Histological and Immunohistochemical Characterization of the Similarity and Difference Between Ovarian Endometriomas and Deep Infiltrating Endometriosis
Abstract
Ovarian endometrioma (OMA) and deep infiltrating endometriosis (DIE) have long been recognized to have different histology and, as such, postulated to be 2 separate disease entities. Few studies, however, have attempted to elucidate the causes for their differences. Making use of ectopic endometrial tissue samples from 25 and 20 women with OMA and DIE, respectively, and control endometrial tissue samples from 25 women without endometriosis, we conducted an immunohistochemical analysis to evaluate the expression of a group of carefully chosen markers for epithelial-mesenchymal transition (EMT), fibroblast-to-myofibroblast transdifferentiation (FMT), smooth muscle metaplasia (SMM), fibrosis, vascularity, hormonal receptors, and proteins involved in epigenetic modifications. We found that both OMA and DIE lesions exhibited the same cellular changes consistent with EMT, FMT, SMM, and fibrosis as already shown in animal models. Compared to OMA, DIE lesions underwent more thorough and extensive EMT, FMT, and SMM and, consequently, displayed significantly higher fibrotic content but less vascularity. The 2 conditions also showed different expression levels of hormonal receptors. Both OMA and DIE lesions, especially the latter, showed significantly higher staining of enhancer of zeste homolog 2, H3K9me3, and H3K27me3 than that of control endometrium, suggesting progressive epigenetic changes concomitant with cellular ones. Finally, proteins that are known to be involved in fibrogenesis, such as thymocyte differentiation antigen 1 and peroxisome proliferator-activated receptor γ , were also aberrantly expressed under both conditions. The many similarities shared by both OMA and DIE indicate that the 2 conditions may actually share the same pathogenesis/pathophysiology. Their differences, however, suggest that the source of these differences may result from the different lesional microenvironments.
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The vast heterogeneity of endometriosis appears to be determined mostly by the lesional microenvironments.
“As we showed previously, however, the vast heterogeneity of endometriosis appears to be determined mostly by the lesional microenvironments80.”
From Platelets induce increased estrogen production through NF-κB and TGF-β1 signaling pathways in endometriotic stromal cells (2020) · cites this paper as [80]
Compared with OE, DE lesions appeared to have gone through EMT, FMT, and SMM more thoroughly and extensively, and exhibited significantly more fibromuscular tissues yet reduced cellularity and vascularity.
“we recently found that, compared with OE, DE lesions appeared to have gone through EMT, FMT, and SMM more thoroughly and more extensively, and, accordingly, exhibited significantly more fibromuscular tissues yet reduced cellularity and vascularity28.”
From Neuropeptides Substance P and Calcitonin Gene Related Peptide Accelerate the Development and Fibrogenesis of Endometriosis (2019) · cites this paper as [28]
Proteins known to be involved in fibrogenesis, such as THY-1 and PPAR-g, were aberrantly expressed in these conditions.
“Proteins that are known to be involved in fibrogenesis, such as THY-1 and PPAR-g, were also aberrantly expressed in these conditions.”
From Pathogenesis of deep endometriosis (2017) · cites this paper as [49]
These conditions may share the same pathogenesis/pathophysiology.
“They showed that these conditions may share the same pathogenesis/pathophysiology.”
From Pathogenesis of deep endometriosis (2017) · cites this paper as [49]
Cites
Giudice, L. C., & Kao, L. C. (2004) · The Lancet · doi:10.1016/s0140-6736(04)17403-5 · Cited by 3,166 · see citing works
Alpha-Smooth Muscle Actin Expression Upregulates Fibroblast Contractile Activity
Hinz, B., Celetta, G., Tomasek, J. J., Gabbiani, G., & Chaponnier, C. (2001) · Molecular Biology of the Cell · doi:10.1091/mbc.12.9.2730 · Cited by 1,288 · see citing works
Nisolle, M., & Donnez, J. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00191-x · Cited by 1,279 · see citing works
Recent Developments in Myofibroblast Biology
Hinz, B., Phan, S. H., Thannickal, V. J., Prunotto, M., Desmoulière, A., Varga, J., De Wever, O., Mareel, M., & Gabbiani, G. (2012) · The American Journal of Pathology · doi:10.1016/j.ajpath.2012.02.004 · Cited by 1,193 · see citing works
Deeply infiltrating pelvic endometriosis: histology and clinical significance
Cornillie, F. J., Oosterlynck, D., Lauweryns, J. M., & Koninckx, P. R. (1990) · Fertility and Sterility · doi:10.1016/s0015-0282(16)53570-5 · Cited by 594 · see citing works
Endometriosis: pathogenetic implications of the anatomic distribution.
Jenkins, S., Olive, D. L., & Haney, A. F. (1986) · PubMed · Cited by 523 · see citing works
Deep endometriosis: definition, diagnosis, and treatment
Koninckx, P. R., Ussia, A., Adamyan, L., Wattiez, A., & Donnez, J. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.07.1061 · Cited by 494 · see citing works
Ovarian endometriosis: a marker for more extensive pelvic and intestinal disease
Redwine, D. B. (1999) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00211-3 · Cited by 408 · see citing works
MeCP2 Controls an Epigenetic Pathway That Promotes Myofibroblast Transdifferentiation and Fibrosis
Mann, J., Chu, D. C. K., Maxwell, A., Oakley, F., Zhu, N., Tsukamoto, H., & Mann, D. A. (2010) · Gastroenterology · doi:10.1053/j.gastro.2009.10.002 · Cited by 397 · see citing works
Rege, T. A., & Hagood, J. S. (2006) · The FASEB Journal · doi:10.1096/fj.05-5460rev · Cited by 369 · 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
Deep endometriosis: a consequence of infiltration or retraction or possibly adenomyosis externa?
Koninckx, P. R., & Martin, D. C. (1992) · Fertility and Sterility · doi:10.1016/s0015-0282(16)55436-3 · Cited by 345 · see citing works
Guo, S.-W. (2009) · Molecular Human Reproduction · doi:10.1093/molehr/gap064 · Cited by 328 · see citing works
Self-citationThe Pathology of Endometriosis
Clement, P. B. (2007) · Advances in Anatomic Pathology · doi:10.1097/pap.0b013e3180ca7d7b · Cited by 326 · see citing works
Role of Estrogen Receptor-β in Endometriosis
Bulun, S., Monsavais, D., Pavone, M., Dyson, M., Xue, Q., Attar, E., Tokunaga, H., & Su, E. (2012) · Seminars in Reproductive Medicine · doi:10.1055/s-0031-1299596 · Cited by 307 · see citing works
Endometriosis results from the dislocation of basal endometrium
Leyendecker, G. (2002) · Human Reproduction · doi:10.1093/humrep/17.10.2725 · Cited by 300 · see citing works
Morphometric study of the stromal vascularization in peritoneal endometriosis
Nisolle, M., Casanas‐Roux, F., Anaf, V., Mine, J.-M., & Donnez, J. (1993) · Fertility and Sterility · doi:10.1016/s0015-0282(16)55823-3 · Cited by 289 · see citing works
Clement, P. B. (1990) · PubMed · Cited by 277 · see citing works
Estrogen Receptor-β, Estrogen Receptor-α, and Progesterone Resistance in Endometriosis
Bulun, S., Cheng, Y.-H., Pavone, M., Xue, Q., Attar, E., Trukhacheva, E., Tokunaga, H., Utsunomiya, H., Yin, P., Luo, X., et al. (2010) · Seminars in Reproductive Medicine · doi:10.1055/s-0029-1242991 · Cited by 243 · see citing works
Loss of Fibroblast Thy-1 Expression Correlates with Lung Fibrogenesis
Hagood, J. S., Prabhakaran, P., Kumbla, P. A., Salazar, L., MacEwen, M. W., Barker, T. H., Ortiz, L. A., Schoeb, T. R., Siegal, G. P., Alexander, C. B., et al. (2005) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)62982-3 · Cited by 226 · see citing works
Pathogenetic Mechanisms of Deep Infiltrating Endometriosis
Tosti, C., Pinzauti, S., Santulli, P., Chapron, C., & Petraglia, F. (2015) · Reproductive Sciences · doi:10.1177/1933719115592713 · Cited by 222 · see citing works
Age-related evolution in color appearance of endometriosis
Redwine, D. B. (1987) · Fertility and Sterility · doi:10.1016/s0015-0282(16)59611-3 · Cited by 214 · see citing works
Zhang, Q., Duan, J., Liu, X., & Guo, S.-W. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.03.015 · Cited by 211 · see citing works
Self-citationTranscriptional characterizations of differences between eutopic and ectopic endometrium
Wu, Y., Kajdacsy-Balla, A., Strawn, E., Basir, Z., Halverson, G., Jailwala, P., Wang, Y., Wang, X., Ghosh, S., & Guo, S.-W. (2006) · Endocrinology · doi:10.1210/en.2005-0426 · Cited by 208 · see citing works
Liu, X., Shen, M., Qi, Q., Zhang, H., & Guo, S.-W. (2016) · Human Reproduction · doi:10.1093/humrep/dew018 · Cited by 190 · see citing works
Self-citationBrosens, I., Gordts, S., & Benagiano, G. (2013) · Human Reproduction · doi:10.1093/humrep/det243 · Cited by 184 · see citing works
Smooth muscles are frequent components of endometriotic lesions
Anaf, V. (2000) · Human Reproduction · doi:10.1093/humrep/15.4.767 · Cited by 183 · see citing works
Endometriosis—A disease because it is characterized by bleeding
Brosens, I. A. (1997) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(97)70482-4 · Cited by 169 · see citing works
Enhanced Myofibroblastic Differentiation and Survival in Thy-1(−) Lung Fibroblasts
Sanders, Y. Y., Kumbla, P. A., & Hagood, J. S. (2006) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2006-0178oc · Cited by 153 · see citing works
Zhang, Q., Duan, J., Olson, M., Fazleabas, A., & Guo, S.-W. (2016) · Reproductive Sciences · doi:10.1177/1933719116641763 · Cited by 149 · see citing works
Self-citationPelvic Endometriosis Diagnosed in an Entire Nation Over 20 Years
Gylfason, J. T., Kristjansson, K. A., Sverrisdottir, G., Jónsdóttir, K., Rafnsson, V., & Geirsson, R. T. (2010) · American Journal of Epidemiology · doi:10.1093/aje/kwq143 · Cited by 144 · see citing works
Ding, D., Liu, X., Duan, J., & Guo, S.-W. (2015) · Human Reproduction · doi:10.1093/humrep/dev025 · Cited by 139 · see citing works
Self-citationMatsuzaki, S., & Darcha, C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0076808 · Cited by 138 · see citing works
Correlation of Endometrial Dating with Basal Body Temperature and Menses
Noyes, R. W., & Haman, J. O. (1953) · Fertility and Sterility · doi:10.1016/s0015-0282(16)31446-7 · Cited by 134 · see citing works
Shen, M., Liu, X., Zhang, H., & Guo, S.-W. (2015) · Human Reproduction · doi:10.1093/humrep/dev314 · Cited by 124 · see citing works
Self-citationZhou, Y., Hagood, J. S., & Murphy-Ullrich, J. E. (2004) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)63330-5 · Cited by 120 · see citing works
Fibrosis and smooth muscle metaplasia in rectovaginal endometriosis
Itoga, T., Matsumoto, T., Takeuchi, H., Yamasaki, S., Sasahara, N., Hoshi, T., & Kinoshita, K. (2003) · Pathology International · doi:10.1046/j.1440-1827.2003.01483.x · Cited by 108 · see citing works
Epigenetic Regulation of Thy-1 by Histone Deacetylase Inhibitor in Rat Lung Fibroblasts
Sanders, Y. Y., Tollefsbol, T. O., Varisco, B. M., & Hagood, J. S. (2010) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2010-0154oc · Cited by 106 · see citing works
Pioglitazone Prevents Early-Phase Hepatic Fibrogenesis Caused by Carbon Tetrachloride
Kon, K., Ikejima, K., Hirose, M., Yoshikawa, M., Enomoto, N., Kitamura, T., Takei, Y., & Sato, N. (2002) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2002.6385 · Cited by 105 · see citing works
Peeters, L. L. H., Vigne, J., Tee, M. K., Zhao, D., Waite, L. L., & Taylor, R. N. (2006) · Angiogenesis · doi:10.1007/s10456-005-9027-4 · Cited by 96 · see citing works
Koumas, L., King, A. E., Critchley, H., KELLY, R. W., & Phipps, R. P. (2001) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)61768-3 · Cited by 94 · see citing works
Histological classification of endometriosis as a predictor of response to treatment
Abrão, M. S., Neme, R. M., Carvalho, F. M., Aldrighi, J. M., & Pinotti, J. A. (2003) · International Journal of Gynecology & Obstetrics · doi:10.1016/s0020-7292(03)00079-1 · Cited by 90 · see citing works
Enhancer of Zeste homolog 2 (EZH2) induces epithelial-mesenchymal transition in endometriosis
Zhang, Q., Dong, P., Liu, X., Sakuragi, N., & Guo, S. (2017) · Scientific Reports · doi:10.1038/s41598-017-06920-7 · Cited by 89 · see citing works
Self-citationGuo, S.-W., Ding, D., Shen, M., & Liu, X. (2015) · Reproductive Sciences · doi:10.1177/1933719115570907 · Cited by 86 · see citing works
Self-citationMechsner, S., Bartley, J., Loddenkemper, C., Salomon, D. S., Starzinski-Powitz, A., & Ebert, A. D. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.11.038 · Cited by 79 · see citing works
Zhang, Q., Liu, X., & Guo, S.-W. (2017) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2016.11.006 · Cited by 76 · see citing works
Self-citationSmooth muscle metaplasia in ovarian endometriosis
Fukunaga (2000) · Histopathology · doi:10.1046/j.1365-2559.2000.00845.x · Cited by 74 · see citing works
Lesion kinetics in a non-human primate model of endometriosis
Harirchian, P., Gashaw, I., Lipskind, S. T., Braundmeier, A. G., Hastings, J. M., Olson, M. R., & Fazleabas, A. T. (2012) · Human Reproduction · doi:10.1093/humrep/des196 · Cited by 72 · see citing works
Garry, R. (2004) · Human Reproduction · doi:10.1093/humrep/deh147 · Cited by 71 · see citing works
van Kaam, K. J. A. F., Schouten, J. P., Nap, A. W., Dunselman, G. A. J., & Groothuis, P. G. (2008) · Human Reproduction · doi:10.1093/humrep/den153 · Cited by 70 · see citing works
Barcena, M. L., Gericke, J., Reichelt, U., Okuducu, A. F., Ebert, A. D., Chiàntera, V., Schneider, A., & Mechsner, S. (2011) · Human Reproduction · doi:10.1093/humrep/der253 · Cited by 68 · see citing works
The Role of PPAR Gamma in Systemic Sclerosis
Dantas, A. T., Pereira, M. C., Rêgo, M. J. B. D. M., da Rocha, L. F., Pitta, I. D. R., Marques, C. D. L., Duarte, Â. L. B. P., & Pitta, M. G. D. R. (2015) · PPAR Research · doi:10.1155/2015/124624 · Cited by 67 · see citing works
Chronic stress accelerates the development of endometriosis in mouse through adrenergic receptor β2
Long, Q., Liu, X., Qi, Q.-M., & Guo, S. (2016) · Human Reproduction · doi:10.1093/humrep/dew237 · Cited by 67 · see citing works
Self-citationThy-1 Signals through PPARγ to Promote Lipofibroblast Differentiation in the Developing Lung
Varisco, B. M., Ambalavanan, N., Whitsett, J. A., & Hagood, J. S. (2012) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2011-0316oc · Cited by 66 · see citing works
TGF-β1 epigenetically modifies Thy-1 expression in primary lung fibroblasts
Neveu, W. A., Mills, S. T., Staitieh, B. S., & Sueblinvong, V. (2015) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00086.2015 · Cited by 66 · see citing works
Expression of smooth muscle markers in so called malignant fibrous histiocytomas
Hasegawa, T., Hasegawa, F., Hirose, T., Sano, T., & Matsuno, Y. (2003) · Journal of Clinical Pathology · doi:10.1136/jcp.56.9.666 · Cited by 62 · see citing works
Bonte, H., Chapron, C., Vieira, M., Fauconnier, A., Barakat, H., Fritel, X., Vacher-Lavenu, M.-C., & Dubuisson, J.-B. (2002) · The Journal of the American Association of Gynecologic Laparoscopists · doi:10.1016/s1074-3804(05)60530-0 · Cited by 61 · see citing works
Fernández-Shaw, S., Shorter, S. C., Naish, C., Barlow, D. H., & Starkey, P. M. (1992) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a137609 · Cited by 57 · see citing works
Boyle, D. P., & McCluggage, W. G. (2009) · Journal of Clinical Pathology · doi:10.1136/jcp.2008.064261 · Cited by 56 · see citing works
Pathogenetic role of the stromal cells in endometriosis and adenomyosis
Mai, K., Yazdi, H. M., Perkins, D. G., et al. (1997) · Histopathology · doi:10.1046/j.1365-2559.1997.4910725.x · Cited by 56 · see citing works
Fibrogenesis in Peritoneal Endometriosis
Matsuzaki, S., Canis, M. J., Darcha, C., Dechelotte, P., Pouly, J. L., & Bruhat, M. (1999) · Gynecologic and Obstetric Investigation · doi:10.1159/000010094 · Cited by 52 · see citing works
Hornung, D., Klingel, K., Dohrn, K., Kandolf, R., Wallwiener, D. R., & Taylor, R. N. (2001) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64664-0 · Cited by 51 · see citing works
Kamergorodsky, G., Ribeiro, P. A., Galvão, M. A. L., Abrão, M. S., Donadio, N., Lemos, N. L. D. B. M., & Aoki, T. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.05.086 · Cited by 49 · see citing works
Increased Nerve Density in Deep Infiltrating Endometriotic Nodules
Anaf, V., El Nakadi, I., De Moor, V., Chapron, C., Pistofidis, G., & Noel, J.-C. (2011) · Gynecologic and Obstetric Investigation · doi:10.1159/000320750 · Cited by 48 · see citing works
MEYER, J. L., ZIMBARDI, D., PODGAEC, S., AMORIM, R. L., ABRÃO, M. S., & RAINHO, C. A. (2014) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2014.1637 · Cited by 47 · see citing works
Hornung, D., Waite, L. L., Ricke, E. A., Bentzien, F., Wallwiener, D. R., & Taylor, R. N. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.7.7615 · Cited by 45 · see citing works
(2009) · PubMed · Cited by 43 · see citing works
Biases in the endometriosis literature
Koninckx, P. R. (1998) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(98)00200-0 · Cited by 42 · see citing works
Is mild endometriosis a progressive disease?
Brosens, I. A. (1994) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a138422 · Cited by 42 · see citing works
Estrogen and progesterone receptors in smooth muscle component of deep infiltrating endometriosis
Noël, J.-C., Chapron, C., Bucella, D., Buxant, F., Peny, M.-O., Fayt, I., Borghese, B., & Anaf, V. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.12.114 · Cited by 41 · see citing works
Activated Platelets Induce Estrogen Receptor β Expression in Endometriotic Stromal Cells
Zhang, Q., Ding, D., Liu, X., & Guo, S.-W. (2015) · Gynecologic and Obstetric Investigation · doi:10.1159/000377629 · Cited by 38 · see citing works
Self-citationLebovic, D. I., Kavoussi, S. K., Lee, J., Banu, S. K., & Arosh, J. A. (2013) · Endocrinology · doi:10.1210/en.2013-1168 · Cited by 36 · see citing works
Ovarian Smooth Muscle Metaplasia
Doss, B. J., Wanek, S. M., Jacques, S. M., Qureshi, F., Ramirez, N. C., & Lawrence, W. D. (1999) · International Journal of Gynecological Pathology · doi:10.1097/00004347-199901000-00008 · Cited by 35 · see citing works
A comparative study of ovarian and pelvic wall-infiltrating endometriosis
Khare, V. K., Martin, D. C., & Eltorky, M. (1996) · The Journal of the American Association of Gynecologic Laparoscopists · doi:10.1016/s1074-3804(96)80006-5 · Cited by 34 · see citing works
Immunohistochemical detection of type I, III, and IV collagen in endometriosis implants
Stovall, D. W., Anners, J., & Halme, J. K. (1992) · Fertility and Sterility · doi:10.1016/s0015-0282(16)55013-4 · Cited by 31 · see citing works
Ultrastructural Changes in Endometriotic Tissue During Danazol Treatment
Schweppe, K.-W., Dmowski, W. P., & Wynn, R. M. (1981) · Fertility and Sterility · doi:10.1016/s0015-0282(16)45612-8 · Cited by 30 · see citing works
Endocrine dependency of endometriosis: an ultrastructural study
Schweppe, K.-W., & Wynn, R. M. (1984) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/0028-2243(84)90143-6 · Cited by 25 · see citing works
PPAR-γ expression in peritoneal endometriotic lesions correlates with pain experienced by patients
McKinnon, B. D., Bersinger, N. A., Huber, A. W., Kühn, A., & Mueller, M. D. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.07.980 · Cited by 24 · see citing works
Li, T., He, H., Liu, R., Wang, S. X., & Pu, D.-M. (2014) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2014.04.001 · Cited by 23 · see citing works
Nerve fiber density in deep nodular endometriotic lesions induced in a baboon experimental model
Donnez, O., Soares, M. P. M., Defrère, S., Dehoux, J., Langendonckt, A. V., Donnez, J., Dolmans, M., & Colette, S. (2013) · Fertility and Sterility · doi:10.1016/j.fertnstert.2013.06.014 · Cited by 23 · see citing works
Overton, C. E., Fernández-Shaw, S., Hicks, B. R., Barlow, D. H., & Starkey, P. M. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)81855-9 · Cited by 22 · see citing works
Endometriosis-Derived Thromboxane A2 Induces Neurite Outgrowth
Yan, D., Liu, X., & Guo, S.-W. (2017) · Reproductive Sciences · doi:10.1177/1933719116670037 · Cited by 17 · see citing works
Self-citationQiu, J., LIU, M., ZHANG, Z., et al. (2012) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/j.1600-0412.2012.01370.x · Cited by 12 · see citing works
Histone deacetylase inhibitors as therapeutics for endometriosis
Li, X., Liu, X., & Guo, S. (2012) · Expert Review of Obstetrics & Gynecology · doi:10.1586/eog.12.52 · Cited by 10 · see citing works
Self-citationVINCI, G., Arkwright, S., Audebourg, A., Radenen, B., Chapron, C., Borghese, B., Dousset, B. E., Méhats, C., Vaiman, D., Vacher‐Lavenu, M., et al. (2016) · Reproductive Sciences · doi:10.1177/1933719116638188 · Cited by 10 · see citing works
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Gordts, S., Koninckx, P., & Brosens, I. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.08.036 · Cited by 241 · see citing works
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Reis, F. M., Coutinho, L. M., Vannuccini, S., Batteux, F., Chapron, C., & Petraglia, F. (2020) · Human Reproduction Update · doi:10.1093/humupd/dmaa009 · Cited by 166 · see citing works
Guo, S.-W. (2018) · Human Reproduction · doi:10.1093/humrep/dey015 · Cited by 116 · see citing works
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Self-citationQi, Q., Liu, X., Zhang, Q., & Guo, S.-W. (2020) · Scientific Reports · doi:10.1038/s41598-020-57997-6 · Cited by 44 · see citing works
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Nie, J., Yi, Y., Liu, X., & Guo, S.-W. (2025) · Human Reproduction Open · doi:10.1093/hropen/hoaf028 · Cited by 11 · see citing works
Self-citation
- Authors
- Liu, X., Zhang, Q., & Guo, S.-W.
- Affiliations
- Fudan University (CN)
- Corresponding author
- Liu, Xishi
- Venue
- Reproductive Sciences
- Published
- 2018-03
- Volume
- 25
- Issue
- 3
- Pages
- 329-340
- ISSN
- 1933-7191 (ISSN-L)
- 1933-7205
- OpenAlex
- W2738561245
- Semantic Scholar
- 84379f483075ecabc3afc7111d7829ffdc5bc53d
- Cited by
- 110
- References
- 85
- Citations by year
- 2026: 11 · 2025: 16 · 2024: 16 · 2023: 10 · 2022: 13 · 2021: 6 · 2020: 16 · 2019: 8 · 2018: 11 · 2017: 3
- FWCI
- 12.07
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Reproductive Sciences (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Natural Science Foundation of China (81370695, 81471434, 81530040, 81671436)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
- Health Sciences › Medicine › Obstetrics and Gynecology › Gynecological conditions and treatments
- Keywords
- endometrioma, deep infiltrating endometriosis, ectopic endometrium, epithelial-mesenchymal transition, fibroblast-to-myofibroblast transdifferentiation, fibrosis, vascularity, hormone receptors, epigenetic modifications, H3K9me3, H3K27me3, TGF-β1, PPARγ, endometriosis pathogenesis
- MeSH terms
- Adult, Endometriosis, Endometrium, Female, Humans, Middle Aged, Ovarian Diseases, Peritoneal Diseases, Biomarkers, Cell Transdifferentiation, Young Adult, Myofibroblasts, Epithelial-Mesenchymal Transition
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