Epigenetic reprogramming of cancer cells via targeted DNA methylation

Epigenetics

Volumn 7, Issue 4, 2012, Pages 350-360

  Rivenbark, Ashley G ^a,b   Stolzenburg, Sabine ^a   Beltran, Adriana S ^a,b   Yuan, Xinni ^a,b   Rots, Marianne G ^a   Strahl, Brian D ^a,b   Blancafort, Pilar ^a,b  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Artificial transcription factors (ATFs); Breast cancer; Cancer cell reprogramming; DNA methylation; Epigenetic reprogramming; Epigenetics; Maspin; SOX2; Zinc finger proteins (ZFPs)

Indexed keywords

DNA METHYLTRANSFERASE 3A; MASPIN; MESSENGER RNA; TRANSCRIPTION FACTOR SOX2; ZINC FINGER PROTEIN;

ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER CELL SUM 159; CELL FATE; CELL MATURATION; CELL PROLIFERATION; CELL STRAIN MCF 7; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; GENE CONTROL; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; NUCLEAR REPROGRAMMING; PHENOTYPE; PROTEIN EXPRESSION;

EID: 84860561774     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.19507     Document Type: Article

References (50)

1. Kouzarides T. Chromatin modifications and their function. Cell 2007; 128:693-705; PMID:17320507 http://dx.doi.org/10.1016/j.cell.2007.02.005.
2. Hashimoto H, Vertino PM, Cheng X. Molecular coupling of DNA methylation and histone methylation. Epigenomics 2010; 2:657-69; PMID:21339843; http://dx.doi.org/10.2217/epi.10.44.
3. Klose RJ, Bird AP. Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 2006; 31:89-97; PMID:16403636; http://dx.doi.org/10.1016/j.tibs.2005.12.008.
4. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev 2002; 16:6-21; PMID:11782440; http://dx.doi.org/10.1101/gad.947102.
5. Jurkowska RZ, Jurkowski TP, Jeltsch A. Structure and function of mammalian DNA methyltransferases. Chembiochem 2011; 12:206-22; PMID:21243710; http://dx.doi.org/10.1002/cbic.201000195.
6. Jin B, Li Y, Robertson KD. DNA methylation: superior or subordinate in the epigenetic hierarchy? Genes Cancer 2011; 2:607-17; PMID:21941617; http://dx.doi.org/10.1177/1947601910393957.
7. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 2003; 349:2042-54; PMID:14627790; http://dx.doi.org/10.1056/NEJMra023075.
8. Momparler RL. Cancer epigenetics. Oncogene 2003; 22:6479-83; PMID:14528271; http://dx.doi.org/10.1038/sj.onc.1206774.
9. Jones PA, Laird PW. Cancer epigenetics comes of age. Nat Genet 1999; 21:163-7; PMID:9988266; http://dx.doi.org/10.1038/5947.
10. Campbell TN, Choy FY. RNA interference: past, present and future. Curr Issues Mol Biol 2005; 7:1-6; PMID:15580776.
11. Kim VN. RNA interference in functional genomics and medicine. J Korean Med Sci 2003; 18:309-18; PMID:12808314.
12. Blancafort P, Segal DJ, Barbas CF, 3rd. Designing transcription factor architectures for drug discovery. Mol Pharmacol 2004; 66:1361-71; PMID:15340042; http://dx.doi.org/10.1124/mol.104.002758.
13. Pavletich NP, Pabo CO. Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A. Science 1991; 252:809-17; PMID:2028256; http://dx.doi.org/10.1126/science.2028256
14. Rebar EJ, Pabo CO. Zinc finger phage: affinity selection of fingers with new DNA-binding specificities. Science 1994; 263:671-3; PMID:8303274; http://dx.doi.org/10.1126/science.8303274.
15. Choo Y, Klug A. Selection of DNA binding sites for zinc fingers using rationally randomized DNA reveals coded interactions. Proc Natl Acad Sci USA 1994; 91:11168-72; PMID:7972028; http://dx.doi.org/10.1073/pnas.91.23.11168.
16. Jamieson AC, Kim SH, Wells JA. In vitro selection of zinc fingers with altered DNA-binding specificity. Biochemistry 1994; 33:5689-95; PMID:8180194; http://dx.doi.org/10.1021/bi00185a004.
17. Segal DJ, Dreier B, Beerli RR, Barbas CF, 3rd. Toward controlling gene expression at will: selection and design of zinc finger domains recognizing each of the 5'-GNN-3' DNA target sequences. Proc Natl Acad Sci USA 1999; 96:2758-63; PMID:10077584; http://dx.doi.org/10.1073/pnas.96.6.2758.
18. Dreier B, Segal DJ, Barbas CF, 3rd. Insights into the molecular recognition of the 5'-GNN-3' family of DNA sequences by zinc finger domains. J Mol Biol 2000; 303:489-502; PMID:11054286; http://dx.doi.org/10.1006/jmbi.2000.4133.
19. Dreier B, Beerli RR, Segal DJ, Flippin JD, Barbas CF, 3rd. Development of zinc finger domains for recognition of the 5'-ANN-3' family of DNA sequences and their use in the construction of artificial transcription factors. J Biol Chem 2001; 276:29466-78; PMID:11340073; http://dx.doi.org/10.1074/jbc.M102604200.
20. Dreier B, Fuller RP, Segal DJ, Lund CV, Blancafort P, Huber A, et al. Development of zinc finger domains for recognition of the 5'-CNN-3' family DNA sequences and their use in the construction of artificial transcription factors. J Biol Chem 2005; 280:35588-97; PMID:16107335; http://dx.doi.org/10.1074/jbc.M506654200.
21. Beerli RR, Segal DJ, Dreier B, Barbas CF, 3rd. Toward controlling gene expression at will: specific regulation of the erbB-2/HER-2 promoter by using polydactyl zinc finger proteins constructed from modular building blocks. Proc Natl Acad Sci USA 1998; 95:14628-33; PMID:9843940; http://dx.doi.org/10.1073/pnas.95.25.14628
22. Segal DJ, Beerli RR, Blancafort P, Dreier B, Effertz K, Huber A, et al. Evaluation of a modular strategy for the construction of novel polydactyl zinc finger DNA-binding proteins. Biochemistry 2003; 42:2137-48; PMID:12590603; http://dx.doi.org/10.1021/bi026806o.
23. Tan S, Guschin D, Davalos A, Lee YL, Snowden AW, Jouvenot Y, et al. Zinc-finger protein-targeted gene regulation: genomewide single-gene specificity. Proc Natl Acad Sci USA 2003; 100:11997-2002; PMID:14514889; http://dx.doi.org/10.1073/pnas.2035056100.
24. Isalan M, Klug A, Choo Y. A rapid, generally applicable method to engineer zinc fingers illustrated by targeting the HIV-1 promoter. Nat Biotechnol 2001; 19:656-60; PMID:11433278; http://dx.doi.org/10.1038/90264.
25. Domann FE, Rice JC, Hendrix MJ, Futscher BW. Epigenetic silencing of maspin gene expression in human breast cancers. Int J Cancer 2000; 85:805-10; PMID:10709100; http://dx.doi.org/10.1002/(SICI)1097-0215(20000315)85:6805::AIDIJC123.0.CO;2-5.
26. Futscher BW, Oshiro MM, Wozniak RJ, Holtan N, Hanigan CL, Duan H, et al. Role for DNA methylation in the control of cell type specific maspin expression. Nat Genet 2002; 31:175-9; PMID:12021783; http://dx.doi.org/10.1038/ng886.
27. Sikorska M, Sandhu JK, Deb-Rinker P, Jezierski A, Leblanc J, Charlebois C, et al. Epigenetic modifications of SOX2 enhancers, SRR1 and SRR2, correlate with in vitro neural differentiation. J Neurosci Res 2008; 86:1680-93; PMID:18293417; http://dx.doi.org/10.1002/jnr.21635.
28. Zhang M, Shi Y, Magit D, Furth PA, Sager R. Reduced mammary tumor progression in WAP-TAg/WAPmaspin bitransgenic mice. Oncogene 2000; 19:6053-8; PMID:11146557; http://dx.doi.org/10.1038/sj.onc.1204006.
29. Shi HY, Liang R, Templeton NS, Zhang M. Inhibition of breast tumor progression by systemic delivery of the maspin gene in a syngeneic tumor model. Mol Ther 2002; 5:755-61; PMID:12027560; http://dx.doi.org/10.1006/mthe.2002.0602.
30. Cher ML, Biliran HR Jr, Bhagat S, Meng Y, Che M, Lockett J, et al. Maspin expression inhibits osteolysis, tumor growth and angiogenesis in a model of prostate cancer bone metastasis. Proc Natl Acad Sci USA 2003; 100:7847-52; PMID:12788977; http://dx.doi.org/10.1073/pnas.1331360100.
31. Watanabe M, Nasu Y, Kashiwakura Y, Kusumi N, Tamayose K, Nagai A, et al. Adeno-associated virus 2-mediated intratumoral prostate cancer gene therapy: long-term maspin expression efficiently suppresses tumor growth. Hum Gene Ther 2005; 16:699-710; PMID:15960601; http://dx.doi.org/10.1089/hum.2005.16.699.
32. Chen Y, Shi L, Zhang L, Li R, Liang J, Yu W, et al. The molecular mechanism governing the oncogenic potential of SOX2 in breast cancer. J Biol Chem 2008; 283:17969-78; PMID:18456656; http://dx.doi.org/10.1074/jbc.M802917200.
33. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 2008; 40:499-507; PMID:18443585; http://dx.doi.org/10.1038/ng.127.
34. Beltran A, Parikh S, Liu Y, Cuevas BD, Johnson GL, Futscher BW, et al. Re-activation of a dormant tumor suppressor gene maspin by designed transcription factors. Oncogene 2007; 26:2791-8; PMID:17057734; http://dx.doi.org/10.1038/sj.onc.1210072.
35. Li F, Papworth M, Minczuk M, Rohde C, Zhang Y, Ragozin S, et al. Chimeric DNA methyltransferases target DNA methylation to specific DNA sequences and repress expression of target genes. Nucleic Acids Res 2007; 35:100-12; PMID:17151075; http://dx.doi.org/10.1093/nar/gkl1035.
36. Bostick M, Kim JK, Estève PO, Clark A, Pradhan S, Jacobsen SE. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 2007; 317:1760-4; PMID:17673620; http://dx.doi.org/10.1126/science.1147939.
37. Sharif J, Muto M, Takebayashi S, Suetake I, Iwamatsu A, Endo TA, et al. The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 2007; 450:908-12; PMID:17994007; http://dx.doi.org/10.1038/nature06397.
38. Lengerke C, Fehm T, Kurth R, Neubauer H, Scheble V, Müller F, et al. Expression of the embryonic stem cell marker SOX2 in early-stage breast carcinoma. BMC Cancer 2011; 11:42; PMID:21276239; http://dx.doi.org/10.1186/1471-2407-11-42
39. Groner AC, Meylan S, Ciuffi A, Zangger N, Ambrosini G, Dénervaud N, et al. KRAB-zinc finger proteins and KAP1 can mediate long-range transcriptional repression through heterochromatin spreading. PLoS Genet 2010; 6:1000869; PMID:20221260; http://dx.doi.org/10.1371/journal.pgen.1000869.
40. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 1998; 393:386-9; PMID:9620804; http://dx.doi.org/10.1038/30764.
41. Blancafort P, Beltran AS. Rational design, selection and specificity of artificial transcription factors (ATFs): the influence of chromatin in target gene regulation. Comb Chem High Throughput Screen 2008; 11:146-58; PMID:18336208; http://dx.doi.org/10.2174/138620708783744453.
42. Margolin JF, Friedman JR, Meyer WK, Vissing H, Thiesen HJ, Rauscher FJ, 3rd. Krüppel-associated boxes are potent transcriptional repression domains. Proc Natl Acad Sci USA 1994; 91:4509-13; PMID:8183939; http://dx.doi.org/10.1073/pnas.91.10.4509.
43. Beltran AS, Sun X, Lizardi PM, Blancafort P. Reprogramming epigenetic silencing: artificial transcription factors synergize with chromatin remodeling drugs to reactivate the tumor suppressor mammary serine protease inhibitor. Mol Cancer Ther 2008; 7:1080-90; PMID:18483297; http://dx.doi.org/10.1158/1535-7163.MCT-07-0526.
44. Beltran AS, Blancafort P. Reactivation of MASPIN in non-small cell lung carcinoma (NSCLC) cells by artificial transcription factors (ATFs). Epigenetics 2011; 6:224-35; PMID:20948306; http://dx.doi.org/10.4161/epi.6.2.13700.
45. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126:663-76; PMID:16904174; http://dx.doi.org/10.1016/j.cell.2006.07.024.
46. Takahashi K, Okita K, Nakagawa M, Yamanaka S. Induction of pluripotent stem cells from fibroblast cultures. Nat Protoc 2007; 2:3081-9; PMID:18079707; http://dx.doi.org/10.1038/nprot.2007.418.
47. Liu X, Constantinescu SN, Sun Y, Bogan JS, Hirsch D, Weinberg RA, et al. Generation of mammalian cells stably expressing multiple genes at predetermined levels. Anal Biochem 2000; 280:20-8; PMID:10805516; http://dx.doi.org/10.1006/abio.2000.4478.
48. Grunau C, Clark SJ, Rosenthal A. Bisulfite genomic sequencing: systematic investigation of critical experimental parameters. Nucleic Acids Res 2001; 29:65-5; PMID:11433041; http://dx.doi.org/10.1093/nar/29.13.e65.
49. Rivenbark AG, Jones WD, Risher JD, Coleman WB. DNA methylation-dependent epigenetic regulation of gene expression in MCF-7 breast cancer cells. Epigenetics 2006; 1:32-44; PMID:17998816; http://dx.doi.org/10.4161/epi.1.1.2358.
50. Roll JD, Rivenbark AG, Jones WD, Coleman WB. DNMT3b overexpression contributes to a hypermethylator phenotype in human breast cancer cell lines. Mol Cancer 2008; 7:15; PMID:18221536; http://dx.doi.org/10.1186/1476-4598-7-15.