Ovarian cancer stem cells: Elusive targets for chemotherapy

Medical Oncology

Volumn 29, Issue 5, 2012, Pages 3400-3408

  Guddati, Achuta Kumar ^a  

^a ST VINCENT S MEDICAL CENTER   (United States)

Author keywords

Cancer stem cells; Chemotherapy; Ovarian cancer; Side population; Target

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER C2; ALDEHYDE DEHYDROGENASE; ALPHA INTERFERON; BEVACIZUMAB; BIOLOGICAL MARKER; BMI1 PROTEIN; CARBOPLATIN; CD133 ANTIGEN; CISPLATIN; DOCETAXEL; DOXORUBICIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPITHELIAL CELL ADHESION MOLECULE; EPOTHILONE B; HERMES ANTIGEN; LIN28 PROTEIN; MICRORNA 214; MULTIDRUG RESISTANCE PROTEIN 1; OCTAMER TRANSCRIPTION FACTOR 4; PACLITAXEL; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN; PROTEIN KINASE B; PROTEIN P53; STEM CELL FACTOR RECEPTOR; TOPOTECAN; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT;

ASYMMETRIC DIVISION; CANCER CHEMOTHERAPY; CANCER PROGNOSIS; CANCER RESISTANCE; CANCER STEM CELL; CANCER SURVIVAL; CELL DIVISION; CELL ISOLATION; CELL LABELING; DISEASE FREE SURVIVAL; EPITHELIAL MESENCHYMAL TRANSITION; GENE OVEREXPRESSION; HUMAN; OVARY CANCER; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; REVIEW; RNA INTERFERENCE; SALVAGE THERAPY; SIDE POPULATION CELL; TUMOR RECURRENCE; TUMOR SUPPRESSOR GENE; DRUG EFFECT; FEMALE; OVARY TUMOR; PATHOLOGY;

ANTINEOPLASTIC AGENTS; FEMALE; HUMANS; NEOPLASTIC STEM CELLS; OVARIAN NEOPLASMS;

EID: 84880322222     PISSN: 13570560     EISSN: 1559131X     Source Type: Journal    
DOI: 10.1007/s12032-012-0252-6     Document Type: Review

References (123)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin. 2010;60(5):277-300. doi: 10.3322/caac.20073.
2. Wikborn C, Pettersson F, Moberg PJ. Delay in diagnosis of epithelial ovarian cancer. Int J Gynaecol Obstet. 1996;52(3):263-7.
3. Martin LP, Schilder RJ. Management of recurrent ovarian carcinoma: current status and future directions. Semin Oncol. 2009;36(2):112-25. doi: 10.1053/j.seminoncol.2008.12.003.
4. Griffiths C. Surgical resection of tumor bulk in the primary treatment of ovarian carcinoma. Nat Cancer Inst Monogr. 1975;42:101-4.
5. Bristow RE, Puri I, Chi DS. Cytoreductive surgery for recurrent ovarian cancer: a meta-analysis. Gynecol Oncol. 2009;112(1):265-74. doi: 10.1016/j.ygyno.2008.08.033.
6. Chen VW, Ruiz B, Killeen JL, Cote TR, Wu XC, Correa CN. Pathology and classification of ovarian tumors. Cancer. 2003;97(10 Suppl):2631-42. doi: 10.1002/cncr.11345.
7. Tavassoli FA, Devilee P, International Agency for Research on Cancer., World Health Organization (2003) Pathology and genetics of tumours of the breast and female genital organs. World Health Organization classification of tumours. IAPS Press, Lyon.
8. Karst AM, Drapkin R. Ovarian cancer pathogenesis: a model in evolution. J Oncol. 2010;2010:932371. doi: 10.1155/2010/932371.
9. Dubeau L. The cell of origin of ovarian epithelial tumours. Lancet Oncol. 2008;9:1191-7.
10. Ness RB, Cottreau C. Possible role of ovarian epithelial inflammation in ovarian cancer. J Natl Cancer Inst. 1999;91(17):1459-67.
11. Ahmed N, Maines-Bandiera S, Quinn MA, Unger WG, Dedhar S, Auersperg N. Molecular pathways regulating EGF-induced epithelio-mesenchymal transition in human ovarian surface epithelium. Am J Physiol Cell Physiol. 2006;290(6):C1532-42. doi: 10.1152/ajpcell.00478.2005.
12. Leeper K, Garcia R, Swisher E, Goff B, Greer B, Paley P. Pathologic findings in prophylactic oophorectomy specimens in high-risk women. Gynecol Oncol. 2002;87(1):52-6.
13. Carcangiu ML, Radice P, Manoukian S, Spatti G, Gobbo M, Pensotti V, Crucianelli R, Pasini B. Atypical epithelial proliferation in fallopian tubes in prophylactic salpingo-oophorectomy specimens from BRCA1 and BRCA2 germline mutation carriers. Int J Gynecol Pathol. 2004;23(1):35-40. doi: 10.1097/01.pgp.0000101082.35393.84.
14. Kindelberger DWLY, Miron A, Hirsch MS, Feltmate C, Medeiros F, Callahan MJ, Garner EO, Gordon RW, Birch C, Berkowitz RS, Muto MG, Crum CP. Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: Evidence for a causal relationship. Am J Surg Pathol. 2007;31(2):161-9.
15. Folkins AK, Jarboe EA, Saleemuddin A, Lee Y, Callahan MJ, Drapkin R, Garber JE, Muto MG, Tworoger S, Crum CP. A candidate precursor to pelvic serous cancer (p53 signature) and its prevalence in ovaries and fallopian tubes from women with BRCA mutations. Gynecol Oncol. 2008;109(2):168-73. doi: 10.1016/j.ygyno.2008.01.012.
16. Jazedje T, Perin PM, Czeresnia CE, Maluf M, Halpern S, Secco M, Bueno DF, Vieira NM, Zucconi E, Zatz M. Human fallopian tube: a new source of multipotent adult mesenchymal stem cells discarded in surgical procedures. J Transl Med. 2009;7:46. doi: 10.1186/1479-5876-7-46.
17. Finch ABM, Lubinski J, Lynch HT, Moller P, Rosen B, Murphy J, Ghadirian P, Friedman E, Foulkes WD, Kim-Sing C, Wagner T, Tung N, Couch F, Stoppa-Lyonnet D, Ainsworth P, Daly M, Pasini B, Gershoni-Baruch R, Eng C, Olopade OI, McLennan J, Karlan B, Weitzel J, Sun P, Narod SA, Hereditary Ovarian Cancer Clinical Study Group. Salpingo-oophorectomy and the risk of ovarian, fallopian tube, and peritoneal cancers in women with a BRCA1 or BRCA2 Mutation. J Am Med Assoc. 2006;296(2):185-92.
18. Wolff EF, Wolff AB, Hongling D, Taylor HS. Demonstration of multipotent stem cells in the adult human endometrium by in vitro chondrogenesis. Reprod Sci. 2007;14(6):524-33. doi: 10.1177/1933719107306896.
19. Schwab KE, Hutchinson P, Gargett CE. Identification of surface markers for prospective isolation of human endometrial stromal colony-forming cells. Hum Reprod. 2008;23(4):934-43. doi: 10.1093/humrep/den051.
20. King SM, Burdette JE. Evaluating the progenitor cells of ovarian cancer: analysis of current animal models. BMB Rep. 2011;44(7):435-45. doi: 10.5483/BMBRep.2011,44(7),pp.435.
21. Shih Ie M, Kurman RJ. Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis. Am J Pathol. 2004;164(5):1511-8.
22. Singer G, Stohr R, Cope L, Dehari R, Hartmann A, Cao DF, Wang TL, Kurman RJ, Shih IM. Patterns of p53 mutations separate ovarian serous borderline tumors and low- and high-grade carcinomas and provide support for a new model of ovarian carcinogenesis: a mutational analysis with immunohistochemical correlation. Am J Surg Pathol. 2005;29(2):218-24.
23. Singer G, Oldt R 3rd, Cohen Y, Wang BG, Sidransky D, Kurman RJ, Shih IM. Mutations in BRAF and KRAS characterize the development of low-grade ovarian serous carcinoma. J Natl Cancer Inst. 2003;95(6):484-6.
24. Ahmed AA, Etemadmoghadam D, Temple J, Lynch AG, Riad M, Sharma R, Stewart C, Fereday S, Caldas C, Defazio A, Bowtell D, Brenton JD. Driver mutations in TP53 are ubiquitous in high grade serous carcinoma of the ovary. J Pathol. 2010;221(1):49-56. doi: 10.1002/path.2696.
25. Samimi G, Fink D, Varki NM, Husain A, Hoskins WJ, Alberts DS, Howell SB. Analysis of MLH1 and MSH2 expression in ovarian cancer before and after platinum drug-based chemotherapy. Clin Cancer Res. 2000;6(4):1415-21.
26. Tothill RW, Tinker AV, George J, Brown R, Fox SB, Lade S, Johnson DS, Trivett MK, Etemadmoghadam D, Locandro B, Traficante N, Fereday S, Hung JA, Chiew YE, Haviv I, Gertig D, DeFazio A, Bowtell DD. Novel molecular subtypes of serous and endometrioid ovarian cancer linked to clinical outcome. Clin Cancer Res. 2008;14(16):5198-208. doi: 10.1158/1078-0432.CCR-08-0196.
27. Bonome T, Lee JY, Park DC, Radonovich M, Pise-Masison C, Brady J, Gardner GJ, Hao K, Wong WH, Barrett JC, Lu KH, Sood AK, Gershenson DM, Mok SC, Birrer MJ. Expression profiling of serous low malignant potential, low-grade, and high-grade tumors of the ovary. Cancer Res. 2005;65(22):10602-12. doi: 10.1158/0008-5472.CAN-05-2240.
28. White YA, Woods DC, Takai Y, Ishihara O, Seki H, Tilly JL. Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nat Med. 2012;18(3):413-21. doi: 10.1038/nm.2669.
29. Szotek PP, Chang HL, Brennand K, Fujino A, Pieretti-Vanmarcke R, Lo Celso C, Dombkowski D, Preffer F, Cohen KS, Teixeira J, Donahoe PK. Normal ovarian surface epithelial label-retaining cells exhibit stem/progenitor cell characteristics. Proc Natl Acad Sci USA. 2008;105(34):12469-73. doi: 10.1073/pnas.0805012105.
30. Virant-Klun I, Rozman P, Cvjeticanin B, Vrtacnik-Bokal E, Novakovic S, Rulicke T, Dovc P, Meden-Vrtovec H. Parthenogenetic embryo-like structures in the human ovarian surface epithelium cell culture in postmenopausal women with no naturally present follicles and oocytes. Stem Cells Dev. 2009;18(1):137-49. doi: 10.1089/scd.2007.0238.
31. Gou S, Liu T, Wang C, Yin T, Li K, Yang M, Zhou J. Establishment of clonal colony-forming assay for propagation of pancreatic cancer cells with stem cell properties. Pancreas. 2007;34(4):429-35. doi: 10.1097/MPA. 0b013e318033f9f4.
32. Dick JE, Bhatia M, Gan O, Kapp U, Wang JC (1997) Assay of human stem cells by repopulation of NOD/SCID mice. Stem Cells 15(Suppl 1):199-203; discussion 204-197. doi: 10.1002/stem.5530150826.
33. Lin KK, Goodell MA. Purification of hematopoietic stem cells using the side population. Methods Enzymol. 2006;420:255-64. doi: 10.1016/S0076-6879(06) 20011-9.
34. Alvi AJ, Clayton H, Joshi C, Enver T, Ashworth A, Vivanco MM, Dale TC, Smalley MJ. Functional and molecular characterisation of mammary side population cells. Breast Cancer Res. 2003;5(1):R1-8.
35. 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(7):3983-3988.
36. Szotek PP, Pieretti-Vanmarcke R, Masiakos PT, Dinulescu DM, Connolly D, Foster R, Dombkowski D, Preffer F, Maclaughlin DT, Donahoe PK. Ovarian cancer side population defines cells with stem cell-like characteristics and Mullerian Inhibiting Substance responsiveness. Proc Natl Acad Sci USA. 2006;103(30):11154-9. doi: 10.1073/pnas.0603672103.
37. Moshaver B, van Rhenen A, Kelder A, van der Pol M, Terwijn M, Bachas C, Westra AH, Ossenkoppele GJ, Zweegman S, Schuurhuis GJ. Identification of a small subpopulation of candidate leukemia-initiating cells in the side population of patients with acute myeloid leukemia. Stem Cells. 2008;26(12):3059-67. doi: 10.1634/stemcells.2007-0861.
38. Zhang HB, Ren CP, Yang XY, Wang L, Li H, Zhao M, Yang H, Yao KT. Identification of label-retaining cells in nasopharyngeal epithelia and nasopharyngeal carcinoma tissues. Histochem Cell Biol. 2007;127(3):347-54. doi: 10.1007/s00418-006-0251-9.
39. Kuwahara R, Kofman AV, Landis CS, Swenson ES, Barendswaard E, Theise ND. The hepatic stem cell niche: identification by label-retaining cell assay. Hepatology. 2008;47(6):1994-2002. doi: 10.1002/hep.22218.
40. Brown MD, Gilmore PE, Hart CA, Samuel JD, Ramani VA, George NJ, Clarke NW. Characterization of benign and malignant prostate epithelial Hoechst 33342 side populations. Prostate. 2007;67(13):1384-96. doi: 10.1002/pros.20620.
41. Addla SK, Brown MD, Hart CA, Ramani VA, Clarke NW. Characterization of the Hoechst 33342 side population from normal and malignant human renal epithelial cells. Am J Physiol Renal Physiol. 2008;295(3):F680-7. doi: 10.1152/ajprenal.90286.2008.
42. Hu L, McArthur C, Jaffe RB. Ovarian cancer stem-like side-population cells are tumourigenic and chemoresistant. Br J Cancer. 2010;102(8):1276-83. doi: 10.1038/sj.bjc.6605626.
43. Fillmore CM, Kuperwasser C. Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res. 2008;10(2):R25. doi: 10.1186/bcr1982.
44. Boutonnat J, Faussat AM, Marie JP, Bignon J, Wdzieczak-Bakala J, Barbier M, Thierry J, Ronot X, Colle PE. Usefulness of PKH fluorescent labelling to study leukemic cell proliferation with various cytostatic drugs or acetyl tetrapeptide-AcSDKP. BMC Cancer. 2005;5:120. doi: 10.1186/1471-2407-5-120.
45. Kusumbe AP, Bapat SA. Cancer stem cells and aneuploid populations within developing tumors are the major determinants of tumor dormancy. Cancer Res. 2009;69(24):9245-53. doi: 10.1158/0008-5472.CAN-09-2802.
46. Tang L, Bergevoet SM, Gilissen C, de Witte T, Jansen JH, van der Reijden BA, Raymakers RA. Hematopoietic stem cells exhibit a specific ABC transporter gene expression profile clearly distinct from other stem cells. BMC Pharmacol. 2010;10:12. doi: 10.1186/1471-2210-10-12.
47. Guo Y, Kock K, Ritter CA, Chen ZS, Grube M, Jedlitschky G, Illmer T, Ayres M, Beck JF, Siegmund W, Ehninger G, Gandhi V, Kroemer HK, Kruh GD, Schaich M. Expression of ABCC-type nucleotide exporters in blasts of adult acute myeloid leukemia: relation to long-term survival. Clin Cancer Res. 2009;15(5):1762-9. doi: 10.1158/1078-0432.CCR-08-0442.
48. Martin V, Xu J, Pabbisetty SK, Alonso MM, Liu D, Lee OH, Gumin J, Bhat KP, Colman H, Lang FF, Fueyo J, Gomez-Manzano C. Tie2-mediated multidrug resistance in malignant gliomas is associated with upregulation of ABC transporters. Oncogene. 2009;28(24):2358-63. doi: 10.1038/onc.2009.103.
49. Donnenberg VS, Meyer EM, Donnenberg AD. Measurement of multiple drug resistance transporter activity in putative cancer stem/progenitor cells. Methods Mol Biol. 2009;568:261-79. doi: 10.1007/978-1-59745-280-9-17.
50. Surowiak P, Materna V, Kaplenko I, Spaczynski M, Dolinska-Krajewska B, Gebarowska E, Dietel M, Zabel M, Lage H. ABCC2 (MRP2, cMOAT) can be localized in the nuclear membrane of ovarian carcinomas and correlates with resistance to cisplatin and clinical outcome. Clin Cancer Res. 2006;12(23):7149-58. doi: 10.1158/1078-0432.CCR-06-0564.
51. Materna V, Stege A, Surowiak P, Priebsch A, Lage H. RNA interference-triggered reversal of ABCC2-dependent cisplatin resistance in human cancer cells. Biochem Biophys Res Commun. 2006;348(1):153-7. doi: 10.1016/j.bbrc.2006.07.022.
52. Baekelandt MM, Holm R, Nesland JM, Trope CG, Kristensen GB. P-glycoprotein expression is a marker for chemotherapy resistance and prognosis in advanced ovarian cancer. Anticancer Res. 2000;20(2):1061-7.
53. Lu L, Katsaros D, Wiley A, Rigault de la Longrais IA, Puopolo M, Yu H. Expression of MDR1 in epithelial ovarian cancer and its association with disease progression. Oncol Res. 2007;16(8):395-403.
54. 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. Ovarian cancer stem cell-like side populations are enriched following chemotherapy and overexpress EZH2. Mol Cancer Ther. 2011;10(2):325-35. doi: 10.1158/1535-7163.MCT-10-0788.
55. Gao Q, Geng L, Kvalheim G, Gaudernack G, Suo Z. Identification of cancer stem-like side population cells in ovarian cancer cell line OVCAR-3. Ultrastruct Pathol. 2009;33(4):175-81. doi: 10.1080/01913120903086072.
56. Wang L, Mezencev R, Bowen NJ, Matyunina LV, McDonald JF. Isolation and characterization of stem-like cells from a human ovarian cancer cell line. Mol Cell Biochem. 2012;363(1-2):257-68. doi: 10.1007/s11010-011-1178-6.
57. Johnatty SE, Beesley J, Paul J, Fereday S, Spurdle AB, Webb PM, Byth K, Marsh S, McLeod H, Harnett PR, Brown R, DeFazio A, Chenevix-Trench G. ABCB1 (MDR 1) polymorphisms and progression-free survival among women with ovarian cancer following paclitaxel/carboplatin chemotherapy. Clin Cancer Res. 2008;14(17):5594-601. doi: 10.1158/1078-0432.CCR-08-0606.
58. Zheng LS, Wang F, Li YH, Zhang X, Chen LM, Liang YJ, Dai CL, Yan YY, Tao LY, Mi YJ, Yang AK, To KK, Fu LW. Vandetanib (Zactima, ZD6474) antagonizes ABCC1- and ABCG2-mediated multidrug resistance by inhibition of their transport function. PLoS ONE. 2009;4(4):e5172. doi: 10.1371/journal.pone.0005172.
59. Calcagno AM, Fostel JM, To KK, Salcido CD, Martin SE, Chewning KJ, Wu CP, Varticovski L, Bates SE, Caplen NJ, Ambudkar SV. Single-step doxorubicin-selected cancer cells overexpress the ABCG2 drug transporter through epigenetic changes. Br J Cancer. 2008;98(9):1515-24. doi: 10.1038/sj.bjc. 6604334.
60. Ma L, Lai D, Liu T, Cheng W, Guo L. Cancer stem-like cells can be isolated with drug selection in human ovarian cancer cell line SKOV3. Acta Biochim Biophys Sin (Shanghai). 2010;42(9):593-602. doi: 10.1093/abbs/gmq067.
61. Corbeil D, Roper K, Hellwig A, Tavian M, Miraglia S, Watt SM, Simmons PJ, Peault B, Buck DW, Huttner WB. The human AC133 hematopoietic stem cell antigen is also expressed in epithelial cells and targeted to plasma membrane protrusions. J Biol Chem. 2000;275(8):5512-20.
62. Vathipadiekal V, Saxena D, Mok SC, Hauschka PV, Ozbun L, Birrer MJ. Identification of a potential ovarian cancer stem cell gene expression profile from advanced stage papillary serous ovarian cancer. PLoS ONE. 2012;7(1):e29079. doi: 10.1371/journal.pone.0029079.
63. Hosonuma S, Kobayashi Y, Kojo S, Wada H, Seino K, Kiguchi K, Ishizuka B. Clinical significance of side population in ovarian cancer cells. Hum Cell. 2011;24(1):9-12. doi: 10.1007/s13577-010-0002-z.
64. Yue Z, Jiang TX, Widelitz RB, Chuong CM. Mapping stem cell activities in the feather follicle. Nature. 2005;438(7070):1026-9. doi: 10.1038/nature04222.
65. Kusumbe AP, Mali AM, Bapat SA. CD133-expressing stem cells associated with ovarian metastases establish an endothelial hierarchy and contribute to tumor vasculature. Stem Cells. 2009;27(3):498-508. doi: 10.1634/stemcells.2008- 0868.
66. Chen SF, Chang YC, Nieh S, Liu CL, Yang CY, Lin YS. Nonadhesive culture system as a model of rapid sphere formation with cancer stem cell properties. PLoS ONE. 2012;7(2):e31864. doi: 10.1371/journal.pone.0031864.
67. Pignata S, Scambia G, Ferrandina G, Savarese A, Sorio R, Breda E, Gebbia V, Musso P, Frigerio L, Del Medico P, Lombardi AV, Febbraro A, Scollo P, Ferro A, Tamberi S, Brandes A, Ravaioli A, Valerio MR, Aitini E, Natale D, Scaltriti L, Greggi S, Pisano C, Lorusso D, Salutari V, Legge F, Di Maio M, Morabito A, Gallo C, Perrone F. Carboplatin plus paclitaxel versus carboplatin plus pegylated liposomal doxorubicin as first-line treatment for patients with ovarian cancer: the MITO-2 randomized phase III trial. J Clin Oncol. 2011;29(27):3628-35. doi: 10.1200/JCO.2010.33.8566.
68. Jaaback K, Johnson N (2006) Intraperitoneal chemotherapy for the initial management of primary epithelial ovarian cancer. Cochrane Database Syst Rev (1):CD005340. doi: 10.1002/14651858.CD005340.pub2.
69. Gadducci A, Conte PF. Intraperitoneal chemotherapy in the management of patients with advanced epithelial ovarian cancer: a critical review of the literature. Int J Gynecol Cancer. 2008;18(5):943-53. doi: 10.1111/j.1525-1438. 2007.01163.x.
70. De Placido S, Scambia G, Di Vagno G, Naglieri E, Lombardi AV, Biamonte R, Marinaccio M, Carteni G, Manzione L, Febbraro A, De Matteis A, Gasparini G, Valerio MR, Danese S, Perrone F, Lauria R, De Laurentiis M, Greggi S, Gallo C, Pignata S. Topotecan compared with no therapy after response to surgery and carboplatin/paclitaxel in patients with ovarian cancer: multicenter Italian trials in ovarian cancer (MITO-1) randomized study. J Clin Oncol. 2004;22(13):2635-42. doi: 10.1200/JCO.2004.09.088.
71. Bolis G, Danese S, Tateo S, Rabaiotti E, D'Agostino G, Merisio C, Scarfone G, Polverino G, Parazzini F. Epidoxorubicin versus no treatment as consolidation therapy in advanced ovarian cancer: results from a phase II study. Int J Gynecol Cancer. 2006;16(Suppl 1):74-8. doi: 10.1111/j.1525-1438.2006. 00313.x.
72. Markman M, Liu PY, Wilczynski S, Monk B, Copeland LJ, Alvarez RD, Jiang C, Alberts D. Phase III randomized trial of 12 versus 3 months of maintenance paclitaxel in patients with advanced ovarian cancer after complete response to platinum and paclitaxel-based chemotherapy: a Southwest oncology group and gynecologic oncology group trial. J Clin Oncol. 2003;21(13):2460-5. doi: 10.1200/JCO.2003.07.013.
73. Pecorelli S, Favalli G, Gadducci A, Katsaros D, Panici PB, Carpi A, Scambia G, Ballardini M, Nanni O, Conte P. Phase III trial of observation versus six courses of paclitaxel in patients with advanced epithelial ovarian cancer in complete response after six courses of paclitaxel/platinum-based chemotherapy: final results of the After-6 protocol 1. J Clin Oncol. 2009;27(28):4642-8. doi: 10.1200/JCO.2009.21.9691.
74. Hall GD, Brown JM, Coleman RE, Stead M, Metcalf KS, Peel KR, Poole C, Crawford M, Hancock B, Selby PJ, Perren TJ. Maintenance treatment with interferon for advanced ovarian cancer: results of the Northern and Yorkshire gynaecology group randomised phase III study. Br J Cancer. 2004;91(4):621-6. doi: 10.1038/sj.bjc.6602037.
75. Berek J, Taylor P, McGuire W, Smith LM, Schultes B, Nicodemus CF. Oregovomab maintenance monoimmunotherapy does not improve outcomes in advanced ovarian cancer. J Clin Oncol. 2009;27(3):418-25. doi: 10.1200/JCO.2008.17.8400.
76. Verheijen RH, Massuger LF, Benigno BB, Epenetos AA, Lopes A, Soper JT, Markowska J, Vyzula R, Jobling T, Stamp G, Spiegel G, Thurston D, Falke T, Lambert J, Seiden MV. Phase III trial of intraperitoneal therapy with yttrium-90-labeled HMFG1 murine monoclonal antibody in patients with epithelial ovarian cancer after a surgically defined complete remission. J Clin Oncol. 2006;24(4):571-8. doi: 10.1200/JCO.2005.02.5973.
77. Perren TJ, Swart AM, Pfisterer J, Ledermann JA, Pujade-Lauraine E, Kristensen G, Carey MS, Beale P, Cervantes A, Kurzeder C, du Bois A, Sehouli J, Kimmig R, Stahle A, Collinson F, Essapen S, Gourley C, Lortholary A, Selle F, Mirza MR, Leminen A, Plante M, Stark D, Qian W, Parmar MK, Oza AM. A phase 3 trial of bevacizumab in ovarian cancer. N Engl J Med. 2011;365(26):2484-96. doi: 10.1056/NEJMoa1103799.
78. Parmar MK, Ledermann JA, Colombo N, du Bois A, Delaloye JF, Kristensen GB, Wheeler S, Swart AM, Qian W, Torri V, Floriani I, Jayson G, Lamont A, Tropé C. Paclitaxel plus platinum-based chemotherapy versus conventional platinum-based chemotherapy in women with relapsed ovarian cancer: the ICON4/AGO-OVAR-2.2 trial. Lancet. 2003;361(9375):2099-106.
79. Gordon AN, Tonda M, Sun S, Rackoff W. Long-term survival advantage for women treated with pegylated liposomal doxorubicin compared with topotecan in a phase 3 randomized study of recurrent and refractory epithelial ovarian cancer. Gynecol Oncol. 2004;95(1):1-8.
80. Ten Bokkel Huinink WW, Sufliarsky J, Smit WM, Spanik S, Wagnerova M, Hirte HW, Kaye S, Johri AR, Oza AM. Safety and efficacy of patupilone in patients with advanced ovarian, primary fallopian, or primary peritoneal cancer: a phase I, open-label, dose-escalation study. J Clin Oncol. 2009;27(19):3097-103. doi: 10.1200/JCO.2008.20.4826.
81. Rustin GJ (2011) Follow-up with CA125 after primary therapy of advanced ovarian cancer has major implications for treatment outcome and trial performances and should not be routinely performed. Ann Oncol 22(Suppl 8):viii45-viii48. doi: 10.1093/annonc/mdr471.
82. Steg AD, Bevis KS, Katre AA, Ziebarth A, Dobbin ZC, Alvarez RD, Zhang K, Conner M, Landen CN. Stem cell pathways contribute to clinical chemoresistance in ovarian cancer. Clin Cancer Res. 2012;18(3):869-81. doi: 10.1158/1078-0432. CCR-11-2188.
83. Meirelles K, Benedict LA, Dombkowski D, Pepin D, Preffer FI, Teixeira J, Tanwar PS, Young RH, MacLaughlin DT, Donahoe PK, Wei X. Human ovarian cancer stem/progenitor cells are stimulated by doxorubicin but inhibited by Mullerian inhibiting substance. Proc Natl Acad Sci USA. 2012;109(7):2358-63. doi: 10.1073/pnas.1120733109.
84. Zhang Y, Wang Z, Yu J, Shi JZ, Wang C, Fu WH, Chen ZW, Yang J. Cancer stem-like cells contribute to cisplatin resistance and progression in bladder cancer. Cancer Lett. 2012;. doi: 10.1016/j.canlet.2012.02.010.
85. Falso MJ, Buchholz BA, White RW. Stem-like cells in bladder cancer cell lines with differential sensitivity to cisplatin. Anticancer Res. 2012;32(3):733-8.
86. Abelson S, Shamai Y, Berger L, Shouval R, Skorecki K, Tzukerman M. Intratumoral heterogeneity in the self-renewal and tumorigenic differentiation of ovarian cancer. Stem Cells. 2012;30(3):415-24. doi: 10.1002/stem.1029.
87. Steffensen KD, Alvero AB, Yang Y, Waldstrom M, Hui P, Holmberg JC, Silasi DA, Jakobsen A, Rutherford T, Mor G. Prevalence of epithelial ovarian cancer stem cells correlates with recurrence in early-stage ovarian cancer. J Oncol. 2011;2011:620523. doi: 10.1155/2011/620523.
88. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008;133(4):704-15. doi: 10.1016/j.cell.2008.03.027.
89. Bapat SA, Mali AM, Koppikar CB, Kurrey NK. Stem and progenitor-like cells contribute to the aggressive behavior of human epithelial ovarian cancer. Cancer Res. 2005;65(8):3025-9. doi: 10.1158/0008-5472.CAN-04-3931.
90. Wani AA, Sharma N, Shouche YS, Bapat SA. Nuclear-mitochondrial genomic profiling reveals a pattern of evolution in epithelial ovarian tumor stem cells. Oncogene. 2006;25(47):6336-44. doi: 10.1038/sj.onc.1209649.
91. 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. Expression of CD133-1 and CD133-2 in ovarian cancer. Int J Gynecol Cancer. 2008;18(3):506-14. doi: 10.1111/j.1525-1438.2007.01056.x.
92. Curley MD, Therrien VA, Cummings CL, Sergent PA, Koulouris CR, Friel AM, Roberts DJ, Seiden MV, Scadden DT, Rueda BR, Foster R. CD133 expression defines a tumor initiating cell population in primary human ovarian cancer. Stem Cells. 2009;27(12):2875-83. doi: 10.1002/stem.236.
93. Zhang S, Balch C, Chan MW, Lai HC, Matei D, Schilder JM, Yan PS, Huang TH, Nephew KP. Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res. 2008;68(11):4311-20. doi: 10.1158/0008-5472.CAN-08-0364.
94. Luo L, Zeng J, Liang B, Zhao Z, Sun L, Cao D, Yang J, Shen K. Ovarian cancer cells with the CD117 phenotype are highly tumorigenic and are related to chemotherapy outcome. Exp Mol Pathol. 2011;91(2):596-602. doi: 10.1016/j.yexmp.2011.06.005.
95. Zhang J, Guo X, Chang DY, Rosen DG, Mercado-Uribe I, Liu J. CD133 expression associated with poor prognosis in ovarian cancer. Mod Pathol. 2012;25(3):456-64. doi: 10.1038/modpathol.2011.170.
96. Richardson GD, Robson CN, Lang SH, Neal DE, Maitland NJ, Collins AT. CD133, a novel marker for human prostatic epithelial stem cells. J Cell Sci. 2004;117(Pt 16):3539-45. doi: 10.1242/jcs.01222.
97. Immervoll H, Hoem D, Sakariassen PO, Steffensen OJ, Molven A. Expression of the "stem cell marker" CD133 in pancreas and pancreatic ductal adenocarcinomas. BMC Cancer. 2008;8:48. doi: 10.1186/1471-2407-8-48.
98. Singh SKHC, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB. Identification of human brain tumour initiating cells. Nature. 2004;432(7015):396-401.
99. 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. Epigenetic regulation of CD133 and tumorigenicity of CD133 + ovarian cancer cells. Oncogene. 2009;28(2):209-18. doi: 10.1038/onc.2008.374.
100. Peng S, Maihle NJ, Huang Y. Pluripotency factors Lin28 and Oct4 identify a sub-population of stem cell-like cells in ovarian cancer. Oncogene. 2010;29(14):2153-9. doi: 10.1038/onc.2009.500.
101. Chang B, Liu G, Xue F, Rosen DG, Xiao L, Wang X, Liu J. ALDH1 expression correlates with favorable prognosis in ovarian cancers. Mod Pathol. 2009;22(6):817-23. doi: 10.1038/modpathol.2009.35.
102. Kobayashi YSK, Hosonuma S, Ohara T, Itamochi H, Isonishi S, Kita T, Wada H, Kojo S, Kiguchi K. Side population is increased in paclitaxel-resistant ovarian cancer cell lines regardless of resistance to cisplatin. Gynecol Oncol. 2011;121(2):390-4.
103. Moserle L, Indraccolo S, Ghisi M, Frasson C, Fortunato E, Canevari S, Miotti S, Tosello V, Zamarchi R, Corradin A, Minuzzo S, Rossi E, Basso G, Amadori A. The side population of ovarian cancer cells is a primary target of IFN-alpha antitumor effects. Cancer Res. 2008;68(14):5658-68. doi: 10.1158/0008-5472.CAN-07-6341.
104. Levina V, Marrangoni AM, DeMarco R, Gorelik E, Lokshin AE. Drug-selected human lung cancer stem cells: cytokine network, tumorigenic and metastatic properties. PLoS ONE. 2008;3(8):e3077. doi: 10.1371/journal.pone.0003077.
105. Oki E, Baba H, Tokunaga E, Nakamura T, Ueda N, Futatsugi M, Mashino K, Yamamoto M, Ikebe M, Kakeji Y, Maehara Y. Akt phosphorylation associates with LOH of PTEN and leads to chemoresistance for gastric cancer. Int J Cancer. 2005;117(3):376-80. doi: 10.1002/ijc.21170.
106. Athanassiadou P, Athanassiades P, Grapsa D, Gonidi M, Athanassiadou AM, Stamati PN, Patsouris E. The prognostic value of PTEN, p53, and beta-catenin in endometrial carcinoma: a prospective immunocytochemical study. Int J Gynecol Cancer. 2007;17(3):697-704. doi: 10.1111/j.1525-1438.2007.00845.x.
107. Mackay HJ, Gallinger S, Tsao MS, McLachlin CM, Tu D, Keiser K, Eisenhauer EA, Oza AM. Prognostic value of microsatellite instability (MSI) and PTEN expression in women with endometrial cancer: results from studies of the NCIC Clinical Trials Group (NCIC CTG). Eur J Cancer. 2010;46(8):1365-73. doi: 10.1016/j.ejca.2010.02.031.
108. Nagata Y, Lan KH, Zhou X, Tan M, Esteva FJ, Sahin AA, Klos KS, Li P, Monia BP, Nguyen NT, Hortobagyi GN, Hung MC, Yu D. PTEN activation contributes to tumor inhibition by trastuzumab, and loss of PTEN predicts trastuzumab resistance in patients. Cancer Cell. 2004;6(2):117-27. doi: 10.1016/j.ccr.2004. 06.022.
109. Asselin E, Mills GB, Tsang BK. XIAP regulates Akt activity and caspase-3-dependent cleavage during cisplatin-induced apoptosis in human ovarian epithelial cancer cells. Cancer Res. 2001;61(5):1862-8.
110. Fraser M, Leung BM, Yan X, Dan HC, Cheng JQ, Tsang BK. p53 is a determinant of X-linked inhibitor of apoptosis protein/Akt-mediated chemoresistance in human ovarian cancer cells. Cancer Res. 2003;63(21):7081-8.
111. Yang X, Fraser M, Moll UM, Basak A, Tsang BK. Akt-mediated cisplatin resistance in ovarian cancer: modulation of p53 action on caspase-dependent mitochondrial death pathway. Cancer Res. 2006;66(6):3126-36. doi: 10.1158/0008-5472.CAN-05-0425.
112. Samimi G, Varki NM, Wilczynski S, Safaei R, Alberts DS, Howell SB. Increase in expression of the copper transporter ATP7A during platinum drug-based treatment is associated with poor survival in ovarian cancer patients. Clin Cancer Res. 2003;9(16 Pt 1):5853-9.
113. Kalayda GV, Wagner CH, Buss I, Reedijk J, Jaehde U. Altered localisation of the copper efflux transporters ATP7A and ATP7B associated with cisplatin resistance in human ovarian carcinoma cells. BMC Cancer. 2008;8:175. doi: 10.1186/1471-2407-8-175.
114. Yang H, Kong W, He L, Zhao JJ, O'Donnell JD, Wang J, Wenham RM, Coppola D, Kruk PA, Nicosia SV, Cheng JQ. MicroRNA expression profiling in human ovarian cancer: miR-214 induces cell survival and cisplatin resistance by targeting PTEN. Cancer Res. 2008;68(2):425-33. doi: 10.1158/0008-5472.CAN-07-2488.
115. Yang GF, He WP, Cai MY, He LR, Luo JH, Deng HX, Guan XY, Zeng MS, Zeng YX, Xie D. Intensive expression of Bmi-1 is a new independent predictor of poor outcome in patients with ovarian carcinoma. BMC Cancer. 2010;10:133. doi: 10.1186/1471-2407-10-133.
116. Wang E, Bhattacharyya S, Szabolcs A, Rodriguez-Aguayo C, Jennings NB, Lopez-Berestein G, Mukherjee P, Sood AK, Bhattacharya R. Enhancing chemotherapy response with Bmi-1 silencing in ovarian cancer. PLoS ONE. 2011;6(3):e17918. doi: 10.1371/journal.pone.0017918.
117. Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG, Keith DE, Levin WJ, Stuart SG, Udove J, Ullrich A, et al. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science. 1989;244(4905):707-12.
118. Rolitsky CD, Theil KS, McGaughy VR, Copeland LJ, Niemann TH. HER-2/neu amplification and overexpression in endometrial carcinoma. Int J Gynecol Pathol. 1999;18(2):138-43.
119. 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 Georgetown, Tex 8(1):158-166.
120. Bellone S, Siegel ER, Cocco E, Cargnelutti M, Silasi DA, Azodi M, Schwartz PE, Rutherford TJ, Pecorelli S, Santin AD. 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. 2009;19(5):860-6. doi: 10.1111/IGC.0b013e3181a8331f.
121. Richter CE, Cocco E, Bellone S, Silasi DA, Ruttinger D, Azodi M, Schwartz PE, Rutherford TJ, Pecorelli S, Santin AD (2010) High-grade, chemotherapy-resistant ovarian carcinomas overexpress epithelial cell adhesion molecule (EpCAM) and are highly sensitive to immunotherapy with MT201, a fully human monoclonal anti-EpCAM antibody. Am J Obstet Gynecol 203 (6):582.e1-7. doi: 10.1016/j.ajog.2010.07.041.
122. Pressey JG, Haas MC, Pressey CS, Kelly VM, Parker JN, Gillespie GY, Friedman GK. CD133 marks a myogenically primitive subpopulation in rhabdomyosarcoma cell lines that are relatively chemoresistant but sensitive to mutant HSV. Pediatr Blood Cancer. 2012;. doi: 10.1002/pbc.24117.
123. Zhang X, Zhang S, Liu Y, Liu J, Ma Y, Zhu Y, Zhang J. Effects of the combination of RAD001 and docetaxel on breast cancer stem cells. Eur J Cancer. 2012;. doi: 10.1016/j.ejca.2012.02.053.