Cited by 136Ovarian cancer diagnosis and treatmentCancer Immunotherapy and BiomarkersBRCA gene mutations in cancer

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Genetically Defined Syngeneic Mouse Models of Ovarian Cancer as Tools for the Discovery of Combination Immunotherapy

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Iyer, Sonia, Zhang, Shuang, Yucel, Simge, Horn, Heiko, Smith, Sean G., Reinhardt, Ferenc, Hoefsmit, Esmee, Assatova, Bimarzhan, Casado, Julia, Meinsohn, Marie-Charlotte, Barrasa, M. Inmaculada, Bell, George W., Pérez-Villatoro, Fernando, Huhtinen, Kaisa, Hynninen, Johanna, Oikkonen, Jaana, Galhenage, Pamoda M., Pathania, Shailja, Hammond, Paula T., Neel, Benjamin G., Farkkila, Anniina, Pépin, David, Weinberg, Robert A.·2021·Cancer Discovery

DOI 10.1158/2159-8290.cd-20-0818PMC PMC8344888

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Abstract

Abstract Despite advances in immuno-oncology, the relationship between tumor genotypes and response to immunotherapy remains poorly understood, particularly in high-grade serous tubo-ovarian carcinomas (HGSC). We developed a series of mouse models that carry genotypes of human HGSCs and grow in syngeneic immunocompetent hosts to address this gap. We transformed murine-fallopian tube epithelial cells to phenocopy homologous recombination–deficient tumors through a combined loss of Trp53, Brca1, Pten, and Nf1 and overexpression of Myc and Trp53R172H, which was contrasted with an identical model carrying wild-type Brca1. For homologous recombination–proficient tumors, we constructed genotypes combining loss of Trp53 and overexpression of Ccne1, Akt2, and Trp53R172H, and driven by KRASG12V or Brd4 or Smarca4 overexpression. These lines form tumors recapitulating human disease, including genotype-driven responses to treatment, and enabled us to identify follistatin as a driver of resistance to checkpoint inhibitors. These data provide proof of concept that our models can identify new immunotherapy targets in HGSC. Significance: We engineered a panel of murine fallopian tube epithelial cells bearing mutations typical of HGSC and capable of forming tumors in syngeneic immunocompetent hosts. These models recapitulate tumor microenvironments and drug responses characteristic of human disease. In a Ccne1-overexpressing model, immune-checkpoint resistance was driven by follistatin. This article is highlighted in the In This Issue feature, p. 211

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PTEN Deficiency in Tubo-Ovarian High-Grade Serous Carcinoma is Associated with Poor Progression-Free Survival and is Mutually Exclusive with CCNE1 Amplification
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ZNFX1 Functions as a Master Regulator of Epigenetically Induced Pathogen Mimicry and Inflammasome Signaling in Cancer
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Modulation of Type I Interferon Responses to Influence Tumor-Immune Cross Talk in PDAC
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“Mutational heterogeneity is associated with a better response to ICI (Reuben et al., 2017; Iyer et al., 2021; Vitale et al., 2021).”
Background
PPT1 is a negative regulator of STING signaling in cancer cells and its inhibition reactivates immune surveillance in cold tumors
Chowdhury, S. R., Parikh, C. N., Kaur, A. N., DeMarco, K. D., Giwa, H. K., Mishra, A., Murphy, K. C., Zhou, L., Ma, B., Ye, T., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2514948122 · Cited by 13
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“Furthermore, recent syngeneic mouse models may more completely mirror HGSC genomics, immunobiology, and tumour epithelial and TME interactions than PDX HGSC tumours that usually have human malignant cells with a mouse TME 128,134–136 .”
Sustained delivery of PARP inhibitor Talazoparib for the treatment of BRCA-deficient ovarian cancer
Yang, S., Green, A., Virani, N. A., Robinson, A., Senat, M., Testino, B., Dinulescu, D. M., & Sridhar, S. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1175617 · Cited by 12
“Syngeneic Brca1; Tp53; Pten; Nf1; Myc genetically engineered mouse models (BPPNM) were also employed in this study (56).”
Localized In Vivo Prodrug Activation Using Radionuclides
Quintana, J. M., Jiang, F., Kang, M., Onecha, V. V., Könik, A., Qin, L., Rodriguez, V. E., Hu, H., Borges, N., Khurana, I., et al. (2025) · Journal of Nuclear Medicine · doi:10.2967/jnumed.124.268559 · Cited by 11
TRAIL-dependent apoptosis of peritoneal mesothelial cells by NK cells promotes ovarian cancer invasion
Steitz, A. M., Schröder, C., Knuth, I., Keber, C. U., Sommerfeld, L., Finkernagel, F., Jansen, J. M., Wagner, U. A. G., Müller‐Brüsselbach, S., Worzfeld, T., et al. (2023) · iScience · doi:10.1016/j.isci.2023.108401 · Cited by 12
“Genetically engineeredmicerecapitulatingthegenomicsandtheTMEofhumanHGSCareavailable, 65–67 butdue to multiple genetic alterations these mouse models require complex breeding programs.”
Background
Chemotherapy induces myeloid-driven spatial T-cell exhaustion in ovarian cancerPreprint
Launonen, I.-M. P., Erkan, E. P., Niemiec, I., Junquera, A., Hincapié-Otero, M. M., Afenteva, D., Liang, Z., Salko, M., Szabo, A., Pérez‐Villatoro, F., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.03.19.585657 · Cited by 11
Leveraging dysregulated tumor metabolism for targeting anticancer bacteria
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“A and BPPNM, which both are genetically defined and establish intraperitoneal tumors recapitulating high-grade serous OC (HGSOC) ( 39 ); and the murine TNBC cell line 4T1 ( 37 , 38 ).”
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“Studies associated with this have led to discovering novel immunotherapeutic approaches towards cancer [9-11].”
Background
The Emerging Role of the Single-Cell and Spatial Tumor Microenvironment in High-Grade Serous Ovarian CancerPreprint
Launonen, I.-M. P., Vähärautio, A., & Färkkilä, A. (2023) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a041314 · Cited by 10
Development of a Patient-Derived 3D Immuno-Oncology Platform to Potentiate Immunotherapy Responses in Ascites-Derived Circulating Tumor Cells
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The Reign of Follistatin in Tumors and Their Microenvironment: Implications for Drug Resistance
Sosa, J., Oyelakin, A., & Sinha, S. (2024) · Biology · doi:10.3390/biology13020130 · Cited by 9
“…analysis of patient-derived xenografts showed that FST is upregulated in ovarian tumors resistant to combination chemotherapy with immune checkpoint inhibitors, whereas the genetic ablation of FST restored drug susceptibility and improved the overall survival of mice with these tumors [84].”
Background
Cycling molecular assemblies for Golgi imaging and disruption
Tan, W., Zhang, Q., Liu, Z., Qiu, K., Mahajan, D., Gerton, T. J., Copperman, N., Dresselhaus, E. C., Xia, C., Lin, C., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-68768-8 · Cited by 8
Unlocking the potential of immunotherapy in platinum-resistant ovarian cancer: rationale, challenges, and novel strategies
Kefas, J., & Flynn, M. (2024) · Cancer Drug Resistance · doi:10.20517/cdr.2024.67 · Cited by 6
Longitudinal prediction of drug response in high-grade serous ovarian cancer organoid cultures aligning with clinical responses
Cavarzerani, E., Caligiuri, I., Bartoletti, M., Corona, G., Perin, T., Palumbo, A., Ditto, A., Occhiali, T., Canzonieri, V., & Rizzolio, F. (2025) · Journal of Advanced Research · doi:10.1016/j.jare.2025.08.009 · Cited by 6
“This platform enabled the identiﬁcation of an effective combination therapy for the CCNE1-ampliﬁed HGSOC subtype [20].”
An integrated genomic approach identifies follistatin as a target of the p63-epidermal growth factor receptor oncogenic network in head and neck squamous cell carcinoma
Oyelakin, A., Sosa, J., Nayak, K. B., Glathar, A. R., Gluck, C. B., Sethi, I., Tsompana, M., Nowak, N. J., Buck, M. J., Romano, R., et al. (2023) · NAR Cancer · doi:10.1093/narcan/zcad038 · Cited by 6
Profiling extracellular vesicles in circulation enables the early detection of ovarian cancerPreprint
Jo, A., Green, A., Medina, J. E., Iyer, S., Öhman, A., McCarthy, E. T., Reinhardt, F., Gerton, T. J., Demehin, D., Mishra, R. K., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.01.19.524549 · Cited by 5
Combination therapy with Chicoric acid and PD-1/PD-L1 blockade improves the immunotherapy response in patient-derived ovarian cancer xenograft model
Lan, H., Zhu, J., Hou, H., Zhang, C., Huo, X., Zhang, Y., Yang, F., Zhou, N., & Zhang, X. (2025) · Cell Communication and Signaling · doi:10.1186/s12964-025-02146-7 · Cited by 4
“Unfortunately, the preclinical models required to address questions regarding the contributions of specific HGSC-specific characteristics to immune evasion have been limited until now [9].”
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
The effects of dietary fat on gut microbial composition and function in a mouse model of ovarian cancer
AlHilli, M. M., Sangwan, N., Myers, A., Tewari, S., Lindner, D. J., Cresci, G., & Reizes, O. (2025) · Journal of Ovarian Research · doi:10.1186/s13048-025-01731-1 · Cited by 3
ID8 cells manifest phenotypic plasticity and molecular heterogeneity of high-grade serous ovarian cancer in response to the local tissue niche
Gupta, R., Shravan, S., Agwane, S. B., Bankar, R., & Bapat, S. A. (2025) · Scientific Reports · doi:10.1038/s41598-025-18264-8 · Cited by 3
Immunocompetent C57BL/6 syngeneic mouse ovarian cancer models with defined genetic alterations
Agadjanian, H., Karlan, B. Y., Walsh, C., & Oršulić, S. (2025) · Scientific Reports · doi:10.1038/s41598-025-18960-5 · Cited by 3
“This structure allowed for a detailed analysis of how specific genetic alterations contribute to tumor growth and therapeutic responses, all thoroughly described in a single publication 14 .”
Myeloid diversity in tumors: Shaped by genes, location, and time
Nogales-Pons, M., Munárriz-Paños, M., Aceña-Gonzalo, T., & Casanova-Acebes, M. (2026) · The Journal of Experimental Medicine · doi:10.1084/jem.20252267 · Cited by 3
Biomaterial considerations for ovarian cancer models
Kramer, M., Criswell, A., & Sewell-Loftin, M. K. (2023) · Frontiers in Materials · doi:10.3389/fmats.2023.1223276 · Cited by 3
The Identification of a Key Regulator of Mitochondrial Metabolism, the LRPPRC Protein, as a Novel Therapeutic Target in SDHA-Overexpressing Ovarian Tumors
Szulta, A., Wang, L., Hasan, A., Kinter, M. T., Pranay, A., Zhu, J., Humphries, K. M., Loveland, B. L., Griffin, T. M., & Bieniasz, M. (2025) · Cancers · doi:10.3390/cancers17121942 · Cited by 3
“Here, to expand our studies exploring the impact of SDHA overexpression on tumor biology, we obtained innovative ovarian cancer cell lines derived from murine fallopian tube epithelium (mFTE) from Dr. Weinberg [21].”
Assessing Preclinical Research Models for Immunotherapy for Gynecologic Malignancies
Dholakia, J., Scalise, C. B., & Arend, R. C. (2021) · Cancers · doi:10.3390/cancers13071694 · Cited by 3
Proteomics discovery of MTDH and SND1 interaction vulnerabilities in ovarian cancer
Esmaeili, P., Nasimian, A., Werner, L., Mosquim, S., Jakobsson, M. E., Gerdtsson, A. S., Kazi, J. U., & Levander, F. (2025) · Scientific Reports · doi:10.1038/s41598-025-26913-1 · Cited by 2
“The results in both showed Bliss scores > 0, indicating synergy 41”
Chemotherapy induces an IL1β-dependent neutrophil recruitment and activation that promote chemoresistance in metastatic ovarian cancer
Miyamoto, T., Ye, Y., Soliman, M. M. H., Manning, B. S., Murphy, B., Zhu, L., Shao, C., Mirji, G., Minakuchi, M., Hamada, K., et al. (2026) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2025-014253 · Cited by 2
Experimental Modeling and Treatment Strategies for Peritoneal Carcinomatosis
Canda, A. E., & Sever, T. (2024) · Turkish Journal of Colorectal Disease · doi:10.4274/tjcd.galenos.2024.2024-10-5 · Cited by 2
Molecular insights into the unique properties of the blood‐circulating proteasome
Leushkin, Y., Morgenstern, D., Ben‐Dor, S., Haffner‐Krausz, R., Zittlau, K. I., Ben‐Nissan, G., & Sharon, M. (2025) · Journal of Extracellular Biology · doi:10.1002/jex2.70034 · Cited by 2
Specific Genetic Mutations Impact Chemotherapy Resistance and Therapeutic Efficacy of Oncolytic Viruses in Ovarian Cancer
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
FSTL3 is a biomarker of poor prognosis and associated with immunotherapy resistance in ovarian cancer
Chauvin, M. Y., Tromelin, E., Roche-Prellezo, J., Lancia, H. H., Meinsohn, M.-C., Coletti, C. M., Nguyen, N. M., Lafont, V., Michaud, H., Mishra, R. K., et al. (2025) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-025-03425-4 · Cited by 4
“B-FST OE ) rendered it resistant to PPC treatment [16].”
Influential
Immune Subtypes Characterization Identifies Clinical Prognosis, Tumor Microenvironment Infiltration, and Immune Response in Ovarian Cancer
Lu, W., Zhang, F., Zhong, X., Wei, J., Xiao, H., & Tu, R. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.801156 · Cited by 2
“Immuno-oncology regimens, which reverse the immune-suppressive tumor microenvironment, may unleash the immune system against cancer cells (Iyer et al., 2021).”
Background
CD47 predominates over CD24 as a macrophage immune checkpoint in cancerPreprint
Allen, J., Meglan, A., Vaccaro, K., Velarde, J., Chen, V., Ribeiro, J., Blandin, J., Gupta, S., Mishra, R. K., Ho, R., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.25.625185 · Cited by 2
Models of High-Grade Serous Ovarian CarcinomaPreprint
Pundel, O. J., & Neel, B. G. (2025) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a041949 · Cited by 2
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
Development of Mouse-Derived Organoid Lines from Fallopian Tube Epithelial Cells for High Grade Serous Ovarian Carcinoma Modeling
González, E. M. H., Hou, J., & Pundel, O. J. (2025) · Journal of Visualized Experiments · doi:10.3791/68753 · Cited by 2
Tumor Microenvironment of Epithelial Ovarian Cancer
Perkins, R. S., Choi, W.-Y., & Zhang, M. S. J. A. W. (2025) · IntechOpen eBooks · doi:10.5772/intechopen.1013212 · Cited by 3
Insights from three decades of BRCA1/2 modeling in mice
Darnold, J.-S., & Jonkers, J. (2026) · Nature Genetics · doi:10.1038/s41588-025-02448-z · Cited by 1
“Mouse FTSECs harboring specific genetic alterations were then propagated in syngeneic immunocompetent mice to study the unique immune environment of BRCA1 / 2 -associated HGSOC to identify treatment strategies and therapeutic targets 43 .”
Activin A-Targeted Therapy in Cancer: An Updated Review on Challenges and Opportunities in Clinical Translation
Rastegar‐Pouyani, N., Farzin, M. A., Karimi, P., Jafarzadeh, E., Abdolvahab, M. H., & Najafi, M. (2024) · Current Pharmaceutical Design · doi:10.2174/0113816128320120240805104433 · Cited by 1
Drug-induced nuclear cathepsin L (nCTSL) defines a targetable DNA damage response axis and PARP inhibitor sensitivity in ovarian cancer
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BRCA mutational status shapes the stromal microenvironment of pancreatic cancer linking CLU + CAF expression with HSF1 signalingPreprint
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Background
PTEN and BRCA1 tumor suppressor loss associated tumor immune microenvironment exhibits differential response to therapeutic STING pathway activation in a murine model of ovarian cancerPreprint
Shakfa, N. E., Li, D., Conseil, G., Lightbody, E. D., Wilson‐Sanchez, J., Hamade, A., Chenard, S. W., Laight, B. J., Afriyie-Asante, A., Tyryshkin, K., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.27.497846 · Cited by 1

Authors: Iyer, S., Zhang, S., Yucel, S., Horn, H., Smith, S. G., Reinhardt, F., Hoefsmit, E., Assatova, B., Casado, J., Meinsohn, M.-C., Barrasa, M. I., Bell, G. W., Pérez-Villatoro, F., Huhtinen, K., Hynninen, J., Oikkonen, J., Galhenage, P. M., Pathania, S., Hammond, P. T., Neel, B. G., Farkkila, A., Pépin, D., & Weinberg, R. A.
Affiliations: Whitehead Institute for Biomedical Research (US)
NYU Langone Health (US)
Broad Institute (US)
Massachusetts Institute of Technology (US)
1Whitehead Institute for Biomedical Research, Cambridge, Massachusetts.
University of Helsinki (FI)
Harvard University (US)
6Research Program in Systems Oncology, University of Helsinki and Helsinki University Hospital, Helsinki, Finland.
University of Turku (FI)
University of Massachusetts Boston (US)
Corresponding author: Pépin, David
Weinberg, Robert A.
ORCID: Iyer, Sonia
Zhang, Shuang
Horn, Heiko
Smith, Sean G.
Assatova, Bimarzhan
Casado, Julia
Meinsohn, Marie-Charlotte
Barrasa, M. Inmaculada
Bell, George W.
Pérez-Villatoro, Fernando
Huhtinen, Kaisa
Hynninen, Johanna
Oikkonen, Jaana
Galhenage, Pamoda M.
Pathania, Shailja
Hammond, Paula T.
Neel, Benjamin G.
Farkkila, Anniina
Pépin, David
Weinberg, Robert A.
Venue: Cancer Discovery
Publisher: American Association for Cancer Research (AACR)
Published: 2021-02-01
Volume: 11
Issue: 2
Pages: 384-407
ISSN: 2159-8274 (ISSN-L)
2159-8290
DOI: 10.1158/2159-8290.cd-20-0818
PMC: PMC8344888
OpenAlex: W3097756289
Cited by: 136
References: 83
Citations by year: 2026: 20 · 2025: 33 · 2024: 24 · 2023: 21 · 2022: 22 · 2021: 13
FWCI: 12.99
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Cancer Discovery (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
UTUPub (University of Turku) (submittedVersion)
Funders: NIH (R01 CA0784561, P01 CA080111)
Ovarian Cancer Research Program (W81XWH-17-1-0212)
US Army Medical Research (21702-5014)
Topics: Health Sciences › Medicine › Oncology › Ovarian cancer diagnosis and treatment
Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › BRCA gene mutations in cancer
Keywords: high-grade serous ovarian cancer, syngeneic mouse model, genetically engineered mouse models, combination immunotherapy, immunotherapy resistance, immune checkpoint inhibitors, follistatin, homologous recombination deficiency, BRCA1, PTEN, neurofibromatosis type 1, c-Myc, cyclin E1, KRAS G12V, BRD4, SMARCA4, tumor microenvironment, immunotherapy response prediction
MeSH terms: Immune Checkpoint Inhibitors, Animals, Disease Models, Animal, Drug Therapy, Combination, Fallopian Tube Neoplasms, Female, Mice, Transgenic, Ovarian Neoplasms, Cystadenocarcinoma, Serous

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Genetically Defined Syngeneic Mouse Models of Ovarian Cancer as Tools for the Discovery of Combination Immunotherapy

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