Ovarian Cancer Cell Line Panel (OCCP): Clinical Importance of In Vitro Morphological Subtypes

Beaufort, Corine M.; Helmijr, Jean C. A.; Piskorz, Anna M.; Hoogstraat, Marlous; Ruigrok-Ritstier, Kirsten; Besselink, Nicolle; Murtaza, Muhammed; van IJcken, Wilfred F. J.; Heine, Anouk A. J.; Smid, Marcel; Koudijs, Marco J.; Brenton, James D.; Berns, Els M. J. J.; Helleman, Jozien

doi:10.1371/journal.pone.0103988

Cited by 406Ovarian cancer diagnosis and treatmentCancer Cells and MetastasisOvarian function and disorders

Ovarian Cancer Cell Line Panel (OCCP): Clinical Importance of In Vitro Morphological Subtypes

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Beaufort, Corine M., Helmijr, Jean C. A., Piskorz, Anna M., Hoogstraat, Marlous, Ruigrok-Ritstier, Kirsten, Besselink, Nicolle, Murtaza, Muhammed, van IJcken, Wilfred F. J. +6 more·2014·PLoS ONE

DOI 10.1371/journal.pone.0103988PMC PMC4167545

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Abstract

Epithelial ovarian cancer is a highly heterogeneous disease and remains the most lethal gynaecological malignancy in the Western world. Therapeutic approaches need to account for inter-patient and intra-tumoural heterogeneity and detailed characterization of in vitro models representing the different histological and molecular ovarian cancer subtypes is critical to enable reliable preclinical testing. There are approximately 100 publicly available ovarian cancer cell lines but their cellular and molecular characteristics are largely undescribed. We have characterized 39 ovarian cancer cell lines under uniform conditions for growth characteristics, mRNA/microRNA expression, exon sequencing, drug response for clinically-relevant therapeutics and collated all available information on the original clinical features and site of origin. We tested for statistical associations between the cellular and molecular features of the lines and clinical features. Of the 39 ovarian cancer cell lines, 14 were assigned as high-grade serous, four serous-type, one low-grade serous and 20 non-serous type. Three morphological subtypes: Epithelial (n = 21), Round (n = 7) and Spindle (n = 12) were identified that showed distinct biological and molecular characteristics, including overexpression of cell movement and migration-associated genes in the Spindle subtype. Comparison with the original clinical data showed association of the spindle-like tumours with metastasis, advanced stage, suboptimal debulking and poor prognosis. In addition, the expression profiles of Spindle, Round and Epithelial morphologies clustered with the previously described C1-stromal, C5-mesenchymal and C4 ovarian subtype expression profiles respectively. Comprehensive profiling of 39 ovarian cancer cell lines under controlled, uniform conditions demonstrates clinically relevant cellular and genomic characteristics. This data provides a rational basis for selecting models to develop specific treatment approaches for histological and molecular subtypes of ovarian cancer.

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Often phenotypes such as drug response observed in vitro have been unable to mirror in vivo models, likely due to factors missing in the tumor microenvironment that are absent from homogeneous cell line cultures such as stromal and immune cells.
“Still, often phenotypes such as drug response observed in vitro have been unable to mirror in vivo models, likely due to factors missing in the tumor microenvironment that are absent from homogeneous cell lines cultures such as stromal and immune cells (Beaufort et al., 2014).”
From Three-dimensional modelling of ovarian cancer: from cell lines to organoids for discovery and personalized medicine (2022) · cites this paper as Beaufort et al., 2014

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Integrated genomic analyses of ovarian carcinoma
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Background
Multifactorial mechanisms associated with broad cross-resistance of ovarian carcinoma cells selected by cyanomorpholino doxorubicin.
Lau, D. H., Lewis, A. D., Ehsan, M. N., & Sikic, B. I. (1991) · PubMed · Cited by 97 · see citing works
Two Multiplex Assays That Simultaneously Identify 22 Possible Mutation Sites in the KRAS, BRAF, NRAS and PIK3CA Genes
Lurkin, I., Stoehr, R., Hurst, C. D., van Tilborg, A. A. G., Knowles, M. A., Hartmann, A., & Zwarthoff, E. C. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008802 · Cited by 95 · cited 1× · see citing works
“SNaPshot analysis was performed as described previously [20– 22] using an Applied Biosystems SNaPshot Multiplex Kit.”
Method
Pathway analysis of gene lists associated with platinum-based chemotherapy resistance in ovarian cancer: The big picture
Helleman, J., Smid, M., Jansen, M. P. H. M., van der Burg, M. E. L., & Berns, E. M. J. J. (2010) · Gynecologic Oncology · doi:10.1016/j.ygyno.2010.01.010 · Cited by 82 · cited 1× · see citing works
“In earlier studies we also observed an association between (TGFbeta-induced) ECM remodeling during EMT and chemotherapy resistance in ovarian cancer [18,79] as well as endocrine therapy resistance in breast cancer [80–82].”
Background
Synergistic inhibition of ovarian cancer cell growth by combining selective PI3K/mTOR and RAS/ERK pathway inhibitors
Sheppard, K. E., Cullinane, C. M., Hannan, K. M., Wall, M., Chan, J., Barber, F., Foo, J. H., Cameron, D. P., Neilsen, A., Ng, P. Y., et al. (2013) · European Journal of Cancer · doi:10.1016/j.ejca.2013.08.007 · Cited by 81 · cited 1× · see citing works
“Worldwide, there are about 100 ovarian cancer cell lines generated as described in literature [12–17] and about 70 of these are available at ATCC, ECACC, RIKEN, DSMZ, JCRB or Cancer Research Technology.”
Background
Mer receptor tyrosine kinase promotes invasion and survival in glioblastoma multiforme
Wang, Y., Moncayo, G. E., Morin, P., Xue, G., Grzmil, M., Lino, M. M., Clément‐Schatlo, V., Frank, S., Merlo, A. U., & Hemmings, B. A. (2012) · Oncogene · doi:10.1038/onc.2012.104 · Cited by 79 · cited 2× · see citing works
“The in vitro Round morphology has been associated with the side population that shares characteristics with tumour stem cells of cervical and gastric tumour cell lines [59,60] as well as with socalled amoeboid migration [61–65].”
Background
cis-diamminedichloroplatinum(II)-resistant sublines derived from two human ovarian tumor cell lines.
Kuppen, P. J. K., Schuitemaker, H., Veer, L. V. ‘., de Bruijn, E. A., van Oosterom, A. T., & Schrier, P. I. (1988) · PubMed · Cited by 76 · see citing works
EphA2 Induces Metastatic Growth Regulating Amoeboid Motility and Clonogenic Potential in Prostate Carcinoma Cells
Taddei, M. L., Parri, M., Angelucci, A., Bianchini, F., Marconi, C., Giannoni, E., Raugei, G., Bologna, M., Calorini, L., & Chiarugi, P. (2011) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-10-0298 · Cited by 76 · cited 2× · see citing works
“The in vitro Round morphology has been associated with the side population that shares characteristics with tumour stem cells of cervical and gastric tumour cell lines [59,60] as well as with socalled amoeboid migration [61–65].”
Background
FilGAP, a Rho/Rho-associated protein kinase–regulated GTPase-activating protein for Rac, controls tumor cell migration
Saito, K., Ozawa, Y., Hibino, K., & Ohta, Y. (2012) · Molecular Biology of the Cell · doi:10.1091/mbc.e12-04-0310 · Cited by 75 · cited 2× · see citing works
“The in vitro Round morphology has been associated with the side population that shares characteristics with tumour stem cells of cervical and gastric tumour cell lines [59,60] as well as with socalled amoeboid migration [61–65].”
Background
o,p′-DDD (mitotane) therapy of adrenal cortical carcinoma. Observations on drug dosage, toxicity, and steroid replacement
Hogan, T. F., Citrin, D. L., Johnson, B. M., Nakamura, S., Davis, T. E., & Borden, E. C. (1978) · Cancer · doi:10.1002/1097-0142(197811)42:5 · Cited by 72 · see citing works
Characterization of a Cell Line Derived From the Ascites of a Patient With Papillary Serous Cystadenocarcinoma of the Ovary 2
Wilson, A. P. (1984) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/72.3.513 · Cited by 72 · see citing works
Notch3 induces epithelial–mesenchymal transition and attenuates carboplatin-induced apoptosis in ovarian cancer cells
Gupta, N., Xu, Z., El‐Sehemy, A., Steed, H. L., & Fu, Y. (2013) · Gynecologic Oncology · doi:10.1016/j.ygyno.2013.03.019 · Cited by 71 · see citing works
Multiplexed array-based and in-solution genomic enrichment for flexible and cost-effective targeted next-generation sequencing
Harakaľová, M., Mokrý, M., Hrdličková, B., Renkens, I., Duran, K. J., van Roekel, H. S., Lansu, N. R., van Roosmalen, M. J., de Bruijn, E., Nijman, I. J., et al. (2011) · Nature Protocols · doi:10.1038/nprot.2011.396 · Cited by 70 · cited 1× · see citing works
“Processing of samples for sequencing on the SOLiD5500 sequencing platform (Life Technologies) was performed on a Sciclone NGS liquid handling robot (Perkin Elmer), based on the protocol for manual library preparation [23].”
Method
Fas signaling promotes motility and metastasis through epithelial–mesenchymal transition in gastrointestinal cancer
Zheng, H., Cai, Y. D., Wang, Y. D., Cui, X., Xie, T., Li, W. J., Peng, L., Zhang, Y., Wang, Z. Q., Wang, J., et al. (2012) · Oncogene · doi:10.1038/onc.2012.126 · Cited by 69 · cited 2× · see citing works
“Epithelial to mesenchymal transition (EMT) is typically defined by the acquisition of a Spindle morphology and up-regulation of mesenchymal markers such as SNAIL, ZEB, TWIST, VIM, FN1 and CAV1 [66–70].”
Background
Mutation discovery by targeted genomic enrichment of multiplexed barcoded samples
Nijman, I. J., Mokrý, M., van Boxtel, R., Toonen, P. W., de Bruijn, E., & Cuppen, E. P. J. G. (2010) · Nature Methods · doi:10.1038/nmeth.1516 · Cited by 67 · cited 1× · see citing works
“[24]) using a custom designed enrichment kit.”
RhoB regulates cell migration through altered focal adhesion dynamics
Vega, F. M. D. L., Colomba, A., Reymond, N., Thomas, M., & Ridley, A. J. (2012) · Open Biology · doi:10.1098/rsob.120076 · Cited by 61 · cited 2× · see citing works
“The in vitro Round morphology has been associated with the side population that shares characteristics with tumour stem cells of cervical and gastric tumour cell lines [59,60] as well as with socalled amoeboid migration [61–65].”
Background
Hyaluronic acid–paclitaxel: effects of intraperitoneal administration against CD44(+) human ovarian cancer xenografts
Stefano, I. D., Battaglia, A., Zannoni, G. F., Prisco, M. G., Fattorossi, A., Travaglia, D., Baroni, S., Renier, D., Scambia, G., Ferlini, C., et al. (2010) · Cancer Chemotherapy and Pharmacology · doi:10.1007/s00280-010-1462-2 · Cited by 58 · cited 4× · see citing works
“Response curves were generated for Carboplatin, Cisplatin, Oxaliplatin, Doxorubicin and 5-Fluorouracil (Intravenous solutions, Pharmachemie, The Netherlands), Paclitaxel (Intravenous solution, Ebewe Pharma, Austria), Docetaxel (dissolved in DMSO, Sigma), and Gemcitabin (for intravenous use, dissolved in PBS, Sun Pharm…”
BackgroundInfluential
Genotypic and Phenotypic Characterization of Side Population of Gastric Cancer Cell Lines
Schmuck, R. B., Warneke, V. S., Behrens, H., Simon, É., Weichert, W., & Röcken, C. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2010.12.043 · Cited by 57 · cited 1× · see citing works
“The in vitro Round morphology has been associated with the side population that shares characteristics with tumour stem cells of cervical and gastric tumour cell lines [59,60] as well as with socalled amoeboid migration [61–65].”
Background
The role of targeted therapy in ovarian cancer
Banerjee, S. N., & Kaye, S. B. (2011) · European Journal of Cancer · doi:10.1016/s0959-8049(11)70155-1 · Cited by 56 · cited 1× · see citing works
“Despite testing of diverse treatment strategies and new cytotoxic agents, optimal primary therapy and survival rates have not substantially changed since the introduction of platinum and taxane treatment [1–3].”
Background
Hotspot mutations in PIK3CA associate with first-line treatment outcome for aromatase inhibitors but not for tamoxifen
Ramirez-Ardila, D. E., Helmijr, J., Look, M. P., Lurkin, I., Ruigrok-Ritstier, K., Laere, S. V., Dirix, L. Y., Sweep, F. C. G. J., Span, P. N., Linn, S. C., et al. (2013) · Breast Cancer Research and Treatment · doi:10.1007/s10549-013-2529-7 · Cited by 54 · see citing works
HUMAN MACROVASCULAR ENDOTHELIAL CELLS: OPTIMIZATION OF CULTURE CONDITIONS
Terramani, T. T., Eton, D., BUI, P. A., WANG, Y., Weaver, F. A., & Yu, H. Y. (2000) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1290/1071-2690(2000)036 · Cited by 54 · see citing works
Cooperative Anti-Invasive Effect of Cdc42/Rac1 Activation and ROCK Inhibition in SW620 Colorectal Cancer Cells with Elevated Blebbing Activity
de Toledo, M., Anguille, C., Roger, L., Roux, P., & Gadéa, G. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048344 · Cited by 51 · see citing works
Integrated genomics of chemotherapy resistant ovarian cancer: A role for extracellular matrix, TGFbeta and regulating microRNAs
Helleman, J., Jansen, M. P. H. M., Burger, C. W., van der Burg, M. E. L., & Berns, E. M. J. J. (2009) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2009.10.016 · Cited by 48 · cited 1× · see citing works
“In earlier studies we also observed an association between (TGFbeta-induced) ECM remodeling during EMT and chemotherapy resistance in ovarian cancer [18,79] as well as endocrine therapy resistance in breast cancer [80–82].”
Background
Mapping of chromosome 3p deletions in human epithelial ovarian tumors
Lounis, H., Mes‐Masson, A., Dion, F., Bradley, W. E. C., Seymour, R. J., Provencher, D. M., & Tonin, P. N. (1998) · Oncogene · doi:10.1038/sj.onc.1202152 · Cited by 46 · see citing works
Four human breast cancer cell lines with biallelic inactivating α-catenin gene mutations
Hollestelle, A., Elstrodt, F., Timmermans, M. A. M., Sieuwerts, A. M., Klijn, J. G. M., Foekens, J. A., den Bakker, M. A., & Schutte, M. E. M. (2009) · Breast Cancer Research and Treatment · doi:10.1007/s10549-009-0545-4 · Cited by 40 · cited 1× · see citing works
“These three morphological phenotypes were previously observed in multiple types of cancer cell lines including cervical, gastric, prostate, colorectal, lung and glioblastoma [59–70] and a panel of 54 breast cancer cell lines [58].”
Background
Sorting and identification of side population cells in the human cervical cancer cell line HeLa
Qi, W., Zhao, C., Zhao, L., Liu, N., Li, X., Yu, W., & Wei, L. (2014) · Cancer Cell International · doi:10.1186/1475-2867-14-3 · Cited by 40 · cited 1× · see citing works
“The in vitro Round morphology has been associated with the side population that shares characteristics with tumour stem cells of cervical and gastric tumour cell lines [59,60] as well as with socalled amoeboid migration [61–65].”
Background
Tumor progression studied by analysis of cellular features of serial ascitic ovarian carcinoma tumors.
Mackillop, W. J., Trent, J. M., Stewart, S. S., & Buick, R. N. (1983) · PubMed · Cited by 31 · see citing works
Effects of interferons on the expression of the proto‐oncogene her‐2 in human ovarian carcinoma cells
Marth, C., Cronauer, M. V., Doppler, W., Öfner, D., Ullrich, A., & Daxenbichler, G. (1992) · International Journal of Cancer · doi:10.1002/ijc.2910500114 · Cited by 31 · see citing works
Plasminogen activator secretion by established lines of human ovarian carcinoma cells in vitro
Karlan, B. Y., Amin, W., Band, V., Zurawski, V. R., & Littlefield, B. A. (1988) · Gynecologic Oncology · doi:10.1016/0090-8258(88)90276-4 · Cited by 26 · see citing works
Characterisation of seven human ovarian tumour cell lines
Wilson, A., Dent, M. F., Pejovic, T. B., Hubbold, L., & Radford, H. (1996) · British Journal of Cancer · doi:10.1038/bjc.1996.428 · Cited by 22 · see citing works
Novel mechanism of reduced proliferation in ovarian clear cell carcinoma cells: Cytoplasmic sequestration of CDK2 by p27
Itamochi, H., Yoshida, T., Walker, C. L., Bartholomeusz, C., Aoki, D., Ishihara, H., Suzuki, N., Kigawa, J., Terakawa, N., & Ueno, N. T. (2011) · Gynecologic Oncology · doi:10.1016/j.ygyno.2011.05.003 · Cited by 22 · cited 1× · see citing works
“Worldwide, there are about 100 ovarian cancer cell lines generated as described in literature [12–17] and about 70 of these are available at ATCC, ECACC, RIKEN, DSMZ, JCRB or Cancer Research Technology.”
Background
Paradoxical increase in DNA cross-linking in a human ovarian carcinoma cell line resistant to cyanomorpholino doxorubicin.
Lau, D. H. M., Ross, K. L., & Sikic, B. I. (1990) · PubMed · Cited by 16 · see citing works
First line therapy: have we made any improvement?
Bookman, M. A. (2011) · European Journal of Cancer · doi:10.1016/s0959-8049(11)70153-8 · Cited by 5 · cited 1× · see citing works
“Despite testing of diverse treatment strategies and new cytotoxic agents, optimal primary therapy and survival rates have not substantially changed since the introduction of platinum and taxane treatment [1–3].”
Background
Differential hRad17 expression by histologic subtype of ovarian cancer
Young, J. L., Koon, E. C., Kwong, J., Welch, W. R., Muto, M. G., Berkowitz, R. S., & Mok, S. C. (2011) · Journal of Ovarian Research · doi:10.1186/1757-2215-4-6 · Cited by 2 · cited 1× · see citing works
“Worldwide, there are about 100 ovarian cancer cell lines generated as described in literature [12–17] and about 70 of these are available at ATCC, ECACC, RIKEN, DSMZ, JCRB or Cancer Research Technology.”
Background

Flagged first, then by citations

Sorted by citations

Rethinking ovarian cancer II: reducing mortality from high-grade serous ovarian cancer
Bowtell, D. D. L., Böhm, S., Ahmed, A. A., Aspuria, P.-J. P., Bast, R. C., Beral, V., Berek, J. S., Birrer, M. J., Blagden, S. P., Bookman, M. A., et al. (2015) · Nature reviews. Cancer · doi:10.1038/nrc4019 · Cited by 1,365 · see citing works
The m6A reader YTHDF1 promotes ovarian cancer progression via augmenting EIF3C translation
Liu, T., Wei, Q., Jin, J., Luo, Q., Liu, Y., Yu, Y., Cheng, C., Li, L., Pi, J., Si, Y., et al. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa048 · Cited by 751 · see citing works
“Albeit A2780 and SKOV3 are most frequently used for ovarian cancer studies, particularly for high-grade serous ovarian cancer, they are probably originated from endometrioid or clear cell ovarian cancer (39).”
Background
High-Grade Serous Ovarian Cancer: Basic Sciences, Clinical and Therapeutic Standpoints
Lisio, M. A., Fu, L., Goyeneche, A. A., Gao, Z., & Telleria, C. M. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20040952 · Cited by 685 · see citing works
The molecular landscape of colorectal cancer cell lines unveils clinically actionable kinase targets
Medico, E., Russo, M., Picco, G., Cancelliere, C., Valtorta, E., Corti, G., Buscarino, M., Isella, C., Lamba, S., Martinoglio, B., et al. (2015) · Nature Communications · doi:10.1038/ncomms8002 · Cited by 302 · see citing works
In vivo tumor growth of high-grade serous ovarian cancer cell lines
Mitra, A. K., Davis, D. A., Tomar, S., Roy, L., Main, H. G., Xie, J., Lantvit, D. D., Cárdenas, H., Fang, F., Liu, Y., et al. (2015) · Gynecologic Oncology · doi:10.1016/j.ygyno.2015.05.040 · Cited by 214 · see citing works
Integrative proteomic profiling of ovarian cancer cell lines reveals precursor cell associated proteins and functional status
Coscia, F., Watters, K. M., Curtis, M., Eckert, M. A., Chiang, C. Y., Tyanova, S., MONTAG, A. G., Lastra, R. R., Lengyel, E. R., & Mann, M. (2016) · Nature Communications · doi:10.1038/ncomms12645 · Cited by 207 · see citing works
“This group also contained the TOV112D and A2780 cell line pairs, previously described as endometrioid in origin 9,24,25 .”
Molecular mechanisms of drug resistance in ovarian cancer
Norouzi‐Barough, L., Sarookhani, M. R., Sharifi, M., Moghbelinejad, S., Jangjoo, S., & Salehi, R. (2017) · Journal of Cellular Physiology · doi:10.1002/jcp.26289 · Cited by 200 · see citing works
“Among the gynecological cancers, ovarian carcinoma is the most lethal malignancy and the sixth leading cause of cancer mortality among women worldwide (Beaufort et al., 2014; Sankaranarayanan & Ferlay, 2006).”
Background
ACSL4 and polyunsaturated lipids support metastatic extravasation and colonization
Wang, Y., Hu, M., Cao, J., Wang, F., Han, J. R., Wu, T. W., Li, L., Yu, J., Fan, Y., Xie, G., et al. (2024) · Cell · doi:10.1016/j.cell.2024.10.047 · Cited by 191 · see citing works
TRIP13 regulates DNA repair pathway choice through REV7 conformational change
Clairmont, C. S., Sarangi, P., Ponnienselvan, K., Galli, L. D., Csete, I. S., Moreau, L. A., Adelmant, G., Chowdhury, D., Marto, J. A., & D’Andrea, A. D. (2020) · Nature Cell Biology · doi:10.1038/s41556-019-0442-y · Cited by 156 · see citing works
Selective Targeting of Cyclin E1-Amplified High-Grade Serous Ovarian Cancer by Cyclin-Dependent Kinase 2 and AKT Inhibition
Au‐Yeung, G., Lang, F., Azar, W. J., Mitchell, T. J., Jarman, K. E., Lackovic, K., Aziz, D., Cullinane, C. M., Pearson, R. B., Mileshkin, L., et al. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-0620 · Cited by 147 · see citing works
Ovarian cancer stem cells: still an elusive entity?
Lupia, M., & Cavallaro, U. (2017) · Molecular Cancer · doi:10.1186/s12943-017-0638-3 · Cited by 149 · see citing works
Formation of stable small cell number three-dimensional ovarian cancer spheroids using hanging drop arrays for preclinical drug sensitivity assays
Raghavan, S. A., Ward, M. R., Rowley, K. R., Wold, R. M., Takayama, S., Buckanovich, R. J., & Mehta, G. (2015) · Gynecologic Oncology · doi:10.1016/j.ygyno.2015.04.014 · Cited by 136 · see citing works
“demonstrated that the OVCAR3 cell line falls under the category of high-grade serous histotype, while the A2780 cell line was more representative of an endometrioid histotype [18].”
Background
Low-grade serous ovarian cancer: State of the science
Slomovitz, B. M., Gourley, C., Carey, M. S., Malpica, A. L., Shih, I., Huntsman, D. D., Fader, A. N., Grisham, R. N., Schlumbrecht, M. P., Sun, C. C., et al. (2020) · Gynecologic Oncology · doi:10.1016/j.ygyno.2019.12.033 · Cited by 133 · see citing works
Distinct transcriptional programs stratify ovarian cancer cell lines into the five major histological subtypes
Barnes, B. M., Nelson, L., Tighe, A., Burghel, G. J., Lin, I., Desai, S. N., McGrail, J. C., Morgan, R. D., & Taylor, S. S. (2021) · Genome Medicine · doi:10.1186/s13073-021-00952-5 · Cited by 138 · see citing works
Epigenetics in ovarian cancer
Natanzon, Y., Goode, E. L., & Cunningham, J. M. (2017) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2017.08.003 · Cited by 134 · see citing works
C/EBPβ enhances platinum resistance of ovarian cancer cells by reprogramming H3K79 methylation
Liu, D., Zhang, X., Li, M., Cao, C., Wan, D., Xi, B., Tan, J., Wang, J., Yang, Z., Feng, X., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03590-5 · Cited by 125 · see citing works
Characterization of Ovarian Cancer Cell Lines as In Vivo Models for Preclinical Studies
Hernandez, L., Kim, M. K., Lyle, L. T., Bunch, K. P., House, C. D., Ning, F., Noonan, A. M., & Annunziata, C. M. (2016) · Gynecologic Oncology · doi:10.1016/j.ygyno.2016.05.028 · Cited by 121 · see citing works
“Recent studies have reported comprehensive data gathered for the most commonly available ovarian cancer cell lines (8, 9).”
Design, synthesis and biological evaluation of thiosemicarbazones, hydrazinobenzothiazoles and arylhydrazones as anticancer agents with a potential to overcome multidrug resistance
Pape, V. F. S., Tóth, S., Füredi, A., Szebényi, K., Lovrics, A., Szabó, P. T., Wiese, M., & Szakács, G. (2016) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2016.03.078 · Cited by 112 · see citing works
SIRT5 Promotes Cisplatin Resistance in Ovarian Cancer by Suppressing DNA Damage in a ROS-Dependent Manner via Regulation of the Nrf2/HO-1 Pathway
Sun, X., Wang, S., Gai, J., Guan, J., Li, J., Li, Y., Zhao, J., Zhao, C., Fu, L., & Li, Q. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00754 · Cited by 110 · see citing works
Ovarian cancer cell lines derived from non-serous carcinomas migrate and invade more aggressively than those derived from high-grade serous carcinomas
Hallas-Potts, A., Dawson, J. C., & Herrington, C. S. (2019) · Scientific Reports · doi:10.1038/s41598-019-41941-4 · Cited by 110 · see citing works
Prognostic and therapeutic value of disruptor of telomeric silencing-1-like (DOT1L) expression in patients with ovarian cancer
Zhang, X., Liu, D., Li, M., Cao, C., Wan, D., Xi, B., Li, W., Tan, J., Wang, J., Wu, Z., et al. (2017) · Journal of Hematology & Oncology · doi:10.1186/s13045-017-0400-8 · Cited by 96 · see citing works
“inhibitors on a larger ovarian cancer cell line panel in vitro, we chose OV90 and CaOV3, which could represent high-grade serous ovarian cancer for CCK8 and colony formation assay [33].”
Altered glutamine metabolism in platinum resistant ovarian cancer
Hudson, C. D., Savadelis, A., Nagaraj, A. B., Joseph, P. L., Avril, S., DiFeo, A. V., & Avril, N. E. (2016) · Oncotarget · doi:10.18632/oncotarget.9317 · Cited by 95 · see citing works
“2) and endometrioid (A2780; [47, 48]) which together account for more than 90% of human ovarian cancer cases, thereby making our results highly clinically relevant.”
Result
Current strategies for different paclitaxel-loaded Nano-delivery Systems towards therapeutic applications for ovarian carcinoma: A review article
Khalifa, A. M., Elsheikh, M. A., Khalifa, A., & Elnaggar, Y. S. R. (2019) · Journal of Controlled Release · doi:10.1016/j.jconrel.2019.08.034 · Cited by 94 · see citing works
The role of GRHL2 and epigenetic remodeling in epithelial–mesenchymal plasticity in ovarian cancer cells
Chung, V. Y., Tan, T. Z., Ye, J., Huang, R., Lai, H., Kappei, D., Wollmann, H., Guccione, E., & Huang, R. Y. (2019) · Communications Biology · doi:10.1038/s42003-019-0506-3 · Cited by 91 · see citing works
Ovarian Carcinoma-Associated Mesenchymal Stem Cells Arise from Tissue-Specific Normal Stroma
Coffman, L. G., Pearson, A. T., Frisbie, L. G., Freeman, Z. T., Christie, E. L., Bowtell, D. D. L., & Buckanovich, R. J. (2018) · Stem Cells · doi:10.1002/stem.2932 · Cited by 87 · see citing works
Current Status of Patient-Derived Ovarian Cancer Models
Maru, Y., & Hippo, Y. (2019) · Cells · doi:10.3390/cells8050505 · Cited by 88 · see citing works
Characterization of SOX2, OCT4 and NANOG in Ovarian Cancer Tumor-Initiating Cells
Robinson, M., Gilbert, S. F., Waters, J. A., Lujano-Olazaba, O., Lara, J., Alexander, L. J., Green, S. E., Burkeen, G., Patrus, O., Sarwar, Z., et al. (2021) · Cancers · doi:10.3390/cancers13020262 · Cited by 84 · see citing works
“SOX2 reached significance across all the confirmed HGSOC lines, while OCT4 and NANOG expression was variable.”
ResultInfluential
YAP induces high-grade serous carcinoma in fallopian tube secretory epithelial cells
Hua, G., Lv, X., He, C., Remmenga, S. W., Rodabough, K. J., Dong, J., Yang, L., Lele, S. M., Yang, P., Zhou, J., et al. (2015) · Oncogene · doi:10.1038/onc.2015.288 · Cited by 83 · see citing works
“OVSAHO, a verified high grade ovarian serous carcinoma cell lines 43, 75 , have been used to replace the FT194-YAP S127A cells to confirm the role of verteporfin and BGJ398 on the growth of ovarian HGSC tumor in vitro using the same experimental design.”
Studying platinum sensitivity and resistance in high-grade serous ovarian cancer: Different models for different questions
Alkema, N. G., Wisman, G. B. A., van der Zee, A. G. J., van Vugt, M. A. T. M., & de Jong, S. (2015) · Drug Resistance Updates · doi:10.1016/j.drup.2015.11.005 · Cited by 80 · see citing works
“Therefore, a shift in in vitro ovarian cancer research is warranted, restricting in vitro experiments to well-defined cell lines that have been characterized extensively (Anglesio et al., 2013; Beaufort et al., 2014).”
Background
Functional characterization of a panel of high-grade serous ovarian cancer cell lines as representative experimental models of the disease
Haley, J., Tomar, S., Pulliam, N., Xiong, S., Perkins, S. M., Karpf, A. R., Mitra, S., Nephew, K. P., & Mitra, A. K. (2016) · Oncotarget · doi:10.18632/oncotarget.9053 · Cited by 80 · see citing works
“” A number of the cell lines listed as “likely high-grade serous” in this study have had this status confirmed in other studies using a variety of metrics [5, 7, 9].”
BackgroundResultInfluential
miR-634 restores drug sensitivity in resistant ovarian cancer cells by targeting the Ras-MAPK pathway
van Jaarsveld, M. T. M., van Kuijk, P. F., Boersma, A. W. M., Helleman, J., van IJcken, W. F. J., Mathijssen, R. H. J., Pothof, J., Berns, E. M. J. J., Verweij, J., & Wiemer, E. A. C. (2015) · Molecular Cancer · doi:10.1186/s12943-015-0464-4 · Cited by 79 · see citing works
“Characteristics of the ovarian cancer cells were published in [50] and the authenticity of cell lines was verified by STR analysis.”
Cell line and patient-derived xenograft models reveal elevated CDCP1 as a target in high-grade serous ovarian cancer
Harrington, B. S., He, Y., Davies, C. M., Wallace, S. J., Adams, M. N., Beaven, E. A., Roche, D., Kennedy, C. J., Chetty, N., Crandon, A. J., et al. (2016) · British Journal of Cancer · doi:10.1038/bjc.2015.471 · Cited by 73 · see citing works
“…cancer, and although the immuno-phenotype of SKOV3 cells most closely resembles the profile seen in HGSC patients (Anglesio et al, 2013), it has recently been proposed that this line is poorly suited as a model for this malignancy (Anglesio et al, 2013; Domcke et al, 2013; Beaufort et al, 2014).”
Background
MicroRNA-503-5p Inhibits the CD97-Mediated JAK2/STAT3 Pathway in Metastatic or Paclitaxel-Resistant Ovarian Cancer Cells
Park, G. B., & Kim, D. (2019) · Neoplasia · doi:10.1016/j.neo.2018.12.005 · Cited by 72 · see citing works
Gene expression of membrane transporters: Importance for prognosis and progression of ovarian carcinoma
Elsnerová, K., Mohelníková-Duchoňová, B., Cerovská, E., Ehrlichová, M., Gut, I., Rob, L., Škapa, P., Hruda, M., Bartáková, A., Bouda, J., et al. (2016) · Oncology Reports · doi:10.3892/or.2016.4599 · Cited by 71 · see citing works
Structure-Based Optimization of a Novel Class of Aldehyde Dehydrogenase 1A (ALDH1A) Subfamily-Selective Inhibitors as Potential Adjuncts to Ovarian Cancer Chemotherapy
Huddle, B. C., Grimley, E. C., Buchman, C. D., Chtcherbinine, M., Debnath, B., Mehta, P., Yang, K., Morgan, C. A., Li, S., Felton, J. A., et al. (2018) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.8b00930 · Cited by 71 · see citing works
Anti-cancer effects of Kaempferia parviflora on ovarian cancer SKOV3 cells
Paramee, S., Sookkhee, S., Sakonwasun, C., Takuathung, M. N., Mungkornasawakul, P., Nimlamool, W., & Potikanond, S. (2018) · BMC Complementary and Alternative Medicine · doi:10.1186/s12906-018-2241-6 · Cited by 68 · see citing works
“Since SKOV3 cells are known to be a high grade serous adenocarcinoma which has been reported to have high metastatic rate [16, 18].”
Background
Three-dimensional modelling of ovarian cancer: from cell lines to organoids for discovery and personalized medicine
Yee, C., Dickson, K.-A., Muntasir, M. N., Ma, Y., & Marsh, D. J. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.836984 · Cited by 66 · see citing works
Lysophospholipid Signaling in the Epithelial Ovarian Cancer Tumor Microenvironment
Xu, Y. (2018) · Cancers · doi:10.3390/cancers10070227 · Cited by 66 · see citing works
Wnt signaling modulator DKK1 as an immunotherapeutic target in ovarian cancer
Betella, I., Turbitt, W. J., Szul, T., Wu, B., Martínez, A., Katre, A. K., Wall, J. A., Norian, L. A., Birrer, M. J., & Arend, R. C. (2020) · Gynecologic Oncology · doi:10.1016/j.ygyno.2020.03.010 · Cited by 66 · see citing works
Targeting the tumour microenvironment in platinum-resistant ovarian cancer
Cummings, M., Freer, C., & Orsi, N. M. (2021) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2021.02.007 · Cited by 65 · see citing works
Therapeutic Gene Silencing Using Targeted Lipid Nanoparticles in Metastatic Ovarian Cancer
Singh, M. S., Ramishetti, S., Landesman‐Milo, D., Goldsmith, M., Chatterjee, S., Palakuri, R., & Peer, D. (2021) · Small · doi:10.1002/smll.202100287 · Cited by 65 · see citing works
NID1, a new regulator of EMT required for metastasis and chemoresistance of ovarian cancer cells
Zhou, Y., Zhu, Y., Fan, X., Zhang, C., Wang, Y., Zhang, L., Zhang, H., Wen, T., Zhang, K., Huo, X., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.16145 · Cited by 63 · see citing works
“Beaufort and colleagues characterized a series of ovarian cancer cell lines into a spindle subtype and an epithelial subtype, based on hierarchical clustering using differentially expressed genes [18].”
Background
Chemotherapy-Induced Distal Enhancers Drive Transcriptional Programs to Maintain the Chemoresistant State in Ovarian Cancer
Shang, S., Yang, J., Jazaeri, A. A., Duval, A. J., Tufan, T., Fischer, N. L., Benamar, M., Guessous, F., Lee, I.-Y., Campbell, R. M., et al. (2019) · Cancer Research · doi:10.1158/0008-5472.can-19-0215 · Cited by 62 · see citing works
“However, recent molecular profiling efforts suggested that the origin of some of these cell lines such as SKOV3 is likely non-serous epithelial ovarian cancer (25, 26).”
Background
DNA methylation changes in epithelial ovarian cancer histotypes
Earp, M. A., & Cunningham, J. M. (2015) · Genomics · doi:10.1016/j.ygeno.2015.09.001 · Cited by 58 · see citing works
Mutant p53 promotes ovarian cancer cell adhesion to mesothelial cells via integrin β4 and Akt signals
Lee, J.-G., Ahn, J., Kim, T. J., Lee, J. H., & Choi, J. (2015) · Scientific Reports · doi:10.1038/srep12642 · Cited by 58 · see citing works
MAP3K8/TPL-2/COT is a potential predictive marker for MEK inhibitor treatment in high-grade serous ovarian carcinomas
Gruosso, T., Garnier, C., Abélanet, S., Kieffer, Y., Lemesre, V., Bellanger, D., Bièche, I., Marangoni, E., Sastre‐Garau, X., Mieulet, V., et al. (2015) · Nature Communications · doi:10.1038/ncomms9583 · Cited by 57 · see citing works
Small molecule inhibitor of TLR4 inhibits ovarian cancer cell proliferation: new insight into the anticancer effect of TAK-242 (Resatorvid)
Kashani, B., Zandi, Z., Bashash, D., Zaghal, A., Momeny, M., Poursani, E. M., Pourbagheri‐Sigaroodi, A., Mousavi, S. A., & Ghaffari, S. H. (2019) · Cancer Chemotherapy and Pharmacology · doi:10.1007/s00280-019-03988-y · Cited by 57 · see citing works
GALNT14 Regulates Ferroptosis and Apoptosis of Ovarian Cancer Through the EGFR/mTOR Pathway
Li, H.-W., Liu, M., Jiang, X., Song, T., Feng, S., Wu, J., Deng, P., & Wang, X. (2021) · Future Oncology · doi:10.2217/fon-2021-0883 · Cited by 56 · see citing works
Serine-Arginine Protein Kinase 1 (SRPK1) as a Prognostic Factor and Potential Therapeutic Target in Cancer: Current Evidence and Future Perspectives
Nikas, I. P., Themistocleous, S., Paschou, S. Α., Tsamis, K. I., & Ryu, H. S. (2019) · Cells · doi:10.3390/cells9010019 · Cited by 54 · see citing works
“used the A2780 ovarian cancer cell line for their experiments [71], which was later found not to represent the most common histology type of ovarian cancer, the high-grade serous carcinoma [89,90].”
Method
GAS6/AXL Inhibition Enhances Ovarian Cancer Sensitivity to Chemotherapy and PARP Inhibition through Increased DNA Damage and Enhanced Replication Stress
Mullen, M. M., Lomonosova, E., Toboni, M. D., Oplt, A., Cybulla, E., Blachut, B., Zhao, P., Noia, H., Wilke, D., Rankin, E. B., et al. (2021) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-21-0302 · Cited by 53 · see citing works
Class I-Histone Deacetylase (HDAC) Inhibition is Superior to pan-HDAC Inhibition in Modulating Cisplatin Potency in High Grade Serous Ovarian Cancer Cell Lines
Bandolik, J. J., Hamacher, A., Schrenk, C., Weishaupt, R., & Kassack, M. U. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20123052 · Cited by 52 · see citing works
“In addition to the four HGSOC cell lines, A2780 was included as a comparison model for ovarian endometrioid adenocarcinoma (type I) [28,29]—a less aggressive type of ovarian cancer.”
The Endometriotic Tumor Microenvironment in Ovarian Cancer
Wendel, J. R. H., Wang, X., & Hawkins, S. M. (2018) · Cancers · doi:10.3390/cancers10080261 · Cited by 51 · see citing works
“COV362 Endometrioid (pleural effusion) Serous TP53, BRCA1, RB1 *, EGFR, APC MYC [178,180,182,196]”
Background
Characterisation of Ovarian Cancer Cell Line NIH-OVCAR3 and Implications of Genomic, Transcriptomic, Proteomic and Functional DNA Damage Response Biomarkers for Therapeutic Targeting
Bradbury, A., O'Donnell, R. L., Drew, Y., Curtin, N. J., & Saha, S. S. (2020) · Cancers · doi:10.3390/cancers12071939 · Cited by 52 · see citing works
“However, more recent studies such as Beaufort et al., 2014 [10] and the GDSC database (https: //www.cancerrxgene. rg/) highlight conflicting results.”
BackgroundResultInfluential
Cellular models of development of ovarian high‐grade serous carcinoma: A review of cell of origin and mechanisms of carcinogenesis
Mei, J., Tian, H., Huang, H.-S., Hsu, C., Liou, Y., Wu, N., Zhang, W., & Chu, T. (2021) · Cell Proliferation · doi:10.1111/cpr.13029 · Cited by 50 · see citing works
Carboplatin response in preclinical models for ovarian cancer: comparison of 2D monolayers, spheroids, ex vivo tumors and in vivo models
Brodeur, M. N., Simeone, K., Leclerc-Deslauniers, K., Fleury, H., Carmona, E., Provencher, D. M., & Mes‐Masson, A. (2021) · Scientific Reports · doi:10.1038/s41598-021-97434-w · Cited by 50 · see citing works
[Cu(o-phthalate)(phenanthroline)] Exhibits Unique Superoxide-Mediated NCI-60 Chemotherapeutic Action through Genomic DNA Damage and Mitochondrial Dysfunction
Slator, C., Barron, N., Howe, O. L., & Kellett, A. (2015) · ACS Chemical Biology · doi:10.1021/acschembio.5b00513 · Cited by 49 · see citing works
Comparison of cell-based assays to quantify treatment effects of anticancer drugs identifies a new application for Bodipy-L-cystine to measure apoptosis
Kumar, N., Afjei, R., Massoud, T. F., & Paulmurugan, R. (2018) · Scientific Reports · doi:10.1038/s41598-018-34696-x · Cited by 49 · see citing works
Establishment of Acquired Cisplatin Resistance in Ovarian Cancer Cell Lines Characterized by Enriched Metastatic Properties with Increased Twist Expression
Bahar, E., Kim, J., Kim, H.-S., & Yoon, H. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21207613 · Cited by 49 · see citing works
“To generate CisR OC cell lines, we selected two OC cell lines including the high-grade serous epithelial OC model cell line, OV-90, and the mixed epithelial OC cell line, SKOV-3 [41,42].”
Method
Effect of estrogen receptor β agonists on proliferation and gene expression of ovarian cancer cells
Schüler‐Toprak, S., Moehle, C., Skrzypczak, M., Ortmann, O., & Treeck, O. (2017) · BMC Cancer · doi:10.1186/s12885-017-3246-0 · Cited by 48 · see citing works
“OVCAR-3 cells were attained from ascites of a patient with highgrade serous ovarian cancer (G3) and exhibit a mutation of p53 [43].”
Genome-Wide Interrogation of Human Cancers Identifies EGLN1 Dependency in Clear Cell Ovarian Cancers
Price, C. O., Gill, S., Ho, Z. V., Davidson, S. M., Merkel, E., McFarland, J. M., Leung, L., Tang, A., Kost‐Alimova, M., Tsherniak, A., et al. (2019) · Cancer Research · doi:10.1158/0008-5472.can-18-2674 · Cited by 46 · see citing works
“To determine whether EGLN1 dependency was enriched in a specific subtype we grouped the ovarian cancer cell lines by historical pathological, molecular and histological subtypes [Supplementary Table 5, adapted from (31, 34, 36)].”
BackgroundMethod
Sox2 promotes expression of the ST6Gal-I glycosyltransferase in ovarian cancer cells
Dorsett, K. A., Jones, R. B., Ankenbauer, K. E., Hjelmeland, A. B., & Bellis, S. L. (2019) · Journal of Ovarian Research · doi:10.1186/s13048-019-0574-5 · Cited by 47 · see citing works
FOXM1 is a downstream target of LPA and YAP oncogenic signaling pathways in high grade serous ovarian cancer
Fan, Q., Cai, Q., & Xu, Y. (2015) · Oncotarget · doi:10.18632/oncotarget.4280 · Cited by 46 · see citing works
“Recently, the most commonly used EOC cell lines, including A2780 and SKOV3, have been considered as non-HGSC cell lines [14, 38] based on genetic and functional characterizations.”
Background
Glucose deprivation elicits phenotypic plasticity via ZEB1-mediated expression of NNMT
Kanska, J. E., Aspuria, P.-J. P., Taylor‐Harding, B., Spurka, L., Funari, V. A., Oršulić, S., Karlan, B. Y., & Wiedemeyer, W. R. (2017) · Oncotarget · doi:10.18632/oncotarget.15429 · Cited by 46 · see citing works
“Similarly, we used CRISPR/Cas9 to deplete NNMT in SKOV3 ovarian cancer cells (endometrioid/clear cell subtype [40]), a cell line previously shown to have high NNMT activity [41].”
Method
Characteristics of in Vivo Model Systems for Ovarian Cancer Studies
Tudrej, P., Kujawa, K. A., Cortez, A. J., & Lisowska, K. M. (2019) · Diagnostics · doi:10.3390/diagnostics9030120 · Cited by 46 · see citing works
“Only OVCAR3 cells, which are described as derived from poorly differentiated papillary adenocarcinoma [51], give such tumors in nude mice [52].”
BackgroundInfluential
Human-Derived Model Systems in Gynecological Cancer Research
Lõhmussaar, K., Boretto, M., & Clevers, H. C. (2020) · Trends in cancer · doi:10.1016/j.trecan.2020.07.007 · Cited by 46 · see citing works
Convergence of Wnt and Notch signaling controls ovarian cancer cell survival
Bocchicchio, S., Tesone, M., & Irusta, G. (2019) · Journal of Cellular Physiology · doi:10.1002/jcp.28775 · Cited by 45 · see citing works
“…β‐catenin and Notch crosstalk could have therapeutic implications, at least, in serous/mucinous and endometroid/clear cells histological subtypes (Beaufort et al., 2014; Domcke, Sinha, Levine, Sander, & Schultz, 2013) C 1 10 20 0.00 0.25 0.50 0.75 1.00 1.25 Concentration of ICG-001 (μM)R el at…”
ResultInfluential
Progesterone Enhances Niraparib Efficacy in Ovarian Cancer by Promoting Palmitoleic-Acid-Mediated Ferroptosis
Wu, N., Zhang, X., Fang, C., Zhu, M., Wang, Z., Jian, L., Tan, W., Wang, Y., Li, H., Xu, X., et al. (2024) · Research · doi:10.34133/research.0371 · Cited by 44 · see citing works
“Molecular characterization of A2780 cells also showed a non-HGSC profile with ARID1A , BRAF , PIK3CA , and PTEN mutations, microsatellite instability, and wild-type TP53 [51–53].”
Background
Nanoparticle delivery systems to combat drug resistance in ovarian cancer
Miller, E., Samec, T., & Alexander-Bryant, A. A. (2020) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2020.102309 · Cited by 44 · see citing works
Differences in MEK inhibitor efficacy in molecularly characterized low-grade serous ovarian cancer cell lines.
Llauradó, M., DiMattia, G. E., Dawson, A., Bamford, S., Anderson, S. A., Hennessy, B. T., Anglesio, M. S., Shepherd, T. G., Salamanca, C. M., Hoenisch, J., et al. (2016) · PubMed Central · Cited by 42 · see citing works
Common biological phenotypes characterize the acquisition of platinum-resistance in epithelial ovarian cancer cells
Sonego, M., Pellizzari, I., Dall’Acqua, A., Pivetta, E., Lorenzon, I., Benevol, S., Bomben, R., Spessotto, P., Sorio, R., Gattei, V., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-07005-1 · Cited by 43 · see citing works
Efficient leukocyte depletion by a novel microfluidic platform enables the molecular detection and characterization of circulating tumor cells
Obermayr, E., Maritschnegg, E., Agreiter, C., Pecha, N., Speiser, P., Helmy-Bader, S., Danzinger, S., Krainer, M., Singer, C., & Zeillinger, R. (2017) · Oncotarget · doi:10.18632/oncotarget.22549 · Cited by 43 · see citing works
“We used two quite different cell lines for the spiking experiments, in terms of EpCAM protein expression, morphology, mutational status, doubling time, et cetera [25].”
Method
Kallikrein-related peptidases represent attractive therapeutic targets for ovarian cancer
Loessner, D., Goettig, P., Preis, S., Felber, J., Bronger, H., Clements, J. A., Dorn, J., & Magdolen, V. (2018) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2018.1512587 · Cited by 43 · see citing works
“Beaufort and colleagues reported that OVCAR-3 have a high grade serous histology and a putative endometrioid/clear cell and clear cell histology for SKOV-3 and ES-2 cells respectively [46].”
Background
Apatinib, a Novel Tyrosine Kinase Inhibitor, Promotes ROS-Dependent Apoptosis and Autophagy via the Nrf2/HO-1 Pathway in Ovarian Cancer Cells
Sun, X., Li, J., Li, Y., Wang, S., & Li, Q. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/3145182 · Cited by 42 · see citing works
“In the control group, A2780 was round, SKOV-3 was epithelial-like, and CAOV-3 was spindle-shaped, in line with previous descriptions of these three OC cell lines [18].”
Result
CELLector: Genomics-Guided Selection of Cancer In Vitro Models
Najgebauer, H., Yang, M., Francies, H. E., Pacini, C., Stronach, E. A., Garnett, M. J., Sáez-Rodríguez, J., & Iorio, F. (2020) · Cell Systems · doi:10.1016/j.cels.2020.04.007 · Cited by 43 · see citing works
Extracellular matrix in high-grade serous ovarian cancer: Advances in understanding of carcinogenesis and cancer biology
Brown, Y., Hua, S., & Tanwar, P. S. (2023) · Matrix Biology · doi:10.1016/j.matbio.2023.02.004 · Cited by 43 · see citing works
Dual Targeting of Epithelial Ovarian Cancer Via Folate Receptor α and the Proton-Coupled Folate Transporter with 6-Substituted Pyrrolo[2,3- d ]pyrimidine Antifolates
Hou, Z., Gattoc, L., O’Connor, C. E., Yang, S., Wallace-Povirk, A., George, C., Orr, S., Polin, L., White, K., Kushner, J., et al. (2017) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-16-0444 · Cited by 42 · see citing works
“The subtypes of the EOC cell lines are as follows: IGROV1, mixed; TOV112D, endometrioid; SKOV3, serous; and A2780, nonspecified (29).”
Background
Withaferin A ameliorates ovarian cancer-induced cachexia and proinflammatory signaling
Straughn, A. R., & Kakar, S. S. (2019) · Journal of Ovarian Research · doi:10.1186/s13048-019-0586-1 · Cited by 42 · see citing works
“A limitation of the study was the cell line of choice used, as recent works have demonstrated that the A2780 cell line is more genetically similar to the relatively rarer endometroid ovarian cancers [50, 51] than high-grade serous ovarian cancer, which accounts for 70% of ovarian carcinomas [52].”
Preclinical models of epithelial ovarian cancer: practical considerations and challenges for a meaningful application
Ciucci, A., Buttarelli, M., Fagotti, A., Scambia, G., & Gallo, D. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04395-y · Cited by 43 · see citing works
“Beaufort and colleagues [10], through a comprehensive profiling of 39 commercially available cell lines, assigned half of them (20) as non-serous type, 14 as high-grade serous, and five as serous-type/low-grade serous.”
Background
Genomic characterization of five commonly used endometrial cancer cell lines
Devor, E. J., Bosquet, J. G., Thiel, K. W., & Leslie, K. K. (2020) · International Journal of Oncology · doi:10.3892/ijo.2020.5139 · Cited by 41 · see citing works
“Since their original establishment, Ishikawa cells have been used as a model for type I endometrial cancer (11) in labs around the world and have appeared in >500 publications based on a PubMed (pubmed.”
Background
Norepinephrine-Induced DNA Damage in Ovarian Cancer Cells
Lamboy-Caraballo, R., Ortíz, C., Acevedo‐Santiago, A., Matta, J. L., Monteiro, Á. N. A., & Armaiz-Peña, G. N. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21062250 · Cited by 41 · see citing works
“Thus, the cytotoxic effect of cisplatin may vary between cell type due to their different genomic background [35] and their ability to respond to cisplatin-induced DNA adducts.”
Background
Super-Enhancer Redistribution as a Mechanism of Broad Gene Dysregulation in Repeatedly Drug-Treated Cancer Cells
Ma, Q., Yang, F., Mackintosh, C., Jayani, R. S., Oh, S., Jin, C., Nair, S. J., Merkurjev, D., Ma, W., Allen, S., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2020.107532 · Cited by 37 · see citing works
The Histone Methyltransferase DOT1L Is a Functional Component of Estrogen Receptor Alpha Signaling in Ovarian Cancer Cells
Salvati, A., Gigantino, V., Nassa, G., Giurato, G., Alexandrova, E., Rizzo, F. M., Tarallo, R., & Weisz, A. (2019) · Cancers · doi:10.3390/cancers11111720 · Cited by 38 · see citing works
“All cell lines were isolated from peritoneal ascites of serous ovarian adenocarcinomas and carry TP53 mutations [43].”
Background
The PI3K/mTOR dual inhibitor GSK458 potently impedes ovarian cancer tumorigenesis and metastasis
Xiao, Y., Yu, Y., Jiang, P., Li, Y., Wang, C., & Zhang, R. (2020) · Cellular Oncology · doi:10.1007/s13402-020-00514-8 · Cited by 39 · see citing works
“Additionally, several widely used epithelial ovarian cancer cells of unclear subtype (A2780, A2780CP, SKOV3, SKOV3TR and SKOV3IP) or with a mixed subtypes (IGROV-1 and HO8910PM), were included [37, 38].”
Background
KLF7: a new candidate biomarker and therapeutic target for high-grade serous ovarian cancer
Donato, M. D., Babini, G., Mozzetti, S., Buttarelli, M., Ciucci, A., Arduini, G., Rosa, M. C. D., Scambia, G., & Gallo, D. (2020) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-020-01775-9 · Cited by 39 · see citing works
Replication catastrophe is responsible for intrinsic PAR glycohydrolase inhibitor-sensitivity in patient-derived ovarian cancer models
Coulson‐Gilmer, C., Morgan, R. D., Nelson, L., Barnes, B. M., Tighe, A., Wardenaar, R., Spierings, D. C. J., Schlecht, H., Burghel, G. J., Foijer, F., et al. (2021) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-021-02124-0 · Cited by 39 · see citing works
“Indeed, two of the PARGi-resistant cell lines, COV362 and OVSAHO, have reported BRCA defects [45, 66, 67] and are PARPi-sensitive.”
Background
Mouse models of epithelial ovarian cancer for preclinical studies
Karakashev, S. V., & Zhang, R. (2021) · 动物学研究 · doi:10.24272/j.issn.2095-8137.2020.382 · Cited by 38 · see citing works
“… lines used in earlier EOC xenograft mouse model studies were SKOV3 and A2870, which were later shown to have originated from ovarian surface epithelium and endometrium tissues, and therefore were not representative of HGSOC (Beaufort et al., 2014; Domcke et al., 2013).”
Background
Genome-wide methylation profiling of ovarian cancer patient-derived xenografts treated with the demethylating agent decitabine identifies novel epigenetically regulated genes and pathways
Tomar, T., de Jong, S., Alkema, N. G., Hoekman, R. L., Meersma, G. J., Klip, H. G., van der Zee, A. G., & Wisman, G. B. A. (2016) · Genome Medicine · doi:10.1186/s13073-016-0361-5 · Cited by 38 · see citing works
“Recent genomic analyses have shown that most commonly used HGSOC cell lines, like SKOV3 and A2780, are less representative models of HGSOC [8, 9].”
Cu( ii ) phenanthroline–phenazine complexes dysregulate mitochondrial function and stimulate apoptosis
Rochford, G., Molphy, Z. E., Kavanagh, K. A., McCann, M., Devereux, M. M., Kellett, A., & Howe, O. L. (2019) · Metallomics · doi:10.1039/c9mt00187e · Cited by 38 · see citing works
Chemotherapy exacerbates ovarian cancer cell migration and cancer stem cell-like characteristics through GLI1
Zhao, Y., He, M., Cui, L., Gao, M., Zhang, M., Yue, F., Shi, T., Yang, X., Pan, Y., Zheng, X., et al. (2020) · British Journal of Cancer · doi:10.1038/s41416-020-0825-7 · Cited by 38 · see citing works
“The putative histological subtype was endometrioid or clear cell.(38) Our results first indicated that all the three cell lines showed similar response to the first- or secondline chemotherapy treatments: the increase in CSC-like characteristics and migration.”
Result
Clinical Value of lncRNA MEG3 in High-Grade Serous Ovarian Cancer
Buttarelli, M., Donato, M. D., Raspaglio, G., Babini, G., Ciucci, A., Martinelli, E., Baccaro, P., Pasciuto, T., Fagotti, A., Scambia, G., et al. (2020) · Cancers · doi:10.3390/cancers12040966 · Cited by 38 · see citing works
Heterogeneity and Clonal Evolution of Acquired PARP Inhibitor Resistance in TP53- and BRCA1 -Deficient Cells
Färkkilä, A., Rodríguez, A., Oikkonen, J., Gulhan, D., Nguyen, H. Q., Domínguez, J., Ramos, S., Mills, C. E., Pérez‐Villatoro, F., Lazaro, J., et al. (2021) · Cancer Research · doi:10.1158/0008-5472.can-20-2912 · Cited by 36 · see citing works
“Previous studies on PARPi resistance have been performed in commercially available BRCA1-deficient cell lines derived from drug-resistant tumors (20, 21) and have focused on single mechanism of resistance (13, 14).”
Background
CRISPR/Cas9, a new approach to successful knockdown of ABCB1/P-glycoprotein and reversal of chemosensitivity in human epithelial ovarian cancer cell line.
Norouzi‐Barough, L., Sarookhani, M. R., Salehi, R., Sharifi, M., & Moghbelinejad, S. (2018) · Europe PMC (PubMed Central) · doi:10.22038/ijbms.2017.25145.6230 · Cited by 38 · see citing works
The mannose receptor LY75 (DEC205/CD205) modulates cellular phenotype and metastatic potential of ovarian cancer cells
Faddaoui, A., Bachvarova, M., Plante, M., Gregoire, J., Renaud, M., Sebastianelli, A., Gobeil, S., Morin, C., Macdonald, E. A., Vanderhyden, B. C., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.7288 · Cited by 37 · see citing works
“SKOV3 represents a serous EOC cell line displaying mesenchymal (spindle-like) phenotype, including no evidence of cell-cell adhesion [24].”
Mutant p53 gain of function induces HER2 over-expression in cancer cells
Román-Rosales, A., Garcı́a-Villa, E., Herrera, L. A., Gariglio, P., & Díaz‐Chávez, J. (2018) · BMC Cancer · doi:10.1186/s12885-018-4613-1 · Cited by 37 · see citing works
Three-Dimensional Biofabrication Models of Endometriosis and the Endometriotic Microenvironment
Wendel, J. R. H., Wang, X., Smith, L. J., & Hawkins, S. M. (2020) · Biomedicines · doi:10.3390/biomedicines8110525 · Cited by 35 · see citing works
“The HEYA8 cell line formed tight, dense spheroids [26] and has been well characterized molecularly as non-high-grade serous [73,74].”
Background
PARP1 blockade is synthetically lethal in XRCC1 deficient sporadic epithelial ovarian cancers
Ali, R., Alabdullah, M., Alblihy, A., Miligy, I. M., Mesquita, K. A., Chan, S. Y. T., Moseley, P. M., Rakha, E. A., & Madhusudan, S. (2019) · Cancer Letters · doi:10.1016/j.canlet.2019.10.035 · Cited by 36 · see citing works
Molecular disruption of DNA polymerase β for platinum sensitisation and synthetic lethality in epithelial ovarian cancers
Ali, R., Alblihy, A., Miligy, I. M., Alabdullah, M. L., Alsaleem, M. A., Toss, M. S., Algethami, M., Abdel-Fatah, T. M. A., Moseley, P. M., Chan, S. Y. T., et al. (2021) · Oncogene · doi:10.1038/s41388-021-01710-y · Cited by 36 · see citing works
Resveratrol Contrasts IL-6 Pro-Growth Effects and Promotes Autophagy-Mediated Cancer Cell Dormancy in 3D Ovarian Cancer: Role of miR-1305 and of Its Target ARH-I
Esposito, A., Ferraresi, A., Salwa, A., Vidoni, C., Dhanasekaran, D. N., & Isidoro, C. (2022) · Cancers · doi:10.3390/cancers14092142 · Cited by 37 · see citing works
Ovarian Cancer: Treatment and Resistance to Pharmacotherapy
Lukanović, D., Kobal, B., & Černe, K. (2022) · Reproductive Medicine · doi:10.3390/reprodmed3020011 · Cited by 35 · see citing works
“This way, they formed the basis for selecting the models of various histological and molecular ovarian cancer types [71].”
Background
The novel ZIP4 regulation and its role in ovarian cancer
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BackgroundInfluential

Modeling the Diversity of Epithelial Ovarian Cancer through Ten Novel Well Characterized Cell Lines Covering Multiple Subtypes of the Disease
Sauriol, S. A., Simeone, K., Portelance, L., Meunier, L., Leclerc-Desaulniers, K., de Ladurantaye, M., Chergui, M., Kendall‐Dupont, J., Rahimi, K., Carmona, E., et al. (2020) · Cancers · doi:10.3390/cancers12082222 · Cited by 15 · see citing works
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Investigating the suitability of in vitro cell lines as models for the major subtypes of epithelial ovarian cancer
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Abstract 4238: Unique ovarian cancer cell line panel: Molecular subtypes and therapy response
Beaufort, C. M., Helmijr, J., Ruigrok-Ritstier, K., Smid, M., Heine, A. A. J., Jansen, M. P. H. M., Berns, E. M. J. J., & Helleman, J. (2012) · Cancer Research · doi:10.1158/1538-7445.am2012-4238
Abstract B43: Characterization of ovarian cancer cells as in vivo models for preclinical studies.
Hernandez, L. F., Kim, M. K., Lyle, L. T., Steeg, P. S., & Annunziata, C. M. (2016) · Clinical Cancer Research · doi:10.1158/1557-3265.ovca15-b43

Authors: Beaufort, C. M., Helmijr, J. C. A., Piskorz, A. M., Hoogstraat, M., Ruigrok-Ritstier, K., Besselink, N., Murtaza, M., van IJcken, W. F. J., Heine, A. A. J., Smid, M., Koudijs, M. J., Brenton, J. D., Berns, E. M. J. J., & Helleman, J.
Affiliations: Erasmus MC Cancer Institute (NL)
University of Cambridge (GB)
University Medical Center Utrecht (NL)
Corresponding author: Berns, Els M. J. J.
ORCID: Helmijr, Jean C. A.
Piskorz, Anna M.
Hoogstraat, Marlous
Besselink, Nicolle
Murtaza, Muhammed
Smid, Marcel
Brenton, James D.
Helleman, Jozien
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2014-09-17
Volume: 9
Issue: 9
Pages: e103988
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0103988
PMC: PMC4167545
OpenAlex: W2015030879
Cited by: 403
References: 89
Citations by year: 2026: 15 · 2025: 24 · 2024: 30 · 2023: 48 · 2022: 38 · 2021: 54 · 2020: 52 · 2019: 41 · 2018: 27 · 2017: 28 · 2016: 25 · 2015: 21
FWCI: 29.95
Type: journal article
Language: en
Update notices: correction (2015-03-23)
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS ONE (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
EUR Research Repository (Erasmus University Rotterdam) (publishedVersion, other-oa)
EUR Research Repository (Erasmus University Rotterdam) (submittedVersion, other-oa)
RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Figshare (submittedVersion, cc-by)
RePub (Erasmus University Rotterdam) (submittedVersion)
Funders: Cancer Research UK (15601)
Universitair Medisch Centrum Utrecht
Topics: Health Sciences › Medicine › Reproductive Medicine › Ovarian cancer diagnosis and treatment
Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
Keywords: epithelial ovarian cancer, ovarian cancer cell lines, morphological subtypes, high-grade serous carcinoma, low-grade serous carcinoma, tumor heterogeneity, metastasis, prognosis, drug response, preclinical models
MeSH terms: Carcinoma, Ovarian Epithelial, Female, Humans, Neoplasms, Glandular and Epithelial, Ovarian Neoplasms, Gene Expression Regulation, Neoplastic, MicroRNAs

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Ovarian Cancer Cell Line Panel (OCCP): Clinical Importance of In Vitro Morphological Subtypes

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