Critical role of Wnt/ß-catenin signaling in driving epithelial ovarian cancer platinum resistance

Oncotarget

Volumn 6, Issue 27, 2015, Pages 23720-23734

  Nagaraj, Anil Belur ^a   Joseph, Peronne ^a   Kovalenko, Olga ^a   Singh, Sareena ^b   Armstrong, Amy ^b   Redline, Raymond ^b   Resnick, Kimberly ^b   Zanotti, Kristine ^b   Waggoner, Steven ^b   Di Feo, Analisa ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

Cancer initiating cells; Patient derived xenograft; Platinum resistance; catenin; Tumor spheres

Indexed keywords

BETA CATENIN; CISPLATIN; N BENZYL 1,2,3,4,8,9 HEXAHYDRO 6 (4 HYDROXYBENZYL) 8 (1 NAPHTHYLMETHYL) 4,7 DIOXO 2H PYRAZINO[1,2 A]PYRIMIDINE 1(6H) CARBOXAMIDE; PLATINUM COMPLEX; WNT PROTEIN; ANTINEOPLASTIC AGENT; FUSED HETEROCYCLIC RINGS; PYRIMIDINONE DERIVATIVE;

ARTICLE; BETA CATENIN SIGNALING PATHWAY; CANCER RESISTANCE; CANCER STEM CELL; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; OVARIAN CANCER CELL LINE; OVARY CARCINOMA; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN TARGETING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; UPREGULATION; WNT SIGNALING PATHWAY; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENETICS; METABOLISM; MORTALITY; MOUSE; MULTICELLULAR SPHEROID; NEOPLASMS, GLANDULAR AND EPITHELIAL; NUDE MOUSE; OVARIAN NEOPLASMS; PATHOLOGY; PHYSIOLOGY; TUMOR CELL CULTURE;

ANIMALS; ANTINEOPLASTIC AGENTS; BETA CATENIN; BRIDGED BICYCLO COMPOUNDS, HETEROCYCLIC; CISPLATIN; DRUG RESISTANCE, NEOPLASM; HUMANS; MICE; MICE, NUDE; NEOPLASMS, GLANDULAR AND EPITHELIAL; NEOPLASTIC STEM CELLS; OVARIAN NEOPLASMS; PYRIMIDINONES; SPHEROIDS, CELLULAR; TUMOR CELLS, CULTURED; WNT PROTEINS; WNT SIGNALING PATHWAY; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84943422762     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4690     Document Type: Article

References (45)

1. Siegel R, Ma J, Zou Z and Jemal A. Cancer statistics, 2014. CA:a cancer journal for clinicians. 2014;64:9-29.
2. Cooke SL and Brenton JD. Evolution of platinum resistance in high-grade serous ovarian cancer. The Lancet Oncology. 2011;12:1169-1174.
3. Ahmed N, Abubaker K, Findlay J and Quinn M. Cancerous ovarian stem cells:obscure targets for therapy but relevant to chemoresistance. Journal of cellular biochemistry. 2013; 114:21-34.
4. Valent P, Bonnet D, De Maria R, Lapidot T, Copland M, Melo JV, Chomienne C, Ishikawa F, Schuringa JJ, Stassi G, Huntly B, Herrmann H, Soulier J, Roesch A, Schuurhuis GJ, Wohrer S, et al. Cancer stem cell definitions and terminology:the devil is in the details. Nature reviews Cancer. 2012;12:767-775.
5. Kim CF and Dirks PB. Cancer and stem cell biology:how tightly intertwined? Cell stem cell. 2008;3:147-150.
6. Steg AD, Bevis KS, Katre AA, Ziebarth A, Dobbin ZC, Alvarez RD, Zhang K, Conner M and Landen CN. Stem cell pathways contribute to clinical chemoresistance in ovarian cancer. Clinical cancer research :an official journal of the American Association for Cancer Research. 2012; 18:869-881.
7. Ahmed N, Abubaker K and Findlay JK. Ovarian cancer stem cells:Molecular concepts and relevance as therapeutic targets. Mol Aspects Med. 2014;39:110-25.
8. 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 and Brown R. Ovarian cancer stem cell-like side populations are enriched following chemotherapy and overexpress EZH2. Molecular cancer therapeutics. 2011; 10(:325-335.
9. Latifi A, Abubaker K, Castrechini N, Ward AC, Liongue C, Dobill F, Kumar J, Thompson EW, Quinn MA, Findlay JK and Ahmed N. Cisplatin treatment of primary and metastatic epithelial ovarian carcinomas generates residual cells with mesenchymal stem cell-like profile. Journal of cellular biochemistry. 2011;112:2850-2864.
10. Tomao F, Papa A, Strudel M, Rossi L, Lo Russo G, Benedetti Panici P, Ciabatta FR and Tomao S. Investigating molecular profiles of ovarian cancer:an update on cancer stem cells. Journal of Cancer. 2014;5:301-310.
11. Anastas JN and Moon RT. WNT signalling pathways as therapeutic targets in cancer. Nature reviews Cancer. 2013; 13:11-26.
12. Heidel FH, Bullinger L, Feng Z, Wang Z, Neff TA, Stein L, Kalaitzidis D, Lane SW and Armstrong SA. Genetic and pharmacologic inhibition of beta-catenin targets imatinib-resistant leukemia stem cells in CML. Cell stem cell. 2012; 10:412-424.
13. Yeung J, Esposito MT, Gandillet A, Zeisig BB, Griessinger E, Bonnet D and So CW. beta-Catenin mediates the establishment and drug resistance of MLL leukemic stem cells. Cancer cell. 2010;18:606-618.
14. Takahashi-Yanaga F and Kahn M. Targeting Wnt signaling: can we safely eradicate cancer stem cells? Clinical cancer research :an official journal of the American Association for Cancer Research. 2010;16:3153-3162.
15. Barbolina MV, Burkhalter RJ and Stack MS. Diverse mechanisms for activation of Wnt signalling in the ovarian tumour microenvironment. The Biochemical journal. 2011; 437:1-12.
16. Lee CM, Shvartsman H, Deavers MT, Wang SC, Xia W, Schmandt R, Bodurka DC, Atkinson EN, Malpica A, Gershenson DM, Hung MC and Lu KH. beta-catenin nuclear localization is associated with grade in ovarian serous carcinoma. Gynecologic oncology. 2003;88:363-368.
17. Gatcliffe TA, Monk BJ, Planutis K and Holcombe RF. Wnt signaling in ovarian tumorigenesis. International journal of gynecological cancer :official journal of the International Gynecological Cancer Society. 2008;18(5):954-962.
18. Arend RC, Londono-Joshi AI, Straughn JM, Jr. and Buchsbaum DJ. The Wnt/beta-catenin pathway in ovarian cancer:a review. Gynecologic oncology. 2013;131:772-779.
19. Bodnar L, Stanczak A, Cierniak S, Smoter M, Cichowicz M, Kozlowski W, Szczylik C, Wieczorek M and LamparskaPrzybysz M. Wnt/beta-catenin pathway as a potential prognostic and predictive marker in patients with advanced ovarian cancer. Journal of ovarian research. 2014;7:16.
20. Zhang W, Liu Y, Sun N, Wang D, Boyd-Kirkup J, Dou X and Han JD. Integrating genomic, epigenomic, and transcriptomic features reveals modular signatures underlying poor prognosis in ovarian cancer. Cell reports. 2013;4:542-553.
21. McAuliffe SM, Morgan SL, Wyant GA, Tran LT, Muto KW, Chen YS, Chin KT, Partridge JC, Poole BB, Cheng KH, Daggett J, Jr., Cullen K, Kantoff E, Hasselbatt K, Berkowitz J, Muto MG, et al. Targeting Notch, a key pathway for ovarian cancer stem cells, sensitizes tumors to platinum therapy. Proceedings of the National Academy of Sciences of the United States of America. 2012;109:E2939-2948.
22. Brugmann SA, Goodnough LH, Gregorieff A, Leucht P, ten Berge D, Fuerer C, Clevers H, Nusse R and Helms JA. Wnt signaling mediates regional specification in the vertebrate face. Development. 2007;134:3283-3295.
23. Staal FJ, Luis TC and Tiemessen MM. WNT signalling in the immune system:WNT is spreading its wings. Nature reviews Immunology. 2008;8:581-593.
24. Yasuda K, Torigoe T, Morita R, Kuroda T, Takahashi A, Matsuzaki J, Kochin V, Asanuma H, Hasegawa T, Saito T, Hirohashi Y and Sato N. Ovarian cancer stem cells are enriched in side population and aldehyde dehydrogenase bright overlapping population. PloS one. 2013;8:e68187.
25. Parker RJ, Eastman A, Bostick-Bruton F and Reed E. Acquired cisplatin resistance in human ovarian cancer cells is associated with enhanced repair of cisplatin-DNA lesions and reduced drug accumulation. The Journal of clinical investigation. 1991;87:772-777.
26. Onder TT, Gupta PB, Mani SA, Yang J, Lander ES and Weinberg RA. Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer research. 2008;68:3645-3654.
27. Rota LM, Lazzarino DA, Ziegler AN, LeRoith D and Wood TL. Determining mammosphere-forming potential: application of the limiting dilution analysis. Journal of mammary gland biology and neoplasia. 2012;17:119-123.
28. Januchowski R, Wojtowicz K and Zabel M. The role of aldehyde dehydrogenase (ALDH) in cancer drug resistance. Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie. 2013;67:669-680.
29. Kuroda T, Hirohashi Y, Torigoe T, Yasuda K, Takahashi A, Asanuma H, Morita R, Mariya T, Asano T, Mizuuchi M, Saito T and Sato N. ALDH1-high ovarian cancer stem-like cells can be isolated from serous and clear cell adenocarcinoma cells, and ALDH1 high expression is associated with poor prognosis. PloS one. 2013;8:e65158.
30. 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 and Sood AK. Targeting aldehyde dehydrogenase cancer stem cells in ovarian cancer. Molecular cancer therapeutics. 2010;9:3186-3199.
31. Wang YC, Yo YT, Lee HY, Liao YP, Chao TK, Su PH and Lai HC. ALDH1-bright epithelial ovarian cancer cells are associated with CD44 expression, drug resistance, and poor clinical outcome. The American journal of pathology. 2012; 180:1159-1169.
32. Silva IA, Bai S, McLean K, Yang K, Griffith K, Thomas D, Ginestier C, Johnston C, Kueck A, Reynolds RK, Wicha MS and Buckanovich RJ. Aldehyde dehydrogenase in combination with CD133 defines angiogenic ovarian cancer stem cells that portend poor patient survival. Cancer research. 2011;71:3991-4001.
33. Condello S, Morgan CA, Nagdas S, Cao L, Turek J, Hurley TD and Matei D. beta-Catenin-regulated ALDH1A1 is a target in ovarian cancer spheroids. Oncogene. 2015; 34:2297-308.
34. Takebe N, Harris PJ, Warren RQ and Ivy SP. Targeting cancer stem cells by inhibiting Wnt, Notch, and Hedgehog pathways. Nature reviews Clinical oncology. 2011;8:97-106.
35. Emami KH, Nguyen C, Ma H, Kim DH, Jeong KW, Eguchi M, Moon RT, Teo JL, Kim HY, Moon SH, Ha JR and Kahn M. A small molecule inhibitor of beta-catenin/CREBbinding protein transcription [corrected]. Proceedings of the National Academy of Sciences of the United States of America. 2004;101:12682-12687.
36. Valkenburg KC, Graveel CR, Zylstra-Diegel CR, Zhong Z and Williams BO. Wnt/beta-catenin Signaling in Normal and Cancer Stem Cells. Cancers. 2011;3:2050-2079.
37. Huang SS, Clarke DC, Gosline SJ, Labadorf A, Chouinard CR, Gordon W, Lauffenburger DA and Fraenkel E. Linking proteomic and transcriptional data through the interactome and epigenome reveals a map of oncogene-induced signaling. PLoS computational biology. 2013;9:e1002887.
38. Flesken-Nikitin A, Hwang CI, Cheng CY, Michurina TV, Enikolopov G and Nikitin AY. Ovarian surface epithelium at the junction area contains a cancer-prone stem cell niche. Nature. 2013;495:241-245.
39. Ng A, Tan S, Singh G, Rizk P, Swathi Y, Tan TZ, Huang RY, Leushacke M and Barker N. Lgr5 marks stem/progenitor cells in ovary and tubal epithelia. Nat Cell Biol. 2014;16:745-57.
40. Arend RC, Londono-Joshi AI, Samant RS, Li Y, Conner M, Hidalgo B, Alvarez RD, Landen CN, Straughn JM and Buchsbaum DJ. Inhibition of Wnt/beta-catenin pathway by niclosamide:A therapeutic target for ovarian cancer. Gynecologic oncology. 2014;134:112-120.
41. Pan JX, Ding K and Wang CY. Niclosamide, an old antihelminthic agent, demonstrates antitumor activity by blocking multiple signaling pathways of cancer stem cells. Chinese journal of cancer. 2012;31:178-184.
42. Michor F and Polyak K. The origins and implications of intratumor heterogeneity. Cancer prevention research. 2010; 3:1361-1364.
43. Hoogstraat M, de Pagter MS, Cirkel GA, van Roosmalen MJ, Harkins TT, Duran K, Kreeftmeijer J, Renkens I, Witteveen PO, Lee CC, Nijman IJ, Guy T, van 't Slot R, Jonges TN, Lolkema MP, Koudijs MJ, et al. Genomic and transcriptomic plasticity in treatment-naive ovarian cancer. Genome research. 2014;24:200-211.
44. Stewart SA, Dykxhoorn DM, Palliser D, Mizuno H, Yu EY, An DS, Sabatini DM, Chen IS, Hahn WC, Sharp PA, Weinberg RA and Novina CD. Lentivirus-delivered stable gene silencing by RNAi in primary cells. Rna. 2003;9:493-501.
45. Parikh A, Lee C, Peronne J, Marchini S, Baccarini A, Kolev V, Romualdi C, Fruscio R, Shah H, Wang F, Mullokandov G, Fishman D, D'Incalci M, Rahaman J, Kalir T, Redline RW, et al. microRNA-181a has a critical role in ovarian cancer progression through the regulation of the epithelialmesenchymal transition. Nature communications. 2014; 5:2977.