Immortalization of T-Cells Is Accompanied by Gradual Changes in CpG Methylation Resulting in a Profile Resembling a Subset of T-Cell Leukemias

Neoplasia (United States)

Volumn 16, Issue 7, 2014, Pages 606-615

  Degerman, Sofie ^a   Landfors, Mattias ^a   Siwicki, Jan Konrad ^b   Revie, John ^d   Borssén, Magnus ^a   Evelönn, Emma ^a   Forestier, Erik ^a   Chrzanowska, Krystyna H ^c   Rydén, Patrik ^a   Keith, W Nicol ^d   Roos, Göran ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b INSTITUTE OF ONCOLOGY   (Poland)

^c CHILDREN'S MEMORIAL HEALTH INSTITUTE   (Poland)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84928759013     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1016/j.neo.2014.07.001     Document Type: Article

References (35)

1. Fridman AL, Tainsky MA Critical pathways in cellular senescence and immortalization revealed by gene expression profiling. Oncogene 2008, 27:5975-5987.
2. Benanti JA, Wang ML, Myers HE, Robinson KL, Grandori C, Galloway DA Epigenetic down-regulation of ARF expression is a selection step in immortalization of human fibroblasts by c-Myc. Mol Cancer Res 2007, 5:1181-1189.
3. Novak P, Jensen TJ, Garbe JC, Stampfer MR, Futscher BW Stepwise DNA methylation changes are linked to escape from defined proliferation barriers and mammary epithelial cell immortalization. Cancer Res 2009, 69:5251-5258.
4. Takai D, Jones PA Comprehensive analysis of CpG islands in human chromosomes 21 and 22. Proc Natl Acad Sci U S A 2002, 99:3740-3745.
5. Liu C, Fang X, Ge Z, Jalink M, Kyo S, Bjorkholm M, Gruber A, Sjöberg J, Xu D The telomerase reverse transcriptase (hTERT) gene is a direct target of the histone methyltransferase SMYD3. Cancer Res 2007, 67:2626-2631.
6. Renaud S, Loukinov D, Abdullaev Z, Guilleret I, Bosman FT, Lobanenkov V, Benhattar J Dual role of DNA methylation inside and outside of CTCF-binding regions in the transcriptional regulation of the telomerase hTERT gene. Nucleic Acids Res 2007, 35:1245-1256.
7. Zinn RL, Pruitt K, Eguchi S, Baylin SB, Herman JG hTERT is expressed in cancer cell lines despite promoter DNA methylation by preservation of unmethylated DNA and active chromatin around the transcription start site. Cancer Res 2007, 67:194-201.
8. Degerman S, Siwicki JK, Osterman P, Lafferty-Whyte K, Nicol Keith W, Roos G Telomerase upregulation is a postcrisis event during senescence bypass and immortalization of two Nijmegen breakage syndrome T cell cultures. Aging Cell 2010, 9:220-235.
9. McCabe MT, Brandes JC, Vertino PM Cancer DNA methylation: molecular mechanisms and clinical implications. Clin Cancer Res 2009, 15:3927-3937.
10. Boultwood J, Wainscoat JS Gene silencing by DNA methylation in haematological malignancies. Br J Haematol 2007, 138:3-11.
11. Esteller M Epigenetics in cancer. N Engl J Med 2008, 358:1148-1159.
12. Costello JF, Frühwald MC, Smiraglia DJ, Rush LJ, Robertson GP, Gao X, Wright FA, Feramisco JD, Peltomaki P, Lang JC, et al. Aberrant CpG-island methylation has non-random and tumour-type-specific patterns. Nat Genet 2000, 24:132-138.
13. Ehrich M, Turner J, Gibbs P, Lipton L, Giovanneti M, Cantor C, van den Boom D Cytosine methylation profiling of cancer cell lines. Proc Natl Acad Sci U S A 2008, 105:4844-4849.
14. Martin-Subero JI, Ammerpohl O, Bibikova M, Wickham-Garcia E, Agirre X, Alvarez S, Bruggemann M, Bug S, Calasanz MJ, Deckert M, et al. A comprehensive microarray-based DNA methylation study of 367 hematological neoplasms. PLoS One 2009, 4:e6986.
15. Teschendorff AE, Menon U, Gentry-Maharaj A, Ramus SJ, Gayther SA, Apostolidou S, Jones A, Lechner M, Beck S, Jacobs IJ, et al. An epigenetic signature in peripheral blood predicts active ovarian cancer. PLoS One 2009, 4:e8274.
16. Shao G, Balajee AS, Hei TK, Zhao Y p16INK4a downregulation is involved in immortalization of primary human prostate epithelial cells induced by telomerase. Mol Carcinog 2008, 47:775-783.
17. Tzatsos A, Pfau R, Kampranis SC, Tsichlis PN Ndy1/KDM2B immortalizes mouse embryonic fibroblasts by repressing the Ink4a/Arf locus. Proc Natl Acad Sci U S A 2009, 106:2641-2646.
18. Koch CM, Joussen S, Schellenberg A, Lin Q, Zenke M, Wagner W Monitoring of cellular senescence by DNA-methylation at specific CpG sites. Aging Cell 2012, 11:366-369.
19. Koch CM, Reck K, Shao K, Lin Q, Joussen S, Ziegler P, Walenda G, Drescher W, Opalka B, May T, et al. Pluripotent stem cells escape from senescence-associated DNA methylation changes. Genome Res 2013, 23:248-259.
20. Bork S, Pfister S, Witt H, Horn P, Korn B, Ho AD, Wagner W DNA methylation pattern changes upon long-term culture and aging of human mesenchymal stromal cells. Aging Cell 2010, 9:54-63.
21. Grafodatskaya D, Choufani S, Ferreira JC, Butcher DT, Lou Y, Zhao C, Scherer SW, Weksberg R EBV transformation and cell culturing destabilizes DNA methylation in human lymphoblastoid cell lines. Genomics 2010, 95:73-83.
22. Zhang Z, Liu J, Kaur M, Krantz ID Characterization of DNA methylation and its association with other biological systems in lymphoblastoid cell lines. Genomics 2012, 99:209-219.
23. Siwicki JK, Degerman S, Chrzanowska KH, Roos G Telomere maintenance and cell cycle regulation in spontaneously immortalized T-cell lines from Nijmegen breakage syndrome patients. Exp Cell Res 2003, 287:178-189.
24. INK4a overexpression, normal pRb/p53, and upregulation of cyclins E or D2. Exp Gerontol 2000, 35:375-388.
25. Borssén M, Palmqvist L, Karrman K, Abrahamsson J, Behrendtz M, Heldrup J, Forestier E, Roos G, Degerman S Promoter DNA methylation pattern identifies prognostic subgroups in childhood T-cell acute lymphoblastic leukemia. PLoS One 2013, 8:e65373.
26. Marabita F, Almgren M, Lindholm ME, Ruhrmann S, Fagerström-Billai F, Jagodic M, Sundberg CJ, Ekstrom TJ, Teschendorff AE, Tegnér J, et al. An evaluation of analysis pipelines for DNA methylation profiling using the Illumina HumanMethylation450 BeadChip platform. Epigenetics 2013, 8:333-346.
27. Teschendorff AE, Marabita F, Lechner M, Bartlett T, Tegner J, Gomez-Cabrero D, Beck S A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450k DNA methylation data. Bioinformatics 2013, 29:189-196.
28. Schmittgen TD, Livak KJ Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008, 3:1101-1108.
29. Ward JH Hierarchical grouping to optimize an objective function. J Am Stat Assoc 1963, 58:236-244.
30. Cancer Genome Atlas Research Network Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N Engl J Med 2013, 368:2059-2074.
31. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, Chevalier B, Johnstone SE, Cole MF, Isono K, et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 2006, 125:301-313.
32. Garbe JC, Bhattacharya S, Merchant B, Bassett E, Swisshelm K, Feiler HS, Wyrobek AJ, Stampfer MR Molecular distinctions between stasis and telomere attrition senescence barriers shown by long-term culture of normal human mammary epithelial cells. Cancer Res 2009, 69:7557-7568.
33. Varley KE, Gertz J, Bowling KM, Parker SL, Reddy TE, Pauli-Behn F, Cross MK, Williams BA, Stamatoyannopoulos JA, Crawford GE, et al. Dynamic DNA methylation across diverse human cell lines and tissues. Genome Res 2013, 23:555-567.
34. Decottignies A, d'Adda di Fagagna F Epigenetic alterations associated with cellular senescence: a barrier against tumorigenesis or a red carpet for cancer?. Semin Cancer Biol 2011, 21:360-366.
35. Cruickshanks HA, McBryan T, Nelson DM, Vanderkraats ND, Shah PP, van Tuyn J, Singh Rai T, Brock C, Donahue G, Dunican DS, et al. Senescent cells harbour features of the cancer epigenome. Nat Cell Biol 2013, 15:1495-1506.