Effect of Trichinella spiralis Infection on Passive Cutaneous Anaphylaxis in Mice - American ...
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INFECTION AND IMMUNITY, Jan. 1977, p. 84-90 Vol. 15, No. 1
Copyright C) 1977 American Society for Microbiology Printed in U.S.A.
Effect of Trichinella spiralis Infection on Passive Cutaneous
Anaphylaxis in Mice
JOHN J. MUNOZ* AND R. L. COLE
Rocky Mountain Laboratory, Hamilton, Montana 59840
Received for publication 28 June 1976
Infection of CFW mice with Trichinella spiralis induced a state of relative
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unresponsiveness to passive cutaneous anaphylaxis (PCA) induced with hen
egg albumin and its corresponding antibodies. The unresponsiveness was to
PCA produced either with immunoglobulin G, (IgG,) or IgE type of antibodies,
but was more pronounced with the latter. As few as 25 larvae given by stomach
tube 20 days before induced this resistance, although 400 larvae induced a
greater resistance. When 400 to 600 larvae were fed to mice, the refractoriness of
these mice to PCA was noticed 15 days later. The sera of infected mice had the
ability to inhibit mainly PCA induced by IgE. This inhibitory property of sera
from infected mice was more pronounced 35 days after infection than 10 months
later, when only weak inhibitory activity was detected. Purified rat IgE in-
hibited the PCA reactions induced in both mice and rats with mouse IgE-type
antibody. At high concentrations, evidence of inhibition of the IgG1-induced
PCA in mice was also obtained. We believe that the relative unresponsiveness
of infected mice is due to an increase in production of IgE which competitively
blocks the mast cell sites for other IgE molecules.
Infection with Trichinella spiralis in some aphylaxis (PCA) induced with either IgG, or
strains of mice induces a state of histamine and IgE type of antibodies.
serotonin hypersensitivity (2, 13) and increases
the levels of immunoglobulin E (IgE) with spec- MATERIALS AND METHODS
ificity to trichinella antigens (3, 11). These
properties are in some respects similar to those T. spiralis. These worms were kept in mice in-
of the substance from Bordetella pertussis that fected by stomach tube with 200 to 600 larvae. When
we have called pertussigen (J. J. Munoz, Fed. larvae were needed, mice infected for at least 1
Proc. 35:813, 1976), which also increases the month were processed by a modification of the
method used by Weatherly (21). Briefly, the method
susceptibility of some mouse strains to vasoac- consists of sacrificing infected mice, removing the
tive amines and increases the levels of IgE with skin, internal organs, heads, tails, and feet, and
specificity to antigens given with it (4). A sig- homogenizing the carcass (mainly muscle and bone)
nificant increase in the levels of IgE with speci- in a Waring Blendor for 60 s in a solution (500 ml/
ficty to a given antigen should induce a state of mouse) of pepsin (1% dried pepsin in 0.5% HCl). The
relative unresponsiveness to other antigens, homogenized suspension was incubated for 2 h at
because IgE fixes strongly to mast cells and 370C with constant shaking and filtered through a
high concentrations of IgE with one specificity double thickness of cheesecloth, and the larvae were
should successfully compete with mast cell allowed to settle for at least 15 min. The superna-
tant fluid was drawn off to about 2.5 cm from the
binding sites for IgE molecules with different bottom. The settled larvae were diluted with saline
specificities. This was demonstrated by Stan- and allowed to settle again in a funnel fitted with a
worth et al. (19, 20) when they showed that clear plastic tube and clamp. When the larvae had
human myeloma IgE or its Fc piece blocked the settled, they were collected in as small a volume as
Prausnitz-Kustner (P-K) reaction in humans possible and washed by being added to the top of a
and by Jarrett et al. (7), who showed competi- funnel filled with fresh physiological saline. This
tive inhibition of IgE in rats. Any treatment process was repeated two or three times until the
that increases IgE production to antigens other larval suspension was cleared of any cloudiness. The
than the one involved in hypersensitivity reac- suspension was standardized by counting the larvae
in a known volume as previously described (13).
tions should competitively inhibit reactions due Mice were infected by means of a stomach tube
to IgE. Therefore, we have explored the possi- (18-gauge animal-feeding needle, Popper and Sons,
bility that mice infected with T. spiralis might Inc.) with 0.1 to 0.2 ml containing the appropriate
become more resistant to passive cutaneous an- number of larvae.
84VOL. 15, 1977 EFFECT OF T. SPIRALIS ON PCA 85
Mice. CFW male and female mice reared in our (NH4)2S04 was added to the dialyzed fluid to bring
laboratory were used. C57BL/6J female mice were the salt concentration to 37% saturation. After
purchased from the Jackson Laboratory, Bar Har- standing overnight at 2 to 50C, the solution was
bor, Me. centrifuged clear and the precipitate was discarded.
B. pertussis extract. B. pertussis extract (BPE) To the supernatant fluid, additional saturated
was made by a modification of the method previ- (NH4)2SO4 was added to bring it to 48% saturation.
ously described (12). Acetone-extracted cells were This mixture was allowed to stand overnight at 2 to
suspended in 1 M NaCl-0.05 M sodium pyrophos- 50C and then centrifuged. The supernatant fluid was
phate at pH 7.4. The suspension was left overnight discarded, and the precipitate was dissolved in bo-
at 2 to 5C with constant stirring, and then the cell rate-NaCl buffer and chromatographed in a Sepha-
debris was separated by centrifugation. The clear rose 6B column (2.5 by 83 cm) equilibrated in the
supernatant fluid was extensively dialyzed against same buffer. The protein peak containing IgE was
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distilled water and lyophilized. rechromatographed in the same column, and the
Mouse antibody. The reaginic type of antibody material under the rather symmetrical peak of IgE
(IgE) was contained in a pool of antisera from was dialyzed against 0.025 M tris(hydroxymethyl)-
C57BL/6J mice immunized intraperitoneally with a aminomethane (Tris)-phosphate buffer, pH 8 (80 ml
mixture of 50 to 125 spg of hen egg albumin (HEA) of 2.5 M Tris + 150 ml of 1 M NaH2PO,, 700 ml of
and 5 to 50 ,ug of BPE dissolved in 0.2 ml of phos- water; the pH was adjusted to 8.0 with 10 N NaOH,
phate-buffered saline. Twenty-one to 26 days later, and the volume was brought up to 6 liters). The di-
the mice were given subcutaneously a booster dose alyzed material was chromatographed on a DE-52
of 5 ug of HEA in saline, and the mice were bled 7 to column (volume of 110 ml) equilibrated with Tris-
9 days later. Sera with high titers of 72-h PCA phosphate buffer. The IgE in this column is not re-
antibody were pooled and titrated for their content tarded and comes off in the first protein peak. This
of anti-HEA of the IgG, (2-h PCA) and IgE (72-h fraction was considered to be pure rat IgE. The frac-
PCA) classes of immunoglobulins by PCA reactions tionation was monitored by gel diffusion tests per-
performed on mice. formed with a specific anti-rat IgE serum kindly
The IgG, type of mouse anti-HEA was produced in supplied by H. Metzger. The final concentration of
C57BL/6J mice that had been immunized intraperi- the IgE was determined by the optical density at 280
toneally with a mixture of 125 ,ug of HEA and 50 j.g nm (optical density/1.36 = milligrams of protein/
of BPE in 0.2 ml of saline. Then, at weekly inter- milliliter).
vals, intraperitoneal injections of 0.5 ml of complete Antigen. Five-times-recrystallized HEA was pur-
Freund adjuvant emulsified in saline were given. chased from Nutritional Biochemicals Corp.
On the 4th week and weekly thereafter, intraperito- PCA reactions. PCA reactions were performed as
neal injections of 0.5 ml of complete Freund adju- previously described (4).
vant containing 6 ,ug of HEA were given until
marked ascites developed. The ascitic fluid was then RESULTS
collected, centrifuged, and kept frozen. This fluid, Effect of T. spirlis infection on PCA reac-
which contained good titers of anti-HEA in both tion. Mice that had been infected with 600 lar-
IgG1 and IgE, was fractionated to separate IgG, from vae 34 days before were used as test animals for
IgE by first precipitating the globulins at 50% satu- PCA reactions. Dilutions of IgG, antibody and
ration with ammonium sulfate. The precipitated
globulins were dialyzed in 0.005 M phosphate buffer IgE antibody were tested in four infected mice
(pH 7.9) and passed through a diethylaminoethyl- and four normal mice by intracutaneous ad-
cellulose column equilibrated with the same buffer. ministration of 0.05 ml of the chosen dilutions.
Fractions were eluted by increasing the buffer con- Two hours later, mice sensitized with IgG, were
centration to 0.02, 0.03, 0.05, and 0.5 M phosphate challenged intravenously with 0.2 ml of a mix-
at pH 7.9. The IgGI was eluted in the 0.02 M frac- ture of 0.5% Evans blue + 0.5% HEA, and the
tion, and the IgE was eluted in the 0.05 M fraction. diameter of the reactions was measured 30 min
The 0.02 M fraction was dialyzed, lyophilized, and later. Mice sensitized with IgE antibody were
then used in the present work. This preparation did
not induce 72-h PCA in mice. The serum with IgE similarly challenged 3 days later, and reactions
antibody, when heated at 560C for 3 h, failed to in- were measured 30 min later. The results are
duce PCA reactions, thus indicating that the anti- given in Table 1.
HEA antibodies were mainly of the IgE class. The It is clear from these results that infected
IgG, did not produce PCA reactions in rat skin, mice did not respond as well as normal mice to
whereas the IgE antibody preparation did in a titer either IgGi- or IgE-mediated PCA. The range of
similar to that obtained in mice as reported by Ovary concentrations of IgE used in this experiment
et al. (15). was rather low, and we did not know from these
Purification of rat myeloma IgEIR, was done results whether infected mice were capable of
from myeloma ascitic fluid. The technique was that responding to PCA induced with IgE. In the
used by H. Metzger (personal communication). following experiments we increased the range
Briefly, it consisted of the following steps. Twenty of concentrations.
milliliters of ascitic fluid was dialyzed against bo-
rate-NaCl buffer (222.6 g of boric acid + 168.3 g of Effect of worm load on PCA reaction. Mice
NaCl in 18 liters of water at pH 8). Saturated were infected with either 25, 100, or 400 larvae86 MUNOZ AND COLE INFECT. IMMUN.
TABLE 1. Effect of T. spiralis infection on PCA' then important to see whether the serum of
Concn of IgG, Dilution of serum contain-
infected animals had a substance that could
Recipient (Aglml) ing IgE prevent PCA reactions from taking place. The
mouse antiserum containing IgE antibody to HEA was
25 50 100 1:3,000 1:2,000 1:1,000 diluted 1:250, and the IgG, preparation was
Normal Ob 11 15 0 6wc 10 made to contain 100 ug/ml. To 0.3 ml of each
0 10 15 0 8w 9 antibody, 0.3 ml of diluted normal or infected
mouse serum was added. Each of two mice was
T. spiralis 0 0 11w 0 0 0 then given intracutaneously 0.05 ml of each
infected 0 0 12w 0 0 0 mixture, and 2 or 72 h later the mice were
a CFW mice that had been infected with 600 T. challenged intravenously with the dye-HEA
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spiralis larvae 34 days earlier were used. mixture.
b Numbers are the diameter in millimeters of the Sera from mice that had been infected for
area of bluing measured on the underside of the various periods of time with T. spiralis were
skin. Each reading represents a separate mouse. used. The sera of infected mice inhibited the
Only one site per mouse was used. PCA induced with IgE to HEA having little
c w, Weak reaction. effect on PCA induced with IgG, (Table 4). In
addition, it is evident that the inhibitory sub-
per mouse. Twenty and 41 days later, the IgE stance was more concentrated in the sera of
and IgG, PCA antibodies were titrated in these mice infected 35 days before bleeding than in
mice (Table 2). those that had carried the infection 4 to 10
Photographs of the reactions obtained 20 months. The sera of normal mice had no de-
days after infection are given in Fig. 1 and 2. monstrable inhibition of either type of anti-
Twenty days after infection, mice infected with body.
only 25 larvae showed a moderate resistance to The substance responsible for this inhibition
manifest reactions induced with antibodies of is most likely IgE. We have demonstrated IgE-
the IgG, or IgE class. When 100 or 400 larvae type antibodies specific for T. spiralis antigens
were given, however, a striking inhibition was by 72-h PCA reactions induced with these sera
observed for both types of antibodies. Forty-one
days after infection, strong inhibition was ob- TABLE 2. Effect of larval load on reactivity of skin to
served after even the small dose of 25 larvae. PCA
Effect of duration of T. spiralis infection on No. of Days Concn of IgG, Dilution of serum
ability of mice to give PCA reactions. This lar- after (Ag/ml) containing IgE
experiment was designed to determine when vae infec-
after infection resistance to PCA was first ob- given tions 25 50 100 1:500 1:250 1:125
served. Mice were infected with 400 larvae and 25 20a 12Wb . 12w 20 +d 7w 14
at intervals thereafter were tested as above for 0 12 14 10 11 14
their ability to develop PCA reactions with the 41 0 0 12 0 + 10
two types of antibodies (Table 3). PCA re- 0 lOw 16 0 0 9w
sponses to IgG, and IgE types of antibodies 100 20 0 low 18 0 10 9w
were inhibited strongly beginning 20 days after 0 0 15 0 7w 10
the infection, and the inhibition seemed 41 0 low 9w 0 0 8w
stronger at 41 days. An unexpected finding in 0 lOw 13 0 0 12w
this experiment was that the PCA reactions 400 20 0 0 10 0 0 0
induced by IgG, antibody were considerably 0 + 14 0 6w 7w
larger in mice that had harbored the infection 41 0 0 12w 0 0 0
for only 10 days than in normal mice or those 0 0 lOw 0 0 NIe
that had carried the infection for 15 days or 0 9w 14 16 10 12 30
longer. The significance of this finding is pres- 11w 16 19 10 13 24
ently under investigation. 11 12 17 10 13 11
Effect of serum from normal and T. spir- 12 10 18 11 14 13
alis-infected mice on PCA reactions. As indi- a On day 20, the diaphragms of six mice per group were
cated in the introduction, T. spiralis infections examined under the microscope for T. spiralis larvae. Mice
augment the levels of IgE in the animal, and infected with 25 larvae had only a few larvae in the dia-
phragm, but all six mice were positive. The diaphragms of
this increase in IgE could be responsible for those receiving 100 and 400 larvae showed increasing num-
preventing, competitively, PCA due to IgE bers of larvae in all mice.
with specificty to other antigens. The previous b. c See Table 1 for meaning of numbers. w, Weak reac-
experiments clearly showed that T. spiralis- tions either ring shaped or with clear center, or with very
light concentration of dye.
infected mice were more resistant to PCA reac- d _ s Doubtful reaction.
tions than were the normal animals. It was eND, Not done.VOL. 15, 1977 EFFECT OF T. SPIRALIS ON PCA 87
CONCENTRATION OF IgG1ANTIBODY TO HEA
25 50 100
womw
.1 V .110,
0 ...J'
i.
z
w
m-
-
'
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-4 -
'U
4(
4c
16
lim.^,.
-i
3
0. 100 *
I'-
0
z
400 9
,^
FIG. 1. PCA reactions performed with different concentrations (in micrograms per milliliter) of the IgG0
type of antibody to HEA in normal mice or in mice infected 20 days earlier with 25, 100, or 400 T. spiralis
larvae given by stomach tube.
using as a challenge dose a saline extract from each antibody received it diluted in saline only.
frozen, thawed, and homogenized larvae mixed The results are given in Table 5.
with Evans blue. Unfortunately, we do not The PCA due to IgG, was not significantly
presently have a way to quantitate mouse IgE inhibited by 250 ,g of rat IgE per ml of the final
other than by PCA reactions. We will attempt mixture. In some experiments, however, rat
in the future to develop such a test by using the IgE at the highest concentration seemed to
technique of producing anti-mouse IgE recently have some inhibitory effect because the PCA
developed by Prouvost-Danon et al. (16), Lang reactions had a completely clear center. The
et al. (9), and S. Lehrer (personal communica- reactions induced by IgE antibody were com-
tion). pletely inhibited by as little as 10 jig of rat IgE
The availability of rat myeloma IgE offers a per ml in the mixture and partially inhibited by
possibility of measuring the effect of this pro- 2 ug/ml. Similar inhibition was obtained in rat
tein on IgE of mice. It is known that mouse IgE skin sensitized with mouse antibody (IgE).
fixes to rat mast cells and that it produces PCA These experiments show that IgE may indeed
reactions in rats (15), and that rat IgE fixes to be responsible for the inhibition observed.
mouse mast cells (17). This indicates that rat There are methods besides worm infestation
IgE may also inhibit the PCA reaction. that stimualte IgE formation to various anti-
Effect of rat IgE on PCA reaction in mice. gens; one is by immunization with B. pertussis
A solution of purified rat myeloma IgE contain- extracts (4), and another is by giving antigen
ing 500 pug/ml was made in physiological saline, mixed with large amounts of alum (18). Prelim-
and then serial 10-fold dilutions were made. inary studies have shown that both of these
Equal volumes of each dilution were mixed methods may also render mice more resistant
with either a solution of IgG, antibody contain- to PCA reaction.
ing 100 gg/ml or a 1:250 dilution of serum con- DISCUSSION
taining IgE antibody. The final concentration
of IgG 'was 50 ,ug/ml, and the final dilution of During a study on the stimulation of IgE in
the IgE-containing serum was 1:500. Two mice mice by an extract from B. pertussis, it oc-
were sensitized per dilution, and two mice for curred to us that stimulation of IgE to a heterol-88 MUNOZ AND COLE INFECT. IMMUN.
DsL UTON OF 1gE ANTIBODY TO HEA
2n.
,
ri2250 7,4;~
z
LU
25
0
~~~ ~
m t. ~ ~
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0
LU
'C
ALI~~~~~~~~~~~~~~~~~~~~~~~~~~
:1 100
i-'i
ci~~~~~~~~~~~~~~~~~l
U-~~~=X -urj tI',
Z400
FIG. 2. PCA reactions performed with different concentrations of the IgE type of antibody to HEA in
normal mice or in mice infected 20 days earlier with 25, 100, or 400 T. spiralis larvae given by stomach tube.
TABLE 3. Effect of duration of T. spiralis infection parasitic worms (5-8, 15). Indirectly, some pub-
on resistance to PCA lished observations have shown that parasitism
Concn of IgG, (jug/1l) Dilution of serum in humans may make them more resistant to
Days after Osno g gm containing IgE allergic responses, since persons infected with
infection helminths were found to give weaker P-K reac-
25 50 100 1:500 1:250 1:125 tions (1). These observations, although they do
10 lOwa.b 25 34 0 10 20 not directly incriminate parasitism as responsi-
11w 25 32 12 9 19 ble for resistance to certain allergic reactions,
15 0 +C 12 0 11w 20 are highly suggestive. Jarrett et al. have defi-
0 15 20 0 9w 12 nitely shown that Nippostrongylus brasiliensis
infections make rats more resistant to PCA re-
20 0 0 10 0 0 0 actions (7).
0 + 14 0 6w 7w
The results presented here also conclusively
41 0 0 12w 0 0 0 show that experimental infection of mice with
0 0 low 0 0 NDd T. spiralis makes these animals strikingly
Uninfected 11w 12 17 10 13 11 more refractory to PCA reactions to a heterolo-
controlse 12w 10 18 11 14 13 gous antigen. Thus, infected mice sensitized
a, bSee Table 1 for meaning of numbers. w, Weak reac-
with anti-HEA of either the IgG1 or IgE class
tion.
did not respond to doses of these antibodies that
±, Doubtful reaction. were fully effective in normal mice of the same
d ND, Not done. sex and age. The refractory state appeared
e
Groups of uninfected mice of the same age and sex as about 7 days after the female worms had depos-
the infected mice were used for each time period, with ited the larvae in the intestinal mucosa and the
results similar to the control group shown in this table; for
that reason the results were omitted. larvae had migrated to the muscle (from 15 to
20 days after oral infection with larvae [10]). It
ogous antigen should block allergic reactions was also apparent that the refractoriness was
involving mast cells. One of the most effective more pronounced 41 days after infection than at
ways of stimulating IgE in animals, and appar- 15 or 20 days. As few as 25 larvae were suffi-
ently humans as well, is infection with certain cient to induce the refractory state, but in thisVOL. 15, 1977 EFFECT OF T. SPIRALIS ON PCA 89
TABLE 4. Effect of T. spiralis-infected mouse sera obtained at different times after infection
50 gg of IgG,/ml in the mixture IgE-containing serum diluted 1:500 in the
Type of mouse serum used mixture
1:2 1:4 1:8 1:16 1:2 1:4 1:8 1:16
Normal 15a 17 15 12wb 13w 15 15 18
14 15 17 17 12w 12 15 18
35 days after infection NDC ND ND ND 0 0 0 low
ND ND ND ND 0 0 0 14w
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4 mo after infection 0 13 13 17 0 12w low 12w
17 14 13 10 0 0 0 12w
10 mo after infection 12 11 15 17 0 12w 12w llw
12 12 11 13 17w llw 11 11
Antibody in saline 15 14
17 14
a
See Table 1 for meaning of numbers.
b w, Weak reaction.
c ND, Not done.
TABLE 5. Effect of rat IgE on PCA reactions in mice also competing with IgG1. This should be fur-
IgE-containing serum ther investigated with purified IgG, and IgE
Final concn of 50 jg of IgG,/ml fractions from mouse serum.
rat IgE (jug~ml in mixture diluted 1:500 in
mixture If the inhibition observed in this work was
250 14a 33 0 0 due to an increased concentration of IgE, one
50 14 0 0 0 should also be able to increase the resistance of
10 13 9 0 0 mice to PCA by other methods known to in-
2 10 10 6wb 8 crease IgE. We are presently investigating this
0.4 15 10 14 12 possibility.
Saline 13 12 14 14 The implication of these findings with re-
a
See Table 1 for meaning of numbers. Columns spect to human allergies involving the IgE and
represent readings from individual mice. possibly the IgG class of immunoglobulins is
b w, Weak reaction. clear. It should be possible to block mast cell
receptors by greatly increasing the IgE concen-
case it took longer to manifest itself. One tration in the blood to antigens that normally
hundred larvae were more effective, and 400 are not present in the environment. If this can
appeared to be even better. Since each mature be done, mast cells may well become relatively
female worm can produce close to 1,000 larvae unresponsive to antigens to which the person is
(10), even the small infective dose of 25 larvae allergic. It has already been shown that IgE
has a potential to produce some 12,500 larvae myeloma protein or its Fc piece blocks the P-K
(assuming that half the infecting larvae are reaction (19, 20). Passive transfer of IgE would
males and half females), which is a significant probably not be practical because of its antigen-
worm mass. The most important factor in the icity, its limited availability, and the required
production of this refractoriness was probably frequent administration. If endogenous produc-
IgE, because sera from infected animals in- tion of IgE were increased, most of these prob-
hibited PCA reactions induced by IgE and puri- lems could be circumvented.
fied rat IgE also inhibited these reactions in ACKNOWLEDGMENTS
both mice and rats. It is clear from the results We wish to express our appreciation to H. Metzger for
that inhibition in infected mice was not exclu- supplying the rat ascitic fluid and the methods to purify the
sively manifested against the IgE class but also rat IgE used in this work. We also would like to thank R. K.
against the IgG1 class. We do not now know Bergman for his help in writing this manuscript.
whether this inhibition was due to IgE alone or LITERATURE CITED
whether an increase in the IgG1 in the infected
mice was responsible for inhibition of IgG1-in- 1. Bazaral, M., H. A. Orgel, and R. N. Hamburger. 1973.
The influence of serum IgE levels of selected recipi-
duced PCA. Since IgG, is normally present in ents, including patients with allergy, helminthiasis
high concentrations in the sera of mice, it is and tuberculosis, on the apparent P-K titre of a re-
more probable that IgE in high titers may be aginic serum. Clin. Exp. Immunol. 14:117-125.90 MUNOZ AND COLE INFECT. IMMUN.
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