Endometriosis is characterized by a distinct pattern of histone 3 and histone 4 lysine modifications

Reproductive Sciences

Volumn 21, Issue 3, 2014, Pages 305-318

  Monteiro, Janice B ^a   Colón Díaz, Maricarmen ^b   García, Miosotis ^c   Gutierrez, Sylvia ^a   Colón, Mariano ^a   Seto, Edward ^d   Laboy, Joaquín ^a   Flores, Idhaliz ^a  

^a PONCE SCHOOL OF MEDICINE   (Puerto Rico)

^b San Juan Bautista School of Medicine   (Puerto Rico)

^c Hato Rey Pathology   (United States)

^d H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

ChIP; endometriosis; epigenetics; histone acetylation; histone code; histone methylation; histone modifications

Indexed keywords

HISTONE H3; HISTONE H4; LYSINE;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOMETRIOSIS; EPIGENETICS; FEMALE; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; HUMAN TISSUE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PURIFICATION; ADOLESCENT; ADULT; CORRELATIONAL STUDY; DOWN REGULATION; ENDOMETRIUM; GENE; GENE EXPRESSION; HISTONE CODE; MAJOR CLINICAL STUDY; STEREOIDOGENIC FACTOR 1 GENE;

CHIP; ENDOMETRIOSIS; EPIGENETICS; HISTONE ACETYLATION; HISTONE CODE; HISTONE METHYLATION; HISTONE MODIFICATIONS;

ACETYLATION; ADOLESCENT; ADULT; ENDOMETRIOSIS; FEMALE; HISTONES; HUMANS; LYSINE; MIDDLE AGED; PROTEIN ARRAY ANALYSIS; YOUNG ADULT;

EID: 84896857928     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719113497267     Document Type: Article

References (83)

1. Bulun SE. Endometriosis. N Engl J Med. 2009; 360 (3). 268-279
2. Giudice LC. Genomics' role in understanding the pathogenesis of endometriosis. Semin Reprod Med. 2003; 21 (2). 119-124
3. Kao LC, Germeyer A, Tulac S, et al. Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology. 2003; 144 (7). 2870-2881
4. Guo SW. Epigenetics of endometriosis. Mol Hum Reprod. 2009; 15 (10). 587-607
5. Jenuwein T, Allis CD. Translating the histone code. Science. 2001; 293 (5532). 1074-1080
6. Turner BM. Cellular memory and the histone code. Cell. 2002; 111 (3). 285-291
7. Ferguson LR, Tatham AL, Lin Z, Denny WA. Epigenetic regulation of gene expression as an anticancer drug target. Curr Cancer Drug Targets. 2011; 11 (2). 199-212
8. Wu Y, Starzinski-Powitz A, Guo SW. Trichostatin A, a histone deacetylase inhibitor, attenuates invasiveness and reactivates E-cadherin expression in immortalized endometriotic cells. Reprod Sci. 2007; 14 (4). 374-382
9. Wu Y, Guo SW. Histone deacetylase inhibitors trichostatin A and valproic acid induce cell cycle arrest and p21 expression in immortalized human endometrial stromal cells. Eur J Obstet Gynecol Reprod Biol. 2008; 137 (2). 198-203
10. Liu M, Liu X, Zhang Y, Guo SW. Valproic acid and progestin inhibit lesion growth and reduce hyperalgesia in experimentally induced endometriosis in rats. Reprod Sci. 2012; 19 (4). 360-373
11. Colón-Díaz M, Báez-Vega P, García M, et al. HDAC1 and HDAC2 are differentially expressed in endometriosis. Reprod Sci. 2012; 19 (5). 483-492
12. Turner BM. Histone acetylation and an epigenetic code. Bioessays. 2000; 22 (9). 836-845
13. Strahl BD, Allis CD. The language of covalent histone modifications. Nature. 2000; 403 (6765). 41-45
14. Gardner KE, Allis CD, Strahl BD. Operating on chromatin, a colorful language where context matters. J Mol Biol. 2011; 409 (1). 36-46
15. Robyr D, Kurdistani SK, Grunstein M. Analysis of genome-wide histone acetylation state and enzyme binding using DNA microarrays. Methods Enzymol. 2004; 376: 289-304
16. Robyr D, Suka Y, Xenarios I, et al. Microarray deacetylation maps determine genome-wide functions for yeast histone deacetylases. Cell. 2002; 109 (4). 437-446
17. Chen C, Zhao M, Yin N, et al. Abnormal histone acetylation and methylation levels in esophageal squamous cell carcinomas. Cancer Invest. 2011; 29 (8). 548-556
18. Taby R, Issa JP. Cancer epigenetics. CA Cancer J Clin. 2010; 60 (6). 376-392
19. Dieker JW, Fransen JH, van Bavel CC, et al. Apoptosis-induced acetylation of histones is pathogenic in systemic lupus erythematosus. Arthritis Rheum. 2007; 56 (6). 1921-1933
20. Hu N, Qiu X, Luo Y, et al. Abnormal histone modification patterns in lupus CD4+ T cells. J Rheumatol. 2008; 35 (5). 804-810
21. Dai Y, Zhang L, Hu C, Zhang Y. Genome-wide analysis of histone H3 lysine 4 trimethylation by ChIP-chip in peripheral blood mononuclear cells of systemic lupus erythematosus patients. Clin Exp Rheumatol. 2010; 28 (2). 158-168
22. Denk F, McMahon SB. Chronic pain: emerging evidence for the involvement of epigenetics. Neuron. 2012; 73 (3). 435-444
23. Fischer JJ, Toedling J, Krueger T, Schueler M, Huber W, Sperling S. Combinatorial effects of four histone modifications in transcription and differentiation. Genomics. 2008; 91 (1). 41-51
24. Noyes RW, Hertig AT, Rock J. Dating the endometrial biopsy. Am J Obstet Gynecol. 1975; 122 (2). 262-263
25. Yost JM, Korboukh I, Liu F, Gao C, Jin J. Targets in epigenetics: inhibiting the methyl writers of the histone code. Curr Chem Genomics. 2011; 5 (suppl 1). 72-84
26. Jeffries MA, Sawalha AH. Epigenetics in systemic lupus erythematosus: leading the way for specific therapeutic agents. Int J Clin Rheumatol. 2011; 6 (4). 423-439
27. Hake SB, Xiao A, Allis CD. Linking the epigenetic 'language' of covalent histone modifications to cancer. Br J Cancer. 2007; 96 ((suppl)). R31-R39
28. Wang GG. Allis CD. "Misinterpretation" of a histone mark is linked to aberrant stem cells and cancer development. Cell Cycle. 2009; 8 (13). 1982-1983
29. Chen H, Hardy TM, Tollefsbol TO. Epigenomics of ovarian cancer and its chemoprevention. Front Genet. 2011; 2: 67
30. Kurdistani SK, Tavazoie S, Grunstein M. Mapping global histone acetylation patterns to gene expression. Cell. 2004; 117 (6). 721-733
31. Baker LA, Allis CD, Wang GG. PHD fingers in human diseases: disorders arising from misinterpreting epigenetic marks. Mutat Res. 2008; 647 (1-2). 3-12
32. Wang GG, Allis CD, Chi P. Chromatin remodeling and cancer, Part I: Covalent histone modifications. Trends Mol Med. 2007; 13 (9). 363-372
33. Mosashvilli D, Kahl P, Mertens C, et al. Global histone acetylation levels: prognostic relevance in patients with renal cell carcinoma. Cancer Sci. 2010; 101 (12). 2664-2669
34. Zhang P, Su Y, Zhao M, Huang W, Lu Q. Abnormal histone modifications in PBMCs from patients with psoriasis vulgaris. Eur J Dermatol. 2011; 21 (4). 552-557
35. Sun HS, Hsiao KY, Hsu CC, Wu MH, Tsai SJ. Transactivation of steroidogenic acute regulatory protein in human endometriotic stromalcells is mediated by the prostaglandin EP2 receptor. Endocrinology. 2003; 144 (9). 3934-3942
36. Giacinti L, Claudio PP, Lopez M, Giordano A. Epigenetic information and estrogen receptor alpha expression in breast cancer. Oncologist. 2006; 11 (1). 1-8
37. Cao D, Bromberg PA, Samet JM. COX-2 expression induced by diesel particles involves chromatin modification and degradation of HDAC1. Am J Respir Cell Mol Biol. 2007; 37 (2). 232-239
38. Coward WR, Watts K, Feghali-Bostwick CA, Knox A, Pang L. Defective histone acetylation is responsible for the diminished expression of cyclooxygenase 2 in idiopathic pulmonary fibrosis. Mol Cell Biol. 2009; 29 (15). 4325-4339
39. Mitani Y, Oue N, Hamai Y, Aung PP, et al. Histone H3 acetylation is associated with reduced p21(WAF1/CIP1) expression by gastric carcinoma. J Pathol. 2005; 205 (1). 65-73
40. Xiaomeng X, Ming Z, Jiezhi M, Xiaoling F. Aberrant histone acetylation and methylation levels in woman with endometriosis. Arch Gynecol Obstet. 2013; 287 (3). 487-494
41. Lu Y, Nie J, Liu X, Zheng Y, Guo SW. Trichostatin A, a histone deacetylase inhibitor, reduces lesion growth and hyperalgesia in experimentally induced endometriosis in mice. Hum Reprod. 2010; 25 (4). 1014-1025
42. Schübeler D, MacAlpine DM, Scalzo D, et al. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 2004; 18 (11). 1263-1271
43. Grandjean V, O'Neill L, Sado T, Turner B, Ferguson-Smith A. Relationship between DNA methylation, histone H4 acetylation and gene expression in the mouse imprinted Igf2-H19 domain. FEBS Lett. 2001; 488 (3). 165-169
44. Wang Z, Zang C, Rosenfeld JA, et al. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet. 2008; 40 (7). 897-903
45. Bernstein BE, Kamal M, Lindblad-Toh K, et al. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell. 2005; 120 (2). 169-181
46. Nishida H, Suzuki T, Kondo S, Miura H, Fujimura Y, Hayashizaki Y. Histone H3 acetylated at lysine 9 in promoter is associated with low nucleosome density in the vicinity of transcription start site in human cell. Chromosome Res. 2006; 14 (2). 203-211
47. Heintzman ND, Hon GC, Hawkins RD, et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature. 2009; 459 (7243). 108-112
48. Roh TY, Ngau WC, Cui K, Landsman D, Zhao K. High-resolution genome-wide mapping of histone modifications. Nat Biotechnol. 2004; 22 (8). 1013-1016
49. Kondo Y, Shen L, Issa JP. Critical role of histone methylation in tumor suppressor gene silencing in colorectal cancer. Mol Cell Biol. 2003; 23 (1). 206-215
50. Voss AK, Collin C, Dixon MP, Thomas T. Moz and retinoic acid coordinately regulate H3K9 acetylation, Hox gene expression, and segment identity. Dev Cell. 2009; 17 (5). 674-686
51. Mohamed MA, Greif PA, Diamond J, et al. Epigenetic events, remodelling enzymes and their relationship to chromatin organization in prostatic intraepithelial neoplasia and prostatic adenocarcinoma. BJU Int. 2007; 99 (4). 908-915
52. Seligson DB, Horvath S, McBrian MA, et al. Global levels of histone modifications predict prognosis in different cancers. Am J Pathol. 2009; 174 (5). 1619-1628
53. Seligson DB, Horvath S, Shi T, et al. Global histone modification patterns predict risk of prostate cancer recurrence. Nature. 2005; 435 (7046). 1262-1266
54. Barlési F, Giaccone G, Gallegos-Ruiz MI, et al. Global histone modifications predict prognosis of resected non small-cell lung cancer. J Clin Oncol. 2007; 25 (28). 4358-4564
55. Abujamra AL, Dos Santos MP, Roesler R, Schwartsmann G, Brunetto AL. Histone deacetylase inhibitors: a new perspective for the treatment of leukemia. Leuk Res. 2010; 34 (6). 687-695
56. Krejcí J, Uhlírová R, Galiová G, Kozubek S, Smigová J, Bártová E. Genome-wide reduction in H3K9 acetylation during human embryonic stem cell differentiation. J Cell Physiol. 2009; 219 (3). 677-687
57. Sadikovic B, Andrews J, Carter D, Robinson J, Rodenhiser DI. Genome-wide H3K9 histone acetylation profiles are altered in benzopyrene-treated MCF7 breast cancer cells. J Biol Chem. 2008; 283 (7). 4051-4060
58. Sadikovic B, Andrews J, Carter D, Robinson J, Rodenhiser DI. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat Genet. 2005; 37 (4). 391-400
59. Pfister S, Rea S, Taipale M, et al. The histone acetyltransferase hMOF is frequently downregulated in primary breast carcinoma and medulloblastoma and constitutes a biomarker for clinical outcome in medulloblastoma. Int J Cancer. 2008; 122 (6). 1207-1213
60. Kapoor-Vazirani P, Kagey JD, Powell DR, Vertino PM. Role of hMOF-dependent histone H4 lysine 16 acetylation in the maintenance of TMS1/ASC gene activity. Cancer Res. 2008; 68 (16). 6810-6821
61. He C, Xu J, Zhang J, et al. High expression of trimethylated histone H3 lysine 4 is associated with poor prognosis in hepatocellular carcinoma. Human Pathol. 2012; 43 (9). 1425-1435
62. Ellinger J, Kahl P, von der Gathen J, et al. Global levels of histone modifications predict prostate cancer recurrence. Prostate. 2010; 70 (1). 61-69
63. Lan F, Bayliss PE, Rinn JL, et al. A histone H3 lysine 27 demethylase regulates animal posterior development. Nature. 2007; 449 (7163). 689-694
64. Bernstein BE, Mikkelsen TS, Xie X, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell. 2006; 125 (2). 315-326
65. Khromov T, Pantakani DV, Nolte J, et al. Global and gene-specific histone modification profiles of mouse multipotent adult germline stem cells. Mol Hum Reprod. 2011; 17 (3). 166-174
66. Pfluger J, Wagner D. Histone modifications and dynamic regulation of genome accessibility in plants. Curr Opin Plant Biol. 2007; 10 (6). 645-652
67. Katoh H, Qin ZS, Liu R, et al. FOXP3 orchestrates H4K16 acetylation and H3K4 trimethylation for activation of multiple genes by recruiting MOF and causing displacement of PLU-1. Mol Cell. 2011; 44 (5). 770-784
68. Seeber LM, van Diest PJ. Epigenetics in ovarian cancer. Methods Mol Biol. 2012; 863: 253-269
69. Crea F. Histone code, human growth and cancer. Oncotarget. 2012; 3 (1). 1-2
70. Munro SK, Farquhar CM, Mitchell MD, Ponnampalam AP. Epigenetic regulation of endometrium during the menstrual cycle. Mol Hum Reprod. 2010; 16 (5). 297-310
71. Sakai N, Maruyama T, Sakurai R, et al. Involvement of histone acetylation in ovarian steroid-induced decidualization of human endometrial stromal cells. J Biol Chem. 2003; 278 (19). 16675-16682
72. Kooistra SM, Helin K. Molecular mechanisms and potential functions of histone demethylases. Nat Rev Mol Cell Biol. 2012; 13 (5). 297-311
73. Brykczynska U, Hisano M, Erkek S, et al. Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat Struct Mol Biol. 2010; 17 (6). 679-687
74. Margueron R, Reinberg D. Chromatin structure and the inheritance of epigenetic information. Nat Rev Genet. 2010; 11 (4). 285-296
75. Zhu B. Reinberg D. Epigenetic inheritance: uncontested? Cell Res. 2011; 21 (3). 435-441
76. Feinberg AP. An epigenetic approach to cancer etiology. Cancer j. 2007; 13 (1). 70-74
77. Taylor HS, Arici A, Olive D, Igarashi P. HOXA10 is expressed in response to sex steroids at the time of implantation in the human endometrium. J Clin Invest. 1998; 101 (7). 1379-1384
78. Troiano RN, Taylor KJ. Sonographically guided therapeutic aspiration of benign-appearing ovarian cysts and endometriomas. AJR Am J Roentgenol. 1998; 171 (6). 1601-1605
79. Wu Y, Halverson G, Basir Z, Strawn E, Yan P, Guo SW. Aberrant methylation at HOXA10 may be responsible for its aberrant expression in the endometrium of patients with endometriosis. Am J Obstet Gynecol. 2005; 193 (2). 371-380
80. Yoshikawa M, Hishikawa K, Marumo T, Fujita T. Inhibition of histone deacetylase activity suppresses epithelial-to-mesenchymal transition induced by TGF-beta1 in human renal epithelial cells. J Am Soc Nephrol. 2007; 18 (1). 58-65
81. Xue Q, Lin Z, Cheng YH, et al. Promoter methylation regulates estrogen receptor 2 in human endometrium and endometriosis. Biol Reprod. 2007; 77 (4). 681-687
82. Xue Q, Lin Z, Yin P, et al. Transcriptional activation of steroidogenic factor-1 by hypomethylation of the 5′ CpG island in endometriosis. J Clin Endocrinol Metab. 2007; 92 (8). 3261-3267
83. Noonan EJ, Place RF. Pookot D, et al. miR-449a targets HDAC-1 and induces growth arrest in prostate cancer. Oncogene. 2009; 28 (14). 1714-1724