The DOI matches its Crossref record; 41 of the 42 references it cites were found in a registry or an index.
Aberrant methylation at HOXA10 may be responsible for its aberrant expression in the endometrium of patients with endometriosis
Abstract
Objective HOXA10, expressed in endometrium, plays an important role in uterine receptivity at the time of implantation. In the endometrium of women with endometriosis, its expression is reduced. The aim of this study was to determine whether the observed aberrant expression of HOXA10 is caused by aberrant methylation of the gene.Study design Endometrial tissues were collected from 6 women with laparoscopically confirmed endometriosis, and 4 women who underwent tubal ligation and were confirmed to have no endometriosis. In addition, menstrual blood from 5 women with no gynecologic complaints was collected and also used as controls. Methylation-specific polymerase chain reaction (PCR) and bisulfite sequencing were performed in 3 fragments in 2 regions of HOXA10 to detect difference in methylation patterns. Real-time reverse transcriptase (RT)-PCR was also performed to measure expression levels of HOXA10 in select cases and controls.Results In all 3 fragments, there were highly statistically significant differences in methylation patterns between women with endometriosis and those without endometriosis. The expression level of HOXA10 was lower in women with endometriosis than those without, as previously reported.Conclusion There is aberrant methylation in the endometrium of women with endometriosis compared with those without endometriosis. The aberrant methylation at HOXA10 may be responsible for the aberrant gene expression in the endometrium of women with endometriosis. This finding suggests that endometriosis may also be an epigenetic disease.
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“these endometrial cells also exhibit hypermethylation of the PR-B promoter, inducing expression of the receptor protein [38,39,40] and finally resulting in a state of progesterone resistance.”
From Endometriosis and Medical Therapy: From Progestogens to Progesterone Resistance to GnRH Antagonists: A Review (2021) · cites this paper as [39]
In the citing paper
“In eutopic endometrial cells of endometriosis patients, HOXA-10 does not show increased expression after ovulation due to hypermethylation and gene silencing of its promoter [39].”
From Endometriosis and Medical Therapy: From Progestogens to Progesterone Resistance to GnRH Antagonists: A Review (2021) · cites this paper as [39]
In the citing paper
“Epigenetic modification is a possible mechanism by which the expression of genes necessary for the establishment of endometriosis is altered.11,12”
From Altered genome-wide methylation in endometriosis (2014) · cites this paper as [12]
In the citing paper
“The hypermethylation of methyltransferase (MGMT) has been reported to decrease apoptotic responses to DNA damage by TP73 and cell proliferation regulation by RBBP7, which in combination with the aberrant expression of HOXA10, increase the susceptibility for endometriosis.12,[41][42][43][44][45][46][47][48]”
From Altered genome-wide methylation in endometriosis (2014) · cites this paper as [12]
Citations
Cites
Jaenisch, R., & Bird, A. (2003) · Nature Genetics · doi:10.1038/ng1089 · Cited by 6,325
Gene Silencing in Cancer in Association with Promoter Hypermethylation
Herman, J. G., & Baylin, S. B. (2003) · New England Journal of Medicine · doi:10.1056/nejmra023075 · Cited by 3,471
Frommer, M., McDonald, L. E., Millar, D. S., Collis, C. M., Watt, F., Grigg, G. W., Molloy, P. L., & Paul, C. L. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.5.1827 · Cited by 3,238
Rw, N., Hertig, A. T., & Rock, J. A. (1950) · Fertility and Sterility · doi:10.1016/s0015-0282(16)30062-0 · Cited by 2,845
MethPrimer: designing primers for methylation PCRs
Li, L.-C., & Dahiya, R. (2002) · Bioinformatics · doi:10.1093/bioinformatics/18.11.1427 · Cited by 2,741
Chromatin modification and epigenetic reprogramming in mammalian development
Li, E. (2002) · Nature Reviews Genetics · doi:10.1038/nrg887 · Cited by 1,900
Eskenazi, B., & Warner, M. L. (1997) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/s0889-8545(05)70302-8 · Cited by 1,617
The power and the promise of DNA methylation markers
Laird, P. W. (2003) · Nature reviews. Cancer · doi:10.1038/nrc1045 · Cited by 1,573
Induction of tumors in mice by genomic hypomethylation
Gaudet, F., Hodgson, J. G., Eden, A., Jackson-Grusby, L., Dausman, J., Gray, J. W., Leonhardt, H., & Jaenisch, R. (2003) · Science · doi:10.1126/science.1083558 · Cited by 1,499
Chromosomal Instability and Tumors Promoted by DNA Hypomethylation
Eden, A., Gaudet, F., Waghmare, A., & Jaenisch, R. (2003) · Science · doi:10.1126/science.1083557 · Cited by 1,401
DNA methylation in health and disease
Robertson, K. D., & Wolffe, A. P. (2000) · Nature Reviews Genetics · doi:10.1038/35049533 · Cited by 1,077
Homeo Boxes in the Study of Development
Gehring, W. J. (1987) · Science · doi:10.1126/science.2884726 · Cited by 899
Kao, L. C., Germeyer, A., Tulac, S., Lobo, S., Yang, J. P., Taylor, R. N., Osteen, K., Lessey, B. A., & Giudice, L. C. (2003) · Endocrinology · doi:10.1210/en.2003-0043 · Cited by 696
Olive, D. L., & Schwartz, L. B. (1993) · New England Journal of Medicine · doi:10.1056/nejm199306173282407 · Cited by 675
Lessey, B. A., Killam, A. P., METZGER, D. A., Haney, A. F., Greene, G. L., & McCarty, K. S. (1988) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-67-2-334 · Cited by 647
Accelerated age-related CpG island methylation in ulcerative colitis.
Issa, J. J., Ahuja, N., Toyota, M., Bronner, M. P., & Brentnall, T. A. (2001) · PubMed · Cited by 627
Loss of Heterozygosity in Normal Tissue Adjacent to Breast Carcinomas
Deng, G., Lü, Y., Zlotnikov, G., Thor, A. D., & Smith, H. S. (1996) · Science · doi:10.1126/science.274.5295.2057 · Cited by 580
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
Stromal estrogen receptors mediate mitogenic effects of estradiol on uterine epithelium
Cooke, P. S., Buchanan, D. L., Young, P., Setiawan, T., Brody, J. R., Korach, K. S., Taylor, J., Lubahn, D. B., & Cunha, G. R. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.12.6535 · Cited by 556
Taylor, H. S., Arici, A. M., Olive, D. L., & Igarashi, P. (1998) · Journal of Clinical Investigation · doi:10.1172/jci1057 · Cited by 555
Sexually dimorphic sterility phenotypes in HoxalO-deficient mice
Satokata, I., Benson, G., & Maas, R. L. (1995) · Nature · doi:10.1038/374460a0 · Cited by 519
Taylor, H. S., Arici, A. M., Olive, D. L., & Igarashi, P. (1998) · Journal of Clinical Investigation · doi:10.1172/jci1597 · Cited by 420
DNA methylation, chromatin inheritance, and cancer
Rountree, M. R., Bachman, K. E., Herman, J. G., & Baylin, S. B. (2001) · Oncogene · doi:10.1038/sj.onc.1204339 · Cited by 389
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 376
Endometriosis results from the dislocation of basal endometrium
Leyendecker, G. (2002) · Human Reproduction · doi:10.1093/humrep/17.10.2725 · Cited by 300
Promoter hypermethylation of multiple genes in nasopharyngeal carcinoma.
Kwong, J., Lo, K. W., To, K., Teo, P. M. L., Johnson, P. J., & Huang, D. P. (2002) · PubMed · Cited by 257
Use of Immunocytochemistry of Progesterone and Estrogen Receptors for Endometrial Dating
García, E., Bouchard, P., de Brux, J., Berdah, J., Frydman, R., SCHAISON, G., Milgröm, E., & Perrot‐Applanat, M. (1988) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-67-1-80 · Cited by 248
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
Press, M. F., Udove, J. A., & Greene, G. L. (1988) · PubMed Central · Cited by 142
Regulation of HOXA-10 and its expression in normal and abnormal endometrium
Gui, Y., Zhang, J., Yuan, L., & Lessey, B. A. (1999) · MHR: Basic science of reproductive medicine · doi:10.1093/molehr/5.9.866 · Cited by 139
Possible involvement of hMLH1, p16INK4a and PTEN in the malignant transformation of endometriosis
Martini, M., Ciccarone, M., Garganese, G., Maggiore, C., Evangelista, A., Rahimi, S., Zannoni, G. F., Vittori, G., & Larocca, L. M. (2002) · International Journal of Cancer · doi:10.1002/ijc.10715 · Cited by 134
Jones, R. K., Bulmer, J. N., & Searle, R. F. (1995) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a135901 · Cited by 129
Epigenetic Variation and Human Disease
Issa, J. J. (2002) · Journal of Nutrition · doi:10.1093/jn/132.8.2388s · Cited by 126
Methylated DNA collected by tampons: a new tool to detect endometrial cancer.
Fiegl, H., Gattringer, C., Widschwendter, A., Schneitter, A., Ramoni, A., Sarlay, D., Gaugg, I., Goebel, G., Müller, H. M., Mueller-Holzner, E., et al. (2004) · Cancer Epidemiology, Biomarkers & Prevention · doi:10.1158/1055-9965.882.13.5 · Cited by 123
Is endometriosis an endometrial disease?
Vinatier, D., Cosson, M., & Dufour, P. (2000) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(99)00263-8 · Cited by 115
The Role of HOX Genes in the Development and Function of the Female Reproductive Tract
Taylor, H. S. (2000) · Seminars in Reproductive Medicine · doi:10.1055/s-2000-13478 · Cited by 101
Nisolle, M., Casanas‐Roux, F., Wyns, C., de MENTEN, Y., Mathieu, P.-E., & Donnez, J. (1994) · Fertility and Sterility · doi:10.1016/s0015-0282(16)57000-9 · Cited by 95
Detection of DNA copy number changes in human endometriosis by comparative genomic hybridization
Gogusev, J., Joliniere, J. B. D., Telvi, L., Doussau, M., du Manoir, S., Stojkoski, A., & Levardon, M. (1999) · Human Genetics · doi:10.1007/s004390051129 · Cited by 93
Widschwendter, M., & Jones, P. A. (2002) · PubMed · Cited by 52
Genomic alterations in the endometrium may be a proximate cause for endometriosis
Guo, S., Wu, Y., Strawn, E., Basir, Z., Wang, Y., Halverson, G., Montgomery, K., & Kajdacsy-Balla, A. (2004) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2004.02.004 · Cited by 46
Self-citationThe potential prognostic, predictive, and therapeutic values of DNA methylation in cancer
Widschwendter, M., & Jones, P. (2002) · UCL Discovery (University College London) · Cited by 21
Cited by
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Laganà, A. S., Garzon, S., Götte, M., Viganò, P., Franchi, M. P., Ghezzi, F., & Martin, D. C. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20225615 · Cited by 503
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 483
Epigenetics across the human lifespan
Kanherkar, R. R., Bhatia-Dey, N., & Csoka, A. B. (2014) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2014.00049 · Cited by 407
Implantation failure: molecular mechanisms and clinical treatment
Çakmak, H., & Taylor, H. S. (2010) · Human Reproduction Update · doi:10.1093/humupd/dmq037 · Cited by 396
Endocrine Regulation of HOX Genes
Daftary, G. S., & Taylor, H. S. (2006) · Endocrine Reviews · doi:10.1210/er.2005-0018 · Cited by 344
Metadata
- Authors
- Wu, Y., Halverson, G., Basir, Z., Strawn, E., Yan, P., & Guo, S.-W.
- Affiliations
- Medical College of Wisconsin (US)
- The Ohio State University (US)
- Corresponding author
- Guo, Sun-Wei
- Venue
- American Journal of Obstetrics and Gynecology
- Publisher
- Elsevier BV
- Published
- 2005-08
- Volume
- 193
- Issue
- 2
- Pages
- 371-380
- ISSN
- 0002-9378 (ISSN-L)
- OpenAlex
- W2076128837
- Cited by
- 283
- References
- 42
- Citations by year
- 2026: 3 · 2025: 11 · 2024: 10 · 2023: 22 · 2022: 13 · 2021: 8 · 2020: 14 · 2019: 18 · 2018: 13 · 2017: 10 · 2016: 23 · 2015: 15 · 2014: 18 · 2013: 16 · 2012: 15
- FWCI
- 8.36
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Obstetrics and Gynecology (publishedVersion)
- PubMed (publishedVersion)
- 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 › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Keywords
- endometriosis, HOXA10, DNA methylation, aberrant gene expression, endometrium, epigenetics, endometrial receptivity, implantation, methylation-specific PCR, bisulfite sequencing
- MeSH terms
- Homeobox A10 Proteins, Base Sequence, DNA-Binding Proteins, Endometriosis, Endometrium, Female, Humans, Polymerase Chain Reaction, Homeodomain Proteins, DNA Methylation, Reverse Transcriptase Polymerase Chain Reaction, Epigenesis, Genetic
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