Harness Organoid Models for Virological Studies in Animals: A Cross-Species Perspective

Sang, Yongming; Miller, Laura C.; Nelli, Rahul K.; Giménez-Lirola, Luis

doi:10.3389/fmicb.2021.725074

Cited by 9 publications

(10 citation statements)

References 137 publications

(503 reference statements)

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“…The debate on whether or not engineered cell-based in vitro models, such as organoids, can faithfully reproduce the structures and functions of the original organ in vivo is ongoing ( 37 , 38 ). Although organoid systems are limited in their ability to mimic the properties of complex in vivo tissues relevant to physiological or pathological processes in tissues, organoid cultures are still useful tools for studying fundamental mechanistic questions ( 39 ).…”

Section: Discussionmentioning

confidence: 99%

Analysis of organoid and immune cell co-cultures by machine learning-empowered image cytometry

Stüve,

Nerb,

Harrer

et al. 2024

Front. Med.

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Organoids are three-dimensional (3D) structures that can be derived from stem cells or adult tissue progenitor cells and exhibit an extraordinary ability to autonomously organize and resemble the cellular composition and architectural integrity of specific tissue segments. This feature makes them a useful tool for analyzing therapeutical relevant aspects, including organ development, wound healing, immune disorders and drug discovery. Most organoid models do not contain cells that mimic the neighboring tissue’s microenvironment, which could potentially hinder deeper mechanistic studies. However, to use organoid models in mechanistic studies, which would enable us to better understand pathophysiological processes, it is necessary to emulate the in situ microenvironment. This can be accomplished by incorporating selected cells of interest from neighboring tissues into the organoid culture. Nevertheless, the detection and quantification of organoids in such co-cultures remains a major technical challenge. These imaging analysis approaches would require an accurate separation of organoids from the other cell types in the co-culture. To efficiently detect and analyze 3D organoids in co-cultures, we developed a high-throughput imaging analysis platform. This method integrates automated imaging techniques and advanced image processing tools such as grayscale conversion, contrast enhancement, membrane detection and structure separation. Based on machine learning algorithms, we were able to identify and classify 3D organoids within dense co-cultures of immune cells. This procedure allows a high-throughput analysis of organoid-associated parameters such as quantity, size, and shape. Therefore, the technology has significant potential to advance contextualized research using organoid co-cultures and their potential applications in translational medicine.

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Section: Discussionmentioning

confidence: 99%

Analysis of organoid and immune cell co-cultures by machine learning-empowered image cytometry

Stüve,

Nerb,

Harrer

et al. 2024

Front. Med.

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“…Moreover, rapid loss of the structure and integrity of stratified organotypic explants is often observed [ 37 ]. Thus, prompt handling after surgeries to transiently retain physiologic relevance of tissue architecture and cellular interactions is required and is prohibitive to long time-course experiments [ 38 ]. Furthermore, these systems are inherently not self-renewing and require patient donors.…”

Section: Meeting In the Middle: 3d Tissue Models To Study Initial Ste...mentioning

confidence: 99%

HIV-1 transmission: modelling and direct visualization in the third dimension

Coomer

Padilla‐Parra

2023

Microscopy

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Identifying initial events of mucosal entry of HIV-1 in laboratory-based, physiologically-relevant and high-throughput contexts may aid in designing effective strategies to block local transmission and spread of HIV-1. Several paradigms have been posited for how HIV-1 crosses mucosal barriers to establish infection based on 2D culture or animal-based models. Nevertheless, despite these models stemming from 2D culture and animal studies, monolayers of cells poorly replicate the complex niche that influences viral entry at mucosal surfaces, whereas animal models often inadequately reproduce human disease pathophysiology and are prohibitively expensive. Organoids, having never been directly utilised in HIV-1 transmission investigations, may offer a compromise between 2D culture and animal models as they provide a platform which mimics the biophysical and biochemical niche of mucosal tissues. Importantly, observation of events downstream of viral inoculation is potentially accessible to researchers via an array of microscopy techniques. Because of the potential insights organoids may provide in this context, we offer this review to highlight key physiological factors of HIV-1 transmission at common mucosal sites and a discussion highlighting how many of these factors can be recapitulated in organoids, their current limitations and what questions can initially be addressed, particularly by a selective inclusion of quantitative light microscopy techniques. Harnessing organoids for direct observation of HIV-1 entry at mucosal sites may uncover potential therapeutic targets which prevent the establishment of HIV-1 infection.

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“…It is now known that many animals including both wildlife and domestic species play an important role in the spread of zoonotic diseases as potential reservoirs. For instance, severe acute respiratory syndrome (SARS), which resulted in a major outbreak worldwide in early 2000s, and the current ongoing pandemic of the new coronavirus 2019 disease (COVID-19) are caused by previously unrecognized coronaviruses which are most likely evolved from bats as a natural reservoir (SARS-CoV and SARS-CoV-2, respectively) ( 18 , 121 ). A recent study demonstrated susceptibility of bat intestinal organoids to SARS-CoV-2 and sustained viral replications in organoids, which could not have been achieved using bat cell lines, by establishing an in vitro infection model ( 122 ).…”

Section: Roles Of Farm and Companion Animal Organoids In One Health I...mentioning

confidence: 99%

“…This study demonstrated previously unculturable novel viruses in established cell lines could be cultured in organoids. Additionally, SARS-CoV-2 has been shown to infect various domestic and wildlife species other than humans including dogs, cats, minks, ferrets, hamsters, lions and tigers ( 121 ). Animal organoids derived from different species would provide an effective tool to evaluate cross-species variations in viral susceptibility or species-specific infectivity of viruses with zoonotic and zooanthroponotic potentials, providing a great alternative to animal models for infection studies.…”

Section: Roles Of Farm and Companion Animal Organoids In One Health I...mentioning

confidence: 99%

Farm and Companion Animal Organoid Models in Translational Research: A Powerful Tool to Bridge the Gap Between Mice and Humans

Kawasaki

Goyama

Tachibana

et al. 2022

Front. Med. Technol.

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Animal organoid models derived from farm and companion animals have great potential to contribute to human health as a One Health initiative, which recognize a close inter-relationship among humans, animals and their shared environment and adopt multi-and trans-disciplinary approaches to optimize health outcomes. With recent advances in organoid technology, studies on farm and companion animal organoids have gained more attention in various fields including veterinary medicine, translational medicine and biomedical research. Not only is this because three-dimensional organoids possess unique characteristics from traditional two-dimensional cell cultures including their self-organizing and self-renewing properties and high structural and functional similarities to the originating tissue, but also because relative to conventional genetically modified or artificially induced murine models, companion animal organoids can provide an excellent model for spontaneously occurring diseases which resemble human diseases. These features of companion animal organoids offer a paradigm-shifting approach in biomedical research and improve translatability of in vitro studies to subsequent in vivo studies with spontaneously diseased animals while reducing the use of conventional animal models prior to human clinical trials. Farm animal organoids also could play an important role in investigations of the pathophysiology of zoonotic and reproductive diseases by contributing to public health and improving agricultural production. Here, we discuss a brief history of organoids and the most recent updates on farm and companion animal organoids, followed by discussion on their potential in public health, food security, and comparative medicine as One Health initiatives. We highlight recent evolution in the culturing of organoids and their integration with organ-on-a-chip systems to overcome current limitations in in vitro studies. We envision multidisciplinary work integrating organoid culture and organ-on-a-chip technology can contribute to improving both human and animal health.

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Harness Organoid Models for Virological Studies in Animals: A Cross-Species Perspective

Cited by 9 publications

References 137 publications

Analysis of organoid and immune cell co-cultures by machine learning-empowered image cytometry

Analysis of organoid and immune cell co-cultures by machine learning-empowered image cytometry

HIV-1 transmission: modelling and direct visualization in the third dimension

Farm and Companion Animal Organoid Models in Translational Research: A Powerful Tool to Bridge the Gap Between Mice and Humans

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