Genome-Wide Identification and Expression Analysis of Potential Antiviral Tripartite Motif Proteins (TRIMs) in Grass Carp (Ctenopharyngodon idella).

Beibei Qin,Chunhua Ding,Zhao Lv,Yadong Deng,Jianming Su,Tiaoyi Xiao

doi:10.3390/biology10121252

Abstract

Simple SummaryGrass carp, Ctenopharyngodon idellus, is an important freshwater cultured teleost in China, and its annual production has reached 5,533,083 tons. However, its aquaculture is severely restricted by hemorrhagic disease caused by the grass carp reovirus (GCRV). For the better control of grass carp hemorrhagic disease, the breeding of resistant grass carp strains based on antiviral immune molecule markers is a potential solution. However, the molecular basis of grass carp’s resistance to GCRV infection remains largely unknown, greatly limiting the breeding of grass carp resistant to hemorrhagic disease. Given the importance of tripartite motif proteins (TRIMs) in animal antiviral immunity, we used the Hidden Markov Model Biological Sequence Analysis software (HMMER) and SMART to identify TRIMs in the grass carp genome and analyze their gene loci, as well as structural and evolutionary features. We also tried to uncover antiviral TRIMs and their mediated immune processes based on two sets of transcriptomes during GCRV infection in grass carp. This study provides information for the understanding of TRIMs and antiviral immunity in grass carp.Tripartite motif proteins (TRIMs), especially B30.2 domain-containing TRIMs (TRIMs-B30.2), are increasingly well known for their antiviral immune functions in mammals, while antiviral TRIMs are far from being identified in teleosts. In the present study, we identified a total of 42 CiTRIMs from the genome of grass carp, Ctenopharyngodon idella, an important cultured teleost in China, based on hmmsearch and SMART analysis. Among these CiTRIMs, the gene loci of 37 CiTRIMs were located on different chromosomes and shared gene collinearities with homologous counterparts from human and zebrafish genomes. They possessed intact conserved RBCC or RB domain assemblies at their N-termini and eight different domains, including the B30.2 domain, at their C-termini. A total of 19 TRIMs-B30.2 were identified, and most of them were clustered into a large branch of CiTRIMs in the dendrogram. Tissue expression analysis showed that 42 CiTRIMs were universally expressed in various grass carp tissues. A total of 11 significantly differentially expressed CiTRIMs were found in two sets of grass carp transcriptomes during grass carp reovirus (GCRV) infection. Three of them, including Cibtr40, CiTRIM103 and CiTRIM109, which all belonged to TRIMs-B30.2, were associated with the type I interferon response during GCRV infection by weighted network co-expression and gene expression trend analyses, suggesting their involvement in antiviral immunity. These findings may offer useful information for understanding the structure, evolution, and function of TRIMs in teleosts and provide potential antiviral immune molecule markers for grass carp.

Highlights

Tripartite motif proteins (TRIMs) are generally characterized by three domains at theN-terminus, including a RING finger domain, one or two B-box domains and a coiledcoil domain, and are known as the RING finger/B-box/coiled-coil (RBCC) domaincontaining proteins [1,2]
A total of 42 CiTRIMs were identified in the grass carp genome with hmmsearch and SMART analysis according to this criterion (Table 2)
37 CiTRIMs were named and numbered with reference to their homologous counterparts from the genomes of zebrafish and humans based on sequence similarity and identity, while five CiTRIMs, including CiTRIM35-50, CiTRIM39-like, CiTRIM111, CiTRIM112 and Cibtr40, whose homologs were not identified in the genomes from zebrafish and humans, and could be found in the teleost genomes of Pimephales promelas and Sinocyclocheilus anshuiensis by BLAST search (Table 2), were given names referring to the nomenclature previously described [10]

Summary

Introduction

Tripartite motif proteins (TRIMs) are generally characterized by three domains at theN-terminus, including a RING finger domain, one or two B-box domains and a coiledcoil domain, and are known as the RING finger/B-box/coiled-coil (RBCC) domaincontaining proteins [1,2]. The complete RBCC domain assemblies have only been discovered in TRIM family proteins from metazoa, such as arthropods, teleosts, amphibians, birds and mammals [4,5,6,7]. The RBCC or RB domain assemblies appear to be conserved in animals, almost every species has more than one TRIM or a specific repertoire of TRIMs, all of which, together, constitute a large protein family with highly variable sequences [4,10]. These TRIM family proteins play multiple roles in animal tissue development [11], metabolism and autophagy [12], transcriptional regulation [13], tumor suppression [14] and viral restriction [15]

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Conclusion