Acute air exposure modulates the microRNA abundance in stress responsive tissues and circulating extracellular vesicles in rainbow trout (Oncorhynchus mykiss)

Cadonic, Ivan; Ikert, Heather; Craig, Paul M.

doi:10.1016/j.cbd.2020.100661

Cited by 15 publications

(17 citation statements)

References 63 publications

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“…This does indicate that EV size profiles differ between taxa and this may, amongst others, also have effects on EV cargo content, including proteomic, post-translationally modified proteomic cargo, as well as other genomic and non-coding RNA and mitochondrial-derived cargo [ 45 ]. Indeed, in teleost, it has been reported that changes in EV numbers and EV deimination protein and microRNA cargo can be a biomarker for environmental temperature factors [ 33 ] and, in response to other stressors, teleost plasma EVs have been found enriched with Hsp70 [ 46 ] and selected micro-RNAs [ 47 ]. In human parasitic disease, EV profiles can also be indicative of infection status [ 48 ].…”

Section: Discussionmentioning

confidence: 99%

The Proteome and Citrullinome of Hippoglossus hippoglossus Extracellular Vesicles—Novel Insights into Roles of the Serum Secretome in Immune, Gene Regulatory and Metabolic Pathways

Magnadóttir

Kraev

Dodds

et al. 2021

IJMS

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Extracellular vesicles (EVs) are lipid bilayer vesicles which are released from cells and play multifaceted roles in cellular communication in health and disease. EVs can be isolated from various body fluids, including serum and plasma, and are usable biomarkers as they can inform health status. Studies on EVs are an emerging research field in teleost fish, with accumulating evidence for important functions in immunity and homeostasis, but remain to be characterised in most fish species, including halibut. Protein deimination is a post-translational modification caused by a conserved family of enzymes, named peptidylarginine deiminases (PADs), and results in changes in protein folding and function via conversion of arginine to citrulline in target proteins. Protein deimination has been recently described in halibut ontogeny and halibut serum. Neither EV profiles, nor total protein or deiminated protein EV cargos have yet been assessed in halibut and are reported in the current study. Halibut serum EVs showed a poly-dispersed population in the size range of 50–600 nm, with modal size of EVs falling at 138 nm, and morphology was further confirmed by transmission electron microscopy. The assessment of EV total protein cargo revealed 124 protein hits and 37 deiminated protein hits, whereof 15 hits were particularly identified in deiminated form only. Protein interaction network analysis showed that deimination hits are involved in a range of gene regulatory, immune, metabolic and developmental processes. The same was found for total EV protein cargo, although a far wider range of pathways was found than for deimination hits only. The expression of complement component C3 and C4, as well as pentraxin-like protein, which were identified by proteomic analysis, was further verified in EVs by western blotting. This showed that C3 is exported in EVs at higher levels than C4 and deiminated C3 was furthermore confirmed to be at high levels in the deimination-enriched EV fractions, while, in comparison, C4 showed very low detection in deimination-enriched EV fractions. Pentraxin was exported in EVs, but not detected in the deimination-enriched fractions. Our findings provide novel insights into EV-mediated communication in halibut serum, via transport of protein cargo, including post-translationally deiminated proteins.

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Section: Discussionmentioning

confidence: 99%

The Proteome and Citrullinome of Hippoglossus hippoglossus Extracellular Vesicles—Novel Insights into Roles of the Serum Secretome in Immune, Gene Regulatory and Metabolic Pathways

Magnadóttir

Kraev

Dodds

et al. 2021

IJMS

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“…Since predicted miRNAs were not validated, novel differentially expressed miRNAs were omitted to improve reliability of the in silico predictions. Only mRNA with a complementarity score greater than 140 and an energy score ( G) less than −20 were used for pathway analysis (Kostyniuk et al, 2019;Cadonic et al, 2020). The script can be accessed in the Supplementary Methods (one-miRNA-all-3UTR.miranda_analysis.sh).…”

Section: Target Prediction and Pathway Analysis Of Differentially Expressed Plasma Micrornamentioning

confidence: 99%

“…Fish experience acute stress when they are exposed to air. This causes a cholinergic response within seconds to minutes and an adrenergic response within minutes to hours (Wendelaar Bonga, 1997;Tort, 2013;Balasch and Tort, 2019;Cadonic et al, 2020). Molecular regulation of this stress response is well studied in fish, however, the role of miRNA in this response is a nascent field of study.…”

Section: Introductionmentioning

confidence: 99%

“…MicroRNAs regulate the response of fish in a tissue-specific manner to a variety of stressors, such as hypoxia in tilapia (Qiang et al, 2020), contaminant exposure in carp (Liu et al, 2020a,b), and overcrowding in rainbow trout (Gonçalves et al, 2020). Additionally, miRNAs are measurable in blood plasma of fish and specific miRNAs are differentially expressed following exposure of rainbow trout to air (Cadonic et al, 2020). However, the entire plasma miRNA response to acute stress has not yet been characterized.…”

Section: Introductionmentioning

confidence: 99%

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High Throughput Sequencing of MicroRNA in Rainbow Trout Plasma, Mucus, and Surrounding Water Following Acute Stress

et al. 2021

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Circulating plasma microRNAs (miRNAs) are well established as biomarkers of several diseases in humans and have recently been used as indicators of environmental exposures in fish. However, the role of plasma miRNAs in regulating acute stress responses in fish is largely unknown. Tissue and plasma miRNAs have recently been associated with excreted miRNAs; however, external miRNAs have never been measured in fish. The objective of this study was to identify the altered plasma miRNAs in response to acute stress in rainbow trout (Oncorhynchus mykiss), as well as altered miRNAs in fish epidermal mucus and the surrounding ambient water. Small RNA was extracted and sequenced from plasma, mucus, and water collected from rainbow trout pre- and 1 h-post a 3-min air stressor. Following small RNA-Seq and pathway analysis, we identified differentially expressed plasma miRNAs that targeted biosynthetic, degradation, and metabolic pathways. We successfully isolated miRNA from trout mucus and the surrounding water and detected differences in miRNA expression 1-h post air stress. The expressed miRNA profiles in mucus and water were different from the altered plasma miRNA profile, which indicated that the plasma miRNA response was not associated with or immediately reflected in external samples, which was further validated through qPCR. This research expands understanding of the role of plasma miRNA in the acute stress response of fish and is the first report of successful isolation and profiling of miRNA from fish mucus or samples of ambient water. Measurements of miRNA from plasma, mucus, or water can be further studied and have potential to be applied as non-lethal indicators of acute stress in fish.

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“…This could have led to an overestimation of the possible organs of origin of specific c-miRNAs, especially for the organs exhibiting low expression of these c-miRNAs. In addition, a recent study in rainbow trout showed that the abundance of specific miRNAs following a stressful event exhibited an inverse relationship between tissues and blood plasma extracellular vesicles that could indicate that the liver and head kidney secreted these miRNAs [ 37 ]. Further analyses monitoring miRNA abundance in fluids and putative tissues and organs of origin over time are needed to further understand the origin of c-miRNAs.…”

Section: Resultsmentioning

confidence: 99%

Circulating miRNA repertoire as a biomarker of metabolic and reproductive states in rainbow trout

et al. 2021

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Background Circulating miRNAs (c-miRNAs) are found in most, if not all, biological fluids and are becoming well-established non-invasive biomarkers of many human pathologies. However, their features in non-pathological contexts and whether their expression profiles reflect normal life history events have received little attention, especially in non-mammalian species. The aim of the present study was to investigate the potential of c-miRNAs to serve as biomarkers of reproductive and metabolic states in fish. Results The blood plasma was sampled throughout the reproductive cycle of female rainbow trout subjected to two different feeding regimes that triggered contrasting metabolic states. In addition, ovarian fluid was sampled at ovulation, and all samples were subjected to small RNA-seq analysis, leading to the establishment of a comprehensive miRNA repertoire (i.e., miRNAome) and enabling subsequent comparative analyses to a panel of RNA-seq libraries from a wide variety of tissues and organs. We showed that biological fluid miRNAomes are complex and encompass a high proportion of the overall rainbow trout miRNAome. While sharing a high proportion of common miRNAs, the blood plasma and ovarian fluid miRNAomes exhibited strong fluid-specific signatures. We further revealed that the blood plasma miRNAome significantly changed depending on metabolic and reproductive states. We subsequently identified three evolutionarily conserved muscle-specific miRNAs or myomiRs (miR-1-1/2-3p, miR-133a-1/2-3p, and miR-206-3p) that accumulated in the blood plasma in response to high feeding rates, making these myomiRs strong candidate biomarkers of active myogenesis. We also identified miR-202-5p as a candidate biomarker for reproductive success that could be used to predict ovulation and/or egg quality. Conclusions Together, these promising results reveal the high potential of c-miRNAs, including evolutionarily conserved myomiRs, as physiologically relevant biomarker candidates and pave the way for the use of c-miRNAs for non-invasive phenotyping in various fish species.

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Acute air exposure modulates the microRNA abundance in stress responsive tissues and circulating extracellular vesicles in rainbow trout (Oncorhynchus mykiss)

Cited by 15 publications

References 63 publications

The Proteome and Citrullinome of Hippoglossus hippoglossus Extracellular Vesicles—Novel Insights into Roles of the Serum Secretome in Immune, Gene Regulatory and Metabolic Pathways

The Proteome and Citrullinome of Hippoglossus hippoglossus Extracellular Vesicles—Novel Insights into Roles of the Serum Secretome in Immune, Gene Regulatory and Metabolic Pathways

High Throughput Sequencing of MicroRNA in Rainbow Trout Plasma, Mucus, and Surrounding Water Following Acute Stress

Circulating miRNA repertoire as a biomarker of metabolic and reproductive states in rainbow trout

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