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Current HIV Research

Editor-in-Chief

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

Review Article

Evolution of Host Target Cell Specificity During HIV-1 Infection

Author(s): Olivia D. Council and Sarah B. Joseph*

Volume 16, Issue 1, 2018

Page: [13 - 20] Pages: 8

DOI: 10.2174/1570162X16666171222105721

Price: $65

Abstract

Background: Many details of HIV-1 molecular virology have been translated into lifesaving antiviral drugs. Yet, we have an incomplete understanding of the cells in which HIV-1 replicates in untreated individuals and persists in during antiretroviral therapy.

Methods: In this review we discuss how viral entry phenotypes have been characterized and the insights they have revealed about the target cells supporting HIV-1 replication. In addition, we will examine whether some HIV-1 variants have the ability to enter cells lacking CD4 (such as astrocytes) and the role that trans-infection plays in HIV-1 replication.

Results: HIV-1 entry into a target cell is determined by whether the viral receptor (CD4) and the coreceptor (CCR5 or CXCR4) are expressed on that cell. Sustained HIV-1 replication in a cell type can produce viral lineages that are tuned to the CD4 density and coreceptor expressed on those cells; a fact that allows us to use Env protein entry phenotypes to infer information about the cells in which a viral lineage has been replicating and adapting.

Conclusion: We now recognize that HIV-1 variants can be divided into three classes representing the primary target cells of HIV-1; R5 T cell-tropic variants that are adapted to entering memory CD4+ T cells, X4 T cell-tropic variants that are adapted to entering naïve CD4+ T cells and Mtropic variants that are adapted to entering macrophages and possibly other cells that express low levels of CD4. While much progress has been made, the relative contribution that infection of different cell subsets makes to viral pathogenesis and persistence is still being unraveled.

Keywords: CD4+ T cells, CCR5, HIV, envelope, tropism, macrophage, coreceptor, entry.

Graphical Abstract
[1]
Malim MH, Bieniasz PD. HIV restriction factors and mechanisms of evasion. Cold Spring Harbor Perspect Med 2012; 2: 16.
[2]
Wilen CB, Tilton JC, Doms RW. HIV: cell binding and entry. In: Bushman FD, Nabel GJ, Swanstrom R, Eds. HIV: From biology to prevention and treatment 2012/08. 22 ed. Cold Spring Harbor, New York: Cold Spring Harb Perspect Med 2012.
[3]
Dimitrov DS. Virus entry: Molecular mechanisms and biomedical applications. Nat Rev Microbiol 2004; 2: 109-22.
[4]
Joseph SB, Arrildt KT, Swanstrom AE, et al. Quantification of entry phenotypes of macrophage-tropic HIV-1 across a wide range of CD4 densities. J Virol 2014; 88: 1858-69.
[5]
Lee B, Sharron M, Montaner LJ, Weissman D, Doms RW. Quantification of CD4, CCR5, and CXCR4 levels on lymphocyte subsets, dendritic cells, and differentially conditioned monocyte-derived macrophages. Proc Natl Acad Sci USA 1999; 96: 5215-20.
[6]
Zamarchi R, Allavena P, Borsetti A, et al. Expression and functional activity of CXCR-4 and CCR-5 chemokine receptors in human thymocytes. Clin Exp Immunol 2002; 127: 321-30.
[7]
Schuitemaker H, Kootstra NA, Degoede REY, Dewolf F, Miedema F, Tersmette M. Monocytotropic human immunodeficiency virus type 1 (HIV-1) variants detectable in all stages of HIV-1 infection lack T-cell line tropism and syncytium-inducing ability in primary T-cell culture. J Virol 1991; 65: 356-63.
[8]
Joseph SB, Arrildt KT, Sturdevant CB, Swanstrom R. HIV-1 target cells in the CNS. J Neurovirol 2015; 21: 276-89.
[9]
Hesselgesser J, Liang M, Hoxie J, et al. Identification and characterization of the CXCR4 chemokine receptor in human T cell lines: Ligand binding, biological activity, and HIV-1 infectivity. J Immunol 1998; 160: 877-83.
[10]
Peters PJ, Sullivan WM, Duenas-Decamp MJ, et al. Non-macrophage-tropic human immunodeficiency virus type 1 R5 envelopes predominate in blood, lymph nodes, and semen: Implications for transmission and pathogenesis. J Virol 2006; 80: 6324-32.
[11]
Simmons G, Wilkinson D, Reeves JD, et al. Primary, syncytium-inducing human immunodeficiency virus type 1 isolates are dual-tropic and most can use either lestr or CCR5 as coreceptors for virus entry. J Virol 1996; 70: 8355-60.
[12]
Arrildt KT, LaBranche CC, Joseph SB, et al. Phenotypic correlates of HIV-1 macrophage tropism. J Virol 2015; 89: 11294-311.
[13]
Naif HM, Li S, Alali M, et al. CCR5 expression correlates with susceptibility of maturing monocytes to human immunodeficiency virus type 1 infection. J Virol 1998; 72: 830-6.
[14]
Sonza S, Maerz A, Uren S, et al. Susceptibility of human monocytes to HIV type 1 infection in vitro is not dependent on their level of CD4 expression. AIDS Res Hum Retroviruses 1995; 11: 769-76.
[15]
Schnell G, Joseph S, Spudich S, Price RW, Swanstrom R. HIV-1 replication in the central nervous system occurs in two distinct cell types. PLoS Pathog 2011; 7: e1002286.
[16]
Schnell G, Spudich S, Harrington P, Price RW, Swanstrom R. Compartmentalized human immunodeficiency virus type 1 originates from long-lived cells in some subjects with HIV-1-associated dementia. Plos Pathogens 2009; 5: e1000395.
[17]
Johnston SH, Lobritz MA, Nguyen S, et al. A quantitative affinity-profiling system that reveals distinct CD4/CCR5 usage patterns among human immunodeficiency virus type 1 and simian immunodeficiency virus strains. J Virol 2009; 83: 11016-26.
[18]
Parrish NF, Wilen CB, Banks LB, et al. Transmitted/founder and chronic subtype C HIV-1 use CD4 and CCR5 receptors with equal efficiency and are not inhibited by blocking the integrin α4β7. Plos Pathogens 2012; 8: e1002686.
[19]
Ping LH, Joseph SB, Anderson JA, et al. Comparison of viral Env proteins from acute and chronic infections with subtype C human immunodeficiency virus type 1 identifies differences in glycosylation and CCR5 utilization and suggests a new strategy for immunogen design. J Virol 2013; 87: 7218-33.
[20]
Isaacman-Beck J, Hermann EA, Yi YJ, et al. Heterosexual transmission of human immunodeficiency virus type 1 subtype C: Macrophage tropism, alternative coreceptor use, and the molecular anatomy of CCR5 utilization. J Virol 2009; 83: 8208-20.
[21]
Li H, Bar KJ, Wang S, et al. High multiplicity infection by HIV-1 in men who have sex with men. PLoS Pathog 2010; 6(5): e1000890.
[22]
Ochsenbauer C, Edmonds TG, Ding HT, et al. Generation of transmitted/founder HIV-1 infectious molecular clones and characterization of their replication capacity in CD4 T lymphocytes and monocyte-derived macrophages. J Virol 2012; 86: 2715-28.
[23]
Salazar-Gonzalez JF, Salazar MG, Keele BF, et al. Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J Exp Med 2009; 206: 1273-89.
[24]
Zhou S, Bednar MM, Sturdevant CB, Hauser BM, Swanstrom R. Deep sequencing of the HIV-1 env gene reveals discrete X4 lineages and linkage disequilibrium between X4 and R5 Viruses in the V1/V2 and V3 Variable regions. J Virol 2016; 90: 7142-58.
[25]
Brenchley JM, Hill BJ, Ambrozak DR, et al. T-cell subsets that harbor human immunodeficiency virus (HIV) in vivo: Implications for HIV pathogenesis. J Virol 2004; 78: 1160-8.
[26]
Fatkenheuer G, Pozniak AL, Johnson MA, et al. Efficacy of short-term monotherapy with maraviroc, a new CCR5 antagonist, in patients infected with HIV-1. Nat Med 2005; 11: 1170-2.
[27]
Hernandez-Novoa B, Madrid-Elena N, Dronda F, et al. Virological response to short-course maraviroc monotherapy does not predict viral tropism in HIV-1-infected treatment-naive patients. J Antimicrob Chemother 2014; 69: 1916-9.
[28]
Gornalusse GG, Mummidi S, Gaitan AA, et al. Epigenetic mechanisms, T-cell activation, and CCR5 genetics interact to regulate T-cell expression of CCR5, the major HIV-1 coreceptor. Proc Natl Acad Sci USA 2015; 112(34): E4762-71.
[29]
Hladik F, Liu HL, Speelmon E, et al. Combined effect of CCR5-Delta 32 heterozygosity and the CCR5 promoter polymorphism-2459 A/G on CCR5 expression and resistance to human immunodeficiency virus type 1 transmission. J Virol 2005; 79: 11677-84.
[30]
Reynes J, Portales P, Segondy M, et al. CD4 T cell surface CCR5 density as a host factor in HIV-1 disease progression. Aids 2001; 15: 1627-34.
[31]
Tang JM, Shelton B, Makhatadze NJ, et al. Distribution of chemokine receptor CCR2 and CCR5 genotypes and their relative contribution to human immunodeficiency virus type 1 (HIV-1) seroconversion, early HIV-1 RNA concentration in plasma, and later disease progression. J Virol 2002; 76: 662-72.
[32]
Wu LJ, Paxton WA, Kassam N, et al. CCR5 levels and expression pattern correlate with infectability by macrophage-tropic HIV-1, in vitro. J Exp Med 1997; 185: 1681-91.
[33]
Reynes J, Portales P, Segondy M, et al. CD4(+) T cell surface CCR5 density as a determining factor of virus load in persons infected with human immunodeficiency virus type 1. J Infect Dis 2000; 181: 927-32.
[34]
Lin YL, Mettling C, Portales P, Reynes J, Clot J, Corbeau P. Cell surface CCR5 density determines the postentry efficiency of R5 HIV-1 infection. Proc Natl Acad Sci USA 2002; 99: 15590-5.
[35]
Duenas-Decamp MJ, Peters PJ, Burton D, Clapham PR. Determinants flanking the CD4 binding loop modulate macrophage tropism of human immunodeficiency virus type 1 R5 envelopes. J Virol 2009; 83: 2575-83.
[36]
Dunfee RL, Thomas ER, Gorry PR, et al. The HIV Env variant N283 enhances macrophage tropism and is associated with brain infection and dementia. Proc Natl Acad Sci USA 2006; 103: 15160-5.
[37]
Gorry PR, Taylor J, Holm GH, et al. Increased CCR5 affinity and reduced CCR5/CD4 dependence of a neurovirulent primary human immunodeficiency virus type 1 isolate. J Virol 2002; 76: 6277-92.
[38]
Martin-Garcia J, Cao W, Varela-Robena A, Plassmeyer ML, Gonzalez-Scarano F. HIV-1 tropism for the central nervous system: Brain-denved envelope glycoproteins with lower CD4 dependence and reduced sensitivity to a fusion inhibitor. Virology 2006; 346: 169-79.
[39]
Peters PJ, Bhattacharya J, Hibbitts S, et al. Biological analysis of human immunodeficiency virus type 1 R5 envelopes amplified from brain and lymph node tissues of AIDS patients with neuropathology reveals two distinct tropism phenotypes and identifies envelopes in the brain that confer an enhanced tropism and fusigenicity for macrophages. J Virol 2004; 78: 6915-26.
[40]
Bednar MM, Hauser BM, Ping LH, et al. R5 Macrophage-Tropic HIV-1 in the Male Genital Tract. J Virol 2015; 89: 10688-92.
[41]
Gray L, Sterjovski J, Churchill M, et al. Uncoupling coreceptor usage of human immunodeficiency virus type 1 (HIV-1) from macrophage tropism reveals biological properties of CCR5-restricted HIV-1 isolates from patients with acquired immunodeficiency syndrome. Virology 2005; 337: 384-98.
[42]
Li S, Juarez J, Alali M, et al. Persistent CCR5 utilization and enhanced macrophage tropism by primary blood human immunodeficiency virus type 1 isolates from advanced stages of disease and comparison to tissue-derived isolates. J Virol 1999; 73: 9741-55.
[43]
Ousman SS, Kubes P. Immune surveillance in the central nervous system. Nat Neurosci 2012; 15: 1096-101.
[44]
Joseph SB, Swanstrom R, Kashuba ADM, Cohen MS. Bottlenecks in HIV-1 transmission: insights from the study of founder viruses. Nat Rev Microbiol 2015; 13: 414-25.
[45]
Moore JP, Cao YZ, Qing L, et al. Primary isolates of human immunodeficiency virus type 1 are relatively resistant to neutralization by monoclonal antibodies to gp120, and their neutralization is not predicted by studies with monomeric gp120. J Virol 1995; 69: 101-9.
[46]
Keir G, Thompson EJ. Proteins as parameters in the discrimination between different blood-CSF barriers. J Neurol Sci 1986; 75: 245-53.
[47]
Pillai SK, Pond SLK, Liu Y, et al. Genetic attributes of cerebrospinal fluid-derived HIV-1 env. Brain 2006; 129: 1872-83.
[48]
O’Connell O, Repik A, Reeves JD, et al. Efficiency of bridging-sheet recruitment explains HIV-1 R5 envelope glycoprotein sensitivity to soluble CD4 and macrophage tropism. J Virol 2013; 87: 187-98.
[49]
Triques K, Stevenson M. Characterization of restrictions to human immunodeficiency virus type 1 infection of monocytes. J Virol 2004; 78: 5523-7.
[50]
Huang W, Frantzell A, Toma J, Fransen S, Whitcomb JM, Stawiski E, et al. Mutational pathways and genetic barriers to CXCR4-mediated entry by human immunodeficiency virus type 1. Virology 2011; 409: 308-18.
[51]
Pollakis G, Kang S, Kliphuis A, Chalaby MIM, Goudsmit J, Paxton WA. N-linked glycosylation of the HIV type-1 gp120 envelope glycoprotein as a major determinant of CCR5 and CXCR4 coreceptor utilization. J Biol Chem 2001; 276: 13433-41.
[52]
Brumme ZL, Goodrich J, Mayer HB, et al. Molecular and clinical epidemiology of CXCR4-using HIV-1 in a large population of antiretroviral-naive individuals. J Infect Dis 2005; 192: 466-74.
[53]
Berger EA, Murphy PM, Farber JM. Chemokine receptors as HIV-1 coreceptors: Roles in viral entry, tropism, and disease. Annu Rev Immunol 1999; 17: 657-700.
[54]
Ping LH, Nelson JAE, Hoffman IF, Schock J, Lamers SL, Goodman M, et al. Characterization of V3 sequence heterogeneity in subtype C human immunodeficiency virus type 1 isolates from Malawi: Underrepresentation of X4 variants. J Virol 1999; 73: 6271-81.
[55]
Zhang H, Tully DC, Zhang TJ, Moriyama H, Thompson J, Wood C. Molecular determinants of HIV-1 subtype C coreceptor transition from R5 to R5X4. Virology 2010; 407: 68-79.
[56]
Zarate S, Pond SLK, Shapshak P, Frost SDW. Comparative study of methods for detecting sequence compartmentalization in human immunodeficiency virus type 1. J Virol 2007; 81: 6643-51.
[57]
Jabara CB, Jones CD, Roach J, Anderson JA, Swanstrom R. Accurate sampling and deep sequencing of the HIV-1 protease gene using a Primer ID. Proc Natl Acad Sci USA 2011; 108: 20166-71.
[58]
Keys JR, Zhou S, Anderson JA, et al. Primer ID Informs next-generation sequencing platforms and reveals preexisting drug resistance mutations in the HIV-1 reverse transcriptase coding domain. AIDS research and human retroviruses 2015; 31: 658-68.
[59]
Ayton S, Faux NG, Bush AI, Alzheimers Dis Neuroimaging I. Ferritin levels in the cerebrospinal fluid predict Alzheimer’s disease outcomes and are regulated by APOE. Nat Commun 2015; 6: 9.
[60]
Ribeiro RM, Hazenberg MD, Perelson AS, Davenport MP. Naive and memory cell turnover as drivers of CCR5-to-CXCR4 tropism switch in human immunodeficiency virus type 1: Implications for therapy. J Virol 2006; 80: 802-9.
[61]
Verhofstede C, Nijhuis M, Vandekerckhove L. Correlation of coreceptor usage and disease progression. Curr Opin HIV AIDS 2012; 7: 432-9.
[62]
Connor RI, Sheridan KE, Ceradini D, Choe S, Landau NR. Change in coreceptor use correlates with disease progression in HIV-1-infected individuals. J Exp Med 1997; 185: 621-8.
[63]
Moore JP, Kitchen SG, Pugach P, Zack JA. The CCR5 and CXCR4 coreceptors - Central to understanding the transmission and pathogenesis of human immunodeficiency virus type 1 infection. Aids Research and Human Retroviruses 2004; 20: 111-26.
[64]
Hunt PW, Harrigan PR, Huang W, et al. Prevalence of CXCR4 tropism among antiretroviral-treated HIV-1 - Infected patients with detectable viremia. J Infect Dis 2006; 194: 926-30.
[65]
Poveda E, Briz V, de Mendoza C, et al. Prevalence of X4 tropic HIV-1 variants in patients with differences in disease stage and exposure to antiretroviral therapy. J Med Virol 2007; 79: 1040-6.
[66]
Shepherd JC, Jacobson LP, Qiao W, et al. Emergence and persistence of CXCR4-tropic HIV-1 in a population of men from the Multicenter AIDS Cohort Study. J Infect Dis 2008; 198: 1104-12.
[67]
Weinberger AD, Perelson AS. Persistence and emergence of X4 virus in HIV infection. Math Biosci Eng 2011; 8(2): 605-26.
[68]
Weiser B, Philpott S, Klimkait T, et al. HIV-1 coreceptor usage and CXCR4-specific viral load predict clinical disease progression during combination antiretroviral therapy. Aids 2008; 22: 469-79.
[69]
Schuitemaker H, van ’t Wout AB, Lusso P. Clinical significance of HIV-1 coreceptor usage. J Transl Med 2011; 9: 17.
[70]
Regoes RR, Bonhoeffer S. The HIV coreceptor switch: a population dynamical perspective. Trends Microbiol 2005; 13: 269-77.
[71]
Dalgleish AG, Beverley PCL, Clapham PR, Crawford DH, Greaves MF, Weiss RA. The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 1984; 312: 763-7.
[72]
Klatzmann D, Champagne E, Chamaret S, et al. T-lymphocyte T4 molecule behaves as the receptor for human retrovirus LAV. Nature 1984; 312: 767-8.
[73]
Bruggeman LA, Ross MD, Tanji N, et al. Renal epithelium is a previously unrecognized site of HIV-1 infection. J Am Soc Nephrol 2000; 11: 2079-87.
[74]
Marras D, Bruggeman LA, Gao F, et al. Replication and compartmentalization of HIV-1 in kidney epithelium of patients with HIV-associated nephropathy. Nat Med 2002; 8: 522-6.
[75]
Bagasra O, Lavi E, Bobroski L, et al. Cellular reservoirs of HIV-1 in the central nervous system of infected individuals: Identification by the combination of in situ polymerase chain reaction and immunohistochemistry. Aids 1996; 10: 573-85.
[76]
Churchill MJ, Wesselingh SL, Cowley D, et al. Extensive astrocyte infection is prominent in human immunodeficiency virus-associated dementia. Ann Neurol 2009; 66: 253-8.
[77]
Nuovo GJ, Alfieri ML. AIDS dementia is associated with massive, activated HIV-1 infection and concomitant expression of several cytokines. Mol Med 1996; 2: 358-66.
[78]
Takahashi K, Wesselingh SL, Griffin DE, McArthur JC, Johnson RT, Glass JD. Localization of HIV-1 in human brain using polymerase chain reaction in situ hybridization and immunocytochemistry. Ann Neurol 1996; 39: 705-11.
[79]
Kolchinsky P, Mirzabekov T, Farzan M, et al. Adaptation of a CCR5-using, primary human immunodeficiency virus type 1 isolate for CD4-independent replication. J Virol 1999; 73: 8120-6.
[80]
LaBranche CC, Hoffman TL, Romano J, et al. Determinants of CD4 independence for a human immunodeficiency virus type 1 variant map outside regions required for coreceptor specificity. J Virol 1999; 73: 10310-9.
[81]
Hoffman TL, LaBranche CC, Zhang WT, et al. Stable exposure of the coreceptor-binding site in a CD4-independent HIV-1 envelope protein. Proc Natl Acad Sci USA 1999; 96: 6359-64.
[82]
Dumonceaux J, Nisole S, Chanel C, et al. Spontaneous mutations in the env gene of the human immunodeficiency virus type 1 NDK isolate are associated with a CD4-independent entry phenotype. J Virol 1998; 72: 512-9.
[83]
Boutet A, Salim H, Taoufik Y, et al. Isolated human astrocytes are not susceptible to infection by M- and T-tropic HIV-1 strains despite functional expression of the chemokine receptors CCR5 and CXCR4. Glia 2001; 34: 165-77.
[84]
Ma M, Geiger JD, Nath A. Characterization of a novel binding site for the human immunodeficiency virus type 1 envelope protein gp120 on human fetal astrocytes. J Virol 1994; 68(10): 6824-8.
[85]
Peudenier S, Hery C, Ng KH, Tardieu M. HIV receptors within the brain: a study of CD4 and MHC-II on human neurons, astrocytes and microglial cells. Res Virol 1991; 142: 145-9.
[86]
Sabri F, Tresoldi E, Di Stefano M, et al. Nonproductive human immunodeficiency virus type 1 infection of human fetal astrocytes: Independence from CD4 and major chemokine receptors. Virology 1999; 264: 370-84.
[87]
Speck RF, Esser U, Penn ML, et al. A trans-receptor mechanism for infection of CD4-negative cells by human immunodeficiency virus type 1. Curr Biol 1999; 9: 547-50.
[88]
Zhang Y, Sloan SA, Clarke LE, et al. Purification and characterization of progenitor and mature human astrocytes reveals transcriptional and functional differences with mouse. Neuron 2016; 89: 37-53.
[89]
Li GH, Anderson C, Jaeger L, Do T, Major EO, Nath A. Cell-to-cell contact facilitates HIV transmission from lymphocytes to astrocytes via CXCR4. Aids 2015; 29: 755-66.
[90]
Liu Y, Liu H, Kim BO, et al. CD4-independent infection of astrocytes by human immunodeficiency virus type 1: Requirement for the human mannose receptor. J Virol 2004; 78: 4120-33.
[91]
McCarthy M, He J, Wood C. HIV-1 strain-associated variability in infection of primary neuroglia. J Neurovirol 1998; 4: 80-9.
[92]
Di Rienzo AM, Aloisi F, Santarcangelo AC, et al. Virological and molecular parameters of HIV-1 infection of human embryonic astrocytes. Arch Virol 1998; 143: 1599-615.
[93]
Vijaykumar TS, Nath A, Chauhan A. Chloroquine mediated molecular tuning of astrocytes for enhanced permissiveness to HIV infection. Virology 2008; 381: 1-5.
[94]
Willey SJ, Reeves JD, Hudson R, et al. Identification of a subset of human immunodeficiency virus type 1 (HIV-1), HIV-2, and simian immunodeficiency virus strains able to exploit an alternative coreceptor on untransformed human brain and lymphoid cells. J Virol 2003; 77: 6138-52.
[95]
Russell RA, Chojnacki J, Jones DM, et al. Astrocytes Resist HIV-1 Fusion but Engulf Infected Macrophage Material. Cell Reports 2017; 18: 1473-83.
[96]
Canki M, Thai JNF, Chao W, Ghorpade A, Potash MJ, Volsky DJ. Highly productive infection with pseudotyped human immunodeficiency virus type 1 (HIV-1) indicates no intracellular restrictions to HIV-1 replication in primary human astrocytes. J Virol 2001; 75: 7925-33.
[97]
Chauhan A. Enigma of HIV-1 latent infection in astrocytes: an in-vitro study using protein kinase C agonist as a latency reversing agent. Microb Infect 2015; 17: 651-9.
[98]
Chauhan A, Khandkar M. Endocytosis of human immunodeficiency virus 1 (HIV-1) in astrocytes: A fiery path to its destination. Microbial Pathogenesis 2015; 78: 1-6.
[99]
Dewhurst S, Bresser J, Stevenson M, Sakai K, Evingerhodges MJ, Volsky DJ. Susceptibility of human glial cells to infection with human immunodeficiency virus (HIV). Febs Letters 1987; 213: 138-43.
[100]
Dewhurst S, Sakai K, Bresser J, Stevenson M, Evingerhodges MJ, Volsky DJ. Persistent productive infection of human glial cells by human immunodeficiency virus (HIV) and by infectious molecular clones of HIV. J Virol 1987; 61: 3774-82.
[101]
Shahabuddin M, Volsky B, Kim H, Sakai K, Volsky DJ. Regulated expression of human immunodeficiency virus type 1 in human glial cells: induction of dormant virus. Pathobiology 1992; 60: 195-205.
[102]
Churchill MJ, Gorry PR, Cowley D, et al. Use of laser capture microdissection to detect integrated HIV-1 DNA in macrophages and astrocytes from autopsy brain tissues. J Neurovirol 2006; 12: 146-52.
[103]
Gorry PR, Ong C, Thorpe J, et al. Astrocyte infection by HIV-1: Mechanisms of restricted virus replication, and role in the pathogenesis of HIV-1-associated dementia. Curr HIV Res 2003; 1: 463-73.
[104]
Thompson KA, Churchill MJ, Gorry PR, et al. Astrocyte specific viral strains in HIV dementia. Annals of Neurology 2004; 56: 873-7.
[105]
Calantone N, Wu F, Klase Z, et al. Tissue Myeloid Cells in SIV-Infected Primates Acquire Viral DNA through Phagocytosis of Infected T Cells. Immunity 2014; 41: 493-502.
[106]
Hijazi K, Wang Y, Scala C, et al. DC-SIGN Increases the Affinity of HIV-1 envelope glycoprotein interaction with CD4. PLoS One 2011; 6.
[107]
Johansson EL, Rudin A, Wassen L, Holmgren J. Distribution of lymphocytes and adhesion molecules in human cervix and vagina. Immunology 1999; 96: 272-7.
[108]
Xu HB, Wang XL, Veazey RS. Mucosal immunology of HIV infection. Immunol Rev 2013; 254: 10-33.
[109]
van Montfort T, Eggink D, Boot M, et al. HIV-1 N-Glycan Composition Governs a Balance between Dendritic Cell-Mediated Viral Transmission and Antigen Presentation. J Immunol 2011; 187: 4676-85.
[110]
Wu L. KewalRamani VN. Dendritic-cell interactions with HIV: infection and viral dissemination. Nat Rev Immunol 2006; 6: 859-68.
[111]
Coulon PG, Richetta C, Rouers A, et al. HIV-Infected Dendritic Cells Present Endogenous MHC Class II-Restricted Antigens to HIV-Specific CD4(+) T Cells. J Immunol 2016; 197: 517-32.
[112]
Arrighi JF, Pion M, Garcia E, et al. DC-SIGN-mediated infectious synapse formation enhances X4 HIV-1 transmission from dendritic cells to T cells. J Exp Med 2004; 200: 1279-88.
[113]
Geijtenbeek TBH, Kwon DS, Torensma R, et al. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 2000; 100: 587-97.
[114]
Jain P, Manuel SL, Khan ZK, Ahuja J, Quann K, Wigdahl B. DC-SIGN Mediates Cell-Free Infection and Transmission of Human T-Cell Lymphotropic Virus Type 1 by Dendritic Cells. J Virol 2009; 83: 10908-21.
[115]
Hammonds JE, Beeman N, Ding LM, et al. Siglec-1 initiates formation of the virus-containing compartment and enhances macrophage-to-T cell transmission of HIV-1. Plos Pathogens 2017; 13: 28.

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