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Biochemical Society Transactions (2011) Volume 39, part 1
Terminal monosaccharide expression on amniotic
glycoproteins as biomarkers of fetus maturity
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Magdalena Orczyk-Pawiłowicz1 and Iwona Katnik-Prastowska
Department of Chemistry and Immunochemistry, Wrocław University of Medicine, Bujwida 44a, 50-345 Wrocław, Poland
Abstract
Glycotypes, particularly those that terminate with sialic acid and fucose are known to play a fundamental
role in human development, during implantation, growth and differentiation of fetal tissues. The present
review describes changes in the exposition of terminal sialic acid and fucose isoforms in the amniotic fluid
glycoconjugates, α 1 -acid glycoprotein and fibronectin during critical stages of pregnancy, i.e. second and third
trimester, perinatal period, delivery and post-date pregnancy. The distinct amniotic glycoforms are suggested
to be implicated in regulatory processes to ensure homoeostasis during pregnancy and to protect the fetus.
These may have the potential of becoming additional laboratory makers in obstetrics to monitor pregnancy.
AF (amniotic fluid) contains bioactive
molecules
AF protects the fetus physically and biochemically and assists
in its development. AF resides in the amniotic cavity that
is lined by the amnion and chorion. The amniotic sac grows
and begins to fill, mainly with water, at approx. 2 weeks
after fertilization. In the 12th week of pregnancy, the AF
contains proteins, carbohydrates, lipids and phospholipids,
all of which aid in the growth of the fetus. AF is produced
by exudation of fluid through the skin of the fetus up to
the 14th week of pregnancy, when keratinization of the skin
occurs. During the 8th–11th week of pregnancy, the fetus
begins to swallow and urinate, which is why the amniotic fluid
consists of fetal urine at the late stages of gestation. Cells from
the amnion and chorion layers secrete proteins into the
AF. The protein and metabolite composition of AF varies
throughout gestation [1]. The growth factors, innate immunity molecules and serum components in AF are believed
to be involved in growth, development and protection of
the fetus against infection. These functional biomolecules are
mainly glycoproteins, several of which have been shown to
exert immunomodulatory effects. Among them are AGP (α 1 acid glycoprotein), glycodelin A and transferrin, which carry
sialyl-Lewisx glycotopes on some of their N-linked glycan
structures. Furthermore, they are known to act as inhibitors
of E-selectin-mediated cell adhesion during acute inflammation [2–6]. The glycans that contain α1,3-linked fucose may
modulate the processes of the acute-phase reaction, whereas
those with α1,2-linked fucose may block the binding of α1,2fucose-dependent bacteria to fetal tissue [5].
AF is a significant contributor to fetal health and
constitutes a potential rich source of biomarkers for diagnosis
Key words: α 1 -acid glycoprotein, amniotic fluid, fibronectin, fucosylation, glycobiomarker,
glycoconjugate, glycotope, sialylation.
Abbreviations used: AF, amniotic fluid; AGP, α 1 -acid glycoprotein; FN, fibronectin; hCG, human
chorionic gonadotropin.
1
To whom correspondence should be addressed (email [email protected]).
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Authors Journal compilation of fetal well-being as well as fetal disorders [7]; however, the
analysis of AF glycoconjugates is possible only after the 13th
week of pregnancy. At this period, an amniocentesis can be
performed for genetic indication of specific disorders [8].
The composition of the AF glycoproteins is known
to change throughout gestation because of its origination
from different sources, i.e. maternal, fetal and placental
tissues all contribute to the pool of AF glycoconjugates.
Therefore the patterns of sialylation and fucosylation in
AF glycoconjugates and individual glycoproteins during the
progression of gestation are the net result of several sites
of their biosynthesis, as well as exchange of this material
between mother, fetus and placenta [9,10].
Current knowledge concerning the glycan structures and
the role of glycoconjugates derived from AF is limited
and focuses mainly on the individual glycoproteins. The
studies are further limited to selected stages of pregnancy and
do not clearly show changes that occur between trimesters.
The question arises as to whether the glycosylation of AF
glycoconjugates remains constant or whether it changes with
the progression of a normal pregnancy.
Biological role of sialic acid and fucose
Structures bearing sialic acid contribute to the homoeostatic
maintenance of circulating glycoproteins through the
asialoglycoprotein receptors [11,12]. Sialylated α2,3- and/or
α2,6-glycans serve as ligands for sialoadhesin and selectin
families or compounds; however, the biological role of
α2,3- and α2,6-linked sialic acids has been suggested to be
quite different. α2,6-Linked sialic acids serve as a receptor
for pathogens and can modulate signal transduction events
in the immune system [11,12], whereas α2,3-linked sialic
acids are important for the viability of peripheral CD8+
T-cells in the cytotoxic-T-cell response [11]. Additionally,
the glycoconjugates bearing sialyl-Lewis antigens play a
role in the prevention of leucocyte adhesion to the fetal
syncytiotrophoblast [4,6].
Biochem. Soc. Trans. (2011) 39, 344–348; doi:10.1042/BST0390344
Glycomarkers for Disease
α1,6-Linked fucose (the core fucose in N-glycans) may
control many biological reactions involved in cell–cell
signalling and adhesion, and it stimulates cell growth and
differentiation. All of these processes can be observed during
the third trimester when intensive growth and development
of the fetus occurs. Moreover, core fucosylation is important
for normal fetal development and reproduction in mice
[13,14]. Terminal α1,2- and α1,3-linked fucoses are part of the
stage-specific embryonic antigens related to the Lewis family
of molecules expressed on N- and O-glycans. They are wellknown ligands in biological recognition [13,15]. α1,2-Linked
fucose has been found to have the potential to modulate
communication, growth and regeneration of neurons [16]. Bifucosylated Lewisy glycotopes participate in cell recognition
and adhesion at the fetal–maternal interface during embryo
implantation, up-regulating the DAG (diacylglycerol)/PKC
(protein kinase C) signalling pathway in human endometrial
cells [17]. Glycoconjugates containing α1,2-linked fucose,
particularly those abundantly expressed on gastric mucosa by
intestinal epithelium of adult mammals, are known to play
a crucial role in host–pathogen interactions. They provide
an attachment ligand for some pathogen receptors playing a
critical role in tissue colonization by the pathogen [13,18].
α1,3-Fucose linked to glycoconjugates is a part of the Lewisx
and sialo-Lewisx antigens, which are essential ligands for E-,
P- and L-selectin binding in cell adhesion [3,19]. Van Dijk
et al. [3] hypothesized with some experimental confirmation
that the sialo-Lewisx determinant on serum AGP has
immunomodulatory properties, inhibiting selectin-mediated
rolling of leucocytes on endothelium in inflamed areas.
Fucosylation and sialylation in the second
trimester
In the second trimester of pregnancy AF glycoconjugates
reveal the presence of oligosaccharides terminated with α2,3and α2,6-linked sialic acids, and fucoses linked via α1,6linkage to core oligosaccharide and α1,3- and α1,2-linked at
the non-reducing termini [20]. At this time, AF AGP and FN
(fibronectin) present mainly maternal-type glycans in terms
of branching, sialylation and/or fucosylation. Both AGP and
FN are terminated with α2,6-linked sialic acid more commonly than α2,3-linked, and are poorly fucosylated [5,21–24].
The glycosylation patterns of these amniotic glycoproteins
resemble that found in plasma AGP of pregnant women [25]
and were quite different from that found in fetal serum [22]. In
the second trimester, AF also contains proteins of fetal origin,
i.e. α1,6-fucosylated-α 1 -fetoprotein, which is synthesized in
the fetal yolk sac and/or fetal liver [8]. Additionally, the
highly fucosylated glycotopes are found on trophoblastic
products secreted into AF, namely as glycodelin [4], hCG
(human chorionic gonadotropin) [26] and transferrin [4,27].
These compounds represent a completely different scheme of
fucosylation compared with maternal serum. The appearance
of different fucosyl-isoforms in the second trimester of
pregnancy exclusively on glycoconjugates of AF, but not
on amniotic AGP and FN, may point to diverse biological
Figure 1 The most prominent alternations of terminal
monosaccharide exposition observed during normal pregnancy
functions of individual proteins. The α1,6-linked core fucose,
essential during organogenesis [14] and involved in integrinmediated cell migration and signal transduction [28], seems
to play a major role in early fetal tissue development early
in the second trimester. Outer α1,2- and α1,3-linked fucoses
are a part of the stage-specific embryonic antigens mentioned
previously [15,29].
Fucosylation and sialylation in the third
trimester
During the third trimester, fetal development is continued
and the fetus grows the most rapidly (Figure 1). With the
physiological development of the organs of the fetus, the expression of the α2,6-linked sialic acid and α1,6-core fucose in
amniotic glycoconjugates increases, whereas the α1,3-linked
fucose decreases [20]. Briese et al. [9] have reported that, in
the third trimester, the sialic acid synthesized by the maternal
tissues crosses the placenta to contribute to fetal growth. The
increased expression of core fucose in pregnancy has been
demonstrated for hCG and transferrin [27,30]. According to
Nemansky et al. [31] the increased core fucosylation of Nglycans may reflect the change from an invasive state to a
more nurturing role of the placenta during pregnancy.
In contrast, the pattern of glycosylation of individual glycoproteins does not match that described above for the total
pool of glycoconjugates. In the third trimester of pregnancy,
the sialylation of AGP and FN, particularly the α2,3-isoform,
significantly increases in relation to the second trimester
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[23,24]. The appearance of α2,3 sialylation is connected with
the implantation of the embryo in the uterus [32], and
development and differentiation in pigs [33]. Vallejo et al. [33]
have found that during the early stage of maturation of the
central nervous system, α2,3-sialylated glycotopes predominate, whereas at the later stages it is replaced by α2,6-linked
sialic acid. α2,3-Sialylated oligosaccharides are also called
oncoembryonic antigen and are frequently expressed in AF
and fetal tissue [24,34,35]. The presence of α2,3-sialic acids in
AF suggests the participation of glycoproteins of fetal origin.
Amniotic AGP and FN become highly decorated with
the core α1,6-fucose at around the 28th–30th week of
pregnancy [5,23]. Nemanski et al. [31] have claimed that the
intensive α1,6-fucosylation of some pregnancy-associated
hormones is due to the high activity of the developmentally
regulated fucosyltransferase. It was shown that the activity
of α1,6-fucosyltransferase increases during the 14th–17th
week of pregnancy and stays at a high level throughout the
early third trimester of pregnancy.
α1,2-Linked fucose on amniotic AGP and FN appear
later, at around the 35th week. The situation with the
appearance of α1,3-linked fucose, which is known to
be a part of the Lewisx antigen, was quite different for
AGP and FN. It appears on AGP, a positive acute-phase
reactant with immunomodulatory activities, at around
the 35th week. In contrast, the FN, an adhesive and
multifunctional protein, lacks α1,3-linked fucose during
all stages of pregnancy [5,23,36]. In AF, the highly
sialylated and fucosylated AGP glycans can interact with
amniotic selectins and play an immunomodulatory role
during late pregnancy [37]. α1,2-Fucosylated glycotopes
found in some glycoproteins share common epitopes
that are ligands for some pathogen receptors [18,38].
These glycotopes of amniotic AGP and FN might act as
soluble inhibitors of the interaction between the receptor
of the pathogen and the host ligand to prevent bacterial
colonization, thus protecting the fetus against infection [5,23].
Fucosylation and sialylation in the
perinatal period
During the perinatal period, the fetus is prepared for
ex utero viability. α2,6-Sialylation of amniotic glycoconjugates increases significantly, whereas α2,3-linked sialic
acid, only slightly. At the same time, the fucosylation
pattern is almost at a constant level [20]. In contrast, the
amniotic AGP and FN sialylation with both types of sialic
acid linkages remains almost unaltered starting from the
third trimester and throughout the perinatal period [23,24].
Moreover, characteristic of the perinatal period is the increase
in the relative amounts of α1,3-, as well as α1,2-, linked fucose
on outer antennae of AGP, and unchanged levels of the core
α1,6-fucosylation of AGP [5]. In the case of FN, during the
perinatal period core fucosylation decreased significantly,
whereas both antenna-fucoses are at the same level as they
were in the third trimester [23]. It has been demonstrated
by Arkwright et al. [39] that the core fucosylation of FN
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Authors Journal compilation was correlated with the synthesis of FN by placenta, and a
significant decrease of the core fucosylation can be related to
the aging of the trophoblast.
Fucosylation and sialylation during
delivery
Delivery is accompanied by a physiological systemic
inflammatory response. Inflammatory activation occurs with
normal-term labour to accelerate processes necessary for successful labour and delivery [40]. During delivery the total glycoconiugates are characterized by α2,6-desialylation, whereas
α2,3-sialylation and the three types of fucosylation remain
nearly unaltered [20]. The α2,6- and α2,3-sialylation, as well
as α1,6-fucosylation of amniotic AGP and all isoforms of FN,
remain almost unchanged during delivery [5,23,24]; however,
delivery is associated with the decrease of outer arm α1,3and α1,2-linked fucose expression in AGP [5]. The changes
in the fucosylation of AGP could be related to the major and
exhausting effort made by the woman during delivery. Delivery is known to provoke an enhanced synthesis of cytokines
[41], some of which are known to initiate and amplify inflammatory processes [40]. As the delivery evokes an acute-phase
reaction, the lower expression of fucoses on amniotic AGP
could be connected with the defucosylation of some acutephase proteins at the early stage (up to 24 h) of an inflammatory reaction, observed in an experimental animal model by
Chavan et al. [42]. Perhaps, the variations in fucosylation are
limited only to the acute-phase glycoproteins.
Fucosylation and sialylation in prolonged
pregnancy
Prolonged pregnancy is associated with increased risks to the
fetus and the mother. There is a risk, particularly with obese
women, of the development of postmaturity syndrome and
intra-uterine growth retardation of the fetus. The timing
of labour or the prolongation of gestation can be altered
by levels of circulating hormones and influenced by high
body mass index [43]. Additionally, the placenta, which is
responsible for transport of nutrients and oxygen to the fetus
and removal of waste products from the fetus, starts aging
and eventually fails in its function [44].
In prolonged pregnancy, the amounts of α2,6-linked sialic
acid, and α1,2- and α1,3-linked fucoses are significantly
higher than those at the perinatal period [20]. Among
all analysed glycotopes of amniotic FN, only α1,2-linked
fucose significantly increases in prolonged pregnancy [23].
FN is known to play an important role in placenta
development during pregnancy [45]. FN expression has been
reported to be associated with placental deterioration and
calcifications [44] and placental vascular disease [46], events
that can provoke a fetal inflammatory cytokine response.
As a consequence, the damaged placental cells no longer
function during pregnancy and are eliminated by apoptosis
[44,47]. Inflammation and apoptosis are accompanied by
the overexpression of fucoses on glycoconjugates [13,48–
50]. Such sugar-printing molecules are ligands for lectin
Glycomarkers for Disease
receptors and are necessary for the removal of postapoptotic material [51]. Assuming that amniotic FN can
be of placental origin, the higher exposition of α1,2fucosylated FN isoforms may be related to the stimulation of
glycosylation pathways by apoptotic processes. In contrast,
amniotic AGP derived from prolonged pregnancy samples
is characterized by a decrease in α2,3-sialylation and α1,2fucosylation [5,24]. The differences in the sialyl- and fucosylglycotope expression on amniotic AGP and FN during
normal stages of pregnancy and associated with pregnancy
complications could be related to the different origin and
functions of these proteins. The analysis of alterations in glycosylation of amniotic AGP and FN as well as amniotic glycoconiugates have the clinical potential to predict a prolonged
pregnancy, a risk for development of post-maturity syndrome
and intra-uterine growth retardation of the fetus [5,20,23,24].
Conclusions
The changes in sialic acid and fucose expositions on some
amniotic glycoconjugates are dynamic, quantitative and
qualitative. Despite the fact that the experimental data
available are fragmentary, it can be concluded that there is no
general scheme for terminal monosaccharide expositions on
particular glycoproteins. The current knowledge concerning
the glycosylation pattern of amniotic glycoproteins provides
the starting point for further structural and functional studies.
They are also appropriate candidates for glycobiomarkers for
predicting the time of delivery, and monitoring pregnancy
and fetal well-being.
Acknowledgement
We are grateful to Professor Carlito B. Lebrilla from University of
California Davis, Davis, CA, U.S.A., for a critical reading of the paper
before submission.
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Received 10 September 2010
doi:10.1042/BST0390344