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First published online 13 December 2006
doi: 10.1242/dev.02743
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1 Departments of Pathology and Laboratory Medicine, Institute of Maternal-Fetal
Biology, Division of Cancer and Developmental Biology, University of Kansas
Medical Center, Kansas City, KS 66160, USA.
2 Departments of Pharmacology, Toxicology, and Therapeutics, Institute of
Maternal-Fetal Biology, Division of Cancer and Developmental Biology,
University of Kansas Medical Center, Kansas City, KS 66160, USA.
3 Departments of Molecular and Integrative Physiology, Institute of
Maternal-Fetal Biology, Division of Cancer and Developmental Biology,
University of Kansas Medical Center, Kansas City, KS 66160, USA.
4 Departments of Obstetrics and Gynecology, Institute of Maternal-Fetal Biology,
Division of Cancer and Developmental Biology, University of Kansas Medical
Center, Kansas City, KS 66160, USA.
* Author for correspondence (e-mail: msoares{at}kumc.edu)
Accepted 14 November 2006
 |
SUMMARY |
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 TOP SUMMARY INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key words: Dprp (Dtprp), Decidua, Pregnancy, Uterus, Null mutation, Adaptations to hypoxia, Mouse
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INTRODUCTION |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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;
Carson et al., 2000). This
close connection facilitates the exchange of nutrients and wastes. Decidual
and trophoblast cells are likely to provide the signaling system that
coordinates the activities of the maternal compartment. Decidual cells are
modified uterine endometrial stromal cells. The differentiation of decidual
cells is one of the earliest uterine adaptations to pregnancy
(DeFeo, 1967;
Parr and Parr, 1989;
Aplin, 2000). Decidual cell
differentiation is exquisitely sensitive to the regulatory actions of
progesterone, interleukin-11, and activators of cyclic AMP/protein kinase A
(Tang et al., 1994;
Lydon et al., 1995;
Brar et al., 1997;
Dimitriadis et al., 2005;
Brosens and Gellersen, 2006).
During gestation, decidual cells are located at the interface separating
invading trophoblast cells from the maternal environment. A number of
important functions have been attributed to decidua
(Bell, 1983;
Aplin, 2000;
Brosens and Gellersen, 2006):
(1) a protective role in controlling trophoblast cell invasion; (2) a
nutritive role for the developing embryo; (3) a role in preventing
immunological rejection of genetically disparate embryonic/fetal tissues; and
(4) an endocrine/paracrine role in controlling maternal adaptations required
for the establishment and maintenance of pregnancy. Pregnancy is dependent
upon decidual cell acquisition of each of these specialized functions.
Disruptions in decidual cell development are not compatible with pregnancy
(Lydon et al., 1995;
Bilinski et al., 1998;
Robb et al., 1998;
Mantena et al., 2006).
Progress in understanding specialized decidual cell functions has been
limited.
Decidual cell signaling is mediated, at least in part, through the
production of cytokines related to prolactin (PRL)
(Tang et al., 1994;
Orwig et al., 1997c;
Telgmann and Gellersen, 1998;
Jabbour and Critchley, 2001).
PRL is a member of a larger collection of structurally-related
hormones/cytokines (the PRL superfamily) with an array of different biological
targets and actions (Wiemers et al.,
2003; Soares,
2004; Alam et al.,
2006). In the rat and mouse, four members of the PRL superfamily
are expressed in uterine decidua: decidual prolactin-related protein (DPRP;
DTPRP - Mouse Genome Informatics) (Roby et
al., 1993; Lin et al.,
1997; Orwig et al.,
1997b), prolactin-like protein B (PLP-B; PRLPB - Mouse Genome
Informatics) (Duckworth et al.,
1988; Croze et al.,
1990; Cohick et al.,
1997; Müller et al.,
1998), PLP-J (PRLPJ - Mouse Genome Informatics)
(Hiraoka et al., 1999;
Ishibashi and Imai, 1999;
Toft and Linzer, 1999;
Dai et al., 2000) and
prolactin itself (Prigent-Tessier et al.,
1999; Kimura et al.,
2001). Each of these decidual PRL family cytokines can be viewed
as a downstream mediator of intrauterine progesterone action.
DPRP is secreted as a glycoprotein by uterine decidual cells and resides in
the decidual extracellular matrix where it binds with high affinity to
heparin-containing molecules (Rasmussen et
al., 1996; Rasmussen et al.,
1997; Orwig et al.,
1997b; Wang et al.,
2000). Little is known about the physiological actions of DPRP. In
this report, we explore the biology of uterine decidual cells through
investigation of the Dprp-null mouse.
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MATERIALS AND METHODS |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Positive plaques were amplified and used to inoculate
LE392 Escherichia coli. A series of forward and reverse
oligonucleotide primer sets based on the mouse Dprp cDNA were
designed and used to sequence exons and exon-intron boundaries. DNA sequencing
was performed with an Applied Biosystems Model 310 sequencer and Applied
Biosystems Dye Terminator Cycle Sequencing Kits (Foster City, CA). The
Dprp targeting vector was constructed by replacing exons 2-6 of the
mouse Dprp gene with the enhanced green fluorescent protein
(EGFP) gene and MC1neo cassette flanked by loxP
sites (Godwin et al., 1998). A
6.6 kb DNA fragment, containing 3.8 kb of 5' flanking DNA and 2.8 kb of
exon 1 and intron A of the mouse Dprp genomic construct, was
subcloned upstream of EGFP. A 6.0 kb DNA fragment of the
Dprp genomic construct containing 3' flanking DNA located
immediately downstream of exon 6 was subcloned downstream of the
MC1neo cassette and upstream of a herpes simplex virus thymidine
kinase gene. The accuracy of vector construction was verified by restriction
enzyme and DNA sequence analyses. A schematic representation of the mouse
Dprp gene and the targeting vector are shown in
Fig. 1. The targeting vector
was introduced into R1 embryonic stem cells
(Nagy et al., 1993) (a
generous gift from Dr Janet Rossant, Samuel Lunenfeld Research Institute,
Toronto, Canada) by electroporation. Cells were selected by exposure to G418
and gangcyclovir. Southern blot analysis was used to identify clones that
appropriately underwent homologous recombination with the targeting vector.
Genomic DNA was isolated, digested with SalI, and fractionated in
0.8% agarose gels. Southern blots were performed with a probe derived from
intron A. Wild-type alleles were characterized by a 21 kb hybridization
signal; homozygous mutant alleles were characterized by a 5.5 kb hybridization
signal. Chimeras were generated by injection into C57BL/6 blastocysts and
transferred into pseudopregnant (C57BL/6xCBA) F1 females. PCR was
routinely used to identify offspring with wild-type and Dprp mutant
alleles. A forward primer corresponding to a nucleotide sequence in intron A
of the Dprp gene (5'-GAGCTTAAACTTCAATGTAAGT-3') was used
with reverse primers corresponding to nucleotide sequences in intron B of the
Dprp gene (5'-GTGTGCTAAATGAACGTAGT-3') and within the
EGFP gene (5'-GTATGGCTGATTATGATCTAGA-3'). PCR was
conducted for 30 cycles under the following conditions: preheat, 94°C for
4 minutes; denature, 94°C for 1 minute; anneal, 60°C for 1 minute; and
extension, 72°C for 1.5 minutes. PCR products (wild-type allele, 676 bp;
mutant allele, 1148 bp) were separated on 1% agarose gels and stained with
Ethidium Bromide. Mice with the Dprp mutation were backcrossed for
six generations to C57BL/6 or 129SvJ genetic backgrounds.
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;
Ain et al., 2006). Alkaline
phosphatase activities in deciduomal tissue were measured as previously
described (Soares, 1987;
Arroyo et al., 2005). The
University of Kansas Medical Center Animal Care and Use Committee approved all
procedures for handling and experimentation with rodents.
Hypobaric hypoxia
Female C57BL/6 pregnant mice were placed in hypobaric chambers beginning on
day 5.5 of gestation, as previously described
(Ho-Chen et al., 2006). Under
these conditions, air is circulated at a barometric pressure of 
420 Torr,
which results in an inspired PO2 of 78 Torr, equivalent to
breathing 11% O2 at sea level. The chambers were opened daily to
clean cages and replenish food and water (15-20 minutes).
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; Orwig et al.,
1997b). Protein concentrations were determined for each sample
using the Bio-Rad DC protein assay (Bio-Rad, Hercules, CA).
Histological analyses
Analyses were performed on 10 µm tissue sections prepared with the aid
of a cryostat. Sections were stained with Hematoxylin and Eosin, or subjected
to biotinylated Griffonia simplicifolia lectin I isolectin
B4 (Vector Laboratories, Peterborough, UK) histochemistry, or used
for immunocytochemistry. Immunocytochemical analyses were used to determine
the distribution of GFP, natural killer (NK) cells, trophoblast cells and
endothelial cells (Ain et al.,
2003) (T.K., L. A. Rempel, J. A. Arroyo and M.J.S., unpublished).
GFP was monitored by fluorescence and immunoreactivity with rabbit anti-GFP
polyclonal antibodies (Chemicon International, Temecula, CA). NK cells were
detected with a rabbit polyclonal anti-perforin 1 antibody (Torrey Pines
Biolabs, Houston, TX). Trophoblast cells were monitored with a rat monoclonal
anti-mouse cytokeratin antibody (TROMA-1; Developmental Studies Hybridoma
Repository, Iowa City, IA). Endothelial cells were localized using a rat
monoclonal anti-mouse endoglin antibody (Developmental Studies Hybridoma
Repository, Iowa City, IA) and a rat monoclonal anti-mouse CD31 antibody (BD
Pharmingen, Franklin Lakes, NJ). TUNEL assays were performed with the In Situ
Cell Death Detection Kit (Roche Applied Science, Penzberg, Germany) according
to the manufacturer's instructions. All processed tissue sections were
examined and images recorded with a Leica MZFLIII stereomicroscope equipped
with a CCD camera (Leica Microsystems GmbH, Welzlar, Germany).
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). The assay
has been effectively used to monitor the phenotypes of decidua and placenta.
The PRL superfamily mini-array assay was performed as previously described
(Dai et al., 2002).
Northern blot analysis
Northern blot analysis was performed as described previously
(Faria et al., 1990). Total
RNA was extracted from tissues using TRIzol reagent (Invitrogen, Carlsbad,
CA). Total RNA (15 µg per lane) was resolved in 1% formaldehyde-agarose
gels, transferred to nylon membranes and crosslinked. Blots were probed with
[
32P]-labeled cDNAs for Dprp
(Orwig et al., 1997b),
Plp-j (Dai et al.,
2000), Plp-b
(Müller et al., 1998) and
metallothionein-I (Mt1) (Liang et
al., 1996). Glyceraldehyde-3-phosphate dehydrogenase
(Gapdh) cDNA was used to evaluate the integrity and equal loading of
RNA samples. At least three different tissue samples from three different
animals were analyzed with each probe for each time point.
RT-PCR analysis
Dprp, Plp-j and Plp-b mRNA levels were estimated by
RT-PCR. Total RNA was isolated from uterine tissues from days 5.5 to 7.5 of
gestation. Total RNA (2 µg) and 0.5 µg of oligo dT were used for reverse
transcription reactions with SuperScript II reverse transcriptase
(Invitrogen). PCR was conducted using Platinium Taq DNA High Fidelity
polymerase (Invitrogen) and Dprp-, Plp-j-, Plp-b- or
Gapdh-specific primers (Table
1). PCR was performed for 30 cycles (denature, 95°C for 45
seconds; anneal, 55°C for 45 seconds; extension, 72°C for 1 minute).
The amplified products were resolved by electrophoresis in 1% agarose gels and
Ethidium Bromide staining.
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;
Weimers et al., 2003). Cryosections (10 µm) of tissues were prepared and
stored at -80°C until used. Plasmids containing cDNAs for mouse
Dprp and Plp-j (Orwig et
al., 1997b; Dai et al.,
2000) were used as templates to synthesize sense and antisense
digoxigenin-labeled riboprobes according to the manufacturer's instructions
(Roche Molecular Biochemicals, Indianapolis, IN).
Statistical analysis
The data were analyzed by analysis of variance and post hoc comparisons
determined by the Newman-Keuls Test.
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RESULTS |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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;
Orwig et al., 1997a;
Wiemers et al., 2003;
Alam et al., 2006).
Dprp-null mutant mice were generated by genetargeting strategies
culminating in the replacement of a region of the Dprp gene (exons 2
through 6) with an in-frame EGFP gene and an MC1neo
cassette. The portion of the Dprp coding sequence remaining in the
mutated gene (exon 1) encodes the first 10 amino acids of the DPRP signal
peptide. A schematic representation of the mouse Dprp gene and the
targeting vector are shown in Fig.
1. Correct homologous recombination was determined by Southern
blotting and PCR analyses. Two mutant ES cell lines (No. 44 and No. 96) with a
normal karyotype were injected into blastocysts in order to generate chimeras.
The No. 44 cell line gave rise to a >95% male chimera. The No. 96 cell line
gave rise to three chimeras, including two males of 40% and 75% chimerism, and
a female of 60% chimerism. Male chimeras from both the No. 44 and No. 96 lines
were bred to C57BL/6 females and successfully transmitted the Dprp
mutant allele to their offspring. Subsequent analyses were derived from mouse
line No. 44. Breeding of mice heterozygous for the Dprp-null mutation
resulted in offspring genotypes that did not significantly deviate from the
expected mendelian ratio (Table
2). The mutation was moved to two inbred strains (C57BL/6 and
129SvJ) following six generations of backcrosses. Homozygous
Dprp-null mutant male and female mice were viable on a mixed 129 SvJ
and C57BL/6 genetic background and following transfer to C57BL/6 and 129SvJ
genetic backgrounds. The offspring exhibited normal postnatal growth rates and
were fertile (Tables 3 and
4). Genetic background did not
significantly affect the phenotype of mice with the Dprp-null
mutation. Genotyping and Dprp expression analyses are shown in
Fig. 1. The gene targeting
strategy successfully disrupted Dprp mRNA and protein expression.
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;
Rasmussen et al., 1997;
Lin et al., 1997;
Orwig et al., 1997b). The
Dprp-null allele contains an EGFP gene inserted into the
Dprp locus. Pregnant heterozygous (+/-) and homozygous null (-/-)
females faithfully expressed EGFP within decidual tissue in locations similar
to endogenous DPRP expression in pregnant wild-type (+/+) females
(Fig. 2). However, the tissue
distribution of EGFP in the mesometrial compartment of Dprp-null mice
was less than the tissue distribution of DPRP protein in the mesometrial
compartment of wild-type mice (Fig.
2). This difference continued to be evident on day 11.5 of
gestation (Fig. 3).
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We next examined decidualization in pseudopregnant wild-type and Dprp-null mice (Fig. 5). Deciduoma formation was similar in mice of both genotypes with only subtle differences, including a modest but significant decrease in deciduomal weight, when expressed per body weight (Fig. 5D). DPRP protein in wild-type and GFP in Dprp-null mice localized predominantly to the anti-mesometrial deciduomal compartment (Fig. 5F-H). Similar to pregnancy, Plp-j mRNA expression was also down-regulated in Dprp-null deciduoma (Fig. 5I).
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Impact of maternal hypoxia on the Dprp-null phenotype
Successful species develop strategies to optimize their reproductive
performance. This optimization is likely to include the evolution of genes
that specifically permit reproduction in physiologically challenging
conditions. The PRL superfamily has been postulated to participate in the
regulation of adaptations to physiological stressors
(Dorshkind and Horseman, 2001;
Ain et al., 2004;
Soares et al., 2006). These
insights led us to examine a role for DPRP in the regulation of
pregnancy-dependent adaptations to physiological stressors. Hypoxia was
selected as a physiological stressor because it is well established that low
oxygen tension promotes extensive tissue remodeling at the maternal-fetal
interface (Zamudio, 2003;
Fryer and Simon, 2006;
Myatt, 2006).
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Histological examination of tissue sections through the uteroplacental compartments revealed prominent adaptive as well as a range of potentially maladaptive responses to hypoxia in the wild-type and Dprp-null mice (Figs 8, 9). The adaptive responses to maternal hypoxia observed in the wild-type uterine mesometrial compartment included compression of the mesometrial decidua and increased depth of endovascular trophoblast cell invasion. The potentially maladaptive responses in the Dprp-null mesometrial compartment included: (1) enlarged mesometrial blood spaces (Fig. 8A,D); (2) distorted chorioallantoic placental organization, including trophoblast giant cell overgrowth (Fig. 8B,E); (3) exaggerated compression of the mesometrial decidua (Fig. 8C,F); and (4) decreased endovascular trophoblast invasion (Fig. 9). These aberrations may be related to the altered mesometrial decidua in the Dprp-null mouse noted above (Fig. 3). The net result is a failure in the placentation-specific adaptations to hypoxia required to ensure maintenance of pregnancy.
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DISCUSSION |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). It functions as a supportive structure that facilitates
placentation and embryonic development and it is established that pregnancy
does not proceed in its absence. In this report, we provide evidence that a
secretory product of the uterine decidua is fundamental to the regulation of
pregnancy-dependent adaptations to hypoxia. The decidual cell secretory
product is a member of the PRL superfamily of hormones/cytokines.
The composition of the PRL superfamily is diverse and species-specific
(Forsyth and Wallis, 2002;
Soares, 2004). In the mouse
and rat the PRL superfamily has expanded, consisting of approximately two
dozen genes, whereas in other species (e.g. human and dog) the superfamily has
but a single constituent (Wiemers et al.,
2003; Alam et al.,
2006). Why mammalian genomes evolved differently with respect to
this classic hormone/cytokine is unknown. We have gained insights into the PRL
superfamily through an examination of the biology of members of the expanded
mouse PRL superfamily and have utilized a standard single gene mutation
approach. Based on gene expression patterns, the PRL superfamily is linked to
pregnancy (Soares, 2004).
Previously, we demonstrated that a trophoblast cell-derived PRL family member,
PLP-A (PRLPA - Mouse Genome Informatics), targets uterine NK cells and imposes
only modest effects on the biology of pregnancy under standard laboratory
housing conditions (Müller et al.,
1999; Ain et al.,
2004). In the current study, we have shown that another member of
the PRL superfamily produced by uterine decidual cells, DPRP, also has subtle
influences under ordinary husbandry conditions. However, both PLP-A and DPRP
modulate pregnancy-dependent adaptations to hypoxia.
Wild-type pregnant mice can effectively adapt to hypoxia without fetal loss
(Ho-Chen et al., 2006).
Adaptations are dependent upon the timing, duration and magnitude of the
hypoxic exposure. Among the pregnancy-dependent adaptations are events
occurring at the maternal-fetal interface. Most notable are a compression of
the mesometrial decidua and alterations in the uterine mesometrial
vasculature, including its interactions with trophoblast cells. Null mutations
in either the Plp-a gene or the Dprp gene interfere with
adaptive responses to hypoxia and result in fetal loss. Under hypoxic
conditions, the absence of PLP-A obstructs early stages of
trophoblast-vascular interactions, disrupting nutrient delivery and leading to
growth restriction (Ain et al.,
2004). The hypoxia-exposed Dprp-null placenta is able to
satisfactorily progress through this early interaction with the maternal
environment but collapses a couple of days later, which is associated with a
series of anomalies in the uterine mesometrial compartment and placenta. The
appearance of vascular lesions, enlarged mesometrial blood spaces, distorted
chorioallantoic placentas, and decreased endovascular trophoblast invasion
characterize the Dprp-null mutant response to hypoxia. The specific
aberration that leads to pregnancy failure is unknown. Some insights into the
Dprp-null phenotype may be deduced from inspection of decidual tissue
adjoining the developing chorioallantoic placenta.
The orientation of the post-implantation uterus is determined by the entry
site of the vasculature. The region associated with vascular entry is referred
to as the mesometrial compartment, and the opposite side of the uterus is
referred to as the anti-mesometrial compartment. Mesometrial and
anti-mesometrial decidua differ structurally and functionally
(Krehbiel, 1937;
Bell, 1983;
Gu and Gibori, 1995). DPRP is
expressed in anti-mesometrial decidua and in a smaller population of
mesometrial decidual cells situated proximal to the developing chorioallantoic
placenta (Orwig et al., 1997b;
Rasmussen et al., 1997) (Figs
2,
3). Decidual cell Dprp
expression is initiated between days 5.5 and 6.5 of gestation in the mouse. In
the present study, abnormalities were not observed in the organization of
anti-mesometrial decidua or in its neighboring tissues from Dprp-null
mice under normoxic or hypoxic conditions. By contrast, prominent differences
were noted in the mesometrial compartments of wild-type and Dprp-null
mice. Such observations place more significance on the mesometrial decidual
cell source of DPRP. This mesometrial decidual structure may be crucial in
coordinating uteroplacental adaptations to hypoxia and may provide a key to
understanding the phenotype of the Dprp-null mouse exposed to
hypoxia.
DPRP is a cytokine possessing an affinity for heparin-containing structures
(Rasmussen et al., 1996;
Wang et al., 2000). Evidence
suggests that DPRP does not circulate but instead is deposited within the
decidual extracellular matrix. Although the DPRP protein is structurally
related to PRL, DPRP does not utilize the PRL-receptor signaling pathway
(Rasmussen et al., 1996). The
mechanism of action of DPRP is unknown but may include an autocrine/paracrine
activity required for the differentiation and/or survival of the mesometrial
decidua (as suggested by the present study). Alternatively, DPRP may
independently modulate mesometrial vascular-trophoblast interactions.
Interestingly, PRL is produced by human decidual cells, possesses an affinity
for heparin (Khurana et al.,
1999), and its targets are likely to be intrauterine
(Jabbour and Critchley, 2001).
Whether human PRL produced by decidual cells functionally overlaps with DPRP
and facilitates adaptations to physiological stressors remains to be
determined.
Investigation of the Dprp-null mouse has permitted a dissection of mechanisms controlling decidual cell adaptations to physiological stressors, and has demonstrated the effectiveness of in vivo hypoxia as a tool for elucidating intrinsic regulatory processes controlling placentation.
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ACKNOWLEDGMENTS |
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