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Distribution and characterization of anionic sites in trophoblast and capillary basal laminas of human placental villi.

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Distribution and Characterization of Anionic Sites in
Trophoblast and Capillary Basal Laminas of Human
Placental Villi
Department of Human Anatomy, School of Medicine, Uniuersity o f California, Dauis,
CA 95616
The distribution of anionic sites was studied in the trophoblastic
and fetal capillary basal laminas of developing human placental villi with the
cationic stain ruthenium red. At 7-12 weeks of gestation the trophoblastic basal
lamina (TBL) contained ruthenium red-positive granules in a quasi-regular array
throughout the lamina densa or sometimes concentrated a t the interstitial surface
of the lamina densa. The capillary basal lamina (CBL) (and anionic sites) were not
present a t this age. Anionic sites were also associated with collagen or reticular
fibrils. At term, the TBL was largely devoid of anionic sites except for some distributed along its interstitial surface. The CBL was present in later gestation and
sometimes had arrays of anionic sites. In order to characterize the anionic sites,
minced pieces of villi were incubated in the presence or absence of either chondroitinase ABC, heparitinase, neuraminidase, or Streptomyces hyaluronidase in appropriate buffer systems. Incubation of early villi with heparitinase resulted in the
disappearance of the TBL-associated sites. Chondroitinase ABC appeared to reduce
staining of collagen-associated sites. In term villi, heparitinase removed those few
sites still associated with the TBL but did not affect sites associated with the CBL
or collagen. Chondroitinase ABC resulted in the disappearance of all anionic sites.
In later gestation, a number of developmentally important macromolecules are
transported across the trophoblast and enter the fetal capillaries. We conclude that
the absence of a n array of polyanionic sites from the term placenta TBL and the
reduction in the amount of extracellular matrix intervening between the trophoblast
and capillaries are adaptations to enhance the exchange of macromolecules across
the placenta.
Basal laminas are sheets of extracellular matrix materials that characteristically underlie epithelia and endothelia and envelop certain other cell types (e.g., smooth
muscle, fat) (Vracko, 1974). Biochemical studies of certain basal laminas have shown that they are composed
of a variety of collagenous and noncollagenous glycoproteins and proteoglycans (Szarfman et al., 1982).For most
tissues the function of the basal laminas is incompletely
understood. They are generally thought to provide structural support and compartmentalization of tissues, and
to serve as a substrate for the attachment of epithelial
or endothelial cells (Vracko, 1974). They also appear to
have important roles in morphogenesis by virtue of their
position at the interface of epithelia and mesenchyme
(Toole, 1981; Sanders, 1983). Another function that has
been established for certain basal laminas is to act as a
size- and charge-selective barrier to macromolecules.
This function has been extensively studied in glomerular basement membrane (Farquhar et al., 1982) and has
been proposed to function similarly in certain capillaries
(Charonis and Wissig, 1983). The charge-selective barrier is attributable to an array of polyanionic proteoglycans associated with the basal lamina (Kanwar and
Farquhar, 1979).
0 1985 ALAN R. LISS, INC.
Human placental villi are covered by a layer of trophoblastic epithelium that is separated from the connective tissue core of the villus by a relatively thick basal
lamina. The connective tissue core contains, among other
things, the developing fetal capillary bed. During the
latter part of gestation the fetal endothelial cells are
associated with a thin basal lamina. During this same
period, certain maternal serum proteins, most notably
IgG, are endocytosed by trophoblast and transported to
the fetal circulation (King, 1982).In fact, fetal IgG levels
may exceed maternal serum levels (Kohler and Farr,
1966).This observation suggested to us that, unlike glomerular basement membrane, the basal laminas in placental villi may be specially adapted to permit the
passage of macromolecules. As a first step toward determining this, we have examined developing placental
villi for the presence and distribution of anionic sites in
trophoblastic and capillary basal laminas.
Received August 15,1984;accepted December 5, 1984
lar and interstitial surfaces of the lamina densa (Fig. 6).
Other ruthenium red-positive sites were associated with
interstitial collagen or reticular fibrils (Fig. 2).
Incubation of minced villi in the presence of heparitinase removed most of the anionic sites associated with
the TBL but had no effect on sites associated with the
collagen fibrils (Fig. 3). Control specimens incubated
under identical conditions, but in the absence of hepariRuthenium Red Staining
tinase, always had stained sites (Fig. 4). Incubation of
In order to determine if anionic sites were present in villi in the presence of chondroitinase ABC resulted in
the basal laminas of trophoblast and fetal capillaries, reduced staining of anionic sites associated with intersome pieces of villi were immersed in a solution of 1% stitial collagen fibrils, but it had no effect on anionic
ruthenium red (Polysciences, Inc., Warrington, PA) in sites associated with the TBL (Fig. 5 ) .Control specimens
McIlvane’s citrate-phosphate buffer (pH 5.6) with or incubated identically, but in the absence of chondroitiwithout 0.2-1.0% Triton X-100 for 1hr at 22°C (Vaccaro nase ABC, showed a typical staining pattern (Fig. 6).
and Brody, 1981). As noted by Vaccaro and Brody, the Incubation in the presence of hyaluronidase or neuraTriton damages the cells but allows the ruthenium red minidase had no apparent effect on staining.
to penetrate and stain the basal lamina- and collagenTerm Villi
associated proteoglycans. Tissue was then fixed overIn
normal term placentas in which
night in 5% glutaraldehyde in citrate-phosphate buffer
red was added to the
containing 1% ruthenium red. The next day the tissue
was washed three times in buffer containing ruthenium fixatives, the TBL was still finely fibrillar and of unired and post fixed in 1%osmium tetroxide containing form density, but it had increased in thickness compared
0.75% ruthenium red. Tissue was then dehydrated in a to early villi (Fig. 7). In addition, the fetal capillaries
series of acetones and embedded in an Epon-araldite were now surrounded by a distinct basal lamina (CBL)
epoxy resin mixture. Thin sections were cut on an ul- (Fig. 7). In villi treated with ruthenium red and Triton
tramicrotome and subsequently stained with lead cit- X-100, anionic sites were absent from the TBL except
rate and uranyl acetate. Sections were examined in a for occasional sites associated with the interstitial side
of the lamina densa (Figs. 8-10]. Anionic sites were
Philips 400 electron microscope.
usually associated with the fetal capillary lamina densa
(Figs. 8, 10) and with interstitial collagen fibrils (Figs.
Enzymatic Digestions
To demonstrate the nature of the anionic sites, minced 9, 10).In some cases, it was difficult to detect ruthenium
pieces of villi were incubated for 45 min a t 37°C with red-positive sites in either lamina densa even though
one of the following enzymes: chondroitinase ABC (Miles nearby collagen fibril-associated sites did stain (Fig. 9).
Incubation of minced term villi in the presence of
Laboratories, Kankakee, lL)1unit/ml in 0.1 M Tris-HC1
removed those few anionic sites associated
buffer, pH 8.0, + 0.1 M NaC1; Streptomyces hyaluronidase (Miles) 100 unitdm1 in 0.1 M acetate buffer, pH 6.0; with the interstitial surface of the TBL, but it had little
heparitinase (Miles) 3 unitsiml in phosphate-buffered effect on staining of collagen and CBL anionic sites (Fig.
saline, pH 7.3; neuraminidase (Worthington Diagnostic 11). Control specimens had a typical staining pattern
Systems, Freehold, NJ) 1unit/ml in 0.1 M acetate buffer, (Fig. 12). Villi incubated in the presence of chondroitipH 5.4,+ 0.1 M NaC1. Controls lacking the enzymes nase ABC showed no staining of TBL, CBL, or collagenwere processed identically. After incubation, the tissue associated sites (Fig. 13).Control villi, incubated identiwas fixed in 5% glutaraldehyde in citrate-phosphate cally but in the absence of the enzyme, had a typical
buffer containing 1% ruthenium red and subsequently staining pattern (Fig. 14). Incubation of villi in the presence of hyaluronidase or neuraminidase did not appear
processed as previously described.
affect the anionic sites demonstrable with ruthenium
For comparison, some villi were fixed in 3% glutaraldehyde in 0.1 M cacodylate-HC1 buffer with 1%w/v red.
tannic acid added immediately before use. Tissue was
subsequently washed in buffer, postfixed in 0 ~ 0 4 and
processed as previously described.
Proteoglycans (PGs) are recognized as common components of basement membranes, although the glycosaRESULTS
minoglycan (GAG) composition and arrangement vary
Early Villi
from tissue to tissue (Hay, 1981;Toole, 1981; Timpl and
In placental villi from early pregnancies (7-12 weeks) Martin, 1982; Charonis and Wissig, 1983). Anionic sites
in which tannic acid (but not ruthenium red) was added have been localized in the basal laminas of several emto the fixative, the trophoblastic basal lamina (TBL) bryonic epithelia (Trelstad et al., 1974; Hay and Meier,
underlying the cyto- and syncytiotrophoblast has a finely 1974; Hay, 1978; Reeves et al., 1980; Meyer et al., 1981;
fibrillar, uniform density (Fig. 1).The fetal capillaries Grant et al., 1983). The anionic sites are about 10-20
a t this stage were often at some distance from the base nm in diameter and tend to occur in a quasi-regular
of the trophoblast. Even when the capillaries were more array on both sides of the lamina densa. In most cases
closely associated with the trophoblast, a basal lamina the PG is predominantly chondroitin sulfate or heparan
was usually absent around the endothelial cells (Fig. 1). sulfate (Toole, 1981; Hay, 1981); sometimes hyaluronate
In villi treated with ruthenium red, electron-dense, and chondroitin sulfate predominate (Cohn et al., 1977).
ruthenium red-positive sites were distributed throughAnionic sites have also been demonstrated in the basal
out the thickness of the lamina densa of the TBL (Fig. lamina of a variety of adult epithelia (Katsuyama et al.,
2) or sometimes were associated mainly with the cellu- 1977; Kanwar and Farquhar, 1979; Gordon and BernPlacentas from five early pregnancies (7-12 weeks)
and five term pregnancies were collected immediately.
Small pieces of placental villi were rinsed briefly in
Earle’s balanced salt solution to remove maternal blood
and processed in several ways, basically following the
techniques of Vaccaro and Brody (1979, 1981).
Fig. 1. Low-magnification micrograph of trophoblast and fetal capillary wall at 10 weeks gestation. No ruthenium red treatment. Trophoblast (TI has a thick basal lamina (TBL). The fetal endothelium (FE)
does not have a basal lamina at this age. x 18,400.
removed, although large granules deeper in the extracellular matrix
are stained. ~ 5 7 , 0 0 0 .
Fig. 4. TBL region, early placenta, control for heparitinase treatment. Anionic sites are associated with the TBL and collagen. ~57,000.
Fig. 2. Trophoblastic basal lamina (TBL) from early placenta after
Triton permeabilization and ruthenium red staining. Anionic sites are
associated with the TBL and with interstitial collagen fibrils (C).
Flg. 5. TBL region, early placenta, after chondroitinase ABC treatment. Anionic sites are still associated with the TBL, although sites
associated with collagen (C) are reduced. x57,OOO.
Fig. 3. TBL region from early placenta after treatment with heparitinase. Virtually all of the TBL-associated anionic sites have been
Flg. 6. TBL reg'on, early placenta, chondroitinase ABC control preparation. Normal staining of anionic sites in TBL is seen. ~ 5 7 , 0 0 0 .
field, 1980; Vaccaro and Brody, 1979, 1981; Brody et al.,
1982; Pino et al., 1982; Essner and Pino, 1982; Charonis
and Wissig, 1983; Vernier et al., 1983). Where it has
been investigated, these basal laminas are rich in heparan sulfate PG (glomerulus, lung alveoli) or hyaluronate and heparan sulfate (mammary gland). In general,
the anionic sites are similar in size and distribution to
those described for embryonic epithelia. Anionic sites
have also been demonstrated in the basal lamina surrounding a variety of blood vessels (Wight and Ross,
1975; Katsuyama et al., 1977; Vaccaro and Brody, 1981;
Ausprunk et a]., 1981; Brody et al., 1982; Simionescu et
al., 1982; Charonis and Wissig, 1983)and in the pericel-
lular basal laminas of muscle, fat, and Schwann cells
(Charonis and Wissig, 1983).
In placental villi, we have demonstrated a developmental change in the pattern of anionic sites in both the
trophoblastic basal lamina and in that of the fetal capillaries. In the case of the TBL, anionic sites decreased
with development and were virtually absent by term. In
the case of the CBL the basal lamina (and anionic sites)
were essentially absent in the early material and were
moderately, but not consistently, well developed by term.
Selective enzymatic digestion demonstrated that the anionic sites associated with the first-trimester TBL probably consist mainly of heparan sulfate. At term, the few
Fig. 7. Base of trophoblast (T) and fetal capillary wall in term placenta. No ruthenium red treatment. TBL is quite thick and the fetal
endothelium (FE) now has a thin basal lamina (CBL). A few collagen
fibrils are interposed between the two basal laminas. ~57,000.
Fig. 10. BL region of term placenta after Triton and ruthenium red
treatment. Sites associated with collagen fibrils are large and heavily
stained. A small number of sites are associated with the interstitial
side of the TBL (arrows), and with the CBL (arrowheads). ~57,000.
Fig. 8. TBL region of term placenta after Triton and ruthenium red
treatment. TBL lacks anionic sites except for occasional ones associated with the interstitial surface of the lamina densa (arrows). The
capillary basal lamina iCBL) does have an array of anionic sites iarrowheads). ~57,000.
Fig. 11. BL region of term placenta after heparitinase treatment.
Anionic sites are still present in the CBL (arrowheads) and to some
extent with collagen fibrils (arrows)but not with the TBL. ~57,000.
Fig. 9. Micrograph of BL region of term placenta after Triton and
ruthenium red treatment, showing a region of close apposition of TBL
and CBL. Anionic sites associated with either BL are rare, even though
anionic sites associated with a nearby collagen fibril are stained (arrowheads). ~57,000.
Fig. 12. Term placenta, heparitinase control. A few anionic sites are
associated with the interstitial surface of the TBL (arrows) and with
the CBL (arrowheads).T, trophoblast; FE, fetal endothelium. ~57,000.
Fig.13. Term placenta, chondroitinaseABC treatment. Anionic s i b
have been removed from the CBL, collagen (C). and interstitial surface
of the TBL. ~57.000.
Fig. 14. Term placenta, chondroitinase ABC control. Anionic sites
awxiated with the CBL, collagen (arrow). and interstitial surface of
the TBL are stained. T,trophoblast, FE, fetal endothelium. ~57.000.
sites associated with the TBL were removed by either
heparitinase or chondroitinase ABC. Those sites associated with the CBL were selectively removed with the
chondroitinase ABC, indicating chondroitin sulfate or
dermatan sulfate. Biochemical and histochemical studies have shown many different GAGSin human placenta
(Lee et al., 1973; Wasserman et al., 1980,1983a,b)These
studies also indicate that dermatan sulfate and chondroitin sulfate are the most abundant GAGS near term
and that a higher proportion of dermatan sulfate is
associated with the placental blood vessels (Wasserman
et al., 1983b). Thus, our results are consistent with the
biochemical studies, although our observations are restricted to the small capillary exchange vessels, whereas
the biochemical studies also included many larger-caliber vessels.
At the present time, we do not have a complete understanding of the different functional roles that the TBL
may have during development. Presumably it plays a
supportive role as in other tissues (Vracko, 1974) and
may have a role in branching morphogenesis as in some
other embryonic systems (Bedield, 1981). In some other
tissues, it has been shown that the basal lamina can act
as a charge-selective permeability barrier to macromolecules. This property of basal laminas has been most
extensively studied in the kidney glomerulus, where the
glomerular basement membrane has a heparan sulfaterich PG layer that presents a negatively charged interface that retards filtration of anionic macromolecules
(Farquhar et al., 1982). Our observation that there is a
virtual absence of ruthenium red-positive anionic sites
in the TBL in later gestation may be of great functional
importance in relation to maternal-fetal transfer of macromolecules. A number of developmentally important
polypeptides and proteins are transported from tho maternal blood, across the trophoblast, and enter the fetal
capillaries. These include maternal IgG, from which the
fetus obtains its passive immunity (see King, 1982, for
references), and to a lesser extent albumin (Gitlin et al.,
1964). The absence of an array of polyanionic sites later
in gestation in the TBL suggests that this structure,
even though it is quite thick, probably presents no significant permeability barrier to macromolecules. In a
number of experimental or pathological situations it has
been shown that the absence or enzymatic removal of
heparan sulfate PG renders the basal lamina permeable
to proteins (Kanwar et al., 1980; Rohrbach et al., 1982;
Myndersse et al., 1983). In the case of TBL, our observations suggest the reduction in anionic sites during
development assures that macromolecules transported
by the trophoblast do not encounter a permeability barrier a t this level, and have access to the fetal capillary
In the case of the fetal capillary basal lamina, we were
able to detect at least some anionic sites, although the
number and arrangement did not always appear to be
as regular as in some other continuous capillary beds
(Charonis and Wissig, 1983). Charonis and Wissig (1983)
reported a regular array of anionic sites around the
continuous capillaries of muscle, although these sites
were not as negatively charged as similar sitcs around
fenestrated capillaries. These sites are apparently heparan sulfate PG (Charonis et al., 19831,but in the fetal
placental capillaries these sites appear to be mainly
chondroitin sulfate or dermatan sulfate. The effect of
the relatively poorly developed array of anionic sites
around fetal placental capillaries on the permeability of
the capillaries to macromolecules is difiicult to assess. If
placental capillaries are compared to the continuous
capillaries of muscle, there might be some discrimination based on charge, although the barrier would be
incomplete, since macromolecules do escape from and
enter muscle capillaries (Renkin, 1978; Noer and Lassen, 1979). Overall, the distribution of anionic sites in
TBL and CBL of the term placenta is such that facilitation of macromolecular transport is accomplished. Finally, near term the fetal capillaries become closely
apposed to the TBL, eliminating most or all of the intervening collagen and ground substance (e.g., Fig. 9). This
developmental change, by reducing additional anionic
sites, would also be expected to facilitate macromolecular transport.
Transport of proteins from mother to fetus is relatively
low during early gestation (Dancis et al., 1961; Gitlin
and Biasucci, 1969). We observed the presence of an
array of heparan sulfate PG in the early TBL, and usually a greater amount of extracellular matrix separating
the TBL from the fetal capillaries. Both these f i ~ t o r s
would be expected to retard exchange of macromolecules
at this age, although the primary b d e r to exchange
be at the level Of~OPhObld.
I wish to thank John Mais for excellent technical assistance and Meg Svetlichny and Clarrise Northern for
typing the manuscript. I also wish to thank Mr. Harry
Lowe and the staff of Sutter Memorial Hospital, and Dr.
Alton Curtis for assistance in obtaining the tissue. This
work was supported by National Institutes of Health
grant HD 11658.
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site, distributions, laminar, trophoblast, anionic, ville, characterization, placental, human, capillary, basal
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