Evolution of Teleost Fish Retroviruses: Characterization of New Retroviruses with Cellular Genes

Abstract

The interactions between retroviruses and their hosts can be of a beneficial or detrimental nature. Some endogenous retroviruses are involved in development, while others cause disease. The Genome Parsing Suite (GPS) is a software tool to track and trace all Retroid agents in any sequenced genome (M. A. McClure et al., Genomics 85:512-523, 2005). Using the GPS, the retroviral content was assessed in four model teleost fish. Eleven new species of fish retroviruses are identified and characterized. The reverse transcriptase protein sequences were used to reconstruct a fish retrovirus phylogeny, thereby, significantly expanding the epsilonretrovirus family. Most of these novel retroviruses encode additional genes, some of which are homologous to cellular genes that would confer viral advantage. Although the fish divergence is much more ancient, retroviruses began infecting fish genomes approximately 4 million years ago.All genetic entities that encode the reverse transcriptase (RT) enzyme are referred to as retroids (22). The formal retroid classification includes endogenous and exogenous retroviruses, as well as pararetroviruses (large DNA viruses), retrotransposons with long terminal repeats (LTRs), retroposons that lack LTRs, retroplasmids, retrointrons, and retrons (20,21,43,44). This classification is based on the phylogeny of the RT protein sequence, the slowest evolving of the retroid gene components (30). In a global analysis of the retroid content of the genomes of the teleost fish Danio rerio (zebrafish), Oryzias latipes (medaka), Gasterosteus aculeatus (stickleback), and Tetraodon nigroviridis (green spotted pufferfish), we identified several new retroviruses (7). Here, we expand those studies, report the genomic details of 11 new fish retroviral species, and provide a reconstruction of the evolutionary history of sequenced fish retroviruses.In general, retroviruses are classified as alpha-, beta-, gamma-, delta-, and epsilonretroviruses, lentiviruses, and spumaviruses. The current characterization of known exogenous and endogenous fish retroviruses places them in the epsilon family (http: //www.ncbi.nlm.nih.gov/ICTVdb/) or between this group and the gammaretroviruses (36). To date, only three members of the epsilon family have been conclusively identified, i.e., walleye dermal sarcoma virus (WDSV) and the walleye epidermal hyperplasia viruses 1 and 2 (WEHV1 and WEHV2), and tentative members include perch hyperplasia virus and snakehead fish retrovirus (SnRV), (http://www.ncbi.nlm.nih.gov/ICTVdb/). Other fish retroviruses include the Atlantic salmon swim bladder sarcoma virus (SSSV) and zebrafish endogenous retrovirus (ZFERV) from D. rerio; both appear to fall between the gamma and epsilon families (36). Studied in less detail is the ERV_Tet species in T. nigroviridis (15), and the retrovirusstickleback (RV-stickleback), RV-brook trout, RV-freshwater houting, and RV-pufferfish retroviruses only identified by using PCR (17).WDSV is associated with the development of seasonal tumors in walleye and, along w...

Phosphorylation of Herpes Simplex Virus 1 dUTPase Upregulated Viral dUTPase Activity To Compensate for Low Cellular dUTPase Activity for Efficient Viral Replication

“…NA viruses and a subset of retroviruses are known to encode homologs of host cell enzymes involved in nucleotide metabolism (e.g., thymidine kinase [TK], ribonucleotide reductase, uracil-DNA glycosylase, and/or dUTPase), which are mostly not essential for viral replication in cell cultures (1)(2)(3)(4)(5)(6)(7). Of these, viral dUTPase (vdUTPase) is of special interest because it is the homolog most widely encoded by viruses (3,(7)(8)(9).…”

A Novel Recombinant Retrovirus in the Genomes of Modern Birds Combines Features of Avian and Mammalian Retroviruses

“…Retroviruses are most commonly analyzed according to phylogenetic relationships of the highly conserved reverse transcriptase (RT) region of pol (7)(8)(9)(10)(11), rather than env. In phylogenetic analyses of the RT region, ERVs cluster into three broad classes that include the known exogenous retroviruses: class I includes gamma-and epsilonretroviruses; class II, beta-, delta-, and alpharetroviruses and lentiviruses; and class III, spumaretroviruses (10).…”

Retroviruses of wild and cultured fish

“…Genetic analysis has shown that fish retroviruses are a highly diverse group compared to other retroviruses (Basta et al 2009). Some of the fish retroviruses exhibit unique features, such as those associated with skin tumors in walleyes which encode cyclin homologs.…”

“…All genetic elements that contain a gene encoding reverse transcriptase (RT) are referred to as retroelements or retroids (Hull 2001, Basta et al 2009). According to the classification proposed by Hull (2001) retroelements comprise two major groups, Retrovirales which consist viral elements and Retrales containing non-viral elements.…”

“…Epsilonretrovirus is the most recent genus added to the family Retroviridae and comprises three fish retroviruses: walleye dermal sarcoma virus (WDSV) and Salmon leukemia virus SLV Oncorhynchus tshawytscha Snakehead retrovirus SnRV Ophicephalus striatus Frerichs et al 1991 Zebrafish endogenous retrovirus ZFERV Danio rerio Shen and Steiner 2002 walleye epidermal hyperplasia viruses type 1 and type 2 (WEHV-1, WEHV-2). Other fish retroviruses have not yet been assigned to a specific genus (Basta et al 2009). The summary data for fish retroviruses are shown in Table 1.…”