EPITHELIUM CELL; GENE ACTIVITY; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; MALIGNANT TRANSFORMATION; MESENCHYME CELL; ONCOGENE H RAS; PHENOTYPE; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN MODIFICATION; SIGNAL TRANSDUCTION;

CACO-2 CELLS; CADHERINS; CELL TRANSFORMATION, NEOPLASTIC; COLORECTAL NEOPLASMS; CYCLIN D1; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONES; HUMANS; MAP KINASE KINASE KINASES; MESENCHYMAL STEM CELLS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RAS PROTEINS; SIGNAL TRANSDUCTION; TRANSGENES;

EID: 77953809781     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2010.01.024     Document Type: Article

References (57)

1. Albanese C., D'Amico M., Reutens A.T., Fu M., Watanabe G., Lee R.J., et al. Activation of the cyclin D1 gene by the E1A-associated protein p300 through AP-1 inhibits cellular apoptosis. J Biol Chem 1999, 274:34186-34195.
2. Andreolas C., Kalogeropoulou M., Voulgari A., Pintzas A. Fra-1 regulates vimentin during Ha-RAS-induced epithelial-mesenchymal transition in human colon carcinoma cells. Int J Cancer 2008, 122:1745-1756.
3. Bakiri L., Lallemand D., Bossy-Wetzel E., Yaniv M. Cell cycle-dependent variations in c-Jun and JunB phosphorylation: a role in the control of cyclin D1 expression. EMBO J 2000, 19:2056-2068.
4. Barski A., Cuddapah S., Cui K., Roh T.Y., Schones D.E., Wang Z., et al. High-resolution profiling of histone methylations in the human genome. Cell 2007, 129:823-837.
5. Berger S.L. Histone modifications in transcriptional regulation. Curr Opin Genet Dev 2002, 12:142-148.
6. Bolos V., Peinado H., Perez-Moreno M.A., Fraga M.F., Esteller M., Cano A. The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors. J Cell Sci 2003, 116:499-511.
7. Cha T.L., Zhou B.P., Xia W., Wu Y., Yang C.C., Chen C.T., et al. Akt-mediated phosphorylation of EZH2 suppresses methylation of lysine 27 in histone H3. Science 2005, 310:306-310.
8. Chadee D.N., Hendzel M.J., Tylipski C.P., Allis C.D., Bazett-Jones D.P., Wright J.A., et al. Increased Ser-10 phosphorylation of histone H3 in mitogen-stimulated and oncogene-transformed mouse fibroblasts. J Biol Chem 1999, 274:24914-24920.
9. Chen C., Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 1987, 7:2745-2752.
10. Comijn J., Berx G., Vermassen P., Verschueren K., van G.L., Bruyneel E., et al. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol Cell 2001, 7:1267-1278.
11. Conacci-Sorrell M., Simcha I., Ben-Yedidia T., Blechman J., Savagner P., Ben-Ze'ev A. Autoregulation of E-cadherin expression by cadherin-cadherin interactions: the roles of beta-catenin signaling, Slug, and MAPK. J Cell Biol 2003, 163:847-857.
12. Di C.L., Raker V.A., Corsaro M., Fazi F., Fanelli M., Faretta M., et al. Methyltransferase recruitment and DNA hypermethylation of target promoters by an oncogenic transcription factor. Science 2002, 295:1079-1082.
13. Drobic B., Espino P.S., Davie J.R. Mitogen- and stress-activated protein kinase 1 activity and histone h3 phosphorylation in oncogene-transformed mouse fibroblasts. Cancer Res 2004, 64:9076-9079.
14. Dumont N., Wilson M.B., Crawford Y.G., Reynolds P.A., Sigaroudinia M., Tlsty T.D. Sustained induction of epithelial to mesenchymal transition activates DNA methylation of genes silenced in basal-like breast cancers. Proc Natl Acad Sci USA 2008, 105:14867-14872.
15. Dyson M.H., Thomson S., Inagaki M., Goto H., Arthur S.J., Nightingale K., et al. MAP kinase-mediated phosphorylation of distinct pools of histone H3 at S10 or S28 via mitogen- and stress-activated kinase 1/2. J Cell Sci 2005, 118:2247-2259.
16. Edelmann W., Yang K., Umar A., Heyer J., Lau K., Fan K., et al. Mutation in the mismatch repair gene Msh6 causes cancer susceptibility. Cell 1997, 91:467-477.
17. Feinberg A.P., Vogelstein B. Hypomethylation of ras oncogenes in primary human cancers. Biochem Biophys Res Commun 1983, 111:47-54.
18. Fraga M.F., Ballestar E., Villar-Garea A., Boix-Chornet M., Espada J., Schotta G., et al. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat Genet 2005, 37:391-400.
19. Herber B., Truss M., Beato M., Muller R. Inducible regulatory elements in the human cyclin D1 promoter. Oncogene 1994, 9:2105-2107.
20. Hilton T.L., Li Y., Dunphy E.L., Wang E.H. TAF1 histone acetyltransferase activity in Sp1 activation of the cyclin D1 promoter. Mol Cell Biol 2005, 25:4321-4332.
21. Hong S., Cho Y.W., Yu L.R., Yu H., Veenstra T.D., Ge K. Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc Natl Acad Sci USA 2007, 104:18439-18444.
22. Hulit J., Wang C., Li Z., Albanese C., Rao M., Di V.D., et al. Cyclin D1 genetic heterozygosity regulates colonic epithelial cell differentiation and tumor number in ApcMin mice. Mol Cell Biol 2004, 24:7598-7611.
23. Joyce D., Bouzahzah B., Fu M., Albanese C., D'Amico M., Steer J., et al. Integration of Rac-dependent regulation of cyclin D1 transcription through a nuclear factor-kappaB-dependent pathway. J Biol Chem 1999, 274:25245-25249.
24. Kimura H., Tada M., Nakatsuji N., Tada T. Histone code modifications on pluripotential nuclei of reprogrammed somatic cells. Mol Cell Biol 2004, 24:5710-5720.
25. Kirmizis A., Bartley S.M., Farnham P.J. Identification of the polycomb group protein SU(Z)12 as a potential molecular target for human cancer therapy. Mol Cancer Ther 2003, 2:113-121.
26. Kleer C.G., Cao Q., Varambally S., Shen R., Ota I., Tomlins S.A., et al. EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Proc Natl Acad Sci USA 2003, 100:11606-11611.
27. Lee R.J., Albanese C., Stenger R.J., Watanabe G., Inghirami G., Haines G.K., et al. pp60(v-src) induction of cyclin D1 requires collaborative interactions between the extracellular signal-regulated kinase, p38, and Jun kinase pathways. A role for cAMP response element-binding protein and activating transcription factor-2 in pp60(v-src) signaling in breast cancer cells. J Biol Chem 1999, 274:7341-7350.
28. Lo W.S., Trievel R.C., Rojas J.R., Duggan L., Hsu J.Y., Allis C.D., et al. Phosphorylation of serine 10 in histone H3 is functionally linked in vitro and in vivo to Gcn5-mediated acetylation at lysine 14. Mol Cell 2000, 5:917-926.
29. Lombaerts M., van W.T., Philippo K., Dierssen J.W., Zimmerman R.M., Oosting J., et al. 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 2006, 94:661-671.
30. Margueron R., Li G., Sarma K., Blais A., Zavadil J., Woodcock C.L., et al. Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms. Mol Cell 2008, 32:503-518.
31. Martin C., Cao R., Zhang Y. Substrate preferences of the EZH2 histone methyltransferase complex. J. Biol Chem. 2006, 281:8365-8370.
32. Meshorer E., Misteli T. Chromatin in pluripotent embryonic stem cells and differentiation. Nat Rev Mol Cell Biol 2006, 7:540-546.
33. Morel A.P., Lievre M., Thomas C., Hinkal G., Ansieau S., Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One 2008, 3:e2888.
34. Nagata D., Suzuki E., Nishimatsu H., Satonaka H., Goto A., Omata M., et al. Transcriptional activation of the cyclin D1 gene is mediated by multiple cis-elements, including SP1 sites and a cAMP-responsive element in vascular endothelial cells. J Biol Chem 2001, 276:662-669.
35. Nakamura N., Takenaga K. Hypomethylation of the metastasis-associated S100A4 gene correlates with gene activation in human colon adenocarcinoma cell lines. Clin Exp Metastasis 1998, 16:471-479.
36. Oikonomou E., Makrodouli E., Evagelidou M., Joyce T., Probert L., Pintzas A. BRAFV600E efficient transformation and induction of MSI versus KRASG12V induction of senescence markers in human colon cancer cells. Neoplasia 2009, 11:1116-1131.
37. Ozdaĝ H., Teschendorff A.E., Ahmed A.A., Hyland S.J., Blenkiron C., Bobrow L., et al. Differential expression of selected histone modifier genes in human solid cancers. BMC Genomics 2006, 7:90-104.
38. Park H., Im J.Y., Kim J., Choi W.S., Kim H.S. Effects of apicidin, a histone deacetylase inhibitor, on the regulation of apoptosis in H-ras-transformed breast epithelial cells. Int J Mol Med 2008, 21:325-333.
39. Park Y.S., Jin M.Y., Kim Y.J., Yook J.H., Kim B.S., Jang S.J. The global histone modification pattern correlates with cancer recurrence and overall survival in gastric adenocarcinoma. Ann Surg Oncol 2008, 15:1968-1976.
40. Roberts M.L., Drosopoulos K.G., Vasileiou I., Stricker M., Taoufik E., Maercker C., et al. Microarray analysis of the differential transformation mediated by Kirsten and Harvey Ras oncogenes in a human colorectal adenocarcinoma cell line. Int J Cancer 2006, 118:616-627.
41. Sakatani T., Kaneda A., Iacobuzio-Donahue C.A., Carter M.G., de Boom W.S., Okano H., et al. Loss of imprinting of Igf2 alters intestinal maturation and tumorigenesis in mice. Science 2005, 307:1976-1978.
42. Seligson D.B., Horvath S., Shi T., Yu H., Tze S., Grunstein M., et al. Global histone modification patterns predict risk of prostate cancer recurrence. Nature 2005, 435:1262-1266.
43. Shaulian E., Karin M. AP-1 in cell proliferation and survival. Oncogene 2001, 20:2390-2400.
44. Shen Q., Uray I.P., Li Y., Krisko T.I., Strecker T.E., Kim H.T., et al. The AP-1 transcription factor regulates breast cancer cell growth via cyclins and E2F factors. Oncogene 2008, 27:366-377.
45. Soloaga A., Thomson S., Wiggin G.R., Rampersaud N., Dyson M.H., Hazzalin C.A., et al. MSK2 and MSK1 mediate the mitogen- and stress-induced phosphorylation of histone H3 and HMG-14. EMBO J 2003, 22:2788-2797.
46. Spurling C.C., Godman C.A., Noonan E.J., Rasmussen T.P., Rosenberg D.W., Giardina C. HDAC3 overexpression and colon cancer cell proliferation and differentiation. Mol Carcinog 2008, 47:137-147.
47. Suter C.M., Martin D.I., Ward R.L. Hypomethylation of L1 retrotransposons in colorectal cancer and adjacent normal tissue. Int J Colorectal Dis 2004, 19:95-101.
48. Sutter T., Doi S., Carnevale K.A., Arber N., Weinstein I.B. Expression of cyclins D1 and E in human colon adenocarcinomas. J Med 1997, 28:285-309.
49. Thiery J.P., Sleeman J.P. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 2006, 7:131-142.
50. Trivier E., De C.D., Jacquot S., Pannetier S., Zackai E., Young I., et al. Mutations in the kinase Rsk-2 associated with Coffin-Lowry syndrome. Nature 1996, 384:567-570.
51. Varambally S., Dhanasekaran S.M., Zhou M., Barrette T.R., Kumar-Sinha C., Sanda M.G., et al. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 2002, 419:624-629.
52. Voulgari A., Voskou S., Tora L., Davidson I., Sasazuki T., Shirasawa S., et al. TATA box-binding protein-associated factor 12 is important for RAS-induced transformation properties of colorectal cancer cells. Mol Cancer Res 2008, 6:1071-1083.
53. Wang Z., Zang C., Rosenfeld J.A., Schones D.E., Barski A., Cuddapah S., et al. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 2008, 40:897-903.
54. Wei Y., Xia W., Zhang Z., Liu J., Wang H., Adsay N.V., et al. Loss of trimethylation at lysine 27 of histone H3 is a predictor of poor outcome in breast, ovarian, and pancreatic cancers. Mol Carcinog 2008, 47:701-706.
55. Wilson A.J., Byun D.S., Popova N., Murray L.B., L'Italien K., Sowa Y., et al. Histone deacetylase 3 (HDAC3) and other class I HDACs regulate colon cell maturation and p21 expression and are deregulated in human colon cancer. J Biol Chem 2006, 281:13548-13558.
56. Zhang X., Wharton W., Yuan Z., Tsai S.C., Olashaw N., Seto E. Activation of the growth-differentiation factor 11 gene by the histone deacetylase (HDAC) inhibitor trichostatin A and repression by HDAC3. Mol Cell Biol 2004, 24:5106-5118.
57. Zhu P., Huber E., Kiefer F., Gottlicher M. Specific and redundant functions of histone deacetylases in regulation of cell cycle and apoptosis. Cell Cycle 2004, 3:1240-1242.