Skip to main content

Advertisement

SpringerLink
Log in

Endometrial Stem/Progenitor Cells

  • Endometrial Cancer (G. Sel, Section Editor)
  • Published:
Current Obstetrics and Gynecology Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

To summarize endometrial stem/progenitor cell biology and endometrial cancer stem cells.

Recent Findings

The subject is relatively new that only about 15 years ago, colony-forming units, as putative endometrial stem/progenitor cells, have been demonstrated in an endometrial sample. Earlier and some recent studies have justifiably focused on endometriosis as the serious gynecologic problem of women. However, on the side of endometrial stem cells research, many current studies are still working on in vitro methods, and the majority of the rest are on animal models. Reported cells as endometrial stem/progenitor cell populations have been heterogeneous such as endometrial mesenchymal stem cells, endometrial epithelial progenitor cells, and side population cells. After the recognition of putative endometrial stem cells, quite a few stem cell markers have been identified. Thereafter, cancer stem cell speculations have raised; in endometrial cancer, CD133+ and CXCR4+ cells, with potential cancer stem cell characteristics, have been shown to have higher antineoplastic resistance than that of other cell populations.

Summary

Endometrial mesenchymal stem cells have plasticity characteristics and may differentiate into mature cells other than endometrium. On the other hand, bone marrow-derived stem cells can differentiate into endometrial cells. Since the endometrial stem/progenitor cells are easy to access, they can be an attractive source for regenerative medicine studies. Even though many markers have been identified for endometrial stem cells, more specific and sensitive marker combinations are yet to be defined for endometrial cancer stem cell in order to aim for more effective treatment approaches.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Jabbour HN, Kelly RW, Fraser HM, Critchley HO. Endocrine regulation of menstruation. Endocr Rev. 2006;27:17–46.

    CAS  PubMed  Google Scholar 

  2. Weissman IL, Shizuru JA. The origins of the identification and isolation of hematopoietic stem cells, and their capability to induce donor-specific transplantation tolerance and treat autoimmune diseases. Blood. 2008;112(9):3543–53.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Prianishnikov VA. A functional model of the structure of the epithelium of normal, hyperplastic and malignant human endometrium: a review. Gynecol Oncol. 1978;6:420–8.

    CAS  PubMed  Google Scholar 

  4. Chan RW, Schwab KE, Gargett CE. Clonogenicity of human endometrial epithelial and stromal cells. Biol Reprod. 2004;70:1738–5.

    CAS  PubMed  Google Scholar 

  5. Gargett CE. Uterine stem cells: what is the evidence? Hum Reprod Update. 2007;13:87–101.

    CAS  PubMed  Google Scholar 

  6. Schwab KE, Chan RW, Gargett CE. Putative stem cell activity of human endometrial epithelial and stromal cells during the menstrual cycle. Fertil Steril. 2005;84:1124–30.

    CAS  PubMed  Google Scholar 

  7. Gargett CE, Schwab KE, Zillwood RM, Nguyen HP, Wu D. Isolation and culture of epithelial progenitors and mesenchymal stem cells from human endometrium. Biol Reprod. 2009;80:1136–45.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Valentijn AJ, Palial K, Al-Lamee H, Tempest N, Drury J, VonZglinicki T, et al. SSEA-1 isolates human endometrial basal glandular epithelial cells: phenotypic and functional characterization and implications in the pathogenesis of endometriosis. Hum Reprod. 2013;28:2695–708.

    CAS  PubMed  Google Scholar 

  9. Gil-Sanchis C, Cervelló I, Mas A, Faus A, Pellicer A, Simón C. Leucine-rich repeat-containing G-protein coupled receptor 5 (Lgr5) as a putative human endometrial stem cell marker. Mol Hum Reprod. 2013;19:407–14.

    CAS  PubMed  Google Scholar 

  10. Gargett CE, Schwab KE, Deane JA. Endometrial stem/progenitor cells: the first 10 years. Hum Reprod Update. 2016;22:137–63.

    CAS  PubMed  Google Scholar 

  11. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8:315–7.

    CAS  PubMed  Google Scholar 

  12. Lin CS, Ning H, Lin G, Lue TF. Is CD34 truly a negative marker for mesenchymal stromal cells? Cytotherapy. 2012;14(10):1159–63.

    CAS  PubMed  Google Scholar 

  13. Ulrich D, Tan KS, Deane J, Schwab K, Cheong A, Rosamilia A, et al. Mesenchymal stem/stromal cells in post-menopausal endometrium. Hum Reprod. 2014;29:1895–905.

    CAS  PubMed  Google Scholar 

  14. Masuda H, Anwar SS, Bühring HJ, Rao JR. Gargett CE.A novel marker of human endometrial mesenchymal stem-like cells. Cell Transplant. 2012;21:2201–14.

    PubMed  Google Scholar 

  15. Schwab KE, Gargett CE. Co-expression of two perivascular cell markers isolates mesenchymal stemlike cells from human endometrium. Hum Reprod. 2007;22:2903–11.

    CAS  PubMed  Google Scholar 

  16. Li L, Xie T. Stem cell niche: structure and function. Annu Rev Cell Dev Biol. 2005;21:605–31.

    CAS  PubMed  Google Scholar 

  17. Du H, Naqvi H, Taylor HS. Ischemia/reperfusion injury promotes and granulocyte colony stimulating factor inhibits migration of bone marrow-derived stem cells to endometrium. Stem Cells Dev. 2012;21:3324–31.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Taylor HS. Endometrial cells derived from donor stem cells in bone marrow transplant recipients. JAMA. 2004;292:81–5.

    CAS  PubMed  Google Scholar 

  19. Tempest N, Maclean A, Hapangama DK. Endometrial Stem Cell Markers: Current Concepts and Unresolved Questions. Int J Mol Sci. 2018:19(10).

  20. Li D, Li H, Wang Y, Eldomany A, Wu J, Yuan C, et al. Development and characterization of a polarized human endometrial cell epithelia in an air-liquid interface state. Stem Cell Res Ther. 2018;9(1):209.

    PubMed  PubMed Central  Google Scholar 

  21. Chan RW, Gargett CE. Identification of label retaining cells in mouse endometrium. Stem Cells. 2006;24:1529–38.

    CAS  PubMed  Google Scholar 

  22. Schofield R. The relationship between the spleen colony-forming cell and the haematopopietic stem cell. A hypothesis Blood Cells. 1978;4:7–25.

    CAS  PubMed  Google Scholar 

  23. Chan RW, Kaitu’u-Lino T, Gargett CE. Role of label-retaining cells in estrogen-induced endometrial regeneration. Reprod Sci. 2012;19:102–14.

    CAS  PubMed  Google Scholar 

  24. Cervelló I, Mas A, Gil-Sanchis C, Peris L, Faus A, Saunders PT, et al. Reconstruction of endometrium from human endometrial side population cell lines. PLoS One. 2011;6:e21221.

    PubMed  PubMed Central  Google Scholar 

  25. Schuring AN, Schulte N, Kelsch R, Ropke A, Kiesel L, Gotte M. Characterization of endometrial mesenchymal stem-like cells obtained by endometrial biopsy during routine diagnostics. Fertil Steril. 2011;95:423–6.

    PubMed  Google Scholar 

  26. Garry R, Hart R, Karthigasu KA, Burke C. A re-appraisal of the morphological changes within the endometrium during menstruation: a hysteroscopic, histological and scanning electron microscopic study. Hum Reprod. 2009;24(6):1393–401.

    CAS  PubMed  Google Scholar 

  27. Garry R, Hart R, Karthigasu KA, Burke C. Structural changes in endometrial basal glands during menstruation. BJOG. 2010;117(10):1175–85.

    CAS  PubMed  Google Scholar 

  28. GaideChevronnay HP, Galant C, Lemoine P, Courtoy PJ, Marbaix E, Henriet P. Spatiotemporal coupling of focal extracellular matrix degradation and reconstruction in the menstrual human endometrium. Endocrinology. 2009;150:5094–105.

    Google Scholar 

  29. Huang CC, Orvis GD, Wang Y, Behringer RR. Stromal-to-epithelial transition during postpartum endometrial regeneration. PLoS One. 2012;7:e44285.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Patterson AL, Zhang L, Arango NA, Teixeira J, Pru JK. Mesenchymal-to-epithelial transition contributes to endometrial regeneration following natural and artificial decidualization. Stem Cells Dev. 2013;22:964–74.

    CAS  PubMed  Google Scholar 

  31. Gargett CE, Masuda H. Adult stem cells in the endometrium. Mol Hum Reprod. 2010;16:818–34.

    CAS  PubMed  Google Scholar 

  32. Evans J, Salamonsen LA, Winship A, Menkhorst E, Nie G, Gargett CE, et al. Fertile ground: human endometrial programming and lessons in health and disease. Nat Rev Endocrinol. 2016;12:654–67.

    CAS  PubMed  Google Scholar 

  33. Challen GA, Little MH. A side order of stem cells: the SP phenotype. Stem Cells. 2006;24:3–12.

    PubMed  Google Scholar 

  34. Cao M, Chan RW, Yeung WS. Label-retaining stromal cells in mouse endometrium awaken for expansion and repair after parturition. Stem Cells Dev. 2015;24:768–80.

    CAS  PubMed  Google Scholar 

  35. Masuda H, Matsuzaki Y, Hiratsu E, Ono M, Nagashima T, Kajitani T, et al. Stem cell-like properties of the endometrial side population: implication in endometrial regeneration. PLoS One. 2010;5:10387.

    Google Scholar 

  36. Cervelló I, Martínez-Conejero JA, Horcajadas JA, Pellicer A, Simón C. Identification, characterization and co-localization of label-retaining cell population in mouse endometrium with typical undifferentiated markers. Hum Reprod. 2007;22:45–51.

    PubMed  Google Scholar 

  37. Zhou S, Schuetz JD, Bunting KD, Colapietro AM, Sampath J, Morris JJ, et al. The ABC transporterBcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med. 2001;7(9):1028–34.

    CAS  PubMed  Google Scholar 

  38. Masuda H, Maruyama T, Gargett CE, Miyazaki K, Matsuzaki Y, Okano H, et al. Endometrial side population cells: potential adult stem/progenitor cells in endometrium. Biol Reprod. 2015;93(4):84.

    PubMed  Google Scholar 

  39. Miyazaki K, Maruyama T, Masuda H, Yamasaki A, Uchida S, Oda 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;7:50749.

    Google Scholar 

  40. Cervelló I, Gil-Sanchis C, Mas A, Delgado-Rosas F, Martínez-Conejero JA, Galán A, et al. Human endometrial side population cells exhibit genotypic, phenotypic and functional features of somatic stem cells. PLoS One. 2010;5:10964.

    Google Scholar 

  41. Tsuji S, Yoshimoto M, Takahashi K, Noda Y, Nakahata T, Heike T. Side population cells contribute to the genesis of human endometrium. Fertil Steril. 2008;90:1528–37.

    PubMed  Google Scholar 

  42. Wolff EF, Wolff AB, Hongling D, Taylor HS. Demonstration of multipotent stem cells in the adult human endometrium by in vitro chondrogenesis. Reprod Sci. 2007;14:524–33.

    CAS  PubMed  Google Scholar 

  43. Ai J, Shahverdi AR, Barough SE, Kouchesfehani HM, Heidari S, Roozafzoon R, et al. Derivation of adipocytes from human endometrial stem cells (EnSCs). J Reprod Infertil. 2012;13:151–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Wang J, Chen S, Zhang C, Stegeman S, Pfaff-Amesse T, Zhang Y, et al. Human endometrial stromal stem cells differentiate into megakaryocytes with the ability to produce functional platelets. PLoS One. 2012;7:44300.

    Google Scholar 

  45. Li HY, Chen YJ, Chen SJ, Kao CL, Tseng LM, Lo WL, et al. Induction of insulin-producing cells derived from endometrial mesenchymal stem-like cells. J Pharmacol Exp Ther. 2010;335:817–29.

    CAS  PubMed  Google Scholar 

  46. Patel AN, Park E, Kuzman M, Benetti F, Silva FJ, Allickson JG. Multipotent menstrual blood stromal stem cells: isolation, characterization, and differentiation. Cell Transplant. 2008;17:303–11.

    PubMed  Google Scholar 

  47. Khanmohammadi M, Khanjani S, Bakhtyari MS, Zarnani AH, Edalatkhah H, Akhondi MM, et al. Proliferation and chondrogenic differentiation potential of menstrual blood and bone marrow-derived stem cells in two-dimensional culture. Int J ematol. 2012;95:484–93.

    Google Scholar 

  48. Meng X, Ichim TE, Zhong J, Rogers A, Yin Z, Jackson J, et al. Endometrial regenerative cells: a novel stem cell population. J Transl Med. 2007;5:57.

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Ulrich D, Muralitharan R, Gargett CE. Toward the use of endometrial and menstrual blood mesenchymal stem cells for cell-based therapies. Expert Opin Biol Ther. 2013;13:1387–400.

    CAS  PubMed  Google Scholar 

  50. Khoury M, Alcayaga-Miranda F, Illanes SE, Figueroa FE. The promising potential of menstrual stem cells for antenatal diagnosis and cell therapy. Front Immunol. 2014;5:205.

    PubMed  PubMed Central  Google Scholar 

  51. Yang XY, Wang W, Li X. In vitro hepatic differentiation of human endometrial stromal stem cells. In Vitro Cell Dev Biol Anim. 2014;50:162–70.

    CAS  PubMed  Google Scholar 

  52. Wolff EF, Gao XB, Yao KV, Andrews ZB, Du H, Elsworth JD, et al. Endometrial stem cell transplantation restores dopamine production in a Parkinson's disease model. J Cell Mol Med. 2011;15:747–55.

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Khanjani S, Khanmohammadi M, Zarnani AH, Akhondi MM, Ahani A, Ghaempanah Z, et al. Comparative evaluation of differentiation potential of menstrual blood- versus bone marrow-derived stem cells into hepatocyte-like cells. PLoS One. 2014;9:86075.

    Google Scholar 

  54. Krause DS, Theise ND, Collector MI, Henegariu O, Hwang S, Gardner R, et al. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell. 2001;105:369–77.

    CAS  PubMed  Google Scholar 

  55. Du H, Taylor HS. Stem cells and female reproduction. Reprod Sci. 2009;16:126–39.

    PubMed  PubMed Central  Google Scholar 

  56. Ikoma T, Kyo S, Maida Y, Ozaki S, Takakura M, Nakao S, et al. Bone marrow-derived cells from male donors can compose endometrial glands in female transplant recipients. Am J Obstet Gynecol. 2009;201:608.400.

    Google Scholar 

  57. Mori Y, Yamawaki K, Ishiguro T, Yoshihara K, Ueda H, Sato A, et al. ALDH-dependent glycolytic activation mediates stemness and paclitaxel resistance in patient-derived spheroid models of uterine endometrial cancer. Stem Cell Reports. 2019;13(4):730–46.

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Hoveizi E, Mohammadi T. Differentiation of endometrial stem cells into insulin-producing cells using signaling molecules and zinc oxide nanoparticles, and three-dimensional culture on nanofibrous scaffolds. J Mater Sci Mater Med. 2019;30(9):101.

    PubMed  Google Scholar 

  59. Santamaria X, Cabanillas S, Cervello I, Arbona C, Raga F, Ferro J, et al. Autologous cell therapy with CD133+ bone marrow-derived stem cells for refractory Asherman’s syndrome and endometrial atrophy: a pilot cohort study. Hum Reprod. 2016;31:1087–96.

    CAS  PubMed  Google Scholar 

  60. Southam CM, Brunschwig A. Quantitative studies of autotransplantation of human cancer. Preliminary report Cancer. 1961;14:971–8.

    Google Scholar 

  61. Lindeman GJ, Visvader JE, Smalley MJ, Eaves CJ. The future of mammary stem cell biology: the power of in vivo transplants. Breast Cancer Res. 2008;10(3):402–3.

    PubMed  PubMed Central  Google Scholar 

  62. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994;367(6464):645–8.

    CAS  PubMed  Google Scholar 

  63. Patrawala L, Calhoun T, Schneider-Broussard R, Li H, Bhatia B, Tang S, et al. Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene. 2006;25(12):1696–708.

    CAS  PubMed  Google Scholar 

  64. Patrawala L, Calhoun-Davis T, Schneider-Broussard R, Tang DG. Hierarchical organization of prostate cancer cells in xenograft tumors: the CD44+ alpha2beta1+ cell population is enriched in tumor-initiating cells. Cancer Res. 2007;15-67(14):6796–805.

    Google Scholar 

  65. Vermeulen L, Todaro M, de Sousa MF, Sprick MR, Kemper K, Perez Alea M, et al. Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proc Natl Acad Sci U S A. 2008;105(36):13427–32.

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Zhang S, Balch C, Chan MW, Lai HC, Matei D, Schilder JM, et al. Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res. 2008\;68(11):4311–20.

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 1997;3(7):730–7.

    CAS  PubMed  Google Scholar 

  68. Rosen JM, Jordan CT. The increasing complexity of the cancer stem cell paradigm. Science. 2009;324(5935):1670–3.

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Hubbard SA, Gargett CE. A cancer stem cell origin for human endometrial carcinoma? Reproduction. 2010;140(1):23–32.

    CAS  PubMed  Google Scholar 

  70. Gorai I, Yanagibashi T, Taki A, Udagawa K, Miyagi E, Nakazawa T, et al. Uterine carcinosarcoma is derived from a single stem cell: an in vitro study. Int J Cancer. 1997;72(5):821–7.

    CAS  PubMed  Google Scholar 

  71. Hubbard SA, Friel AM, Kumar B, Zhang L, Rueda BR, Gargett CE. Evidence for cancer stem cells in human endometrial carcinoma. Cancer Res. 2009;69(21):8241–8.

    CAS  PubMed  Google Scholar 

  72. Friel AM, Sergent PA, Patnaude C, Szotek PP, Oliva E, Scadden DT, et al. Functional analyses of the cancer stem cell-like properties of human endometrial tumor initiating cells. Cell Cycle. 2008;7(2):242–9.

    CAS  PubMed  Google Scholar 

  73. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer. 2008;8(10):755–68.

    CAS  PubMed  Google Scholar 

  74. •• Sun Y, Yoshida T, Okabe M, Zhou K, Wang F, Soko C, et al. Isolation of stem-like cancer cells in primary endometrial cancer using cell surface markers CD133 and CXCR4. Transl Oncol. 2017;10(6):976–87 The CD133+CXCR4+ primary endometrial cancer cells had higher clonogenic ability and also more resistant to anti-cancer drugs than other subpopulations indicating that CD133+CXCR4+ cells may possess some characteristics of CSCs in primary endometrial cancer.

    PubMed  PubMed Central  Google Scholar 

  75. • Shao H, Ma L, Jin F, Zhou Y, Tao M, Teng Y. Immune inhibitory receptor LILRB2 is critical for the endometrial cancer progression. Biochem Biophys Res Commun. 2018;506(1):243–50 Knockdown of LILRB2 results in a dramatic decrease in the proliferation, colony formation and migration in several endometrial cancer cell lines in vitro.

    CAS  PubMed  Google Scholar 

  76. Lobo NA, Shimono Y, Qian D, Clarke MF. The biology of cancer stem cells. Annu Rev Cell Dev Biol. 2007;23:675–99.

    CAS  PubMed  Google Scholar 

  77. Götte M, Wolf M, Staebler A, Buchweitz O, Kelsch R, Schüring AN, et al. Increased expression of the adult stem cell marker Musashi-1 in endometriosis and endometrial carcinoma. J Pathol. 2008;215(3):317–29.

    PubMed  Google Scholar 

  78. Sureban SM, May R, George RJ, Dieckgraefe BK, McLeod HL, Ramalingam S, et al. Knockdown of RNA binding protein musashi-1 leads to tumor regression in vivo. Gastroenterology. 2008;134(5):1448–58.

    CAS  PubMed  Google Scholar 

  79. Ma L, Xu YL, Ding WJ, Shao HF, Teng YC. Prognostic value of musashi-1 in endometrioid adenocarcinoma. Int J Clin Exp Pathol. 2015;8:4564–72.

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Gotte M, Greve B, Kelsch R, Muller-Uthoff H, Weiss K, KharabiMasouleh B, et al. The adult stem cell marker musashi-1 modulates endometrial carcinoma cell cycle progression and apoptosis via Notch-1 and p21WAF1/CIP1. Int J Cancer. 2011;129:2042–9.

    PubMed  Google Scholar 

  81. Saegusa M, Hashimura M, Suzuki E, Yoshida T, Kuwata T. Transcriptional up-regulation of SOX9 by NF-κB in endometrial carcinoma cells, modulating cell proliferation through alteration in the p14(ARF)/p53/p21(WAF1) pathway. Am J Pathol. 2012;181:684–92.

    CAS  PubMed  Google Scholar 

  82. Gonzalez G, Mehra S, Wang Y, Akiyama H, Behringer RR. SOX9 overexpression in uterine epithelia induces endometrial gland hyperplasia. Differentiation. 2016;92:204–15.

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Xie X, Zheng X, Wang J, Chen L. Clinical significance of twist, e-cadherin, and n-cadherin protein expression in endometrioid adenocarcinoma. J Cancer Res Ther. 2017;13:817–22.

    CAS  PubMed  Google Scholar 

  84. Cobellis L, Caprio F, Trabucco E, Mastrogiacomo A, Coppola G, Manente L, et al. The pattern of expression of notch protein members in normal and pathological endometrium. J Anat. 2008;213:464–47.

    PubMed  PubMed Central  Google Scholar 

  85. Wang C, Cui T, Feng W, Li H, Hu L. Role of numb expression and nuclear translocation in endometrial cancer. Oncol Lett. 2015;9:1531–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Rutella S, Bonanno G, Procoli A, Mariotti A, Corallo M, Prisco MG, et al. Cells with characteristics of cancer stem/progenitor cells express the CD133 antigen in human endometrial tumors. Clin Cancer Res. 2009;15(13):4299–311.

    CAS  PubMed  Google Scholar 

  87. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell. 2007;1(5):555–67.

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Horst D, Kriegl L, Engel J, Kirchner T, Jung A. CD133 expression is an independent prognostic marker for low survival in colorectal cancer. Br J Cancer, 2008. 99(8):1285–9.

  89. Zeppernick F, Ahmadi R, Campos B, Dictus C, Helmke BM, Becker N, et al. Stem cell marker CD133 affects clinical outcome in glioma patients. Clin Cancer Res. 2008;14(1):123–9.

    CAS  PubMed  Google Scholar 

  90. Abraham BK, Fritz P, McClellan M, Hauptvogel P, Athelogou M, Brauch H. Prevalence of CD44+/CD24−/low cells in breast cancer may not be associated with clinical outcome but may favor distant metastasis. Clin Cancer Res. 2005;11(3):1154–9.

    CAS  PubMed  Google Scholar 

  91. Kern SE, Shibata D. The fuzzy math of solid tumor stem cells: a perspective. Cancer Res. 2007;67(19):8985–8.

    CAS  PubMed  Google Scholar 

  92. Elbasateeny SS, Salem AA, Abdelsalam WA, Salem RA. Immunohistochemical expression of cancer stem cell related markers CD44 and CD133 in endometrial cancer. Pathol Res Pract. 2016;212(1):10–6.

    CAS  PubMed  Google Scholar 

  93. Park JY, Hong D, Park JY. Association between morphological patterns of myometrial invasion and cancer stem cell markers in endometrial endometrioid carcinoma. Pathol Oncol Res. 2019;25(1):123–30.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Obstetrics and Gynecology, Faculty of Medicine, Division of Gynecologic Oncology, Aydın Adnan Menderes University, Aydın, Turkey

    Hasan YÜKSEL

  2. Department of Obstetrics and Gynecology, Faculty of Medicine, Specialist in Medical Genetics, Aydın Adnan Menderes University, Aydın, Turkey

    Emre ZAFER

Authors
  1. Hasan YÜKSEL
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emre ZAFER
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hasan YÜKSEL.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Human and Animal Rights

This article does not contain any studies with human or animal subjects performed by any of the authors.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is part of the Topical Collection on Endometrial Cancer

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

YÜKSEL, H., ZAFER, E. Endometrial Stem/Progenitor Cells. Curr Obstet Gynecol Rep 9, 7–14 (2020). https://doi.org/10.1007/s13669-020-00278-w

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13669-020-00278-w

Keywords

Search

Navigation