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Patient-derived tumor organoids: a new avenue for preclinical research and precision medicine in oncology

Thorel, Lucie, Perréard, Marion, Florent, Romane, Divoux, Jordane, Coffy, Sophia, Vincent, Audrey, Gaggioli, Cédric, Guasch, Géraldine, Gidrol, Xavier, Weiswald, Louis-Bastien, Poulain, Laurent·2024·Experimental & Molecular Medicine
DOI 10.1038/s12276-024-01272-5PMC PMC11297165
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Abstract

Over the past decade, the emergence of patient-derived tumor organoids (PDTOs) has broadened the repertoire of preclinical models and progressively revolutionized three-dimensional cell culture in oncology. PDTO can be grown from patient tumor samples with high efficiency and faithfully recapitulates the histological and molecular characteristics of the original tumor. Therefore, PDTOs can serve as invaluable tools in oncology research, and their translation to clinical practice is exciting for the future of precision medicine in oncology. In this review, we provide an overview of methods for establishing PDTOs and their various applications in cancer research, starting with basic research and ending with the identification of new targets and preclinical validation of new anticancer compounds and precision medicine. Finally, we highlight the challenges associated with the clinical implementation of PDTO, such as its representativeness, success rate, assay speed, and lack of a tumor microenvironment. Technological developments and autologous cocultures of PDTOs and stromal cells are currently ongoing to meet these challenges and optimally exploit the full potential of these models. The use of PDTOs as standard tools in clinical oncology could lead to a new era of precision oncology in the coming decade.

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Fig. 1 Timeline of the development of tumor cell models in oncology (created with BioRender.com). Adapted from199.
Fig. 1 Timeline of the development of tumor cell models in oncology (created with BioRender.com). Adapted from199.CC BY · PubMed Central
Fig. 2 Procedure for the generation of PDTOs. Schematic representation of the various stages in the production of tumor organoids for research purposes (created with BioRender.com). Adapted from199.
Fig. 2 Procedure for the generation of PDTOs. Schematic representation of the various stages in the production of tumor organoids for research purposes (created with BioRender.com). Adapted from199.CC BY · PubMed Central
Fig. 3 Contribution of PDTO to the fields of basic research and precision oncology (created with BioRender.com).
Fig. 3 Contribution of PDTO to the fields of basic research and precision oncology (created with BioRender.com).CC BY · PubMed Central
Fig. 4 Future challenges for using PDTO in clinical practice (created with BioRender.com). Adapted from 200.
Fig. 4 Future challenges for using PDTO in clinical practice (created with BioRender.com). Adapted from 200.CC BY · PubMed Central
Fig. 5 Coculture of PDTOs with autologous stromal and immune cells broadens therapies that could be tested. DC dendritic cell, NK natural killer cell, Mɸ macrophage, TLR toll-like receptor, BiKEs bispecific killer cell engagers, TriKEs trispecific killer cell engagers, ICB immune checkpoint blockade (created with BioRender.com).
Fig. 5 Coculture of PDTOs with autologous stromal and immune cells broadens therapies that could be tested. DC dendritic cell, NK natural killer cell, Mɸ macrophage, TLR toll-like receptor, BiKEs bispecific killer cell engagers, TriKEs trispecific killer cell engagers, ICB immune checkpoint blockade (created with BioRender.com).CC BY · PubMed Central
Fig. 6 Vascularization and microfluidic applications for PDTO. a Representation of a classical 96-well plate with PDTOs grown in a Matrigel bed. b Representation of a serpentine microfluidic chip with a single PDTO vascularized with endothelial cells and an endothelial network in the gel, thus allowing for perfusion of the medium and/or drugs in the PDTO. The addition of flow improved vascular network formation (created with BioRender.com).
Fig. 6 Vascularization and microfluidic applications for PDTO. a Representation of a classical 96-well plate with PDTOs grown in a Matrigel bed. b Representation of a serpentine microfluidic chip with a single PDTO vascularized with endothelial cells and an endothelial network in the gel, thus allowing for perfusion of the medium and/or drugs in the PDTO. The addition of flow improved vascular network formation (created with BioRender.com).CC BY · PubMed Central

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Metadata

Authors
Thorel, L., Perréard, M., Florent, R., Divoux, J., Coffy, S., Vincent, A., Gaggioli, C., Guasch, G., Gidrol, X., Weiswald, L.-B., & Poulain, L.
Venue
Experimental & Molecular Medicine
Publisher
Springer Science and Business Media LLC
Published
2024-07-01
Volume
56
Issue
7
Pages
1531-1551
ISSN
2092-6413
DOI
10.1038/s12276-024-01272-5
PMC
PMC11297165
Cited by
236
References
37
Language
en
Licence

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