MicroRNA-based therapeutics for inflammatory disorders of the microbiota-gut-brain axis

Datta, Néha; Johnson, Cheri A.; Kao, Dina; Gurnani, Pratik; Ghaemmaghami, Amir M.; Polytarchou, Christos; Monaghan, Tanya

doi:10.1016/j.phrs.2023.106870

Cited by 12 publications

(1 citation statement)

References 327 publications

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“…Disruption of serotonin homeostasis in the gut, characterized by an excess level of extracellular serotonin, can lead to intestinal inflammation and leaky gut, thereby contributing to pathological disorders, such as inflammatory bowel disease (IBD) or irritable bowel syndrome (IBS) [10,18,19]. In the intestinal epithelium of Crohn's disease (CD) and ulcerative colitis (UC) patients, elevated levels of serotonin correlated with reduced expression of SERT [20] and upregulation of miRNAs that target SERT mRNA, such as miR-24 and miR-200a [21,22]. Also, serotonin signaling modulates the gut microbiota composition towards a dysbiosis profile that causes inflammation and, therefore, susceptibility to colitis [23].…”

Section: Introductionmentioning

confidence: 99%

Modulation of Serotonin-Related Genes by Extracellular Vesicles of the Probiotic Escherichia coli Nissle 1917 in the Interleukin-1β-Induced Inflammation Model of Intestinal Epithelial Cells

Olivo-Martínez,

Martínez-Ruiz,

Cordero-Alday

et al. 2024

IJMS

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Inflammatory bowel disease (IBD) is a chronic inflammatory condition involving dysregulated immune responses and imbalances in the gut microbiota in genetically susceptible individuals. Current therapies for IBD often have significant side-effects and limited success, prompting the search for novel therapeutic strategies. Microbiome-based approaches aim to restore the gut microbiota balance towards anti-inflammatory and mucosa-healing profiles. Extracellular vesicles (EVs) from beneficial gut microbes are emerging as potential postbiotics. Serotonin plays a crucial role in intestinal homeostasis, and its dysregulation is associated with IBD severity. Our study investigated the impact of EVs from the probiotic Nissle 1917 (EcN) and commensal E. coli on intestinal serotonin metabolism under inflammatory conditions using an IL-1β-induced inflammation model in Caco-2 cells. We found strain-specific effects. Specifically, EcN EVs reduced free serotonin levels by upregulating SERT expression through the downregulation of miR-24, miR-200a, TLR4, and NOD1. Additionally, EcN EVs mitigated IL-1β-induced changes in tight junction proteins and oxidative stress markers. These findings underscore the potential of postbiotic interventions as a therapeutic approach for IBD and related pathologies, with EcN EVs exhibiting promise in modulating serotonin metabolism and preserving intestinal barrier integrity. This study is the first to demonstrate the regulation of miR-24 and miR-200a by probiotic-derived EVs.

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Section: Introductionmentioning

confidence: 99%

Modulation of Serotonin-Related Genes by Extracellular Vesicles of the Probiotic Escherichia coli Nissle 1917 in the Interleukin-1β-Induced Inflammation Model of Intestinal Epithelial Cells

Olivo-Martínez,

Martínez-Ruiz,

Cordero-Alday

et al. 2024

IJMS

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Role of Exosomes in Parkinson’s and Alzheimer’s Diseases

Sharma,

Tyagi,

Chandra

et al. 2024

Exosomes Based Drug Delivery Strategies for Brain Disorders

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Exosomal MiRNA Therapy for Central Nervous System Injury Diseases

Chang,

Weiping,

Jibing

2024

Cell Mol Neurobiol

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Central nervous system diseases include central nervous system injury diseases, neurodegenerative diseases, and other conditions. MicroRNAs (miRNAs) are important regulators of gene expression, with therapeutic potential in modulating genes, pathways, and cells associated with central nervous system injury diseases. This article comprehensively reviews the therapeutic role of exosomal miRNAs in various central nervous system injury diseases, including traumatic brain injury, ischemic stroke, intracerebral hemorrhage, optic nerve injury, and spinal cord injury. This review covers the pathophysiology, animal models, miRNA transfection, administration methods, behavioral tests for evaluating treatment efficacy, and the mechanisms of action of miRNA-based therapies. Finally, this article discusses the future directions of miRNA therapy for central nervous system injury diseases. Graphical Abstract

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MicroRNA-based therapeutics for inflammatory disorders of the microbiota-gut-brain axis

Cited by 12 publications

References 327 publications

Modulation of Serotonin-Related Genes by Extracellular Vesicles of the Probiotic Escherichia coli Nissle 1917 in the Interleukin-1β-Induced Inflammation Model of Intestinal Epithelial Cells

Modulation of Serotonin-Related Genes by Extracellular Vesicles of the Probiotic Escherichia coli Nissle 1917 in the Interleukin-1β-Induced Inflammation Model of Intestinal Epithelial Cells

Role of Exosomes in Parkinson’s and Alzheimer’s Diseases

Exosomal MiRNA Therapy for Central Nervous System Injury Diseases

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