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Published in: Reviews in Endocrine and Metabolic Disorders 4/2012

01-12-2012

Endometrial regeneration and endometrial stem/progenitor cells

Authors: Caroline E. Gargett, Hong P. T. Nguyen, Louie Ye

Published in: Reviews in Endocrine and Metabolic Disorders | Issue 4/2012

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Abstract

The functional layer of the human endometrium is a highly regenerative tissue undergoing monthly cycles of growth, differentiation and shedding during a woman’s reproductive years. Fluctuating levels of circulating estrogen and progesterone orchestrate this dramatic remodeling of human endometrium. The thin inactive endometrium of postmenopausal women which resembles the permanent basal layer of cycling endometrium retains the capacity to respond to exogenous sex steroid hormones to regenerate into a thick functional endometrium capable of supporting pregnancy. Endometrial regeneration also follows parturition and endometrial resection. In non menstruating rodents, endometrial epithelium undergoes rounds of proliferation and apoptosis during estrus cycles. The recent identification of adult stem cells in both human and mouse endometrium suggests that epithelial progenitor cells and the mesenchymal stem/stromal cells have key roles in the cyclical regeneration of endometrial epithelium and stroma. This review will summarize the evidence for endometrial stem/progenitor cells, examine their role in mouse models of endometrial epithelial repair and estrogen-induced endometrial regeneration, and also describe the generation of endometrial-like epithelium from human embryonic stem cells. With markers now available for identifying endometrial mesenchymal stem/stromal cells, their possible role in gynecological diseases associated with abnormal endometrial proliferation and their potential application in cell-based therapies to regenerate reproductive and other tissues will be discussed.
Literature
1.
2.
go back to reference Jabbour HN, Kelly RW, Fraser HM, Critchley HOD. Endocrine regulation of menstruation. Endocr Rev. 2006;27:17–46.PubMedCrossRef Jabbour HN, Kelly RW, Fraser HM, Critchley HOD. Endocrine regulation of menstruation. Endocr Rev. 2006;27:17–46.PubMedCrossRef
3.
go back to reference McLennan CE, Rydell AH. Extent of endometrial shedding during normal menstruation. Obstet Gynecol. 1965;26:605–21.PubMed McLennan CE, Rydell AH. Extent of endometrial shedding during normal menstruation. Obstet Gynecol. 1965;26:605–21.PubMed
4.
go back to reference Padykula HA. Regeneration of the primate uterus: the role of stem cells. Ann N Y Acad Sci. 1991;622:47–56.PubMedCrossRef Padykula HA. Regeneration of the primate uterus: the role of stem cells. Ann N Y Acad Sci. 1991;622:47–56.PubMedCrossRef
5.
go back to reference Spencer TE, Hayashi K, Hu J, Carpenter KD. Comparative developmental biology of the mammalian uterus. Curr Top Dev Biol. 2005;68:85–122.PubMedCrossRef Spencer TE, Hayashi K, Hu J, Carpenter KD. Comparative developmental biology of the mammalian uterus. Curr Top Dev Biol. 2005;68:85–122.PubMedCrossRef
6.
go back to reference Ferenczy A, Bergeron C. Histology of the human endometrium: from birthe to senescence. Ann N Y Acad Sci. 1991;622:6–27.PubMedCrossRef Ferenczy A, Bergeron C. Histology of the human endometrium: from birthe to senescence. Ann N Y Acad Sci. 1991;622:6–27.PubMedCrossRef
7.
go back to reference Ettinger B, Bainton L, Upmalis DH, Citron JT, Vangessel A. Comparison of endometrial growth produced by unopposed conjugated estrogens or by micronized estradiol in postmenopausal women. Am J Obstet Gynecol. 1997;176:112–7.PubMedCrossRef Ettinger B, Bainton L, Upmalis DH, Citron JT, Vangessel A. Comparison of endometrial growth produced by unopposed conjugated estrogens or by micronized estradiol in postmenopausal women. Am J Obstet Gynecol. 1997;176:112–7.PubMedCrossRef
8.
go back to reference Paulson RJ, Boostanfar R, Saadat P, Mor E, Tourgeman DE, Slater CC, Francis MM, Jain JK. Pregnancy in the sixth decade of life: obstetric outcomes in women of advanced reproductive age. JAMA. 2002;288:2320–3.PubMedCrossRef Paulson RJ, Boostanfar R, Saadat P, Mor E, Tourgeman DE, Slater CC, Francis MM, Jain JK. Pregnancy in the sixth decade of life: obstetric outcomes in women of advanced reproductive age. JAMA. 2002;288:2320–3.PubMedCrossRef
9.
go back to reference Sauer MV, Miles RA, Dahmoush L, Paulson RJ, Press M, Moyer D. Evaluating the effect of age on endometrial responsiveness to hormone replacement therapy: a histologic ultrasonographic, and tissue receptor analysis. J Assist Reprod Genet. 1993;10:47–52.PubMedCrossRef Sauer MV, Miles RA, Dahmoush L, Paulson RJ, Press M, Moyer D. Evaluating the effect of age on endometrial responsiveness to hormone replacement therapy: a histologic ultrasonographic, and tissue receptor analysis. J Assist Reprod Genet. 1993;10:47–52.PubMedCrossRef
10.
go back to reference Klaassens AH, van Wijk FH, Hanifi-Moghaddam P, Sijmons B, Ewing PC, Ten Kate-Booij MJ, Kooi GS, Kloosterboer HJ, Blok LJ, Burger CW. Histological and immunohistochemical evaluation of postmenopausal endometrium after 3 weeks of treatment with tibolone, estrogen only, or estrogen plus progestagen. Fertil Steril. 2006;86:352–61.PubMedCrossRef Klaassens AH, van Wijk FH, Hanifi-Moghaddam P, Sijmons B, Ewing PC, Ten Kate-Booij MJ, Kooi GS, Kloosterboer HJ, Blok LJ, Burger CW. Histological and immunohistochemical evaluation of postmenopausal endometrium after 3 weeks of treatment with tibolone, estrogen only, or estrogen plus progestagen. Fertil Steril. 2006;86:352–61.PubMedCrossRef
11.
go back to reference Nguyen HPT, Sprung CN, Gargett CE. Differential expression of Wnt signaling molecules between pre- and postmenopausal endometrial epithelial cells suggests a population of putative epithelial stem/progenitor cells reside in the basalis layer. Endocrinol. 2012;153:2870–83.CrossRef Nguyen HPT, Sprung CN, Gargett CE. Differential expression of Wnt signaling molecules between pre- and postmenopausal endometrial epithelial cells suggests a population of putative epithelial stem/progenitor cells reside in the basalis layer. Endocrinol. 2012;153:2870–83.CrossRef
12.
go back to reference Gaide Chevronnay 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.PubMedCrossRef Gaide Chevronnay 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.PubMedCrossRef
13.
go back to reference Henriet P, Gaide Chevronnay HP, Marbaix E. The endocrine and paracrine control of menstruation. Mol Cell Endocrinol. 2011. Henriet P, Gaide Chevronnay HP, Marbaix E. The endocrine and paracrine control of menstruation. Mol Cell Endocrinol. 2011.
14.
go back to reference Maybin J, Critchley H. Repair and regeneration of the human endometrium. Expert Rev Obstet Gynecol. 2009;4:283–98.CrossRef Maybin J, Critchley H. Repair and regeneration of the human endometrium. Expert Rev Obstet Gynecol. 2009;4:283–98.CrossRef
15.
go back to reference Ludwig H, Metzger H, Frauli M. Endometrium: tissue remodelling and regeneration. In: D’Arcangues C, Fraser IS, Newton JR, Odlind V, editors. Contraception and mechanisms of endometrial bleeding. Cambridge University Press; 1990. 441–6. Ludwig H, Metzger H, Frauli M. Endometrium: tissue remodelling and regeneration. In: D’Arcangues C, Fraser IS, Newton JR, Odlind V, editors. Contraception and mechanisms of endometrial bleeding. Cambridge University Press; 1990. 441–6.
16.
go back to reference Okulicz WC, Scarrell R. Estrogen receptor α and progesterone receptor in the rhesus endometrium during the late secretory phase and menses. Proc Soc Exp Biol Med. 1998;218:316–21.PubMed Okulicz WC, Scarrell R. Estrogen receptor α and progesterone receptor in the rhesus endometrium during the late secretory phase and menses. Proc Soc Exp Biol Med. 1998;218:316–21.PubMed
17.
go back to reference Kaitu’u-Lino TJ, Morison NB, Salamonsen LA. Estrogen is not essential for full endometrial restoration after breakdown: lessons from a mouse model. Endocrinol. 2007;148:5105–11.CrossRef Kaitu’u-Lino TJ, Morison NB, Salamonsen LA. Estrogen is not essential for full endometrial restoration after breakdown: lessons from a mouse model. Endocrinol. 2007;148:5105–11.CrossRef
18.
go back to reference 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;24:1393–401.PubMedCrossRef 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;24:1393–401.PubMedCrossRef
19.
go back to reference Garry R, Hart R, Karthigasu KA, Burke C. Structural changes in endometrial basal glands during menstruation. BJOG. 2010;117:1175–85.PubMedCrossRef Garry R, Hart R, Karthigasu KA, Burke C. Structural changes in endometrial basal glands during menstruation. BJOG. 2010;117:1175–85.PubMedCrossRef
20.
go back to reference Cao W, Mah K, Carroll RS, Slayden OD, Brenner RM. Progesterone withdrawal up-regulates fibronectin and integrins during menstruation and repair in the rhesus macaque endometrium. Hum Reprod. 2007;22:3223–31.PubMedCrossRef Cao W, Mah K, Carroll RS, Slayden OD, Brenner RM. Progesterone withdrawal up-regulates fibronectin and integrins during menstruation and repair in the rhesus macaque endometrium. Hum Reprod. 2007;22:3223–31.PubMedCrossRef
21.
go back to reference Evans J, Kaitu’u-Lino T, Salamonsen LA. Extracellular matrix dynamics in scar-free endometrial repair: perspectives from mouse in vivo and human in vitro studies. Biol Reprod. 2011;85:511–23.PubMedCrossRef Evans J, Kaitu’u-Lino T, Salamonsen LA. Extracellular matrix dynamics in scar-free endometrial repair: perspectives from mouse in vivo and human in vitro studies. Biol Reprod. 2011;85:511–23.PubMedCrossRef
22.
go back to reference Ferenczy A, Bertrand G, Gelfand MM. Proliferation kinetics of human endometrium during the normal menstrual cycle. Am J Obstet Gynecol. 1979;133:859–67.PubMed Ferenczy A, Bertrand G, Gelfand MM. Proliferation kinetics of human endometrium during the normal menstrual cycle. Am J Obstet Gynecol. 1979;133:859–67.PubMed
23.
go back to reference Padykula HA, Coles LG, Okulicz WC, Rapaport SI, McCracken JA, King Jr NW, Longcope C, Kaiserman-Abramof IR. The basalis of the primate endometrium: a bifunctional germinal compartment. Biol Reprod. 1989;40:681–90.PubMedCrossRef Padykula HA, Coles LG, Okulicz WC, Rapaport SI, McCracken JA, King Jr NW, Longcope C, Kaiserman-Abramof IR. The basalis of the primate endometrium: a bifunctional germinal compartment. Biol Reprod. 1989;40:681–90.PubMedCrossRef
24.
go back to reference Brenner RM, Slayden OD, Rodgers WH, Critchley HOD, Carroll R, Nie XJ, Mah K. Immunocytochemical assessment of mitotic activity with an antibody to phosphorylated histone H3 in the macaque and human endometrium. Hum Reprod. 2003;18:1185–93.PubMedCrossRef Brenner RM, Slayden OD, Rodgers WH, Critchley HOD, Carroll R, Nie XJ, Mah K. Immunocytochemical assessment of mitotic activity with an antibody to phosphorylated histone H3 in the macaque and human endometrium. Hum Reprod. 2003;18:1185–93.PubMedCrossRef
25.
26.
go back to reference Slayden OD, Brenner RM. Hormonal regulation and localization of estrogen, progestin and androgen receptors in the endometrium of nonhuman primates: effects of progesterone receptor antagonists. Arch Histol Cytol. 2004;67:393–409.PubMedCrossRef Slayden OD, Brenner RM. Hormonal regulation and localization of estrogen, progestin and androgen receptors in the endometrium of nonhuman primates: effects of progesterone receptor antagonists. Arch Histol Cytol. 2004;67:393–409.PubMedCrossRef
27.
go back to reference Couse JF, Korach KS. Estrogen receptor null mice: what have we learned and where will they lead us? Endocr Rev. 1999;20:358–417.PubMedCrossRef Couse JF, Korach KS. Estrogen receptor null mice: what have we learned and where will they lead us? Endocr Rev. 1999;20:358–417.PubMedCrossRef
28.
go back to reference Cooke PS, Buchanan DL, Young P, Setiawan T, Brody J, Korach KS, Taylor J, Lubahn DB, Cunha GR. Stromal estrogen receptors mediate mitogenic effects of estradiol on uterine epithelium. Proc Natl Acad Sci U S A. 1997;94:6535–40.PubMedCrossRef Cooke PS, Buchanan DL, Young P, Setiawan T, Brody J, Korach KS, Taylor J, Lubahn DB, Cunha GR. Stromal estrogen receptors mediate mitogenic effects of estradiol on uterine epithelium. Proc Natl Acad Sci U S A. 1997;94:6535–40.PubMedCrossRef
29.
go back to reference Kurita T, Medina R, Schabel AB, Young P, Gama P, Parekh TV, Brody J, Cunha GR, Osteen KG, Bruner-Tran KL, Gold LI. The activation function-1 domain of estrogen receptor alpha in uterine stromal cells is required for mouse but not human uterine epithelial response to estrogen. Differentiation. 2005;73:313–22.PubMedCrossRef Kurita T, Medina R, Schabel AB, Young P, Gama P, Parekh TV, Brody J, Cunha GR, Osteen KG, Bruner-Tran KL, Gold LI. The activation function-1 domain of estrogen receptor alpha in uterine stromal cells is required for mouse but not human uterine epithelial response to estrogen. Differentiation. 2005;73:313–22.PubMedCrossRef
30.
go back to reference Tong W, Niklaus A, Zhu L, Pan H, Chen B, Aubuchon M, Santoro N, Pollard JW. Estrogen and progesterone regulation of cell proliferation in the endometrium of muridae and humans. In: Aplin JD, Fazleabas A, Glasser SR, Giudice LC, editors. The Endometrium. Molecular, cellular, and clinical perspectives. 2nd ed. London: Informa Healthcare; 2008. p. 99–122.CrossRef Tong W, Niklaus A, Zhu L, Pan H, Chen B, Aubuchon M, Santoro N, Pollard JW. Estrogen and progesterone regulation of cell proliferation in the endometrium of muridae and humans. In: Aplin JD, Fazleabas A, Glasser SR, Giudice LC, editors. The Endometrium. Molecular, cellular, and clinical perspectives. 2nd ed. London: Informa Healthcare; 2008. p. 99–122.CrossRef
31.
go back to reference van der Horst PH, Wang Y, van der Zee M, Burger CW, Blok LJ. Interaction between sexhormones and WNT/beta-catenin signal transduction in endometrial physiology and disease. Mol Cell Endocrinol. 2011. doi:10.1016/j.mce.2011.06.010. van der Horst PH, Wang Y, van der Zee M, Burger CW, Blok LJ. Interaction between sexhormones and WNT/beta-catenin signal transduction in endometrial physiology and disease. Mol Cell Endocrinol. 2011. doi:10.​1016/​j.​mce.​2011.​06.​010.
32.
go back to reference Hou XN, Tan Y, Li ML, Dey SK, Das SK. Canonical Wnt signaling is critical to estrogen-mediated uterine growth. Mol Endocrinol. 2004;18:3035–49.PubMedCrossRef Hou XN, Tan Y, Li ML, Dey SK, Das SK. Canonical Wnt signaling is critical to estrogen-mediated uterine growth. Mol Endocrinol. 2004;18:3035–49.PubMedCrossRef
33.
go back to reference Cong F, Varmus H. Nuclear-cytoplasmic shuttling of Axin regulates subcellular localization of β−catenin. Proc Natl Acad Sci U S A. 2004;101:2882–7.PubMedCrossRef Cong F, Varmus H. Nuclear-cytoplasmic shuttling of Axin regulates subcellular localization of β−catenin. Proc Natl Acad Sci U S A. 2004;101:2882–7.PubMedCrossRef
34.
go back to reference Critchley HOD, Brenner RM, Henderson TA, Williams K, Nayak NR, Slayden OD, Millar MR, Saunders PTK. Estrogen receptor β, but not estrogen receptor α, is present in the vascular endothelium of the human and nonhuman primate endometrium. J Clin Endocrinol Metab. 2001;86:1370–8.PubMedCrossRef Critchley HOD, Brenner RM, Henderson TA, Williams K, Nayak NR, Slayden OD, Millar MR, Saunders PTK. Estrogen receptor β, but not estrogen receptor α, is present in the vascular endothelium of the human and nonhuman primate endometrium. J Clin Endocrinol Metab. 2001;86:1370–8.PubMedCrossRef
35.
go back to reference Lecce G, Meduri G, Ancelin M, Bergeron C, Perrot-Applanat M. Presence of estrogen receptor β in the human endometrium through the cycle: expression in glandular, stromal, and vascular cells. J Clin Endocrinol Metab. 2001;86:1379–86.PubMedCrossRef Lecce G, Meduri G, Ancelin M, Bergeron C, Perrot-Applanat M. Presence of estrogen receptor β in the human endometrium through the cycle: expression in glandular, stromal, and vascular cells. J Clin Endocrinol Metab. 2001;86:1379–86.PubMedCrossRef
36.
go back to reference Wada-Hiraike O, Hiraike H, Okinaga H, Imamov O, Barros RPA, Morani A, Omoto Y, Warner M, Gustafsson JA. Role of estrogen receptor β in uterine stroma and epithelium: insights from estrogen receptor β-/- mice. Proc Natl Acad Sci U S A. 2006;103:18350–5.PubMedCrossRef Wada-Hiraike O, Hiraike H, Okinaga H, Imamov O, Barros RPA, Morani A, Omoto Y, Warner M, Gustafsson JA. Role of estrogen receptor β in uterine stroma and epithelium: insights from estrogen receptor β-/- mice. Proc Natl Acad Sci U S A. 2006;103:18350–5.PubMedCrossRef
37.
go back to reference Salamonsen LA. Tissue injury and repair in the female human reproductive tract. Reproduction. 2003;125:301–11.PubMedCrossRef Salamonsen LA. Tissue injury and repair in the female human reproductive tract. Reproduction. 2003;125:301–11.PubMedCrossRef
38.
go back to reference Schwab KE, Gargett CE. Co-expression of two perivascular cell markers isolates mesenchymal stem-like cells from human endometrium. Hum Reprod. 2007;22:2903–11.PubMedCrossRef Schwab KE, Gargett CE. Co-expression of two perivascular cell markers isolates mesenchymal stem-like cells from human endometrium. Hum Reprod. 2007;22:2903–11.PubMedCrossRef
39.
go back to reference Masuda H, Matsuzaki Y, Hiratsu E, Ono M, Nagashima T, Kajitani T, Arase T, Oda H, Uchida H, Asada H, Ito M, Yoshimura N, Maruyama T, Okano H. Stem cell-like properties of the endometrial side population: implication in endometrial regeneration. PLoS One. 2010;5:e10387.PubMedCrossRef Masuda H, Matsuzaki Y, Hiratsu E, Ono M, Nagashima T, Kajitani T, Arase T, Oda H, Uchida H, Asada H, Ito M, Yoshimura N, Maruyama T, Okano H. Stem cell-like properties of the endometrial side population: implication in endometrial regeneration. PLoS One. 2010;5:e10387.PubMedCrossRef
40.
41.
go back to reference Maruyama T, Masuda H, Ono M, Kajitani T, Yoshimura Y. Human uterine stem/progenitor cells: their possible role in uterine physiology and pathology. Reproduction. 2010;140:11–22.PubMedCrossRef Maruyama T, Masuda H, Ono M, Kajitani T, Yoshimura Y. Human uterine stem/progenitor cells: their possible role in uterine physiology and pathology. Reproduction. 2010;140:11–22.PubMedCrossRef
42.
43.
go back to reference Chan RWS, Schwab KE, Gargett CE. Clonogenicity of human endometrial epithelial and stromal cells. Biol Reprod. 2004;70:1738–50.PubMedCrossRef Chan RWS, Schwab KE, Gargett CE. Clonogenicity of human endometrial epithelial and stromal cells. Biol Reprod. 2004;70:1738–50.PubMedCrossRef
44.
go back to reference 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 Suppl 2:1124–30.PubMedCrossRef 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 Suppl 2:1124–30.PubMedCrossRef
45.
go back to reference Gargett CE, Schwab KE, Zillwood RM, Nguyen HPT, Wu D. Isolation and culture of epithelial progenitors and mesenchymal stem cells from human endometrium. Biol Reprod. 2009;80:1136–45.PubMedCrossRef Gargett CE, Schwab KE, Zillwood RM, Nguyen HPT, Wu D. Isolation and culture of epithelial progenitors and mesenchymal stem cells from human endometrium. Biol Reprod. 2009;80:1136–45.PubMedCrossRef
46.
go back to reference Dominici M, Le BK, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The international society for cellular therapy position statement. Cytotherapy. 2006;8:315–7.PubMedCrossRef Dominici M, Le BK, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The international society for cellular therapy position statement. Cytotherapy. 2006;8:315–7.PubMedCrossRef
47.
go back to reference Morrison SJ, Shah NM, Anderson DJ. Regulatory mechanisms in stem cell biology. Cell. 1997;88:287–98.PubMedCrossRef Morrison SJ, Shah NM, Anderson DJ. Regulatory mechanisms in stem cell biology. Cell. 1997;88:287–98.PubMedCrossRef
48.
go back to reference Wolff EF, Wolff AB, Du H, Taylor HS. Demonstration of multipotent stem cells in the adult human endometrium by in vitro chondrogenesis. Reprod Sci. 2007;14:524–33.PubMedCrossRef Wolff EF, Wolff AB, Du H, Taylor HS. Demonstration of multipotent stem cells in the adult human endometrium by in vitro chondrogenesis. Reprod Sci. 2007;14:524–33.PubMedCrossRef
49.
go back to reference Wolff EF, Gao XB, Yao KV, Andrews ZB, Du H, Elsworth JD, Taylor HS. Endometrial stem cell transplantation restores dopamine production in a parkinson’s disease model. J Cell Mol Med. 2010;15:747–55.CrossRef Wolff EF, Gao XB, Yao KV, Andrews ZB, Du H, Elsworth JD, Taylor HS. Endometrial stem cell transplantation restores dopamine production in a parkinson’s disease model. J Cell Mol Med. 2010;15:747–55.CrossRef
50.
go back to reference Santamaria X, Massasa EE, Feng Y, Wolff E, Taylor HS. Derivation of insulin producing cells from human endometrial stromal stem cells and use in the treatment of murine diabetes. Mol Ther. 2011;19:2065–71.PubMedCrossRef Santamaria X, Massasa EE, Feng Y, Wolff E, Taylor HS. Derivation of insulin producing cells from human endometrial stromal stem cells and use in the treatment of murine diabetes. Mol Ther. 2011;19:2065–71.PubMedCrossRef
51.
go back to reference Dimitrov R, Timeva T, Kyurkchiev D, Stamenova M, Shterev A, Kostova P, Zlatkov V, Kehayov I, Kyurkchiev S. Characterisation of clonogenic stromal cells isolated from human endometrium. Reprod. 2008;135:551–8.CrossRef Dimitrov R, Timeva T, Kyurkchiev D, Stamenova M, Shterev A, Kostova P, Zlatkov V, Kehayov I, Kyurkchiev S. Characterisation of clonogenic stromal cells isolated from human endometrium. Reprod. 2008;135:551–8.CrossRef
52.
go back to reference Goodell MA, Rosenzweig M, Kim H, Marks DF, DeMaria MA, Paradis G, Grupp SA, Sieff CA, Mulligan RC, Johnson RP. Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nat Med. 1997;12:1337–45.CrossRef Goodell MA, Rosenzweig M, Kim H, Marks DF, DeMaria MA, Paradis G, Grupp SA, Sieff CA, Mulligan RC, Johnson RP. Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nat Med. 1997;12:1337–45.CrossRef
53.
54.
go back to reference Cervello I, Gil-Sanchis C, Mas A, Gado-Rosas F, Martinez-Conejero JA, Galan A, Martinez-Romero A, Martinez S, Navarro I, Ferro J, Horcajadas JA, Esteban FJ, O’Connor JE, Pellicer A, Simon C. Human endometrial side population cells exhibit genotypic, phenotypic and functional features of somatic stem cells. PLoS One. 2010;5:e10964.PubMedCrossRef Cervello I, Gil-Sanchis C, Mas A, Gado-Rosas F, Martinez-Conejero JA, Galan A, Martinez-Romero A, Martinez S, Navarro I, Ferro J, Horcajadas JA, Esteban FJ, O’Connor JE, Pellicer A, Simon C. Human endometrial side population cells exhibit genotypic, phenotypic and functional features of somatic stem cells. PLoS One. 2010;5:e10964.PubMedCrossRef
55.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
56.
go back to reference Kato K, Yoshimoto M, Kato K, Adachi S, Yamayoshi A, Arima T, Asanoma K, Kyo S, Nakahata T, Wake N. Characterization of side-population cells in human normal endometrium. Hum Reprod. 2007;22:1214–23.PubMedCrossRef Kato K, Yoshimoto M, Kato K, Adachi S, Yamayoshi A, Arima T, Asanoma K, Kyo S, Nakahata T, Wake N. Characterization of side-population cells in human normal endometrium. Hum Reprod. 2007;22:1214–23.PubMedCrossRef
57.
go back to reference Hu FF, Jing X, Cui YG, Qian XQ, Mao YD, Liao LM, Liu JY. Isolation and characterization of side population cells in the postpartum murine endometrium. Reprod Sci. 2010;17:629–42.PubMedCrossRef Hu FF, Jing X, Cui YG, Qian XQ, Mao YD, Liao LM, Liu JY. Isolation and characterization of side population cells in the postpartum murine endometrium. Reprod Sci. 2010;17:629–42.PubMedCrossRef
58.
go back to reference Xu J, Hu FF, Cui YG, Luo J, Jiang CY, Gao L, Qian XQ, Mao YD, Liu JY. Effect of estradiol on proliferation and differentiation of side population stem/progenitor cells from murine endometrium. Reprod Biol Endocrinol. 2011;9:103.PubMedCrossRef Xu J, Hu FF, Cui YG, Luo J, Jiang CY, Gao L, Qian XQ, Mao YD, Liu JY. Effect of estradiol on proliferation and differentiation of side population stem/progenitor cells from murine endometrium. Reprod Biol Endocrinol. 2011;9:103.PubMedCrossRef
59.
go back to reference Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, Andriolo G, Sun B, Zheng B, Zhang L, Norotte C, Teng PN, Traas J, Schugar R, Deasy BM, Badylak S, Buhring HJ, Giacobino JP, Lazzari L, Huard J, Peault B. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008;3:301–13.PubMedCrossRef Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, Andriolo G, Sun B, Zheng B, Zhang L, Norotte C, Teng PN, Traas J, Schugar R, Deasy BM, Badylak S, Buhring HJ, Giacobino JP, Lazzari L, Huard J, Peault B. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008;3:301–13.PubMedCrossRef
61.
go back to reference Spitzer TL, Rojas A, Zelenko Z, Aghajanova L, Erikson DW, Barragan F, Meyer M, Tamaresis JS, Hamilton AE, Irwin JC, Giudice LC. Perivascular human endometrial mesenchymal stem cells express pathways relevant to self-renewal, lineage specification, and functional phenotype. Biol Reprod. 2012;86:58, 1–16.PubMedCrossRef Spitzer TL, Rojas A, Zelenko Z, Aghajanova L, Erikson DW, Barragan F, Meyer M, Tamaresis JS, Hamilton AE, Irwin JC, Giudice LC. Perivascular human endometrial mesenchymal stem cells express pathways relevant to self-renewal, lineage specification, and functional phenotype. Biol Reprod. 2012;86:58, 1–16.PubMedCrossRef
62.
go back to reference Murphy MP, Wang H, Patel AN, Kambhampati S, Angle N, Chan K, Marleau AM, Pyszniak A, Carrier E, Ichim TE, Riordan NH. Allogeneic endometrial regenerative cells: an “Off the shelf solution” for critical limb ischemia? J Transl Med. 2008;6:45.PubMedCrossRef Murphy MP, Wang H, Patel AN, Kambhampati S, Angle N, Chan K, Marleau AM, Pyszniak A, Carrier E, Ichim TE, Riordan NH. Allogeneic endometrial regenerative cells: an “Off the shelf solution” for critical limb ischemia? J Transl Med. 2008;6:45.PubMedCrossRef
63.
65.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
66.
go back to reference Koks CM, Groothuis PG, Dunselman GJ, de Goeij AM, Evers JH. Adhesion of shed menstrual tissue in an in-vitro model using amnion and peritoneum: a light and electron microscopic study. Hum Reprod. 1999;14:816–22.PubMedCrossRef Koks CM, Groothuis PG, Dunselman GJ, de Goeij AM, Evers JH. Adhesion of shed menstrual tissue in an in-vitro model using amnion and peritoneum: a light and electron microscopic study. Hum Reprod. 1999;14:816–22.PubMedCrossRef
67.
go back to reference Cui CH, Uyama T, Miyado K, Terai M, Kyo S, Kiyono T, Umezawa A. Menstrual blood-derived cells confer human dystrophin expression in the murine model of duchenne muscular dystrophy via cell fusion and myogenic transdifferentiation. Mol Biol Cell. 2007;18:1586–94.PubMedCrossRef Cui CH, Uyama T, Miyado K, Terai M, Kyo S, Kiyono T, Umezawa A. Menstrual blood-derived cells confer human dystrophin expression in the murine model of duchenne muscular dystrophy via cell fusion and myogenic transdifferentiation. Mol Biol Cell. 2007;18:1586–94.PubMedCrossRef
68.
go back to reference Hida N, Nishiyama N, Miyoshi S, Kira S, Segawa K, Uyama T, Mori T, Miyado K, Ikegami Y, Cui CH, Kiyono T, Kyo S, Shimizu T, Okano T, Sakamoto M, Ogawa S, Umezawa A. Novel cardiac precursor-like cells from human menstrual blood-derived mesenchymal cells. Stem Cells. 2008;26:1695–704.PubMedCrossRef Hida N, Nishiyama N, Miyoshi S, Kira S, Segawa K, Uyama T, Mori T, Miyado K, Ikegami Y, Cui CH, Kiyono T, Kyo S, Shimizu T, Okano T, Sakamoto M, Ogawa S, Umezawa A. Novel cardiac precursor-like cells from human menstrual blood-derived mesenchymal cells. Stem Cells. 2008;26:1695–704.PubMedCrossRef
69.
go back to reference Meng X, Ichim TE, Zhong J, Rogers A, Yin Z, Jackson J, Wang H, Ge W, Bogin V, Chan KW, Thebaud B, Riordan NH. Endometrial regenerative cells: a novel stem cell population. J Transl Med. 2007;5:57.PubMedCrossRef Meng X, Ichim TE, Zhong J, Rogers A, Yin Z, Jackson J, Wang H, Ge W, Bogin V, Chan KW, Thebaud B, Riordan NH. Endometrial regenerative cells: a novel stem cell population. J Transl Med. 2007;5:57.PubMedCrossRef
70.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
71.
go back to reference Anwar S, Buhring HJ, Gargett CE. A single perivascular marker identifies MSC in human endometrium and menstrual blood. Aust Health Med Res Congr. 2008;4:P700. Anwar S, Buhring HJ, Gargett CE. A single perivascular marker identifies MSC in human endometrium and menstrual blood. Aust Health Med Res Congr. 2008;4:P700.
72.
go back to reference Musina RA, Belyavski AV, Tarusova OV, Solovyova EV, Sukhikh GT. Endometrial mesenchymal stem cells isolated from the menstrual blood. Bull Exp Biol Med. 2008;145:539–43.PubMedCrossRef Musina RA, Belyavski AV, Tarusova OV, Solovyova EV, Sukhikh GT. Endometrial mesenchymal stem cells isolated from the menstrual blood. Bull Exp Biol Med. 2008;145:539–43.PubMedCrossRef
73.
go back to reference Sasson IE, Taylor HS. Stem cells and the pathogenesis of endometriosis. Ann N Y Acad Sci. 2008;1127:106–15.PubMedCrossRef Sasson IE, Taylor HS. Stem cells and the pathogenesis of endometriosis. Ann N Y Acad Sci. 2008;1127:106–15.PubMedCrossRef
74.
go back to reference Starzinski-Powitz A, Zeitvogel A, Schreiner A, Baumann R. In search of pathogenic mechanims in endometriosis: the challenge for molecular cell biology. Curr Mol Med. 2001;1:655–64.PubMedCrossRef Starzinski-Powitz A, Zeitvogel A, Schreiner A, Baumann R. In search of pathogenic mechanims in endometriosis: the challenge for molecular cell biology. Curr Mol Med. 2001;1:655–64.PubMedCrossRef
75.
go back to reference Masuda H, Maruyama T, Hiratsu E, Yamane J, Iwanami A, Nagashima T, Ono M, Miyoshi H, Okano HJ, Ito M, Tamaoki N, Nomura T, Okano H, Matsuzaki Y, Yoshimura Y. Noninvasive and real-time assessment of reconstructed functional human endometrium in NOD/SCID/γ c null immunodeficient mice. Proc Natl Acad Sci U S A. 2007;104:1925–30.PubMedCrossRef Masuda H, Maruyama T, Hiratsu E, Yamane J, Iwanami A, Nagashima T, Ono M, Miyoshi H, Okano HJ, Ito M, Tamaoki N, Nomura T, Okano H, Matsuzaki Y, Yoshimura Y. Noninvasive and real-time assessment of reconstructed functional human endometrium in NOD/SCID/γ c null immunodeficient mice. Proc Natl Acad Sci U S A. 2007;104:1925–30.PubMedCrossRef
76.
go back to reference Cervello I, Mas A, Gil-Sanchis C, Peris L, Faus A, Saunders PT, Critchley HO, Simon C. Reconstruction of endometrium from human endometrial side population cell lines. PLoS One. 2011;6:e21221.PubMedCrossRef Cervello I, Mas A, Gil-Sanchis C, Peris L, Faus A, Saunders PT, Critchley HO, Simon C. Reconstruction of endometrium from human endometrial side population cell lines. PLoS One. 2011;6:e21221.PubMedCrossRef
77.
go back to reference Brody JR, Cunha GR. Histologic, morphometric, and immunocytochemical analysis of myometrial development in rats and mice: I. Normal development. Am J Anat. 1989;186:1–20.PubMedCrossRef Brody JR, Cunha GR. Histologic, morphometric, and immunocytochemical analysis of myometrial development in rats and mice: I. Normal development. Am J Anat. 1989;186:1–20.PubMedCrossRef
78.
go back to reference Chan RW, Gargett CE. Identification of label-retaining cells in mouse endometrium. Stem Cells. 2006;24:1529–38.PubMedCrossRef Chan RW, Gargett CE. Identification of label-retaining cells in mouse endometrium. Stem Cells. 2006;24:1529–38.PubMedCrossRef
79.
go back to reference Chan RWS, Kaitu’u-Lino T, Gargett CE. Role of label-retaining cells in estrogen-induced endometrial regeneration. Reprod Sci. 2012;19:102–14.PubMedCrossRef Chan RWS, Kaitu’u-Lino T, Gargett CE. Role of label-retaining cells in estrogen-induced endometrial regeneration. Reprod Sci. 2012;19:102–14.PubMedCrossRef
80.
go back to reference Martin L, Finn CA. Interactions of oestradiol and progestins in the mouse uterus. J Endocrinol. 1970;48:109–15.PubMedCrossRef Martin L, Finn CA. Interactions of oestradiol and progestins in the mouse uterus. J Endocrinol. 1970;48:109–15.PubMedCrossRef
81.
go back to reference Martin L, Finn CA, Trinder G. Hypertrophy and hyperplasia in the mouse uterus after oestrogen treatment: an autoradiographic study. J Endocrinol. 1973;56:133–44.PubMedCrossRef Martin L, Finn CA, Trinder G. Hypertrophy and hyperplasia in the mouse uterus after oestrogen treatment: an autoradiographic study. J Endocrinol. 1973;56:133–44.PubMedCrossRef
82.
go back to reference Walter LM, Rogers PAW, Girling JE. The role of progesterone in endometrial angiogenesis in pregnant and ovariectomised mice. Reproduction. 2005;129:765–77.PubMedCrossRef Walter LM, Rogers PAW, Girling JE. The role of progesterone in endometrial angiogenesis in pregnant and ovariectomised mice. Reproduction. 2005;129:765–77.PubMedCrossRef
83.
go back to reference Brasted M, White CA, Kennedy TG, Salamonsen LA. Mimicking the events of menstruation in the murine uterus. Biol Reprod. 2003;69:1273–80.PubMedCrossRef Brasted M, White CA, Kennedy TG, Salamonsen LA. Mimicking the events of menstruation in the murine uterus. Biol Reprod. 2003;69:1273–80.PubMedCrossRef
84.
go back to reference Cervello I, Martinez-Conejero JA, Horcajadas JA, Pellicer A, Simon C. Identification, characterization and co-localization of label-retaining cell population in mouse endometrium with typical undifferentiated markers. Hum Reprod. 2007;22:45–51.PubMedCrossRef Cervello I, Martinez-Conejero JA, Horcajadas JA, Pellicer A, Simon C. Identification, characterization and co-localization of label-retaining cell population in mouse endometrium with typical undifferentiated markers. Hum Reprod. 2007;22:45–51.PubMedCrossRef
85.
go back to reference Szotek PP, Chang HL, Zhang L, Preffer F, Dombkowski D, Donahoe PK, Teixeira J. Adult mouse myometrial label-retaining cells divide in response to gonadotropin stimulation. Stem Cells. 2007;25:1317–25.PubMedCrossRef Szotek PP, Chang HL, Zhang L, Preffer F, Dombkowski D, Donahoe PK, Teixeira J. Adult mouse myometrial label-retaining cells divide in response to gonadotropin stimulation. Stem Cells. 2007;25:1317–25.PubMedCrossRef
86.
go back to reference Gargett CE, Chan RW, Schwab KE. Endometrial stem cells. Curr Opin Obstet Gynecol. 2007;19:377–83.PubMedCrossRef Gargett CE, Chan RW, Schwab KE. Endometrial stem cells. Curr Opin Obstet Gynecol. 2007;19:377–83.PubMedCrossRef
87.
go back to reference Kaitu’u-Lino TJ, Ye L, Salamonsen LA, Girling JE, Gargett CE. Identification of label-retaining perivascular cells in a mouse model of endometrial decidualization, breakdown, and repair. Biol Reprod. 2012;86:184, 1–8. doi:10.1095/biolreprod.112.099309:. Kaitu’u-Lino TJ, Ye L, Salamonsen LA, Girling JE, Gargett CE. Identification of label-retaining perivascular cells in a mouse model of endometrial decidualization, breakdown, and repair. Biol Reprod. 2012;86:184, 1–8. doi:10.​1095/​biolreprod.​112.​099309:​.
88.
go back to reference Kaitu’u-Lino TJ, Ye L, Gargett CE. Reepithelialization of the uterine surface arises from endometrial glands: evidence from a functional mouse model of breakdown and repair. Endocrinology. 2010;151:3386–95.PubMedCrossRef Kaitu’u-Lino TJ, Ye L, Gargett CE. Reepithelialization of the uterine surface arises from endometrial glands: evidence from a functional mouse model of breakdown and repair. Endocrinology. 2010;151:3386–95.PubMedCrossRef
89.
go back to reference Mayani H, Alvarado-Moreno JA, Flores-Guzman P. Biology of human hematopoietic stem and progenitor cells present in circulation. Arch Med Res. 2003;34:476–88.PubMedCrossRef Mayani H, Alvarado-Moreno JA, Flores-Guzman P. Biology of human hematopoietic stem and progenitor cells present in circulation. Arch Med Res. 2003;34:476–88.PubMedCrossRef
90.
go back to reference He Q, Wan C, Li G. Concise review: multipotent mesenchymal stromal cells in blood. Stem Cells. 2007;25:69–77.PubMedCrossRef He Q, Wan C, Li G. Concise review: multipotent mesenchymal stromal cells in blood. Stem Cells. 2007;25:69–77.PubMedCrossRef
91.
go back to reference Robb AO, Mills NL, Smith IB, Short A, Tura-Ceide O, Barclay GR, Blomberg A, Critchley HO, Newby DE, Denison FC. Influence of menstrual cycle on circulating endothelial progenitor cells. Hum Reprod. 2009;24:619–25.PubMedCrossRef Robb AO, Mills NL, Smith IB, Short A, Tura-Ceide O, Barclay GR, Blomberg A, Critchley HO, Newby DE, Denison FC. Influence of menstrual cycle on circulating endothelial progenitor cells. Hum Reprod. 2009;24:619–25.PubMedCrossRef
92.
go back to reference Korbling M, Estrov Z. Adult stem cells for tissue repair - A new therapeutic concept? N Engl J Med. 2003;349:570–82.PubMedCrossRef Korbling M, Estrov Z. Adult stem cells for tissue repair - A new therapeutic concept? N Engl J Med. 2003;349:570–82.PubMedCrossRef
93.
go back to reference Bratincsak A, Brownstein MJ, Cassiani-Ingoni R, Pastorino S, Szalayova I, Toth ZE, Key S, Nemeth K, Pickel J, Mezey E. CD45-positive blood cells give rise to uterine epithelial cells in mice. Stem Cells. 2007;25:2820–6.PubMedCrossRef Bratincsak A, Brownstein MJ, Cassiani-Ingoni R, Pastorino S, Szalayova I, Toth ZE, Key S, Nemeth K, Pickel J, Mezey E. CD45-positive blood cells give rise to uterine epithelial cells in mice. Stem Cells. 2007;25:2820–6.PubMedCrossRef
94.
go back to reference Taylor HS. Endometrial cells derived from donor stem cells in bone marrow transplant recipients. JAMA. 2004;292:81–5.PubMedCrossRef Taylor HS. Endometrial cells derived from donor stem cells in bone marrow transplant recipients. JAMA. 2004;292:81–5.PubMedCrossRef
95.
go back to reference Mints M, Jansson M, Sadeghi B, Westgren M, Uzunel M, Hassan M, Palmblad J. Endometrial endothelial cells are derived from donor stem cells in a bone marrow transplant recipient. Hum Reprod. 2008;23:139–43.PubMedCrossRef Mints M, Jansson M, Sadeghi B, Westgren M, Uzunel M, Hassan M, Palmblad J. Endometrial endothelial cells are derived from donor stem cells in a bone marrow transplant recipient. Hum Reprod. 2008;23:139–43.PubMedCrossRef
96.
go back to reference Ikoma T, Kyo S, Maida Y, Ozaki S, Takakura M, Nakao S, Inoue M. Bone marrow-derived cells from male donors can compose endometrial glands in female transplant recipients. Am J Obstet Gynecol. 2009;201:608-e1–8.CrossRef Ikoma T, Kyo S, Maida Y, Ozaki S, Takakura M, Nakao S, Inoue M. Bone marrow-derived cells from male donors can compose endometrial glands in female transplant recipients. Am J Obstet Gynecol. 2009;201:608-e1–8.CrossRef
97.
go back to reference Cervello I, Gil-Sanchis C, Mas A, Faus A, Sanz J, Moscardo F, Higueras G, Sanz MA, Pellicer A, Simon C. Bone marrow-derived cells from male donors do not contribute to the endometrial side population of the recipient. PLoS One. 2012;7:e30260.PubMedCrossRef Cervello I, Gil-Sanchis C, Mas A, Faus A, Sanz J, Moscardo F, Higueras G, Sanz MA, Pellicer A, Simon C. Bone marrow-derived cells from male donors do not contribute to the endometrial side population of the recipient. PLoS One. 2012;7:e30260.PubMedCrossRef
98.
go back to reference Aghajanova L, Horcajadas JA, Esteban FJ, Giudice LC. The bone marrow-derived human mesenchymal stem cell: potential progenitor of the endometrial stromal fibroblast. Biol Reprod. 2010;82:1076–87.PubMedCrossRef Aghajanova L, Horcajadas JA, Esteban FJ, Giudice LC. The bone marrow-derived human mesenchymal stem cell: potential progenitor of the endometrial stromal fibroblast. Biol Reprod. 2010;82:1076–87.PubMedCrossRef
99.
go back to reference Du H, Taylor HS. Contribution of bone marrow-derived stem cells to endometrium and endometriosis. Stem Cells. 2007;25:2082–6.PubMedCrossRef Du H, Taylor HS. Contribution of bone marrow-derived stem cells to endometrium and endometriosis. Stem Cells. 2007;25:2082–6.PubMedCrossRef
100.
go back to reference Du H, Taylor HS. Stem cells in female reproduction. Reprod Sci. 2010;16:126–39. Du H, Taylor HS. Stem cells in female reproduction. Reprod Sci. 2010;16:126–39.
101.
go back to reference Masuda H, Kalka C, Takahashi T, Yoshida M, Wada M, Kobori M, Itoh R, Iwaguro H, Eguchi M, Iwami Y, Tanaka R, Nakagawa Y, Sugimoto A, Ninomiya S, Hayashi S, Kato S, Asahara T. Estrogen-mediated endothelial progenitor cell biology and kinetics for physiological postnatal vasculogenesis. Circ Res. 2007;101:598–606.PubMedCrossRef Masuda H, Kalka C, Takahashi T, Yoshida M, Wada M, Kobori M, Itoh R, Iwaguro H, Eguchi M, Iwami Y, Tanaka R, Nakagawa Y, Sugimoto A, Ninomiya S, Hayashi S, Kato S, Asahara T. Estrogen-mediated endothelial progenitor cell biology and kinetics for physiological postnatal vasculogenesis. Circ Res. 2007;101:598–606.PubMedCrossRef
102.
go back to reference Zhang WB, Cheng MJ, Huang YT, Jiang W, Cong Q, Zheng YF, Xu CJ. A study in vitro on differentiation of bone marrow mesenchymal stem cells into endometrial epithelial cells in mice. Eur J Obstet Gynecol Reprod Biol. 2012;160:185–90.PubMedCrossRef Zhang WB, Cheng MJ, Huang YT, Jiang W, Cong Q, Zheng YF, Xu CJ. A study in vitro on differentiation of bone marrow mesenchymal stem cells into endometrial epithelial cells in mice. Eur J Obstet Gynecol Reprod Biol. 2012;160:185–90.PubMedCrossRef
103.
go back to reference Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282:1145–7.PubMedCrossRef Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282:1145–7.PubMedCrossRef
104.
go back to reference Murry CE, Keller G. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell. 2008;132:661–80.PubMedCrossRef Murry CE, Keller G. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell. 2008;132:661–80.PubMedCrossRef
105.
go back to reference Trounson A. The production and directed differentiation of human embryonic stem cells. Endocr Rev. 2006;27:208–19.PubMedCrossRef Trounson A. The production and directed differentiation of human embryonic stem cells. Endocr Rev. 2006;27:208–19.PubMedCrossRef
106.
go back to reference Schwartz SD, Hubschman JP, Heilwell G, Franco-Cardenas V, Pan CK, Ostrick RM, Mickunas E, Gay R, Klimanskaya I, Lanza R. Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet. 2012;379:713–20.PubMedCrossRef Schwartz SD, Hubschman JP, Heilwell G, Franco-Cardenas V, Pan CK, Ostrick RM, Mickunas E, Gay R, Klimanskaya I, Lanza R. Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet. 2012;379:713–20.PubMedCrossRef
107.
go back to reference Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131:861–72.PubMedCrossRef Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131:861–72.PubMedCrossRef
108.
go back to reference Ye L, Mayberry R, Lo CY, Britt KL, Stanley EG, Elefanty AG, Gargett CE. Generation of human female reproductive tract epithelium from human embryonic stem cells. PLoS One. 2011;6:e21136.PubMedCrossRef Ye L, Mayberry R, Lo CY, Britt KL, Stanley EG, Elefanty AG, Gargett CE. Generation of human female reproductive tract epithelium from human embryonic stem cells. PLoS One. 2011;6:e21136.PubMedCrossRef
109.
go back to reference Ye L, Evans J, Gargett CE. Lim1/LIM1 is expressed in developing and adult mouse and human endometrium. Histochem Cell Biol. 2012;137:527–36.PubMedCrossRef Ye L, Evans J, Gargett CE. Lim1/LIM1 is expressed in developing and adult mouse and human endometrium. Histochem Cell Biol. 2012;137:527–36.PubMedCrossRef
111.
go back to reference Kao AP, Wang KH, Chang CC, Lee JN, Long CY, Chen HS, Tsai CF, Hsieh TH, Tsai EM. Comparative study of human eutopic and ectopic endometrial mesenchymal stem cells and the development of an in vivo endometriotic invasion model. Fertil Steril. 2011;95:1308–15.PubMedCrossRef Kao AP, Wang KH, Chang CC, Lee JN, Long CY, Chen HS, Tsai CF, Hsieh TH, Tsai EM. Comparative study of human eutopic and ectopic endometrial mesenchymal stem cells and the development of an in vivo endometriotic invasion model. Fertil Steril. 2011;95:1308–15.PubMedCrossRef
112.
go back to reference Chan RW, Ng EH, Yeung WS. Identification of cells with colony-forming activity, self-renewal capacity, and multipotency in ovarian endometriosis. Am J Pathol. 2011;178:2832–44.PubMedCrossRef Chan RW, Ng EH, Yeung WS. Identification of cells with colony-forming activity, self-renewal capacity, and multipotency in ovarian endometriosis. Am J Pathol. 2011;178:2832–44.PubMedCrossRef
113.
go back to reference Fazleabas AT, Brudney A, Gurates B, Chai D, Bulun S. A modified baboon model for endometriosis. Ann N Y Acad Sci. 2002;955:308–17.PubMedCrossRef Fazleabas AT, Brudney A, Gurates B, Chai D, Bulun S. A modified baboon model for endometriosis. Ann N Y Acad Sci. 2002;955:308–17.PubMedCrossRef
114.
go back to reference Bokor A, Debrock S, Drijkoningen M, Goossens W, Fulop V, D’Hooghe T. Quantity and quality of retrograde menstruation: a case control study. Reprod Biol Endocrinol. 2009;7:123.PubMedCrossRef Bokor A, Debrock S, Drijkoningen M, Goossens W, Fulop V, D’Hooghe T. Quantity and quality of retrograde menstruation: a case control study. Reprod Biol Endocrinol. 2009;7:123.PubMedCrossRef
115.
go back to reference Gargett CE, Tan C, Masuda H, Anwar SS, Ciurej I, Rao J, Weston G. Identification of endometrial stem cells in menstrual blood and peritoneal fluid of women with endometriosis. 11th World Congress on Endometriosis. 2011; Sept 4–7:P3-334-(p 198). Gargett CE, Tan C, Masuda H, Anwar SS, Ciurej I, Rao J, Weston G. Identification of endometrial stem cells in menstrual blood and peritoneal fluid of women with endometriosis. 11th World Congress on Endometriosis. 2011; Sept 4–7:P3-334-(p 198).
116.
go back to reference Pardal R, Clarke MF, Morrison SJ. Applying the principles of stem-cell biology to cancer. Nature Rev Cancer. 2003;3:895–902.CrossRef Pardal R, Clarke MF, Morrison SJ. Applying the principles of stem-cell biology to cancer. Nature Rev Cancer. 2003;3:895–902.CrossRef
117.
go back to reference Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer. 2008;8:755–68.PubMedCrossRef Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer. 2008;8:755–68.PubMedCrossRef
118.
go back to reference Jordan CT. Searching for leukemia stem cells - Not yet the end of the road? Cancer Cell. 2006;10:253–4.PubMedCrossRef Jordan CT. Searching for leukemia stem cells - Not yet the end of the road? Cancer Cell. 2006;10:253–4.PubMedCrossRef
119.
go back to reference Nguyen LV, Vanner R, Dirks P, Eaves CJ. Cancer stem cells: an evolving concept. Nat Rev Cancer. 2012;12:133–43.PubMed Nguyen LV, Vanner R, Dirks P, Eaves CJ. Cancer stem cells: an evolving concept. Nat Rev Cancer. 2012;12:133–43.PubMed
120.
go back to reference Di Cristofano A, Ellenson LH. Endometrial carcinoma. Ann Rev Pathol Mech Dis. 2007;2:57–85.CrossRef Di Cristofano A, Ellenson LH. Endometrial carcinoma. Ann Rev Pathol Mech Dis. 2007;2:57–85.CrossRef
121.
go back to reference Friel AM, Sergent PA, Patnaude C, Szotek PP, Oliva E, Scadden DT, Seiden MV, Foster R, Rueda BR. Functional analyses of the cancer stem cell-like properties of human endometrial tumor initiating cells. Cell Cycle. 2008;7:242–9.PubMedCrossRef Friel AM, Sergent PA, Patnaude C, Szotek PP, Oliva E, Scadden DT, Seiden MV, Foster R, Rueda BR. Functional analyses of the cancer stem cell-like properties of human endometrial tumor initiating cells. Cell Cycle. 2008;7:242–9.PubMedCrossRef
122.
go back to reference Hubbard SA, Friel AM, Kumar B, Zhang L, Rueda BR, Gargett CE. Evidence for cancer stem cells in human endometrial carcinoma. Cancer Res. 2009;69:8241–8.PubMedCrossRef Hubbard SA, Friel AM, Kumar B, Zhang L, Rueda BR, Gargett CE. Evidence for cancer stem cells in human endometrial carcinoma. Cancer Res. 2009;69:8241–8.PubMedCrossRef
123.
go back to reference Kato K, Takao T, Kuboyama A, Tanaka Y, Ohgami T, Yamaguchi S, Adachi S, Yoneda T, Ueoka Y, Kato K, Hayashi S, Asanoma K, Wake N. Endometrial cancer side-population cells show prominent migration and have a potential to differentiate into the mesenchymal cell lineage. Am J Pathol. 2010;176:381–92.PubMedCrossRef Kato K, Takao T, Kuboyama A, Tanaka Y, Ohgami T, Yamaguchi S, Adachi S, Yoneda T, Ueoka Y, Kato K, Hayashi S, Asanoma K, Wake N. Endometrial cancer side-population cells show prominent migration and have a potential to differentiate into the mesenchymal cell lineage. Am J Pathol. 2010;176:381–92.PubMedCrossRef
124.
go back to reference Rutella S, Bonanno G, Procoli A, Mariotti A, Corallo M, Prisco MG, Eramo A, Napoletano C, Gallo D, Perillo A, Nuti M, Pierelli L, Testa U, Scambia G, Ferrandina G. Cells with characteristics of cancer stem/progenitor cells express the CD133 antigen in human endometrial tumors. Clin Cancer Res. 2009;15:4299–311.PubMedCrossRef Rutella S, Bonanno G, Procoli A, Mariotti A, Corallo M, Prisco MG, Eramo A, Napoletano C, Gallo D, Perillo A, Nuti M, Pierelli L, Testa U, Scambia G, Ferrandina G. Cells with characteristics of cancer stem/progenitor cells express the CD133 antigen in human endometrial tumors. Clin Cancer Res. 2009;15:4299–311.PubMedCrossRef
125.
go back to reference Friel AM, Zhang L, Curley MD, Therrien VA, Sergent PA, Belden SE, Borger DR, Mohapatra G, Zukerberg LR, Foster R, Rueda BR. Epigenetic regulation of CD133 and tumorigenicity of CD133 positive and negative endometrial cancer cells. Reprod Biol Endocrinol. 2010;8:147.PubMedCrossRef Friel AM, Zhang L, Curley MD, Therrien VA, Sergent PA, Belden SE, Borger DR, Mohapatra G, Zukerberg LR, Foster R, Rueda BR. Epigenetic regulation of CD133 and tumorigenicity of CD133 positive and negative endometrial cancer cells. Reprod Biol Endocrinol. 2010;8:147.PubMedCrossRef
127.
go back to reference Hubbard SA, Gargett CE. A cancer stem cell origin for human endometrial cancer? Reproduction. 2010;140:23–32.PubMedCrossRef Hubbard SA, Gargett CE. A cancer stem cell origin for human endometrial cancer? Reproduction. 2010;140:23–32.PubMedCrossRef
128.
go back to reference Gargett CE, Healy DL. Generating receptive endometrium in Asherman’s syndrome. J Hum Reprod Sci. 2011;4:49–52.PubMed Gargett CE, Healy DL. Generating receptive endometrium in Asherman’s syndrome. J Hum Reprod Sci. 2011;4:49–52.PubMed
129.
go back to reference Yu D, Wong Y-M, Cheong Y, Xia E, Li T-C. Asherman’s syndrome - one century later. Fert Steril. 2008;89:759–79.CrossRef Yu D, Wong Y-M, Cheong Y, Xia E, Li T-C. Asherman’s syndrome - one century later. Fert Steril. 2008;89:759–79.CrossRef
130.
go back to reference Panayiotides I, Weyers S, Bosteels J, Van Herendael B. Intrauterine adhesions (IUA): has there been progress in understanding and treatment over the last 20 years? Gynecol Surg. 2009;6:197–211.CrossRef Panayiotides I, Weyers S, Bosteels J, Van Herendael B. Intrauterine adhesions (IUA): has there been progress in understanding and treatment over the last 20 years? Gynecol Surg. 2009;6:197–211.CrossRef
131.
go back to reference Lo ST, Ramsay P, Pierson R, Manconi F, Munro MG, Fraser IS. Endometrial thickness measured by ultrasound scan in women with uterine outlet obstruction due to intrauterine or upper cervical adhesions. Hum Reprod. 2008;23:306–9.PubMedCrossRef Lo ST, Ramsay P, Pierson R, Manconi F, Munro MG, Fraser IS. Endometrial thickness measured by ultrasound scan in women with uterine outlet obstruction due to intrauterine or upper cervical adhesions. Hum Reprod. 2008;23:306–9.PubMedCrossRef
132.
go back to reference Schenker JG, Margalioth EJ. Intrauterine adhesions: an updated appraisal. Fertil Steril. 1982;37:593–610.PubMed Schenker JG, Margalioth EJ. Intrauterine adhesions: an updated appraisal. Fertil Steril. 1982;37:593–610.PubMed
133.
go back to reference Nagori CB, Panchal SY, Patel H. Endometrial regeneration using autologous adult stem cells followed by conception by in vitro fertilization in a patient of severe Asherman’s syndrome. J Hum Reprod Sci. 2011;4:43–8.PubMedCrossRef Nagori CB, Panchal SY, Patel H. Endometrial regeneration using autologous adult stem cells followed by conception by in vitro fertilization in a patient of severe Asherman’s syndrome. J Hum Reprod Sci. 2011;4:43–8.PubMedCrossRef
134.
go back to reference Alawadhi FA, Taylor HS. Treatment with Bone Marrow Derived Stem Cells (BMDSCs) improves fertility in a murine model of asherman’s syndrome. Reprod Sci. 2012;19:O-136. Alawadhi FA, Taylor HS. Treatment with Bone Marrow Derived Stem Cells (BMDSCs) improves fertility in a murine model of asherman’s syndrome. Reprod Sci. 2012;19:O-136.
135.
go back to reference Caplan AI. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol. 2007;213:341–7.PubMedCrossRef Caplan AI. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol. 2007;213:341–7.PubMedCrossRef
136.
go back to reference Prockop DJ. Repair of tissues by adult stem/progenitor cells (MSCs): controversies, myths, and changing paradigms. Mol Ther. 2009;17:939–46.PubMedCrossRef Prockop DJ. Repair of tissues by adult stem/progenitor cells (MSCs): controversies, myths, and changing paradigms. Mol Ther. 2009;17:939–46.PubMedCrossRef
137.
go back to reference Massasa EE, Taylor HS. Use of endometrial stem cells in regenerative medicine. Regen Med. 2012;7:133–5.PubMedCrossRef Massasa EE, Taylor HS. Use of endometrial stem cells in regenerative medicine. Regen Med. 2012;7:133–5.PubMedCrossRef
138.
go back to reference Zhong Z, Patel AN, Ichim TE, Riordan NH, Wang H, Min WP, Woods EJ, Reid M, Mansilla E, Marin GH, Drago H, Murphy MP, Minev B. Feasibility investigation of allogeneic endometrial regenerative cells. J Transl Med. 2009;7:15.PubMedCrossRef Zhong Z, Patel AN, Ichim TE, Riordan NH, Wang H, Min WP, Woods EJ, Reid M, Mansilla E, Marin GH, Drago H, Murphy MP, Minev B. Feasibility investigation of allogeneic endometrial regenerative cells. J Transl Med. 2009;7:15.PubMedCrossRef
141.
go back to reference Schmidt D, Mol A, Neuenschwander S, Breymann C, Gossi M, Zund G, Turina M, Hoerstrup SP. Living patches engineered from human umbilical cord derived fibroblasts and endothelial progenitor cells. Eur J Cardiothorac Surg. 2005;27:795–800.PubMedCrossRef Schmidt D, Mol A, Neuenschwander S, Breymann C, Gossi M, Zund G, Turina M, Hoerstrup SP. Living patches engineered from human umbilical cord derived fibroblasts and endothelial progenitor cells. Eur J Cardiothorac Surg. 2005;27:795–800.PubMedCrossRef
142.
go back to reference Gargett CE. Identification and characterisation of human endometrial stem/progenitor cells. Aust N Z J Obstet Gynaecol. 2006;46:250–3.PubMedCrossRef Gargett CE. Identification and characterisation of human endometrial stem/progenitor cells. Aust N Z J Obstet Gynaecol. 2006;46:250–3.PubMedCrossRef
143.
go back to reference Smith FJ, Holman CD, Moorin RE, Tsokos N. Lifetime risk of undergoing surgery for pelvic organ prolapse. Obstet Gynecol. 2010;116:1096–100.PubMedCrossRef Smith FJ, Holman CD, Moorin RE, Tsokos N. Lifetime risk of undergoing surgery for pelvic organ prolapse. Obstet Gynecol. 2010;116:1096–100.PubMedCrossRef
Metadata
Title
Endometrial regeneration and endometrial stem/progenitor cells
Authors
Caroline E. Gargett
Hong P. T. Nguyen
Louie Ye
Publication date
01-12-2012
Publisher
Springer US
Published in
Reviews in Endocrine and Metabolic Disorders / Issue 4/2012
Print ISSN: 1389-9155
Electronic ISSN: 1573-2606
DOI
https://doi.org/10.1007/s11154-012-9221-9

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