Cancerous ovarian stem cells: Obscure targets for therapy but relevant to chemoresistance

Journal of Cellular Biochemistry

Volumn 114, Issue 1, 2013, Pages 21-34

  Ahmed, Nuzhat ^a,b,c   Abubaker, Khalid ^a,b   Findlay, Jock ^a,b,c   Quinn, Michael ^a,c  

^a ROYAL WOMEN'S HOSPITAL   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

CHEMORESISTANCE; OVARIAN CARCINOMA; RECURRENCE; STEM CELL MARKERS

Indexed keywords

ADECATUMUMAB; ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE ISOENZYME 1; CARBOPLATIN; CATUMAXOMAB; CD133 ANTIGEN; CD24 ANTIGEN; CISPLATIN; EPITHELIAL CELL ADHESION MOLECULE; HERMES ANTIGEN; IMATINIB; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MICRORNA; MICRORNA 214; MICRORNA 30A; MICRORNA 451; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NOTCH RECEPTOR; OCTAMER TRANSCRIPTION FACTOR 4; PACLITAXEL; PLATINUM DERIVATIVE; SILTUXIMAB; STAT3 PROTEIN; STEM CELL FACTOR RECEPTOR; TAXANE DERIVATIVE; UNCLASSIFIED DRUG; UNINDEXED DRUG; WNT PROTEIN;

CANCER CELL CULTURE; CANCER GRADING; CANCER GROWTH; CANCER PATIENT; CANCER RECURRENCE; CANCER RESISTANCE; CANCER STEM CELL; CARCINOGENESIS; CARCINOMA IN SITU; CELL POPULATION; CELL RENEWAL; CELL SURVIVAL; CLEAR CELL CARCINOMA; CYTOREDUCTIVE SURGERY; ENDOMETRIUM CARCINOMA; HUMAN; NONHUMAN; OVARIAN CARCINOGENESIS; OVARY CANCER; OVARY CARCINOMA; OVARY CYST; PRIORITY JOURNAL; REVIEW; TREATMENT RESPONSE; UTERINE TUBE;

ADENOCARCINOMA, CLEAR CELL; ANTINEOPLASTIC AGENTS; CARCINOMA IN SITU; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; CYSTADENOCARCINOMA, SEROUS; FALLOPIAN TUBES; FEMALE; HUMANS; MOLECULAR TARGETED THERAPY; NEOPLASMS, GLANDULAR AND EPITHELIAL; NEOPLASTIC STEM CELLS; OVARIAN NEOPLASMS; OVARY; TUMOR MARKERS, BIOLOGICAL;

EID: 84869445970     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24317     Document Type: Review

References (147)

1. Agoff SN, Mendelin JE, Grieco VS, Garcia RL,. 2002. Unexpected gynecologic neoplasms in patients with proven or suspected BRCA-1 or -2 mutations: Implications for gross examination, cytology, and clinical follow-up. Am J Surg Pathol 26: 171-178.
2. Aguilar-Gallardo C, Rutledge EC, Martinez-Arroyo AM, Hidalgo JJ, Domingo S, Simon C,. 2012. Overcoming challenges of ovarian cancer stem cells: Novel therapeutic approaches. Stem Cell Rev 8: 994-1010.
3. Ahmed N, Maines-Bandiera S, Quinn MA, Unger WG, Dedhar S, Auersperg N,. 2006. Molecular pathways regulating EGF-induced epithelio-mesenchymal transition in human ovarian surface epithelium. Am J Physiol Cell Physiol 290: C1532-C1542.
4. Ahmed N, Thompson EW, Quinn MA,. 2007. Epithelial-mesenchymal interconversions in normal ovarian surface epithelium and ovarian carcinomas: An exception to the norm. J Cell Physiol 213: 581-588.
5. Ahmed N, Abubaker K, Findlay J, Quinn M,. 2010. Epithelial mesenchymal transition and cancer stem cell-like phenotypes facilitate chemoresistance in recurrent ovarian cancer. Curr Cancer Drug Targets 10: 268-278.
6. Aktas B, Tewes M, Fehm T, Hauch S, Kimmig R, Kasimir-Bauer S,. 2009. Stem cell and epithelial-mesenchymal transition markers are frequently overexpressed in circulating tumor cells of metastatic breast cancer patients. Breast Cancer Res 11: R46.
7. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF,. 2003. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100: 3983-3988.
8. Alvero AB, Chen R, Fu HH, Montagna M, Schwartz PE, Rutherford T, Silasi DA, Steffensen KD, Waldstrom M, Visintin I, Mor G,. 2009. Molecular phenotyping of human ovarian cancer stem cells unravels the mechanisms for repair and chemoresistance. Cell Cycle 8: 158-166.
9. Auersperg N, Maines-Bandiera SL, Dyck HG, Kruk PA,. 1994. Characterization of cultured human ovarian surface epithelial cells: Phenotypic plasticity and premalignant changes. Lab Invest 71: 510-518.
10. Auersperg N, Wong AS, Choi KC, Kang SK, Leung PC,. 2001. Ovarian surface epithelium: Biology, endocrinology, and pathology. Endocr Rev 22: 255-288.
11. Baba T, Convery PA, Matsumura N, Whitaker RS, Kondoh E, Perry T, Huang Z, Bentley RC, Mori S, Fujii S, Marks JR, Berchuck A, Murphy SK,. 2009. Epigenetic regulation of CD133 and tumorigenicity of CD133+ ovarian cancer cells. Oncogene 28: 209-218.
12. Bapat SA, Mali AM, Koppikar CB, Kurrey NK,. 2005. Stem and progenitor-like cells contribute to the aggressive behavior of human epithelial ovarian cancer. Cancer Res 65: 3025-3029.
13. Barker N, Clevers H,. 2007. Tracking down the stem cells of the intestine: Strategies to identify adult stem cells. Gastroenterology 133: 1755-1760.
14. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ, Clevers H,. 2007. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449: 1003-1007.
15. Bates J,. 2008. Cancer stem cells-emerging therapeutic, diagnostic and market opportunities. in Report.
16. Bellone S, Siegel ER, Cocco E, Cargnelutti M, Silasi DA, Azodi M, Schwartz PE, Rutherford TJ, Pecorelli S, Santin AD,. 2009. Overexpression of epithelial cell adhesion molecule in primary, metastatic, and recurrent/chemotherapy-resistant epithelial ovarian cancer: Implications for epithelial cell adhesion molecule-specific immunotherapy. Int J Gynecol Cancer 19: 860-866.
17. Bignotti E, Tassi RA, Calza S, Ravaggi A, Bandiera E, Rossi E, Donzelli C, Pasinetti B, Pecorelli S, Santin AD,. 2007. Gene expression profile of ovarian serous papillary carcinomas: Identification of metastasis-associated genes. Am J Obstet Gynecol 196: 245 e1-e11.
18. Borovski T, De Sousa EMF, Vermeulen L, Medema JP,. 2011. Cancer stem cell niche: The place to be. Cancer Res 71: 634-639.
19. Bose D, Zimmerman LJ, Pierobon M, Petricoin E, Tozzi F, Parikh A, Fan F, Dallas N, Xia L, Gaur P, Samuel S, Liebler DC, Ellis LM,. 2011. Chemoresistant colorectal cancer cells and cancer stem cells mediate growth and survival of bystander cells. Br J Cancer 105: 1759-1767.
20. Bourguignon LY, Peyrollier K, Xia W, Gilad E,. 2008. Hyaluronan-CD44 interaction activates stem cell marker Nanog, Stat-3-mediated MDR1 gene expression, and ankyrin-regulated multidrug efflux in breast and ovarian tumor cells. J Biol Chem 283: 17635-17651.
21. 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 Med Genomics 2: 71.
22. Bristow RE, Tomacruz RS, Armstrong DK, Trimble EL, Montz FJ,. 2002. Survival effect of maximal cytoreductive surgery for advanced ovarian carcinoma during the platinum era: A meta-analysis. J Clin Oncol 20: 1248-1259.
23. Buick RN, Pullano R, Trent JM,. 1985. Comparative properties of five human ovarian adenocarcinoma cell lines. Cancer Res 45: 3668-3676.
24. Chang B, Liu G, Xue F, Rosen DG, Xiao L, Wang X, Liu J,. 2009. ALDH1 expression correlates with favorable prognosis in ovarian cancers. Mod Pathol 22: 817-823.
25. Chao YL, Shepard CR, Wells A,. 2010. Breast carcinoma cells re-express E-cadherin during mesenchymal to epithelial reverting transition. Mol Cancer 9: 179.
26. Chen X, Horiuchi A, Kikuchi N, Osada R, Yoshida J, Shiozawa T, Konishi I,. 2007. Hedgehog signal pathway is activated in ovarian carcinomas, correlating with cell proliferation: It's inhibition leads to growth suppression and apoptosis. Cancer Sci 98: 68-76.
27. Choi YP, Shim HS, Gao MQ, Kang S, Cho NH,. 2011. Molecular portraits of intratumoral heterogeneity in human ovarian cancer. Cancer Lett 307: 62-71.
28. Colomiere M, Ward AC, Riley C, Trenerry MK, Cameron-Smith D, Findlay J, Ackland L, Ahmed N,. 2009. Cross talk of signals between EGFR and IL-6R through JAK2/STAT3 mediate epithelial-mesenchymal transition in ovarian carcinomas. Br J Cancer 100: 134-144.
29. Creighton CJ, Li X, Landis M, Dixon JM, Neumeister VM, Sjolund A, Rimm DL, Wong H, Rodriguez A, Herschkowitz JI, Fan C, Zhang X, He X, Pavlick A, Gutierrez MC, Renshaw L, Larionov AA, Faratian D, Hilsenbeck SG, Perou CM, Lewis MT, Rosen JM, Chang JC,. 2009. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci USA 106: 13820-13825.
30. Curley MD, Garrett LA, Schorge JO, Foster R, Rueda BR,. 2011. Evidence for cancer stem cells contributing to the pathogenesis of ovarian cancer. Front Biosci 16: 368-392.
31. Das M, Mohanty C, Sahoo SK,. 2009. Ligand-based targeted therapy for cancer tissue. Expert Opin Drug Deliv 6: 285-304.
32. Dressman HK, Berchuck A, Chan G, Zhai J, Bild A, Sayer R, Cragun J, Clarke J, Whitaker RS, Li L, Gray J, Marks J, Ginsburg GS, Potti A, West M, Nevins JR, Lancaster JM,. 2007. An integrated genomic-based approach to individualized treatment of patients with advanced-stage ovarian cancer. J Clin Oncol 25: 517-525.
33. Ellington AD, Szostak JW,. 1990. In vitro selection of RNA molecules that bind specific ligands. Nature 346: 818-822.
34. Ferrandina G, Bonanno G, Pierelli L, Perillo A, Procoli A, Mariotti A, Corallo M, Martinelli E, Rutella S, Paglia A, Zannoni G, Mancuso S, Scambia G,. 2008. Expression of CD133-1 and CD133-2 in ovarian cancer. Int J Gynecol Cancer 18: 506-514.
35. Folkins AK, Saleemuddin A, Garrett LA, Garber JE, Muto MG, Tworoger SS, Crum CP,. 2009. Epidemiologic correlates of ovarian cortical inclusion cysts (CICs) support a dual precursor pathway to pelvic epithelial cancer. Gynecol Oncol 115: 108-111.
36. Gao MQ, Choi YP, Kang S, Youn JH, Cho NH,. 2010. CD24+ cells from hierarchically organized ovarian cancer are enriched in cancer stem cells. Oncogene 29: 2672-2680.
37. Gao S, Zhao X, Lin B, Hu Z, Yan L, Gao J,. 2012. Clinical implications of REST and TUBB3 in ovarian cancer and its relationship to paclitaxel resistance. Tumour Biol Jun 10 [Epub ahead of print].
38. García Campelo MRACG, Aparicio Gallego G, Grande Pulido E, Antón Aparicio LM,. 2011. Stem cell and lung cancer development: Blaming the Wnt, Hh and Notch signalling pathway. Clin Transl Oncol 13: 77-83.
39. Gatcliffe TA, Monk BJ, Planutis K, Holcombe RF,. 2008. Wnt signaling in ovarian tumorigenesis. Int J Gynecol Cancer 18: 954-962.
40. Ginsburg GS, Willard HF,. 2009. Genomic and personalized medicine: Foundations and applications. Transl Res 154: 277-287.
41. Glinsky GV,. 2007. Stem cell origin of death-from-cancer phenotypes of human prostate and breast cancers. Stem Cell Rev 3: 79-93.
42. Glinsky GV,. 2008. " Stemness" genomics law governs clinical behavior of human cancer: Implications for decision making in disease management. J Clin Oncol 26: 2846-2853.
43. Gotlieb WH, Saumet J, Beauchamp MC, Gu J, Lau S, Pollak MN, Bruchim I,. 2008. In vitro metformin anti-neoplastic activity in epithelial ovarian cancer. Gynecol Oncol 110: 246-250.
44. Guddati AM,. 2012. Ovarian cancer stem cells: Elusive targets for chemotherapy. Med Oncol May 26 [Epub ahead of print].
45. Guo Y, Nemeth J, O'Brien C, Susa M, Liu X, Zhang Z, Choy E, Mankin H, Hornicek F, Duan Z,. 2010. Effects of siltuximab on the IL-6-induced signaling pathway in ovarian cancer. Clin Cancer Res 16: 5759-5769.
46. Haviv I, Thompson EW,. 2012. Soiling the seed: Microenvironment and epithelial mesenchymal plasticity. Cancer Microenviron 5: 1-3.
47. Heider KH, Kuthan H, Stehle G, Munzert G,. 2004. CD44v6: A target for antibody-based cancer therapy. Cancer Immunol Immunother 53: 567-579.
48. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, Bruns CJ, Heeschen C,. 2007. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1: 313-323.
49. Hill RP,. 2006. Identifying cancer stem cells in solid tumors: Case not proven. Cancer Res 66: 1891-1895; discussion 1890.
50. Hosonuma S, Kobayashi Y, Kojo S, Wada H, Seino K, Kiguchi K, Ishizuka B,. 2011. Clinical significance of side population in ovarian cancer cells. Hum Cell 24: 9-12.
51. Hu X, Macdonald DM, Huettner PC, Feng Z, El Naqa IM, Schwarz JK, Mutch DG, Grigsby PW, Powell SN, Wang X,. 2009. A miR-200 microRNA cluster as prognostic marker in advanced ovarian cancer. Gynecol Oncol 114: 457-464.
52. Hu L, McArthur C, Jaffe RB,. 2010. Ovarian cancer stem-like side-population cells are tumourigenic and chemoresistant. Br J Cancer 102: 1276-1283.
53. Huber MA, Kraut N, Beug H,. 2005. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol 17: 548-558.
54. Huh WK, Sill MW, Darcy KM, Elias KM, Hoffman JS, Boggess JF, Alvarez RD, Long HJ, O'Malley DM, Birrer MJ,. 2010. Efficacy and safety of imatinib mesylate (Gleevec) and immunohistochemical expression of c-Kit and PDGFR-beta in a Gynecologic Oncology Group Phase Il Trial in women with recurrent or persistent carcinosarcomas of the uterus. Gynecol Oncol 117: 248-254.
55. Ieda M, Fu JD, Delgado-Olguin P, Vedantham V, Hayashi Y, Bruneau BG, Srivastava D,. 2010. Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 142: 375-386.
56. Jazaeri AA, Bryant JL, Park H, Li H, Dahiya N, Stoler MH, Ferriss JS, Dutta A,. 2011. Molecular requirements for transformation of fallopian tube epithelial cells into serous carcinoma. Neoplasia 13: 899-911.
57. Jazedje T, Perin PM, Czeresnia CE, Maluf M, Halpern S, Secco M, Bueno DF, Vieira NM, Zucconi E, Zatz M,. 2009. Human fallopian tube: A new source of multipotent adult mesenchymal stem cells discarded in surgical procedures. J Transl Med 7: 46.
58. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ,. 2009. Cancer statistics, 2009. CA Cancer J Clin 59: 225-249.
59. Karst AM, Drapkin R,. 2010. Ovarian cancer pathogenesis: A model in evolution. J Oncol 2010: 932371.
60. Karst AM, Levanon K, Drapkin R,. 2011. Modeling high-grade serous ovarian carcinogenesis from the fallopian tube. Proc Natl Acad Sci USA 108: 7547-7552.
61. Kelly PN, Dakic A, Adams JM, Nutt SL, Strasser A,. 2007. Tumor growth need not be driven by rare cancer stem cells. Science 317: 337.
62. Kindelberger DW, Lee Y, Miron A, Hirsch MS, Feltmate C, Medeiros F, Callahan MJ, Garner EO, Gordon RW, Birch C, Berkowitz RS, Muto MG, Crum CP,. 2007. Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: Evidence for a causal relationship. Am J Surg Pathol 31: 161-169.
63. Kristiansen G, Denkert C, Schluns K, Dahl E, Pilarsky C, Hauptmann S,. 2002. CD24 is expressed in ovarian cancer and is a new independent prognostic marker of patient survival. Am J Pathol 161: 1215-1221.
64. Kryczek I, Liu S, Roh M, Vatan L, Szeliga W, Wei S, Banerjee M, Mao Y, Kotarski J, Wicha MS, Liu R, Zou W,. 2012. Expression of aldehyde dehydrogenase and CD133 defines ovarian cancer stem cells. Int J Cancer 130: 29-39.
65. Kuhn E, Kurman RJ, Shih IM,. 2012. Ovarian cancer is an imported disease: Fact or fiction ? Curr Obstet Gynecol Rep 1: 1-9.
66. Kumar MS, Erkeland SJ, Pester RE, Chen CY, Ebert MS, Sharp PA, Jacks T,. 2008. Suppression of non-small cell lung tumor development by the let-7 microRNA family. Proc Natl Acad Sci USA 105: 3903-3908.
67. Kurman RJ, Shih Ie M,. 2008. Pathogenesis of ovarian cancer: Lessons from morphology and molecular biology and their clinical implications. Int J Gynecol Pathol 27: 151-160.
68. Kurtz JE, Dufour P,. 2010. Adecatumumab: An anti-EpCAM monoclonal antibody, from the bench to the bedside. Expert Opin Biol Ther 10: 951-958.
69. Landen CN, Jr., Goodman B, Katre AA, Steg AD, Nick AM, Stone RL, Miller LD, Mejia PV, Jennings NB, Gershenson DM, Bast RC, Jr., Coleman RL, Lopez-Berestein G, Sood AK,. 2010. Targeting aldehyde dehydrogenase cancer stem cells in ovarian cancer. Mol Cancer Ther 9: 3186-3199.
70. Latifi A, Abubaker K, Castrechini N, Ward AC, Liongue C, Dobill F, Kumar J, Thompson EW, Quinn MA, Findlay JK, Ahmed N,. 2011. Cisplatin treatment of primary and metastatic epithelial ovarian carcinomas generates residual cells with mesenchymal stem cell-like profile. J Cell Biochem. 112: 2850-2864.
71. Lee CM, Shvartsman H, Deavers MT, Wang SC, Xia W, Schmandt R, Bodurka DC, Atkinson EN, Malpica A, Gershenson DM, Hung MC, Lu KH,. 2003. beta-catenin nuclear localization is associated with grade in ovarian serous carcinoma. Gynecol Oncol 88: 363-368.
72. Lee JH, Canny MD, De Erkenez A, Krilleke D, Ng YS, Shima DT, Pardi A, Jucker F,. 2005. A therapeutic aptamer inhibits angiogenesis by specifically targeting the heparin binding domain of VEGF165. Proc Natl Acad Sci USA 102: 18902-18907.
73. Lee Y, Miron A, Drapkin R, Nucci MR, Medeiros F, Saleemuddin A, Garber J, Birch C, Mou H, Gordon RW, Cramer DW, McKeon FD, Crum CP,. 2007. A candidate precursor to serous carcinoma that originates in the distal fallopian tube. J Pathol 211: 26-35.
74. Lengyel E,. 2010. Ovarian cancer development and metastasis. Am J Pathol 177: 1053-1064.
75. Leskela S, Leandro-Garcia LJ, Mendiola M, Barriuso J, Inglada-Perez L, Munoz I, Martinez-Delgado B, Redondo A, de Santiago J, Robledo M, Hardisson D, Rodriguez-Antona C,. 2010. The miR-200 family controls beta-tubulin III expression and is associated with paclitaxel-based treatment response and progression-free survival in ovarian cancer patients. Endocr Relat Cancer 18: 85-95.
76. Levanon K, Crum C, Drapkin R,. 2008. New insights into the pathogenesis of serous ovarian cancer and its clinical impact. J Clin Oncol 26: 5284-5293.
77. Levanon K, Ng V, Piao HY, Zhang Y, Chang MC, Roh MH, Kindelberger DW, Hirsch MS, Crum CP, Marto JA, Drapkin R,. 2010. Primary ex vivo cultures of human fallopian tube epithelium as a model for serous ovarian carcinogenesis. Oncogene 29: 1103-1113.
78. Liao H, Zhou Q, Gu Y, Duan T, Feng Y,. 2012. Luteinizing hormone facilitates angiogenesis in ovarian epithelial tumor cells and metformin inhibits the effect through the mTOR signaling pathway. Oncol Rep 27: 1873-1878.
79. 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. Exp Mol Pathol 91: 596-602.
80. Marhaba R, Klingbeil P, Nuebel T, Nazarenko I, Buechler MW, Zoeller M,. 2008. CD44 and EpCAM: Cancer-initiating cell markers. Curr Mol Med 8: 784-804.
81. Matei D, Emerson RE, Schilder J, Menning N, Baldridge LA, Johnson CS, Breen T, McClean J, Stephens D, Whalen C, Sutton G,. 2008. Imatinib mesylate in combination with docetaxel for the treatment of patients with advanced, platinum-resistant ovarian cancer and primary peritoneal carcinomatosis: A Hoosier Oncology Group trial. Cancer 113: 723-732.
82. McClanahan T, Koseoglu S, Smith K, Grein J, Gustafson E, Black S, Kirschmeier P, Samatar AA,. 2006. Identification of overexpression of orphan G protein-coupled receptor GPR49 in human colon and ovarian primary tumors. Cancer Biol Ther 5: 419-426.
83. Medeiros F, Muto MG, Lee Y, Elvin JA, Callahan MJ, Feltmate C, Garber JE, Cramer DW, Crum CP,. 2006. The tubal fimbria is a preferred site for early adenocarcinoma in women with familial ovarian cancer syndrome. Am J Surg Pathol 30: 230-236.
84. Meng E, Long B, Sullivan P, McClellan S, Finan MA, Reed E, Shevde L, Rocconi RP,. 2012. CD44+/CD24-ovarian cancer cells demonstrate cancer stem cell properties and correlate to survival. Clin Exp Metastasis May 18 [Epub ahead of print].
85. Mimeault M, Batra SK,. 2008. Targeting of cancer stem/progenitor cells plus stem cell-based therapies: The ultimate hope for treating and curing aggressive and recurrent cancers. Panminerva Med 50: 3-18.
86. Missailidis S, Hardy A,. 2009. Aptamers as inhibitors of target proteins. Expert Opin Ther Pat 19: 1073-1082.
87. Morris RJ, Liu Y, Marles L, Yang Z, Trempus C, Li S, Lin JS, Sawicki JA, Cotsarelis G,. 2004. Capturing and profiling adult hair follicle stem cells. Nat Biotechnol 22: 411-417.
88. Mundhenke C, Weigel MT, Sturner KH, Roesel F, Meinhold-Heerlein I, Bauerschlag DO, Schem C, Hilpert F, Jonat W, Maass N,. 2008. Novel treatment of ovarian cancer cell lines with Imatinib mesylate combined with Paclitaxel and Carboplatin leads to receptor-mediated antiproliferative effects. J Cancer Res Clin Oncol 134: 1397-1405.
89. Murdoch WJ, Martinchick JF,. 2004. Oxidative damage to DNA of ovarian surface epithelial cells affected by ovulation: Carcinogenic implication and chemoprevention. Exp Biol Med (Maywood) 229: 546-552.
90. Oliver TG, Mercer KL, Sayles LC, Burke JR, Mendus D, Lovejoy KS, Cheng MH, Subramanian A, Mu D, Powers S, Crowley D, Bronson RT, Whittaker CA, Bhutkar A, Lippard SJ, Golub T, Thomale J, Jacks T, Sweet-Cordero EA,. 2010. Chronic cisplatin treatment promotes enhanced damage repair and tumor progression in a mouse model of lung cancer. Genes Dev 24: 837-852.
91. Orian-Rousseau V,. 2010. CD44, a therapeutic target for metastasising tumours. Eur J Cancer 46: 1271-1277.
92. Ozols RF,. 2006. Systemic therapy for ovarian cancer: Current status and new treatments. Semin Oncol 33: S3-S11.
93. Ozols RF, Bookman MA, Connolly DC, Daly MB, Godwin AK, Schilder RJ, Xu X, Hamilton TC,. 2004. Focus on epithelial ovarian cancer. Cancer Cell 5: 19-24.
94. Palacios J, Gamallo C,. 1998. Mutations in the beta-catenin gene (CTNNB1) in endometrioid ovarian carcinomas. Cancer Res 58: 1344-1347.
95. Peng S, Maihle NJ, Huang Y,. 2010. Pluripotency factors Lin28 and Oct4 identify a sub-population of stem cell-like cells in ovarian cancer. Oncogene 29: 2153-2159.
96. Permuth-Wey J, Sellers TA,. 2009. Epidemiology of ovarian cancer. Methods Mol Biol 472: 413-437.
97. Piek JM, van Diest PJ, Zweemer RP, Jansen JW, Poort-Keesom RJ, Menko FH, Gille JJ, Jongsma AP, Pals G, Kenemans P, Verheijen RH,. 2001. Dysplastic changes in prophylactically removed Fallopian tubes of women predisposed to developing ovarian cancer. J Pathol 195: 451-456.
98. Piek JM, Torrenga B, Hermsen B, Verheijen RH, Zweemer RP, Gille JJ, Kenemans P, van Diest PJ, Menko FH,. 2003. Histopathological characteristics of BRCA1- and BRCA2-associated intraperitoneal cancer: A clinic-based study. Fam Cancer 2: 73-78.
99. Pu Y, Zhu Z, Liu H, Zhang J, Liu J, Tan W,. 2010. Using aptamers to visualize and capture cancer cells. Anal Bioanal Chem 397: 3225-3233.
100. Rask K, Nilsson A, Brannstrom M, Carlsson P, Hellberg P, Janson PO, Hedin L, Sundfeldt K,. 2003. Wnt-signalling pathway in ovarian epithelial tumours: Increased expression of beta-catenin and GSK3beta. Br J Cancer 89: 1298-1304.
101. Resnick KE, Alder H, Hagan JP, Richardson DL, Croce CM, Cohn DE,. 2009. The detection of differentially expressed microRNAs from the serum of ovarian cancer patients using a novel real-time PCR platform. Gynecol Oncol 112: 55-59.
102. Ricken A, Lochhead P, Kontogiannea M, Farookhi R,. 2002. Wnt signaling in the ovary: Identification and compartmentalized expression of wnt-2, wnt-2b, and frizzled-4 mRNAs. Endocrinology 143: 2741-2749.
103. Risch HA, McLaughlin JR, Cole DE, Rosen B, Bradley L, Fan I, Tang J, Li S, Zhang S, Shaw PA, Narod SA,. 2006. Population BRCA1 and BRCA2 mutation frequencies and cancer penetrances: A kin-cohort study in Ontario, Canada. J Natl Cancer Inst 98: 1694-1706.
104. Rizzo S, Hersey JM, Mellor P, Dai W, Santos-Silva A, Liber D, Luk L, Titley I, Carden CP, Box G, Hudson DL, Kaye SB, Brown R,. 2011. Ovarian cancer stem cell-like side populations are enriched following chemotherapy and overexpress EZH2. Mol Cancer Ther 10: 325-335.
105. Rogakou EP, Boon C, Redon C, Bonner WM,. 1999. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146: 905-916.
106. Ruiz-Vela A, Aguilar-Gallardo C, Martinez-Arroyo AM, Soriano-Navarro M, Ruiz V, Simon C,. 2011. Specific unsaturated fatty acids enforce the transdifferentiation of human cancer cells toward adipocyte-like cells. Stem Cell Rev 7: 898-909.
107. Saad AF, Hu W, Sood AK,. 2010. Microenvironment and pathogenesis of epithelial ovarian cancer. Horm Cancer 1: 277-290.
108. Schatton T, Murphy GF, Frank NY, Yamaura K, Waaga-Gasser AM, Gasser M, Zhan Q, Jordan S, Duncan LM, Weishaupt C, Fuhlbrigge RC, Kupper TS, Sayegh MH, Frank MH,. 2008. Identification of cells initiating human melanomas. Nature 451: 345-349.
109. Schauer IG, Sood AK, Mok S, Liu J,. 2011. Cancer-associated fibroblasts and their putative role in potentiating the initiation and development of epithelial ovarian cancer. Neoplasia 13: 393-405.
110. Scheil-Bertram S, Tylus-Schaaf P, du Bois A, Harter P, Oppitz M, Ewald-Riegler N, Fisseler-Eckhoff A,. 2010. Excision repair cross- complementation group 1 protein overexpression as a predictor of poor survival for high-grade serous ovarian adenocarcinoma. Gynecol Oncol 119: 325-331.
111. Schilder RJ, Sill MW, Lee RB, Shaw TJ, Senterman MK, Klein-Szanto AJ, Miner Z, Vanderhyden BC,. 2008. Phase II evaluation of imatinib mesylate in the treatment of recurrent or persistent epithelial ovarian or primary peritoneal carcinoma: A Gynecologic Oncology Group Study. J Clin Oncol 26: 3418-3425.
112. Seimetz D, Lindhofer H, Bokemeyer C,. 2010. Development and approval of the trifunctional antibody catumaxomab (anti-EpCAM x anti-CD3) as a targeted cancer immunotherapy. Cancer Treat Rev 36: 458-467.
113. Sell S,. 2004. Stem cell origin of cancer and differentiation therapy. Crit Rev Oncol Hematol 51: 1-28.
114. Semple RK, Chatterjee VK, O'Rahilly S,. 2006. PPAR gamma and human metabolic disease. J Clin Invest 116: 581-589.
115. Shigdar S, Lin J, Yu Y, Pastuovic M, Wei M, Duan W,. 2011. RNA aptamer against a cancer stem cell marker epithelial cell adhesion molecule. Cancer Sci 102: 991-998.
116. Silva IA, Bai S, McLean K, Yang K, Griffith K, Thomas D, Ginestier C, Johnston C, Kueck A, Reynolds RK, Wicha MS, Buckanovich RJ,. 2011. Aldehyde dehydrogenase in combination with CD133 defines angiogenic ovarian cancer stem cells that portend poor patient survival. Cancer Res 71: 3991-4001.
117. Smith LM, Nesterova A, Ryan MC, Duniho S, Jonas M, Anderson M, Zabinski RF, Sutherland MK, Gerber HP, Van Orden KL, Moore PA, Ruben SM, Carter PJ,. 2008. CD133/prominin-1 is a potential therapeutic target for antibody-drug conjugates in hepatocellular and gastric cancers. Br J Cancer 99: 100-109.
118. Society AC,. 2007. Cancer facts and figures. www.cancer.org.
119. Soignet SL, Benedetti F, Fleischauer A, Parker BA, Truglia JA, Ra Crisp M, Warrell RP, Jr., 1998. Clinical study of 9-cis retinoic acid (LGD1057) in acute promyelocytic leukemia. Leukemia 12: 1518-1521.
120. Spizzo G, Went P, Dirnhofer S, Obrist P, Moch H, Baeuerle PA, Mueller-Holzner E, Marth C, Gastl G, Zeimet AG,. 2006. Overexpression of epithelial cell adhesion molecule (Ep-CAM) is an independent prognostic marker for reduced survival of patients with epithelial ovarian cancer. Gynecol Oncol 103: 483-488.
121. Staud F, Pavek P,. 2005. Breast cancer resistance protein (BCRP/ABCG2). Int J Biochem Cell Biol 37: 720-725.
122. Steg AD, Katre AA, Goodman B, Han HD, Nick AM, Stone RL, Coleman RL, Alvarez RD, Lopez-Berestein G, Sood AK, Landen CN,. 2011. Targeting the notch ligand JAGGED1 in both tumor cells and stroma in ovarian cancer. Clin Cancer Res 17: 5674-5685.
123. Steg AD, Bevis KS, Katre AA, Ziebarth A, Dobbin ZC, Alvarez RD, Zhang K, Conner M, Landen CN,. 2012a. Stem cell pathways contribute to clinical chemoresistance in ovarian cancer. Clin Cancer Res 18: 869-881.
124. Steg AD, Katre AA, Bevis KS, Ziebarth A, Dobbin ZC, Shah MM, Alvarez RD, Landen CN, Jr., 2012b. Smoothened Antagonists Reverse Taxane Resistance in Ovarian Cancer. Mol Cancer Ther 11: 1587-1597.
125. 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. Proc Natl Acad Sci USA 103: 11154-11159.
126. Szotek PP, Chang HL, Brennand K, Fujino A, Pieretti-Vanmarcke R, Lo Celso C, Dombkowski D, Preffer F, Cohen KS, Teixeira J, Donahoe PK,. 2008. Normal ovarian surface epithelial label-retaining cells exhibit stem/progenitor cell characteristics. Proc Natl Acad Sci USA 105: 12469-12473.
127. Tanese K, Fukuma M, Yamada T, Mori T, Yoshikawa T, Watanabe W, Ishiko A, Amagai M, Nishikawa T, Sakamoto M,. 2008. G-protein-coupled receptor GPR49 is up-regulated in basal cell carcinoma and promotes cell proliferation and tumor formation. Am J Pathol 173: 835-843.
128. Taylor DD, Gercel-Taylor C,. 2008. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 110: 13-21.
129. Thorsen SB, Obad S, Jensen NF, Stenvang J, Kauppinen S,. 2012. The therapeutic potential of MicroRNAs in cancer. Cancer J 18: 275-284.
130. van der Gun BT, Melchers LJ, Ruiters MH, de Leij LF, McLaughlin PM, Rots MG,. 2010. EpCAM in carcinogenesis: The good, the bad or the ugly. Carcinogenesis 31: 1913-1921.
131. van Jaarsveld MT, Helleman J, Berns EM, Wiemer EA,. 2010. MicroRNAs in ovarian cancer biology and therapy resistance. Int J Biochem Cell Biol 42: 1282-1290.
132. Vathipadiekal V, Saxena D, Mok SC, Hauschka PV, Ozbun L, Birrer MJ,. 2012. Identification of a potential ovarian cancer stem cell gene expression profile from advanced stage papillary serous ovarian cancer. PLoS ONE 7: e29079.
133. Vierbuchen T, Ostermeier A, Pang ZP, Kokubu Y, Sudhof TC, Wernig M,. 2010. Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463: 1035-1041.
134. Vignati S, Albertini V, Rinaldi A, Kwee I, Riva C, Oldrini R, Capella C, Bertoni F, Carbone GM, Catapano CV,. 2006. Cellular and molecular consequences of peroxisome proliferator-activated receptor-gamma activation in ovarian cancer cells. Neoplasia 8: 851-861.
135. Virant-Klun I, Zech N, Rozman P, Vogler A, Cvjeticanin B, Klemenc P, Malicev E, Meden-Vrtovec H,. 2008. Putative stem cells with an embryonic character isolated from the ovarian surface epithelium of women with no naturally present follicles and oocytes. Differentiation 76: 843-856.
136. Wang YC, Yo YT, Lee HY, Liao YP, Chao TK, Su PH, Lai HC,. 2012. ALDH1-bright epithelial ovarian cancer cells are associated with CD44 expression, drug resistance, and poor clinical outcome. Am J Pathol 180: 1159-1169.
137. Wooster R, Weber BL,. 2003. Breast and ovarian cancer. N Engl J Med 348: 2339-2347.
138. Wright K, Wilson P, Morland S, Campbell I, Walsh M, Hurst T, Ward B, Cummings M, Chenevix-Trench G,. 1999. beta-catenin mutation and expression analysis in ovarian cancer: Exon 3 mutations and nuclear translocation in 16% of endometrioid tumours. Int J Cancer 82: 625-629.
139. Wu Q, Guo R, Lin M, Zhou B, Wang Y,. 2011. MicroRNA-200a inhibits CD133/1+ ovarian cancer stem cells migration and invasion by targeting E-cadherin repressor ZEB2. Gynecol Oncol 122: 149-154.
140. Xu K, Liang X, Shen K, Cui D, Zheng Y, Xu J, Fan Z, Qiu Y, Li Q, Ni L, Liu J,. 2012a. MiR-297 modulate multidrug resistance in human colorectal carcinoma by down-regulating MRP-2. Biochem J 446: 291-300.
141. Xu K, Liang X, Shen K, Sun L, Cui D, Zhao Y, Tian J, Ni L, Liu J,. 2012b. MiR-222 modulate multidrug resistance in human colorectal carcinoma by down-regulating ADAM-17. Exp Cell Res 318: 2168-2177.
142. Yamashita T, Ji J, Budhu A, Forgues M, Yang W, Wang HY, Jia H, Ye Q, Qin LX, Wauthier E, Reid LM, Minato H, Honda M, Kaneko S, Tang ZY, Wang XW,. 2009. EpCAM-positive hepatocellular carcinoma cells are tumor-initiating cells with stem/progenitor cell features. Gastroenterology 136: 1012-1024.
143. Yang X, Lin X, Zhong X, Kaur S, Li N, Liang S, Lassus H, Wang L, Katsaros D, Montone K, Zhao X, Zhang Y, Butzow R, Coukos G, Zhang L,. 2010. Double-negative feedback loop between reprogramming factor LIN28 and microRNA let-7 regulates aldehyde dehydrogenase 1-positive cancer stem cells. Cancer Res 70: 9463-9472.
144. Zhang GY, Ahmed N, Riley C, Oliva K, Barker G, Quinn MA, Rice GE,. 2005. Enhanced expression of peroxisome proliferator-activated receptor gamma in epithelial ovarian carcinoma. Br J Cancer 92: 113-119.
145. 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 Res 68: 4311-4320.
146. Zhong X, Li N, Liang S, Huang Q, Coukos G, Zhang L,. 2010. Identification of microRNAs regulating reprogramming factor LIN28 in embryonic stem cells and cancer cells. J Biol Chem 285: 41961-41971.
147. Zhou S, Schuetz JD, Bunting KD, Colapietro AM, Sampath J, Morris JJ, Lagutina I, Grosveld GC, Osawa M, Nakauchi H, Sorrentino BP,. 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. Nat Med 7: 1028-1034.