Dynamic Evolution of Retroviral Envelope Genes in Egg-Laying Mammalian Genomes

Author:

Kitao Koichi1,Shoji Hiyori1,Miyazawa Takayuki1,Nakagawa So234ORCID

Affiliation:

1. Laboratory of Virus-Host Coevolution, Institute for Frontier Life and Medical Sciences, Kyoto University , Sakyo-ku, Kyoto , Japan

2. Department of Molecular Life Science, Tokai University School of Medicine , Isehara, Kanagawa , Japan

3. Division of Genome Sciences, Institute of Medical Sciences, Tokai University , Isehara, Kanagawa , Japan

4. Division of Interdisciplinary Merging of Health Research, Micro/Nano Technology Center, Tokai University , Hiratsuka, Kanagawa , Japan

Abstract

AbstractIndependently acquired envelope (env) genes from endogenous retroviruses have contributed to the placental trophoblast cell–cell fusion in therian mammals. Egg-laying mammals (monotremes) are an important sister clade for understanding mammalian placental evolution, but the env genes in their genomes have yet to be investigated. Here, env-derived open reading frames (env-ORFs) encoding more than 400 amino acid lengths were searched in the genomes of two monotremes: platypus and echidna. Only two env-ORFs were present in the platypus genome, whereas 121 env-ORFs were found in the echidna genome. The echidna env-ORFs were phylogenetically classified into seven groups named env-Tac1 to -Tac7. Among them, the env-Tac1 group contained only a single gene, and its amino acid sequence showed high similarity to those of the RD114/simian type D retroviruses. Using the pseudotyped virus assay, we demonstrated that the Env-Tac1 protein utilizes echidna sodium-dependent neutral amino acid transporter type 1 and 2 (ASCT1 and ASCT2) as entry receptors. Moreover, the Env-Tac1 protein caused cell–cell fusion in human 293T cells depending on the expression of ASCT1 and ASCT2. These results illustrate that fusogenic env genes are not restricted to placental mammals, providing insights into the evolution of retroviral genes and the placenta.

Publisher

Oxford University Press (OUP)

Subject

Genetics,Molecular Biology,Ecology, Evolution, Behavior and Systematics

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