Human organoids: model systems for human biology and medicine

Kim, Jihoon; Koo, Bon-Kyoung; Knoblich, Juergen A.

doi:10.1038/s41580-020-0259-3

Cited by 2,187Pluripotent Stem Cells Research3D Printing in Biomedical ResearchCancer Cells and Metastasis

Human organoids: model systems for human biology and medicine

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Kim, Jihoon, Koo, Bon-Kyoung, Knoblich, Juergen A.·2020·Nature Reviews Molecular Cell Biology

DOI 10.1038/s41580-020-0259-3PMC PMC7339799

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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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Several patient-derived organoid models, including pancreas, colorectal, and liver cancer, exhibit heterogeneous responses to known chemotherapeutic and anticancer agents.
“In particular, for cancer treatment, several different patient-derived organoid models tested, including but not limited to: pancreas, colorectal and liver cancer all exhibit heterogeneous responses to known chemotherapeutic and anticancer agents49,132,212.”
From Organoids (2022) · cites this paper as [212]
The cancer-organoid discussion (section labelled “Box 2 | Human organoids and SARS-coronavirus 2”; page unavailable) identifies models derived from colon, pancreatic and liver cancers and describes differing drug activity in matched cancer organoids. The References list drug-screening studies for these cancers, but the review does not establish that organoids from each of the three cancer types exhibited heterogeneous responses to chemotherapeutic or anticancer agents. (LLM, conf=0.83)
Experimental — accuracy not yet measured
Human brain organoids can fully replicate human biology and potentially reduce translational barriers from experimental findings to therapeutic applications.
“Meanwhile, being entirely derived from human cells, these organoids can fully replicate human biology and potentially reduce the translational barriers from experimental findings to therapeutic applications (20–22), offering advantages over animal models (23–25).”
From Understanding monocyte-driven neuroinflammation in Alzheimer’s disease using human cortical organoid microphysiological systems (2025) · cites this paper as [20]
The ‘Bridging the gap between animal models and humans’ section says human organoids may represent human tissue more accurately than animal models, and the Conclusions describe their potential in clinical translational research. But ‘Assessing interactions with other organs and the environment’ says organoids mimic only part of the human body, so the claim that brain organoids can fully replicate human biology overstates the source. Page numbers are unavailable in our copy. (LLM, conf=0.90)
Experimental — accuracy not yet measured
The versatile skin OTC-based platform is ideally suited for investigating a broad range of physiological and pathological scenarios, with significant potential for advancing understanding of skin developmental biology, disease modeling, and regenerative medicine.
“The versatile skin OTC-based platform is ideally suited for investigating a broad range of physiological and pathological scenarios, presenting significant potential for advancing our understanding of skin developmental biology, disease modeling, and applications in regenerative medicine [69–71].”
From Diversity of human skin three-dimensional organotypic cultures (2024) · cites this paper as [71]
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Modelling human hepato-biliary-pancreatic organogenesis from the foregut–midgut boundary
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Pluripotent stem cell-derived organoids: using principles of developmental biology to grow human tissues in a dish
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Epigenetic resetting of human pluripotency
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Differentiated human airway organoids to assess infectivity of emerging influenza virus
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Organoid cultures recapitulate esophageal adenocarcinoma heterogeneity providing a model for clonality studies and precision therapeutics
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DNA Methylation and Transcription Patterns in Intestinal Epithelial Cells From Pediatric Patients With Inflammatory Bowel Diseases Differentiate Disease Subtypes and Associate With Outcome
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Rectal Organoids Enable Personalized Treatment of Cystic Fibrosis
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Dishing out mini-brains: Current progress and future prospects in brain organoid research
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Human embryonic stem cells: research, ethics and policy
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Reconstruction of the mouse extrahepatic biliary tree using primary human extrahepatic cholangiocyte organoids
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Growth of Epithelial Organoids in a Defined Hydrogel
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A novel human gastric primary cell culture system for modelling Helicobacter pylori infection in vitro
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Wnt/β-catenin promotes gastric fundus specification in mice and humans
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Pooled In Vitro and In Vivo CRISPR-Cas9 Screening Identifies Tumor Suppressors in Human Colon Organoids
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Human iPSC banking: barriers and opportunities
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Alterations in the epithelial stem cell compartment could contribute to permanent changes in the mucosa of patients with ulcerative colitis
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Human Fetal TNF-α-Cytokine-Producing CD4+ Effector Memory T Cells Promote Intestinal Development and Mediate Inflammation Early in Life
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Zika-Virus-Encoded NS2A Disrupts Mammalian Cortical Neurogenesis by Degrading Adherens Junction Proteins
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Organoid and Assembloid Technologies for Investigating Cellular Crosstalk in Human Brain Development and Disease.
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Genome-Scale CRISPR Screening in Human Intestinal Organoids Identifies Drivers of TGF-β Resistance
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Human kidney organoids: progress and remaining challenges
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Validated germline-competent embryonic stem cell lines from nonobese diabetic mice
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Modeling rotavirus infection and antiviral therapy using primary intestinal organoids
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Co-culture with intestinal epithelial organoids allows efficient expansion and motility analysis of intraepithelial lymphocytes
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Epidemiology of human noroviruses and updates on vaccine development
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DNA methylation defines regional identity of human intestinal epithelial organoids and undergoes dynamic changes during development
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PEG-4MAL hydrogels for human organoid generation, culture, and in vivo delivery
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Esophageal Organoids from Human Pluripotent Stem Cells Delineate Sox2 Functions during Esophageal Specification
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Expansion of Adult Human Pancreatic Tissue Yields Organoids Harboring Progenitor Cells with Endocrine Differentiation Potential
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Stem Cells, Genome Editing, and the Path to Translational Medicine
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A Primary Human Macrophage-Enteroid Co-Culture Model to Investigate Mucosal Gut Physiology and Host-Pathogen Interactions
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Systematic Identification of Culture Conditions for Induction and Maintenance of Naive Human Pluripotency
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Modeling infectious diseases and host-microbe interactions in gastrointestinal organoids
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Mechanically and chemically defined hydrogel matrices for patient-derived colorectal tumor organoid culture
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The worm in us – Caenorhabditis elegans as a model of human disease
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Mesenchymal Stem Cells Increase Alveolar Differentiation in Lung Progenitor Organoid Cultures
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3D Modeling of Esophageal Development using Human PSC-Derived Basal Progenitors Reveals a Critical Role for Notch Signaling
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The zebrafish issue ofDevelopment
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Single cell analysis of Crohn’s disease patient-derived small intestinal organoids reveals disease activity-dependent modification of stem cell properties
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One-step generation of conditional and reversible gene knockouts
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Development of Collagen-Based 3D Matrix for Gastrointestinal Tract-Derived Organoid Culture
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Organoid models for translational pancreatic cancer research
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A critical look: challenges in differentiating human pluripotent stem cells into desired cell-types and organoids
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Patient-Derived Colorectal Cancer Organoids Upregulate Revival Stem Cell Marker Genes following Chemotherapeutic Treatment
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Gene Targeting in Human Pluripotent CellsPreprint
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Understanding the role of steroids in typical and atypical brain development: Advantages of using a “brain in a dish” approach
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In this review, Huch and Koo summarize the development of various organoid culture systems and compare mouse and human systems.

Sorted by citations

Engineering organoids
Hofer, M., & Lutolf, M. P. (2021) · Nature Reviews Materials · doi:10.1038/s41578-021-00279-y · Cited by 1,184 · see citing works
Organoids
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Towards organoid culture without Matrigel
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Detection of Viral Infections by Innate Immunity
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Building consensus on definition and nomenclature of hepatic, pancreatic, and biliary organoids
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Human cerebral organoids — a new tool for clinical neurology research
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Volumetric Bioprinting of Organoids and Optically Tuned Hydrogels to Build Liver‐Like Metabolic Biofactories
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Tumor organoids: applications in cancer modeling and potentials in precision medicine
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BANKSY unifies cell typing and tissue domain segmentation for scalable spatial omics data analysis
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Organoids: The current status and biomedical applications
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Decellularization in Tissue Engineering and Regenerative Medicine: Evaluation, Modification, and Application Methods
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Cell Therapy: Types, Regulation, and Clinical Benefits
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Glycometabolic reprogramming-induced XRCC1 lactylation confers therapeutic resistance in ALDH1A3-overexpressing glioblastoma
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Physiological and pathological roles of lipogenesis
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Human neural tube morphogenesis in vitro by geometric constraints
Karzbrun, E., Khankhel, A. H., Megale, H. C., Glasauer, S. M. K., Wyle, Y., Britton, G., Warmflash, A., Kosik, K. S., Siggia, E. D., Shraiman, B. I., et al. (2021) · Nature · doi:10.1038/s41586-021-04026-9 · Cited by 246 · see citing works
Patient-derived tumor organoids: a new avenue for preclinical research and precision medicine in oncology
Thorel, L., Perréard, M., Florent, R., Divoux, J., Coffy, S., Vincent, A., Gaggioli, C., Guasch, G., Gidrol, X., Weiswald, L., et al. (2024) · Experimental & Molecular Medicine · doi:10.1038/s12276-024-01272-5 · Cited by 228 · see citing works
Organoids and organs-on-chips: Insights into human gut-microbe interactions
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Radiotherapy as a tool to elicit clinically actionable signalling pathways in cancer
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Organoids: a systematic review of ethical issues
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Microplastics in the human digestive environment: A focus on the potential and challenges facing in vitro gut model development
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Lineage recording in human cerebral organoids
He, Z., Maynard, A., Jain, A., Gerber, T., Petri, R., Lin, H., Santel, M., Ly, K. C. H., Dupré, J.-S., Sidow, L., et al. (2021) · Nature Methods · doi:10.1038/s41592-021-01344-8 · Cited by 204 · see citing works
Engineering neurovascular organoids with 3D printed microfluidic chips
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Self-citation

Authors: Kim, J., Koo, B.-K., & Knoblich, J. A.
Affiliations: Institute of Molecular Biotechnology (AT)
Corresponding author: Koo, Bon-Kyoung
Knoblich, Juergen A.
ORCID: Kim, Jihoon
Koo, Bon-Kyoung
Knoblich, Juergen A.
Venue: Nature Reviews Molecular Cell Biology
Publisher: Springer Science and Business Media LLC
Published: 2020-07-07
Volume: 21
Issue: 10
Pages: 571-584
ISSN: 1471-0072 (ISSN-L)
1471-0080
DOI: 10.1038/s41580-020-0259-3
PMC: PMC7339799
OpenAlex: W3040646360
Cited by: 2,187
References: 210
Citations by year: 2026: 311 · 2025: 410 · 2024: 409 · 2023: 381 · 2022: 352 · 2021: 291 · 2020: 31
FWCI: 25.25
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Nature Reviews Molecular Cell Biology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Österreichischen Akademie der Wissenschaften
Austrian Science Fund (Z_153_B09)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Keywords: human organoids, stem cell-derived organoids, alternative to animal models, disease modeling, organogenesis, infectious diseases, genetic disorders, tumor models, patient-derived organoids, drug discovery
MeSH terms: Animals, Biology, Communicable Diseases, Genetic Engineering, Humans, Medicine, Neoplasms, Organoids, Stem Cells, Genetic Diseases, Inborn

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Human organoids: model systems for human biology and medicine

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