Tumor organoids for primary liver cancers: A systematic review of current applications in diagnostics, disease modeling, and drug screening

Background & Aims: Liver cancer-related deaths are projected to exceed one million annually by 2030. Existing therapies have significant limitations, including severe side effects and inconsistent efficacy. Innovative therapeutic approaches to address primary liver cancer (PLC) have led to t...

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Main Authors: Ayesha A. Qureshi, Chase J. Wehrle, Sofia Ferreira-Gonzalez, Chunbao Jiao, Hanna Hong, Neda Dadgar, Jorge Arpi-Palacios, Yee Phoon Phong, Jaekeun Kim, Keyue Sun, Koji Hashimoto, David CH. Kwon, Charles Miller, Nic Leipzig, Wen Wee Ma, Jos Melenhorst, Federico Aucejo, Andrea Schlegel
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:JHEP Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S258955592400168X
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author Ayesha A. Qureshi
Chase J. Wehrle
Sofia Ferreira-Gonzalez
Chunbao Jiao
Hanna Hong
Neda Dadgar
Jorge Arpi-Palacios
Yee Phoon Phong
Jaekeun Kim
Keyue Sun
Koji Hashimoto
David CH. Kwon
Charles Miller
Nic Leipzig
Wen Wee Ma
Jos Melenhorst
Federico Aucejo
Andrea Schlegel
author_facet Ayesha A. Qureshi
Chase J. Wehrle
Sofia Ferreira-Gonzalez
Chunbao Jiao
Hanna Hong
Neda Dadgar
Jorge Arpi-Palacios
Yee Phoon Phong
Jaekeun Kim
Keyue Sun
Koji Hashimoto
David CH. Kwon
Charles Miller
Nic Leipzig
Wen Wee Ma
Jos Melenhorst
Federico Aucejo
Andrea Schlegel
author_sort Ayesha A. Qureshi
collection DOAJ
description Background & Aims: Liver cancer-related deaths are projected to exceed one million annually by 2030. Existing therapies have significant limitations, including severe side effects and inconsistent efficacy. Innovative therapeutic approaches to address primary liver cancer (PLC) have led to the ongoing development of tumor-derived organoids. These are sophisticated three-dimensional structures capable of mimicking native tissue architecture and function in vitro, improving our ability to model in vivo homeostasis and disease. Methods: This systematic review consolidates known literature on human and mouse liver organoids across all PLC subtypes, emphasizing diagnostic precision, disease modeling, and drug screening capabilities. Results: Across all 39 included studies, organoids were most frequently patient-derived, closely followed by cancer cell line-derived. The literature concentrated on hepatocellular carcinoma and intrahepatic cholangiocarcinoma, while exploration of other subtypes was limited. These studies demonstrate a valuable role for PLC organoid cultures in biomarker discovery, disease modeling, and therapeutic exploration. Conclusions: Encouraging advances such as organoid-on-a-chip and co-culturing systems hold promise for advancing treatment regimens for PLC. Standardizing in vitro protocols is crucial to integrate research breakthroughs into practical treatment strategies for PLC. Impact and implications:: This study provides an overview of the current understanding of tumor-derived organoids in primary liver cancers, emphasizing their potential in diagnostics, disease modeling, and drug screening. The scientific foundation rests on the organoids' ability to replicate the tumor microenvironment and genetic landscape, opening new avenues for personalized therapies. These insights are crucial for both researchers and clinicians, as patient-derived organoids can help identify biomarkers and therapeutic targets. Physicians and policymakers can harness these advances to drive progress in precision medicine, while recognizing the challenges involved in standardizing organoid models for clinical implementation.
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spelling doaj-art-581bcbb4523c4064b9c28f9533a139f52024-11-30T07:13:50ZengElsevierJHEP Reports2589-55592024-12-01612101164Tumor organoids for primary liver cancers: A systematic review of current applications in diagnostics, disease modeling, and drug screeningAyesha A. Qureshi0Chase J. Wehrle1Sofia Ferreira-Gonzalez2Chunbao Jiao3Hanna Hong4Neda Dadgar5Jorge Arpi-Palacios6Yee Phoon Phong7Jaekeun Kim8Keyue Sun9Koji Hashimoto10David CH. Kwon11Charles Miller12Nic Leipzig13Wen Wee Ma14Jos Melenhorst15Federico Aucejo16Andrea Schlegel17Nationwide Children's Hospital, Abigail Wexner Research Institute, 575 Children's Crossroad, Columbus, OH, 43215, USATransplantation Center, Cleveland Clinic, OH, USACIR Centre for Inflammation Research, University of Edinburgh, 5 Little France Drive Edinburgh, EH16 4UU, UKDepartment of Immunology, Lerner Research Institute, Cleveland Clinic, Cleveland, OH, USATransplantation Center, Cleveland Clinic, OH, USACleveland Clinic Foundation, Taussig Cancer Institute, Cleveland, OH, USA; Translational Hematology & Oncology Research, Cleveland Clinic, Enterprise Cancer Institute, Cleveland, OH, USACleveland Clinic Foundation, Lerner Research Institute, Center for Immunotherapy and Precision Immuno-Oncology, Cleveland, OH, USACleveland Clinic Foundation, Lerner Research Institute, Center for Immunotherapy and Precision Immuno-Oncology, Cleveland, OH, USATransplantation Center, Cleveland Clinic, OH, USADepartment of Immunology, Lerner Research Institute, Cleveland Clinic, Cleveland, OH, USATransplantation Center, Cleveland Clinic, OH, USATransplantation Center, Cleveland Clinic, OH, USATransplantation Center, Cleveland Clinic, OH, USAThe University of Akron, Department of Chemical, Biomolecular, and Corrosion Engineering, Akron, OH, USACleveland Clinic Foundation, Taussig Cancer Institute, Cleveland, OH, USACleveland Clinic Foundation, Lerner Research Institute, Center for Immunotherapy and Precision Immuno-Oncology, Cleveland, OH, USATransplantation Center, Cleveland Clinic, OH, USATransplantation Center, Cleveland Clinic, OH, USA; Department of Immunology, Lerner Research Institute, Cleveland Clinic, Cleveland, OH, USA; Corresponding author. Address: 9500 Euclid Avenue, Cleveland, OH 44195, USA; Tel. (216) 339-0741.Background & Aims: Liver cancer-related deaths are projected to exceed one million annually by 2030. Existing therapies have significant limitations, including severe side effects and inconsistent efficacy. Innovative therapeutic approaches to address primary liver cancer (PLC) have led to the ongoing development of tumor-derived organoids. These are sophisticated three-dimensional structures capable of mimicking native tissue architecture and function in vitro, improving our ability to model in vivo homeostasis and disease. Methods: This systematic review consolidates known literature on human and mouse liver organoids across all PLC subtypes, emphasizing diagnostic precision, disease modeling, and drug screening capabilities. Results: Across all 39 included studies, organoids were most frequently patient-derived, closely followed by cancer cell line-derived. The literature concentrated on hepatocellular carcinoma and intrahepatic cholangiocarcinoma, while exploration of other subtypes was limited. These studies demonstrate a valuable role for PLC organoid cultures in biomarker discovery, disease modeling, and therapeutic exploration. Conclusions: Encouraging advances such as organoid-on-a-chip and co-culturing systems hold promise for advancing treatment regimens for PLC. Standardizing in vitro protocols is crucial to integrate research breakthroughs into practical treatment strategies for PLC. Impact and implications:: This study provides an overview of the current understanding of tumor-derived organoids in primary liver cancers, emphasizing their potential in diagnostics, disease modeling, and drug screening. The scientific foundation rests on the organoids' ability to replicate the tumor microenvironment and genetic landscape, opening new avenues for personalized therapies. These insights are crucial for both researchers and clinicians, as patient-derived organoids can help identify biomarkers and therapeutic targets. Physicians and policymakers can harness these advances to drive progress in precision medicine, while recognizing the challenges involved in standardizing organoid models for clinical implementation.http://www.sciencedirect.com/science/article/pii/S258955592400168Xorganoid3D cell cultureliver cancerhepatocellular carcinomacholangiocarcinomadiagnosis
spellingShingle Ayesha A. Qureshi
Chase J. Wehrle
Sofia Ferreira-Gonzalez
Chunbao Jiao
Hanna Hong
Neda Dadgar
Jorge Arpi-Palacios
Yee Phoon Phong
Jaekeun Kim
Keyue Sun
Koji Hashimoto
David CH. Kwon
Charles Miller
Nic Leipzig
Wen Wee Ma
Jos Melenhorst
Federico Aucejo
Andrea Schlegel
Tumor organoids for primary liver cancers: A systematic review of current applications in diagnostics, disease modeling, and drug screening
JHEP Reports
organoid
3D cell culture
liver cancer
hepatocellular carcinoma
cholangiocarcinoma
diagnosis
title Tumor organoids for primary liver cancers: A systematic review of current applications in diagnostics, disease modeling, and drug screening
title_full Tumor organoids for primary liver cancers: A systematic review of current applications in diagnostics, disease modeling, and drug screening
title_fullStr Tumor organoids for primary liver cancers: A systematic review of current applications in diagnostics, disease modeling, and drug screening
title_full_unstemmed Tumor organoids for primary liver cancers: A systematic review of current applications in diagnostics, disease modeling, and drug screening
title_short Tumor organoids for primary liver cancers: A systematic review of current applications in diagnostics, disease modeling, and drug screening
title_sort tumor organoids for primary liver cancers a systematic review of current applications in diagnostics disease modeling and drug screening
topic organoid
3D cell culture
liver cancer
hepatocellular carcinoma
cholangiocarcinoma
diagnosis
url http://www.sciencedirect.com/science/article/pii/S258955592400168X
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