The role and advances of endometrial stem/progenitor cells in the pathogenesis of endometriosis_West China Medical Journal

Authors：

ZHU Daxiu ^1,2 , ZHANG Zhenzhen ^1,2 , ZHU Li ^1,2 , HUANG Meihua ^1,2 ,  WAN Guiping ^1,2

1. Department of Gynecology, Affiliated Hospital of Integrated Traditional Chinese and Western Medicine, Nanjing University of Chinese Medicine, Nanjing , Jiangsu 210008, P. R. China;
2. Department of Gynecology, Jiangsu Province Academy of Traditional Chinese Medicine, Nanjing, Jiangsu 210008, P. R. China;

Corresponding author：

WAN Guiping, Email: wanguiping@263.net

Keywords：

Endometrial stem/progenitor cells; Endometriosis; Markers; Signaling pathway

DOI：

10.7507/1002-0179.201908035

Video：

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Endometriosis (EM) is a common benign gynecological disease with complex pathogenesis and lack of unified understanding. In recent years, the theory of stem/progenitor cells has gradually been recognized by scholars. The presence of stem/progenitor cells in the endometrium and researchers’ understanding of stem/progenitor cell specific markers has been further developed, which is of great significance for sorting stem/progenitor cells and further elucidating their roles in the pathogenesis of EM. At present, more endometrial stem cell signaling pathways have been studied including Wnt, Hedgehog, Notch, phosphatidylinositol-3-kinase/protein kinase B, Smad/connective tissue growth factor, CXCL12/CXCR4, etc. These signaling pathways can regulate stem cell involvement in the pathogenesis of EM. Exploring how signaling pathways to regulate stem cell involvement in the pathogenesis of EM can help elucidate the specific pathogenesis of EM and provide new directions for its treatment. This paper will summarize them.

Citation： ZHU Daxiu, ZHANG Zhenzhen, ZHU Li, HUANG Meihua, WAN Guiping. The role and advances of endometrial stem/progenitor cells in the pathogenesis of endometriosis. West China Medical Journal, 2020, 35(1): 84-88. doi: 10.7507/1002-0179.201908035 Copy

1.	Hufnagel D, Li F, Cosar E, et al. The role of stem cells in the etiology and pathophysiology of endometriosis. Semin Reprod Med, 2015, 33(5): 333-340.
2.	中华医学会妇产科学分会子宫内膜异位症协作组. 子宫内膜异位症的诊治指南. 中华妇产科杂志, 2015, 50(3): 161-169.
3.	Oliveira FR, Dela Cruz C, Del Puerto HL, et al. Stem cells: are they the answer to the puzzling etiology of endometriosis?. Histol Histopathol, 2012, 27(1): 23-29.
4.	Sampson JA. Peritoneal endometriosis due to menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol, 1927, 14(4): 93-94.
5.	Brosens I, Benagiano G. Is neonatal uterine bleeding involved in the pathogenesis of endometriosis as a source of stem cells?. Fertil Steril, 2013, 100(3): 622-623.
6.	Gargett CE, Schwab KE, Brosens JJ, et al. Potential role of endometrial stem/progenitor cells in the pathogenesis of early-onset endometriosis. Mol Hum Reprod, 2014, 20(7): 591-598.
7.	于聪祥, 宋静慧. 干细胞在子宫内膜异位症发病中的意义. 国际妇产科学杂志, 2013, 40(1): 27-30.
8.	Chan RW, Schwab KE, Gargett CE. Clonogenicity of human endometrial epithelial and stromal cells. Biol Reprod, 2004, 70(6): 1738-1750.
9.	Kao AP, Wang KH, Chang CC, et al. Comparative study of human eutopic and ectopic endometrial mesenchymal stem cells and the development of an in vivo endometriotic invasion model. Fertil Steril, 2011, 95(4): 1308-1315.
10.	Dhesi AS, Morelli SS. Endometriosis: a role for stem cells. Womens Health (Lond), 2015, 11(1): 35-49.
11.	Cousins FL, O DF, Gargett CE. Endometrial stem/progenitor cells and their role in the pathogenesis of endometriosis. Best Pract Res Clin Obstet Gynaecol, 2018, 50: 27-38.
12.	Gargett CE, Masuda H. Adult stem cells in the endometrium. Mol Hum Reprod, 2010, 16(11): 818-834.
13.	Schwab KE, Gargett CE. Co-expression of two perivascular cell markers isolates mesenchymal stem-like cells from human endometrium. Hum Reprod, 2007, 22(11): 2903-2911.
14.	Masuda H, Anwar SS, Bühring HJ. A novel marker of human endometrial mesenchymal stem-like cells. Cell Transplant, 2012, 21(10): 2201-2214.
15.	Ulrich D, Tan KS, Deane J, et al. Mesenchymal stem/stromal cells in post-menopausal endometrium. Hum Reprod, 2014, 29(9): 1895-1905.
16.	Nguyen HPT, Xiao L, Deane JA, et al. N-cadherin identifies human endometrial epithelial progenitor cells by in vitro stem cell assays. Hum Reprod, 2017, 32(11): 2254-2268.
17.	李林翰, 钱欢欢, 朱姝, 等. 内皮祖细胞在子宫内膜异位症血管形成中的研究进展. 国际妇产科学杂志, 2017, 44(4): 455-458.
18.	Kato K. Stem cells in human normal endometrium and endometrial cancer cells: characterization of side population cell. Kaohsiung J Med Sci, 2012, 28(2): 63-71.
19.	Miyazaki K, Maruyama T, Masuda H, et al. Stem cell-like differentiation potentials of endometrial side population cells as revealed by a newly developed in vivo endometrial stem cell assay. PLoS One, 2012, 7(12): e50749.
20.	Gurung S, Deane JA, Masuda H, et al. Stem cells in endometrial physiology. Semin Reprod Med, 2015, 33(5): 326-332.
21.	Mohammed MK, Shao C, Wang J, et al. Wnt/β-catenin signaling plays an ever-expanding role in stem cell self-renewal, tumorigenesis and cancer chemoresistance. Genes Dis, 2016, 3(1): 11-40.
22.	Zhang Y. Ganoderma lucidum (Reishi) suppresses proliferation and migration of breast cancer cells via inhibiting Wnt/β-catenin signaling. Biochem Biophys Res Commun, 2017, 488(4): 679-684.
23.	Yu WZ, Chen XM, Niu WB, et al. Role of Wnt5a in the differentiation of human embryonic stem cells into endometrium -like cells. Int J Clin Exp Pathol, 2015, 8(5): 5478-5484.
24.	Li J, Dai Y, Zhu H, et al. Endometriotic mesenchymal stem cells significantly promote fibrogenesis in ovarian endometrioma through the Wnt/β-catenin pathway by paracrine production of TGF-β1 and Wnt1. Hum Reprod, 2016, 31(6): 1224-1235.
25.	Lee RT, Zhao Z, Ingham PW. Hedgehog signalling. Development, 2016, 143(3): 367-372.
26.	Valenti G, Quinn HM, Heynen GJJE, et al. Cancer stem cells regulate cancer-associated fibroblasts via activation of hedgehog signaling in mammary gland tumors. Cancer Res, 2017, 77(8): 2134-2147.
27.	卢小路, 徐海波, 石梦莹. 半枝莲通过 Hedgehog 信号通路抑制结肠肿瘤干细胞自我更新. 中药药理与临床, 2015, 31(1): 139-141.
28.	Götte M, Wolf M, Staebler A, et al. Increased expression of the adult stem cell marker Musashi-1 in endometriosis and endometrial carcinoma. J Pathol, 2008, 215(3): 317-329.
29.	Götte M, Wolf M, Staebler A, et al. Aberrant expression of the pluripotency marker SOX-2 in endometriosis. Fertil Steril, 2011, 95(1): 338-341.
30.	Heard ME, Simmons CD, Simmen FA, et al. Krüppel-like factor 9 deficiency in uterine endometrial cells promotes ectopic lesion establishment associated with activated notch and hedgehog signaling in a mouse model of endometriosis. Endocrinology, 2014, 155(4): 1532-1546.
31.	Schüring AN, Dahlhues B, Korte A, et al. The endometrial stem cell markers notch-1 and numb are associated with endometriosis. Reprod Biomed Online, 2018, 36(3): 294-301.
32.	He H, Liu R, Xiong W, et al. Lentiviral vector-mediated down-regulation of Notch1 in endometrial stem cells results in proliferation and migration in endometriosis. Mol Cell Endocrinol, 2016, 434: 210-218.
33.	Diao R, Wei W, Zhao J, et al. CCL19/CCR7 contributes to the pathogenesis of endometriosis via PI3K/Akt pathway by regulating the proliferation and invasion of ESCs. Am J Reprod Immunol, 2017, 78(5).
34.	Franco-Murillo Y, Miranda-Rodríguez JA, Rendón-Huerta E, et al. Unremitting cell proliferation in the secretory phase of eutopic endometriosis: involvement of pAkt and pGSK3β. Reprod Sci, 2015, 22(4): 502-510.
35.	Zhang Z, Wang J, Chen Y, et al. Activin a promotes myofibroblast differentiation of endometrial mesenchymal stem cells via STAT3-dependent Smad/CTGF pathway. Cell Commun Signal, 2019, 17(1): 45.
36.	Li F, Alderman MH 3rd, Tal A, et al. Hematogenous dissemination of mesenchymal stem cells from endometriosis. Stem Cells, 2018, 36(6): 881-890.

1. Hufnagel D, Li F, Cosar E, et al. The role of stem cells in the etiology and pathophysiology of endometriosis. Semin Reprod Med, 2015, 33(5): 333-340.
2. 中华医学会妇产科学分会子宫内膜异位症协作组. 子宫内膜异位症的诊治指南. 中华妇产科杂志, 2015, 50(3): 161-169.
3. Oliveira FR, Dela Cruz C, Del Puerto HL, et al. Stem cells: are they the answer to the puzzling etiology of endometriosis?. Histol Histopathol, 2012, 27(1): 23-29.
4. Sampson JA. Peritoneal endometriosis due to menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol, 1927, 14(4): 93-94.
5. Brosens I, Benagiano G. Is neonatal uterine bleeding involved in the pathogenesis of endometriosis as a source of stem cells?. Fertil Steril, 2013, 100(3): 622-623.
6. Gargett CE, Schwab KE, Brosens JJ, et al. Potential role of endometrial stem/progenitor cells in the pathogenesis of early-onset endometriosis. Mol Hum Reprod, 2014, 20(7): 591-598.
7. 于聪祥, 宋静慧. 干细胞在子宫内膜异位症发病中的意义. 国际妇产科学杂志, 2013, 40(1): 27-30.
8. Chan RW, Schwab KE, Gargett CE. Clonogenicity of human endometrial epithelial and stromal cells. Biol Reprod, 2004, 70(6): 1738-1750.
9. Kao AP, Wang KH, Chang CC, et al. Comparative study of human eutopic and ectopic endometrial mesenchymal stem cells and the development of an in vivo endometriotic invasion model. Fertil Steril, 2011, 95(4): 1308-1315.
10. Dhesi AS, Morelli SS. Endometriosis: a role for stem cells. Womens Health (Lond), 2015, 11(1): 35-49.
11. Cousins FL, O DF, Gargett CE. Endometrial stem/progenitor cells and their role in the pathogenesis of endometriosis. Best Pract Res Clin Obstet Gynaecol, 2018, 50: 27-38.
12. Gargett CE, Masuda H. Adult stem cells in the endometrium. Mol Hum Reprod, 2010, 16(11): 818-834.
13. Schwab KE, Gargett CE. Co-expression of two perivascular cell markers isolates mesenchymal stem-like cells from human endometrium. Hum Reprod, 2007, 22(11): 2903-2911.
14. Masuda H, Anwar SS, Bühring HJ. A novel marker of human endometrial mesenchymal stem-like cells. Cell Transplant, 2012, 21(10): 2201-2214.
15. Ulrich D, Tan KS, Deane J, et al. Mesenchymal stem/stromal cells in post-menopausal endometrium. Hum Reprod, 2014, 29(9): 1895-1905.
16. Nguyen HPT, Xiao L, Deane JA, et al. N-cadherin identifies human endometrial epithelial progenitor cells by in vitro stem cell assays. Hum Reprod, 2017, 32(11): 2254-2268.
17. 李林翰, 钱欢欢, 朱姝, 等. 内皮祖细胞在子宫内膜异位症血管形成中的研究进展. 国际妇产科学杂志, 2017, 44(4): 455-458.
18. Kato K. Stem cells in human normal endometrium and endometrial cancer cells: characterization of side population cell. Kaohsiung J Med Sci, 2012, 28(2): 63-71.
19. Miyazaki K, Maruyama T, Masuda H, et al. Stem cell-like differentiation potentials of endometrial side population cells as revealed by a newly developed in vivo endometrial stem cell assay. PLoS One, 2012, 7(12): e50749.
20. Gurung S, Deane JA, Masuda H, et al. Stem cells in endometrial physiology. Semin Reprod Med, 2015, 33(5): 326-332.
21. Mohammed MK, Shao C, Wang J, et al. Wnt/β-catenin signaling plays an ever-expanding role in stem cell self-renewal, tumorigenesis and cancer chemoresistance. Genes Dis, 2016, 3(1): 11-40.
22. Zhang Y. Ganoderma lucidum (Reishi) suppresses proliferation and migration of breast cancer cells via inhibiting Wnt/β-catenin signaling. Biochem Biophys Res Commun, 2017, 488(4): 679-684.
23. Yu WZ, Chen XM, Niu WB, et al. Role of Wnt5a in the differentiation of human embryonic stem cells into endometrium -like cells. Int J Clin Exp Pathol, 2015, 8(5): 5478-5484.
24. Li J, Dai Y, Zhu H, et al. Endometriotic mesenchymal stem cells significantly promote fibrogenesis in ovarian endometrioma through the Wnt/β-catenin pathway by paracrine production of TGF-β1 and Wnt1. Hum Reprod, 2016, 31(6): 1224-1235.
25. Lee RT, Zhao Z, Ingham PW. Hedgehog signalling. Development, 2016, 143(3): 367-372.
26. Valenti G, Quinn HM, Heynen GJJE, et al. Cancer stem cells regulate cancer-associated fibroblasts via activation of hedgehog signaling in mammary gland tumors. Cancer Res, 2017, 77(8): 2134-2147.
27. 卢小路, 徐海波, 石梦莹. 半枝莲通过 Hedgehog 信号通路抑制结肠肿瘤干细胞自我更新. 中药药理与临床, 2015, 31(1): 139-141.
28. Götte M, Wolf M, Staebler A, et al. Increased expression of the adult stem cell marker Musashi-1 in endometriosis and endometrial carcinoma. J Pathol, 2008, 215(3): 317-329.
29. Götte M, Wolf M, Staebler A, et al. Aberrant expression of the pluripotency marker SOX-2 in endometriosis. Fertil Steril, 2011, 95(1): 338-341.
30. Heard ME, Simmons CD, Simmen FA, et al. Krüppel-like factor 9 deficiency in uterine endometrial cells promotes ectopic lesion establishment associated with activated notch and hedgehog signaling in a mouse model of endometriosis. Endocrinology, 2014, 155(4): 1532-1546.
31. Schüring AN, Dahlhues B, Korte A, et al. The endometrial stem cell markers notch-1 and numb are associated with endometriosis. Reprod Biomed Online, 2018, 36(3): 294-301.
32. He H, Liu R, Xiong W, et al. Lentiviral vector-mediated down-regulation of Notch1 in endometrial stem cells results in proliferation and migration in endometriosis. Mol Cell Endocrinol, 2016, 434: 210-218.
33. Diao R, Wei W, Zhao J, et al. CCL19/CCR7 contributes to the pathogenesis of endometriosis via PI3K/Akt pathway by regulating the proliferation and invasion of ESCs. Am J Reprod Immunol, 2017, 78(5).
34. Franco-Murillo Y, Miranda-Rodríguez JA, Rendón-Huerta E, et al. Unremitting cell proliferation in the secretory phase of eutopic endometriosis: involvement of pAkt and pGSK3β. Reprod Sci, 2015, 22(4): 502-510.
35. Zhang Z, Wang J, Chen Y, et al. Activin a promotes myofibroblast differentiation of endometrial mesenchymal stem cells via STAT3-dependent Smad/CTGF pathway. Cell Commun Signal, 2019, 17(1): 45.
36. Li F, Alderman MH 3rd, Tal A, et al. Hematogenous dissemination of mesenchymal stem cells from endometriosis. Stem Cells, 2018, 36(6): 881-890.

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