Recently identified drug resistance biomarkers in ovarian cancer

Expert Review of Molecular Diagnostics

Volumn 16, Issue 5, 2016, Pages 569-578

  Davidson, Ben ^a,b  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

ascites; chemotherapy resistance; DNA repair; histology; microRNA; mitosis; Ovarian cancer; progression

Indexed keywords

53BP1 PROTEIN; ARID1A PROTEIN; ATM PROTEIN; AURORA B KINASE; BETA TUBULIN; BRCA1 PROTEIN; BRCA2 PROTEIN; CHECKPOINT KINASE 2; COL4A2 PROTEIN; DUAL SPECIFICITY TYROSINE REGULATED KINASE 2; FOCAL ADHESION KINASE; GAMMA SECRETASE; HISTONE H2AX; MICRORNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; NOTCH3 RECEPTOR; PACLITAXEL; PROTEIN; PROTEIN CDC42; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RHOC PROTEIN; SPECTRIN; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR RELA; TUMOR MARKER; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; UNINDEXED DRUG; WEE1 PROTEIN; Y BOX BINDING PROTEIN 1; ANTINEOPLASTIC AGENT; BRCA1 PROTEIN, HUMAN; BRCA2 PROTEIN, HUMAN; HDAC4 PROTEIN, HUMAN; HISTONE DEACETYLASE; REPRESSOR PROTEIN; STAT1 PROTEIN; STAT1 PROTEIN, HUMAN;

ALLELIC IMBALANCE; CANCER SURVIVAL; CD3+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHROMOSOME 19P; COMPARATIVE GENOMIC HYBRIDIZATION; DNA REPAIR; DOWN REGULATION; DRUG RESISTANCE; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HETEROZYGOSITY LOSS; HUMAN; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING; MICROARRAY ANALYSIS; MICROTUBULE; MITOSIS; MITOSIS INHIBITION; OVARY CARCINOMA; OVERALL SURVIVAL; PROGRESSION FREE SURVIVAL; RECOMBINATION REPAIR; REVIEW; RNA SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM; SOMATIC MUTATION; WILD TYPE; ADENOCARCINOMA, CLEAR CELL; CYSTADENOCARCINOMA, SEROUS; DISEASE COURSE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MORTALITY; OVARIAN NEOPLASMS; SURVIVAL ANALYSIS;

ADENOCARCINOMA, CLEAR CELL; ANTINEOPLASTIC AGENTS; BIOMARKERS, TUMOR; BRCA1 PROTEIN; BRCA2 PROTEIN; CYSTADENOCARCINOMA, SEROUS; DISEASE PROGRESSION; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONE DEACETYLASES; HUMANS; MICRORNAS; OVARIAN NEOPLASMS; REPRESSOR PROTEINS; STAT1 TRANSCRIPTION FACTOR; SURVIVAL ANALYSIS;

EID: 84961206197     PISSN: 14737159     EISSN: 17448352     Source Type: Journal    
DOI: 10.1586/14737159.2016.1156532     Document Type: Review

References (91)

1. Siegel R, Ma J, Zou Z, et al. Cancer statistics, 2014. CA Cancer J Clin. 2014;64(1):9-29.
2. 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.
3. 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.
4. 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.
5. Prat J. Ovarian carcinomas: five distinct diseases with different origins, genetic alterations, and clinicopathological features. Virchows Arch. 2012;460(3):237-249.
6. Kurman RJ, Carcangiu ML, Herrington CS, et al., Eds. WHO classification of tumours of female reproductive organs. Lyon, France: IARC; 2014.
7. 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.
8. Weissman SM, Weiss SM, Newlin AC. Genetic testing by cancer site: ovary. Cancer J. 2012;18(4):320-327.
9. Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature. 2011;474(7353):609-615.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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.
15. 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.
16. 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.
17. 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.
18. 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.
19. 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.
20. 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.
21. 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.
22. 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.
23. 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.
24. 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 doi:10.1002/mc.22363. [Epub ahead of print].
25. 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.
26. 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.
27. 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.
28. 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.
29. 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.
30. 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.
31. 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.
32. 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.
33. 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.
34. 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.
35. 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.
36. Shih Ie M, 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.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. 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.
44. 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.
45. 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.
46. Katz B, Tropé CG, Reich R, et al. MicroRNAs in ovarian cancer. Hum Pathol. 2015;46(9):1245-1256.
47. 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.
48. 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.
49. 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.
50. 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.
51. 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.
52. 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.
53. Vang S, Wu HT, Fischer A, et al. Identification of ovarian cancer metastatic miRNAs. PLoS One. 2013;8:e58226.
54. 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.
55. 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.
56. 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.
57. Wang ZC, Birkbak NJ, Culhane AC, et al Australian ovarian cancer study group, Matulonis UA. Profiles of genomic instability in highgrade serous ovarian cancer predict treatment outcome. Clin Cancer Res. 2012;18(20):5806-5815.
58. 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.
59. 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.
60. 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.
61. 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.
62. 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.
63. 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.
64. 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.
65. 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.
66. 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.
67. 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.
68. 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.
69. Patch AM, Christie EL, Etemadmoghadam D, et al. Whole-genome characterization of chemoresistant ovarian cancer. Nature. 2015;521(7553):489-494.
70. Ahmed N, Stenvers KL. Getting to know ovarian cancer ascites: opportunities for targeted therapy-based translational research. Front Oncol. 2013;3:256.
71. 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.
72. Abubaker K, Luwor RB, Zhu H, et al. Inhibition of the JAK2/STAT3 pathway in ovarian cancer results in the loss of cancer stem celllike characteristics and a reduced tumor burden. BMC Cancer. 2014;14:317.
73. 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.
74. 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.
75. 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.
76. 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.
77. 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.
78. 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.
79. 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.
80. 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.
81. 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.
82. 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.
83. 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.
84. 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.
85. 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.
86. 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.
87. 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.
88. Domcke S, Sinha R, Levine DA, et al. Evaluating cell lines as tumour models by comparison of genomic profiles. Nat Commun. 2013;4:2126.
89. 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.
90. Blagden SP. Harnessing Pandemonium: The Clinical Implications of Tumor Heterogeneity in Ovarian Cancer. Front Oncol. 2015;5:149.
91. 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.