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

Organoids. ​

Literature Information ​

DOI10.1038/s43586-022-00174-y
PMID37325195
JournalNature reviews. Methods primers
Impact Factor56.0
JCR QuartileQ1
Publication Year2022
Times Cited348
KeywordsOrganoids, Tissue Engineering, Disease Modeling, Drug Discovery, Personalized Medicine
Literature TypeJournal Article
ISSN2662-8449
Issue2()
AuthorsZixuan Zhao, Xinyi Chen, Anna M Dowbaj, Aleksandra Sljukic, Kaitlin Bratlie, Luda Lin, Eliza Li Shan Fong, Gowri Manohari Balachander, Zhaowei Chen, Alice Soragni, Meritxell Huch, Yi Arial Zeng, Qun Wang, Hanry Yu

TL;DR ​

This Primer discusses the significance of organoids as versatile in vitro models that mirror the complexity of human tissues, facilitating studies on development, disease, and personalized medicine. It outlines various engineering strategies for their development and highlights essential considerations for generating robust organoids, while also addressing limitations and future priorities in organoid research.

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Organoids · Tissue Engineering · Disease Modeling · Drug Discovery · Personalized Medicine

Abstract ​

Organoids have attracted increasing attention because they are simple tissue-engineered cell-based in vitro models that recapitulate many aspects of the complex structure and function of the corresponding in vivo tissue. They can be dissected and interrogated for fundamental mechanistic studies on development, regeneration, and repair in human tissues. Organoids can also be used in diagnostics, disease modeling, drug discovery, and personalized medicine. Organoids are derived from either pluripotent or tissue-resident stem (embryonic or adult) or progenitor or differentiated cells from healthy or diseased tissues, such as tumors. To date, numerous organoid engineering strategies that support organoid culture and growth, proliferation, differentiation and maturation have been reported. This Primer serves to highlight the rationale underlying the selection and development of these materials and methods to control the cellular/tissue niche; and therefore, structure and function of the engineered organoid. We also discuss key considerations for generating robust organoids, such as those related to cell isolation and seeding, matrix and soluble factor selection, physical cues and integration. The general standards for data quality, reproducibility and deposition within the organoid community is also outlined. Lastly, we conclude by elaborating on the limitations of organoids in different applications, and key priorities in organoid engineering for the coming years.

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Primary Questions Addressed ​

  1. What are the specific challenges faced in the differentiation and maturation of organoids derived from different types of stem cells?
  2. How do the mechanical properties of the extracellular matrix influence the growth and functionality of organoids in various applications?
  3. In what ways can organoids be utilized to model specific diseases beyond cancer, and what are the implications for personalized medicine?
  4. What advancements in organoid engineering techniques have shown the most promise for improving reproducibility and data quality in research?
  5. How do organoids compare to traditional animal models in terms of their predictive value for human responses in drug discovery and development?

Key Findings ​

Research Background and Objectives ​

Organoids have emerged as innovative in vitro models that replicate the complex structure and functionality of human tissues. Their utility spans fundamental research in development, regeneration, and repair, as well as applications in diagnostics, disease modeling, drug discovery, and personalized medicine. This Primer aims to elucidate the rationale behind the selection and development of materials and methods for organoid engineering, addressing the challenges in creating robust organoids.

Main Methods/Materials/Experimental Design ​

The development of organoids involves several key strategies that ensure their growth, proliferation, differentiation, and maturation. The following flowchart illustrates the main components of organoid engineering:

Mermaid diagram
  1. Organoid Source Selection: Organoids can be derived from pluripotent stem cells or tissue-resident stem/progenitor cells from both healthy and diseased tissues.
  2. Cell Isolation and Seeding: This step is crucial for ensuring that the right cell types are used and are adequately seeded in the culture system.
  3. Matrix Selection: The extracellular matrix (ECM) plays a significant role in providing structural support and biochemical signals.
  4. Soluble Factor Selection: Growth factors and cytokines are added to influence cell behavior and organoid development.
  5. Physical Cues Integration: Mechanical and physical properties of the culture environment can affect organoid formation and function.
  6. Organoid Growth and Maturation: Monitoring the growth and maturation of organoids to ensure they develop appropriately.
  7. Characterization and Quality Control: Establishing standards for data quality and reproducibility within the organoid research community.

Key Results and Findings ​

  • Organoids effectively mimic the architecture and functionality of their in vivo counterparts, making them suitable for a wide range of applications.
  • The choice of source cells, matrices, and soluble factors significantly impacts the success of organoid cultures.
  • Robust organoids can be generated by optimizing these parameters, which leads to improved reproducibility and reliability in experimental outcomes.

Main Conclusions/Significance/Innovation ​

The Primer highlights the importance of careful selection of materials and methods in organoid engineering, emphasizing the need for standardization in data quality and reproducibility. It presents a comprehensive overview of the current state of organoid technology and identifies critical areas for future development. The insights provided can guide researchers in optimizing organoid culture systems for various applications, thereby enhancing the translational potential of organoid research.

Research Limitations and Future Directions ​

Despite their advantages, organoids have limitations, including:

  • Variability in organoid generation and behavior depending on the source and culture conditions.
  • Challenges in recapitulating the full complexity of in vivo environments, particularly in disease modeling.

Future research priorities include:

  • Developing more sophisticated culture systems that better mimic the in vivo niche.
  • Standardizing protocols to improve reproducibility across different laboratories.
  • Exploring new applications of organoids in personalized medicine and regenerative therapies.

This Primer serves as a foundational reference for researchers in the field, guiding the optimization and application of organoids in biomedical research.

References ​

  1. Engineering human islet organoids from iPSCs using an organ-on-chip platform. - Tingting Tao;Yaqing Wang;Wenwen Chen;Zhongyu Li;Wentao Su;Yaqiong Guo;Pengwei Deng;Jianhua Qin - Lab on a chip (2019)
  2. Detection of CFTR function and modulation in primary human nasal cell spheroids. - John J Brewington;Erin T Filbrandt;F J LaRosa;Alicia J Ostmann;Lauren M Strecker;Rhonda D Szczesniak;John P Clancy - Journal of cystic fibrosis : official journal of the European Cystic Fibrosis Society (2018)
  3. Expansion of Adult Human Pancreatic Tissue Yields Organoids Harboring Progenitor Cells with Endocrine Differentiation Potential. - Cindy J M Loomans;Nerys Williams Giuliani;Jeetindra Balak;Femke Ringnalda;Léon van Gurp;Meritxell Huch;Sylvia F Boj;Toshiro Sato;Lennart Kester;Susana M Chuva de Sousa Lopes;Matthias S Roost;Susan Bonner-Weir;Marten A Engelse;Ton J Rabelink;Harry Heimberg;Robert G J Vries;Alexander van Oudenaarden;Françoise Carlotti;Hans Clevers;Eelco J P de Koning - Stem cell reports (2018)
  4. Modelling Cryptosporidium infection in human small intestinal and lung organoids. - Inha Heo;Devanjali Dutta;Deborah A Schaefer;Nino Iakobachvili;Benedetta Artegiani;Norman Sachs;Kim E Boonekamp;Gregory Bowden;Antoni P A Hendrickx;Robert J L Willems;Peter J Peters;Michael W Riggs;Roberta O'Connor;Hans Clevers - Nature microbiology (2018)
  5. Non-genetic engineering of cells for drug delivery and cell-based therapy. - Qun Wang;Hao Cheng;Haisheng Peng;Hao Zhou;Peter Y Li;Robert Langer - Advanced drug delivery reviews (2015)
  6. Overlooked? Underestimated? Effects of Substrate Curvature on Cell Behavior. - Danielle Baptista;Liliana Teixeira;Clemens van Blitterswijk;Stefan Giselbrecht;Roman Truckenmüller - Trends in biotechnology (2019)
  7. In vitro expansion of single Lgr5+ liver stem cells induced by Wnt-driven regeneration. - Meritxell Huch;Craig Dorrell;Sylvia F Boj;Johan H van Es;Vivian S W Li;Marc van de Wetering;Toshiro Sato;Karien Hamer;Nobuo Sasaki;Milton J Finegold;Annelise Haft;Robert G Vries;Markus Grompe;Hans Clevers - Nature (2013)
  8. Integrative multi-omics analysis of intestinal organoid differentiation. - Rik Gh Lindeboom;Lisa van Voorthuijsen;Koen C Oost;Maria J Rodríguez-Colman;Maria V Luna-Velez;Cristina Furlan;Floriane Baraille;Pascal Wtc Jansen;Agnès Ribeiro;Boudewijn Mt Burgering;Hugo J Snippert;Michiel Vermeulen - Molecular systems biology (2018)
  9. Beyond bar and line graphs: time for a new data presentation paradigm. - Tracey L Weissgerber;Natasa M Milic;Stacey J Winham;Vesna D Garovic - PLoS biology (2015)
  10. Organoid cultures derived from patients with advanced prostate cancer. - Dong Gao;Ian Vela;Andrea Sboner;Phillip J Iaquinta;Wouter R Karthaus;Anuradha Gopalan;Catherine Dowling;Jackline N Wanjala;Eva A Undvall;Vivek K Arora;John Wongvipat;Myriam Kossai;Sinan Ramazanoglu;Luendreo P Barboza;Wei Di;Zhen Cao;Qi Fan Zhang;Inna Sirota;Leili Ran;Theresa Y MacDonald;Himisha Beltran;Juan-Miguel Mosquera;Karim A Touijer;Peter T Scardino;Vincent P Laudone;Kristen R Curtis;Dana E Rathkopf;Michael J Morris;Daniel C Danila;Susan F Slovin;Stephen B Solomon;James A Eastham;Ping Chi;Brett Carver;Mark A Rubin;Howard I Scher;Hans Clevers;Charles L Sawyers;Yu Chen - Cell (2014)

Literatures Citing This Work ​

  1. Patient-Derived Organoids: The Beginning of a New Era in Ovarian Cancer Disease Modeling and Drug Sensitivity Testing. - Iason Psilopatis;Alexandros G Sykaras;Georgios Mandrakis;Kleio Vrettou;Stamatios Theocharis - Biomedicines (2022)
  2. Human Brain Organoids in Migraine Research: Pathogenesis and Drug Development. - Parisa Gazerani - International journal of molecular sciences (2023)
  3. A Beginner's Guide to Cell Culture: Practical Advice for Preventing Needless Problems. - Sabine Weiskirchen;Sarah K Schröder;Eva Miriam Buhl;Ralf Weiskirchen - Cells (2023)
  4. Primary human organoids models: Current progress and key milestones. - Giuseppe Calà;Beatrice Sina;Paolo De Coppi;Giovanni Giuseppe Giobbe;Mattia Francesco Maria Gerli - Frontiers in bioengineering and biotechnology (2023)
  5. Revolutionizing Disease Modeling: The Emergence of Organoids in Cellular Systems. - Rita Silva-Pedrosa;António José Salgado;Pedro Eduardo Ferreira - Cells (2023)
  6. Advanced In Vitro Three-Dimensional Skin Models of Atopic Dermatitis. - Hye-Jeong Jang;Jung Bok Lee;Jeong-Kee Yoon - Tissue engineering and regenerative medicine (2023)
  7. Patient Derived Organoids (PDOs), Extracellular Matrix (ECM), Tumor Microenvironment (TME) and Drug Screening: State of the Art and Clinical Implications of Ovarian Cancer Organoids in the Era of Precision Medicine. - Giulia Spagnol;Francesca Sensi;Orazio De Tommasi;Matteo Marchetti;Giulio Bonaldo;Livia Xhindoli;Marco Noventa;Marco Agostini;Roberto Tozzi;Carlo Saccardi - Cancers (2023)
  8. Three-Dimensional Bioprinting of Organoid-Based Scaffolds (OBST) for Long-Term Nanoparticle Toxicology Investigation. - Amparo Guerrero Gerbolés;Maricla Galetti;Stefano Rossi;Francesco Paolo Lo Muzio;Silvana Pinelli;Nicola Delmonte;Cristina Caffarra Malvezzi;Claudio Macaluso;Michele Miragoli;Ruben Foresti - International journal of molecular sciences (2023)
  9. Opportunities and challenges to engineer 3D models of tumor-adaptive immune interactions. - Rahul M Visalakshan;Mary K Lowrey;Mauricio G C Sousa;Haylie R Helms;Abrar Samiea;Carolyn E Schutt;Josh M Moreau;Luiz E Bertassoni - Frontiers in immunology (2023)
  10. iPSC-derived three-dimensional brain organoid models and neurotropic viral infections. - Michael Swingler;Martina Donadoni;Anna Bellizzi;Senem Cakir;Ilker K Sariyer - Journal of neurovirology (2023)

... (338 more literatures)

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