DNA sequence context as a marker of CpG methylation instability in normal and cancer tissues.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
03 02 2020
Historique:
received: 03 05 2019
accepted: 13 01 2020
entrez: 5 2 2020
pubmed: 6 2 2020
medline: 20 11 2020
Statut: epublish

Résumé

DNA methylation alterations are related to multiple molecular mechanisms. The DNA context of CpG sites plays a crucial role in the maintenance and stability of methylation patterns. The quantitative relationship between DNA composition and DNA methylation has been studied in normal as well as pathological conditions, showing that DNA methylation status is highly dependent on the local sequence context. In this work, we describe this relationship by analyzing the DNA sequence context associated to methylation profiles in both physiological and pathological conditions. In particular, we used DNA motifs to describe methylation stability patterns in normal tissues and aberrant methylation events in cancer lesions. In this manuscript, we show how different groups of DNA sequences can be related to specific epigenetic events, across normal and cancer tissues, and provide a thorough structural and functional characterization of these sequences.

Identifiants

pubmed: 32015379
doi: 10.1038/s41598-020-58331-w
pii: 10.1038/s41598-020-58331-w
pmc: PMC6997448
doi:

Substances chimiques

Genetic Markers 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1721

Références

Szyf, M. Nongenetic inheritance and transgenerational epigenetics. Trends. Mol. Med. Elsevier Ltd. 21, 134–44 (2015).
doi: 10.1016/j.molmed.2014.12.004
Sánchez-Romero, M. A., Cota, I. & Casadesús, J. DNA methylation in bacteria: From the methyl group to the methylome. Curr. Opin. Microbiol. 25, 9–16 (2015).
doi: 10.1016/j.mib.2015.03.004
Boyes, J. & Bird, A. Repression of genes by DNA methylation depends on CpG density and promoter strength: evidence for involvement of a methyl-CpG binding protein. EMBO J. 11, 327–333 (1992).
doi: 10.1002/j.1460-2075.1992.tb05055.x
Baubec, T. & Schübeler, D. Genomic patterns and context specific interpretation of DNA methylation. Curr. Opin. Genet. Dev. 25, 85–92 (2014).
doi: 10.1016/j.gde.2013.11.015
Weber, M. & Schübeler, D. Genomic patterns of DNA methylation: targets and function of an epigenetic mark. Curr. Opin. Cell. Biol. 19, 273–280 (2007).
doi: 10.1016/j.ceb.2007.04.011
Wagner, J. R. et al. The relationship between DNA methylation, genetic and expression inter-individual variation in untransformed human fibroblasts. Genome Biol. 15, R37 (2014).
doi: 10.1186/gb-2014-15-2-r37
Haerter, J. O., Lövkvist, C., Dodd, I. B. & Sneppen, K. Collaboration between CpG sites is needed for stable somatic inheritance of DNA methylation states. Nucleic Acids Res. 42, 2235–2244 (2014).
doi: 10.1093/nar/gkt1235
McCabe, M. T., Brandes, J. C. & Vertino, P. M. Cancer DNA Methylation: Molecular Mechanisms and Clinical Implications. Clin. Cancer Res. 15, 3927–3937 (2009).
doi: 10.1158/1078-0432.CCR-08-2784
Bartlett, T. E.et al. Corruption of the Intra-Gene DNA Methylation Architecture Is a Hallmark of Cancer. PLoS One 8 (2013).
doi: 10.1371/journal.pone.0068285
Hansen, K. D. et al. Increased methylation variation in epigenetic domains across cancer types. Nat. Genet. 43, 768–775 (2011).
doi: 10.1038/ng.865
Ghorbani, M., Themis, M. & Payne, A. Genome wide classification and characterisation of CpG sites in cancer and normal cells. Comput. Biol. Med. 68, 57–66 (2016).
doi: 10.1016/j.compbiomed.2015.09.023
Vaiopoulos, A. G., Athanasoula, K. C. & Papavassiliou, A. G. Epigenetic modifications in colorectal cancer: Molecular insights and therapeutic challenges. Biochim. Biophys. Acta 1842, 971–980 (2014).
doi: 10.1016/j.bbadis.2014.02.006
Cancer Genome Atlas Research Network et al. The Cancer Genome Atlas Pan-Cancer analysis project. Nat. Genet. NIH Public Access; 45, 1113–1120, http://www.ncbi.nlm.nih.gov/pubmed/24071849 (2013).
Calza, S. et al. EPIC-Italy cohorts and multipurpose national surveys. A comparison of some socio-demographic and life-style characteristics. 89, 615–623, http://www.ncbi.nlm.nih.gov/pubmed/14870826 .
Zheng, X., Zhang, N., Wu, H. J. & Wu, H. Estimating and accounting for tumor purity in the analysis of DNA methylation data from cancer studies. Genome Biol. 18, 17, https://doi.org/10.1186/s13059-016-1143-5 (2017).
doi: 10.1186/s13059-016-1143-5 pubmed: 28122605 pmcid: 5267453
Deng, M., Brägelmann, J., Kryukov, I., Saraiva-Agostinho, N. & Perner, S. FirebrowseR: an R client to the Broad Institute’s Firehose Pipeline. Database, http://www.ncbi.nlm.nih.gov/pubmed/28062517 (2017).
Bailey, T. L. DREME: motif discovery in transcription factor ChIP-seq data. Bioinformatics 27, 1653–1659, http://www.ncbi.nlm.nih.gov/pubmed/21543442 (2011).
doi: 10.1093/bioinformatics/btr261
Gupta, S., Stamatoyannopoulos, J. A., Bailey, T. L. & Noble, W. Quantifying similarity between motifs. Genome Biol. 8, R24, https://doi.org/10.1186/gb-2007-8-2-r24 (2007).
doi: 10.1186/gb-2007-8-2-r24 pubmed: 17324271 pmcid: 1852410
Yin, Y. et al. Impact of cytosine methylation on DNA binding specificities of human transcription factors. Science 356, eaaj2239, http://www.ncbi.nlm.nih.gov/pubmed/28473536 (2017).
doi: 10.1126/science.aaj2239
Han, H. et al. TRRUST v2: an expanded reference database of human and mouse transcriptional regulatory interactions. Nucleic Acids Res. 46, D380–386, http://www.ncbi.nlm.nih.gov/pubmed/29087512 (2018).
doi: 10.1093/nar/gkx1013
Iguchi-Ariga, S. M. & Schaffner, W. CpG methylation of the cAMP-responsive enhancer/promoter sequence TGACGTCA abolishes specific factor binding as well as transcriptional activation. Genes Dev. 3, 612–619, http://www.ncbi.nlm.nih.gov/pubmed/2545524 (1989).
Anantharaman, A. et al. Role of Helix-Loop-Helix Proteins during Differentiation of Erythroid Cells. Mol. Cell Biol. 31, 1332–1343, http://www.ncbi.nlm.nih.gov/pubmed/21282467 (2011).
doi: 10.1128/MCB.01186-10
Sawadogo, M., Van Dyke, M. W., Gregor, P. D. & Roeder, R. G. Multiple forms of the human gene-specific transcription factor USF. I. Complete purification and identification of USF from HeLa cell nuclei. J. Biol. Chem. 263, 11985–11993, http://www.ncbi.nlm.nih.gov/pubmed/3403558 (1988).
Sawadogo, M. Multiple forms of the human gene-specific transcription factor USF. II. DNA binding properties and transcriptional activity of the purified HeLa USF. J. Biol. Chem. 263, 11994–12001, http://www.ncbi.nlm.nih.gov/pubmed/3403559 (1988).
Baylin, S. B. DNA methylation and gene silencing in cancer. Nat. Clin. Pract. Oncol. 2, S4–11 (2005).
doi: 10.1038/ncponc0354
Meergans, T., Albig, W. & Doenecke, D. Conserved sequence elements in human main type-H1 histone gene promoters: their role in H1 gene expression. Eur. J. Biochem. 256:436–46, http://www.ncbi.nlm.nih.gov/pubmed/9760185 (1998).
Lam, L. L. et al. Factors underlying variable DNA methylation in a human community cohort. Proc. Natl. Acad. Sci. 109, 17253–17260 (2012).
doi: 10.1073/pnas.1121249109
Jiang, R. et al. Discordance of DNA Methylation Variance Between two Accessible Human Tissues. Sci. Rep. 5, 8257 (2015).
doi: 10.1038/srep08257
Palumbo, D., Affinito, O., Monticelli, A. & Cocozza, S. DNA Methylation variability among individuals is related to CpGs cluster density and evolutionary signatures. BMC Genomics. 19, 229 (2018).
doi: 10.1186/s12864-018-4618-9
Milani, L. et al. DNA methylation for subtype classification and prediction of treatment outcome in patients with childhood acute lymphoblastic leukemia. Child A. Glob. J. Child Res. 115, 1214–1225 (2010).
Feltus, F. A., Lee, E. K., Costello, J. F., Plass, C. & Vertino, P. M. DNA motifs associated with aberrant CpG island methylation. Genomics. 87, 572–579, http://www.ncbi.nlm.nih.gov/pubmed/16487676 (2006).
Seldeen, K. L., McDonald, C. B., Deegan, B. J. & Farooq, A. Single nucleotide variants of the TGACTCA motif modulate energetics and orientation of binding of the Jun-Fos heterodimeric transcription factor. Biochemistry. 48, 1975–1983, http://www.ncbi.nlm.nih.gov/pubmed/19215067 (2009).
Toyota, M. et al. CpG island methylator phenotype in colorectal cancer. Proc. Natl Acad. Sci. USA 96, 8681–8686 (1999).
doi: 10.1073/pnas.96.15.8681
An, C. et al. Prognostic significance of CpG island methylator phenotype and microsatellite instability in gastric carcinoma. Clin. Cancer Res. 11, 656–663 (2005).
pubmed: 15701853
Kusano, M. et al. Genetic, epigenetic, and clinicopathologic features of gastric carcinomas with the CpG island methylator phenotype and an association with Epstein–Barr virus. Cancer. 106, 1467–1479 (2006).
doi: 10.1002/cncr.21789
Oue, N. et al. DNA methylation of multiple genes in gastric carcinoma: association with histological type and CpG island methylator phenotype. Cancer Sci. 94, 901–905 (2003).
doi: 10.1111/j.1349-7006.2003.tb01373.x
Toyota, M. et al. Aberrant methylation in gastric cancer associated with the CpG island methylator phenotype. Cancer Res. 59, 5438–5442 (1999).
pubmed: 10554013
Marsit, C. J. et al. Examination of a CpG island methylator phenotype and implications of methylation profiles in solid tumors. Cancer Res. 66, 10621–10629 (2006).
doi: 10.1158/0008-5472.CAN-06-1687
Shen, L. et al. DNA methylation and environmental exposures in human hepatocellular carcinoma. J. Natl. Cancer Inst. 94, 755–761 (2002).
doi: 10.1093/jnci/94.10.755
Strathdee, G. et al. Primary ovarian carcinomas display multiple methylator phenotypes involving known tumor suppressor genes. Am J. Pathol. 158, 1121–1127 (2001).
doi: 10.1016/S0002-9440(10)64059-X
Sasaki, M. et al. Multiple promoters of catechol-O-methyltransferase gene are selectively inactivated by CpG hypermethylation in endometrial cancer. Cancer Res. 63, 3101–3106 (2003).
pubmed: 12810635
Fang, F. et al. Breast cancer methylomes establish an epigenomic foundation for metastasis. Sci. Transl. Med. 3, 75ra25 (2011).
doi: 10.1126/scitranslmed.3001875
Li, Q. et al. Concordant methylation of the ER and N33 genes in glioblastoma multiforme. Oncogene 16, 3197–3202 (1998).
doi: 10.1038/sj.onc.1201831
Garcia-Manero, G. et al. DNA methylation of multiple promoter-associated CpG islands in adult acute lymphocytic leukemia. Clin. Cancer Res. 8, 2217–2224 (2002).
pubmed: 12114423
Hughes, L. A. E. et al. The CpG island methylator phenotype in colorectal cancer: Progress and problems. Biochimica et Biophysica Acta 1825, 77–85 (2012).
pubmed: 22056543
Nazemalhosseini, M. E., Kuppen, P. J., Aghdaei, H. A. & Zali, M. R. The CpG island methylator phenotype (CIMP) in colorectal cancer. Gastroenterol Hepatol Bed Bench. 6, 120–128 (2013).
Ghule, P. N. et al. p53 checkpoint ablation exacerbates the phenotype of Hinfp dependent histone H4 deficiency. Cell Cycle. 14, 2501–2508, http://www.ncbi.nlm.nih.gov/pubmed/26030398 (2015).
doi: 10.1080/15384101.2015.1049783
Daftari, P., Gavva, N. R. & Shen, C. K. J. Distinction between AP1 and NF-E2 factor-binding at specific chromatin regions in mammalian cells. Oncogene. 18, 5482–5486, http://www.ncbi.nlm.nih.gov/pubmed/10498903 (1999).
Chen, T. K., Smith, L. M., Gebhardt, D. K., Birrer, M. J. & Brown, P. H. Activation and inhibition of the AP-1 complex in human breast cancer cells. Mol. Carcinog. 15, 215–226, http://www.ncbi.nlm.nih.gov/pubmed/8597534 (1996).
Kharman-Biz, A. et al. Expression of activator protein-1 (AP-1) family members in breast cancer. BMC Cancer 13, 441, http://www.ncbi.nlm.nih.gov/pubmed/24073962 (2013).
Ding, X. et al. Epigenetic Activation of AP1 Promotes Squamous Cell Carcinoma Metastasis. Sci. Signal. 6, ra28–ra28, http://www.ncbi.nlm.nih.gov/pubmed/23633675 (2013).
doi: 10.1126/scisignal.2003884
Bertoli, C., Herlihy, A. E., Pennycook, B. R., Kriston-Vizi, J. & de Bruin, R. A. M. Sustained E2F-Dependent Transcription Is a Key Mechanism to Prevent Replication-Stress-Induced DNA Damage. Cell. Rep. 15, 1412–1422, http://www.ncbi.nlm.nih.gov/pubmed/27160911 (2016).
Hsu, J. & Sage, J. Novel functions for the transcription factor E2F4 in development and disease. Cell Cycle. 15, 3183–3190, http://www.ncbi.nlm.nih.gov/pubmed/27753528 (2016).
Bertoli, C., Skotheim, J. M. & de Bruin, R. A. M. Control of cell cycle transcription during G1 and S phases. Nat. Rev. Mol. Cell. Biol. 14, 518–528, http://www.ncbi.nlm.nih.gov/pubmed/23877564 (2013).

Auteurs

Giovanni Scala (G)

Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland.
Department of Biology, University of Naples Federico II, 80126, Naples, Italy.

Antonio Federico (A)

Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland.

Domenico Palumbo (D)

Department of Molecular Medicine and Medical Biotechnology, University of Naples "Federico II", Naples, Italy.

Sergio Cocozza (S)

Department of Molecular Medicine and Medical Biotechnology, University of Naples "Federico II", Naples, Italy.

Dario Greco (D)

Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland. dario.greco@tuni.fi.
BioMediTech Institute, Tampere University, Tampere, Finland. dario.greco@tuni.fi.
Institute of Biotechnology, University of Helsinki, Helsinki, Finland. dario.greco@tuni.fi.

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