THE TRANSFER OF ANTIBODY FORMATION BY MEANS OF A POLYMORPHONUCLEAR EXUDATE

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FOLIA BIOLOGICA
The Transfer of Antibody Formation by Means of a Polymorphonuclear
Exudate
J. STERZL
Institute of Biology, Czechoslovak Academy of Science, Department of Microbiology, Praha
In earlier experiments in hyperimmunised animals it was demonstrated that by
freezing and thawing proteins could be extracted from the repeatedly washed cells
of a polymorphonuclear exudate, which became bound with the specific antigen.
On making an electrophoretic study of the rate of movement at different pH, it
was seen that the character of these proteins was not identical with the serum anti-
bodies. Following immunisation with a single dose of the antigen, antibodies were
demonstrated in polymorphonuclear cells for only a short period after immunisation
(~terzl 1952, 1954).
In the latest work the presence of developing antibodies in tissues is determined
by means of their transfer to non-immunised recipients which do not themselves
react to an antigen by antibody formation (animals irradiated by X-ray, five-day-old
rabbits - Sterzl 1955). In the present work the same method is used for carrying
out a revision of earlier results on the basis of which it was assumed that antibodies
are also formed in the cells of a polymorphonuclear exudate.
The polymorhonuclear exudate was prepared by filling normal and immunised rabbits with 300 - 400 ml.
physiological saline administered intraperitoneally. After 4-5 hours the exudate is drawn off and
sedimentation of the cells is carried out by centrifuging at 500 g. The cellular sediment is washed three
times in gelatinous physiological saline. During washing the number of cells is adjusted to approximately
? 20-30,000/,ul., according to the degree of turbidity, and is then determined exactly by counting in
a Biirker chamber. In the case of every exudate a smear is taken and a differential count made from
100 cells. Polymorphonuclear cells and typical lymphocytes are determined precisely; the other cells
of the peritoneal exudate are grouped together as macrophages, in view of the difficulty of precise differ-
entiation. After four hours' peritoneal filling in rabbits, the cells in the exudate other than polymorpho-
nuclear cells average only 5-20 %. Adult rabbits weighing 2-3 kg. were used as donors; these were
immunised by the intravenous route with Salmonella paratyphi B inactivated by heating for one hour
at 70 ?C. The number of doses and the intervals between the doses are given in the text to figures. In
experiments in which cells were isolated from non-immunised animals and mixed with the antigen in
vitro, the same antigen (S. paratyphi B) was used. The amount of spleen cells used in the experiment
and the amount of antigen added to the cells in vitro are the same as in a previous communication
(Sterzl 1957). These data are given in greater detail in the text relating to the individual figures.
The serum used for adsorption on to the cells of the peritoneal exudate and for experiments with the
passive transfer of antibodies to young rabbits was rabbit serum obtained by immunisation with the
same strain of S. paratyphi B as that used as the antigen. The titre of the serum was 1 : 400, i. e. it was
not lower than the titre of antibodies in the serum of any of the donors from whose peritoneal
exudate cells were obtained.
Washed cells, concentrated to the given number, were transferred by the intraperitoneal route to
ve-day-old rabbits from which blood was collected by cardiac puncture. The collection intervals are
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shown in the various figures concerned. The exact method for determining antibodies in young rabbits
has already been described (9terzl 1955). The agglutinations were placed in a refrigerator and the
results read off after four and six days.
Transfer of Cells of Polymorphonuclear Exudate Obtained at Various Intervals
from Rabbits Immunised with One Dose of Antigen
Altogether 11 experiments were carried out in this series, transfer being made to
57 young rabbits from 11 litters. Rabbits were immunised with 1 ml. bacterial
antigen by the intravenous route and peritoneal exudate produced at various
intervals following immunisation. A different donor was used for every experiment-
8 8 Fig. 1. Formation of antibodies following transfer to young rabbits
by means of cells of peritoneal exudate from donor (rabbit) im-
munised with single dose of antigen (108 micro-organisms). x: days
after immunisation when peritoneal exudate was produced and cells
a obtained. Every recipient is denoted by one point.y: antibody values.
The highest antibody titres reached during the ten days following
transfer are always given. Recordings were made only from animals
8 J which survived and in which all collections of blood were made.
1 2 3 4 5 6 7 8
The exudates were prepared in the rabbits 2, 3, 4, 5, 6, 7 and 8 days after commencing
immunisation. A survey of the results is given in fig. 1. It is seen that a positive
demonstration of antibodies was obtained by the transfer of cells of peritoneal
exudate isolated from rabbits four and five days after immunisation. The course of
antibody formation following the transfer of cells from a rabbit four days after
immunisation is shown in fig. 2. On comparing these results with results obtained
from the transfer of spleen cells (~terzl 1955, 1957) it is seen that in the present
experiments with the transfer of cells of polymorphonuclear exudate antibody
formation is less regular and very restricted as regards time.
Transfer of Cells of Polymorphonuclear Exudate Obtained from Repeatedly
Immunised and Revaccinated Animals
In four experiments, rabbits which had been repeatedly immunised a number
of times were used as donors. Transfer was made to 32 young rabbits. Fig. 3 gives
an example of a transfer of cells from a revaccinated animal; fig. 4 shows the result
of a transfer of cells from a repeatedly and intensively immunised donor. The doses
are given in the appended text. As compared with immunisation with a single dose,
a marked increase in the intensity of antibody formation in the recipients was
observed, which was also of longer duration and more standard in character. The
intensive and uniform formation of antibodies following the transfer of cells from
a repeatedly and intensively immunised donor is particularly striking. As compared
with the cell counts in the peritoneal exudate of animals immunised once and
several times, it is seen that the intensive antibody formation observed in these
last experiments cannot be explained by different percentual proportion of the
various types of cells in the peritoneal exudate.
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i
Fig. 2. Fig. 3.
Fig. 2. Normal rabbit immunised with 1 ml. (108micro-organisms) four days before formation of perito-
neal exudate from 400 ml. physiological saline. Exudate drawn off after five hours by puncture and
centrifuged. Exudate fluid, freed from cells, lyophilized (120 ml.) and dissolved in 6 ml. Agglutination
titre of concentrated exudate fluid 1 : 16, rabbit serum 1:64. Cells washed and injected intraperitoneally
in young rabbits in amounts of 1 ml. (228 x 106 cells). Extraction of cells carried out by freezing and
thawing; agglutination reaction of extract negative. Cell count: polymorphonuclears 82, lymphocytes 17,
macrophages 1. x: age of rabbits in days, y: titre of antibodies.
Fig. 3. Rabbits Nos. 801, 802, 803, 804, born 7. 12. 1954 and injected on fifth day of life with nucleo-
protein fractions. Revaccinated on 12. 4. 1955 with 1 ml Salmonella paratyphi B, intravenously (107 micro-
organisms), on 9. 5. 1955 with 1 ml. (2 x 109 micro-organisms). On 10. 5. 1955 filling of rabbits with
physiological saline carried out; after washing, cells injected in amounts of 2 ml. (40 x 106 micro-organ-
isms) in young rabbits. Cell count in exudates:
Rabbit No. 801: polymorphonuclears 98, lymphocytes 6, macrophages 6,
No. 802: polymorphonuclears 91, lymphocytes 9, macrophages 0,
No. 803: polymorphonuclears 90, lymphocytes 8, macrophages 2,
No. 804: polymorphonuclears 82, lymphocytes 8, macrophages 10.
Young rabbits Nos. 201 and 202 injected with 1 ml. leucocytes from donor No. 801 - full lines.
Young rabbits Nos. 203 and 204 injected with leucycytes from donor No. 803 - dashed line.
Young rabbits Nos. 205 and 206 injected with leucocytes from donor No. 804 - dotted line.
Young rabbits Nos. 207 and 208 injected with leucocytes from donor No. 802 - dash and two dots.
Control without injection - two dashes and two dots. x: age of rabbits in days; y: titre of antibodies.
Fig 4. Rabbit No. 42, immunised from 30. 9. 1955 to 30. 1. 1956 three times weekly, first with seven
doses of a suspension of 108 micro-organisms/ml., then with 20 doses of 2 x 109 micro-organisms/ml.
Three days after last injection peritoneal exudate produced by a filling of 400 ml. physiological saline.
After five hours the exudate was drawn off and the cells centrifuged. The supernatant fluid (80 ml.) was
dried by lyophilization and dissolved in 5 ml. distilled water and dialyzed against physiological saline.
Agglutination in the concentrated fluid was negative, l ml. of a washed suspension of cells (24 x 108 cells)
injected intraperitoneally in five-day-old rabbits. Differential count: polymorphonuclears 82, lympho-
cytes 6, macrophages 12, x: age of young rabbit and time of blood collection in days.y: titre of
antibodies in blood of young rabbits.
Fig. S. Normal rabbit filled with 500 ml. physiological saline. Resultant exudate washed five times in
physiological saline. 228 x 106 cells/ml. After washing the cells were mixed with the antigen (1 cell of
exudate to 2 micro-organisms of S. paratyphi B. The mixture was injected intraperitoneally in young
abbits. x: age of young rabbit and time of blood collection in days. y: titre of antibodies in
blood of young rabbits.
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Transfer of Cells of Polymorphonuclear Exudate of Non-immunised Animals after
Mixing with Antigen in vitro
Six experiments were carried out in this series, with transfer to 40 young animals.
These experiments were based on the experience that if cells which are capable of
changing their metabolism (e. g. spleen cells) are mixed with the antigen in vitro,
they are able to form antibodies on being transferred intraperitoneally to young
animals (~terzl 1957). The cells of peritoneal exudate from normal animals were
therefore isolated, mixed with the antigen and transferred to young rabbits by the
intraperitoneal route. In none of these experiments was antibody formation observed
in the first period following the transfer. The recording from one group (fig. 5)
shows that antibodies cannot be demonstrated until the young animals are them-
selves able to react actively to an antigen by the formation of antibodies.
Transfer of Leucocytes from Non-immunised Animals, Incubated in vitro with
Immune Serum
An attempt was made in earlier experiments (~terzl 1952) to ascertain whether
the transfer of antibody formation by means of cells of polymorphonuclear exudate
is true antibody formation, or whether serum antibodies are only adsorbed on to the
cells. In the present experiments, in which the transfer of cells was used to demonstrate
antibody formation, the control experiments were carried out by the same method.
A known amount of serum antibodies was adsorbed
on to the cells of a peritoneal exudate, the cells
were washed three times in gelatinous physiolog-
ical saline and transferred by the intraperitoneal
route to young rabbits. In all, three such experi-
rabbits
In no
25
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i
d
t
t
.
yo
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s were carr
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on
5 8 10 12 14 17 21 25 30 men
case antibody was found, either in the young ani-
Fig. 6. Normal rabbit filled with 450 ml. mals or in extracts of leucocytes. A detailed des-
physiological saline; exudate drawn off
after five. hours. Differential count: cription of one of these experiments is given in
polymorphonuclears 86, lymphocytes fig. 6. In the same way, no decrease in the titre of
10, macrophages 4. After washing, antibodies (i. e. adsorption by the cells) was found
183 x 105 cells/ ml. Cells transferred following incubation of cells together with serum
to two young rabbits - dashed lines.
Remainder centrifuged and suspended of a known titre. Negative demonstration of anti-
in the same volume of immune serum bodies following transfer is easily understandable
against S. paratyphi B (titre 1: 400). when antibodies were not found even by direct
Incubated with serum for 30 minutes agglutination in an extract of cells. Passive
at 37? C and 30 r. p. m. After incu-
bation serum removed and titre of an- transfer of serum of the given titre (1 : 400) was
tibodies again determined (no change.) demonstrated in the serum of young rabbits if the
Cell sediment washed three times and injection was made with 1 ml. of concentrated
suspended in original amount of fluid. serum and serum diluted in the proportion of
Number of cells 176 x 105/1 ml., 1 ml.
cells injected intraperitoneany in 1:10. On injecting serum diluted in the proportion
young rabbits. Extract made from of 1:100, antibodies were not demonstrated sero-
2 ml. suspension of leucocytes by freez- logically in the blood of young rabbits. It may
ing and thawing; agglutination react- therefore be assumed that if a slight amount of
ion of extract negative.
antibodies remains adsorbed on to the polymorpho-
nuclear leucocytes, it will not be possible to demon-
strate these antibodies serologically in the blood of young rabbits following transfer.
There is also a possibility, however, that a serologically demonstrable amount
of antibodies, adsorbed on to the cells, may become bound, during preparation of the
extract by freezing and thawing, to some components of the cells and lose their
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serological effectiveness. In such a case, although they might be present, it would
not be possible to demonstrate the antibodies. This eventuality was verified by
mixing a centrifuged suspension of cells (30 X 106/ml.) obtained from rabbit exudate
with the same amount of serum of the titre given above. Extraction of the cells was
carried out by freezing and thawing immediately after mixing with the serum and
after incubating at 37 ?C for 30 minutes. No change occurred in the titre of antibodies
in the serum, either after simple incubation (they were not adsorbed on to the cells)
or on mixing the cells with antibodies and disrupting them. This shows that cell
components are not bound with serum antibodies in such a way as to mask their
serological activity.
From these control experiments it is concluded that the antibody formation
ascertained in preceding experiments following the transfer of cells of a polymorpho-
nuclear exudate to young rabbits is the expression of biological activity of the cells
and does not represent a passive transfer of already formed antibodies, but is the
outcome of an active process of antibody formation by the cells.
Di8cu88ion
The literature on the question of antibody formation and its association with
different types of cells has already been reviewed in an earlier communication
(Sterzl 1954, pp. 45-51). It was shown that a number of authors associate antibody
formation only with certain particular types of cells. More recently, especially among
Scandinavian authors (Bjorneboe, Gormsen and Lundquist 1947, Fagraeus 1948)
and in the work of Ehrich et al. (1949) some authors have come to regard plasmatic
cells as the main site of antibody formation (e. g., Coons et al. 1955, Forshter 1955).
Other experimental results, however, provide evidence that further types of cells
participate in the formation of antibodies (Girard and Murray 1954, Roberts and
Dixon 1955, Sinkovics 1955, Stoner and, Hale 1955).
Not only in theory, but also in the experimental work, very little attention is
paid to the participation of phagocytic cells in antibody formation. Any such study
is based on the assumption expressed by Ehrich, Harris and Mertens (1946) that the
participation of phagocytosing cells consists merely in engulfing and digesting the
antigen so as to prepare the way for the actually active cells, the lymphocytes and
plasmocytes. Since it has been demonstrated, however (Walsh and Smith 1951,
Roberts 1955) that antigen digested by phagocytes decreases the antibody reaction,
it is concluded that this does not participate in antibody formation. Further proof
is to be found in experiments (Ehrich et al. 1946, Roberts 1955) demonstrating that
phagocytic cells which invade inflammation of the skin or peritoneum and are then
injected with antigen, do not form antibodies. It may be assumed that mature
phagocytic cells which invade artificially produced inflammation are not capable
of antibody formation. This is also demonstrated in our experiments in which the
cells of an exudate were isolated, mixed with antigen and administered to young
rabbits. No formation of antibodies was demonstrated in any of these experiments.
On the other hand, antibody transfer was demonstrated using the same types of
exudate cells, when the cells were collected four and five days after immunisation.
The author takes the view that these experiments confirm the assumption that the
cells of mesenchymal tissue can change their metabolism if they come into contact
with antigen, not in a mature state, but in the course of their development.
It is especially necessary to estimate whether the transfer of antibody formation
to young rabbits is mediated by the polymorphonuclear cells or whether other types
of cells contained in small amounts in the exudate are responsible. When making the
transfer, amounts of 20-30 X 106 cells are used; this is the smallest amount found
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to be satisfactory in making a transfer of very effective spleen cells. It is an amount
many times less than that used by Harris (1954), the smallest quantity used by whom
is 150 X 106. Since the transfer of antibody formation is also directly dependent on
the quantity of transferred cells, it is hardly likely that so small a percentage of
lymphocytes and macrophages would participate in the antibody reaction. In order
to form a definite conclusion, however, it would be necessary to follow up the
morphological fate of the various types of cells transferred and to ascertain whether
the proportion determined by the count in the smear does not change in the recipient
through proliferation of one type of cell.
The above results again support the assumption that antibody formation is
a metabolic change in various cells and tissues. Particular significance is attached to
the metabolic change in the course of immunisation in cells such as polymorpho-
nuclear cells, which participate directly and to a large extent in the defence processes
of the organism.
Summary
An investigation was made of the possibility of transferring antibody formation
from adult immunised rabbits by means of cells of a polymorphonuclear exudate
to five-day-old rabbits. Following a single immunisation dose of antigen (108
microorganisms of Salmonella paratyphi B), antibody formation was transferred
to young rabbits by means of the cells of a polymorphoumlear exudate only
when the cells had been obtained from the exudate four days after immunis-
ation at the earliest. Antibody formation in young animals, when produced
by the cells, of a donor, immunised by a single dose, is of short duration and not
standard in character. The cells of a polymorphonuclear exudate obtained from adult
donors repeatedly immunised with several doses of antigen produce antibody
formation in young animals which is more intense, of longer duration and of a more
standard nature than that produced by the-transfer of cells from donors immunised
with a single dose of antigen. The cells of a polymorphonuclear exudate obtained
from normal, non-immunised rabbits and mixed with the antigen in vitro, never
form antibodies on being transferred intraperitoneally to young rabbits. Adsorption
of antibodies on to polymorphonuclear leucocytes was not demonstrated, either by
direct serological tests or by transfer of the cells to young rabbits. It is concluded
that the cells of polymorphonuclear exudate also participate in immunity processes
in the organism, but only those cells that have come into contact with the antigen
in the course of their development, and not the mature cells of polymorphonuclear
exudate.
B j o r n e b o e, M., G o r m s e n, H., Lundquist, F.: Further Experimental Studies
on the Role of Plasma Cells as Antibody Producers. J. Immunol. 55 : 121, 1947.
Coons, A. H., L e d u s, E. H., C o n n o 1 1 y, J. M.: Studies on Antibody Production.
1. Method for the Histochemical Demonstration of Specific Antibody and its Application to
a Study of the Hyperimmune Rabbit. J. Exp. Med. 102 : 49, 1955.
E h r i c h, W. E., H a r r i s, T. N., M e r t e n s, E.: The Absence of Antibody in the
Macrophages during Maximum Antibody Formation. J. Exp. Med. 83 : 373, 1946.
E h r i c h, W. E., D r a b k i n, D. L., F o r m a n, C.: Nucleic Acid and Production of
Antibodies by Plasma Cells. J. Exp. Med. 90 : 157, 1949.
E h r i c h, W. E.: Cellular Sources of Antibodies. Blood Cells and Plasma Proteins. New
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G i r a r d, K. F., M u r r a y, E. G. D.: The Presence of Antibody in Macrophage Extracts.
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Harris, S., Harris, T. N., Farber, M. B.: Studies on the Transfer of Lymph
Node Cells. I. Appearance of Antibody in Recipients of Cells from Donor Rabbits Injected with
Antigen. J. Immunol. 72 : 148, 1954.
R o b e r t s, K. B.: The Failure of Macrophages to Produce Antibodies. Brit. J. Exp. Pathol.
36 : 199, 1955.
R o b e r t s, J. C., D i x o n, J. F.: The Transfer of Lymph Node Cells in the Study of the
Immune Response to Foreign Proteins. J. Exp. Med. 102 : 379, 1955.
S i n k o v i c s, J.: Virus Neutralisation Experiments with Lymphoid Cell and Lymph Node
Extracts. Acta microbiol. 2 : 385, 1955.
S t o n e r, R. D., H a 1 e, W. M.: Antibody Production by Thymus and Peyer's Patches in
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bilkovinami. Cs. biologie 1 : 285, 1952.
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D o p m T e p, (1). K.: K BOnpocy 0 MexaHHaMe o6pa3oBaHHH alTHTeii JIHM( IO1 gHbiMH HJIeTHaMH.
MMEH (11) : 100, 1955.
III T e p u JI b, H.: AoKa3aTeIIbCTBO HaJIH'IHH HOpMaJIbHbIX H HMMyHHbIX y-rJIo6yJIHHOB B nefKo-
ijHTax. iicJi. BHOJIorHH 1 : 299, 1952.
IIepeHeceHt3e o6pa3OBaHHH aHTHTeJI I{JIeTHaMH
IIOJIYIMOp( OHyKJIeapHOPO mccygaTa
B CBoeit pa6oTe MII OHpe);eJIHJLH, B03MOH HO JIH C nOMOlgbio KJIeTOK nOJII3MOp~0-
HyKJLeapHoro aKCcyl;aTa nepeHeCTH CHOCO6HOCTb K 06pa8OBaHI3IO allTHTCJI OT B3pOC-
JIbIX HMMyHH3HPOBaHHbIX KPOJIHHOB Ha 5-JjHeBHbIX KpOJIbtIaT. Hoe ie OJ;HOpa3OB01ft
HMMyHH3HpyIOHIe 1903bI aHTHreHa (108 MHKpo60B S. paratyphi B) ygaBaJfocb nepe-
AaTb HpOJIbtIaTaM aTy CHOCO6HOCTb KJIeTKaMH noJIHMOp()oxyHJleapxoro axccyJ;aTa
TOJIhKO B CJIy=iae, eciiH 8TH KJIeTKH 6bIJIH rio iytieHbi H3 aHCCyJ;aTa He paHbHIe 4 AMR
noc.le HMMyHH3aI.HH. CHO006HOCTb K o6pa3OBaHHIO allTHTeii, BbI3bIBaeMaH y MOJIOJ;bIX
?KHBOTHbIX KJICTKaMI3 JjoHopa, HMMyHH3HpOBaHHOro OAHOpa3OBO]ft J;o3Olf, oHa3bl-
BaeTCFI HeCTaHgapTHOR H cxoponpexoJ;xii elk. KJIeTHH nOJIHMOp~OHyK ueapHoro
3Kccyg[aTa, noiIy'IeHHoro OT B3POCJIbIX J[OHOpOB, HOBTOPHO HMMyHH3HpOBaBHIHXCH
HeCKOJIbKHMH J O3aMH aHTHreHa, BbI3EIBaIOT Y MOJIOJ[HIX H HBOTHbIX 60JIee HHTOH-
CLIBHoe, 6oJiee J;JIITeJibHOe H 6oJiee cTaHgapTHOe o6pa30BaHHe allTHTeii, ileM nepeHOC
KJIeTOK OT AOHOpOB, HMMyHH3HPOBaHHbIX OJ[HOi3 A03oft aHTHreHa. KJIeTKH noJIH-
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BaHHbIX KPOJIIIKOB H CMeinaHHbie c allTHreHOM in vitro, nocile nepenoca B HOJIOCTb
6plonIIIHM KpOJIbtiaTaM Hit B OJ;HOM cJiygae He BhI3bIBaJIH o6pa3OBaHHH aHTHTeJI.
Harn1BHe agCOp6L(I1H allTHTeJI Ha nOJIHMOp4OHyKJIeapHbie JleilKOI;HTbi He 6bLJIO HaMH
JjOKa3aH0 HH nyTeM npJIMbIX repo ioriiIecHHX TeCTOB, HH HyTeM nepeHOca KJIeTOK
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11MMyHHTeTa, HO 3T0 6bIBalOT TOJIbKO Te KJIeTKH, KOTOpble CTOJIKHyJIHCb c allTmreHOM
B nponecce CBoero pa3BHTHH, a He y1Ke C(OpMHpOBaBIIIHeCH KJIeTKH noJIHMOp4 o-
HyKJleapHoro axccy);aTa.
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