The evolution and immunomodulatory role of Zc3h12 proteins in zebrafish (Danio rerio)

Yang, Shuaiqi; Xu, Xiaowei; Zhang, Ailong; Wang, Yunchao; Ji, Guangdong; Sun, Chen; Li, Hongyan

doi:10.1016/j.ijbiomac.2023.124214

Cited by 2 publications

(4 citation statements)

References 64 publications

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“…1 a,b), also recently showed by Yang et al . 23 . The full-length zebrafish zc3h12a sequence (XM_021466808.1; Gene ID: 798235; NCBI) encodes a 579 amino acid Mcpip1 protein with high (82.90%) amino acid identity to common carp Mcpip1 and intermediate (~ 50%) amino acid identity to amphibian, reptilian, bird and mammalian MCPIP1.…”

Section: Resultsmentioning

confidence: 99%

MCPIP1 functions as a safeguard of early embryonic development

Lichawska-Cieslar,

Szukala,

Prajsnar

et al. 2023

Sci Rep

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Monocyte chemoattractant protein-induced protein 1 (MCPIP1), also called Regnase-1, is an RNase that has been described as a key negative modulator of inflammation. MCPIP1 also controls numerous tumor-related processes, such as proliferation, apoptosis and differentiation. In this study, we utilized a zebrafish model to investigate the role of Mcpip1 during embryogenic development. Our results demonstrated that during embryogenesis, the expression of the zc3h12a gene encoding Mcpip1 undergoes dynamic changes. Its transcript levels gradually increase from the 2-cell stage to the spherical stage and then decrease rapidly. We further found that ectopic overexpression of wild-type Mcpip1 but not the catalytically inactive mutant form resulted in an embryonic lethal phenotype in zebrafish embryos (24 hpf). At the molecular level, transcriptomic profiling revealed extensive changes in the expression of genes encoding proteins important in the endoplasmic reticulum stress response and in protein folding as well as involved in the formation of primary germ layer, mesendoderm and endoderm development, heart morphogenesis and cell migration. Altogether, our results demonstrate that the expression of zc3h12a must be tightly controlled during the first cell divisions of zebrafish embryos and that a rapid decrease in its mRNA expression is an important factor promoting proper embryo development.

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Section: Resultsmentioning

confidence: 99%

MCPIP1 functions as a safeguard of early embryonic development

Lichawska-Cieslar,

Szukala,

Prajsnar

et al. 2023

Sci Rep

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“…The Regnase and Roquin RNA-binding proteins collaboratively control the degradation of mRNA and maintain homeostasis and the immune system. Previously, we elucidated the evolution of the Regnase-encoded Zc3h12 gene family and uncovered the immunomodulatory role of Regnases in zebrafish [ 29 ]. However, information regarding the evolution of Roquins in zebrafish is lacking.…”

Section: Discussionmentioning

confidence: 99%

“…Across invertebrates, jawless vertebrates, and vertebrates, there are generally one, two, and four Zc3h12 genes, respectively. Notably, in bony fish, which experienced three or four rounds of WGD events, the number of zc3h12 genes varies greatly [ 29 ]. Zc3h12 underwent two rounds of gene duplication events, along with exceptional species-specific gene duplication or loss events during teleost evolution [ 29 ].…”

Section: Discussionmentioning

confidence: 99%

“…Notably, in bony fish, which experienced three or four rounds of WGD events, the number of zc3h12 genes varies greatly [ 29 ]. Zc3h12 underwent two rounds of gene duplication events, along with exceptional species-specific gene duplication or loss events during teleost evolution [ 29 ]. Both the Roquin and Regnase families participate in post-transcriptionally regulating mRNA and are involved in immune responses.…”

Section: Discussionmentioning

confidence: 99%

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Bioinformatic Analysis of Roquin Family Reveals Their Potential Role in Immune System

Li,

Yang,

Zhang

et al. 2024

IJMS

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The Roquin family is a recognized RNA-binding protein family that plays vital roles in regulating the expression of pro-inflammatory target gene mRNA during the immune process in mammals. However, the evolutionary status of the Roquin family across metazoans remains elusive, and limited studies are found in fish species. In this study, we discovered that the RC3H genes underwent a single round of gene duplication from a primitive ancestor during evolution from invertebrates to vertebrates. Furthermore, there were instances of species-specific gene loss events or teleost lineage-specific gene duplications throughout evolution. Domain/motif organization and selective pressure analysis revealed that Roquins exhibit high homology both within members of the family within the same species and across species. The three rc3h genes in zebrafish displayed similar expression patterns in early embryos and adult tissues, with rc3h1b showing the most prominent expression among them. Additionally, the promoter regions of the zebrafish rc3h genes contained numerous transcription factor binding sites similar to those of mammalian homologs. Moreover, the interaction protein network of Roquin and the potential binding motif in the 3’-UTR of putative target genes analysis both indicated that Roquins have the potential to degrade target mRNA through mechanisms similar to those of mammalian homologs. These findings shed light on the evolutionary history of Roquin among metazoans and hypothesized their role in the immune systems of zebrafish.

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The evolution and immunomodulatory role of Zc3h12 proteins in zebrafish (Danio rerio)

Cited by 2 publications

References 64 publications

MCPIP1 functions as a safeguard of early embryonic development

MCPIP1 functions as a safeguard of early embryonic development

Bioinformatic Analysis of Roquin Family Reveals Their Potential Role in Immune System

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