The importance of interaction between MicroRNAs and gut microbiota in several pathways

Behrouzi, Ava; Ashrafian, Fatemeh; Mazaheri, Hoora; Lari, Arezou; Nouri, Matineh; Riazi-Rad, Farhad; Tavassol, Zahra Hoseini; Siadat, Seyed Davar

doi:10.1016/j.micpath.2020.104200

Cited by 33 publications

(29 citation statements)

References 123 publications

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“…Having described the composition of these initial communities, an obvious question is how do the transcriptomes of host tissues respond to these early events, and what regulatory mechanisms (e.g., miRNAs) drive these responses? Several miRNA studies have shown differences between germfree and colonized mice; for example, when 8-week-old germfree mice were exposed to microbiota for several days, the host tissues reprogramed their transcription through miRNAs ( 5 , 64 ). Similarly, miRNAs present in breast milk rapidly shape the microbiome of the gut by playing a key role in immunomodulation ( 65 ), a common event in the establishment of beneficial symbioses (e.g., references 66 – 68 ).…”

Section: Discussionmentioning

confidence: 99%

“…Accommodation to a beneficial microbial symbiosis has been associated with pronounced changes in gene expression in host tissues ( 1 – 4 ), and recent studies have provided evidence that the activity of microRNAs (miRNAs) represents a major mechanism by which these processes are regulated ( 5 , 6 ). This mode of regulation plays a crucial role in ensuring that proper gene expression patterns are established and maintained in each host cell type ( 7 ).…”

Section: Introductionmentioning

confidence: 99%

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MicroRNA-Mediated Regulation of Initial Host Responses in a Symbiotic Organ

2021

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One of the most important events in an animal’s life history is the initial colonization by its microbial symbionts, yet little is known about this event’s immediate impacts on the extent of host gene expression or the molecular mechanisms controlling it. MicroRNAs (miRNAs) are short, noncoding RNAs that bind to target mRNAs, rapidly shaping gene expression by posttranscriptional control of mRNA translation and decay. Here, we show that, in the experimentally tractable binary squid-vibrio symbiosis, colonization of the light organ induces extensive changes in the miRNA transcriptome. Examination of the squid genome revealed the presence of evolutionarily conserved genes encoding elements essential for the production and processing of miRNAs. At 24 h postcolonization, 215 host miRNAs were detected in the light organ, 26 of which were differentially expressed in response to the symbionts. A functional enrichment analysis of genes potentially targeted by downregulation of certain miRNAs at the initiation of symbiosis revealed two major gene ontology (GO) term categories, neurodevelopment and tissue remodeling. This symbiont-induced downregulation is predicted to promote these activities in host tissues and is consistent with the well-described tissue remodeling that occurs at the onset of the association. Conversely, predicted targets of upregulated miRNAs, including the production of mucus, are consistent with attenuation of immune responses by symbiosis. Taken together, our data provide evidence that, at the onset of symbiosis, host miRNAs in the light organ drive alterations in gene expression that (i) orchestrate the symbiont-induced development of host tissues, and (ii) facilitate the partnership by dampening the immune response. IMPORTANCE Animals often acquire their microbiome from the environment at each generation, making the initial interaction of the partners a critical event in the establishment and development of a stable, healthy symbiosis. However, the molecular nature of these earliest interactions is generally difficult to study and poorly understood. We report that, during the initial 24 h of the squid-vibrio association, a differential expression of host miRNAs is triggered by the presence of the microbial partner. Predicted mRNA targets of these miRNAs were associated with regulatory networks that drive tissue remodeling and immune suppression, two major symbiosis-induced developmental outcomes in this and many other associations. These results implicate regulation by miRNAs as key to orchestrating the critical transcriptional responses that occur very early during the establishment of a symbiosis. Animals with more complex microbiota may have similar miRNA-driven responses as their association is initiated, supporting an evolutionary conservation of symbiosis-induced developmental mechanisms.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

MicroRNA-Mediated Regulation of Initial Host Responses in a Symbiotic Organ

2021

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“…Host–microbiota interactions play a vital role in intestinal homeostasis, and miRNAs have been considered to be key molecular regulators for mediating such interactions ( Behrouzi et al, 2020 ). The addition of probiotics can also interfere with these interactions and influence the expression of miRNAs ( Teng et al, 2018 ).…”

Section: Exploration Of Mirna-based Molecular Mechanism Of Probioticsmentioning

confidence: 99%

“…MicroRNAs (miRNAs) are considered to be important regulators in the host gene expression process, and some are found to be significantly related to the microbial community or specific bacteria ( Hasan and Yang, 2019 ). Recent studies have proposed the functional role of miRNAs played in shaping gut microbiota ( Moloney et al, 2019 ; Behrouzi et al, 2020 ). These host-derived miRNAs were able to enter bacterial cells to cultivate or inhibit specific bacteria ( Liu et al, 2016 ; Spinler et al, 2019 ).…”

Section: Introductionmentioning

confidence: 99%

Probiotics and MicroRNA: Their Roles in the Host–Microbe Interactions

Zhao

Zeng

et al. 2021

Front. Microbiol.

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Probiotics are widely accepted to be beneficial for the maintenance of the gut homeostasis – the dynamic and healthy interactions between host and gut microorganisms. In addition, emerging as a key molecule of inter-domain communication, microRNAs (miRNAs) can also mediate the host–microbe interactions. However, a comprehensive description and summary of the association between miRNAs and probiotics have not been reported yet. In this review, we have discussed the roles of probiotics and miRNAs in host–microbe interactions and proposed the association of probiotics with altered miRNAs in various intestinal diseases and potential molecular mechanisms underlying the action of probiotics. Furthermore, we provided a perspective of probiotics–miRNA–host/gut microbiota axis applied in search of disease management highly associated with the gut microbiome, which will potentially prove to be beneficial for future studies.

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“…The susceptibility of bacterial cells to eukaryotic miRNAs has been demonstrated by observing that some miRNAs such as miR-1, miR-130a, and miR-2392 can efficiently enter mitochondria and regulate the translation of specific mitochondrial genome-encoded transcripts [94][95][96]. These findings settled the bases for studying the impact of miRNAs on gut microbiota composition and dynamics [51,81,90,[97][98][99]. Liu et al for the first time demonstrated that host-fecal miRNAs can modulate gut microbiota composition by modifying the relative abundance of bacteria, considered at a family-level taxonomy.…”

Section: Fecal Mirnas Contribute To Gut Microbiota Shapingmentioning

confidence: 99%

Fecal microRNAs as Innovative Biomarkers of Intestinal Diseases and Effective Players in Host-Microbiome Interactions

Sarshar

Scribano

Ambrosi

et al. 2020

Cancers

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Over the past decade, short non-coding microRNAs (miRNAs), including circulating and fecal miRNAs have emerged as important modulators of various cellular processes by regulating the expression of target genes. Recent studies revealed the role of miRNAs as powerful biomarkers in disease diagnosis and for the development of innovative therapeutic applications in several human conditions, including intestinal diseases. In this review, we explored the literature and summarized the role of identified dysregulated fecal miRNAs in intestinal diseases, with particular focus on colorectal cancer (CRC) and celiac disease (CD). The aim of this review is to highlight one fascinating aspect of fecal miRNA function related to gut microbiota shaping and bacterial metabolism influencing. The role of miRNAs as “messenger” molecules for inter kingdom communications will be analyzed to highlight their role in the complex host-bacteria interactions. Moreover, whether fecal miRNAs could open up new perspectives to develop novel suitable biomarkers for disease detection and innovative therapeutic approaches to restore microbiota balance will be discussed.

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The importance of interaction between MicroRNAs and gut microbiota in several pathways

Cited by 33 publications

References 123 publications

MicroRNA-Mediated Regulation of Initial Host Responses in a Symbiotic Organ

MicroRNA-Mediated Regulation of Initial Host Responses in a Symbiotic Organ

Probiotics and MicroRNA: Their Roles in the Host–Microbe Interactions

Fecal microRNAs as Innovative Biomarkers of Intestinal Diseases and Effective Players in Host-Microbiome Interactions

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