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Expression Profiles of Vpx/Vpr Proteins Are Co-Related with The fmicb-07-01211 July 30, 2016 Time: 14:6 # 1 ORIGINAL RESEARCH published: 03 August 2016 doi: 10.3389/fmicb.2016.01211 Expression Profiles of Vpx/Vpr Proteins Are Co-related with the Primate Lentiviral Lineage Yosuke Sakai1, Ariko Miyake2, Naoya Doi1, Hikari Sasada1, Yasuyuki Miyazaki3, Akio Adachi1* and Masako Nomaguchi1* 1 Department of Microbiology, Tokushima University Graduate School of Medical Science, Tokushima, Japan, 2 Laboratory of Molecular Immunology and Infectious Disease, Joint Faculty of Veterinary Medicine, Yamaguchi University, Yamaguchi, Japan, 3 Department of Microbiology and Cell Biology, Tokyo Metropolitan Institute of Medical Science, Tokyo, Japan Viruses of human immunodeficiency virus type 2 (HIV-2) and some simian immunodeficiency virus (SIV) lineages carry a unique accessory protein called Vpx. Vpx is essential or critical for viral replication in natural target cells such as macrophages and T lymphocytes. We have previously shown that a poly-proline motif (PPM) located at the C-terminal region of Vpx is required for its efficient expression in two strains of HIV-2 and SIVmac, and that the Vpx expression levels of the two clones are significantly different. Notably, the PPM sequence is conserved and confined to Vpx and Vpr proteins derived from certain lineages of HIV-2/SIVs. In this study, Vpx/Vpr proteins from diverse Edited by: Akihide Ryo, primate lentiviral lineages were experimentally and phylogenetically analyzed to obtain Yokohama City University, Japan the general expression picture in cells. While both the level and PPM-dependency of Reviewed by: Vpx/Vpr expression in transfected cells varied among viral strains, each viral group, Mikako Fujita, based on Vpx/Vpr amino acid sequences, was found to exhibit a characteristic Kumamoto University, Japan Mako Toyoda, expression profile. Moreover, phylogenetic tree analyses on Gag and Vpx/Vpr proteins Kumamoto University, Japan gave essentially the same results. Taken together, our study described here suggests *Correspondence: that each primate lentiviral lineage may have developed a unique expression pattern of Akio Adachi [email protected] Vpx/Vpr proteins for adaptation to its hostile cellular and species environments in the Masako Nomaguchi process of viral evolution. [email protected] Keywords: HIV-2, SIV, Vpx, Vpr, PPM Specialty section: This article was submitted to Virology, INTRODUCTION a section of the journal Frontiers in Microbiology Human immunodeficiency virus types 1 and 2 (HIV-1 and HIV-2) are believed to be generated Received: 21 April 2016 by extensive cross-species and/or intra-species transmissions of naturally occurring lentiviruses Accepted: 20 July 2016 in African primates (Sharp and Hahn, 2011). To date, more than 40 primate species in Africa Published: 03 August 2016 have been reported to harbor lentiviruses, structurally similar to HIV-1 and HIV-2 (Sharp and Citation: Hahn, 2011). Although the evolution and phylogeny of these viruses have been shown to be Sakai Y, Miyake A, Doi N, Sasada H, complicated (Sharp and Hahn, 2011; Shaw and Hunter, 2012; Swanstrom and Coffin, 2012), there Miyazaki Y, Adachi A and are currently eight main lineages in HIV/simian immunodeficiency viruses (SIVs) (Peeters and Nomaguchi M (2016) Expression Courgnaud, 2002; Gordon et al., 2005)(Figure 1A). The genomes of various HIV/SIVs individually Profiles of Vpx/Vpr Proteins Are Co-related with the Primate Lentiviral contain a unique set of accessory genes designated nef, vif, vpu, vpr and vpx (Figure 1B). Accessory Lineage. Front. Microbiol. 7:1211. proteins encoded by these genes mainly function to inactivate host restriction factors, and thus doi: 10.3389/fmicb.2016.01211 optimize viral replication (Blanco-Melo et al., 2012; Harris et al., 2012; Malim and Bieniasz, 2012; Frontiers in Microbiology | www.frontiersin.org 1 August 2016 | Volume 7 | Article 1211 fmicb-07-01211 July 30, 2016 Time: 14:6 # 2 Sakai et al. Phylogenetic Analysis of Vpx/Vpr Expression Simon et al., 2015). While all HIV/SIVs commonly have nef, MATERIALS AND METHODS vif and vpr genes, vpu and vpx genes are unique to some viral lineages. Upon directing at the vpx, vpr, and vpu genes, Virus Origins various HIV/SIVs can be grouped into three types (Fujita et al., Origins of SIVs are as follows (see also Figure 1). Prototype 2010)(Figure 1B): prototype viruses with vpr only; HIV-1 type viruses: SIVagm (isolated from the African green monkey); viruses carrying vpr and vpu; HIV-2 type viruses carrying vpr SIVmnd-1 (mandrill); SIVlst (l’Hoest’s monkey); SIVsun (sun- and vpx. Thus, vpx and vpu are unique to HIV-2 type and tailed monkey); SIVsyk (Sykes’ monkey); SIVdeb (DeBrazza’s HIV-1 type viruses, respectively. Of note, Vpr and Vpx proteins monkey); SIVtal (talapoin monkey); SIVasc (red-tailed guenon); show significant structural and functional similarities (Khamsri SIVcol (colobus monkey); SIVwrc (western red colobus); et al., 2006; Ayinde et al., 2010; Fujita et al., 2010). Among the SIVolc (olive colobus); SIVkrc (Kibale red colobus). HIV-1 major HIV/SIV lineages, viruses of the two groups, i.e., HIV- type viruses: SIVcpz (chimpanzee); SIVgor (gorilla); SIVgsn 2/SIVsmm/stm/mac and SIVrcm/SIVdrl/mnd-2 (Figure 1A), (greater spot-nosed monkey); SIVmon (mona monkey); SIVmus have both Vpx and Vpr (Figure 1B). (mustached monkey); SIVden (Dent’s monkey). HIV-2 type Vpx is a virion-associated protein of 12–16 kDa, and exerts viruses: SIVsmm (sooty mangabey monkey); SIVmac (macaque its function in the early stage of infection. Without functional monkey); SIVstm (stump-tailed macaque); SIVrcm (red-capped Vpx, HIV-2 type viruses are unable or impeded to grow in mangabey); SIVmnd-2 (mandrill); SIVdrl (drill monkey). natural target cells (Fujita et al., 2010). Recently, a cellular anti- viral factor SAMHD1 has been identified as target for Vpx Plasmids (Hrecka et al., 2011; Laguette et al., 2011). However, a SAMHD1- FLAG-tagged pEF-F expression plasmids for HIV-2 GL- independent mechanism(s) is still likely to exist (Fujita et al., AN Vpx (Genbank accession no., M30895), SIVmac239 2012; Nomaguchi et al., 2014a; Schaller et al., 2014). From a Vpx (M33262), and their d7P (a complete deletion of structural point of view, although Vpx and Vpr are closely seven consecutive prolines) mutants have been previously related and comprise three helices as described above, they described (Miyake et al., 2014a). To generate new FLAG- are distinct from each other. Vpx has a zinc finger motif that tagged expression plasmids for Vpx/Vpr proteins in this stabilizes the helical structure (Schwefel et al., 2014), which is study, vpx and vpr genes were synthesized (GenScript) not present in Vpr. Notably, there is a well-conserved poly- and cloned into pEF-F as described above. New Vpx and proline motif (PPM), consisting of seven consecutive prolines, Vpr proteins analyzed in this study are as follows (see also at the C-terminus of HIV-2 and SIVmac Vpx proteins (Miyake Figure 2): HIV-2 ALI Vpx (AF082339); HIV-2 EHO Vpx et al., 2014a). We previously showed that an HIV-2 mutant virus (U27200); HIV-2 Abt96 Vpx (AF208027); SIVsmm PGM53 carrying multi-substitutional mutations in the PPM sequence Vpx (AF077017); SIVstm 37_16 Vpx (M83293); SIVsmm did not grow at all in human macrophages and grew much SL92B Vpx (AF334679); SIVmac 251BK28 Vpx (M19499); more poorly than wild-type (WT) virus in a simian T-cell SIVrcm 02CM8081 Vpx (HM803689); SIVrcm GAB1 Vpx line, exactly like a Vpx-minus mutant (Fujita et al., 2008). (AF382829); SIVrcm NG411 Vpx (AF349680); SIVdrl FAO Subsequent molecular studies demonstrated that PPM enhanced Vpx (AY159321); SIVmnd-2 M14 Vpx (AF328295); SIVmnd-2 Vpx expression at a translation level, not influencing the stability 5440 Vpx (AY159322); SIVagm VER AGM3 Vpr (M30931); of the protein (Miyake et al., 2014a,b). Our previous work also SIVagm TYO1 Vpr (DJ048201); SIVagm VER AGM155 Vpr showed that HIV-1 and HIV-2 Vpr proteins were expressed (M29975); SIVagm VER 9063 Vpr (L40990); SIVagm GRI at a much lower level relative to HIV-2 Vpx, and that the 677 Vpr (M66437). PPM-deletion mutants were constructed expression level of the two Vpr proteins was not enhanced by the QuikChange site-directed mutagenesis kit (Agilent significantly by simply adding the HIV-2 Vpx PPM sequence Technologies) or by overlap extension PCR using WT clones as (Miyake et al., 2014a). Furthermore, despite a high overall templates. homology of HIV-2 Vpx and SIVmac Vpx, their expression levels in transfected cells were significantly different (Miyake et al., 2014a). Transfection In this report, we performed a linkage study between Human kidney 293T cells used for transfection experiments the Vpx expression profiles and viral phylogeny. Expression were cultured and maintained as previously described plasmids for a wide variety of Vpx proteins derived from (Miyake et al., 2014a). For transfection, 4.0 mg of diverse primate immunodeficiency viruses (Figure 1) were each plasmid DNA was introduced into 293T cells constructed, and monitored for their expression levels and by 9.0 ml of Lipofectamine 2000 (Thermo Fisher PPM-dependency on the protein expression in transfected cells Scientific). using SIVagm Vpr proteins as comparative controls. In parallel, phylogenetic trees based on Vpx/Vpr and Gag amino acid Western Blotting sequences were constructed to determine viral evolutionary Western blot analysis of transfected cell lysates using anti- relationships. The results obtained show that each viral lineage FLAG M2 antibody (Sigma) or anti-b-actin AC-15 antibody has its characteristic expression property, suggesting a link (Sigma) was conducted as described previously (Miyake et al., between the Vpx/Vpr expression pattern and viral evolutionary 2014a,b). Briefly, supernatants of cell lysates were prepared position. at 24 h post-transfection, and normalized for total protein Frontiers in Microbiology| www.frontiersin.org 2 August 2016| Volume 7| Article 1211 fmicb-07-01211 July 30, 2016 Time: 14:6 # 3 Sakai et al.
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