Journal of General Virology (1995), 76, 1675-1686. Printed in GreatBritain 1675
Stepwise analysis of reverse transcription in a cell-to-cell human
immunodeficiency virus infection model: kinetics and implications
Litsa Karageorgos, 1 Peng Li 1. and Christopher J. Burrell 1,2
1National Centre for HIV Virology Research, Institute of Medical and Veterinary Science, Frome Road,
Adelaide 5000, South Australia and 2Department of Microbiology and Immunology, University of Adelaide,
North Terrace, Adelaide 5000, South Australia, Australia
We have investigated the kinetics of human immuno-
deficiency virus (HIV) reverse transcription in infected T
cells, using a synchronized, one-step, cell-to-cell in-
fection model and quantitative PCR assays for the
different DNA intermediate structures that are found
sequentially during reverse transcription. Different
efficiencies that might arise from the use of different
primers and other PCR conditions were normalized by
conversion of each PCR product signal to copy numbers
by comparing with standards. After an initial lag period,
the minus-strand strong-stop viral DNA was detected
first. This was followed by the post-transfer newly
extended minus-strand viral DNA and then by the plus-
strand strong-stop DNA and fully extended minus-
strand DNA. Kinetic data indicated that, once reverse
transcription was initiated, the HIV reverse transcriptase
synthesized minus-strand DNA at a rate of
150-180 bases/min, and that the first template transfer
and the initiation of the plus-strand DNA synthesis
imposed specific time delays. In contrast, minus-strand
viral DNA synthesized after the second template transfer
appeared at a time point very close to the time of the
appearance of the last piece of DNA synthesized just
before the second template switch, suggesting that the
second switch occurred very rapidly. Taken together,
our results define more accurately than was previously
possible the rates of several of the steps in HIV reverse
transcription in infected T cell lines and indicate
different mechanisms for the two distinct template
switches during retrovirus reverse transcription.
Introduction
One of the key early events in retrovirus replication is the
reverse transcription of the single-stranded viral RNA
into double-stranded DNA, which is catalysed by the
virus-encoded reverse transcriptase. This process can be
divided into several discrete steps: (i) synthesis of a short
stretch of DNA ('the minus-strand strong-stop DNA')
from the primer binding site (PBS) near the 5' end of one
genomic viral RNA molecule, using a tRNA as primer;
(ii) transfer of the minus-strand strong-stop DNA from
the 5' end of the viral RNA to the 3' end of the same, or
a second molecule of viral RNA; (iii) continued synthesis
of the minus-strand DNA, accompanied by degradation
of the RNA template by RNase H activity of the viral
reverse transcriptase [this process leaves a polypurine
tract (PPT) at specific sites in the 3' end of the viral RNA
to serve as the primer for the synthesis of the plus-strand
viral DNA using the minus-strand DNA as template];
* Author for correspondence.Fax + 61 8 228 7538. e-mail jmcinnes
@microb.adelaide.edu.au
(iv) this newly synthesized short stretch of plus-strand
DNA ('plus-strand strong-stop DNA') is then trans-
ferred from the 5' end to the 3' end of newly made,
partially completed minus-strand DNA; (v) after the
second template transfer, the remainder of the plus-
strand DNA as well as the 3' end of the minus-strand
DNA is synthesized, to yield a linear double-stranded
DNA with all sequences in the viral RNA plus duplicated
U3 and U5 sequences present in the long terminal
repeats (for reviews see Varmus & Brown, 1989; Coffin,
1990; Li et al., 1993; Jones et al., 1994).
Although these basic steps have been known for some
time from studies of type C retroviruses [some aspects of
these have recently been confirmed for the human
immunodeficiency virus (HIV)] a detailed kinetic study
to delineate the multiple events in this process has been
lacking and the current data are highly controversial.
Studies on type C retroviruses showed that the first
complete linear DNA molecules could be detected
approximately 4 h after infection (Varmus & Swanstrom,
1984, 1985; Varmus & Brown, 1989). For HIV, our
laboratory and others using one-step virus growth
conditions showed by infection with either cell-free virus
0001-3007 © 1995 SGM