Epigenetic aberration of gene expression in endometriosis

Frontiers in Bioscience - Elite

Volumn 5 E, Issue 3, 2013, Pages 900-910

  Izawa, Masao ^a   Taniguchi, Fuminori ^a   Terakawa, Naoki ^a   Harada, Tasuku ^a  

^a TOTTORI UNIVERSITY   (Japan)

Author keywords

Aberrant DNA methylation; Aberrant gene expression; Endometriosis; Epigenetic disorder; Review

Indexed keywords

AROMATASE; ESTROGEN; ESTROGEN RECEPTOR BETA; HISTONE DEACETYLASE INHIBITOR; INTERLEUKIN 8; MESSENGER RNA; PROGESTERONE RECEPTOR; STEROIDOGENIC FACTOR 1; TRANSCRIPTION FACTOR HOXA10; UVOMORULIN;

AGING; ARTICLE; CHROMOSOME 15Q; CPG ISLAND; DNA METHYLATION; DOWN REGULATION; ENDOMETRIOSIS; ENVIRONMENTAL FACTOR; ESTROGEN ACTIVITY; ESTROGEN SYNTHESIS; GENE EXPRESSION; GENETIC ASSOCIATION; HISTONE MODIFICATION; HUMAN; IMMUNOPRECIPITATION; MONOZYGOTIC TWINS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; UTERUS;

EID: 84884305617     PISSN: 19450494     EISSN: 19450508     Source Type: Journal    
DOI: 10.2741/e669     Document Type: Article

References (108)

1. L.C. Giudice and L.C. Kao: Endometriosis. Lancet 364, 1789-1799 (2004)
2. B.S. Verkauf: Incidence, symptoms, and signs of endometriosis in fertile and infertile women. J Fla Med Assoc 74, 671-675 (1987)
3. R.J. Kurman and IeM. Shih: The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory. Am J Surg Pathol 34, 433-443 (2010)
4. R.J. Kurman and IeM. Shih: Molecular pathogenesis and extraovarian origin of epithelial ovarian cancer-shifting the paradigm. Hum Pathol 42, 918-931 (2011)
5. S.L. Berger, T. Kouzarides, R. Shiekhattar and A. Shilatifard: An operational definition of epigenetics. Genes Dev. 23, 781-783 (2009)
6. M. Esteller: Epigenetics in cancer. N. Engl. J. Med. 358, 1148-1159 (2008)
7. P.A. Jones and S.B. Baylin: The epigenomics of cancer. Cell 128, 683-692 (2007)
8. M. Rodríguez-Paredes and M. Esteller: Cancer epigenetics reaches mainstream oncology. Nat. Med. 17, 330-339 (2011)
9. G. Li and D. Reinberg: Chromatin higher-order structures and gene regulation. Curr Opin Genet Dev. 21, 175-186 (2011)
10. M. Esteller. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet. 8, 286-298 (2007)
11. R.A. Irizarry, C. Ladd-Acosta, B. Wen, Z. Wu, C. Montano, P. Onyango, H. Cui, K. Gabo, M. Rongione, M. Webster, H. Ji, J.B. Potash, S. Sabunciyan, A.P. Feinberg: The human colon cancer methylome shows similar hypo-and hypermethylation at conserved tissue-specific CpG island shores. Nat. Genet. 41, 178-186 (2009)
12. S-W. Guo: Epigenetics of endometriosis. Mol Hum Reprod 15, 587-607 (2009)
13. K. Nasu, Y. Kawano, Y. Tsukamoto, M. Takano, N. Takai, H. Li, Y. Furukawa, W. Abe, M. Moriyama and H. Narahara: Aberrant DNA methylation status of endometriosis: epigenetics as the pathogenesis, biomarker and therapeutic target. J Obstet Gynaecol Res 37, 683-95 (2011)
14. J.A. Sampson: Peritoneal endometriosis due to menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol 14, 422-469 (1927)
15. W. Paul Dmowski and D.P. Braun: Immunology of endometriosis. Best Pract Res Clin Obstet Gynaecol 18, 245-263 (2004)
16. M.Y. Wu and H.N. Ho: The role of cytokines in endometriosis. Am J Reprod Immunol 49, 285-296 (2003)
17. L. Schulke, M. Berbic, F. Manconi, N. Tokushige, R. Markham and I.S. Fraser: Dendritic cell populations in the eutopic and ectopic endometrium of women with endometriosis. Hum Reprod 24, 1695-703 (2009)
18. M. Sugamata, T. Ihara and I. Uchiide: Increase of activated mast cells in human endometriosis. Am J Reprod Immunol 53, 120-125 (2005)
19. S. Podgaec, M.S. Abrao, J.A. Dias Jr, L.V. Rizzo, R.M. de Oliveira and E.C. Baracat: Endometriosis: an inflammatory disease with a Th2 immune response component. Hum Reprod 22, 1373-1379 (2007)
20. C.C. Hsu, B.C. Yang, M.H. Wu and K.E. Huang: Enhanced interleukin-4 expression in patients with endometriosis. Fertil Steril 67, 1059-1064 (1997)
21. Y.S. Antsiferova, N.Y. Sotnikova, L.V. Posiseeva and A.L. Shor: Changes in the T-helper cytokine profile and in lymphocyte activation at the systemic and local levels in women with endometriosis. Fertil Steril 84, 1705-1711 (2005)
22. Z. Ouyang, Y. Hirota, Y. Osuga, K. Hamasaki, A. Hasegawa, T. Tajima, T. Hirata, K. Koga, O. Yoshino, M. Harada, Y. Takemura, E. Nose, T. Yano and Y. Taketani: Interleukin-4 stimulates proliferation of endometriotic stromal cells. Am J Pathol 173, 463-469 (2008)
23. M. Izawa, T. Harada, I. Deura, F. Taniguchi, T. Iwabe and N. Terakawa: Drug-induced apoptosis was markedly attenuated in endometriotic stromal cells. Hum Reprod 21, 600-604 (2006)
24. A. Watanabe, F. Taniguchi, M. Izawa, K. Suou, T. Uegaki, E. Takai, N. Terakawa and T. Harada: The role of survivin in the resistance of endometriotic stromal cells to drug-induced apoptosis. Hum Reprod 24, 3172-3179 (2009)
25. T. Iwabe, T. Harada T, T. Tsudo, M. Tanikawa, Y. Oonahara and N. Terakawa: Pathogenetic significance of increased levels of interleukin-8 in the peritoneal fluid of patients with endometriosis. Fertil Steril 69, 924-930 (1998)
26. T. Iwabe, T. Harada T, T. Tsudo, Y. Nagano, S. Yoshida, M. Tanikawa and N. Terakawa: Tumor necrosis factor-A promotes proliferation of endometriotic stromal cells by inducing interleukin-8 gene and protein expression. J Clin Endocrinol Metab 85, 824-829 (2000)
27. Y. Sakamoto, T. Harada, S. Horie, Y. Iba, F. Taniguchi, S. Yoshida, T. Iwabe and N. Terakawa: Tumor necrosis factor-a-induced interleukin-8 (IL-8) expression in endometriotic stromal cells, probably through nuclear factor-kB activation: gonadotropin-releasing hormone agonist treatment reduced IL-8 expression. J Clin Endocrinol Metab 88, 730-735 (2003)
28. A.M. Dlugi, J.D. Miller and J. Knittle: Lupron depot (leuprolide acetate for depot suspension) in the treatment of endometriosis: a randomized, placebo-controlled, double blind study. Fertil Steril 54, 419-427 (1990)
29. R.W. Shaw: An open randomized comparative study of the effect of goserelin depot and danazol in the treatment of endometriosis. Fertil Steril 58, 265-272 (1992)
30. D.L. Olive and E.A. Pritts: Treatment of Endometriosis. N Engl J Med 345, 266-275 (2001)
31. S.E. Bulun, Z. Lin, G. Imir, S. Amin, M. Demura, B. Yilmag, R. Martin, H. Utsunomiya, S. Thung, B. Gurates, M. Tamura, D. Langoi and S. Deb: Regulation of aromatase expression in estrogen-responsive breast and uterine disease: from bench to treatment. Pharmacol Rev 57, 359-383 (2005)
32. M. Izawa, T. Harada, Y. Ohama, Y. Takenaka, F. Taniguchi and N. Terakawa: An epigenetic disorder may cause aberrant expression of aromatase gene in endometriotic stromal cells. Fertil Steril 89, 1390-1396 (2008)
33. L.S. Noble, E.R. Simpson, A. Johns and S.E. Bulun : Aromatase expression in endometriosis. J Clin Endocrinol Metab81, 174-179 (1996)
34. J. Kitawaki, T. Noguchi, T. Amatsu, K. Maeda, K. Tsukamoto, T. Yamamoto, S. Fushiki, Y Osawa and H. Honjo: Expression of aromatase cytochrome P450 protein and messenger ribonucleic acid in human endometriotic and adenomyotic tissues but not in normal endometrium. Biol Reprod 57, 514-519 (1997)
35. S.E. Bulun, K. Zeitoun, K. Takayama, L. Noble, D. Michael, E. Simpson, A. Johns, M. Putman and H. Sasano: Estrogen production in endometriosis and use of aromatase inhibitors to treat endometriosis. Endocr Relat Cancer 6, 293-301(1999)
36. E.R. Simpson, M.Q. Michael, V.R. Agarwal, M.M. Hinshelwood, S.E. Bulun and Y. Zhao: Expression of the CYP19 (aromatase) gene: An unusual case of alternative promoter usage. FASEB J 11, 29-36 (1997)
37. M. Izawa, F. Taniguchi, T. Uegaki, E. Takai, T. Iwabe, N. Terakawa and T. Harada: Demethylation of a nonpromoter cytosine-phosphate-guanine island in the aromatase gene may cause the aberrant up-regulation in endometriotic tissues. Fertil Steril 95, 33-39 (2011)
38. E.C. Chang , T.H. Charn, S-H. Park, W.G. Helferich, B. Komm, J.A. Katzenellenbogen and B.S. Katzenellenbogen: Estrogen Receptors alpha and beta as determinants of gene expression: influence of ligand, dose, and chromatin binding. Mol Endocrinol 22, 1032-1043(2008)
39. T.H.Charn, T-B. Liu, E.C. Chang, Y.K. Lee, J.A. Katzenellenbogen and B.S. Katznellenbogen: Gemomewide dynamics of chromatin binding of estrogen receptors a and βmutual restriction and competitive site selection. Mol Endocrinol 24, 47-59 (2010)
40. J. Fujimoto, R. Hirose, H. Sakaguchi and T. Tamaya: Expression of oestrogen receptor-alpha and-beta in ovarian endometriomata. Mol Hum Reprod 5, 742-747(1999)
41. A.W. Brandenberger, D.I. Lebovic, M.K. Tee, I.P. Ryan, J.F. Tseng, R.B. Jaffe and R.N. Taylor: Oestrogen receptor (ER)-alpha and ER-beta isoforms in normal endometrial and endometriosis-derived stromal cells. Mol Hum Reprod 5, 651-655 (1999)
42. Q. Xue , Z. Lin , Y.H. Cheng, C.C. Huang, E. Marsh, P. Yin, M.P. Milad, E. Confino, S. Reierstad, J. Innes and S.E. Bulun: Promoter methylation regulates estrogen receptor 2 in human endometrium and endometriosis. Biol Reprod 77, 681-687 (2007)
43. E. Trukhacheva, Z. Lin, S. Reierstad, Y.H. Cheng, M. Milad and S.E. Bulun: Estrogen receptor (ER) beta regulates ERalpha expression in stromal cells derived from ovarian endometriosis. J Clin Endocrinol Metab 94, 615-622 (2009)
44. I. Juhasz-Bfss, C. Fischer, C. Lattrich, M. Skrzypczak, E. Malik, O. Ortmann and O. Treeck: Endometrial expression of estrogen receptor β and its splice variants in patients with and without endometriosis. Arch. Gynecol. Obstet. 284, 885-891 (2011)
45. S.E. Bulun, Z. Lin, G. Imir, S. Amin, M. Demura, B. Yilmaz, R. Martin, H. Utsunomiya, S. Thung, B. Gurates, M. Tamura, D. Langoi and S. Deb: Regulation of aromatase expression in estrogen-responsive breast and uterine disease: From bench to treatment. Pharmacol Rev 57, 359-383 (2005)
46. E. Attar and S.E. Bulun: Aromatase and other steroidogenic genes in endometriosis: Translational aspects. Hum Reprod Update 12, 49-56 (2006)
47. Y.K. Leung, P. Mak, S. Hassan and S.M. Ho: Estrogen receptor (ER)-beta isoforms: a key to understanding ERbeta signaling. Proc Natl Acad Sci USA 103, 13162-13167 (2006)
48. J.J. Brosens, N. Hayashi and J.O. White: Progesterone receptor regulates decidual prolactin expression in differentiating human endometrial stromal cells. Endocrinology 140, 4809-4820 (1999)
49. A.T. Fazleabas, A. Brudney, D. Chai, D. Langoi and S.E. Bulun: Steroid receptor and aromatase expression in baboon endometriotic lesions. Fertil Steril 80, 820-827 (2003)
50. S.E. Bulun, Y.H. Cheng, P. Yin, G. Imir, H. Utsunomiya, E. Attar, J. Innes and J.J. Kim: P: Progesterone resistance in endometriosis: Link to failure to metabolize estradiol. Mol Cell Endocrinol 248, 94-103 (2006)
51. B.A. Lessey, D.A. Metzger, A.F. Haney and K.S. McCarty Jr: Immunohistochemical analysis of estrogen and progesterone receptors in endometriosis: Comparison with normal endometrium during the menstrual cycle and the effect of medical therapy. Fertil Steril 51, 409-415 (1989)
52. G.R. Attia, K. Zeitoun, D. Edwards, A. Johns, B.R. Carr and S.E. Bulun: Progesterone receptor isoform A but not B is expressed in endometriosis. J Clin Endocrinol Metab 85, 2897-2902 (2000)
53. Q. Xue, Z. Lin, P. Yin, M.P. Milad, Y.H. Chen, E. Confino, S. Reierstad and S.E. Bulun: Transcriptional activation of steroidogenic factor-1 by hypomethylation of the 5' CpG island in endometriosis. J Clin Endocrinol Metab 92, 3261-3267 (2007)
54. B. Lee, H. Du and H.S. Taylor: Experimental murine endometriosis induces DNA methylation and altered gene expression in eutopic endometrium. Biol Reprod 80, 79-85 (2009)
55. P. Vercellini, I. Cortesi and P.G. Crosignani: Progestins for symptomatic endometriosis: A critical analysis of the evidence. Fertil Steril 68, 393-401 (1997)
56. Y. Wu, E. Strawn, Z. Basir, G. Halverson and S-W. Guo: Promoter hypermethylation of progesterone receptor isoform B (PR-B) in endometriosis. Epigenetics 1, 106-111 (2006)
57. Y. Wu, A. Starzinski-Powitz and S-W. Guo: Prolonged stimulation with tumor necrosis factor-alpha induced partial methylation at PR-B promoter in immortalized epitheliallike endometriotic cells. Fertil Steril 90, 234-237 (2008)
58. Y. Wu, X. Shi and S-W. Guo: The knockdown of progesterone receptor isoform B (PR-B) promotes proliferation in immortalized endometrial stromal cells. Fertil Steril 90, 1320-1323 (2008)
59. D.A. Rice, A.R. Mouw, A.M. Bogerd and K.L. Parker: A shared promoter element regulates the expression of three steroidogenic enzymes. Mol Endocrinol 5, 1552-1561 (1991)
60. K. Morohashi, S. Honda, Y. Inomata, H. Handa and T. Omura: A common trans-acting factor, Ad4-binding protein, to the promoters of steroidogenic P-450s. J Biol Chem 267, 17913-17919 (1992)
61. K. Zeitoun, K. Takayama, M.D. Michael and S.E. Bulun: Stimulation of aromatase P450 promoter (II) activity in endometriosis and its inhibition in endometrium are regulated by competitive binding of steroidogenic factor-1 and chicken ovalbumin upstream promoter transcription factor to the same cis-acting element. Mol Endocrinol 13, 239-253 (1999)
62. H. Utsunomiya, Y.H. Cheng, Z. Lin, S. Reierstad, P. Yin, E. Attar, Q. Que, G. Imir, S. Thung, E. Trukhacheva, T. Suzuki, H. Sasano, J.J. Kim, N. Yaegashi and S.E. Bulun: Upstream stimulatory factor-2 regulates steroidogenic factor-1 expression in endometriosis. Mol Endocrinol 22, 904-914 (2008)
63. U.H. Frixen, J. Behrens, M. Sachs, G. Eberle, B. Voss, A. Warda, D. Löchner and W. Birchmeier: E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J Cell Biol 113, 173-185 (1991)
64. A. Starzinski-Powitz, R. Gaetje, A. Zeitvogel, S. Kotzian, H. Handrow-Metzmacher, G. Herrmann, E. Fanning and R. Baumann:Tracing cellular and molecular mechanisms involved in endometriosis. Hum Reprod Update 4, 724-729 (1998)
65. Y. Wu, A. Starzinski-Powitz and S-W. Guo: Trichostatin A, a histone deacetylase inhibitor, attenuates invasiveness and reactivates E-cadherin expression in immortalized endometriotic cells. Reprod Sci 14, 374-382 (2007)
66. D.M. Bornman, S. Mathew, J. Alsruhe, J.G. Herman and E. Gabrielson: Methylation of the E-cadherin gene in bladder neoplasia and in normal urothelial epithelium from elderly individuals. Am J Pathol. 159, 831-835 (2001)
67. H.S. Taylor, C. Bagot, A. Kardana, D. Olive and A. Arici: HOX gene expression is altered in the endometrium of women with endometriosis. Hum Reprod 14, 1328-1331 (1999)
68. H.S. Taylor, A. Arici, D. Olive and P. Igarashi: HOXA10 is expressed in response to sex steroids at the time of implantation in the human endometrium. J Clin Invest 101, 1379-1384 (1998)
69. Y. Gui, J. Zhang, L. Yuan and B.A. Lessey: Regulation of HOXA-10 is and its expression in normal and abnormal endometrium. Mol Hum Reprod 5, 866-873 (1999)
70. Y. Wu, G. Halverson, Z. Basir, E. Strawn, P. Yan and S-W. Guo: Aberrant methylation at HOXA10 may be responsible for its aberrant expression in the endometrium of patients with endometriosis. Am J Obstet Gynecol 193, 371-380 (2005)
71. P.W. Laird: Principles and challenges of genomewide DNA methylation analysis. Principles and challenges of genomewide DNA methylation analysis. Nat Rev Genet 11,191-203 (2010)
72. T. Arimoto, T. Katagiri, K. Oda, T. Tsunoda, T. Yasugi, Y. Osuga, H. Yoshikawa, O. Nishii, T. Yano, Y. Taketani and Nakamura Y: Genome-wide cDNA microarray analysis of gene-expression profiles involved in ovarian endometriosis. Int J Oncol 22, 551-560 (2003)
73. S. Matsuzaki, M. Canis, C. Vaurs-Barriere, J.L.Pouly, O. Boespflug-Tanguy, F. Penault-Llorca, P. Dechelotte , B. Dastugue, K. Okamura and G. Mage: DNA microarray analysis of gene expression profiles in deep endometriosis using laser capture microdissection. Mol Hum Reprod 10, 719-728 (2004)
74. B. Borghese, S. Barbaux, F. Mondon, P. Santulli, G. Pierre, G. Chapron and D. Vaimin: Genome-wide profiling of methylated promoters in endometriosis reveals a subtelomeric location of hypermethylation. Mol Endocrinol 24, 1872-85 (2010)
75. S. Uno, H. Zembutsu, A. Hirasawa, A. Takahashi, M. Kubo, T. Akahane, D. Aoki, N. Kamatani, K. Hirata and Y. Nakamura: A genome-wide association study identifies genetic variants in the CDKN2BAS locus associated with endometriosis in Japanese. Nat Genet 42, 707-710 (2010)
76. S. Adachi, A. Tajima, J. Quan, K. Haino, K. Yoshihara, H. Masuzaki, H. Katabuchi, K. Ikuma, H. Suginami, N. Nishida, R. Kuwano, Y. Okazaki, Y. Kawamura, T. Sasaki, K. Tokunaga, I. Inoue and K. Tanaka: Meta-analysis of genomewide association scans for genetic susceptibility to endometriosis in Japanese population. J Hum Genet 55, 816-21 (2010)
77. J.N. Painter, C.A. Anderson, D.R. Nyholt, S. Macgregor, J. Lin, S.H. Lee, A. Lambert, Z.Z. Zhao, F. Roseman, Q. Guo, S.D. Gordon, L. Wallace, A.K. Henders, P.M. Visscher, P. Kraft, N.G. Martin, A.P. Morris, S.A. Treloar, S.H. Kennedy, S.A. Missmer, G.W. Montgomery and K.T. Zondervan: Genome-wide association study identifies a locus at 7p15.2 associated with endometriosis. Nat Genet 43, 51-54 (2011)
78. T. Jenuwein, C.D. Allis,Translating the histone code. Science 293, 1074-1080 (2001)
79. V.L. Wilson and P.A. Jones: DNA methylation decreases in aging but not in immortal cells. Science 220, 1055-1057 (1983)
80. M.F. Fraga, E.Ballestar, M.F. Paz , S. Ropero, F. Setien, M.L. Ballestar, D. Heine-Suñer, J.C. Cigudosa, M. Urioste, J. Benitez, M. Boix-Chornet, A. Sanchez-Aguilera, C. Ling, E. Carlsson, P. Poulsen, Z. Vaag A, Stephan, T.D. Spector, Y.Z. Wu, C. Plass and M. Esteller: Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci USA 102, 10604-10609 (2005)
81. A. Petronis: Epigenetics and twins: three variations on the theme. Trends Genet 22, 347-350 (2006)
82. R. Simmons: Developmental origins of adult metabolic disease: concepts and controversies. Trends Endocrinol Metab16, 390-394 (2005)
83. L. Gordon, J.H. Joo, R. Andronikos, M. Ollikainen, E.M. Wallace, M.P. Umstad, M. Permezel, A. Oshlack, R. Morley, J.B. Carlin , R. Saffery, G.K. Smyth and J.M. Craig: Expression discordance of monozygotic twins at birth: effect of intrauterine environment and a possible mechanism for fetal programming. Epigenetics 6, 579-592 (2005)
84. K.A. Lillycrop, E.S. Phillips, A.A. Jackson, M.A. Hanson and G.C. Burdge: Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 135, 1382-1386 (2005)
85. K.A. Lillycrop: Effect of maternal diet on the epigenome: implications for human metabolic disease. Proc Nutr Soc 70, 64-72 (2011)
86. S.K. Barnes and S.E. Ozanne: Pathways linking the early environment to long-term health and lifespan. Prog Biophys Mol Biol 106, 323-36 (2011)
87. R. Feil: Environmental and nutritional effects on the epigenetic regulation of genes. Mutat Res 600, 46-57 (2006)
88. R. Jaenisch and A. Bird: Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33, 245-254 (2003)
89. J.R. Dobosy, V.X. Fu, J.A. Desotelle, R. Srinivasan, M.L. Kenowski, N. Almassi, R. Weindruch, J. Svaren and D.F. Jarrard : A methyl-deficient diet modifies histone methylation and alters Igf2 and H19 repression in the prostate. Prostate 68, 1187-1195 (2008)
90. W.Czyz, J.M. Morahan, G.C. Ebers and S.V. Ramagopalan : Genetic, environmental and stochastic factors in monozygotic twin discordance with a focus on epigenetic differences. BMC Med. 10, 93 (2012) [Epub ahead of print].
91. Environmental epigenetics: prospects for studying epigenetic mediation of exposure-response relationships. V.K. Cortessis, D.C. Thomas, A.J. Levine, C.V. Breton, T.M. Mack, K.D. Siegmund, R.W. Haile and P.W. Laird : Environmental epigenetics: prospects for studying epigenetic mediation of exposure-response relationships. Hum. Genet. 131, 1565-1589 (2012)
92. M.A. Casillas Jr., N. Lopatina, L.G. Andrews and T.O. Tollefsbol: Transcriptional control of the DNA methyltransferases is altered in aging and neoplasticallytransformed human fibroblasts. Mol Cell Biochem 252, 33-43 (2003)
93. J.P. Issa: Age-related epigenetic changes and the immune system. Clin Immunol 109, 103-108 (2003)
94. V.L. Biron, K.J. McManus, N. Hu, M.J. Hendzel and D.A. Underhill: Distinct dynamics and distribution of histone methyl-lysine derivatives in mouse development. Dev Biol 276, 337-351 (2004)
95. M. Prokocimer, A. Margalit A and Y. Gruenbaum: The nuclear lamina and its proposed roles in tumorigenesis: projection on the hematologic malignancies and future targeted therapy. J Struct Biol 155, 351-360 (2006)
96. B. Sarg, E. Koutzamani, W. Helliger, I. Rundquist, H.H. Lindner: Postsynthetic trimethylation of histone H4 at lysine 20 in mammalian tissues is associated with aging. J Biol Chem 277, 39195-39201 (2002)
97. D.E. Olins and A.L. Olins: Granulocyte heterochromatin: defining the epigenome. BMC Cell Biol 6, 39 (2005)
98. M.F. Fraga, E. Ballestar, A. Villar-Garea, M. Boix-Chornet, J. Espada, G. Schotta, T. Bonaldi, C. Haydon, S. Ropero, K. Petrie, N.G. Iyer, A. Pérez-Rosado, E. Calvo, J.A. Lopez, A. Cano, M.J. Calasanz , D. Colomer, M.A. Piris, N. Ahn, A. Imhof , C. Caldas, T. Jenuwein and M. Esteller: Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat Genet 37, 391-400 (2005)
99. I.P. Pogribny, S.A. Ross, V.P. Tryndyak, M. Pogribna, L.A. Poirier and T.V. Karpinets : Histone H3 lysine 9 and H4 lysine 20 trimethylation and the expression of Suv4-20h2 and Suv-39h1 histone methyltransferases in hepatocarcinogenesis induced by methyl deficiency in rats. Carcinogenesis 27, 1180-1186 (2006)
100. V.P. Tryndyak, Q. Kovalchuk and I.P. Pogribny: Loss of DNA methylation and histone H4 lysine 20 trimethylation in human breast cancer cells is associated with aberrant expression of DNA methyltransferase 1, Suv4-20h2 histone methyltransferase and methyl-binding proteins. Cancer Biol Ther 5, 65-70 (2006)
101. V.P. Tryndyak, L. Muskhelishvili, O. Kovalchuk, R. Rodriguez-Juarez, B. Montgomery, M.I. Churchwell, S.A. Ross, F.A. Beland and I.P. Pogribny: Effect of long-term tamoxifen exposure on genotoxic and epigenetic changes in rat liver: implications for tamoxifen-induced hepatocarcinogenesis. Carcinogenesis 27, 1713-1720 (2006)
102. C.J. Peter and S. Akbarian: Balancing histone methylation activities in psychiatric disorders. Trends Mol. Med. 17, 372-379 (2011)
103. W.B. Ershler and D.L. Longo: Aging and cancer: issues of basic and clinical science. J Natl Cancer Inst 89, 1489-1497 (1997)
104. J. Cadinanos, I. Varela, C. López-Otín and J.M. Freije: From immature lamin to premature aging: molecular pathways and therapeutic opportunities. Cell Cycle 4, 1732-1735 (2005)
105. F. Eckhardt, J. Lewin, R. Cortese, V.K. Rakyan, J. Attwood, M. Burger, J. Burton, T.V. Cox, R. Davies, T.A. Down , C. Haefliger, R. Horton, K. Howe, D.K. Jackson, J. Kunde, C. Koenig, J. Liddle, D. Niblett, T. Otto, R. Pettett, S. Seemann, C. Thompson, T. West, J. Rogers, A. Olek, K. Berlin and S. Beck: DNA methylation profiling of human chromosomes 6, 20 and 22. Nat Genet 38, 1378-1385 (2006)
106. A.K. Maunakea, R. P. Nagarajan, M. Bilenky, T. J. Ballinger, C. D'Souza, S. D. Fouse1, B. E. Johnson, C. Hong, C. Nielsen, Y. Zhao, G. Turecki, A. Delaney, R. Varhol, N. Thiessen, K. Shchors, V. M. Heine, D. H. Rowitch, X. Xing, C. Fiore, M. Schillebeeckx, S. J. M. Jones, D. Haussler, M. A. Marra, M. Hirst, T. Wang and J. F. Costello: Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 466, 253-257 (2010)
107. N.Shenker and J.M. Flanagan: Intragenic DNA methylation: implication of this epigenetic mechanism for cancer research. Br J Cancer 106, 248-253 (2012)
108. C.X. Song, K.E. Szulwach, Y. Fu, Q. Dai, C. Yi, X. Li, Y. Li, C.H. Chen, W. Zhang, X. Jian, J. Wang, L. Zhang, T.J. Looney, B. Zhang, L.A. Godley, L.M. Hicks, B.T. Lahn, P. Jin and C. He: Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcytosine. Nat. Biotechnol. 29, 68-72 (2011)