Erythroid differentiation regulator-1 induced by microbiota in early life drives intestinal stem cell proliferation and regeneration

Abo, Hirohito; Chassaing, Benoît; Harusato, Akihito; Quirós, Miguel; Brazil, Jennifer C.; Ngo, Vu L.; Viennois, Émilie; Merlin, Didier; Gewirtz, Andrew T.; Nusrat, Asma; Denning, Timothy L.

doi:10.1038/s41467-019-14258-z

Cited by 43 publications

(37 citation statements)

References 51 publications

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“…It is also crucial to fully characterize the status of animals from which IESC are isolated to produced intestinal organoids (e.g. developmental stage, diet, gut microbiota, infectious status) since IESC imprinting in vivo might impact long term epithelial phenotype in organoids in vitro [ 57 , 58 ]. However, human studies showed that traces of epigenetic regulation in intestinal organoids (related for example to effects of microbiota or chronic disease condition) were progressively erased during cell culture passaging for amplification [ 59 ].…”

Section: Future Directions Of Research With Livestock Intestinal Orgamentioning

confidence: 99%

Intestinal organoids in farm animals

Beaumont

Blanc

Cherbuy

et al. 2021

Vet Res

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In livestock species, the monolayer of epithelial cells covering the digestive mucosa plays an essential role for nutrition and gut barrier function. However, research on farm animal intestinal epithelium has been hampered by the lack of appropriate in vitro models. Over the past decade, methods to culture livestock intestinal organoids have been developed in pig, bovine, rabbit, horse, sheep and chicken. Gut organoids from farm animals are obtained by seeding tissue-derived intestinal epithelial stem cells in a 3-dimensional culture environment reproducing in vitro the stem cell niche. These organoids can be generated rapidly within days and are formed by a monolayer of polarized epithelial cells containing the diverse differentiated epithelial progeny, recapitulating the original structure and function of the native epithelium. The phenotype of intestinal organoids is stable in long-term culture and reflects characteristics of the digestive segment of origin. Farm animal intestinal organoids can be amplified in vitro, cryopreserved and used for multiple experiments, allowing an efficient reduction of the use of live animals for experimentation. Most of the studies using livestock intestinal organoids were used to investigate host-microbe interactions at the epithelial surface, mainly focused on enteric infections with viruses, bacteria or parasites. Numerous other applications of farm animal intestinal organoids include studies on nutrient absorption, genome editing and bioactive compounds screening relevant for agricultural, veterinary and biomedical sciences. Further improvements of the methods used to culture intestinal organoids from farm animals are required to replicate more closely the intestinal tissue complexity, including the presence of non-epithelial cell types and of the gut microbiota. Harmonization of the methods used to culture livestock intestinal organoids will also be required to increase the reproducibility of the results obtained in these models. In this review, we summarize the methods used to generate and cryopreserve intestinal organoids in farm animals, present their phenotypes and discuss current and future applications of this innovative culture system of the digestive epithelium.

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Section: Future Directions Of Research With Livestock Intestinal Orgamentioning

confidence: 99%

Intestinal organoids in farm animals

Beaumont

Blanc

Cherbuy

et al. 2021

Vet Res

View full text Add to dashboard Cite

show abstract

“…Apart from microbial sensing, the microbiota shapes the functionality and performance of the intestinal epithelial stem cell niche during development. Bacterial exposure at weaning affected gene expression of the erythroid differentiation regulator-1 ( Erdr1 ), which is important for stem cell proliferation and regeneration after epithelial damage in the neonatal colon ( 159 ). However, already before weaning, microbial metabolites influence intestinal epithelial renewal.…”

Section: Gastrointestinal Epithelial Barrier and Gut Commensals Early In Lifementioning

confidence: 99%

Maternal Microbiota, Early Life Colonization and Breast Milk Drive Immune Development in the Newborn

et al. 2021

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The innate immune system is the oldest protection strategy that is conserved across all organisms. Although having an unspecific action, it is the first and fastest defense mechanism against pathogens. Development of predominantly the adaptive immune system takes place after birth. However, some key components of the innate immune system evolve during the prenatal period of life, which endows the newborn with the ability to mount an immune response against pathogenic invaders directly after birth. Undoubtedly, the crosstalk between maternal immune cells, antibodies, dietary antigens, and microbial metabolites originating from the maternal microbiota are the key players in preparing the neonate’s immunity to the outer world. Birth represents the biggest substantial environmental change in life, where the newborn leaves the protective amniotic sac and is exposed for the first time to a countless variety of microbes. Colonization of all body surfaces commences, including skin, lung, and gastrointestinal tract, leading to the establishment of the commensal microbiota and the maturation of the newborn immune system, and hence lifelong health. Pregnancy, birth, and the consumption of breast milk shape the immune development in coordination with maternal and newborn microbiota. Discrepancies in these fine-tuned microbiota interactions during each developmental stage can have long-term effects on disease susceptibility, such as metabolic syndrome, childhood asthma, or autoimmune type 1 diabetes. In this review, we will give an overview of the recent studies by discussing the multifaceted emergence of the newborn innate immune development in line with the importance of maternal and early life microbiota exposure and breast milk intake.

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“…In healthy subjects, the gut microbiota is in homeostasis. The alteration of intestinal microbiota is reported to be linked to the development of inflammation present in different pathological conditions such as chronic intestinal disease, inflammatory bowel disease, asthma, diabetes mellitus, and metabolic syndrome [ 147 , 148 , 149 , 150 , 151 , 152 ]. The dysregulation in nutrient absorption and metabolism has been associated to obesity [ 153 , 154 ].…”

Section: Th17 and Treg Dysregulation In Obesity-induced Inflammationmentioning

confidence: 99%

Adipose Tissue Immunomodulation and Treg/Th17 Imbalance in the Impaired Glucose Metabolism of Children with Obesity

et al. 2021

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In the last few decades, obesity has increased dramatically in pediatric patients. Obesity is a chronic disease correlated with systemic inflammation, characterized by the presence of CD4 and CD8 T cell infiltration and modified immune response, which contributes to the development of obesity related diseases and metabolic disorders, including impaired glucose metabolism. In particular, Treg and Th17 cells are dynamically balanced under healthy conditions, but imbalance occurs in inflammatory and pathological states, such as obesity. Some studies demonstrated that peripheral Treg and Th17 cells exhibit increased imbalance with worsening of glucose metabolic dysfunction, already in children with obesity. In this review, we considered the role of adipose tissue immunomodulation and the potential role played by Treg/T17 imbalance on the impaired glucose metabolism in pediatric obesity. In the patient care, immune monitoring could play an important role to define preventive strategies of pediatric metabolic disease treatments.

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Erythroid differentiation regulator-1 induced by microbiota in early life drives intestinal stem cell proliferation and regeneration

Cited by 43 publications

References 51 publications

Intestinal organoids in farm animals

Intestinal organoids in farm animals

Maternal Microbiota, Early Life Colonization and Breast Milk Drive Immune Development in the Newborn

Adipose Tissue Immunomodulation and Treg/Th17 Imbalance in the Impaired Glucose Metabolism of Children with Obesity

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