Using epigenomic studies in monozygotic twins to improve our understanding of cancer

Epigenomics

Volumn 6, Issue 3, 2014, Pages 299-309

  Roos, Leonie ^a   Spector, Timothy D ^a   Bell, Christopher G ^a  

^a ST THOMAS HOSPITAL   (United Kingdom)

Author keywords

cancer; discordant monozygotic twins; DNA methylation; environment; epigenetics; twin study

Indexed keywords

TUMOR MARKER;

CPG ISLAND; DNA METHYLATION; EPIGENETICS; GENETIC PREDISPOSITION; GENETICS; HUMAN; MONOZYGOTIC TWINS; NEOPLASM; PATHOLOGY; PROCEDURES; TWINS;

CPG ISLANDS; DNA METHYLATION; EPIGENOMICS; GENETIC PREDISPOSITION TO DISEASE; HUMANS; NEOPLASMS; TUMOR MARKERS, BIOLOGICAL; TWIN STUDIES AS TOPIC; TWINS, MONOZYGOTIC;

EID: 84905819315     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.14.13     Document Type: Review

References (114)

1. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 100(1), 57-70 (2000
2. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 144(5), 646-674 (2011
3. Klein AP, Brune KA, Petersen GM et al. Prospective risk of pancreatic cancer in familial pancreatic cancer kindreds. Cancer Res. 64(7), 2634-2638 (2004
4. Geary J, Sasieni P, Houlston R et al. Gene-related cancer spectrum in families with hereditary non-polyposis colorectal cancer (HNPCC). Fam. Cancer 7(2), 163-172 (2008
5. Casadei S, Norquist BM, Walsh T et al. Contribution of inherited mutations in the BRCA2-interacting protein PALB2 to familial breast cancer. Cancer Res. 71(6), 2222-2229 (2011
6. Van Dongen J, Slagboom PE, Draisma HH, Martin NG, Boomsma DI. The continuing value of twin studies in the omics era. Nat. Rev. Genet. 13(9), 640-653 (2012
7. Hall J. Twinning. Lancet 362(9385), 735-743 (2003
8. Hall JG. Twins and twinning. Am. J. Med. Genet. 61(3), 202-204 (1996
9. Hamamy HA, Ajlouni HK, Ajlouni KM. Familial monozygotic twinning: report of an extended multigeneration family. Twin Res. 7(3), 219-222 (2004
10. Kendler KS, Prescott CA. A population-based twin study of lifetime major depression in men and women. Arch. Gen. Psychiatry 56(1), 39-44 (1999
11. MacGregor AJ, Snieder H, Rigby AS et al. Characterizing the quantitative genetic contribution to rheumatoid arthritis using data from twins. Arthritis Rheum. 43(1), 30-37 (2000
12. Sadovnick AD, Armstrong H, Rice GP et al. A populationbased study of multiple sclerosis in twins: update. Ann. Neurol. 33(3), 281-285 (1993
13. Bogdanos DP, Smyk DS, Rigopoulou EI et al. Twin studies in autoimmune disease: genetics, gender and environment. J. Autoimmun. 38(2-3), J156-169 (2012
14. Manolio TA. Bringing genome-wide association findings into clinical use. Nat. Rev. Genet. 14(8), 549-558 (2013
15. Lichtenstein P, Holm NV, Verkasalo PK et al. Environmental and heritable factors in the causation of cancer-analyses of cohorts of twins from Sweden, Denmark, and Finland. N. Engl. J. Med. 343(2), 78-85 (2000
16. Feinberg AP. An epigenetic approach to cancer etiology. Cancer J. 13(1), 70-74 (2007
17. Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447(7143), 425-432 (2007
18. Kota SK, Feil R. Epigenetic transitions in germ cell development and meiosis. Develop. Cell 19(5), 675-686 (2010
19. Talens RP, Christensen K, Putter H et al. Epigenetic variation during the adult lifespan: cross-sectional and longitudinal data on monozygotic twin pairs. Aging Cell 11(4), 694-703 (2012
20. Wong CC, Caspi A, Williams B et al. A longitudinal study of epigenetic variation in twins. Epigenetics 5(6), 516-526 (2010
21. Rakyan VK, Down TA, Maslau S et al. Human agingassociated DNA hypermethylation occurs preferentially at bivalent chromatin domains. Genome Res. 20(4), 434-439 (2010
22. Teschendorff AE, Menon U, Gentry-Maharaj A et al. Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer. Genome Res. 20(4), 440-446 (2010
23. Feil R, Fraga MF. Epigenetics and the environment: emerging patterns and implications. Nat. Rev. Genet. 13(2), 97-109 (2011
24. Weaver IC, Cervoni N, Champagne FA et al. Epigenetic programming by maternal behavior. Nat. Neurosci. 7(8), 847-854 (2004
25. Anderson OS, Nahar MS, Faulk C et al. Epigenetic responses following maternal dietary exposure to physiologically relevant levels of bisphenol A. Environ. Mol. Mutagen. 53(5), 334-342 (2012
26. Tobi EW, Lumey LH, Talens RP et al. DNA methylation differences after exposure to prenatal famine are common and timing-and sex-specific. Hum. Mol. Genet. 18(21), 4046-4053 (2009
27. Liu Y, Aryee MJ, Padyukov L et al. Epigenome-wide association data implicate DNA methylation as an intermediary of genetic risk in rheumatoid arthritis. Nat. Biotechnol. 31(2), 142-147 (2013
28. Hansen KD, Timp W, Bravo HC et al. Increased methylation variation in epigenetic domains across cancer types. Nat. Genet. 43(8), 768-775 (2011
29. Baylin SB, Jones PA. A decade of exploring the cancer epigenome-biological and translational implications. Nat. Rev. Cancer 11(10), 726-734 (2011
30. Dawson MA, Kouzarides T, Huntly BJ. Targeting epigenetic readers in cancer. N. Engl. J. Med. 367(7), 647-657 (2012
31. Plass C, Pfister SM, Lindroth AM, Bogatyrova O, Claus R, Lichter P. Mutations in regulators of the epigenome and their connections to global chromatin patterns in cancer. Nat. Rev. Genet. 14(11), 765-780 (2013
32. Jones S, Wang TL, Shih Ie M et al. Frequent mutations of chromatin remodeling gene ARID1A in ovarian clear cell carcinoma. Science 330(6001), 228-231 (2010
33. You JS, Jones PA. Cancer genetics and epigenetics: two sides of the same coiñ Cancer Cell 22(1), 9-20 (2012
34. Bert SA, Robinson MD, Strbenac D et al. Regional activation of the cancer genome by long-range epigenetic remodeling. Cancer Cell 23(1), 9-22 (2013
35. Garcia P, Manterola C, Araya JC et al. Promoter methylation profile in preneoplastic and neoplastic gall bladder lesions. Mol. Carcinogen. 48(1), 79-89 (2009
36. Baylin SB, Ohm JE. Epigenetic gene silencing in cancer-A mechanism for early oncogenic pathway addictioñ Nat. Rev. Cancer 6(2), 107-116 (2006
37. Shahrzad S, Bertrand K, Minhas K, Coomber BL. Induction of DNA hypomethylation by tumor hypoxia. Epigenetics 2(2), 119-125 (2007
38. Harris AL. Hypoxia-A key regulatory factor in tumour growth. Nat. Rev. Cancer 2(1), 38-47 (2002
39. Feinberg AP, Ohlsson R, Henikoff S. The epigenetic progenitor origin of human cancer. Nat. Rev. Genet. 7(1), 21-33 (2006
40. Timp W, Feinberg AP. Cancer as a dysregulated epigenome allowing cellular growth advantage at the expense of the host. Nat. Rev. Cancer 13(7), 497-510 (2013
41. Ziller MJ, Gu H, Muller F et al. Charting a dynamic DNA methylation landscape of the human genome. Nature 500(7463), 477-481 (2013
42. Illingworth RS, Gruenewald-Schneider U, Webb S et al. Orphan CpG islands identify numerous conserved promoters in the mammalian genome. PLoS Genet. 6(9), e1001134 (2010
43. Illingworth R, Kerr A, Desousa D et al. A novel CpG island set identifies tissue-specific methylation at developmental gene loci. PLoS Biol. 6(1), e22 (2008
44. Maunakea AK, Nagarajan RP, Bilenky M et al. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 466(7303), 253-257 (2010
45. Weber M, Hellmann I, Stadler MB et al. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat. Genet. 39(4), 457-466 (2007
46. Bird A. DNA methylation patterns and epigenetic memory. Genes Develop. 16(1), 6-21 (2002
47. Hellman A, Chess A. Gene body-specific methylation on the active X chromosome. Science 315(5815), 1141-1143 (2007
48. Ball MP, Li JB, Gao Y et al. Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells. Nat. Biotechnol. 27(4), 361-368 (2009
49. Aran D, Toperoff G, Rosenberg M, Hellman A. Replication timing-related and gene body-specific methylation of active human genes. Hum. Mol. Genet. 20(4), 670-680 (2011
50. Esteller M. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat. Rev. Genet. 8(4), 286-298 (2007
51. Feinberg AP, Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature 301(5895), 89-92 (1983
52. Gama-Sosa MA, Slagel VA, Trewyn RW et al. The 5-methylcytosine content of DNA from human tumors. Nucleic Acids Res. 11(19), 6883-6894 (1983
53. Hon GC, Hawkins RD, Caballero OL et al. Global DNA hypomethylation coupled to repressive chromatin domain formation and gene silencing in breast cancer. Genome Res. 22(2), 246-258 (2012
54. Berman BP, Weisenberger DJ, Aman JF et al. Regions of focal DNA hypermethylation and long-range hypomethylation in colorectal cancer coincide with nuclear lamina-associated domains. Nat. Genet. 44(1), 40-46 (2012
55. Nishigaki M, Aoyagi K, Danjoh I et al. Discovery of aberrant expression of R-RAS by cancer-linked DNA hypomethylation in gastric cancer using microarrays. Cancer Res. 65(6), 2115-2124 (2005
56. De Smet C, De Backer O, Faraoni I, Lurquin C, Brasseur F, Boon T. The activation of human gene MAGE-1 in tumor cells is correlated with genome-wide demethylation. Proc. Natl Acad. Sci. USA 93(14), 7149-7153 (1996
57. Lim JH, Kim SP, Gabrielson E, Park YB, Park JW, Kwon TK. Activation of human cancer/testis antigen gene, XAGE-1, in tumor cells is correlated with CpG island hypomethylation. Int. J. Cancer 116(2), 200-206 (2005
58. Akiyama Y, Maesawa C, Ogasawara S, Terashima M, Masuda T. Cell-type-specific repression of the maspin gene is disrupted frequently by demethylation at the promoter region in gastric intestinal metaplasia and cancer cells. Am. J. Pathol. 163(5), 1911-1919 (2003
59. Feinberg AP, Tycko B. The history of cancer epigenetics. Nat. Rev. Cancer 4(2), 143-153 (2004
60. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N. Engl. J. Med. 349(21), 2042-2054 (2003
61. Schuebel KE, Chen W, Cope L et al. Comparing the DNA hypermethylome with gene mutations in human colorectal cancer. PLoS Genet. 3(9), 1709-1723 (2007
62. Esteller M, Corn PG, Baylin SB, Herman JG. A gene hypermethylation profile of human cancer. Cancer Res. 61(8), 3225-3229 (2001
63. Ohtani-Fujita N, Fujita T, Aoike A, Osifchin NE, Robbins PD, Sakai T. CpG methylation inactivates the promoter activity of the human retinoblastoma tumor-suppressor gene. Oncogene 8(4), 1063-1067 (1993
64. Gonzalez-Zulueta M, Bender CM, Yang AS et al. Methylation of the 5CpG island of the p16/CDKN2 tumor suppressor gene in normal and transformed human tissues correlates with gene silencing. Cancer Res. 55(20), 4531-4535 (1995
65. Kane MF, Loda M, Gaida GM et al. Methylation of the hMLH1 promoter correlates with lack of expression of hMLH1 in sporadic colon tumors and mismatch repairdefective human tumor cell lines. Cancer Res. 57(5), 808-811 (1997
66. Herman JG, Latif F, Weng Y et al. Silencing of the VHL tumor-suppressor gene by DNA methylation in renal carcinoma. Proc. Natl Acad. Sci. USA 91(21), 9700-9704 (1994
67. Rice JC, Massey-Brown KS, Futscher BW. Aberrant methylation of the BRCA1 CpG island promoter is associated with decreased BRCA1 mRNA in sporadic breast cancer cells. Oncogene 17(14), 1807-1812 (1998
68. Saito Y, Liang G, Egger G et al. Specific activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells. Cancer Cell 9(6), 435-443 (2006
69. Esteller M. Epigenetic gene silencing in cancer: the DNA hypermethylome. Hum. Mol. Genet. 16(1), R50-R59 (2007
70. Irizarry RA, Ladd-Acosta C, Wen B et al. The human colon cancer methylome shows similar hypo-and hyper-methylation at conserved tissue-specific CpG island shores. Nat. Genet. 41(2), 178-186 (2009
71. Doi A, Park IH, Wen B et al. Differential methylation of tissue-and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat. Genet. 41(12), 1350-1353 (2009
72. Hodges E, Molaro A, Dos Santos CO et al. Directional DNA methylation changes and complex intermediate states accompany lineage specificity in the adult hematopoietic compartment. Mol. Cell 44(1), 17-28 (2011
73. Bock C. Analysing and interpreting DNA methylation data. Nat. Rev. Genet. 13(10), 705-719 (2012
74. Stadler MB, Murr R, Burger L et al. DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480(7378), 490-495 (2011
75. Schlesinger F, Smith AD, Gingeras TR, Hannon GJ, Hodges E. De novo DNA demethylation and noncoding transcription define active intergenic regulatory elements. Genome Res. 23(10), 1601-1614 (2013
76. Ward MC, Wilson MD, Barbosa-Morais NL et al. Latent regulatory potential of human-specific repetitive elements. Mol. Cell 49(2), 262-272 (2013
77. Ernst J, Kheradpour P, Mikkelsen TS et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473(7345), 43-49 (2011
78. Wang H, Maurano MT, Qu H et al. Widespread plasticity in CTCF occupancy linked to DNA methylation. Genome Res. 22(9), 1680-1688 (2012
79. Hu S, Wan J, Su Y et al. DNA methylation presents distinct binding sites for human transcription factors. eLife 2, e00726 (2013
80. Bell JT, Spector TD. A twin approach to unraveling epigenetics. Trends Genet. 27(3), 116-125 (2011
81. Gordon L, Joo JH, Andronikos R et al. Expression discordance of monozygotic twins at birth: effect of intrauterine environment and a possible mechanism for fetal programming. Epigenetics 6(5), 579-592 (2011
82. Hasler R, Begun A, Freitag-Wolf S et al. Genetic control of global gene expression levels in the intestinal mucosa: a human twin study. Physiol. Genomics 38(1), 73-79 (2009
83. Martino DJ, Tulic MK, Gordon L et al. Evidence for agerelated and individual-specific changes in DNA methylation profile of mononuclear cells during early immune development in humans. Epigenetics 6(9), 1085-1094 (2011
84. Bell JT, Saffery R. The value of twins in epigenetic epidemiology. Int. J. Epidemiol. 41(1), 140-150 (2012
85. Fraga MF, Ballestar E, Paz MF et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl Acad. Sci. USA 102(30), 10604-10609 (2005
86. Kaminsky ZA, Tang T, Wang SC et al. DNA methylation profiles in monozygotic and dizygotic twins. Nat. Genet. 41(2), 240-245 (2009
87. Bell JT, Tsai PC, Yang TP et al. Epigenome-wide scans identify differentially methylated regions for age and agerelated phenotypes in a healthy ageing population. PLoS Genet. 8(4), e1002629 (2012
88. Grundberg E, Meduri E, Sandling JK et al. Global analysis of DNA methylation variation in adipose tissue from twins reveals links to disease-associated variants in distal regulatory elements. Am. J. Human Genet. 93(5), 876-890 (2013
89. Petronis A, Gottesman, Ii, Kan P et al. Monozygotic twins exhibit numerous epigenetic differences: clues to twin discordance? Schizophren. Bull. 29(1), 169-178 (2003
90. Mill J, Dempster E, Caspi A, Williams B, Moffitt T, Craig I. Evidence for monozygotic twin (MZ) discordance in methylation level at two CpG sites in the promoter region of the catechol-O-methyltransferase (COMT) gene. Am. J. Med. Genet. B Neuropsychiatr. Genet. 141B(4), 421-425 (2006
91. Oates NA, Van Vliet J, Duffy DL et al. Increased DNA methylation at the AXIN1 gene in a monozygotic twin from a pair discordant for a caudal duplication anomaly. Am. J. Human Genet. 79(1), 155-162 (2006
92. Weksberg R, Shuman C, Caluseriu O et al. Discordant KCNQ1OT1 imprinting in sets of monozygotic twins discordant for Beckwith-Wiedemann syndrome. Hum. Mol. Genet. 11(11), 1317-1325 (2002
93. Kuratomi G, Iwamoto K, Bundo M et al. Aberrant DNA methylation associated with bipolar disorder identified from discordant monozygotic twins. Mol. Psychiatry 13(4), 429-441 (2008
94. Javierre BM, Fernandez AF, Richter J et al. Changes in the pattern of DNA methylation associate with twin discordance in systemic lupus erythematosus. Genome Res. 20(2), 170-179 (2010
95. Selmi C, Feghali-Bostwick CA, Lleo A et al. X chromosome gene methylation in peripheral lymphocytes from monozygotic twins discordant for scleroderma. Clin. Exp. Immunol. 169(3), 253-262 (2012
96. Nguyen A, Rauch TA, Pfeifer GP, Hu VW. Global methylation profiling of lymphoblastoid cell lines reveals epigenetic contributions to autism spectrum disorders and a novel autism candidate gene, RORA, whose protein product is reduced in autistic brain. FASEB J. 24(8), 3036-3051 (2010
97. Wong CC, Meaburn EL, Ronald A et al. Methylomic analysis of monozygotic twins discordant for autism spectrum disorder and related behavioural traits. Mol. Psychiatry 19, 495-503 (2013
98. Dempster EL, Pidsley R, Schalkwyk LC et al. Diseaseassociated epigenetic changes in monozygotic twins discordant for schizophrenia and bipolar disorder. Hum. Mol. Genet. 20(24), 4786-4796 (2011
99. Bell JT, Loomis AK, Butcher LM et al. Differential methylation of the TRPA1 promoter in pain sensitivity. Nat. Commun. 5, 2978 (2014
100. Davies MN, Volta M, Pidsley R et al. Functional annotation of the human brain methylome identifies tissue-specific epigenetic variation across brain and blood. Genome Biol. 13(6), R43 (2012
101. Horvath S, Zhang Y, Langfelder P et al. Aging effects on DNA methylation modules in human brain and blood tissue. Genome Biol. 13(10), R97 (2012
102. Garber JE, Offit K. Hereditary cancer predisposition syndromes. J. Clin. Oncol. 23(2), 276-292 (2005
103. Galetzka D, Hansmann T, El Hajj N et al. Monozygotic twins discordant for constitutive BRCA1 promoter methylation, childhood cancer and secondary cancer. Epigenetics 7(1), 47-54 (2012
104. Huen MS, Sy SM, Chen J. BRCA1 and its toolbox for the maintenance of genome integrity. Nat. Rev. Mol. Cell Biol. 11(2), 138-148 (2010
105. Dobrovic A, Simpfendorfer D. Methylation of the BRCA1 gene in sporadic breast cancer. Cancer Res. 57(16), 3347-3350 (1997
106. Rice JC, Ozcelik H, Maxeiner P, Andrulis I, Futscher BW. Methylation of the BRCA1 promoter is associated with decreased BRCA1 mRNA levels in clinical breast cancer specimens. Carcinogenesis 21(9), 1761-1765 (2000
107. Stefansson OA, Esteller M. Epigenetic modifications in breast cancer and their role in personalized medicine. Am. J. Pathol. 183(4), 1052-1063 (2013
108. Heyn H, Carmona FJ, Gomez A et al. DNA methylation profiling in breast cancer discordant identical twins identifies DOK7 as novel epigenetic biomarker. Carcinogenesis 34(1), 102-108 (2013
109. Koestler DC, Christensen B, Karagas MR et al. Bloodbased profiles of DNA methylation predict the underlying distribution of cell types: a validation analysis. Epigenetics 8(8), 816-826 (2013
110. Mill J, Heijmans BT. From promises to practical strategies in epigenetic epidemiology. Nat. Rev. Genet. 14(8), 585-594 (2013
111. Hur YM, Craig JM. Twin registries worldwide: an important resource for scientific research. Twin Res. Hum. Genet. 16(1), 1-12 (2013
112. Nabilsi NH, Pardo CE, Zajac-Kaye M, Kladde MP. Breast cancer epigenetics: biomarkers and therapeutic potential. In: Cell and Molecular Biology of Breast Cancer. Schatten H (Ed.). Humana Press, NY, USA, 211-259 (2013
113. Reyon D, Maeder ML, Khayter C et al. Engineering customized TALE nucleases (TALENs) and TALE transcription factors by fast ligation-based automatable solidphase high-throughput (FLASH) assembly. Curr. Protoc. Mol. Biol. 12, 12 (2013
114. Ramalingam S, Annaluru N, Chandrasegaran S. A CRISPR way to engineer the human genome. Genome Biol. 14(2), 107 (2013).