Co-evolution of primate SAMHD1 and lentivirus Vpx leads to the loss of the vpx gene in HIV-1 ancestor

Chiyu Zhang; Suresh de Silva; Jian-Hua Wang; Li Wu

doi:10.1371/journal.pone.0037477

Back

Co-evolution of primate SAMHD1 and lentivirus Vpx leads to the loss of the vpx gene in HIV-1 ancestor

Journal article

Open access

Peer reviewed

Co-evolution of primate SAMHD1 and lentivirus Vpx leads to the loss of the vpx gene in HIV-1 ancestor

Chiyu Zhang, Suresh de Silva, Jian-Hua Wang and Li Wu

PloS one, Vol.7(5), pp.e37477-e37477

2012

DOI: 10.1371/journal.pone.0037477

PMCID: PMC3345027

PMID: 22574228

Files and links (1)

url

https://doi.org/10.1371/journal.pone.0037477View

Published (Version of record) Open Access

Abstract

Cross-species transmission and adaptation of simian immunodeficiency viruses (SIVs) to humans have given rise to human immunodeficiency viruses (HIVs). HIV type 1 (HIV-1) and type 2 (HIV-2) were derived from SIVs that infected chimpanzee (SIVcpz) and sooty mangabey (SIVsm), respectively. The HIV-1 restriction factor SAMHD1 inhibits HIV-1 infection in human myeloid cells and can be counteracted by the Vpx protein of HIV-2 and the SIVsm lineage. However, HIV-1 and its ancestor SIVcpz do not encode a Vpx protein and HIV-1 has not evolved a mechanism to overcome SAMHD1-mediated restriction. Here we show that the co-evolution of primate SAMHD1 and lentivirus Vpx leads to the loss of the vpx gene in SIVcpz and HIV-1. We found evidence for positive selection of SAMHD1 in orangutan, gibbon, rhesus macaque, and marmoset, but not in human, chimpanzee and gorilla that are natural hosts of Vpx-negative HIV-1, SIVcpz and SIVgor, respectively, indicating that vpx drives the evolution of primate SAMHD1. Ancestral host state reconstruction and temporal dynamic analyses suggest that the most recent common ancestor of SIVrcm, SIVmnd, SIVcpz, SIVgor and HIV-1 was a SIV that had a vpx gene; however, the vpx gene of SIVcpz was lost approximately 3643 to 2969 years ago during the infection of chimpanzees. Thus, HIV-1 could not inherit the lost vpx gene from its ancestor SIVcpz. The lack of Vpx in HIV-1 results in restricted infection in myeloid cells that are important for antiviral immunity, which could contribute to the AIDS pandemic by escaping the immune responses.

Humans

Viral Regulatory and Accessory Proteins - genetics

SAM Domain and HD Domain-Containing Protein 1

Selection, Genetic

Viral Proteins - genetics

Primates - virology

Monomeric GTP-Binding Proteins - genetics

Phylogeny

HIV-1 - genetics

Simian Immunodeficiency Virus - physiology

Primates - genetics

Simian Immunodeficiency Virus - genetics

Animals

Evolution, Molecular

Details

Title: Subtitle: Co-evolution of primate SAMHD1 and lentivirus Vpx leads to the loss of the vpx gene in HIV-1 ancestor
Creators: Chiyu Zhang - Institute of Life Sciences, Jiangsu University, Zhenjiang, Jiangsu, China. zhangcy1999@ips.ac.cn
Suresh de Silva
Jian-Hua Wang
Li Wu
Resource Type: Journal article
Publication Details: PloS one, Vol.7(5), pp.e37477-e37477
DOI: 10.1371/journal.pone.0037477
PMID: 22574228
PMCID: PMC3345027
NLM abbreviation: PLoS One
ISSN: 1932-6203
eISSN: 1932-6203
Publisher: Public Library of Science; United States
Grant note: R21 AI102822 / NIAID NIH HHS R21 AI078762 / NIAID NIH HHS AI078762 / NIAID NIH HHS R21 AI098524 / NIAID NIH HHS AI098524 / NIAID NIH HHS
Language: English
Date published: 2012
Academic Unit: Microbiology and Immunology
Record Identifier: 9984001116302771

Metrics

24 Record Views

33 Times Cited - Web of Science