A New Spontaneously Transformed Syngeneic Model of High-Grade Serous Ovarian Cancer with a Tumor-Initiating Cell Population
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Improving screening and treatment options for patients with epithelial ovarian cancer has been a major challenge in cancer research. Development of novel diagnostic and therapeutic approaches, particularly for the most common subtype, high-grade serous ovarian cancer (HGSC), has been hampered by controversies over the origin of the disease and a lack of spontaneous HGSC models to resolve this controversy. Over long-term culture in our laboratory, an ovarian surface epithelial (OSE) cell line spontaneously transformed OSE (STOSE). The objective of this study was to determine if the STOSE cell line is a good model of HGSC. STOSE cells grow faster than early passage parental M0505 cells with a doubling time of 13 and 48 h, respectively. STOSE cells form colonies in soft agar, an activity for which M0505 cells have negligible capacity. Microarray analysis identified 1755 down-regulated genes and 1203 up-regulated genes in STOSE compared to M0505 cells, many associated with aberrant Wnt/β-catenin and Nf-κB signaling. Upregulation of Ccnd1 and loss of Cdkn2a in STOSE tumors is consistent with changes identified in human ovarian cancers by The Cancer Genome Atlas. Intraperitoneal injection of STOSE cells into severe combined immunodeficient and syngeneic FVB/N mice produced cytokeratin+, WT1+, inhibin-, and PAX8+ tumors, a histotype resembling human HGSC. Based on evidence that a SCA1+ stem cell-like population exists in M0505 cells, we examined a subpopulation of SCA1+ cells that is present in STOSE cells. Compared to SCA1- cells, SCA1+ STOSE cells have increased colony-forming capacity and form palpable tumors 8 days faster after intrabursal injection into FVB/N mice. This study has identified the STOSE cells as the first spontaneous murine model of HGSC and provides evidence for the OSE as a possible origin of HGSC. Furthermore, this model provides a novel opportunity to study how normal stem-like OSE cells may transform into tumor-initiating cells.
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Injection with M0505 cells resulted in Pax8+ tumors with similar histology to human high-grade serous ovarian cancer.
“Injection with M0505 cells (derived from spontaneously transformed OSE of FVB/N mice) resulted in Pax8+ tumors with similar histology to human HGSOC (McCloskey 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 McCloskey et al., 2014
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Cites
Hallmarks of Cancer: The Next Generation
Hanahan, D., & Weinberg, R. A. (2011) · Cell · doi:10.1016/j.cell.2011.02.013 · Cited by 66,590 · see citing works
Cancer Incidence in Five Continents
Doll, R., Muir, C. S., & Waterhouse, J. A. H. (1970) · Springer eBooks · doi:10.1007/978-3-642-85851-2 · Cited by 8,485 · see citing works
Integrated genomic analyses of ovarian carcinoma
Perou, C. M. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/hvp3-wg08 · Cited by 7,927 · see citing works
Cancer Incidence in Five Continents
(1966) · doi:10.1007/978-3-642-85849-9 · Cited by 5,936 · see citing works
A candidate precursor to serous carcinoma that originates in the distal fallopian tube
Lee, Y., Miron, A., Drapkin, R., Nucci, M. R., Medeiros, F., Saleemuddin, A., Garber, J. E., Birch, C., Mou, H., Gordon, R., et al. (2006) · The Journal of Pathology · doi:10.1002/path.2091 · Cited by 897 · see citing works
Piek, J. M. J., van Diest, P. J., Zweemer, R. P., Jansen, J. W., Poort-Keesom, R. J. J., Menko, F. H., Gille, J. J. P., Jongsma, A. P. M., Pals, G., Kenemans, P., et al. (2001) · The Journal of Pathology · doi:10.1002/path.1000 · Cited by 785 · see citing works
Bray, F., Ferlay, J., Laversanne, M., Brewster, D., Mbalawa, C. G., Kohler, B., Piñeros, M., Steliarova‐Foucher, E., Swaminathan, R., Antoni, S., et al. (2015) · International Journal of Cancer · doi:10.1002/ijc.29670 · Cited by 645 · see citing works
Development of a Syngeneic Mouse Model for Events Related to Ovarian Cancer
Roby, K. F., Taylor, C. C., Sweetwood, J. P., Cheng, Y., Pace, J. L., Tawfik, O., Persons, D. L., Smith, P. G., & Terranova, P. F. (2000) · Carcinogenesis · doi:10.1093/carcin/21.4.585 · Cited by 593 · see citing works
Species- and cell type-specific requirements for cellular transformation
Rangarajan, A., Hong, S. J., Gifford, A., & Weinberg, R. A. (2004) · Cancer Cell · doi:10.1016/j.ccr.2004.07.009 · Cited by 555 · see citing works
Distinct requirements for Ras oncogenesis in human versus mouse cellsPreprint
Hamad, N. M., Elconin, J. H., Karnoub, A. E., Bai, W., Rich, J. N., Abraham, R. T., Der, C. J., & Counter, C. M. (2002) · Genes & Development · doi:10.17615/zkd7-3774 · Cited by 430 · see citing works
Induction of ovarian cancer by defined multiple genetic changes in a mouse model system
Oršulić, S., Li, Y., Soslow, R. A., Vitale-Cross, L. A., Gutkind, J. S., & VARMUS, H. E. (2002) · Cancer Cell · doi:10.1016/s1535-6108(01)00002-2 · Cited by 358 · see citing works
Ovarian surface epithelium at the junction area contains a cancer-prone stem cell niche
Flesken‐Nikitin, A., Hwang, C., Cheng, C.-Y., Michurina, T. V., Enikolopov, G., & Nikitin, A. Y. (2013) · Nature · doi:10.1038/nature11979 · Cited by 345 · see citing works
GWAS meta-analysis and replication identifies three new susceptibility loci for ovarian cancer
Study, A. C., Pharoah, P. D. P., Australian Ovarian Cancer Study Group, Tsai, Y.-Y., Ramus, S. J., Phelan, C. M., Goode, E. L., Lawrenson, K., Buckley, M. A., Fridley, B. L., et al. (2013) · Nature Genetics · doi:10.1038/ng.2564 · Cited by 341 · see citing works
A genome-wide association study identifies susceptibility loci for ovarian cancer at 2q31 and 8q24
Goode, E. L., Cancer), T. A. C. S. (., The Australian Ovarian Cancer Study Group, Chenevix‐Trench, G., Song, H., Ramus, S. J., Notaridou, M., Lawrenson, K., Widschwendter, M., Vierkant, R. A., et al. (2010) · Nature Genetics · doi:10.1038/ng.668 · Cited by 338 · see citing works
Shaw, T. J., Senterman, M. K., Dawson, K. M., Crane, C. A., & Vanderhyden, B. C. (2004) · Molecular Therapy · doi:10.1016/j.ymthe.2004.08.013 · Cited by 278 · see citing works
Self-citationSerous Carcinogenesis in the Fallopian Tube
Jarboe, E. A., Folkins, A. K., Nucci, M. R., Kindelberger, D. W., Drapkin, R., Miron, A., Lee, Y., & Crum, C. P. (2008) · International Journal of Gynecological Pathology · doi:10.1097/pgp.0b013e31814b191f · Cited by 273 · see citing works
Histologic Subtypes of Ovarian Carcinoma
Soslow, R. A. (2008) · International Journal of Gynecological Pathology · doi:10.1097/pgp.0b013e31815ea812 · Cited by 258 · see citing works
CpG Island Methylation of DNA Damage Response Genes in Advanced Ovarian Cancer
Teodoridis, J. M., Hall, J. A., Marsh, S., Kannall, H. D., Smyth, C., Curto, J., Siddiqui, N. A., Gabra, H., McLeod, H. L., Strathdee, G. R., et al. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-1187 · Cited by 256 · see citing works
Epithelial ovarian cancer experimental models
Lengyel, E. R., Burdette, J. E., Kenny, H. A., Matei, D. E., Pilrose, J. M., Haluska, P., Nephew, K. P., Hales, D. B., & Stack, M. S. (2013) · Oncogene · doi:10.1038/onc.2013.321 · Cited by 209 · see citing works
Histopathology of Ovarian Tumors in Laying Hens
Barua, A., Bitterman, P., Abramowicz, J. S., Dirks, A. L., Bahr, J. M., Hales, D. B., Bradaric, M. J., Edassery, S. L., Rotmensch, J., & Luborsky, J. L. (2009) · International Journal of Gynecological Cancer · doi:10.1111/igc.0b013e3181a41613 · Cited by 152 · see citing works
Ovarian cancer stem cells: Working towards the root of stemness
Foster, R., Buckanovich, R. J., & Rueda, B. R. (2012) · Cancer Letters · doi:10.1016/j.canlet.2012.10.023 · Cited by 148 · see citing works
Changes in gene expression during progression of ovarian carcinoma
Tapper, J., Kettunen, E., El-Rifai, W. M., Seppälä, M. T., Andersson, L. C., & Knuutila, S. (2001) · Cancer Genetics and Cytogenetics · doi:10.1016/s0165-4608(01)00386-7 · Cited by 141 · see citing works
The Retinoic Acid Synthesis Gene ALDH1a2 Is a Candidate Tumor Suppressor in Prostate Cancer
Kim, H., Lapointe, J., Kaygusuz, G., Ong, D. E., Li, C., van de Rijn, M., Brooks, J. D., & Pollack, J. R. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-4562 · Cited by 139 · see citing works
Integrated genomic analyses of ovarian carcinoma
The Cancer Genome Atlas Research Network (2011) · Nature · doi:10.1038/nature10166 · Cited by 129 · see citing works
A Mouse Model for the Molecular Characterization of Brca1-Associated Ovarian Carcinoma
Xing, D., & Oršulić, S. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-1495 · Cited by 127 · see citing works
Auersperg, N. (2013) · Gynecologic Oncology · doi:10.1016/j.ygyno.2013.03.021 · Cited by 123 · see citing works
Testa, J. R., Getts, L. A., Salazar, H., Liu, Z., Handel, L. M., Godwin, A. K., & Hamilton, T. C. (1994) · PubMed · Cited by 110 · see citing works
Wang, H., Rosen, D. G., Wang, H., Fuller, G. N., Zhang, W., & Liu, J. (2006) · Modern Pathology · doi:10.1038/modpathol.3800637 · Cited by 101 · see citing works
Greenaway, J., Moorehead, R., Shaw, P., & Petrik, J. (2008) · Gynecologic Oncology · doi:10.1016/j.ygyno.2007.10.035 · Cited by 100 · see citing works
Silencing of the UCHL1 gene in human colorectal and ovarian cancers
Okochi‐Takada, E., Nakazawa, K., Wakabayashi, M., Mori, A., Ichimura, S., Yasugi, T., & Ushijima, T. (2006) · International Journal of Cancer · doi:10.1002/ijc.22025 · Cited by 98 · see citing works
Birch, A. H., Arcand, S. L., Oros, K. K., Rahimi, K., Watters, A. K., Provencher, D. M., Greenwood, C. M. T., Mes‐Masson, A., & Tonin, P. N. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028250 · Cited by 98 · see citing works
Roberts, P. C., Mottillo, E. P., Baxa, A. C., Heng, H. H., Doyon‐Reale, N., Grégoire, L., Lancaster, W. D., Rabah, R. M., & Schmelz, E. M. (2005) · Neoplasia · doi:10.1593/neo.05358 · Cited by 97 · see citing works
Lv, L., Zhang, T., Yi, Q., Huang, Y., Wang, Z., Hou, H., Zhang, H., Zheng, W., Hao, Q., Guo, Z., et al. (2012) · Cell Cycle · doi:10.4161/cc.21196 · Cited by 89 · see citing works
Dai, W., Teodoridis, J. M., Zeller, C., Graham, J., Hersey, J., Flanagan, J. M., Stronach, E. A., Millan, D. W. M., Siddiqui, N. A., Paul, J., et al. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-3021 · Cited by 88 · see citing works
Methylation‐associated silencing of the Wnt antagonist SFRP1 gene in human ovarian cancers
Takada, T., Yagi, Y., Maekita, T., Imura, M., Nakagawa, S., Tsao, S., Miyamoto, K., Yoshino, O., Yasugi, T., Taketani, Y., et al. (2004) · Cancer Science · doi:10.1111/j.1349-7006.2004.tb03255.x · Cited by 87 · see citing works
Cancer stem cells niche: A target for novel cancer therapeutics
Yi, S., Hao, Y., Nan, K., & Fan, T. (2012) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2012.10.004 · Cited by 84 · see citing works
Rose, R., Tocco, Granger, Disaia, Hamilton, Santin, & Hiserodt (1996) · American Journal of Obstetrics and Gynecology · doi:10.1053/ob.1996.v175.a73595 · Cited by 79 · see citing works
Auersperg, N. (2013) · International Journal of Gynecological Pathology · doi:10.1097/pgp.0b013e3182800ad5 · Cited by 77 · see citing works
Autotaxin delays apoptosis induced by carboplatin in ovarian cancer cells
Vidot, S., Witham, J., Agarwal, R., Greenhough, S., Bamrah, H. S., Tigyi, G., Kaye, S. B., & Richardson, A. (2010) · Cellular Signalling · doi:10.1016/j.cellsig.2010.01.017 · Cited by 75 · see citing works
Rho, S. B., Dong, S. M., Kang, S., Seo, S., Yoo, C. W., Lee, D. O., Woo, J. S., & Park, S. (2008) · Carcinogenesis · doi:10.1093/carcin/bgn206 · Cited by 71 · see citing works
Weberpals, J. I., Clark-Knowles, K. V., & Vanderhyden, B. C. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2007.11.3902 · Cited by 69 · see citing works
Self-citationPre-Invasive Ovarian Mucinous Tumors Are Characterized by CDKN2A and RAS Pathway Aberrations
Hunter, S. M., Gorringe, K. L., Christie, M., Rowley, S. M., Bowtell, D. D. L., Chenevix‐Trench, G., & Campbell, I. G. (2012) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-12-1103 · Cited by 68 · see citing works
Methylation of tumor suppressor genes in ovarian cancer
OZDEMIR, F., Altınışık, J., Karateke, A., Çoksüer, H., & Buyru, N. (2012) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2012.715 · Cited by 67 · see citing works
Walker, G. E., Macleod, K., Williams, A. R. W., Cameron, D., Smyth, J. F., & Langdon, S. P. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-2245 · Cited by 66 · see citing works
Notaridou, M., Quaye, L., Dafou, D., Jones, C., Song, H., Høgdall, E. V. S., Kjær, S. K., Christensen, L. L., Høgdall, C. K., Blaakær, J., et al. (2010) · International Journal of Cancer · doi:10.1002/ijc.25554 · Cited by 64 · see citing works
Gamwell, L. F., Collins, O. M., & Vanderhyden, B. C. (2012) · Biology of Reproduction · doi:10.1095/biolreprod.112.100347 · Cited by 61 · see citing works
Self-citationChen, X.-X., Zhang, J., Zhang, Z.-H., Li, H.-X., Cheng, W.-J., & Liu, J.-S. (2013) · Human Pathology · doi:10.1016/j.humpath.2013.05.001 · Cited by 58 · see citing works
Cancer stem cells: A stride towards cancer cure?
Sengupta, A., & Cancelas, J. A. (2010) · Journal of Cellular Physiology · doi:10.1002/jcp.22213 · Cited by 56 · see citing works
Zhao, G., Chen, J., Deng, Y., Gao, F., Zhu, J., Feng, Z., Lv, X.-H., & Zhao, Z. (2011) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2011.03.140 · Cited by 51 · see citing works
Stammer, K., Edassery, S. L., Barua, A., Bitterman, P., Bahr, J. M., Hales, D. B., & Luborsky, J. L. (2008) · Gynecologic Oncology · doi:10.1016/j.ygyno.2007.12.030 · Cited by 48 · see citing works
Urzúa, U., Roby, K. F., Gangi, L., Cherry, J. M., Powell, J. I., & Munroe, D. J. (2005) · Journal of Cellular Physiology · doi:10.1002/jcp.20522 · Cited by 46 · see citing works
Jones, P., & Drapkin, R. (2013) · Frontiers in Oncology · doi:10.3389/fonc.2013.00217 · Cited by 46 · see citing works
Scurr, L. L., Guminski, A. D., Chiew, Y.-E., Balleine, R. L., Sharma, R. N., Lei, Y., Pryor, K., Wain, G., Brand, A. H., Byth, K., et al. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-5189 · Cited by 44 · see citing works
Cyclin D1 predicts the prognosis of advanced serous ovarian cancer
Hashimoto, T., Yanaihara, N., Okamoto, A., Nikaido, T., Saito, M., Takakura, S., YASUDA, M., Sasaki, H., Ochiai, K., & Tanaka, T. (2011) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2011.194 · Cited by 43 · see citing works
Touma, S. E., Perner, S., Rubin, M. A., Nanus, D. M., & Gudas, L. J. (2009) · Biochemical Pharmacology · doi:10.1016/j.bcp.2009.06.022 · Cited by 40 · see citing works
Revisiting ovarian cancer preclinical models: Implications for a better management of the disease
Ricci, F., Broggini, M., & Damia, G. L. M. (2013) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2013.01.005 · Cited by 35 · see citing works
Haraldson, K., Kashuba, V. I., Dmitriev, A. A., Senchenko, V. N., Kudryavtseva, A. V., Pavlova, T. V., Александровна, Б. Э., Валерьевна, П. И., Kondratov, O., Rynditch, A. V., et al. (2012) · Biochimie · doi:10.1016/j.biochi.2012.01.019 · Cited by 29 · see citing works
Technical challenges and limitations of current mouse models of ovarian cancer
Garson, K., Gamwell, L. F., Pitre, E. M., & Vanderhyden, B. C. (2012) · Journal of Ovarian Research · doi:10.1186/1757-2215-5-39 · Cited by 28 · see citing works
Self-citationDeng, B., Zhang, S., Miao, Y., Han, Z., Zhang, X., Wen, F., & Zhang, Y. (2012) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/1756-9966-31-19 · Cited by 27 · see citing works
Kulkarni-Datar, K. S., Oršulić, S., Foster, R., & Rueda, B. R. (2013) · Cancer Letters · doi:10.1016/j.canlet.2013.06.014 · Cited by 24 · see citing works
Epiregulin as a marker for the initial steps of ovarian cancer development
Amsterdam, A. (2011) · International Journal of Oncology · doi:10.3892/ijo.2011.1123 · Cited by 21 · see citing works
Quinn, M. C. J., Filali-Mouhim, A., Provencher, D. M., Mes‐Masson, A., & Tonin, P. N. (2009) · Molecular Carcinogenesis · doi:10.1002/mc.20511 · Cited by 19 · see citing works
Thrombomodulin mediates the progression of epithelial ovarian cancer cells
Chen, L. M., Wang, W., Lee, J. C., Chiu, F.-H., Wu, C. T., Tai, C.-J., Wang, C., Tai, C. J., Huang, M. T., & Chang, Y. (2013) · Tumor Biology · doi:10.1007/s13277-013-0958-x · Cited by 15 · see citing works
Serum Autotaxin is not a Useful Biomarker for Ovarian Cancer
Nakamura, K., Igarashi, K., Ohkawa, R., Yokota, H., Masuda, A., Nakagawa, S., Yano, T., Ikeda, H., Aoki, J., & Yatomi, Y. (2012) · Lipids · doi:10.1007/s11745-012-3691-0 · Cited by 15 · see citing works
Padilla‐Nash, H. M., McNeil, N. E., Yi, M., Nguyen, Q. T., Hu, Y., Wangsa, D., Mack, D. L., Hummon, A. B., Case, C., Cardin, É., et al. (2013) · Carcinogenesis · doi:10.1093/carcin/bgt138 · Cited by 13 · see citing works
Locke, J. A., Zafarana, G., Malloff, C. A., Lam, W. L., Sykes, J. R., Pintilie, M., Ramnarine, V. R., Meng, A. X., Ahmed, O., Jurišica, I., et al. (2011) · The Prostate · doi:10.1002/pros.22478 · Cited by 12 · see citing works
Urzúa, U., Best, L., & Munroe, D. J. (2010) · Molecular BioSystems · doi:10.1039/c005220e · Cited by 8 · see citing works
A new mechanism of release from senescence: suppression of p16INK4a by beta‐catenin
Curley, D. P., & Bosenberg, M. W. (2008) · Pigment Cell & Melanoma Research · doi:10.1111/j.1755-148x.2007.00434.x · Cited by 5 · see citing works
Epithelial Ovarian Cancer Experimental Models
Lengyel, E. R., Burdette, J., Kenny, H., Matei, D. E., Pilrose, J. M., Haluska, P., Nephew, K. P., & Hales, D. (2014) · PMC · Cited by 2 · see citing works
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Exosomes Increase the Therapeutic Index of Doxorubicin in Breast and Ovarian Cancer Mouse Models
Hadla, M., Palazzolo, S., Corona, G., Caligiuri, I., Canzonieri, V., Toffoli, G., & Rizzolio, F. (2016) · Nanomedicine · doi:10.2217/nnm-2016-0154 · Cited by 285 · see citing works
Wan, C., Keany, M. P., Dong, H., Al-Alem, L., Pandya, U. M., Lazo, S., Boehnke, K., Lynch, K. N., Xu, R., Zarrella, D. T., et al. (2020) · Cancer Research · doi:10.1158/0008-5472.can-20-1674 · Cited by 197 · see citing works
Castagnoli, L., Cancila, V., Cordoba-Romero, S. L., Faraci, S., Talarico, G., Belmonte, B., Iorio, M. V., Milani, M., Volpari, T., Chiodoni, C., et al. (2019) · Oncogene · doi:10.1038/s41388-019-0700-2 · Cited by 184 · see citing works
Lõhmussaar, K., Kopper, O., Korving, J., Begthel, H., Vreuls, C. P. H., van Es, J. H., & Clevers, H. C. (2020) · Nature Communications · doi:10.1038/s41467-020-16432-0 · Cited by 122 · see citing works
Hodgkinson, K. M., Forrest, L. A., Vuong, N., Garson, K., Djordjevic, B., & Vanderhyden, B. C. (2018) · Oncogene · doi:10.1038/s41388-018-0377-y · Cited by 87 · see citing works
Self-citationBarger, C. J., Zhang, W., Hillman, J. C., Stablewski, A. B., Higgins, M. J., Vanderhyden, B. C., Odunsi, K. O., & Karpf, A. R. (2015) · Oncotarget · doi:10.18632/oncotarget.4546 · Cited by 80 · see citing works
Self-citationEpithelial ovarian cancer stem cells: underlying complexity of a simple paradigm
Garson, K., & Vanderhyden, B. C. (2014) · Reproduction · doi:10.1530/rep-14-0234 · Cited by 73 · see citing works
Self-citationAutomated classification of multiphoton microscopy images of ovarian tissue using deep learning
Huttunen, M. J., Hassan, A., McCloskey, C. W., Fasih, S., Upham, J., Vanderhyden, B. C., Boyd, R. W., & Murugkar, S. (2018) · Journal of Biomedical Optics · doi:10.1117/1.jbo.23.6.066002 · Cited by 69 · see citing works
Self-citationYee, 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
Ovarian Cancer Immunotherapy: Preclinical Models and Emerging Therapeutics
McCloskey, C. W., Rodriguez, G. M., Galpin, K. J. C., & Vanderhyden, B. C. (2018) · Cancers · doi:10.3390/cancers10080244 · Cited by 61 · see citing works
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To, S. K. Y., Mak, A. S. C., Fung, Y. M. E., Che, C., Ss, L., Deng, W., Ru, B., Zhang, J., & Wong, A. S. T. (2017) · Oncogene · doi:10.1038/onc.2017.185 · Cited by 50 · see citing works
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
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Bobbs, A. S., Cole, J. M., & Dahl, K. D. C. (2015) · Cancer Growth and Metastasis · doi:10.4137/cgm.s21221 · Cited by 48 · see citing works
Spena, C. R., Stefano, L. D., Palazzolo, S., Salis, B., Granchi, C., Minutolo, F., Tuccinardi, T., Fratamico, R., Crotti, S., DaRonco, S., et al. (2018) · Journal of Controlled Release · doi:10.1016/j.jconrel.2018.04.055 · Cited by 48 · see citing works
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Tudrej, P., Kujawa, K. A., Cortez, A. J., & Lisowska, K. M. (2019) · Diagnostics · doi:10.3390/diagnostics9030120 · Cited by 46 · see citing works
Rodgers, L. H., hAinmhire, E. Ó., Young, A. N., & Burdette, J. E. (2016) · Oncotarget · doi:10.18632/oncotarget.9051 · Cited by 44 · see citing works
Thomas, E. D., Meza‐Perez, S., Bevis, K. S., Randall, T. D., Gillespie, G. Y., Langford, C. P., & Alvarez, R. D. (2016) · Journal of Ovarian Research · doi:10.1186/s13048-016-0282-3 · Cited by 43 · see citing works
Alwosaibai, K., Abedini, A., Al-Hujaily, E. M., Tang, Y., Garson, K., Collins, O. M., & Vanderhyden, B. C. (2017) · Oncotarget · doi:10.18632/oncotarget.20173 · Cited by 40 · see citing works
Self-citationKarthikeyan, S., Russo, A., Dean, M., Lantvit, D. D., Endsley, M. P., & Burdette, J. E. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.07.003 · Cited by 40 · see citing works
UnPAXing the Divergent Roles of PAX2 and PAX8 in High-Grade Serous Ovarian Cancer
Hardy, L. R., Salvi, A., & Burdette, J. E. (2018) · Cancers · doi:10.3390/cancers10080262 · Cited by 34 · see citing works
Hardy, L. R., Pergande, M. R., Esparza, K., Heath, K. N., Önyüksel, H., Cologna, S. M., & Burdette, J. E. (2019) · Oncogene · doi:10.1038/s41388-019-0842-2 · Cited by 33 · see citing works
Rodriguez, G. M., Galpin, K. J. C., Cook, D. P., Yakubovich, E., Maranda, V., Macdonald, E. A., Wilson‐Sanchez, J., Thomas, A. L., Burdette, J. E., & Vanderhyden, B. C. (2022) · Cancer Research Communications · doi:10.1158/2767-9764.crc-22-0017 · Cited by 32 · see citing works
Self-citationComparative analysis of syngeneic mouse models of high-grade serous ovarian cancer
Cook, D. P., Galpin, K. J. C., Rodriguez, G. M., Shakfa, N. E., Wilson‐Sanchez, J., Echaibi, M., Pereira, M., Matuszewska, K., Haagsma, J., Murshed, H., et al. (2023) · Communications Biology · doi:10.1038/s42003-023-05529-z · Cited by 31 · see citing works
Self-citationAbedini, A., Sayed, C., Carter, L. E., Boerboom, D., & Vanderhyden, B. C. (2020) · Scientific Reports · doi:10.1038/s41598-020-66559-9 · Cited by 27 · see citing works
Self-citationCrawford, A. J., Forjaz, A., Bons, J., Bhorkar, I., Roy, T., Schell, D., Queiroga, V., Ren, K., Kramer, D., Huang, W., et al. (2024) · Science Advances · doi:10.1126/sciadv.adp6285 · Cited by 26 · see citing works
Divergent Roles of PAX2 in the Etiology and Progression of Ovarian Cancer
Al-Hujaily, E. M., Tang, Y., Yao, D., Carmona, E., Garson, K., & Vanderhyden, B. C. (2015) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-15-0121-t · Cited by 26 · see citing works
Self-citationLuo, Y., Shreeder, B., Jenkins, J. W., Shi, H., Lamichhane, P., Zhou, K., Bahr, D. A., Kurian, S., Jones, K. A., Daum, J. I., et al. (2023) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2023-007661 · Cited by 25 · see citing works
Endsley, M. P., Moyle-Heyrman, G., Karthikeyan, S., Lantvit, D. D., Davis, D. A., Wei, J., & Burdette, J. E. (2015) · Frontiers in Oncology · doi:10.3389/fonc.2015.00154 · Cited by 23 · see citing works
Prognostic values of GMPS, PR, CD40, and p21 in ovarian cancer
Wang, P., Zhang, Z., Ma, Y., Lu, J., Zhao, H., Wang, S., Tan, M. J., & Li, B. (2019) · PeerJ · doi:10.7717/peerj.6301 · Cited by 23 · see citing works
Strategies for Delivery of siRNAs to Ovarian Cancer Cells
Farra, R., Maruna, M., Perrone, F. M., Grassi, M., Benedetti, F. M., Maddaloni, M., Boustani, M. E., Parisi, S., Rizzolio, F., Forte, G., et al. (2019) · Pharmaceutics · doi:10.3390/pharmaceutics11100547 · Cited by 23 · see citing works
Non-Invasive Fluorescent Monitoring of Ovarian Cancer in an Immunocompetent Mouse Model
Wilson, A., Wilson, K., Bilandzic, M., Moffitt, L. R., Makanji, M., Gorrell, M. D., Oehler, M. K., Rainczuk, A., Stephens, A. N., & Plebanski, M. (2018) · Cancers · doi:10.3390/cancers11010032 · Cited by 20 · see citing works
James, N. E., Woodman, M. F., DiSilvestro, P., & Ribeiro, J. R. (2020) · Cancers · doi:10.3390/cancers12082150 · Cited by 19 · see citing works
Galpin, K. J. C., Rodriguez, G. M., Maranda, V., Cook, D. P., Macdonald, E. A., Murshed, H., Zhao, S., McCloskey, C. W., Chruscinski, A., Levy, G. A., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-51217-1 · Cited by 20 · see citing works
Self-citationJi, M., Liu, L., Hou, Y., & Li, B. (2019) · Oncology Reports · doi:10.3892/or.2019.7116 · Cited by 19 · see citing works
Mendoza-Martinez, A. K., Loessner, D., Mata, Á., & Azevedo, H. S. (2021) · Cancers · doi:10.3390/cancers13225745 · Cited by 18 · see citing works
Wang, X., Li, H., & Zheng, P. (2022) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2022/6009107 · Cited by 17 · see citing works
RetractedBorel, S., Prikryl, E. A., Vuong, N., Jonkman, J. E. N., Vanderhyden, B. C., Wilson, B. C., & Murugkar, S. (2015) · Analytical Methods · doi:10.1039/c5ay02462e · Cited by 16 · see citing works
Self-citationSurendran, A., Jamalkhah, M., Poutou, J., Birtch, R., Lawson, C., Dave, J., Crupi, M. J. F., Mayer, J., Taylor, V., Petryk, J., et al. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1099459 · Cited by 15 · see citing works
Self-citationBRMS1L suppresses ovarian cancer metastasis via inhibition of the β-catenin-wnt pathway
Cao, P., Zhao, S., Sun, Z., Jiang, N., Shang, Y., Wang, Y., Gu, J., & Li, S. (2018) · Experimental Cell Research · doi:10.1016/j.yexcr.2018.08.013 · Cited by 15 · see citing works
The Development of Nanoparticles for the Detection and Imaging of Ovarian Cancers
Henderson, E. C., Huynh, G. T., Wilson, K., Plebanski, M., & Corrie, S. R. (2021) · Biomedicines · doi:10.3390/biomedicines9111554 · Cited by 13 · see citing works
PTEN Loss Shapes Macrophage Dynamics in High-Grade Serous Ovarian Carcinoma
Spear, S., Saux, O. L., Mirza, H., Iyer, N., Tyson, K., Grundland-Freile, F., Walton, J. B., Woodman, C. A., Jarvis, S., Ennis, D. P., et al. (2024) · Cancer Research · doi:10.1158/0008-5472.can-23-3890 · Cited by 10 · see citing works
Self-citationVuong, N., Salah, O. S., & Vanderhyden, B. C. (2017) · Scientific Reports · doi:10.1038/s41598-017-16219-2 · Cited by 10 · see citing works
Self-citationRodriguez, G. M., Yakubovich, E., Murshed, H., Maranda, V., Galpin, K. J. C., Cudmore, A. O., Hanna, A. M. R., Macdonald, E. A., Ramesh, S., Garson, K., et al. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1295208 · Cited by 9 · see citing works
Self-citationBarbolina, M. V. (2022) · Cancers · doi:10.3390/cancers14184535 · Cited by 9 · see citing works
Precision-engineered biomimetics: the human fallopian tubePreprint
Crawford, A. J., Forjaz, A., Bhorkar, I., Roy, T., Schell, D., Queiroga, V., Ren, K., Kramer, D., Bons, J., Huang, W., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.06.06.543923 · Cited by 8 · see citing works
Zhu, Y., Abedini, A., Rodriguez, G. M., McCloskey, C. W., Abou‐Hamad, J., Salah, O. S., Larocque, J., Tsoi, M. F., Boerboom, D., Cook, D. P., et al. (2025) · Oncogene · doi:10.1038/s41388-025-03387-z · Cited by 7 · see citing works
Self-citationChang, Y., Chu, T., & Ding, D. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232213843 · Cited by 6 · see citing works
Development and Characterization of a Luciferase Labeled, Syngeneic Murine Model of Ovarian Cancer
Russell, S., Lim, F., Peters, P., Wardell, S. E., Whitaker, R. S., Chang, C., Previs, R. A., & McDonnell, D. P. (2022) · Cancers · doi:10.3390/cancers14174219 · Cited by 5 · see citing works
Transglutaminase 2 regulates ovarian cancer metastasis by modulating the immune microenvironment
Ibrahim, D., Grondin, M., Galpin, K. J. C., Asif, S., Thompson, E., Nersesian, S., Abou‐Hamad, J., Echaibi, M., Rodriguez, G. M., Navals, P., et al. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1639853 · Cited by 3 · see citing works
Self-citationOvarian Cancer Research in the Post Genomic Era — Challenges and Opportunities
Goyeneche, A. A., & Telleria, C. M. (2016) · InTech eBooks · doi:10.5772/60600 · Cited by 3 · see citing works
Wang, W., Alvero, A. B., Qin, Y., Wang, M., Fox, A. L., Li, Y., Millman, M., Kemper, A., Mor, G., Liu, X., et al. (2026) · Molecular Oncology · doi:10.1002/1878-0261.70224 · Cited by 2 · see citing works
Cudmore, A. O., Rodriguez, G. M., Maranda, V., Boroujeni, S. F., Murshed, H., Macdonald, E. A., Grondin, M., Garson, K., Matuszewska, K., Diallo, J., et al. (2025) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-24-0906 · Cited by 2 · see citing works
Self-citationOvarian Cancer and the Environment: Rodent Models
Vanderhyden, B. C., & Dorward, A. M. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.10927-4 · Cited by 2 · see citing works
Self-citationHowell, V. M., & Davidson, B. (2015) · Frontiers in Oncology · doi:10.3389/fonc.2015.00205 · Cited by 2 · see citing works
Ovarian Cancer and the Environment: Rodent Models
Vanderhyden, B. C., & Dorward, A. M. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-95488-4.00099-1 · Cited by 1 · see citing works
Self-citationPotential of IMNN-001 in epithelial ovarian cancer: assessment of clinical findings
Thaker, P. H., Lindborg, S. R., Limon, A. E., Faller, D. V., Bradley, W. H., Anwer, K., & Alvarez, R. D. (2026) · Expert Opinion on Investigational Drugs · doi:10.1080/13543784.2026.2636926 · Cited by 1 · see citing works
BRCA1 expression, proliferative and apoptotic activities in ovarian epithelial inclusions
Wang, Y., Wang, Y., Li, W., Hong, S., Zhao, M., Zhang, X., & Zheng, W. (2017) · Journal of Ovarian Research · doi:10.1186/s13048-017-0307-6 · Cited by 1 · see citing works
Development of Raman Spectroscopy as a Clinical Diagnostic Tool
Borel, S. (2016) · TSpace (University of Toronto)
PAX2 Induces Tubular-Like Structures in Normal and Ovarian Cancer CellsPreprint
Alwosaibai, K., Al-Hujaily, E. M., Alamri, S., Garson, K., & Vanderhyden, B. C. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.01.14.906438
Self-citationModels of ovarian cancer to test new agents
Sodi, V. L., Craig, A. D., Peri, S., & Connolly, D. C. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-819840-7.00012-1
Murazov, Y. G., Стуков, А. Н., Нюганен, А. О., & Artem`eva, A. (2021) · Voprosy Onkologii · doi:10.37469/0507-3758-2021-67-2-300-308
Li, B., Zhang, H., Guo, Y. C., Liu, L., Hou, Y., Wang, P., Jiang, F., Zhang, Z., & Hei, T. K. (2019) · doi:10.21203/rs.2.15828/v2
Spear, S., Saux, O. L., Mirza, H., Tyson, K., Bickel, J. K., Grundland-Freile, F., Siskos, A., Balcells, C. D., Walton, J. B., Woodman, C. A., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.07.18.549474
Models of high-grade serous carcinoma of tubo-ovarian origin
Padmanabhan, A., Dwivedi, S. K. D., Merritt, M. A., Verma, P., Buckanovich, R. J., Lang, J. D., Dimmick, H. L., Nephew, K. P., Drapkin, R., Brubaker, L. W., et al. (2026) · Oncology Reviews · doi:10.3389/or.2026.1849834
- Authors
- McCloskey, C. W., Goldberg, R. L., Carter, L. E., Gamwell, L. F., Al-Hujaily, E. M., Collins, O., Macdonald, E. A., Garson, K., Daneshmand, M., Carmona, E., & Vanderhyden, B. C.
- Affiliations
- University of Ottawa (CA)
- Corresponding author
- Vanderhyden, Barbara C.
- ORCID
- Venue
- Frontiers in Oncology
- Publisher
- Frontiers Media SA
- Published
- 2014-03-18
- Volume
- 4
- Pages
- 53-53
- ISSN
- 2234-943X (ISSN-L)
- PMC
- PMC3957277
- OpenAlex
- W2108852607
- Cited by
- 67
- References
- 68
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 5 · 2023: 5 · 2022: 6 · 2021: 4 · 2020: 6 · 2019: 10 · 2018: 8 · 2017: 4 · 2016: 6 · 2015: 6 · 2014: 1
- FWCI
- 6.87
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Oncology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Cancer Research Society
- China Scholarship Council
- Health Canada
- Canadian Institutes of Health Research
- Canadian Cancer Society Research Institute
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Ovarian cancer diagnosis and treatment
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › BRCA gene mutations in cancer
- Keywords
- high-grade serous ovarian cancer, spontaneous transformation, ovarian surface epithelial cells, cancer stem cells, spinocerebellar ataxia type 1, syngeneic mouse model, Wnt/β-catenin signaling, NF-κB signaling, CCND1, CDKN2A, tumor origin, epithelial ovarian cancer
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