Comparison of two-dimensional and three-dimensional culture systems and their responses to chemotherapy in cells representing disease progression of high-grade serous ovarian cancer

High-grade serous cancer is the most common type of ovarian cancer and is usually diagnosed at advanced stages with high mortality due to recurrence and eventual resistance to standard platinum therapy. The aim of this study was to compare two-dimensional (2D) versus tridimensional (3D) cell culture...

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Main Authors: Naya El Mokbel, Alicia A. Goyeneche, Rewati Prakash, Benjamin N. Forgie, Farah H. Abdalbari, Xing Zeng, Basile Tessier-Cloutier, Shuk On Annie Leung, Carlos M. Telleria
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Biochemistry and Biophysics Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2405580824002024
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author Naya El Mokbel
Alicia A. Goyeneche
Rewati Prakash
Benjamin N. Forgie
Farah H. Abdalbari
Xing Zeng
Basile Tessier-Cloutier
Shuk On Annie Leung
Carlos M. Telleria
author_facet Naya El Mokbel
Alicia A. Goyeneche
Rewati Prakash
Benjamin N. Forgie
Farah H. Abdalbari
Xing Zeng
Basile Tessier-Cloutier
Shuk On Annie Leung
Carlos M. Telleria
author_sort Naya El Mokbel
collection DOAJ
description High-grade serous cancer is the most common type of ovarian cancer and is usually diagnosed at advanced stages with high mortality due to recurrence and eventual resistance to standard platinum therapy. The aim of this study was to compare two-dimensional (2D) versus tridimensional (3D) cell culture as a preclinical model of response to carboplatin, paclitaxel and niraparib using PEO1, PEO4 and PEO6 cell lines, which were generated from the same patient along disease progression. Morphologically, cells formed flat adherent layers versus spheroidal structures with different compaction patterns in 2D and 3D respectively. In 2D, apoptosis was rare whereas in 3D cells formed a multilayered structure with an outer layer of live proliferating cells and an inner core of apoptotic cells. Furthermore, a differential capacity to produce ATP was observed among the cell lines in 3D but not in 2D. While response to carboplatin, paclitaxel and niraparib in both settings followed a similar trend, a lower sensitivity was observed in 3D with respect to 2D. Overall, 3D cell culture is likely more reflective of the in vivo cellular tumor behavior and more suitable of therapeutic evaluation given its added complexity absent in 2D.
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spelling doaj-art-700bf3ed34844eb6b08df2d216c52d672025-08-20T02:30:32ZengElsevierBiochemistry and Biophysics Reports2405-58082024-12-014010183810.1016/j.bbrep.2024.101838Comparison of two-dimensional and three-dimensional culture systems and their responses to chemotherapy in cells representing disease progression of high-grade serous ovarian cancerNaya El Mokbel0Alicia A. Goyeneche1Rewati Prakash2Benjamin N. Forgie3Farah H. Abdalbari4Xing Zeng5Basile Tessier-Cloutier6Shuk On Annie Leung7Carlos M. Telleria8McGill University, Experimental Pathology Unit, Department of Pathology, Faculty of Medicine and Health Sciences, Montreal, QC, CanadaMcGill University, Experimental Pathology Unit, Department of Pathology, Faculty of Medicine and Health Sciences, Montreal, QC, CanadaMcGill University, Experimental Pathology Unit, Department of Pathology, Faculty of Medicine and Health Sciences, Montreal, QC, CanadaMcGill University, Experimental Pathology Unit, Department of Pathology, Faculty of Medicine and Health Sciences, Montreal, QC, CanadaMcGill University, Experimental Pathology Unit, Department of Pathology, Faculty of Medicine and Health Sciences, Montreal, QC, CanadaMcGill University Health Centre, Division of Gynecologic Oncology, Department of Obstetrics and Gynecology, Montreal, QC, CanadaMcGill University, Experimental Pathology Unit, Department of Pathology, Faculty of Medicine and Health Sciences, Montreal, QC, CanadaMcGill University Health Centre, Division of Gynecologic Oncology, Department of Obstetrics and Gynecology, Montreal, QC, Canada; Research Institute of the McGill University Health Centre, Cancer Research Program, Montreal, QC, Canada; Corresponding author. McGill University Health Centre, Division of Gynecologic Oncology, Department of Obstetrics and Gynecology, Montreal, QC, Canada.McGill University, Experimental Pathology Unit, Department of Pathology, Faculty of Medicine and Health Sciences, Montreal, QC, Canada; Research Institute of the McGill University Health Centre, Cancer Research Program, Montreal, QC, Canada; Corresponding author. McGill University, Experimental Pathology Unit, Department of Pathology, Faculty of Medicine and Health Sciences, Montreal, QC, Canada.High-grade serous cancer is the most common type of ovarian cancer and is usually diagnosed at advanced stages with high mortality due to recurrence and eventual resistance to standard platinum therapy. The aim of this study was to compare two-dimensional (2D) versus tridimensional (3D) cell culture as a preclinical model of response to carboplatin, paclitaxel and niraparib using PEO1, PEO4 and PEO6 cell lines, which were generated from the same patient along disease progression. Morphologically, cells formed flat adherent layers versus spheroidal structures with different compaction patterns in 2D and 3D respectively. In 2D, apoptosis was rare whereas in 3D cells formed a multilayered structure with an outer layer of live proliferating cells and an inner core of apoptotic cells. Furthermore, a differential capacity to produce ATP was observed among the cell lines in 3D but not in 2D. While response to carboplatin, paclitaxel and niraparib in both settings followed a similar trend, a lower sensitivity was observed in 3D with respect to 2D. Overall, 3D cell culture is likely more reflective of the in vivo cellular tumor behavior and more suitable of therapeutic evaluation given its added complexity absent in 2D.http://www.sciencedirect.com/science/article/pii/S2405580824002024Ultra-low attachmentAnchorage-free3D culture2D cultureHigh grade serous ovarian cancerAnticancer drugs
spellingShingle Naya El Mokbel
Alicia A. Goyeneche
Rewati Prakash
Benjamin N. Forgie
Farah H. Abdalbari
Xing Zeng
Basile Tessier-Cloutier
Shuk On Annie Leung
Carlos M. Telleria
Comparison of two-dimensional and three-dimensional culture systems and their responses to chemotherapy in cells representing disease progression of high-grade serous ovarian cancer
Biochemistry and Biophysics Reports
Ultra-low attachment
Anchorage-free
3D culture
2D culture
High grade serous ovarian cancer
Anticancer drugs
title Comparison of two-dimensional and three-dimensional culture systems and their responses to chemotherapy in cells representing disease progression of high-grade serous ovarian cancer
title_full Comparison of two-dimensional and three-dimensional culture systems and their responses to chemotherapy in cells representing disease progression of high-grade serous ovarian cancer
title_fullStr Comparison of two-dimensional and three-dimensional culture systems and their responses to chemotherapy in cells representing disease progression of high-grade serous ovarian cancer
title_full_unstemmed Comparison of two-dimensional and three-dimensional culture systems and their responses to chemotherapy in cells representing disease progression of high-grade serous ovarian cancer
title_short Comparison of two-dimensional and three-dimensional culture systems and their responses to chemotherapy in cells representing disease progression of high-grade serous ovarian cancer
title_sort comparison of two dimensional and three dimensional culture systems and their responses to chemotherapy in cells representing disease progression of high grade serous ovarian cancer
topic Ultra-low attachment
Anchorage-free
3D culture
2D culture
High grade serous ovarian cancer
Anticancer drugs
url http://www.sciencedirect.com/science/article/pii/S2405580824002024
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