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Previous Article | Next Article 
Journal of Virology, September 2000, p. 8757-8761, Vol. 74, No. 18
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Is the 135S Poliovirus Particle an Intermediate during Cell
Entry?
Yan
Huang,1
James
M.
Hogle,2 and
Marie
Chow1,*
Department of Microbiology and Immunology, University of
Arkansas for Medical Sciences, Little Rock, Arkansas
72205,1 and Department of Biological
Chemistry and Molecular Pharmacology, Harvard Medical School, Boston,
Massachusetts 021152
Received 18 January 2000/Accepted 20 June 2000
 |
ABSTRACT |
Poliovirus binding to its receptor (PVR) on the cell surface
induces a conformational transition which generates an altered particle
with a sedimentation value of 135S versus the 160S of the native
virion. A number of lines of evidence suggest that the 135S particle is
a cell entry intermediate. However, the low infection efficiencies of
the 135S particle and the absence of detectable 135S particles during
infection at 26°C by the cold-adapted mutants argue against a role
for the 135S particle during the cell entry process. We show here that
binding of 135S-antibody complexes to the Fc receptor (CDw32) increases
the infectivity of these particles by 2 to 3 orders of magnitude. Thus,
the low efficiency of infection by 135S particles is due in part to the low binding affinity of these particles. In addition, we show that
there is an additional stage in the entry process that is associated
with RNA release. This stage occurs after formation of the 135S
particle, is rate limiting during infection at 37°C, but not at
26°C, and is PVR independent. The data also demonstrate that during
infection at 26°C, the rate-limiting step is the PVR-mediated conversion of wild-type 160S particles to 135S particles. This suggests
that during infection at 26°C by the cold-adapted viruses, 135S
particles are formed, but they fail to accumulate to detectable levels
because the subsequent post-135S particle events occur at a
significantly faster rate than the initial conversion of 160S to 135S
particles. These data support a model in which the 135S particle is an
intermediate during poliovirus entry.
| |
TEXT |
Poliovirus is a picornavirus whose
7,400-nucleotide positive-sense RNA genome is encapsidated in an
icosahedral protein shell formed by 60 copies of four capsid proteins
(VP1, VP2, VP3, and VP4). Virus entry into cells is initiated by
binding to the poliovirus receptor (PVR) on the cell surface. PVR
binding induces conformational rearrangements within the virus particle
which leads to the formation of an altered particle sedimenting at 135S
(versus the 160S sedimentation value of the native particle) and the
coordinate relocation of capsid protein VP4 and VP1 N termini from the
interior of the virion to the outer surface of the particle
(9).
A number of lines of evidence suggest that the 135S particles (also
known as "A particles") are intermediates in the cell entry
pathway. Thus, the 135S particles are able to bind to liposomes and
insert into lipid bilayers to form ion channels (9, 17). In
addition, it has been shown that 135S particles infect cells in a
receptor-independent fashion (6) and that drugs (for
example, Win 51711) that inhibit the conversion of 160S particles to
the 135S form by binding to the poliovirus capsid prevent infection (3, 8, 12, 13, 20). However, two observations raise serious
questions in some people's minds about the role of the 135S particle
as a true intermediate in entry. First, although the 135S particle can
infect cells in the absence of PVR expression, infection is highly
inefficient (6). Thus, it has been proposed that the
infectivity of the 135S particle resulted from the presence of small
amounts of the infectious RNA genome that are randomly released due to
breakage or degradation of the 135S particles. Second, the 135S
particles are not detected during infection at 26°C with virus
mutants which have been selected to grow at this lower temperature
(7).
Here, we present data to counter these arguments. Specifically, we show
that efficiency can be significantly improved when an alternative
mechanism is provided for high-affinity binding of 135S particles to
the cell surface. Thus, the low efficiency of infection of the 135S
particle is due in part to the low binding affinity of this particle to
cells. Furthermore, we show that there exists an additional stage in
the entry process, which occurs after formation of the 135S particle,
which is rate limiting at 37°C. Detectable levels of 135S particles
accumulate during infection at 37°C because the rate of production of
135S is faster than this rate-limiting downstream stage. Data also
demonstrate that genome entry by wild-type virus at 26°C is
significantly more rapid when initiated with the wild-type 135S
particles than with the 160S particles, indicating that it is the
PVR-mediated conversion of 160S to 135S particles and not the
downstream stage that is rate limiting at 26°C. Thus, an alternative
interpretation of the failure to detect the 135S particles during
infection at 26°C is that at the lower temperature, the 135S
particles do not accumulate to detectable concentrations because
subsequent downstream (post-135S particle) events during virus entry
occur at a significantly faster rate than the initial conversion of
160S to 135S particles.
Antibody enhancement of 135S particle infection.
The 135S
particles bind to cells via a receptor-independent, nonsaturable,
low-affinity interaction that may simply reflect 135S particles binding
to cell membranes (6). This suggested that the efficiency of
135S particle infections might be greater if these particles could bind
to cells at higher affinity and that this higher-affinity interaction
could potentially be achieved by binding 135S particle-antibody
complexes to Fc receptors. Previous studies had shown that
foot-and-mouth disease virus-antibody complexes could mediate
infection in normally nonsusceptible cells by binding to the Fc
receptor (11). In that study, however, parallel experiments with poliovirus-antibody complexes were not infectious. Similar studies
with the C3 monoclonal antibody with poliovirus 160S and 135S particles
also failed to show antibody-mediated infection with Fc receptor (S. Curry, unpublished observations). More recently, Arita et al. have
shown with different antibodies that binding of 160S-antibody complexes
to Fc receptors can inefficiently compensate for PVR binding to
initiate infection (1).
We have investigated a specific monoclonal antibody (MAb6) that binds
to neutralizing antigenic site 2 of 160S particles and also binds to
135S particles with slightly lower affinities (9). The
135S-MAb6 complexes were used to infect mouse L cells
(L/CD32+), a cell line which stably expresses Fc gamma
receptors (CDw32+) (2). The resultant titers
were measured over the course of infection (Fig.
1A). Viral titers increased over time,
indicating that the titers resulted from active replication rather than
titers from input virus particles. The infectivities of the
135S-antibody complexes were 2 to 3 orders of magnitude higher than
that of 135S particles alone and were dependent on antibody
concentrations. No enhancement was observed when 135S was incubated
with a nonpolio-virus-specific antibody, OKT3 (Fig. 1A). The increased
efficiency was dependent on Fc-receptor binding of the 135S-antibody
complexes, because antibody enhancement of 135S infection did not occur
in CDw32
L cells or in Rat-2 cells (data not shown). In
addition, coincubation or preincubation of the CDw32+ L
cells with the nonspecific immunoglobulin G (IgG) inhibited binding of
the 135S-MAb6 complex to Fc receptor and prevented the
antibody-mediated increases in titers (Fig. 1B). At very high dilutions
(105), MAb6 also mediated infection of 160S particles on
these cells. However, at the antibody concentrations used for the 135S
experiments, MAb6 neutralizes the infectivity of 160S particles rather
than enhances it (Fig. 1C). This provides further evidence that the infectivity observed is not due to trace amounts of unconverted 160S
particles.
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FIG. 1.
Antibody enhancement of infections by 135S particles.
(A) Poliovirus 135S particles were generated in vitro by preincubating
purified 160S virus in 20 mM Tris-HCl (pH 7.5)-2 mM
CaCl2-0.1% Tween 20 at 55°C for 2 min and subsequently
chilling the mixture on ice. The levels of residual 160S particles
present in these samples of 135S particles were shown to be negligible
by the equivalent titers observed when assayed on Rat-2 cells
(PVR) and on CV-1 cells (PVR+). Dilutions of
MAb6 ( ) or of nonspecific IgG (*) ascites fluids were made in PBS
and incubated with the in vitro-generated 135S particles
(108 particles) for 1 h at 0°C. The antibody-virus
complexes were added to L/CD32+ cells (5 × 105) for 1 h at 20°C, the cells were washed with PBS
to remove unbound virus or antibody complexes, and infection at 37°C
was initiated with addition of prewarmed medium (Dulbecco's modified
medium-5% fetal calf serum). Samples were harvested at various hours
p.i. and lysed by freeze-thaw three times, and the resultant virus
titers were measured in triplicate by plaque assay on HeLa cells. The
average titers at 4 and 6 h p.i. are shown. Titers at 0 h
p.i. were below the detectable levels (<50 PFU/ml) for all samples.
(B) L/CD32+ cells were incubated with 135S-MAb6 complexes
(102 dilution of ascites fluid) in the presence of
various concentrations of purified nonspecific IgG (0, 10, or 50 µg)
and washed with PBS, and infection at 37°C was initiated by addition
of prewarmed medium. The resultant titers were measured by plaque
assay. The titer obtained upon infection with 135S particles alone is
indicated by the dotted line. (C) L/CD32+ cells were
incubated with 160S particles in PBS (B) or with 160S-MAb6 complexes
(102 dilution of ascites fluid) (MAb6) and washed with
PBS, and infection at 37°C was initiated by addition of prewarmed
medium. Samples were harvested at various hours p.i. and lysed by
freeze-thaw three times. Virus titers were measured by plaque assay on
HeLa cells. The titers at 0, 4, and 6 h p.i. are shown.
|
|
Although the increased infectivity of the 135S-MAb6 complex is not
equivalent to that of the wild-type 160S particle, the resultant titers
from the 135S-MAb6 infections indicate that the infectivity of the 135S
particle is reduced at most 1 to 2 orders of magnitude from that of the
160S particle and is comparable with that observed with several
previously characterized viable poliovirus mutants (15, 16).
Thus, the low infectivity of the 135S particle is explained in part by
the absence of a high-affinity interaction with the cell surface which
can be partially compensated for by the affinity of the antibody-Fc
receptor interaction. Moreover, the MAb-dependent increase in titers
complements previous observations which showed that the infectivity of
135S particles is dependent on the N-terminal 31 amino acids of VP1 and
is resistant to digestion with RNase (6). These data
reinforce the conclusion that 135S particles are infectious and this
infectivity is not dependent on PVR expression on the cell surface.
NR sensitivity of 135S particle infection.
Previous studies
have demonstrated that the infectivity of poliovirus grown in the
presence of neutral red (NR) is photosensitive (5, 19). This
photosensitivity results from the incorporation of the dye within the
interior of the virion in close proximity to the RNA and subsequent
modification of the RNA genome by the locally high concentrations of
the photoactivated dye after exposure to visible light. During
infection with NR-poliovirus, the period of photosensitivity has been
correlated with the kinetics of RNA release and is thought to be due to
diffusion of this chromogenic dye away from the RNA upon release of the
genome into the cytoplasm. Infection by NR-virus is light sensitive
only at initial stages of infection, and this period of
photosensitivity has been used to characterize viable mutants which are
defective in uncoating (10). It was of interest to determine
whether infection by NR-135S particles was photosensitive and, if so,
to compare the periods of photosensitivity as a measure of RNA release.
If the 135S particle is an intermediate in the entry process, then one
would predict that a similar (perhaps even shorter) period of
photosensitivity would be observed during infection by NR-135S particles.
NR-135S particles were generated in vitro from NR-160S particles. To
determine the optimal time of light irradiation, the NR-135S and
NR-160S particles were exposed to increasing periods of light
irradiation, and the residual viral titers were measured by plaque
assay (10). The decay curves for NR-135S and -160S particles
were very similar. Viral titers for both the 160S and 135S forms of
viral particles dropped 300- to 400-fold within a 5-min period of light
exposure, indicating that the infectivities of 135S and 160S particles
were equivalently sensitive to light (data not shown). The period
during which infection by NR-135S particles was light sensitive was
measured by exposing cell monolayers to light at different times
postinfection (p.i.). This photosensitive period was compared with that
observed for infections with NR-160S particles (Fig.
2A). As observed previously, infection by
NR-160S particles becomes light resistant within 20 to 30 min p.i.
(half-time for acquiring photoresistance for 160S
[T1/2-160S] = 17 min p.i.) (10).
Similarly, infection by NR-135S particles becomes photoresistant within
20 to 25 min (T1/2-135S = 15 min p.i.).
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FIG. 2.
Photosensitivity of infection with NR-135S particles.
(A) [35S]methionine-labeled virus was grown in the
presence of NR (5, 19). NR-135S particles were converted in
vitro from NR-160S particles and diluted to the appropriate titers with
PBS. HeLa cell monolayers were incubated in the dark at 4°C for
1 h with 300 to 400 PFU of NR-135S () or NR-160S ( )
particles. The cells were washed with PBS, and infection was initiated
in the dark with the addition of a Dulbecco's modified medium-5%
fetal calf serum-0.8% agarose overlay. At the indicated times p.i.
the monolayers were exposed to white light for 10 min at 20°C and
then subsequently returned to 37°C for 48 h to allow the plaque
assay to develop. The resistant titers from duplicate infectious center
assays were averaged, and the percentage of light-resistant viral
infections was calculated based on the 100% value representing the
average titers obtained when infections were constantly maintained in
the dark. Representative results for a set of parallel infections with
160S and 135S particles are shown. (B) In vitro-converted NR-135S
particles were incubated in PBS at 26°C ( ) or at 37°C (,
). At various times, aliquots were taken to infect Rat-2 cell
monolayers, the monolayers were exposed to light (, ) or
maintained in the dark (), and then infection was initiated by the
addition of prewarmed medium. Cells were harvested at 6 h, and the
resultant titers were determined by plaque assay.
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|
Photosensitivity is dependent on the concentration of NR present in the
particle. It is possible that the conformational changes associated
with formation of the 135S particle result in a particle with increased
permeability, which leads to diffusion of NR out of the particle. If
this were the case, then the period of photosensitivity observed during
infection for NR-135S particles could represent the kinetics of NR
diffusion out of the particle rather than the kinetics of RNA release
into the cell. To test for this, NR-135S particles were incubated in
phosphate-buffered saline (PBS) at 26 or 37°C. At various times of
incubation, samples were exposed to light and the proportion of viral
titer that was photosensitive was measured (Fig. 2B). The intrinsic
infectivity of the 135S particles remains unchanged over the incubation
period and is reflected by the minimal change in viral titers when the
samples were maintained in the dark. However, when the 135S virus
particle was exposed to light, virus titers significantly decreased at all times examined. These data indicate that the appearance of photoresistant viral titers at 20 to 25 min p.i. is not an artifact of
passive loss of NR, but rather is dependent on downstream events in the
entry pathway which are initiated upon interaction of 135S particles
with cells.
Interestingly, the transition from photosensitivity to photoresistance
began, for infections by either 135S or 160S particles, at
approximately 10 to 15 min p.i. The exact periods of light sensitivity
for infections with 160S and 135S particles varied from experiment to
experiment, with values for T1/2-160S ranging between 16 to 19 min p.i. and T1/2-135S ranging
between 14 and 17 min p.i. The variation in half-times likely reflects
the several different preparations of virus and passages of HeLa cells
used over the course of these studies. Thus, when reviewed over the entire range of experiments, the differences between the
T1/2-160S and T1/2-135S
are of marginal statistical significance. However, when measured for
infections by 135S and 160S particles done in parallel, the period of
photosensitivity (as quantitated by T1/2 values)
was always shorter for 135S particles than for 160S particles. The
steep rise in photoresistant viral titers demonstrates that infections
with either 135S particles or 160S particles are highly synchronous
(Fig. 2A). Moreover, the appearance of photoresistant virus at 10 to 25 min p.i. identifies an additional stage which occurs downstream from
the initial receptor-mediated conformational rearrangements that form
135S particles. The length of this NR-sensitive interval is similar,
irrespective of whether infection is initiated by 160S or 135S
particles. This suggests that the stage (demarcated by NR sensitivity)
is rate limiting during infection at 37°C.
Poliovirus entry during infection at 26°C.
Previous studies
indicated that infection at 26°C by wild-type virus is nonproductive
because of a block in RNA synthesis (7). Consistent with
viral RNA synthesis being inhibited during infections with wild-type
virus, the cold-adapted mutants contain mutations in 2C, a
nonstructural protein involved in viral RNA replication, which enable
these mutants to overcome this block and allow productive replication
at 26°C (7). To look for the presence of an NR-sensitive
stage in virus entry during infection at 26°C with wild-type virus,
it was necessary to separate the events associated with virus entry and
uncoating from the process of RNA transcription and replication. This
is possible if replication of wild-type virus can occur after the
infected cells were initially incubated at 26°C for a period of time
and subsequently shifted to 37°C. To test for this, cells were
initially infected with wild-type virus at 26°C. At various times
p.i. at 26°C, the cells were shifted to 37°C, and the resultant
viral titers were measured. Consistent with the presence of a block in
RNA synthesis, no viral titers were detected when the infections with
wild-type virus were maintained at 26°C over a 16-h period. However,
for up to 6 h at 26°C, if the infections subsequently were
shifted to 37°C, the titers recovered from these temperature shift
infections were 50 to 80% of the titers obtained from infections
occurring completely at 37°C (data not shown). These data indicate
that subsequent poliovirus replication is not significantly compromised
by the initial incubation period at 26°C. Thus, after light exposure to block infection by RNA genomes remaining within the viral particles, RNA genomes released from NR-virus particles during virus entry at
26°C can be detected by the replication of these genomes at 37°C.
Cell monolayers were infected with wild-type NR-135S or -160S particles
at 26°C in the dark. At various times p.i., the monolayers were
exposed to light at room temperature and then returned to 26°C. After
the last time point at 6 h, all samples (including samples which
were maintained in the dark) were shifted to 37°C to allow completion
of the replication cycle, and the resultant viral titers were measured
(Fig. 3). Infections with NR-160S
particles remain highly photosensitive over the 6-h period at 26°C,
indicating that very few particles had uncoated their genomes. In
striking contrast, photoresistant viral titers are detected in NR-135S infections within 1 h p.i. and continue to increase until
infection with these particles becomes largely photoresistant at 4 h p.i. at 26°C. Moreover, there is an interval (between 3 and 4 h p.i.) during the infection at 26°C in which a sharp increase in
photoresistant titers occurs. This indicates that a similar
NR-sensitive stage exists during infection at 26°C and suggests that
release of RNA from 135S particles during infection at 26°C is
relatively synchronous. The half-time for acquiring photoresistance
(T1/2-135S) is approximately 3.5 h. In
contrast, T1/2-160S has not been measurable, but
it is significantly longer than 6 h for 160S at 26°C. This is
consistent with the conversion of 160S to 135S particles at 26°C
being slow and rate limiting in these infections. Thus, the failure to
observe 135S particles during infection at 26°C is expected, because
the 135S particles are being consumed more rapidly than they are being produced.
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FIG. 3.
Photosensitivity of 135S infection at 26°C. NR-160S
() and in vitro-converted NR-135S () particles (300 to 400 PFU)
were bound to HeLa cell monolayers for 1 h at 4°C. In the dark,
cells were washed with PBS at 4°C, and infection was initiated by the
addition of medium prewarmed to 26°C and maintained in a 5%
CO2 incubator at 26°C. At various hours p.i., the
monolayers were exposed to white light for 10 min and returned to the
incubator at 26°C. One set of infected monolayers were maintained
constantly in the dark at 26°C. At 6 h p.i., an agarose overlay
was added to all monolayers, and the cells were shifted to a 5%
CO2 incubator at 37°C. The photoresistant titers were
measured after 48 h p.i. The percentage of light-resistant viral
infections was calculated based on the 100% value representing the
titers obtained for infections maintained in the dark, which were
initiated at 26°C and subsequently shifted to 37°C.
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|
Roles of PVR during poliovirus entry.
The data presented here
counter several arguments that have been raised against a role for 135S
particles during poliovirus entry into cells and are consistent with a
model in which 135S particles are an intermediate of the viral entry
pathway. First, enhancement of 135S particle infection by antibody-Fc
receptor interactions (Fig. 1) demonstrates that the ability to infect cells in a PVR-independent manner is an inherent property of 135S particles. Thus, the infection inefficiencies of 135S particles at
37°C are due in part to the low binding affinity of these particles to the cell. Second, there is at least an additional stage during virus
entry which occurs during infection at 37°C at a significantly later
time after the PVR-mediated 160S-to-135S conformational transition
(Fig. 2). This stage appears to be rate limiting during infection at
37°C, thus allowing accumulation of detectable levels of 135S
particles. In contrast, it appears that at 26°C, the conversion of
160S to 135S particles by PVR is rate limiting. Infection with 135S
particles bypasses the requirement for PVR-mediated conversions at
26°C, and, consequently, genome release during infection with 135S
particles is synchronous and more rapid at this lower temperature (Fig.
3).
If the 135S particle is an intermediate during virus entry, then the
differences observed in infection efficiencies of the 160S versus 135S
particles at 37 and 26°C confirm that PVR serves at least two roles
during virus entry (1, 4, 14). First, PVR provides a
high-affinity binding site that the virus uses to "dock" with the
cell surface. Second, PVR binding induces the 160S-to-135S
conformational transition to occur at physiological temperatures. In
vitro, these conformational rearrangements can also be triggered at
elevated temperatures in the absence of PVR, indicating that this
conformational transition is an energy-requiring event. Indeed, recent
measurements suggest that the energy of activation
(Ea) of this transition is quite large
on the
order of 100 to 140 kcaland that the rate of this transition in the absence of PVR is very slow at 37°C (18). Thus, in
addition to its docking function, PVR interaction alters the energetics of the 160S-135S transition such that it can readily occur under physiological conditions.
Finally, the interval of NR sensitivity defines a temporal window
during which an additional stage in the entry pathway occurs which is
associated with RNA release. This stage also occurs during infection of
Rat-2 cells with 135S particles, indicating that this event is
independent of PVR expression. The steep transition from
photosensitivity to photoresistance suggests that this stage occurs
synchronously during infection. This synchrony suggests that additional
unknown factors may be required to trigger RNA release.
| |
ACKNOWLEDGMENTS |
We are grateful to M. Tosteson for valuable discussions and
critiques. We thank M. Cannon and A. Khanolkar for the gifts of CDw32+ L cells and purified OKT3 IgG.
This work was supported by Public Health Service grants AI22627 and
AI42390 from the National Institute of Allergy and Infectious Diseases.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: University of
Arkansas for Medical Sciences, 4301 W. Markham, Slot 511, Little Rock, AR 72205. Phone: (501) 686-5155. Fax: (501) 686-5362.
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Journal of Virology, September 2000, p. 8757-8761, Vol. 74, No. 18
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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