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

Human organoids: model systems for human biology and medicine. ​

Literature Information ​

DOI10.1038/s41580-020-0259-3
PMID32636524
JournalNature reviews. Molecular cell biology
Impact Factor90.2
JCR QuartileQ1
Publication Year2020
Times Cited935
Keywordshuman organoids, biomedicine, disease models, stem cells, 3D culture systems
Literature TypeJournal Article, Research Support, Non-U.S. Gov't, Review
ISSN1471-0072
Pages571-584
Issue21(10)
AuthorsJihoon Kim, Bon-Kyoung Koo, Juergen A Knoblich

TL;DR ​

This review highlights the emerging role of human organoids—stem cell-derived 3D culture systems—as powerful models for studying human biology and disease, addressing limitations of traditional animal models. By facilitating research on infectious diseases, genetic disorders, and cancers through patient-derived samples, organoids offer significant advantages, although challenges remain in their widespread adoption for reducing animal experimentation.

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human organoids · biomedicine · disease models · stem cells · 3D culture systems

Abstract ​

The historical reliance of biological research on the use of animal models has sometimes made it challenging to address questions that are specific to the understanding of human biology and disease. But with the advent of human organoids - which are stem cell-derived 3D culture systems - it is now possible to re-create the architecture and physiology of human organs in remarkable detail. Human organoids provide unique opportunities for the study of human disease and complement animal models. Human organoids have been used to study infectious diseases, genetic disorders and cancers through the genetic engineering of human stem cells, as well as directly when organoids are generated from patient biopsy samples. This Review discusses the applications, advantages and disadvantages of human organoids as models of development and disease and outlines the challenges that have to be overcome for organoids to be able to substantially reduce the need for animal experiments.

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Primary Questions Addressed ​

  1. How do human organoids compare to traditional animal models in terms of replicating human-specific disease mechanisms?
  2. What are the potential ethical implications of using human organoids in biomedical research?
  3. In what ways can organoids derived from patient samples enhance personalized medicine approaches?
  4. What are the current limitations of human organoids in modeling complex organ systems or multi-organ interactions?
  5. How might advancements in organoid technology impact drug discovery and development processes?

Key Findings ​

Research Background and Purpose ​

The reliance on animal models in biomedical research has often hindered the understanding of human-specific biology and diseases. Human organoids, derived from stem cells, present a promising alternative that can replicate the architecture and function of human organs in vitro. This review explores the applications, advantages, and limitations of human organoids in modeling human development and diseases, emphasizing their potential to reduce the need for animal experimentation.

Main Methods/Materials/Experimental Design ​

Human organoids can be generated from both pluripotent stem cells (PSCs) and adult stem cells (AdSCs). The process typically involves three main steps:

  1. Germ Layer Specification: PSCs are directed to differentiate into endoderm, mesoderm, or ectoderm.
  2. Induction and Maturation: Cells are cultured with specific growth factors and signaling molecules to achieve the desired organ type.
  3. 3D Culture: Organoids are formed and maintained in a three-dimensional matrix to promote physiological complexity.
Mermaid diagram

Key Results and Findings ​

  • Modeling Human Diseases: Organoids have been successfully used to model various diseases, including infectious diseases (e.g., Zika virus), genetic disorders (e.g., cystic fibrosis), and cancers. They provide a platform for drug testing and understanding disease mechanisms.
  • Personalized Medicine: Patient-derived organoids allow for tailored therapeutic approaches by assessing drug responses specific to an individual's genetic makeup.
  • Genetic Engineering: The integration of CRISPR technology with organoid systems enables precise genetic modifications, facilitating the study of gene functions and disease pathways.

Main Conclusions/Significance/Innovation ​

Human organoids represent a significant advancement in biomedical research, offering a more accurate representation of human physiology compared to traditional animal models. They enable researchers to explore human-specific biological processes and diseases, potentially leading to breakthroughs in personalized medicine and therapeutic interventions.

Research Limitations and Future Directions ​

Despite their promise, organoid technology faces several challenges:

  • Standardization: There is a lack of universally accepted protocols for organoid generation and maintenance, leading to variability in results across studies.
  • Complexity: While organoids can model specific tissues, they do not replicate the interactions between different organ systems, limiting their application in studying systemic diseases.
  • Microenvironment: The absence of a fully functional microenvironment in organoid cultures may affect their physiological relevance.

Future research should focus on improving the complexity of organoid systems, establishing standardized protocols, and integrating organoids with organ-on-a-chip technologies to better mimic human biology and inter-organ communication.

References ​

  1. Progress and potential in organoid research. - Giuliana Rossi;Andrea Manfrin;Matthias P Lutolf - Nature reviews. Genetics (2018)
  2. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. - Toshiro Sato;Daniel E Stange;Marc Ferrante;Robert G J Vries;Johan H Van Es;Stieneke Van den Brink;Winan J Van Houdt;Apollo Pronk;Joost Van Gorp;Peter D Siersema;Hans Clevers - Gastroenterology (2011)
  3. Human Intestinal Organoids Maintain Self-Renewal Capacity and Cellular Diversity in Niche-Inspired Culture Condition. - Masayuki Fujii;Mami Matano;Kohta Toshimitsu;Ai Takano;Yohei Mikami;Shingo Nishikori;Shinya Sugimoto;Toshiro Sato - Cell stem cell (2018)
  4. Cerebral organoids model human brain development and microcephaly. - Madeline A Lancaster;Magdalena Renner;Carol-Anne Martin;Daniel Wenzel;Louise S Bicknell;Matthew E Hurles;Tessa Homfray;Josef M Penninger;Andrew P Jackson;Juergen A Knoblich - Nature (2013)
  5. Kidney organoids from human iPS cells contain multiple lineages and model human nephrogenesis. - Minoru Takasato;Pei X Er;Han S Chiu;Barbara Maier;Gregory J Baillie;Charles Ferguson;Robert G Parton;Ernst J Wolvetang;Matthias S Roost;Susana M Chuva de Sousa Lopes;Melissa H Little - Nature (2015)
  6. Long-Term Expansion of Functional Mouse and Human Hepatocytes as 3D Organoids. - Huili Hu;Helmuth Gehart;Benedetta Artegiani;Carmen LÖpez-Iglesias;Florijn Dekkers;Onur Basak;Johan van Es;Susana M Chuva de Sousa Lopes;Harry Begthel;Jeroen Korving;Maaike van den Born;Chenhui Zou;Corrine Quirk;Luis Chiriboga;Charles M Rice;Stephanie Ma;Anne Rios;Peter J Peters;Ype P de Jong;Hans Clevers - Cell (2018)
  7. Long-term, hormone-responsive organoid cultures of human endometrium in a chemically defined medium. - Margherita Y Turco;Lucy Gardner;Jasmine Hughes;Tereza Cindrova-Davies;Maria J Gomez;Lydia Farrell;Michael Hollinshead;Steven G E Marsh;Jan J Brosens;Hilary O Critchley;Benjamin D Simons;Myriam Hemberger;Bon-Kyoung Koo;Ashley Moffett;Graham J Burton - Nature cell biology (2017)
  8. Modeling mouse and human development using organoid cultures. - Meritxell Huch;Bon-Kyoung Koo - Development (Cambridge, England) (2015)
  9. Organoids: A historical perspective of thinking in three dimensions. - Marina Simian;Mina J Bissell - The Journal of cell biology (2017)
  10. Organogenesis in a dish: modeling development and disease using organoid technologies. - Madeline A Lancaster;Juergen A Knoblich - Science (New York, N.Y.) (2014)

Literatures Citing This Work ​

  1. Integrating Biosensors in Organs-on-Chip Devices: A Perspective on Current Strategies to Monitor Microphysiological Systems. - Erika Ferrari;Cecilia Palma;Simone Vesentini;Paola Occhetta;Marco Rasponi - Biosensors (2020)
  2. Patient-Derived Xenograft vs. Organoids: A Preliminary Analysis of Cancer Research Output, Funding and Human Health Impact in 2014-2019. - Lindsay J Marshall;Marcia Triunfol;Troy Seidle - Animals : an open access journal from MDPI (2020)
  3. Hijacking of Lipid Droplets by Hepatitis C, Dengue and Zika Viruses-From Viral Protein Moonlighting to Extracellular Release. - Alexandra P M Cloherty;Andrea D Olmstead;Carla M S Ribeiro;François Jean - International journal of molecular sciences (2020)
  4. COVID-19 lessons from the dish: Dissecting CNS manifestations through brain organoids. - Nicolò Caporale;Giuseppe Testa - The EMBO journal (2021)
  5. Synthetic Biology Approaches in The Development of Engineered Therapeutic Microbes. - Minjeong Kang;Donghui Choe;Kangsan Kim;Byung-Kwan Cho;Suhyung Cho - International journal of molecular sciences (2020)
  6. A Perspective on Organoids for Virology Research. - Adithya Sridhar;Salvatore Simmini;Carla M S Ribeiro;Caroline Tapparel;Melvin M Evers;Dasja Pajkrt;Katja Wolthers - Viruses (2020)
  7. Understanding and Treating Niemann-Pick Type C Disease: Models Matter. - Valentina Pallottini;Frank W Pfrieger - International journal of molecular sciences (2020)
  8. Trends and challenges in modeling glioma using 3D human brain organoids. - Aruljothi Mariappan;Gladiola Goranci-Buzhala;Lucia Ricci-Vitiani;Roberto Pallini;Jay Gopalakrishnan - Cell death and differentiation (2021)
  9. Patient-Derived Tumor Organoids for Drug Repositioning in Cancer Care: A Promising Approach in the Era of Tailored Treatment. - Silvia Vivarelli;Saverio Candido;Giuseppe Caruso;Luca Falzone;Massimo Libra - Cancers (2020)
  10. Extracellular Matrix Mechanical Properties and Regulation of the Intestinal Stem Cells: When Mechanics Control Fate. - Lauriane Onfroy-Roy;Dimitri Hamel;Julie Foncy;Laurent Malaquin;Audrey Ferrand - Cells (2020)

... (925 more literatures)

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