Epigenetic aberration of gene expression in endometriosis
Open accessAbstract
Endometriosis is an estrogen-dependent inflammatory disease. In endometriotic tissues, a high-estrogen environment associated with up-regulation of the aromatase gene has been well documented. There is accumulating evidence supporting a concept that endometriosis is a disease associated with an epigenetic disorder. Epigenetics is one of the most expanding fields in the current biomedical research. The word 'epigenetics' refers to the study of mitotically and/or meiotically heritable changes in gene expression that occur without changes in the DNA sequence. The disruption of such changes (epigenetic aberration or disorder) underlies a wide variety of pathologies. Epigenetic regulation includes DNA methylation and histone modifications, and is responsible for a number of gene transcription associated with chromatin modifications that distinguish the states of diseases. In this review, we summarized our studies as well as recent studies from other laboratories using an epigenetic approach focused on DNA methylation. We also summarized studies using advanced technologies including Genome-Wide (GW) methylation profiling analysis and GW Association Study (GWAS). We reviewed recent monozygotic twins studies in relation to environmental factors since they may provide insight into the epigenetic background of endometriosis. Finally, we referred to a new concept of GW DNA methylation.
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Increased proliferation, invasion, and resistance to apoptosis may potentially explain the pathogenesis of endometriosis; several of these characteristic behaviors have been previously linked to epigenetic alterations.
“Increased proliferation, invasion, and resistance to apoptosis may potentially explain the pathogenesis of endometriosis; several of these characteristic behaviors of endometriosis have been previously linked to epigenetic alterations.23,24”
From Altered genome-wide methylation in endometriosis (2014) · cites this paper as [23]
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Jenuwein, T., & Allis, C. D. (2001) · Science · doi:10.1126/science.1063127 · Cited by 9,756 · see citing works
Jaenisch, R., & Bird, A. (2003) · Nature Genetics · doi:10.1038/ng1089 · Cited by 6,325 · see citing works
Jones, P. A., & Baylin, S. B. (2007) · Cell · doi:10.1016/j.cell.2007.01.029 · Cited by 4,515 · see citing works
Esteller, M. (2008) · New England Journal of Medicine · doi:10.1056/nejmra072067 · Cited by 3,681 · see citing works
Sampson, J. A. (1927) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(15)30003-x · Cited by 2,334 · see citing works
Irizarry, R. A., Ladd-Acosta, C., Wen, B., Wu, Z., Montano, C., Onyango, P., Cui, H., Gabo, K., Rongione, M., Webster, M., et al. (2009) · Nature Genetics · doi:10.1038/ng.298 · Cited by 2,177 · see citing works
Cancer epigenomics: DNA methylomes and histone-modification maps
Esteller, M. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2005 · Cited by 2,150 · see citing works
Fraga, M. F., Ballestar, E., Villar‐Garea, A., Boix-Chornet, M., Espada, J., Schotta, G., Bonaldi, T., Haydon, C. E., Ropero, S., Petrie, K. R., et al. (2005) · Nature Genetics · doi:10.1038/ng1531 · Cited by 1,926 · see citing works
An operational definition of epigenetics: Figure 1.Preprint
Berger, S. L., Kouzarides, T., Shiekhattar, R., & Shilatifard, A. (2009) · Genes & Development · doi:10.1101/gad.1787609 · Cited by 1,889 · see citing works
The Origin and Pathogenesis of Epithelial Ovarian Cancer: A Proposed Unifying Theory
Kurman, R. J., & Shih, I. (2010) · The American Journal of Surgical Pathology · doi:10.1097/pas.0b013e3181cf3d79 · Cited by 1,850 · see citing works
Conserved role of intragenic DNA methylation in regulating alternative promoters
Maunakea, A. K., Nagarajan, R. P., Bilenky, M., Ballinger, T. J., D’Souza, C., Fouse, S. D., Johnson, B. E., Hong, C., Nielsen, C., Zhao, Y., et al. (2010) · Nature · doi:10.1038/nature09165 · Cited by 1,743 · see citing works
Principles and challenges of genome-wide DNA methylation analysis
Laird, P. W. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2732 · Cited by 1,574 · see citing works
E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells.
Frixen, U. H., Behrens, J., Sachs, M., Eberle, G., Voß, B., Warda, A., Löchner, D., & Birchmeier, W. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.113.1.173 · Cited by 1,550 · see citing works
DNA methylation profiling of human chromosomes 6, 20 and 22
Eckhardt, F., Lewin, J., Cortese, R., Rakyan, V. K., Attwood, J., Burger, M., Burton, J. H., Cox, T. V., Davies, R., Down, T. A., et al. (2006) · Nature Genetics · doi:10.1038/ng1909 · Cited by 1,350 · see citing works
Cancer epigenetics reaches mainstream oncology
Rodríguez‐Paredes, M., & Esteller, M. (2011) · Nature Medicine · doi:10.1038/nm.2305 · Cited by 1,207 · see citing works
Lillycrop, K. A., Phillips, E. S., Jackson, A. A., Hanson, M. A., & Burdge, G. C. (2005) · Journal of Nutrition · doi:10.1093/jn/135.6.1382 · Cited by 1,139 · see citing works
Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcytosine
Song, C., Szulwach, K. E., Fu, Y., Dai, Q., Yi, C., Li, X., Li, Y., Chen, C.-H., Zhang, W., Jian, X., et al. (2010) · Nature Biotechnology · doi:10.1038/nbt.1732 · Cited by 1,089 · see citing works
Molecular pathogenesis and extraovarian origin of epithelial ovarian cancer—Shifting the paradigm
Kurman, R. J., & Shih, I. (2011) · Human Pathology · doi:10.1016/j.humpath.2011.03.003 · Cited by 1,076 · see citing works
DNA Methylation Decreases in Aging But Not in Immortal Cells
Wilson, V. L., & Jones, P. A. (1983) · Science · doi:10.1126/science.6844925 · Cited by 649 · see citing works
Aromatase expression in endometriosis.
Noble, L. S., Simpson, E. R., Johns, A., & Bulun, S. E. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.1.8550748 · Cited by 566 · see citing works
A common trans-acting factor, Ad4-binding protein, to the promoters of steroidogenic P-450s.
Morohashi, K.-I., Honda, S., Inomata, Y., Handa, H., & Omura, T. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)37129-7 · Cited by 537 · see citing works
Bulun, S. E., Lin, Z., Imir, G., Amin, S., Demura, M., Yilmaz, B., Martin, R., Utsunomiya, H., Thung, S., Gurates, B., et al. (2005) · Pharmacological Reviews · doi:10.1124/pr.57.3.6 · Cited by 531 · see citing works
Progesterone Receptor Isoform A But Not B Is Expressed in Endometriosis
Attia, G. R. (2000) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.85.8.2897 · Cited by 488 · see citing works
Chromatin higher-order structures and gene regulation
Li, G., & Reinberg, D. (2011) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2011.01.022 · Cited by 454 · see citing works
Progesterone resistance in endometriosis: link to failure to metabolize estradiol.
Bulun, S. E., Cheng, Y.-H., Yin, P., Imir, G., Utsunomiya, H., Attar, E., Innes, J., & Julie Kim, J. (2006) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2005.11.041 · Cited by 397 · see citing works
HOX gene expression is altered in the endometrium of women with endometriosis
Taylor, H. S. (1999) · Human Reproduction · doi:10.1093/humrep/14.5.1328 · Cited by 372 · see citing works
Promoter Methylation Regulates Estrogen Receptor 2 in Human Endometrium and Endometriosis1
Xue, Q., Lin, Z., Cheng, Y.-H., Huang, C.-C., Marsh, E., Yin, P., Milad, M. P., Confino, E., Reierstad, S., Innes, J., et al. (2007) · Biology of Reproduction · doi:10.1095/biolreprod.107.061804 · Cited by 346 · see citing works
Olive, D. L., & Pritts, E. A. (2001) · New England Journal of Medicine · doi:10.1056/nejm200107263450407 · Cited by 340 · see citing works
Guo, S.-W. (2009) · Molecular Human Reproduction · doi:10.1093/molehr/gap064 · Cited by 328 · see citing works
Promoter Hypermethylation of Progesterone Receptor Isoform B (PR-B) in Endometriosis
Wu, Y., Strawn, E., Basir, Z., Halverson, G., & Guo, S. (2006) · Epigenetics · doi:10.4161/epi.1.2.2766 · Cited by 323 · see citing works
Cortessis, V. K., Thomas, D. C., Levine, A. J., Breton, C. V., Mack, T. M., Siegmund, K. D., Haile, R. W., & Laird, P. W. (2012) · Human Genetics · doi:10.1007/s00439-012-1189-8 · Cited by 319 · see citing works
The role of cytokines in endometriosis
Wu, M., & Ho, H. (2003) · American Journal of Reproductive Immunology · doi:10.1034/j.1600-0897.2003.01207.x · Cited by 317 · see citing works
Brosens, J. J., Hayashi, N., & WHITE, J. O. (1999) · Endocrinology · doi:10.1210/endo.140.10.7070 · Cited by 316 · see citing works
Genome-wide association study identifies a locus at 7p15.2 associated with endometriosis
Painter, J. N., Anderson, C. A., Nyholt, D. R., Macgregor, S., Lin, J., Lee, S. H., Lambert, A., Zhao, Z. Z., Roseman, F., Guo, Q., et al. (2011) · Nature Genetics · doi:10.1038/ng.731 · Cited by 308 · see citing works
Kitawaki, J., Noguchi, T., Amatsu, T., Maeda, K., Tsukamoto, K., Yamamoto, T., Fushiki, S., Osawa, Y., & Honjo, H. (1997) · Biology of Reproduction · doi:10.1095/biolreprod57.3.514 · Cited by 305 · see citing works
Wu, Y., Halverson, G., Basir, Z., Strawn, E., Yan, P., & Guo, S.-W. (2005) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2005.01.034 · Cited by 283 · see citing works
Endometriosis: an inflammatory disease with a Th2 immune response component
Podgaec, S., Abrão, M. S., Dias, J., Rizzo, L. V., de Oliveira, R. M., & Baracat, E. C. (2007) · Human Reproduction · doi:10.1093/humrep/del516 · Cited by 279 · see citing works
Dlugi, A. M., Miller, J. D., & Knittle, J. (1990) · Fertility and Sterility · doi:10.1016/s0015-0282(16)53755-8 · Cited by 279 · see citing works
Uno, S., Zembutsu, H., Hirasawa, A., Takahashi, A., Kubo, M., Akahane, T., Aoki, D., Kamatani, N., Hirata, K., & Nakamura, Y. (2010) · Nature Genetics · doi:10.1038/ng.612 · Cited by 259 · see citing works
Aromatase and other steroidogenic genes in endometriosis: translational aspects.
Attar, E., & Bulun, S. E. (2006) · Human Reproduction Update · doi:10.1093/humupd/dmi034 · Cited by 255 · see citing works
Sarg, B., Koutzamani, E., Helliger, W., Rundquist, I., & Lindner, H. H. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m205166200 · Cited by 252 · see citing works
Progestins for symptomatic endometriosis: a critical analysis of the evidence
Vercellini, P., Cortesi, I., & Crosignani, P. G. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00193-3 · Cited by 229 · see citing works
Dmowski, W. P., & Braun, D. P. (2004) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2004.02.001 · Cited by 225 · see citing works
Environmental and nutritional effects on the epigenetic regulation of genes
Feil, R. (2006) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2006.05.029 · Cited by 223 · see citing works
Xue, Q., Lin, Z., Yin, P., Milad, M. P., Cheng, Y.-H., Confino, E., Reierstad, S., & Bulun, S. E. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-0494 · Cited by 219 · see citing works
Zeitoun, K., Takayama, K., Michael, M. D., & Bulun, S. E. (1999) · Molecular Endocrinology · doi:10.1210/mend.13.2.0229 · Cited by 216 · see citing works
A Shared Promoter Element Regulates the Expression of Three Steridogenic Enzymes
Rice, D. A., Mouw, A. R., Bogerd, A. M., & Parker, K. L. (1991) · Molecular Endocrinology · doi:10.1210/mend-5-10-1552 · Cited by 206 · see citing works
Lee, B., Du, H., & Taylor, H. S. (2009) · Biology of Reproduction · doi:10.1095/biolreprod.108.070391 · Cited by 204 · see citing works
Epigenetics and twins: three variations on the theme
Petronis, A. (2006) · Trends in Genetics · doi:10.1016/j.tig.2006.04.010 · Cited by 193 · see citing works
Progesterone Receptor Isoform A But Not B Is Expressed in Endometriosis1
Attia, G. R., Zeitoun, K., Edwards, D., Johns, A., Carr, B. R., & Bulun, S. E. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.8.6739 · Cited by 193 · see citing works
Iwabe, T., Harada, T., Tsudo, T., Tanikawa, M., Onohara, Y., & Terakawa, N. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00049-1 · Cited by 189 · see citing works
Age-related epigenetic changes and the immune system
Issa, J. J. (2003) · Clinical Immunology · doi:10.1016/s1521-6616(03)00203-1 · Cited by 181 · see citing works
Intragenic DNA methylation: implications of this epigenetic mechanism for cancer research
Shenker, N. S., & Flanagan, J. M. (2011) · British Journal of Cancer · doi:10.1038/bjc.2011.550 · Cited by 180 · see citing works
Dendritic cell populations in the eutopic and ectopic endometrium of women with endometriosis
Schulke, L., Berbic, M., Manconi, F., Tokushige, N., Markham, R., & Fraser, I. S. (2009) · Human Reproduction · doi:10.1093/humrep/dep071 · Cited by 176 · see citing works
Lessey, B. A., Metzger, D. A., Haney, A. F., & McCarty, K. S. (1989) · Fertility and Sterility · doi:10.1016/s0015-0282(16)60545-9 · Cited by 176 · see citing works
Chang, E. C., Charn, T. H., Park, S.-H., Helferich, W. G., Komm, B. S., Katzenellenbogen, J. A., & Katzenellenbogen, B. S. (2008) · Molecular Endocrinology · doi:10.1210/me.2007-0356 · Cited by 168 · see citing works
Brandenberger, A. W. (1999) · Molecular Human Reproduction · doi:10.1093/molehr/5.7.651 · Cited by 165 · see citing works
Tryndyak, V., Kovalchuk, O., & Pogribny, I. P. (2006) · Cancer Biology & Therapy · doi:10.4161/cbt.5.1.2288 · Cited by 158 · see citing works
Antsiferova, Y. S., Sotnikova, N. Y., Посисеева, Л. В., & Shor, A. L. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.05.066 · Cited by 155 · see citing works
Sakamoto, Y., Harada, T., Horie, S., Iba, Y., Taniguchi, F., Yoshida, S., Iwabe, T., & Terakawa, N. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020666 · Cited by 153 · see citing works
Aging and Cancer: Issues of Basic and Clinical Science
Ershler, W. B., & Longo, D. L. (1997) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/89.20.1489 · Cited by 151 · see citing works
Pogribny, I. P., Ross, S. A., Tryndyak, V., Pogribna, M., Poirier, L. A., & Karpinets, T. V. (2006) · Carcinogenesis · doi:10.1093/carcin/bgi364 · Cited by 149 · see citing works
Pathways linking the early environment to long-term health and lifespan
Barnes, S. K., & Ozanne, S. E. (2010) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2010.12.005 · Cited by 143 · see citing works
Trukhacheva, E., Lin, Z., Reierstad, S., Cheng, Y.-H., Milad, M., & Bulun, S. E. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-1466 · Cited by 143 · see citing works
Incidence, symptoms, and signs of endometriosis in fertile and infertile women.
Bs, V. (1987) · PubMed · Cited by 141 · see citing works
Taylor, H. S., Arici, A. M., Olive, D. L., & Igarashi, P. (1998) · Journal of Clinical Investigation · doi:10.1172/jci1057 · Cited by 131 · see citing works
Genome-wide cDNA microarray analysis of gene-expression profiles involved in ovarian endometriosis.
Arimoto, T., Katagiri, T., Oda, K., Tsunoda, T., Yasugi, T., Osuga, Y., Yoshikawa, H., Nishii, O., Yano, T., Taketani, Y., et al. (2003) · PubMed · Cited by 125 · see citing works
Estrogen production in endometriosis and use of aromatase inhibitors to treat endometriosis.
Bulun, S. E., Zeitoun, K. M., Takayama, K., Noble, L., Michael, D., Simpson, E. R., Johns, A., Putman, M., & Sasano, H. (1999) · Endocrine Related Cancer · doi:10.1677/erc.0.0060293 · Cited by 124 · see citing works
Expression of oestrogen receptor-alpha and -beta in ovarian endometriomata
Fujimoto, J. (1999) · Molecular Human Reproduction · doi:10.1093/molehr/5.8.742 · Cited by 123 · see citing works
Czyż, W., Morahan, J., Ebers, G., & Ramagopalan, S. (2012) · BMC Medicine · doi:10.1186/1741-7015-10-93 · Cited by 120 · see citing works
Enhanced interleukin-4 expression in patients with endometriosis
Hsu, C., Yang, B.-C., Wu, M., & Huang, K. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)81439-2 · Cited by 120 · see citing works
Shaw, R. W. (1992) · Fertility and Sterility · doi:10.1016/s0015-0282(16)55205-4 · Cited by 119 · see citing works
Developmental origins of adult metabolic disease: concepts and controversies
Simmons, R. A. (2005) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2005.08.004 · Cited by 118 · see citing works
Bornman, D. M., Mathew, S., Alsruhe, J. P., Herman, J. G., & Gabrielson, E. W. (2001) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)61758-0 · Cited by 118 · see citing works
Matsuzaki, S., Canis, M. J., Vaurs‐Barrière, C., Pouly, J.-L., Boespflug‐Tanguy, O., Penault-Llorca, F. M., Dechelotte, P., Dastugue, B., Okamura, K., & Mage, G. (2004) · Molecular Human Reproduction · doi:10.1093/molehr/gah097 · Cited by 117 · see citing works
Steroid receptor and aromatase expression in baboon endometriotic lesions
Fazleabas, A. T., Brudney, A., Chai, D. C., Langoi, D., & Bulun, S. E. (2003) · Fertility and Sterility · doi:10.1016/s0015-0282(03)00982-8 · Cited by 111 · see citing works
Balancing histone methylation activities in psychiatric disorders
Peter, C. J., & Akbarian, S. (2011) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2011.02.003 · Cited by 110 · see citing works
Effect of maternal diet on the epigenome: implications for human metabolic disease
Lillycrop, K. A. (2011) · Proceedings of The Nutrition Society · doi:10.1017/s0029665110004027 · Cited by 108 · see citing works
Interleukin-4 Stimulates Proliferation of Endometriotic Stromal Cells
Ouyang, Z., Hirota, Y., Osuga, Y., Hamasaki, K., Hasegawa, A., Tajima, T., Hirata, T., Koga, K., Yoshino, O., Harada, M., et al. (2008) · American Journal Of Pathology · doi:10.2353/ajpath.2008.071044 · Cited by 105 · see citing works
Wu, Y., Starzinski‐Powitz, A., & Guo, S. (2007) · Reproductive Sciences · doi:10.1177/1933719107302913 · Cited by 104 · see citing works
Adachi, S., Tajima, A., Quan, J., Haino, K., Yoshihara, K., Masuzaki, H., Katabuchi, H., Ikuma, K., Suginami, H., Nishida, N., et al. (2010) · Journal of Human Genetics · doi:10.1038/jhg.2010.118 · Cited by 103 · see citing works
Epigenetic Differences Arise During the Lifetime of Monozygotic Twins
Lipman, T. H., & Tiedje, L. B. (2006) · MCN The American Journal of Maternal/Child Nursing · doi:10.1097/00005721-200605000-00016 · Cited by 100 · see citing works
Nasu, K., Kawano, Y., Tsukamoto, Y., Takano, M., Takai, N., Li, H., Furukawa, Y., Abe, W., Moriyama, M., & Narahara, H. (2011) · Journal of obstetrics and gynaecology research · doi:10.1111/j.1447-0756.2011.01663.x · Cited by 88 · see citing works
Distinct dynamics and distribution of histone methyl-lysine derivatives in mouse development
Biron, V. L., McManus, K. J., Hu, N., Hendzel, M. J., & Underhill, D. A. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.08.038 · Cited by 86 · see citing works
Tryndyak, V. (2005) · Carcinogenesis · doi:10.1093/carcin/bgl050 · Cited by 84 · see citing works
Izawa, M., Harada, T., Taniguchi, F., Ohama, Y., Takenaka, Y., & Terakawa, N. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.03.078 · Cited by 83 · see citing works
Self-citationBrosens, J. J. (1999) · Endocrinology · doi:10.1210/en.140.10.4809 · Cited by 76 · see citing works
Wu, Y., Starzinski‐Powitz, A., & Guo, S. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.06.008 · Cited by 73 · see citing works
Izawa, M., Taniguchi, F., Uegaki, T., Takai, E., Iwabe, T., Terakawa, N., & Harada, T. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.06.024 · Cited by 73 · see citing works
Self-citationUpstream stimulatory factor-2 regulates steroidogenic factor-1 expression in endometriosis
Utsunomiya, H., Cheng, Y.-H., Lin, Z., Reierstad, S., Yin, P., Attar, E., Xue, Q., Imir, G., Thung, S., Trukhacheva, E., et al. (2008) · Molecular Endocrinology · doi:10.1210/me.2006-0302 · Cited by 72 · see citing works
Dobosy, J. R., Fu, V. X., Desotelle, J. A., Srinivasan, R., Kenowski, M. L., Almassi, N., Weindruch, R. H., Svaren, J. P., & Jarrard, D. F. (2008) · The Prostate · doi:10.1002/pros.20782 · Cited by 70 · see citing works
Prokocimer, M., Margalit, A., & Gruenbaum, Y. (2006) · Journal of Structural Biology · doi:10.1016/j.jsb.2006.02.016 · Cited by 70 · see citing works
Gordon, L., Joo, J. E., Andronikos, R. H., Ollikainen, M., Wallace, E. M., Umstad, M. P., Permezel, M., Oshlack, A., Morley, R., Carlin, J. B., et al. (2011) · Epigenetics · doi:10.4161/epi.6.5.15072 · Cited by 69 · see citing works
Tracing cellular and molecular mechanisms involved in endometriosis
Starzinski‐Powitz, A. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.724 · Cited by 62 · see citing works
The role of survivin in the resistance of endometriotic stromal cells to drug-induced apoptosis
Watanabe, A., Taniguchi, F., Izawa, M., Suou, K., Uegaki, T., Takai, E., Terakawa, N., & Harada, T. (2009) · Human Reproduction · doi:10.1093/humrep/dep305 · Cited by 50 · see citing works
Self-citationDrug-induced apoptosis was markedly attenuated in endometriotic stromal cells
Izawa, M., Harada, T., Deura, I., Taniguchi, F., Iwabe, T., & Terakawa, N. (2005) · Human Reproduction · doi:10.1093/humrep/dei372 · Cited by 43 · see citing works
Self-citationWu, Y., Shi, X., & Guo, S. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.10.049 · Cited by 42 · see citing works
Juhasz‐Böss, I., Fischer, C., Lattrich, C., Skrzypczak, M., Malik, E., Ortmann, O., & Treeck, O. (2010) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-010-1768-7 · Cited by 41 · see citing works
Granulocyte heterochromatin: defining the epigenome
Olins, D. E., & Olins, A. L. (2005) · BMC Cell Biology · doi:10.1186/1471-2121-6-39 · Cited by 34 · see citing works
From Immature Lamin to Premature Aging: Molecular Pathways and Therapeutic Opportunities
Cadiñanos, J., Varela, I., López-Otı́n, C., & Freije, J. M. P. (2005) · Cell Cycle · doi:10.4161/cc.4.12.2202 · Cited by 32 · see citing works
Genome-Wide Association Study Identifies a Locus at 7p15.2 Associated With Endometriosis
Painter, J. N., Anderson, C. A., Nyholt, D. R., MacGregor, S., Lin, J., Lee, S., Lambert, A. W., Zhao, Z., Roseman, F., Guo, Q., et al. (2011) · Obstetrical & Gynecological Survey · doi:10.1097/ogx.0b013e318210cea1 · Cited by 12 · see citing works
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The Origin and Pathogenesis of Endometriosis
Wang, Y., Nicholes, K., & Shih, I. (2019) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathmechdis-012419-032654 · Cited by 466 · see citing works
Guidelines for the design, analysis and interpretation of ‘omics’ data: focus on human endometrium
Altmäe, S., Esteban, F. J., Stavreus-Evers, A., Simón, C., Giudice, L., Lessey, B. A., Horcajadas, J. A., Macklon, N. S., D'Hooghe, T., Campoy, C., et al. (2014) · Human Reproduction Update · doi:10.1093/humupd/dmt048 · Cited by 151 · see citing works
Loss of HDAC3 results in nonreceptive endometrium and female infertility
Kim, T. H., Yoo, J., Choi, K., Shin, J., Leach, R. E., Fazleabas, A. T., Young, S. L., Lessey, B. A., Yoon, H., & Jeong, J. (2019) · Science Translational Medicine · doi:10.1126/scitranslmed.aaf7533 · Cited by 142 · see citing works
Epigenetic Dysregulation in Endometriosis: Implications for Pathophysiology and Therapeutics
Marquardt, R. M., Tran, D. N., Lessey, B. A., Rahman, M. S., & Jeong, J. (2023) · Endocrine Reviews · doi:10.1210/endrev/bnad020 · Cited by 130 · see citing works
Molecular aspects of development and regulation of endometriosis
Aznaurova, Y. B., M.B.Zhumataev, M. B. Z., Roberts, T. K., Aliper, A. M., & Zhavoronkov, A. A. (2014) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-12-50 · Cited by 116 · see citing works
Environmentally Induced Epigenetic Transgenerational Inheritance of Reproductive Disease1
Nilsson, E. E., & Skinner, M. K. (2015) · Biology of Reproduction · doi:10.1095/biolreprod.115.134817 · Cited by 91 · see citing works
Genetic, Epigenetic, and Steroidogenic Modulation Mechanisms in Endometriosis
Zubrzycka, A., Zubrzycki, M., Perdas, E., & Zubrzycka, M. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9051309 · Cited by 97 · see citing works
Sofo, V., Götte, M., Laganà, A. S., Salmeri, F. M., Triolo, O., Sturlese, E., Retto, G., Alfa, M., Granese, R., & Abrão, M. S. (2015) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-015-3739-5 · Cited by 88 · see citing works
Li, Y., Adur, M. K., Kannan, A., Dávila, J., Zhao, Y., Nowak, R. A., Bagchi, M. K., Bagchi, I. C., & Li, Q. (2016) · PLoS ONE · doi:10.1371/journal.pone.0165347 · Cited by 88 · see citing works
Altered genome-wide methylation in endometriosis
Naqvi, H., Ilagan, Y., Krikun, G., & Taylor, H. S. (2014) · Reproductive Sciences · doi:10.1177/1933719114532841 · Cited by 82 · see citing works
Kobayashi, H., Imanaka, S., Nakamura, H., & Tsuji, A. (2014) · Molecular Medicine Reports · doi:10.3892/mmr.2014.2057 · Cited by 79 · see citing works
Role of Oxidative Stress in Epigenetic Modification in Endometriosis
Ito, F., Yamada, Y., 重光, 愛., Akinishi, M., Kaniwa, H., Miyake, R., Yamanaka, S., & Kobayashi, H. (2017) · Reproductive Sciences · doi:10.1177/1933719117704909 · Cited by 79 · see citing works
Identifying the Biological Basis of GWAS Hits for Endometriosis1
Fung, J. N., Rogers, P. A. W., & Montgomery, G. W. (2015) · Biology of Reproduction · doi:10.1095/biolreprod.114.126458 · Cited by 69 · see citing works
Monsivais, D., Dyson, M. T., Yin, P., Navarro, A., Coon, J. S., Pavone, M. E., & Bulun, S. E. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.01.012 · Cited by 62 · see citing works
Wan, S., Sun, Y., Zong, J., Meng, W., Yan, J., Chen, K., Wang, S., Guo, D., Xiao, Z., Zhou, Q., et al. (2023) · Cell Death and Disease · doi:10.1038/s41419-023-05866-1 · Cited by 63 · see citing works
The epigenetic correlation among ovarian cancer, endometriosis and PCOS: A review
Throwba, H., Unnikrishnan, L., Pangath, M., Vasudevan, K., Jayaraman, S., Li, M., Iyaswamy, A., Palaniyandi, K., & Gnanasampanthapandian, D. (2022) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2022.103852 · Cited by 55 · see citing works
A Review of the Epigenetic Contributions to Endometriosis
Grimstad, F. W., & DeCherney, A. H. (2017) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0000000000000298 · Cited by 51 · see citing works
Endometriosis research in the -omics era
Goulielmos, G. N., Matalliotakis, M., Matalliotaki, C., Eliopoulos, E., Matalliotakis, I., & Zervou, M. I. (2020) · Gene · doi:10.1016/j.gene.2020.144545 · Cited by 49 · see citing works
Mita, S., Shimizu, Y., Sato, A., Notsu, T., Imada, K., & Kyo, S. (2013) · Fertility and Sterility · doi:10.1016/j.fertnstert.2013.10.038 · Cited by 43 · see citing works
Shan, J., Li, D., & Wang, X.-Q. (2023) · Biomolecules · doi:10.3390/biom13030430 · Cited by 40 · see citing works
Szukiewicz, D., Stangret, A., Ruiz‐Ruiz, C., Olivares, E. G., Şoriţău, O., Șușman, S., & Szewczyk, G. (2021) · Stem Cell Reviews and Reports · doi:10.1007/s12015-020-10115-5 · Cited by 41 · see citing works
Redox regulation of microRNAs in endometriosis-associated pain
Wright, K. R., Mitchell, B. L., & Santanam, N. (2017) · Redox Biology · doi:10.1016/j.redox.2017.04.037 · Cited by 40 · see citing works
Novel agents for the medical treatment of endometriosis
Platteeuw, L., & D’Hooghe, T. (2014) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0000000000000084 · Cited by 32 · see citing works
Epigenetic dysregulation of endometriosis susceptibility genes (Review)
Koike, N., Higashiura, Y., Akasaka, J., Uekuri, C., Ito, F., & Kobayashi, H. (2015) · Molecular Medicine Reports · doi:10.3892/mmr.2015.3635 · Cited by 25 · see citing works
Loss of CDYL Results in Suppression of CTNNB1 and Decreased Endometrial Receptivity
Zhou, X., Xu, B., Zhang, D., Jiang, X., Chang, H., Leung, P. C. K., Xia, X., & Zhang, A. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00105 · Cited by 25 · see citing works
Joshi, N., Kohan‐Ghadr, H., Roqueiro, D., Yoo, J., Fru, K. N., Hestermann, E. V., Yuan, L., Ho, S., Jeong, J., Young, S. L., et al. (2021) · Molecular Human Reproduction · doi:10.1093/molehr/gaab018 · Cited by 23 · see citing works
Kobayashi, H., Uekuri, C., & Shigetomi, H. (2013) · Gynecological Endocrinology · doi:10.3109/09513590.2013.831832 · Cited by 21 · see citing works
Izawa, M., Taniguchi, F., & Harada, T. (2018) · American Journal of Reproductive Immunology · doi:10.1111/aji.13078 · Cited by 24 · see citing works
Self-citationCurbing Inflammation in Multiple Sclerosis and Endometriosis: Should Mast Cells Be Targeted?
Hart, D. A. (2015) · International Journal of Inflammation · doi:10.1155/2015/452095 · Cited by 19 · see citing works
Innovations in classical hormonal targets for endometriosis
Pluchino, N., Freschi, L., Wenger, J., & Streuli, I. (2015) · Expert Review of Clinical Pharmacology · doi:10.1586/17512433.2016.1129895 · Cited by 19 · see citing works
Mahajan, V., Farquhar, C. M., & Ponnampalam, A. P. (2019) · Molecular Reproduction and Development · doi:10.1002/mrd.23299 · Cited by 18 · see citing works
Imprinting genes associated with endometriosis
Kobayashi, H. (2014) · Europe PMC (PubMed Central) · doi:10.17877/de290r-176 · Cited by 14 · see citing works
Yan, H.-J., Zhou, S., Yang, L., Zhang, H., Deng, C.-Y., Qi, H., & Li, F. (2015) · Experimental Cell Research · doi:10.1016/j.yexcr.2015.12.015 · Cited by 11 · see citing works
Genes Downregulated in Endometriosis Are Located Near the Known Imprinting Genes
Kobayashi, H., Higashiura, Y., Koike, N., Akasaka, J., Uekuri, C., Iwai, K., Niiro, E., Morioka, S., & Yamada, Y. (2014) · Reproductive Sciences · doi:10.1177/1933719114526473 · Cited by 10 · see citing works
Liu, T., Xiao, L. Y., Pei, T., Luo, B., Tan, J., Long, Y., Huang, X. H., Ouyang, Y., & Huang, W. (2022) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.15526 · Cited by 9 · see citing works
Szukiewicz, D. (2022) · Vitamins and hormones · doi:10.1016/bs.vh.2022.11.005 · Cited by 10 · see citing works
OMICs Studies and Endometriosis Biomarker Identification
Saare, M., Peters, M., Aints, A., Laisk, T., Salumets, A., & Altmäe, S. (2017) · Springer eBooks · doi:10.1007/978-3-319-59856-7_12 · Cited by 8 · see citing works
Smoking and endometriosis: A narrative review
Vallée, A., Féki, A., Josseran, L., & Ayoubi, J.-M. (2025) · Tobacco Induced Diseases · doi:10.18332/tid/203429 · Cited by 5 · see citing works
Epigenetic background of the most common non-oncologic gynecological diseases
Joó, J. G., Csatlós, É., Brubel, R., Bokor, A., Karabélyos, C., & Rigó, J. J. (2014) · Orvosi Hetilap · doi:10.1556/oh.2014.29860 · Cited by 1 · see citing works
Review article: IMPRINTING GENES ASSOCIATED WITH ENDOMETRIOSIS
Kobayashi, H. (2014)
Association between DNMT3L polymorphic variants and the risk of endometriosis-associated infertility
Mostowska, A., Szczepańska, M., Wirstlein, P. K., Skrzypczak, J., & Jagodziński, P. P. (2015) · Molecular Medicine Reports · doi:10.3892/mmr.2015.4626
Research in Benign Gynaecology
Gerval, M., & Panay, N. (2017) · Cambridge University Press eBooks · doi:10.1017/9781107585775.030
Discerning Endometriosis as a Multifaceted Entity: A Comprehensive Review
Sah, S. K. (2020) · Biomedical Journal of Scientific & Technical Research · doi:10.26717/bjstr.2020.31.005132
Carcinomas de ovário associados à endometriose
Barreta, A. (2018) · doi:10.47749/t/unicamp.2018.998809
Meidyana, S. (2023) · Bali Medical Journal · doi:10.15562/bmj.v12i1.3816
Classification of Endometriosis: A Systematic Review
Saremi, A. T., & Nateghi, M. R. (2022) · ملیون. · doi:10.61186/sjrm.7.3.195
Luo, Y., Cen, C., Liu, H., Mo, D., Fu, P.-T., Liu, X., Liu, L., Wei, L., Gan, Q., Bi, Y., et al. (2025) · medRxiv · doi:10.1101/2025.02.22.25322723
Importancia de la Transformación Digital en las Organizaciones
Cárdenas, J. E. C. (2025) · Dimensión Empresarial · doi:10.15665/0jgkbb60
- Authors
- Izawa, M.
- Affiliations
- Tottori University (JP)
- Corresponding author
- Izawa, Masao
- Venue
- Frontiers in Bioscience
- Publisher
- IMR Press
- Published
- 2013
- Volume
- E5
- Issue
- 3
- Pages
- 900-910
- ISSN
- 1944-7892 (ISSN-L)
- 1945-0494
- 1945-0508
- DOI
- 10.2741/e669
- OpenAlex
- W2030333317
- Cited by
- 49
- References
- 103
- Citations by year
- 2025: 3 · 2023: 4 · 2022: 4 · 2021: 2 · 2020: 5 · 2019: 3 · 2018: 2 · 2017: 5 · 2016: 2 · 2015: 8 · 2014: 8 · 2013: 3
- FWCI
- 1.14
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Frontiers in Bioscience-Elite (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Japan Society for the Promotion of Science (18591800, 22591824)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Plant and fungal interactions
- Keywords
- endometriosis, epigenetics, DNA methylation, histone modifications, aromatase, estrogen, gene expression regulation, monozygotic twins, environmental factors, genome-wide methylation profiling, genome-wide association study
- MeSH terms
- Endometriosis, Estrogens, Female, Humans, Gene Expression, DNA Methylation, Epigenesis, Genetic, Genome-Wide Association Study
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