From www.bloodjournal.org by guest on June 18, 2017. For personal use only.
Erythropoiesis
Chimeras:
and
Contribution
By Olli
Lymphocyte
cells
sac-embryo
and
have
been
chimeras
Erythroid
cells
red
blood.
cells
From
At
erythrocytes
in
90%
days
of
development.
V
ERTEBRATE
show
B locus
of
in
of
changes
early embryo
elaborates
which
is succeeded
cells
The
further
embryo
containing
in the
place
chimeras.3’4
chick
Using
yolk
sac,
quail
it has
of
were
at
up
different
species
erythro-
embryos
7
of
red cell series
The cellular
red cells has
and the timing
in quail-chick
of
stem
cells
or
if not
bryonic
stem
quantitatively
ing proportions
intraembryonic
minimal
site
of
primitive
yolk
cell
in an increasing
of primitive
number
and
Blood.
slow
in others.
Furthermore,
Vol. 59, No. 2 (February),
1982
by
These
stem
are
from
chicken
stem
involved
as well
layer
obtained
early
erythroid
cells
erythrocytes
the
la-like
a triple
results
that
transiently
using
yolk
cells.
in the
while
production
of
as of lymphocytes.
both
of T
I 3 of incubation.
Thus,
B cells.
beyond
has not been possible
stem cells participate
stem
cell
reserve
day
to determine
to the seeding
destined
to
ensure
the
thymus
and
were always
entirely
it
whether
yolk sac
of the permanent
erythropoiesis.
bursa
of
populated
quail-chick
by intraem-
hemopoietic
cells, the spleen on the other hand
small
and seemingly
transient
yolk-saccell populations.5
bryonic
harbored
derived
can
These
problems
chick
yolk-sac-embryo
be approached
using
chickchimeras
capable
of hatching
and developing
chimeras,
using
into
adulthood.68
sex chromosome
T and
serum
study,
chick-chick
yolkhave been used to analyze the
intraemis
give
and
to declin-
to
while
the
definitive
and only
to a
the chimeras
usually
the
confirmed
the early
cells for the lymphoid
present
chirneras
developmental
stem
cells
shift
in erythropoiesis
intraembryonic
stem
to
from
cells.
yolk
For
sac
this
purpose,
alloantigens
of the chicken
major
histocompatibility
locus (B complex)
have been used as markers to trace
the origin
of cells
in allogeneically
constructed
chimeras.
In the chicken,
the B complex
is
considered
to be analogous
In the three-locus
model
to the MHC
of mammals.
of chicken
B complex,
B-F
From
the Department
ofMedical
ty, Turku,
Finland
and the Institute
Microbiology.
d’Embryologie
College
de France.
Nogent-sur-Marne,
Supported
in part by a contract
by
intraembryonicin some chimeras,
In
and
IgG
system.68
sac-embryo
B lymphocytes
on these
of specifi-
have
of stem
production.4
stimulated
Studies
analysis
allotype
determination,
intraembryonic
origin
erythrocytes.
rapid
only
for
cally
However,
the period
during
which
yolk sac stem
cells give off an erythroid
progeny
has not been determined
precisely.
In the xenogeneic
chimeras,
the
replacement
of yolk-sac-derived
derived
red cells is irregular,
produces
as
antisera
respectively.
cells
indicate
lymphocytes.
anti-la
on a
to erythropoiesis
sac stem cells
erythrocytes,
give
rise
bursa
the
a
stem
sac and
erythrocytes
of definitive
stem
cells
amount
red
yolk
cell contribution
different.
The
rise to all or most
erythrocytes
the
qualitatively,
sac
embryo-
that
chick,
yolk-sac-derived.
Both types of stem cells were
observed
to have similar
potentialities
in erythropoiesis; the hemoglobin
pattern
was evolved
rather
by a
time program
than the anatomical
origin
of erythroHowever,
on
Such
into
in ovo
demonstrated
cells formed
within
the embryo
replace
yolk sac stem
cells in their erythropoietic
function.3’4
The hemoglobin switch
has been investigated
in the two populations
of red cells,
i.e. quail,
intraembryonic-derived,
and
cyte
cells.
chimeras
Although
chimeras
hemoglobins.
grafted
bursa
and
system.
do not develop
red
red
day
and
allogeneic
and
embryonic
in
anti-B
detected
blood.
cells
observed
thymus
intraembryonic
peripheral
not
the
definitive
the
specific
immunofluorescence
17-18
early
using
in
yolk-sac-derived
was
antigens
adult type erythrocytes.
sac produces
primitive
been
cells
detection
a primitive
by definitive
Recently
their origin
has
been
studied
derived
found
the
mdi-
in their
and permanent
from
Cells
Dieterlen-Li#{232}vre
are
change
by
of these
yolk-sac-derived
after
erythrocytes
analyzed
making
is taken
Francoise
the
peripheral
cells
carrying
the adult
hemoglobin
types.”2
origin
of the precursors
of the definitive
been unknown.
the
appearance
antigens.
and
from
into
yolk
circulation
by the second
incubation
in
yolk-
embryo-derived
no
poiesis.”2
The
cell population,
Their
the
blood
hatching.
Toivanen,
yolk-sac-
proportions.
EMBRYOS
erythrocytes
or
blood
onwards,
developmental
maturating
chicken
sac
incubation,
peripheral
After
Paavo
demonstrated
increasing
of the
the
a majority
of incubation
appear
chick-chick
peripheral
days
represent
9 days
approximately
7
in the Chick
Yolk-Sac-Embryo
Sac and Intraembryonic
Stem
changes
in
yolk
were
in the
chimeras.
derived
the
mesenchyme
Martin,
ontogenetic
at
from
immunofluorescence
allogeneic
Claude
studied
differing
derived
intraembryonic
rect
Lassila,
development
erythroid
Lymphopoiesis
of Yolk
grants
Cancer
from
Sigrid
France
NIH
(NOI-CB-74l
Jus#{232}lius Foundation
and
77) and
the
Finnish
Union.
Submitted
Address
Medical
the
with
Turku
Univer.cidu CNRS
et du
January
reprint
15. 1981;
requests
Microbiology.
Turku
to
accepted
Dr.
Olli
University.
October
9, /981.
Lassila.
SF-20520
Department
Turku
of
52,
Finland.
© I 982 by Grune
& Stratton,
Inc.
0006-497l/82/5902--0026$l.OO/O
377
From www.bloodjournal.org by guest on June 18, 2017. For personal use only.
378
LASSILA
Laboratories,
determines
the histocompatibility
antigens
on leukocytes and erythrocytes,
B-L
determines
an antigen
present
on B lymphocytes,
and B-G determines
an
antigen
unique
to
erythrocytes.9”#{176}
(products
of the B-L
and molecular
weight
alloantigens
expression
gens of mammalian
anti-Ia
alloantisera
lymphocytes,
bodies
were
anti-B
chick
and embryonic
Ia-like
containing
against
alloantigens
coded
by B-F
used to detect
histocompatibility
erythrocytes
or anti-B’5
mm
anti-
and
B-G
loci
Chick
AND
a control.
Israel),
chimeras.
MATERIALS
were
METHODS
mm
line
Leghorn
These
locus;
line
lines
are
B2B2 (Ia21a2).
I ); the
eggs
were
sac.
and
The
onto
the
central
area
previously.’3
is destined
At least
Detection
ofla-Like
erythroid
type
I
of appropriate
weekly
for
5
erythrocytes
chicken
served
serum
PBS,
20
(Miles-Yeda,
the cells
were
washed
twice
under
a Leitz
Ploemopak
i1 of
Rehovot,
incubated
and
for
30
mounted
in
ultraviolet
counted.
Antigens
by Triple
Layer
line
used
present
are
the embryo,
amnion,
erythrocytes,
sera
have
Dulbecco’s
to the
Fc-IgG,
blastoderm
was
30 mm
V (B’5B’5)
yolk
sac, replacing
the
were
to
gives
as described
a technique
36-42
rise
the
hr of incubation
(8-20
l
PBS
diluted
from
was
diluted
I :20,
was
the
as described
used
added
to absorb
added
cells
above.
IgG
and
were
in each
anti-Ia
2
anti-
washes
to
were
with
chicken
incubated
(Miles-Yeda,
were
twice
for
chicken
and
serum
30
Rehovot,
incubated
and
of
antisera
was removed
the cells
washed
Normal
Details
antiserum
the
was
was
these
of these
After
the supernatant
cells
as a control
earlier.’5
rabbit
anti-rabbit
Ivanyi
cells/mI)
at 4#{176}C;
anti-Ia2
30 mm
‘‘
and
lO
30 mm
mounted,
and
(NCS)
diluted
test.
Indirect
RESULTS
from
the
With
t1 of
immunofluo-
and
x
sensitivity
4#{176}C,20
washing,
for
used
and
goat
at 4#{176}C.
Thereafter,
I :20
layer
Galton
as described
described.’
I :400,
cells
(1-5
been
of FITC-conjugated
counted
Cells
at
spin
bursa
by
methods
specificity,
at 4#{176}C.
After
Israel),
diluted
and
previously
slow
and
suspension
prepared
schedules
with
chick
area
were
using
A triple
described
Ia antisera
used
separated
temperature
previously.8
20 zl of cell
with
anti-Ia’5
were
at room
technique
immunization
zones
mm
as described
In brief,
incubated
and
the chimeras
peripheral
Dulbecco’s
were
collected
at appropri-
by venipuncture
blood
phosphate-buffered
and
saline
washed
(PBS;
Flow
Figure
1 describes
positive
(80.5
100
±
the
cells
erythroid
proportions
in
the
17.1;
mean
±
SD)
are
of
of type
B’5
blood
stages
of
most of the
of
developred cells
B’5, i.e. differ-
cells.
B2-positive
from
yolk-sac-derived
of embryo-derived
B2 and
peripheral
chimeras
at different
7 days of incubation,
entiated
proportion
80
Later,
the
erythrocytes
increases
rapidly
so that they make up the majority
of
blood
erythrocytes
(93.2 ± 4.6)
in 17-18-day-old
chimeras.
At the same time,
erythrocytes
taken
from
C.) 600
Ui
embryonic
spleen and bone marrow
are mostly
embryo
derived,
expressing
B2 surface
antigens
(Table
I ). It
should
be noted,
however,
that
a low percentage
of
yolk-sac-derived
B’5-positive
red cells is still found
in
40
UI
*
using
were
were
30
by cross-
erythrocytes
and
lymphocytes
staining
allogeneic
ment.
At
(I)
-J
_1
‘U
cells
62 g, 30
obtained
used)4
of grafting.
cells
with
times
400
blood
centrifugation,
I :20 was
two
examined
chickens
IgG
one
incubated
produced
Dulbecco’s
anti-chicken
only
20 jzl of a
20 zl of anti-B2
and
blood
Normal
with
the cells
and
microscope.
P (B2B2)
according
embryos
at the time
ate intervals
male
pools
2 washes
with
were
peripheral
I :20, was added
1 :5 glycerol-PBS
rescence
humidity.
two defined
vascular
of line
Detection
ofErythroid
Immunofluorescence
The
V adult
using
used
cells,
PBS)
antisera
+ 4#{176}C
overnight.
at 4#{176}C.
Thereafter
were
P of genotype
in a Funki
relative
to produce
peripheral
removed,
The
line
incubated
blastoderm,
area
were
Chimeras
the age-matched
equivalent
somites)
area
at
histocompatibility
and
65%
the colonies
University,
major
(la’tIa’t)
at 37#{176}C
and
avian
central
allantois,
grafted
B’tB’t
from
Turku
at the
Yolk-Sac-Embryo
In the developing
yolk
embryos
Microbiology,
fertile
The
egg incubator
Allogeneic
and
P chick
homozygous
V is of genotype
automatic
(Fig.
V and
of Medical
Department
used.
P and
rabbit
diluted
was mixed
Dulbecco’s
of adult
After
Peripheral
the
anti-B’5
was
on erythroid
Immunofluorescence
Embryos
White
and
absorbed
at 40#{176}C
for 2 hr and
as
cells/mI)
with
of line
chimera
antigens
1:50
injections
Antisera
Each
group
x l0
at 4#{176}C.
Anti-B2
FITC-conjugated
antigens
on
in allogeneic
thymocytes
(1-5
(diluted
intravenous
wk.
Scotland).
B blood
immunizations
In the present
study,
to detect
chicken
B
antisera
Irvine,
To detect
suspension
cell
locus) are by cellular
analogous
to Ia anti-
species.”2
were
used
and
Chicken
time.
ET AL.
2:1
1
A
1
DAYS
-r--
I
4
#{243}
11
13
15
17
19
“
-
‘
4
2
WEEKS
these organs at 1 7-1 8 days of incubation.
B locus antigens
were also studied
on embryonic
thymus
cells and Ia antigens
on bursa
cells. At the
HATCHING
Fig. 1 .
Evolution
of red cell populations
in peripheral
blood of
yolk-sac-embryo
chimeras
constructed
at 2 days of incubation
of
B1’B’
yolk sacs and B2B2 embryos.
Frequency
of cells reacting
with anti-B’5
or anti-B2
is given.
stages investigated,
about
cells expressed
embryo-type
were
null
the
values
cells;
one-fourth
yolk-sac-type
obtained
with
of
antigens
(B’5)
the
cells
normal
the
(B2),
thymus
the
rest
did not exceed
chicken
serum
From www.bloodjournal.org by guest on June 18, 2017. For personal use only.
ERVTHROID
STEM
Table
IN THE
CHICKEN
1 . Analysis
of Erythroid
and Spleen
of Allogeneic
Marrow
The
CELLS
Chimeras
Were
B”B”
Cells
in the
Sacs
Age of Embryo
BoneMarrow
l7days
Spleen
Bone
on Day 2 of Incubation
1 8 days
Each line represents
NCS, normal
3.
The
Chimeras
Anti-B”
Cells
of Allogeneic
Were
in the Embryonic
Yolk-Sac-Embryo
Constructed
Yolk
Sacs
87.7
5.9
1.8
Percent
83.1
6.9
73.7
69.4
2.3
2.1
1.4
8.1
2.7
14.7
1.9
1.5
3.3
1.4
40.1
1.3
2.3
29.3
0.8
1.9
54.3
2.2
2.0
35.4
1.3
0.9
2 1 .7
0.6
0.8
25.8
1.4
1.1
1.2
4.3
89.7
2.5
0.8
64.4
7.9
2.4
l7days
l8days
Peripheral
blood
4 wk
Each line represents
2).
Bursa
cells
also
expressed
unoperated,
age-matched
lines.
The results
about
antisera
used is this study
4.
normal
chimera.
one
chicken
serum.
Ia
antigens
of embryonic
origin
(Ia2), whereas
values for
the yolk-sac-type
(Ia’5) cells did not exceed
the control
values
(Table
3). The values obtained
for bursa and
thymus
cells
of these
chimeras
using
anti-Ia
and
anti-B
antisera,
respectively,
are within
the range
obtained
for normal,
bryos
of both chicken
specificity
of different
demonstrated
in Table
NCS
8.2
3.3
14 days
With
AntiIaS
3.5
serum.
(Table
of Cells Positive
Anti-la2
1 .2
12.3
bursa
of
15.7
69.8
Embryonic
and
on Day 2 of Incubation
Age
Organ
Bursa
Chimeras.
and B2B2 Embryos
With
NCS
NCS.
Two
chimeras
of Lymphold
Blood
one chimera.
chicken
used as control
Analysis
Peripheral
of
of Red Cells Positive
8 1 .5
1 8 days
Spleen
Table
B”B’5
Anti-B2
l7days
marrow
Bone
Chimeras.
and B2B2 Embryos
Percent
Organ
Embryonic
Yolk-Sac-Embryo
Constructed
Yolk
379
emthe
are
by embryo-derived
cytes
homospecific
yolk
sac differing
locus (B complex)
appeared
consistent
tion the chimeras
derived
from
be compared
previously
in quail
of 23 histoincompatible
yolk-sac-embryo
hatched,
and their peripheral
blood erythro-
chimeras
cytes and lymphocytes
were analyzed
at 2 and 4 wk of
age. No
cellular
chimerism
was
observed,
either
according
to the B anitgens
expressed
on erythrocytes
(Fig.
1 ) or to Ia antigens
expressed
on peripheral
blood
lympocytes
(Table
3). All erythrocytes
bore embryoderived
antigens
(B2), so did all lymphocytes
(Ia2).
erythrocytes
chimeras
composed
was analyzed
in
of an embryo
and
by the major
histocompatibility
antigens.
The replacement
pattern
and rapid.
At 10 days of incubaretained
only about 30% of red cells
yolk sac stem cells. This finding
should
to the development
shift in erythropoiesis
established
in heterospecific
i.e.,
chimeras,
chick
yolk
sac.35
In these
of chick by quail red cells in
embryos
with
the replacement
individual
embryos
obeyed
an unpredictable
time
course.
This was probably
due to species differences,
such as the larger size of chick yolk sac or the quicker
developmental
rhythm
of the quail.
Thus,
the analysis
of homospecific
chimeras
not only
confirms
the
primordial
tive
role
stem
of intraembryonic
erythropoiesis
but
also
discloses
cells
in defini-
a calendar
of
DISCUSSION
erythropoietic
The
cell
system
a fascinating
provides
populations
study,
the
model
during
in
for
the
of
embryo
the
yolk-sac-derived
Table
4.
Analysis
Thymus
on erythroid
In
ontogenesis.
replacement
chick
studies
2.
Analysis
Allogeneic
of Lymphoid
Cells
Yolk-Sac-Embryo
Constructed
B1B”
Chimeras.
Yolk
Sacs
Anti-B2
l4days
l7days
l8days
Each line represents
NCS. normal
chicken
Embryonic
The
Chimeras
on Day 2 of Incubation
Thymus
of Cells
Positive
Anti-B”
Cells
in the
19-Day-Old
Unopereted
Chicken
Percent
Organ
Line
B2B2
of
Were
B’5B’5
of
Anti-B2
NCS
32.8
1.7
1.4
24.3
0.4
0.5
42.4
32.6
1.6
0.5
Percent
Anti-la2
NCS
With
Anti-B”
1.0
1.0
With
of Cells Positive
Embryonic
Embryo
25.7
0.7
1.2
and B2B2 Embryos
Percent
Age
in the
of Normal
present
erythro-
Thymus
Table
of Lymphoid
and Bursa
0.5
33.5
of Cells Positive
Anti-Ia”
1.0
With
NCS
23.1
2.3
3.1
45.9
1.5
0.9
30.1
15.3
1.4
0.8
1.2
29.8
1.7
2.0
0.8
38.4
1.0
1.0
31.2
1.4
1.7
21.4
0.8
34.1
2.7
one chimera.
serum.
Bursa
B2B2
B’5B’5
1.5
31.5
1.0
0.5
0.8
45.0
0.5
1.9
1.0
30.2
0.5
Each line represents
NCS. normal
chicken
one embryo.
serum.
From www.bloodjournal.org by guest on June 18, 2017. For personal use only.
LASSILA
380
replacement
very
probably
development
strated
that
extinct;
seeding
(Fig.
yolk
to that
similar
1 ). Furthermore,
sac stem
cells
in other
words
none of
the permanent
erythropoietic
demonentirely
them
particpate
pool.
in
The study of histocompatibility
marked
cell populations in hemopoietic
organs
further
confirms
that yolk
sac stem cells colonize
transiently
some organs
only, as
was shown
by means of the quail-chick
nuclear
marker.5 In both
oc chimeras,
types
only
a small
tion of yolk sac lineage
cells is observed
period
in the bone marrow
and spleen,
possible
that
yolk-sac-derived
contribu-
for a short
though
it is
erythroid
cells
observed
in these organs
are circulatory
erythrocytes
and thus
do not represent
any true colonization.
Both chimeric
models
demonstrate
that
the thymus
and bursa
of
Fabricius
are not colonized
by yolk sac stem cells,
although
in the present
study
it cannot
be totally
excluded
due
Interference
cellular
to the presence
of null cells.
by the rejection
mechanism
evolution
observed
in
this
with
study
the
be
can
excluded.
The period
when erythropoiesis
shifts most
rapidly
from yolk sac to intraembryonic
stem cells, i.e.,
7-1 0 days of incubation,
precedes
the ontogeny
of
T-cell-mediated
embryo.
immune
functions
in
the
of the
thymus
and
bursa
the
yolk-sac-derived
cells
of definitive
erythrocytes.
that yolk sac stem cells
progeny
strated
are capable
blastoderms
give
a small
the thymic
we can postulate
cells
with
equal
rudi-
existence
qualitative
of
cells
it is interesting
of
yolk-sac-derived
produce
early,
tran-
most
intraemuntil
a later
and lympho-
to compare
the kinetics
erythrocytes
by
with
definitive
embryo-derived
erythrocytes
evolution
of primitive
versus
the quantitative
erythrocytes
as
described
by Bruns
and
Ingram.’9
At all stages
of
development,
this comparison
reveals a close parallelism
between
These
data
and those
indicate
that
our
findings
erythrocytes
sac stem
cells
are
small.
Diffuse
hemopoiesis
to
of Bruns
since
produced,
the
erythropoiesis
occurs
the
and
first
within
Ingram.
definitive
participation
becomes
of yolk
extremely
the
embryo
during
days 6-10 of incubation.
cular
hemocytoblasts
form
hemopoietic
mesenchyme
around
the heart
and
early
chick
The extravasfoci in the
aorta,
in the
mesonephros
and in the mesentery
of
chick
embryo.2#{176} It is likely
that
some
6-8-day-old
of the cells
involved
colonize
organ
cells
in these
hematopoietic
rudiments.
obtained
processes
In fact, we
from
7-day
or
1
It has been demonat head-fold
stage of
of colonizing
ment.’t
On these bases
two categories
of stem
also
sac stem
differentiation,
while
cells remain
unactivated
to definitive
erythropoiesis
poiesis.
Finally,
of replacement
by intraem-
bryonic
cells
and
their
increasing
involvement
in
erythropoiesis
indicate
that they become
active
in the
second wave of embryonic
hemopoiesis.
Hemopoiesis
in normal
chick embryo
up to 5 days of incubation
is
present
mostly
in the yolk
sac, producing
mainly
primitive
erythrocytes.
However,
on the basis of hemoglobin
switching
in quail-chick
chimeras4
and of in
vitro
cultures
of “deembryonated”
chick
blastoderms,’7
sient
erythroid
bryonic
stem
phase
leading
mesenchyme
are capable
and B lymphocytes
after
chick
16
Colonization
Yolk
potentiality.
in normal
it was
become
ET AL.
into
the
have demonstrated
intraembryonic
of developing
transfer
into
that
chick
to functional
T
irradiated
chick
immu-
cyclophosphamide-treated
nodeficient
chick embryos.22
Our results
do not comprise
the earlier
events
of
hemopoietic
differentiation
and possible
cell exchange
between
the embryo
and the yolk sac prior
to the
grafting.
At
least
no vascular
route
exists
for the cell
migration
from the yolk sac to the embryo
before
or at
the time of grafting.
In conclusion,
this study on allogeneic
chick-chick
chimeras
demonstrates
that intraembryonic
stem cells
are the only progenitors
of lymphocytes
and of permanent erythropoiesis.
tive erythrocytes
production
Yolk sac stem cells
and may participate
of the first
definitive
give off primishortly
in the
erythrocytes.
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From www.bloodjournal.org by guest on June 18, 2017. For personal use only.
1982 59: 377-381
Erythropoiesis and lymphopoiesis in the chick yolk-sac-embryo chimeras:
contribution of yolk sac and intraembryonic stem cells
O Lassila, C Martin, P Toivanen and F Dieterlen-Lievre
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