Endometrial regeneration and endometrial stem/progenitor cells

Reviews in Endocrine and Metabolic Disorders

Volumn 13, Issue 4, 2012, Pages 235-251

  Gargett, Caroline E ^a,b   Nguyen, Hong P T ^a,b,c   Ye, Louie ^a,b  

^a HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adult stem cells; Endometrial regeneration; Endometrium; Epithelial progenitor cells; Mesenchymal stem cells

Indexed keywords

ESTROGEN;

ADULT STEM CELL; ARTICLE; BONE MARROW; CANCER STEM CELL; CELL THERAPY; CLONOGENESIS; DISEASE ASSOCIATION; EMBRYONIC STEM CELL; ENDOMETRIAL REGENERATION; ENDOMETRIAL STEM CELL; ENDOMETRIOSIS; GYNECOLOGIC DISEASE; HUMAN; MENSTRUAL CYCLE; MESENCHYMAL STEM CELL; MESENCHYMAL STROMA CELL; NONHUMAN; POSTMENOPAUSE; REGENERATION; STEM CELL; TISSUE REGENERATION;

ANIMALS; ENDOMETRIUM; FEMALE; HUMANS; REGENERATION; STEM CELL TRANSPLANTATION; STEM CELLS; UTERINE DISEASES;

EID: 84874661812     PISSN: 13899155     EISSN: 15732606     Source Type: Journal    
DOI: 10.1007/s11154-012-9221-9     Document Type: Article

References (144)

1. Gargett CE. Uterine stem cells: what is the evidence? Hum Reprod Update. 2007;13:87-101. (Pubitemid 44932827)
2. Jabbour HN, Kelly RW, Fraser HM, Critchley HOD. Endocrine regulation of menstruation. Endocr Rev. 2006;27:17-46. (Pubitemid 43228237)
3. McLennan CE, Rydell AH. Extent of endometrial shedding during normal menstruation. Obstet Gynecol. 1965;26:605-21.
4. Padykula HA. Regeneration of the primate uterus: the role of stem cells. Ann N Y Acad Sci. 1991;622:47-56.
5. Spencer TE, Hayashi K, Hu J, Carpenter KD. Comparative developmental biology of the mammalian uterus. Curr Top Dev Biol. 2005;68:85-122. (Pubitemid 43631285)
6. Ferenczy A, Bergeron C. Histology of the human endometrium: from birthe to senescence. Ann N Y Acad Sci. 1991;622:6-27.
7. 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. (Pubitemid 127780758)
8. 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. (Pubitemid 35291763)
9. 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. (Pubitemid 23136596)
10. 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. (Pubitemid 44118976)
11. 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.
12. 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.
13. Henriet P, Gaide Chevronnay HP, Marbaix E. The endocrine and paracrine control of menstruation. Mol Cell Endocrinol. 2011.
14. Maybin J, Critchley H. Repair and regeneration of the human endometrium. Expert Rev Obstet Gynecol. 2009;4:283-98.
15. 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. 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.
17. 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. (Pubitemid 47481555)
18. 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.
19. Garry R, Hart R, Karthigasu KA, Burke C. Structural changes in endometrial basal glands during menstruation. BJOG. 2010;117:1175-85.
20. 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. (Pubitemid 351696761)
21. 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.
22. Ferenczy A, Bertrand G, Gelfand MM. Proliferation kinetics of human endometrium during the normal menstrual cycle. Am J Obstet Gynecol. 1979;133:859-67. (Pubitemid 9141387)
23. 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. (Pubitemid 19149774)
24. 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. (Pubitemid 36740562)
25. Gargett CE, Rogers PAW. Human endometrial angiogenesis. Reproduction. 2001;121:181-6. (Pubitemid 32175540)
26. 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. (Pubitemid 40417399)
27. Couse JF, Korach KS. Estrogen receptor null mice: what have we learned and where will they lead us? Endocr Rev. 1999;20:358-417. (Pubitemid 30654784)
28. 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. (Pubitemid 27270720)
29. 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. (Pubitemid 41594448)
30. 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.
31. 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. 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. (Pubitemid 39577924)
33. 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. (Pubitemid 38327705)
34. 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. (Pubitemid 32323030)
35. 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. (Pubitemid 32323031)
36. -/- mice. Proc Natl Acad Sci U S A. 2006;103:18350-5. (Pubitemid 44872762)
37. Salamonsen LA. Tissue injury and repair in the female human reproductive tract. Reproduction. 2003;125:301-11. (Pubitemid 36395578)
38. 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. (Pubitemid 351709405)
39. 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.
40. Gargett CE, Masuda H. Adult stem cells in the endometrium. Mol Hum Reprod. 2010;16:818-34.
41. 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.
42. Du HL, Taylor HS. Stem cells and reproduction. Curr Opin Obstet Gynecol. 2010;22:235-41.
43. Chan RWS, Schwab KE, Gargett CE. Clonogenicity of human endometrial epithelial and stromal cells. Biol Reprod. 2004;70:1738-50. (Pubitemid 38715630)
44. 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. (Pubitemid 41396537)
45. 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.
46. 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. (Pubitemid 44269669)
47. Morrison SJ, Shah NM, Anderson DJ. Regulatory mechanisms in stem cell biology. Cell. 1997;88:287-98. (Pubitemid 27131370)
48. 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. (Pubitemid 351168784)
49. 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.
50. 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.
51. 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. (Pubitemid 351578161)
52. 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. (Pubitemid 28011033)
53. Challen GA, Little MH. A side order of stem cells: the SP phenotype. Stem Cells. 2006;24:3-12.
54. 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.
55. 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.
56. 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. (Pubitemid 47062787)
57. 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.
58. 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.
59. 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.
60. Gargett CE, Ye L. Endometrial reconstruction from stem cells. Fertil Steril. 2012. doi: 10.1016/j.fertnstert.2012.05.004:.
61. 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.
62. 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.
63. Caplan AI. Why are MSCs therapeutic? New data: new insight. J Pathol. 2009;217:318-24.
64. Masuda H, Anwar SS, Buhring HJ, Rao JR, Gargett CE. A novel marker of human endometrial mesenchymal stem-like cells. Cell Transplant. 2012. doi: 10.3727/096368911X637362:.
65. 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.
66. 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. (Pubitemid 29131269)
67. 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. (Pubitemid 46717542)
68. 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.
69. 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. (Pubitemid 351167679)
70. 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. (Pubitemid 351717333)
71. 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. 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.
73. Sasson IE, Taylor HS. Stem cells and the pathogenesis of endometriosis. Ann N Y Acad Sci. 2008;1127:106-15. (Pubitemid 351565719)
74. 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. (Pubitemid 33772941)
75. null immunodeficient mice. Proc Natl Acad Sci U S A. 2007;104:1925-30. (Pubitemid 46239880)
76. 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.
77. 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. (Pubitemid 19213506)
78. Chan RW, Gargett CE. Identification of label-retaining cells in mouse endometrium. Stem Cells. 2006;24:1529-38. (Pubitemid 44464670)
79. Chan RWS, Kaitu'u-Lino T, Gargett CE. Role of label-retaining cells in estrogen-induced endometrial regeneration. Reprod Sci. 2012;19:102-14.
80. Martin L, Finn CA. Interactions of oestradiol and progestins in the mouse uterus. J Endocrinol. 1970;48:109-15.
81. 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.
82. Walter LM, Rogers PAW, Girling JE. The role of progesterone in endometrial angiogenesis in pregnant and ovariectomised mice. Reproduction. 2005;129:765-77. (Pubitemid 40872827)
83. Brasted M, White CA, Kennedy TG, Salamonsen LA. Mimicking the events of menstruation in the murine uterus. Biol Reprod. 2003;69:1273-80. (Pubitemid 37173862)
84. 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. (Pubitemid 44942665)
85. 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. (Pubitemid 46684892)
86. Gargett CE, Chan RW, Schwab KE. Endometrial stem cells. Curr Opin Obstet Gynecol. 2007;19:377-83. (Pubitemid 47067103)
87. 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. 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.
89. 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. (Pubitemid 38084701)
90. He Q, Wan C, Li G. Concise review: multipotent mesenchymal stromal cells in blood. Stem Cells. 2007;25:69-77. (Pubitemid 46052976)
91. 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.
92. Korbling M, Estrov Z. Adult stem cells for tissue repair - A new therapeutic concept? N Engl J Med. 2003;349:570-82. (Pubitemid 36951370)
93. 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. (Pubitemid 350127866)
94. Taylor HS. Endometrial cells derived from donor stem cells in bone marrow transplant recipients. JAMA. 2004;292:81-5. (Pubitemid 38923797)
95. 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. (Pubitemid 351767317)
96. 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.
97. 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.
98. 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.
99. Du H, Taylor HS. Contribution of bone marrow-derived stem cells to endometrium and endometriosis. Stem Cells. 2007;25:2082-6. (Pubitemid 47258186)
100. Du H, Taylor HS. Stem cells in female reproduction. Reprod Sci. 2010;16:126-39.
101. 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. (Pubitemid 351325877)
102. 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.
103. 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. (Pubitemid 28516247)
104. Murry CE, Keller G. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell. 2008;132:661-80. (Pubitemid 351260059)
105. Trounson A. The production and directed differentiation of human embryonic stem cells. Endocr Rev. 2006;27:208-19.
106. 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.
107. 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. (Pubitemid 350138099)
108. 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.
109. 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.
110. Giudice LC, Kao LC. Endometriosis. Lancet. 2004;364:1789-99. (Pubitemid 39488065)
111. 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.
112. 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.
113. 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. (Pubitemid 34271088)
114. 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.
115. 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. Pardal R, Clarke MF, Morrison SJ. Applying the principles of stem-cell biology to cancer. Nature Rev Cancer. 2003;3:895-902. (Pubitemid 37500174)
117. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer. 2008;8:755-68.
118. Jordan CT. Searching for leukemia stem cells - Not yet the end of the road? Cancer Cell. 2006;10:253-4. (Pubitemid 44512195)
119. Nguyen LV, Vanner R, Dirks P, Eaves CJ. Cancer stem cells: an evolving concept. Nat Rev Cancer. 2012;12:133-43.
120. Di Cristofano A, Ellenson LH. Endometrial carcinoma. Ann Rev Pathol Mech Dis. 2007;2:57-85. (Pubitemid 46448060)
121. 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. (Pubitemid 351366525)
122. 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.
123. 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.
124. 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.
125. 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.
126. Mather JP. Cancer stem cells: in vitro models. Stem Cells. 2012;30:95-9.
127. Hubbard SA, Gargett CE. A cancer stem cell origin for human endometrial cancer? Reproduction. 2010;140:23-32.
128. Gargett CE, Healy DL. Generating receptive endometrium in Asherman's syndrome. J Hum Reprod Sci. 2011;4:49-52.
129. Yu D, Wong Y-M, Cheong Y, Xia E, Li T-C. Asherman's syndrome - one century later. Fert Steril. 2008;89:759-79. (Pubitemid 351491241)
130. 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.
131. 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. (Pubitemid 351651262)
132. Schenker JG, Margalioth EJ. Intrauterine adhesions: an updated appraisal. Fertil Steril. 1982;37:593-610. (Pubitemid 12161096)
133. 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.
134. 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. Caplan AI. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol. 2007;213:341-7. (Pubitemid 47509711)
136. Prockop DJ. Repair of tissues by adult stem/progenitor cells (MSCs): controversies, myths, and changing paradigms. Mol Ther. 2009;17:939-46.
137. Massasa EE, Taylor HS. Use of endometrial stem cells in regenerative medicine. Regen Med. 2012;7:133-5.
138. 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.
139. Medistem. Medistem and ERCell Initiate Phase II RECOVER-ERC Heart Failure Trial. http://medisteminccom/2012/medistem-and-ercell-initiate-phase-ii- recover-erc-heart-failure-trial/. 2012.
140. Atala A. Engineering organs. Curr Opin Biotechnol. 2009;20:575-92.
141. 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. (Pubitemid 40590049)
142. Gargett CE. Identification and characterisation of human endometrial stem/progenitor cells. Aust N Z J Obstet Gynaecol. 2006;46:250-3. (Pubitemid 44056736)
143. Smith FJ, Holman CD, Moorin RE, Tsokos N. Lifetime risk of undergoing surgery for pelvic organ prolapse. Obstet Gynecol. 2010;116:1096-100.
144. FDA Public Health Notification. Urogynecologic surgical mesh: update on the safety and effectiveness of transvaginal placement for pelvic organ prolapse. http://wwwfdagov/downloads/MedicalDevices/Safety/AlertsandNotices/ UCM262760.pdf. 2011.