HIV-1 infection of human macrophages directly induces viperin which inhibits viral production

Blood - Tập 120 - Trang 778-788 - 2012
Najla Nasr1, Susan Maddocks1, Stuart G. Turville1, Andrew N. Harman1, Natalie Woolger1, Karla J. Helbig2, John Wilkinson1, Chris R. Bye3, Thomas K. Wright1, Dharshini Rambukwelle1, Heather Donaghy1, Michael R. Beard2, Anthony L. Cunningham1
1Centre for Virus Research, Westmead Millennium Institute, Westmead and the University of Sydney, Sydney, Australia
2School of Molecular and Biomedical Science, University of Adelaide, Adelaide, Australia
3Florey Neuroscience Institutes, University of Melbourne, Melbourne, Australia

Tóm tắt

Abstract

Macrophages are key target cells for HIV-1. HIV-1BaL induced a subset of interferon-stimulated genes in monocyte-derived macrophages (MDMs), which differed from that in monocyte-derived dendritic cells and CD4 T cells, without inducing any interferons. Inhibition of type I interferon induction was mediated by HIV-1 inhibition of interferon-regulated factor (IRF3) nuclear translocation. In MDMs, viperin was the most up-regulated interferon-stimulated genes, and it significantly inhibited HIV-1 production. HIV-1 infection disrupted lipid rafts via viperin induction and redistributed viperin to CD81 compartments, the site of HIV-1 egress by budding in MDMs. Exogenous farnesol, which enhances membrane protein prenylation, reversed viperin-mediated inhibition of HIV-1 production. Mutagenesis analysis in transfected cell lines showed that the internal S-adenosyl methionine domains of viperin were essential for its antiviral activity. Thus viperin may contribute to persistent noncytopathic HIV-1 infection of macrophages and possibly to biologic differences with HIV-1–infected T cells.


Tài liệu tham khảo

Meltzer, 1992, Mononuclear phagocytes as targets, tissue reservoirs, and immunoregulatory cells in human immunodeficiency virus disease., Curr Top Microbiol Immunol, 181, 239 Kedzierska, 2002, The role of monocytes and macrophages in the pathogenesis of HIV-1 infection., Curr Med Chem, 9, 1893, 10.2174/0929867023368935 Chen, 2007, Determination of virus burst size in vivo using a single-cycle SIV in rhesus macaques., Proc Natl Acad Sci U S A, 104, 19079, 10.1073/pnas.0707449104 Dimitrov, 1993, Quantitation of human immunodeficiency virus type 1 infection kinetics., J Virol, 67, 2182, 10.1128/JVI.67.4.2182-2190.1993 Naif, 1999, Definition of the stage of host cell genetic restriction of replication of human immunodeficiency virus type 1 in monocytes and monocyte-derived macrophages by using twins., J Virol, 73, 4866, 10.1128/JVI.73.6.4866-4881.1999 Sonza, 2002, Selectively reduced tat mRNA heralds the decline in productive human immunodeficiency virus type 1 infection in monocyte-derived macrophages., J Virol, 76, 12611, 10.1128/JVI.76.24.12611-12621.2002 Hrecka, 2011, Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein., Nature, 474, 658, 10.1038/nature10195 Katze, 2002, Viruses and interferon: a fight for supremacy., Nat Rev Immunol, 2, 675, 10.1038/nri888 de Veer, 2001, Functional classification of interferon-stimulated genes identified using microarrays., J Leukoc Biol, 69, 912, 10.1189/jlb.69.6.912 Sadler, 2008, Interferon-inducible antiviral effectors., Nat Rev Immunol, 8, 559, 10.1038/nri2314 O'Neill, 2010, Sensing and signaling in antiviral innate immunity., Curr Biol, 20, R328, 10.1016/j.cub.2010.01.044 Yoneyama, 2010, Recognition of viral nucleic acids in innate immunity., Rev Med Virol, 20, 4, 10.1002/rmv.633 Gendelman, 1990, A selective defect of interferon alpha production in human immunodeficiency virus-infected monocytes., J Exp Med, 172, 1433, 10.1084/jem.172.5.1433 Gessani, 1994, Induction of beta interferon by human immunodeficiency virus type 1 and its gp120 protein in human monocytes-macrophages: role of beta interferon in restriction of virus replication., J Virol, 68, 1983, 10.1128/JVI.68.3.1983-1986.1994 Kornbluth, 1989, Interferons and bacterial lipopolysaccharide protect macrophages from productive infection by human immunodeficiency virus in vitro., J Exp Med, 169, 1137, 10.1084/jem.169.3.1137 Perno, 1994, In vitro activity of inhibitors of late stages of the replication of HIV in chronically infected macrophages., J Leukoc Biol, 56, 381, 10.1002/jlb.56.3.381 Woelk, 2004, Interferon gene expression following HIV type 1 infection of monocyte-derived macrophages., AIDS Res Hum Retroviruses, 20, 1210, 10.1089/aid.2004.20.1210 Doehle, 2009, Human immunodeficiency virus type 1 mediates global disruption of innate antiviral signaling and immune defenses within infected cells., J Virol, 83, 10395, 10.1128/JVI.00849-09 Okumura, 2008, HIV-1 accessory proteins VPR and Vif modulate antiviral response by targeting IRF-3 for degradation., Virology, 373, 85, 10.1016/j.virol.2007.10.042 Harman, 2011, HIV infection of dendritic cells subverts the interferon induction pathway via IRF1 and inhibits type 1 interferon production., Blood, 118, 298, 10.1182/blood-2010-07-297721 Chin, 2001, Viperin (cig5), an IFN-inducible antiviral protein directly induced by human cytomegalovirus., Proc Natl Acad Sci U S A, 98, 15125, 10.1073/pnas.011593298 Helbig, 2005, Analysis of ISG expression in chronic hepatitis C identifies viperin as a potential antiviral effector., Hepatology, 42, 702, 10.1002/hep.20844 Helbig, 2011, The antiviral protein viperin inhibits hepatitis C virus replication via interaction with nonstructural protein 5A., Hepatology, 54, 1506, 10.1002/hep.24542 Harman, 2006, HIV induces maturation of monocyte-derived dendritic cells and Langerhans cells., J Immunol, 177, 7103, 10.4049/jimmunol.177.10.7103 Turville, 2004, Immunodeficiency virus uptake, turnover, and 2-phase transfer in human dendritic cells., Blood, 103, 2170, 10.1182/blood-2003-09-3129 Harman, 2009, HIV-1-infected dendritic cells show 2 phases of gene expression changes, with lysosomal enzyme activity decreased during the second phase., Blood, 114, 85, 10.1182/blood-2008-12-194845 Lewin, 1999, Use of real-time PCR and molecular beacons to detect virus replication in human immunodeficiency virus type 1-infected individuals on prolonged effective antiretroviral therapy., J Virol, 73, 6099, 10.1128/JVI.73.7.6099-6103.1999 Turville, 2008, Resolution of de novo HIV production and trafficking in immature dendritic cells., Nat Methods, 5, 75, 10.1038/nmeth1137 Smyth, 2004, Linear models and empirical Bayes methods for assessing differential expression in microarray experiments., Statistical Applications in Genetics and Molecular Biology, 10.2202/1544-6115.1027 Dennis, 2003, DAVID: Database for Annotation, Visualization, and Integrated Discovery., Genome Biol, 4, P3, 10.1186/gb-2003-4-5-p3 Estaquier, 2002, Effects of antiretroviral drugs on human immunodeficiency virus type 1-induced CD4(+) T-cell death., J Virol, 76, 5966, 10.1128/JVI.76.12.5966-5973.2002 Fensterl, 2011, The ISG56/IFIT1 gene family., J Interferon Cytokine Res, 31, 71, 10.1089/jir.2010.0101 Lu, 2011, The IFITM proteins inhibit HIV-1 infection., J Virol, 85, 2126, 10.1128/JVI.01531-10 Deneka, 2007, In macrophages, HIV-1 assembles into an intracellular plasma membrane domain containing the tetraspanins CD81, CD9, and CD53., J Cell Biol, 177, 329, 10.1083/jcb.200609050 Carter, 2009, HIV entry in macrophages is dependent on intact lipid rafts., Virology, 386, 192, 10.1016/j.virol.2008.12.031 Wang, 2007, The interferon-inducible protein viperin inhibits influenza virus release by perturbing lipid rafts., Cell Host Microbe, 2, 96, 10.1016/j.chom.2007.06.009 Szkopińska, 2005, Farnesyl diphosphate synthase: regulation of product specificity., Acta Biochim Pol, 52, 45, 10.18388/abp.2005_3485 Ye, 2003, Disruption of hepatitis C virus RNA replication through inhibition of host protein geranylgeranylation., Proc Natl Acad Sci U S A, 100, 15865, 10.1073/pnas.2237238100 Coberley, 2004, Impact on genetic networks in human macrophages by a CCR5 strain of human immunodeficiency virus type 1., J Virol, 78, 11477, 10.1128/JVI.78.21.11477-11486.2004 Boudinot, 2000, Vesicular stomatitis virus and pseudorabies virus induce a vig1/cig5 homologue in mouse dendritic cells via different pathways., J Gen Virol, 81, 2675, 10.1099/0022-1317-81-11-2675 Ruvolo, 2003, The Epstein-Barr virus SM protein induces STAT1 and interferon-stimulated gene expression., J Virol, 77, 3690, 10.1128/JVI.77.6.3690-3701.2003 Hinson, 2009, The N-terminal amphipathic alpha-helix of viperin mediates localization to the cytosolic face of the endoplasmic reticulum and inhibits protein secretion., J Biol Chem, 284, 4705, 10.1074/jbc.M807261200 Grigorov, 2006, Assembly of infectious HIV-1 in human epithelial and T-lymphoblastic cell lines., J Mol Biol, 359, 848, 10.1016/j.jmb.2006.04.017 Jiang, 2008, Identification of three interferon-inducible cellular enzymes that inhibit the replication of hepatitis C virus., J Virol, 82, 1665, 10.1128/JVI.02113-07 Wang, 2012, Viperin inhibits hepatitis C virus replication by interfering with the binding of NS5A to host protein hVAP-33., J Gen Virol, 93, 83, 10.1099/vir.0.033860-0 Leung, 2008, HIV-1 assembly: viral glycoproteins segregate quantally to lipid rafts that associate individually with HIV-1 capsids and virions., Cell Host Microbe, 3, 285, 10.1016/j.chom.2008.04.004 Okumura, 2006, Innate antiviral response targets HIV-1 release by the induction of ubiquitin-like protein ISG15., Proc Natl Acad Sci U S A, 103, 1440, 10.1073/pnas.0510518103 Rivieccio, 2006, TLR3 ligation activates an antiviral response in human fetal astrocytes: a role for viperin/cig5., J Immunol, 177, 4735, 10.4049/jimmunol.177.7.4735