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Hypoxia-induced miR-92a regulates p53 signaling pathway and apoptosis by targeting calcium-sensing receptor in genetically improved farmed tilapia (Oreochromis niloticus).

ABSTRACT: miR-92a miRNAs are immune molecules that regulate apoptosis (programmed cell death) during the immune response. Apoptosis helps to maintain the dynamic balance in tissues of fish under hypoxia stress. The aim of this study was to explore the role and potential mechanisms of miR-92a in the liver of tilapia under hypoxia stress. We first confirmed that CaSR (encoding a calcium-sensing receptor) is a target gene of miR-92a in genetically improved farmed tilapia (GIFT) using luciferase reporter gene assays. In GIFT under hypoxia stress, miR-92a was up-regulated and CaSR was down-regulated in a time-dependent manner. Knocked-down CaSR expression led to inhibited expression of p53, TP53INP1, and caspase-3/8, reduced the proportion of apoptotic hepatocytes, and decreased the activity of calcium ions induced by hypoxia in hepatocytes. GIFT injected in the tail vein with an miR-92a agomir showed up-regulation of miR-92a and down-regulation of CaSR, p53, TP53INP1, and caspase-3/8 genes in the liver, resulting in lower serum aspartate aminotransferase and alanine aminotransferase activities under hypoxia stress. These findings suggest that stimulation of miR-92a interferes with hypoxia-induced apoptosis in hepatocytes of GIFT by targeting CaSR, thereby alleviating liver damage. These results provide new insights into the adaptation mechanisms of GIFT to hypoxia stress.

SUBMITTER: Qiang J

PROVIDER: S-EPMC7660578 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Hypoxia-induced miR-92a regulates p53 signaling pathway and apoptosis by targeting calcium-sensing receptor in genetically improved farmed tilapia (Oreochromis niloticus).

Qiang Jun J He Jie J Tao Yi-Fan YF Bao Jin-Wen JW Zhu Jun-Hao JH Xu Pao P

PloS one 20201112 11

miR-92a miRNAs are immune molecules that regulate apoptosis (programmed cell death) during the immune response. Apoptosis helps to maintain the dynamic balance in tissues of fish under hypoxia stress. The aim of this study was to explore the role and potential mechanisms of miR-92a in the liver of tilapia under hypoxia stress. We first confirmed that CaSR (encoding a calcium-sensing receptor) is a target gene of miR-92a in genetically improved farmed tilapia (GIFT) using luciferase reporter gene ...[more]

PMID: 33180826

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Project description:Nile tilapia, Oreochromis niloticus is the third most commonly farmed finfish species in the world, accounting for nearly 5% of global aquaculture production. In the past few decades much of the success of this species has been attributed to the development and distribution of Genetically Improved Farmed Tilapia (GIFT). Despite the increasing availability of GIFT, the productivity of small-scale farming remains highly variable, particularly in developing nations. Commercial fish-feed pellets can increase fish farm productivity; however, many small-scale farmers rely on other means of feeding fish due to the high cost and limited availability of commercial fish feed pellets. Therefore, understanding how locally-sourced feeds affect the production of GIFT is an important step towards improving feeding practices, particularly for farmers with low financial capital. This study used stable isotope analysis (SIA) and 16S rRNA gene sequencing to compare the effects of a locally-sourced vegetable-based diet and commercial pellet-based diets on the relative condition, nutrient assimilation patterns and gastrointestinal microbiota of GIFT. GIFT fed a locally-sourced diet were smaller, and in a significantly poorer condition than those fed with commercial fish feeds. SIA showed no differences in dietary carbon between the two diets; however, δ13C, poor fish condition and the abundance of specific bacterial taxa (of such as Fusobacteria) were correlated. SIA revealed that GIFT fed locally-sourced diets that predominantly consisted of vegetables were significantly enriched in δ15N despite a perceived lack of dietary protein. This enrichment suggests that GIFT fed a locally-sourced diet may be supplementing their diet via cannibalism, a behaviour representative of poor farming practice. Overall this study highlights the need to increase the availability of suitable GIFT feeds in developing nations. The development a low-cost feed alternative could improve the success of small-scale GIFT farmers in PNG, increasing both food and income security within the region.

Project description:Genetically improved farmed tilapia (GIFT, Oreochromis niloticus) are intensively farmed in China, where most of the yield derives from the pond culture system (PCS). The in-pond raceway system (IPRS) is a new type of highly efficient aquaculture mode, and has been recommended as a novel system for GIFT farming. To determine the effects of these culture modes on the gut microbiome of GIFT, we conducted a 90-days experiment in IPRS and PCS units. A 16S rRNA gene profile analysis showed that the composition of gut microbiota in GIFT under IPRS and PCS conditions gradually separated as rearing progressed, with divergent responses by the midgut and hindgut bacteria. The α-diversity in hindgut decreased significantly by day 90, as compared with on day 7 (p < 0.05), with a significantly greater decrease in PCS-reared fish than in IPRS fish (p < 0.05). The α-diversity of microbiota in midgut remained stable (p > 0.05). The overall dominant gut bacteria were Bacteroidetes, Proteobacteria, and Firmicutes. Rearing mode affected the taxonomic profile of the gut bacteria; in midgut, IPRS samples had more Firmicutes and Fusobacteria compared with PCS samples, but less Proteobacteria, Verrucomicrobia, and Actinobacteria. Firmicutes was enriched in IPRS hindgut, and Fusobacteria was enriched in PCS hindgut. Using random-forest models and LEfSe, we also screened core taxa that could discriminate between the gut microbial communities under IPRS and PCS conditions. The genus Cetobacterium (of family Fusobacteriaceae) was significantly enriched in midgut in IPRS fish, and enriched in hindgut in PCS fish. The genus Clostridium sensu stricto (of family Clostridiaceae 1) was significantly enriched in both IPRS midgut and hindgut. Analysis with PICRUSt2 software revealed that the culture modes were similar in their effects on the gut microbial metabolic functions. The predicted pathways were significantly enriched in the metabolism class (level 1). Further, the relative abundance of functions related to amino acid metabolic, carbohydrate metabolic, energy metabolic, and metabolic of cofactors and vitamins were high at hierarchy level 2, as the metabolic activity of intestinal bacteria is especially active. Overall, this study enhances our understanding of the characteristics of gut microbiota in GIFT under IPRS and PCS culture modes. Moreover, our findings provide insights into the microecological balance in IPRS units, and a theoretical reference for further development of this culture system.

Project description:MicroRNAs (miRNAs) are a class of small non-coding RNAs (18-25 nucleotides) that result in RNA silencing and post-transcriptional regulation of gene expression by binding to the 3'-untranslated regions of their target mRNAs. Mature miRNAs are widely reported in plants, animals and some viruses, which involved in the innate immune response, inflammatory diseases, cell signal transduction, and metabolism. Under temperature stress, miRNA expression is regulated to cope with the stress response. Up-regulation of 18 miRNAs and down-regulation of 11 miRNAs were found in the rat jejunum after heat treatment. 25 miRNA different expression under the cold and normal conditions were identified in zebrafish (Danio rerio). However, miRNAs involved in heat stress in GIFT have not been detected, and potentially important miRNA-signal pathway could have been overlooked. Study of the regulatory function of miRNA in heat-stress response is a crucial topic in the research of fish physiology. MiRNA expression profiles of tilapia in a variety of tissue have been studied recently by high-throughput next-generation sequencing technology (NGST). The expression levels of 218 miRNAs (e.g., miR-17, miR-29, miR-155 and miR-214) were significantly altered in tilapia kidney at 6-72h post- S. agalactiae infection. Additionally, 635 mature miRNAs were identified post-hatch day 5 in tilapia XX and XY gonads, in which 62 and 49 miRNAs showed different expression respectively (e.g., sex-biased miRNAs: miR-9, miR-21, miR-30a, miR-96, miR-200b, miR-212 and miR-7977). The gene expressions may contribute to immune regulation and stress adaptation in fish by heat stress. The levels of immune-related gene (e.g., immunoglobulin M, lysozyme, hepcidin and transferrin) expression were significantly up-regulated in turbot (Scophthalmus maximus) post-48h heat stress. HSPs play an important role in fish exposed to environmental stress. Some highly conserved HSPs could be synthesized in sculpins Oligocottus maculosus, turbot and GIFT in response to heat stress. Fatty acid composition and utilization in fish could be affected by heat stress. △6-desaturase-α and elongation of long chain fatty acids 5α (Elovl 5α) are involved in poly unsaturated fatty acid biosynthesis, which were obviously up-regulated in common carp (Cyprinus carpio) by heat stress, and help to increase fatty acid metabolism and maintain fluidity of cell membrane. However, in these studies the several genes were generated from known and functional protein-coding genes. The significance of mRNA transcriptome to heat-stress response in fish are far from clear. Thus, the study of miRNA and mRNA expression profiles may help us better understand the molecular mechanisms and signaling pathway of heat stress.

Dataset Information

Hypoxia-induced miR-92a regulates p53 signaling pathway and apoptosis by targeting calcium-sensing receptor in genetically improved farmed tilapia (Oreochromis niloticus).

Publications

Hypoxia-induced miR-92a regulates p53 signaling pathway and apoptosis by targeting calcium-sensing receptor in genetically improved farmed tilapia (Oreochromis niloticus).

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