DOI: 10.1099/vir.0.011726-0. Human immunodeficiency virus type 1 Vpr: functions and molecular interactions

Human immunodeficiency virus type 1 Vpr: functions and molecular interactions

10.1099/vir.0.011726-0

Crossref journal-article

Microbiology Society

Journal of General Virology (345)

Abstract

Human immunodeficiency virus type 1 (HIV-1) viral protein R (Vpr) is an accessory protein that interacts with a number of cellular and viral proteins. The functions of many of these interactions in the pathogenesis of HIV-1 have been identified. Deletion of thevprgene reduces the virulence of HIV-1 dramatically, indicating the importance of this protein for the virus. This review describes the current findings on several established functions of HIV-1 Vpr and some possible roles proposed for this protein. Because Vpr exploits cellular proteins and pathways to influence the biology of HIV-1, understanding the functions of Vpr usually involves the study of cellular pathways. Several functions of Vpr are attributed to the virion-incorporated protein, but some of them are attributed to the expression of Vpr in HIV-1-infected cells. The structure of Vpr may be key to understanding the variety of its interactions. Due to the critical role of Vpr in HIV-1 pathogenicity, study of the interactions between Vpr and cellular proteins may help us to understand the mechanism(s) of HIV-1 pathogenicity.

Bibliography

Romani, B., & Engelbrecht, S. (2009). Human immunodeficiency virus type 1 Vpr: functions and molecular interactions. Journal of General Virology, 90(8), 1795â1805.

Authors 2

Bizhan Romani (first)
Susan Engelbrecht (additional)

References 108 Referenced 43

10.1006/jmbi.1996.0485 / J Mol Biol / The human immunodeficiency virus type 1 Vpr transactivator: cooperation with promoter-bound activator domains and binding to TFIIB by Agostini (1996)
10.1016/S0014-5793(99)00501-3 / FEBS Lett / The HIV-1 Vpr co-activator induces a conformational change in TFIIB by Agostini (1999)
10.2174/1570162052772988 / Curr HIV Res / The role of Vpr in HIV-1 pathogenesis by Andersen (2005)
10.1016/j.yexmp.2008.03.015 / Exp Mol Pathol / HIV-1 Vpr: mechanisms of G2 arrest and apoptosis by Andersen (2008)
10.1007/s11904-004-0007-x / Curr HIV/AIDS Rep / HIV accessory proteins and surviving the host cell by Anderson (2004)
10.1023/A:1026487609215 / Apoptosis / A C-terminal domain of HIV-1 accessory protein Vpr is involved in penetration, mitochondrial dysfunction and apoptosis of human CD4+ lymphocytes by Arunagiri (1997)
10.1093/intimm/14.1.13 / Int Immunol / HIV-1 viral protein R compromises cellular function in vivo by Ayyavoo (2002)
10.1074/jbc.274.13.9083 / J Biol Chem / Incorporation of Vpr into human immunodeficiency virus type 1 requires a direct interaction with the p6 domain of the p55 Gag precursor by Bachand (1999)
10.1152/ajpendo.00163.2006 / Am J Physiol Endocrinol Metab / Effects of transgenic expression of HIV-1 Vpr on lipid and energy metabolism in mice by Balasubramanyam (2007)
10.1084/jem.193.4.F11 / J Exp Med / HIV and apoptosis: death and the mitochondrion by Basanez (2001)
10.1096/fj.07-8697rev / FASEB J / Reverse transcription of the HIV-1 pandemic by Basavapathruni (2007)
10.1371/journal.ppat.0030085 / PLoS Pathog / HIV-1 Vpr-mediated G2 arrest involves the DDB1–CUL4AVPRBP E3 ubiquitin ligase by Belzile (2007)
10.1186/1742-4690-4-16 / Retrovirology / Antagonistic interaction of HIV-1 Vpr with Hsf-mediated cellular heat shock response and Hsp16 in fission yeast ( Schizosaccharomyces pombe ) by Benko (2007)
10.1097/00002030-200409030-00022 / AIDS / APOBEC3G versus reverse transcriptase in the generation of HIV-1 drug-resistance mutations by Berkhout (2004)
10.1128/JVI.70.2.697-704.1996 / J Virol / Human immunodeficiency virus type 1 Vpr protein binds to the uracil DNA glycosylase DNA repair enzyme by Bouhamdan (1996)
10.1074/jbc.273.14.8009 / J Biol Chem / Diversity of HIV-1 Vpr interactions involves usage of the WXXF motif of host cell proteins by Bouhamdan (1998)
10.1146/annurev.cellbio.15.1.269 / Annu Rev Cell Dev Biol / Biochemical pathways of caspase activation during apoptosis by Budihardjo (1999)
10.1007/BF02253252 / J Biomed Sci / Differential apoptosis effects of primate lentiviral Vpr and Vpx in mammalian cells by Chang (2000)
10.1091/mbc.e03-09-0691 / Mol Biol Cell / HIV-1 Vpr induces defects in mitosis, cytokinesis, nuclear structure, and centrosomes by Chang (2004)
10.1099/0022-1317-83-10-2339 / J Gen Virol / Roles of uracil–DNA glycosylase and dUTPase in virus replication by Chen (2002)
10.1074/jbc.M403875200 / J Biol Chem / Vpr-mediated incorporation of UNG2 into HIV-1 particles is required to modulate the virus mutation rate and for replication in macrophages by Chen (2004)
10.4049/jimmunol.165.6.3293 / J Immun / Dual role of the HIV-1 Vpr protein in the modulation of the apoptotic response of T cells by Conti (2000)
10.1529/biophysj.106.081240 / Biophys J / Analysis of a generic model of eukaryotic cell-cycle regulation by Csikasz-Nagy (2006)
10.1126/science.1063957 / Science / Dynamic disruptions in nuclear envelope architecture and integrity induced by HIV-1 Vpr by de Noronha (2001)
10.1006/viro.2001.1007 / Virology / HIV-1 Vpr induces cell cycle G2 arrest in fission yeast ( Schizosaccharomyces pombe ) through a pathway involving regulatory and catalytic subunits of PP2A and acting on both Wee1 and Cdc25 by Elder (2001)
10.1046/j.1432-1033.2001.01895.x / Eur J Biochem / Solution structure of human immunodeficiency virus type 1 Vpr (13–33) peptide in micelles by Engler (2001)
10.1073/pnas.95.9.5281 / Proc Natl Acad Sci U S A / HIV transcriptional activation by the accessory protein, VPR, is mediated by the p300 co-activator by Felzien (1998)
10.1128/JVI.70.2.1027-1032.1996 / J Virol / Role of the karyopherin pathway in human immunodeficiency virus type 1 nuclear import by Gallay (1996)
10.1073/pnas.94.18.9825 / Proc Natl Acad Sci U S A / HIV-1 infection of nondividing cells through the recognition of integrase by the importin/karyopherin pathway by Gallay (1997)
10.1074/jbc.M610056200 / J Biol Chem / Insights into the multiple roles of pausing in HIV-1 reverse transcriptase-promoted strand transfers by Gao (2007)
10.1101/gad.12.19.2973 / Genes Dev / The complexity of p53 modulation: emerging patterns from divergent signals by Giaccia (1998)
10.1007/BF01279896 / Protoplasma / Cullins and cell cycle control by Gieffers (2000)
10.1038/nm0198-065 / Nat Med / HIV-1 Vpr increases viral expression by manipulation of the cell cycle: a mechanism for selection of Vpr in vivo by Goh (1998)
10.1016/j.virol.2003.10.007 / Virology / The human immunodeficiency virus Vpr protein binds Cdc25C: implications for G2 arrest by Goh (2004)
10.1016/S0092-8674(00)00003-9 / Cell / Apoptotic pathways: paper wraps stone blunts scissors by Green (2000)
10.1128/JVI.69.11.6705-6711.1995 / J Virol / Human immunodeficiency virus type 1 viral protein R (Vpr) arrests cells in the G2 phase of the cell cycle by inhibiting p34cdc2 activity by He (1995)
10.1186/1747-1028-2-5 / Cell Div / Stealing the spotlight: CUL4–DDB1 ubiquitin ligase docks WD40-repeat proteins to destroy by Higa (2007)
10.1073/pnas.0702102104 / Proc Natl Acad Sci U S A / Lentiviral Vpr usurps Cul4–DDB1[VprBP] E3 ubiquitin ligase to modulate cell cycle by Hrecka (2007)
10.3109/13550280009015823 / J Neurovirol / Effects of extracellular human immunodeficiency virus type 1 Vpr protein in primary rat cortical cell cultures by Huang (2000)
10.1128/JVI.01098-07 / J Virol / Human immunodeficiency virus type 1 Vpr induces cell cycle G2 arrest through Srk1/MK2-mediated phosphorylation of Cdc25 by Huard (2008)
10.1084/jem.191.1.33 / J Exp Med / The HIV-1 viral protein R induces apoptosis via a direct effect on the mitochondrial permeability transition pore by Jacotot (2000)
10.1084/jem.193.4.509 / J Exp Med / Control of mitochondrial membrane permeabilization by adenine nucleotide translocator interacting with HIV-1 viral protein R and Bcl-2 by Jacotot (2001)
10.1083/jcb.143.4.875 / J Cell Biol / Characterization of HIV-1 Vpr nuclear import: analysis of signals and pathways by Jenkins (1998)
10.1016/j.molcel.2006.08.010 / Mol Cell / A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1 by Jin (2006)
10.1128/JVI.73.9.7132-7137.1999 / J Virol / The presence of human immunodeficiency virus type 1 Vpr correlates with a decrease in the frequency of mutations in a plasmid shuttle vector by Jowett (1999)
10.1073/pnas.0802203105 / Proc Natl Acad Sci U S A / Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection by Keele (2008)
10.1073/pnas.0507900102 / Proc Natl Acad Sci U S A / Formation of apoptosome is initiated by cytochrome c -induced dATP hydrolysis and subsequent nucleotide exchange on Apaf-1 by Kim (2005)
10.1196/annals.1321.013 / Ann N Y Acad Sci / Human immunodeficiency virus type-1 accessory protein Vpr: a causative agent of the AIDS-related insulin resistance/lipodystrophy syndrome? by Kino (2004)
10.1128/JVI.76.19.9724-9734.2002 / J Virol / Human immunodeficiency virus type 1 (HIV-1) accessory protein Vpr induces transcription of the HIV-1 and glucocorticoid-responsive promoters by binding directly to p300/CBP coactivators by Kino (2002)
10.1128/JVI.79.5.2780-2787.2005 / J Virol / Vpr protein of human immunodeficiency virus type 1 binds to 14-3-3 proteins and facilitates complex formation with Cdc25C: implications for cell cycle arrest by Kino (2005)
10.1128/JVI.02094-07 / J Virol / Human immunodeficiency virus type 1 Vpr inhibits axonal outgrowth through induction of mitochondrial dysfunction by Kitayama (2008)
10.1016/S0960-9822(03)00008-3 / Curr Biol / Evolution of eukaryotic cell cycle regulation: stepwise addition of regulatory kinases and late advent of the CDKs by Krylov (2003)
10.1128/JVI.68.3.1926-1934.1994 / J Virol / Requirement of the Pr55gag precursor for incorporation of the Vpr product into human immunodeficiency virus type 1 viral particles by Lavallee (1994)
10.1186/1742-4690-2-11 / Retrovirology / The Vpr protein from HIV-1: distinct roles along the viral life cycle by Le Rouzic (2005)
10.1074/jbc.M207439200 / J Biol Chem / Docking of HIV-1 Vpr to the nuclear envelope is mediated by the interaction with the nucleoporin hCG1 by Le Rouzic (2002)
10.1128/JVI.71.9.6315-6322.1997 / J Virol / Nucleotide substitutions within U5 are critical for efficient reverse transcription of human immunodeficiency virus type 1 with a primer binding site complementary to tRNAHis by Li (1997)
10.1128/JVI.01979-07 / J Virol / Infection with Vpr-positive human immunodeficiency virus type 1 impairs NK cell function indirectly through cytokine dysregulation of infected target cells by Majumder (2008)
10.1006/viro.1996.0436 / Virology / The mutation rate of human immunodeficiency virus type 1 is influenced by the vpr gene by Mansky (1996)
10.1128/JVI.74.15.7039-7047.2000 / J Virol / The interaction of Vpr with uracil DNA glycosylase modulates the human immunodeficiency virus type 1 in vivo mutation rate by Mansky (2000)
10.1016/s1016-8478(23)12897-4 / Mol Cells / Role of HIV Vpr as a regulator of apoptosis and an effector on bystander cells by Moon (2006)
10.1128/JVI.74.20.9727-9731.2000 / J Virol / Human immunodeficiency virus type 1 Vpr protein is incorporated into the virion in significantly smaller amounts than Gag and is phosphorylated in infected cells by Müller (2000)
10.1189/jlb.68.3.366 / J Leukoc Biol / HIV-1 Vpr regulates expression of β chemokines in human primary lymphocytes and macrophages by Muthumani (2000)
10.1089/104454902760330237 / DNA Cell Biol / The HIV-1 accessory gene vpr can inhibit antigen-specific immune function by Muthumani (2002a)
10.1074/jbc.M205313200 / J Biol Chem / HIV-1 Vpr induces apoptosis through caspase 9 in T cells and peripheral blood mononuclear cells by Muthumani (2002b)
10.1089/104454904773819824 / DNA Cell Biol / HIV-1 Vpr and anti-inflammatory activity by Muthumani (2004a)
10.1093/intimm/dxh190 / Int Immunol / HIV-1 Vpr inhibits the maturation and activation of macrophages and dendritic cells in vitro by Muthumani (2004b)
10.1016/j.ymthe.2005.05.009 / Mol Ther / HIV-1 viral protein-R (Vpr) protects against lethal superantigen challenge while maintaining homeostatic T cell levels in vivo by Muthumani (2005)
10.1038/ncb1352 / Nat Cell Biol / The HIV-1 Vpr and glucocorticoid receptor complex is a gain-of-function interaction that prevents the nuclear localization of PARP-1 by Muthumani (2006)
10.1128/JVI.01928-06 / J Virol / A novel nuclear import of Vpr promoted by importin α is crucial for HIV-1 replication in macrophages by Nitahara-Kasahara (2007)
10.1189/jlb.0306189 / J Leukoc Biol / Inhibition of HIV-1 replication by RNA interference of p53 expression by Pauls (2006)
10.1073/pnas.95.8.4595 / Proc Natl Acad Sci U S A / Extracellular HIV-1 virus protein R causes a large inward current and cell death in cultured hippocampal neurons: implications for AIDS pathology by Piller (1998)
10.1128/JVI.73.5.4230-4238.1999 / J Virol / The amino-terminal region of Vpr from human immunodeficiency virus type 1 forms ion channels and kills neurons by Piller (1999)
10.1128/JVI.00947-07 / J Virol / Vpr is required for efficient Nef expression from unintegrated HIV-1 DNA by Poon (2007)
10.1074/jbc.M209311200 / J Biol Chem / Functional role of HIV-1 virion-associated uracil DNA glycosylase 2 in the correction of G : U mispairs to G : C pairs by Priet (2003)
10.1074/jbc.M203905200 / J Biol Chem / Carboxyl terminus of hVIP/mov34 is critical for HIV-1-Vpr interaction and glucocorticoid-mediated signaling by Ramanathan (2002)
10.1242/jcs.115.7.1435 / J Cell Sci / Essential role of human CDT1 in DNA replication and chromatin licensing by Rialland (2002)
10.1128/JVI.69.2.882-888.1995 / J Virol / The human immunodeficiency virus type 1 vpr gene prevents cell proliferation during chronic infection by Rogel (1995)
10.1016/j.brainres.2009.03.024 / Brain Res / HIV-1 Vpr deregulates calcium secretion in neural cells by Rom (2009)
10.1038/sj.cdd.4401089 / Cell Death Differ / The C-terminal moiety of HIV-1 Vpr induces cell death via a caspase-independent mitochondrial pathway by Roumier (2002)
10.1074/jbc.273.32.20052 / J Biol Chem / Cooperative actions of HIV-1 Vpr and p53 modulate viral gene transcription by Sawaya (1998)
10.1074/jbc.M005197200 / J Biol Chem / Cooperative interaction between HIV-1 regulatory proteins Tat and Vpr modulates transcription of the viral genome by Sawaya (2000)
{'key': 'R82', 'first-page': '103', 'article-title': 'The cell cycle, cyclin-dependent kinases, and viral infections: new horizons and unexpected connections', 'volume': '5', 'author': 'Schang', 'year': '2003', 'journal-title': 'Prog Cell Cycle Res'} / Prog Cell Cycle Res / The cell cycle, cyclin-dependent kinases, and viral infections: new horizons and unexpected connections by Schang (2003)
10.1210/me.2007-0124 / Mol Endocrinol / Human immunodeficiency virus (HIV)-1 viral protein R suppresses transcriptional activity of peroxisome proliferator-activated receptor γ and inhibits adipocyte differentiation: implications for HIV-associated lipodystrophy by Shrivastav (2008)
10.1073/pnas.142313699 / Proc Natl Acad Sci U S A / Evidence for a cytopathogenicity determinant in HIV-1 Vpr by Somasundaran (2002)
10.1186/1743-422X-5-99 / Virol J / A comprehensive analysis of the naturally occurring polymorphisms in HIV-1 Vpr: potential impact on CTL epitopes by Srinivasan (2008)
10.1128/JVI.72.4.3037-3044.1998 / J Virol / Human immunodeficiency virus type 1 (HIV-1) viral protein R (Vpr) interacts with Lys-tRNA synthetase: implications for priming of HIV-1 reverse transcription by Stark (1998)
10.1073/pnas.96.21.12039 / Proc Natl Acad Sci U S A / Lentiviral delivery of HIV-1 Vpr protein induces apoptosis in transformed cells by Stewart (1999)
10.4049/jimmunol.158.1.512 / J Immun / Nuclear import of HIV-1 DNA in resting CD4+ T cells requires a cyclosporin A-sensitive pathway by Sun (1997)
10.1016/j.bbrc.2009.01.180 / Biochem Biophys Res Commun / Inhibition of human immunodeficiency virus type 1 (HIV-1) nuclear import via Vpr–importin α interactions as a novel HIV-1 therapy by Suzuki (2009)
10.1089/104454904773819798 / DNA Cell Biol / HIV-1 Vpr: genetic diversity and functional features from the perspective of structure by Tungaturthi (2004)
10.1016/j.jmb.2006.10.057 / J Mol Biol / Phospholamban interacts with HAX-1, a mitochondrial protein with anti-apoptotic function by Vafiadaki (2006)
10.1091/mbc.e08-06-0587 / Mol Biol Cell / The anti-apoptotic protein HAX-1 interacts with SERCA2 and regulates its protein levels to promote cell survival by Vafiadaki (2009)
10.1074/jbc.M502211200 / J Biol Chem / Synthetic Vpr protein activates activator protein-1, c-jun N-terminal kinase, and NF- κ B and stimulates HIV-1 transcription in promonocytic cells and primary macrophages by Varin (2005)
10.1101/gad.12.2.175 / Genes Dev / HIV-1 Vpr interacts with the nuclear transport pathway to promote macrophage infection by Vodicka (1998)
10.1074/jbc.270.43.25564 / J Biol Chem / Interaction of virion protein Vpr of human immunodeficiency virus type 1 with cellular transcription factor Sp1 and trans-activation of viral long terminal repeat by Wang (1995)
10.1016/0378-1119(96)00312-5 / Gene / Characterization of a leucine-zipper-like domain in Vpr protein of human immunodeficiency virus type 1 by Wang (1996)
10.1089/dna.2007.0707 / DNA Cell Biol / The HIV-1 Vif protein mediates degradation of Vpr and reduces Vpr-induced cell cycle arrest by Wang (2008)
10.1002/bies.950080607 / Bioessays / A conserved eukaryotic cell cycle control by Warbrick (1988)
10.1074/jbc.M703955200 / J Biol Chem / The HIV1 protein Vpr acts to promote G2 cell cycle arrest by engaging a DDB1 and cullin4A-containing ubiquitin ligase complex using VprBP/DCAF1 as an adaptor by Wen (2007)
10.1128/JVI.71.12.9732-9742.1997 / J Virol / Human immunodeficiency virus type 1 Vpr interacts with HHR23A, a cellular protein implicated in nucleotide excision DNA repair by Withers-Ward (1997)
10.1016/j.virol.2007.10.036 / Virology / Cell-surface processing of extracellular human immunodeficiency virus type 1 Vpr by proprotein convertases by Xiao (2008)
10.1074/jbc.M207982200 / J Biol Chem / Genetic selection of peptide inhibitors of human immunodeficiency virus type 1 Vpr by Yao (2002)
10.1128/JVI.79.21.13735-13746.2005 / J Virol / Human immunodeficiency virus type 1 Vpr interacts with antiapoptotic mitochondrial protein HAX-1 by Yedavalli (2005)
10.1083/jcb.200407156 / J Cell Biol / The FG-repeat asymmetry of the nuclear pore complex is dispensable for bulk nucleocytoplasmic transport in vivo by Zeitler (2004)
{'key': 'R105', 'first-page': '270', 'article-title': 'HIV-1 viral protein R (Vpr) & host cellular responses', 'volume': '121', 'author': 'Zhao', 'year': '2005', 'journal-title': 'Indian J Med Res'} / Indian J Med Res / HIV-1 viral protein R (Vpr) & host cellular responses by Zhao (2005)
10.1128/JVI.75.8.3791-3801.2001 / J Virol / Comparison of cell cycle arrest, transactivation, and apoptosis induced by the simian immunodeficiency virus SIVagm and human immunodeficiency virus type 1 vpr genes by Zhu (2001)
10.1023/A:1021653119934 / Apoptosis / Upregulation of survivin by HIV-1 Vpr by Zhu (2003)
10.1074/jbc.M204783200 / J Biol Chem / Regulation of the Apaf-1/caspase-9 apoptosome by caspase-3 and XIAP by Zou (2003)

Dates

Type	When
Created	16 years, 1 month ago (July 10, 2009, 2:38 p.m.)
Deposited	1 year, 5 months ago (March 15, 2024, 1:05 a.m.)
Indexed	1 month ago (Aug. 2, 2025, 12:06 a.m.)
Issued	16 years, 1 month ago (Aug. 1, 2009)
Published	16 years, 1 month ago (Aug. 1, 2009)
Published Print	16 years, 1 month ago (Aug. 1, 2009)

Funders 0

None

BibTeX

@article{Romani_2009, title={Human immunodeficiency virus type 1 Vpr: functions and molecular interactions}, volume={90}, ISSN={1465-2099}, url={http://dx.doi.org/10.1099/vir.0.011726-0}, DOI={10.1099/vir.0.011726-0}, number={8}, journal={Journal of General Virology}, publisher={Microbiology Society}, author={Romani, Bizhan and Engelbrecht, Susan}, year={2009}, month=aug, pages={1795–1805} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        2
      ]
    ],
    "date-time": "2025-08-02T04:06:51Z",
    "timestamp": 1754107611225
  },
  "reference-count": 108,
  "publisher": "Microbiology Society",
  "issue": "8",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2009,
        8,
        1
      ]
    ]
  },
  "abstract": "<jats:p>Human immunodeficiency virus type 1 (HIV-1) viral protein R (Vpr) is an accessory protein that interacts with a number of cellular and viral proteins. The functions of many of these interactions in the pathogenesis of HIV-1 have been identified. Deletion of the<jats:italic>vpr</jats:italic>gene reduces the virulence of HIV-1 dramatically, indicating the importance of this protein for the virus. This review describes the current findings on several established functions of HIV-1 Vpr and some possible roles proposed for this protein. Because Vpr exploits cellular proteins and pathways to influence the biology of HIV-1, understanding the functions of Vpr usually involves the study of cellular pathways. Several functions of Vpr are attributed to the virion-incorporated protein, but some of them are attributed to the expression of Vpr in HIV-1-infected cells. The structure of Vpr may be key to understanding the variety of its interactions. Due to the critical role of Vpr in HIV-1 pathogenicity, study of the interactions between Vpr and cellular proteins may help us to understand the mechanism(s) of HIV-1 pathogenicity.</jats:p>",
  "DOI": "10.1099/vir.0.011726-0",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2009,
        7,
        10
      ]
    ],
    "date-time": "2009-07-10T18:38:34Z",
    "timestamp": 1247251114000
  },
  "page": "1795-1805",
  "source": "Crossref",
  "is-referenced-by-count": 43,
  "title": "Human immunodeficiency virus type 1 Vpr: functions and molecular interactions",
  "prefix": "10.1099",
  "volume": "90",
  "author": [
    {
      "given": "Bizhan",
      "family": "Romani",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Pathology, Division of Medical Virology, University of Stellenbosch, Tygerberg 7505, South Africa"
        }
      ]
    },
    {
      "given": "Susan",
      "family": "Engelbrecht",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "National Health Laboratory Services, Tygerberg 7505, South Africa"
        },
        {
          "name": "Department of Pathology, Division of Medical Virology, University of Stellenbosch, Tygerberg 7505, South Africa"
        }
      ]
    }
  ],
  "member": "345",
  "reference": [
    {
      "key": "R1",
      "doi-asserted-by": "crossref",
      "first-page": "599",
      "DOI": "10.1006/jmbi.1996.0485",
      "article-title": "The human immunodeficiency virus type 1 Vpr transactivator: cooperation with promoter-bound activator domains and binding to TFIIB",
      "volume": "261",
      "author": "Agostini",
      "year": "1996",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "R2",
      "doi-asserted-by": "crossref",
      "first-page": "235",
      "DOI": "10.1016/S0014-5793(99)00501-3",
      "article-title": "The HIV-1 Vpr co-activator induces a conformational change in TFIIB",
      "volume": "450",
      "author": "Agostini",
      "year": "1999",
      "journal-title": "FEBS Lett"
    },
    {
      "key": "R3",
      "doi-asserted-by": "crossref",
      "first-page": "43",
      "DOI": "10.2174/1570162052772988",
      "article-title": "The role of Vpr in HIV-1 pathogenesis",
      "volume": "3",
      "author": "Andersen",
      "year": "2005",
      "journal-title": "Curr HIV Res"
    },
    {
      "key": "R4",
      "doi-asserted-by": "crossref",
      "first-page": "2",
      "DOI": "10.1016/j.yexmp.2008.03.015",
      "article-title": "HIV-1 Vpr: mechanisms of G2 arrest and apoptosis",
      "volume": "85",
      "author": "Andersen",
      "year": "2008",
      "journal-title": "Exp Mol Pathol"
    },
    {
      "key": "R5",
      "doi-asserted-by": "crossref",
      "first-page": "47",
      "DOI": "10.1007/s11904-004-0007-x",
      "article-title": "HIV accessory proteins and surviving the host cell",
      "volume": "1",
      "author": "Anderson",
      "year": "2004",
      "journal-title": "Curr HIV/AIDS Rep"
    },
    {
      "key": "R6",
      "doi-asserted-by": "crossref",
      "first-page": "69",
      "DOI": "10.1023/A:1026487609215",
      "article-title": "A C-terminal domain of HIV-1 accessory protein Vpr is involved in penetration, mitochondrial dysfunction and apoptosis of human CD4+ lymphocytes",
      "volume": "2",
      "author": "Arunagiri",
      "year": "1997",
      "journal-title": "Apoptosis"
    },
    {
      "key": "R7",
      "doi-asserted-by": "crossref",
      "first-page": "13",
      "DOI": "10.1093/intimm/14.1.13",
      "article-title": "HIV-1 viral protein R compromises cellular function in vivo",
      "volume": "14",
      "author": "Ayyavoo",
      "year": "2002",
      "journal-title": "Int Immunol"
    },
    {
      "key": "R8",
      "doi-asserted-by": "crossref",
      "first-page": "9083",
      "DOI": "10.1074/jbc.274.13.9083",
      "article-title": "Incorporation of Vpr into human immunodeficiency virus type 1 requires a direct interaction with the p6 domain of the p55 Gag precursor",
      "volume": "274",
      "author": "Bachand",
      "year": "1999",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "R9",
      "doi-asserted-by": "crossref",
      "first-page": "E40",
      "DOI": "10.1152/ajpendo.00163.2006",
      "article-title": "Effects of transgenic expression of HIV-1 Vpr on lipid and energy metabolism in mice",
      "volume": "292",
      "author": "Balasubramanyam",
      "year": "2007",
      "journal-title": "Am J Physiol Endocrinol Metab"
    },
    {
      "key": "R10",
      "doi-asserted-by": "crossref",
      "first-page": "F11",
      "DOI": "10.1084/jem.193.4.F11",
      "article-title": "HIV and apoptosis: death and the mitochondrion",
      "volume": "193",
      "author": "Basanez",
      "year": "2001",
      "journal-title": "J Exp Med"
    },
    {
      "key": "R11",
      "doi-asserted-by": "crossref",
      "first-page": "3795",
      "DOI": "10.1096/fj.07-8697rev",
      "article-title": "Reverse transcription of the HIV-1 pandemic",
      "volume": "21",
      "author": "Basavapathruni",
      "year": "2007",
      "journal-title": "FASEB J"
    },
    {
      "key": "R12",
      "doi-asserted-by": "crossref",
      "first-page": "E85",
      "DOI": "10.1371/journal.ppat.0030085",
      "article-title": "HIV-1 Vpr-mediated G2 arrest involves the DDB1\u2013CUL4AVPRBP E3 ubiquitin ligase",
      "volume": "3",
      "author": "Belzile",
      "year": "2007",
      "journal-title": "PLoS Pathog"
    },
    {
      "key": "R13",
      "doi-asserted-by": "crossref",
      "first-page": "16",
      "DOI": "10.1186/1742-4690-4-16",
      "article-title": "Antagonistic interaction of HIV-1 Vpr with Hsf-mediated cellular heat shock response and Hsp16 in fission yeast ( Schizosaccharomyces pombe )",
      "volume": "4",
      "author": "Benko",
      "year": "2007",
      "journal-title": "Retrovirology"
    },
    {
      "key": "R14",
      "doi-asserted-by": "crossref",
      "first-page": "1861",
      "DOI": "10.1097/00002030-200409030-00022",
      "article-title": "APOBEC3G versus reverse transcriptase in the generation of HIV-1 drug-resistance mutations",
      "volume": "18",
      "author": "Berkhout",
      "year": "2004",
      "journal-title": "AIDS"
    },
    {
      "key": "R15",
      "doi-asserted-by": "crossref",
      "first-page": "697",
      "DOI": "10.1128/JVI.70.2.697-704.1996",
      "article-title": "Human immunodeficiency virus type 1 Vpr protein binds to the uracil DNA glycosylase DNA repair enzyme",
      "volume": "70",
      "author": "Bouhamdan",
      "year": "1996",
      "journal-title": "J Virol"
    },
    {
      "key": "R16",
      "doi-asserted-by": "crossref",
      "first-page": "8009",
      "DOI": "10.1074/jbc.273.14.8009",
      "article-title": "Diversity of HIV-1 Vpr interactions involves usage of the WXXF motif of host cell proteins",
      "volume": "273",
      "author": "Bouhamdan",
      "year": "1998",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "R17",
      "doi-asserted-by": "crossref",
      "first-page": "269",
      "DOI": "10.1146/annurev.cellbio.15.1.269",
      "article-title": "Biochemical pathways of caspase activation during apoptosis",
      "volume": "15",
      "author": "Budihardjo",
      "year": "1999",
      "journal-title": "Annu Rev Cell Dev Biol"
    },
    {
      "key": "R18",
      "doi-asserted-by": "crossref",
      "first-page": "322",
      "DOI": "10.1007/BF02253252",
      "article-title": "Differential apoptosis effects of primate lentiviral Vpr and Vpx in mammalian cells",
      "volume": "7",
      "author": "Chang",
      "year": "2000",
      "journal-title": "J Biomed Sci"
    },
    {
      "key": "R19",
      "doi-asserted-by": "crossref",
      "first-page": "1793",
      "DOI": "10.1091/mbc.e03-09-0691",
      "article-title": "HIV-1 Vpr induces defects in mitosis, cytokinesis, nuclear structure, and centrosomes",
      "volume": "15",
      "author": "Chang",
      "year": "2004",
      "journal-title": "Mol Biol Cell"
    },
    {
      "key": "R20",
      "doi-asserted-by": "crossref",
      "first-page": "2339",
      "DOI": "10.1099/0022-1317-83-10-2339",
      "article-title": "Roles of uracil\u2013DNA glycosylase and dUTPase in virus replication",
      "volume": "83",
      "author": "Chen",
      "year": "2002",
      "journal-title": "J Gen Virol"
    },
    {
      "key": "R21",
      "doi-asserted-by": "crossref",
      "first-page": "28419",
      "DOI": "10.1074/jbc.M403875200",
      "article-title": "Vpr-mediated incorporation of UNG2 into HIV-1 particles is required to modulate the virus mutation rate and for replication in macrophages",
      "volume": "279",
      "author": "Chen",
      "year": "2004",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "R22",
      "doi-asserted-by": "crossref",
      "first-page": "3293",
      "DOI": "10.4049/jimmunol.165.6.3293",
      "article-title": "Dual role of the HIV-1 Vpr protein in the modulation of the apoptotic response of T cells",
      "volume": "165",
      "author": "Conti",
      "year": "2000",
      "journal-title": "J Immun"
    },
    {
      "key": "R23",
      "doi-asserted-by": "crossref",
      "first-page": "4361",
      "DOI": "10.1529/biophysj.106.081240",
      "article-title": "Analysis of a generic model of eukaryotic cell-cycle regulation",
      "volume": "90",
      "author": "Csikasz-Nagy",
      "year": "2006",
      "journal-title": "Biophys J"
    },
    {
      "key": "R24",
      "doi-asserted-by": "crossref",
      "first-page": "1105",
      "DOI": "10.1126/science.1063957",
      "article-title": "Dynamic disruptions in nuclear envelope architecture and integrity induced by HIV-1 Vpr",
      "volume": "294",
      "author": "de Noronha",
      "year": "2001",
      "journal-title": "Science"
    },
    {
      "key": "R25",
      "doi-asserted-by": "crossref",
      "first-page": "359",
      "DOI": "10.1006/viro.2001.1007",
      "article-title": "HIV-1 Vpr induces cell cycle G2 arrest in fission yeast ( Schizosaccharomyces pombe ) through a pathway involving regulatory and catalytic subunits of PP2A and acting on both Wee1 and Cdc25",
      "volume": "287",
      "author": "Elder",
      "year": "2001",
      "journal-title": "Virology"
    },
    {
      "key": "R26",
      "doi-asserted-by": "crossref",
      "first-page": "389",
      "DOI": "10.1046/j.1432-1033.2001.01895.x",
      "article-title": "Solution structure of human immunodeficiency virus type 1 Vpr (13\u201333) peptide in micelles",
      "volume": "268",
      "author": "Engler",
      "year": "2001",
      "journal-title": "Eur J Biochem"
    },
    {
      "key": "R27",
      "doi-asserted-by": "crossref",
      "first-page": "5281",
      "DOI": "10.1073/pnas.95.9.5281",
      "article-title": "HIV transcriptional activation by the accessory protein, VPR, is mediated by the p300 co-activator",
      "volume": "95",
      "author": "Felzien",
      "year": "1998",
      "journal-title": "Proc Natl Acad Sci U S A"
    },
    {
      "key": "R28",
      "doi-asserted-by": "crossref",
      "first-page": "1027",
      "DOI": "10.1128/JVI.70.2.1027-1032.1996",
      "article-title": "Role of the karyopherin pathway in human immunodeficiency virus type 1 nuclear import",
      "volume": "70",
      "author": "Gallay",
      "year": "1996",
      "journal-title": "J Virol"
    },
    {
      "key": "R29",
      "doi-asserted-by": "crossref",
      "first-page": "9825",
      "DOI": "10.1073/pnas.94.18.9825",
      "article-title": "HIV-1 infection of nondividing cells through the recognition of integrase by the importin/karyopherin pathway",
      "volume": "94",
      "author": "Gallay",
      "year": "1997",
      "journal-title": "Proc Natl Acad Sci U S A"
    },
    {
      "key": "R30",
      "doi-asserted-by": "crossref",
      "first-page": "6222",
      "DOI": "10.1074/jbc.M610056200",
      "article-title": "Insights into the multiple roles of pausing in HIV-1 reverse transcriptase-promoted strand transfers",
      "volume": "282",
      "author": "Gao",
      "year": "2007",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "R31",
      "doi-asserted-by": "crossref",
      "first-page": "2973",
      "DOI": "10.1101/gad.12.19.2973",
      "article-title": "The complexity of p53 modulation: emerging patterns from divergent signals",
      "volume": "12",
      "author": "Giaccia",
      "year": "1998",
      "journal-title": "Genes Dev"
    },
    {
      "key": "R32",
      "doi-asserted-by": "crossref",
      "first-page": "20",
      "DOI": "10.1007/BF01279896",
      "article-title": "Cullins and cell cycle control",
      "volume": "211",
      "author": "Gieffers",
      "year": "2000",
      "journal-title": "Protoplasma"
    },
    {
      "key": "R33",
      "doi-asserted-by": "crossref",
      "first-page": "65",
      "DOI": "10.1038/nm0198-065",
      "article-title": "HIV-1 Vpr increases viral expression by manipulation of the cell cycle: a mechanism for selection of Vpr in vivo",
      "volume": "4",
      "author": "Goh",
      "year": "1998",
      "journal-title": "Nat Med"
    },
    {
      "key": "R34",
      "doi-asserted-by": "crossref",
      "first-page": "337",
      "DOI": "10.1016/j.virol.2003.10.007",
      "article-title": "The human immunodeficiency virus Vpr protein binds Cdc25C: implications for G2 arrest",
      "volume": "318",
      "author": "Goh",
      "year": "2004",
      "journal-title": "Virology"
    },
    {
      "key": "R35",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1016/S0092-8674(00)00003-9",
      "article-title": "Apoptotic pathways: paper wraps stone blunts scissors",
      "volume": "102",
      "author": "Green",
      "year": "2000",
      "journal-title": "Cell"
    },
    {
      "key": "R36",
      "doi-asserted-by": "crossref",
      "first-page": "6705",
      "DOI": "10.1128/JVI.69.11.6705-6711.1995",
      "article-title": "Human immunodeficiency virus type 1 viral protein R (Vpr) arrests cells in the G2 phase of the cell cycle by inhibiting p34cdc2 activity",
      "volume": "69",
      "author": "He",
      "year": "1995",
      "journal-title": "J Virol"
    },
    {
      "key": "R37",
      "doi-asserted-by": "crossref",
      "first-page": "5",
      "DOI": "10.1186/1747-1028-2-5",
      "article-title": "Stealing the spotlight: CUL4\u2013DDB1 ubiquitin ligase docks WD40-repeat proteins to destroy",
      "volume": "2",
      "author": "Higa",
      "year": "2007",
      "journal-title": "Cell Div"
    },
    {
      "key": "R38",
      "doi-asserted-by": "crossref",
      "first-page": "11778",
      "DOI": "10.1073/pnas.0702102104",
      "article-title": "Lentiviral Vpr usurps Cul4\u2013DDB1[VprBP] E3 ubiquitin ligase to modulate cell cycle",
      "volume": "104",
      "author": "Hrecka",
      "year": "2007",
      "journal-title": "Proc Natl Acad Sci U S A"
    },
    {
      "key": "R39",
      "doi-asserted-by": "crossref",
      "first-page": "202",
      "DOI": "10.3109/13550280009015823",
      "article-title": "Effects of extracellular human immunodeficiency virus type 1 Vpr protein in primary rat cortical cell cultures",
      "volume": "6",
      "author": "Huang",
      "year": "2000",
      "journal-title": "J Neurovirol"
    },
    {
      "key": "R40",
      "doi-asserted-by": "crossref",
      "first-page": "2904",
      "DOI": "10.1128/JVI.01098-07",
      "article-title": "Human immunodeficiency virus type 1 Vpr induces cell cycle G2 arrest through Srk1/MK2-mediated phosphorylation of Cdc25",
      "volume": "82",
      "author": "Huard",
      "year": "2008",
      "journal-title": "J Virol"
    },
    {
      "key": "R41",
      "doi-asserted-by": "crossref",
      "first-page": "33",
      "DOI": "10.1084/jem.191.1.33",
      "article-title": "The HIV-1 viral protein R induces apoptosis via a direct effect on the mitochondrial permeability transition pore",
      "volume": "191",
      "author": "Jacotot",
      "year": "2000",
      "journal-title": "J Exp Med"
    },
    {
      "key": "R42",
      "doi-asserted-by": "crossref",
      "first-page": "509",
      "DOI": "10.1084/jem.193.4.509",
      "article-title": "Control of mitochondrial membrane permeabilization by adenine nucleotide translocator interacting with HIV-1 viral protein R and Bcl-2",
      "volume": "193",
      "author": "Jacotot",
      "year": "2001",
      "journal-title": "J Exp Med"
    },
    {
      "key": "R43",
      "doi-asserted-by": "crossref",
      "first-page": "875",
      "DOI": "10.1083/jcb.143.4.875",
      "article-title": "Characterization of HIV-1 Vpr nuclear import: analysis of signals and pathways",
      "volume": "143",
      "author": "Jenkins",
      "year": "1998",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "R44",
      "doi-asserted-by": "crossref",
      "first-page": "709",
      "DOI": "10.1016/j.molcel.2006.08.010",
      "article-title": "A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1",
      "volume": "23",
      "author": "Jin",
      "year": "2006",
      "journal-title": "Mol Cell"
    },
    {
      "key": "R45",
      "doi-asserted-by": "crossref",
      "first-page": "7132",
      "DOI": "10.1128/JVI.73.9.7132-7137.1999",
      "article-title": "The presence of human immunodeficiency virus type 1 Vpr correlates with a decrease in the frequency of mutations in a plasmid shuttle vector",
      "volume": "73",
      "author": "Jowett",
      "year": "1999",
      "journal-title": "J Virol"
    },
    {
      "key": "R46",
      "doi-asserted-by": "crossref",
      "first-page": "7552",
      "DOI": "10.1073/pnas.0802203105",
      "article-title": "Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection",
      "volume": "105",
      "author": "Keele",
      "year": "2008",
      "journal-title": "Proc Natl Acad Sci U S A"
    },
    {
      "key": "R47",
      "doi-asserted-by": "crossref",
      "first-page": "17545",
      "DOI": "10.1073/pnas.0507900102",
      "article-title": "Formation of apoptosome is initiated by cytochrome c -induced dATP hydrolysis and subsequent nucleotide exchange on Apaf-1",
      "volume": "102",
      "author": "Kim",
      "year": "2005",
      "journal-title": "Proc Natl Acad Sci U S A"
    },
    {
      "key": "R48",
      "doi-asserted-by": "crossref",
      "first-page": "153",
      "DOI": "10.1196/annals.1321.013",
      "article-title": "Human immunodeficiency virus type-1 accessory protein Vpr: a causative agent of the AIDS-related insulin resistance/lipodystrophy syndrome?",
      "volume": "1024",
      "author": "Kino",
      "year": "2004",
      "journal-title": "Ann N Y Acad Sci"
    },
    {
      "key": "R49",
      "doi-asserted-by": "crossref",
      "first-page": "9724",
      "DOI": "10.1128/JVI.76.19.9724-9734.2002",
      "article-title": "Human immunodeficiency virus type 1 (HIV-1) accessory protein Vpr induces transcription of the HIV-1 and glucocorticoid-responsive promoters by binding directly to p300/CBP coactivators",
      "volume": "76",
      "author": "Kino",
      "year": "2002",
      "journal-title": "J Virol"
    },
    {
      "key": "R50",
      "doi-asserted-by": "crossref",
      "first-page": "2780",
      "DOI": "10.1128/JVI.79.5.2780-2787.2005",
      "article-title": "Vpr protein of human immunodeficiency virus type 1 binds to 14-3-3 proteins and facilitates complex formation with Cdc25C: implications for cell cycle arrest",
      "volume": "79",
      "author": "Kino",
      "year": "2005",
      "journal-title": "J Virol"
    },
    {
      "key": "R51",
      "doi-asserted-by": "crossref",
      "first-page": "2528",
      "DOI": "10.1128/JVI.02094-07",
      "article-title": "Human immunodeficiency virus type 1 Vpr inhibits axonal outgrowth through induction of mitochondrial dysfunction",
      "volume": "82",
      "author": "Kitayama",
      "year": "2008",
      "journal-title": "J Virol"
    },
    {
      "key": "R52",
      "doi-asserted-by": "crossref",
      "first-page": "173",
      "DOI": "10.1016/S0960-9822(03)00008-3",
      "article-title": "Evolution of eukaryotic cell cycle regulation: stepwise addition of regulatory kinases and late advent of the CDKs",
      "volume": "13",
      "author": "Krylov",
      "year": "2003",
      "journal-title": "Curr Biol"
    },
    {
      "key": "R53",
      "doi-asserted-by": "crossref",
      "first-page": "1926",
      "DOI": "10.1128/JVI.68.3.1926-1934.1994",
      "article-title": "Requirement of the Pr55gag precursor for incorporation of the Vpr product into human immunodeficiency virus type 1 viral particles",
      "volume": "68",
      "author": "Lavallee",
      "year": "1994",
      "journal-title": "J Virol"
    },
    {
      "key": "R54",
      "doi-asserted-by": "crossref",
      "first-page": "11",
      "DOI": "10.1186/1742-4690-2-11",
      "article-title": "The Vpr protein from HIV-1: distinct roles along the viral life cycle",
      "volume": "2",
      "author": "Le Rouzic",
      "year": "2005",
      "journal-title": "Retrovirology"
    },
    {
      "key": "R55",
      "doi-asserted-by": "crossref",
      "first-page": "45091",
      "DOI": "10.1074/jbc.M207439200",
      "article-title": "Docking of HIV-1 Vpr to the nuclear envelope is mediated by the interaction with the nucleoporin hCG1",
      "volume": "277",
      "author": "Le Rouzic",
      "year": "2002",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "R56",
      "doi-asserted-by": "crossref",
      "first-page": "6315",
      "DOI": "10.1128/JVI.71.9.6315-6322.1997",
      "article-title": "Nucleotide substitutions within U5 are critical for efficient reverse transcription of human immunodeficiency virus type 1 with a primer binding site complementary to tRNAHis",
      "volume": "71",
      "author": "Li",
      "year": "1997",
      "journal-title": "J Virol"
    },
    {
      "key": "R57",
      "doi-asserted-by": "crossref",
      "first-page": "7189",
      "DOI": "10.1128/JVI.01979-07",
      "article-title": "Infection with Vpr-positive human immunodeficiency virus type 1 impairs NK cell function indirectly through cytokine dysregulation of infected target cells",
      "volume": "82",
      "author": "Majumder",
      "year": "2008",
      "journal-title": "J Virol"
    },
    {
      "key": "R58",
      "doi-asserted-by": "crossref",
      "first-page": "391",
      "DOI": "10.1006/viro.1996.0436",
      "article-title": "The mutation rate of human immunodeficiency virus type 1 is influenced by the vpr gene",
      "volume": "222",
      "author": "Mansky",
      "year": "1996",
      "journal-title": "Virology"
    },
    {
      "key": "R59",
      "doi-asserted-by": "crossref",
      "first-page": "7039",
      "DOI": "10.1128/JVI.74.15.7039-7047.2000",
      "article-title": "The interaction of Vpr with uracil DNA glycosylase modulates the human immunodeficiency virus type 1 in vivo mutation rate",
      "volume": "74",
      "author": "Mansky",
      "year": "2000",
      "journal-title": "J Virol"
    },
    {
      "key": "R60",
      "doi-asserted-by": "crossref",
      "first-page": "7",
      "DOI": "10.1016/s1016-8478(23)12897-4",
      "article-title": "Role of HIV Vpr as a regulator of apoptosis and an effector on bystander cells",
      "volume": "21",
      "author": "Moon",
      "year": "2006",
      "journal-title": "Mol Cells"
    },
    {
      "key": "R61",
      "doi-asserted-by": "crossref",
      "first-page": "9727",
      "DOI": "10.1128/JVI.74.20.9727-9731.2000",
      "article-title": "Human immunodeficiency virus type 1 Vpr protein is incorporated into the virion in significantly smaller amounts than Gag and is phosphorylated in infected cells",
      "volume": "74",
      "author": "M\u00fcller",
      "year": "2000",
      "journal-title": "J Virol"
    },
    {
      "key": "R62",
      "doi-asserted-by": "crossref",
      "first-page": "366",
      "DOI": "10.1189/jlb.68.3.366",
      "article-title": "HIV-1 Vpr regulates expression of \u03b2 chemokines in human primary lymphocytes and macrophages",
      "volume": "68",
      "author": "Muthumani",
      "year": "2000",
      "journal-title": "J Leukoc Biol"
    },
    {
      "key": "R63",
      "doi-asserted-by": "crossref",
      "first-page": "689",
      "DOI": "10.1089/104454902760330237",
      "article-title": "The HIV-1 accessory gene vpr can inhibit antigen-specific immune function",
      "volume": "21",
      "author": "Muthumani",
      "year": "2002a",
      "journal-title": "DNA Cell Biol"
    },
    {
      "key": "R64",
      "doi-asserted-by": "crossref",
      "first-page": "37820",
      "DOI": "10.1074/jbc.M205313200",
      "article-title": "HIV-1 Vpr induces apoptosis through caspase 9 in T cells and peripheral blood mononuclear cells",
      "volume": "277",
      "author": "Muthumani",
      "year": "2002b",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "R65",
      "doi-asserted-by": "crossref",
      "first-page": "239",
      "DOI": "10.1089/104454904773819824",
      "article-title": "HIV-1 Vpr and anti-inflammatory activity",
      "volume": "23",
      "author": "Muthumani",
      "year": "2004a",
      "journal-title": "DNA Cell Biol"
    },
    {
      "key": "R66",
      "doi-asserted-by": "crossref",
      "first-page": "103",
      "DOI": "10.1093/intimm/dxh190",
      "article-title": "HIV-1 Vpr inhibits the maturation and activation of macrophages and dendritic cells in vitro",
      "volume": "17",
      "author": "Muthumani",
      "year": "2004b",
      "journal-title": "Int Immunol"
    },
    {
      "key": "R67",
      "doi-asserted-by": "crossref",
      "first-page": "910",
      "DOI": "10.1016/j.ymthe.2005.05.009",
      "article-title": "HIV-1 viral protein-R (Vpr) protects against lethal superantigen challenge while maintaining homeostatic T cell levels in vivo",
      "volume": "12",
      "author": "Muthumani",
      "year": "2005",
      "journal-title": "Mol Ther"
    },
    {
      "key": "R68",
      "doi-asserted-by": "crossref",
      "first-page": "170",
      "DOI": "10.1038/ncb1352",
      "article-title": "The HIV-1 Vpr and glucocorticoid receptor complex is a gain-of-function interaction that prevents the nuclear localization of PARP-1",
      "volume": "8",
      "author": "Muthumani",
      "year": "2006",
      "journal-title": "Nat Cell Biol"
    },
    {
      "key": "R69",
      "doi-asserted-by": "crossref",
      "first-page": "5284",
      "DOI": "10.1128/JVI.01928-06",
      "article-title": "A novel nuclear import of Vpr promoted by importin \u03b1 is crucial for HIV-1 replication in macrophages",
      "volume": "81",
      "author": "Nitahara-Kasahara",
      "year": "2007",
      "journal-title": "J Virol"
    },
    {
      "key": "R70",
      "doi-asserted-by": "crossref",
      "first-page": "659",
      "DOI": "10.1189/jlb.0306189",
      "article-title": "Inhibition of HIV-1 replication by RNA interference of p53 expression",
      "volume": "80",
      "author": "Pauls",
      "year": "2006",
      "journal-title": "J Leukoc Biol"
    },
    {
      "key": "R71",
      "doi-asserted-by": "crossref",
      "first-page": "4595",
      "DOI": "10.1073/pnas.95.8.4595",
      "article-title": "Extracellular HIV-1 virus protein R causes a large inward current and cell death in cultured hippocampal neurons: implications for AIDS pathology",
      "volume": "95",
      "author": "Piller",
      "year": "1998",
      "journal-title": "Proc Natl Acad Sci U S A"
    },
    {
      "key": "R72",
      "doi-asserted-by": "crossref",
      "first-page": "4230",
      "DOI": "10.1128/JVI.73.5.4230-4238.1999",
      "article-title": "The amino-terminal region of Vpr from human immunodeficiency virus type 1 forms ion channels and kills neurons",
      "volume": "73",
      "author": "Piller",
      "year": "1999",
      "journal-title": "J Virol"
    },
    {
      "key": "R73",
      "doi-asserted-by": "crossref",
      "first-page": "10515",
      "DOI": "10.1128/JVI.00947-07",
      "article-title": "Vpr is required for efficient Nef expression from unintegrated HIV-1 DNA",
      "volume": "81",
      "author": "Poon",
      "year": "2007",
      "journal-title": "J Virol"
    },
    {
      "key": "R74",
      "doi-asserted-by": "crossref",
      "first-page": "4566",
      "DOI": "10.1074/jbc.M209311200",
      "article-title": "Functional role of HIV-1 virion-associated uracil DNA glycosylase 2 in the correction of G\u200a:\u200aU mispairs to G\u200a:\u200aC pairs",
      "volume": "278",
      "author": "Priet",
      "year": "2003",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "R75",
      "doi-asserted-by": "crossref",
      "first-page": "47854",
      "DOI": "10.1074/jbc.M203905200",
      "article-title": "Carboxyl terminus of hVIP/mov34 is critical for HIV-1-Vpr interaction and glucocorticoid-mediated signaling",
      "volume": "277",
      "author": "Ramanathan",
      "year": "2002",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "R76",
      "doi-asserted-by": "crossref",
      "first-page": "1435",
      "DOI": "10.1242/jcs.115.7.1435",
      "article-title": "Essential role of human CDT1 in DNA replication and chromatin licensing",
      "volume": "115",
      "author": "Rialland",
      "year": "2002",
      "journal-title": "J Cell Sci"
    },
    {
      "key": "R77",
      "doi-asserted-by": "crossref",
      "first-page": "882",
      "DOI": "10.1128/JVI.69.2.882-888.1995",
      "article-title": "The human immunodeficiency virus type 1 vpr gene prevents cell proliferation during chronic infection",
      "volume": "69",
      "author": "Rogel",
      "year": "1995",
      "journal-title": "J Virol"
    },
    {
      "key": "R78",
      "doi-asserted-by": "crossref",
      "first-page": "81",
      "DOI": "10.1016/j.brainres.2009.03.024",
      "article-title": "HIV-1 Vpr deregulates calcium secretion in neural cells",
      "volume": "1275",
      "author": "Rom",
      "year": "2009",
      "journal-title": "Brain Res"
    },
    {
      "key": "R79",
      "doi-asserted-by": "crossref",
      "first-page": "1212",
      "DOI": "10.1038/sj.cdd.4401089",
      "article-title": "The C-terminal moiety of HIV-1 Vpr induces cell death via a caspase-independent mitochondrial pathway",
      "volume": "9",
      "author": "Roumier",
      "year": "2002",
      "journal-title": "Cell Death Differ"
    },
    {
      "key": "R80",
      "doi-asserted-by": "crossref",
      "first-page": "20052",
      "DOI": "10.1074/jbc.273.32.20052",
      "article-title": "Cooperative actions of HIV-1 Vpr and p53 modulate viral gene transcription",
      "volume": "273",
      "author": "Sawaya",
      "year": "1998",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "R81",
      "doi-asserted-by": "crossref",
      "first-page": "35209",
      "DOI": "10.1074/jbc.M005197200",
      "article-title": "Cooperative interaction between HIV-1 regulatory proteins Tat and Vpr modulates transcription of the viral genome",
      "volume": "275",
      "author": "Sawaya",
      "year": "2000",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "R82",
      "first-page": "103",
      "article-title": "The cell cycle, cyclin-dependent kinases, and viral infections: new horizons and unexpected connections",
      "volume": "5",
      "author": "Schang",
      "year": "2003",
      "journal-title": "Prog Cell Cycle Res"
    },
    {
      "key": "R83",
      "doi-asserted-by": "crossref",
      "first-page": "234",
      "DOI": "10.1210/me.2007-0124",
      "article-title": "Human immunodeficiency virus (HIV)-1 viral protein R suppresses transcriptional activity of peroxisome proliferator-activated receptor \u03b3 and inhibits adipocyte differentiation: implications for HIV-associated lipodystrophy",
      "volume": "22",
      "author": "Shrivastav",
      "year": "2008",
      "journal-title": "Mol Endocrinol"
    },
    {
      "key": "R84",
      "doi-asserted-by": "crossref",
      "first-page": "9503",
      "DOI": "10.1073/pnas.142313699",
      "article-title": "Evidence for a cytopathogenicity determinant in HIV-1 Vpr",
      "volume": "99",
      "author": "Somasundaran",
      "year": "2002",
      "journal-title": "Proc Natl Acad Sci U S A"
    },
    {
      "key": "R85",
      "doi-asserted-by": "crossref",
      "first-page": "99",
      "DOI": "10.1186/1743-422X-5-99",
      "article-title": "A comprehensive analysis of the naturally occurring polymorphisms in HIV-1 Vpr: potential impact on CTL epitopes",
      "volume": "5",
      "author": "Srinivasan",
      "year": "2008",
      "journal-title": "Virol J"
    },
    {
      "key": "R86",
      "doi-asserted-by": "crossref",
      "first-page": "3037",
      "DOI": "10.1128/JVI.72.4.3037-3044.1998",
      "article-title": "Human immunodeficiency virus type 1 (HIV-1) viral protein R (Vpr) interacts with Lys-tRNA synthetase: implications for priming of HIV-1 reverse transcription",
      "volume": "72",
      "author": "Stark",
      "year": "1998",
      "journal-title": "J Virol"
    },
    {
      "key": "R87",
      "doi-asserted-by": "crossref",
      "first-page": "12039",
      "DOI": "10.1073/pnas.96.21.12039",
      "article-title": "Lentiviral delivery of HIV-1 Vpr protein induces apoptosis in transformed cells",
      "volume": "96",
      "author": "Stewart",
      "year": "1999",
      "journal-title": "Proc Natl Acad Sci U S A"
    },
    {
      "key": "R88",
      "doi-asserted-by": "crossref",
      "first-page": "512",
      "DOI": "10.4049/jimmunol.158.1.512",
      "article-title": "Nuclear import of HIV-1 DNA in resting CD4+ T cells requires a cyclosporin A-sensitive pathway",
      "volume": "158",
      "author": "Sun",
      "year": "1997",
      "journal-title": "J Immun"
    },
    {
      "key": "R89",
      "doi-asserted-by": "crossref",
      "first-page": "838",
      "DOI": "10.1016/j.bbrc.2009.01.180",
      "article-title": "Inhibition of human immunodeficiency virus type 1 (HIV-1) nuclear import via Vpr\u2013importin \u03b1 interactions as a novel HIV-1 therapy",
      "volume": "380",
      "author": "Suzuki",
      "year": "2009",
      "journal-title": "Biochem Biophys Res Commun"
    },
    {
      "key": "R90",
      "doi-asserted-by": "crossref",
      "first-page": "207",
      "DOI": "10.1089/104454904773819798",
      "article-title": "HIV-1 Vpr: genetic diversity and functional features from the perspective of structure",
      "volume": "23",
      "author": "Tungaturthi",
      "year": "2004",
      "journal-title": "DNA Cell Biol"
    },
    {
      "key": "R91",
      "doi-asserted-by": "crossref",
      "first-page": "65",
      "DOI": "10.1016/j.jmb.2006.10.057",
      "article-title": "Phospholamban interacts with HAX-1, a mitochondrial protein with anti-apoptotic function",
      "volume": "367",
      "author": "Vafiadaki",
      "year": "2006",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "R92",
      "doi-asserted-by": "crossref",
      "first-page": "306",
      "DOI": "10.1091/mbc.e08-06-0587",
      "article-title": "The anti-apoptotic protein HAX-1 interacts with SERCA2 and regulates its protein levels to promote cell survival",
      "volume": "20",
      "author": "Vafiadaki",
      "year": "2009",
      "journal-title": "Mol Biol Cell"
    },
    {
      "key": "R93",
      "doi-asserted-by": "crossref",
      "first-page": "42557",
      "DOI": "10.1074/jbc.M502211200",
      "article-title": "Synthetic Vpr protein activates activator protein-1, c-jun N-terminal kinase, and NF- \u03ba B and stimulates HIV-1 transcription in promonocytic cells and primary macrophages",
      "volume": "280",
      "author": "Varin",
      "year": "2005",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "R94",
      "doi-asserted-by": "crossref",
      "first-page": "175",
      "DOI": "10.1101/gad.12.2.175",
      "article-title": "HIV-1 Vpr interacts with the nuclear transport pathway to promote macrophage infection",
      "volume": "12",
      "author": "Vodicka",
      "year": "1998",
      "journal-title": "Genes Dev"
    },
    {
      "key": "R95",
      "doi-asserted-by": "crossref",
      "first-page": "25564",
      "DOI": "10.1074/jbc.270.43.25564",
      "article-title": "Interaction of virion protein Vpr of human immunodeficiency virus type 1 with cellular transcription factor Sp1 and trans-activation of viral long terminal repeat",
      "volume": "270",
      "author": "Wang",
      "year": "1995",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "R96",
      "doi-asserted-by": "crossref",
      "first-page": "7",
      "DOI": "10.1016/0378-1119(96)00312-5",
      "article-title": "Characterization of a leucine-zipper-like domain in Vpr protein of human immunodeficiency virus type 1",
      "volume": "178",
      "author": "Wang",
      "year": "1996",
      "journal-title": "Gene"
    },
    {
      "key": "R97",
      "doi-asserted-by": "crossref",
      "first-page": "267",
      "DOI": "10.1089/dna.2007.0707",
      "article-title": "The HIV-1 Vif protein mediates degradation of Vpr and reduces Vpr-induced cell cycle arrest",
      "volume": "27",
      "author": "Wang",
      "year": "2008",
      "journal-title": "DNA Cell Biol"
    },
    {
      "key": "R98",
      "doi-asserted-by": "crossref",
      "first-page": "202",
      "DOI": "10.1002/bies.950080607",
      "article-title": "A conserved eukaryotic cell cycle control",
      "volume": "8",
      "author": "Warbrick",
      "year": "1988",
      "journal-title": "Bioessays"
    },
    {
      "key": "R99",
      "doi-asserted-by": "crossref",
      "first-page": "27046",
      "DOI": "10.1074/jbc.M703955200",
      "article-title": "The HIV1 protein Vpr acts to promote G2 cell cycle arrest by engaging a DDB1 and cullin4A-containing ubiquitin ligase complex using VprBP/DCAF1 as an adaptor",
      "volume": "282",
      "author": "Wen",
      "year": "2007",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "R100",
      "doi-asserted-by": "crossref",
      "first-page": "9732",
      "DOI": "10.1128/JVI.71.12.9732-9742.1997",
      "article-title": "Human immunodeficiency virus type 1 Vpr interacts with HHR23A, a cellular protein implicated in nucleotide excision DNA repair",
      "volume": "71",
      "author": "Withers-Ward",
      "year": "1997",
      "journal-title": "J Virol"
    },
    {
      "key": "R101",
      "doi-asserted-by": "crossref",
      "first-page": "384",
      "DOI": "10.1016/j.virol.2007.10.036",
      "article-title": "Cell-surface processing of extracellular human immunodeficiency virus type 1 Vpr by proprotein convertases",
      "volume": "372",
      "author": "Xiao",
      "year": "2008",
      "journal-title": "Virology"
    },
    {
      "key": "R102",
      "doi-asserted-by": "crossref",
      "first-page": "48816",
      "DOI": "10.1074/jbc.M207982200",
      "article-title": "Genetic selection of peptide inhibitors of human immunodeficiency virus type 1 Vpr",
      "volume": "277",
      "author": "Yao",
      "year": "2002",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "R103",
      "doi-asserted-by": "crossref",
      "first-page": "13735",
      "DOI": "10.1128/JVI.79.21.13735-13746.2005",
      "article-title": "Human immunodeficiency virus type 1 Vpr interacts with antiapoptotic mitochondrial protein HAX-1",
      "volume": "79",
      "author": "Yedavalli",
      "year": "2005",
      "journal-title": "J Virol"
    },
    {
      "key": "R104",
      "doi-asserted-by": "crossref",
      "first-page": "583",
      "DOI": "10.1083/jcb.200407156",
      "article-title": "The FG-repeat asymmetry of the nuclear pore complex is dispensable for bulk nucleocytoplasmic transport in vivo",
      "volume": "167",
      "author": "Zeitler",
      "year": "2004",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "R105",
      "first-page": "270",
      "article-title": "HIV-1 viral protein R (Vpr) & host cellular responses",
      "volume": "121",
      "author": "Zhao",
      "year": "2005",
      "journal-title": "Indian J Med Res"
    },
    {
      "key": "R106",
      "doi-asserted-by": "crossref",
      "first-page": "3791",
      "DOI": "10.1128/JVI.75.8.3791-3801.2001",
      "article-title": "Comparison of cell cycle arrest, transactivation, and apoptosis induced by the simian immunodeficiency virus SIVagm and human immunodeficiency virus type 1 vpr genes",
      "volume": "75",
      "author": "Zhu",
      "year": "2001",
      "journal-title": "J Virol"
    },
    {
      "key": "R107",
      "doi-asserted-by": "crossref",
      "first-page": "71",
      "DOI": "10.1023/A:1021653119934",
      "article-title": "Upregulation of survivin by HIV-1 Vpr",
      "volume": "8",
      "author": "Zhu",
      "year": "2003",
      "journal-title": "Apoptosis"
    },
    {
      "key": "R108",
      "doi-asserted-by": "crossref",
      "first-page": "8091",
      "DOI": "10.1074/jbc.M204783200",
      "article-title": "Regulation of the Apaf-1/caspase-9 apoptosome by caspase-3 and XIAP",
      "volume": "278",
      "author": "Zou",
      "year": "2003",
      "journal-title": "J Biol Chem"
    }
  ],
  "container-title": "Journal of General Virology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.microbiologyresearch.org/content/journal/jgv/10.1099/vir.0.011726-0?crawler=true",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        3,
        15
      ]
    ],
    "date-time": "2024-03-15T05:05:57Z",
    "timestamp": 1710479157000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.microbiologyresearch.org/content/journal/jgv/10.1099/vir.0.011726-0"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2009,
        8,
        1
      ]
    ]
  },
  "references-count": 108,
  "journal-issue": {
    "issue": "8",
    "published-print": {
      "date-parts": [
        [
          2009,
          8,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1099/vir.0.011726-0",
  "relation": {},
  "ISSN": [
    "0022-1317",
    "1465-2099"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        2009,
        8,
        1
      ]
    ]
  }
}