Stem/progenitor cells and the regeneration potentials in the human uterus

Reproductive Medicine and Biology

Volumn 9, Issue 1, 2010, Pages 9-16

  Maruyama, Tetsuo ^a  

^a KEIO UNIVERSITY   (Japan)

Author keywords

Endometrium; Myometrium; Regeneration; Side population; Stem cell

Indexed keywords

ANGIOGENESIS; CELL POPULATION; ENDOMETRIOSIS; ENDOMETRIUM; ENDOMETRIUM CELL; ENDOTHELIUM CELL; HUMAN; MENSTRUATION; MYOMETRIUM; NONHUMAN; PRIORITY JOURNAL; REVIEW; SMOOTH MUSCLE FIBER; STEM CELL; TISSUE REGENERATION; UTERUS REGENERATION;

EID: 77649234945     PISSN: 14455781     EISSN: 14470578     Source Type: Journal    
DOI: 10.1007/s12522-009-0032-y     Document Type: Review

References (59)

1. R Passier LW van Laake CL Mummery 2008 Stem-cell-based therapy and lessons from the heart Nature 453 322 329 10.1038/nature07040 1:CAS:528:DC%2BD1cXlvV2qtbY%3D 18480813 (Pubitemid 351693138)
2. J Yu JA Thomson 2008 Pluripotent stem cell lines Genes Dev 22 1987 1997 10.1101/gad.1689808 1:CAS:528:DC%2BD1cXpslKqsLY%3D 18676805
3. CE Gargett 2007 Uterine stem cells: what is the evidence? Hum Reprod Update 13 87 101 10.1093/humupd/dml045 1:STN:280:DC%2BD28jitVGjtA%3D%3D 16960017 (Pubitemid 44932827)
4. M Ono T Maruyama Y Yoshimura 2008 Regeneration and adult stem cells in the human female reproductive tract Stem Cells Cloning Adv Appl 1 23 29 1:CAS:528:DC%2BD1MXhtFejs70%3D
5. T Maruyama Y Yoshimura 2008 Molecular and cellular mechanisms for differentiation and regeneration of the uterine endometrium Endocr J 55 795 810 10.1507/endocrj.K08E-067 1:CAS:528:DC%2BD1MXhtVGgu7s%3D 18580040
6. HA Padykula LG Coles WC Okulicz SI Rapaport JA McCracken NW King Jr, et al. 1989 The basalis of the primate endometrium: a bifunctional germinal compartment Biol Reprod 40 681 690 10.1095/biolreprod40.3.681 1:STN:280:DyaL1MzjsF2jsQ%3D%3D 2758097 (Pubitemid 19149774)
7. RW Chan KE Schwab CE Gargett 2004 Clonogenicity of human endometrial epithelial and stromal cells Biol Reprod 70 1738 1750 10.1095/biolreprod.103. 024109 1:CAS:528:DC%2BD2cXktlOmt7o%3D 14766732 (Pubitemid 38715630)
8. HN Jabbour RW Kelly HM Fraser HO Critchley 2006 Endocrine regulation of menstruation Endocr Rev 27 17 46 10.1210/er.2004-0021 1:CAS:528: DC%2BD28XitFSit7Y%3D 16160098 (Pubitemid 43228237)
9. Strauss III JF, Lessey BA: The structure, function, and evaluation of the female reproductive tract. In: Strauss III JF, Barbieri RL, editors. Yen and Jaffe's Reproductive Endocrinology. Physiology, Pathophysiology, and Clinical Management, 5th ed. Amsterdam: Elsevier Saunders; 2004. p. 255-305.
10. J Donnez P Smoes S Gillerot F Casanas-Roux M Nisolle 1998 Vascular endothelial growth factor (VEGF) in endometriosis Hum Reprod 13 1686 1690 10.1093/humrep/13.6.1686 1:CAS:528:DyaK1cXkslOlu7w%3D 9688413 (Pubitemid 28310515)
11. A Fujishita A Hasuo KN Khan H Masuzaki H Nakashima T Ishimaru 1999 Immunohistochemical study of angiogenic factors in endometrium and endometriosis Gynecol Obstet Invest 48 Suppl 1 36 44 10.1159/000052867 1:CAS:528: DyaK1MXnsVemsLo%3D 10559663
12. LC Giudice LC Kao 2004 Endometriosis Lancet 364 1789 1799 10.1016/S0140-6736(04)17403-5 15541453 (Pubitemid 39488065)
13. SE Bulun 2009 Endometriosis N Engl J Med 360 268 279 10.1056/ NEJMra0804690 1:CAS:528:DC%2BD1MXnsFGhtA%3D%3D 19144942
14. NM Zamah MG Dodson LC Stephens VC Buttram Jr PK Besch RH Kaufman 1984 Transplantation of normal and ectopic human endometrial tissue into athymic nude mice Am J Obstet Gynecol 149 591 597 1:STN:280:DyaL2c3ltl2itw%3D%3D 6742039
15. A Bergqvist S Jeppsson S Kullander O Ljungberg 1985 Human uterine endometrium and endometriotic tissue transplanted into nude mice. Morphologic effects of various steroid hormones Am J Pathol 121 337 341 1:CAS:528: DyaL28XhsFehtg%3D%3D 4061568
16. RJ Zaino PG Satyaswaroop R Mortel 1985 Histologic response of normal human endometrium to steroid hormones in athymic mice Hum Pathol 16 867 872 10.1016/S0046-8177(85)80126-X 1:STN:280:DyaL2M3oslWltQ%3D%3D 3161816 (Pubitemid 15238268)
17. D Aoki Y Katsuki A Shimizu C Kakinuma S Nozawa 1994 Successful heterotransplantation of human endometrium in SCID mice Obstet Gynecol 83 220 228 1:STN:280:DyaK2c7hvFGjsA%3D%3D 8290184
18. KL Bruner LM Matrisian WH Rodgers F Gorstein KG Osteen 1997 Suppression of matrix metalloproteinases inhibits establishment of ectopic lesions by human endometrium in nude mice J Clin Invest 99 2851 2857 10.1172/JCI119478 1:CAS:528:DyaK2sXktV2qtb8%3D 9185507
19. JT Awwad RA Sayegh XJ Tao T Hassan ST Awwad K Isaacson 1999 The SCID mouse: an experimental model for endometriosis Hum Reprod 14 3107 3111 10.1093/humrep/14.12.3107 1:STN:280:DC%2BD3c%2FmvFygsw%3D%3D 10601104
20. S Tabibzadeh S Miller WC Dodson PG Satyaswaroop 1999 An experimental model for the endometriosis in athymic mice Front Biosci 4 C4 C9 10.2741/tabibzad 1:STN:280:DyaK1Mzit1elug%3D%3D 10393127
21. R Grümmer F Schwarzer K Bainczyk H Hess-Stumpp PA Regidor AE Schindler, et al. 2001 Peritoneal endometriosis: validation of an in vivo model Hum Reprod 16 1736 1743 10.1093/humrep/16.8.1736 11473975
22. LH Greenberg OD Slayden 2004 Human endometriotic xenografts in immunodeficient RAG-2/gamma(c)KO mice Am J Obstet Gynecol 190 1788 1795 10.1016/j.ajog.2004.02.047 1:CAS:528:DC%2BD2cXmtlSnsbs%3D 15284801 (Pubitemid 39006219)
23. M Fortin M Lepine Y Merlen I Thibeault C Rancourt D Gosselin, et al. 2004 Quantitative assessment of human endometriotic tissue maintenance and regression in a noninvasive mouse model of endometriosis Mol Ther 9 540 547 10.1016/j.ymthe.2003.12.012 1:CAS:528:DC%2BD2cXjtVChu70%3D 15093184 (Pubitemid 38578804)
24. R Matsuura-Sawada T Murakami Y Ozawa H Nabeshima J Akahira Y Sato, et al. 2005 Reproduction of menstrual changes in transplanted human endometrial tissue in immunodeficient mice Hum Reprod 20 1477 1484 10.1093/humrep/deh783 15734760 (Pubitemid 40852236)
25. null immunodeficient mice Proc Natl Acad Sci U S A 104 1925 1930 10.1073/pnas.0604310104 1:CAS:528:DC%2BD2sXitVejs7k%3D 17261813 (Pubitemid 46239880)
26. R Gazvani A Templeton 2002 Peritoneal environment, cytokines and angiogenesis in the pathophysiology of endometriosis Reproduction 123 217 226 10.1530/rep.0.1230217 1:CAS:528:DC%2BD38XhsFChsbg%3D 11866688
27. J Fujimoto H Sakaguchi R Hirose H Wen T Tamaya 1999 Angiogenesis in endometriosis and angiogenic factors Gynecol Obstet Invest 48 Suppl 1 14 20 10.1159/000052864 1:CAS:528:DyaK1MXnsVemsL8%3D 10559660
28. RN Taylor DI Lebovic MD Mueller 2002 Angiogenic factors in endometriosis Ann N Y Acad Sci 955 89 100 10.1111/j.1749-6632.2002.tb02769.x 1:CAS:528:DC%2BD38XjtFOks7g%3D 11949968 discussion 118, 396-406
29. M Nisolle F Casanas-Roux J Donnez 2000 Early-stage endometriosis: adhesion and growth of human menstrual endometrium in nude mice Fertil Steril 74 306 312 10.1016/S0015-0282(00)00601-4 1:STN:280:DC%2BD3cvht1Wjtw%3D%3D 10927049 (Pubitemid 30604195)
30. KL Bruner-Tran D Webster-Clair KG Osteen 2002 Experimental endometriosis: the nude mouse as a xenographic host Ann N Y Acad Sci 955 328 339 10.1111/j.1749-6632.2002.tb02793.x 11949959
31. ML Hull DS Charnock-Jones CL Chan KL Bruner-Tran KG Osteen BD Tom, et al. 2003 Antiangiogenic agents are effective inhibitors of endometriosis J Clin Endocrinol Metab 88 2889 2899 10.1210/jc.2002-021912 1:CAS:528: DC%2BD3sXkslCrtr8%3D 12788903
32. J Eggermont J Donnez F Casanas-Roux H Scholtes A Van Langendonckt 2005 Time course of pelvic endometriotic lesion revascularization in a nude mouse model Fertil Steril 84 492 499 10.1016/j.fertnstert.2005.03.034 16084895 (Pubitemid 41125275)
33. B St Croix C Rago V Velculescu G Traverso KE Romans E Montgomery, et al. 2000 Genes expressed in human tumor endothelium Science 289 1197 1202 10.1126/science.289.5482.1197 1:CAS:528:DC%2BD3cXmt1WhsLo%3D 10947988 (Pubitemid 30650733)
34. B Bussolati I Deambrosis S Russo MC Deregibus G Camussi 2003 Altered angiogenesis and survival in human tumor-derived endothelial cells FASEB J 17 1159 1161 1:CAS:528:DC%2BD3sXktl2js7w%3D 12709414
35. C Dabrosin S Gyorffy P Margetts C Ross J Gauldie 2002 Therapeutic effect of angiostatin gene transfer in a murine model of endometriosis Am J Pathol 161 909 918 1:CAS:528:DC%2BD38XnsFOisr8%3D 12213719
36. AW Nap AW Griffioen GA Dunselman JC Bouma-Ter Steege VL Thijssen JL Evers, et al. 2004 Antiangiogenesis therapy for endometriosis J Clin Endocrinol Metab 89 1089 1095 10.1210/jc.2003-031406 1:CAS:528:DC%2BD2cXisVWrtb4%3D 15001592 (Pubitemid 38368395)
37. E Seli A Arici 2003 Endometriosis: interaction of immune and endocrine systems Semin Reprod Med 21 135 144 10.1055/s-2003-41320 1:CAS:528: DC%2BD3sXms1yisbg%3D 12917783 (Pubitemid 36875689)
38. L Yao C Sgadari K Furuke ET Bloom J Teruya-Feldstein G Tosato 1999 Contribution of natural killer cells to inhibition of angiogenesis by interleukin-12 Blood 93 1612 1621 1:CAS:528:DyaK1MXhsFeru7o%3D 10029590
39. null mouse: an excellent recipient mouse model for engraftment of human cells Blood 100 3175 3182 10.1182/blood-2001-12-0207 1:CAS:528:DC%2BD38XosVSisLg%3D 12384415 (Pubitemid 35217065)
40. CH Contag MH Bachmann 2002 Advances in in vivo bioluminescence imaging of gene expression Annu Rev Biomed Eng 4 235 260 10.1146/annurev.bioeng.4.111901. 093336 1:CAS:528:DC%2BD38XoslWmsrs%3D 12117758 (Pubitemid 35217421)
41. H Masuda H Okano T Maruyama Y Yoshimura H Okano Y Matsuzaki 2008 In vivo imaging in humanized mice Curr Top Microbiol Immunol 324 179 197 10.1007/978-3-540-75647-7-12 1:CAS:528:DC%2BD1cXosFGns7w%3D 18481461
42. HA Padykula 1991 Regeneration in the primate uterus: the role of stem cells Ann N Y Acad Sci 622 47 56 10.1111/j.1749-6632.1991.tb37849.x 1:STN:280:DyaK3M3ptVGjtA%3D%3D 2064204
43. VA Prianishnikov 1978 On the concept of stem cell and a model of functional-morphological structure of the endometrium Contraception 18 213 223 10.1016/S0010-7824(78)80015-8 1:CAS:528:DyaE1MXhvFKrsg%3D%3D 569035
44. M Tanaka S Kyo T Kanaya N Yatabe M Nakamura Y Maida, et al. 2003 Evidence of the monoclonal composition of human endometrial epithelial glands and mosaic pattern of clonal distribution in luminal epithelium Am J Pathol 163 295 301 12819034
45. RM Brenner OD Slayden WH Rodgers HO Critchley R Carroll XJ Nie, et al. 2003 Immunocytochemical assessment of mitotic activity with an antibody to phosphorylated histone H3 in the macaque and human endometrium Hum Reprod 18 1185 1193 10.1093/humrep/deg255 1:CAS:528:DC%2BD3sXltFygtrY%3D 12773444 (Pubitemid 36740562)
46. R van Os LM Kamminga G de Haan 2004 Stem cell assays: something old, something new, something borrowed Stem Cells 22 1181 1190 10.1634/stemcells. 2004-0095 15579638 (Pubitemid 39636397)
47. KE Schwab RW Chan CE Gargett 2005 Putative stem cell activity of human endometrial epithelial and stromal cells during the menstrual cycle Fertil Steril 84 Suppl 2 1124 1130 10.1016/j.fertnstert.2005.02.056 1:CAS:528:DC%2BD2MXhtFOqtLbF 16210003 (Pubitemid 41396537)
48. KE Schwab CE Gargett 2007 Co-expression of two perivascular cell markers isolates mesenchymal stem-like cells from human endometrium Hum Reprod 22 2903 2911 10.1093/humrep/dem265 1:CAS:528:DC%2BD2sXht1Shu7bP 17872908 (Pubitemid 351709405)
49. MA Goodell K Brose G Paradis AS Conner RC Mulligan 1996 Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo J Exp Med 183 1797 1806 10.1084/jem.183.4.1797 1:CAS:528: DyaK28XisFemsLw%3D 8666936 (Pubitemid 26134320)
50. GA Challen MH Little 2006 A side order of stem cells: the SP phenotype Stem Cells 24 3 12 10.1634/stemcells.2005-0116 16449630
51. K Kato M Yoshimoto K Kato S Adachi A Yamayoshi T Arima, et al. 2007 Characterization of side-population cells in human normal endometrium Hum Reprod 22 1214 1223 10.1093/humrep/del514 1:CAS:528:DC%2BD2sXntlWnu7Y%3D 17283036 (Pubitemid 47062787)
52. R Dimitrov T Timeva D Kyurkchiev M Stamenova A Shterev P Kostova, et al. 2008 Characterization of clonogenic stromal cells isolated from human endometrium Reproduction 135 551 558 10.1530/REP-07-0428 1:CAS:528: DC%2BD1cXltFOnu7s%3D 18367513 (Pubitemid 351578161)
53. JY Kim S Tavare D Shibata 2005 Counting human somatic cell replications: methylation mirrors endometrial stem cell divisions Proc Natl Acad Sci USA 102 17739 17744 10.1073/pnas.0503976102 1:CAS:528:DC%2BD2MXhtlegs73L 16314580 (Pubitemid 41803567)
54. HS Taylor 2004 Endometrial cells derived from donor stem cells in bone marrow transplant recipients JAMA 292 81 85 10.1001/jama.292.1.81 1:CAS:528:DC%2BD2cXls1elsbg%3D 15238594 (Pubitemid 38923797)
55. Ramsey EM. Anatomy of the human uterus. In: Chard T, Grudzinskas JG, editors. The uterus. Cambridge: Cambridge University Press; 1994. p. 18-40.
56. O Shynlova A Oldenhof A Dorogin Q Xu J Mu N Nashman, et al. 2006 Myometrial apoptosis: activation of the caspase cascade in the pregnant rat myometrium at midgestation Biol Reprod 74 839 849 10.1095/biolreprod.105.048124 1:CAS:528:DC%2BD28Xjsl2jtbg%3D 16407500
57. M Ono T Maruyama H Masuda T Kajitani T Nagashima T Arase, et al. 2007 Side population in human uterine myometrium displays phenotypic and functional characteristics of myometrial stem cells Proc Natl Acad Sci USA 104 18700 18705 10.1073/pnas.0704472104 1:CAS:528:DC%2BD2sXhtl2msLfO 18003928 (Pubitemid 350210760)
58. NA Arango PP Szotek TF Manganaro E Oliva PK Donahoe J Teixeira 2005 Conditional deletion of beta-catenin in the mesenchyme of the developing mouse uterus results in a switch to adipogenesis in the myometrium Dev Biol 288 276 283 10.1016/j.ydbio.2005.09.045 1:CAS:528:DC%2BD2MXht1OltbzL 16256976 (Pubitemid 41713169)
59. PP Szotek HL Chang L Zhang F Preffer D Dombkowski PK Donahoe, et al. 2007 Adult mouse myometrial label-retaining cells divide in response to gonadotropin stimulation Stem Cells 25 1317 1325 10.1634/stemcells.2006-0204 1:CAS:528:DC%2BD2sXlvF2jsrY%3D 17289934 (Pubitemid 46684892)