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Journal of Virology, July 2000, p. 6227-6229, Vol. 74, No. 13
0022-538X/00/$04.00+0
Respiratory Syncytial Virus G and/or SH
Glycoproteins Modify CC and CXC Chemokine mRNA Expression in the
BALB/c Mouse
Ralph A.
Tripp,*
Les
Jones, and
Larry J.
Anderson
Division of Viral and Rickettsial Diseases,
National Center of Infectious Diseases, Centers for Disease Control
and Prevention, Atlanta, Georgia 30333
Received 18 January 2000/Accepted 11 April 2000
 |
ABSTRACT |
Chemokine mRNA expression by pulmonary leukocytes following
infection of BALB/c mice with two strains of respiratory syncytial virus (RSV) and one strain of parainfluenza virus type 3 (PIV-3) was
determined. The results suggest that RSV G and/or SH proteins inhibit
early MIP-1
, MIP-1
, MIP-2, MCP-1, and IP-10 mRNA expression. TCA-3 mRNA expression was found to be increased during PIV-3 infection.
 |
TEXT |
Respiratory syncytial virus (RSV) is
a major cause of lower respiratory tract disease in infants and young
children and is associated with bronchiolitis (3, 4).
Bronchiolitis is manifested by obstruction of the airways and is
associated with the inflammatory response to infection (7-9, 17,
31). The viral and host factors contributing to the inflammatory
response are not well understood but likely involve the production of
cytokines and chemokines by immune and respiratory epithelial cells.
For example, in mice, the enhanced disease that occurs following
formalin-inactivated RSV vaccination is associated with a Th2 cytokine
response (6, 10, 11, 30), while live RSV infection does not
induce enhanced disease and is associated with a Th1 cytokine response
(15, 27, 29). The link between cytokine production and
enhanced disease is supported by abrogation of enhanced disease when
interleukin 4 (IL-4) and IL-10 are neutralized with antibodies
(6). Recent studies suggest that the RSV G glycoprotein is
an important determinant of the cytokine response associated with
enhanced disease (12, 18, 19). For example, G and/or SH
glycoproteins alter Th1 cytokine, particularly gamma interferon
(IFN-
), expression as well as decrease polymorphonuclear leukocyte
(PMN) and NK cell trafficking to the lung (27, 29). It has
been proposed that lack of IFN-
and CD8+ T-cell
regulation of the CD4+ T-cell response to RSV infection may
contribute to enhanced disease (14, 26).
Antigen nonspecific granular cells that produce chemokines govern the
earliest stages of the inflammatory response. Chemokines promote an
influx of immune cells to the site of infection, which in turn express
chemokines that help refine the inflammatory response. Several groups
have shown in vitro that epithelial cells respond to RSV infection by
expressing IL-8, RANTES, MIP-1
, and MIP-1
(13, 22),
suggesting that these chemokines are important during RSV infection;
however, the characteristics of the chemokine response to in vivo RSV
infection have not been well studied.
In this study, we examined the kinetics of chemokine mRNA expression by
pulmonary leukocytes following primary infection of 4- to 6-week-old
female BALB/c mice (Harlan Sprague Dawley Laboratories, Indianapolis,
Ind.) with two strains of RSV, one which has the G and SH genes (B1)
and one which lacks them (CP52), or with the JS strain of parainfluenza
virus type 3 (PIV-3), all of which were propagated as described
previously (28, 29). Mice were intranasally infected with
104 PFU of B1, CP52, or PIV-3 diluted in phosphate-buffered
saline (PBS) or with uninfected Vero cell-free lysate (VCL) (GIBCO,
Grand Island, N.Y.). At various times postinfection (p.i.);
bronchoalveolar lavage (BAL) cells from 4 to 6 mice/time point were
collected by washing the lungs three times with 1 ml of PBS (GIBCO)
containing 1% bovine serum albumin (Sigma, St. Louis, Mo.). Total cell
numbers in the BAL cells of B1-infected mice ranged from 3.4 × 105 to 9 × 105 cells/ml, in CP52-infected
mice they ranged from 5 × 105 to 8.5 × 105 cells/ml and in PIV-3-infected mice they ranged from
5 × 105 to 12 × 105 cells/ml. RNA
isolation and multiprobe RNase protection analysis were performed
according to the instructions of the probe manufacturer (PharMingen,
San Diego, Calif.). BAL cells were used for RNA extraction. Total RNA
was extracted using RNA STAT-50 LS (TEL-TEST Inc., Friendswood, Tex.)
as described by the manufacturer. Chemokine mRNA was detected by RNase
protection analysis using the RiboQuant Multi-Probe RNase Protection
Assay System (PharMingen). 32P-labeled antisense RNA probes
specific for eight chemokine mRNA sequences and two housekeeping mRNA
sequences were used to detect CC chemokines (RANTES, Eotaxin, MIP-1
,
MIP-1
, MIP-2, MCP-1 and TCA-3), CXC chemokine (IP-10), and the L32
and GAPDH housekeeping genes.
The mean results from experiments (n
3) examining
chemokine mRNA expression at 0, 8, 18, 36, 72, 144, and 240 h p.i.
with B1, CP52, and PIV-3 are shown in Fig.
1 and 2.
Overall, there was low constitutive expression of the macrophage
inflammatory proteins MIP-1
, MIP-1
, and MIP-2, as well as of
MCP-1 and IP-10, followed by a marked early chemokine response to
infection and a return to constitutive levels, followed by a small,
second increase in chemokine expression later in the infection. At
8 h p.i., MIP, IP-10, and MCP-1 expression peaked for the two RSV
strains, whereas at 18 h p.i. MIP and TCA-3 expression peaked for
PIV-3 (Fig. 1 and 2). By 36 h p.i., except for that of RANTES,
chemokine expression had returned to near constitutive levels (Fig. 1).
The magnitude of RANTES mRNA expression varied following virus
infection or VCL treatment, and no virus-specific increases were
detected (Fig. 1). Overall, treatment of mice with uninfected VCL
induced a chemokine expression pattern similar to that for B1
infection, but having a much lower magnitude.

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FIG. 1.
Mean band density ratios for RANTES, MIP-1 , MIP-1 ,
and MIP-2 mRNA expression. mRNA was isolated from BAL cells collected
from 4 to 6 mice/time point during three or more separate experiments
with CP52-, B1-, or PIV-3-infected or naïve mice. Chemokine
mRNA expression was quantified using a PhosphorImager to determine band
densities. The band density ratio was determined by dividing the mean
band density of the L32 housekeeping gene by the mean band density of
the chemokine. Error bars, standard errors of the means.
|
|

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FIG. 2.
Mean band density ratios for IP-10, MCP-1, and TCA-3
mRNA expression. mRNA was isolated from BAL cells collected from 4 to 6 mice/time point during three or more separate experiments with CP52-,
B1-, or PIV-3-infected or naïve mice. Chemokine mRNA expression
was quantified using a PhosphorImager to determine band densities. The
band density ratio was determined by dividing the mean band density of
the L32 housekeeping gene by the mean band density of the chemokine.
Error bars, standard errors of the means.
|
|
There was consistently higher expression of MIP, MCP-1, and IP-10 mRNAs
following CP52 infection than there was following B1 infection (Fig. 1
and 2). To control for by-products in the virus inoculum that might
affect chemokine induction, mice were infected with sucrose
gradient-purified (5) B1 or CP52 virus (data not shown).
Both purified viruses induced MIP, RANTES, IP-10, and MCP-1 mRNA
expression between 8 h and 18 h p.i.; however, CP52 induced
higher chemokine expression than B1 (e.g., 34% greater for MIP-1
,
37% greater for MIP-1
, 22% greater for MIP-2, and 67% greater for
IP-10). TCA-3 mRNA was also induced by purified CP52 but was not
observed following infection with CP52-infected VCL; however, the
magnitude of expression was significantly lower than that observed
following PIV-3 infection. Since the titers of B1 and CP52 in the lung
are comparable at day 3 p.i. (29), the differences in
MIP, MCP-1, and IP-10 expression are likely due to the absence of G
and/or SH proteins.
As observed previously (29), the absence of the G and SH
genes (as in strain CP52) consistently resulted in more PMN and NK
cells in the lung of mice than did the presence of the G and SH genes
(as in strain B1), whereas PIV-3-infected mice had intermediate levels
of cells positive for these surface markers (data not shown).
The present study suggests that G and/or SH gene expression reduces
MIP, MCP-1, and IP-10 mRNA expression. Chemokines interact with
receptors expressed by Th1 cells (CCR5, CXCR3, and CXCR5) (23; P. Loetscher, M. Uguccioni, L. Bordoli, M. Baggiolini, B. Moser, C. Chizzolini, and J. M. Dayer, Letter,
Nature 391:344-345, 1998) and with those preferentially
expressed by Th2 cells (CCR3, CCR4, and CCR8) (16, 20, 21, 25,
32). MIPs interact with CCR1 and CCR5, MCP-1 interacts with the
CCR2 receptor, and IP-10 interacts with the CXCR3 receptor on Th1 cells
(1, 2, 24, 33). In earlier studies we showed decreased Th1
cytokine (IFN-
) expression after infection with B1 compared to after
infection with CB52, which lacks these genes (29). The
decreased MIP, MCP-1, and IP-10 expression associated with G and/or SH
glycoproteins likely impairs the Th1 response; thus, these chemokines
may be important in RSV immunity or disease pathogenesis.
 |
FOOTNOTES |
*
Corresponding author. Mailing address: Centers for
Disease Control and Prevention, 1600 Clifton Rd., MS G09, Atlanta, GA
30333. Phone: (404) 639-3427. Fax: (404) 639-1307. E-mail:
rgt3{at}cdc.gov.
 |
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Journal of Virology, July 2000, p. 6227-6229, Vol. 74, No. 13
0022-538X/00/$04.00+0
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