Curated Papers > High-impact authoritative literature on "organoids"

Organoid culture systems to study host-pathogen interactions.

Literature Information

DOI	10.1016/j.coi.2017.07.012
PMID	28756233
Journal	Current opinion in immunology
Impact Factor	5.8
JCR Quartile	Q1
Publication Year	2017
Times Cited	102
Keywords	Organoid culture, Host-microbe interactions, Viral infection, Bacterial infection, Microbe co-culture
Literature Type	Journal Article, Review
ISSN	0952-7915
Pages	15-22
Issue	48()
Authors	Devanjali Dutta, Hans Clevers

TL;DR

This paper reviews recent advancements in host-microbe interaction studies using organoid cultures, emphasizing their utility in modeling infections like Zika virus and various bacterial and viral pathogens. The findings underscore the potential of these refined systems to deepen our understanding of microbial colonization and its links to diseases such as cancer, paving the way for innovative research approaches in microbiology and pathology.

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Organoid culture · Host-microbe interactions · Viral infection · Bacterial infection · Microbe co-culture

Abstract

Recent advances in host-microbe interaction studies in organoid cultures have shown great promise and have laid the foundation for much more refined future studies using these systems. Modeling of Zika virus (ZIKV) infection in cerebral organoids have helped us understand its association with microcephaly. Similarly, the pathogenesis of bacterial (Helicobacter pylori, Clostridium difficile) and viral (Norovirus, Rotaviruses) infections have been precisely dissected in organoid cultures. Additionally, direct associations between microbial colonization of tissues and diseases like cancer have also been deciphered. Here we discuss the most recent and striking studies on host-microbe interactions in organoid cultures, highlighting various methods which can be used for developing microbe-organoid co-culture systems.

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Primary Questions Addressed

1. What are the specific advantages of using organoid cultures over traditional cell culture methods in studying host-pathogen interactions?
2. How can organoid culture systems be optimized to better mimic the in vivo environment for studying various pathogens?
3. What are the limitations of current organoid models in understanding complex host-pathogen interactions, and how can future research address these?
4. In what ways can the findings from organoid studies on pathogens like Zika virus and Helicobacter pylori inform clinical practices or therapeutic strategies?
5. How do different types of organoid cultures (e.g., intestinal, cerebral) influence the outcomes of host-pathogen interaction studies?

Key Findings

Research Background and Objectives

Recent advancements in host-microbe interaction studies utilizing organoid cultures have opened new avenues for understanding complex biological processes. The primary objective of this research is to explore how organoid models can be used to investigate the interactions between microbes and host tissues, particularly in the context of infections and diseases such as Zika virus (ZIKV) infection, gastrointestinal infections, and cancer.

Main Methods/Materials/Experimental Design

The research emphasizes various methodologies employed in developing microbe-organoid co-culture systems. These methods enable the modeling of host-microbe interactions with a focus on specific pathogens. The following flowchart illustrates the technical approach used in these studies:

1. Organoid Culture Development: Establishing organoid cultures from human tissues to serve as a model for studying host responses.
2. Infection with Pathogens: Introducing specific pathogens (e.g., ZIKV, Helicobacter pylori, Clostridium difficile) into the organoid cultures.
3. Microbial Colonization Assessment: Evaluating the extent and nature of microbial colonization within the organoids.
4. Pathogenesis Analysis: Investigating the mechanisms by which these microbes induce disease states or alter host physiology.
5. Disease Association Studies: Linking microbial interactions to diseases such as microcephaly and gastrointestinal disorders.
6. Data Interpretation and Insights: Drawing conclusions based on experimental results to inform future research directions.

Key Results and Findings

• Zika Virus and Microcephaly: Studies using cerebral organoids have demonstrated a clear association between ZIKV infection and the development of microcephaly, providing insights into the virus's impact on neural development.
• Bacterial and Viral Pathogenesis: The research has successfully dissected the pathogenic mechanisms of various bacteria (e.g., Helicobacter pylori, Clostridium difficile) and viruses (e.g., Norovirus, Rotaviruses) within organoid models.
• Microbial Colonization and Cancer: Direct links between microbial colonization of tissues and the onset of cancer have been established, indicating a potential area for therapeutic intervention.

Main Conclusions/Significance/Innovativeness

The studies underscore the potential of organoid cultures as powerful tools for modeling host-microbe interactions. They provide significant insights into the pathogenesis of infections and the role of microbes in various diseases. The innovative use of organoid systems allows for a more nuanced understanding of these interactions, paving the way for the development of targeted therapies and preventive strategies.

Research Limitations and Future Directions

While the findings are promising, there are several limitations to consider:

• Model Limitations: Organoid models may not fully replicate the complexity of in vivo systems, potentially limiting the generalizability of results.
• Pathogen Diversity: The studies primarily focus on a select few pathogens, which may not represent the full spectrum of microbial interactions in human health and disease.

Future Directions:

• Expanding the range of pathogens studied within organoid systems to include more diverse microbial communities.
• Enhancing the complexity of organoid cultures to better mimic the physiological environment of human tissues.
• Investigating the therapeutic potential of modulating host-microbe interactions to prevent or treat diseases.

By addressing these limitations and exploring new avenues, future research can further elucidate the critical roles that microbes play in health and disease.

References

1. Modeling rotavirus infection and antiviral therapy using primary intestinal organoids. - Yuebang Yin;Marcel Bijvelds;Wen Dang;Lei Xu;Annemiek A van der Eijk;Karen Knipping;Nesrin Tuysuz;Johanna F Dekkers;Yijin Wang;Jeroen de Jonge;Dave Sprengers;Luc J W van der Laan;Jeffrey M Beekman;Derk Ten Berge;Herold J Metselaar;Hugo de Jonge;Marion P G Koopmans;Maikel P Peppelenbosch;Qiuwei Pan - Antiviral research (2015)
2. Paneth cell extrusion and release of antimicrobial products is directly controlled by immune cell-derived IFN-γ. - Henner F Farin;Wouter R Karthaus;Pekka Kujala;Maryam Rakhshandehroo;Gerald Schwank;Robert G J Vries;Eric Kalkhoven;Edward E S Nieuwenhuis;Hans Clevers - The Journal of experimental medicine (2014)
3. Drosophila as a model for homeostatic, antibacterial, and antiviral mechanisms in the gut. - Xi Liu;Jeffrey J Hodgson;Nicolas Buchon - PLoS pathogens (2017)
4. Age-Associated Microbial Dysbiosis Promotes Intestinal Permeability, Systemic Inflammation, and Macrophage Dysfunction. - Netusha Thevaranjan;Alicja Puchta;Christian Schulz;Avee Naidoo;J C Szamosi;Chris P Verschoor;Dessi Loukov;Louis P Schenck;Jennifer Jury;Kevin P Foley;Jonathan D Schertzer;Maggie J Larché;Donald J Davidson;Elena F Verdú;Michael G Surette;Dawn M E Bowdish - Cell host & microbe (2017)
5. Influence of human immunodeficiency virus infection on the course of hepatitis C virus infection: a meta-analysis. - C S Graham;L R Baden;E Yu;J M Mrus;J Carnie;T Heeren;M J Koziel - Clinical infectious diseases : an official publication of the Infectious Diseases Society of America (2001)
6. Salmonella Manipulation of Host Signaling Pathways Provokes Cellular Transformation Associated with Gallbladder Carcinoma. - Tiziana Scanu;Robbert M Spaapen;Jeroen M Bakker;Chandra Bhan Pratap;Lin-en Wu;Ingrid Hofland;Annegien Broeks;Vijay Kumar Shukla;Mohan Kumar;Hans Janssen;Ji-Ying Song;E Andra Neefjes-Borst;Hein te Riele;David W Holden;Gopal Nath;Jacques Neefjes - Cell host & microbe (2015)
7. An in vivo model of human small intestine using pluripotent stem cells. - Carey L Watson;Maxime M Mahe;Jorge Múnera;Jonathan C Howell;Nambirajan Sundaram;Holly M Poling;Jamie I Schweitzer;Jefferson E Vallance;Christopher N Mayhew;Ying Sun;Gregory Grabowski;Stacy R Finkbeiner;Jason R Spence;Noah F Shroyer;James M Wells;Michael A Helmrath - Nature medicine (2014)
8. In vitro generation of human pluripotent stem cell derived lung organoids. - Briana R Dye;David R Hill;Michael A H Ferguson;Yu-Hwai Tsai;Melinda S Nagy;Rachel Dyal;James M Wells;Christopher N Mayhew;Roy Nattiv;Ophir D Klein;Eric S White;Gail H Deutsch;Jason R Spence - eLife (2015)
9. Persistence and toxin production by Clostridium difficile within human intestinal organoids result in disruption of epithelial paracellular barrier function. - Jhansi L Leslie;Sha Huang;Judith S Opp;Melinda S Nagy;Masayuki Kobayashi;Vincent B Young;Jason R Spence - Infection and immunity (2015)
10. Zika virus impairs growth in human neurospheres and brain organoids. - Patricia P Garcez;Erick Correia Loiola;Rodrigo Madeiro da Costa;Luiza M Higa;Pablo Trindade;Rodrigo Delvecchio;Juliana Minardi Nascimento;Rodrigo Brindeiro;Amilcar Tanuri;Stevens K Rehen - Science (New York, N.Y.) (2016)

Literatures Citing This Work

1. The Use of Ex Vivo Organ Cultures in Tick-Borne Virus Research. - Jeffrey M Grabowski;Danielle K Offerdahl;Marshall E Bloom - ACS infectious diseases (2018)
2. Human organoid cultures: transformative new tools for human virus studies. - Sasirekha Ramani;Sue E Crawford;Sarah E Blutt;Mary K Estes - Current opinion in virology (2018)
3. Basal interferon signaling and therapeutic use of interferons in controlling rotavirus infection in human intestinal cells and organoids. - Mohamad S Hakim;Sunrui Chen;Shihao Ding;Yuebang Yin;Aqsa Ikram;Xiao-Xia Ma;Wenshi Wang;Maikel P Peppelenbosch;Qiuwei Pan - Scientific reports (2018)
4. Human Intestinal Enteroids for the Study of Bacterial Adherence, Invasion, and Translocation. - Nina M Poole;Anubama Rajan;Anthony W Maresso - Current protocols in microbiology (2018)
5. Modeling Host-Pathogen Interactions in the Context of the Microenvironment: Three-Dimensional Cell Culture Comes of Age. - Jennifer Barrila;Aurélie Crabbé;Jiseon Yang;Karla Franco;Seth D Nydam;Rebecca J Forsyth;Richard R Davis;Sandhya Gangaraju;C Mark Ott;Carolyn B Coyne;Mina J Bissell;Cheryl A Nickerson - Infection and immunity (2018)
6. Potential application of cell reprogramming techniques for cancer research. - Shigeo Saito;Ying-Chu Lin;Yukio Nakamura;Richard Eckner;Kenly Wuputra;Kung-Kai Kuo;Chang-Shen Lin;Kazunari K Yokoyama - Cellular and molecular life sciences : CMLS (2019)
7. Microglia innately develop within cerebral organoids. - Paul R Ormel;Renata Vieira de Sá;Emma J van Bodegraven;Henk Karst;Oliver Harschnitz;Marjolein A M Sneeboer;Lill Eva Johansen;Roland E van Dijk;Nicky Scheefhals;Amber Berdenis van Berlekom;Eduardo Ribes Martínez;Sandra Kling;Harold D MacGillavry;Leonard H van den Berg;René S Kahn;Elly M Hol;Lot D de Witte;R Jeroen Pasterkamp - Nature communications (2018)
8. The migration and fusion events related to ROCK activity strongly influence the morphology of chicken embryo intestinal organoids. - Małgorzata Pierzchalska;Małgorzata Panek;Maja Grabacka - Protoplasma (2019)
9. 2D- and 3D-Based Intestinal Stem Cell Cultures for Personalized Medicine. - Yuan Liu;Ye-Guang Chen - Cells (2018)
10. A complex human gut microbiome cultured in an anaerobic intestine-on-a-chip. - Sasan Jalili-Firoozinezhad;Francesca S Gazzaniga;Elizabeth L Calamari;Diogo M Camacho;Cicely W Fadel;Amir Bein;Ben Swenor;Bret Nestor;Michael J Cronce;Alessio Tovaglieri;Oren Levy;Katherine E Gregory;David T Breault;Joaquim M S Cabral;Dennis L Kasper;Richard Novak;Donald E Ingber - Nature biomedical engineering (2019)

... (92 more literatures)

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