The Endometrial Stem/Progenitor Cells and Their Niches.

Endometrial Diseases Endometrial Regeneration Endometrial stem/progenitor Cells Interaction Niches

Journal

Stem cell reviews and reports
ISSN: 2629-3277
Titre abrégé: Stem Cell Rev Rep
Pays: United States
ID NLM: 101752767

Informations de publication

Date de publication:
18 Apr 2024
Historique:
accepted: 10 04 2024
medline: 18 4 2024
pubmed: 18 4 2024
entrez: 18 4 2024
Statut: aheadofprint

Résumé

Endometrial stem/progenitor cells are a type of stem cells with the ability to self-renew and differentiate into multiple cell types. They exist in the endometrium and form niches with their neighbor cells and extracellular matrix. The interaction between endometrial stem/progenitor cells and niches plays an important role in maintaining, repairing, and regenerating the endometrial structure and function. This review will discuss the characteristics and functions of endometrial stem/progenitor cells and their niches, the mechanisms of their interaction, and their roles in endometrial regeneration and diseases. Finally, the prospects for their applications will also be explored.

Identifiants

pubmed: 38635126
doi: 10.1007/s12015-024-10725-3
pii: 10.1007/s12015-024-10725-3
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : FDCT
ID : SKL-QRCM (MUST)-2023-2025

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Evans, J., Salamonsen, L. A., Winship, A., Menkhorst, E., Nie, G., Gargett, C. E., & Dimitriadis, E. (2016). Fertile ground: Human endometrial programming and lessons in health and disease. Nature Reviews. Endocrinology, 12(11), 654–667.
pubmed: 27448058 doi: 10.1038/nrendo.2016.116
Timeva, T., Shterev, A., & Kyurkchiev, S. (2014). Recurrent implantation failure: The role of the endometrium. Journal of Reproduction and Fertility, 15(4), 173–183.
Bashiri, A., Halper, K. I., & Orvieto, R. (2018). Recurrent implantation failure-update overview on etiology, diagnosis, treatment and future directions. Reproductive Biology and Endocrinology: Rb&E, 16(1), 121.
doi: 10.1186/s12958-018-0414-2
de Miguel-Gomez, L., Lopez-Martinez, S., Frances-Herrero, E., Rodriguez-Eguren, A., Pellicer, A., & Cervello, I. (2021). Stem Cells and the Endometrium: From the Discovery of Adult Stem Cells to Pre-Clinical Models. Cells 10, (3).
Jin, S. (2019). Bipotent stem cells support the cyclical regeneration of endometrial epithelium of the murine uterus. Proc Natl Acad Sci U S A, 116(14), 6848–6857.
pubmed: 30872480 pmcid: 6452687 doi: 10.1073/pnas.1814597116
Chan, R. W., Schwab, K. E., & Gargett, C. E. (2004). Clonogenicity of human endometrial epithelial and stromal cells. Biology of Reproduction, 70(6), 1738–1750.
pubmed: 14766732 doi: 10.1095/biolreprod.103.024109
Gargett, C. E. (2007). Review article: Stem cells in human reproduction. Reprod Sci, 14(5), 405–424.
pubmed: 17913960 doi: 10.1177/1933719107306231
Prianishnikov, V. A. (1978). On the concept of stem cell and a model of functional-morphological structure of the endometrium. Contraception, 18(3), 213–223.
pubmed: 569035 doi: 10.1016/S0010-7824(78)80015-8
Al-Lamee, H., Hill, C. J., Turner, F., Phan, T., Drakeley, A. J., Hapangama, D. K., & Tempest, N. (2022). The Role of Endometrial Stem/Progenitor Cells in Recurrent Reproductive Failure. Journal of personalized medicine 12, (5).
Wang, X., Liu, L., Mou, S., Zhao, H., Fang, J., Xiang, Y., Zhao, T., Sha, T., Ding, J., & Hao, C. (2019). Investigation of platelet-rich plasma in increasing proliferation and migration of endometrial mesenchymal stem cells and improving pregnancy outcome of patients with thin endometrium. Journal of Cellular Biochemistry, 120(5), 7403–7411.
pubmed: 30506864 doi: 10.1002/jcb.28014
Gargett, C. E., Schwab, K. E., & Deane, J. A. (2016). Endometrial stem/progenitor cells: The first 10 years. Human Reproduction Update, 22(2), 137–163.
pubmed: 26552890
Moore, K. A., & Lemischka, I. R. (2006). Stem cells and their niches. Science, 311(5769), 1880–1885.
pubmed: 16574858 doi: 10.1126/science.1110542
Schwab, K. E., & Gargett, C. E. (2007). Co-expression of two perivascular cell markers isolates mesenchymal stem-like cells from human endometrium. Human Reproduction, 22(11), 2903–2911.
pubmed: 17872908 doi: 10.1093/humrep/dem265
Li, T., Chan, R. W. S., Li, R. H. W., Ng, E. H. Y., Zhang, S., & Yeung, W. S. B. (2024). Endometrial mesenchymal stromal/stem cells improve regeneration of injured endometrium in mice. Biological Research, 57(1), 6.
pubmed: 38347646 pmcid: 10863157 doi: 10.1186/s40659-024-00484-3
Kong, Y., Shao, Y., Ren, C., & Yang, G. (2021). Endometrial stem/progenitor cells and their roles in immunity, clinical application, and endometriosis. Stem Cell Research & Therapy, 12(1), 474.
doi: 10.1186/s13287-021-02526-z
Giri, J., & Modi, D. (2023). Endometrial and placental stem cells in successful and pathological pregnancies. Journal of Assisted Reproduction and Genetics, 40(7), 1509–1522.
pubmed: 37338750 doi: 10.1007/s10815-023-02856-2
Hong, I. S. (2024). Endometrial stem cells: Orchestrating dynamic regeneration of Endometrium and their implications in Diverse Endometrial disorders. International Journal of Biological Sciences, 20(3), 864–879.
pubmed: 38250149 pmcid: 10797688 doi: 10.7150/ijbs.89795
Lee, J. W., & Lee, H. Y. (2023). Exploring distinct properties of endometrial stem cells through advanced single-cell analysis platforms. Stem Cell Research & Therapy, 14(1), 379.
doi: 10.1186/s13287-023-03616-w
Schwab, K. E., Chan, R. W., & Gargett, C. E. (2005). Putative stem cell activity of human endometrial epithelial and stromal cells during the menstrual cycle. Fertility and Sterility, 84(Suppl 2), 1124–1130.
pubmed: 16210003 doi: 10.1016/j.fertnstert.2005.02.056
Gotte, M., Wolf, M., Staebler, A., Buchweitz, O., Kelsch, R., Schuring, A. N., & Kiesel, L. (2008). Increased expression of the adult stem cell marker Musashi-1 in endometriosis and endometrial carcinoma. The Journal of Pathology, 215(3), 317–329.
pubmed: 18473332 doi: 10.1002/path.2364
Borlongan, C. V., Kaneko, Y., Maki, M., Yu, S. J., Ali, M., Allickson, J. G., Sanberg, C. D., Kuzmin-Nichols, N., & Sanberg, P. R. (2010). Menstrual blood cells display stem cell-like phenotypic markers and exert neuroprotection following transplantation in experimental stroke. Stem Cells and Development, 19(4), 439–452.
pubmed: 19860544 pmcid: 3158424 doi: 10.1089/scd.2009.0340
Masuda, H., Anwar, S. S., Buhring, H. J., Rao, J. R., & Gargett, C. E. (2012). A novel marker of human endometrial mesenchymal stem-like cells. Cell Transplantation, 21(10), 2201–2214.
pubmed: 22469435 doi: 10.3727/096368911X637362
Zhu, X., Yu, F., Yan, G., Hu, Y., Sun, H., & Ding, L. (2021). Human endometrial perivascular stem cells exhibit a limited potential to regenerate endometrium after xenotransplantation. Human Reproduction, 36(1), 145–159.
pubmed: 33283858
Wolff, E. F., Wolff, A. B., Hongling, D., & Taylor, H. S. (2007). Demonstration of multipotent stem cells in the adult human endometrium by in vitro chondrogenesis. Reprod Sci, 14(6), 524–533.
pubmed: 17959881 doi: 10.1177/1933719107306896
Bhartiya, D., Patel, H., Ganguly, R., Shaikh, A., Shukla, Y., Sharma, D., & Singh, P. (2018). Novel insights into Adult and Cancer Stem Cell Biology. Stem Cells and Development, 27(22), 1527–1539.
pubmed: 30051749 doi: 10.1089/scd.2018.0118
Du, X., Yuan, Q., Qu, Y., Zhou, Y., & Bei, J. (2016). Endometrial Mesenchymal Stem Cells Isolated from Menstrual Blood by Adherence. Stem Cells Int 2016, 3573846.
Gargett, C. E., Schwab, K. E., Zillwood, R. M., Nguyen, H. P., & Wu, D. (2009). Isolation and culture of epithelial progenitors and mesenchymal stem cells from human endometrium. Biology of Reproduction, 80(6), 1136–1145.
pubmed: 19228591 pmcid: 2849811 doi: 10.1095/biolreprod.108.075226
Hapangama, D. K., Drury, J., Da Silva, L., Al-Lamee, H., Earp, A., Valentijn, A. J., Edirisinghe, D. P., Murray, P. A., Fazleabas, A. T., & Gargett, C. E. (2019). Abnormally located SSEA1+/SOX9 + endometrial epithelial cells with a basalis-like phenotype in the eutopic functionalis layer may play a role in the pathogenesis of endometriosis. Human Reproduction, 34(1), 56–68.
pubmed: 30496412 doi: 10.1093/humrep/dey336
Valentijn, A. J., Palial, K., Al-Lamee, H., Tempest, N., Drury, J., Von Zglinicki, T., Saretzki, G., Murray, P., Gargett, C. E., & Hapangama, D. K. (2013). SSEA-1 isolates human endometrial basal glandular epithelial cells: Phenotypic and functional characterization and implications in the pathogenesis of endometriosis. Human Reproduction, 28(10), 2695–2708.
pubmed: 23847113 doi: 10.1093/humrep/det285
Masuda, H., Maruyama, T., Hiratsu, E., Yamane, J., Iwanami, A., Nagashima, T., Ono, M., Miyoshi, H., Okano, H. J., Ito, M., Tamaoki, N., Nomura, T., Okano, H., Matsuzaki, Y., & Yoshimura, Y. (2007). Noninvasive and real-time assessment of reconstructed functional human endometrium in NOD/SCID/gamma c(null) immunodeficient mice. Proc Natl Acad Sci U S A, 104(6), 1925–1930.
pubmed: 17261813 pmcid: 1794295 doi: 10.1073/pnas.0604310104
Nguyen, H. P. T., Xiao, L., Deane, J. A., Tan, K. S., Cousins, F. L., Masuda, H., Sprung, C. N., Rosamilia, A., & Gargett, C. (2017). E., N-cadherin identifies human endometrial epithelial progenitor cells by in vitro stem cell assays. Human Reproduction, 32(11), 2254–2268.
pubmed: 29040564 doi: 10.1093/humrep/dex289
Kato, K., Yoshimoto, M., Kato, K., Adachi, S., Yamayoshi, A., Arima, T., Asanoma, K., Kyo, S., Nakahata, T., & Wake, N. (2007). Characterization of side-population cells in human normal endometrium. Human Reproduction, 22(5), 1214–1223.
pubmed: 17283036 doi: 10.1093/humrep/del514
Tsuji, S., Yoshimoto, M., Takahashi, K., Noda, Y., Nakahata, T., & Heike, T. (2008). Side population cells contribute to the genesis of human endometrium. Fertility and Sterility, 90(4 Suppl), 1528–1537.
pubmed: 18462721 doi: 10.1016/j.fertnstert.2007.08.005
Dimitrov, R., Timeva, T., Kyurkchiev, D., Stamenova, M., Shterev, A., Kostova, P., Zlatkov, V., Kehayov, I., & Kyurkchiev, S. (2008). Characterization of clonogenic stromal cells isolated from human endometrium. Reproduction, 135(4), 551–558.
pubmed: 18367513 doi: 10.1530/REP-07-0428
Masuda, H., Matsuzaki, Y., Hiratsu, E., Ono, M., Nagashima, T., Kajitani, T., Arase, T., Oda, H., Uchida, H., Asada, H., Ito, M., Yoshimura, Y., Maruyama, T., & Okano, H. (2010). Stem cell-like properties of the endometrial side population: Implication in endometrial regeneration. PLoS One 5, (4), e10387.
Zhou, S., Schuetz, J. D., Bunting, K. D., Colapietro, A. M., Sampath, J., Morris, J. J., Lagutina, I., Grosveld, G. C., Osawa, M., Nakauchi, H., & Sorrentino, B. P. (2001). The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nature Medicine, 7(9), 1028–1034.
pubmed: 11533706 doi: 10.1038/nm0901-1028
Guo, C., Zhu, H., Huang, W., Li, S., Qu, W., Liu, Y., & Tan, A. (2010). Side population cells in the human decidua of early pregnancy exhibit stem/progenitor cell-like characteristics. Reproductive Biomedicine Online, 21(6), 783–793.
pubmed: 21051287 doi: 10.1016/j.rbmo.2010.07.010
Cervello, I., Gil-Sanchis, C., Mas, A., Delgado-Rosas, F., Martinez-Conejero, J. A., Galan, A., Martinez-Romero, A., Martinez, S., Navarro, I., Ferro, J., Horcajadas, J. A., Esteban, F. J., O’Connor, J. E., Pellicer, A., & Simon, C. (2010). Human endometrial side population cells exhibit genotypic, phenotypic and functional features of somatic stem cells. PLoS One 5, (6), e10964.
Cervello, I., Mas, A., Gil-Sanchis, C., Peris, L., Faus, A., Saunders, P. T., Critchley, H. O., & Simon, C. (2011). Reconstruction of endometrium from human endometrial side population cell lines. PLoS One 6, (6), e21221.
Kucia, M., Zhang, Y. P., Reca, R., Wysoczynski, M., Machalinski, B., Majka, M., Ildstad, S. T., Ratajczak, J., Shields, C. B., & Ratajczak, M. Z. (2006). Cells enriched in markers of neural tissue-committed stem cells reside in the bone marrow and are mobilized into the peripheral blood following stroke. Leukemia, 20(1), 18–28.
pubmed: 16270036 doi: 10.1038/sj.leu.2404011
Ratajczak, M. Z., Zuba-Surma, E. K., Wysoczynski, M., Ratajczak, J., & Kucia, M. (2008). Very small embryonic-like stem cells: Characterization, developmental origin, and biological significance. Experimental Hematology, 36(6), 742–751.
pubmed: 18474305 pmcid: 2430762 doi: 10.1016/j.exphem.2008.03.010
Bhartiya, D., Singh, P., Sharma, D., & Kaushik, A. (2022). Very small embryonic-like stem cells (VSELs) regenerate whereas mesenchymal stromal cells (MSCs) rejuvenate diseased reproductive tissues. Stem Cell Rev Rep, 18(5), 1718–1727.
pubmed: 34410593 doi: 10.1007/s12015-021-10243-6
Singh, P., & Bhartiya, D. (2021). Pluripotent stem (VSELs) and progenitor (EnSCs) cells exist in adult mouse Uterus and Show Cyclic changes Across Estrus cycle. Reprod Sci, 28(1), 278–290.
pubmed: 32710237 doi: 10.1007/s43032-020-00250-2
Ratajczak, M. Z., Ratajczak, J., & Kucia, M. (2019). Very small embryonic-like Stem cells (VSELs). Circ Res, 124(2), 208–210.
pubmed: 30653438 pmcid: 6461217 doi: 10.1161/CIRCRESAHA.118.314287
Bhartiya, D., Shaikh, A., Anand, S., Patel, H., Kapoor, S., Sriraman, K., Parte, S., & Unni, S. (2016). Endogenous, very small embryonic-like stem cells: Critical review, therapeutic potential and a look ahead. Human Reproduction Update, 23(1), 41–76.
pubmed: 27614362 doi: 10.1093/humupd/dmw030
Singh, P., Metkari, S., & Bhartiya, D. (2022). Additional evidence to support OCT-4 positive VSELs and EnSCs as the elusive tissue-resident stem/progenitor cells in adult mice uterus. Stem Cell Research & Therapy, 13(1), 60.
doi: 10.1186/s13287-022-02703-8
Kaushik, A., & Bhartiya, D. (2020). Additional evidence to establish existence of two stem cell populations including VSELs and SSCs in adult mouse testes. Stem Cell Rev Rep, 16(5), 992–1004.
pubmed: 32578128 doi: 10.1007/s12015-020-09993-6
Kaushik, A., Anand, S., & Bhartiya, D. (2020). Altered Biology of testicular VSELs and SSCs by neonatal endocrine disruption results in defective spermatogenesis, reduced fertility and tumor initiation in adult mice. Stem Cell Rev Rep, 16(5), 893–908.
pubmed: 32592162 doi: 10.1007/s12015-020-09996-3
Sharma, D., & Bhartiya, D. (2022). Dysfunctional ovarian stem cells due to neonatal endocrine disruption result in PCOS and ovarian insufficiency in adult mice. Stem Cell Rev Rep, 18(8), 2912–2927.
pubmed: 35834052 doi: 10.1007/s12015-022-10414-z
Singh, P., & Bhartiya, D. (2023). Mouse uterine stem cells are affected by endocrine disruption and initiate uteropathies. Reproduction, 165(3), 249–268.
pubmed: 36488194
Bhartiya, D. (2023). Correction to: Ovarian stem cells are always accompanied by very small embryonic-like stem cells in adult mammalian ovary. J Ovarian Res, 16(1), 163.
pubmed: 37580763 pmcid: 10424364 doi: 10.1186/s13048-023-01254-7
Watt, F. M., & Hogan, B. L. (2000). Out of Eden: Stem cells and their niches. Science, 287(5457), 1427–1430.
pubmed: 10688781 doi: 10.1126/science.287.5457.1427
Spradling, A., Drummond-Barbosa, D., & Kai, T. (2001). Stem cells find their niche. Nature, 414(6859), 98–104.
pubmed: 11689954 doi: 10.1038/35102160
Ahmed, M., & Ffrench-Constant, C. (2016). Extracellular matrix regulation of Stem Cell Behavior. Current Stem Cell Reports, 2(3), 197–206.
pubmed: 27547708 pmcid: 4972867 doi: 10.1007/s40778-016-0056-2
Alsobaie, S., Alsobaie, T., Alshammary, A. F., Abudawood, M., & Mantalaris, A. (2023). Alginate beads as a Promising Tool for successful production of viable and Pluripotent Human-Induced pluripotent stem cells in a 3D culture system. Stem Cells Cloning, 16, 61–73.
pubmed: 37790697 pmcid: 10544263
Cervello, I., Santamaria, X., Miyazaki, K., Maruyama, T., & Simon, C. (2015). Cell therapy and tissue Engineering from and toward the Uterus. Seminars in Reproductive Medicine, 33(5), 366–372.
pubmed: 26285168 doi: 10.1055/s-0035-1559581
Chacon-Martinez, C. A., Koester, J., & Wickstrom, S. A. (2018). Signaling in the stem cell niche: regulating cell fate, function and plasticity. Development 145, (15).
de Miguel-Gomez, L., Ferrero, H., Lopez-Martinez, S., Campo, H., Lopez-Perez, N., Faus, A., Hervas, D., Santamaria, X., Pellicer, A., & Cervello, I. (2020). Stem cell paracrine actions in tissue regeneration and potential therapeutic effect in human endometrium: A retrospective study. Bjog, 127(5), 551–560.
pubmed: 31876085 doi: 10.1111/1471-0528.16078
Gargett, C. E., & Masuda, H. (2010). Adult stem cells in the endometrium. Molecular Human Reproduction, 16(11), 818–834.
pubmed: 20627991 doi: 10.1093/molehr/gaq061
Schofield, R. (1978). The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells, 4(1-2), 7–25.
pubmed: 747780
Hall, P. A., & Watt, F. M. (1989). Stem cells: The generation and maintenance of cellular diversity. Development, 106(4), 619–633.
pubmed: 2562658 doi: 10.1242/dev.106.4.619
Hurwitz, S. N., Jung, S. K., & Kurre, P. (2020). Hematopoietic stem and progenitor cell signaling in the niche. Leukemia, 34(12), 3136–3148.
pubmed: 33077865 doi: 10.1038/s41375-020-01062-8
Gerber-Ferder, Y., Cosgrove, J., Duperray-Susini, A., Missolo-Koussou, Y., Dubois, M., Stepaniuk, K., Pereira-Abrantes, M., Sedlik, C., Lameiras, S., Baulande, S., Bendriss-Vermare, N., Guermonprez, P., Passaro, D., Perie, L., Piaggio, E., & Helft, J. (2023). Breast cancer remotely imposes a myeloid bias on haematopoietic stem cells by reprogramming the bone marrow niche. Nature Cell Biology, 25(12), 1736–1745.
pubmed: 38036749 doi: 10.1038/s41556-023-01291-w
Morrison, S. J., & Scadden, D. T. (2014). The bone marrow niche for haematopoietic stem cells. Nature, 505(7483), 327–334.
pubmed: 24429631 pmcid: 4514480 doi: 10.1038/nature12984
Scadden, D. T. (2006). The stem-cell niche as an entity of action. Nature, 441(7097), 1075–1079.
pubmed: 16810242 doi: 10.1038/nature04957
Sui, B. D., Zhu, B., Hu, C. H., Zhao, P., & Jin, Y. (2019). Reconstruction of Regenerative Stem Cell Niche by Cell Aggregate Engineering. Methods in Molecular Biology, 2002, 87–99.
pubmed: 30187400 doi: 10.1007/7651_2018_186
Velikic, G., Maric, D. M., Maric, D. L., Supic, G., Puletic, M., Dulic, O., & Vojvodic, D. (2024). Harnessing the Stem Cell Niche in Regenerative Medicine: Innovative Avenue to Combat Neurodegenerative diseases. International Journal of Molecular Sciences 25, (2).
Lane, S. W., Williams, D. A., & Watt, F. M. (2014). Modulating the stem cell niche for tissue regeneration. Nature Biotechnology, 32(8), 795–803.
pubmed: 25093887 pmcid: 4422171 doi: 10.1038/nbt.2978
Rozario, T., & DeSimone, D. W. (2010). The extracellular matrix in development and morphogenesis: A dynamic view. Development Biology, 341(1), 126–140.
doi: 10.1016/j.ydbio.2009.10.026
Dzamba, B. J., & DeSimone, D. W. (2018). Extracellular matrix (ECM) and the sculpting of embryonic tissues. Current Topics in Developmental Biology, 130, 245–274.
pubmed: 29853179 doi: 10.1016/bs.ctdb.2018.03.006
Li, X., Lv, H. F., Zhao, R., Ying, M. F., Samuriwo, A. T., & Zhao, Y. Z. (2021). Recent developments in bio-scaffold materials as delivery strategies for therapeutics for endometrium regeneration. Mater Today Bio, 11, 100101.
pubmed: 34036261 pmcid: 8138682 doi: 10.1016/j.mtbio.2021.100101
Tempest, N., Baker, A. M., Wright, N. A., & Hapangama, D. K. (2018). Does human endometrial LGR5 gene expression suggest the existence of another hormonally regulated epithelial stem cell niche? Human Reproduction, 33(6), 1052–1062.
pubmed: 29648645 pmcid: 5972618 doi: 10.1093/humrep/dey083
Tempest, N., Hill, C. J., Maclean, A., Marston, K., Powell, S. G., Al-Lamee, H., & Hapangama, D. K. (2022). Novel microarchitecture of human endometrial glands: Implications in endometrial regeneration and pathologies. Human Reproduction Update, 28(2), 153–171.
pubmed: 34875046 doi: 10.1093/humupd/dmab039
Cervello, I., Gil-Sanchis, C., Santamaria, X., Faus, A., Vallve-Juanico, J., Diaz-Gimeno, P., Genolet, O., Pellicer, A., & Simon, C. (2017). Leucine-rich repeat-containing G-protein-coupled receptor 5-positive cells in the endometrial stem cell niche. Fertility and Sterility, 107(2), 510–519e3.
pubmed: 27887719 doi: 10.1016/j.fertnstert.2016.10.021
Liu, Y., Liang, S., Yang, F., Sun, Y., Niu, L., Ren, Y., Wang, H., He, Y., Du, J., Yang, J., & Lin, J. (2020). Biological characteristics of endometriotic mesenchymal stem cells isolated from ectopic lesions of patients with endometriosis. Stem Cell Research & Therapy, 11(1), 346.
doi: 10.1186/s13287-020-01856-8
Ren, G., Zhao, X., Zhang, L., Zhang, J., L’Huillier, A., Ling, W., Roberts, A. I., Le, A. D., Shi, S., Shao, C., & Shi, Y. (2010). Inflammatory cytokine-induced intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 in mesenchymal stem cells are critical for immunosuppression. The Journal of Immunology, 184(5), 2321–2328.
pubmed: 20130212 doi: 10.4049/jimmunol.0902023
Du, W., Li, X., Chi, Y., Ma, F., Li, Z., Yang, S., Song, B., Cui, J., Ma, T., Li, J., Tian, J., Yang, Z., Feng, X., Chen, F., Lu, S., Liang, L., Han, Z. B., & Han, Z. C. (2016). VCAM-1 + placenta chorionic villi-derived mesenchymal stem cells display potent pro-angiogenic activity. Stem Cell Research & Therapy, 7, 49.
doi: 10.1186/s13287-016-0297-0
Lenero, C., Kaplan, L. D., Best, T. M., & Kouroupis, D. (2022). CD146 + Endometrial-Derived Mesenchymal Stem/Stromal Cell Subpopulation Possesses Exosomal Secretomes with Strong Immunomodulatory miRNA Attributes. Cells 11, (24).
Data, K., Marcinkowska, K., Bus, K., Valihrach, L., Pawlak, E., & Smieszek, A. (2023). beta-lactoglobulin affects the oxidative status and viability of equine endometrial progenitor cells via lncRNA-mRNA-miRNA regulatory associations. Journal of Cellular and Molecular Medicine, 27(7), 927–938.
pubmed: 36860157 pmcid: 10064025 doi: 10.1111/jcmm.17694
Salamonsen, L. A., Hutchison, J. C., & Gargett, C. E. (2021). Cyclical endometrial repair and regeneration. Development 148, (17).
Gellersen, B., & Brosens, J. J. (2014). Cyclic decidualization of the human endometrium in reproductive health and failure. Endocrine Reviews, 35(6), 851–905.
pubmed: 25141152 doi: 10.1210/er.2014-1045
Critchley, H. O., Brenner, R. M., Henderson, T. A., Williams, K., Nayak, N. R., Slayden, O. D., Millar, M. R., & Saunders, P. T. (2001). Estrogen receptor beta, but not estrogen receptor alpha, is present in the vascular endothelium of the human and nonhuman primate endometrium. Journal of Clinical Endocrinology and Metabolism, 86(3), 1370–1378.
pubmed: 11238534
Ashary, N., Tiwari, A., & Modi, D. (2018). Embryo implantation: War in Times of Love. Endocrinology, 159(2), 1188–1198.
pubmed: 29319820 doi: 10.1210/en.2017-03082
Miner, J. H., & Yurchenco, P. D. (2004). Laminin functions in tissue morphogenesis. Annual Review of Cell and Developmental Biology, 20, 255–284.
pubmed: 15473841 doi: 10.1146/annurev.cellbio.20.010403.094555
Mishra, A., Ganguli, N., Majumdar, S. S., & Modi, D. (2022). Loss of HOXA10 causes endometrial hyperplasia progressing to endometrial cancer. Journal of Molecular Endocrinology, 69(3), 431–444.
pubmed: 35917434 doi: 10.1530/JME-22-0051
Owusu-Akyaw, A., Krishnamoorthy, K., Goldsmith, L. T., & Morelli, S. S. (2019). The role of mesenchymal-epithelial transition in endometrial function. Human Reproduction Update, 25(1), 114–133.
pubmed: 30407544 doi: 10.1093/humupd/dmy035
Gamage, T. K., Perry, J. J., Fan, V., Groom, K., Chamley, L. W., & James, J. L. (2020). Side-Population trophoblasts exhibit the differentiation potential of a trophoblast Stem Cell Population, persist to term, and are reduced in fetal growth restriction. Stem Cell Rev Rep, 16(4), 764–775.
pubmed: 32548656 doi: 10.1007/s12015-020-09991-8
Dreisler, E., & Kjer, J. J. (2019). Asherman’s syndrome: Current perspectives on diagnosis and management. Int J Womens Health, 11, 191–198.
pubmed: 30936754 pmcid: 6430995 doi: 10.2147/IJWH.S165474
Shaffer, W. (1986). Role of uterine adhesions in the cause of multiple pregnancy losses. Clinical Obstetrics and Gynecology, 29(4), 912–924.
pubmed: 3545591 doi: 10.1097/00003081-198612000-00016
Lee, W. L., Liu, C. H., Cheng, M., Chang, W. H., Liu, W. M., & Wang, P. H. (2021). Focus on the Primary Prevention of Intrauterine Adhesions: Current Concept and Vision. Int J Mol Sci 22, (10).
Han, Q., & Du, Y. (2020). Advances in the application of Biomimetic Endometrium Interfaces for Uterine Bioengineering in Female Infertility. Frontiers in Bioengineering and Biotechnology, 8, 153.
pubmed: 32181248 pmcid: 7059418 doi: 10.3389/fbioe.2020.00153
Wei, C., Pan, Y., Zhang, Y., Dai, Y., Jiang, L., Shi, L., Yang, W., Xu, S., Zhang, Y., Xu, W., Zhang, Y., Lin, X., & Zhang, S. (2020). Overactivated sonic hedgehog signaling aggravates intrauterine adhesion via inhibiting autophagy in endometrial stromal cells. Cell Death and Disease, 11(9), 755.
pubmed: 32934215 pmcid: 7492405 doi: 10.1038/s41419-020-02956-2
Benor, A., Gay, S., & DeCherney, A. (2020). An update on stem cell therapy for Asherman syndrome. Journal of Assisted Reproduction and Genetics, 37(7), 1511–1529.
pubmed: 32445154 pmcid: 7376809 doi: 10.1007/s10815-020-01801-x
Gao, Y., Wu, G., Xu, Y., Zhao, D., & Zheng, L. (2021). Stem cell-based therapy for Asherman Syndrome: Promises and challenges. Cell Transplantation, 30, 9636897211020734.
pubmed: 34105392 doi: 10.1177/09636897211020734
Gargett, C. E., Nguyen, H. P., & Ye, L. (2012). Endometrial regeneration and endometrial stem/progenitor cells. Rev Endocr Metab Disord, 13(4), 235–251.
pubmed: 22847235 doi: 10.1007/s11154-012-9221-9
Capela, A., & Temple, S. (2006). LeX is expressed by principle progenitor cells in the embryonic nervous system, is secreted into their environment and binds Wnt-1. Development Biology, 291(2), 300–313.
doi: 10.1016/j.ydbio.2005.12.030
Shafrir, A. L., Farland, L. V., Shah, D. K., Harris, H. R., Kvaskoff, M., Zondervan, K., & Missmer, S. A. (2018). Risk for and consequences of endometriosis: A critical epidemiologic review. Best Pract Res Clin Obstet Gynaecol, 51, 1–15.
pubmed: 30017581 doi: 10.1016/j.bpobgyn.2018.06.001
Giudice, L. C., & Kao, L. C. (2004). Endometriosis Lancet 364, (9447), 1789–1799.
pubmed: 15541453 doi: 10.1016/S0140-6736(04)17403-5
Sampson, J. A. (1927). Metastatic or embolic endometriosis, due to the Menstrual dissemination of endometrial tissue into the venous circulation. American Journal of Pathology, 3(2), 93–11043.
pubmed: 19969738 pmcid: 1931779
Habiba, M., Benagiano, G., & Guo, S. W. (2023). An Appraisal of the Tissue Injury and Repair (TIAR) Theory on the Pathogenesis of Endometriosis and Adenomyosis. Biomolecules 13, (6).
Maruyama, T., & Revised, A. (2022). Stem cell theory for the pathogenesis of endometriosis. Journal of Personalized Medicine 12, (2).
Zhang, Q., Liang, J., Xu, D., Gao, T., Zhang, J., Liang, H., Wang, W., Ling, B., & Feng, D. (2023). The Biological characteristics of Eutopic and ectopic endometrial progenitor cells in endometriosis. Curr Stem Cell Res Ther, 18(8), 1172–1183.
pubmed: 36740801 doi: 10.2174/1574888X18666230203162452
Nisenblat, V., Bossuyt, P. M., Farquhar, C., Johnson, N., & Hull, M. L. (2016). Imaging modalities for the non-invasive diagnosis of endometriosis. Cochrane Database Systematic Review 2, (2), CD009591.
Klemmt, P. A., Carver, J. G., Koninckx, P., McVeigh, E. J., & Mardon, H. J. (2007). Endometrial cells from women with endometriosis have increased adhesion and proliferative capacity in response to extracellular matrix components: Towards a mechanistic model for endometriosis progression. Human Reproduction, 22(12), 3139–3147.
pubmed: 17921481 doi: 10.1093/humrep/dem262
Imperiale, L., Nisolle, M., Noel, J. C., & Fastrez, M. (2023). Three types of endometriosis: Pathogenesis, diagnosis and treatment. State of the art. J Clin Med 12, (3).
Jimbo, H., Hitomi, Y., Yoshikawa, H., Yano, T., Momoeda, M., Sakamoto, A., Tsutsumi, O., Taketani, Y., & Esumi, H. (1997). Evidence for monoclonal expansion of epithelial cells in ovarian endometrial cysts. American Journal of Pathology, 150(4), 1173–1178.
pubmed: 9094973 pmcid: 1858174
Tamura, M., Fukaya, T., Murakami, T., Uehara, S., & Yajima, A. (1998). Cytogenetic analysis of cells from endometriotic cysts of the human ovary. Cancer Genetics and Cytogenetics, 102(2), 155–157.
pubmed: 9546073
Silveira, C. G., Krampe, J., Ruhland, B., Diedrich, K., Hornung, D., & Agic, A. (2012). Cold-shock domain family member YB-1 expression in endometrium and endometriosis. Human Reproduction, 27(1), 173–182.
pubmed: 22095791 doi: 10.1093/humrep/der368
Forte, A., Schettino, M. T., Finicelli, M., Cipollaro, M., Colacurci, N., Cobellis, L., & Galderisi, U. (2009). Expression pattern of stemness-related genes in human endometrial and endometriotic tissues. Molecular Medicine, 15(11–12), 392–401.
pubmed: 19690622 pmcid: 2727462 doi: 10.2119/molmed.2009.00068
Song, W. W., Lu, H., Hou, W. J., Xu, G. X., Zhang, J. H., Sheng, Y. H., Cheng, M. J., & Zhang, R. (2014). Expression of vascular endothelial growth factor C and anti-angiogenesis therapy in endometriosis. Int J Clin Exp Pathol, 7(11), 7752–7759.
pubmed: 25550812 pmcid: 4270624
Song, Y., Xiao, L., Fu, J., Huang, W., Wang, Q., Zhang, X., & Yang, S. (2014). Increased expression of the pluripotency markers sex-determining region Y-box 2 and nanog homeobox in ovarian endometriosis. Reproductive Biology and Endocrinology: Rb&E, 12, 42.
doi: 10.1186/1477-7827-12-42
Kao, A. P., Wang, K. H., Chang, C. C., Lee, J. N., Long, C. Y., Chen, H. S., Tsai, C. F., Hsieh, T. H., & Tsai, E. M. (2011). Comparative study of human eutopic and ectopic endometrial mesenchymal stem cells and the development of an in vivo endometriotic invasion model. Fertility and Sterility, 95(4), 1308–15e1.
pubmed: 21047634 doi: 10.1016/j.fertnstert.2010.09.064
Alencar, A. K. N., Swan, K. F., Pridjian, G., Lindsey, S. H., & Bayer, C. L. (2023). Connecting G protein-coupled estrogen receptor biomolecular mechanisms with the pathophysiology of preeclampsia: A review. Reproductive Biology and Endocrinology: Rb&E, 21(1), 60.
doi: 10.1186/s12958-023-01112-7
Aukes, A. M., Arion, K., Bone, J. N., Li, J., Vidler, M., Bellad, M. B., Charantimath, U., Goudar, S. S., Hoodbhoy, Z., Katageri, G., Macuacua, S., Mallapur, A. A., Munguambe, K., Qureshi, R. N., Sacoor, C., Sevene, E., Sheikh, S., Vala, A., Lewis, G., Bhutta, Z. A., von Dadelszen, P., Magee, L. A., & Group, C. T. S. (2021). Causes and circumstances of maternal death: A secondary analysis of the community-level interventions for pre-eclampsia (CLIP) trials cohort. Lancet Glob Health, 9(9), e1242–e1251.
pubmed: 34332699 pmcid: 8370879 doi: 10.1016/S2214-109X(21)00263-1
Bokslag, A., Teunissen, P. W., Franssen, C., van Kesteren, F., Kamp, O., Ganzevoort, W., Paulus, W. J., & de Groot, C. J. M. (2017). Effect of early-onset preeclampsia on cardiovascular risk in the fifth decade of life. American Journal of Obstetrics and Gynecology, 216(5), 523–523. e1-e7.
doi: 10.1016/j.ajog.2017.02.015
Haug, E. B., Horn, J., Markovitz, A. R., Fraser, A., Vatten, L. J., Macdonald-Wallis, C., Tilling, K., Romundstad, P. R., Rich-Edwards, J. W., & Asvold, B. O. (2018). Life Course trajectories of Cardiovascular Risk factors in women with and without Hypertensive disorders in first pregnancy: The HUNT study in Norway. J Am Heart Assoc 7, (15), e009250.
Rana, S., Lemoine, E., Granger, J. P., & Karumanchi, S. A. (2019). Preeclampsia: Pathophysiology, Challenges, and Perspectives. Circ Res 124, (7), 1094–1112.
Burton, G. J., Redman, C. W., Roberts, J. M., & Moffett, A. (2019). Pre-eclampsia: Pathophysiology and clinical implications. Bmj, 366, l2381.
pubmed: 31307997 doi: 10.1136/bmj.l2381
Allerkamp, H. H., Clark, A. R., Lee, T. C., Morgan, T. K., Burton, G. J., & James, J. L. (2021). Something old, something new: Digital quantification of uterine vascular remodelling and trophoblast plugging in historical collections provides new insight into adaptation of the utero-placental circulation. Human Reproduction, 36(3), 571–586.
pubmed: 33600565 doi: 10.1093/humrep/deaa303
Burton, G. J., Woods, A. W., Jauniaux, E., & Kingdom, J. C. (2009). Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy. Placenta, 30(6), 473–482.
pubmed: 19375795 pmcid: 2697319 doi: 10.1016/j.placenta.2009.02.009
Jensen, O. E., & Chernyavsky, I. L. (2019). Blood flow and transport in the human placenta. Annual Review of Fluid Mechanics, 51, 25–47.
pubmed: 38410641 doi: 10.1146/annurev-fluid-010518-040219
Zhao, G., Zhou, X., Chen, S., Miao, H., Fan, H., Wang, Z., Hu, Y., & Hou, Y. (2014). Differential expression of microRNAs in decidua-derived mesenchymal stem cells from patients with pre-eclampsia. Journal of Biomedical Science, 21(1), 81.
pubmed: 25135655 pmcid: 4237795 doi: 10.1186/s12929-014-0081-3
Bills, V. L., Hamdollah-Zadeh, M., Soothill, P. W., Harper, S. J., & Bates, D. O. (2014). The role of VEGF-A165b in trophoblast survival. Bmc Pregnancy and Childbirth, 14, 278.
pubmed: 25128406 pmcid: 4143552 doi: 10.1186/1471-2393-14-278
Zhafir Asyura, M. M. A., Komariah, M., Amirah, S., Faisal, E. G., Maulana, S., Platini, H., & Pahria, T. (2023). Analysis of varying MicroRNAs as a Novel Biomarker for early diagnosis of Preeclampsia: A scoping systematic review of the Observational Study. Int J Prev Med, 14, 36.
pubmed: 37351051 pmcid: 10284242 doi: 10.4103/ijpvm.ijpvm_156_22
Romberg, S. I., Kreis, N. N., Friemel, A., Roth, S., Souto, A. S., Hoock, S. C., Fischer, K., Nowak, T., Solbach, C., Louwen, F., Ritter, A., & Yuan, J. (2022). Human placental mesenchymal stromal cells are ciliated and their ciliation is compromised in preeclampsia. Bmc Medicine, 20(1), 35.
pubmed: 35081949 pmcid: 8793243 doi: 10.1186/s12916-021-02203-1
Plaks, V., Kong, N., & Werb, Z. (2015). The cancer stem cell niche: How essential is the niche in regulating stemness of tumor cells? Cell Stem Cell, 16(3), 225–238.
pubmed: 25748930 pmcid: 4355577 doi: 10.1016/j.stem.2015.02.015
Kilmister, E. J., & Tan, S. T. (2021). The role of the renin-angiotensin system in the Cancer Stem Cell Niche. Journal of Histochemistry and Cytochemistry, 69(12), 835–847.
pubmed: 34165363 pmcid: 8647629 doi: 10.1369/00221554211026295
Brasseur, K., Gevry, N., & Asselin, E. (2017). Chemoresistance and targeted therapies in ovarian and endometrial cancers. Oncotarget, 8(3), 4008–4042.
pubmed: 28008141 doi: 10.18632/oncotarget.14021
Peluso, J. J., & Pru, J. K. (2021). Progesterone Receptor Membrane Component (PGRMC)1 and PGRMC2 and Their Roles in Ovarian and Endometrial Cancer. Cancers (Basel) 13, (23).
Lapidot, T., Sirard, C., Vormoor, J., Murdoch, B., Hoang, T., Caceres-Cortes, J., Minden, M., Paterson, B., Caligiuri, M. A., & Dick, J. E. (1994). A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature, 367(6464), 645–648.
pubmed: 7509044 doi: 10.1038/367645a0
Zhao, W., Li, Y., & Zhang, X. (2017). Stemness-related markers in Cancer. Cancer Transl Med, 3(3), 87–95.
pubmed: 29276782 pmcid: 5737740 doi: 10.4103/ctm.ctm_69_16
Banz-Jansen, C., Helweg, L. P., & Kaltschmidt, B. (2022). Endometrial Cancer Stem Cells: Where Do We Stand and Where Should We Go? Int J Mol Sci 23, (6).
Giannone, G., Attademo, L., Scotto, G., Genta, S., Ghisoni, E., Tuninetti, V., Aglietta, M., Pignata, S., & Valabrega, G. (2019). Endometrial Cancer stem cells: Role, characterization and therapeutic implications. Cancers (Basel), 11, 11.
doi: 10.3390/cancers11111820
Lu, H., Ju, D. D., Yang, G. D., Zhu, L. Y., Yang, X. M., Li, J., Song, W. W., Wang, J. H., Zhang, C. C., Zhang, Z. G., & Zhang, R. (2019). Targeting cancer stem cell signature gene SMOC-2 overcomes chemoresistance and inhibits cell proliferation of endometrial carcinoma. EBioMedicine, 40, 276–289.
pubmed: 30594556 doi: 10.1016/j.ebiom.2018.12.044
Polyak, K., & Hahn, W. C. (2006). Roots and stems: Stem cells in cancer. Nature Medicine, 12(3), 296–300.
pubmed: 16520777 doi: 10.1038/nm1379
Batlle, E., & Clevers, H. (2017). Cancer stem cells revisited. Nature Medicine, 23(10), 1124–1134.
pubmed: 28985214 doi: 10.1038/nm.4409
Afify, S. M., & Seno, M. (2019). Conversion of Stem cells to Cancer Stem cells: Undercurrent of Cancer initiation. Cancers (Basel) 11, (3).
Ratajczak, M. Z., Zuba-Surma, E., Wojakowski, W., Suszynska, M., Mierzejewska, K., Liu, R., Ratajczak, J., Shin, D. M., & Kucia, M. (2014). Very small embryonic-like stem cells (VSELs) represent a real challenge in stem cell biology: Recent pros and cons in the midst of a lively debate. Leukemia, 28(3), 473–484.
pubmed: 24018851 doi: 10.1038/leu.2013.255

Auteurs

Baolan Sun (B)

Department of Clinical Laboratory, Affiliated Hospital of Nantong University, Nantong, China. lanbao0218@163.com.
The State Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, Macau, China. lanbao0218@163.com.

Xi Cheng (X)

Department of Obstetrics and Gynecology, Affiliated Hospital of Nantong University, Nantong, China.

Qiang Wu (Q)

Department of Clinical Laboratory, Affiliated Hospital of Nantong University, Nantong, China. qwu@must.edu.mo.

Classifications MeSH