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Preferential replication of HIV-1 in the CD45RO memory cell subset of primary CD4 lymphocytes in vitro.
C A Spina, … , H E Prince, D D Richman
C A Spina, … , H E Prince, D D Richman
Published April 1, 1997
Citation Information: J Clin Invest. 1997;99(7):1774-1785. https://doi.org/10.1172/JCI119342.
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Preferential replication of HIV-1 in the CD45RO memory cell subset of primary CD4 lymphocytes in vitro.

Abstract

The ability of HIV-1 to establish an infection and replicate to high copy number in CD4 lymphocytes is dependent on both the activation state of the cell and virus-encoded regulatory proteins that modulate viral gene expression. To study these required virus-cell interactions, we have used an in vitro cell model of acute HIV infection of quiescent, primary CD4 lymphocytes and subsequent induction of T cell activation and virus replication by lectin or CD3 receptor cross-linking. Experiments were done to determine if the capacity of HIV to establish infection and complete replication was impacted by the maturational state of the CD4 cell target or the specific signal induction pathway engaged during activation. Primary CD4 cells were FACS-sorted into the major phenotypic subsets representative of memory (CD45RO) and naive (CD45RA) cells. Levels of virus replication were compared between infection with wild-type NL4-3 virus and an isogenic mutant containing a deletion in nef regulatory gene. PHA mitogen stimulation was compared with anti-CD3, with and without anti-CD28 costimulation, for induction of cell proliferation and virus replication. In both infected and uninfected cells, the RA cell subset exhibited significantly greater response to CD3/CD28 stimulation than did the RO cell subset. In contrast, the majority of virus replication occurred consistently in the RO cell subset. Deletion of HIV nef function caused a severe reduction in viral replication, especially in the RA naive cell subset after CD3 induction. PCR analysis of viral DNA formation, during infection of quiescent cells, demonstrated that the observed differences in HIV replication capacity between RO and RA cell subsets were not due to inherent differences in cell susceptibility to infection. Our results indicate that HIV replication is enhanced selectively in CD45RO memory phenotype cells through the probable contribution of specialized cellular factors which are produced during CD3-initiated signal transduction.

Authors

C A Spina, H E Prince, D D Richman

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Marked differences in quantity of infectious human immunodeficiency virus type 1 detected in persons with controlled plasma viremia by a simple enhanced culture method
CL Tremblay, F Giguel, DP Merrill, JT Wong, E Rosenberg, S Kalams, BD Walker, RT D'Aquila, MS Hirsch 		Journal of clinical microbiology 2000
Therapeutic targeting of human immunodeficiency virus type-1 latency: current clinical realities and future scientific possibilities
ST Butera 		Antiviral Research 2000
Good or evil: CD26 and HIV infection
T Ohtsuki, H Tsuda, C Morimoto 		Journal of Dermatological Science 2000
The effects of interleukin-2 therapy on the viral reservoir in HIV+ patients
S Zanussi, P Depaoli 		Biomedecine & Pharmacotherapy 2000
Persistence of episomal HIV-1 infection intermediates in patients on highly active anti-retroviral therapy
ME Sharkey, I Teo, T Greenough, N Sharova, K Luzuriaga, JL Sullivan, RP Bucy, LG Kostrikis, A Haase, C Veryard, RE Davaro, SH Cheeseman, JS Daly, C Bova, RT Ellison, B Mady, KK Lai, G Moyle, M Nelson, B Gazzard, S Shaunak, M Stevenson 		Nature Medicine 2000
Correlation of virus load and soluble L-selectin, a marker of immune activation, in pediatric HIV-1 infection:
AP Kourtis, SR Nesheim, D Thea, C Ibegbu, AJ Nahmias, FK Lee 		AIDS 2000
Enhanced levels of functional HIV-1 co-receptors on human mucosal T cells demonstrated using intestinal biopsy tissue:
PA Anton, J Elliott, MA Poles, IM McGowan, J Matud, LE Hultin, K Grovit-Ferbas, CR Mackay, IS Chen, JV Giorgi 		AIDS 2000
Primary HIV-1 infection of human CD4+ T cells passaged into SCID mice leads to selection of chronically infected cells through a massive Fas-mediated autocrine suicide of uninfected cells
S Parlato, SM Santini, C Lapenta, M Spada, M Logozzi, P Rizza, E Proietti, F Belardelli, S Fais 		Cell Death and Differentiation 2000
Immunological memory and acquired immunodeficiency syndrome pathogenesis
AJ McMichael, PC Doherty, A Kaur, M Rosenzweig, RP Johnson 		Philosophical Transactions of The Royal Society B Biological Sciences 2000
Linkage of the CCR5Δ32 Mutation with a Functional Polymorphism of CD45RA
HX Liao, DC Montefiori, DD Patel, DM Lee, WK Scott, M Pericak-Vance, BF Haynes 		Journal of immunology (Baltimore, Md. : 1950) 2000
Highly efficient gene transfer in naive human T cells with a murine leukemia virus-based vector
V Dardalhon, S Jaleco, C Rebouissou, C Ferrand, N Skander, L Swainson, P Tiberghien, H Spits, N Noraz, N Taylor 		Blood 2000
Infection of CD4 + Memory T Cells by HIV-1 Requires Expression of Phosphodiesterase 4
Y Sun, L Li, F Lau, JA Beavo, EA Clark 		Journal of immunology (Baltimore, Md. : 1950) 2000
Dynamics of CCR5 Expression by CD4 + T Cells in Lymphoid Tissues during Simian Immunodeficiency Virus Infection
RS Veazey, KG Mansfield, IC Tham, AC Carville, DE Shvetz, AE Forand, AA Lackner 		Journal of virology 2000
Identifying the Target Cell in Primary Simian Immunodeficiency Virus (SIV) Infection: Highly Activated Memory CD4 + T Cells Are Rapidly Eliminated in Early SIV Infection In Vivo
RS Veazey, IC Tham, KG Mansfield, MA DeMaria, AE Forand, DE Shvetz, LV Chalifoux, PK Sehgal, AA Lackner 		Journal of virology 2000
Inhibition of CD3/CD28-Mediated Activation of the MEK/ERK Signaling Pathway Represses Replication of X4 but Not R5 Human Immunodeficiency Virus Type 1 in Peripheral Blood CD4 + T Lymphocytes
W Popik, PM Pitha 		Journal of virology 2000
Effect of Long-Term Infection with nef-Defective Attenuated HIV Type 1 on CD4+ and CD8+ T Lymphocytes: Increased CD45RO+ CD4+ T Lymphocytes and Limited Activation of CD8+ T Lymphocytes
JJ Zaunders, AF Geczy, WB Dyer, LB McIntyre, MA Cooley, LJ Ashton, CH Raynes-Greenow, J Learmont, DA Cooper, JS Sullivan 		AIDS Research and Human Retroviruses 1999
Dynamics of Provirus Load and Lymphocyte Subsets after Interleukin 2 Treatment in HIV-Infected Patients
S Zanussi, C Simonelli, MT Bortolin, M D'Andrea, M Comar, U Tirelli, M Giacca, PD Paoli 		AIDS Research and Human Retroviruses 1999
Immunological changes in peripheral blood and in lymphoid tissue after treatment of HIV-infected subjects with highly active anti-retroviral therapy (HAART) or HAART + IL-2
S Zanussi, C Simonelli, MT Bortolin, M D'Andrea, C Crepaldi, E Vaccher, G Nasti, D Politi, L Barzan, U Tirelli, PD Paoli 		Clinical & Experimental Immunology 1999
The mode and duration of anti-CD28 costimulation determine resistance to infection by macrophage-tropic strains of human immunodeficiency virus type 1 in vitro
JR Creson, AA Lin, Q Li, DF Broad, MR Roberts, SJ Anderson 		Journal of virology 1999
Human immunodeficiency virus type 1 strains R5 and X4 induce different pathogenic effects in hu-PBL-SCID mice, depending on the state of activation/differentiation of human target cells at the time of primary infection
S Fais, C Lapenta, SM Santini, M Spada, S Parlato, M Logozzi, P Rizza, F Belardelli 		Journal of virology 1999
Quantification of CD4, CCR5, and CXCR4 levels on lymphocyte subsets, dendritic cells, and differentially conditioned monocyte-derived macrophages
B Lee, M Sharron, LJ Montaner, D Weissman, RW Doms 		Proceedings of the National Academy of Sciences 1999
Viral dynamics of acute HIV-1 infection
SJ Little, AR McLean, CA Spina, DD Richman, DV Havlir 		Journal of Experimental Medicine 1999
Current concepts in human immunodeficiency virus infection and AIDS
SA Schwartz, MP Nair 		Clinical and diagnostic laboratory immunology 1999
Altered Expression of CD4, CD54, CD62L, and CCR5 in Primary Lymphocytes Productively Infected with the Human Immunodeficiency Virus
G Marodon, NR Landau, DN Posnett 		AIDS Research and Human Retroviruses 1999
Viral Dynamics of Acute HIV-1 Infection
SJ Little, AR McLean, CA Spina, DD Richman, DV Havlir 		Journal of Experimental Medicine 1999
Deficient Cellular Immunity--Finding and Fixing the Defects
PD Greenberg, SR Riddell 		Science 1999
Consistent Viral Evolutionary Changes Associated with the Progression of Human Immunodeficiency Virus Type 1 Infection
R Shankarappa, JB Margolick, SJ Gange, AG Rodrigo, D Upchurch, H Farzadegan, P Gupta, CR Rinaldo, GH Learn, , XL Huang, JI Mullins 		Journal of virology 1999
Both Memory and CD45RA + /CD62L + Naive CD4 + T Cells Are Infected in Human Immunodeficiency Virus Type 1-Infected Individuals
MA Ostrowski, TW Chun, SJ Justement, I Motola, MA Spinelli, J Adelsberger, LA Ehler, SB Mizell, CW Hallahan, AS Fauci 		Journal of virology 1999
Highly active antiretroviral therapy during early HIV infection reverses T-cell activation and maturation abnormalities
LR Bisset, RW Cone, W Huber, M Battegay, PL Vernazza, R Weber, PJ Grob, M Opravil 		AIDS 1998
Getting to the HAART of T cell dynamics
M Roederer 		Nature Medicine 1998
Diverse host responses and outcomes following simian immunodeficiency virus SIVmac239 infection in sooty mangabeys and rhesus macaques
A Kaur, RM Grant, RE Means, H McClure, M Feinberg, RP Johnson 		Journal of virology 1998
Multiple modes of cellular activation and virus transmission in HIV infection: a role for chronically and latently infected cells in sustaining viral replication
Z Grossman, MB Feinberg, WE Paul 		Proceedings of the National Academy of Sciences 1998
Productive infection of neonatal CD8+ T lymphocytes by HIV-1
LP Yang, JL Riley, RG Carroll, CH June, J Hoxie, BK Patterson, Y Ohshima, RJ Hodes, G Delespesse 		Journal of Experimental Medicine 1998
Productive Infection of Neonatal CD8+ T Lymphocytes by HIV-1
LP Yang, JL Riley, RG Carroll, CH June, J Hoxie, BK Patterson, Y Ohshima, RJ Hodes, G Delespesse 		Journal of Experimental Medicine 1998
Multiple modes of cellular activation and virus transmission in HIV infection: A role for chronically and latently infected cells in sustaining viral replication
Z Grossman, MB Feinberg, WE Paul 		Proceedings of the National Academy of Sciences 1998
Human Lymphoblastoid CD4+ T Cells Become Permissive to Macrophage-Tropic Strains of Human Immunodeficiency Virus Type 1 after Passage into Severe Combined Immunodeficient Mice through In Vivo Upregulation of CCR5: In Vivo Dynamics of CD4+ T-Cell Differentiation in Pathogenesis of AIDS
C Lapenta, S Parlato, M Spada, SM Santini, P Rizza, M Logozzi, E Proietti, F Belardelli, S Fais 		Journal of virology 1998
Naı̈ve and Memory CD4 T Cells Differ in Their Susceptibilities to Human Immunodeficiency Virus Type 1 Infection following CD28 Costimulation: Implications for Transmission and Pathogenesis
JL Riley, BL Levine, N Craighead, T Francomano, D Kim, RG Carroll, CH June 		Journal of virology 1998
Progression to the G 1 b Phase of the Cell Cycle Is Required for Completion of Human Immunodeficiency Virus Type 1 Reverse Transcription in T Cells
YD Korin, JA Zack 		Journal of virology 1998
Recovery of Replication-Competent HIV Despite Prolonged Suppression of Plasma Viremia
JK Wong, M Hezareh, HF Günthard, DV Havlir, CC Ignacio, CA Spina, DD Richman 		Science 1997
Progress in Nucleic Acid Research and Molecular Biology
FS Collins, SM Weissman 		Progress in nucleic acid research and molecular biology 1984

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