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Infection and Immunity, February 1999, p. 989-993, Vol. 67, No. 2
0019-9567/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Interleukin-5 Transgenic Mice Show Enhanced
Resistance to Primary Infections with Nippostrongylus
brasiliensis but Not Primary Infections with
Toxocara canis
Lindsay A.
Dent,1,*
Christine M.
Daly,1
Graham
Mayrhofer,1
Trudy
Zimmerman,1
Ann
Hallett,1
Leon P.
Bignold,2
Jenette
Creaney,3 and
Jim C.
Parsons3
Departments of Microbiology and
Immunology1 and
Pathology,2 University of Adelaide,
Adelaide, South Australia, and
Victorian Institute of
Animal Science, Attwood, Victoria,3 Australia
Received 2 June 1998/Returned for modification 24 July
1998/Accepted 29 October 1998
 |
ABSTRACT |
In this study, interleukin-5 (IL-5) transgenic mice with lifelong
eosinophilia were assessed for resistance to primary infections with
two tissue-invading nematodes, Nippostrongylus brasiliensis and Toxocara canis. Relative to nontransgenic littermates,
three lines of IL-5 transgenic mice with varying degrees of
eosinophilia all displayed enhanced resistance to N. brasiliensis. Although the timing of final worm expulsion was
similar in transgenic and nontransgenic hosts, intestinal
worms in transgenic mice were fewer in number throughout infection,
failed to increase in size over the course of the infection, and were
much less fecund. In contrast, T. canis larvae were
recovered in similar numbers from tissues of transgenic mice with
"low" or "high" eosinophilia and from nontransgenic mice.
These results and other data suggest that eosinophils can contribute to
host resistance to some parasite species. Parasite transit time
through the host may correlate with relative sensitivity to eosinophils.
| |
TEXT |
Tissue-invasive helminth species
often induce intense tissue and peripheral blood eosinophilia. It has
long been argued that eosinophils may kill some species of parasites or
at least impede larval migration and development. Early studies
suggested that depletion of eosinophils with polyclonal
antieosinophil antibodies impaired immunity to Schistosoma
mansoni (13) and Trichinella spiralis
(7). More recent studies have shown that while monoclonal anti-interleukin-5 (IL-5) antibodies can decrease eosinophilia induced
by infections with these parasite species, in all cases the parasite
burden remained unchanged (8, 18, 19). Our own data suggest
that in IL-5 transgenic mice, eosinophilia may even be
counterproductive in primary infections with both S. mansoni and T. spiralis (2, 3). Nevertheless,
depletion studies with anti-IL-5 antibody suggest that IL-5 and/or
eosinophilia are protective against some helminth species, including
Strongyloides venezuelensis and Angiostrongylus
cantonensis (11, 17).
This study addresses the importance of eosinophils in resistance to two
tissue-invasive intestinal helminths. Nippostrongylus brasiliensis was chosen because it has a very short transit time through the host, and Toxocara canis was selected because it
remains in the host for extended periods of time. We used two lines of IL-5 transgenic mice (Tg5C1 and Tg5C2) which have been described elsewhere (2-4, 20) and another previously unreported but
related IL-5 transgenic line, Tg5C3 (44 transgene copies). These IL-5 transgenic lines can be divided into "low-" (Tg5C1) and
"high-level" (Tg5C2 and Tg5C3) eosinophilia categories, having
approximately two (Tg5C1) to eight times (Tg5C2 and Tg5C3) more
peripheral blood eosinophils than nontransgenic mice infected with the
helminth Mesocestoides corti, a known inducer of
eosinophilia (4). Since these lines of IL-5 transgenic mice
have proven difficult to establish as homozygotes, all transgenic
animals described were heterozygotes, and the nontransgenic control
animals were generated from the same litters. N. brasiliensis and T. canis were passaged, cultured, and enumerated using conventional techniques (9, 16). In all
experiments mice either were injected subcutaneously (s.c.) at the base
of the neck with approximately 500 N. brasiliensis L3
infective larvae or were given 500 infective T. canis
eggs by gavage. Statistical significance of the data was assessed by two-tailed Student's t test using Excel for Macintosh 4.0 (Microsoft), where P < 0.05 was considered significant.
N. brasiliensis egg production.
Eggs produced by
N. brasiliensis infecting nontransgenic CBA/Ca mice were
released in large numbers in the feces from six to eight days
postinfection (PI) but were never detected outside of this period (Fig.
1). In contrast, worms infecting IL-5
transgenic CBA/Ca mice produced few eggs and when detected, peak
production tended to be delayed by one to two days (Fig. 1). Counts of
eggs in feces remained very low throughout the course of infection in
Tg5C1 and Tg5C2 transgenic mice (Fig. 1) and in experiments with Tg5C3
mice whose results are not presented. While egg production in
low-eosinophilia Tg5C1 mice was greater than in high-eosinophilia Tg5C2
animals, it failed to reach statistical significance. However, a clear
difference between the lines was the absence of eggs in any of the
Tg5C2 mice on Day 6 PI.
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FIG. 1.
Mean egg production by N. brasiliensis worms
in two lines of IL-5 transgenic mice. No eggs were detected in any
Tg5C2 mouse on day 6 PI. Asterisks denote statistically significant
comparisons with the corresponding nontransgenic (NTg) control group
(P < 0.02). There were three mice/group.
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Intestinal N. brasiliensis worms.
Large numbers of
worms were found in the small intestines of nontransgenic mice as early
as 3 days PI, and this level of infection was maintained for at least
another 2 days (Fig. 2). In contrast, worm numbers were much lower in both low- and high-eosinophilia IL-5
transgenic lines. Intestinal worm numbers in IL-5 transgenic mice in
this and other experiments peaked later than in nontransgenic controls.
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FIG. 2.
N. brasiliensis intestinal worm burden in
IL-5 transgenic and control nontransgenic mice. Asterisks denote
statistically significant comparisons with the nontransgenic control
group (P  0.05). There were three to four
mice/group.
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Low egg counts in transgenic mice were not simply due to a paucity of
worms. In a separate experiment, a mean of 27.7 (standard
error of the
mean, 5.9) worms in nontransgenic mice produced 14.3
eggs/fecal sample,
whereas a similar number of worms (28.3 ± 2.3)
in Tg5C2 mice did
not produce eggs at a level detectable with
the same techniques. Thus,
while it is likely that few parasites
survived migration from the s.c.
site of inoculation in IL-5 transgenic
mice, those that did reach the
gut also appeared to be less fecund.
Neither was this result due to an
absence of female worms in transgenic
mice. In a typical experiment,
worm sex ratios of 213 females
to 108 males (i.e., 66% female) and 30 females to 14 males (i.e.,
69% female) for nontransgenic and
transgenic mice, respectively,
were
determined.
Worms were detected in the gut 3 days after s.c. injection of L3 larvae
into nontransgenic mice and typically, they could
be detected for 7 to
9 days PI. During this period of residence
in the gut of nontransgenic
hosts, worms mature (
9) and increase
in length (Fig.
3). The mean lengths of worms recovered
from the
lower gastrointestinal tracts of each of the three IL-5
transgenic
lines were significantly less (
P < 0.003)
than those of worms
found in nontransgenic mice at all three time
points (Fig.
3).
Male worms are smaller than female worms
(
9), but since worm
sex ratios were approximately the same
in transgenic and nontransgenic
hosts, this does not explain the
observed differences in average
worm size. Taken together, these
results suggest that the average
growth rates of worms recovered from
transgenic animals during
the course of infections were lower than
those seen in nontransgenic
hosts. Worms recovered from transgenic mice
were often pale in
appearance, suggesting that they were malnourished.
Worms also
failed to localize in the preferred anterior third of the
gut
in each of the IL-5 transgenic mouse lines tested (data not shown),
and this may adversely affect worm nutrition. The reduced fecundity
routinely observed in infections in IL-5 transgenic mice may be
directly related to poor growth and development of intestinal
worms,
but this is reversible. When transferred surgically to
naive hosts,
intestinal worms recovered from transgenic mice developed
sufficiently
to produce eggs (unpublished results).
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FIG. 3.
Length of worms recovered from the intestine of IL-5
transgenic and nontransgenic mice. Asterisks denote statistically
significant comparisons with the relevant nontransgenic control group
for each day of infection (P < 0.003). Values are
means (± standard errors of the means) worm length calculated from 6 to 58 worms/group. Worms were recovered from two to four mice/group
except for the day 7 nontransgenic group, for which the mean represents
measurements for 24 worms found in one mouse only.
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Other studies with IL-5-overexpression transgenic mice and with IL-5
receptor
-chain knockout mice show that animals with
high levels of
IL-5 and eosinophilia also have enhanced resistance
to the nematode
A. cantonensis (
22). Although the
IL-5-overexpression
transgene construct and background strain employed
to generate
the mice (
24) used by these workers were
different from those
used in our study, the results support the
hypothesis that eosinophilia
can impair the migration of some
tissue-invasive parasite species
and reduce their reproductive success.
Treatment of mice with
anti-IL-5 antibodies can abolish eosinophilia
induced by
N. brasiliensis (
1), and it has been
shown to result in increased parasite
load in mice infected with
S. venezuelensis (
11),
A. cantonensis (
17), and
Onchocerca spp. (
6,
12),
adding further support
to this
hypothesis.
Our results and those of another study in which eosinophilia was
prevented by treating animals with anti-IL-5 antibodies
(
10),
suggest that IL-5 and eosinophils may not influence
greatly the
expulsion of adult
N. brasiliensis worms.
Rather, eosinophils
appear to be important in the killing of larvae
either at the
site of the initial infection or elsewhere during their
passage
to the gut. Other data (
1a) suggest that eosinophils
are recruited
to the site of inoculation of
N. brasiliensis larvae within 6
h and, most significantly, that
this is a major phase in which
the migration of the parasites is
inhibited. However it also seems
likely that viable larvae which
complete migration to the gut
in IL-5 transgenic mice experience
further damage or maturational
inhibition once they reach this site.
The worms do not increase
in length from days 3 to 7 PI in IL-5
transgenic hosts, but it
has yet to be determined whether egg
production is suppressed
due to a general effect on nutrition or
development or whether
it is a more specific effect on mating or
fecundity.
Blood and tissue eosinophilia in N. brasiliensis-infected mice.
Leukocytes in samples of
tail blood were enumerated with a Coulter ZF automated cell counter
(Coulter Electronics, Harpenden, England). Differential cell counts
were performed on methanol-fixed blood films stained with Giemsa. Mean
peripheral blood eosinophil counts in uninfected Tg5C2 mice were
approximately 100 times greater than those in nontransgenic mice (Fig.
4). Eosinophils represented 72 and 4% of
total peripheral blood leukocytes for Tg5C2 and
nontransgenic groups, respectively. Tg5C2 transgenic mice
infected with N. brasiliensis showed a 35 to 50%
decline in peripheral blood eosinophilia in the early stages of
infection (days 1 to 9 PI), but total numbers of eosinophils returned
to preinfection levels by 15 days PI, i.e., well after worm expulsion
(Fig. 4). A modest decline, followed by a fourfold increase in
eosinophil numbers was noted in nontransgenic mice, with counts peaking
on days 9 and 11 of infection (maximum of 15% of total leukocytes).
This maximum occurred at or soon after the time of worm expulsion (Fig.
4).
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FIG. 4.
Mean total peripheral blood eosinophils in IL-5
transgenic (closed box) and nontransgenic (open circle) mice infected
with N. brasiliensis (five mice/group). Asterisks
represent statistically significant differences from values for the
corresponding uninfected (day 0) mice (P < 0.05).
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Eosinophils were also enumerated in hematoxylin and eosin-stained
histological sections of formalin-fixed small intestine.
Samples were
taken 3 cm posterior to the pyloric sphincter and
eosinophils were
enumerated in either 10 or 20 villus crypt units
(
14) per
mouse. Eosinophils were relatively common in the lamina
propria and
submucosa of the guts of all uninfected mice. The
numbers of
eosinophils detected in the guts of nontransgenic mice
increased
dramatically approximately 6 days after worms had arrived
in the lumen
of the small intestine, i.e., circa day 9 PI (Fig.
5). Eosinophil numbers increased earlier
in transgenic than in
nontransgenic mice (Fig.
5; day 6 versus day 9 PI, respectively),
but peak levels were seen at approximately the same
time
at or
shortly after worm expulsion (day 11; Fig.
5). Most of the
increase
in eosinophils in infected transgenic mice occurred within the
lamina propria and submucosa. At most times postinfection, intestinal
eosinophil numbers were greater in transgenic than in nontransgenic
mice. However, the numbers in transgenic mice returned to baseline
(uninfected) levels by day 15 PI, while those in the small intestines
of nontransgenic mice remained elevated at this time.
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FIG. 5.
Tissue eosinophils in histological sections of the small
intestines of (IL-5 Tg5C2 transgenic [grey bars] and nontransgenic
[NTg] [open bars]) mice infected with N. brasiliensis. Each value is a group mean for 3 or 4 mice and was
calculated from means of counts on 10 or 20 villus crypt units (VCU)
for each mouse in a group. Asterisks represent a statistically
significant difference from values for the corresponding nontransgenic
mice on the days indicated (P < 0.05).
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While we cannot exclude the possibility that overexpression of IL-5 may
mediate resistance through other mechanisms, our results
are consistent
with the hypothesis that the development and fecundity
of adult worms
may be affected adversely by the presence of large
numbers of
eosinophils in the lamina propria of the gut. It is
possible that local
production of IL-5 enhances activation of
eosinophil functions
that are deleterious to
N. brasiliensis intestinal
worms, since expression of IL-5 in gut tissue has been shown to
correlate with differential resistance to
N. brasiliensis in BALB/c
and C57BL/6 mice (
25). While
IL-5 is also a growth and differentiation
factor for B lymphocytes
and promotes immunoglobulin A (IgA) production
in the mouse, the
very short course of a primary infection makes
unlikely any
contribution from the humoral arm of the adaptive
immune
response.
T. canis infection in IL-5 transgenic mice.
T. canis infections induce very substantial blood
eosinophilia, and the granulomas which form around larvae are rich in
eosinophils. Eosinophilia is suppressed in T. canis-infected pregnant and lactating dogs, and it has been
suggested that this may facilitate parasite transmission to newborn
offspring. Treatment of infected mice with anti-IL-5 antibodies
suppresses both blood and tissue eosinophilia induced by this
parasite but does not seem to influence the number of larvae
subsequently recovered from the liver (15). Our experiments were designed to assess the significance of preexisting eosinophilia on
the survival and migration of T. canis larvae.
Twenty-eight days postinfection, the numbers of larvae recovered from
the brain, liver, and muscles were similar in Tg5C1 (low eosinophilia)
and Tg5C2 (high eosinophilia) IL-5 transgenic mice and in
nontransgenic CBA/Ca mice (Table
1). At this time, peripheral blood
eosinophil counts in nontransgenic mice had risen approximately
20-fold, while those in infected Tg5C1 and Tg5C2 mice were 10- and
20-fold higher, respectively, than in infected nontransgenic animals. Eosinophils were prominent in liver granulomas found in both transgenic and nontransgenic mice, suggesting that recruitment of these leukocytes to areas of larval deposition was unimpaired in all lines (data not
shown).
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TABLE 1.
T. canis larvae recovered from tissues of
IL-5 transgenic and nontransgenic mice infected with 500 eggs per
os 28 days previously
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Sugane and colleagues (
21) studied
T. canis
infections in mice expressing a different IL-5 transgene construct
(
24) and
found that overexpression of IL-5 and eosinophilia
did not influence
the number of larvae recoverable from the lungs
within the first
2 weeks of exposure to the parasite. The present study
supports
and extends both this observation and our earlier studies
(
15).
Even late in infection (i.e., 28 days PI) we could
find no effects
of eosinophilia on larval numbers recovered from either
eosinophil-rich
tissues, such as liver and muscle, or from relatively
eosinophil-poor
brain tissue. Our observations are also consistent with
the report
that mice unable to mount an eosinophil response due to
disruption
of IL-5 genes (
23) carry numbers of larvae
similar to those
of wild-type mice. In our experimental model, unlike
natural infections
in pregnant and lactating dogs, eosinophilia cannot
be dramatically
down-regulated during
T. canis
infections. Our findings suggest
therefore, that the suppression of
eosinophilia seen during pregnancy
in dogs may not be essential for
T. canis larval migration and
transmission to
offspring.
This study provides evidence that a preexisting state of
eosinophilia enhances resistance to primary infections with
N. brasiliensis but does not promote clearance of
T. canis larvae. On first appraisal,
IL-5 transgenic
mice may seem an artificial model from which to
draw conclusions about
immunity to parasites in natural infections.
However, many humans and
other animals are exposed to tissue-invasive
parasites for much of
their lives. Although initially generated
as part of a
parasite-specific response, a state of constant eosinophilia
may
contribute nonspecifically to immunity to newly encountered
helminth
species. The resistance of IL-5 transgenic mice to infection
with
N. brasiliensis, without preexisting specific immunity,
provides
evidence to support the hypothesis that eosinophilia alone can
confer at least partial resistance. Preexisting eosinophilia,
especially in the tissues, might be expected to be most beneficial
for
resistance to parasites which normally spend only a short
period of
time in tissues of the host, i.e., where only an early
response can be
effective in preventing passage of larvae to definitive
sites, such as
the
gut.
It seems likely that although infections with many parasite species
induce eosinophilia, not all helminths will be susceptible
to these
leukocytes. In contrast to organisms such as
N. brasiliensis,
helminths which parasitize the host for long periods
are likely
to have evolved strategies which make them resistant to the
actions
of eosinophils. Treatment with anti-IL-5 antibody does not seem
to alter parasite burdens in mice infected with a range of other
parasite species, including
S. mansoni (
18,
19)
and
T. spiralis (
8). Our earlier studies
with other parasite species, including
S. mansoni
(
3) and
T. spiralis (
2), suggest
that chronic
eosinophilia and/or overexpression of IL-5 may, by
mechanisms
yet to be determined, actually be detrimental to host
resistance
against some infections. In contrast, in this study we have
shown
that
T. canis does not seem to be either
advantaged or disadvantaged
in eosinophilic IL-5 transgenic mice.
Therefore, eosinophilia
may not be a universally beneficial response to
all invasive helminths.
These results provide support for a
reassessment of the importance
of innate immune mechanisms
(
5), particularly those operating
in infections with
metazoan
parasites.
| |
ACKNOWLEDGMENTS |
This work was supported in part by the Australian Research Council,
Adelaide Channel 7 Children's Research Foundation, and the University
of Adelaide Faculties of Science and Medicine.
Thanks to Hans Schoppe and Marjorie Quinn (Department of Pathology,
University of Adelaide) and the staff of the Department of Pathology,
Institute of Medical and Veterinary Science, Adelaide, for preparation
of tissues for histology.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Microbiology and Immunology, University of Adelaide, North Tce.,
Adelaide, South Australia, Australia, 5005. Phone: 61 8 8303 4155. Fax: 61 8 8303 4362. E-mail:
ldent{at}microb.adelaide.edu.au.
Editor:
J. M. Mansfield
| |
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Infection and Immunity, February 1999, p. 989-993, Vol. 67, No. 2
0019-9567/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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