Long-term label retaining cells localize to distinct regions within the female reproductive epithelium

Cell Cycle

Volumn 12, Issue 17, 2013, Pages 2888-2898

  Patterson, Amanda L ^a   Pru, James K ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Endocervix; Endometrial regeneration; Endometrium; Female reproductive tract; Label retaining cells; Oviduct; Stem cells; Transition zone; Uterus

Indexed keywords

BROXURIDINE; ESTROGEN RECEPTOR ALPHA; PROGESTERONE RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CELL LABELING; CELL PROLIFERATION; CELL REGENERATION; CELLULAR DISTRIBUTION; ENDOMETRIUM; ENDOMETRIUM CELL; EPITHELIZATION; FEMALE; LABEL RETAINING CELL; MOUSE; NONHUMAN; OVIDUCT; PROTEIN EXPRESSION; STEM CELL; TRANSGENIC MOUSE; UTERINE ENDOCERVIX;

MUS; MUS MUSCULUS;

ENDOCERVIX; ENDOMETRIAL REGENERATION; ENDOMETRIUM; FEMALE REPRODUCTIVE TRACT; LABEL-RETAINING CELLS; OVIDUCT; STEM CELLS; TRANSITION ZONE; UTERUS;

ANIMALS; ANIMALS, NEWBORN; CELL MOVEMENT; CELL PROLIFERATION; EMBRYO, MAMMALIAN; ENDOMETRIUM; EPITHELIAL CELLS; EPITHELIUM; ESTROGEN RECEPTOR ALPHA; FEMALE; GENITALIA, FEMALE; GREEN FLUORESCENT PROTEINS; MICE; MITOSIS; OVIDUCTS; PREGNANCY; PROTO-ONCOGENE PROTEINS C-KIT; RECEPTORS, PROGESTERONE; REGENERATION; STAINING AND LABELING; TIME FACTORS; UTERUS;

EID: 84883582359     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.25917     Document Type: Article

References (44)

1. 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:e1-8; PMID:19800602; http://dx.doi.org/10.1016/j.ajog.2009.07.026
2. Du H, Taylor HS. Contribution of bone marrowderived stem cells to endometrium and endometriosis. Stem Cells 2007; 25:2082-6; PMID:17464086; http://dx.doi.org/10.1634/stemcells.2006-0828
3. Taylor HS. Endometrial cells derived from donor stem cells in bone marrow transplant recipients. JAMA 2004; 292:81-5; PMID:15238594; http://dx.doi.org/ 10.1001/jama.292.1.81
4. Cervelló I, Gil-Sanchis C, Mas A, Faus A, Sanz J, Moscardó F, Higueras G, Sanz MA, Pellicer A, Simón C. Bone marrow-derived cells from male donors do not contribute to the endometrial side population of the recipient. PLoS One 2012; 7:e30260; PMID:22276168; http://dx.doi.org/10.1371/ journal.pone.0030260
5. Chan RWS, Schwab KE, Gargett CE. Clonogenicity of human endometrial epithelial and stromal cells. Biol Reprod 2004; 70:1738-50; PMID:14766732; http://dx.doi.org/10.1095/biolreprod.103.024109
6. Wolff EF, Wolff AB, Hongling Du, Taylor HS. Demonstration of multipotent stem cells in the adult human endometrium by in vitro chondrogenesis. Reprod Sci 2007; 14:524-33; PMID:17959881; http://dx.doi.org/10.1177/1933719107306896
7. 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; PMID:19228591; http://dx.doi.org/10. 1095/biolreprod.108.075226
8. Cervelló I, Gil-Sanchis C, Mas A, Delgado-Rosas F, Martínez-Conejero JA, Galán A, Martínez-Romero A, Martínez S, Navarro I, Ferro J, et al. Human endometrial side population cells exhibit genotypic, phenotypic and functional features of somatic stem cells. PLoS One 2010; 5:e10964; PMID:20585575; http://dx.doi.org/10.1371/ journal.pone.0010964
9. Cervelló I, Mas A, Gil-Sanchis C, Peris L, Faus A, Saunders PT, Critchley HO, Simón C. Reconstruction of endometrium from human endometrial side population cell lines. PLoS One 2011;6:e21221; PMID:21712999; http://dx.doi.org/10.1371/journal.pone.0021221
10. Chan RWS, Gargett CE. Identification of labelretaining cells in mouse endometrium. Stem Cells 2006; 24:1529-38; PMID:16456137; http://dx.doi.org/10. 1634/stemcells.2005-0411
11. 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; PMID:17289934; http://dx.doi.org/10.1634/stemcells.2006-0204
12. Chan RW, Kaitu'u-Lino T, Gargett CE. Role of label-retaining cells in estrogen-induced endometrial regeneration. Reprod Sci 2012; 19:102-14; PMID:22064386; http://dx.doi.org/10.1177/1933719111414207
13. 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; PMID:22402967; http://dx.doi.org/10.1095/biolreprod.112.099309
14. Kiel MJ, He S, Ashkenazi R, Gentry SN, Teta M, Kushner JA, Jackson TL, Morrison SJ. Haematopoietic stem cells do not asymmetrically segregate chromosomes or retain BrdU. Nature 2007; 449:238-42; PMID:17728714; http://dx.doi.org/10.1038/nature06115
15. Cairns J. Mutation selection and the natural history of cancer. Nature 1975; 255:197-200; PMID:1143315; http://dx.doi.org/10.1038/255197a0
16. Potten CS, Owen G, Booth D. Intestinal stem cells protect their genome by selective segregation of template DNA strands. J Cell Sci 2002; 115:2381-8; PMID:12006622
17. Smith GH. Label-retaining epithelial cells in mouse mammary gland divide asymmetrically and retain their template DNA strands. Development 2005; 132:681-7; PMID:15647322; http://dx.doi.org/10.1242/dev.01609
18. Conboy MJ, Karasov AO, Rando TA. High incidence of non-random template strand segregation and asymmetric fate determination in dividing stem cells and their progeny. PLoS Biol 2007; 5:e102; PMID:17439301; http://dx.doi.org/10.1371/ journal.pbio.0050102
19. Tumbar T, Guasch G, Greco V, Blanpain C, Lowry WE, Rendl M, Fuchs E. Defining the epithelial stem cell niche in skin. Science 2004; 303:359-63; PMID:14671312; http://dx.doi.org/10.1126/science.1092436
20. Hochedlinger K, Yamada Y, Beard C, Jaenisch R. Ectopic expression of Oct-4 blocks progenitor-cell differentiation and causes dysplasia in epithelial tissues. Cell 2005; 121:465-77; PMID:15882627; http://dx.doi.org/10.1016/j.cell. 2005.02.018
21. Szotek PP, Chang HL, Brennand K, Fujino A, Pieretti-Vanmarcke R, Lo Celso C, Dombkowski D, Preffer F, Cohen KS, Teixeira J, et al. Normal ovarian surface epithelial label-retaining cells exhibit stem/progenitor cell characteristics. Proc Natl Acad Sci U S A 2008; 105:12469-73; PMID:18711140; http://dx.doi.org/ 10.1073/pnas.0805012105
22. Wang Y, Sacchetti A, van Dijk MR, van der Zee M, van der Horst PH, Joosten R, Burger CW, Grootegoed JA, Blok LJ, Fodde R. Identification of quiescent, stem-like cells in the distal female reproductive tract. PLoS One 2012; 7:e40691; PMID:22848396; http://dx.doi.org/10.1371/journal.pone.0040691
23. Runck LA, Kramer M, Ciraolo G, Lewis AG, Guasch G. Identification of epithelial label-retaining cells at the transition between the anal canal and the rectum in mice. Cell Cycle 2010; 9:3039-45; PMID:20647777; http://dx.doi.org/10.4161/cc.9.15.12437
24. Ishimoto T, Oshima H, Oshima M, Kai K, Torii R, Masuko T, Baba H, Saya H, Nagano O. CD44+ slow-cycling tumor cell expansion is triggered by cooperative actions of Wnt and prostaglandin E2 in gastric tumorigenesis. Cancer Sci 2010; 101:673-8; PMID:20028388; http://dx.doi.org/10.1111/j.1349-7006.2009.01430.x
25. Mcnairn AJ, Guasch G. Epithelial transition zones: merging microenvironments, niches, and cellular transformation. Eur J Dermatol 2011; 21(Suppl 2):21-8; PMID:21628126
26. Martens JE, Smedts FM, Ploeger D, Helmerhorst TJ, Ramaekers FC, Arends JW, Hopman AH. Distribution pattern and marker profile show two subpopulations of reserve cells in the endocervical canal. Int J Gynecol Pathol 2009; 28:381-8; PMID:19483623; http://dx.doi.org/10.1097/PGP.0b013e31819932f8
27. Wang H, Eriksson H, Sahlin L. Estrogen receptors alpha and beta in the female reproductive tract of the rat during the estrous cycle. Biol Reprod 2000; 63:1331-40; PMID:11058536; http://dx.doi.org/10.1095/biolreprod63.5.1331
28. Ramos JG, Varayoud J, Bosquiazzo VL, Luque EH, Muñoz-de-Toro M. Cellular turnover in the rat uterine cervix and its relationship to estrogen and progesterone receptor dynamics. Biol Reprod 2002; 67:735-42; PMID:12193379; http://dx.doi.org/10.1095/biolreprod.101.002402
29. Yang A, Kaghad M, Wang Y, Gillett E, Fleming MD, Dötsch V, Andrews NC, Caput D, McKeon F. p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities. Mol Cell 1998; 2:305-16; PMID:9774969; http://dx.doi.org/10.1016/S1097-2765(00)80275-0
30. Branham WS, Sheehan DM, Zehr DR, Ridlon E, Nelson CJ. The postnatal ontogeny of rat uterine glands and age-related effects of 17 beta-estradiol. Endocrinology 1985; 117:2229-37; PMID:4042984; http://dx.doi.org/10.1210/endo- 117-5-2229
31. 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; PMID:2782286; http://dx.doi.org/10.1002/aja.1001860102
32. Hu J, Gray CA, Spencer TE. Gene expression profiling of neonatal mouse uterine development. Biol Reprod 2004; 70:1870-6; PMID:14985250; http://dx.doi.org/10.1095/biolreprod.103.026336
33. Patterson AL, Zhang L, Arango NA, Teixeira J, Pru JK. Mesenchymal-to-epithelial transition contributes to endometrial regeneration following natural and artificial decidualization. Stem Cells Dev 2013; 22:964-74; PMID:23216285; http://dx.doi.org/10.1089/scd.2012.0435
34. Huang CC, Orvis GD, Wang Y, Behringer RR. Stromal-to-epithelial transition during postpartum endometrial regeneration. PLoS One 2012; 7:e44285; PMID:22970108; http://dx.doi.org/10.1371/journal.pone.0044285
35. Ludwig H, Metzger H. The re-epithelization of endometrium after menstrual desquamation. Arch Gynakol 1976; 221:51-60; PMID:989268; http://dx.doi.org/10. 1007/BF00667681
36. Ludwig H, Spornitz UM. Microarchitecture of the human endometrium by scanning electron microscopy: menstrual desquamation and remodeling. Ann N Y Acad Sci 1991; 622:28-46; PMID:2064187; ht tp: //dx.doi .org /10.1111/j.1749-6632.19.tb37848.x
37. Ferenczy A, Bertrand G, Gelfand MM. Studies on the cytodynamics of human endometrial regeneration. III. In vitro short-term incubation historadioautography. Am J Obstet Gynecol 1979; 134:297-304; PMID:453263
38. Padykula HA. Regeneration in the primate uterus: the role of stem cells. Ann N Y Acad Sci 1991; 622:47-56; PMID:2064204; http://dx.doi.org/10.1111/j. 1749-6632.1991.tb37849.x
39. Padykula HA, Coles LG, Okulicz WC, Rapaport SI, McCracken JA, King NW Jr., Longcope C, Kaiserman-Abramof IR. The basalis of the primate endometrium: a bifunctional germinal compartment. Biol Reprod 1989; 40:681-90; PMID:2758097; http://dx.doi.org/10.1095/biolreprod40.3.681
40. 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; PMID:20444944; http://dx.doi.org/10.1210/en.2009-1334
41. Paik DY, Janzen DM, Schafenacker AM, Velasco VS, Shung MS, Cheng D, Huang J, Witte ON, Memarzadeh S. Stem-like epithelial cells are concentrated in the distal end of the fallopian tube: a site for injury and serous cancer initiation. Stem Cells 2012; 30:2487-97; PMID:22911892; http://dx.doi.org/10. 1002/stem.1207
42. Kim J, Coffey DM, Creighton CJ, Yu Z, Hawkins SM, Matzuk MM. High-grade serous ovarian cancer arises from fallopian tube in a mouse model. Proc Natl Acad Sci U S A 2012; 109:3921-6; PMID:22331912; http://dx.doi.org/10.1073/pnas. 1117135109
43. Herfs M, Yamamoto Y, Laury A, Wang X, Nucci MR, McLaughlin-Drubin ME, Münger K, Feldman S, McKeon FD, Xian W, et al. A discrete population of squamocolumnar junction cells implicated in the pathogenesis of cervical cancer. Proc Natl Acad Sci U S A 2012; 109:10516-21; PMID:22689991; http://dx.doi.org/10.1073/pnas.1202684109
44. 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; PMID:19843861; http://dx.doi.org/10.1158/0008-5472.CAN-08-4808