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Current HIV Research

Editor-in-Chief

ISSN (Print): 1570-162X
ISSN (Online): 1873-4251

Research Article

Plasma Membrane Proteomic Profile Discovers Macrophage-capping Protein Related to Latent HIV-1

Author(s): Yujiao Zhang, Yinzhong Shen, Lin Yin, Tangkai Qi, Xiaofang Jia, Hongzhou Lu and Lijun Zhang*

Volume 17, Issue 1, 2019

Page: [42 - 52] Pages: 11

DOI: 10.2174/1570162X17666190506155222

Abstract

Background: Due to the persistence of latent HIV-infected cellular reservoirs, HIV virus can not be eradicated completely.

Objective: To identify proteins related to HIV latency, we performed a subcellular proteomic study in HIV latent cell lines.

Methods: An established HIV-1 latent cell model (J-Lat Tat-GFP Clone A7 cells, A7 cells) and its parental cell line (Jurkat cells) were used. The plasma membrane (PM) fraction from cultured cells was enriched through aqueous two-phase partition. PM proteins were extracted and then separated using two-dimensional electrophoresis (2DE). Differentially expressed proteins were identified by mass spectrometry, and verified by western blotting.

Results: Thirteen non-redundant proteins were identified to be differentially expressed in the A7 PM fraction compared to those in the Jurkat PM. Eight had a PM location through Gene Ontology (GO) analysis. A differential protein network of CAPG-ACTR3-CD3D was detected to have interactions with HIV Vpr, Tat, gp160, etc. through STRING software analysis. One of the differential proteins (Macrophage-capping protein (CAPG)) was verified by western blotting to be down- regulated in two cell lines and HIV resting CD4+ T cells negatively selected from patients.

Conclusion: We identified 13 proteins in A7 compared to Jurkat cells. CAPG may be a potential biomarker related to HIV latency.

Keywords: HIV, latency, proteomics, plasma membrane, CAPG, resting CD4+ T cells, reservoirs.

Graphical Abstract
[1]
Trickey AMM, Vehreschild JJ, Obel N, et al. Survival of HIV-positive patients starting antiretroviral therapy between 1996 and 2013: a collaborative analysis of cohort studies. Lancet HIV 2017; 4(8): e349-56.
[http://dx.doi.org/10.1016/S2352-3018(17)30066-8] [PMID: 28501495]
[2]
Edelman EJ, Gordon KS, Glover J, McNicholl IR, Fiellin DA, Justice AC. The next therapeutic challenge in HIV: polypharmacy. Drugs Aging 2013; 30(8): 613-28.
[http://dx.doi.org/10.1007/s40266-013-0093-9] [PMID: 23740523]
[3]
Eisele E, Siliciano RF. Redefining the viral reservoirs that prevent HIV-1 eradication. Immunity 2012; 37(3): 377-88.
[http://dx.doi.org/10.1016/j.immuni.2012.08.010] [PMID: 22999944]
[4]
Kumar A, Abbas W, Herbein G. HIV-1 latency in monocytes/macrophages. Viruses 2014; 6(4): 1837-60.
[http://dx.doi.org/10.3390/v6041837] [PMID: 24759213]
[5]
Rosca EC, Rosca O, Simu M, Chirileanu RD. HIV-associated neurocognitive disorders: a historical review. Neurologist 2012; 18(2): 64-7.
[http://dx.doi.org/10.1097/NRL.0b013e318247bc7a] [PMID: 22367830]
[6]
Merlini E, Bai F, Bellistrì GM, Tincati C, d’Arminio Monforte A, Marchetti G. Evidence for polymicrobic flora translocating in peripheral blood of HIV-infected patients with poor immune response to antiretroviral therapy. PLoS One 2011; 6(4): e18580.
[http://dx.doi.org/10.1371/journal.pone.0018580] [PMID: 21494598]
[7]
Kumar A, Abbas W, Bouchat S, et al. Limited HIV-1 Reactivation in Resting CD4+ T cells from Aviremic Patients under Protease Inhibitors. Sci Rep 2016; 6: 38313.
[http://dx.doi.org/10.1038/srep38313] [PMID: 27922055]
[8]
Spina CA, Anderson J, Archin NM, et al. An in-depth comparison of latent HIV-1 reactivation in multiple cell model systems and resting CD4+ T cells from aviremic patients. PLoS Pathog 2013; 9(12): e1003834.
[http://dx.doi.org/10.1371/journal.ppat.1003834] [PMID: 24385908]
[9]
Mbonye U, Karn J. Control of HIV latency by epigenetic and non-epigenetic mechanisms. Curr HIV Res 2011; 9(8): 554-67.
[http://dx.doi.org/10.2174/157016211798998736] [PMID: 22211660]
[10]
Carrillo J, Clotet B, Blanco J. Antibodies and antibody derivatives: New partners in HIV eradication strategies. Front Immunol 2018; 9: 2429.
[http://dx.doi.org/10.3389/fimmu.2018.02429] [PMID: 30405624]
[11]
Romani B, Allahbakhshi E. Underlying mechanisms of HIV-1 latency. Virus Genes 2017; 53(3): 329-39.
[http://dx.doi.org/10.1007/s11262-017-1443-1] [PMID: 28258391]
[12]
Coiras M, Lopez-Huertas MR, Alcami J. HIV-1 latency and eradication of long-term viral reservoirs. Discov Med 2010; 9(46): 185-91.
[PMID: 20350483]
[13]
Castro-Gonzalez S, Colomer-Lluch M, Serra-Moreno R. Barriers for HIV Cure: The Latent Reservoir. AIDS Res Hum Retroviruses 2018; 34(9): 739-59.
[http://dx.doi.org/10.1089/aid.2018.0118] [PMID: 30056745]
[14]
Donnelly MR, Ciborowski P. Proteomics, biomarkers, and HIV-1: A current perspective. Proteomics Clin Appl 2016; 10(2): 110-25.
[http://dx.doi.org/10.1002/prca.201500002] [PMID: 26033875]
[15]
Chertova E, Chertov O, Coren LV, et al. Proteomic and biochemical analysis of purified human immunodeficiency virus type 1 produced from infected monocyte-derived macrophages. J Virol 2006; 80(18): 9039-52.
[http://dx.doi.org/10.1128/JVI.01013-06] [PMID: 16940516]
[16]
Rasheed S, Yan JS, Hussain A, Lai B. Proteomic characterization of HIV-modulated membrane receptors, kinases and signaling proteins involved in novel angiogenic pathways. J Transl Med 2009; 7: 75.
[http://dx.doi.org/10.1186/1479-5876-7-75] [PMID: 19712456]
[17]
Ciuffi A, Mohammadi P, Golumbeanu M, di Iulio J, Telenti A. Bioinformatics and HIV latency. Curr HIV/AIDS Rep 2015; 12(1): 97-106.
[http://dx.doi.org/10.1007/s11904-014-0240-x] [PMID: 25586146]
[18]
Tyagi M, Iordanskiy S, Ammosova T, et al. Reactivation of latent HIV-1 provirus via targeting protein phosphatase-1. Retrovirology 2015; 12: 63.
[http://dx.doi.org/10.1186/s12977-015-0190-4] [PMID: 26178009]
[19]
Pérez M, de Vinuesa AG, Sanchez-Duffhues G, et al. Bryostatin-1 synergizes with histone deacetylase inhibitors to reactivate HIV-1 from latency. Curr HIV Res 2010; 8(6): 418-29.
[http://dx.doi.org/10.2174/157016210793499312] [PMID: 20636281]
[20]
Berro R, de la Fuente C, Klase Z, et al. Identifying the membrane proteome of HIV-1 latently infected cells. J Biol Chem 2007; 282(11): 8207-18.
[http://dx.doi.org/10.1074/jbc.M606324200] [PMID: 17237230]
[21]
Zhang L, Jia X, Jin JO, Lu H, Tan Z. Recent 5-year Findings and Technological Advances in the Proteomic Study of HIV-associated Disorders. Genomics Proteomics Bioinformatics 2017; 15(2): 110-20.
[http://dx.doi.org/10.1016/j.gpb.2016.11.002] [PMID: 28391008]
[22]
Vit O, Petrak J. Integral membrane proteins in proteomics. How to break open the black box? J Proteomics 2017; 153: 8-20.
[http://dx.doi.org/10.1016/j.jprot.2016.08.006] [PMID: 27530594]
[23]
Ono A. HIV-1 assembly at the plasma membrane. Vaccine 2010; 28(Suppl. 2): B55-9.
[http://dx.doi.org/10.1016/j.vaccine.2009.10.021] [PMID: 20510745]
[24]
Abbas W, Herbein G. Plasma membrane signaling in HIV-1 infection. Biochim Biophys Acta 2014; 1838(4): 1132-42.
[http://dx.doi.org/10.1016/j.bbamem.2013.06.020] [PMID: 23806647]
[25]
Eggink D, Bontjer I, de Taeye SW, Langedijk JPM, Berkhout B, Sanders RW. HIV-1 anchor inhibitors and membrane fusion inhibitors target distinct but overlapping steps in virus entry. J Biol Chem 2019; 294(15): 5736-46.
[http://dx.doi.org/10.1074/jbc.RA119.007360] [PMID: 30696772]
[26]
Sigalov AB. Transmembrane interactions as immunotherapeutic targets: lessons from viral pathogenesis. Adv Exp Med Biol 2007; 601: 335-44.
[http://dx.doi.org/10.1007/978-0-387-72005-0_36] [PMID: 17713022]
[27]
Shukla HD, Vaitiekunas P, Cotter RJ. Advances in membrane proteomics and cancer biomarker discovery: current status and future perspective. Proteomics 2012; 12(19-20): 3085-104.
[http://dx.doi.org/10.1002/pmic.201100519] [PMID: 22890602]
[28]
Orsburn BC, Stockwin LH, Newton DL. Challenges in plasma membrane phosphoproteomics. Expert Rev Proteomics 2011; 8(4): 483-94.
[http://dx.doi.org/10.1586/epr.11.40] [PMID: 21819303]
[29]
Qu X, Ying H, Wang X, et al. Histone deacetylase inhibitor MC1293 induces latent HIV-1 reactivation by histone modification in vitro latency cell lines. Curr HIV Res 2013; 11(1): 24-9.
[PMID: 23092175]
[30]
Ying H, Zhang Y, Lin S, Han Y, Zhu HZ. Histone deacetylase inhibitor Scriptaid reactivates latent HIV-1 promoter by inducing histone modification in in vitro latency cell lines. Int J Mol Med 2010; 26(2): 265-72.
[PMID: 20596607]
[31]
Ying H, Zhang Y, Zhou X, et al. Selective histonedeacetylase inhibitor M344 intervenes in HIV-1 latency through increasing histone acetylation and activation of NF-kappaB. PLoS One 2012; 7(11): e48832.
[http://dx.doi.org/10.1371/journal.pone.0048832] [PMID: 23166597]
[32]
Abreu CM, Price SL, Shirk EN, et al. Dual role of novel ingenol derivatives from Euphorbia tirucalli in HIV replication: inhibition of de novo infection and activation of viral LTR. PLoS One 2014; 9(5): e97257.
[http://dx.doi.org/10.1371/journal.pone.0097257] [PMID: 24827152]
[33]
Lenasi T, Contreras X, Peterlin BM. Transcriptional interference antagonizes proviral gene expression to promote HIV latency. Cell Host Microbe 2008; 4(2): 123-33.
[http://dx.doi.org/10.1016/j.chom.2008.05.016] [PMID: 18692772]
[34]
Wong VC, Fong LE, Adams NM, Xue Q, Dey SS, Miller-Jensen K. Quantitative evaluation and optimization of co-drugging to improve anti-HIV latency therapy. Cell Mol Bioeng 2014; 7(3): 320-33.
[http://dx.doi.org/10.1007/s12195-014-0336-9] [PMID: 26191086]
[35]
Bolther M, Dalgaard LS, Kristensen LH, Tarp BD, Jensen-Fangel S. Testing for hepatitis B virus and HIV in patients with chronic hepatitis C: screening performance and outcome. Scand J Infect Dis 2014; 46(10): 686-92.
[http://dx.doi.org/10.3109/00365548.2014.929734] [PMID: 25134654]
[36]
Lu DY, Wu HY, Yarla NS, Xu B, Ding J, Lu TR. HAART in HIV/AIDS treatments: Future trends. Infect Disord Drug Targets 2018; 18(1): 15-22.
[http://dx.doi.org/10.2174/1871526517666170505122800] [PMID: 28474549]
[37]
Choveau FS, Zhang J, Bierbower SM, Sharma R, Shapiro MS. The role of the carboxyl terminus helix C-D linker in regulating KCNQ3 K+ current amplitudes by controlling channel trafficking. PLoS One 2015; 10(12): e0145367.
[http://dx.doi.org/10.1371/journal.pone.0145367] [PMID: 26692086]
[38]
Wang H, Gao Z, Liu X, et al. Targeted production of reactive oxygen species in mitochondria to overcome cancer drug resistance. Nat Commun 2018; 9(1): 562.
[http://dx.doi.org/10.1038/s41467-018-02915-8] [PMID: 29422620]
[39]
Zhang L, Jia X, Zhang X, et al. Alpha-1 antitrypsin variants in plasma from HIV-infected patients revealed by proteomic and glycoproteomic analysis. Electrophoresis 2010; 31(20): 3437-45.
[http://dx.doi.org/10.1002/elps.201000153] [PMID: 20859951]
[40]
Zhang L, Jia X, Zhang X, et al. Proteomic analysis of PBMCs: characterization of potential HIV-associated proteins. Proteome Sci 2010; 8: 12.
[http://dx.doi.org/10.1186/1477-5956-8-12] [PMID: 20222986]
[41]
Zhang L, Peng X, Zhang Z, et al. Subcellular proteome analysis unraveled annexin A2 related to immune liver fibrosis. J Cell Biochem 2010; 110(1): 219-28.
[http://dx.doi.org/10.1002/jcb.22529] [PMID: 20225235]
[42]
Kanoke A, Fujimura M, Niizuma K, et al. Temporal profile of magnetic resonance angiography and decreased ratio of regulatory T cells after immunological adjuvant administration to mice lacking RNF213, a susceptibility gene for moyamoya disease. Brain Res 2016; 1642: 1-9.
[http://dx.doi.org/10.1016/j.brainres.2016.03.009] [PMID: 26972532]
[43]
Zehn D, Cohen CJ, Reiter Y, Walden P. Extended presentation of specific MHC-peptide complexes by mature dendritic cells compared to other types of antigen-presenting cells. Eur J Immunol 2004; 34(6): 1551-60.
[http://dx.doi.org/10.1002/eji.200324355] [PMID: 15162424]
[44]
Wagner M, Poeck H, Jahrsdoerfer B, et al. IL-12p70-dependent Th1 induction by human B cells requires combined activation with CD40 ligand and CpG DNA. J Immunol 2004; 172(2): 954-63.
[http://dx.doi.org/10.4049/jimmunol.172.2.954] [PMID: 14707068]
[45]
Crawford GE, Holt IE, Mullikin JC, et al. Identifying gene regulatory elements by genome-wide recovery of DNase hypersensitive sites. Proc Natl Acad Sci USA 2004; 101(4): 992-7.
[http://dx.doi.org/10.1073/pnas.0307540100] [PMID: 14732688]
[46]
Finney HM, Akbar AN, Lawson AD. Activation of resting human primary T cells with chimeric receptors: costimulation from CD28, inducible costimulator, CD134, and CD137 in series with signals from the TCR zeta chain. J Immunol 2004; 172(1): 104-13.
[http://dx.doi.org/10.4049/jimmunol.172.1.104] [PMID: 14688315]
[47]
Zitt C, Strauss B, Schwarz EC, et al. Potent inhibition of Ca2+ release-activated Ca2+ channels and T-lymphocyte activation by the pyrazole derivative BTP2. J Biol Chem 2004; 279(13): 12427-37.
[http://dx.doi.org/10.1074/jbc.M309297200] [PMID: 14718545]
[48]
Wu W, Chen J, Ding Q, et al. Function of the macrophage-capping protein in colorectal carcinoma. Oncol Lett 2017; 14(5): 5549-55.
[http://dx.doi.org/10.3892/ol.2017.6888] [PMID: 29113183]
[49]
Bin-Jaliah I. Natural Hypoxia is Not a Limiting Factor in Evaluating the Novel Arylidene Derivative MLT-401 Against an In Vitro Colorectal Cancer Model. Cell Physiol Biochem 2018; 46(5): 2082-9.
[http://dx.doi.org/10.1159/000489448] [PMID: 29723868]
[50]
Mohammadi P, Ciuffi A, Beerenwinkel N. Dynamic models of viral replication and latency. Curr Opin HIV AIDS 2015; 10(2): 90-5.
[http://dx.doi.org/10.1097/COH.0000000000000136] [PMID: 25565177]
[51]
Finzi D, Blankson J, Siliciano JD, et al. Latent infection of CD4+ T cells provides a mechanism for lifelong persistence of HIV-1, even in patients on effective combination therapy. Nat Med 1999; 5(5): 512-7.
[http://dx.doi.org/10.1038/8394] [PMID: 10229227]
[52]
Shirakawa K, Chavez L, Hakre S, Calvanese V, Verdin E. Reactivation of latent HIV by histone deacetylase inhibitors. Trends Microbiol 2013; 21(6): 277-85.
[http://dx.doi.org/10.1016/j.tim.2013.02.005] [PMID: 23517573]
[53]
Archin NM, Margolis DM. Emerging strategies to deplete the HIV reservoir. Curr Opin Infect Dis 2014; 27(1): 29-35.
[http://dx.doi.org/10.1097/QCO.0000000000000026] [PMID: 24296585]
[54]
Descours B, Petitjean G, López-Zaragoza JL, et al. CD32a is a marker of a CD4 T-cell HIV reservoir harbouring replication-competent proviruses. Nature 2017; 543(7646): 564-7.
[http://dx.doi.org/10.1038/nature21710] [PMID: 28297712]
[55]
Cao S, Slack SD, Levy CN, et al. Hybrid nanocarriers incorporating mechanistically distinct drugs for lymphatic CD4+ T cell activation and HIV-1 latency reversal. Sci Adv 2019; 5(3): eaav6322.
[http://dx.doi.org/10.1126/sciadv.aav6322] [PMID: 30944862]
[56]
Takata H, Kessing C, Sy A, et al. Modeling HIV-1 latency using primary CD4+ T cells from HIV-1 infected ART suppressed individuals. J Virol 2019; 93(11): 02248-18.
[http://dx.doi.org/10.1128/JVI.02248-18] [PMID: 30918072]
[57]
Bruner KM, Wang Z, Simonetti FR, et al. A quantitative approach for measuring the reservoir of latent HIV-1 proviruses. Nature 2019; 566(7742): 120-5.
[http://dx.doi.org/10.1038/s41586-019-0898-8] [PMID: 30700913]
[58]
Symons J, Chopra A, Malatinkova E, et al. HIV integration sites in latently infected cell lines: evidence of ongoing replication. Retrovirology 2017; 14(1): 2.
[http://dx.doi.org/10.1186/s12977-016-0325-2] [PMID: 28086908]
[59]
Trejbalová K, Kovářová D, Blažková J, et al. Development of 5′ LTR DNA methylation of latent HIV-1 provirus in cell line models and in long-term-infected individuals. Clin Epigenetics 2016; 8: 19.
[http://dx.doi.org/10.1186/s13148-016-0185-6] [PMID: 26900410]
[60]
Arenaccio C, Anticoli S, Manfredi F, Chiozzini C, Olivetta E, Federico M. Latent HIV-1 is activated by exosomes from cells infected with either replication-competent or defective HIV-1. Retrovirology 2015; 12: 87.
[http://dx.doi.org/10.1186/s12977-015-0216-y] [PMID: 26502902]
[61]
Eriksson S, Graf EH, Dahl V, et al. Comparative analysis of measures of viral reservoirs in HIV-1 eradication studies. PLoS Pathog 2013; 9(2): e1003174.
[http://dx.doi.org/10.1371/journal.ppat.1003174] [PMID: 23459007]
[62]
Kuznetsov VA, Stepanov VS, Berzofsky JA, Belyakov IM. Assessment of the relative therapeutic effects of vaccines on virus load and immune responses in small groups at several time points: efficacy of mucosal and subcutaneous polypeptide vaccines in rhesus macaques exposed to SHIV. J Clin Virol 2004; 31(Suppl. 1): S69-82.
[http://dx.doi.org/10.1016/j.jcv.2004.09.006] [PMID: 15567097]
[63]
Elliott JH, McMahon JH, Chang CC, et al. Short-term administration of disulfiram for reversal of latent HIV infection: a phase 2 dose-escalation study. Lancet HIV 2015; 2(12): e520-9.
[http://dx.doi.org/10.1016/S2352-3018(15)00226-X] [PMID: 26614966]
[64]
Pantaleo G, Graziosi C, Demarest JF, et al. HIV infection is active and progressive in lymphoid tissue during the clinically latent stage of disease. Nature 1993; 362(6418): 355-8.
[http://dx.doi.org/10.1038/362355a0] [PMID: 8455722]
[65]
Rasmussen TA, Tolstrup M, Brinkmann CR, et al. Panobinostat, a histone deacetylase inhibitor, for latent-virus reactivation in HIV-infected patients on suppressive antiretroviral therapy: a phase 1/2, single group, clinical trial. Lancet HIV 2014; 1(1): e13-21.
[http://dx.doi.org/10.1016/S2352-3018(14)70014-1] [PMID: 26423811]
[66]
Jordan A, Bisgrove D, Verdin E. HIV reproducibly establishes a latent infection after acute infection of T cells in vitro. EMBO J 2003; 22(8): 1868-77.
[http://dx.doi.org/10.1093/emboj/cdg188] [PMID: 12682019]
[67]
Emiliani S, Van Lint C, Fischle W, et al. A point mutation in the HIV-1 Tat responsive element is associated with postintegration latency. Proc Natl Acad Sci USA 1996; 93(13): 6377-81.
[http://dx.doi.org/10.1073/pnas.93.13.6377] [PMID: 8692823]
[68]
Emiliani S, Fischle W, Ott M, Van Lint C, Amella CA, Verdin E. Mutations in the tat gene are responsible for human immunodeficiency virus type 1 postintegration latency in the U1 cell line. J Virol 1998; 72(2): 1666-70.
[PMID: 9445075]
[69]
Iglesias-Ussel M, Vandergeeten C, Marchionni L, Chomont N, Romerio F. High levels of CD2 expression identify HIV-1 latently infected resting memory CD4+ T cells in virally suppressed subjects. J Virol 2013; 87(16): 9148-58.
[http://dx.doi.org/10.1128/JVI.01297-13] [PMID: 23760244]
[70]
Cohn LB, Silva IT, Oliveira TY, et al. HIV-1 integration landscape during latent and active infection. Cell 2015; 160(3): 420-32.
[http://dx.doi.org/10.1016/j.cell.2015.01.020] [PMID: 25635456]
[71]
Dumaual CM, Steere BA, Walls CD, Wang M, Zhang ZY, Randall SK. Integrated analysis of global mRNA and protein expression data in HEK293 cells overexpressing PRL-1. PLoS One 2013; 8(9): e72977.
[http://dx.doi.org/10.1371/journal.pone.0072977] [PMID: 24019887]
[72]
Sun Y, Hu B, Fan C, et al. iTRAQ-based quantitative subcellular proteomic analysis of Avibirnavirus-infected cells. Electrophoresis 2015; 36(14): 1596-611.
[http://dx.doi.org/10.1002/elps.201500014] [PMID: 25929241]
[73]
Wang XY, Yu HZ, Xu JP, et al. Comparative Subcellular Proteomics Analysis of Susceptible and Near-isogenic Resistant Bombyx mori (Lepidoptera) Larval Midgut Response to BmNPV infection. Sci Rep 2017; 7: 45690.
[http://dx.doi.org/10.1038/srep45690] [PMID: 28361957]
[74]
Wu X, Wang S, Yu Y, et al. Subcellular proteomic analysis of human host cells infected with H3N2 swine influenza virus. Proteomics 2013; 13(22): 3309-26.
[http://dx.doi.org/10.1002/pmic.201300180] [PMID: 24115376]
[75]
Mannová P, Fang R, Wang H, et al. Modification of host lipid raft proteome upon hepatitis C virus replication. Mol Cell Proteomics 2006; 5(12): 2319-25.
[http://dx.doi.org/10.1074/mcp.M600121-MCP200] [PMID: 16943187]
[76]
Zhang L, Xie J, Wang X, et al. Proteomic analysis of mouse liver plasma membrane: use of differential extraction to enrich hydrophobic membrane proteins. Proteomics 2005; 5(17): 4510-24.
[http://dx.doi.org/10.1002/pmic.200401318] [PMID: 16222721]
[77]
Matheson NJ, Sumner J, Wals K, et al. Cell Surface Proteomic Map of HIV Infection Reveals Antagonism of Amino Acid Metabolism by Vpu and Nef. Cell Host Microbe 2015; 18(4): 409-23.
[http://dx.doi.org/10.1016/j.chom.2015.09.003] [PMID: 26439863]
[78]
Haller C, Müller B, Fritz JV, et al. HIV-1 Nef and Vpu are functionally redundant broad-spectrum modulators of cell surface receptors, including tetraspanins. J Virol 2014; 88(24): 14241-57.
[http://dx.doi.org/10.1128/JVI.02333-14] [PMID: 25275127]
[79]
Barber EK, Dasgupta JD, Schlossman SF, Trevillyan JM, Rudd CE. The CD4 and CD8 antigens are coupled to a protein-tyrosine kinase (p56lck) that phosphorylates the CD3 complex. Proc Natl Acad Sci USA 1989; 86(9): 3277-81.
[http://dx.doi.org/10.1073/pnas.86.9.3277] [PMID: 2470098]
[80]
Li T, Hong X, Zhao J, et al. Gelsolin-like actin-capping protein is associated with patient prognosis, cellular apoptosis and proliferation in prostate cancer. Biomarkers Med 2016; 10(12): 1251-60.
[http://dx.doi.org/10.2217/bmm-2016-0186] [PMID: 27924630]
[81]
Kok YL, Ciuffi A, Metzner KJ. Unravelling HIV-1 Latency, One cell at a time. Trends Microbiol 2017; 25(11): 932-41.
[http://dx.doi.org/10.1016/j.tim.2017.06.002] [PMID: 28668335]
[82]
Baxter AE, Niessl J, Fromentin R, et al. Single-cell characterization of viral translation-competent reservoirs in HIV-infected individuals. Cell Host Microbe 2016; 20(3): 368-80.
[http://dx.doi.org/10.1016/j.chom.2016.07.015] [PMID: 27545045]

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