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Distribution of extracellular matrix in the migratory pathway of avian primordial germ cells.

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Distribution of Extracellular Matrix in the Migratory
Pathway of Avian Primordial Germ Cells
Departments of Avian Science (L.E.U., U.K.A.) and Zoology (C.A.E.),
University of California, Davis, California 95616
The appearance and distribution of extracellular matrix (ECM)
was documented along the migratory route of chicken primordial germ cells
(PGCs). The antimouse embryonal carcinoma cell antibody, EMA-1, was used to
label PGCs (Urven et al.: Development 103:299-304, 1988). Antibodies against
laminin, fibronectin, chondroitin sulfate proteoglycan and collagen type IV were
used to label extracellular matrix components. When the PGCs emerged from the
epiblast, all four ECM molecules were restricted principally to the basement membrane of the epiblast. Chondroitin sulfate was also located between hypoblast cells
during this period. In late germinal crescent stages, when the PGCs entered the
lumina of blood vessels, the same ECM molecules were more widespread in the
mesoderm and in extracellular spaces. In addition, laminin and collagen type IV
were identified on lateral surfaces of ectodermal cells at this stage. When the germ
cells moved through the mesenchyme into the germinal ridge, the ECM molecules
were found around mesenchymal cells, and, in the cases of laminin, fibronectin and
collagen type IV, in the basement membranes of the germinal ridge epithelia.
Because the appearance of these ECM components is temporally and spatially
correlated with the movement of PGCs, we suggest that early PGC migration may
depend on their timely appearance.
The extracellular matrix (ECM) provides support; a
substratum against which cells can exert traction; and,
in some cases, directional cues to migrating cells
(Heasman and Wylie, 1981; Turner et al., 1983; Erickson, 1987; Hammarback, 1988). Embryonic systems
are particularly useful for studies of the role of the
ECM in cell migration. We have been especially interested in the control of primordial germ cell (PGC) migration.
PGCs are undifferentiated cells that ultimately give
rise to spermatogonia and oogonia. In vertebrates, they
originate outside the embryo proper and travel by various routes, depending on the species, to the developing
gonads. Avian PGCs serve as a good model for control
of embryonic cell migration for several reasons. In
birds, PGCs are easily identified on the basis of morphology, in conjunction with either histochemical
(Meyer, 1964) or immunological (Pardenaud et al.,
1987; Urven et al., 1988) markers. They migrate
through a variety of tissue types and display several
morphogenetic behaviors. PGCs initially appear in the
epiblast and invaginate into the blastocoel (EyalGiladi et al., 1981; Sutasurya et al., 1983; Ginsburg
and Eyal-Giladi, 1986; Pardenaud et al., 1987; Urven
et al., 1988). Later, as mesoderm invades the anterior
and lateral regions of the area pellucida, PGCs are located in the blastocoel, mesoderm and hypoblast of the
“germinal crescent.” They then enter the developing
extra-embryonic splanchnic blood vessels and are passively carried to the level of the germinal ridges (gonadal anlagen), where they leave the vasculature and
migrate actively through the intervening mesenchyme
0 1989 ALAN R. IJSS, INC
into the germinal ridge epithelium (Swift, 1914;
Meyer, 1964; Clawson and Domm, 1969; Fujimoto et
al., 1976). The germinal ridge is the sole migratory
target of PGCs, unlike neural crest cells or neurites,
which have multiple paths and numerous destinations.
ECM molecules found in the migratory pathway of
PGCs may act to control their migration. Fibronectin,
in particular, has been implicated in the control of PGC
migration in amphibians (Cathalot and Brustis, 1986;
Wylie and Heasman, 1982), birds (Critchley et al.,
1979; England, 19831, and mammals (Alvarez-Buylla
and Merchant-Larios, 1986; Donovan et al., 1987). Laminin has also been shown to aid in the adhesion of
mouse PGCs in vitro (Donovan et al., 1987), suggesting
that it may affect PGC migration, at least in mammals.
These and other ECM molecules have been suggested
to have roles in the migration of a variety of other cell
types as well. Fibronectin has been shown to affect adhesion and migration in vitro of selected cell lines
(Goodman and Newgreen, 19851, fibroblasts (Couchman et al., 1982,19831,neural crest cells (Newgreen et
al., 1982; Erickson and Turley, 1983; Rovasio et al.,
1983; Tucker and Erickson, 1984), involuting mesodermal cells (Boucat et al., 1984a,b), and myogenic cells
(Turner et al., 1983). Fibroblasts (Couchman et al.,
19831,neurite growth cones (Hammarback et al., 19881,
R e c e i v z e p t e m b e r 12, 1988; accepted October 31, 1988.
Address reprint requests to Lance E. Urven, Dept. of Population
Dynamics, The Johns Hopkins University School of Public Health,
615 N. Wolfe Street, Baltimore, MD, 21205.
TABLE 1. Antibodies used to identify extracellular matrix components in the
migratory pathways of avian primordial germ cells
PGC surface
Collagen type IV
Mouse IgM
Dr. E.M. Eddy
Goat IgG
Rabbit IgG
Rabbit IgG
Mouse IgM
Organon Teknika
Dr. H. Kleinman
Dr. H. Kleinman
neural crest cells (Rovasio et al., 1983; Bilozur and Hay, man of the National Institutes of Health, Bethesda,
19881, and a variety of epithelial and mesenchymal cell Maryland. The antifibronectin is commercially availlines (Goodman and Newgreen, 1985) have also been able (Organon Teknika, One Technology Court, Malshown to adhere to andor migrate on laminin in vitro. vern, PA, 19355) and was made in goat against human
Collagen type IV, adsorbed to culture plates, allows plasma fibronectin. The antichondroitin sulfate is a
attachment of fibroblasts (Murray et al., 19791, endo- commercial monoclonal antibody specific for the glythelial cells (Herbst et al., 19881,hepatocytes (Ruben et cosaminoglycan portion of native chondroitin sulfate
al., 1981), and some permanent cell lines (Aumailley proteoglycan (ICN Immunobiologicals, P.O. Box 1200,
and Timpl, 1986). Chondroitin sulfate, on the other Lisle, IL, 60532). Each slide was rinsed twice in PBS,
hand, has been shown to decrease cell adhesion in cul- washed for 10 minutes in 0.2 M glycine to quench
tures of neural crest cells (Newgreen et al., 1982; Erick- autofluorescence, rinsed again in PBS, and dipped in
son and Turley, 1983; Tucker and Erickson, 1984).
PBS with 2% bovine serum albumen. Primary antibodWe have examined chicken embryos for the presence ies were applied dropwise to the sections and allowed to
of laminin, fibronectin, collagen type IV, and chon- incubate for 1.5 to 2 hours in a humidified chamber,
droitin sulfate in the PGC migratory pathway. We followed by two rinses in PBS. The presence of primary
have first considered the location of specific ECM mol- antibody binding was indicated by secondary labeling
ecules at the onset of migration t o address the possi- using rhodamine isothiocyanate-conjugated antimouse
bility that PGC movement may await the presentation antibody (Organon Teknika) to indicate EMA-1, or
of suitable substrates. Secondly, we have determined fluorescein-conjugated secondary antibody directed
whether any particular components show differential against the appropriate immunoglobulin class (Ordistribution in the PGC pathway. Of the components ganon Teknika) to indicate the anti-ECM antibodies.
studied, only fibronectin has been previously examined Secondary antibodies were diluted 1 5 0 in PBS, applied
specifically with reference to the avian PGC migratory in the same manner as described above for primary
pathway (Critchley et al., 1979; Sanders, 1982; En- antibodies, and incubated for 30 minutes. Control sections were incubated in PBS in place of primary antigland, 1983; Fujimoto and Yoshinaga, 1986).
body to test for nonspecific binding of secondary antiMATERIALS AND METHODS
bodies and tissue autofluorescence. After rinsing twice
White leghorn chicken embryos were dissected from in PBS, slides were mounted in 2% n-propyl gallate in
the yolk after 1,2,3,4,and 5 days of incubation at 37°C glycerol (Giloh and Sedat, 1982), then studied and phoand 55% relative humidity. Each embryo was staged tographed with a Leitz Dialux 20 photomicroscope
according to the criteria of Hamburger and Hamilton equipped for epif luorescence.
(1951; referred to hereafter as H & H stages) and rinsed
thoroughly in phosphate-buffered saline (PBS) prior to
for 1 day (stages 4-6
fixation for 1hour with 4% paraformaldehyde in PBS.
Embryos were then washed three times in PBS before H & H), PGCs are the only EMA-1-positive cells vena 2-hour infiltration, first in PBS containing 15% su- tral to the EMA-1-positive epiblast (Fig. 1A). They are
crose, then in PBS containing 30% sucrose. Embryos distributed in the anterior half of the area pellucida in
were maintained on a revolving table during fixation,
rinses, and infiltrations to enhance penetration of solutions. Embryos were embedded in O.C.T. compound
(Miles Scientific Division, Miles Laboratories, Inc., C IV collagen type IV Abbreviations
30W475 North Aurora Road, Naperville, IL 60566) un- ce coelomic epithelium
Cs chondroitin sulfate
der liquid nitrogen, and stored at -30°C.
Serial sections were cut a t 12 pm with a Bright Cry- ec extra-embryonic ectoderm
ostat model OTF/AS/MR. Sections were either double- em
en endoderm
labeled or alternately labeled for PGCs using EMA-1 ep epiblast
antibody (Hahnel and Eddy, 1986; Urven et al., 19881, Fn fibronectin
generously donated by Dr. E.M. Eddy, and for extra- h hypoblast
Ln laminin
cellular matrix components using the antibodies listed m
in Table 1.Antilaminin and anticollagen type IV were me mesenchyme
made in rabbit and kindly provided by Dr. H. K. Klein- Schematic diagrams indicate the level of section for each figure.
Fig. 1 . Paraformaldehyde-fixed, frozen sections of gastrula stage (1-day, stage 4-6
H & H) chick embryos immunofluorescently labeled to indicate A) EMA-1-positive
PGCs (arrowheads) emerging from the EMA-1-positive epiblast; B) laminin distribution in the same section; C)fibronectin in a comparable section; D) collagen type IV in
a comparable section; E) chondroitin sulfate in a n adjacent section to that shown in A
and B. Scale bar = 50 fim.
TABLE 2. Immunofluorescent detection of ECM components in the early germinal
crescent of chicken embryos at 1 day of incubation (stages 4-6, Hamburger and
Hamilton, 1951)'
Collagen type IV
Chondroitin sulfate
+ + ,strong fluorescence; + , moderate or scattered fluorescence; -, no fluorescence above background.
TABLE 3. Immunofluorescent detection of ECM components in the late germinal
crescent of chicken embryos at two days of incubation (stages 9 to 10, Hamburger
and Hamilton, 1951)'
Collagen type IV
Chondroitin sulfate
+ + , strong fluorescence; + ,moderate or scattered fluorescence; -, no fluorescence above background.
TABLE 4. Immunofluorescent detection of ECM components in the germinal ridge
area of chicken embryos at three to five days of incubation (stages 15-26,
Hamburger and Hamilton, 1951)'
Collagen type IV
Chondroitin sulfate
Germinal ridge
basement membrane
Germinal ridge
+ + , strong fluorescence; + ,moderate or scattered fluorescence; -, no fluorescence above background.
the region called the germinal crescent (Swift, 1914).
At these stages, all four ECM components were found
principally in the basement membrane of the epiblast
(Fig. 1B-E; Table 2). With the exception of collagen
type IV, all these antibodies faintly labeled the surfaces of some scattered mesodermal cells. Chondroitin
sulfate was seen intermittently within the hypoblast.
When PGCs were entering or becoming trapped in
germinal crescent blood vessels in 2-day (stages 8-11
H & H) embryos (Fig. 2; Table 3),the ECM components
we examined became more widespread in the mesodermal mesenchyme. Laminin and collagen type IV were
present in the ectodermal basement membrane as well
as on the lateral surfaces of these cells. Some barely
detectable labeling occurred in the ectodermal basement membranes stained with antifibronectin and
antichondroitin sulfate antibodies. Laminin, collagen
type IV, and chondroitin sulfate were scattered on the
surfaces of some endoderm cells.
By the third day of incubation (stages 15-18 H & H),
PGCs were beginning to emerge from blood vessels of
the splanchnopleure and from the dorsal aorta at the
level of the germinal ridges. They then migrated
through the intervening mesenchyme and penetrated
the mesothelium near the coelomic angle (Fig. 3A). By
the fifth day of incubation (stages 25-26 H & H), many
of the PGCs have reached the germinal ridges.
Throughout this period, fibronectin and chondroitin
sulfate were seen in all mesenchyme a t the level of the
germinal ridge, including that near the germinal ridge
and in the mesentery (Fig. 3C,E; Table 4). Collagen
type IV and laminin were also present among mesenchyme cells, though a t a reduced level as compared
to that in basement membranes. Fibronectin, collagen
type IV, and laminin were found in the basement membranes of the germinal ridge epithelia. None of the antibodies labeled the apical or lateral surfaces of the
germinal ridge epithelium cells.
We have examined the distribution of laminin, fibronectin, collagen type IV, and chondroitin sulfate in the
pathway of migrating avian PGCs. All these ECM molecules have been implicated in adhesion and motility of
various other cell types. The fibronectin distribution
described here is similar to that seen in other studies of
the chick gastrula (Critchley et al., 1979;Sanders, 1982;
England, 1983). Fibronectin has previously been reported to disappear from the dorsal mesentery at stage
23 H & H, after PGC migration is complete (Fujimoto
and Yoshinaga, 1986). In our study, fibronectin could
still be found in this tissue as late as stage 26 H & H (5
days). This is the first report to describe the appearance
of laminin, collagen type IV, and chondroitin sulfate in
the PGC migratory route. All four ECM components
occurred in both the germinal crescent and near the
germinal ridge. Because the four are essentially codistributed spatially and temporally, any of them may
Fig. 2. Paraformaldehyde-fixed, frozen sections of late germinal crescent stage (2day, stage 8-11 H & H) chick embryos immunofluorescently labeled to indicate A)
EMA-I-positive PGC (arrowhead) in the endoderm; B) laminin distribution at the left
side of the section shown in A; C ) fibronectin in a comparable section; D) collagen type
IV in a comparable section; E) chondroitin sulfate in a n alternate section to that shown
in A and B. Scale bar=50 pm.
Fig. 3. Paraformaldehyde-fixed, frozen sections of germinal ridge stage (4-day, stage
20-22) chick embryos immunofluorescently labeled to indicate: A) PGCs (arrowheads)
in the germinal ridge epithelium; B) laminin distribution in the same section; C )
fibronectin in a comparable section; D) collagen type IV in a comparable section; E)
chondroitin sulfate in a n adjacent section to that shown in A and B. Scale bar = 50 pm.
have roles as specific substrata required for PGC migration in vivo. Even laminin and collagen type IV,
which are considered to be principally associated with
basement membranes (Kleinman et al., 19841, are
found to some extent among the mesenchyme in the
migratory pathway. If the presence of a n ECM component alone conferred directionality to PGCs, we would
expect to find one or more of them distributed strictly in
the migratory pathway. However, the four ECM components all occurred in mesenchyme of the sclerotome
and other areas outside of the migratory pathway a t the
level of the germinal ridges.
We have not addressed the possibility that quantitative differences in the concentration of ECM components may occur along the PGC migratory pathway. It
is possible that substrate concentration gradients may
give PGCs directional cues, in addition to the chemotactic guidance proposed by other investigators (Dubois,
1965; Dubois, 1968; Kuwana et al., 1986). In vitro experimental analysis of PGC behavior will be needed to
provide data addressing this question. Herbst et al.
(1988) demonstrated the feasibility of this approach in
their studies of endothelial cell movement on adsorbed
gradients of collagen type IV.
Our results indicate that PGC migration is coincident
with the appearance of at least four ECM molecules.
When PGCs first leave the epiblast, migration is limited
to some fairly restricted movement on the basement
membrane (Critchley et al., 1979; England, 1983) or the
hypoblast (Lee et al., 1978). Mesoderm and mesodermal
ECM are rare in the germinal crescent at this time.
When the PGCs are moving into the splanchnic blood
vessels, ECM becomes available throughout the mesenchyme as mesoderm and its associated ECM advance
into the region from the primitive streak. More ECM
becomes available between the epiblast and splanchnopleure when PGCs must move through the area to
enter the blood vasculature. ECM formation is temporally and spatially correlated with the migration of
PGCs, and its appearance may allow early PGC movement.
Similarly, at the end of the migratory pathway, ECM
is plentiful in basement membranes and among the
mesenchyme cells through which PGCs travel. ECM is
not seen between germinal ridge epithelium cells
where the PGCs ultimately settle. Again, active migration is correlated with the presence of ECM, whereas
presumably less motile PGCs in the germinal ridge
epithelium do not have access to ECM.
The migration of PGCs from the germinal crescent to
the germinal ridges is clearly correlated with the presence of laminin, fibronectin, collagen type IV, and chondroitin sulfate. These molecules are present outside the
PGC migratory pathway, as well, and therefore cannot
guide PGCs to the germinal ridge simply on the basis of
their presence or absence. Which, if any, of these ECM
components may be specifically required for PGC adhesion and locomotion remains to be investigated.
Based on present observations, however, it is likely that
the departure of the PGCs from the germinal ridge
requires the prior appearance of the ECM.
The authors wish to thank Dr. E.M. Eddy and Dr.
H.K. Kleinman for their penerous "
gifts of the EMA-1
and antilaminin and anticollagen type IV antibodies,
respectively. We greatly appreciate the advice and suggestions of Dr. J.R. McCarrey. This work was supported, in part, by a USDA Competitive Research grant
87-CRCR-1-2301 and by a n NIH Genetics Training
grant 5-T32-GM07467.
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