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Cited by 67Ovarian cancer diagnosis and treatmentEndometrial and Cervical Cancer TreatmentsOvarian function and disorders

FOXM1 expression is significantly associated with chemotherapy resistance and adverse prognosis in non-serous epithelial ovarian cancer patients

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Tassi, Renata A., Todeschini, Paola, Siegel, Eric R., Calza, Stefano, Cappella, Paolo, Ardighieri, Laura, Cadei, Moris, Bugatti, Mattia +18 more·2017·Journal of Experimental & Clinical Cancer Research
DOI 10.1186/s13046-017-0536-yPMC PMC5422964
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Abstract

BACKGROUND: Epithelial ovarian cancer (EOC) is a spectrum of different diseases, which makes their treatment a challenge. Forkhead box M1 (FOXM1) is an oncogene aberrantly expressed in many solid cancers including serous EOC, but its role in non-serous EOCs remains undefined. We examined FOXM1 expression and its correlation to prognosis across the three major EOC subtypes, and its role in tumorigenesis and chemo-resistance in vitro. METHODS: Gene signatures were generated by microarray for 14 clear-cell and 26 endometrioid EOCs, and 15 normal endometrium snap-frozen biopsies. Validation of FOXM1 expression was performed by RT-qPCR and immunohistochemistry in the same samples and additionally in 50 high-grade serous EOCs and in their most adequate normal controls (10 luminal fallopian tube and 20 ovarian surface epithelial brushings). Correlations of FOXM1 expression to clinic-pathological parameters and patients' prognosis were evaluated by Kaplan-Meier and Cox proportional-hazards analyses. OVCAR-3 and two novel deeply characterized EOC cell lines (EOC-CC1 and OSPC2, with clear-cell and serous subtype, respectively) were employed for in vitro studies. Effects of FOXM1 inhibition by transient siRNA transfection were evaluated on cell-proliferation, cell-cycle, colony formation, invasion, and response to conventional first- and second-line anticancer agents, and to the PARP-inhibitor olaparib. Gene signatures of FOXM1-silenced cell lines were generated by microarray and confirmed by RT-qPCR. RESULTS: A significant FOXM1 mRNA up-regulation was found in EOCs compared to normal controls. FOXM1 protein overexpression significantly correlated to serous histology (p = 0.001) and advanced FIGO stage (p = 0.004). Multivariate analyses confirmed FOXM1 protein overexpression as an independent indicator of worse disease specific survival in non-serous EOCs, and of shorter time to progression in platinum-resistant cases. FOXM1 downregulation in EOC cell lines inhibited cell growth and clonogenicity, and promoted the cytotoxic effects of platinum compounds, doxorubicin hydrochloride and olaparib. Upon FOXM1 knock-down in EOC-CC1 and OSPC2 cells, microarray and RT-qPCR analyses revealed the deregulation of several common and other unique subtype-specific FOXM1 putative targets involved in cell cycle, metastasis, DNA repair and drug response. CONCLUSIONS: FOXM1 is up-regulated in all three major EOCs subtypes, and is a prognostic biomarker and a potential combinatorial therapeutic target in platinum resistant disease, irrespective of tumor histology.

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Authors
Tassi, R. A., Todeschini, P., Siegel, E. R., Calza, S., Cappella, P., Ardighieri, L., Cadei, M., Bugatti, M., Romani, C., Bandiera, E., Zanotti, L., Tassone, L., Guarino, D., Santonocito, C., Capoluongo, E. D., Beltrame, L., Erba, E., Marchini, S., D’Incalci, M., Donzelli, C., Santin, A. D., Pecorelli, S., Sartori, E., Bignotti, E., Odicino, F., & Ravaggi, A.
Affiliations
  • University of Brescia (IT)
  • University of Arkansas for Medical Sciences (US)
  • Nerviano Medical Sciences (IT)
  • Azienda Socio Sanitaria Territoriale degli Spedali Civili di Brescia (IT)
  • Agostino Gemelli University Polyclinic (IT)
  • Mario Negri Institute for Pharmacological Research (IT)
  • Yale University (US)
Corresponding author
Tassi, Renata A.
ORCID
Venue
Journal of Experimental & Clinical Cancer Research
Publisher
Springer Science and Business Media LLC
Published
2017-05-08
Volume
36
Issue
1
Pages
63-63
ISSN
  • 0392-9078 (ISSN-L)
  • 1756-9966
DOI
10.1186/s13046-017-0536-y
PMC
PMC5422964
OpenAlex
W2612361414
Cited by
67
References
3
Citations by year
2026: 3 · 2025: 6 · 2024: 5 · 2023: 6 · 2022: 10 · 2021: 10 · 2020: 11 · 2019: 9 · 2018: 6 · 2017: 1
FWCI
8.58
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Journal of Experimental & Clinical Cancer Research (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)
  • Institutional Research Information System (Università degli Studi di Brescia) (submittedVersion)
Funders
  • Fondazione Cariplo
  • Istituto Superiore di Sanità (527/B4/4)
  • Università degli Studi di Brescia
  • National Institutes of Health (CA154460, UL1TR001863)
  • National Cancer Institute (U01CA176067)
  • National Center for Advancing Translational Sciences
Topics
  • Health Sciences › Medicine › Reproductive Medicine › Ovarian cancer diagnosis and treatment
  • Health Sciences › Medicine › Obstetrics and Gynecology › Endometrial and Cervical Cancer Treatments
  • Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
Keywords
FOXM1, epithelial ovarian cancer, ovarian clear cell carcinoma, endometrioid ovarian cancer, chemoresistance, platinum resistance, prognosis, olaparib, PARP inhibitors, cell proliferation, cell cycle, tumor invasion, gene expression signatures, oncogenes, disease-specific survival, time to progression, histological subtypes, FIGO stage
MeSH terms
Forkhead Box Protein M1, Carcinoma, Ovarian Epithelial, Adult, Aged, Aged, 80 and over, Antineoplastic Combined Chemotherapy Protocols, Cell Movement, Cell Transformation, Neoplastic, DNA Repair, Female, Humans, Middle Aged, Neoplasm Metastasis, Neoplasm Staging, Neoplasms, Glandular and Epithelial, Ovarian Neoplasms, Prognosis, Biomarkers, Tumor, Gene Expression Regulation, Neoplastic, Cystadenocarcinoma, Serous, Disease Progression, Drug Resistance, Neoplasm, Protein Isoforms, Gene Expression Profiling, RNA, Small Interfering, Cell Line, Tumor, Cell Proliferation, Kaplan-Meier Estimate, Gene Knockdown Techniques, Neoplasm Grading

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