Aberrant de novo methylation of the p16INK4A CpG island is initiated post gene silencing in association with chromatin remodelling and mimics nucleosome positioning

Human Molecular Genetics

Volumn 18, Issue 16, 2009, Pages 3098-3109

  Hinshelwood, Rebecca A ^a   Melki, John R ^b   Huschtscha, Lily I ^c   Paul, Cheryl ^a   Song, Jenny Z ^a   Stirzaker, Clare ^a   Reddel, Roger R ^c,d   Clark, Susan J ^a  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b Human Genetic Signatures   (Australia)

^c CHILDREN'S MEDICAL RESEARCH INSTITUTE   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; GENOMIC DNA; HISTONE; HISTONE H3;

ACETYLATION; ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CELL SELECTION; CELLULAR DISTRIBUTION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DNA MODIFICATION; GENE LOCATION; GENE REPRESSION; GENE SILENCING; GENETIC ASSOCIATION; GENETIC EPIGENESIS; HUMAN; HUMAN CELL; HUMAN TISSUE; NUCLEOSOME; PRIORITY JOURNAL;

ACETYLATION; BREAST NEOPLASMS; CELL LINE, TUMOR; CELLS, CULTURED; CHROMATIN ASSEMBLY AND DISASSEMBLY; CPG ISLANDS; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DNA METHYLATION; EPIGENESIS, GENETIC; EPITHELIAL CELLS; FEMALE; GENE SILENCING; HISTONES; HUMANS; METHYLATION; NUCLEOSOMES;

EID: 68049104358     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddp251     Document Type: Article

References (50)

1. Kornberg, R.D. (1974) Chromatin structure: A repeating unit of histones and DNA. Science, 184, 868-871.
2. Schones, D.E., Cui, K., Cuddapah, S., Roh, T.Y., Barski, A., Wang, Z., Wei, G. and Zhao, K. (2008) Dynamic regulation of nucleosome positioning in the human genome. Cell, 132, 887-898.
3. Li, B., Carey, M. and Workman, J.L. (2007) The role of chromatin during transcription. Cell, 128, 707-719.
4. Baylin, S.B., Esteller, M., Rountree, M.R., Bachman, K.E., Schuebel, K. and Herman, J.G. (2001) Aberrant patterns of DNA methylation, chromatin formation and gene expression in cancer. Hum. Mol. Genet., 10 687-692.
5. Baylin, S.B. (2005) DNA methylation and gene silencing in cancer. Nat. Clin. Pract. Oncol., 2 (Suppl 1.), S4-S11.
6. Jones, P.A. (2005) Overview of cancer epigenetics. Semin. Hematol. 42, S3-S8.
7. Gal-Yam, E.N., Saito, Y., Egger, G. and Jones, P.A. (2008) Cancer epigenetics: Modifications, screening, and therapy. Annu. Rev. Med. 59, 267-280.
8. Gardiner-Garden, M. and Frommer, M. (1987) CpG islands in vertebrate genomes. J. Mol. Biol., 196, 261-282.
9. Bird, A.P. (1986) CpG-rich islands and the function of DNA methylation. Nature, 321, 209-213.
10. Wong, D.J., Foster, S.A., Galloway, D.A. and Reid, B.J. (1999) Progressive region-specific de novo methylation of the p16 CpG island in primary human mammary epithelial cell strains during escape from M(0) growth arrest. Mol. Cell. Biol., 19, 5642-5651.
11. Clark, S.J. and Melki, J. (2002) DNA methylation and gene silencing in cancer: Which is the guilty party? Oncogene, 21, 5380-5387.
12. Sherr, C.J. (2001) The ink4a/arf network in tumour suppression. Nat. Rev. Mol. Cell. Biol., 2, 731-737.
13. Rocco, J.W. and Sidransky, D. (2001) p16(MTS-1/CDKN2/INK4a) in cancer progression. Exp. Cell. Res., 264, 42-55.
14. Herman, J.G. (1999) p16(INK4): Involvement early and often in gastrointestinal malignancies. Gastroenterology, 116, 483-485.
15. Belinsky, S.A., Nikula, K.J., Palmisano, W.A., Michels, R., Saccomanno, G., Gabrielson, E., Baylin, S.B. and Herman, J.G. (1998) Aberrant methylation of p16(INK4a) is an early event in lung cancer and a potential biomarker for early diagnosis. Proc. Natl Acad. Sci. USA 95, 11891-11896.
16. Nuovo, G.J., Plaia, T.W., Belinsky, S.A., Baylin, S.B. and Herman, J.G. (1999) In situ detection of the hypermethylation-induced inactivation of the p16 gene as an early event in oncogenesis. Proc. Natl Acad. Sci. USA, 96, 12754-12759.
17. Noble, J.R., Rogan, E.M., Neumann, A.A., Maclean, K., Bryan, T.M. and Reddel, R.R. (1996) Association of extended in vitro proliferative potential with loss of p16INK4 expression. Oncogene, 13, 1259-1268.
18. Foster, S.A., Wong, D.J., Barrett, M.T. and Galloway, D.A. (1998) Inactivation of p16 in human mammary epithelial cells by CpG island methylation. Mol. Cell. Biol., 18, 1793-1801.
19. Huschtscha, L.I., Noble, J.R., Neumann, A.A., Moy, E.L., Barry, P., Melki, J.R., Clark, S.J. and Reddel, R.R. (1998) Loss of p16INK4 expression by methylation is associated with lifespan extension of human mammary epithelial cells. Cancer Res., 58, 3508-3512.
20. Brenner, A.J., Stampfer, M.R. and Aldaz, C.M. (1998) Increased p16 expression with first senescence arrest in human mammary epithelial cells and extended growth capacity with p16 inactivation. Oncogene 17, 199-205.
21. Romanov, S.R., Kozakiewicz, B.K., Holst, C.R., Stampfer, M.R., Haupt, L.M. and Tlsty, T.D. (2001) Normal human mammary epithelial cells spontaneously escape senescence and acquire genomic changes. Nature 409, 633-637.
22. Holst, C.R., Nuovo, G.J., Esteller, M., Chew, K., Baylin, S.B., Herman, J.G. and Tlsty, T.D. (2003) Methylation of p16(INK4a) promoters occurs in vivo in histologically normal human mammary epithelia. Cancer Res. 63, 1596-1601.
23. Crawford, Y.G., Gauthier, M.L., Joubel, A., Mantei, K., Kozakiewicz, K., Afshari, C.A. and Tlsty, T.D. (2004) Histologically normal human mammary epithelia with silenced p16(INK4a) overexpress COX-2, promoting a premalignant program. Cancer Cell, 5, 263-273.
24. Hammond, S.L., Ham, R.G. and Stampfer, M.R. (1984) Serum-free growth of human mammary epithelial cells: Rapid clonal growth in defined medium and extended serial passage with pituitary extract. Proc. Natl Acad. Sci. USA, 81, 5435-5439.
25. Stampfer, M.R. and Bartley, J.C. (1985) Induction of transformation and continuous cell lines from normal human mammary epithelial cells after exposure to benzo[a]pyrene. Proc. Natl Acad. Sci. USA, 82, 2394-2398.
26. Sandhu, C., Donovan, J., Bhattacharya, N., Stampfer, M., Worland, P. and Slingerland, J. (2000) Reduction of Cdc25A contributes to cyclin E1-Cdk2 inhibition at senescence in human mammary epithelial cells. Oncogene 19, 5314-5323.
27. Stampfer, M.R., Yaswen, P., Casto, B.C. and Schuler, C.F. (1992) Transformation of Human Epithelial Cells: Moleculare and Oncogene Mechanisms. CRC Press Inc., Boca Raton.
28. Tlsty, T.D., Romanov, S.R., Kozakiewicz, B.K., Holst, C.R., Haupt, L.M. and Crawford, Y.G. (2001) Loss of chromosomal integrity in human mammary epithelial cells subsequent to escape from senescence. J. Mammary Gland Biol. Neoplasia, 6, 235-243.
29. Tlsty, T.D., Crawford, Y.G., Holst, C.R., Fordyce, C.A., Zhang, J., McDermott, K., Kozakiewicz, K. and Gauthier, M.L. (2004) Genetic and epigenetic changes in mammary epithelial cells may mimic early events in carcinogenesis. J. Mammary Gland Biol. Neoplasia, 9, 263-274.
30. Hinshelwood, R.A., Huschtscha, L.I., Melki, J., Stirzaker, C., Abdipranoto, A., Vissel, B., Ravasi, T., Wells, C.A., Hume, D.A., Reddel, R.R. et al. (2007) Concordant epigenetic silencing of transforming growth factor-beta signaling pathway genes occurs early in breast carcinogenesis. Cancer Res., 67, 11517-11527.
31. Fatemi, M., Pao, M.M., Jeong, S., Gal-Yam, E.N., Egger, G., Weisenberger, D.J. and Jones, P.A. (2005) Footprinting of mammalian promoters: Use of a CpG DNA methyltransferase revealing nucleosome positions at a single molecule level. Nucleic Acids Res., 33 e176.
32. Kladde, M.P. and Simpson, R.T. (1996) Chromatin structure mapping in vivo using methyltransferases. Methods Enzymol., 274, 214-233.
33. Hinshelwood, R.A. and Clark, S.J. (2008) Breast cancer epigenetics: normal human mammary epithelial cells as a model system. J. Mol. Med.
34. Baylin, S. and Bestor, T.H. (2002) Altered methylation patterns in cancer cell genomes: Cause or consequence? Cancer Cell, 1, 299-305.
35. Bachman, K.E., Park, B.H., Rhee, I., Rajagopalan, H., Herman, J.G., Baylin, S.B., Kinzler, K.W. and Vogelstein, B. (2003) Histone modifications and silencing prior to DNA methylation of a tumor suppressor gene. Cancer Cell, 3, 89-95.
36. Stein, R., Razin, A. and Cedar, H. (1982) In vitro methylation of the hamster adenine phosphoribosyltransferase gene inhibits its expression in mouse L cells. Proc. Natl Acad. Sci. USA, 79, 3418-3422.
37. Busslinger, M., Hurst, J. and Flavell, R.A. (1983) DNA methylation and the regulation of globin gene expression. Cell, 34, 197-206.
38. Yisraeli, J., Frank, D., Razin, A. and Cedar, H. (1988) Effect of in vitro DNA methylation on beta-globin gene expression. Proc. Natl Acad. Sci. USA, 85, 4638-4642.
39. Stirzaker, C., Song, J.Z., Davidson, B. and Clark, S.J. (2004) Transcriptional gene silencing promotes DNA hypermethylation through a sequential change in chromatin modifications in cancer cells. Cancer Res., 64, 3871-3877.
40. Gal-Yam, E.N., Jeong, S., Tanay, A., Egger, G., Lee, A.S. and Jones, P.A. (2006) Constitutive nucleosome depletion and ordered factor assembly at the GRP78 promoter revealed by single molecule footprinting. PLoS. Genet., 2, e160.
41. Mito, Y., Henikoff, J.G. and Henikoff, S. (2005) Genome-scale profiling of histone H3.3 replacement patterns. Nat. Genet., 37, 1090-1097.
42. Lin, J.C., Jeong, S., Liang, G., Takai, D., Fatemi, M., Tsai, Y.C., Egger, G., Gal-Yam, E.N. and Jones, P.A. (2007) Role of nucleosomal occupancy in the epigenetic silencing of the MLH1 CpG island. Cancer Cell, 12, 432-444.
43. Ohm, J.E., McGarvey, K.M., Yu, X., Cheng, L., Schuebel, K.E., Cope, L., Mohammad, H.P., Chen, W., Daniel, V.C., Yu, W. et al. (2007) A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat. Genet., 39, 237-242.
44. Widschwendter, M., Fiegl, H., Egle, D., Mueller-Holzner, E., Spizzo, G., Marth, C., Weisenberger, D.J., Campan, M., Young, J., Jacobs, I. et al. (2007) Epigenetic stem cell signature in cancer. Nat. Genet. 39, 157-158.
45. Huschtscha, L.I., Neumann, A.A., Noble, J.R. and Reddel, R.R. (2001) Effects of simian virus 40 T-antigens on normal human mammary epithelial cells reveal evidence for spontaneous alterations in addition to loss of p16(INK4a) expression. Exp. Cell. Res., 265, 125-134.
46. Millar, D.S., Warnecke, P.M., Melki, J.R. and Clark, S.J. (2002) Methylation sequencing from limiting DNA: Embryonic, fixed, and microdissected cells. Methods, 27, 108-113.
47. Micke, P., Ostman, A., Lundeberg, J. and Ponten, F. (2005) Laser-assisted cell microdissection using the PALM system. Methods Mol. Biol., 293, 151-166.
48. Clark, S.J., Harrison, J., Paul, C.L. and Frommer, M. (1994) High sensitivity mapping of methylated cytosines. Nucleic Acids Res., 22, 2990-2997.
49. Clark, S.J., Statham, A., Stirzaker, C., Molloy, P.L. and Frommer, M. (2006) DNA methylation: Bisulphite modification and analysis. Nat. Protoc., 1, 2353-2364.
50. Frigola, J., Song, J., Stirzaker, C., Hinshelwood, R.A., Peinado, M.A. and Clark, S.J. (2006) Epigenetic remodeling in colorectal cancer results in coordinate gene suppression across an entire chromosome band. Nat. Genet., 38, 540-549.