Modeling High-Grade Serous Carcinoma: How Converging Insights into Pathogenesis and Genetics Are Driving Better Experimental Platforms

Overview

Journal Front Oncol

Specialty Oncology

Date 2013 Aug 30

PMID 23986883

Citations 25

Authors

Paul Michael Jones

Ronny Drapkin

Affiliations

Soon will be listed here.

Abstract

Recent developments in the study of epithelial ovarian cancer have called into question the traditional views regarding the site of tumor initiation. Histopathologic studies and genomic analyses suggest that extra-ovarian sites, like the fallopian tube, may harbor the coveted cell of origin and could therefore contribute significantly to the development of high-grade serous ovarian carcinoma (HG-SOC). Our ability to validate these emerging genomic and pathologic observations and characterize the early transformation events of HG-SOC hinges on the development of novel model systems. Currently, there are only a handful of new model systems that are addressing these concerns. This review will chronicle the convergent evolution of these ovarian cancer model systems in the context of the changing pathologic and genomic understanding of HG-SOC.

Citing Articles

Combined assembloid modeling and 3D whole-organ mapping captures the microanatomy and function of the human fallopian tube.

Crawford A, Forjaz A, Bons J, Bhorkar I, Roy T, Schell D Sci Adv. 2024; 10(39):eadp6285.

PMID: 39331707 PMC: 11430475. DOI: 10.1126/sciadv.adp6285.

Lifetime Exposure to Cigarette Smoke, B-Cell Tumor Immune Infiltration, and Immunoglobulin Abundance in Ovarian Tumors.

Hathaway C, Townsend M, Wang T, Vinci C, Jake-Schoffman D, Hecht J Cancer Epidemiol Biomarkers Prev. 2024; 33(6):796-803.

PMID: 38517322 PMC: 11147730. DOI: 10.1158/1055-9965.EPI-23-1142.

Patient-derived organoid culture in epithelial ovarian cancers-Techniques, applications, and future perspectives.

Chan W, Mo X, Ip P, Tse K Cancer Med. 2023; 12(19):19714-19731.

PMID: 37776168 PMC: 10587945. DOI: 10.1002/cam4.6521.

Gain-of-function p53 blocks apoptosis in a precursor model of ovarian high-grade serous carcinoma.

Haagsma J, Kolendowski B, Buensuceso A, Valdes Y, DiMattia G, Shepherd T Sci Rep. 2023; 13(1):11424.

PMID: 37452087 PMC: 10349050. DOI: 10.1038/s41598-023-38609-5.

The organoid: A research model for ovarian cancer.

Chang Y, Wu K, Harnod T, Ding D Tzu Chi Med J. 2022; 34(3):255-260.

PMID: 35912056 PMC: 9333109. DOI: 10.4103/tcmj.tcmj_63_21.

References

El-Naggar S, Malik M, Kakar S . Small interfering RNA against PTTG: a novel therapy for ovarian cancer. Int J Oncol. 2007; 31(1):137-43. View

King S, Burdette J . Evaluating the progenitor cells of ovarian cancer: analysis of current animal models. BMB Rep. 2011; 44(7):435-45. PMC: 3677720. DOI: 10.5483/BMBRep.2011.44.7.435. View

Yang G, Rosen D, Colacino J, Mercado-Uribe I, Liu J . Disruption of the retinoblastoma pathway by small interfering RNA and ectopic expression of the catalytic subunit of telomerase lead to immortalization of human ovarian surface epithelial cells. Oncogene. 2006; 26(10):1492-8. DOI: 10.1038/sj.onc.1209905. View

Shih I, Kurman R . Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis. Am J Pathol. 2004; 164(5):1511-8. PMC: 1615664. DOI: 10.1016/s0002-9440(10)63708-x. View

Gregoire L, Munkarah A, Rabah R, Morris R, Lancaster W . Organotypic culture of human ovarian surface epithelial cells: a potential model for ovarian carcinogenesis. In Vitro Cell Dev Biol Anim. 1998; 34(8):636-9. DOI: 10.1007/s11626-996-0012-z. View

Jazaeri A, Bryant J, Park H, Li H, Dahiya N, Stoler M . Molecular requirements for transformation of fallopian tube epithelial cells into serous carcinoma. Neoplasia. 2011; 13(10):899-911. PMC: 3201567. DOI: 10.1593/neo.11138. View

Kim J, Coffey D, Creighton C, Yu Z, Hawkins S, Matzuk M . High-grade serous ovarian cancer arises from fallopian tube in a mouse model. Proc Natl Acad Sci U S A. 2012; 109(10):3921-6. PMC: 3309733. DOI: 10.1073/pnas.1117135109. View

Li C, Liu B, Wen Z, Li H . Inhibition of CD44 expression by small interfering RNA to suppress the growth and metastasis of ovarian cancer cells in vitro and in vivo. Folia Biol (Praha). 2009; 54(6):180-6. View

Fong M, Kakar S . Ovarian cancer mouse models: a summary of current models and their limitations. J Ovarian Res. 2009; 2(1):12. PMC: 2762470. DOI: 10.1186/1757-2215-2-12. View

10.

Lawrenson K, Benjamin E, Turmaine M, Jacobs I, Gayther S, Dafou D . In vitro three-dimensional modelling of human ovarian surface epithelial cells. Cell Prolif. 2009; 42(3):385-93. PMC: 6760819. DOI: 10.1111/j.1365-2184.2009.00604.x. View

11.

Molthoff C, Calame J, Pinedo H, Boven E . Human ovarian cancer xenografts in nude mice: characterization and analysis of antigen expression. Int J Cancer. 1991; 47(1):72-9. DOI: 10.1002/ijc.2910470114. View

12.

Kusakari T, Kariya M, Mandai M, Tsuruta Y, Hamid A, Fukuhara K . C-erbB-2 or mutant Ha-ras induced malignant transformation of immortalized human ovarian surface epithelial cells in vitro. Br J Cancer. 2003; 89(12):2293-8. PMC: 2395276. DOI: 10.1038/sj.bjc.6601423. View

13.

Massazza G, Tomasoni A, Lucchini V, Allavena P, Erba E, Colombo N . Intraperitoneal and subcutaneous xenografts of human ovarian carcinoma in nude mice and their potential in experimental therapy. Int J Cancer. 1989; 44(3):494-500. DOI: 10.1002/ijc.2910440320. View

14.

Resta L, Russo S, Colucci G, Prat J . Morphologic precursors of ovarian epithelial tumors. Obstet Gynecol. 1993; 82(2):181-6. View

15.

Connolly D, Bao R, Nikitin A, Stephens K, Poole T, Hua X . Female mice chimeric for expression of the simian virus 40 TAg under control of the MISIIR promoter develop epithelial ovarian cancer. Cancer Res. 2003; 63(6):1389-97. View

16.

Roby K, TAYLOR C, Sweetwood J, Cheng Y, Pace J, Tawfik O . Development of a syngeneic mouse model for events related to ovarian cancer. Carcinogenesis. 2000; 21(4):585-91. DOI: 10.1093/carcin/21.4.585. View

17.

Ho C, Kurman R, Dehari R, Wang T, Shih I . Mutations of BRAF and KRAS precede the development of ovarian serous borderline tumors. Cancer Res. 2004; 64(19):6915-8. DOI: 10.1158/0008-5472.CAN-04-2067. View

18.

Kenny H, Krausz T, Yamada S, Lengyel E . Use of a novel 3D culture model to elucidate the role of mesothelial cells, fibroblasts and extra-cellular matrices on adhesion and invasion of ovarian cancer cells to the omentum. Int J Cancer. 2007; 121(7):1463-72. DOI: 10.1002/ijc.22874. View

19.

Karst A, Drapkin R . The new face of ovarian cancer modeling: better prospects for detection and treatment. F1000 Med Rep. 2011; 3:22. PMC: 3206707. DOI: 10.3410/M3-22. View

20.

Korch C, Spillman M, Jackson T, Jacobsen B, Murphy S, Lessey B . DNA profiling analysis of endometrial and ovarian cell lines reveals misidentification, redundancy and contamination. Gynecol Oncol. 2012; 127(1):241-8. PMC: 3432677. DOI: 10.1016/j.ygyno.2012.06.017. View