Genome-Wide DNA Methylation Analysis Reveals a Potential Mechanism for the Pathogenesis and Development of Uterine Leiomyomas

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Maekawa, Ryo ^a   Sato, Shun ^a   Yamagata, Yoshiaki ^a   Asada, Hiromi ^a   Tamura, Isao ^a   Lee, Lifa ^a   Okada, Maki ^a   Tamura, Hiroshi ^a   Takaki, Eiichi ^a   Nakai, Akira ^a   Sugino, Norihiro ^a  

^a YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN; ESTROGEN RECEPTOR ALPHA; MESSENGER RNA;

APOPTOSIS; ARTICLE; CARCINOGENESIS; CLINICAL ARTICLE; COL4A1 GENE; COL4A2 GENE; COL6A3 GENE; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; FEMALE; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC ASSOCIATION; HUMAN; HUMAN TISSUE; IRS1 GENE; JAPANESE; MYOMETRIUM; PATHOGENESIS; PROMOTER REGION; UTERUS MYOMA;

ADULT; APOPTOSIS REGULATORY PROTEINS; CHROMOSOMES, HUMAN, X; COLLAGEN TYPE IV; COLLAGEN TYPE VI; DNA METHYLATION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; INSULIN RECEPTOR SUBSTRATE PROTEINS; LEIOMYOMA; MIDDLE AGED; RECEPTORS, ESTROGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; UTERINE NEOPLASMS;

EID: 84879271613     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066632     Document Type: Article

References (56)

1. Stewart EA, (2001) Uterine fibroids. Lancet 357: 293-298.
2. Bajekal N, Li TC, (2000) Fibroids, infertility and pregnancy wastage. Hum Reprod Update 6: 614-620.
3. Chiaffarino F, Parazzini F, La Vecchia C, Chatenoud L, Di Cintio E, et al. (1999) Diet and uterine myomas. Obstet Gynecol 94: 395-398.
4. Faerstein E, Szklo M, Rosenshein N, (2001) Risk factors for uterine leiomyoma: a practice-based case-control study. I. African-American heritage, reproductive history, body size, and smoking. Am J Epidemiol 153: 1-10.
5. Faerstein E, Szklo M, Rosenshein NB, (2001) Risk factors for uterine leiomyoma: a practice-based case-control study. II. Atherogenic risk factors and potential sources of uterine irritation. Am J Epidemiol 153: 11-19.
6. Shiota K, Yanagimachi R, (2002) Epigenetics by DNA methylation for development of normal and cloned animals. Differentiation 69: 162-166.
7. Lieb JD, Beck S, Bulyk ML, Farnham P, Hattori N, et al. (2006) Applying whole-genome studies of epigenetic regulation to study human disease. Cytogenet Genome Res 114: 1-15.
8. Shiota K, Kogo Y, Ohgane J, Imamura T, Urano A, et al. (2002) Epigenetic marks by DNA methylation specific to stem, germ and somatic cells in mice. Genes Cells 7: 961-969.
9. Iwatani M, Ikegami K, Kremenska Y, Hattori N, Tanaka S, et al. (2006) Dimethyl sulfoxide has an impact on epigenetic profile in mouse embryoid body. Stem Cells 24: 2549-2556.
10. Wu Q, Ohsako S, Ishimura R, Suzuki JS, Tohyama C, (2004) Exposure of mouse preimplantation embryos to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) alters the methylation status of imprinted genes H19 and Igf2. Biol Reprod 70: 1790-1797.
11. Yamagata Y, Maekawa R, Asada H, Taketani T, Tamura I, et al. (2009) Aberrant DNA methylation status in human uterine leiomyoma. Mol Hum Reprod 15: 259-267.
12. Maekawa R, Yagi S, Ohgane J, Yamagata Y, Asada H, et al. (2011) Disease-dependent differently methylated regions (D-DMRs) of DNA are enriched on the X chromosome in uterine leiomyoma. J Reprod Dev 57: 604-612.
13. Navarro A, Yin P, Monsivais D, Lin SM, Du P, et al. (2012) Genome-wide DNA methylation indicates silencing of tumor suppressor genes in uterine leiomyoma. PLoS One 7: e33284.
14. Hitchler MJ, Wikainapakul K, Yu L, Powers K, Attatippaholkun W, et al. (2006) Epigenetic regulation of manganese superoxide dismutase expression in human breast cancer cells. Epigenetics 1: 163-171.
15. Greathouse KL, Bredfeldt T, Everitt JI, Lin K, Berry T, et al. (2012) Environmental estrogens differentially engage the histone methyltransferase EZH2 to increase risk of uterine tumorigenesis. Mol Cancer Res 10: 546-557.
16. Kawakami T, Zhang C, Taniguchi T, Kim CJ, Okada Y, et al. (2004) Characterization of loss-of-inactive X in Klinefelter syndrome and female-derived cancer cells. Oncogene 23: 6163-6169.
17. Sirchia SM, Ramoscelli L, Grati FR, Barbera F, Coradini D, et al. (2005) Loss of the inactive X chromosome and replication of the active X in BRCA1-defective and wild-type breast cancer cells. Cancer Res 65: 2139-2146.
18. Asada H, Yamagata Y, Taketani T, Matsuoka A, Tamura H, et al. (2008) Potential link between estrogen receptor-alpha gene hypomethylation and uterine fibroid formation. Mol Hum Reprod 14: 539-545.
19. Saeed AI, Sharov V, White J, Li J, Liang W, et al. (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34: 374-378.
20. Marinescu V, Kohane I, Riva A, (2005) The MAPPER database: a multi-genome catalog of putative transcription factor binding sites. Nucleic Acids Res 33: D91-97.
21. Huang W, Sherman BT, Tan Q, Kir J, Liu D, et al. (2007) DAVID Bioinformatics Resources: expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acids Res 35: W169-175.
22. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, et al. (2011) Integrative genomics viewer. Nat Biotechnol 29: 24-26.
23. Kumaki Y, Oda M, Okano M, (2008) QUMA: quantification tool for methylation analysis. Nucleic Acids Res 36: W170-175.
24. Feng G, Du P, Krett NL, Tessel M, Rosen S, et al. (2010) A collection of bioconductor methods to visualize gene-list annotations. BMC Res Notes 3: 10.
25. Vanharanta S, Wortham NC, Laiho P, Sjoberg J, Aittomaki K, et al. (2005) 7q deletion mapping and expression profiling in uterine fibroids. Oncogene 24: 6545-6554.
26. Gilden M, Malik M, Britten J, Delgado T, Levy G, et al. (2012) Leiomyoma fibrosis inhibited by liarozole, a retinoic acid metabolic blocking agent. Fertil Steril.
27. Weston G, Trajstman AC, Gargett CE, Manuelpillai U, Vollenhoven BJ, et al. (2003) Fibroids display an anti-angiogenic gene expression profile when compared with adjacent myometrium. Mol Hum Reprod 9: 541-549.
28. Peng DF, Razvi M, Chen H, Washington K, Roessner A, et al. (2009) DNA hypermethylation regulates the expression of members of the Mu-class glutathione S-transferases and glutathione peroxidases in Barrett's adenocarcinoma. Gut 58: 5-15.
29. Morelli C, Garofalo C, Sisci D, del Rincon S, Cascio S, et al. (2004) Nuclear insulin receptor substrate 1 interacts with estrogen receptor alpha at ERE promoters. Oncogene 23: 7517-7526.
30. Esposito DL, Aru F, Lattanzio R, Morgano A, Abbondanza M, et al. (2012) The insulin receptor substrate 1 (IRS1) in intestinal epithelial differentiation and in colorectal cancer. PLoS One 7: e36190.
31. Martoriati A, Doumont G, Alcalay M, Bellefroid E, Pelicci PG, et al. (2005) dapk1, encoding an activator of a p19ARF-p53-mediated apoptotic checkpoint, is a transcription target of p53. Oncogene 24: 1461-1466.
32. Raval A, Tanner SM, Byrd JC, Angerman EB, Perko JD, et al. (2007) Downregulation of death-associated protein kinase 1 (DAPK1) in chronic lymphocytic leukemia. Cell 129: 879-890.
33. Claus R, Hackanson B, Poetsch AR, Zucknick M, Sonnet M, et al. (2012) Quantitative analyses of DAPK1 methylation in AML and MDS. Int J Cancer 131: E138-142.
34. Missaoui N, Hmissa S, Trabelsi A, Traore C, Mokni M, et al. (2011) Promoter hypermethylation of CDH13, DAPK1 and TWIST1 genes in precancerous and cancerous lesions of the uterine cervix. Pathol Res Pract 207: 37-42.
35. Bernard D, Augert A, (2010) NUAK1 links genomic instability and senescence. Aging (Albany NY) 2: 317-319.
36. Hou X, Liu JE, Liu W, Liu CY, Liu ZY, et al. (2011) A new role of NUAK1: directly phosphorylating p53 and regulating cell proliferation. Oncogene 30: 2933-2942.
37. Ono M, Maruyama T, Masuda H, Kajitani T, Nagashima T, et al. (2007) Side population in human uterine myometrium displays phenotypic and functional characteristics of myometrial stem cells. Proc Natl Acad Sci U S A 104: 18700-18705.
38. Ono M, Qiang W, Serna VA, Yin P, Coon JST, et al. (2012) Role of stem cells in human uterine leiomyoma growth. PLoS One 7: e36935.
39. Zhang P, Zhang C, Hao J, Sung CJ, Quddus MR, et al. (2006) Use of X-chromosome inactivation pattern to determine the clonal origins of uterine leiomyoma and leiomyosarcoma. Hum Pathol 37: 1350-1356.
40. White MF, (2002) IRS proteins and the common path to diabetes. Am J Physiol Endocrinol Metab 283: E413-422.
41. Reiss K, Del Valle L, Lassak A, Trojanek J, (2012) Nuclear IRS-1 and cancer. J Cell Physiol 227: 2992-3000.
42. DeAngelis T, Chen J, Wu A, Prisco M, Baserga R, (2006) Transformation by the simian virus 40 T antigen is regulated by IGF-I receptor and IRS-1 signaling. Oncogene 25: 32-42.
43. Valentinis B, Romano G, Peruzzi F, Morrione A, Prisco M, et al. (1999) Growth and differentiation signals by the insulin-like growth factor 1 receptor in hemopoietic cells are mediated through different pathways. J Biol Chem 274: 12423-12430.
44. Cesarone G, Garofalo C, Abrams MT, Igoucheva O, Alexeev V, et al. (2006) RNAi-mediated silencing of insulin receptor substrate 1 (IRS-1) enhances tamoxifen-induced cell death in MCF-7 breast cancer cells. J Cell Biochem 98: 440-450.
45. del Rincon SV, Guo Q, Morelli C, Shiu HY, Surmacz E, et al. (2004) Retinoic acid mediates degradation of IRS-1 by the ubiquitin-proteasome pathway, via a PKC-dependant mechanism. Oncogene 23: 9269-9279.
46. D'Ambrosio C, Keller SR, Morrione A, Lienhard GE, Baserga R, et al. (1995) Transforming potential of the insulin receptor substrate 1. Cell Growth Differ 6: 557-562.
47. Tseng YH, Butte AJ, Kokkotou E, Yechoor VK, Taniguchi CM, et al. (2005) Prediction of preadipocyte differentiation by gene expression reveals role of insulin receptor substrates and necdin. Nat Cell Biol 7: 601-611.
48. Strange RC, Spiteri MA, Ramachandran S, Fryer AA, (2001) Glutathione-S-transferase family of enzymes. Mutat Res 482: 21-26.
49. Townsend DM, Tew KD, (2003) The role of glutathione-S-transferase in anti-cancer drug resistance. Oncogene 22: 7369-7375.
50. Etcheverry A, Aubry M, de Tayrac M, Vauleon E, Boniface R, et al. (2010) DNA methylation in glioblastoma: impact on gene expression and clinical outcome. BMC Genomics 11: 701.
51. Bell A, Bell D, Weber RS, El-Naggar AK, (2011) CpG island methylation profiling in human salivary gland adenoid cystic carcinoma. Cancer 117: 2898-2909.
52. Kearns PR, Chrzanowska-Lightowlers ZM, Pieters R, Veerman A, Hall AG, (2003) Mu class glutathione S-transferase mRNA isoform expression in acute lymphoblastic leukaemia. Br J Haematol 120: 80-88.
53. Skubitz K, Skubitz A, (2003) Differential gene expression in leiomyosarcoma. Cancer 98: 1029-1038.
54. Morelli C, Garofalo C, Bartucci M, Surmacz E, (2003) Estrogen receptor-alpha regulates the degradation of insulin receptor substrates 1 and 2 in breast cancer cells. Oncogene 22: 4007-4016.
55. Sun M, Paciga JE, Feldman RI, Yuan Z, Coppola D, et al. (2001) Phosphatidylinositol-3-OH Kinase (PI3K)/AKT2, activated in breast cancer, regulates and is induced by estrogen receptor alpha (ERalpha) via interaction between ERalpha and PI3K. Cancer Res 61: 5985-5991.
56. Campbell RA, Bhat-Nakshatri P, Patel NM, Constantinidou D, Ali S, et al. (2001) Phosphatidylinositol 3-kinase/AKT-mediated activation of estrogen receptor alpha: a new model for anti-estrogen resistance. J Biol Chem 276: 9817-9824.