Abstract
Human immunodeficiency virus type 1 (HIV-1) viral DNA synthesis in quiescent and activated peripheral blood lymphocytes (PBLs) was studied. Incomplete viral DNA (previously demonstrated to be associated with HIV-1 virions) is carried by HIV-1 virions into quiescent and activated PBLs, contributing to the formation of an early viral DNA pool in these cells. The viral DNA is subsequently completed but only extremely slowly and inefficiently in quiescent PBLs compared to that in stimulated PBLs. We find that this correlates with significantly lower levels of dNTP substrates in quiescent compared to activated PBLs. At these low dNTP concentrations, HIV-1 reverse transcriptase acts in a partially distributive manner. Increasing dNTP concentrations from the levels of quiescent PBLs to the levels of activated PBLs increases the processive action of reverse transcriptase, which in turn stimulates rapid and efficient formation of full-length DNA. Furthermore, hydroxyurea treatment of stimulated PBLs decreases the dNTP levels and the DNA synthesis rate to levels comparable to quiescent PBLs. Our data therefore indicate that low levels of dNTP may explain why HIV-1 DNA is synthesized slowly and inefficiently in quiescent PBLs and suggest that pharmacologic induction of low dNTP levels represents a therapeutic approach for inhibition of HIV-1 replication.
MeSH Terms
Adult
DNA Replication/drug effects
DNA, Viral/biosynthesis,drug effects
Deoxyribonucleotides/blood
HIV Reverse Transcriptase
HIV-1/drug effects,genetics,physiology
Humans
Hydroxyurea/pharmacology
In Vitro Techniques
Lymphocyte Activation
Lymphocytes/drug effects,metabolism,microbiology
RNA-Directed DNA Polymerase/metabolism
Virus Replication/drug effects
Chemicals
DNA, Viral
Deoxyribonucleotides
HIV Reverse Transcriptase
RNA-Directed DNA Polymerase
Hydroxyurea
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Gao W Y
Laboratory of Medicinal Chemistry, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892.
Cara A
Gallo R C
Lori F
References (15)
15 references, click to expand
-
Thymidine kinase, deoxycytidine kinase and deoxycytidylate deaminase activities in phytohaemagglutinin stimulated human lymphocytes.
Exp Cell Res. 1971 Oct;68(2):283-90
PMID: 5124474
-
Mechanism and fidelity of HIV reverse transcriptase.
J Biol Chem. 1992 Dec 25;267(36):25988-97
PMID: 1281479
-
Detection, isolation, and continuous production of cytopathic retroviruses (HTLV-III) from patients with AIDS and pre-AIDS.
Science. 1984 May 4;224(4648):497-500
PMID: 6200935
-
Endoproteolytic cleavage of gp160 is required for the activation of human immunodeficiency virus.
Cell. 1988 Apr 8;53(1):55-67
PMID: 2450679
-
Human immunodeficiency virus 1 reverse transcriptase. Template binding, processivity, strand displacement synthesis, and template switching.
J Biol Chem. 1989 Mar 15;264(8):4669-78
PMID: 2466838
-
Enzymatic assay for deoxyribonucleoside triphosphates using synthetic oligonucleotides as template primers.
Anal Biochem. 1989 Aug 1;180(2):222-6
PMID: 2554751
-
HIV-1 replication is controlled at the level of T cell activation and proviral integration.
EMBO J. 1990 May;9(5):1551-60
PMID: 2184033
-
HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure.
Cell. 1990 Apr 20;61(2):213-22
PMID: 2331748
-
Analysis of mutagenesis induced by a thermolabile T4 phage deoxycytidylate hydroxymethylase suggests localized deoxyribonucleotide pool imbalance.
Mol Gen Genet. 1991 Apr;226(1-2):257-64
PMID: 2034218
-
Quiescent T lymphocytes as an inducible virus reservoir in HIV-1 infection.
Science. 1991 Oct 18;254(5030):423-7
PMID: 1925601
-
Incompletely reverse-transcribed human immunodeficiency virus type 1 genomes in quiescent cells can function as intermediates in the retroviral life cycle.
J Virol. 1992 Mar;66(3):1717-25
PMID: 1371173
-
Partial reverse transcripts in virions from human immunodeficiency and murine leukemia viruses.
J Virol. 1992 Aug;66(8):4893-900
PMID: 1378513
-
Viral DNA carried by human immunodeficiency virus type 1 virions.
J Virol. 1992 Aug;66(8):5067-74
PMID: 1378514
-
An overview of the clinical experience with hydroxyurea.
Semin Oncol. 1992 Jun;19(3 Suppl 9):11-9
PMID: 1641651
-
DNA polymerases in prokaryotes and eukaryotes: mode of action and biological implications.
Experientia. 1983 Jan 15;39(1):1-25
PMID: 6297955