Keywords
How to Cite
Abstract
A systematic review of modern methods of experimental study of ovarian cancer using traditional (immunocompetent, genetically engineered and immunodeficient) and non-traditional (that don’t belong to the mammals) animal models,established and primary cultures of human ovarian cancer, including three-dimensional organotypic spheroids (3D- models ex vivo) is presented. The prospects of the considered models for studying of the pathogenesis of various molecular-genetic and histological variants of ovarian cancer, as well as for developing methods of personalized treatment, are discussed. The limitations of modern animal models are indicated. The greatest attention is paid to studies on immunodeficient animals using xenografts based on established cultures of human ovarian cancer cells and on tumor tissue obtained directly from the patients (patient derived xenografts, PDX). The questions of various variants of xenograft transplantation with an emphasis on the problems of orthotopic transplantation of human ovarian cancer into immunodeficient mice and the relevance of methods for local humanization in heterotopic transplantation are considered. The most promising, from the point of the author’s view, approaches to studying the effectiveness of drug therapy for ovarian cancer in immunodeficient animal models are outlined. To prepare a systematic review, a literature search was carried out on the Scopus, Web of Science, Med Line, PubMed, Cyber Leninka, RSCI databases. The analysis used literature sources indexed in the Scopus and Web of Science databases (97%) and the RSCI. More than 60% of the works amount has been published over the past 5 years.
References
Городнова Т.В., Соколенко А.П., Кулигина Е.Ш. и др. Особенности рецидивирования распространенного BCRA-позитивного рака яичников // Вопросы онкологии. 2017;63(2):298–303 [Gorodnova T.V., Sokolenko A.P., Kuligina E.Sh. et al. Features of recurrence of BCRA-positive ovarian cancer // Problems in oncology. 2017;63(2):298–303. In Russ.].
Румянцев А.А., Тюляндина А.С., Покатаев И.А., Тюляндин С.А. Спорные вопросы оптимальной тактики хирургического лечения больных распространенным раком яичников // Злокачественные опухоли. 2017;7(3):13–22. https: // doi: 10.18027 / 2224–5057–2017–7–3–13–22 [Rumyantsev A.A., Tjulandina A.S., Pokataev I.A., Tjulandin S.A. Controversies in surgical treatment of advanced ovarian cancer // Malignant Tumours. 2017;7(3):13–22. https: // doi: 10.18027 / 2224–5057–2017–7–3–13–22 (In Russ.)].
Mihanfar A, Fattahi A, Nejabati HR. MicroRNA-mediated drug resistance in ovarian cancer // J Cell Physiol. 2019;234(4):3180–3191. https: // doi: 10.1002/jcp.26060
Lengyel E, Burdette JE, Kenny HA, Matei D, Pilrose J, Haluska P, Nephew KP, Hales DB, Stack M.S. Epithelial Ovarian Cancer Experimental Models // Oncogene. 2014 Jul 10;33(28):3619–3633. https: // doi: 10.1038/onc.2013.321
Cortez AJ, Tudrej P, Kujawa KA, Lisowska KM. Advances in ovarian cancer therapy // Cancer Chemother. Pharmacol. 2018;81(1):17–38. https: // doi: 10.1007/s00280-017-3501-8
Виллерт А.Б., Коломиец Л.А., Юнусова Н.В., Фесик Е.А. Молекулярно-генетические подтипы рака яичников: перспективы дальнейших исследований // Вопросы онкологии. 2019;65(1):56–62 [Villert A.B., Kolomiets L.A., Unusova N.V., Fesik E.A. Molecular and genetic subtypes of ovarian cancer: prospects for further studies // Problems in oncology. 2019; 65(1): 56–62 (In Russ.)].
Горошинская И.А., Сурикова Е.И., Шалашная Е.В. и др. Cостояние свободнорадикальных процессов при раке яичников с разной распространенностью и течением заболевания. Известия высших учебных заведений // Северо-Кавказский регион. Серия: естественные науки. 2017;(4–2):10–19. https: // doi: 10.23683/0321-3005-2017-4-2-10-19 [Goroshinskaya I.A., Surikova E.I, Shalashnaya E.V. et al. State of free radical processes in ovarian cancer with different prevalence and course of the disease. Izvestiya vuzov // Severo-Kavkazskii Region. Natural Science. 2017;(4–2): 10–19 . https: // doi: 10.23683/0321-3005-2017-4-2-10-19 (In Russ.)].
Maru Y, Hippo Y. Current Status of Patient-Derived Ovarian Cancer Models // Cells. 2019;8(5):505. https: // doi: 10.3390/cells8050505.
Cybulska P, Stewart JM, Sayad A et al. A Genomically Characterized Collection of High-Grade Serous Ovarian Cancer Xenografts for Preclinical Testing // Am. J. Pathol. 2018;188(5):1120–11. https: // doi: 10.1016/j.ajpath.2018.01.019
Damia G, Broggini M. Platinum Resistance in Ovarian Cancer: Role of DNA Repair // Cancers 2019, 11(1):119. https: // doi: 10.3390/cancers11010119
Rosales-Nieves AE, Gonzalez-Reyes A. Genetics and mechanisms of ovarian cancer: Parallels between Drosophila and humans // Semin. Cell Dev. Biol. 2014;28:104–109. https: // doi: 10.1016/j.semcdb.2014.03.031
Tudrej P, Kujawa KA, Cortez AJ, Lisowska KM. Characteristics of in Vivo Model Systems for Ovarian Cancer Studies // Diagnostics (Basel). 2019;9(3):120. https: // doi: 10.3390/diagnostics9030120
Hardwick LJA, Philpott A. Xenopus Models of Cancer: Expanding the Oncologist's Toolbox. Front Physiol. 2018;9:1660. doi: 10.3389/fphys.2018.01660
Barua A, Bitterman P, Abramowicz JS et al. Histopathology of ovarian tumors in laying hens a preclinical model of human ovarian cancer // Int. J. Gynecol. Cancer. 2009;19(4):531–539. https: // doi: 10.1111/IGC.0b013e3181a41613
Bernardo AM, Thorsteinsdottir S, Mummery CL. Advantages of the avian model for human ovarian cancer // Mol. Clin. Oncol. 2015;3(6):1191–1198. https: // doi: 10.3892/mco.2015.619
Ribatti D. The chick embryo chorioallantoic membrane (CAM). A multifaceted experi-mental model // Mech. Dev. 2016;141:70–77. https: // doi: 10.1016/j.mod.2016.05.003. Трад. Мод. 1 Синг.
Daniel D. Development. ID8: A syngeneic mouse model for testing ovarian cancer immunotherapies. 07.11.2017. The site of Covance. Available at https: // www.covance.com/industry-solutions/oncology/preclinical/tumor-spotlights/id8-syngeneic-mouse-model-testing-ovarian-cancer-immunotherapies.html 10.06.2020. Accessed 10.09.2020.
Fan L, Liu Y, Zhang X et al. Establishment of Fischer 344 rat model of ovarian cancer with lymphatic metastasis // Arch Gynecol Obstet. 2014;289(1):149–154. https: // doi: 10.1007/s00404-013-2937-2
Беспалов В.Г., Вышинская Е.А., Васильева И.Н. и др. Повышение эффективности лечения канцероматоза брюшной полости с помощью интраперитонеальной полихимиотерапии на модели диссеминированного рака яичника // Вопросы онкологии. 2018;64(3):440‒444 [Bespalov V.G., Vyshinskaya E.A., Vasilyeva I.N. et al. Improvement of efficiency of treatment of abdominal canceromatosis by intraperitoneal polychemotherapy on model of disseminated ovarian cancer // Problems in oncology. 2018; 64(3):440‒444 (In Russ.)].
Sawyer TW, Koevary JW, Rice PFS, Barton JK. In Vivo Optical Coherence Tomography of a Mouse Model of Spontaneous Ovarian Cancer. In “Clinical and Preclinical Optical Diagnostics» II, Vol. EB101 of SPIE Proceedings (Optical Society of America, 2019), paper 11073_49. Available at https: // www.osapublishing.org/abstract.cfm?URI=ECBO-2019-11073_4. Accessed 19.08.2020
House CD, Hernandez L, Annunziata CM. Recent technological advances in using mouse models to study ovarian cancer // Front. Oncol. 2014;4:26. https: // doi: 10.3389/fonc.2014.00026
Погосянц Е.Е., Пригожина Е.Л., Еголина Н.А. Перевиваемая опухоль яичника крысы // Вопросы онкологии. 1962;11:29–36 [Pogosyants Ye.Ye., Prigozhina Ye.L., Yegolina N.A. Transplanted ovarian rat tumor // Problems in Oncology. 1962; 11:29–36 (In Russ.)].
Киреева Г.С., Беляева О.А., Сенчик К.Ю. и др. Асцитная опухоль яичников у крыс — адекватная доклиническая модель канцероматоза для изучения интраперитонеального химиоперфузионного лечения. Современное состояние вопроса // Сибирский онкологический журнал. 2019;18(1):71–78. https: // doi: 10.21294/1814-4861-2019-18-1-71-78 [Kireeva G.S., Belyaeva O.A., Senchik K.Y., Bespalov V.G., Stukov A.N., Gubareva E.A., Maydin M.A. Ascitic ovarian cancer is an adequate preclinical model of carcinomatosis to study intraperitoneal chemoperfusion treatment // Siberian Journal of Oncology. 2019;18 (1):71–78. https: // doi: 10.21294/1814-4861-2019-18-1-71-78 (In Russ.].
Cai Q, Yan L, Xu Y. Anoikis resistance is a critical feature of highly aggressive ovarian cancer cells // Oncogene. 2015;34(25):3315–3324. https: // doi: 10.1038/onc.2014.264
McCloskey CW, Goldberg RL, Carter LE et al. A new spontaneously transformed syngeneic model of high-grade serous ovarian cancer with a tumor-initiating cell population // Front. Oncol. 2014;4:53. https: // doi: 10.3389/fonc.2014.00053
Kuhn E, Tisato V, Rimondi E, Secchiero P. Current Preclinical Models of Ovarian Cancer // J Carcinog Mutagen 2015, 6(2):1-9. https: // doi: 10.4172/2157-2518.1000220
Gargiulo G. Next-Generation in vivo Modeling of Human Cancers. Review article // Front. Oncol. 2018;8:429. https: // doi: 10.3389/fonc.2018.00429
Mullany LK, Richards JS. Minireview: Animal Models and Mechanisms of Ovarian Cancer Development // Endocrinology. 2012;153(4):1585–1592. https: // doi: 10.1210/en.2011-2121
Harlan B, Nikitin AYu. A Quest for Better Mouse Models of Breast and Ovarian Cancers // EBioMedicine. 2015;2(10):1268–1269. https: // doi: 10.1016/j.ebiom.2015.09.017
Flesken-Nikitin A, Hwang C-I, Cheng C-Y et al. Ovarian surface epithelium at the junction area contains a cancer-prone stem cell niche // Nature. 2013;495(7440):241–245. https: // doi: 10.1038/nature11979
Kim J, Coey DM, Creighton CJ et al. High-grade serous ovarian cancer arises from fallopian tube in a mouse model // Proc. Natl. Acad. Sci. USA. 2012;109:3921–3926. https: // doi: 10.1073/pnas.1117135109
Purnell BA. Modeling Ovarian Cancer // Science. 2012;335(6074):1280–1281. https: // doi: 10.1126/science.335.6074.1280-d
Perets R, Wyant GA, Muto KW et al. Transformation of the fallopian tube secretory epithelium leads to high-grade serous ovarian cancer in BRCA, Tp53, Pten models // Cancer Cell 2013, 24(6):751–765. https: // doi: 10.1016/j.ccr.2013.10.013
Fong MY, Kakar SS. Ovarian cancer mouse models: a summary of current models and their limitations // J Ovarian Res. 2009;2(1):12. https: // doi: 10.1186/1757-2215-2-12
Rygaard J, Povlsen CO. Heterotransplantation of a human malignant tumour to «Nude» mice // Acta Pathol Microbiol Scand. 1969;77(4):758–760. https: // doi: 10.1111/j.1699-0463.1969.tb04520.x
Szadvari I, Krizanova O, Babula P. Athymic nude mice as an experimental model for cancer treatment // Physiol. Res. 2016;65 (4):441–453. https: // doi: 10.33549/physiolres.933526
De La Rochere P, Guil-Luna S, Decaudin D, Azar G, Sidhu SS, Piaggio E. Humanized Mice for the Study of Immuno-Oncology // Trends in Immunology. 2018;39(9):748–63. https: // doi: 10.1016/j.it.2018.07.00
Кит О.И., Жукова Г.В., Максимов А.Ю. и др. Ортотопические ксенографты глиальных опухолей человека: история, технологии, достижения и проблемы // Медицинский вестник Северного Кавказа. 2020;15(1):133–139. https: // doi: 10.14300/mnnc.2020.15034 [Kit O.I., Zhukova GV., Maximov A.Yu. et al. Orthotopic grafts of human malignant gliomas: history, technologies, achievements and problems // Medical News of North Caucasus. 2020;15(1):133–139. https: // doi: 10.14300/mnnc.2020.15034] (In Russ.)].
Балдуева И.А., Данилова А.Б., Нехаева Т.Л., Беляев А.М. Клеточная линия рака яичника человека 533 OOS. Патент на изобретение RU 2650759 C1, 17.04.2018. Заявка № 2017126922 от 26.07.2017 [Baldueva I.A., Danilova A.B., Nekhaeva T.L., Belyaev A.M. Human ovarian cancer cell line 533 OOS. Invention patent. RU 2650759 C1, 17.04.2018]. (in Russ.)].
Генетические и биологические коллекции Российской Федерации. Российская коллекция клеточных культур позвоночных. https: // doi: www.sevin.ru/collections/cellcolls/rcccm.html. Accessed 07.09.2020 [Geneticheskie i biologicheskie kollektsii Rossiiskoi Federatsii. Rossiiskaia kollektsiia kletochnykh kultur pozvonochnykh. Genetic and biological collections of the Russian Federation. Russian collection of vertebrate cell cultures]. (in Russ.). https: // doi: www.sevin.ru/collections/cellcolls/rcccm.html . Accessed 07.09.2020].
Letourneau IJ, Quinn MC, Wang LL et al. Derivation and characterization of matched cell lines from primary and recurrent serous ovarian cancer // BMC Cancer. 2012;12:379. https: // doi: 10.1186/1471-2407-12-37912, 379
Tudrej P, Kujawa KA, Cortez AJ, Lisowska KM. Characteristics of in vitro model systems for ovarian cancer studies // Oncol. Clin. Pract. 2019;15(5):246–259. https: // doi: 10.5603/OCP.2019.0024.
Tudrej P, Olbryt M, Zembala-Nozynska E et al. Establishment and characterization of the novel high-grade serous ovarian cancer cell line OVPA8 // Int. J. Mol. Sci. 2018;19(7):1–26. https: // doi: 10.3390/ijms19072080
Guo J, Cai J, Zhang Y et al. Estalishment of two ovarian cancer orthotopic xenograft mouse models for in vivo imaging: A comparative study // International Journal of Oncology. 2017;1199–1208. https: // doi: 10.3892/ijo.2017.411
Kiguchi K, Kubota T, Aoki D et al. A patient-like orthotopic implantation nude mouse model of highly metastatic human ovarian cancer // Clin. Exp. Metastasis. 1998;16:751–756. 1998. https: // doi: 10.1023/A:1006537013317
Cordero AB, Kwon Y, Hua X, Godwin AK. In vivo Imaging and Therapeutic Treatments in an Orthotopic Mouse Model of Ovarian Cancer // J. Vis. Exp. 2010;42:e2125. https: // doi: 10.3791/2125
Magnotti E, Marasco WA. The latest animal models of ovarian cancer for novel drug discovery // Expert. Opin. Drug Discov. 2018;13:249–257. https: // doi: 10.1080/17460441.2018.1426567
Hernandez L, Kim MK, Lyle LT et al. Characterization of ovarian cancer cell lines as in vivo models for preclinical studies // Gynecol. Oncol. 2016;142(2):332–340. https: // doi: 10.1016/j.ygyno.2016.05
Zhao Ya, Cao J, Melamed A et al. Losartan treatment enhances chemotherapy efficacy and reduces ascites in ovarian cancer models by normalizing the tumor stroma // PNAS. 2019;116 (6):2210–2219. https: // doi: 10.1073/pnas.1818357116
Hasan N, Ohman AW, Dinulescu DM. The promise and challenge of ovarian cancer models // Transl Cancer Res. 2015;4(1):14–28. https: // doi: 10.3978/j.issn.2218-676X.2015.01.02
Dobbin ZC, Katre AA, Steg AD et al. Using Heterogeneity of the Patient-Derived Xenograft Model to Identify the Chemoresistant Population in Ovarian Cancer // Oncotarget. 2014;5(18):8750–64. https: // doi: 10.18632/oncotarget.2373
Fu X, Hoffman RM. Human ovarian carcinoma metastatic models constructed in nude mice by orthotopic transplantation of histologically-intact patient specimens // Anticancer Res. 1993;13(2):283–286.
Bogden AE, Haskell PM, LePage DJ et al. Growth of human tumor xenografts implanted under the renal capsule of normal immunocompetent mice // Exp Cell Biol. 1979;47(4):281–93. https: // doi: 10.1159/000162947
Maeda K, Ushijima H, Shimamoto T et al. Clinical application of subrenal capsule assay in ovarian cancer // Nihon Sanka Fujinka Gakkai zasshi. 1989;41(12):1896–1902. Japanese.
Gonzalez H, Hagerling C, Werb Z. Roles of the immune system in cancer: from tumor initiation to metastatic progression // Genes Dev. 2018;32(19–20):1267–1284. https: // doi: 10.1101/gad.314617.118
Bankert RB, Balu-Iyer SV, Odunsi K et al. Humanized mouse model of ovarian cancer recapitulates patient solid tumor progression, ascites formation, and metastasis // PLoS ONE. 2011, 6(9):e24420. https: // doi: 10.1371/journal.pone.0024420
Fu SH, Wang J, Sun W et al. Preclinical humanized mouse model with ectopic ovarian tissues // Experimental and Therapeutic Medicine. 2014;8(3):742–746. https: // doi: 10.3892/etm.2014.1819
Непомнящих Т.С., Гаврилова Е.В., Максютов Р.А. Некоторые аспекты использования алло- и ксенографтных моделей при разработке противораковых вакцин и онколитических вирусов // Медицинская иммунология. 2019, 21(2):221–230. https: // doi: 10.15789/1563-0625-2019-2-221-230 [Nepomnyashchikh T.S., Gavrilova E.V., Maksyutov RA. Some applications of allo- and xenograft models for developing novel anticancer vaccines and oncolytic viruses // Medical Immunology (Russia). 2019;21(2):221–230. https: // doi: 10.15789/1563-0625-2019-2-221-230 (In Russ.)].
Villacorta-Martin C, Craig AJ, Villanueva A. Divergent evolutionary trajectories in transplanted tumor models // Nat Genet. 2017;49(11):1565–1566. https: // doi: 10.1038/ng.3983. PMID: 29074950
Ben-David U, Beroukhim R, Golub TR. Genomic evolution of cancer models: perils and opportunities // Nat Rev Cancer. 2019;19:97–109. https: // doi: 10.1038/s41568-018-0095
Maniati E, Berlato C, Gopinathan G et al. Mouse Ovarian Cancer Models Recapitulate the Human Tumor Microenvironment and Patient Response to Treatment // Cell Rep. 2020;30(2):525–540.e7. https: // doi: 10.1016/j.celrep.2019.12.034
White EA, Kenny HA, Lengyel E. Three-dimensional modeling of ovarian cancer // Adv. Drug. Deliv. Rev. 2014;79–80:184–192. https: // doi: 10.1016/j.addr.2014.07.003
Prina-Mello A, Jain N, Liu B et al. Culturing substrates influence the morphological, mechanical and biochemical features of lung adenocarcinoma cells cultured in 2D or 3D // Tissue Cell. 2018;50:15–30. https: // doi: 10.1016/j.tice.2017.11.003
Tzanakakis GN, Giatagana EM, Kuskov A, Nikitovic D. Proteoglycans in the Pathogenesis of Hormone- Dependent Cancers: Mediators and Effectors // Cancers. 2020;12(9). https: // doi: 10.3390/cancers12092401
Просекина Е.А., Данилова А.Б., Нехаева Т.Л., Балдуева И.А. Создание трёхмерных клеточных моделей для решения теоретических и практических задач современной онкологии // Вопросы онкологии. 2019;65(5):629–637 [Prosekina E.A., Danilova A.B., Nehaeva TL, Baldueva I.A. The creating of three-dimensional cellular models to solve theoretical and practical problems of modern oncology // Problems in oncology. 2019;65(5):629–637 (In Russ.)].
Watters KM, Bajwa P, Kenny HA. Organotypic 3D Models of the Ovarian Cancer Tumor Microenvironment // Cancers. 2018;10(8):265–274. https: // doi: org/10.3390/cancers10080265
Lu M, Henry CE, Lai H, Khine YY et al. A new 3D organotypic model of ovarian cancer to help evaluate the antimetastatic activity of RAPTA-C conjugated micelles // Biomater Sci. 2019;7(4):1652–1660. https: // doi: 10.1039/c8bm01326h
Полозников А.А., Никулин С.В., Болотина Л.В. и др. Сравнение 2d- и 3d-культур аденокарциномы прямой кишки как моделей для тестирования лекарственных препаратов // Известия Академии наук. Серия химическая. 2019;12:2377–2380 [Poloznikov A.A., Alexeev BY, Nikulin SV. et al.Comparison of 2d and 3d cell cultures of colorectal adenocarcinoma as models for drug screening // Russian chemical bulletin. 2019;68(12):2377–2380 (InRuss.)].
Kopper O, de Witte CJ, Lõhmussaar K et al. An organoid platform for ovarian cancer captures intra- and interpatient heterogeneity // Nat Med. 2019;25(5):m838–849. https: // doi: 10.1038/s41591-019-0422-6
Maru Y, Tanaka N, Itami M, Hippo Y. Efficient use of patient-derived organoids as a preclinical model for gynecologic tumors // Gynecol Oncol. 2019;154(1):189–198. https: // doi: 10.1016/j.ygyno.2019.05.005
Lengyel E, Burdette JE, Kenny HA et al. Epithelial Ovarian Cancer Experimental Models // Oncogene. 2014;33(28):3619–3633. https: // doi: 10.1038/onc.2013.321
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
© АННМО «Вопросы онкологии», Copyright (c) 2021