Recently identified drug resistance biomarkers in ovarian cancer

References

• Siegel R, Ma J, Zou Z, et al. Cancer statistics, 2014. CA Cancer J Clin. 2014;64(1):9–29.
   PubMed Web of Science ®Google Scholar
• Colombo PE, Fabbro M, Theillet C, et al. Sensitivity and resistance to treatment in the primary management of epithelial ovarian cancer. Crit Rev Oncol Hematol. 2014;89(2):207–216.
   PubMed Web of Science ®Google Scholar
• Thibault B, Castells M, Delord JP, et al. Ovarian cancer microenvironment: implications for cancer dissemination and chemoresistance acquisition. Cancer Metastasis Rev. 2014;33(1):17–39.
   PubMed Web of Science ®Google Scholar
• Gillet JP, Calcagno AM, Varma S, et al. Redefining the relevance of established cancer cell lines to the study of mechanisms of clinical anti-cancer drug resistance. Proc Natl Acad Sci U S A. 2011;108(46):18708–18713.
   PubMed Web of Science ®Google Scholar
• Prat J. Ovarian carcinomas: five distinct diseases with different origins, genetic alterations, and clinicopathological features. Virchows Arch. 2012;460(3):237–249.
   PubMed Web of Science ®Google Scholar
• Kurman RJ, Carcangiu ML, Herrington CS, et al., Eds. WHO classification of tumours of female reproductive organs. Lyon, France: IARC; 2014.
   Google Scholar
• Gilks CB, Ionescu DN, Kalloger SE, et al; Cheryl brown ovarian cancer outcomes unit of the British Columbia cancer agency. Tumor cell type can be reproducibly diagnosed and is of independent prognostic significance in patients with maximally debulked ovarian carcinoma. Hum Pathol. 2008;39(8):1239–1251.
   PubMed Web of Science ®Google Scholar
• Weissman SM, Weiss SM, Newlin AC. Genetic testing by cancer site: ovary. Cancer J. 2012;18(4):320–327.
   PubMed Web of Science ®Google Scholar
• Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature. 2011;474(7353):609–615.
   PubMed Web of Science ®Google Scholar
• Alsop K, Fereday S, Meldrum C, et al. BRCA mutation frequency and patterns of treatment response in BRCA mutation-positive women with ovarian cancer: a report from the Australian ovarian cancer study group. J Clin Oncol. 2012;30(21):2654–2663.
   PubMed Web of Science ®Google Scholar
• Yang D, Khan S, Sun Y, et al. Association of BRCA1 and BRCA2 mutations with survival, chemotherapy sensitivity, and gene mutator phenotype in patients with ovarian cancer. Jama. 2011;306(14):1557–1565.
   PubMed Web of Science ®Google Scholar
• Norquist B, Wurz KA, Pennil CC, et al. Secondary somatic mutations restoring BRCA1/2 predict chemotherapy resistance in hereditary ovarian carcinomas. J Clin Oncol. 2011;29(22):3008–3015.
   PubMed Web of Science ®Google Scholar
• Barber LJ, Sandhu S, Chen L, et al. Secondary mutations in BRCA2 associated with clinical resistance to a PARP inhibitor. J Pathol. 2013;229(3):422–429.
   PubMed Web of Science ®Google Scholar
• Birkbak NJ, Wang ZC, Kim JY, et al. Telomeric allelic imbalance indicates defective DNA repair and sensitivity to DNA-damaging agents. Cancer Discov. 2012;2(4):366–375.
   PubMed Web of Science ®Google Scholar
• Abkevich V, Timms KM, Hennessy BT, et al. Patterns of genomic loss of heterozygosity predict homologous recombination repair defects in epithelial ovarian cancer. Br J Cancer. 2012;107(10):1776–1782.
   PubMed Web of Science ®Google Scholar
• Watkins JA, Irshad S, Grigoriadis A, et al. Genomic scars as biomarkers of homologous recombination deficiency and drug response in breast and ovarian cancers. Breast Cancer Res. 2014;16(3):211.
   PubMed Web of Science ®Google Scholar
• Furlong F, Fitzpatrick P, O’Toole S, et al. Low MAD2 expression levels associate with reduced progression-free survival in patients with high-grade serous epithelial ovarian cancer. J Pathol. 2012;226(5):746–755.
   PubMed Web of Science ®Google Scholar
• Alkema NG, Tomar T, Van Der Zee AG, et al. Checkpoint kinase 2 (Chk2) supports sensitivity to platinum-based treatment in high grade serous ovarian cancer. Gynecol Oncol. 2014;133(3):591–598.
   PubMed Web of Science ®Google Scholar
• Slipicevic A, Holth A, Hellesylt E, et al. Wee1 is a novel independent prognostic marker of poor survival in post-chemotherapy ovarian carcinoma effusions. Gynecol Oncol. 2014;135(1):118–124.
   PubMed Web of Science ®Google Scholar
• Hetland TE, Hellesylt E, Flørenes VA, et al. Class III beta-tubulin expression in advanced-stage serous ovarian carcinoma effusions is associated with poor survival and primary chemoresistance. Hum Pathol. 2011;42(7):1019–1026.
   PubMed Web of Science ®Google Scholar
• Donato MD, Fanelli M, Mariani M, et al. Nek6 and Hif-1α cooperate with the cytoskeletal gateway of drug resistance to drive outcome in serous ovarian cancer. Am J Cancer Res. 2015;5(6):1862–1877.
   PubMed Web of Science ®Google Scholar
• Hetland TE, Nymoen DA, Holth A, et al. Aurora-B expression in metastatic effusions from advanced-stage ovarian serous carcinoma is predictive of intrinsic chemotherapy resistance. Hum Pathol. 2013;44(5):777–785.
   PubMed Web of Science ®Google Scholar
• Park J, Chen X, Tropè CG, et al. Notch3 overexpression is related to the recurrence of ovarian cancer and confers resistance to carboplatin. Am J Pathol. 2010;177(3):1087–1094.
   PubMed Web of Science ®Google Scholar
• Kang H, Jeong JY, Song JY, et al. Notch3-specific inhibition using siRNA knockdown or GSI sensitizes paclitaxel-resistant ovarian cancer cells. Mol Carcinog. 2015. Jul 24. doi:10.1002/mc.22363. [Epub ahead of print].
   Web of Science ®Google Scholar
• Brown CW, Brodsky AS, Freiman RN. Notch3 overexpression promotes anoikis resistance in epithelial ovarian cancer via upregulation of COL4A2. Mol Cancer Res. 2015;13(1):78–85.
   PubMed Web of Science ®Google Scholar
• Jung JG, Stoeck A, Guan B, et al. Notch3 interactome analysis identified WWP2 as a negative regulator of Notch3 signaling in ovarian cancer. PLoS Genet. 2014;10(10):e1004751.
   PubMed Web of Science ®Google Scholar
• Yang G, Xiao X, Rosen DG, et al. The biphasic role of NF-kappaB in progression and chemoresistance of ovarian cancer. Clin Cancer Res. 2011;17(8):2181–2194.
   PubMed Web of Science ®Google Scholar
• Katagiri A, Nakayama K, Rahman MT, et al. Loss of ARID1A expression is related to shorter progression-free survival and chemoresistance in ovarian clear cell carcinoma. Mod Pathol. 2012;25(2):282–288.
   PubMed Web of Science ®Google Scholar
• Canet B, Pons C, Espinosa I, et al. Ovarian clear cell carcinomas: RHO GTPases may contribute to explain their singular biologic behavior. Hum Pathol. 2011;42(6):833–839.
   PubMed Web of Science ®Google Scholar
• Yamaguchi N, Mimoto R, Yanaihara N, et al. DYRK2 regulates epithelial-mesenchymal-transition and chemosensitivity through snail degradation in ovarian serous adenocarcinoma. Tumour Biol. 2015;36(8):5913–5923.
   PubMed Web of Science ®Google Scholar
• Tsofack SP, Meunier L, Sanchez L, et al. Low expression of the X-linked ribosomal protein S4 in human serous epithelial ovarian cancer is associated with a poor prognosis. BMC Cancer. 2013;13:303.
   PubMed Web of Science ®Google Scholar
• Kang Y, Hu W, Ivan C, et al. Role of focal adhesion kinase in regulating YB-1-mediated paclitaxel resistance in ovarian cancer. J Natl Cancer Inst. 2013;105(19):1485–1495.
   PubMedGoogle Scholar
• Bösmüller H, Haitchi-Petnehazy S, Webersinke G, et al. Intratumoral lymphocyte density in serous ovarian carcinoma is superior to ERCC1 expression for predicting response to platinum-based therapy. Virchows Arch. 2011;459(2):183–191.
   PubMed Web of Science ®Google Scholar
• Bachmayr-Heyda A, Aust S, Heinze G, et al. Prognostic impact of tumor infiltrating CD8+ T cells in association with cell proliferation in ovarian cancer patients–a study of the OVCAD consortium. BMC Cancer. 2013;13:422.
   PubMed Web of Science ®Google Scholar
• Pölcher M, Braun M, Friedrichs N, et al. Foxp3(+) cell infiltration and granzyme B(+)/Foxp3(+) cell ratio are associated with outcome in neoadjuvant chemotherapy-treated ovarian carcinoma. Cancer Immunol Immunother. 2010;59(6):909–919.
   PubMed Web of Science ®Google Scholar
• Shih IeM, Nakayama K, Wu G, et al. Amplification of the ch19p13.2 NACC1 locus in ovarian high-grade serous carcinoma. Mod Pathol. 2011;24(5):638–645.
   PubMed Web of Science ®Google Scholar
• Nakayama K, Nakayama N, Davidson B, et al. A BTB/POZ protein, NAC-1, is related to tumor recurrence and is essential for tumor growth and survival. Proc Natl Acad Sci USA. 2006;103:18739–18744.
   PubMed Web of Science ®Google Scholar
• Maeda O, Shibata K, Hosono S, et al. Spectrin αII and βII tetramers contribute to platinum anticancer drug resistance in ovarian serous adenocarcinoma. Int J Cancer. 2012;130(1):113–121.
   PubMed Web of Science ®Google Scholar
• Li C, Li Y, Wang X, et al. Elevated expression of astrocyte elevated gene-1 (AEG-1) is correlated with cisplatin-based chemoresistance and shortened outcome in patients with stages III-IV serous ovarian carcinoma. Histopathology. 2012;60(6):953–963.
   PubMed Web of Science ®Google Scholar
• Miyamoto M, Takano M, Iwaya K, et al. X-chromosome-linked inhibitor of apoptosis as a key factor for chemoresistance in clear cell carcinoma of the ovary. Br J Cancer. 2014;110(12):2881–2886.
   PubMed Web of Science ®Google Scholar
• Seagle BL, Yang CP, Eng KH, et al. TP53 hot spot mutations in ovarian cancer: selective resistance to microtubule stabilizers in vitro and differential survival outcomes from the cancer genome atlas. Gynecol Oncol. 2015;138(1):159–164.
   PubMed Web of Science ®Google Scholar
• Williams E, Martin S, Moss R, et al. Co-expression of VEGF and CA9 in ovarian high-grade serous carcinoma and relationship to survival. Virchows Arch. 2012;461(1):33–39.
   PubMed Web of Science ®Google Scholar
• Yu Y, Gaillard S, Phillip JM, et al. Inhibition of spleen tyrosine kinase potentiates paclitaxel-induced cytotoxicity in ovarian cancer cells by stabilizing microtubules. Cancer Cell. 2015;28(1):82–96.
   PubMed Web of Science ®Google Scholar
• Vaksman V, Davidson B, Tropé C, et al. Calreticulin expression is reduced in ovarian serous carcinoma effusions compared with primary tumors and solid metastases. Hum Pathol. 2013;44:2677–2683.
   PubMed Web of Science ®Google Scholar
• Garg AD, Elsen S, Krysko DV, et al. Resistance to anticancer vaccination effect is controlled by a cancer cell-autonomous phenotype that disrupts immunogenic phagocytic removal. Oncotarget. 2015;6(29):26841–26860.
   PubMed Web of Science ®Google Scholar
• Katz B, Tropé CG, Reich R, et al. MicroRNAs in ovarian cancer. Hum Pathol. 2015;46(9):1245–1256.
   PubMed Web of Science ®Google Scholar
• Sun C, Li N, Yang Z, et al. miR-9 regulation of BRCA1 and ovarian cancer sensitivity to cisplatin and PARP inhibition. J Natl Cancer Inst. 2013;105(22):1750–1758.
   PubMed Web of Science ®Google Scholar
• Chan JK, Blansit K, Kiet T, et al. The inhibition of miR-21 promotes apoptosis and chemosensitivity in ovarian cancer. Gynecol Oncol. 2014;132(3):739–744.
   PubMed Web of Science ®Google Scholar
• Pink RC, Samuel P, Massa D, et al. The passenger strand, miR-21-3p, plays a role in mediating cisplatin resistance in ovarian cancer cells. Gynecol Oncol. 2015;137(1):143–151.
   PubMed Web of Science ®Google Scholar
• Parikh A, Lee C, Joseph P, et al. microRNA-181a has a critical role in ovarian cancer progression through the regulation of the epithelial-mesenchymal transition. Nat Commun. 2014;5:2977.
   PubMed Web of Science ®Google Scholar
• Huh JH, Kim TH, Kim K, et al. Dysregulation of miR-106a and miR-591 confers paclitaxel resistance to ovarian cancer. Br J Cancer. 2013;109(2):452–461.
   PubMed Web of Science ®Google Scholar
• Tang Z, Ow GS, Thiery JP, et al. Meta-analysis of transcriptome reveals let-7b as an unfavorable prognostic biomarker and predicts molecular and clinical subclasses in high-grade serous ovarian carcinoma. Int J Cancer. 2014;134(2):306–318.
   PubMed Web of Science ®Google Scholar
• Vang S, Wu HT, Fischer A, et al. Identification of ovarian cancer metastatic miRNAs. PLoS One. 2013;8:e58226.
   PubMed Web of Science ®Google Scholar
• Vecchione A, Belletti B, Lovat F, et al. A microRNA signature defines chemoresistance in ovarian cancer through modulation of angiogenesis. Proc Natl Acad Sci USA. 2013;110(24):9845–9850.
   PubMed Web of Science ®Google Scholar
• Verhaak RG, Tamayo P, Yang JY, et al. Cancer genome atlas research network. Prognostically relevant gene signatures of high-grade serous ovarian carcinoma. J Clin Invest. 2013;123(1):517–525.
   PubMed Web of Science ®Google Scholar
• Tan DS, Iravani M, McCluggage WG, et al. Genomic analysis reveals the molecular heterogeneity of ovarian clear cell carcinomas. Clin Cancer Res. 2011;17(6):1521–1534.
   PubMed Web of Science ®Google Scholar
• Wang ZC, Birkbak NJ, Culhane AC, et al Australian ovarian cancer study group, Matulonis UA. Profiles of genomic instability in high-grade serous ovarian cancer predict treatment outcome. Clin Cancer Res. 2012;18(20):5806–5815.
   PubMed Web of Science ®Google Scholar
• Barlin JN, Jelinic P, Olvera N, et al. Validated gene targets associated with curatively treated advanced serous ovarian carcinoma. Gynecol Oncol. 2013;128(3):512–517.
   PubMed Web of Science ®Google Scholar
• Teng PN, Wang G, Hood BL, et al. Identification of candidate circulating cisplatin-resistant biomarkers from epithelial ovarian carcinoma cell secretomes. Br J Cancer. 2014;110(1):123–132.
   PubMed Web of Science ®Google Scholar
• Bateman NW, Jaworski E, Ao W, et al. Elevated AKAP12 in paclitaxel-resistant serous ovarian cancer cells is prognostic and predictive of poor survival in patients. J Proteome Res. 2015;14(4):1900–1910.
   PubMed Web of Science ®Google Scholar
• Koti M, Siu A, Clément I, et al. A distinct pre-existing inflammatory tumour microenvironment is associated with chemotherapy resistance in high-grade serous epithelial ovarian cancer. Br J Cancer. 2015;112(7):1215–1222.
   PubMed Web of Science ®Google Scholar
• Stronach EA, Alfraidi A, Rama N, et al. HDAC4-regulated STAT1 activation mediates platinum resistance in ovarian cancer. Cancer Res. 2011;71(13):4412–4422.
   PubMed Web of Science ®Google Scholar
• Koti M, Gooding RJ, Nuin P, et al. Identification of the IGF1/PI3K/NFκB/ERK gene signalling networks associated with chemotherapy resistance and treatment response in high-grade serous epithelial ovarian cancer. BMC Cancer. 2013;13:549.
   PubMed Web of Science ®Google Scholar
• Marchion DC, Cottrill HM, Xiong Y, et al. BAD phosphorylation determines ovarian cancer chemosensitivity and patient survival. Clin Cancer Res. 2011;17(19):6356–6366.
   PubMed Web of Science ®Google Scholar
• Cowin PA, George J, Fereday S, et al. Australian ovarian cancer study. LRP1B deletion in high-grade serous ovarian cancers is associated with acquired chemotherapy resistance to liposomal doxorubicin. Cancer Res. 2012;72(16):4060–4073.
   PubMed Web of Science ®Google Scholar
• Cohen S, Mosig R, Moshier E, et al. Interferon regulatory factor 1 is an independent predictor of platinum resistance and survival in high-grade serous ovarian carcinoma. Gynecol Oncol. 2014;134(3):591–598.
   PubMed Web of Science ®Google Scholar
• Zeimet AG, Reimer D, Wolf D, et al.Intratumoral interferon regulatory factor (IRF)-1 but not IRF-2 is of relevance in predicting patient outcome in ovarian cancer. Int J Cancer. 2009;124(10):2353–2360.
   PubMed Web of Science ®Google Scholar
• Schwarz RF, Ng CK, Cooke SL, et al. Spatial and temporal heterogeneity in high-grade serous ovarian cancer: a phylogenetic analysis. PLoS Med. 2015;12:e1001789.
   PubMed Web of Science ®Google Scholar
• Patch AM, Christie EL, Etemadmoghadam D, et al. Whole-genome characterization of chemoresistant ovarian cancer. Nature. 2015;521(7553):489–494.
   PubMed Web of Science ®Google Scholar
• Ahmed N, Stenvers KL. Getting to know ovarian cancer ascites: opportunities for targeted therapy-based translational research. Front Oncol. 2013;3:256.
   PubMedGoogle Scholar
• Latifi A, Luwor RB, Bilandzic M, et al. Isolation and characterization of tumor cells from the ascites of ovarian cancer patients: molecular phenotype of chemoresistant ovarian tumors. PLoS One. 2012;7(10):e46858.
   PubMed Web of Science ®Google Scholar
• Abubaker K, Luwor RB, Zhu H, et al. Inhibition of the JAK2/STAT3 pathway in ovarian cancer results in the loss of cancer stem cell-like characteristics and a reduced tumor burden. BMC Cancer. 2014;14:317.
   PubMed Web of Science ®Google Scholar
• Rizzo S, Hersey JM, Mellor P, et al. Ovarian cancer stem cell-like side populations are enriched following chemotherapy and overexpress EZH2. Mol Cancer Ther. 2011;10(2):325–335.
   PubMed Web of Science ®Google Scholar
• Meng E, Long B, Sullivan P, et al. CD44+/CD24- ovarian cancer cells demonstrate cancer stem cell properties and correlate to survival. Clin Exp Metastasis. 2012;29(8):939–948.
   PubMed Web of Science ®Google Scholar
• Meng E, Mitra A, Tripathi K, et al. ALDH1A1 maintains ovarian cancer stem cell-like properties by altered regulation of cell cycle checkpoint and DNA repair network signaling. PLoS One. 2014;9(9):e107142.
   PubMed Web of Science ®Google Scholar
• Kerr EH, Frederick PJ, Egger ME, et al. Lung resistance-related protein (LRP) expression in malignant ascitic cells as a prognostic marker for advanced ovarian serous carcinoma. Ann Surg Oncol. 2013;20(9):3059–3065.
   PubMed Web of Science ®Google Scholar
• Huang H, Li Y, Liu J, et al. Screening and identification of biomarkers in ascites related to intrinsic chemoresistance of serous epithelial ovarian cancers. PLoS One. 2012;7(12):e51256.
   PubMed Web of Science ®Google Scholar
• Lane D, Matte I, Garde-Granger P, et al. Inflammation-regulating factors in ascites as predictive biomarkers of drug resistance and progression-free survival in serous epithelial ovarian cancers. BMC Cancer. 2015;15:492.
   Google Scholar
• Becker MA, Haluska P Jr, Bale LK, et al. A novel neutralizing antibody targeting pregnancy-associated plasma protein-a inhibits ovarian cancer growth and ascites accumulation in patient mouse tumorgrafts. Mol Cancer Ther. 2015;14(4):973–981.
   PubMed Web of Science ®Google Scholar
• Gillet JP, Wang J, Calcagno AM, et al. Clinical relevance of multidrug resistance gene expression in ovarian serous carcinoma effusions. Mol Pharm. 2011;8:2080–2088.
   PubMed Web of Science ®Google Scholar
• Nymoen DA, Holth A, Hetland Falkenthal TE, et al. CIAPIN1 and ABCA13 are markers of poor survival in metastatic ovarian serous carcinoma. Mol Cancer. 2015;14:44.
   PubMed Web of Science ®Google Scholar
• Gillet JP, Calcagno AM, Varma S, et al. Multidrug resistance-linked gene signature predicts overall survival of patients with primary ovarian serous carcinoma. Clin Cancer Res. 2012;18:3197–3206.
   PubMed Web of Science ®Google Scholar
• Nymoen DA, Hetland Falkenthal TE, Holth A, et al. Expression and clinical role of chemoresponse-associated genes in ovarian serous carcinoma. Gynecol Oncol. 2015;139:30–39.
   PubMed Web of Science ®Google Scholar
• Srivastava AK, Han C, Zhao R, et al. Enhanced expression of DNA polymerase eta contributes to cisplatin resistance of ovarian cancer stem cells. Proc Natl Acad Sci U S A. 2015;112(14):4411–4416.
   PubMed Web of Science ®Google Scholar
• Kwon AY, Kim GI, Jeong JY, et al. VAV3 overexpressed in cancer stem cells is a poor prognostic indicator in ovarian cancer patients. Stem Cells Dev. 2015;24(13):1521–1535.
   PubMed Web of Science ®Google Scholar
• Ayub TH, Keyver-Paik MD, Debald M, et al. Accumulation of ALDH1-positive cells after neoadjuvant chemotherapy predicts treatmentresistance and prognosticates poor outcome in ovarian cancer. Oncotarget. 2015;6(18):16437–16448.
   PubMed Web of Science ®Google Scholar
• Janzen DM, Tiourin E, Salehi JA, et al. An apoptosis-enhancing drug overcomes platinum resistance in a tumour-initiating subpopulation of ovarian cancer. Nat Commun. 2015;6:7956.
   PubMed Web of Science ®Google Scholar
• Domcke S, Sinha R, Levine DA, et al. Evaluating cell lines as tumour models by comparison of genomic profiles. Nat Commun. 2013;4:2126.
   PubMed Web of Science ®Google Scholar
• Bashashati A, Ha G, Tone A, et al. Distinct evolutionary trajectories of primary high-grade serous ovarian cancers revealed through spatial mutational profiling. J Pathol. 2013;231(1):21–34.
   PubMed Web of Science ®Google Scholar
• Blagden SP. Harnessing Pandemonium: The Clinical Implications of Tumor Heterogeneity in Ovarian Cancer. Front Oncol. 2015;5:149.
   PubMed Web of Science ®Google Scholar
• Nowicka A, Marini FC, Solley TN, et al. Human omental-derived adipose stem cells increase ovarian cancer proliferation, migration, and chemoresistance. PLoS One. 2013;8(12):e81859.
   PubMed Web of Science ®Google Scholar