MicroRNAs regulate gene plasticity during cold shock in zebrafish larvae

Hung, I. Chen; Hsiao, Yu-Chuan; Sun, Hao; Chen, Tsung-Ming; Lee, Shyh-Jye

doi:10.1186/s12864-016-3239-4

Cited by 41 publications

(31 citation statements)

References 55 publications

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“…We characterised the network of protein-protein interactions (PPI) that indicated all studied proteins have functions related to the vertebrate circadian system, as they interact with core circadian proteins (supplementary table S3). Interestingly, we found that most PER and CRY proteins of Squalius interact with BHLHe41 (basic helix-loop-helix family, member e41), a protein associated with biochemical pathways activated in response to cold temperatures, as previously observed in cold shock responses in zebrafish larvae (Hung et al 2016).…”

Section: Identification and In Silico Characterisation Of Circadian-rsupporting

confidence: 74%

Adaptation and convergence in circadian-related genes in Iberian freshwater fish

Moreno

Sousa

Jesus

et al. 2019

Preprint

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The circadian clock is a biological timing system that improves the inherent ability of organisms to deal with environmental fluctuations. It is regulated by daily alternations of light but can also be affected by temperature. Fish, as ectothermic, have an increased dependence on the environmental temperature and thus are good models to study the integration of temperature within the circadian system. Here, we studied four species of freshwater fish of Squalius genus, distributed across a latitudinal gradient in Portugal with variable conditions of light and temperature. We identified and characterised the expected sixteen genes belonging to four main gene families (Cryptochromes, Period, CLOCK and BMAL) involved in the circadian system. We conducted phylogenetic analysis and tested these genes for the presence of signatures of selection based on dN/dS that revealed the presence of mutations under positive selection in nine genes. Furthermore, we analysed functional features of the proteins and found that these mutations alter protein isoelectric point and aliphatic index. Additionally, in 50% of the genes we found a pattern of convergence uncovered by the phylogenetic clustering of S. aradensis and S. pyrenaicus from Almargem, which inhabit basins with similar environmental conditions. Although this clustering can be explained by incomplete lineage sorting, evidence of positive selection in one gene in the two species and similar functional features in seven proteins are consistent with convergence at protein level. Our results highlight the importance of integrating sequence-based functional protein characterisation with dN/dS-based methods when studying the molecular adaptation of species.

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Section: Identification and In Silico Characterisation Of Circadian-rsupporting

confidence: 74%

Adaptation and convergence in circadian-related genes in Iberian freshwater fish

Moreno

Sousa

Jesus

et al. 2019

Preprint

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“…In the literatures, the family of miR-29 was found to respond to environmental stress and cellular repairing processes. In zebrafish model, the involvement of miR-29 in acute environmental stress (cold stress) was studied [39], in which the miR targeted on a core clock gene per2 to enhance cold tolerance of the fish larvae. Moreover, miR-29b was reported to play a role in cell regeneration, associated with the processes of cell survival and cytoskeleton reorganization in zebrafish [40].…”

Section: Discussionmentioning

confidence: 99%

Genome-wide analysis of MicroRNA-messenger RNA interactome in ex-vivo gill filaments, Anguilla japonica

Nong

et al. 2020

BMC Genomics

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Background: Gills of euryhaline fishes possess great physiological and structural plasticity to adapt to large changes in external osmolality and to participate in ion uptake/excretion, which is essential for the re-establishment of fluid and electrolyte homeostasis. The osmoregulatory plasticity of gills provides an excellent model to study the role of microRNAs (miRs) in adaptive osmotic responses. The present study is to characterize an ex-vivo gill filament culture and using omics approach, to decipher the interaction between tonicity-responsive miRs and gene targets, in orchestrating the osmotic stress-induced responses. Results: Ex-vivo gill filament culture was exposed to Leibovitz's L-15 medium (300 mOsmol l − 1 ) or the medium with an adjusted osmolality of 600 mOsmol l − 1 for 4, 8 and 24 h. Hypertonic responsive genes, including osmotic stress transcriptional factor, Na + /Cl − -taurine transporter, Na + /H + exchange regulatory cofactor, cystic fibrosis transmembrane regulator, inward rectifying K + channel, Na + /K + -ATPase, and calcium-transporting ATPase were significantly upregulated, while the hypo-osmotic gene, V-type proton ATPase was downregulated. The data illustrated that the ex-vivo gill filament culture exhibited distinctive responses to hyperosmotic challenge. In the hyperosmotic treatment, four key factors (i.e. drosha RNase III endonuclease, exportin-5, dicer ribonuclease III and argonaute-2) involved in miR biogenesis were dysregulated (P < 0.05). Transcriptome and miR-sequencing of gill filament samples at 4 and 8 h were conducted and two downregulated miRs, miR-29b-3p and miR-200b-3p were identified. An inhibition of miR-29b-3p and miR-200b-3p in primary gill cell culture led to an upregulation of 100 and 93 gene transcripts, respectively. Commonly upregulated gene transcripts from the hyperosmotic experiments and miR-inhibition studies, were overlaid, in which two miR-29b-3p target-genes [Krueppel-like factor 4 (klf4), Homeobox protein Meis2] and one miR-200b-3p target-gene (slc17a5) were identified. Integrated miR-mRNA-omics analysis revealed the specific binding of miR-29b-3p on Klf4 and miR-200b-3p on slc17a5. The target-genes are known to regulate differentiation of gill ionocytes and cellular osmolality.(Continued on next page) Conclusions: In this study, we have characterized the hypo-osmoregulatory responses and unraveled the modulation of miR-biogenesis factors/the dysregulation of miRs, using ex-vivo gill filament culture. MicroRNAmessenger RNA interactome analysis of miR-29b-3p and miR-200b-3p revealed the gene targets are essential for osmotic stress responses.

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“…Moreover, in agreement with results from Danio rerio and other sh species [20,21,37,38] (summary on Table S1), we detected possible diversi cation in functions of the circadian genes that may have arisen to optimize important biological processes, synchronised with the circadian oscillation. We found that in Squalius the set of predicted protein-protein interactions in CRY, PER and BMAL (Table S3) involve circadian related proteins, but also proteins with other biological functions, namely BHLHe41 (basic helixloop-helix family, member e41) and HSF2 (heat-shock factor 2), involved in temperature response [22,[39][40][41], or with NFIL3-5 (nuclear factor, interleukin 3-regulates, member 5), a protein involved in immune response [42].…”

Section: Identi Cation Of Paralogs and Orthologs Of All Circadian Genmentioning

confidence: 99%

Adaptation and convergence in circadian-related genes in Iberian freshwater fish

Moreno

Jesus

Sousa³

et al. 2020

Preprint

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BackgroundThe circadian clock is a biological timing system that improves the ability of organisms to deal with environmental fluctuations. At the molecular level it consists of a network of transcription-translation feedback loops, involving genes that activate (bmal and clock – positive loop) and repress expression (cryptochrome (cry) and period (per) – negative loop). This is regulated by daily alternations of light but can also be affected by temperature. Fish, as ectothermic, depend on the environmental temperature and thus are good models to study its integration within the circadian system. Here, we studied the molecular evolution of circadian genes in four Squalius freshwater fish species, distributed across Western Iberian rivers affected by two climatic types with different environmental conditions (e.g. light and temperature). S. carolitertii and S. pyrenaicus inhabit the colder northern region under Atlantic climate type, while S. torgalensis, S. aradensis and some populations of S. pyrenaicus inhabit the warmer southern region affected by summer droughts, under Mediterranean climate type. ResultsWe identified 16 circadian-core genes in the Squalius species using a comparative transcriptomics approach. We detected evidence of positive selection in nine of these genes using methods based on dN/dS. Positive selection was mainly found in cry and per genes of the negative loop of the cycle, with 11 putatively adaptive substitutions mostly located on protein domains. Evidence for positive selection is predominant in southern populations affected by the Mediterranean climate type. By predicting protein features we found that changes at sites under positive selection can impact protein thermostability by changing their aliphatic index and isoelectric point. Additionally, in nine genes, the phylogenetic clustering of species that belong to different clades but inhabit southern basins with similar environmental conditions indicated evolutionary convergence.ConclusionsOur results support that temperature may be a strong selective pressure driving the evolution of genes involved in the circadian system. By integrating sequence-based functional protein prediction with dN/dS-based methods to detect selection we also uncovered adaptive convergence in the southern populations, probably related to their similar thermal conditions.

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MicroRNAs regulate gene plasticity during cold shock in zebrafish larvae

Cited by 41 publications

References 55 publications

Adaptation and convergence in circadian-related genes in Iberian freshwater fish

Adaptation and convergence in circadian-related genes in Iberian freshwater fish

Genome-wide analysis of MicroRNA-messenger RNA interactome in ex-vivo gill filaments, Anguilla japonica

Adaptation and convergence in circadian-related genes in Iberian freshwater fish

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