DNA methylation abnormalities at gene promoters are extensive and variable in the elderly and phenocopy cancer cells

FASEB Journal

Volumn 28, Issue 7, 2014, Pages 3261-3272

  Gautrey, Hannah E ^a   Van Otterdijk, Sanne D ^a   Cordell, Heather J ^a   Bond, John ^b   Collerton, Joanna ^b   Davies, Karen ^b   Eccles, Martin ^b   Jagger, Carol ^b   James, Oliver ^b   Kirkwood, Tom ^b   Martin Ruiz, Carmen ^b   Robinson, Louise ^b   Von Zglinicki, Thomas ^b   Mathers, John C ^a   Strathdee, Gordon ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b Institute for Genetic Medicine Institute for Ageing and Health Newcastle University ^*  (United Kingdom)

Author keywords

Aging; Cell type specific; CpG island; Epigenetics

Indexed keywords

BISULFITE; DNA;

AGING; ARTICLE; CANCER CELL; CANCER DIAGNOSIS; CANCER RISK; CELL TYPE; COHORT ANALYSIS; CPG ISLAND; DNA METHYLATION; DNA MODIFICATION; FOLLOW UP; GENE EXPRESSION; GENETIC VARIABILITY; HEMATOLOGIC MALIGNANCY; HEMATOPOIETIC CELL; HUMAN; HYPOTHESIS; LEUKOCYTE; LYMPHOMA; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PYROSEQUENCING; TUMOR SUPPRESSOR GENE;

AGING; CELL TYPE SPECIFIC; CPG ISLAND; EPIGENETICS;

AGED, 80 AND OVER; AGING; CELL LINE, TUMOR; CPG ISLANDS; DNA METHYLATION; HUMANS; NEOPLASMS; PROMOTER REGIONS, GENETIC;

EID: 84903693608     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-246173     Document Type: Article

References (51)

1. Bray, F., Jemal, A., Grey, N., Ferlay, J., and Forman, D. (2012) Global cancer transitions according to the Human Development Index (2008-2030): a population-based study. Lancet Oncol. 13, 790-801
2. Costello, J. F., and Plass, C. (2001) Methylation matters. J. Med. Genet. 38, 285-303 (Pubitemid 32433981)
3. Bird, A. P., and Wolffe, A. P. (1999) Methylation-induced repression-belts, braces, and chromatin. Cell 99, 451-454 (Pubitemid 129746827)
4. Kulis, M., and Esteller, M. (2010) DNA methylation and cancer. Adv. Genet. 70, 27-56
5. Fahrner, J. A., Eguchi, S., Herman, J. G., and Baylin, S. B. (2002) Dependence of histone modifications and gene expression on DNA hypermethylation in cancer. Cancer Res. 62, 7213-7218 (Pubitemid 36025241)
6. Jacinto, F. V., and Esteller, M. (2007) Mutator pathways unleashed by epigenetic silencing in human cancer. Mutagenesis 22, 247-253 (Pubitemid 47216613)
7. Fraga, M. F., and Esteller, M. (2007) Epigenetics and aging: the targets and the marks. Trends Genet. 23, 413-418 (Pubitemid 47088010)
8. Bollati, V., Schwartz, J., Wright, R., Litonjua, A., Tarantini, L., Suh, H., Sparrow, D., Vokonas, P., and Baccarelli, A. (2009) Decline in genomic DNA methylation through aging in a cohort of elderly subjects. Mech. Ageing Dev. 130, 234-239
9. Bjornsson, H. T., Sigurdsson, M. I., Fallin, M. D., Irizarry, R. A., Aspelund, T., Cui, H., Yu, W., Rongione, M. A., Ekstrom, T. J., Harris, T. B., Launer, L. J., Eiriksdottir, G., Leppert, M. F., Sapienza, C., Gudnason, V., and Feinberg, A. P. (2008) Intra-individual change over time in DNA methylation with familial clustering. JAMA 299, 2877-2883 (Pubitemid 351930887)
10. DePinho, R. A. (2000) The age of cancer. Nature 408, 248-254
11. Portela, A., and Esteller, M. (2010) Epigenetic modifications and human disease. Nat. Biotechnol. 28, 1057-1068
12. Collerton, J., Barrass, K., Bond, J., Eccles, M., Jagger, C., James, O., Martin-Ruiz, C., Robinson, L., von Zglinicki, T., and Kirk-wood, T. (2007) The Newcastle 85+ study: biological, clinical and psychosocial factors associated with healthy ageing: study protocol. BMC Geriatr. 7, 14
13. Collerton, J., Davies, K., Jagger, C., Kingston, A., Bond, J., Eccles, M. P., Robinson, L. A., Martin-Ruiz, C, von Zglinicki, T., James, O. F., and Kirkwood, T. B. (2009) Health and disease in 85 year olds: baseline findings from the Newcastle 85+ cohort study. BMJ339, b4904
14. Chase, D. S., Tawn, E.J., Parker, L., Jonas, P., Parker, C. O., and Burn, J. (1998) The North Cumbria Community Genetics Project. J. Med. Genet. 35, 413-416 (Pubitemid 28211638)
15. Pearce, M. S., Unwin, N. C., Parker, L., and Craft, A. W. (2009) Cohort profile: the Newcastle Thousand Families 1947 birth cohort. Int. J. Epidemiol. 38, 932-937
16. McKay, J. A., Groom, A., Potter, C, Coneyworth, L. J., Ford, D., Mathers, J. C, andRelton, C. L. (2012) Genetic and non-genetic influences during pregnancy on infant global and site specific DNA methylation: role for folate gene variants and vitamin B12. PLoS ONE 7, e33290
17. Potter, C, McKay, J., Groom, A., Ford, D., Coneyworth, L., Mathers, J. C, and Relton, C. L. (2013) Influence of DNMT genotype on global and site specific DNA methylation patterns in neonates and pregnant women. PLoS ONE 8, e76506
18. Martin-Ruiz, C, Jagger, C, Kingston, A., Collerton, J., Catt, M., Davies, K., Dunn, M., Hilkens, C, Keavney, B., Pearce, S. H., den Elzen, W. P., Talbot, D., Wiley, L., Bond, J., Mathers, J. C, Eccles, M. P., Robinson, L., James, O., Kirkwood, T. B., and von Zglinicki, T. (2011) Assessment of a large panel of candidate biomarkers of ageing in the Newcastle 85+ study. Mech. Ageing Dev. 132, 496-502
19. Ferguson, S., Gautrey, H. E., and Strathdee, G. (2011) The dual role of HLXB9 in leukemia. Pediatr. Blood Cancer 56, 349-352
20. Herman, J. G., Jen, J., Merlo, A., and Baylin, S. B. (1996) Hypermethylation-associated inactivation indicates a tumor suppressor role for p15INK4B. Cancer Res. 56, 722-727
21. Kuang, S. Q., Bai, H., Fang, Z. H., Lopez, G., Yang, H., Tong, W., Wang, Z. Z., and Garcia-Manero, G. (2010) Aberrant DNA methylation and epigenetic inactivation of Eph receptor tyrosine kinases and ephrin ligands in acute lymphoblastic leukemia. Blood 115, 2412-2419
22. Thathia, S. H., Ferguson, S., Gautrey, H. E., van Otterdijk, S. D., Hili, M., Rand, V., Moorman, A. V., Meyer, S., Brown, R., and Strathdee, G. (2012) Epigenetic inactivation of TWIST2 in acute lymphoblastic leukemia modulates proliferation, cell survival and chemosensitivity. Haematologica 97, 371-378
23. Tong, W. G., Wierda, W. G., Lin, E., Kuang, S. Q., Bekele, B. N., Estrov, Z., Wei, Y, Yang, H., Keating, M. J., and Garcia-Manero, G (2010) Genome-wide DNA methylation profiling of chronic lymphocytic leukemia allows identification of epigenetically repressed molecular pathways with clinical impact. Epigenetics 5, 499-508
24. Di Gioia, S., Bianchi, P., Destro, A., Grizzi, F., Malesci, A., Laghi, L., Levrero, M., Morabito, A., and Roncalli, M. (2006) Quantitative evaluation of RASSF1A methylation in the non-lesional, regenerative and neoplastic liver. BMC Cancer 6, 89
25. Kanaya, T., Kyo, S., Maida, Y., Yatabe, N., Tanaka, M., Naka-mura, M., and Inoue, M. (2003) Frequent hypermethylation of MLH1 promoter in normal endometrium of patients with endometrial cancers. Oncogene 22, 2352-2360 (Pubitemid 36566790)
26. Kwabi-Addo, B., Chung, W., Shen, L., Ittmann, M., Wheeler, T., Jelinek, J., and Issa, J. P. (2007) Age-related DNA methylation changes in normal human prostate tissues. Clin. Cancer Res. 13, 3796-3802 (Pubitemid 47037584)
27. Tamura, G. (2004) Promoter methylation status of tumor suppressor and tumor-related genes in neoplastic and nonneoplastic gastric epithelia. Histol. Histopathol. 19, 221-228 (Pubitemid 38111266)
28. Yu, C. E., Cudaback, E., Foraker, J., Thomson, Z., Leong, L., Lutz, F., Gill, J. A., Saxton, A., Kraemer, B., Navas, P., Keene, C. D., Montine, T., and Bekris, L. M. (2013) Epigenetic signature and enhancer activity of the human APOE gene. Hum. Mol. Genet. 22, 5036-5047
29. Strathdee, G., Sim, A., Soutar, R., Holyoake, T. L., and Brown, R (2007) HOXA5 is targeted by cell-type-specific CpG island methylation in normal cells and during the development of acute myeloid leukaemia. Carcinogenesis 28, 299-309 (Pubitemid 46321845)
30. Sullivan, M. J., Taniguchi, T., Jhee, A., Kerr, N., and Reeve, A. E. (1999) Relaxation of IGF2 imprinting in Wilms tumours associated with specific changes in IGF2 methylation. Oncogene 18, 7527-7534 (Pubitemid 30035053)
31. Costello, J. F., Fruhwald, M. C., Smiraglia, D. J., Rush, L. J., Robertson, G. P., Gao, X., Wright, F. A., Feramisco, J. D., Peltomaki, P., Lang, J. C., Schuller, D. E., Yu, L., Bloomfield, C. D., Caligiuri, M. A., Yates, A., Nishikawa, R., Su Huang, H., Petrelli, N.J., Zhang, X., O'Dorisio, M. S., Held, W. A., Cavenee, W. K., and Plass, C. (2000) Aberrant CpG-island methylation has non-random and tumour-type-specific patterns. Nat. Genet. 24, 132-138 (Pubitemid 30094712)
32. Toyota, M., and Issa, J. P. (1999) CpG island methylator phenotypes in aging and cancer. Semin. Cancer Biol. 9, 349-357 (Pubitemid 29532861)
33. Jones, P. A., and Laird, P. W. (1999) Cancer epigenetics comes of age. Nat. Genet. 21, 163-167 (Pubitemid 29070360)
34. Tapp, H. S., Commane, D. M., Bradburn, D. M., Arasaradnam, R, Mathers, J. C, Johnson, I. T., and Belshaw, N. J. (2013) Nutritional factors and gender influence age-related DNA methylation in the human rectal mucosa. Aging Cell 12, 148-155
35. Scholz, C, Nimmrich, I., Burger, M., Becker, E., Dorken, B., Ludwig, W. D., and Maier, S. (2005) Distinction of acute lymphoblastic leukemia from acute myeloid leukemia through microarray-based DNA methylation analysis. Ann. Hematol. 84, 236-244 (Pubitemid 40425070)
36. Wikby, A., Mansson, I. A., Johansson, B., Strindhall, J., and Nilsson, S. E. (2008) The immune risk profile is associated with age and gender: findings from three Swedish population studies of individuals 20-100 years of age. Biogerontology 9, 299-308
37. Issa, J. P. (1999) Aging, DNA methylation and cancer. Crit. Rev. Oncol. Hematol. 32, 31-43
38. Feinberg, A. P., Ohlsson, R., and Henikoff, S. (2006) The epigenetic progenitor origin of human cancer. Nature Rev. Genet. 7, 21-33 (Pubitemid 41828945)
39. Teschendorff, A. E., Menon, U., Gentry-Maharaj, A., Ramus, S. J., Weisenberger, D. J., Shen, H., Campan, M., Noushmehr, H., Bell, C. G., Maxwell, A. P., Savage, D. A., Mueller-Holzner, E., Marth, C., Kocjan, G., Gayther, S. A., Jones, A., Beck, S., Wagner, W., Laird, P. W., Jacobs, I. J., and Widschwendter, M. (2010) Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer. Genome Res. 20, 440-446
40. Rakyan, V. K., Down, T. A., Maslau, S., Andrew, T., Yang, T. P., Beyan, H., Whittaker, P., McCann, O. T., Finer, S., Valdes, A. M., Leslie, R. D., Deloukas, P., and Spector, T. D. (2010) Human aging-associated DNA hypermethylation occurs preferentially at bivalent chromatin domains. Genome Res. 20, 434-439
41. Gemma, C., Ramagopalan, S. V., Down, T. A., Beyan, H., Hawa, M. I., Holland, M. L., Hurd, P. J., Giovannoni, G., David Leslie, R., Ebers, G. C., and Rakyan, V. K. (2013) Inactive or moderately active human promoters are enriched for inter-individual epi-alleles. Genome Biol. 14, R43
42. Toyota, M., Ahuja, N., Ohe-Toyota, M., Herman, J. G., Baylin, S. B., and Issa, J. P. (1999) CpG island methylator phenotype in colorectal cancer. Proc. Natl. Acad. Sci. U. S. A. 96, 8681-8686 (Pubitemid 29354851)
43. Hughes, L. A., Melotte, V., de Schrijver, J., de Maat, M., Smit, V. T., Bovee, J. V., French, P. J., van den Brandt, P. A., Schouten, L. J., de Meyer, T., van Criekinge, W., Ahuja, N., Herman, J. G., Weijenberg, M. P., and van Engeland, M. (2013) The CpG island methylator phenotype: what's in a name? Cancer Res. 73, 5858-5868
44. Teschendorff, A. E., West, J., and Beck, S. (2013) Age-associated epigenetic drift: implications, and a case of epigenetic thrift? Hum. Mol. Genet. 22, R7-R15
45. Zhang, D., Cheng, L., Badner, J. A., Chen, C., Chen, Q., Luo, W., Craig, D. W., Redman, M., Gershon, E. S., and Liu, C. (2010) Genetic control of individual differences in gene-specific meth-ylation in human brain. Am. J. Hum. Genet. 86, 411-419
46. Boks, M. P., Derks, E. M., Weisenberger, D. J., Strengman, E., Janson, E., Sommer, I. E., Kahn, R. S., and Ophoff, R. A. (2009) The relationship of DNA methylation with age, gender and genotype in twins and healthy controls. PLoS ONE 4, e6767
47. Brennan, K., Garcia-Closas, M., Orr, N., Fletcher, O., Jones, M., Ashworth, A., Swerdlow, A., Thorne, H., Riboli, E., Vineis, P., Dorronsoro, M., Clavel-Chapelon, F., Panico, S., Onland-Moret, N. C., Trichopoulos, D., Kaaks, R., Khaw, K. T., Brown, R., and Flanagan, J. M. (2012) Intragenic ATM methylation in peripheral blood DNA as a biomarker of breast cancer risk. Cancer Res. 72, 2304-2313
48. Beerman, I., Bock, C., Garrison, B. S., Smith, Z. D., Gu, H., Meissner, A., and Rossi, D. J. (2013) Proliferation-dependent alterations of the DNA methylation landscape underlie hema-topoietic stem cell aging. Cell Stem Cell 12, 413-425
49. Bock, C., Beerman, I., Lien, W. H., Smith, Z. D., Gu, H., Boyle, P., Gnirke, A., Fuchs, E., Rossi, D. J., and Meissner, A. (2012) DNA methylation dynamics during in vivo differentiation of blood and skin stem cells. Mol. Cell. 47, 633-647
50. Keshet, I., Schlesinger, Y., Farkash, S., Rand, E., Hecht, M., Segal, E., Pikarski, E., Young, R. A., Niveleau, A., Cedar, H., and Simon, I. (2006) Evidence for an instructive mechanism of de novo methylation in cancer cells. Nat. Genet. 38, 149-153 (Pubitemid 43177227)
51. Raval, A., Lucas, D. M., Matkovic, J. J., Bennett, K. L., Li-yanarachchi, S., Young, D. C., Rassenti, L., Kipps, T. J., Grever, M. R., Byrd, J. C., and Plass, C. (2005) TWIST2 demonstrates differential methylation in immunoglobulin variable heavy chain mutated and unmutated chronic lymphocytic leukemia. J. Clin. Oncol. 23, 3877-3885 (Pubitemid 46218690)