Identification and differential regulation of microRNAs during thyroid hormone-dependent metamorphosis in Microhyla fissipes

Abstract

BackgroundAnuran metamorphosis, which is obligatorily initiated and sustained by thyroid hormone (TH), is a dramatic example of extensive morphological, biochemical and cellular changes occurring during post-embryonic development. Thus, it provides an ideal model to understand the actions of the hormone and molecular mechanisms underlying these developmental and apoptotic processes. In addition to transcriptional factors, microRNAs (miRNAs) play key roles in diverse biological processes via post-transcriptional repression of mRNAs. However, the possible role of miRNAs in anuran metamorphosis is not well understood. Screening and identification of TH-responding miRNAs are required to reveal the integrated regulatory mechanisms of TH during metamorphosis. Given the specific role of TRs during M. fissipes metamorphosis and the characteristics of M. fissipes as an ideal model, Illumina sequencing technology was employed to get a full scope of miRNA in M. fissipes metamorphosis treated by T3.ResultsMorphological and histological analysis revealed that 24 h T3 treatment M. fissipes tadpoles resembled that at the climax of natural metamorphosis. Thus, small RNA libraries were constructed from control and 24 h T3 treatment groups. A total of 164 conserved miRNAs and 36 predicted novel miRNAs were characterized. Furthermore, 5′ first and ninth nucleotides of miRNAs were significantly enriched in U in our study. In all, 21 miRNAs were differentially expressed between the T3 and control groups (p < 0.01). A total of 10,206 unigenes were identified as target genes of these differentially expressed miRNAs. KEGG pathway analysis indicated that the most overrepresented miRNA target genes were enriched in the “PI3k-Akt signaling pathway”. In addition, a network associated with the TH signaling pathway provides an opportunity to further understand the complex biological processes that occur in metamorphosis.ConclusionsWe identified a large number of miRNAs during M. fissipes metamorphosis, and 21 of them were differentially expressed in the two groups that represented two different metamorphic stages. These miRNAs may play important roles during metamorphosis. The study gives us clues for further studies of the mechanisms of anuran metamorphosis and provides a model to study the mechanism of TH-affected biological processes in humans.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4848-x) contains supplementary material, which is available to authorized users.

Screening and identification of microRNAs during larval metamorphic development of Chinese mitten crab Eriocheir sinensis

“…We compared the metamorphosis of Chinese mitten crab with that of other species, such as Bombyx mori (Liu et al, 2010), insects (Ylla, Piulachs, & Belles, 2017), ascidian (Zhang et al, 2018) and Microhyla fissipes (Liu, Zhu, Liu, Wang, & Jiang, 2018). We found that miRNAs are involved in the abnormal development of these species, which is similar to the results of our studies.…”

“…For example, in M. fissipes (Liu et al, 2018), the main regulatory miR-NAs are miR-143a, miR-181a-5p and miR-22-3p. Conversely, miR-216b, miR-183 and miR-217 regulate the metamorphosis of ascidians (Zhang et al, 2018).…”

“…Similarly, steroids have two principal biological functions: (a) certain steroids (such as cholesterol) are important components of cell membranes which alter membrane fluidity, and (b) many steroids are signalling molecules that activate steroid hormone receptors, while steroid hormones play important roles in maintaining life, by regulating body development and immune regulation. The main pathways involved in the metamorphosis of M. fissipes(Liu et al, 2018) include the P13K-Akt, mToR and TH signalling pathways, whilst in ascidian, these the MAPK, Rap 1, Ras and transforming growth factor β (TGF-β) signalling pathways(Zhang et al, 2018). MiRNAs of different species may be involved in different pathways, because the mode of metamorphosis varies between species.…”

Temporal and spatial transcriptomic dynamics across brain development in Xenopus laevis tadpoles

“…A partial explanation for the discrepancy between the expected decrease in proliferation and the observed mRNA expression of proliferation-upregulating genes could be a concurrent change in posttranscriptional regulation. Studies in the closely related anuran M. fissipes found that during metamorphosis, miRNAs targeting the PI3K-AKT pathway were the most significantly enriched group, indicating that miRNA regulation plays a significant role in metamorphic development ( Liu et al 2018 ). miRNA expression during Xenopus metamorphosis has previously been profiled ( Hikosaka et al 2007 ), but target genes for these miRNAs have yet to be identified.…”

Multi-organ transcriptomic landscape of Ambystoma velasci metamorphosis

“…This process is widely distributed in many invertebrate and vertebrate groups 1 such as cnidarians, insects, fishes and amphibians. During metamorphosis, a series of changes take place to allow the organism to adapt in different environments 2,3,4,5 . In amphibians, this process allows aquatic tadpoles to transform into terrestrial juvenile organisms 1,6,7,16 .…”