Epithelial ovarian cancer stem cells: Underlying complexity of a simple paradigm

Reproduction

Volumn 149, Issue 2, 2015, Pages R59-R70

  Garson, Kenneth ^a   Vanderhyden, Barbara C ^a,b  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALDH1 ANTIGEN; BREAST CANCER RESISTANCE PROTEIN; BROXURIDINE; CD133 ANTIGEN; CD24 ANTIGEN; EPITHELIAL CELL ADHESION MOLECULE; HERMES ANTIGEN; LGR5 ANTIGEN; LY6A ANTIGEN; MEMBRANE ANTIGEN; STEM CELL FACTOR RECEPTOR; TUMOR ANTIGEN; UNCLASSIFIED DRUG; ALDEHYDE DEHYDROGENASE ISOENZYME 1; GLYCOPROTEIN; ISOENZYME; LEUKOCYTE ANTIGEN; PEPTIDE; RETINAL DEHYDROGENASE; TUMOR MARKER;

ARTICLE; CANCER PROGNOSIS; CANCER STEM CELL; CARCINOGENESIS; CELL PROLIFERATION; CELL RENEWAL; CONSENSUS; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; IMMUNOHISTOCHEMISTRY; NONHUMAN; OVARY; OVARY CARCINOMA; PATHOGENESIS; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; SOMATIC CELL; STEM CELL NICHE; TUMOR INITIATING CELL; UTERINE TUBE; ANIMAL; CHEMISTRY; DRUG EFFECTS; DRUG RESISTANCE; FEMALE; NEOPLASMS, GLANDULAR AND EPITHELIAL; OVARIAN NEOPLASMS; PATHOLOGY; STEM CELL; TUMOR RECURRENCE;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD44; DRUG RESISTANCE, NEOPLASM; FALLOPIAN TUBES; FEMALE; GLYCOPROTEINS; HUMANS; ISOENZYMES; NEOPLASM RECURRENCE, LOCAL; NEOPLASMS, GLANDULAR AND EPITHELIAL; OVARIAN NEOPLASMS; OVARY; PEPTIDES; RETINAL DEHYDROGENASE; STEM CELLS; TUMOR MARKERS, BIOLOGICAL;

EID: 84921286307     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-14-0234     Document Type: Article

References (98)

1. Ahmed N, Abubaker K, Findlay J & Quinn M 2013 Cancerous ovarian stem cells: obscure targets for therapy but relevant to chemoresistance. Journal of Cellular Biochemistry 114 21-34. (doi:10.1002/jcb.24317)
2. Alvero AB, Chen R, Fu HH, Montagna M, Schwartz PE, Rutherford T, Silasi DA, Steffensen KD,Waldstrom M, Visintin I et al. 2009 Molecular phenotyping of human ovarian cancer stem cells unravels the mechanisms for repair and chemoresistance. Cell Cycle 8 158-166. (doi:10.4161/cc.8.1.7533)
3. Auersperg N 2013 The stem-cell profile of ovarian surface epithelium is reproduced in the oviductal fimbriae, with increased stem-cell marker density in distal parts of the fimbriae. International Journal of Gynecological Pathology 32 444-453. (doi:10.1097/PGP.0b013e3182800ad5)
4. Auersperg N,Woo MM & Gilks CB 2008 The origin of ovarian carcinomas: a developmental view. Gynecologic Oncology 110 452-454. (doi:10.1016/j.ygyno.2008.05.031)
5. + ovarian cancer cells. Oncogene 28 209-218. (doi:10.1038/onc.2008.374)
6. Bapat SA, Mali AM, Koppikar CB & Kurrey NK 2005 Stem and progenitorlike cells contribute to the aggressive behavior of human epithelial ovarian cancer. Cancer Research 65 3025-3029. (doi:10.1158/0008- 5472.CAN-04-3931)
7. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ et al. 2007 Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449 1003-1007. (doi:10.1038/nature06196)
8. Bell DA 2005 Origins and molecular pathology of ovarian cancer. Modern Pathology 18 (Suppl 2) S19-S32. (doi:10.1038/modpathol.3800306)
9. Bell DA & Scully RE 1994 Early de novo ovarian carcinoma. Astudy of fourteen cases. Cancer 73 1859-1864. (doi:10.1002/1097-0142(19940401)73:7!1859::AID-CNCR2820730714O3.0.CO;2-L)
10. Bowen NJ, Walker LD, Matyunina LV, Logani S, Totten KA, Benigno BB & McDonald JF 2009 Gene expression profiling supports the hypothesis that human ovarian surface epithelia are multipotent and capable of serving as ovarian cancer initiating cells. BMC Medical Genomics 2 71. (doi:10.1186/1755-8794-2-71)
11. Buick RN & MacKillop WJ 1981 Measurement of self-renewal in culture of clonogenic cells from human ovarian carcinoma. British Journal of Cancer 44 349-355. (doi:10.1038/bjc.1981.191)
12. Carcangiu ML, Radice P, Manoukian S, Spatti G, Gobbo M, Pensotti V, Crucianelli R & Pasini B 2004 Atypical epithelial proliferation in fallopian tubes in prophylactic salpingo-oophorectomy specimens from BRCA1 and BRCA2 germline mutation carriers. International Journal of Gynecological Pathology 23 35-40. (doi:10.1097/01.pgp.0000101082.35393.84)
13. Carlson JW, Miron A, Jarboe EA, Parast MM, Hirsch MS, Lee Y, Muto MG, Kindelberger D & Crum CP 2008 Serous tubal intraepithelial carcinoma: its potential role in primary peritoneal serous carcinoma and serous cancer prevention. Journal of Clinical Oncology 26 4160-4165. (doi:10. 1200/JCO.2008.16.4814)
14. Challen GA & Little MH 2006 A side order of stem cells: the SP phenotype. Stem Cells 24 3-12. (doi:10.1634/stemcells.2005-0116)
15. Chefetz I, Alvero AB, Holmberg JC, Lebowitz N, Craveiro V, Yang-Hartwich Y, Yin G, Squillace L, Gurrea Soteras M, Aldo P et al. 2013 TLR2 enhances ovarian cancer stem cell self-renewal and promotes tumor repair and recurrence. Cell Cycle 12 511-521. (doi:10.4161/cc.23406)
16. Connolly DC, Bao R, Nikitin AY, Stephens KC, Poole TW, Hua X, Harris SS, VanderhydenBC&HamiltonTC 2003Female mice chimeric for expression of the simian virus 40 TAg under control of the MISIIR promoter develop epithelial ovarian cancer. Cancer Research 63 1389-1397.
17. Craveiro V, Yang-Hartwich Y, Holmberg JC, Sumi NJ, Pizzonia J, Griffin B, Gill SK, Silasi DA, Azodi M, Rutherford T et al. 2013 Phenotypic modifications in ovarian cancer stem cells following paclitaxel treatment. Cancer Medicine 2 751-762. (doi:10.1002/cam4.115)
18. Crum CP, McKeon FD & Xian W 2012 BRCA, the oviduct, and the space and time continuum of pelvic serous carcinogenesis. International Journal of Gynecological Cancer 22 (Suppl 1) S29-S34. (doi:10.1097/IGC.0b013e31824d7269)
19. Crum CP, Herfs M, Ning G, Bijron JG, Howitt BE, Jimenez CA, Hanamornroongruang S, McKeon FD & Xian W 2013 Through the glass darkly: intraepithelial neoplasia, top-down differentiation, and the road to ovarian cancer. JournalofPathology 231 402-412. (doi:10.1002/path.4263)
20. Curley MD, Therrien VA,Cummings CL, Sergent PA, Koulouris CR, Friel AM, Roberts DJ, Seiden MV, Scadden DT, Rueda BR et al. 2009 CD133 expression defines a tumor initiating cell population in primary human ovarian cancer. Stem Cells 27 2875-2883. (doi:10.1002/stem.236)
21. Dean M, Fojo T & Bates S 2005 Tumour stem cells and drug resistance. Nature Reviews. Cancer 5 275-284. (doi:10.1038/nrc1590)
22. Dubeau L 1999 The cell of origin of ovarian epithelial tumors and the ovarian surface epithelium dogma: does the emperor have no clothes? Gynecologic Oncology 72 437-442. (doi:10.1006/gyno.1998.5275)
23. Feeley KM & Wells M 2001 Precursor lesions of ovarian epithelial malignancy. Histopathology 38 87-95. (doi:10.1046/j.1365-2559.2001.01042.x)
24. Flesken-Nikitin A, Hwang CI, Cheng CY, Michurina TV, Enikolopov G & Nikitin AY 2013 Ovarian surface epithelium at the junction area contains a cancer-prone stem cell niche. Nature 495 241-245. (doi:10.1038/nature11979)
25. Folkins AK, Jarboe EA, Saleemuddin A, Lee Y, Callahan MJ, Drapkin R, Garber JE, Muto MG, Tworoger S & Crum CP 2008 A candidate precursor to pelvic serous cancer (p53 signature) and its prevalence in ovaries and fallopian tubes from women with BRCA mutations. Gynecologic Oncology 109 168-173. (doi:10.1016/j.ygyno.2008.01.012)
26. Gamwell LF, Collins O & Vanderhyden BC 2012 The mouse ovarian surface epithelium contains a population of LY6A (SCA-1) expressing progenitor cells that are regulated by ovulation-associated factors. Biology of Reproduction 87 80. (doi:10.1095/biolreprod.112.100347)
27. + cells from hierarchically organized ovarian cancer are enriched in cancer stem cells. Oncogene 29 2672-2680. (doi:10.1038/onc.2010.35)
28. Garson K, Gamwell LF, Pitre EM & Vanderhyden BC 2012 Technical challenges and limitations of current mouse models of ovarian cancer. Journal of Ovarian Research 5 39. (doi:10.1186/1757-2215-5-39)
29. Golebiewska A, Brons NH, Bjerkvig R & Niclou SP 2011 Critical appraisal of the side population assay in stem cell and cancer stem cell research. Cell Stem Cell 8 136-147. (doi:10.1016/j.stem.2011.01.007)
30. Grosse-Gehling P, Fargeas CA, Dittfeld C, Garbe Y, Alison MR, Corbeil D & Kunz-Schughart LA 2013 CD133 as a biomarker for putative cancer stem cells in solid tumours: limitations, problems and challenges. Journal of Pathology 229 355-378. (doi:10.1002/path.4086)
31. Hamburger AW & Salmon SE 1977 Primary bioassay of human tumor stem cells. Science 197 461-463. (doi:10.1126/science.560061)
32. Holmes C & Stanford WL 2007 Concise review: stem cell antigen-1: expression, function, and enigma. Stem Cells 25 1339-1347. (doi:10.1634/stemcells.2006-0644)
33. Hoyer PE, Byskov AG & Mollgard K 2005 Stem cell factor and c-Kit in human primordial germ cells and fetal ovaries. Molecular and Cellular Endocrinology 234 1-10. (doi:10.1016/j.mce.2004.09.012)
34. Hu L, McArthur C & Jaffe RB 2010 Ovarian cancer stem-like sidepopulation cells are tumourigenic and chemoresistant. British Journal of Cancer 102 1276-1283. (doi:10.1038/sj.bjc.6605626)
35. Hummitzsch K, Irving-Rodgers HF, Hatzirodos N, Bonner W, Sabatier L, Reinhardt DP, Sado Y, Ninomiya Y,Wilhelm D & Rodgers RJ 2013 A new model of development of the mammalian ovary and follicles. PLoS ONE 8 e55578. (doi:10.1371/journal.pone.0055578)
36. Imrich S,HachmeisterM&GiresO 2012 EpCAM and its potential role in tumorinitiating cells. CellAdhesion & Migration 6 30-38. (doi:10.4161/cam.18953)
37. Jaggupilli A & Elkord E 2012 Significance of CD44 and CD24 as cancer stem cell markers: an enduring ambiguity. Clinical & Developmental Immunology 2012 708036. (doi:10.1155/2012/708036)
38. Jarboe E, Folkins A, Nucci MR, Kindelberger D, Drapkin R, Miron A, Lee Y & Crum CP 2008 Serous carcinogenesis in the fallopian tube: a descriptive classification. International Journal of Gynecological Pathology 27 1-9. (doi:10.1097/pgp.0b013e31814b191f)
39. Jordan NV, Johnson GL & Abell AN 2011 Tracking the intermediate stages of epithelial-mesenchymal transition in epithelial stem cells and cancer. Cell Cycle 10 2865-2873. (doi:10.4161/cc.10.17.17188)
40. Kern SE & Shibata D 2007 The fuzzy math of solid tumor stem cells: a perspective. Cancer Research 67 8985-8988. (doi:10.1158/0008-5472.CAN-07-1971)
41. Koo BK& CleversH 2014 Stem cellsmarked by the R-spondin receptor LGR5. Gastroenterology 147 289-302. (doi:10.1053/j.gastro.2014.05.007)
42. Kryczek I, Liu S, Roh M, Vatan L, Szeliga W, Wei S, Banerjee M, Mao Y, Kotarski J, Wicha MS et al. 2012 Expression of aldehyde dehydrogenase and CD133 defines ovarian cancer stem cells. International Journal of Cancer 130 29-39. (doi:10.1002/ijc.25967)
43. Kulkarni-Datar K, Orsulic S, Foster R & Rueda BR 2013 Ovarian tumor initiating cell populations persist following paclitaxel and carboplatin chemotherapy treatment in vivo. Cancer Letters 339 237-246. (doi:10.1016/j.canlet.2013.06.014)
44. Kusumbe AP, Mali AM & Bapat SA 2009 CD133-expressing stem cells associated with ovarian metastases establish an endothelial hierarchy and contribute to tumor vasculature. Stem Cells 27 498-508. (doi:10.1634/stemcells.2008-0868)
45. de Lau WB, Snel B & Clevers HC 2012 The R-spondin protein family. Genome Biology 13 242. (doi:10.1186/gb-2012-13-3-242)
46. Lee Y, Miron A, Drapkin R, Nucci MR, Medeiros F, Saleemuddin A, Garber J, Birch C, Mou H, Gordon RW et al. 2007 A candidate precursor to serous carcinoma that originates in the distal fallopian tube. Journal of Pathology 211 26-35. (doi:10.1002/path.2091)
47. Lennartsson J & Ronnstrand L 2012 Stem cell factor receptor/c-Kit: from basic science to clinical implications. Physiological Reviews 92 1619-1649. (doi:10.1152/physrev.00046.2011)
48. Lili LN, Matyunina LV, Walker LD, Wells SL, Benigno BB & McDonald JF 2013 Molecular profiling supports the role of epithelial-to-mesenchymal transition (EMT) in ovarian cancer metastasis. Journal of Ovarian Research 6 49. (doi:10.1186/1757-2215-6-49)
49. Lowe KA, Chia VM, Taylor A, O'Malley C, Kelsh M, MohamedM,Mowat FS & Goff B 2013 An international assessment of ovarian cancer incidence and mortality. Gynecologic Oncology 130 107-114. (doi:10.1016/j. ygyno.2013.03.026)
50. Lu M, Jolly MK, Levine H, Onuchic JN & Ben-Jacob E 2013 MicroRNA-based regulation of epithelial-hybrid-mesenchymal fate determination. PNAS 110 18144-18149. (doi:10.1073/pnas.1318192110)
51. Luo L, Zeng J, Liang B, Zhao Z, Sun L, Cao D, Yang J & Shen K 2011 Ovarian cancer cells with the CD117 phenotype are highly tumorigenic and are related to chemotherapy outcome. Experimental and Molecular Pathology 91 596-602. (doi:10.1016/j.yexmp.2011.06.005)
52. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M et al. 2008 The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133 704-715. (doi:10.1016/j.cell.2008.03.027)
53. Mannik J, Alzayady K & Ghazizadeh S 2010 Regeneration of multilineage skin epithelia by differentiated keratinocytes. Journal of Investigative Dermatology 130 388-397. (doi:10.1038/jid.2009.244)
54. Marcato P, Dean CA, Giacomantonio CA & Lee PW 2011 Aldehyde dehydrogenase: its role as a cancer stem cell marker comes down to the specific isoform. Cell Cycle 10 1378-1384. (doi:10.4161/cc.10.9.15486)
55. McCloskey CW, Goldberg RL, Carter LE, Gamwell LF, Al-Hujaily EM, Collins O, Macdonald EA, Garson K, Daneshmand M, Carmona E et al. 2014 A new spontaneously transformed syngeneic model of high-grade serous ovarian cancer with a tumor-initiating cell population. Frontiers in Oncology 4 53. (doi:10.3389/fonc.2014.00053)
56. Mehra K, Mehrad M, Ning G, Drapkin R, McKeon FD, Xian W & Crum CP 2011 STICS, SCOUTs and p53 signatures; a newlanguage for pelvic serous carcinogenesis. Frontiers in Bioscience 3 625-634. (doi:10.2741/e275)
57. Moserle L, Indraccolo S,Ghisi M, FrassonC, Fortunato E, Canevari S, Miotti S, ToselloV, ZamarchiR,CorradinA et al. 2008The side population of ovarian cancer cells is a primary target of IFN-α antitumor effects. Cancer Research 68 5658-5668. (doi:10.1158/0008-5472.CAN-07-6341)
58. Motohara T, Masuko S, Ishimoto T, Yae T, Onishi N, Muraguchi T, Hirao A, Matsuzaki Y, Tashiro H, Katabuchi H et al. 2011 Transient depletion of p53 followed by transduction of c-Myc and K-Ras converts ovarian stemlike cells into tumor-initiating cells. Carcinogenesis 32 1597-1606. (doi:10.1093/carcin/bgr183)
59. Nagano O & Saya H 2004 Mechanism and biological significance of CD44 cleavage. Cancer Science 95 930-935. (doi:10.1111/j.1349-7006.2004.tb03179.x)
60. Ng A, Tan S, Singh G, Rizk P, Swathi Y, Tan TZ, Huang RY, Leushacke M & Barker N 2014 Lgr5 marks stem/progenitor cells in ovary and tubal epithelia. Nature Cell Biology 16 745-757. (doi:10.1038/ncb3000)
61. O'Brien CA, Pollett A, Gallinger S & Dick JE 2007 A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445 106-110. (doi:10.1038/nature05372)
62. Okada S, Nakauchi H, Nagayoshi K, Nishikawa S, Nishikawa S, Miura Y & Suda T 1991 Enrichment and characterization of murine hematopoietic stem cells that express c-kit molecule. Blood 78 1706-1712.
63. Okamoto I, Kawano Y, Murakami D, Sasayama T, Araki N, Miki T,Wong AJ & Saya H 2001 Proteolytic release of CD44 intracellular domain and its role in the CD44 signaling pathway. Journal of Cell Biology 155 755-762. (doi:10.1083/jcb.200108159)
64. Paik DY, Janzen DM, Schafenacker AM, Velasco VS, Shung MS, Cheng D, Huang J, Witte ON & Memarzadeh S 2012 Stem-like epithelial cells are concentrated in the distal end of the fallopian tube: a site for injury and serous cancer initiation. Stem Cells 30 2487-2497. (doi:10.1002/stem.1207)
65. Parte S, Bhartiya D, Telang J, Daithankar V, Salvi V, Zaveri K & Hinduja I 2011 Detection, characterization, and spontaneous differentiation in vitro of very small embryonic-like putative stem cells in adult mammalian ovary. Stem Cells and Development 20 1451-1464. (doi:10.1089/scd.2010.0461)
66. Patel H, Bhartiya D, Parte S, Gunjal P, Vedulkar S & Bhatt M 2013 Follicle stimulating hormone modulates ovarian stem cells through alternately spliced receptor variant FSH-R3. Journal of Ovarian Research 6 52. (doi:10.1186/1757-2215-6-52)
67. Patterson AL & Pru JK 2013 Long-term label retaining cells localize to distinct regions within the female reproductive epithelium. Cell Cycle 12 2888-2898. (doi:10.4161/cc.25917)
68. Piek JM, van Diest PJ, Zweemer RP, Jansen JW, Poort-Keesom RJ, Menko FH, Gille JJ, Jongsma AP, Pals G, Kenemans P et al. 2001 Dysplastic changes in prophylactically removed fallopian tubes of women predisposed to developing ovarian cancer. Journal of Pathology 195 451-456. (doi:10.1002/path.1000)
69. Pothuri B, Leitao MM, Levine DA, Viale A, Olshen AB, Arroyo C, Bogomolniy F, Olvera N, Lin O, Soslow RA et al. 2010 Genetic analysis of the early natural history of epithelial ovarian carcinoma. PLoS ONE 5 e10358. (doi:10.1371/journal.pone.0010358)
70. Pruitt KD, Brown GR, Hiatt SM, Thibaud-Nissen F, Astashyn A, Ermolaeva O, Farrell CM, Hart J, Landrum MJ, McGarvey KM et al. 2014 RefSeq: an update on mammalian reference sequences. Nucleic Acids Research 42 D756-D763. (doi:10.1093/nar/gkt1114)
71. Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM & Morrison SJ 2008 Efficient tumour formation by single human melanoma cells. Nature 456 593-598. (doi:10.1038/nature07567)
72. Rahman M, Deleyrolle L, Vedam-Mai V, Azari H, Abd-El-Barr M & Reynolds BA 2011 The cancer stem cell hypothesis: failures and pitfalls. Neurosurgery 68 531-545 (discussion 545). (doi:10.1227/NEU.0b013e3181ff9eb5)
73. Roh MH, Kindelberger D & Crum CP 2009 Serous tubal intraepithelial carcinoma and the dominant ovarian mass: clues to serous tumor origin? American Journal of Surgical Pathology 33 376-383. (doi:10.1097/PAS.0b013e3181868904)
74. Rompolas P, Mesa KR & Greco V 2013 Spatial organization within a niche as a determinant of stem-cell fate. Nature 502 513-518. (doi:10.1038/nature12602)
75. Schulte BA, Rao KP, Kreutner A, Thomopoulos GN & Spicer SS 1985 Histochemical examination of glycoconjugates of epithelial cells in the human fallopian tube. Laboratory Investigation 52 207-219.
76. Shi MF, Jiao J, Lu WG, Ye F, Ma D, Dong QG & Xie X 2010 Identification of cancer stem cell-like cells from human epithelial ovarian carcinoma cell line. Cellular and Molecular Life Sciences 67 3915-3925. (doi:10.1007/s00018-010-0420-9)
77. Shi J, Zhou Z, Di W & Li N 2013 Correlation of CD44v6 expression with ovarian cancer progression and recurrence. BMC Cancer 13 182. (doi:10.1186/1471-2407-13-182)
78. Silva IA, Bai S, McLean K, Yang K, Griffith K, Thomas D, Ginestier C, Johnston C, Kueck A, Reynolds RK et al. 2011 Aldehyde dehydrogenase in combination with CD133 defines angiogenic ovarian cancer stem cells that portend poor patient survival. Cancer Research 71 3991-4001. (doi:10.1158/0008-5472.CAN-10-3175)
79. Stewart JM, Shaw PA, Gedye C, Bernardini MQ, Neel BG & Ailles LE 2011 Phenotypic heterogeneity and instability of human ovarian tumorinitiating cells. PNAS 108 6468-6473. (doi:10.1073/pnas.1005529108)
80. Storms RW, Trujillo AP, Springer JB, Shah L, Colvin OM, Ludeman SM & Smith C 1999 Isolation of primitive human hematopoietic progenitors on the basis of aldehyde dehydrogenase activity. PNAS 96 9118-9123. (doi:10.1073/pnas.96.16.9118)
81. Szotek PP, Pieretti-Vanmarcke R, Masiakos PT, Dinulescu DM, Connolly D, Foster R, Dombkowski D, Preffer F, Maclaughlin DT & Donahoe PK 2006 Ovarian cancer side population defines cells with stem cell-like characteristics and Mullerian inhibiting substance responsiveness. PNAS 103 11154-11159. (doi:10.1073/pnas.0603672103)
82. Szotek PP, Chang HL, Brennand K, Fujino A, Pieretti-Vanmarcke R, Lo Celso C,DombkowskiD, Preffer F, Cohen KS, Teixeira J et al. 2008 Normal ovarian surface epithelial label-retaining cells exhibit stem/progenitor cell characteristics. PNAS 105 12469-12473. (doi:10.1073/pnas.0805012105)
83. Tata PR, Mou H, Pardo-Saganta A, Zhao R, Prabhu M, Law BM, Vinarsky V, Cho JL, Breton S, Sahay A et al. 2013 Dedifferentiation of committed epithelial cells into stem cells in vivo. Nature 503 218-223. (doi:10.1038/nature12777)
84. Teyssier JR, Couillin P, Benard J, Ravisse N, Ulrich E & Cornillet P 1992 A multidrug-resistant ovarian carcinoma cell line with a malignant suppressed phenotype is a CD44 gene expression defective mutant. Cancer Genetics and Cytogenetics 60 14-19. (doi:10.1016/0165-4608(92)90225-W)
85. Thomson S, Petti F, Sujka-Kwok I, Mercado P, Bean J, Monaghan M, Seymour SL, Argast GM, Epstein DM & Haley JD 2011 A systems view of epithelial-mesenchymal transition signaling states. Clinical & Experimental Metastasis 28 137-155. (doi:10.1007/s10585-010-9367-3)
86. Tonary AM, Macdonald EA, Faught W, Senterman MK & Vanderhyden BC 2000 Lack of expression of c-KIT in ovarian cancers is associated with poor prognosis. International Journal of Cancer 89 242-250. (doi:10.1002/1097-0215(20000520)89:3!242::AID-IJC6O3.0.CO;2-6)
87. Tsai JH, Donaher JL, Murphy DA, Chau S & Yang J 2012 Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell 22 725-736. (doi:10.1016/j.ccr.2012.09.022)
88. Usongo M & Farookhi R 2012 b-Catenin/Tcf-signaling appears to establish the murine-ovarian surface epithelium (OSE) and remains active in selected postnatal OSE cells. BMC Developmental Biology 12 17. (doi:10.1186/1471-213X-12-17)
89. Virant-Klun I, Skutella T, Hren M, Gruden K, Cvjeticanin B, Vogler A & Sinkovec J 2013a Isolation of small SSEA-4-positive putative stem cells from the ovarian surface epithelium of adult human ovaries by two different methods. BioMed Research International 2013 690415. (doi:10.1155/2013/690415)
90. Virant-Klun I, Skutella T, Kubista M, Vogler A, Sinkovec J & Meden-Vrtovec H 2013b Expression of pluripotency and oocyte-related genes in single putative stem cells from human adult ovarian surface epithelium cultured in vitro in the presence of follicular fluid. BioMed Research International 2013 861460. (doi:10.1155/2013/861460)
91. 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 2012 Identification of quiescent, stem-like cells in the distal female reproductive tract. PLoS ONE 7 e40691. (doi:10.1371/journal.pone.0040691)
92. Wei X, Dombkowski D, Meirelles K, Pieretti-Vanmarcke R, Szotek PP, Chang HL, Preffer FI, Mueller PR, Teixeira J, MacLaughlin DT et al. 2010 Mullerian inhibiting substance preferentially inhibits stem/progenitors in human ovarian cancer cell lines compared with chemotherapeutics. PNAS 107 18874-18879. (doi:10.1073/pnas.1012667107)
93. Williams K, Motiani K, Giridhar PV & Kasper S 2013 CD44 integrates signaling in normal stem cell, cancer stem cell and (pre)metastatic niches. Experimental Biology and Medicine 238 324-338. (doi:10.1177/1535370213480714)
94. Yin G, Alvero AB, Craveiro V, Holmberg JC, Fu HH, Montagna MK, Yang Y, Chefetz-Menaker I, Nuti S, Rossi M et al. 2013 Constitutive proteasomal degradation of TWIST-1 in epithelial-ovarian cancer stem cells impacts differentiation and metastatic potential. Oncogene 32 39-49. (doi:10.1038/onc.2012.33)
95. Zhan Q,Wang C & Ngai S 2013 Ovarian cancer stem cells: a new target for cancer therapy. BioMed Research International 2013 916819. (doi:10.1155/2013/916819)
96. Zhang S, Balch C, Chan MW, Lai HC, Matei D, Schilder JM, Yan PS, Huang TH & Nephew KP 2008 Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Research 68 4311-4320. (doi:10.1158/0008-5472.CAN-08-0364)
97. Zhou S, Schuetz JD, Bunting KD, Colapietro AM, Sampath J, Morris JJ, Lagutina I, Grosveld GC, Osawa M, Nakauchi H et al. 2001 The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nature Medicine 7 1028-1034. (doi:10.1038/nm0901-1028)
98. Zoller M 2011 CD44: can a cancer-initiating cell profit from an abundantly expressed molecule? Nature Reviews. Cancer 11 254-267. (doi:10.1038/nrc3023)