MicroRNA 135 regulates HOXA10 expression in endometriosis
Open accessAbstract
CONTEXT: Homeo box A10 (HOXA10) regulates endometrial receptivity and its expression is decreased in women with endometriosis. Although sex steroids regulate HOXA10, these hormones are unaltered in endometriosis. We hypothesized a role for microRNA in the regulation of HOXA10. OBJECTIVE: MicroRNA 135a and -b are small noncoding RNA with predicted targets that include HOXA10. We evaluated miR135a/b expression and HOXA10 regulation in endometrium from subjects with and without endometriosis. DESIGN: The design of the study was the measurement of miR135a/b expression by quantitative PCR and in vitro analysis of HOXA10 regulation. SETTING: The study was conducted at a university medical center. PATIENTS: Patients included 50 controls and 32 women with endometriosis. INTERVENTIONS: Study interventions included endometrial biopsies and in vitro transfection. MAIN OUTCOME MEASURES: miR135a/b and HOXA10 expression were measured in the study. RESULTS: All endometrial samples expressed miR135a and -b. miR135a expression in controls was increased during the proliferative phase, decreased at the time of ovulation, and increased during the luteal phase. Subjects with endometriosis had 3-fold higher expression of miR135a in the proliferative phase than controls. miR135b showed less variation across the menstrual cycle; however, it was significantly increased in women with endometriosis in the proliferative and secretory phases. HOXA10 expression was simultaneously repressed in the endometrium of women with endometriosis. Transfection of endometrial stromal cells with mir135a/b or miR135a/b inhibitors resulted in the altered expression of HOXA10 mRNA and protein. miR135a or -b decreased luciferase expression driven by the HOXA10 3' untranslated region containing the miR135 binding site. miR135a regulation of HOXA10 was absent in MCF-7 cells, demonstrating cell specificity. CONCLUSIONS: HOXA10 was aberrantly regulated in the endometrium of women with endometriosis by both miR135a and miR135b. Increased microRNA expression likely suppresses genes required for implantation.
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There is a discrepancy between the level of miRNA expression in tissues and in blood.
“Furthermore, there seems to be a discrepancy between the level of miRNA expression in tissues (111) and in blood (109).”
From Biomarkers in endometriosis: Challenges and opportunities (2017) · cites this paper as [111]
The overexpression of these miRNAs correlated with the downregulation of HOXA10 in endometrium from women with endometriosis.
“The overexpression of these miRNAs correlated with the downregulation of HOXA10 in endometrium from women with endometriosis.”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [127]
miR-135a (proliferative phase) and miR-135b (proliferative and secretory phases) were investigated due to their predicted interaction with Homeobox protein (HOX) A10.
“For example, miR-135a (proliferative phase) and miR-135b (proliferative and secretory phases) were investigated due to their predicted interaction with Homeobox protein (HOX) A10 [127].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [127]
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1 retracted
The Expression and Ovarian Steroid Regulation of Endometrial Micro-RNAs
Toloubeydokhti, T., Pan, Q., Luo, X., Bukulmez, O., & Chegini, N. (2008) · Reproductive Sciences · doi:10.1177/1933719108324132 · Cited by 83 · see citing works
RetractedHomeobox genes and axial patterning
McGinnis, W., & Krumlauf, R. (1992) · Cell · doi:10.1016/0092-8674(92)90471-n · Cited by 2,674 · 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
Bulun, S. E. (2009) · New England Journal of Medicine · doi:10.1056/nejmra0804690 · Cited by 1,772 · see citing works
Croce, C. M. (2008) · New England Journal of Medicine · doi:10.1056/nejmra072367 · Cited by 1,055 · see citing works
Endometriosis and infertility: pathophysiology and management
de Ziegler, D., Borghese, B., & Chapron, C. (2010) · The Lancet · doi:10.1016/s0140-6736(10)60490-4 · Cited by 836 · see citing works
Effect of endometriosis on in vitro fertilization
Barnhart, K. T., Dunsmoor-Su, R. F., & Coutifaris, C. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03112-6 · Cited by 798 · see citing works
Burney, R. O., Talbi, S., Hamilton, A. E., Vo, K. C., Nyegaard, M., Nezhat, C. R., Lessey, B. A., & Giudice, L. C. (2007) · Endocrinology · doi:10.1210/en.2006-1692 · Cited by 735 · see citing works
A microRNA signature for a BMP2-induced osteoblast lineage commitment program
Li, Z., Hassan, M. Q., Volinia, S., van Wijnen, A. J., Stein, J. L., Croce, C. M., Lian, J. B., & Stein, G. S. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0804438105 · Cited by 549 · see citing works
Benson, G. V., Lim, H. J., Paria, B. C., Satokata, I., Dey, S. K., & Maas, R. L. (1996) · Development · doi:10.1242/dev.122.9.2687 · Cited by 501 · see citing works
Regulation of the Adenomatous Polyposis Coli Gene by the miR-135 Family in Colorectal Cancer
Nagel, R., le Sage, C., Diosdado, B., van der Waal, M. S., Vrielink, J. A. F. O., Bolijn, A. S., Meijer, G. A., & Agami, R. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-0951 · Cited by 471 · see citing works
Taylor, H. S., Vanden Heuvel, G. B., & Igarashi, P. (1997) · Biology of Reproduction · doi:10.1095/biolreprod57.6.1338 · Cited by 463 · see citing works
Self-citationContribution of Bone Marrow-Derived Stem Cells to Endometrium and Endometriosis
Du, H., & Taylor, H. S. (2007) · Stem Cells · doi:10.1634/stemcells.2006-0828 · Cited by 449 · cited 1× · see citing works
“We now realize that endometriosis also has a genetic component, is influenced by epigenetics, and adult stem cells may contribute (3, 4).”
BackgroundSelf-citationTaylor, H. S., Arici, A. M., Olive, D. L., & Igarashi, P. (1998) · Journal of Clinical Investigation · doi:10.1172/jci1597 · Cited by 420 · see citing works
Self-citationHOX 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
Self-citationMicroRNA-regulated pathways associated with endometriosis
Ohlsson Teague, E. M. C., Van der Hoek, K. H., Van der Hoek, M. B., Perry, N., Wagaarachchi, P., Robertson, S. A., Print, C. G., & Hull, L. M. (2009) · Molecular Endocrinology · doi:10.1210/me.2008-0387 · Cited by 357 · 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
Kuokkanen, S., Chen, B., Ojalvo, L., Benard, L., Santoro, N., & Pollard, J. W. (2010) · Biology of Reproduction · doi:10.1095/biolreprod.109.081059 · Cited by 288 · see citing works
Burney, R. O., Hamilton, A. E., Aghajanova, L., Vo, K. C., Nezhat, C. N., Lessey, B. A., & Giudice, L. C. (2009) · MHR: Basic science of reproductive medicine · doi:10.1093/molehr/gap068 · Cited by 254 · see citing works
Zanatta, A., da Rocha, A. M., Carvalho, F. M., Pereira, R., Taylor, H. S., Motta, E. L. A., Baracat, E. C., & Serafini, P. C. (2010) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-010-9471-y · Cited by 206 · see citing works
Self-citationLee, B., Du, H., & Taylor, H. S. (2009) · Biology of Reproduction · doi:10.1095/biolreprod.108.070391 · Cited by 204 · see citing works
Self-citationMechanistic and Therapeutic Implications of Angiogenesis in Endometriosis
Taylor, R. N., Yu, J., Torres, P. B., Schickedanz, A. C., Park, J. K., Mueller, M. D., & Sidell, N. (2008) · Reproductive Sciences · doi:10.1177/1933719108324893 · Cited by 195 · see citing works
Regulation of JAK2 by miR-135a: prognostic impact in classic Hodgkin lymphoma
Navarro, A., Díaz, T., Martı́nez, A., Gayà, A., Pons, A., Gel, B., Codony, C., Ferrer, G., Martı́nez, C., Montserrat, E., et al. (2009) · Blood · doi:10.1182/blood-2009-02-204842 · Cited by 169 · see citing works
Chung, T. K. H., Cheung, T., Huen, N., et al. (2008) · International Journal of Cancer · doi:10.1002/ijc.24071 · Cited by 167 · see citing works
A KRAS -Variant in Ovarian Cancer Acts as a Genetic Marker of Cancer Risk
Ratner, E., Lu, L., Boeke, M., Barnett, R. E., Nallur, S. V., Chin, L. J., Pelletier, C., Blitzblau, R. C., Tassi, R. A., Paranjape, T., et al. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-0689 · Cited by 137 · 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
Self-citationDefining the proliferative phase endometrial defect
Bromer, J. G., Aldad, T. S., & Taylor, H. S. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.12.066 · Cited by 69 · see citing works
Self-citationHOXA10 expression in ectopic endometrial tissue
Browne, H. N., & Taylor, H. S. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.10.072 · Cited by 54 · see citing works
Self-citationLi, L., Zhang, H., Zhi, R., et al. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.01042.x · Cited by 44 · see citing works
Vitiello, D., Pinard, R., & Taylor, H. S. (2008) · Reproductive Sciences · doi:10.1177/1933719108316911 · Cited by 36 · see citing works
Self-citationEndometriosis is not associated with or linked to the GALT gene
Stefánsson, H., Einarsdottir, A., Geirsson, R. T., Jónsdóttir, K., Sverrisdottir, G., Gudnadottir, V. G., Gunnarsdottir, S., Manolescu, A. R., Gulcher, J. R., & Stefánsson, K. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(01)02862-x · Cited by 26 · see citing works
Uppugunduri, C. R. S. (2010) · Medical Hypotheses · doi:10.1016/j.mehy.2010.11.032 · Cited by 5 · see citing works
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Biomarkers in endometriosis: Challenges and opportunities
Ahn, S. H., Singh, V., & Tayade, C. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.01.009 · Cited by 242 · see citing works
Update on biomarkers for the detection of endometriosis
Fassbender, A., Burney, R. O., F. O, D., D’Hooghe, T., & Giudice, L. (2015) · BioMed Research International · doi:10.1155/2015/130854 · Cited by 195 · see citing works
“The overexpression of these miRNAs correlated with the downregulation of HOXA10 in endometrium from women with endometriosis.”
InfluentialCirculating microRNAs as potential biomarkers for endometriosis
Cho, S., Mutlu, L., Grechukhina, O., & Taylor, H. S. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.02.013 · Cited by 181 · see citing works
Self-citationFassbender, A., Vodolazkaia, A., Saunders, P., Lebovic, D., Waelkens, E., De Moor, B., & D'Hooghe, T. (2013) · Fertility and Sterility · doi:10.1016/j.fertnstert.2013.01.097 · Cited by 150 · see citing works
Tissue and circulating microRNA influence reproductive function in endometrial disease
Louise Hull, M., & Nisenblat, V. (2013) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2013.07.012 · Cited by 69 · see citing works
Shen, L., Yang, S., Huang, W., Xu, W., Wang, Q., Song, Y., & Liu, Y. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-3010 · Cited by 57 · see citing works
Endometriosis, infertility and MicroRNA’s: A review
Raja, M. H. R., Farooqui, N., Zuberi, N., Ashraf, M., Azhar, A., Baig, R., Badar, B., & Rehman, R. (2021) · Journal of Gynecology Obstetrics and Human Reproduction · doi:10.1016/j.jogoh.2021.102157 · Cited by 53 · see citing works
Circulating microRNA profile throughout the menstrual cycle
Rekker, K., Saare, M., Roost, A. M., Salumets, A., & Peters, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0081166 · Cited by 52 · see citing works
Identification of MicroRNAs as Potential Biomarkers in Ovarian Endometriosis
Gu, C.-L., Zhang, Z., Fan, W.-S., Li, L.-A., Ye, M.-X., Zhang, Q., Zhang, N.-N., Li, Z., & Meng, Y.-G. (2020) · Reproductive Sciences · doi:10.1007/s43032-020-00148-z · Cited by 31 · see citing works
- Authors
- Petracco, R., Grechukhina, O., Popkhadze, S., Massasa, E., Zhou, Y., & Taylor, H. S.
- Affiliations
- Yale University (US)
- Corresponding author
- Taylor, Hugh S.
- Venue
- The Journal of Clinical Endocrinology & Metabolism
- Publisher
- The Endocrine Society
- Published
- 2011-12
- Volume
- 96
- Issue
- 12
- Pages
- E1925-E1933
- ISSN
- 0021-972X (ISSN-L)
- 1945-7197
- PMC
- PMC3232619
- OpenAlex
- W2148211949
- Cited by
- 138
- References
- 32
- Citations by year
- 2026: 7 · 2025: 8 · 2024: 8 · 2023: 7 · 2022: 11 · 2021: 5 · 2020: 9 · 2019: 16 · 2018: 14 · 2017: 9 · 2016: 7 · 2015: 9 · 2014: 15 · 2013: 8 · 2012: 5
- FWCI
- 10.02
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD0562668)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Keywords
- endometriosis, HOXA10, endometrium, endometrial receptivity, menstrual cycle, endometrial stromal cells, 3' untranslated region, gene expression regulation, embryo implantation, cell specificity, MCF-7 cells, endometrial biopsy, proliferative phase
- MeSH terms
- Homeobox A10 Proteins, Adult, Cells, Cultured, Endometriosis, Endometrium, Female, Humans, Menstrual Cycle, Middle Aged, Embryo Implantation, Stromal Cells, Homeodomain Proteins, MicroRNAs
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