Identification of cells with colony-forming activity, self-renewal capacity, and multipotency in ovarian endometriosis
Open accessAbstract
Endometriosis, the growth of endometrial tissue outside the uterine cavity, is a common gynecological disorder affecting 10% to 15% of women in their reproductive years. Retrograde menstrual shedding containing endometrial stem/progenitor cells has been postulated to be involved in its pathogenesis. In this study, we identified putative endometriotic stem/progenitor cells by their colony-forming potential, self-renewal capacity, and multipotency. Purified epithelial and stromal cells isolated from ovarian endometriotic cysts formed large and small colony-forming units (CFUs) in clonogenic assay. The colony-forming activity of epithelial and stromal cells was found to differ greatly between autologous endometrium and ovarian endometrioma samples. The large CFUs could propagate more than the small CFUs. The endometriotic epithelial small CFUs expressed epithelial markers (epithelial cell adhesion molecule, cytokeratin, and α6 integrin); only occasional large CFUs expressed α6 integrin. Aside from the expression of fibroblast markers, stromal CFUs also expressed three somatic stem cell markers: sal-like 4, CD133, and Musashi-1. Endometriotic stromal cells derived from large CFUs could differentiate into four mesenchymal lineages when cultured in the respective inducing-media, as determined by histochemical staining and RT-PCR of lineage specific markers. These findings demonstrate that ovarian endometrioma contains a subset of cells displaying somatic stem cell properties.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
MSCs and epithelial progenitor cells isolated from ovarian endometriomas do not show increased clonogenicity or self-renewal compared to endometrial stem cells.
“Remarkably, MSCs and epithelial progenitor cells isolated from ovarian endometriomas do not show increased clonogenicity or self-renewal compared to endometrial stem cells, which might have explained the increased survival capacity in endometriosis (Chan et al., 2011;Li et al., 2014).”
From Endometriosis and nuclear receptors (2019) · cites this paper as Chan et al., 2011
The Clonogenicity section reports significantly lower colony-forming efficiency for both epithelial and stromal cells from ovarian endometriomas than from normal endometrium. The Serial Cloning section measures self-renewal within endometrioma-derived colonies, comparing large with small colonies, but does not compare their self-renewal with endometrial stem cells. The proposed link to increased survival capacity is not established by these passages. (LLM, conf=0.87)
Experimental — accuracy not yet measuredEndometriotic lesions harbor multipotent, colony-forming MSCs.
“Similar to endometrium, endometriotic lesions also harbor multipotent, colony-forming MSCs (Chan et al., 2011).”
From Endometriosis and nuclear receptors (2019) · cites this paper as Chan et al., 2011
The Abstract reports colony-forming cells isolated from ovarian endometriotic cysts, and the Cellular Phenotypes and Multipotency section reports that stromal large CFUs differentiated into four mesenchymal lineages. The study describes these as putative stem/progenitor cells and examines ovarian endometriomas, so it does not establish the claim for endometriotic lesions generally or definitively identify the cells as MSCs. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Multilineage potential of adult human mesenchymal stem cells
Pittenger, M. F., Mackay, A. M., Beck, S. C., Jaiswal, R. K., Douglas, R., Mosca, J. D., Moorman, M. A., Simonetti, D. W., Craig, S., & Marshak, D. R. (1999) · Science · doi:10.1126/science.284.5411.143 · Cited by 21,052 · see citing works
Asahara, T., Masuda, H., Takahashi, T., Kalka, C., Pastore, C., Silver, M., Kearne, M., Magner, M., & Isner, J. M. (1999) · Circulation Research · doi:10.1161/01.res.85.3.221 · Cited by 3,249 · see citing works
Giudice, L. C., & Kao, L. C. (2004) · The Lancet · doi:10.1016/s0140-6736(04)17403-5 · Cited by 3,166 · see citing works
Revised American Society for Reproductive Medicine classification of endometriosis: 1996
American Society for Reproductive Medicine (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)81391-x · Cited by 3,018 · 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
mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer.Preprint
Tontonoz, P., Hu, E., Graves, R. A., Budavari, A. I., & Spiegelman, B. M. (1994) · Genes & Development · doi:10.1101/gad.8.10.1224 · Cited by 2,182 · 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
(1984) · PubMed · Cited by 997 · see citing works
Noyes, R. W., Hertig, A. T., & Rock, J. (1975) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(16)33500-1 · Cited by 941 · see citing works
Recurrence of endometriosis and its control
Guo, S.-W. (2009) · Human Reproduction Update · doi:10.1093/humupd/dmp007 · Cited by 719 · see citing works
Clonogenicity of Human Endometrial Epithelial and Stromal Cells1
Chan, R. W. S., Schwab, K. E., & Gargett, C. E. (2004) · Biology of Reproduction · doi:10.1095/biolreprod.103.024109 · Cited by 653 · see citing works
Self-citationZhang, J., Tam, W.-L., Tong, G. Q., Wu, Q., Chan, H.-Y., Soh, B.-S., Lou, Y., Yang, J., Ma, Y., Chai, L., et al. (2006) · Nature Cell Biology · doi:10.1038/ncb1481 · Cited by 568 · see citing works
Schwab, K. E., & Gargett, C. E. (2007) · Human Reproduction · doi:10.1093/humrep/dem265 · Cited by 545 · see citing works
Endometrial cells derived from donor stem cells in bone marrow transplant recipients
Taylor, H. S. (2004) · JAMA · doi:10.1001/jama.292.1.81 · Cited by 510 · see citing works
Isolation and Culture of Epithelial Progenitors and Mesenchymal Stem Cells from Human Endometrium1
Gargett, C. E., Schwab, K. E., Zillwood, R. M., Nguyen, H. P. T., & Wu, D. (2009) · Biology of Reproduction · doi:10.1095/biolreprod.108.075226 · Cited by 476 · see citing works
Contribution 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
“In mice, bone-marrow–derived cells from male donors are involved in endometrial gland formation of female transplant recipients(52) and in ectopic endometrial implants within the peritoneal cavity.(37) Endometrial stromal cells isolated by the expression of perivascular markers [melanoma cell adhesion molecule (MCAM,…”
BackgroundTondreau, T., Meuleman, N., Delforge, A., Dejeneffe, M., Leroy, R., Massy, M., Mortier, C., Bron, D., & Lagneaux, L. (2005) · Stem Cells · doi:10.1634/stemcells.2004-0330 · Cited by 438 · see citing works
Epigenetic regulation of CD133 and tumorigenicity of CD133+ ovarian cancer cells
Baba, T., Convery, P. A., Matsumura, N., Whitaker, R. S., Kondoh, E., Perry, T., Huang, Z., Bentley, R. C., Mori, S., Fujii, S., et al. (2008) · Oncogene · doi:10.1038/onc.2008.374 · Cited by 419 · see citing works
Donnez, J., Nisolle, M., Gillet, N., Smets, M., Bassil, S., & Casanas-Roux, F. (1996) · Human Reproduction · doi:10.1093/humrep/11.3.641 · Cited by 360 · see citing works
Masuda, H., Matsuzaki, Y., Hiratsu, E., Ono, M., Nagashima, T., Kajitani, T., Arase, T., Oda, H., Uchida, H., Asada, H., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010387 · Cited by 303 · see citing works
Prostaglandin E2 Stimulates Aromatase Expression in Endometriosis-Derived Stromal Cells
Noble, L. S. (1997) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.82.2.600 · Cited by 301 · 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
Vinatier, D., Orazi, G., Cosson, M., & Dufour, P. (2001) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(00)00405-x · Cited by 299 · see citing works
CD133 as a Marker for Cancer Stem Cells: Progresses and Concerns
Wu, Y., & Wu, P. Y. (2009) · Stem Cells and Development · doi:10.1089/scd.2008.0338 · Cited by 297 · see citing works
Frid, M. G., Shekhonin, B. V., Koteliansky, V., & Glukhova, M. A. (1992) · Developmental Biology · doi:10.1016/0012-1606(92)90104-o · Cited by 274 · see citing works
Identification of Label-Retaining Cells in Mouse Endometrium
Chan, R., & Gargett, C. E. (2006) · Stem Cells · doi:10.1634/stemcells.2005-0411 · Cited by 265 · see citing works
Self-citationIsolation, characterization, and comparison of human endometrial and endometriosis cells in vitro
Ryan, I., Schriock, E. D., & Taylor, R. N. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.78.3.8126136 · Cited by 250 · see citing works
Schwab, K. E., Chan, R. W. S., & Gargett, C. E. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.02.056 · Cited by 249 · see citing works
Self-citationEstrogen 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
Characterization of side-population cells in human normal endometrium
Kato, K., Yoshimoto, M., Kato, K., Adachi, S., Yamayoshi, A., Arima, T., Asanoma, K., Kyo, S., Nakahata, T., & Wake, N. (2007) · Human Reproduction · doi:10.1093/humrep/del514 · Cited by 240 · see citing works
Apoptosis and expression of Bcl-2 and Bax in eutopic endometrium from women with endometriosis
Meresman, G. F., Vighi, S., Buquet, R. A., Ortiz, O. C., Tesone, M., & Rumi, L. S. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(00)01522-3 · Cited by 213 · see citing works
Schwab, K. E., Hutchinson, P. E., & Gargett, C. E. (2008) · Human Reproduction · doi:10.1093/humrep/den051 · Cited by 205 · see citing works
Endometriosis: A dysfunction and disease of the archimetra
Leyendecker, G. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.752 · Cited by 199 · see citing works
Sumathi, V. P., & McCluggage, W. G. (2002) · Journal of Clinical Pathology · doi:10.1136/jcp.55.5.391 · Cited by 197 · see citing works
Götte, M., Wolf, M., Staebler, A., Buchweitz, O., Kelsch, R., Schüring, A. N., & Kiesel, L. (2008) · The Journal of Pathology · doi:10.1002/path.2364 · Cited by 195 · see citing works
Hormone and growth factor signaling in endometrial renewal: Role of stem/progenitor cells
Gargett, C. E., Chan, R., & Schwab, K. E. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.02.026 · Cited by 192 · see citing works
Self-citationCervelló, I., Gil-Sanchis, C., Mas, A., Delgado-Rosas, F., Martínez-Conejero, J. A., Galán, A., Martínez-Romero, A., Martínez, S., Navarro, I., Ferro, J., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010964 · Cited by 187 · see citing works
Brandenberger, A. W. (1999) · Molecular Human Reproduction · doi:10.1093/molehr/5.7.651 · Cited by 165 · see citing works
Rutella, S., Bonanno, G., Procoli, A., Mariotti, A., Corallo, M., Prisco, M. G., Eramo, A., Napoletano, C., Gallo, D., Perillo, A., et al. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-1883 · Cited by 155 · see citing works
Cell proliferation is increased in the endometrium of women with endometriosis
Wingfield, M. B., Macpherson, A., Healy, D. L., & Rogers, P. A. W. (1995) · Fertility and Sterility · doi:10.1016/s0015-0282(16)57733-4 · Cited by 155 · see citing works
Nisolle, M., Casanas-Roux, F., & Donnez, J. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00341-5 · Cited by 148 · 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
Gargett, C. E., Chan, R., & Schwab, K. E. (2007) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0b013e328235a5c6 · Cited by 141 · see citing works
Self-citationEndometrioid Adenocarcinoma of the Ovary and Its Relationship to Endometriosis
McMeekin, D. S., Burger, R. A., Manetta, A., DiSaia, P. J., & Berman, M. L. (1995) · Gynecologic Oncology · doi:10.1006/gyno.1995.1271 · Cited by 140 · see citing works
Ikoma, T., Kyo, S., Maida, Y., Ozaki, S., Takakura, M., Nakao, S., & Inoue, M. (2009) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2009.07.026 · Cited by 137 · see citing works
Expression of estrogen receptor alpha and beta in peritoneal and ovarian endometriosis
Matsuzaki, S., Murakami, T., Uehara, S., Canis, M., Sasano, H., & Okamura, K. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(01)01783-6 · Cited by 133 · see citing works
Akoum, A. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)84754-1 · Cited by 132 · see citing works
Johnson, M. C., Torres, M. J., Alves, A., Bacallao, K., Fuentes, A., Vega, M., & Boric, M. A. (2005) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-3-45 · Cited by 117 · see citing works
Expression Pattern of Stemness-Related Genes in Human Endometrial and Endometriotic Tissues
Forte, A., Schettino, M. T., Finicelli, M., Cipollaro, M., Colacurci, N., Cobellis, L., & Galderisi, U. (2009) · Molecular Medicine · doi:10.2119/molmed.2009.00068 · Cited by 86 · see citing works
Secondary müllerian system and endometriosis
Fujii, S. (1991) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(91)90255-p · Cited by 84 · see citing works
Kaitu’u‐Lino, T. J., Ye, L., & Gargett, C. E. (2010) · Endocrinology · doi:10.1210/en.2009-1334 · Cited by 70 · see citing works
Aberrant portions of the müllerian duct found in an ovary
Russell, W. (1979) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(79)90890-1 · Cited by 60 · 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
Expression pattern of integrin adhesion molecules in endometriosis and human endometrium
Regidor, P. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.710 · Cited by 49 · see citing works
Matsuzaki, S., Uehara, S., Murakami, T., Fujiwara, J., Funato, T., & Okamura, K. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(00)00712-3 · Cited by 41 · see citing works
Okamura, H., Katabuchi, H., Nitta, M., & Ohtake, H. (2006) · Microscopy Research and Technique · doi:10.1002/jemt.20306 · Cited by 39 · see citing works
Jürgensen, A., Mettler, L., Volkov, N. I., & Parwaresch, R. M. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58502-1 · Cited by 37 · see citing works
Nakayama, K., Masuzawa, H., Li, S.-F., Yoshikawa, F., Toki, T., Nikaido, T., Silverberg, S. G., & Fujii, S. (1994) · International Journal of Gynecological Pathology · doi:10.1097/00004347-199410000-00009 · Cited by 32 · see citing works
鈴木, 昭., Horiuchi, A., Oka, K., Miyamoto, T., Kashima, H., & Shiozawa, T. (2010) · Archiv für Pathologische Anatomie und Physiologie und für Klinische Medicin · doi:10.1007/s00428-010-0884-x · Cited by 27 · see citing works
Song, I. O., Hong, S. R., Huh, Y., Yoo, K. J., Koong, M. K., Jun, J. Y., & Kang, I. S. (1998) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1998.tb00384.x · Cited by 17 · see citing works
Akoum, A., Jolicoeur, Boutouil, M., Paradis, I., Drouin, R., Maheux, R., & Lemay, A. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)90669-5 · Cited by 14 · see citing works
Flagged first, then by citations
4 of the 65 references couldn’t be matched to a known paper.
Research works printed but not linked: 3
- Chan et al AJP June 2011, Vol. 178, No.
- Meyer R: U ¨ber eine adenomatöse Wucherung der Serosa in einer Bauchnarbe [On an adenomatous proliferation of the serosa in an abdominal scar]. German. Z Geburtsh Gynakol 1903, 49:32-41
- Chan RW, Schwab KE, Gargett CE: Clonogenicity of human endo- metrial epithelial and stromal cells. Biol Reprod 2004, 70:1738 -1750
Cited by
Sorted by citations
Endometrial stem/progenitor cells: the first 10 years
Gargett, C. E., Schwab, K. E., & Deane, J. A. (2015) · Human Reproduction Update · doi:10.1093/humupd/dmv051 · Cited by 561 · see citing works
Fertile ground: human endometrial programming and lessons in health and disease
Evans, J., Salamonsen, L. A., Winship, A., Menkhorst, E. M., Nie, G., Gargett, C. E., & Dimitriadis, E. (2016) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2016.116 · Cited by 371 · see citing works
Endometriosis and nuclear receptors
Yilmaz, B. D., & Bulun, S. E. (2019) · Human Reproduction Update · doi:10.1093/humupd/dmz005 · Cited by 243 · see citing works
Endometrial regeneration and endometrial stem/progenitor cells
Gargett, C. E., Nguyen, P. H., & Ye, L. (2012) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-012-9221-9 · Cited by 243 · see citing works
Pathogenesis of endometriosis: Interaction between Endocrine and inflammatory pathways
Patel, B. G., Lenk, E. E., Lebovic, D. I., Shu, Y., Yu, J., & Taylor, R. N. (2018) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2018.01.006 · Cited by 195 · see citing works
Lin, Y.-H., Chen, Y.-H., Chang, H.-Y., Au, H., Tzeng, C., & Huang, Y. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19082385 · Cited by 187 · see citing works
The Role of Integrin α6 (CD49f) in Stem Cells: More than a Conserved Biomarker
Krebsbach, P. H., & Villa-Diaz, L. G. (2017) · Stem Cells and Development · doi:10.1089/scd.2016.0319 · Cited by 177 · see citing works
Potential role of endometrial stem/progenitor cells in the pathogenesis of early-onset endometriosis
Gargett, C. E., Schwab, K. E., Brosens, J. J., Puttemans, P., Benagiano, G., & Brosens, I. A. (2014) · Molecular Human Reproduction · doi:10.1093/molehr/gau025 · Cited by 165 · see citing works
Endometrial stem/progenitor cells and their role in the pathogenesis of endometriosis
Cousins, F. L., O, D. F., & Gargett, C. E. (2018) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2018.01.011 · Cited by 158 · see citing works
The Role of Stem Cells in the Etiology and Pathophysiology of Endometriosis
Hufnagel, D. H., Li, F., Çoşar, E., Krikun, G., & Taylor, H. S. (2015) · Seminars in Reproductive Medicine · doi:10.1055/s-0035-1564609 · Cited by 132 · see citing works
Mesenchymal Stem Cells as a Bio Organ for Treatment of Female Infertility
Esfandyari, S., Chugh, R. M., Park, H.-S., Hobeika, E. M., Ulin, M., & Al-Hendy, A. A. (2020) · Cells · doi:10.3390/cells9102253 · Cited by 120 · see citing works
Using Mesenchymal Stem Cells to Treat Female Infertility: An Update on Female Reproductive Diseases
Zhao, Y., Chen, S.-R., Su, P., Huang, F.-H., Shi, Y., Shi, Q.-Y., & Lin, S. (2019) · Stem Cells International · doi:10.1155/2019/9071720 · Cited by 119 · see citing works
Nikoo, S., Ebtekar, M., Jeddi‐Tehrani, M., Shervin, A., Bozorgmehr, M., Vafaei, S., Kazemnejad, S., & Zarnani, A.-H. (2014) · Molecular Human Reproduction · doi:10.1093/molehr/gau044 · Cited by 107 · see citing works
DNA methylation in endometriosis (Review)
KOUKOURA, O., SIFAKIS, S., & SPANDIDOS, D. A. (2016) · Molecular Medicine Reports · doi:10.3892/mmr.2016.4925 · Cited by 103 · see citing works
Gao, L., Huang, Z., Lin, H., Tian, Y., Li, P., & Lin, S. (2018) · Reproductive Sciences · doi:10.1177/1933719118799201 · Cited by 84 · see citing works
Endometrial Stem/Progenitor Cells–Their Role in Endometrial Repair and Regeneration
Cousins, F. L., Filby, C. E., & Gargett, C. E. (2022) · Frontiers in Reproductive Health · doi:10.3389/frph.2021.811537 · Cited by 81 · see citing works
New concepts on the etiology of endometriosis
Cousins, F. L., McKinnon, B. D., Mortlock, S., Fitzgerald, H. C., Zhang, C., Montgomery, G. W., & Gargett, C. E. (2023) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.15549 · Cited by 82 · see citing works
Heard, M. E., Simmons, C. D., Simmen, F. A., & Simmen, R. C. M. (2014) · Endocrinology · doi:10.1210/en.2013-1947 · Cited by 68 · see citing works
Wolff, E. F., Mutlu, L., Massasa, E. E., Elsworth, J. D., Redmond, D. E., & Taylor, H. S. (2014) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.12433 · Cited by 66 · see citing works
Regenerating endometrium from stem/progenitor cells
Deane, J. A., Gualano, R. C., & Gargett, C. E. (2013) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0b013e32836024e7 · Cited by 65 · see citing works
Forte, A., Cipollaro, M., & Galderisi, U. (2013) · Clinical Science · doi:10.1042/cs20130099 · Cited by 63 · see citing works
Expression of the pluripotent transcription factor OCT4 promotes cell migration in endometriosis
Chang, J.-H., Au, H., Lee, W.-C., Chi, C., Ling, T., Wang, L.-M., Kao, S., Huang, Y., & Tzeng, C. (2013) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.11.033 · Cited by 60 · see citing works
Chan, R. W. S., Lee, C., Ng, E. H. Y., & Yeung, W. S. B. (2017) · Cell Proliferation · doi:10.1111/cpr.12330 · Cited by 45 · see citing works
Self-citationA Revised Stem Cell Theory for the Pathogenesis of Endometriosis
Maruyama, T. (2022) · Journal of Personalized Medicine · doi:10.3390/jpm12020216 · Cited by 45 · see citing works
Cao, M., Chan, R., Cheng, F. H. C., Li, J., Li, T., Pang, R. T. K., Lee, C., Li, R., Ng, E. H. Y., Chiu, P. C. N., et al. (2019) · Stem Cells · doi:10.1002/stem.3070 · Cited by 42 · see citing works
Self-citationLiu, Y., Zhang, Z., Yang, F., Wang, H., Liang, S., Wang, H., Yang, J., & Lin, J. (2020) · Biology of Reproduction · doi:10.1093/biolre/ioaa011 · Cited by 43 · see citing works
The Krüppel-like factors in female reproductive system pathologies
Simmen, R. C. M., Heard, M. E., Simmen, A. M., Montales, M. T. E., Marji, M., Scanlon, S. A., & Pabona, J. M. P. (2015) · Journal of Molecular Endocrinology · doi:10.1530/jme-14-0310 · Cited by 41 · see citing works
Liu, Y., Liang, S., Yang, F., Sun, Y., Niu, L., Ren, Y., Wang, H., He, Y., Du, J., Yang, J., et al. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-01856-8 · Cited by 41 · see citing works
Cellular Origins of Endometriosis: Towards Novel Diagnostics and Therapeutics
Filby, C. E., Rombauts, L. J. F., Montgomery, G. W., Giudice, L. C., & Gargett, C. E. (2020) · Seminars in Reproductive Medicine · doi:10.1055/s-0040-1713429 · Cited by 40 · see citing works
Pittatore, G., BiolSci, A. M., Benedetto, C., Bussolati, B., & Revelli, A. (2013) · Reproductive Sciences · doi:10.1177/1933719113503405 · Cited by 37 · see citing works
TGF-βI Regulates Cell Migration through Pluripotent Transcription Factor OCT4 in Endometriosis
Au, H., Chang, J.-H., Wu, Y.-C., Kuo, Y., Chen, Y.-H., Lee, W.-C., Chang, T., Lan, P., Kuo, H.-C., Lee, K., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0145256 · Cited by 37 · see citing works
Integrin α6 (CD49f), The Microenvironment and Cancer Stem Cells
Bigoni-Ordóñez, G. D., Czarnowski, D., Parsons, T. M., Madlambayan, G. J., & Villa-Diaz, L. (2018) · Current Stem Cell Research & Therapy · doi:10.2174/1574888x13666181002151330 · Cited by 25 · see citing works
Filby, C. E., Wyatt, K. A., Mortlock, S., Cousins, F. L., McKinnon, B. D., Tyson, K., Montgomery, G. W., & Gargett, C. E. (2021) · Journal of Personalized Medicine · doi:10.3390/jpm11121314 · Cited by 34 · see citing works
Xu, S. M., Chan, R., Ng, E. H. Y., & Yeung, W. S. B. (2016) · Experimental Cell Research · doi:10.1016/j.yexcr.2016.11.020 · Cited by 31 · see citing works
Self-citationSomatic Stem Cells and Their Dysfunction in Endometriosis
Djokovic, D., & Calhaz–Jorge, C. (2015) · Frontiers in Surgery · doi:10.3389/fsurg.2014.00051 · Cited by 32 · see citing works
Canosa, S., Moggio, A., Brossa, A., Pittatore, G., Marchino, G. L., Leoncini, S., Benedetto, C., Revelli, A., & Bussolati, B. (2017) · Molecular Human Reproduction · doi:10.1093/molehr/gax006 · Cited by 31 · see citing works
The Clinical Applications of Endometrial Mesenchymal Stem Cells
Zuo, W., Xie, B., Li, C., Yan, Y., Zhang, Y., Liu, W. Q., Huang, J., & Chen, D. (2017) · Biopreservation and Biobanking · doi:10.1089/bio.2017.0057 · Cited by 31 · see citing works
Xu, S. M., Chan, R., Li, T., Ng, E. H. Y., & Yeung, W. S. B. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-01750-3 · Cited by 29 · see citing works
Self-citationExpression and localisation of osteopontin and prominin-1 (CD133) in patients with endometriosis
D’AMICO, F., SKARMOUTSOU, E., QUADERNO, G., MALAPONTE, G., LA CORTE, C., SCIBILIA, G., D’AGATE, G., SCOLLO, P., FRAGGETTA, F., SPANDIDOS, D. A., et al. (2013) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2013.1325 · Cited by 28 · see citing works
Ma, S., Hirata, T., Arakawa, T., Sun, H. J., Neriishi, K., Fukuda, S., Nakazawa, A., Wang, Y., Harada, M., Hirota, Y., et al. (2020) · Reproductive Sciences · doi:10.1007/s43032-019-00041-4 · Cited by 28 · see citing works
Endometrial stem/progenitor cells
Maruyama, T. (2014) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.12501 · Cited by 27 · see citing works
Endometriosis: A Role for Stem Cells
Dhesi, A. S., & Morelli, S. S. (2015) · Women s Health · doi:10.2217/whe.14.57 · Cited by 25 · see citing works
The pathogenesis of endometriosis and adenomyosis: insights from single-cell RNA sequencing
Li, Q., Shi, J., Dai, Y., Li, X., Gu, Z., Yan, H., & Leng, J. (2024) · Biology of Reproduction · doi:10.1093/biolre/ioae032 · Cited by 20 · see citing works
The Search for Biomarkers in Endometriosis: a Long and Windy Road
Králíčková, M., Větvička, V., Fiala, L., Laganà, A. S., & Garzon, S. (2021) · Reproductive Sciences · doi:10.1007/s43032-021-00668-2 · Cited by 20 · see citing works
The Pathogenesis of Endometriosis: Are Endometrial Stem/Progenitor Cells Involved?
Laganà, A. S., & Naem, A. (2022) · Stem cell biology and regenerative medicine · doi:10.1007/978-3-030-90111-0_9 · Cited by 21 · see citing works
Sicking, M., Falke, I., Löblein, M. T., Eich, H. T., Götte, M., Greve, B., & Troschel, F. M. (2023) · Biomarker Research · doi:10.1186/s40364-023-00516-2 · Cited by 19 · see citing works
Singh, P., Metkari, S., & Bhartiya, D. (2021) · Stem Cell Reviews and Reports · doi:10.1007/s12015-021-10279-8 · Cited by 19 · see citing works
Li, L., Gao, H., Pan, L., Zhao, Y., Liang, Z., Zhang, Q., & Wang, D. (2021) · Annals of Palliative Medicine · doi:10.21037/apm-21-2175 · Cited by 16 · see citing works
Chen, Y., Wang, J.-H., Yan, J., Liang, Y., Zhang, X., & Zhou, F. (2013) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2013.11.025 · Cited by 17 · see citing works
Park, S.-R., Kim, S., Kim, S., Park, J.-R., & Hong, I. (2022) · Experimental & Molecular Medicine · doi:10.1038/s12276-022-00858-1 · Cited by 16 · see citing works
Therapeutic restoration of female reproductive and endocrine dysfunction using stem cells
Liu, X., Li, J., Wang, W., Ren, X., & Hu, J. (2023) · Life Sciences · doi:10.1016/j.lfs.2023.121658 · Cited by 18 · see citing works
Wilczyński, J. R., Szubert, M., Paradowska, E., & Wilczyński, M. (2022) · Cancers · doi:10.3390/cancers15010111 · Cited by 15 · see citing works
He, H., Liu, R., Xiong, W., Pu, D., Wang, S., & Li, T. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.07.004 · Cited by 15 · see citing works
Nanoparticle labeling identifies slow cycling human endometrial stromal cells
Xiang, L., Chan, R., Ng, E. H. Y., & Yeung, W. S. B. (2014) · Stem Cell Research & Therapy · doi:10.1186/scrt473 · Cited by 13 · see citing works
Self-citationAbomaray, F., Gidlöf, S. B., & Gotherstrom, C. O. T. (2017) · Stem Cells International · doi:10.1155/2017/3215962 · Cited by 14 · see citing works
A bird-eye view of diaphragmatic endometriosis: current practices and future perspectives
Naem, A., Roman, H., Martin, D. C., & Krentel, H. (2024) · Frontiers in Medicine · doi:10.3389/fmed.2024.1505399 · Cited by 17 · see citing works
Establishment of endometriotic models: the past and future
Gu, Z., Jia, S., & Leng, J. (2020) · Chinese Medical Journal · doi:10.1097/cm9.0000000000000885 · Cited by 13 · see citing works
Stem Cells in Endometrium and Endometriosis
Ulukuş, M. (2015) · Women s Health · doi:10.2217/whe.15.43 · Cited by 13 · see citing works
Othman, E. R., Meligy, F. Y., Sayed, A. A.-R., El‐Mokhtar, M. A., & Refaiy, A. M. (2017) · Reproductive Sciences · doi:10.1177/1933719117697124 · Cited by 13 · see citing works
Lin, K., Ma, J., Wu, R., Zhou, C., & Lin, J. (2013) · Reproductive Sciences · doi:10.1177/1933719113492205 · Cited by 11 · see citing works
Mitranovici, M.-I., Costăchescu, D., Voidăzan, S. T., Munteanu, M. S., Buicu, C.-F., Oală, I. E., Ivan, V. M., Apostol, A., Melinte, I. M., Crișan, A., et al. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252312749 · Cited by 10 · see citing works
Analysis of CARD10 and CARD11 somatic mutations in patients with ovarian endometriosis
Zou, Y., Zhou, J., Wang, F., Zhang, Z., Liu, F., Luo, Y., Tan, J., Zeng, X., Wan, X., & Huang, O. (2018) · Oncology Letters · doi:10.3892/ol.2018.8659 · Cited by 10 · see citing works
Cressoni, A. C. L., Penariol, L. B. C., Padovan, C. C., Orellana, M. D., Silva, J. C. R. E., Poli‐Neto, O. B., Ferriani, R. A., de Paz, C. C. P., & Meola, J. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24065963 · Cited by 9 · see citing works
Adult Stem Cells in the Pathogenesis and Treatment of Endometriosis
Cousins, F. L., Xiao, L. Y., & Gargett, C. E. (2017) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.5301/jeppd.5000310 · Cited by 7 · see citing works
Endometriosis: Are Stem Cells Involved?
Králíčková, M. (2015) · International Journal of Clinical and Experimental Medical Sciences · doi:10.11648/j.ijcems.20150103.16 · Cited by 6 · see citing works
Perinatal origin of endometriosis revisited
Brosens, I. A., & Benagiano, G. (2015) · Gynecological Endocrinology · doi:10.3109/09513590.2015.1017458 · Cited by 6 · see citing works
Velho, R. V., Danielyan, I., Mechsner, S., & Götte, M. (2023) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2023.07.017 · Cited by 6 · see citing works
Bairagi, S., Gopal, J., Nathan, A. A., Babu, S., Kumar, N. P., & Dixit, M. (2012) · Human Reproduction · doi:10.1093/humrep/der457 · Cited by 6 · see citing works
New approaches to the treatment of endometriosis
Татарчук, Т. Ф., Захаренко, Н. Ф., & Тутченко, Т. Н. (2013) · Reproductive Endocrinology · doi:10.18370/2309-4117.2013.11.36-42 · Cited by 5 · see citing works
Target Localization and Tracking Using WSN
Jondhale, S. R., Maheswar, R., & Lloret, J. (2021) · EAI/Springer Innovations in Communication and Computing · doi:10.1007/978-3-030-74061-0_2 · Cited by 5 · see citing works
Deraya, I. E., Hestiantoro, A., Muharam, R., Marwali, M. L. S., Darmawi, D., & Asmarinah, A. (2020) · IOP Conference Series Earth and Environmental Science · doi:10.1088/1755-1315/457/1/012079 · Cited by 5 · see citing works
Taylor, R. N., & Lebovic, D. I. (2013) · Elsevier eBooks · doi:10.1016/b978-1-4557-2758-2.00026-3 · Cited by 5 · see citing works
Expression and significance of CD133 and ABCG2 in endometriosis
Liu, S., Zhou, J., & Wen, J. (2015) · Clinical and Experimental Obstetrics & Gynecology · doi:10.12891/ceog1978.2015 · Cited by 5 · see citing works
Mechanisms and applications of mesenchymal stem cell exosomes in enhancing fertility
Wang, Y., Wang, R., Zhao, Y., Han, N., Han, X.-J., Shi, T. S., Liu, Y., Zhao, N., Li, S., Wang, S., et al. (2025) · Stem Cell Research & Therapy · doi:10.1186/s13287-025-04729-0 · Cited by 6 · see citing works
The Biological Characteristics of Eutopic and Ectopic Endometrial Progenitor Cells in Endometriosis
Zhang, Q., Liang, J., Xu, D., Gao, T., Zhang, J., Liang, H., Wang, W., Ling, B., & Feng, D. (2023) · Current Stem Cell Research & Therapy · doi:10.2174/1574888x18666230203162452 · Cited by 4 · see citing works
Survey of Existing RSSI-Based L&T Systems
Jondhale, S. R., Maheswar, R., & Lloret, J. (2021) · EAI/Springer Innovations in Communication and Computing · doi:10.1007/978-3-030-74061-0_3 · Cited by 4 · see citing works
Song, Y., Wang, L., & Zhang, Y. (2023) · Medicine · doi:10.1097/md.0000000000036707 · Cited by 3 · see citing works
Contrast-Enhanced Ultrasonography in Sclerotherapy for Ovarian Endometrial Cyst
Shao, X., Dong, X., Kong, D., Zhang, L., Wang, L., & Wang, S. (2018) · Ultrasound in Medicine & Biology · doi:10.1016/j.ultrasmedbio.2018.03.025 · Cited by 3 · see citing works
Characteristic and Regenerative Potential of Human Endometrial Stem Cells and Progenitors
Ghamari, A., Daghigh, F., Mohebbi, A., Rahimi, Y., Shojaie, L., & Zolbin, M. M. (2021) · Springer eBooks · doi:10.1007/978-981-16-0301-3_3 · Cited by 2 · see citing works
Trophoblast, amniotic fluid, endometrium, and bone marrow
Simón, C., Pellicer, A., & Pera, R. A. R. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139540742.011 · Cited by 2 · see citing works
Gupta, S., Harlev, A., Agarwal, A. K., Rakhit, M., Ellis-Kahana, J., & Parikh, S. (2015) · SpringerBriefs in reproductive biology · doi:10.1007/978-3-319-18308-4_10 · Cited by 2 · see citing works
Adult stem cells in the human endometrium
Gargett, C. E., Cervelló, I., Nguyen, H. P. T., & Simón, C. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139540742.012 · Cited by 2 · see citing works
Şimşek, H. U., Şimşek, T., Duruksu, G., Rençber, S. F., & Yazır, Y. (2024) · Balkan Medical Journal · doi:10.4274/balkanmedj.galenos.2024.2024-6-95 · Cited by 1 · see citing works
Stem Cell as the Novel Pathogenesis of Endometriosis
Tsai, E. (2012) · InTech eBooks · doi:10.5772/29695 · Cited by 1 · see citing works
Role of Stem Cells in the Pathogenesis of Endometriosis
Maruyama, T. (2014) · Springer eBooks · doi:10.1007/978-4-431-54421-0_4 · Cited by 1 · see citing works
Characteristics and Therapeutic Potential of Menstrual Blood-Derived Stem Cells
Achmad, N., & Götte, M. (2014) · Springer eBooks · doi:10.1007/978-1-4471-6542-2_7 · Cited by 1 · see citing works
Markowski, D. N., Küpker, W., & BULLERDIEK, J. (2012) · Gynäkologische Endokrinologie · doi:10.1007/s10304-012-0483-9 · Cited by 1 · see citing works
Endocrine Aspects of Endometrial Stem Cell Function in Reproductive-Age Women
Götte, M., & Kiesel, L. (2013) · Journal für Kardiologie (Krause & Pachernegg GmbH) · Cited by 1 · see citing works
Side Population Cells in Human Adenomyotic Lesions Display Characteristics of Endometrial Stem Cells
Huang, W., Zhu, S., Xiao, L. Y., Zhou, M., Zhang, X., Yang, S., Wei, X., & Sun, H. (2015) · International Journal of Stem Cell Research and Transplantation · doi:10.19070/2328-3548-si01001
The potential role of stem cells in the pathogenesis of endometriosis
Олеговна, Д. С., Berlim, Y. D., Станиславович, Г. В., Викторовна, К. Л., & Arechan, K. A. (2017) · Russian Journal of Human Reproduction · doi:10.17116/repro201723266-71
Rozati, R., Tabasum, W., Mehdi, A. G., Ayapati, V. A., Bhadria, A., & Fatima, S. (2019) · International Journal of Clinical Obstetrics and Gynaecology · doi:10.33545/gynae.2019.v3.i1d.33
Feasibility of serum-free culture in isolating endometriotic stem cells
Liu, S., Tian, X., Cui, H., Zhang, Q., & Hua, K. (2019) · Clinical and Experimental Obstetrics & Gynecology · doi:10.12891/ceog4921.2019
Etiopathogenesis of internal and external genital endometriosis (evolution of views)
Pechenikova, V. A., & Akopyan, R. A. (2018) · Bulletin of the Russian Military Medical Academy · doi:10.17816/brmma12352
Menstruation: Myths, Mechanisms, Models and Malfunctions
(2024) · Frontiers research topics · doi:10.3389/978-2-8325-4935-3
Xu, S., Chan, R., Li, T., Ng, E. H. Y., & Yeung, W. S. B. (2020) · Figshare · doi:10.6084/m9.figshare.12502919
Self-citationResearch Advances in Stem Cell-Mediated Immune and Inflammatory Mechanisms in Endometriosis
肖, 婷. (2026) · Advances in Clinical Medicine · doi:10.12677/acm.2026.1641235
Biomaterial Tools for Modeling Endometriosis
Theriault, H. S., & Harley, B. A. C. (2026) · Springer eBooks · doi:10.1007/978-3-032-10745-9_9
- Authors
- Chan, R. W. S., Ng, E. H. Y., & Yeung, W. S. B.
- Affiliations
- University of Hong Kong (HK)
- Corresponding author
- Chan, Rachel Wah Shan
- Venue
- The American Journal of Pathology
- Publisher
- Elsevier BV
- Published
- 2011-06
- Volume
- 178
- Issue
- 6
- Pages
- 2832-2844
- ISSN
- 0002-9440 (ISSN-L)
- PMC
- PMC3123988
- OpenAlex
- W2083418262
- Cited by
- 98
- References
- 65
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 5 · 2023: 8 · 2022: 5 · 2021: 7 · 2020: 9 · 2019: 5 · 2018: 8 · 2017: 8 · 2016: 4 · 2015: 12 · 2014: 8 · 2013: 12 · 2012: 4
- FWCI
- 8.59
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- American Journal Of Pathology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- The HKU Scholars Hub (University of Hong Kong) (submittedVersion)
- Funders
- General Research Fund of Shanghai Normal University
- Research Grants Council, University Grants Committee (HKU 7822/09M)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Keywords
- endometrioma, colony-forming units, self-renewal, multipotency, mesenchymal differentiation, epithelial cells, stromal cells, CD133, Musashi-1, endometriosis pathogenesis
- MeSH terms
- Adult, Cell Differentiation, Clone Cells, Endometriosis, Endometrium, Epithelial Cells, Female, Humans, Immunohistochemistry, Mesoderm, Middle Aged, Ovary, Phenotype, Stem Cells, Stromal Cells, Cell Lineage, Multipotent Stem Cells, Cell Shape, Cell Proliferation, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review