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Characterization of red-capped mangabey tetherin: implication for the co-evolution of primates and their lentiviruses.

ABSTRACT: Primate lentiviruses including human immunodeficiency virus type 1 (HIV-1) and simian immunodeficiency viruses (SIVs) evolved through the acquisition of antagonists against intrinsic host restriction factors, such as tetherin. It is widely accepted that HIV-1 has emerged by zoonotic transmission of SIV in chimpanzee (SIVcpz), and that SIVcpz Nef protein antagonizes chimpanzee tetherin. Although Nef of SIVcpz shares a common ancestor with that of SIVrcm, an SIV in red-capped mangabey (Cercocebus torquatus), it remains unclear whether SIVrcm Nef can antagonize tetherin of its natural host. In this study, we determine the sequence of red-capped mangabey tetherin for the first time and directly demonstrate that SIVrcm Nef is the bona fide antagonist of red-capped mangabey tetherin. These findings suggest that SIVrcm Nef is the functional ancestor of SIVcpz Nef. Moreover, molecular phylogenetic analyses reveal that tetherins of the genus Cercocebus have experienced adaptive evolution, which is presumably promoted by primate lentiviruses.

SUBMITTER: Kobayashi T

PROVIDER: S-EPMC4078312 | biostudies-literature | 2014 Jul

REPOSITORIES: biostudies-literature

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Characterization of red-capped mangabey tetherin: implication for the co-evolution of primates and their lentiviruses.

Kobayashi Tomoko T Takeuchi Junko S JS Ren Fengrong F Matsuda Kenta K Sato Kei K Kimura Yuichi Y Misawa Naoko N Yoshikawa Rokusuke R Nakano Yusuke Y Yamada Eri E Tanaka Hiroshi H Hirsch Vanessa M VM Koyanagi Yoshio Y

Scientific reports 20140702

Primate lentiviruses including human immunodeficiency virus type 1 (HIV-1) and simian immunodeficiency viruses (SIVs) evolved through the acquisition of antagonists against intrinsic host restriction factors, such as tetherin. It is widely accepted that HIV-1 has emerged by zoonotic transmission of SIV in chimpanzee (SIVcpz), and that SIVcpz Nef protein antagonizes chimpanzee tetherin. Although Nef of SIVcpz shares a common ancestor with that of SIVrcm, an SIV in red-capped mangabey (Cercocebus ...[more]

PMID: 24984862

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Project description:Bats are recognized as important reservoirs of viruses deadly to other mammals, including humans. These infections are typically nonpathogenic in bats, raising questions about host response differences that might exist between bats and other mammals. Tetherin is a restriction factor which inhibits the release of a diverse range of viruses from host cells, including retroviruses, coronaviruses, filoviruses, and paramyxoviruses, some of which are deadly to humans and transmitted by bats. Here, we characterize the tetherin genes from 27 bat species, revealing that they have evolved under strong selective pressure, and that fruit bats and vesper bats express unique structural variants of the tetherin protein. Tetherin was widely and variably expressed across fruit bat tissue types and upregulated in spleen tissue when stimulated with Toll-like receptor agonists. The expression of two computationally predicted splice isoforms of fruit bat tetherin was verified. We identified an additional third unique splice isoform which includes a C-terminal region that is not homologous to known mammalian tetherin variants but was functionally capable of restricting the release of filoviral virus-like particles. We also report that vesper bats possess and express at least five tetherin genes, including structural variants, more than any other mammal reported to date. These findings support the hypothesis of differential antiviral gene evolution in bats relative to other mammals. IMPORTANCE Bats are an important host of various viruses which are deadly to humans and other mammals but do not cause outward signs of illness in bats. Furthering our understanding of the unique features of the immune system of bats will shed light on how they tolerate viral infections, potentially informing novel antiviral strategies in humans and other animals. This study examines the antiviral protein tetherin, which prevents viral particles from escaping their host cell. Analysis of tetherin from 27 bat species reveals that it is under strong evolutionary pressure, and we show that multiple bat species have evolved to possess more tetherin genes than other mammals, some of which encode structurally unique tetherins capable of activity against different viral particles. These data suggest that bat tetherin plays a potentially broad and important role in the management of viral infections in bats.

Dataset Information

Characterization of red-capped mangabey tetherin: implication for the co-evolution of primates and their lentiviruses.

Publications

Characterization of red-capped mangabey tetherin: implication for the co-evolution of primates and their lentiviruses.

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