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Curated Papers > Recent high-impact research on "organoids" (IF≥30, last 5 years)

Organoid models of gastrointestinal cancers in basic and translational research. ​

Literature Information ​

DOI10.1038/s41575-019-0255-2
PMID32099092
JournalNature reviews. Gastroenterology & hepatology
Impact Factor51.0
JCR QuartileQ1
Publication Year2020
Times Cited96
KeywordsOrganoid technology, Gastrointestinal cancers, Tumor models, Personalized medicine, Therapy response
Literature TypeJournal Article, Review
ISSN1759-5045
Pages203-222
Issue17(4)
AuthorsHarry Cheuk Hay Lau, Onno Kranenburg, Haipeng Xiao, Jun Yu

TL;DR ​

This review highlights the significance of organoid technology as a superior method for studying gastrointestinal cancers, which constitute a significant portion of global cancer cases, by preserving the genetic and phenotypic traits of tumors compared to traditional cell culture methods. The findings emphasize organoids' potential in predicting therapeutic outcomes, while also addressing current limitations and suggesting improvements for enhancing their utility in drug discovery and personalized medicine.

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Organoid technology · Gastrointestinal cancers · Tumor models · Personalized medicine · Therapy response

Abstract ​

Cancer is a major public health problem worldwide. Gastrointestinal cancers account for approximately one-third of the total global cancer incidence and mortality. Historically, the mechanisms of tumour initiation and progression in the gastrointestinal tract have been studied using cancer cell lines in vitro and animal models. Traditional cell culture methods are associated with a strong selection of aberrant genomic variants that no longer reflect the original tumours in terms of their (metastatic) behaviour or response to therapy. Organoid technology has emerged as a powerful alternative method for culturing gastrointestinal tumours and the corresponding normal tissues in a manner that preserves their genetic, phenotypic and behavioural traits. Importantly, accumulating evidence suggests that organoid cultures have great value in predicting the outcome of therapy in individual patients. Herein, we review the current literature on organoid models of the most common gastrointestinal cancers, including colorectal cancer, gastric cancer, oesophageal cancer, liver cancer and pancreatic cancer, and their value in modelling tumour initiation, metastatic progression and therapy response. We also explore the limitations of current organoid models and discuss how they could be improved to maximally benefit basic and translational research in the future, especially in the fields of drug discovery and personalized medicine.

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Primary Questions Addressed ​

  1. How do organoid models compare to traditional animal models in terms of accurately reflecting the tumor microenvironment of gastrointestinal cancers?
  2. What specific advantages do organoid cultures offer in the context of personalized medicine for gastrointestinal cancer patients?
  3. In what ways can organoid technology be enhanced to better model the metastatic behavior of gastrointestinal tumors?
  4. How might the integration of organoid models with advanced imaging techniques improve our understanding of tumor progression in gastrointestinal cancers?
  5. What are the current limitations of organoid models in predicting therapy responses, and what strategies could be implemented to overcome these challenges?

Key Findings ​

Key Insights ​

  1. Research Background and Purpose: The study addresses the significant public health challenge posed by gastrointestinal (GI) cancers, which represent roughly one-third of global cancer cases and deaths. Traditional methods for investigating the mechanisms behind tumor initiation and progression, primarily through cancer cell lines and animal models, have limitations. These methods often lead to the selection of altered genomic variants that fail to accurately reflect the original tumors' characteristics, particularly in terms of metastatic behavior and therapeutic responses. The purpose of this study is to review the emerging organoid technology as a more effective alternative for modeling GI cancers, exploring its potential to preserve the genetic, phenotypic, and behavioral traits of tumors and normal tissues.

  2. Main Methods and Findings: The review synthesizes current literature on organoid models for various GI cancers, including colorectal, gastric, esophageal, liver, and pancreatic cancers. Organoids are 3D structures derived from stem cells that can mimic the architecture and functionality of real tissues. The findings suggest that organoid cultures maintain important genetic fidelity and are capable of recapitulating the tumor microenvironment, thereby providing a more accurate platform for studying tumor biology. Importantly, they show promise in predicting individual patient responses to therapies, making them a valuable tool in personalized medicine.

  3. Core Conclusions: Organoid technology represents a significant advancement over traditional cell culture methods, facilitating a more authentic representation of GI tumors. The ability of organoids to predict therapeutic outcomes could lead to improved personalized treatment strategies. However, the review also highlights the limitations of current organoid models, such as challenges in mimicking the full complexity of tumor microenvironments and the need for standardization in organoid culture practices.

  4. Research Significance and Impact: The insights from this study underscore the potential of organoid models to revolutionize both basic and translational research in oncology. By bridging the gap between in vitro studies and patient-specific treatment approaches, organoids could enhance drug discovery processes and lead to more effective therapies for GI cancers. Future improvements in organoid technology could maximize its utility in research, thereby contributing to better patient outcomes and advancing the field of personalized medicine. The findings emphasize the necessity for ongoing research to refine organoid methodologies and expand their applicability across various cancer types.

References ​

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Literatures Citing This Work ​

  1. Cholangiocarcinoma 2020: the next horizon in mechanisms and management. - Jesus M Banales;Jose J G Marin;Angela Lamarca;Pedro M Rodrigues;Shahid A Khan;Lewis R Roberts;Vincenzo Cardinale;Guido Carpino;Jesper B Andersen;Chiara Braconi;Diego F Calvisi;Maria J Perugorria;Luca Fabris;Luke Boulter;Rocio I R Macias;Eugenio Gaudio;Domenico Alvaro;Sergio A Gradilone;Mario Strazzabosco;Marco Marzioni;Cédric Coulouarn;Laura Fouassier;Chiara Raggi;Pietro Invernizzi;Joachim C Mertens;Anja Moncsek;Sumera I. Ilyas;Julie Heimbach;Bas Groot Koerkamp;Jordi Bruix;Alejandro Forner;John Bridgewater;Juan W Valle;Gregory J Gores - Nature reviews. Gastroenterology & hepatology (2020)
  2. Three-Dimensional Culture Systems in Gastric Cancer Research. - George Alzeeb;Jean-Philippe Metges;Laurent Corcos;Catherine Le Jossic-Corcos - Cancers (2020)
  3. Beyond just a tight fortress: contribution of stroma to epithelial-mesenchymal transition in pancreatic cancer. - Ashenafi Bulle;Kian-Huat Lim - Signal transduction and targeted therapy (2020)
  4. Human Intestinal Tissue Explant Exposure to Silver Nanoparticles Reveals Sex Dependent Alterations in Inflammatory Responses and Epithelial Cell Permeability. - Kuppan Gokulan;Katherine Williams;Sarah Orr;Sangeeta Khare - International journal of molecular sciences (2020)
  5. Gut microbiota: impacts on gastrointestinal cancer immunotherapy. - Harry Cheuk Hay Lau;Joseph Jao-Yiu Sung;Jun Yu - Gut microbes (2021)
  6. miR-335-5p suppresses gastric cancer progression by targeting MAPK10. - Yi Gao;Yanfeng Wang;Xiaofei Wang;Changan Zhao;Fenghui Wang;Juan Du;Huahua Zhang;Haiyan Shi;Yun Feng;Dan Li;Jing Yan;Yan Yao;Weihong Hu;Ruxin Ding;Mengjie Zhang;Lumin Wang;Chen Huang;Jing Zhang - Cancer cell international (2021)
  7. Challenges and Opportunities in NUT Carcinoma Research. - Maxwell C Hakun;Bin Gu - Genes (2021)
  8. Microfluidic Organoids-on-a-Chip: Quantum Leap in Cancer Research. - Fahriye Duzagac;Gloria Saorin;Lorenzo Memeo;Vincenzo Canzonieri;Flavio Rizzolio - Cancers (2021)
  9. Organoids Are Limited in Modeling the Colon Adenoma-Carcinoma Sequence. - Yoshihisa Tokumaru;Masanori Oshi;Ankit Patel;Wanqing Tian;Li Yan;Nobuhisa Matsuhashi;Manabu Futamura;Kazuhiro Yoshida;Kazuaki Takabe - Cells (2021)
  10. Wogonoside promotes apoptosis and ER stress in human gastric cancer cells by regulating the IRE1α pathway. - Qian Gu;Canhong Zhu;Xi Wu;Lianghuan Peng;Genya Huang;Rong Hu - Experimental and therapeutic medicine (2021)

... (86 more literatures)

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