/ . Embryol. exp. Morph. Vol. 24, 3, pp. 497-509, 1970
Printed in Great Britain
497
The origin and movement
of prelung cells in the chick embryo as determined
by radioautographic mapping
By GLENN C. ROSENQUIST 1
From the Department of Pediatrics, The Johns Hopkins Hospital
SUMMARY
The origin of the prelung cells was determined by tracing the movements of [3H]thymidinelabelled grafts excised from medium-streak to 4-somite stage chick embryos and transplanted
to the epiblast, streak, and endoderm-mesoderm of similarly staged recipient embryos.
At the medium-streak stage the prelung endoderm cells are in the anterior third of the
primitive streak; they shortly begin to migrate anteriorly and laterally into the endoderm
layer. They are folded into the gut beginning at about the 4-somite stage, and begin to reach
their definitive position in the ventrolateral gut wall at the .10- to 16-somite stage. At the
± 22-somite stage the prelung endoderm begins to burrow into the overlying splanchnic layer
of mesoderm, pushing the prelung mesoderm ahead of it.
At the medium-streak stage the prelung mesoderm is in the epiblast (dorsal) layer about
half-way to the lateral margin of the area pellucida on either side of the streak, at a level
about half-way between the anterior and posterior ends of the streak. From this position the
prelung mesoderm migrates medially to the streak and is invaginated into the mesoderm
layer at a position about half-way between the anterior and posterior ends of the streak. As
a section of the dorsal mesentery, it migrates anteriorly and laterally from the streak into the
splanchnic mesoderm lateral to the somites. From the head process stage to the early somite
stages, the prelung mesoderm is located posterior to the prelung endoderm. The prelung
mesoderm continues to migrate with the splanchnic mesoderm into the mesentery dorsal to
the heart, where it invests the prelung endoderm after the 16- to 19-somite stage. Beginning
at about the 22-somite stage, the prelung endoderm penetrates the prelung mesoderm and the
bilateral bronchi are formed.
INTRODUCTION
The radioautographic mapping of the primitive-streak to head-process stage
chick embryo (Rosenquist, 1966) demonstrated that the endoderm which will
form the ventral side of the gut originates in the anterior end of the streak, while
the lateral plate mesoderm which covers the gut originates in the epiblast layer
lateral to the primitive streak. In this previous mapping study the differentiation
of the lung from these tissues was not described because embryos older than the
17-somite stage were not investigated.
The development of the lung in birds has been described by Locy & Larsell
(1916). The lung primordia develop when endoderm buds arising from the
1
Author's address: Cardiac Clinic, Children's Medical and Surgical Center, The Johns
Hopkins Hospital, Baltimore, Maryland 21205, U.S.A.
498
G. C. ROSENQUIST
ventral wall of the gut burrow into the adjacent splanchnic mesoderm and
extend ventrally, laterally and posteriorly from their point of origin into the
coelomic space dorsal to the heart (Figs. 1J, 3J). Using radioautographic
analysis, the present investigation traces the movements of [3H]thymidinelabelled transplants from their original positions in the epiblast and streak of
recipient embryos into the lung buds of these embryos.
MATERIALS AND METHODS
The methods of staging and preparation of recipient and [3H]thymidinelabelled donor embryos and of transplantation and radioautographic analysis
of the grafts were identical to those described in a previous publication (Rosenquist, 1970), and the description will not be repeated here.
Although part of each of the forty transplants illustrated in Figs. 1 and 3 lay
in the prelung region, the number of embryos investigated was relatively small,
and each transplant contained cells other than prelung cells (as indicated in
Table 1). Therefore the positions of the transplants at each stage in Figs. 1 and 3
suggest the location of the prelung region at that stage, but do not define it
precisely. The mapping of the prelung region is based upon the following
assumptions: (1) that previous studies have established the general position of
the endoderm which will form the gut and the lateral plate mesoderm in the
early stages of development without mapping every part of these tissues at each
stage (Rosenquist, 1966). Consequently, a small number of transplants, carefully placed, can demonstrate the position of more specific portions of the
embryo, such as the lung. (2) That graft positions in different embryos at the
same stage are homologous even if the embryos were incubated for different
lengths of time, and that the pathways followed by more than one accurately
placed graft can be used to follow movements of a group of cells through several
stages of development. (3) That maps of presumptive organ-forming regions of
the embryo are valid even if structures other than lung buds in the recipient
embryos contain labelled cells.
Throughout the text and figures, an asterisk (*) after the embryo number
indicates that the position shown is that of the graft after its migration in the
host embryo.
RESULTS
Prelung endoderm
At the medium-streak stage the presumptive prelung endoderm cells were in
the anterior third of the primitive streak, as illustrated by the migration of the
grafts in embryos 1 and 2 (Table 1, Fig. 1 A). At the late medium-streak stage
there were still some prelung cells in the streak, but some also were found in the
endoderm layer anterior and lateral to the anterior end of the streak (embryos
3-5, Table 1, Fig. IB). At the definitive-streak stage some of the prelung
endoderm remained clustered around the anterior end of the streak (embryos
Origin ofprelung cells
499
Table 1. Position of labelled cells in recipient embryos carrying tritiated thymidinelabelled grafts*
Embryo Stage Incuno. grafted batedj
(h)
1
2
3
4
5
6
7
8
9
10
II
12
.13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
MS
MS
LMS
LMS
LMS
DS
DS
HP
HP
HP
10
28
24
10
23
45
10
18
5
7
HP
HP
HP
HP
HP
HP
HE
HE
25
MS
MS
LMS
LMS
LMS
LMS
4
24
28
66
36
45
53
39
88
35
7
17
24
13
36
DS
4
DS
HP
HP
HP
HP
HP
HP
HP
HP
HP
HF
35
25
19
4
7
58
72
14
25
9
17
29
66
78
35
66
86
Stage
fixed
DS
95
10 5
HP
HP
±22 5
HF
10 5
15
45
HF
16 5
185
±22 5
±22 5
±22 5
±22 5
±22 5
ELB
15 5
DS
15
10 5
HF
17 5
HP
85
HF
IS
±22 5
ELB
IS
16 5
25
10 5
165
ELB
ELB
±22 5
±22 5
Position of labelled cells
£7V in and near 5/
Ventrolateral gut and YS EN; head M, notochord
Ventrolateral gut, dorsal gut, and YS EN
EN in and near 5/; M near St
EN anterolateral to 5/
Ventrolateral gut EN; LP M
EN anterolateral to 5/
Ventrolateral gut EN; nephrotomal M
EN, M anterolateral to 5/
YS and ventrolateral gut EN; paraxial and nephrotomal
M
EN, M anterolateral to 5/
YS and ventrolateral gut EN; paraxial and LP M
YS and ventrolateral gut EN; paraxial and LP M
Ventrolateral gut EN; LP M
YS and ventrolateral gut EN; paraxial and LP M
YS and ventrolateral gut EN; paraxial and LP M
YS and ventrolateral gut EN; paraxial and LP M
YS and ventrolateral gut EN; paraxial and LP M
YS and ventrolateral gut EN; paraxial and LP M
Paraxial and LP M
M in and near St
LP M anterolateral to 5/
Paraxial and LP M
LP M anterolateral to 5/; EN in and near 5/
LP M
LP M lateral to 5/; EN in and near St
Paraxial and LP M
LP M anterolateral to 5/; EN near St
LP M anterolateral to St; EN near 5/
LP M; YS EN
LPM; YS EN
LP M; YS EN
LPM; YS EN
LP M; YS EN
LPM; YS EN
LP M; YS EN
LP M; dorsal gut and 75 EN
LPM; YS EN
LP M; dorsal gut EN
LP M; dorsal gut EN
* Key to abbreviations: DS, definitive-streak stage; ELB, early limb-bud stage; EN,
endoderm; HE, head-fold stage; HP, head-process stage; LMS, late medium-streak stage;
LP, lateral plate; M, mesoderm; MS, medium-streak stage; 5, somite; 5/, streak; YS,
yolk sac.
t Hours of incubation after placement of the graft.
500
G. C. ROSENQUIST
1*, 6, 7, Table 1, Fig. 1C). At the head-process stage (embryos 4*, 5*, 8-16,
Table 1, Fig. 1D) the prelung endoderm had migrated away from the streak into
the zone of endoderm which is destined for the ventrolateral wall of the gut
(Fig. 5, left). By the head-fold to 1-somite stage, the prelung cells had moved
away from the anterior end of the streak, either by actual migration in an
anterior direction or as a result of the posterior regression of the streak. The
transplants in embryos 7*, 9*, 11*, 17 and 18 (Table 1, Fig. IE) were located
DS
"••»..
LMS
•
HF-1 S
Jmr
•••
..••••"
ft
HP
9-10 S
2-4 S
1
ft '
l\ W10*
Fig. 1. The location of grafts from embryos 1-19 is shown. At the medium-streak
(MS) stage, the prelung endoderm (contained in the shaded areas which represent
the endodermal part of each graft) is located in the anterior part of the streak. It
migrates from the streak, beginning at about the late medium-streak (LMS) stage.
By the head-process (HP) stage, the prelung endoderm has moved into area pellucida
about half-way between the lateral margin and the streak, extending a short distance
anteriorly from the anterior end of the streak (see also Fig. 5, left) into the endodermal region destined for the ventral wall of the gut. From the head-fold (HF) to
the 16- to 18-somite (16-18 S) stage the prelung endoderm moves progressively
closer to the anterior intestinal portal (E, F) and is invaginated into the ventrolateral
gut wall dorsal to the heart (G, H). At the ± 22-somite stage, the prelung endoderm
begins to burrow into the overlying prelung mesoderm. The beginnings of bronchus
formation are noted at the early limb-bud (ELB) stage.
As in the text, an asterisk (*) after the embryo number indicates that the position
shown is that of the graft after its migration in the host embryo. Each graft is
therefore shown in two positions: immediately after it was placed, and after
incubation. DS = definitive-streak stage.
7*
Origin ofprelung cells
Fig. 2. (A) Cross-section (x 200) showing labelled cells (black dots over nuclei) from
a graft placed originally in the endoderm-mesoderm layer of a 2-somite stage
recipient embryo. The labelled endoderm in the graft has migrated from its original
position lateral and slightly posterior to the anterior intestinal portal (embryo 19,
Fig. 1F) into the ventrolateral wall of the gut at the early limb-bud stage, where
some of the cells have formed part of the wall of the lung bud (embryo 19*, Table 1,
Fig. U). (B) Cross-section (x200) showing labelled cells from a graft placed
originally in the endoderm-mesoderm layer of a head-fold stage recipient embryo.
The labelled mesoderm in the graft has migrated from its original position slightly
lateral and anterior to the anterior end of the streak (embryo 37, Fig. 3E) into the
proximal part of the splanchnic layer of the lateral plate mesoderm, and has
invested the unlabelled lung bud on the right side of the embryo (embryo 37*,
Table 1, Fig. 3J).
501
502
G. C. ROSENQUIST
between the head-fold and streak, but like the transplants at the 2- to 4-somite
stage they had not as yet been invaginated into the gut (embryos 10*, 19,
Table 1, Fig. IF).
In contrast, at the 9- to 10-somite stage the grafts in embryos 2*, 3* and 8*
(Table 1, Fig. 1G) had been partially folded into the gut. By the 16- to 18-somite
stage most of the prelung endoderm had been invaginated into the gut, where it
comprised the ventrolateral wall (embryos 12*, 13*, Table 1, Fig. 1H). At the
± 22-somite stage all of the prelung endoderm had been inverted from yolk sac
to ventrolateral gut wall. The gut had been invested by the layer of splanchnic
mesoderm which was the dorsal mesoderm of the heart prior to its looping. In
embryos 6* and 14*—18* (Fig. II) there were bilateral bulges on the anterolateral wall of the gut which were the beginnings of bronchus formation. The
labelled grafts participated in the development; however, in none of these
embryos had these bulges branched to form bronchi at the time the embryo was
fixed. At the early limb-bud stage bronchi had begun to form, as the prelung
endoderm burrowed into the splanchnic mesoderm (embryo 19*, Table 1,
Figs. U, 2 A).
Prelung mesoderm
At the medium-streak stage the presumptive prelung mesoderm was in the
epiblast layer at a level about one-third to one-half the distance from the anterior to the posterior end of the streak and about half-way between the streak
and the lateral margin of the area pellucida (embryos 20 and 21, Table 1,
Fig. 3 A). At the late medium-streak stage, prelung mesoderm was found at a
level approximately one-third to one-half the distance between the anterior and
posterior ends of the streak, either in the streak or in the adjacent epiblast
(embryos 22-25, Table 1, Fig. 3B). At the definitive-streak stage, the prelung
mesoderm had begun to migrate through the streak into mesoderm (embryo 26,
Table 1, Fig. 3C), although some was still found in the streak and adjacent
epiblast (embryos 21*, 27, Table 1, Fig. 3C). By the head-process stage, the
prelung mesoderm had migrated away from the streak into the mesoderm
destined for the part of the lateral plate between the nephrotome and the heartforming region (embryos 26* and 28-36, Table 1, Fig. 3D). At the head-fold to
1-somite stage, the prelung mesoderm was located even farther from the streak,
but posterior to the prelung endoderm (compare embryos 22*, 24*, 28* and 37,
Table 1, Fig. 3E, with embryos 7*, 9*, 11*, 17 and 18, Table 1, Fig. IE). At the
2- to 3-somite stage, the prelung mesoderm was in the mesoderm layer lateral
to the streak and slightly posterior to the last somite, i.e. in the part of the
mesoderm layer which would form the most medial part of the lateral plate
(embryos 29*, 34*, 38-40, Table 1, Fig. 3F). At the 7- to 10-somite stage the
prelung mesoderm had migrated anteriorly into the splanchnic mesoderm dorsal
to the sinus venosus (embryos 23*, 27*, 32*, 35*, Table 1, Fig. 3G). By the 15to 17-somite stage the prelung mesoderm in the dorsal mesentery had begun to
Origin of prelung cells
503
adhere more closely to the ventral wall of the gut, from its lateral margin to the
ventral midline (embryos 20*, 25*, 33*, 36*, Table 1, Fig. 3H). By the ±22somite stage this section of the splanchnic mesoderm clung closely to the
bilaterally bulging endodermal lung buds at the ventrolateral side of the gut, as
illustrated in embryos 30*, 39* and 40* (Table 1, Fig. 31). At the early limb-bud
stage the prelung mesoderm had been further displaced by the burrowing tips
of the endodermal lung buds which had sprouted from the anterolateral gut wall
(embryos 31*, 37*, 38*, Table 1, Figs. 3J, 2B).
DS
LMS
20
HP
HF-1S
24
23
\ 22
7-10 S
15-17S
Fig. 3. The location of grafts from embryos 20-40 is shown. At the medium-streak
(MS) stage the prelung mesoderm (contained in the shaded areas which represent
the mesodermal part of each graft) is located in the epiblast layer (left half of each
figure). It migrates progressively toward the streak, which it reaches at about the
late medium-streak (LMS) stage. By the definitive-streak (DS) stage, some of the
prelung mesoderm has migrated through the streak into the lateral plate mesoderm
(right half of each figure), reaching a position anterior to the anterior end of the
streak some time after the head-process (HP) stage. As part of the most proximal
lateral plate mesoderm (i.e. that which is adjacent to the nephrotome), it moves
progressively toward the anterior intestinal portal, and is folded with the splanchnic
layer to the midline of the embryo ventral to the gut, where by the 15- to 17-somite
(15-17 S) stage, it has begun to invest the ventral wall of the gut. By the 22-somite
stage the bulging anteroventral wall of the gut has begun to penetrate the prelung
mesoderm; the latter invests the bronchi on each side of the embryo by the early
limb-bud(£Zi?) stage. As in Fig. 1, each graft is shown in two positions: immediately
after it was placed, and after incubation (marked with an asterisk). HF = headfold stage.
32
E M B 24
504
G. C. ROSENQUIST
DISCUSSION
Previous attempts to locate the presumptive pulmonogenic regions of the
chick embryo utilized the technique of transplanting fragments cut from donor
embryos of primitive-streak to head-fold stages to the chorioallantoic membranes of host embryos, where differentiation of the fragments was observed
after 7-9 additional days of incubation. Using this method of culture, Willier &
Rawles (1931) and Hunt (1934) first noted that respiratory epithelium may
differentiate from full-thickness (epiblast and hypoblast) grafts removed from
definitive-streak and head-process-stage embryos. Rudnick (1933) systematically
probed the potencies of anterior versus posterior, and lateral versus medial
fragments in the definitive-streak and head-process-stage embryo, noting that
pseudostratified epithelium of the respiratory type (without bronchi) was
present in all fragments while trachea was present in all parts of the blastoderm
tested except the midline of the embryo posterior to the anterior end of the
streak (Fig. 4A. C). Unexplained was (1) the finding that the lung cells would
not differentiate into bronchi unless the cultures were made from fragments
which contained the rudimentary lung buds (i.e. cut from 3 to 4-day-old donor
embryos), and (2) the presence of pretracheal cells in the midline fragment
anterior to the streak. It had been supposed previously that this region of
endoderm anterior to the streak was destined for the dorsal gut, and the trachea
was known to develop from a groove along the ventral wall of the gut. The
mapping of the head-process-stage blastoderm by Rawles (1936) gave essentially
the same results as those of Rudnick (Fig. 4E), except those at the level slightly
caudal to the anterior end of the streak. Rawles found respiratory tract cells in
the right- but not in the left-hand fragment, a finding which she ascribed to
right-sided dominance.
Hunt (1937) also found a widespread potential for development of respiratory
epithelium anterior to the anterior end of the streak, but found it in the mesectoderm (epiblast) rather than in the mesentoderm (hypoblast), except possibly at
the definitive-streak and head-process stages (Fig. 4B, D). Since it had already
been established that the lung forms from an endodermal bud which burrows
into a mesodermal sheath, Hunt's finding of presumptive respiratory tube
material in mesectoderm rather than in mesentoderm suggested that the endoderm and/or mesoderm cells which would form the lung were still in the epiblast
layer at stages prior to definitive streak, and possibly later as well.
In radioautographic mapping studies which utilized [3H]thymidine-labelled
grafts, Rosenquist (1964, 1965, 1966) confirmed the work of Hunt (1937),
demonstrating that in the chick embryo (1) the hypoblast layer lateral and
anterior to the streak contains no pregut endoderm at the early streak stages,
and (2) beginning at about the medium-streak stage, the pregut endoderm
migrates in an anterior and lateral direction from the anterior portion of the
streak. Additional workers have independently come to this conclusion (Modak,
Origin ofprelung cells
505
1965; Nicolet, 1965; Gallera & Nicolet, 1969). Furthermore, it is now known
that by the head-process stage these pregut cells have moved into a semicircular
zone of endoderm which extends across the midline of the area pellucida anterior
and lateral to the anterior end of the streak (Fig. 5, left). This semicircular zone
is divided into two parts: an inner semicircular zone which will form the dorsal
wall of the gut and an outer crescent-shaped zone destined for the ventral wall
of the gut. The gut is formed (1) by anteroposterior elongation of the dorsal gut
zone, and (2) by inversion (invagination) of the ventral gut zone at the anterior
DS
/'r
c
D
/
(
/
E
\
;
J
I
HP
HP
i
i
A
i
HP
Fig. 4. Hatched regions in each figure represent prelung material identified by
previous investigators using grafts to chorioallantoic membrane. A and C, Rudnick
(1933); B and D, Hunt (1937); E, Rawles (1936). (White area, C, was not tested.)
The position of the presumptive prelung material shown here is consistent with the
findings of the present study; however, these previous investigators used very large
grafts and did not distinguish between the prelung cells of the epiblast and those
of the hypoblast. Their experiments were therefore unsuitable for detailed tracing
of the morphogenetic movements of the pulmonogenic cells. DS = definitive-streak
stage; HP = head-process stage.
32-2
506
G. C. ROSENQUIST
intestinal portal (Rosenquist, 1966). The present study shows that the prelung
region at the posterior ends of the crescent (Figs. 1D, 5, left) is inverted and
compressed into bilateral sites along the ventral wall of the gut (Figs. II, J; 5,
Fig. 5. At the head-process stage {HP, left) most of the prelung endoderm (broken
cross-hatching) is located at the posterior ends of the crescent-shaped region which
has invaginated into the ventral gut by the 16-somite stage (Rosenquist, 1966; 16 S
right). Solid cross-hatching lateral and posterior to the crescent (left) represents
prelung endoderm (see also Fig. 1D) located in the yolk-sac surface near the
anterior intestinal portal at the 16-somite stage (right); the present study suggests
that this material is inverted into the prelung portion of the gut after the 16-somite
stage. In right and left drawings the line A B CB'A' represents the boundary between
endoderm cells destined for yolk sac and ventral gut, while the line ADEFE'D' A'
represents the boundary between endoderm cells destined for ventral and dorsal
gut. By the 16-somite stage (right) all of the endoderm cells along the line ABCB' A'
have converged to form the lip of the anterior intestinal portal; the material inside
the crescent (left) has been inverted and compressed to form the thickened ventral
wall of the gut. Thus, the triangular zones of prelung endoderm A BD and A'B' D'
(left) have inverted to form the triangles ADB and A'D'B' (right). The crosssection through the gut at the level of D and D' (center) illustrates the position of
the prelung endoderm (cross-hatching) along the ventrolateral wall of the gut (see
also Fig. 1H). The three figures are drawn to scale.
Origin of prelung cells
507
center, right). Since the prelung endoderm does not complete these movements
until after the 16- to 19-somite stage, intimate contact between prelung endoderm and prelung mesoderm does not occur until about the third day of incubation. This probably explains why histologically and morphologically normal
lung tissue did not differentiate from chorioallantoic membrane grafts unless the
fragments were cut from the donor embryos after the lung buds had formed
(third or fourth day of incubation, Rudnick, 1933). This delay in contact between prelung endoderm and prelung mesoderm may also explain why the
fragments of definitive-streak and head-process stage embryos formed meandering respiratory tubes (but not lung) in chorioallantoic membrane cultures
(Rudnick, 1933); the prelung endoderm from the posterior ends of the crescent
may have burrowed into the non-specific mesoderm with which it came into
contact in culture, rather than into the prelung mesoderm, from which it was
separated.
Still unexplained is the finding that histologically and morphologically normal
trachea will differentiate from blastoderm fragments transplanted to chorioallantoic membrane cultures at the definitive-streak and head-process stages,
when bronchi will not (Rudnick, 1933). Radioautographic mapping of the
pregut regions of the embryo (Rosenquist, 1966) has determined that the
endoderm in the midline (between points C and F, Fig. 5) is inverted and compressed into the ventral midline of the gut between the anterior intestinal portal
and the future stoma (the site of the future trachea). It may be that trachea
differentiated in Rudnick's cultures either because the pretracheal endoderm
was isolated with the pretracheal mesoderm, or because pretracheal endoderm
did not require an organ-specific mantle of mesoderm for differentiation.
Neither the present nor previous radioautographic studies has explained why
respiratory tubules differentiated from mesectoderm anterior to the anterior end
of the streak in Hunt's chorioallantoic membrane cultures of head-process stage
blastoderm fragments. Previous mapping of the head-process stage embryo has
indicated there are no pre-endoderm cells in epiblast anterior to the streak at
this stage (Rosenquist, 1966). However, it may be speculated that a few prelung
endoderm cells adhered to the mesectoderm layer in Hunt's fragments, or that
the prelung mesoderm contained in such fragments was able to induce adjacent
epithelium (in this case, ectoderm) to form respiratory tubules.
In future research it should be possible to segregate the prelung endoderm
from the prelung mesoderm in vitro, so that their developmental potential may
be studied prior to the formation of the lung. Such research also might offer
insight into abnormal lung development, as well as reawakening interest in the
early development of organs which arise from endoderm destined for other
parts of the digestive system.
508
G. C. ROSENQUIST
RESUME
Mise en evidence, par marquage radioautographique, de Vorigine et des mouvements des cellules presomptives de Vebauche pulmonaire dans Vembryon
de poulet
L'origine des cellules constituant Pebauche presomptive pulmonaire a ete determined en
suivant les mouvements de greffes marquees a la [3H]thymidine, excisees a des stades s'etendant de la ligne primitive moyenne a celui de 4 somites et transplanted ensuite dans M'epiblaste'
(ectophylle), la ligne primitive et Pendoderme-mesoderme d'embryons recepteurs du stade
correspondant.
Au stade de la ligne primitive moyenne les cellules endodermiques correspondant au
poumon se trouvent dans le tiers anterieur de la ligne primitive; rapidement elles se mettent
a migrer vers l'avant et le dehors au sein du feuillet endodermique. Elles se replient dans
l'ebauche de l'enteron vers le stade a 4 somites et commencent a atteindre leur position
definitive dans la paroi enterique ventro-laterale aux stades de 10 a 16 somites. Au stade de
plus ou moins 22 somites, l'ebauche presomptive du poumon commence a creuser la couche
splanchnique du mesoderme qui la recouvre, repoussant ainsi le mesoderme presomptif du
poumon.
Au stade de la ligne primitive moyenne le mesoderme presomptif du poumon se trouve
dans la couche (dorsale) de Pepiblaste (ectophylle), a peu pres a mi-chemin entre la limite
laterale de l'area pellucida de chaque cote de la ligne primitive, a un niveau situe a mi-chemin
entre les extremites anterieure et posterieure de la ligne. A partir de cette position, l'ebauche
mesodermique presomptive du poumon se deplace vers le dedans jusqu'a la ligne primitive
et est invaginee dans le feuillet mesodermique a mi-hauteur de la ligne primitive. En tant que
partie du mesentere dorsal, elle emigre vers l'avant et les cotes dans le mesoderme splanchnique
en dehors des somites. Depuis le stade du prolongement cephalique jusqu'a celui des premiers
somites, l'ebauche mesodermique presomptive du poumon est situee en arriere de Pendodermique. Cette ebauche mesodermique continue a migrer avec Pensemble du mesodermique
splanchnique vers le mesentere situe dorsalement par rapport au coeur ou il entoure l'ebauche
endodermique apres le stade du 16e au 19e somite. Commencant a le faire au stade de 22
somites, Pendoderme pre-pulmonaire penetre dans le mesoderme correspondant et y forme
les bronches bilaterales.
This investigation was supported by USPHS research grants HE 10191 and K3 HE 20074
from the National Heart Institute. The author wishes to thank James D. Ebert for his
continued interest in this research, and Soame D. Christianson for help in the preparation
of the manuscript.
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{Manuscript received 10 March 1970)